Skip to main content

Advertisement

SpringerLink
Log in

The extracellular matrix in tumor progression and metastasis

  • Review
  • Published:
Clinical & Experimental Metastasis Aims and scope Submit manuscript

Abstract

The extracellular matrix (ECM) constitutes the scaffold of tissues and organs. It is a complex network of extracellular proteins, proteoglycans and glycoproteins, which form supramolecular aggregates, such as fibrils and sheet-like networks. In addition to its biochemical composition, including the covalent intermolecular cross-linkages, the ECM is also characterized by its biophysical parameters, such as topography, molecular density, stiffness/rigidity and tension. Taking these biochemical and biophysical parameters into consideration, the ECM is very versatile and undergoes constant remodeling. This review focusses on this remodeling of the ECM under the influence of a primary solid tumor mass. Within this tumor stroma, not only the cancer cells but also the resident fibroblasts, which differentiate into cancer-associated fibroblasts (CAFs), modify the ECM. Growth factors and chemokines, which are tethered to and released from the ECM, as well as metabolic changes of the cells within the tumor bulk, add to the tumor-supporting tumor microenvironment. Metastasizing cancer cells from a primary tumor mass infiltrate into the ECM, which variably may facilitate cancer cell migration or act as barrier, which has to be proteolytically breached by the infiltrating tumor cell. The biochemical and biophysical properties therefore determine the rates and routes of metastatic dissemination. Moreover, primed by soluble factors of the primary tumor, the ECM of distant organs may be remodeled in a way to facilitate the engraftment of metastasizing cancer cells. Such premetastatic niches are responsible for the organotropic preference of certain cancer entities to colonize at certain sites in distant organs and to establish a metastasis. Translational application of our knowledge about the cancer-primed ECM is sparse with respect to therapeutic approaches, whereas tumor-induced ECM alterations such as increased tissue stiffness and desmoplasia, as well as breaching the basement membrane are hallmark of malignancy and diagnostically and histologically harnessed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ADAMTS:

A disintegrin and metalloproteinase with thrombospondin motifs

CAF:

Cancer-associated fibroblast

CCN:

CTGF, Cyr61, and NOV

CTGF:

Connective tissue growth

CXCL12 = SDF.1:

C-X-X chemokine 12 = stroma cell-derived factor-1

Cyr61:

Cysteine-rich angiogenic protein 61

DDR:

Discoidin domain receptor

ECM:

Extracellular matrix

ED-A, -B:

Extra domain-A, -B

EGF-L:

Epidermal growth factor-like

EGFR:

Epidermal growth factor receptor

Ela-2:

Neutrophil elastase

ERC:

Elastin receptor complex

Endo180:

Endocytic receptor 180 = C-type mannose receptor 2

FNFr:

Fibronectin fragment

GAG:

Glycosaminoglycan

GPVI:

Glycoprotein VI

HGF:

Hepatocyte growth factor

IGF-1R:

Insulin-like growth factor 1 receptor

IL:

Interleukin

KRAS:

Kirsten rat sarcoma oncogene

LAIR-1:

Leukocyte-associated immunoglobulin-like receptor 1

LG3, 4:

Laminin globular domain 3, 4

LOX/LOXL:

Lysyl oxidase/lysyl oxidase-like

LRP6:

Low-density lipoprotein receptor-related protein 6

LY75:

Lymphocyte antigen 75 (CD205, DEC-205)

MET:

Mesenchymal-epithelial transition factor proto-oncogene, hepatocyte growth factor receptor, HGFR

MMP:

Matrix metalloproteinase

MR:

Mannose receptor

MuSK:

Muscle-specific kinase

NC1:

Non-collagenous domain 1

NCAM-L1:

Neural cell adhesion molecule L1

NOV:

Nephroblastoma overexpressed gene

NrCAM:

Neuron-glial related cell adhesion molecule

PAR:

Protease-activated receptor

PD-1/PD-L1:

Programmed death-1/programmed death ligand-1

PDGF:

Platelet-derived growth factor

PLA2R:

Phospholipase-A2-receptor

Sema3F:

Semaphorin 3F

SIBLING:

Small integrin-binding ligand-N-linked glycoprotein

SLRP:

Small leucine-rich proteoglycan

SPARC:

Secreted protein, acid and rich in cysteine

TAM:

Tumor-associated macrophage

TF:

Tissue factor

TLR-2, -4:

Toll-like receptor-2, -4

TME:

Tumor microenvironment

TGF-β:

Transforming growth factor-β

Treg:

Regulatory T cell

VEGF:

Vascular endothelial growth factor

VEGFR2:

Vascular endothelial growth factor receptor 2

VM:

Vasculogenic mimicry

References

  1. Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70

    Article  CAS  PubMed  Google Scholar 

  2. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674. https://doi.org/10.1016/j.cell.2011.02.013

    Article  CAS  PubMed  Google Scholar 

  3. Paul CD, Mistriotis P, Konstantopoulos K (2017) Cancer cell motility: lessons from migration in confined spaces. Nat Rev Cancer 17(2):131–140. https://doi.org/10.1038/nrc.2016.123

    Article  CAS  PubMed  Google Scholar 

  4. Theocharis AD, Skandalis SS, Gialeli C, Karamanos NK (2016) Extracellular matrix structure. Adv Drug Deliv Rev 97:4–27. https://doi.org/10.1016/j.addr.2015.11.001

    Article  CAS  PubMed  Google Scholar 

  5. Chang TT, Thakar D, Weaver VM (2017) Force-dependent breaching of the basement membrane. Matrix Biol 57–58:178–189. https://doi.org/10.1016/j.matbio.2016.12.005

    Article  CAS  PubMed  Google Scholar 

  6. Walker C, Mojares E, Del Rio Hernandez A (2018) Role of extracellular matrix in development and cancer progression. Int J Mol Sci 19(10):3028. https://doi.org/10.3390/ijms19103028

    Article  CAS  PubMed Central  Google Scholar 

  7. Kalluri R (2016) The biology and function of fibroblasts in cancer. Nat Rev Cancer 16(9):582–598. https://doi.org/10.1038/nrc.2016.73

    Article  CAS  PubMed  Google Scholar 

  8. Rozario T, DeSimone DW (2010) The extracellular matrix in development and morphogenesis: a dynamic view. Dev Biol 341(1):126–140. https://doi.org/10.1016/j.ydbio.2009.10.026

    Article  CAS  PubMed  Google Scholar 

  9. Halper J, Kjaer M (2014) Basic components of connective tissues and extracellular matrix: elastin, fibrillin, fibulins, fibrinogen, fibronectin, laminin, tenascins and thrombospondins. Adv Exp Med Biol 802:31–47. https://doi.org/10.1007/978-94-007-7893-1_3

    Article  CAS  PubMed  Google Scholar 

  10. Singh B, Fleury C, Jalalvand F, Riesbeck K (2012) Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host. FEMS Microbiol Rev 36(6):1122–1180. https://doi.org/10.1111/j.1574-6976.2012.00340.x

    Article  CAS  PubMed  Google Scholar 

  11. Halfter W, Oertle P, Monnier CA, Camenzind L, Reyes-Lua M, Hu H, Candiello J, Labilloy A, Balasubramani M, Henrich PB, Plodinec M (2015) New concepts in basement membrane biology. FEBS J 282(23):4466–4479. https://doi.org/10.1111/febs.13495

    Article  CAS  PubMed  Google Scholar 

  12. Mak KM, Mei R (2017) Basement membrane type IV collagen and laminin: an overview of their biology and value as fibrosis biomarkers of liver disease. Anat Rec (Hoboken) 300(8):1371–1390. https://doi.org/10.1002/ar.23567

    Article  CAS  Google Scholar 

  13. McCarthy KJ (2015) The basement membrane proteoglycans perlecan and agrin: something old, something new. Curr Top Membr 76:255–303. https://doi.org/10.1016/bs.ctm.2015.09.001

    Article  PubMed  Google Scholar 

  14. Miller RT (2017) Mechanical properties of basement membrane in health and disease. Matrix Biol 57–58:366–373. https://doi.org/10.1016/j.matbio.2016.07.001

    Article  CAS  PubMed  Google Scholar 

  15. Randles MJ, Humphries MJ, Lennon R (2017) Proteomic definitions of basement membrane composition in health and disease. Matrix Biol 57–58:12–28. https://doi.org/10.1016/j.matbio.2016.08.006

    Article  CAS  PubMed  Google Scholar 

  16. Liang J, Jiang D, Noble PW (2016) Hyaluronan as a therapeutic target in human diseases. Adv Drug Deliv Rev 97:186–203. https://doi.org/10.1016/j.addr.2015.10.017

    Article  CAS  PubMed  Google Scholar 

  17. Iozzo RV, Schaefer L (2015) Proteoglycan form and function: a comprehensive nomenclature of proteoglycans. Matrix Biol 42:11–55. https://doi.org/10.1016/j.matbio.2015.02.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Schaefer L, Tredup C, Gubbiotti MA, Iozzo RV (2017) Proteoglycan neofunctions: regulation of inflammation and autophagy in cancer biology. FEBS J 284(1):10–26. https://doi.org/10.1111/febs.13963

    Article  CAS  PubMed  Google Scholar 

  19. Ricard-Blum S (2011) The collagen family. Cold Spring Harb Perspect Biol 3(1):a004978. https://doi.org/10.1101/cshperspect.a004978

    Article  PubMed  PubMed Central  Google Scholar 

  20. An B, Lin YS, Brodsky B (2016) Collagen interactions: drug design and delivery. Adv Drug Deliv Rev 97:69–84. https://doi.org/10.1016/j.addr.2015.11.013

    Article  CAS  PubMed  Google Scholar 

  21. Mao M, Alavi MV, Labelle-Dumais C, Gould DB (2015) Type IV collagens and basement membrane diseases: cell biology and pathogenic mechanisms. Curr Top Membr 76:61–116. https://doi.org/10.1016/bs.ctm.2015.09.002

    Article  PubMed  Google Scholar 

  22. Bhattacharjee A, Bansal M (2005) Collagen structure: the Madras triple helix and the current scenario. IUBMB Life 57(3):161–172. https://doi.org/10.1080/15216540500090710

    Article  CAS  PubMed  Google Scholar 

  23. Brodsky B, Persikov AV (2005) Molecular structure of the collagen triple helix. Adv Protein Chem 70:301–339. https://doi.org/10.1016/S0065-3233(05)70009-7

    Article  CAS  PubMed  Google Scholar 

  24. Beck K, Brodsky B (1998) Supercoiled protein motifs: the collagen triple-helix and the α-helical coiled coil. J Struct Biol 122(1–2):17–29. https://doi.org/10.1006/jsbi.1998.3965

    Article  CAS  PubMed  Google Scholar 

  25. Provenzano PP, Vanderby R Jr (2006) Collagen fibril morphology and organization: implications for force transmission in ligament and tendon. Matrix Biol 25(2):71–84. https://doi.org/10.1016/j.matbio.2005.09.005

    Article  CAS  PubMed  Google Scholar 

  26. Boudko SP, Danylevych N, Hudson BG, Pedchenko VK (2018) Basement membrane collagen IV: isolation of functional domains. Methods Cell Biol 143:171–185. https://doi.org/10.1016/bs.mcb.2017.08.010

    Article  PubMed  Google Scholar 

  27. Cummings CF, Pedchenko V, Brown KL, Colon S, Rafi M, Jones-Paris C, Pokydeshava E, Liu M, Pastor-Pareja JC, Stothers C, Ero-Tolliver IA, McCall AS, Vanacore R, Bhave G, Santoro S, Blackwell TS, Zent R, Pozzi A, Hudson BG (2016) Extracellular chloride signals collagen IV network assembly during basement membrane formation. J Cell Biol 213(4):479–494. https://doi.org/10.1083/jcb.201510065

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Vanacore RM, Friedman DB, Ham AJ, Sundaramoorthy M, Hudson BG (2005) Identification of S-hydroxylysyl-methionine as the covalent cross-link of the noncollagenous (NC1) hexamer of the α1α1α2 collagen IV network: a role for the post-translational modification of lysine 211 to hydroxylysine 211 in hexamer assembly. J Biol Chem 280(32):29300–29310. https://doi.org/10.1074/jbc.M502752200

    Article  CAS  PubMed  Google Scholar 

  29. Heljasvaara R, Aikio M, Ruotsalainen H, Pihlajaniemi T (2017) Collagen XVIII in tissue homeostasis and dysregulation—lessons learned from model organisms and human patients. Matrix Biol 57–58:55–75. https://doi.org/10.1016/j.matbio.2016.10.002

    Article  CAS  PubMed  Google Scholar 

  30. Shaw LM, Olsen BR (1991) FACIT collagens: diverse molecular bridges in extracellular matrices. Trends Biochem Sci 16(5):191–194

    Article  CAS  PubMed  Google Scholar 

  31. Has C, Bruckner-Tuderman L (2006) Molecular and diagnostic aspects of genetic skin fragility. J Dermatol Sci 44(3):129–144. https://doi.org/10.1016/j.jdermsci.2006.08.003

    Article  CAS  PubMed  Google Scholar 

  32. Barker HE, Cox TR, Erler JT (2012) The rationale for targeting the LOX family in cancer. Nat Rev Cancer 12(8):540–552. https://doi.org/10.1038/nrc3319

    Article  CAS  PubMed  Google Scholar 

  33. Eckert RL, Fisher ML, Grun D, Adhikary G, Xu W, Kerr C (2015) Transglutaminase is a tumor cell and cancer stem cell survival factor. Mol Carcinog 54(10):947–958. https://doi.org/10.1002/mc.22375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Li B, Cerione RA, Antonyak M (2011) Tissue transglutaminase and its role in human cancer progression. Adv Enzymol Relat Areas Mol Biol 78:247–293

    Article  CAS  PubMed  Google Scholar 

  35. Saitow CB, Wise SG, Weiss AS, Castellot JJ, Kaplan DL (2013) Elastin biology and tissue engineering with adult cells. Biomol Concepts 4(2):173–185. https://doi.org/10.1515/bmc-2012-0040

    Article  CAS  PubMed  Google Scholar 

  36. Kim YM, Kim EC, Kim Y (2011) The human lysyl oxidase-like 2 protein functions as an amine oxidase toward collagen and elastin. Mol Biol Rep 38(1):145–149. https://doi.org/10.1007/s11033-010-0088-0

    Article  CAS  PubMed  Google Scholar 

  37. Mezzenga R, Mitsi M (2018) The molecular dance of fibronectin: conformational flexibility leads to functional versatility. Biomacromol. https://doi.org/10.1021/acs.biomac.8b01258

    Article  Google Scholar 

  38. White ES, Muro AF (2011) Fibronectin splice variants: understanding their multiple roles in health and disease using engineered mouse models. IUBMB Life 63(7):538–546. https://doi.org/10.1002/iub.493

    Article  CAS  PubMed  Google Scholar 

  39. Kumra H, Reinhardt DP (2016) Fibronectin-targeted drug delivery in cancer. Adv Drug Deliv Rev 97:101–110. https://doi.org/10.1016/j.addr.2015.11.014

    Article  CAS  PubMed  Google Scholar 

  40. Woods A, Longley RL, Tumova S, Couchman JR (2000) Syndecan-4 binding to the high affinity heparin-binding domain of fibronectin drives focal adhesion formation in fibroblasts. Arch Biochem Biophys 374(1):66–72. https://doi.org/10.1006/abbi.1999.1607

    Article  CAS  PubMed  Google Scholar 

  41. Prasad A, Clark RA (2018) Fibronectin interaction with growth factors in the context of general ways extracellular matrix molecules regulate growth factor signaling. G Ital Dermatol Venereol 153(3):361–374. https://doi.org/10.23736/S0392-0488.18.05952-7

