More Than a Barrier: How the Endothelium Instructs Metastasis

  • Candice Alexandra Grzelak
  • Andrea Rachel Lim
  • Cyrus Michael Ghajar
Chapter

Abstract

For metastasis to occur, a tumor cell must interact with endothelium at many steps and on multiple levels. The first half of this chapter highlights specific ligand–receptor interactions between tumor cells and the endothelium required for successful metastatic dissemination to occur, with an eye on how the specificity of endothelium influences this process in different tissues. The second half of this chapter focuses on interactions between disseminated tumor cells (DTCs) and endothelium post-extravasation. Evidence that a niche comprised by microvasculature is responsible for both maintaining cellular dormancy and facilitating tumor cell outgrowth is presented. By contrasting these studies with the known roles of endothelial-derived signals in development, maintenance of organ homeostasis, wound healing, and in stem cell niches, we describe how endothelium could dictate these opposing cellular responses during metastasis. Elaborating upon the role of endothelium as a regulator of DTC dormancy and outgrowth in multiple tissues—perhaps for multiple cancers—will guide development of therapies to combat and even prevent metastasis.

Keywords

Endothelium Metastasis Micrometastasis Breast cancer Disseminated tumor cell Circulating tumor cell Tumor dormancy Microenvironment Perivascular niche Angiocrine Signaling Capillary Intravasation Extravasation 

