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Cellular and Molecular Life Sciences

, Volume 70, Issue 23, pp 4431–4448 | Cite as

Positive and negative influence of the matrix architecture on antitumor immune surveillance

  • Elisa Peranzoni
  • Ana Rivas-Caicedo
  • Houcine Bougherara
  • Hélène Salmon
  • Emmanuel DonnadieuEmail author
Review

Abstract

The migration of T cells and access to tumor antigens is of utmost importance for the induction of protective anti-tumor immunity. Once having entered a malignant site, T cells encounter a complex environment composed of non-tumor cells along with the extracellular matrix (ECM). It is now well accepted that a deregulated ECM favors tumor progression and metastasis. Recent progress in imaging technologies has also highlighted the impact of the matrix architecture found in solid tumor on immune cells and especially T cells. In this review, we argue that the ability of T cells to mount an antitumor response is dependent on the matrix structure, more precisely on the balance between pro-migratory reticular fiber networks and unfavorable migration zones composed of dense and aligned ECM structures. Thus, the matrix architecture, that has long been considered to merely provide the structural framework of connective tissues, can play a key role in facilitating or suppressing the antitumor immune surveillance. A new challenge in cancer therapy will be to develop approaches aimed at altering the architecture of the tumor stroma, rendering it more permissive to antitumor T cells.

Keywords

Tumor T cells Stroma Extracellular matrix Motility Imaging 

Abbreviations

3D

Three-dimensional

ECM

Extracellular matrix

EMT

Epithelial-mesenchymal transition

FRC

Fibroblastic reticular cells

LOX

Lysyl oxidase

LTi

Lymphoid tissue inducer

MMP

Metalloproteinases

SHG

Second-harmonic generation

SLO

Secondary lymphoid organs

TACS

Tumor-associated collagen signature

TIL

Tumor-infiltrating lymphocytes

TLO

Tertiary lymphoid organs

Notes

Acknowledgments

We thank Nadège Bercovici and Alain Trautmann for critical reading of the manuscript. We are grateful to Diane Damotte and Marie-Aude Le Frère-Belda for providing the human specimens shown in Fig. 1. This work was supported in part by grants from the Ligue Nationale Contre le Cancer and the Institut National Contre le Cancer. Ana Rivas-Caicedo is supported by an Association pour la recherche sur le Cancer postdoctoral fellowship. Elisa Peranzoni is a recipient of the Fondazione Italiana per la Ricerca sul Cancro.