    Article  PubMed  Google Scholar 

  42. Dosio F, Arpicco S, Stella B, Fattal E (2016) Hyaluronic acid for anticancer drug and nucleic acid delivery. Adv Drug Deliv Rev 97:204–236. https://doi.org/10.1016/j.addr.2015.11.011

    Article  CAS  PubMed  Google Scholar 

  43. Neill T, Schaefer L, Iozzo RV (2016) Decorin as a multivalent therapeutic agent against cancer. Adv Drug Deliv Rev 97:174–185. https://doi.org/10.1016/j.addr.2015.10.016

    Article  CAS  PubMed  Google Scholar 

  44. Gubbiotti MA, Neill T, Iozzo RV (2017) A current view of perlecan in physiology and pathology: a mosaic of functions. Matrix Biol 57–58:285–298. https://doi.org/10.1016/j.matbio.2016.09.003

    Article  CAS  PubMed  Google Scholar 

  45. Harvey SJ, Miner JH (2008) Revisiting the glomerular charge barrier in the molecular era. Curr Opin Nephrol Hypertens 17(4):393–398. https://doi.org/10.1097/MNH.0b013e32830464de

    Article  CAS  PubMed  Google Scholar 

  46. Aumailley M (2013) The laminin family. Cell Adhes Migr 7(1):48–55. https://doi.org/10.4161/cam.22826

    Article  Google Scholar 

  47. Hohenester E, Engel J (2002) Domain structure and organisation in extracellular matrix proteins. Matrix Biol 21(2):115–128

    Article  CAS  PubMed  Google Scholar 

  48. Rousselle P, Beck K (2013) Laminin 332 processing impacts cellular behavior. Cell Adhes Migr 7(1):122–134. https://doi.org/10.4161/cam.23132

    Article  Google Scholar 

  49. Hohenester E, Yurchenco PD (2013) Laminins in basement membrane assembly. Cell Adhes Migr 7(1):56–63. https://doi.org/10.4161/cam.21831

    Article  Google Scholar 

  50. Thakur R, Mishra DP (2016) Matrix reloaded: CCN, tenascin and SIBLING group of matricellular proteins in orchestrating cancer hallmark capabilities. Pharmacol Ther 168:61–74. https://doi.org/10.1016/j.pharmthera.2016.09.002

    Article  CAS  PubMed  Google Scholar 

  51. Viloria K, Hill NJ (2016) Embracing the complexity of matricellular proteins: the functional and clinical significance of splice variation. Biomol Concepts 7(2):117–132. https://doi.org/10.1515/bmc-2016-0004

    Article  CAS  PubMed  Google Scholar 

  52. Sawyer AJ, Kyriakides TR (2016) Matricellular proteins in drug delivery: therapeutic targets, active agents, and therapeutic localization. Adv Drug Deliv Rev 97:56–68. https://doi.org/10.1016/j.addr.2015.12.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Sofeu Feugaing DD, Gotte M, Viola M (2013) More than matrix: the multifaceted role of decorin in cancer. Eur J Cell Biol 92(1):1–11. https://doi.org/10.1016/j.ejcb.2012.08.004

    Article  CAS  PubMed  Google Scholar 

  54. Yoshida T, Akatsuka T, Imanaka-Yoshida K (2015) Tenascin-C and integrins in cancer. Cell Adhes Migr 9(1–2):96–104. https://doi.org/10.1080/19336918.2015.1008332

    Article  CAS  Google Scholar 

  55. Brellier F, Martina E, Degen M, Heuze-Vourc’h N, Petit A, Kryza T, Courty Y, Terracciano L, Ruiz C, Chiquet-Ehrismann R (2012) Tenascin-W is a better cancer biomarker than tenascin-C for most human solid tumors. BMC Clin Pathol 12:14. https://doi.org/10.1186/1472-6890-12-14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Chiquet-Ehrismann R, Hagios C, Matsumoto K (1994) The tenascin gene family. Perspect Dev Neurobiol 2(1):3–7

    CAS  PubMed  Google Scholar 

  57. Bellahcene A, Castronovo V, Ogbureke KU, Fisher LW, Fedarko NS (2008) Small integrin-binding ligand N-linked glycoproteins (SIBLINGs): multifunctional proteins in cancer. Nat Rev Cancer 8(3):212–226. https://doi.org/10.1038/nrc2345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Kamili NA, Arthur CM, Gerner-Smidt C, Tafesse E, Blenda A, Dias-Baruffi M, Stowell SR (2016) Key regulators of galectin-glycan interactions. Proteomics 16(24):3111–3125. https://doi.org/10.1002/pmic.201600116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Naschberger E, Liebl A, Schellerer VS, Schutz M, Britzen-Laurent N, Kolbel P, Schaal U, Haep L, Regensburger D, Wittmann T, Klein-Hitpass L, Rau TT, Dietel B, Meniel VS, Clarke AR, Merkel S, Croner RS, Hohenberger W, Sturzl M (2016) Matricellular protein SPARCL1 regulates tumor microenvironment-dependent endothelial cell heterogeneity in colorectal carcinoma. J Clin Invest 126(11):4187–4204. https://doi.org/10.1172/JCI78260

    Article  PubMed  PubMed Central  Google Scholar 

  60. Roberts DD, Kaur S, Isenberg JS (2017) Regulation of cellular redox signaling by matricellular proteins in vascular biology, immunology, and cancer. Antioxid Redox Signal 27(12):874–911. https://doi.org/10.1089/ars.2017.7140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Gonzalez-Gonzalez L, Alonso J (2018) Periostin: a matricellular protein with multiple functions in cancer development and progression. Front Oncol 8:225. https://doi.org/10.3389/fonc.2018.00225

    Article  PubMed  PubMed Central  Google Scholar 

  62. Vincent KM, Postovit LM (2018) Matricellular proteins in cancer: a focus on secreted Frizzled-related proteins. J Cell Commun Signal 12(1):103–112. https://doi.org/10.1007/s12079-017-0398-2

    Article  PubMed  Google Scholar 

  63. Grosche J, Meissner J, Eble JA (2018) More than a syllable in fib-ROS-is: the role of ROS on the fibrotic extracellular matrix and on cellular contacts. Mol Aspects Med 63:30–46. https://doi.org/10.1016/j.mam.2018.03.005

    Article  CAS  PubMed  Google Scholar 

  64. Holle AW, Young JL, Van Vliet KJ, Kamm RD, Discher D, Janmey P, Spatz JP, Saif T (2018) Cell-extracellular matrix mechanobiology: forceful tools and emerging needs for basic and translational research. Nano Lett 18(1):1–8. https://doi.org/10.1021/acs.nanolett.7b04982

    Article  CAS  PubMed  Google Scholar 

  65. Stroka KM, Konstantopoulos K (2014) Physical biology in cancer. 4. Physical cues guide tumor cell adhesion and migration. Am J Physiol Cell Physiol 306(2):C98–C109. https://doi.org/10.1152/ajpcell.00289.2013

    Article  CAS  PubMed  Google Scholar 

  66. Barczyk M, Carracedo S, Gullberg D (2010) Integrins. Cell Tissue Res 339(1):269–280. https://doi.org/10.1007/s00441-009-0834-6

    Article  CAS  PubMed  Google Scholar 

  67. Campbell ID, Humphries MJ (2011) Integrin structure, activation, and interactions. Cold Spring Harb Perspect Biol 3(3):a004994. https://doi.org/10.1101/cshperspect.a004994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Humphries JD, Chastney MR, Askari JA, Humphries MJ (2018) Signal transduction via integrin adhesion complexes. Curr Opin Cell Biol 56:14–21. https://doi.org/10.1016/j.ceb.2018.08.004

    Article  CAS  PubMed  Google Scholar 

  69. Horton ER, Humphries JD, James J, Jones MC, Askari JA, Humphries MJ (2016) The integrin adhesome network at a glance. J Cell Sci 129(22):4159–4163. https://doi.org/10.1242/jcs.192054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, Waterman CM (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468(7323):580–584. https://doi.org/10.1038/nature09621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Winograd-Katz SE, Fassler R, Geiger B, Legate KR (2014) The integrin adhesome: from genes and proteins to human disease. Nat Rev Mol Cell Biol 15(4):273–288. https://doi.org/10.1038/nrm3769

    Article  CAS  PubMed  Google Scholar 

  72. Geiger B, Yamada KM (2011) Molecular architecture and function of matrix adhesions. Cold Spring Harb Perspect Biol 3(5):a005033. https://doi.org/10.1101/cshperspect.a005033

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Zaidel-Bar R, Geiger B (2010) The switchable integrin adhesome. J Cell Sci 123(Pt 9):1385–1388. https://doi.org/10.1242/jcs.066183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Carulli S, Beck K, Dayan G, Boulesteix S, Lortat-Jacob H, Rousselle P (2012) Cell surface proteoglycans syndecan-1 and -4 bind overlapping but distinct sites in laminin α3 LG45 protein domain. J Biol Chem 287(15):12204–12216. https://doi.org/10.1074/jbc.M111.300061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Bachy S, Letourneur F, Rousselle P (2008) Syndecan-1 interaction with the LG4/5 domain in laminin-332 is essential for keratinocyte migration. J Cell Physiol 214(1):238–249. https://doi.org/10.1002/jcp.21184

    Article  CAS  PubMed  Google Scholar 

  76. Soares MA, Teixeira FC, Fontes M, Areas AL, Leal MG, Pavao MS, Stelling MP (2015) Heparan sulfate proteoglycans may promote or inhibit cancer progression by interacting with integrins and affecting cell migration. Biomed Res Int 2015:453801. https://doi.org/10.1155/2015/453801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Pantazaka E, Papadimitriou E (2014) Chondroitin sulfate-cell membrane effectors as regulators of growth factor-mediated vascular and cancer cell migration. Biochim Biophys Acta 1840(8):2643–2650. https://doi.org/10.1016/j.bbagen.2014.01.009

    Article  CAS  PubMed  Google Scholar 

  78. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmouliere A, Varga J, De Wever O, Mareel M, Gabbiani G (2012) Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 180(4):1340–1355. https://doi.org/10.1016/j.ajpath.2012.02.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Otranto M, Sarrazy V, Bonte F, Hinz B, Gabbiani G, Desmouliere A (2012) The role of the myofibroblast in tumor stroma remodeling. Cell Adh Migr 6(3):203–219. https://doi.org/10.4161/cam.20377

    Article  PubMed  PubMed Central  Google Scholar 

  80. Dvorak HF (1986) Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 315(26):1650–1659. https://doi.org/10.1056/nejm198612253152606

    Article  CAS  PubMed  Google Scholar 

  81. Dvorak HF (2015) Tumors: wounds that do not heal-redux. Cancer Immunol Res 3(1):1–11. https://doi.org/10.1158/2326-6066.Cir-14-0209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Kuzet SE, Gaggioli C (2016) Fibroblast activation in cancer: when seed fertilizes soil. Cell Tissue Res 365(3):607–619. https://doi.org/10.1007/s00441-016-2467-x

    Article  CAS  PubMed  Google Scholar 

  83. Desmouliere A, Guyot C, Gabbiani G (2004) The stroma reaction myofibroblast: a key player in the control of tumor cell behavior. Int J Dev Biol 48(5–6):509–517. https://doi.org/10.1387/ijdb.041802ad

    Article  CAS  PubMed  Google Scholar 

  84. Caja L, Dituri F, Mancarella S, Caballero-Diaz D, Moustakas A, Giannelli G, Fabregat I (2018) TGF-β and the tissue microenvironment: relevance in fibrosis and cancer. Int J Mol Sci 19(5):1294. https://doi.org/10.3390/ijms19051294

    Article  CAS  PubMed Central  Google Scholar 

  85. Khan Z, Marshall JF (2016) The role of integrins in TGFβ activation in the tumour stroma. Cell Tissue Res 365(3):657–673. https://doi.org/10.1007/s00441-016-2474-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wang M, Zhao J, Zhang L, Wei F, Lian Y, Wu Y, Gong Z, Zhang S, Zhou J, Cao K, Li X, Xiong W, Li G, Zeng Z, Guo C (2017) Role of tumor microenvironment in tumorigenesis. J Cancer 8(5):761–773. https://doi.org/10.7150/jca.17648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Crotti S, Piccoli M, Rizzolio F, Giordano A, Nitti D, Agostini M (2017) Extracellular matrix and colorectal cancer: how surrounding microenvironment affects cancer cell behavior? J Cell Physiol 232(5):967–975. https://doi.org/10.1002/jcp.25658

    Article  CAS  PubMed  Google Scholar 

  88. Erdogan B, Webb DJ (2017) Cancer-associated fibroblasts modulate growth factor signaling and extracellular matrix remodeling to regulate tumor metastasis. Biochem Soc Trans 45(1):229–236. https://doi.org/10.1042/BST20160387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Cunderlikova B (2016) Clinical significance of immunohistochemically detected extracellular matrix proteins and their spatial distribution in primary cancer. Crit Rev Oncol Hematol 105:127–144. https://doi.org/10.1016/j.critrevonc.2016.04.017

    Article  CAS  PubMed  Google Scholar 

  90. Rizzacasa B, Morini E, Pucci S, Murdocca M, Novelli G, Amati F (2017) LOX-1 and its splice variants: a new challenge for atherosclerosis and cancer-targeted therapies. Int J Mol Sci 18(2):290. https://doi.org/10.3390/ijms18020290

    Article  CAS  PubMed Central  Google Scholar 

  91. Huang L, Xu AM, Liu W (2015) Transglutaminase 2 in cancer. Am J Cancer Res 5(9):2756–2776

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Rojas A, Anazco C, Gonzalez I, Araya P (2018) Extracellular matrix glycation and receptor for advanced glycation end-products activation: a missing piece in the puzzle of the association between diabetes and cancer. Carcinogenesis 39(4):515–521. https://doi.org/10.1093/carcin/bgy012

    Article  CAS  PubMed  Google Scholar 

  93. Malik R, Lelkes PI, Cukierman E (2015) Biomechanical and biochemical remodeling of stromal extracellular matrix in cancer. Trends Biotechnol 33(4):230–236. https://doi.org/10.1016/j.tibtech.2015.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Malik R, Luong T, Cao X, Han B, Shah N, Franco-Barraza J, Han L, Shenoy VB, Lelkes PI, Cukierman E (2018) Rigidity controls human desmoplastic matrix anisotropy to enable pancreatic cancer cell spread via extracellular signal-regulated kinase 2. Matrix Biol 1:2. https://doi.org/10.1016/j.matbio.2018.11.001

    Article  CAS  Google Scholar 

  95. Tolle RC, Gaggioli C, Dengjel J (2018) Three-dimensional cell culture conditions affect the proteome of cancer-associated fibroblasts. J Proteome Res 17(8):2780–2789. https://doi.org/10.1021/acs.jproteome.8b00237

    Article  CAS  PubMed  Google Scholar 

  96. Ronca R, Sozzani S, Presta M, Alessi P (2009) Delivering cytokines at tumor site: the immunocytokine-conjugated anti-EDB-fibronectin antibody case. Immunobiology 214(9–10):800–810. https://doi.org/10.1016/j.imbio.2009.06.005

    Article  CAS  PubMed  Google Scholar 

  97. Ramamonjisoa N, Ackerstaff E (2017) Characterization of the tumor microenvironment and tumor-stroma interaction by non-invasive preclinical imaging. Front Oncol 7:3. https://doi.org/10.3389/fonc.2017.00003