Abbreviations

ADAM

A disintegrin and metalloproteinase

Aes

Amino-terminal enhancer of split

ATP

Adenosine triphosphate

BBB

Blood–brain barrier

CXCL12

Chemokine (C-X-C Motif) ligand 12

CXCR7

C-X-C chemokine receptor type 7

Dll4

Delta-like protein 4

DTC

Disseminated tumor cell

EC

Endothelial cell

ECM

Extracellular matrix

EGF

Epidermal growth factor

Eph

Ephrin

HB-EGF

Heparin-binding EGF-like growth factor

HSC

Hematopoietic stem cell

HSPC

Hematopoietic stem and progenitor cell

ICAM-1

Intercellular adhesion molecule 1

IgG

Immunoglobulin

IL

Interleukin

L1CAM

L1 cell adhesion molecule

LGALS3BP

Galectin-3-binding protein

LSEC

Liver sinusoidal endothelial cell

MAPK

Mitogen-activated protein kinase

MENAINV

Mammalian enabled homologue, invasion

MLCK

Myosin light chain kinase

NO

Nitric oxide

NSC

Neural stem cell

PDGF

Platelet-derived growth factor

PECAM

Platelet endothelial cell adhesion molecule

POSTN

Periostin

PSGL1

P-selectin glycoprotein ligand 1

PVN

Perivascular niche

SCF

Stem cell factor

sLex

Tetrasaccharide sialyl Lewis x antigen

SVZ

Subventricular zone

TGF

Transforming growth factor

TMEM

Tumor microenvironment of metastasis

TNFα

Tumor necrosis factor-α

TSP-1

Thrombospondin-1

VCAM-1

Vascular cell adhesion molecule 1

VEGF

Vascular endothelial growth factor

VEGFR

Vascular endothelial growth factor receptor

vWF

Von Willebrand factor

References

  1. 1.
    Ewing J. Lymphoepithelioma. Am J Pathol. 1929;5(2):99–108.7.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Paget S. The distribution of secondary growths in cancer of the breast. Lancet. 1889;133(3421):571–3.CrossRefGoogle Scholar
  3. 3.
    Hart IR, Fidler IJ. Role of organ selectivity in the determination of metastatic patterns of B16 melanoma. Cancer Res. 1980;40(7):2281–7.PubMedGoogle Scholar
  4. 4.
    Schatteman GC, Awad O. Hemangioblasts, angioblasts, and adult endothelial cell progenitors. Anat Rec A Discov Mol Cell Evol Biol. 2004;276(1):13–21.PubMedCrossRefGoogle Scholar
  5. 5.
    Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol. 1995;11:73–91.PubMedCrossRefGoogle Scholar
  6. 6.
    Aird WC. Endothelial cell heterogeneity. Cold Spring Harb Perspect Med. 2012;2(1):a006429.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Nolan DJ, Ginsberg M, Israely E, Palikuqi B, Poulos MG, James D, et al. Molecular signatures of tissue-specific microvascular endothelial cell heterogeneity in organ maintenance and regeneration. Dev Cell. 2013;26(2):204–19.PubMedCrossRefGoogle Scholar
  8. 8.
    Cunha GR. Stromal induction and specification of morphogenesis and cytodifferentiation of the epithelia of the Mullerian ducts and urogenital sinus during development of the uterus and vagina in mice. J Exp Zool. 1976;196(3):361–70.PubMedCrossRefGoogle Scholar
  9. 9.
    Cunha GR, Baskin L. Mesenchymal-epithelial interaction techniques. Differentiation. 2016;91(4–5):20–7.PubMedCrossRefGoogle Scholar
  10. 10.
    De Bruyn PP, Cho Y. Vascular endothelial invasion via transcellular passage by malignant cells in the primary stage of metastases formation. J Ultrastruct Res. 1982;81(2):189–201.PubMedCrossRefGoogle Scholar
  11. 11.
    Khuon S, Liang L, Dettman RW, Sporn PH, Wysolmerski RB, Chew TL. Myosin light chain kinase mediates transcellular intravasation of breast cancer cells through the underlying endothelial cells: a three-dimensional FRET study. J Cell Sci. 2010;123(Pt 3):431–40.PubMedPubMedCentralCrossRefGoogle Scholar
  12. 12.
    Sonoshita M, Aoki M, Fuwa H, Aoki K, Hosogi H, Sakai Y, et al. Suppression of colon cancer metastasis by Aes through inhibition of Notch signaling. Cancer Cell. 2011;19(1):125–37.PubMedCrossRefGoogle Scholar
  13. 13.
    Frohlich C, Klitgaard M, Noer JB, Kotzsch A, Nehammer C, Kronqvist P, et al. ADAM12 is expressed in the tumour vasculature and mediates ectodomain shedding of several membrane-anchored endothelial proteins. Biochem J. 2013;452(1):97–109.PubMedCrossRefGoogle Scholar
  14. 14.
    Ohlig S, Farshi P, Pickhinke U, van den Boom J, Hoing S, Jakuschev S, et al. Sonic hedgehog shedding results in functional activation of the solubilized protein. Dev Cell. 2011;20(6):764–74.PubMedCrossRefGoogle Scholar
  15. 15.
    Dyczynska E, Sun D, Yi H, Sehara-Fujisawa A, Blobel CP, Zolkiewska A. Proteolytic processing of delta-like 1 by ADAM proteases. J Biol Chem. 2007;282(1):436–44.PubMedCrossRefGoogle Scholar