References

  1. 1.
    Pages F, Galon J, Dieu-Nosjean MC, Tartour E, Sautes-Fridman C, Fridman WH (2009) Immune infiltration in human tumors: a prognostic factor that should not be ignored. Oncogene 29(8):1093–1102PubMedGoogle Scholar
  2. 2.
    Kerkar SP, Restifo NP (2012) Cellular constituents of immune escape within the tumor microenvironment. Cancer Res 72(13):3125–3130PubMedGoogle Scholar
  3. 3.
    Fisher DT, Chen Q, Appenheimer MM, Skitzki J, Wang WC, Odunsi K, Evans SS (2006) Hurdles to lymphocyte trafficking in the tumor microenvironment: implications for effective immunotherapy. Immunol Invest 35(3–4):251–277PubMedGoogle Scholar
  4. 4.
    Vazquez-Cintron EJ, Monu NR, Frey AB (2010) Tumor-induced disruption of proximal TCR-mediated signal transduction in tumor-infiltrating CD8+ lymphocytes inactivates antitumor effector phase. J Immunol 185(12):7133–7140. doi: 10.4049/jimmunol.1001157 PubMedGoogle Scholar
  5. 5.
    Wang SF, Fouquet S, Chapon M, Salmon H, Regnier F, Labroquere K, Badoual C, Damotte D, Validire P, Maubec E, Delongchamps NB, Cazes A, Gibault L, Garcette M, Dieu-Nosjean MC, Zerbib M, Avril MF, Prevost-Blondel A, Randriamampita C, Trautmann A, Bercovici N (2011) Early T cell signalling is reversibly altered in PD-1+ T lymphocytes infiltrating human tumors. PLoS One 6(3):e17621PubMedGoogle Scholar
  6. 6.
    Ohtani H (2007) Focus on TILs: prognostic significance of tumor infiltrating lymphocytes in human colorectal cancer. Cancer Immun 7:4PubMedGoogle Scholar
  7. 7.
    Salmon H, Franciszkiewicz K, Damotte D, Dieu-Nosjean MC, Validire P, Trautmann A, Mami-Chouaib F, Donnadieu E (2012) Matrix architecture defines the preferential localization and migration of T cells into the stroma of human lung tumors. J Clin Invest 122(3):899–910PubMedGoogle Scholar
  8. 8.
    Verdegaal EM, Hoogstraten C, Sandel MH, Kuppen PJ, Brink AA, Claas FH, Gorsira MC, Graadt van Roggen JF, Osanto S (2007) Functional CD8+ T cells infiltrate into nonsmall cell lung carcinoma. Cancer Immunol Immunother 56(5):587–600. doi: 10.1007/s00262-006-0214-y PubMedGoogle Scholar
  9. 9.
    Wakabayashi O, Yamazaki K, Oizumi S, Hommura F, Kinoshita I, Ogura S, Dosaka-Akita H, Nishimura M (2003) CD4+ T cells in cancer stroma, not CD8+ T cells in cancer cell nests, are associated with favorable prognosis in human non-small cell lung cancers. Cancer Sci 94(11):1003–1009PubMedGoogle Scholar
  10. 10.
    Frey AB, Monu N (2008) Signaling defects in anti-tumor T cells. Immunol Rev 222:192–205. doi: 10.1111/j.1600-065X.2008.00606.x PubMedGoogle Scholar
  11. 11.
    Molon B, Ugel S, Del Pozzo F, Soldani C, Zilio S, Avella D, De Palma A, Mauri P, Monegal A, Rescigno M, Savino B, Colombo P, Jonjic N, Pecanic S, Lazzarato L, Fruttero R, Gasco A, Bronte V, Viola A (2011) Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells. J Exp Med 208(10):1949–1962PubMedGoogle Scholar
  12. 12.
    Pivarcsi A, Muller A, Hippe A, Rieker J, van Lierop A, Steinhoff M, Seeliger S, Kubitza R, Pippirs U, Meller S, Gerber PA, Liersch R, Buenemann E, Sonkoly E, Wiesner U, Hoffmann TK, Schneider L, Piekorz R, Enderlein E, Reifenberger J, Rohr UP, Haas R, Boukamp P, Haase I, Nurnberg B, Ruzicka T, Zlotnik A, Homey B (2007) Tumor immune escape by the loss of homeostatic chemokine expression. Proc Natl Acad Sci USA 104(48):19055–19060PubMedGoogle Scholar