    Article  PubMed  PubMed Central  Google Scholar 

  98. Micke P, Ostman A (2004) Tumour-stroma interaction: cancer-associated fibroblasts as novel targets in anti-cancer therapy? Lung Cancer 45(Suppl 2):S163–S175. https://doi.org/10.1016/j.lungcan.2004.07.977

    Article  PubMed  Google Scholar 

  99. Hirata E, Sahai E (2017) Tumor microenvironment and differential responses to therapy. Cold Spring Harb Perspect Med 7(7):a026781. https://doi.org/10.1101/cshperspect.a026781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Topalovski M, Brekken RA (2016) Matrix control of pancreatic cancer: new insights into fibronectin signaling. Cancer Lett 381(1):252–258. https://doi.org/10.1016/j.canlet.2015.12.027

    Article  CAS  PubMed  Google Scholar 

  101. Zollinger AJ, Smith ML (2017) Fibronectin, the extracellular glue. Matrix Biol 60–61:27–37. https://doi.org/10.1016/j.matbio.2016.07.011

    Article  CAS  PubMed  Google Scholar 

  102. Han Z, Lu ZR (2017) Targeting fibronectin for cancer imaging and therapy. J Mater Chem B 5(4):639–654. https://doi.org/10.1039/C6TB02008A

    Article  CAS  PubMed  Google Scholar 

  103. Wang K, Seo BR, Fischbach C, Gourdon D (2016) Fibronectin mechanobiology regulates tumorigenesis. Cell Mol Bioeng 9:1–11. https://doi.org/10.1007/s12195-015-0417-4

    Article  CAS  PubMed  Google Scholar 

  104. Bachman H, Nicosia J, Dysart M, Barker TH (2015) Utilizing fibronectin integrin-binding specificity to control cellular responses. Adv Wound Care (New Rochelle) 4(8):501–511. https://doi.org/10.1089/wound.2014.0621

    Article  Google Scholar 

  105. Kanchanawong P, Waterman CM (2012) Advances in light-based imaging of three-dimensional cellular ultrastructure. Curr Opin Cell Biol 24(1):125–133. https://doi.org/10.1016/j.ceb.2011.11.010

    Article  CAS  PubMed  Google Scholar 

  106. Chiovaro F, Martina E, Bottos A, Scherberich A, Hynes NE, Chiquet-Ehrismann R (2015) Transcriptional regulation of tenascin-W by TGF-β signaling in the bone metastatic niche of breast cancer cells. Int J Cancer 137(8):1842–1854. https://doi.org/10.1002/ijc.29565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Adams JC, Chiquet-Ehrismann R, Tucker RP (2015) The evolution of tenascins and fibronectin. Cell Adhes Migr 9(1–2):22–33. https://doi.org/10.4161/19336918.2014.970030

    Article  CAS  Google Scholar 

  108. Martina E, Chiquet-Ehrismann R, Brellier F (2010) Tenascin-W: an extracellular matrix protein associated with osteogenesis and cancer. Int J Biochem Cell Biol 42(9):1412–1415. https://doi.org/10.1016/j.biocel.2010.06.004

    Article  CAS  PubMed  Google Scholar 

  109. Degen M, Brellier F, Schenk S, Driscoll R, Zaman K, Stupp R, Tornillo L, Terracciano L, Chiquet-Ehrismann R, Ruegg C, Seelentag W (2008) Tenascin-W, a new marker of cancer stroma, is elevated in sera of colon and breast cancer patients. Int J Cancer 122(11):2454–2461. https://doi.org/10.1002/ijc.23417

    Article  CAS  PubMed  Google Scholar 

  110. Degen M, Brellier F, Kain R, Ruiz C, Terracciano L, Orend G, Chiquet-Ehrismann R (2007) Tenascin-W is a novel marker for activated tumor stroma in low-grade human breast cancer and influences cell behavior. Cancer Res 67(19):9169–9179. https://doi.org/10.1158/0008-5472.CAN-07-0666

    Article  CAS  PubMed  Google Scholar 

  111. Kim BG, An HJ, Kang S, Choi YP, Gao MQ, Park H, Cho NH (2011) Laminin-332-rich tumor microenvironment for tumor invasion in the interface zone of breast cancer. Am J Pathol 178(1):373–381. https://doi.org/10.1016/j.ajpath.2010.11.028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  112. Tsuruta D, Kobayashi H, Imanishi H, Sugawara K, Ishii M, Jones JC (2008) Laminin-332-integrin interaction: a target for cancer therapy? Curr Med Chem 15(20):1968–1975

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Marinkovich MP (2007) Tumour microenvironment: laminin 332 in squamous-cell carcinoma. Nat Rev Cancer 7(5):370–380. https://doi.org/10.1038/nrc2089

    Article  CAS  PubMed  Google Scholar 

  114. Guess CM, Lafleur BJ, Weidow BL, Quaranta V (2009) A decreased ratio of laminin-332 β3 to gamma2 subunit mRNA is associated with poor prognosis in colon cancer. Cancer Epidemiol Biomark Prev 18(5):1584–1590. https://doi.org/10.1158/1055-9965.EPI-08-1027

    Article  CAS  Google Scholar 

  115. Guess CM, Quaranta V (2009) Defining the role of laminin-332 in carcinoma. Matrix Biol 28(8):445–455. https://doi.org/10.1016/j.matbio.2009.07.008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Chen J, Wang W, Wei J, Zhou D, Zhao X, Song W, Sun Q, Huang P, Zheng S (2015) Overexpression of β3 chains of laminin-332 is associated with clinicopathologic features and decreased survival in patients with pancreatic adenocarcinoma. Appl Immunohistochem Mol Morphol 23(7):516–521. https://doi.org/10.1097/PAI.0000000000000115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. Katayama M, Funakoshi A, Sumii T, Sanzen N, Sekiguchi K (2005) Laminin gamma2-chain fragment circulating level increases in patients with metastatic pancreatic ductal cell adenocarcinomas. Cancer Lett 225(1):167–176. https://doi.org/10.1016/j.canlet.2004.11.052

    Article  CAS  PubMed  Google Scholar 

  118. Ramovs V, Te Molder L, Sonnenberg A (2017) The opposing roles of laminin-binding integrins in cancer. Matrix Biol 57–58:213–243. https://doi.org/10.1016/j.matbio.2016.08.007

    Article  CAS  PubMed  Google Scholar 

  119. Yamada M, Sekiguchi K (2015) Molecular basis of laminin-integrin interactions. Curr Top Membr 76:197–229. https://doi.org/10.1016/bs.ctm.2015.07.002

    Article  PubMed  Google Scholar 

  120. Tripathi M, Nandana S, Yamashita H, Ganesan R, Kirchhofer D, Quaranta V (2008) Laminin-332 is a substrate for hepsin, a protease associated with prostate cancer progression. J Biol Chem 283(45):30576–30584. https://doi.org/10.1074/jbc.M802312200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Tripathi M, Potdar AA, Yamashita H, Weidow B, Cummings PT, Kirchhofer D, Quaranta V (2011) Laminin-332 cleavage by matriptase alters motility parameters of prostate cancer cells. Prostate 71(2):184–196. https://doi.org/10.1002/pros.21233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Cavaco ACM, Rezaei M, Caliandro MF, Lima AM, Stehling M, Dhayat SA, Haier J, Brakebusch C, Eble JA (2018) The interaction between laminin-332 and α3β1 integrin determines differentiation and maintenance of CAFs, and supports invasion of pancreatic duct adenocarcinoma cells. Cancers (Basel) 11(1):14. https://doi.org/10.3390/cancers11010014

    Article  Google Scholar 

  123. Luo Z, Wang Q, Lau WB, Lau B, Xu L, Zhao L, Yang H, Feng M, Xuan Y, Yang Y, Lei L, Wang C, Yi T, Zhao X, Wei Y, Zhou S (2016) Tumor microenvironment: the culprit for ovarian cancer metastasis? Cancer Lett 377(2):174–182. https://doi.org/10.1016/j.canlet.2016.04.038

    Article  CAS  PubMed  Google Scholar 

  124. Paszek MJ, Zahir N, Johnson KR, Lakins JN, Rozenberg GI, Gefen A, Reinhart-King CA, Margulies SS, Dembo M, Boettiger D, Hammer DA, Weaver VM (2005) Tensional homeostasis and the malignant phenotype. Cancer Cell 8(3):241–254. https://doi.org/10.1016/j.ccr.2005.08.010

    Article  CAS  PubMed  Google Scholar 

  125. Giussani M, Merlino G, Cappelletti V, Tagliabue E, Daidone MG (2015) Tumor-extracellular matrix interactions: identification of tools associated with breast cancer progression. Semin Cancer Biol 35:3–10. https://doi.org/10.1016/j.semcancer.2015.09.012

    Article  CAS  PubMed  Google Scholar 

  126. Sundquist E, Renko O, Salo S, Magga J, Cervigne NK, Nyberg P, Risteli J, Sormunen R, Vuolteenaho O, Zandonadi F, Paes Leme AF, Coletta RD, Ruskoaho H, Salo T (2016) Neoplastic extracellular matrix environment promotes cancer invasion in vitro. Exp Cell Res 344(2):229–240. https://doi.org/10.1016/j.yexcr.2016.04.003

    Article  CAS  PubMed  Google Scholar 

  127. Te Boekhorst V, Friedl P (2016) plasticity of cancer cell invasion-mechanisms and implications for therapy. Adv Cancer Res 132:209–264. https://doi.org/10.1016/bs.acr.2016.07.005

    Article  Google Scholar 

  128. Bhowmick NA, Neilson EG, Moses HL (2004) Stromal fibroblasts in cancer initiation and progression. Nature 432(7015):332–337. https://doi.org/10.1038/nature03096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Cavaco A, Rezaei M, Niland S, Eble JA (2017) Collateral damage intended: cancer-associated fibroblasts and vasculature are potential targets in cancer therapy. Int J Mol Sci 18(11):2355. https://doi.org/10.3390/ijms18112355

    Article  CAS  PubMed Central  Google Scholar 

  130. Marchiq I, Pouyssegur J (2016) Hypoxia, cancer metabolism and the therapeutic benefit of targeting lactate/H(+) symporters. J Mol Med (Berl) 94(2):155–171. https://doi.org/10.1007/s00109-015-1307-x

    Article  CAS  Google Scholar 

  131. Nielsen N, Lindemann O, Schwab A (2014) TRP channels and STIM/ORAI proteins: sensors and effectors of cancer and stroma cell migration. Br J Pharmacol 171(24):5524–5540. https://doi.org/10.1111/bph.12721

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Tochhawng L, Deng S, Pervaiz S, Yap CT (2013) Redox regulation of cancer cell migration and invasion. Mitochondrion 13(3):246–253. https://doi.org/10.1016/j.mito.2012.08.002

    Article  CAS  PubMed  Google Scholar 

  133. Xing Y, Zhao S, Zhou BP, Mi J (2015) Metabolic reprogramming of the tumour microenvironment. FEBS J 282(20):3892–3898. https://doi.org/10.1111/febs.13402

    Article  CAS  PubMed  Google Scholar 

  134. Baluna RG, Eng TY, Thomas CR (2006) Adhesion molecules in radiotherapy. Radiat Res 166(6):819–831. https://doi.org/10.1667/RR0380.1

    Article  CAS  PubMed  Google Scholar 

  135. Borek C (2004) Dietary antioxidants and human cancer. Integr Cancer Ther 3(4):333–341. https://doi.org/10.1177/1534735404270578

    Article  CAS  PubMed  Google Scholar 

  136. Westbury CB, Yarnold JR (2012) Radiation fibrosis–current clinical and therapeutic perspectives. Clin Oncol (R Coll Radiol) 24(10):657–672. https://doi.org/10.1016/j.clon.2012.04.001

    Article  CAS  Google Scholar 

  137. Yahyapour R, Motevaseli E, Rezaeyan A, Abdollahi H, Farhood B, Cheki M, Rezapoor S, Shabeeb D, Musa AE, Najafi M, Villa V (2018) Reduction-oxidation (redox) system in radiation-induced normal tissue injury: molecular mechanisms and implications in radiation therapeutics. Clin Transl Oncol 20(8):975–988. https://doi.org/10.1007/s12094-017-1828-6

    Article  CAS  PubMed  Google Scholar 

  138. Polanska UM, Orimo A (2013) Carcinoma-associated fibroblasts: non-neoplastic tumour-promoting mesenchymal cells. J Cell Physiol 228(8):1651–1657. https://doi.org/10.1002/jcp.24347

    Article  CAS  PubMed  Google Scholar 

  139. Koch S, Claesson-Welsh L (2012) Signal transduction by vascular endothelial growth factor receptors. Cold Spring Harb Perspect Med 2(7):a006502. https://doi.org/10.1101/cshperspect.a006502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Melincovici CS, Bosca AB, Susman S, Marginean M, Mihu C, Istrate M, Moldovan IM, Roman AL, Mihu CM (2018) Vascular endothelial growth factor (VEGF) - key factor in normal and pathological angiogenesis. Rom J Morphol Embryol 59(2):455–467

    PubMed  Google Scholar 

  141. Miyazono K, Katsuno Y, Koinuma D, Ehata S, Morikawa M (2018) Intracellular and extracellular TGF-β signaling in cancer: some recent topics. Front Med 12(4):387–411. https://doi.org/10.1007/s11684-018-0646-8

    Article  PubMed  Google Scholar 

  142. Crafts TD, Jensen AR, Blocher-Smith EC, Markel TA (2015) Vascular endothelial growth factor: therapeutic possibilities and challenges for the treatment of ischemia. Cytokine 71(2):385–393. https://doi.org/10.1016/j.cyto.2014.08.005

    Article  CAS  PubMed  Google Scholar 

  143. Iozzo RV, Sanderson RD (2011) Proteoglycans in cancer biology, tumour microenvironment and angiogenesis. J Cell Mol Med 15(5):1013–1031. https://doi.org/10.1111/j.1582-4934.2010.01236.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. Zanotelli MR, Reinhart-King CA (2018) Mechanical forces in tumor angiogenesis. Adv Exp Med Biol 1092:91–112. https://doi.org/10.1007/978-3-319-95294-9_6

    Article  PubMed  PubMed Central  Google Scholar 

  145. Edgar LT, Maas SA, Guilkey JE, Weiss JA (2015) A coupled model of neovessel growth and matrix mechanics describes and predicts angiogenesis in vitro. Biomech Model Mechanobiol 14(4):767–782. https://doi.org/10.1007/s10237-014-0635-z

    Article  PubMed  Google Scholar 

  146. Sund M, Xie L, Kalluri R (2004) The contribution of vascular basement membranes and extracellular matrix to the mechanics of tumor angiogenesis. APMIS 112(7–8):450–462. https://doi.org/10.1111/j.1600-0463.2004.t01-1-apm11207-0806.x

    Article  CAS  PubMed  Google Scholar 

  147. Knopik-Skrocka A, Kręplewska P, Jarmołowska-Jurczyszyn D (2017) Tumor blood vessels and vasculogenic mimicry – Current knowledge and searching for new cellular/molecular targets of anti-angiogenic therapy. Adv Cell Biol 5(1):50–71. https://doi.org/10.1515/acb-2017-0005

    Article  Google Scholar 

  148. Zuazo-Gaztelu I, Casanovas O (2018) Unraveling the role of angiogenesis in cancer ecosystems. Front Oncol 8:248. https://doi.org/10.3389/fonc.2018.00248