  16. 16.
    Asakura M, Kitakaze M, Takashima S, Liao Y, Ishikura F, Yoshinaka T, et al. Cardiac hypertrophy is inhibited by antagonism of ADAM12 processing of HB-EGF: metalloproteinase inhibitors as a new therapy. Nat Med. 2002;8(1):35–40.PubMedCrossRefGoogle Scholar
  17. 17.
    Robinson BD, Sica GL, Liu YF, Rohan TE, Gertler FB, Condeelis JS, et al. Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res. 2009;15(7):2433–41.PubMedPubMedCentralCrossRefGoogle Scholar
  18. 18.
    Wyckoff J, Wang W, Lin EY, Wang Y, Pixley F, Stanley ER, et al. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors. Cancer Res. 2004;64(19):7022–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 2007;67(6):2649–56.PubMedCrossRefGoogle Scholar
  20. 20.
    Di Modugno F, DeMonte L, Balsamo M, Bronzi G, Nicotra MR, Alessio M, et al. Molecular cloning of hMena (ENAH) and its splice variant hMena+11a: epidermal growth factor increases their expression and stimulates hMena+11a phosphorylation in breast cancer cell lines. Cancer Res. 2007;67(6):2657–65.PubMedPubMedCentralCrossRefGoogle Scholar
  21. 21.
    Di Modugno F, Iapicca P, Boudreau A, Mottolese M, Terrenato I, Perracchio L, et al. Splicing program of human MENA produces a previously undescribed isoform associated with invasive, mesenchymal-like breast tumors. Proc Natl Acad Sci U S A. 2012;109(47):19280–5.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Di Modugno F, Mottolese M, DeMonte L, Trono P, Balsamo M, Conidi A, et al. The cooperation between hMena overexpression and HER2 signalling in breast cancer. PLoS One. 2010;5(12):e15852.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Roussos ET, Balsamo M, Alford SK, Wyckoff JB, Gligorijevic B, Wang Y, et al. Mena invasive (MenaINV) promotes multicellular streaming motility and transendothelial migration in a mouse model of breast cancer. J Cell Sci. 2011;124(Pt 13):2120–31.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Reymond N, d’Agua BB, Ridley AJ. Crossing the endothelial barrier during metastasis. Nat Rev Cancer. 2013;13(12):858–70.PubMedCrossRefGoogle Scholar
  25. 25.
    Carman CV, Springer TA. A transmigratory cup in leukocyte diapedesis both through individual vascular endothelial cells and between them. J Cell Biol. 2004;167(2):377–88.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Mamdouh Z, Mikhailov A, Muller WA. Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J Exp Med. 2009;206(12):2795–808.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Muller WA. Mechanisms of leukocyte transendothelial migration. Annu Rev Pathol. 2011;6:323–44.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    van Buul JD, Allingham MJ, Samson T, Meller J, Boulter E, Garcia-Mata R, et al. RhoG regulates endothelial apical cup assembly downstream from ICAM1 engagement and is involved in leukocyte trans-endothelial migration. J Cell Biol. 2007;178(7):1279–93.PubMedPubMedCentralCrossRefGoogle Scholar
  29. 29.
    Arvanitis C, Khuon S, Spann R, Ridge KM, Chew TL. Structure and biomechanics of the endothelial transcellular circumferential invasion array in tumor invasion. PLoS One. 2014;9(2):e89758.PubMedPubMedCentralCrossRefGoogle Scholar
  30. 30.
    Baluk P, Fuxe J, Hashizume H, Romano T, Lashnits E, Butz S, et al. Functionally specialized junctions between endothelial cells of lymphatic vessels. J Exp Med. 2007;204(10):2349–62.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Kerjaschki D, Bago-Horvath Z, Rudas M, Sexl V, Schneckenleithner C, Wolbank S, et al. Lipoxygenase mediates invasion of intrametastatic lymphatic vessels and propagates lymph node metastasis of human mammary carcinoma xenografts in mouse. J Clin Invest. 2011;121(5):2000–12.PubMedPubMedCentralCrossRefGoogle Scholar
  32. 32.
    Ding Z, Liu Z, Bi Y, Tian H, Li G, Song T. Morphological study of the interaction between M21 melanoma and lymphatic endothelium. Lymphology. 2005;38(2):87–91.PubMedGoogle Scholar
  33. 33.
    Glinskii OV, Huxley VH, Glinsky GV, Pienta KJ, Raz A, Glinsky VV. Mechanical entrapment is insufficient and intercellular adhesion is essential for metastatic cell arrest in distant organs. Neoplasia. 2005;7(5):522–7.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Hynes RO. Integrins: a family of cell surface receptors. Cell. 1987;48(4):549–54.PubMedCrossRefGoogle Scholar
  35. 35.