  13. 13.
    Lepelletier Y, Smaniotto S, Hadj-Slimane R, Villa-Verde DM, Nogueira AC, Dardenne M, Hermine O, Savino W (2007) Control of human thymocyte migration by Neuropilin-1/Semaphorin-3A-mediated interactions. Proc Natl Acad Sci USA 104(13):5545–5550. doi: 10.1073/pnas.0700705104 PubMedGoogle Scholar
  14. 14.
    Vianello F, Olszak IT, Poznansky MC (2005) Fugetaxis: active movement of leukocytes away from a chemokinetic agent. J Mol Med (Berl) 83(10):752–763. doi: 10.1007/s00109-005-0675-z Google Scholar
  15. 15.
    Mrass P, Petravic J, Davenport MP, Weninger W (2010) Cell-autonomous and environmental contributions to the interstitial migration of T cells. Semin Immunopathol. doi: 10.1007/s00281-010-0212-1
  16. 16.
    Frantz C, Stewart KM, Weaver VM (2010) The extracellular matrix at a glance. J Cell Sci 123(Pt 24):4195–4200PubMedGoogle Scholar
  17. 17.
    Xiao Q, Ge G (2012) Lysyl oxidase, extracellular matrix remodeling and cancer metastasis. Cancer Microenviron 5(3):261–273. doi: 10.1007/s12307-012-0105-z PubMedGoogle Scholar
  18. 18.
    Kessenbrock K, Plaks V, Werb Z (2010) Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141(1):52–67. doi: 10.1016/j.cell.2010.03.015 PubMedGoogle Scholar
  19. 19.
    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):931–941PubMedGoogle Scholar
  20. 20.
    Brown E, McKee T, diTomaso E, Pluen A, Seed B, Boucher Y, Jain RK (2003) Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 9(6):796–800. doi: 10.1038/nm879 PubMedGoogle Scholar
  21. 21.
    Levental KR, Yu H, Kass L, Lakins JN, Egeblad M, Erler JT, Fong SF, Csiszar K, Giaccia A, Weninger W, Yamauchi M, Gasser DL, Weaver VM (2009) Matrix cross-linking forces tumor progression by enhancing integrin signaling. Cell 139(5):891–906PubMedGoogle Scholar
  22. 22.
    Provenzano PP, Eliceiri KW, Campbell JM, Inman DR, White JG, Keely PJ (2006) Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med 4(1):38. doi: 10.1186/1741-7015-4-38 PubMedGoogle Scholar
  23. 23.
    Provenzano PP, Inman DR, Eliceiri KW, Knittel JG, Yan L, Rueden CT, White JG, Keely PJ (2008) Collagen density promotes mammary tumor initiation and progression. BMC Med 6:11PubMedGoogle Scholar
  24. 24.
    Gritsenko PG, Ilina O, Friedl P (2012) Interstitial guidance of cancer invasion. J Pathol 226(2):185–199. doi: 10.1002/path.3031 PubMedGoogle Scholar
  25. 25.
    Duffield JS, Lupher M, Thannickal VJ, Wynn TA (2012) Host responses in tissue repair and fibrosis. Annu Rev Pathol. doi: 10.1146/annurev-pathol-020712-163930
  26. 26.
    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. doi: 10.1016/j.ajpath.2012.02.004 PubMedGoogle Scholar
  27. 27.
    Hinz B (2007) Formation and function of the myofibroblast during tissue repair. J Invest Dermatol 127(3):526–537. doi: 10.1038/sj.jid.5700613 PubMedGoogle Scholar
  28. 28.
    Wynn TA, Ramalingam TR (2012) Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat Med 18(7):1028–1040PubMedGoogle Scholar
  29. 29.
    Neyt K, Perros F, GeurtsvanKessel CH, Hammad H, Lambrecht BN (2012) Tertiary lymphoid organs in infection and autoimmunity. Trends Immunol 33(6):297–305. doi: 10.1016/j.it.2012.04.006 PubMedGoogle Scholar
  30. 30.