    Article  PubMed  PubMed Central  Google Scholar 

  149. Dudley AC (2012) Tumor endothelial cells. Cold Spring Harb Perspect Med 2(3):a006536. https://doi.org/10.1101/cshperspect.a006536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Angara K, Borin TF, Arbab AS (2017) Vascular mimicry: a novel neovascularization mechanism driving anti-angiogenic therapy (AAT) resistance in glioblastoma. Transl Oncol 10(4):650–660. https://doi.org/10.1016/j.tranon.2017.04.007

    Article  PubMed  PubMed Central  Google Scholar 

  151. Dunleavey JM, Dudley AC (2012) Vascular mimicry: concepts and implications for anti-angiogenic therapy. Curr Angiogenes 1(2):133–138. https://doi.org/10.2174/2211552811201020133

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Seftor RE, Hess AR, Seftor EA, Kirschmann DA, Hardy KM, Margaryan NV, Hendrix MJ (2012) Tumor cell vasculogenic mimicry: from controversy to therapeutic promise. Am J Pathol 181(4):1115–1125. https://doi.org/10.1016/j.ajpath.2012.07.013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Reid SE, Kay EJ, Neilson LJ, Henze AT, Serneels J, McGhee EJ, Dhayade S, Nixon C, Mackey JB, Santi A, Swaminathan K, Athineos D, Papalazarou V, Patella F, Roman-Fernandez A, ElMaghloob Y, Hernandez-Fernaud JR, Adams RH, Ismail S, Bryant DM, Salmeron-Sanchez M, Machesky LM, Carlin LM, Blyth K, Mazzone M, Zanivan S (2017) Tumor matrix stiffness promotes metastatic cancer cell interaction with the endothelium. EMBO J 36(16):2373–2389. https://doi.org/10.15252/embj.201694912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. Folberg R, Maniotis AJ (2004) Vasculogenic mimicry. APMIS 112(7–8):508–525. https://doi.org/10.1111/j.1600-0463.2004.apm11207-0810.x

    Article  PubMed  Google Scholar 

  155. Cao Z, Bao M, Miele L, Sarkar FH, Wang Z, Zhou Q (2013) Tumour vasculogenic mimicry is associated with poor prognosis of human cancer patients: a systemic review and meta-analysis. Eur J Cancer 49(18):3914–3923. https://doi.org/10.1016/j.ejca.2013.07.148

    Article  PubMed  Google Scholar 

  156. Hutchenreuther J, Vincent K, Norley C, Racanelli M, Gruber SB, Johnson TM, Fullen DR, Raskin L, Perbal B, Holdsworth DW, Postovit LM, Leask A (2018) Activation of cancer-associated fibroblasts is required for tumor neovascularization in a murine model of melanoma. Matrix Biol. https://doi.org/10.1016/j.matbio.2018.06.003

    Article  PubMed  Google Scholar 

  157. Seftor RE, Seftor EA, Kirschmann DA, Hendrix MJ (2002) Targeting the tumor microenvironment with chemically modified tetracyclines: inhibition of laminin 5 gamma2 chain promigratory fragments and vasculogenic mimicry. Mol Cancer Ther 1(13):1173–1179

    CAS  PubMed  Google Scholar 

  158. Qiao L, Liang N, Zhang J, Xie J, Liu F, Xu D, Yu X, Tian Y (2015) Advanced research on vasculogenic mimicry in cancer. J Cell Mol Med 19(2):315–326. https://doi.org/10.1111/jcmm.12496

    Article  PubMed  PubMed Central  Google Scholar 

  159. Velez DO, Tsui B, Goshia T, Chute CL, Han A, Carter H, Fraley SI (2017) 3D collagen architecture induces a conserved migratory and transcriptional response linked to vasculogenic mimicry. Nat Commun 8(1):1651. https://doi.org/10.1038/s41467-017-01556-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  160. Labelle M, Hynes RO (2012) The initial hours of metastasis: the importance of cooperative host-tumor cell interactions during hematogenous dissemination. Cancer Discov 2(12):1091–1099. https://doi.org/10.1158/2159-8290.CD-12-0329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  161. Sleeman JP, Cady B, Pantel K (2012) The connectivity of lymphogenous and hematogenous tumor cell dissemination: biological insights and clinical implications. Clin Exp Metastasis 29(7):737–746. https://doi.org/10.1007/s10585-012-9489-x

    Article  PubMed  Google Scholar 

  162. Zhu T, Hu X, Wei P, Shan G (2018) Molecular background of the regional lymph node metastasis of gastric cancer. Oncol Lett 15(3):3409–3414. https://doi.org/10.3892/ol.2018.7813

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Jones D, Pereira ER, Padera TP (2018) Growth and immune evasion of lymph node metastasis. Front Oncol 8:36. https://doi.org/10.3389/fonc.2018.00036

    Article  PubMed  PubMed Central  Google Scholar 

  164. Pircher A, Wolf D, Heidenreich A, Hilbe W, Pichler R, Heidegger I (2017) Synergies of targeting tumor angiogenesis and immune checkpoints in non-small cell lung cancer and renal cell cancer: from basic concepts to clinical reality. Int J Mol Sci 18(11):2291. https://doi.org/10.3390/ijms18112291

    Article  CAS  PubMed Central  Google Scholar 

  165. Schito L (2018) Bridging angiogenesis and immune evasion in the hypoxic tumor microenvironment. Am J Physiol Regul Integr Comp Physiol 1:4. https://doi.org/10.1152/ajpregu.00209.2018

    Article  CAS  Google Scholar 

  166. Cimpean AM, Tamma R, Ruggieri S, Nico B, Toma A, Ribatti D (2017) Mast cells in breast cancer angiogenesis. Crit Rev Oncol Hematol 115:23–26. https://doi.org/10.1016/j.critrevonc.2017.04.009

    Article  PubMed  Google Scholar 

  167. Gajewski TF, Schreiber H, Fu YX (2013) Innate and adaptive immune cells in the tumor microenvironment. Nat Immunol 14(10):1014–1022. https://doi.org/10.1038/ni.2703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Quail DF, Joyce JA (2013) Microenvironmental regulation of tumor progression and metastasis. Nat Med 19(11):1423–1437. https://doi.org/10.1038/nm.3394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  169. Sangaletti S, Chiodoni C, Tripodo C, Colombo MP (2017) The good and bad of targeting cancer-associated extracellular matrix. Curr Opin Pharmacol 35:75–82. https://doi.org/10.1016/j.coph.2017.06.003

    Article  CAS  PubMed  Google Scholar 

  170. Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM (2012) Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012:948098. https://doi.org/10.1155/2012/948098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  171. Shevach EM (2009) Mechanisms of foxp3 + T regulatory cell-mediated suppression. Immunity 30(5):636–645. https://doi.org/10.1016/j.immuni.2009.04.010

    Article  CAS  PubMed  Google Scholar 

  172. Sica A, Massarotti M (2017) Myeloid suppressor cells in cancer and autoimmunity. J Autoimmun 85:117–125. https://doi.org/10.1016/j.jaut.2017.07.010

    Article  CAS  PubMed  Google Scholar 

  173. Zhao H, Liao X, Kang Y (2017) Tregs: where we are and what comes next? Front Immunol 8:1578. https://doi.org/10.3389/fimmu.2017.01578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  174. Dermani FK, Samadi P, Rahmani G, Kohlan AK, Najafi R (2019) PD-1/PD-L1 immune checkpoint: potential target for cancer therapy. J Cell Physiol 234(2):1313–1325. https://doi.org/10.1002/jcp.27172

    Article  CAS  PubMed  Google Scholar 

  175. Hahn AW, Gill DM, Pal SK, Agarwal N (2017) The future of immune checkpoint cancer therapy after PD-1 and CTLA-4. Immunotherapy 9(8):681–692. https://doi.org/10.2217/imt-2017-0024

    Article  CAS  PubMed  Google Scholar 

  176. Hatae R, Chamoto K (2016) Immune checkpoint inhibitors targeting programmed cell death-1 (PD-1) in cancer therapy. Rinsho Ketsueki 57(10):2224–2231. https://doi.org/10.11406/rinketsu.57.2224

    Article  PubMed  Google Scholar 

  177. Chakravarthy A, Khan L, Bensler NP, Bose P, De Carvalho DD (2018) TGF-β-associated extracellular matrix genes link cancer-associated fibroblasts to immune evasion and immunotherapy failure. Nat Commun 9(1):4692. https://doi.org/10.1038/s41467-018-06654-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Rhee I (2016) Diverse macrophages polarization in tumor microenvironment. Arch Pharm Res 39(11):1588–1596. https://doi.org/10.1007/s12272-016-0820-y

    Article  CAS  PubMed  Google Scholar 

  179. Torcellan T, Stolp J, Chtanova T (2017) In vivo imaging sheds light on immune cell migration and function in cancer. Front Immunol 8:309. https://doi.org/10.3389/fimmu.2017.00309

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Jacquemet G, Hamidi H, Ivaska J (2015) Filopodia in cell adhesion, 3D migration and cancer cell invasion. Curr Opin Cell Biol 36:23–31. https://doi.org/10.1016/j.ceb.2015.06.007

    Article  CAS  PubMed  Google Scholar 

  181. Angst BD, Marcozzi C, Magee AI (2001) The cadherin superfamily. J Cell Sci 114(Pt 4):625–626

    CAS  PubMed  Google Scholar 

  182. Bertocchi C, Wang Y, Ravasio A, Hara Y, Wu Y, Sailov T, Baird MA, Davidson MW, Zaidel-Bar R, Toyama Y, Ladoux B, Mege RM, Kanchanawong P (2017) Nanoscale architecture of cadherin-based cell adhesions. Nat Cell Biol 19(1):28–37. https://doi.org/10.1038/ncb3456

    Article  CAS  PubMed  Google Scholar 

  183. Gloushankova NA, Rubtsova SN, Zhitnyak IY (2017) Cadherin-mediated cell-cell interactions in normal and cancer cells. Tissue Barriers 5(3):e1356900. https://doi.org/10.1080/21688370.2017.1356900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  184. Harrison OJ, Jin X, Hong S, Bahna F, Ahlsen G, Brasch J, Wu Y, Vendome J, Felsovalyi K, Hampton CM, Troyanovsky RB, Ben-Shaul A, Frank J, Troyanovsky SM, Shapiro L, Honig B (2011) The extracellular architecture of adherens junctions revealed by crystal structures of type I cadherins. Structure 19(2):244–256. https://doi.org/10.1016/j.str.2010.11.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  185. Leckband DE, de Rooij J (2014) Cadherin adhesion and mechanotransduction. Annu Rev Cell Dev Biol 30:291–315. https://doi.org/10.1146/annurev-cellbio-100913-013212

    Article  CAS  PubMed  Google Scholar 

  186. Cichon MA, Radisky DC (2014) Extracellular matrix as a contextual determinant of transforming growth factor-β signaling in epithelial-mesenchymal transition and in cancer. Cell Adhes Migr 8(6):588–594. https://doi.org/10.4161/19336918.2014.972788

    Article  Google Scholar 

  187. Pietila M, Ivaska J, Mani SA (2016) Whom to blame for metastasis, the epithelial-mesenchymal transition or the tumor microenvironment? Cancer Lett 380(1):359–368. https://doi.org/10.1016/j.canlet.2015.12.033

    Article  CAS  PubMed  Google Scholar 

  188. Yu Y, Xiao CH, Tan LD, Wang QS, Li XQ, Feng YM (2014) Cancer-associated fibroblasts induce epithelial-mesenchymal transition of breast cancer cells through paracrine TGF-β signalling. Br J Cancer 110(3):724–732. https://doi.org/10.1038/bjc.2013.768

    Article  CAS  PubMed  Google Scholar 

  189. Eatemadi A, Aiyelabegan HT, Negahdari B, Mazlomi MA, Daraee H, Daraee N, Eatemadi R, Sadroddiny E (2017) Role of protease and protease inhibitors in cancer pathogenesis and treatment. Biomed Pharmacother 86:221–231. https://doi.org/10.1016/j.biopha.2016.12.021

    Article  CAS  PubMed  Google Scholar 

  190. Wolf K, Friedl P (2011) Extracellular matrix determinants of proteolytic and non-proteolytic cell migration. Trends Cell Biol 21(12):736–744. https://doi.org/10.1016/j.tcb.2011.09.006

    Article  CAS  PubMed  Google Scholar 

  191. Stefanidakis M, Koivunen E (2006) Cell-surface association between matrix metalloproteinases and integrins: role of the complexes in leukocyte migration and cancer progression. Blood 108(5):1441–1450. https://doi.org/10.1182/blood-2006-02-005363

    Article  CAS  PubMed  Google Scholar 

  192. Nagase H, Visse R, Murphy G (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 69(3):562–573. https://doi.org/10.1016/j.cardiores.2005.12.002

    Article  CAS  PubMed  Google Scholar 

  193. Jacob A, Prekeris R (2015) The regulation of MMP targeting to invadopodia during cancer metastasis. Front Cell Dev Biol 3:4. https://doi.org/10.3389/fcell.2015.00004

    Article  PubMed  PubMed Central  Google Scholar 

  194. Ren F, Tang R, Zhang X, Madushi WM, Luo D, Dang Y, Li Z, Wei K, Chen G (2015) Overexpression of MMP family members functions as prognostic biomarker for breast cancer patients: a systematic review and meta-analysis. PLoS ONE 10(8):e0135544. https://doi.org/10.1371/journal.pone.0135544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  195. Vandooren J, Van den Steen PE, Opdenakker G (2013) Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9): the next decade. Crit Rev Biochem Mol Biol 48(3):222–272. https://doi.org/10.3109/10409238.2013.770819

    Article  CAS  PubMed  Google Scholar 

  196. Huang H (2018) Matrix metalloproteinase-9 (MMP-9) as a cancer biomarker and MMP-9 biosensors: recent advances. Sensors (Basel) 18(10):3249. https://doi.org/10.3390/s18103249

    Article  CAS  Google Scholar 

  197. Zhang X, Huang S, Guo J, Zhou L, You L, Zhang T, Zhao Y (2016) Insights into the distinct roles of MMP-11 in tumor biology and future therapeutics (review). Int J Oncol 48(5):1783–1793. https://doi.org/10.3892/ijo.2016.3400

    Article  CAS  PubMed  Google Scholar 

  198. Castro-Castro A, Marchesin V, Monteiro P, Lodillinsky C, Rosse C, Chavrier P (2016) Cellular and molecular mechanisms of MT1-MMP-dependent cancer cell invasion. Annu Rev Cell Dev Biol 32:555–576. https://doi.org/10.1146/annurev-cellbio-111315-125227

    Article  CAS  PubMed  Google Scholar 

  199. Pahwa S, Stawikowski MJ, Fields GB (2014) Monitoring and inhibiting MT1-MMP during cancer initiation and progression. Cancers (Basel) 6(1):416–435. https://doi.org/10.3390/cancers6010416

    Article  CAS  Google Scholar 

  200. Alcantara MB, Dass CR (2013) Regulation of MT1-MMP and MMP-2 by the serpin PEDF: a promising new target for metastatic cancer. Cell Physiol Biochem 31(4–5):487–494. https://doi.org/10.1159/000350069

    Article  CAS  PubMed  Google Scholar 

  201. Poincloux R, Lizarraga F, Chavrier P (2009) Matrix invasion by tumour cells: a focus on MT1-MMP trafficking to invadopodia. J Cell Sci 122(Pt 17):3015–3024. https://doi.org/10.1242/jcs.034561

    Article  CAS  PubMed  Google Scholar 

  202. Radisky ES, Radisky DC (2015) Matrix metalloproteinases as breast cancer drivers and therapeutic targets. Front Biosci 20:1144–1163. https://doi.org/10.2741/4364