    Seguin L, Desgrosellier JS, Weis SM, Cheresh DA. Integrins and cancer: regulators of cancer stemness, metastasis, and drug resistance. Trends Cell Biol. 2015;25(4):234–40.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Zhang H, Wong CC, Wei H, Gilkes DM, Korangath P, Chaturvedi P, et al. HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene. 2012;31(14):1757–70.PubMedCrossRefGoogle Scholar
  37. 37.
    Singh B, Fu C, Bhattacharya J. Vascular expression of the alpha(v)beta(3)-integrin in lung and other organs. Am J Physiol Lung Cell Mol Physiol. 2000;278(1):L217–26.PubMedCrossRefGoogle Scholar
  38. 38.
    Valiente M, Obenauf AC, Jin X, Chen Q, Zhang XH, Lee DJ, et al. Serpins promote cancer cell survival and vascular co-option in brain metastasis. Cell. 2014;156(5):1002–16.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Skobe M, Hawighorst T, Jackson DG, Prevo R, Janes L, Velasco P, et al. Induction of tumor lymphangiogenesis by VEGF-C promotes breast cancer metastasis. Nat Med. 2001;7(2):192–8.PubMedCrossRefGoogle Scholar
  40. 40.
    Garmy-Susini B, Avraamides CJ, Desgrosellier JS, Schmid MC, Foubert P, Ellies LG, et al. PI3Kalpha activates integrin alpha4beta1 to establish a metastatic niche in lymph nodes. Proc Natl Acad Sci U S A. 2013;110(22):9042–7.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Chen MB, Whisler JA, Jeon JS, Kamm RD. Mechanisms of tumor cell extravasation in an in vitro microvascular network platform. Integr Biol (Camb). 2013;5(10):1262–71.CrossRefGoogle Scholar
  42. 42.
    Piali L, Hammel P, Uherek C, Bachmann F, Gisler RH, Dunon D, et al. CD31/PECAM-1 is a ligand for alpha v beta 3 integrin involved in adhesion of leukocytes to endothelium. J Cell Biol. 1995;130(2):451–60.PubMedCrossRefGoogle Scholar
  43. 43.
    Bauer K, Mierke C, Behrens J. Expression profiling reveals genes associated with transendothelial migration of tumor cells: a functional role for alphavbeta3 integrin. Int J Cancer. 2007;121(9):1910–8.PubMedCrossRefGoogle Scholar
  44. 44.
    Lorger M, Felding-Habermann B. Capturing changes in the brain microenvironment during initial steps of breast cancer brain metastasis. Am J Pathol. 2010;176(6):2958–71.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Paku S, Dome B, Toth R, Timar J. Organ-specificity of the extravasation process: an ultrastructural study. Clin Exp Metastasis. 2000;18(6):481–92.PubMedCrossRefGoogle Scholar
  46. 46.
    Kienast Y, von Baumgarten L, Fuhrmann M, Klinkert WE, Goldbrunner R, Herms J, et al. Real-time imaging reveals the single steps of brain metastasis formation. Nat Med. 2010;16(1):116–22.PubMedCrossRefGoogle Scholar
  47. 47.
    Bos PD, Zhang XH, Nadal C, Shu W, Gomis RR, Nguyen DX, et al. Genes that mediate breast cancer metastasis to the brain. Nature. 2009;459(7249):1005–9.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 48.
    Borsig L, Wong R, Feramisco J, Nadeau DR, Varki NM, Varki A. Heparin and cancer revisited: mechanistic connections involving platelets, P-selectin, carcinoma mucins, and tumor metastasis. Proc Natl Acad Sci U S A. 2001;98(6):3352–7.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Camerer E, Qazi AA, Duong DN, Cornelissen I, Advincula R, Coughlin SR. Platelets, protease-activated receptors, and fibrinogen in hematogenous metastasis. Blood. 2004;104(2):397–401.PubMedCrossRefGoogle Scholar
  50. 50.
    Erpenbeck L, Nieswandt B, Schon M, Pozgajova M, Schon MP. Inhibition of platelet GPIb alpha and promotion of melanoma metastasis. J Invest Dermatol. 2010;130(2):576–86.PubMedCrossRefGoogle Scholar
  51. 51.
    Erpenbeck L, Rubant S, Hardt K, Santoso S, Boehncke WH, Schon MP, et al. Constitutive and functionally relevant expression of JAM-C on platelets. Thromb Haemost. 2010;103(4):857–9.PubMedCrossRefGoogle Scholar
  52. 52.
    Erpenbeck L, Schon MP. Deadly allies: the fatal interplay between platelets and metastasizing cancer cells. Blood. 2010;115(17):3427–36.PubMedPubMedCentralCrossRefGoogle Scholar
  53. 53.
    Gay LJ, Felding-Habermann B. Contribution of platelets to tumour metastasis. Nat Rev Cancer. 2011;11(2):123–34.PubMedCrossRefGoogle Scholar
  54. 54.
    Honn KV, Tang DG, Chen YQ. Platelets and cancer metastasis: more than an epiphenomenon. Semin Thromb Hemost. 1992;18(4):392–415.PubMedCrossRefGoogle Scholar
  55. 55.
    Im JH, Fu W, Wang H, Bhatia SK, Hammer DA, Kowalska MA, et al. Coagulation facilitates tumor cell spreading in the pulmonary vasculature during early metastatic colony formation. Cancer Res. 2004;64(23):8613–9.PubMedCrossRefGoogle Scholar