    Link A, Hardie DL, Favre S, Britschgi MR, Adams DH, Sixt M, Cyster JG, Buckley CD, Luther SA (2011) Association of T-zone reticular networks and conduits with ectopic lymphoid tissues in mice and humans. Am J Pathol 178(4):1662–1675. doi: 10.1016/j.ajpath.2010.12.039 PubMedGoogle Scholar
  31. 31.
    Aloisi F, Pujol-Borrell R (2006) Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 6(3):205–217. doi: 10.1038/nri1786 PubMedGoogle Scholar
  32. 32.
    Stranford S, Ruddle NH (2012) Follicular dendritic cells, conduits, lymphatic vessels, and high endothelial venules in tertiary lymphoid organs: parallels with lymph node stroma. Front Immunol 3:350. doi: 10.3389/fimmu.2012.00350 PubMedGoogle Scholar
  33. 33.
    Link A, Vogt TK, Favre S, Britschgi MR, Acha-Orbea H, Hinz B, Cyster JG, Luther SA (2007) Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nat Immunol 8(11):1255–1265. doi: 10.1038/ni1513 PubMedGoogle Scholar
  34. 34.
    Gretz JE, Anderson AO, Shaw S (1997) Cords, channels, corridors and conduits: critical architectural elements facilitating cell interactions in the lymph node cortex. Immunol Rev 156:11–24PubMedGoogle Scholar
  35. 35.
    Roozendaal R, Mebius RE, Kraal G (2008) The conduit system of the lymph node. Int Immunol 20(12):1483–1487. doi: 10.1093/intimm/dxn110 PubMedGoogle Scholar
  36. 36.
    Bajenoff M, Egen JG, Koo LY, Laugier JP, Brau F, Glaichenhaus N, Germain RN (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity 25(6):989–1001. doi: 10.1016/j.immuni.2006.10.011 PubMedGoogle Scholar
  37. 37.
    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. doi: 10.1056/NEJM198612253152606 PubMedGoogle Scholar
  38. 38.
    Lu P, Weaver VM, Werb Z (2012) The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 196(4):395–406PubMedGoogle Scholar
  39. 39.
    Cukierman E, Bassi DE (2010) Physico-mechanical aspects of extracellular matrix influences on tumorigenic behaviors. Semin Cancer Biol 20(3):139–145. doi: 10.1016/j.semcancer.2010.04.004 PubMedGoogle Scholar
  40. 40.
    Conklin MW, Eickhoff JC, Riching KM, Pehlke CA, Eliceiri KW, Provenzano PP, Friedl A, Keely PJ (2011) Aligned collagen is a prognostic signature for survival in human breast carcinoma. Am J Pathol 178(3):1221–1232. doi: 10.1016/j.ajpath.2010.11.076 PubMedGoogle Scholar
  41. 41.
    Soikkeli J, Podlasz P, Yin M, Nummela P, Jahkola T, Virolainen S, Krogerus L, Heikkila P, von Smitten K, Saksela O, Holtta E (2010) Metastatic outgrowth encompasses COL-I, FN1, and POSTN upregulation and assembly to fibrillar networks regulating cell adhesion, migration, and growth. Am J Pathol 177(1):387–403. doi: 10.2353/ajpath.2010.090748 PubMedGoogle Scholar
  42. 42.
    Cipponi A, Mercier M, Seremet T, Baurain JF, Theate I, van den Oord J, Stas M, Boon T, Coulie PG, van Baren N (2012) Neogenesis of lymphoid structures and antibody responses occur in human melanoma metastases. Cancer Res 72(16):3997–4007. doi: 10.1158/0008-5472.CAN-12-1377 PubMedGoogle Scholar
  43. 43.
    Dieu-Nosjean MC, Antoine M, Danel C, Heudes D, Wislez M, Poulot V, Rabbe N, Laurans L, Tartour E, de Chaisemartin L, Lebecque S, Fridman WH, Cadranel J (2008) Long-term survival for patients with non-small-cell lung cancer with intratumoral lymphoid structures. J Clin Oncol 26(27):4410–4417PubMedGoogle Scholar
  44. 44.