    Article  CAS  Google Scholar 

  203. Parvanescu V, Georgescu M, Georgescu I, Surlin V, Patrascu S, Picleanu AM, Georgescu E (2015) The role of matrix metalloproteinase-9 (MMP-9) as a prognostic factor in epithelial and lymphatic neoplasia. Chirurgia (Bucur) 110(6):506–510

    CAS  Google Scholar 

  204. Tam EM, Moore TR, Butler GS, Overall CM (2004) Characterization of the distinct collagen binding, helicase and cleavage mechanisms of matrix metalloproteinase 2 and 14 (gelatinase A and MT1-MMP): the differential roles of the MMP hemopexin c domains and the MMP-2 fibronectin type II modules in collagen triple helicase activities. J Biol Chem 279(41):43336–43344. https://doi.org/10.1074/jbc.M407186200

    Article  CAS  PubMed  Google Scholar 

  205. Farina AR, Mackay AR (2014) Gelatinase B/MMP-9 in tumour pathogenesis and progression. Cancers (Basel) 6(1):240–296. https://doi.org/10.3390/cancers6010240

    Article  CAS  Google Scholar 

  206. Overall CM (2001) Matrix metalloproteinase substrate binding domains, modules and exosites. Overview and experimental strategies. Methods Mol Biol 151:79–120

    CAS  PubMed  Google Scholar 

  207. Thakur V, Bedogni B (2016) The membrane tethered matrix metalloproteinase MT1-MMP at the forefront of melanoma cell invasion and metastasis. Pharmacol Res 111:17–22. https://doi.org/10.1016/j.phrs.2016.05.019

    Article  CAS  PubMed  Google Scholar 

  208. Sato H, Takino T (2010) Coordinate action of membrane-type matrix metalloproteinase-1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion. Cancer Sci 101(4):843–847. https://doi.org/10.1111/j.1349-7006.2010.01498.x

    Article  CAS  PubMed  Google Scholar 

  209. Saad S, Gottlieb DJ, Bradstock KF, Overall CM, Bendall LJ (2002) Cancer cell-associated fibronectin induces release of matrix metalloproteinase-2 from normal fibroblasts. Cancer Res 62(1):283–289

    CAS  PubMed  Google Scholar 

  210. Itoh Y (2006) MT1-MMP: a key regulator of cell migration in tissue. IUBMB Life 58(10):589–596. https://doi.org/10.1080/15216540600962818

    Article  CAS  PubMed  Google Scholar 

  211. Itoh Y, Seiki M (2006) MT1-MMP: a potent modifier of pericellular microenvironment. J Cell Physiol 206(1):1–8. https://doi.org/10.1002/jcp.20431

    Article  CAS  PubMed  Google Scholar 

  212. Eddy RJ, Weidmann MD, Sharma VP, Condeelis JS (2017) Tumor cell invadopodia: invasive protrusions that orchestrate metastasis. Trends Cell Biol 27(8):595–607. https://doi.org/10.1016/j.tcb.2017.03.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  213. Revach OY, Geiger B (2014) The interplay between the proteolytic, invasive, and adhesive domains of invadopodia and their roles in cancer invasion. Cell Adhes Migr 8(3):215–225

    Article  Google Scholar 

  214. Bagnato A, Rosano L (2018) Endothelin-1 receptor drives invadopodia: exploiting how β-arrestin-1 guides the way. Small GTPases 9(5):394–398. https://doi.org/10.1080/21541248.2016.1235526

    Article  CAS  PubMed  Google Scholar 

  215. Alekhina O, Burstein E, Billadeau DD (2017) Cellular functions of WASP family proteins at a glance. J Cell Sci 130(14):2235–2241. https://doi.org/10.1242/jcs.199570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  216. Frugtniet B, Jiang WG, Martin TA (2015) Role of the WASP and WAVE family proteins in breast cancer invasion and metastasis. Breast Cancer (Dove Med Press) 7:99–109. https://doi.org/10.2147/BCTT.S59006

    Article  CAS  PubMed Central  Google Scholar 

  217. Parekh A, Weaver AM (2016) Regulation of invadopodia by mechanical signaling. Exp Cell Res 343(1):89–95. https://doi.org/10.1016/j.yexcr.2015.10.038

    Article  CAS  PubMed  Google Scholar 

  218. Jeannot P, Besson A (2017) Cortactin function in invadopodia. Small GTPases. https://doi.org/10.1080/21541248.2017.1405773

    Article  PubMed  Google Scholar 

  219. Linder S (2007) The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol 17(3):107–117. https://doi.org/10.1016/j.tcb.2007.01.002

    Article  CAS  PubMed  Google Scholar 

  220. Nicholas NS, Pipili A, Lesjak MS, Wells CM (2017) Differential role for PAK1 and PAK4 during the invadopodia lifecycle. Small GTPases. https://doi.org/10.1080/21541248.2017.1295830

    Article  PubMed  PubMed Central  Google Scholar 

  221. Seano G, Primo L (2015) Podosomes and invadopodia: tools to breach vascular basement membrane. Cell Cycle 14(9):1370–1374. https://doi.org/10.1080/15384101.2015.1026523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  222. Deryugina EI, Quigley JP (2015) Tumor angiogenesis: MMP-mediated induction of intravasation- and metastasis-sustaining neovasculature. Matrix Biol 44–46:94–112. https://doi.org/10.1016/j.matbio.2015.04.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  223. Genis L, Galvez BG, Gonzalo P, Arroyo AG (2006) MT1-MMP: universal or particular player in angiogenesis? Cancer Metastasis Rev 25(1):77–86. https://doi.org/10.1007/s10555-006-7891-z

    Article  PubMed  Google Scholar 

  224. Binder MJ, McCoombe S, Williams ED, McCulloch DR, Ward AC (2017) The extracellular matrix in cancer progression: role of hyalectan proteoglycans and ADAMTS enzymes. Cancer Lett 385:55–64. https://doi.org/10.1016/j.canlet.2016.11.001

    Article  CAS  PubMed  Google Scholar 

  225. Branch KM, Hoshino D, Weaver AM (2012) Adhesion rings surround invadopodia and promote maturation. Biol Open 1(8):711–722. https://doi.org/10.1242/bio.20121867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  226. Zara M, Canobbio I, Visconte C, Canino J, Torti M, Guidetti GF (2018) Molecular mechanisms of platelet activation and aggregation induced by breast cancer cells. Cell Signal 48:45–53. https://doi.org/10.1016/j.cellsig.2018.04.008

    Article  CAS  PubMed  Google Scholar 

  227. Covic L, Kuliopulos A (2018) Protease-activated receptor 1 as therapeutic target in breast, lung, and ovarian cancer: pepducin approach. Int J Mol Sci 19(8):2237. https://doi.org/10.3390/ijms19082237

    Article  CAS  PubMed Central  Google Scholar 

  228. Liu X, Yu J, Song S, Yue X, Li Q (2017) Protease-activated receptor-1 (PAR-1): a promising molecular target for cancer. Oncotarget 8(63):107334–107345. https://doi.org/10.18632/oncotarget.21015

    Article  PubMed  PubMed Central  Google Scholar 

  229. Monboisse JC, Oudart JB, Ramont L, Brassart-Pasco S (1840) Maquart FX (2014) Matrikines from basement membrane collagens: a new anti-cancer strategy. Biochim Biophys Acta 8:2589–2598. https://doi.org/10.1016/j.bbagen.2013.12.029

    Article  CAS  Google Scholar 

  230. Tran KT, Lamb P, Deng JS (2005) Matrikines and matricryptins: implications for cutaneous cancers and skin repair. J Dermatol Sci 40(1):11–20. https://doi.org/10.1016/j.jdermsci.2005.05.001

    Article  CAS  PubMed  Google Scholar 

  231. Hornebeck W, Maquart FX (2003) Proteolyzed matrix as a template for the regulation of tumor progression. Biomed Pharmacother 57(5–6):223–230

    Article  CAS  PubMed  Google Scholar 

  232. Ramont L, Brassart-Pasco S, Thevenard J, Deshorgue A, Venteo L, Laronze JY, Pluot M, Monboisse JC, Maquart FX (2007) The NC1 domain of type XIX collagen inhibits in vivo melanoma growth. Mol Cancer Ther 6(2):506–514. https://doi.org/10.1158/1535-7163.MCT-06-0207

    Article  CAS  PubMed  Google Scholar 

  233. Brassart-Pasco S, Senechal K, Thevenard J, Ramont L, Devy J, Di Stefano L, Dupont-Deshorgue A, Brezillon S, Feru J, Jazeron JF, Diebold MD, Ricard-Blum S, Maquart FX, Monboisse JC (2012) Tetrastatin, the NC1 domain of the α4(IV) collagen chain: a novel potent anti-tumor matrikine. PLoS ONE 7(4):e29587. https://doi.org/10.1371/journal.pone.0029587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  234. Folkman J (2006) Antiangiogenesis in cancer therapy–endostatin and its mechanisms of action. Exp Cell Res 312(5):594–607. https://doi.org/10.1016/j.yexcr.2005.11.015

    Article  CAS  PubMed  Google Scholar 

  235. Liu X, Nie W, Xie Q, Chen G, Li X, Jia Y, Yin B, Qu X, Li Y, Liang J (2018) Endostatin reverses immunosuppression of the tumor microenvironment in lung carcinoma. Oncol Lett 15(2):1874–1880. https://doi.org/10.3892/ol.2017.7455

    Article  CAS  PubMed  Google Scholar 

  236. Hope C, Emmerich PB, Papadas A, Pagenkopf A, Matkowskyj KA, Van De Hey DR, Payne SN, Clipson L, Callander NS, Hematti P, Miyamoto S, Johnson MG, Deming DA, Asimakopoulos F (2017) Versican-derived matrikines regulate Batf3-dendritic cell differentiation and promote T cell infiltration in colorectal cancer. J Immunol 199(5):1933–1941. https://doi.org/10.4049/jimmunol.1700529

    Article  CAS  PubMed  Google Scholar 

  237. Poluzzi C, Iozzo RV, Schaefer L (2016) Endostatin and endorepellin: a common route of action for similar angiostatic cancer avengers. Adv Drug Deliv Rev 97:156–173. https://doi.org/10.1016/j.addr.2015.10.012

    Article  CAS  PubMed  Google Scholar 

  238. Woodall BP, Nystrom A, Iozzo RA, Eble JA, Niland S, Krieg T, Eckes B, Pozzi A, Iozzo RV (2008) Integrin α2β1 is the required receptor for endorepellin angiostatic activity. J Biol Chem 283(4):2335–2343. https://doi.org/10.1074/jbc.M708364200

    Article  CAS  PubMed  Google Scholar 

  239. Grahovac J, Wells A (2014) Matrikine and matricellular regulators of EGF receptor signaling on cancer cell migration and invasion. Lab Invest 94(1):31–40. https://doi.org/10.1038/labinvest.2013.132

    Article  CAS  PubMed  Google Scholar 

  240. Da Silva J, Lameiras P, Beljebbar A, Berquand A, Villemin M, Ramont L, Dukic S, Nuzillard JM, Molinari M, Gautier M, Brassart-Pasco S, Brassart B (2018) Structural characterization and in vivo pro-tumor properties of a highly conserved matrikine. Oncotarget 9(25):17839–17857. https://doi.org/10.18632/oncotarget.24894

    Article  PubMed  PubMed Central  Google Scholar 

  241. Scandolera A, Odoul L, Salesse S, Guillot A, Blaise S, Kawecki C, Maurice P, El Btaouri H, Romier-Crouzet B, Martiny L, Debelle L, Duca L (2016) The elastin receptor complex: a unique matricellular receptor with high anti-tumoral potential. Front Pharmacol 7:32. https://doi.org/10.3389/fphar.2016.00032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  242. Duca L, Floquet N, Alix AJ, Haye B, Debelle L (2004) Elastin as a matrikine. Crit Rev Oncol Hematol 49(3):235–244. https://doi.org/10.1016/j.critrevonc.2003.09.007

    Article  PubMed  Google Scholar 

  243. Alexander S, Friedl P (2012) Cancer invasion and resistance: interconnected processes of disease progression and therapy failure. Trends Mol Med 18(1):13–26. https://doi.org/10.1016/j.molmed.2011.11.003

    Article  PubMed  Google Scholar 

  244. Devreotes P, Horwitz AR (2015) Signaling networks that regulate cell migration. Cold Spring Harb Perspect Biol 7(8):a005959. https://doi.org/10.1101/cshperspect.a005959

    Article  PubMed  PubMed Central  Google Scholar 

  245. Ridley AJ, Schwartz MA, Burridge K, Firtel RA, Ginsberg MH, Borisy G, Parsons JT, Horwitz AR (2003) Cell migration: integrating signals from front to back. Science 302(5651):1704–1709. https://doi.org/10.1126/science.1092053

    Article  CAS  PubMed  Google Scholar 

  246. Schwartz MA, Horwitz AR (2006) Integrating adhesion, protrusion, and contraction during cell migration. Cell 125(7):1223–1225. https://doi.org/10.1016/j.cell.2006.06.015

    Article  CAS  PubMed  Google Scholar 

  247. Vicente-Manzanares M, Horwitz AR (2011) Cell migration: an overview. Methods Mol Biol 769:1–24. https://doi.org/10.1007/978-1-61779-207-6_1

    Article  CAS  PubMed  Google Scholar 

  248. Vicente-Manzanares M, Webb DJ, Horwitz AR (2005) Cell migration at a glance. J Cell Sci 118(Pt 21):4917–4919. https://doi.org/10.1242/jcs.02662

    Article  CAS  PubMed  Google Scholar 

  249. Aguilar-Cuenca R, Juanes-Garcia A, Vicente-Manzanares M (2014) Myosin II in mechanotransduction: master and commander of cell migration, morphogenesis, and cancer. Cell Mol Life Sci 71(3):479–492. https://doi.org/10.1007/s00018-013-1439-5

    Article  CAS  PubMed  Google Scholar 

  250. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR (2009) Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 10(11):778–790. https://doi.org/10.1038/nrm2786

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  251. Vicente-Manzanares M, Choi CK, Horwitz AR (2009) Integrins in cell migration–the actin connection. J Cell Sci 122(Pt 2):199–206. https://doi.org/10.1242/jcs.018564

    Article  CAS  PubMed  Google Scholar 

  252. Yamaguchi H, Condeelis J (2007) Regulation of the actin cytoskeleton in cancer cell migration and invasion. Biochim Biophys Acta 1773(5):642–652. https://doi.org/10.1016/j.bbamcr.2006.07.001

    Article  CAS  PubMed  Google Scholar 

  253. Ungefroren H, Witte D, Lehnert H (2018) The role of small GTPases of the Rho/Rac family in TGF-β-induced EMT and cell motility in cancer. Dev Dyn 247(3):451–461. https://doi.org/10.1002/dvdy.24505

    Article  CAS  PubMed  Google Scholar 

  254. Lawson CD, Ridley AJ (2018) Rho GTPase signaling complexes in cell migration and invasion. J Cell Biol 217(2):447–457. https://doi.org/10.1083/jcb.201612069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  255. Casalou C, Faustino A, Barral DC (2016) Arf proteins in cancer cell migration. Small GTPases 7(4):270–282. https://doi.org/10.1080/21541248.2016.1228792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  256. Kale VP, Hengst JA, Desai DH, Amin SG, Yun JK (2015) The regulatory roles of ROCK and MRCK kinases in the plasticity of cancer cell migration. Cancer Lett 361(2):185–196. https://doi.org/10.1016/j.canlet.2015.03.017