  56. 56.
    Nierodzik ML, Karpatkin S. Thrombin induces tumor growth, metastasis, and angiogenesis: evidence for a thrombin-regulated dormant tumor phenotype. Cancer Cell. 2006;10(5):355–62.PubMedCrossRefGoogle Scholar
  57. 57.
    Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood. 2005;105(1):178–85.PubMedCrossRefGoogle Scholar
  58. 58.
    Schumacher D, Strilic B, Sivaraj KK, Wettschureck N, Offermanns S. Platelet-derived nucleotides promote tumor-cell transendothelial migration and metastasis via P2Y2 receptor. Cancer Cell. 2013;24(1):130–7.PubMedCrossRefGoogle Scholar
  59. 59.
    Kaplan RN, Riba RD, Zacharoulis S, Bramley AH, Vincent L, Costa C, et al. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche. Nature. 2005;438(7069):820–7.PubMedPubMedCentralCrossRefGoogle Scholar
  60. 60.
    Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18(6):883–91.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–35.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Lammert E, Cleaver O, Melton D. Induction of pancreatic differentiation by signals from blood vessels. Science. 2001;294(5542):564–7.PubMedCrossRefGoogle Scholar
  63. 63.
    Matsumoto K, Yoshitomi H, Rossant J, Zaret KS. Liver organogenesis promoted by endothelial cells prior to vascular function. Science. 2001;294(5542):559–63.PubMedCrossRefGoogle Scholar
  64. 64.
    DeLeve LD, Wang X, Hu L, McCuskey MK, McCuskey RS. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol. 2004;287(4):G757–63.Google Scholar
  65. 65.
    Deleve LD, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology. 2008;48(3):920–30.PubMedPubMedCentralCrossRefGoogle Scholar
  66. 66.
    Rafii S, Butler JM, Ding BS. Angiocrine functions of organ-specific endothelial cells. Nature. 2016;529(7586):316–25.PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Iwakiri Y, Shah V, Rockey DC. Vascular pathobiology in chronic liver disease and cirrhosis – current status and future directions. J Hepatol. 2014;61(4):912–24.PubMedPubMedCentralCrossRefGoogle Scholar
  68. 68.
    Kobayashi H, Butler JM, O’Donnell R, Kobayashi M, Ding BS, Bonner B, et al. Angiocrine factors from Akt-activated endothelial cells balance self-renewal and differentiation of haematopoietic stem cells. Nat Cell Biol. 2010;12(11):1046–56.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    Ottone C, Krusche B, Whitby A, Clements M, Quadrato G, Pitulescu ME, et al. Direct cell-cell contact with the vascular niche maintains quiescent neural stem cells. Nat Cell Biol. 2014;16(11):1045–56.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Ghajar CM, Peinado H, Mori H, Matei IR, Evason KJ, Brazier H, et al. The perivascular niche regulates breast tumour dormancy. Nat Cell Biol. 2013;15(7):807–17.PubMedPubMedCentralCrossRefGoogle Scholar
  71. 71.
    Ghajar CM. Metastasis prevention by targeting the dormant niche. Nat Rev Cancer. 2015;15(4):238–47.PubMedPubMedCentralCrossRefGoogle Scholar
  72. 72.
    Butler JM, Kobayashi H, Rafii S. Instructive role of the vascular niche in promoting tumour growth and tissue repair by angiocrine factors. Nat Rev Cancer. 2010;10(2):138–46.PubMedPubMedCentralCrossRefGoogle Scholar
  73. 73.
    Braet F, Wisse E. Structural and functional aspects of liver sinusoidal endothelial cell fenestrae: a review. Comp Hepatol. 2002;1(1):1.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Wisse E. An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res. 1970;31(1):125–50.PubMedCrossRefGoogle Scholar
  75. 75.
    Wisse E, Braet F, Luo D, De Zanger R, Jans D, Crabbe E, et al. Structure and function of sinusoidal lining cells in the liver. Toxicol Pathol. 1996;24(1):100–11.PubMedCrossRefGoogle Scholar
  76. 76.
    Wisse E. Kupffer cell reactions in rat liver under various conditions as observed in the electron microscope. J Ultrastruct Res. 1974;46(3):499–520.PubMedCrossRefGoogle Scholar
  77. 77.
    Wisse E. Observations on the fine structure and peroxidase cytochemistry of normal rat liver Kupffer cells. J Ultrastruct Res. 1974;46(3):393–426.PubMedCrossRefGoogle Scholar
  78. 78.
    Wake K. Perisinusoidal stellate cells (fat-storing cells, interstitial cells, lipocytes), their related structure in and around the liver sinusoids, and vitamin A-storing cells in extrahepatic organs. Int Rev Cytol. 1980;66:303–53.PubMedCrossRefGoogle Scholar
  79. 79.