    Martinet L, Garrido I, Filleron T, Le Guellec S, Bellard E, Fournie JJ, Rochaix P, Girard JP (2011) Human solid tumors contain high endothelial venules: association with T- and B-lymphocyte infiltration and favorable prognosis in breast cancer. Cancer Res 71(17):5678–5687. doi: 10.1158/0008-5472.CAN-11-0431 PubMedGoogle Scholar
  45. 45.
    de Chaisemartin L, Goc J, Damotte D, Validire P, Magdeleinat P, Alifano M, Cremer I, Fridman WH, Sautes-Fridman C, Dieu-Nosjean MC (2011) Characterization of chemokines and adhesion molecules associated with T cell presence in tertiary lymphoid structures in human lung cancer. Cancer Res 71(20):6391–6399. doi: 10.1158/0008-5472.CAN-11-0952 PubMedGoogle Scholar
  46. 46.
    Cirri P, Chiarugi P (2011) Cancer associated fibroblasts: the dark side of the coin. Am J Cancer Res 1(4):482–497PubMedGoogle Scholar
  47. 47.
    Amatangelo MD, Bassi DE, Klein-Szanto AJ, Cukierman E (2005) Stroma-derived three-dimensional matrices are necessary and sufficient to promote desmoplastic differentiation of normal fibroblasts. Am J Pathol 167(2):475–488 167/2/475PubMedGoogle Scholar
  48. 48.
    Ng CP, Hinz B, Swartz MA (2005) Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro. J Cell Sci 118(Pt 20):4731–4739. doi: 10.1242/jcs.02605 PubMedGoogle Scholar
  49. 49.
    Peduto L, Dulauroy S, Lochner M, Spath GF, Morales MA, Cumano A, Eberl G (2009) Inflammation recapitulates the ontogeny of lymphoid stromal cells. J Immunol 182(9):5789–5799. doi: 10.4049/jimmunol.0803974 PubMedGoogle Scholar
  50. 50.
    Chioda M, Peranzoni E, Desantis G, Papalini F, Falisi E, Solito S, Mandruzzato S, Bronte V (2011) Myeloid cell diversification and complexity: an old concept with new turns in oncology. Cancer Metastasis Rev 30(1):27–43PubMedGoogle Scholar
  51. 51.
    Pollard JW (2009) Trophic macrophages in development and disease. Nat Rev Immunol 9(4):259–270PubMedGoogle Scholar
  52. 52.
    Schmid MC, Varner JA (2010) Myeloid cells in the tumor microenvironment: modulation of tumor angiogenesis and tumor inflammation. J Oncol 2010:201026. doi: 10.1155/2010/201026 PubMedGoogle Scholar
  53. 53.
    Murdoch C, Muthana M, Coffelt SB, Lewis CE (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 8(8):618–631. doi: 10.1038/nrc2444 PubMedGoogle Scholar
  54. 54.
    Duffield JS, Forbes SJ, Constandinou CM, Clay S, Partolina M, Vuthoori S, Wu S, Lang R, Iredale JP (2005) Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J Clin Invest 115(1):56–65PubMedGoogle Scholar
  55. 55.
    Karlmark KR, Weiskirchen R, Zimmermann HW, Gassler N, Ginhoux F, Weber C, Merad M, Luedde T, Trautwein C, Tacke F (2009) Hepatic recruitment of the inflammatory Gr1 + monocyte subset upon liver injury promotes hepatic fibrosis. Hepatology 50(1):261–274PubMedGoogle Scholar
  56. 56.
    Kisseleva T, Brenner DA (2008) Mechanisms of fibrogenesis. Exp Biol Med (Maywood) 233(2):109–122Google Scholar
  57. 57.
    Ramachandran P, Iredale JP (2012) Macrophages: central regulators of hepatic fibrogenesis and fibrosis resolution. J Hepatol 56(6):1417–1419PubMedGoogle Scholar
  58. 58.
    Fichtner-Feigl S, Strober W, Kawakami K, Puri RK, Kitani A (2006) IL-13 signaling through the IL-13alpha2 receptor is involved in induction of TGF-beta1 production and fibrosis. Nat Med 12(1):99–106PubMedGoogle Scholar
  59. 59.
    Ingman WV, Wyckoff J, Gouon-Evans V, Condeelis J, Pollard JW (2006) Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland. Dev Dyn 235(12):3222–3229PubMedGoogle Scholar