    Article  CAS  PubMed  Google Scholar 

  257. Huttenlocher A, Horwitz AR (2011) Integrins in cell migration. Cold Spring Harb Perspect Biol 3(9):a005074. https://doi.org/10.1101/cshperspect.a005074

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  258. Bays JL, DeMali KA (2017) Vinculin in cell-cell and cell-matrix adhesions. Cell Mol Life Sci 74(16):2999–3009. https://doi.org/10.1007/s00018-017-2511-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  259. Goldmann WH (2016) Role of vinculin in cellular mechanotransduction. Cell Biol Int 40(3):241–256. https://doi.org/10.1002/cbin.10563

    Article  PubMed  Google Scholar 

  260. Grashoff C, Hoffman BD, Brenner MD, Zhou R, Parsons M, Yang MT, McLean MA, Sligar SG, Chen CS, Ha T, Schwartz MA (2010) Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466(7303):263–266. https://doi.org/10.1038/nature09198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  261. Ehrlicher AJ, Krishnan R, Guo M, Bidan CM, Weitz DA, Pollak MR (2015) Α-actinin binding kinetics modulate cellular dynamics and force generation. Proc Natl Acad Sci U S A 112(21):6619–6624. https://doi.org/10.1073/pnas.1505652112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  262. Roca-Cusachs P, del Rio A, Puklin-Faucher E, Gauthier NC, Biais N, Sheetz MP (2013) Integrin-dependent force transmission to the extracellular matrix by α-actinin triggers adhesion maturation. Proc Natl Acad Sci USA 110(15):E1361–E1370. https://doi.org/10.1073/pnas.1220723110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  263. Carisey A, Tsang R, Greiner AM, Nijenhuis N, Heath N, Nazgiewicz A, Kemkemer R, Derby B, Spatz J, Ballestrem C (2013) Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr Biol 23(4):271–281. https://doi.org/10.1016/j.cub.2013.01.009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  264. Zaidel-Bar R, Milo R, Kam Z, Geiger B (2007) A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120(Pt 1):137–148. https://doi.org/10.1242/jcs.03314

    Article  CAS  PubMed  Google Scholar 

  265. Bays JL, Peng X, Tolbert CE, Guilluy C, Angell AE, Pan Y, Superfine R, Burridge K, DeMali KA (2014) Vinculin phosphorylation differentially regulates mechanotransduction at cell-cell and cell-matrix adhesions. J Cell Biol 205(2):251–263. https://doi.org/10.1083/jcb.201309092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  266. Dobrokhotov O, Samsonov M, Sokabe M, Hirata H (2018) Mechanoregulation and pathology of YAP/TAZ via Hippo and non-Hippo mechanisms. Clin Transl Med 7(1):23. https://doi.org/10.1186/s40169-018-0202-9

    Article  PubMed  PubMed Central  Google Scholar 

  267. Noguchi S, Saito A, Nagase T (2018) YAP/TAZ signaling as a molecular link between fibrosis and cancer. Int J Mol Sci 19(11):3674. https://doi.org/10.3390/ijms19113674

    Article  CAS  PubMed Central  Google Scholar 

  268. Zanconato F, Cordenonsi M, Piccolo S (2016) YAP/TAZ at the roots of cancer. Cancer Cell 29(6):783–803. https://doi.org/10.1016/j.ccell.2016.05.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  269. Palecek SP, Loftus JC, Ginsberg MH, Lauffenburger DA, Horwitz AF (1997) Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385(6616):537–540. https://doi.org/10.1038/385537a0

    Article  CAS  PubMed  Google Scholar 

  270. Gritsenko PG, Ilina O, Friedl P (2012) Interstitial guidance of cancer invasion. J Pathol 226(2):185–199. https://doi.org/10.1002/path.3031

    Article  CAS  PubMed  Google Scholar 

  271. Wolf K, Alexander S, Schacht V, Coussens LM, von Andrian UH, van Rheenen J, Deryugina E, Friedl P (2009) Collagen-based cell migration models in vitro and in vivo. Semin Cell Dev Biol 20(8):931–941. https://doi.org/10.1016/j.semcdb.2009.08.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  272. Deng J, Zhao C, Spatz JP, Wei Q (2017) Nanopatterned adhesive, stretchable hydrogel to control ligand spacing and regulate cell spreading and migration. ACS Nano 11(8):8282–8291. https://doi.org/10.1021/acsnano.7b03449

    Article  CAS  PubMed  Google Scholar 

  273. Arnold M, Hirschfeld-Warneken VC, Lohmuller T, Heil P, Blummel J, Cavalcanti-Adam EA, Lopez-Garcia M, Walther P, Kessler H, Geiger B, Spatz JP (2008) Induction of cell polarization and migration by a gradient of nanoscale variations in adhesive ligand spacing. Nano Lett 8(7):2063–2069. https://doi.org/10.1021/nl801483w

    Article  CAS  PubMed  Google Scholar 

  274. Alfano M, Nebuloni M, Allevi R, Zerbi P, Longhi E, Luciano R, Locatelli I, Pecoraro A, Indrieri M, Speziali C, Doglioni C, Milani P, Montorsi F, Salonia A (2016) Linearized texture of three-dimensional extracellular matrix is mandatory for bladder cancer cell invasion. Sci Rep 6:36128. https://doi.org/10.1038/srep36128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  275. Krause M, Wolf K (2015) Cancer cell migration in 3D tissue: negotiating space by proteolysis and nuclear deformability. Cell Adh Migr 9(5):357–366. https://doi.org/10.1080/19336918.2015.1061173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  276. Wolf K, Te Lindert M, Krause M, Alexander S, Te Riet J, Willis AL, Hoffman RM, Figdor CG, Weiss SJ, Friedl P (2013) Physical limits of cell migration: control by ECM space and nuclear deformation and tuning by proteolysis and traction force. J Cell Biol 201(7):1069–1084. https://doi.org/10.1083/jcb.201210152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  277. Denais CM, Gilbert RM, Isermann P, McGregor AL, te Lindert M, Weigelin B, Davidson PM, Friedl P, Wolf K, Lammerding J (2016) Nuclear envelope rupture and repair during cancer cell migration. Science 352(6283):353–358. https://doi.org/10.1126/science.aad7297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  278. Petrie RJ, Yamada KM (2016) Multiple mechanisms of 3D migration: the origins of plasticity. Curr Opin Cell Biol 42:7–12. https://doi.org/10.1016/j.ceb.2016.03.025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  279. Doyle AD, Petrie RJ, Kutys ML, Yamada KM (2013) Dimensions in cell migration. Curr Opin Cell Biol 25(5):642–649. https://doi.org/10.1016/j.ceb.2013.06.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  280. Petrie RJ, Harlin HM, Korsak LI, Yamada KM (2017) Activating the nuclear piston mechanism of 3D migration in tumor cells. J Cell Biol 216(1):93–100. https://doi.org/10.1083/jcb.201605097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  281. Friedl P, Locker J, Sahai E, Segall JE (2012) Classifying collective cancer cell invasion. Nat Cell Biol 14(8):777–783. https://doi.org/10.1038/ncb2548

    Article  CAS  PubMed  Google Scholar 

  282. Friedl P, Gilmour D (2009) Collective cell migration in morphogenesis, regeneration and cancer. Nat Rev Mol Cell Biol 10(7):445–457. https://doi.org/10.1038/nrm2720

    Article  CAS  PubMed  Google Scholar 

  283. Khalil AA, Ilina O, Gritsenko PG, Bult P, Span PN, Friedl P (2017) Collective invasion in ductal and lobular breast cancer associates with distant metastasis. Clin Exp Metastasis 34(6–7):421–429. https://doi.org/10.1007/s10585-017-9858-6

    Article  PubMed  PubMed Central  Google Scholar 

  284. Das T, Spatz JP (2016) Getting a grip on collective cell migration. Nat Cell Biol 18(12):1265–1267. https://doi.org/10.1038/ncb3447

    Article  CAS  PubMed  Google Scholar 

  285. Park JA, Atia L, Mitchel JA, Fredberg JJ, Butler JP (2016) Collective migration and cell jamming in asthma, cancer and development. J Cell Sci 129(18):3375–3383. https://doi.org/10.1242/jcs.187922

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  286. Ramos Gde O, Bernardi L, Lauxen I, Sant’Ana Filho M, Horwitz AR, Lamers ML (2016) Fibronectin modulates cell adhesion and signaling to promote single cell migration of highly invasive oral squamous cell carcinoma. PLoS ONE 11(3):e0151338. https://doi.org/10.1371/journal.pone.0151338

    Article  CAS  PubMed  Google Scholar 

  287. Wolf K, Wu YI, Liu Y, Geiger J, Tam E, Overall C, Stack MS, Friedl P (2007) Multi-step pericellular proteolysis controls the transition from individual to collective cancer cell invasion. Nat Cell Biol 9(8):893–904. https://doi.org/10.1038/ncb1616

    Article  CAS  PubMed  Google Scholar 

  288. Han T, Kang D, Ji D, Wang X, Zhan W, Fu M, Xin HB, Wang JB (2013) How does cancer cell metabolism affect tumor migration and invasion? Cell Adh Migr 7(5):395–403. https://doi.org/10.4161/cam.26345

    Article  PubMed  PubMed Central  Google Scholar 

  289. Lehmann S, Te Boekhorst V, Odenthal J, Bianchi R, van Helvert S, Ikenberg K, Ilina O, Stoma S, Xandry J, Jiang L, Grenman R, Rudin M, Friedl P (2017) Hypoxia induces a HIF-1-dependent transition from collective-to-amoeboid dissemination in epithelial cancer cells. Curr Biol 27(3):392–400. https://doi.org/10.1016/j.cub.2016.11.057

    Article  CAS  PubMed  Google Scholar 

  290. Gaggioli C, Hooper S, Hidalgo-Carcedo C, Grosse R, Marshall JF, Harrington K, Sahai E (2007) Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat Cell Biol 9(12):1392–1400. https://doi.org/10.1038/ncb1658

    Article  CAS  PubMed  Google Scholar 

  291. Erpenbeck L, Schön MP (2010) Deadly allies: the fatal interplay between platelets and metastizing cancer cells. Blood 115(17):3427–3436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  292. Camerer E (2004) Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood 104:397–401

    Article  CAS  PubMed  Google Scholar 

  293. Weisel JW, Litvinov RI (2017) Fibrin formation, structure and properties. Subcell Biochem 82:405–456. https://doi.org/10.1007/978-3-319-49674-0_13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  294. O’Sullivan JM, Preston RJS, Robson T, O’Donnell JS (2018) Emerging Roles for von Willebrand Factor in Cancer Cell Biology. Semin Thromb Hemost 44(2):159–166. https://doi.org/10.1055/s-0037-1607352

    Article  CAS  PubMed  Google Scholar 

  295. Bauer AT, Suckau J, Frank K, Desch A, Goertz L, Wagner AH, Hecker M, Goerge T, Umansky L, Beckhove P, Utikal J, Gorzelanny C, Diaz-Valdes N, Umansky V, Schneider SW (2015) von Willebrand factor fibers promote cancer-associated platelet aggregation in malignant melanoma of mice and humans. Blood 125(20):3153–3163. https://doi.org/10.1182/blood-2014-08-595686

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  296. Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A, Rodrigues G, Psaila B, Kaplan RN, Bromberg JF, Kang Y, Bissell MJ, Cox TR, Giaccia AJ, Erler JT, Hiratsuka S, Ghajar CM, Lyden D (2017) Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer 17(5):302–317. https://doi.org/10.1038/nrc.2017.6

    Article  CAS  PubMed  Google Scholar 

  297. Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9(4):285–293. https://doi.org/10.1038/nrc2621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  298. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, Molina H, Kohsaka S, Di Giannatale A, Ceder S, Singh S, Williams C, Soplop N, Uryu K, Pharmer L, King T, Bojmar L, Davies AE, Ararso Y, Zhang T, Zhang H, Hernandez J, Weiss JM, Dumont-Cole VD, Kramer K, Wexler LH, Narendran A, Schwartz GK, Healey JH, Sandstrom P, Labori KJ, Kure EH, Grandgenett PM, Hollingsworth MA, de Sousa M, Kaur S, Jain M, Mallya K, Batra SK, Jarnagin WR, Brady MS, Fodstad O, Muller V, Pantel K, Minn AJ, Bissell MJ, Garcia BA, Kang Y, Rajasekhar VK, Ghajar CM, Matei I, Peinado H, Bromberg J, Lyden D (2015) Tumour exosome integrins determine organotropic metastasis. Nature 527(7578):329–335. https://doi.org/10.1038/nature15756

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  299. Geraud C, Koch PS, Damm F, Schledzewski K, Goerdt S (2014) The metastatic cycle: metastatic niches and cancer cell dissemination. J Dtsch Dermatol Ges 12(11):1012–1019. https://doi.org/10.1111/ddg.12451

    Article  PubMed  Google Scholar 

  300. Aguado BA, Bushnell GG, Rao SS, Jeruss JS, Shea LD (2017) Engineering the pre-metastatic niche. Nat Biomed Eng 1. https://doi.org/10.1038/s41551-017-0077

  301. Liu Y, Cao X (2016) Characteristics and significance of the pre-metastatic niche. Cancer Cell 30(5):668–681. https://doi.org/10.1016/j.ccell.2016.09.011

    Article  CAS  PubMed  Google Scholar 

  302. Rezaeeyan H, Shirzad R, McKee TD, Saki N (2018) Role of chemokines in metastatic niche: new insights along with a diagnostic and prognostic approach. APMIS 126(5):359–370. https://doi.org/10.1111/apm.12818

    Article  CAS  PubMed  Google Scholar 

  303. Nogues L, Benito-Martin A, Hergueta-Redondo M, Peinado H (2018) The influence of tumour-derived extracellular vesicles on local and distal metastatic dissemination. Mol Aspects Med 60:15–26. https://doi.org/10.1016/j.mam.2017.11.012

    Article  CAS  PubMed  Google Scholar 

  304. Lobb RJ, Lima LG, Moller A (2017) Exosomes: key mediators of metastasis and pre-metastatic niche formation. Semin Cell Dev Biol 67:3–10. https://doi.org/10.1016/j.semcdb.2017.01.004

    Article  CAS  PubMed  Google Scholar 

  305. Gartland A, Erler JT, Cox TR (2016) The role of lysyl oxidase, the extracellular matrix and the pre-metastatic niche in bone metastasis. J Bone Oncol 5(3):100–103. https://doi.org/10.1016/j.jbo.2016.04.001

    Article  PubMed  PubMed Central  Google Scholar 

  306. Peinado H, Lavotshkin S, Lyden D (2011) The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 21(2):139–146. https://doi.org/10.1016/j.semcancer.2011.01.002

    Article  CAS  PubMed  Google Scholar 

  307. Hoye AM, Erler JT (2016) Structural ECM components in the premetastatic and metastatic niche. Am J Physiol Cell Physiol 310(11):C955–C967. https://doi.org/10.1152/ajpcell.00326.2015

    Article  PubMed  Google Scholar 

  308. Descot A, Oskarsson T (2013) The molecular composition of the metastatic niche. Exp Cell Res 319(11):1679–1686. https://doi.org/10.1016/j.yexcr.2013.04.017