    Wake K. “Sternzellen” in the liver: perisinusoidal cells with special reference to storage of vitamin A. Am J Anat. 1971;132(4):429–62.PubMedCrossRefGoogle Scholar
  80. 80.
    Ito T, Nemoto M. Kupfer’s cells and fat storing cells in the capillary wall of human liver. Okajimas Folia Anat Jpn. 1952;24(4):243–58.PubMedCrossRefGoogle Scholar
  81. 81.
    Warren A, Le Couteur DG, Fraser R, Bowen DG, McCaughan GW, Bertolino P. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology. 2006;44(5):1182–90.PubMedCrossRefGoogle Scholar
  82. 82.
    Boulter L, WY L, Forbes SJ. Differentiation of progenitors in the liver: a matter of local choice. J Clin Invest. 2013;123(5):1867–73.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    Pellicoro A, Ramachandran P, Iredale JP, Fallowfield JA. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat Rev Immunol. 2014;14(3):181–94.PubMedCrossRefGoogle Scholar
  84. 84.
    Friedman SL, Roll FJ, Boyles J, Bissell DM. Hepatic lipocytes: the principal collagen-producing cells of normal rat liver. Proc Natl Acad Sci U S A. 1985;82(24):8681–5.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Xie G, Wang X, Wang L, Wang L, Atkinson RD, Kanel GC, et al. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology. 2012;142(4):918–27.e6.PubMedCrossRefGoogle Scholar
  86. 86.
    Jarnagin WR, Rockey DC, Koteliansky VE, Wang SS, Bissell DM. Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol. 1994;127(6 Pt 2):2037–48.PubMedCrossRefGoogle Scholar
  87. 87.
    Rockey DC, Fouassier L, Chung JJ, Carayon A, Vallee P, Rey C, et al. Cellular localization of endothelin-1 and increased production in liver injury in the rat: potential for autocrine and paracrine effects on stellate cells. Hepatology. 1998;27(2):472–80.PubMedCrossRefGoogle Scholar
  88. 88.
    Cao Z, Lis R, Ginsberg M, Chavez D, Shido K, Rabbany SY, et al. Targeting of the pulmonary capillary vascular niche promotes lung alveolar repair and ameliorates fibrosis. Nat Med. 2016;22(2):154–62.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kramann R, Schneider RK, DiRocco DP, Machado F, Fleig S, Bondzie PA, et al. Perivascular Gli1+ progenitors are key contributors to injury-induced organ fibrosis. Cell Stem Cell. 2015;16(1):51–66.PubMedCrossRefGoogle Scholar
  90. 90.
    Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer. 2006;6(6):425–36.PubMedCrossRefGoogle Scholar
  91. 91.
    Kiel MJ, Yilmaz OH, Iwashita T, Yilmaz OH, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109–21.PubMedCrossRefGoogle Scholar
  92. 92.
    Kiel MJ, Radice GL, Morrison SJ. Lack of evidence that hematopoietic stem cells depend on N-cadherin-mediated adhesion to osteoblasts for their maintenance. Cell Stem Cell. 2007;1(2):204–17.PubMedCrossRefGoogle Scholar
  93. 93.
    Chen JY, Miyanishi M, Wang SK, Yamazaki S, Sinha R, Kao KS, et al. Hoxb5 marks long-term haematopoietic stem cells and reveals a homogenous perivascular niche. Nature. 2016;530(7589):223–7.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Broudy VC. Stem cell factor and hematopoiesis. Blood. 1997;90(4):1345–64.PubMedGoogle Scholar
  95. 95.
    Ding L, Saunders TL, Enikolopov G, Morrison SJ. Endothelial and perivascular cells maintain haematopoietic stem cells. Nature. 2012;481(7382):457–62.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Inra CN, Zhou BO, Acar M, Murphy MM, Richardson J, Zhao Z, et al. A perisinusoidal niche for extramedullary haematopoiesis in the spleen. Nature. 2015;527(7579):466–71.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Stoletov K, Strnadel J, Zardouzian E, Momiyama M, Park FD, Kelber JA, et al. Role of connexins in metastatic breast cancer and melanoma brain colonization. J Cell Sci. 2013;126(Pt 4):904–13.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Gimbrone MA Jr, Leapman SB, Cotran RS, Folkman J. Tumor dormancy in vivo by prevention of neovascularization. J Exp Med. 1972;136(2):261–76.Google Scholar
  99. 99.
    Casey SC, Li Y, Felsher DW. An essential role for the immune system in the mechanism of tumor regression following targeted oncogene inactivation. Immunol Res. 2014;58(2–3):282–91.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med. 1971;285(21):1182–6.PubMedCrossRefGoogle Scholar
  101. 101.
    Townson JL, Chambers AF. Dormancy of solitary metastatic cells. Cell Cycle. 2006;5(16):1744–50.PubMedCrossRefGoogle Scholar
  102. 102.