  60. 60.
    Kitagawa K, Wada T, Furuichi K, Hashimoto H, Ishiwata Y, Asano M, Takeya M, Kuziel WA, Matsushima K, Mukaida N, Yokoyama H (2004) Blockade of CCR2 ameliorates progressive fibrosis in kidney. Am J Pathol 165(1):237–246PubMedGoogle Scholar
  61. 61.
    Toh B, Wang X, Keeble J, Sim WJ, Khoo K, Wong WC, Kato M, Prevost-Blondel A, Thiery JP, Abastado JP (2011) Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor. PLoS Biol 9(9):e1001162. doi: 10.1371/journal.pbio.1001162 PubMedGoogle Scholar
  62. 62.
    Bonde AK, Tischler V, Kumar S, Soltermann A, Schwendener RA (2012) Intratumoral macrophages contribute to epithelial-mesenchymal transition in solid tumors. BMC Cancer 12:35PubMedGoogle Scholar
  63. 63.
    Ye XZ, Xu SL, Xin YH, Yu SC, Ping YF, Chen L, Xiao HL, Wang B, Yi L, Wang QL, Jiang XF, Yang L, Zhang P, Qian C, Cui YH, Zhang X, Bian XW (2012) Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-beta1 signaling pathway. J Immunol 189(1):444–453PubMedGoogle Scholar
  64. 64.
    Kawase A, Ishii G, Nagai K, Ito T, Nagano T, Murata Y, Hishida T, Nishimura M, Yoshida J, Suzuki K, Ochiai A (2008) Podoplanin expression by cancer associated fibroblasts predicts poor prognosis of lung adenocarcinoma. Int J Cancer 123(5):1053–1059PubMedGoogle Scholar
  65. 65.
    Tsujino T, Seshimo I, Yamamoto H, Ngan CY, Ezumi K, Takemasa I, Ikeda M, Sekimoto M, Matsuura N, Monden M (2007) Stromal myofibroblasts predict disease recurrence for colorectal cancer. Clin Cancer Res 13(7):2082–2090PubMedGoogle Scholar
  66. 66.
    Yamashita M, Ogawa T, Zhang X, Hanamura N, Kashikura Y, Takamura M, Yoneda M, Shiraishi T (2012) Role of stromal myofibroblasts in invasive breast cancer: stromal expression of alpha-smooth muscle actin correlates with worse clinical outcome. Breast Cancer 19(2):170–176PubMedGoogle Scholar
  67. 67.
    Franke FE, Von Georgi R, Zygmunt M, Munstedt K (2003) Association between fibronectin expression and prognosis in ovarian carcinoma. Anticancer Res 23(5b):4261–4267PubMedGoogle Scholar
  68. 68.
    Anttila MA, Tammi RH, Tammi MI, Syrjanen KJ, Saarikoski SV, Kosma VM (2000) High levels of stromal hyaluronan predict poor disease outcome in epithelial ovarian cancer. Cancer Res 60(1):150–155PubMedGoogle Scholar
  69. 69.
    Auvinen P, Tammi R, Parkkinen J, Tammi M, Agren U, Johansson R, Hirvikoski P, Eskelinen M, Kosma VM (2000) Hyaluronan in peritumoral stroma and malignant cells associates with breast cancer spreading and predicts survival. Am J Pathol 156(2):529–536PubMedGoogle Scholar
  70. 70.
    Tammi RH, Kultti A, Kosma VM, Pirinen R, Auvinen P, Tammi MI (2008) Hyaluronan in human tumors: pathobiological and prognostic messages from cell-associated and stromal hyaluronan. Semin Cancer Biol 18(4):288–295PubMedGoogle Scholar
  71. 71.
    Sis B, Sarioglu S, Sokmen S, Sakar M, Kupelioglu A, Fuzun M (2005) Desmoplasia measured by computer assisted image analysis: an independent prognostic marker in colorectal carcinoma. J Clin Pathol 58(1):32–38PubMedGoogle Scholar
  72. 72.
    Nadiarnykh O, LaComb RB, Brewer MA, Campagnola PJ (2010) Alterations of the extracellular matrix in ovarian cancer studied by second harmonic generation imaging microscopy. BMC Cancer 10:94PubMedGoogle Scholar
  73. 73.