    Article  CAS  PubMed  Google Scholar 

  309. Cox TR, Rumney RMH, Schoof EM, Perryman L, Hoye AM, Agrawal A, Bird D, Latif NA, Forrest H, Evans HR, Huggins ID, Lang G, Linding R, Gartland A, Erler JT (2015) The hypoxic cancer secretome induces pre-metastatic bone lesions through lysyl oxidase. Nature 522(7554):106–110. https://doi.org/10.1038/nature14492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  310. El-Haibi CP, Bell GW, Zhang J, Collmann AY, Wood D, Scherber CM, Csizmadia E, Mariani O, Zhu C, Campagne A, Toner M, Bhatia SN, Irimia D, Vincent-Salomon A, Karnoub AE (2012) Critical role for lysyl oxidase in mesenchymal stem cell-driven breast cancer malignancy. Proc Natl Acad Sci USA 109(43):17460–17465. https://doi.org/10.1073/pnas.1206653109

    Article  PubMed  PubMed Central  Google Scholar 

  311. Pickup MW, Laklai H, Acerbi I, Owens P, Gorska AE, Chytil A, Aakre M, Weaver VM, Moses HL (2013) Stromally derived lysyl oxidase promotes metastasis of transforming growth factor-β-deficient mouse mammary carcinomas. Cancer Res 73(17):5336–5346. https://doi.org/10.1158/0008-5472.CAN-13-0012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  312. Jablonska J, Lang S, Sionov RV, Granot Z (2017) The regulation of pre-metastatic niche formation by neutrophils. Oncotarget 8(67):112132–112144. https://doi.org/10.18632/oncotarget.22792

    Article  PubMed  PubMed Central  Google Scholar 

  313. Yumoto K, Eber MR, Berry JE, Taichman RS, Shiozawa Y (2014) Molecular pathways: niches in metastatic dormancy. Clin Cancer Res 20(13):3384–3389. https://doi.org/10.1158/1078-0432.CCR-13-0897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  314. Oskarsson T, Batlle E, Massague J (2014) Metastatic stem cells: sources, niches, and vital pathways. Cell Stem Cell 14(3):306–321. https://doi.org/10.1016/j.stem.2014.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  315. Leprini A, Querze G, Zardi L (1994) Tenascin isoforms: possible targets for diagnosis and therapy of cancer and mechanisms regulating their expression. Perspect Dev Neurobiol 2(1):117–123

    CAS  PubMed  Google Scholar 

  316. Nicolo G, Salvi S, Oliveri G, Borsi L, Castellani P, Zardi L (1990) Expression of tenascin and of the ED-B containing oncofetal fibronectin isoform in human cancer. Cell Differ Dev 32(3):401–408

    Article  CAS  PubMed  Google Scholar 

  317. Vandooren J, Opdenakker G, Loadman PM, Edwards DR (2016) Proteases in cancer drug delivery. Adv Drug Deliv Rev 97:144–155. https://doi.org/10.1016/j.addr.2015.12.020

    Article  CAS  PubMed  Google Scholar 

  318. Piperigkou Z, Manou D, Karamanou K, Theocharis AD (2018) Strategies to target matrix metalloproteinases as therapeutic approach in cancer. Methods Mol Biol 1731:325–348. https://doi.org/10.1007/978-1-4939-7595-2_27

    Article  CAS  PubMed  Google Scholar 

  319. Gingras D, Batist G, Beliveau R (2001) AE-941 (Neovastat): a novel multifunctional antiangiogenic compound. Expert Rev Anticancer Ther 1(3):341–347. https://doi.org/10.1586/14737140.1.3.341

    Article  CAS  PubMed  Google Scholar 

  320. Gingras D, Boivin D, Deckers C, Gendron S, Barthomeuf C, Beliveau R (2003) Neovastat–a novel antiangiogenic drug for cancer therapy. Anticancer Drugs 14(2):91–96. https://doi.org/10.1097/01.cad.0000054520.85618.3f

    Article  CAS  PubMed  Google Scholar 

  321. Lu C, Lee JJ, Komaki R, Herbst RS, Feng L, Evans WK, Choy H, Desjardins P, Esparaz BT, Truong MT, Saxman S, Kelaghan J, Bleyer A, Fisch MJ (2010) Chemoradiotherapy with or without AE-941 in stage III non-small cell lung cancer: a randomized phase III trial. J Natl Cancer Inst 102(12):859–865. https://doi.org/10.1093/jnci/djq179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  322. Rizvi NA, Humphrey JS, Ness EA, Johnson MD, Gupta E, Williams K, Daly DJ, Sonnichsen D, Conway D, Marshall J, Hurwitz H (2004) A phase I study of oral BMS-275291, a novel nonhydroxamate sheddase-sparing matrix metalloproteinase inhibitor, in patients with advanced or metastatic cancer. Clin Cancer Res 10(6):1963–1970

    Article  CAS  PubMed  Google Scholar 

  323. Leighl NB, Paz-Ares L, Douillard JY, Peschel C, Arnold A, Depierre A, Santoro A, Betticher DC, Gatzemeier U, Jassem J, Crawford J, Tu D, Bezjak A, Humphrey JS, Voi M, Galbraith S, Hann K, Seymour L, Shepherd FA (2005) Randomized phase III study of matrix metalloproteinase inhibitor BMS-275291 in combination with paclitaxel and carboplatin in advanced non-small-cell lung cancer: National Cancer Institute of Canada-Clinical Trials Group Study BR.18. J Clin Oncol 23(12):2831–2839. https://doi.org/10.1200/JCO.2005.04.044

    Article  CAS  PubMed  Google Scholar 

  324. Hirte H, Vergote IB, Jeffrey JR, Grimshaw RN, Coppieters S, Schwartz B, Tu D, Sadura A, Brundage M, Seymour L (2006) A phase III randomized trial of BAY 12-9566 (tanomastat) as maintenance therapy in patients with advanced ovarian cancer responsive to primary surgery and paclitaxel/platinum containing chemotherapy: a National Cancer Institute of Canada Clinical Trials Group Study. Gynecol Oncol 102(2):300–308. https://doi.org/10.1016/j.ygyno.2005.12.020

    Article  CAS  PubMed  Google Scholar 

  325. Hande KR, Collier M, Paradiso L, Stuart-Smith J, Dixon M, Clendeninn N, Yeun G, Alberti D, Binger K, Wilding G (2004) Phase I and pharmacokinetic study of prinomastat, a matrix metalloprotease inhibitor. Clin Cancer Res 10(3):909–915

    Article  CAS  PubMed  Google Scholar 

  326. Bissett D, O’Byrne KJ, von Pawel J, Gatzemeier U, Price A, Nicolson M, Mercier R, Mazabel E, Penning C, Zhang MH, Collier MA, Shepherd FA (2005) Phase III study of matrix metalloproteinase inhibitor prinomastat in non-small-cell lung cancer. J Clin Oncol 23(4):842–849. https://doi.org/10.1200/JCO.2005.03.170

    Article  CAS  PubMed  Google Scholar 

  327. Paemen L, Martens E, Masure S, Opdenakker G (1995) Monoclonal antibodies specific for natural human neutrophil gelatinase B used for affinity purification, quantitation by two-site ELISA and inhibition of enzymatic activity. Eur J Biochem 234(3):759–765

    Article  CAS  PubMed  Google Scholar 

  328. Martens E, Leyssen A, Van Aelst I, Fiten P, Piccard H, Hu J, Descamps FJ, Van den Steen PE, Proost P, Van Damme J, Liuzzi GM, Riccio P, Polverini E, Opdenakker G (2007) A monoclonal antibody inhibits gelatinase B/MMP-9 by selective binding to part of the catalytic domain and not to the fibronectin or zinc binding domains. Biochim Biophys Acta 1770(2):178–186. https://doi.org/10.1016/j.bbagen.2006.10.012

    Article  CAS  PubMed  Google Scholar 

  329. Devy L, Huang L, Naa L, Yanamandra N, Pieters H, Frans N, Chang E, Tao Q, Vanhove M, Lejeune A, van Gool R, Sexton DJ, Kuang G, Rank D, Hogan S, Pazmany C, Ma YL, Schoonbroodt S, Nixon AE, Ladner RC, Hoet R, Henderikx P, Tenhoor C, Rabbani SA, Valentino ML, Wood CR, Dransfield DT (2009) Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis. Cancer Res 69(4):1517–1526. https://doi.org/10.1158/0008-5472.CAN-08-3255

    Article  CAS  PubMed  Google Scholar 

  330. Lemaitre V, D’Armiento J (2006) Matrix metalloproteinases in development and disease. Birth Defects Res C 78(1):1–10. https://doi.org/10.1002/bdrc.20065

    Article  CAS  Google Scholar 

  331. Li L, Li H (2013) Role of microRNA-mediated MMP regulation in the treatment and diagnosis of malignant tumors. Cancer Biol Ther 14(9):796–805. https://doi.org/10.4161/cbt.25936

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  332. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS, Krichevsky AM (2008) MicroRNA 21 promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 28(17):5369–5380. https://doi.org/10.1128/MCB.00479-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  333. Costa PM, Cardoso AL, Custodia C, Cunha P, Pereira de Almeida L, Pedroso de Lima MC (2015) MiRNA-21 silencing mediated by tumor-targeted nanoparticles combined with sunitinib: a new multimodal gene therapy approach for glioblastoma. J Control Release 207:31–39. https://doi.org/10.1016/j.jconrel.2015.04.002

    Article  CAS  PubMed  Google Scholar 

  334. Chan N, Willis A, Kornhauser N, Ward MM, Lee SB, Nackos E, Seo BR, Chuang E, Cigler T, Moore A, Donovan D, Vallee Cobham M, Fitzpatrick V, Schneider S, Wiener A, Guillaume-Abraham J, Aljom E, Zelkowitz R, Warren JD, Lane ME, Fischbach C, Mittal V, Vahdat L (2017) Influencing the tumor microenvironment: a phase II study of copper depletion using tetrathiomolybdate in patients with breast cancer at high risk for recurrence and in preclinical models of lung metastases. Clin Cancer Res 23(3):666–676. https://doi.org/10.1158/1078-0432.CCR-16-1326

    Article  CAS  PubMed  Google Scholar 

  335. Hecht JR, Benson AB 3rd, Vyushkov D, Yang Y, Bendell J, Verma U (2017) A phase II, randomized, double-blind, placebo-controlled study of simtuzumab in combination with FOLFIRI for the second-line treatment of metastatic KRAS mutant colorectal adenocarcinoma. Oncologist 22(3):243-e223. https://doi.org/10.1634/theoncologist.2016-0479

    Article  CAS  Google Scholar 

  336. Benson AB 3rd, Wainberg ZA, Hecht JR, Vyushkov D, Dong H, Bendell J, Kudrik F (2017) A phase II randomized, double-blind, placebo-controlled study of simtuzumab or placebo in combination with gemcitabine for the first-line treatment of pancreatic adenocarcinoma. Oncologist 22(3):241-e215. https://doi.org/10.1634/theoncologist.2017-0024

    Article  CAS  Google Scholar 

  337. Barry-Hamilton V, Spangler R, Marshall D, McCauley S, Rodriguez HM, Oyasu M, Mikels A, Vaysberg M, Ghermazien H, Wai C, Garcia CA, Velayo AC, Jorgensen B, Biermann D, Tsai D, Green J, Zaffryar-Eilot S, Holzer A, Ogg S, Thai D, Neufeld G, Van Vlasselaer P, Smith V (2010) Allosteric inhibition of lysyl oxidase-like-2 impedes the development of a pathologic microenvironment. Nat Med 16(9):1009–1017. https://doi.org/10.1038/nm.2208

    Article  CAS  PubMed  Google Scholar 

  338. Rodriguez HM, Vaysberg M, Mikels A, McCauley S, Velayo AC, Garcia C, Smith V (2010) Modulation of lysyl oxidase-like 2 enzymatic activity by an allosteric antibody inhibitor. J Biol Chem 285(27):20964–20974. https://doi.org/10.1074/jbc.M109.094136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  339. Rasmussen HS, McCann PP (1997) Matrix metalloproteinase inhibition as a novel anticancer strategy: a review with special focus on batimastat and marimastat. Pharmacol Ther 75(1):69–75

    Article  CAS  PubMed  Google Scholar 

  340. Cathcart J, Pulkoski-Gross A, Cao J (2015) Targeting matrix metalloproteinases in cancer: bringing new life to old ideas. Genes Dis 2(1):26–34. https://doi.org/10.1016/j.gendis.2014.12.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  341. Rao BG (2005) Recent developments in the design of specific matrix metalloproteinase inhibitors aided by structural and computational studies. Curr Pharm Des 11(3):295–322

    Article  CAS  PubMed  Google Scholar 

  342. Au JL, Yeung BZ, Wientjes MG, Lu Z, Wientjes MG (2016) Delivery of cancer therapeutics to extracellular and intracellular targets: determinants, barriers, challenges and opportunities. Adv Drug Deliv Rev 97:280–301. https://doi.org/10.1016/j.addr.2015.12.002

    Article  CAS  PubMed  Google Scholar 

  343. Rodriguez-Cabello JC, Arias FJ, Rodrigo MA, Girotti A (2016) Elastin-like polypeptides in drug delivery. Adv Drug Deliv Rev 97:85–100. https://doi.org/10.1016/j.addr.2015.12.007

    Article  CAS  PubMed  Google Scholar 

  344. Arosio D, Casagrande C (2016) Advancement in integrin facilitated drug delivery. Adv Drug Deliv Rev 97:111–143. https://doi.org/10.1016/j.addr.2015.12.001

    Article  CAS  PubMed  Google Scholar 

  345. Multhaupt HA, Leitinger B, Gullberg D, Couchman JR (2016) Extracellular matrix component signaling in cancer. Adv Drug Deliv Rev 97:28–40. https://doi.org/10.1016/j.addr.2015.10.013

    Article  CAS  PubMed  Google Scholar 

  346. Hinderer S, Layland SL, Schenke-Layland K (2016) ECM and ECM-like materials—biomaterials for applications in regenerative medicine and cancer therapy. Adv Drug Deliv Rev 97:260–269. https://doi.org/10.1016/j.addr.2015.11.019

    Article  CAS  PubMed  Google Scholar 

  347. Celia-Terrassa T, Kang Y (2018) Metastatic niche functions and therapeutic opportunities. Nat Cell Biol 20(8):868–877. https://doi.org/10.1038/s41556-018-0145-9

    Article  CAS  PubMed  Google Scholar 

  348. Ordonez-Moran P, Huelsken J (2014) Complex metastatic niches: already a target for therapy? Curr Opin Cell Biol 31:29–38. https://doi.org/10.1016/j.ceb.2014.06.012

    Article  CAS  PubMed  Google Scholar 

  349. Horton ER, Astudillo P, Humphries MJ, Humphries JD (2016) Mechanosensitivity of integrin adhesion complexes: role of the consensus adhesome. Exp Cell Res 343(1):7–13. https://doi.org/10.1016/j.yexcr.2015.10.025

    Article  CAS  PubMed  Google Scholar 

  350. Murphy DA, Courtneidge SA (2011) The ‘ins’ and ‘outs’ of podosomes and invadopodia: characteristics, formation and function. Nat Rev Mol Cell Biol 12(7):413–426. https://doi.org/10.1038/nrm3141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  351. Leitinger B, Hohenester E (2007) Mammalian collagen receptors. Matrix Biol 26(3):146–155. https://doi.org/10.1016/j.matbio.2006.10.007

    Article  CAS  PubMed  Google Scholar 

  352. Torres PH, Sousa GL, Pascutti PG (2011) Structural analysis of the N-terminal fragment of the antiangiogenic protein endostatin: a molecular dynamics study. Proteins 79(9):2684–2692. https://doi.org/10.1002/prot.23096

    Article  CAS  PubMed  Google Scholar 

  353. Oudart JB, Monboisse JC, Maquart FX, Brassart B, Brassart-Pasco S, Ramont L (2017) Type XIX collagen: a new partner in the interactions between tumor cells and their microenvironment. Matrix Biol 57–58:169–177. https://doi.org/10.1016/j.matbio.2016.07.010