    O’Shaughnessy J. Extending survival with chemotherapy in metastatic breast cancer. Oncologist. 2005;10(Suppl 3):20–9.PubMedCrossRefGoogle Scholar
  103. 103.
    Uhr JW, Pantel K. Controversies in clinical cancer dormancy. Proc Natl Acad Sci U S A. 2011;108(30):12396–400.PubMedPubMedCentralCrossRefGoogle Scholar
  104. 104.
    Good DJ, Polverini PJ, Rastinejad F, Le Beau MM, Lemons RS, Frazier WA, et al. A tumor suppressor-dependent inhibitor of angiogenesis is immunologically and functionally indistinguishable from a fragment of thrombospondin. Proc Natl Acad Sci U S A. 1990;87(17):6624–8.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Franses JW, Baker AB, Chitalia VC, Edelman ER. Stromal endothelial cells directly influence cancer progression. Sci Transl Med. 2011;3(66):66ra5.PubMedPubMedCentralCrossRefGoogle Scholar
  106. 106.
    Catena R, Bhattacharya N, El Rayes T, Wang S, Choi H, Gao D, et al. Bone marrow-derived Gr1+ cells can generate a metastasis-resistant microenvironment via induced secretion of thrombospondin-1. Cancer Discov. 2013;3(5):578–89.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Kang SY, Halvorsen OJ, Gravdal K, Bhattacharya N, Lee JM, Liu NW, et al. Prosaposin inhibits tumor metastasis via paracrine and endocrine stimulation of stromal p53 and Tsp-1. Proc Natl Acad Sci U S A. 2009;106(29):12115–20.PubMedPubMedCentralCrossRefGoogle Scholar
  108. 108.
    Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161(6):1163–77.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 109.
    Mazzone M, Dettori D, Leite de Oliveira R, Loges S, Schmidt T, Jonckx B, et al. Heterozygous deficiency of PHD2 restores tumor oxygenation and inhibits metastasis via endothelial normalization. Cell. 2009;136(5):839–51.PubMedPubMedCentralCrossRefGoogle Scholar
  110. 110.
    Hellstrom M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, Lindblom P, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445(7129):776–80.PubMedCrossRefGoogle Scholar
  111. 111.
    Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, Lewis J. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development. 2007;134(5):839–44.PubMedCrossRefGoogle Scholar
  112. 112.
    Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, Yancopoulos GD, et al. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci U S A. 2007;104(9):3219–24.PubMedPubMedCentralCrossRefGoogle Scholar
  113. 113.
    Siekmann AF, Lawson ND. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature. 2007;445(7129):781–4.PubMedCrossRefGoogle Scholar
  114. 114.
    Suchting S, Freitas C, le Noble F, Benedito R, Breant C, Duarte A, et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci U S A. 2007;104(9):3225–30.PubMedPubMedCentralCrossRefGoogle Scholar
  115. 115.
    Jakobsson L, Franco CA, Bentley K, Collins RT, Ponsioen B, Aspalter IM, et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol. 2010;12(10):943–53.PubMedCrossRefGoogle Scholar
  116. 116.
    Bierie B, Moses HL. Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer. 2006;6(7):506–20.PubMedCrossRefGoogle Scholar
  117. 117.
    Kim S, Takahashi H, Lin WW, Descargues P, Grivennikov S, Kim Y, et al. Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature. 2009;457(7225):102–6.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Malanchi I, Santamaria-Martinez A, Susanto E, Peng H, Lehr HA, Delaloye JF, et al. Interactions between cancer stem cells and their niche govern metastatic colonization. Nature. 2012;481(7379):85–9.CrossRefGoogle Scholar
  119. 119.
    Oskarsson T, Acharyya S, Zhang XH, Vanharanta S, Tavazoie SF, Morris PG, et al. Breast cancer cells produce tenascin C as a metastatic niche component to colonize the lungs. Nat Med. 2011;17(7):867–74.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Soikkeli J, Podlasz P, Yin M, Nummela P, Jahkola T, Virolainen S, et al. Metastatic outgrowth encompasses COL-I, FN1, and POSTN up-regulation and assembly to fibrillar networks regulating cell adhesion, migration, and growth. Am J Pathol. 2010;177(1):387–403.PubMedPubMedCentralCrossRefGoogle Scholar
  121. 121.
    Rice GE, Bevilacqua MP. An inducible endothelial cell surface glycoprotein mediates melanoma adhesion. Science. 1989;246(4935):1303–6.PubMedCrossRefGoogle Scholar
  122. 122.
    Weibel ER, Palade GE. New cytoplasmic components in arterial endothelia. J Cell Biol. 1964;23:101–12.PubMedPubMedCentralCrossRefGoogle Scholar
  123. 123.
    Wagner DD, Olmsted JB, Marder VJ. Immunolocalization of von Willebrand protein in Weibel-Palade bodies of human endothelial cells. J Cell Biol. 1982;95(1):355–60.PubMedCrossRefGoogle Scholar
  124. 124.
    Bonfanti R, Furie BC, Furie B, Wagner DD. PADGEM (GMP140) is a component of Weibel-Palade bodies of human endothelial cells. Blood. 1989;73(5):1109–12.PubMedGoogle Scholar
  125. 125.
    McEver RP, Beckstead JH, Moore KL, Marshall-Carlson L, Bainton DF. GMP-140, a platelet alpha-granule membrane protein, is also synthesized by vascular endothelial cells and is localized in Weibel-Palade bodies. J Clin Invest. 1989;84(1):92–9.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol. 2007;7(10):803–15.PubMedCrossRefGoogle Scholar
  127. 127.
    Garofalo A, Chirivi RG, Foglieni C, Pigott R, Mortarini R, Martin-Padura I, et al. Involvement of the very late antigen 4 integrin on melanoma in interleukin 1-augmented experimental metastases. Cancer Res. 1995;55(2):414–9.PubMedGoogle Scholar
  128. 128.
    Okahara H, Yagita H, Miyake K, Okumura K. Involvement of very late activation antigen 4 (VLA-4) and vascular cell adhesion molecule 1 (VCAM-1) in tumor necrosis factor alpha enhancement of experimental metastasis. Cancer Res. 1994;54(12):3233–6.PubMedGoogle Scholar
  129. 129.
    Mendoza L, Olaso E, Anasagasti MJ, Fuentes AM, Vidal-Vanaclocha F. Mannose receptor-mediated endothelial cell activation contributes to B16 melanoma cell adhesion and metastasis in liver. J Cell Physiol. 1998;174(3):322–30.PubMedCrossRefGoogle Scholar
  130. 130.
    Vidal-Vanaclocha F, Alvarez A, Asumendi A, Urcelay B, Tonino P, Dinarello CA. Interleukin 1 (IL-1)-dependent melanoma hepatic metastasis in vivo; increased endothelial adherence by IL-1-induced mannose receptors and growth factor production in vitro. J Natl Cancer Inst. 1996;88(3–4):198–205.Google Scholar
  131. 131.
    Vidal-Vanaclocha F, Amezaga C, Asumendi A, Kaplanski G, Dinarello CA. Interleukin-1 receptor blockade reduces the number and size of murine B16 melanoma hepatic metastases. Cancer Res. 1994;54(10):2667–72.PubMedGoogle Scholar
  132. 132.
    Franses JW, Drosu NC, Gibson WJ, Chitalia VC, Edelman ER. Dysfunctional endothelial cells directly stimulate cancer inflammation and metastasis. Int J Cancer. 2013;133(6):1334–44.PubMedPubMedCentralCrossRefGoogle Scholar
  133. 133.
    Barkan D, El Touny LH, Michalowski AM, Smith JA, Chu I, Davis AS, et al. Metastatic growth from dormant cells induced by a col-I-enriched fibrotic environment. Cancer Res. 2010;70(14):5706–16.PubMedPubMedCentralCrossRefGoogle Scholar
  134. 134.
    Warren A, Bertolino P, Cogger VC, McLean AJ, Fraser R, Le Couteur DG. Hepatic pseudocapillarization in aged mice. Exp Gerontol. 2005;40(10):807–12.PubMedCrossRefGoogle Scholar
  135. 135.
    McLean AJ, Cogger VC, Chong GC, Warren A, Markus AM, Dahlstrom JE, et al. Age-related pseudocapillarization of the human liver. J Pathol. 2003;200(1):112–7.PubMedCrossRefGoogle Scholar
  136. 136.
    Pablos JL, Santiago B, Galindo M, Torres C, Brehmer MT, Blanco FJ, et al. Synoviocyte-derived CXCL12 is displayed on endothelium and induces angiogenesis in rheumatoid arthritis. J Immunol. 2003;170(4):2147–52.PubMedCrossRefGoogle Scholar
  137. 137.
    Lebrin F, Deckers M, Bertolino P, Ten Dijke P. TGF-beta receptor function in the endothelium. Cardiovasc Res. 2005;65(3):599–608.PubMedCrossRefGoogle Scholar
  138. 138.
    Eppihimer MJ, Gunn J, Freeman GJ, Greenfield EA, Chernova T, Erickson J, et al. Expression and regulation of the PD-L1 immunoinhibitory molecule on microvascular endothelial cells. Microcirculation. 2002;9(2):133–45.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Khatib AM, Auguste P, Fallavollita L, Wang N, Samani A, Kontogiannea M, et al. Characterization of the host proinflammatory response to tumor cells during the initial stages of liver metastasis. Am J Pathol. 2005;167(3):749–59.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Khatib AM, Kontogiannea M, Fallavollita L, Jamison B, Meterissian S, Brodt P. Rapid induction of cytokine and E-selectin expression in the liver in response to metastatic tumor cells. Cancer Res. 1999;59(6):1356–61.PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Candice Alexandra Grzelak
    • 1
  • Andrea Rachel Lim
    • 1
  • Cyrus Michael Ghajar
    • 1
  1. 1.Public Health Sciences DivisionFred Hutchinson Cancer Research CenterSeattleUSA

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