    Article  CAS  PubMed  Google Scholar 

  354. Nagase H, Fields GB (1996) Human matrix metalloproteinase specificity studies using collagen sequence-based synthetic peptides. Biopolymers 40(4):399–416. https://doi.org/10.1002/(SICI)1097-0282(1996)40:4%3C399:AID-BIP5%3E3.0.CO;2-R

    Article  CAS  PubMed  Google Scholar 

  355. Mithieux SM, Weiss AS (2005) Elastin. Adv Protein Chem 70:437–461. https://doi.org/10.1016/S0065-3233(05)70013-9

    Article  CAS  PubMed  Google Scholar 

  356. Wells JM, Gaggar A, Blalock JE (2015) MMP generated matrikines. Matrix Biol 44–46:122–129. https://doi.org/10.1016/j.matbio.2015.01.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  357. Cain SA, Mularczyk EJ, Singh M, Massam-Wu T, Kielty CM (2016) ADAMTS-10 and -6 differentially regulate cell-cell junctions and focal adhesions. Sci Rep 6:35956. https://doi.org/10.1038/srep35956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  358. Bax DV, Mahalingam Y, Cain S, Mellody K, Freeman L, Younger K, Shuttleworth CA, Humphries MJ, Couchman JR, Kielty CM (2007) Cell adhesion to fibrillin-1: identification of an Arg-Gly-Asp-dependent synergy region and a heparin-binding site that regulates focal adhesion formation. J Cell Sci 120(Pt 8):1383–1392. https://doi.org/10.1242/jcs.003954

    Article  CAS  PubMed  Google Scholar 

  359. Jovanovic J, Iqbal S, Jensen S, Mardon H, Handford P (2008) Fibrillin-integrin interactions in health and disease. Biochem Soc Trans 36(Pt 2):257–262. https://doi.org/10.1042/BST0360257

    Article  CAS  PubMed  Google Scholar 

  360. Joshi R, Goihberg E, Ren W, Pilichowska M, Mathew P (2017) Proteolytic fragments of fibronectin function as matrikines driving the chemotactic affinity of prostate cancer cells to human bone marrow mesenchymal stromal cells via the α5β1 integrin. Cell Adh Migr 11(4):305–315. https://doi.org/10.1080/19336918.2016.1212139

    Article  CAS  PubMed  Google Scholar 

  361. White ES, Baralle FE, Muro AF (2008) New insights into form and function of fibronectin splice variants. J Pathol 216(1):1–14. https://doi.org/10.1002/path.2388

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  362. Faron G, Balepa L, Parra J, Fils JF, Gucciardo L (2018) The fetal fibronectin test: 25 years after its development, what is the evidence regarding its clinical utility? A systematic review and meta-analysis. J Matern Fetal Neonatal Med. https://doi.org/10.1080/14767058.2018.1491031

    Article  PubMed  Google Scholar 

  363. Sawicka KM, Seeliger M, Musaev T, Macri LK, Clark RA (2015) Fibronectin interaction and enhancement of growth factors: importance for wound healing. Adv Wound Care (New Rochelle) 4(8):469–478. https://doi.org/10.1089/wound.2014.0616

    Article  Google Scholar 

  364. Wang Y, Ni H (2016) Fibronectin maintains the balance between hemostasis and thrombosis. Cell Mol Life Sci 73(17):3265–3277. https://doi.org/10.1007/s00018-016-2225-y

    Article  CAS  PubMed  Google Scholar 

  365. Mercuri FA, Maciewicz RA, Tart J, Last K, Fosang AJ (2000) Mutations in the interglobular domain of aggrecan alter matrix metalloproteinase and aggrecanase cleavage patterns Evidence that matrix metalloproteinase cleavage interferes with aggrecanase activity. J Biol Chem 275(42):33038–33045

    Article  CAS  PubMed  Google Scholar 

  366. Viapiano MS, Hockfield S, Matthews RT (2008) BEHAB/brevican requires ADAMTS-mediated proteolytic cleavage to promote glioma invasion. J Neurooncol 88(3):261–272. https://doi.org/10.1007/s11060-008-9575-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  367. Demircan K, Topcu V, Takigawa T, Akyol S, Yonezawa T, Ozturk G, Ugurcu V, Hasgul R, Yigitoglu MR, Akyol O, McCulloch DR, Hirohata S (2014) ADAMTS4 and ADAMTS5 knockout mice are protected from versican but not aggrecan or brevican proteolysis during spinal cord injury. Biomed Res Int 2014:693746. https://doi.org/10.1155/2014/693746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  368. Li H, Leung TC, Hoffman S, Balsamo J, Lilien J (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149(6):1275–1288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  369. Mohan V, Wyatt EV, Gotthard I, Phend KD, Diestel S, Duncan BW, Weinberg RJ, Tripathy A, Maness PF (2018) Neurocan inhibits semaphorin 3F induced dendritic spine remodeling through NrCAM in cortical neurons. Front Cell Neurosci 12:346. https://doi.org/10.3389/fncel.2018.00346

    Article  PubMed  PubMed Central  Google Scholar 

  370. Wu Y, Chen L, Zheng PS, Yang BB (2002) β 1-Integrin-mediated glioma cell adhesion and free radical-induced apoptosis are regulated by binding to a C-terminal domain of PG-M/versican. J Biol Chem 277(14):12294–12301. https://doi.org/10.1074/jbc.M110748200

    Article  CAS  PubMed  Google Scholar 

  371. Overall CM (2002) Molecular determinants of metalloproteinase substrate specificity: matrix metalloproteinase substrate binding domains, modules, and exosites. Mol Biotechnol 22(1):51–86. https://doi.org/10.1385/MB:22:1:051

    Article  CAS  PubMed  Google Scholar 

  372. Iozzo RV, Moscatello DK, McQuillan DJ, Eichstetter I (1999) Decorin is a biological ligand for the epidermal growth factor receptor. J Biol Chem 274(8):4489–4492

    Article  CAS  PubMed  Google Scholar 

  373. Moreth K, Iozzo RV, Schaefer L (2012) Small leucine-rich proteoglycans orchestrate receptor crosstalk during inflammation. Cell Cycle 11(11):2084–2091. https://doi.org/10.4161/cc.20316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  374. Goldoni S, Humphries A, Nystrom A, Sattar S, Owens RT, McQuillan DJ, Ireton K, Iozzo RV (2009) Decorin is a novel antagonistic ligand of the Met receptor. J Cell Biol 185(4):743–754. https://doi.org/10.1083/jcb.200901129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  375. Khan GA, Girish GV, Lala N, Di Guglielmo GM, Lala PK (2011) Decorin is a novel VEGFR-2-binding antagonist for the human extravillous trophoblast. Mol Endocrinol 25(8):1431–1443. https://doi.org/10.1210/me.2010-0426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  376. Hausser H, Wedekind P, Sperber T, Peters R, Hasilik A, Kresse H (1996) Isolation and cellular localization of the decorin endocytosis receptor. Eur J Cell Biol 71(4):325–331

    CAS  PubMed  Google Scholar 

  377. Nastase MV, Young MF, Schaefer L (2012) Biglycan: a multivalent proteoglycan providing structure and signals. J Histochem Cytochem 60(12):963–975. https://doi.org/10.1369/0022155412456380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  378. Grindel B, Li Q, Arnold R, Petros J, Zayzafoon M, Muldoon M, Stave J, Chung LW, Farach-Carson MC (2016) Perlecan/HSPG2 and matrilysin/MMP-7 as indices of tissue invasion: tissue localization and circulating perlecan fragments in a cohort of 288 radical prostatectomy patients. Oncotarget 7(9):10433–10447. https://doi.org/10.18632/oncotarget.7197

    Article  PubMed  PubMed Central  Google Scholar 

  379. Eble JA, Wucherpfennig KW, Gauthier L, Dersch P, Krukonis E, Isberg RR, Hemler ME (1998) Recombinant soluble human α3β1 integrin: purification, processing, regulation, and specific binding to laminin-5 and invasin in a mutually exclusive manner. Biochemistry 37(31):10945–10955. https://doi.org/10.1021/bi980175+

    Article  CAS  PubMed  Google Scholar 

  380. Kaasboll OJ, Gadicherla AK, Wang JH, Monsen VT, Hagelin EMV, Dong MQ, Attramadal H (2018) Connective tissue growth factor (CCN2) is a matricellular preproprotein controlled by proteolytic activation. J Biol Chem 293(46):17953–17970. https://doi.org/10.1074/jbc.RA118.004559

    Article  PubMed  PubMed Central  Google Scholar 

  381. Su JL, Chiou J, Tang CH, Zhao M, Tsai CH, Chen PS, Chang YW, Chien MH, Peng CY, Hsiao M, Kuo ML, Yen ML (2010) CYR61 regulates BMP-2-dependent osteoblast differentiation through the αvβ3 integrin/integrin-linked kinase/ERK pathway. J Biol Chem 285(41):31325–31336. https://doi.org/10.1074/jbc.M109.087122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  382. Crockett JC, Schutze N, Tosh D, Jatzke S, Duthie A, Jakob F, Rogers MJ (2007) The matricellular protein CYR61 inhibits osteoclastogenesis by a mechanism independent of αvβ3 and αvβ5. Endocrinology 148(12):5761–5768. https://doi.org/10.1210/en.2007-0473

    Article  CAS  PubMed  Google Scholar 

  383. Chen CC, Young JL, Monzon RI, Chen N, Todorovic V, Lau LF (2007) Cytotoxicity of TNFα is regulated by integrin-mediated matrix signaling. EMBO J 26(5):1257–1267. https://doi.org/10.1038/sj.emboj.7601596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  384. Tsai HC, Chang AC, Tsai CH, Huang YL, Gan L, Chen CK, Liu SC, Huang TY, Fong YC, Tang CH (2019) CCN2 promotes drug resistance in osteosarcoma by enhancing ABCG2 expression. J Cell Physiol 234(6):9297–9307. https://doi.org/10.1002/jcp.27611

    Article  CAS  PubMed  Google Scholar 

  385. Babic AM, Chen CC, Lau LF (1999) Fisp12/mouse connective tissue growth factor mediates endothelial cell adhesion and migration through integrin αvβ3, promotes endothelial cell survival, and induces angiogenesis in vivo. Mol Cell Biol 19(4):2958–2966

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  386. Scherberich A, Tucker RP, Degen M, Brown-Luedi M, Andres AC, Chiquet-Ehrismann R (2005) Tenascin-W is found in malignant mammary tumors, promotes α8 integrin-dependent motility and requires p38MAPK activity for BMP-2 and TNF-α induced expression in vitro. Oncogene 24(9):1525–1532. https://doi.org/10.1038/sj.onc.1208342

    Article  CAS  PubMed  Google Scholar 

  387. Martina E, Degen M, Ruegg C, Merlo A, Lino MM, Chiquet-Ehrismann R, Brellier F (2010) Tenascin-W is a specific marker of glioma-associated blood vessels and stimulates angiogenesis in vitro. FASEB J 24(3):778–787. https://doi.org/10.1096/fj.09-140491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  388. Gillan L, Matei D, Fishman DA, Gerbin CS, Karlan BY, Chang DD (2002) Periostin secreted by epithelial ovarian carcinoma is a ligand for αVβ3 and αVβ5 integrins and promotes cell motility. Cancer Res 62(18):5358–5364

    CAS  PubMed  Google Scholar 

  389. Kakizaki Y, Makino N, Tozawa T, Honda T, Matsuda A, Ikeda Y, Ito M, Saito Y, Kimura W, Ueno Y (2016) Stromal fibrosis and expression of matricellular proteins correlate with histological grade of intraductal papillary mucinous neoplasm of the pancreas. Pancreas 45(8):1145–1152. https://doi.org/10.1097/MPA.0000000000000617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  390. Thijssen VL, Rabinovich GA, Griffioen AW (2013) Vascular galectins: regulators of tumor progression and targets for cancer therapy. Cytokine Growth Factor Rev 24(6):547–558. https://doi.org/10.1016/j.cytogfr.2013.07.003

    Article  CAS  PubMed  Google Scholar 

  391. Mendez-Huergo SP, Blidner AG, Rabinovich GA (2017) Galectins: emerging regulatory checkpoints linking tumor immunity and angiogenesis. Curr Opin Immunol 45:8–15. https://doi.org/10.1016/j.coi.2016.12.003

    Article  CAS  PubMed  Google Scholar 

  392. Agnihotri R, Crawford HC, Haro H, Matrisian LM, Havrda MC, Liaw L (2001) Osteopontin, a novel substrate for matrix metalloproteinase-3 (stromelysin-1) and matrix metalloproteinase-7 (matrilysin). J Biol Chem 276(30):28261–28267. https://doi.org/10.1074/jbc.M103608200

    Article  CAS  PubMed  Google Scholar 

  393. Takafuji V, Forgues M, Unsworth E, Goldsmith P, Wang XW (2007) An osteopontin fragment is essential for tumor cell invasion in hepatocellular carcinoma. Oncogene 26(44):6361–6371. https://doi.org/10.1038/sj.onc.1210463

    Article  CAS  PubMed  Google Scholar 

  394. Furger KA, Allan AL, Wilson SM, Hota C, Vantyghem SA, Postenka CO, Al-Katib W, Chambers AF, Tuck AB (2003) Β3 integrin expression increases breast carcinoma cell responsiveness to the malignancy-enhancing effects of osteopontin. Mol Cancer Res 1(11):810–819

    CAS  PubMed  Google Scholar 

  395. Rangaswami H, Bulbule A, Kundu GC (2006) Osteopontin: role in cell signaling and cancer progression. Trends Cell Biol 16(2):79–87. https://doi.org/10.1016/j.tcb.2005.12.005

    Article  CAS  PubMed  Google Scholar 

  396. Teramoto H, Castellone MD, Malek RL, Letwin N, Frank B, Gutkind JS, Lee NH (2005) Autocrine activation of an osteopontin-CD44-Rac pathway enhances invasion and transformation by H-RasV12. Oncogene 24(3):489–501. https://doi.org/10.1038/sj.onc.1208209

    Article  CAS  PubMed  Google Scholar 

  397. Ye QH, Qin LX, Forgues M, He P, Kim JW, Peng AC, Simon R, Li Y, Robles AI, Chen Y, Ma ZC, Wu ZQ, Ye SL, Liu YK, Tang ZY, Wang XW (2003) Predicting hepatitis B virus-positive metastatic hepatocellular carcinomas using gene expression profiling and supervised machine learning. Nat Med 9(4):416–423. https://doi.org/10.1038/nm843

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

To study different aspect of tumor biology, J.A.E. receives financial support from Deutsche Forschungsgemeinschaft (SFB1009 A09) (MMP14 in invadopodia), from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013/under the REA Grant agreement n° [316610] (CAF differentiation in tumor stroma), and from the Wilhelm Sander Stiftung (grant:2016.113.1 to J.A.E.) (Interactions between tumor and endothelial cells).

Author information

Authors and Affiliations

  1. Institute of Physiological Chemistry and Pathobiochemistry, University of Münster, Waldeyerstr. 15, 48149, Münster, Germany

    Johannes A. Eble & Stephan Niland

Authors
  1. Johannes A. Eble
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Stephan Niland
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes A. Eble.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eble, J.A., Niland, S. The extracellular matrix in tumor progression and metastasis. Clin Exp Metastasis 36, 171–198 (2019). https://doi.org/10.1007/s10585-019-09966-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10585-019-09966-1

Keywords

Search

Navigation