    Wozniak MA, Desai R, Solski PA, Der CJ, Keely PJ (2003) ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J Cell Biol 163(3):583–595PubMedGoogle Scholar
  74. 74.
    Smith E, Breznik J, Lichty BD (2011) Strategies to enhance viral penetration of solid tumors. Hum Gene Ther 22(9):1053–1060. doi: 10.1089/hum.2010.227 PubMedGoogle Scholar
  75. 75.
    Butcher DT, Alliston T, Weaver VM (2009) A tense situation: forcing tumour progression. Nat Rev Cancer 9(2):108–122. doi: 10.1038/nrc2544 PubMedGoogle Scholar
  76. 76.
    Sangaletti S, Colombo MP (2008) Matricellular proteins at the crossroad of inflammation and cancer. Cancer Lett 267(2):245–253. doi: 10.1016/j.canlet.2008.03.027 PubMedGoogle Scholar
  77. 77.
    Chong HC, Tan CK, Huang RL, Tan NS (2012) Matricellular proteins: a sticky affair with cancers. J Oncol 2012:351089. doi: 10.1155/2012/351089 PubMedGoogle Scholar
  78. 78.
    Kudo-Saito C, Shirako H, Takeuchi T, Kawakami Y (2009) Cancer metastasis is accelerated through immunosuppression during Snail-induced EMT of cancer cells. Cancer Cell 15(3):195–206. doi: 10.1016/j.ccr.2009.01.023 PubMedGoogle Scholar
  79. 79.
    Parekh K, Ramachandran S, Cooper J, Bigner D, Patterson A, Mohanakumar T (2005) Tenascin-C, over expressed in lung cancer down regulates effector functions of tumor infiltrating lymphocytes. Lung Cancer 47(1):17–29. doi: 10.1016/j.lungcan.2004.05.016 PubMedGoogle Scholar
  80. 80.
    Alvarez MJ, Prada F, Salvatierra E, Bravo AI, Lutzky VP, Carbone C, Pitossi FJ, Chuluyan HE, Podhajcer OL (2005) Secreted protein acidic and rich in cysteine produced by human melanoma cells modulates polymorphonuclear leukocyte recruitment and antitumor cytotoxic capacity. Cancer Res 65(12):5123–5132. doi: 10.1158/0008-5472.CAN-04-1102 PubMedGoogle Scholar
  81. 81.
    Sangaletti S, Stoppacciaro A, Guiducci C, Torrisi MR, Colombo MP (2003) Leukocyte, rather than tumor-produced SPARC, determines stroma and collagen type IV deposition in mammary carcinoma. J Exp Med 198(10):1475–1485. doi: 10.1084/jem.20030202 PubMedGoogle Scholar
  82. 82.
    Adair-Kirk TL, Senior RM (2008) Fragments of extracellular matrix as mediators of inflammation. Int J Biochem Cell Biol 40(6–7):1101–1110. doi: 10.1016/j.biocel.2007.12.005 PubMedGoogle Scholar
  83. 83.
    Sorokin L (2010) The impact of the extracellular matrix on inflammation. Nat Rev Immunol 10(10):712–723 10.1038/nri2852PubMedGoogle Scholar
  84. 84.
    Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, Mecham RP, Senior RM, Shapiro SD (2006) Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest 116(3):753–759. doi: 10.1172/JCI25617 PubMedGoogle Scholar
  85. 85.
    Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, Folkerts G, Nijkamp FP, Blalock JE (2006) A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 12(3):317–323. doi: 10.1038/nm1361 PubMedGoogle Scholar
  86. 86.
    Midwood K, Sacre S, Piccinini AM, Inglis J, Trebaul A, Chan E, Drexler S, Sofat N, Kashiwagi M, Orend G, Brennan F, Foxwell B (2009) Tenascin-C is an endogenous activator of Toll-like receptor 4 that is essential for maintaining inflammation in arthritic joint disease. Nat Med 15(7):774–780. doi: 10.1038/nm.1987 PubMedGoogle Scholar
  87. 87.
    Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, Homer RJ, Goldstein DR, Bucala R, Lee PJ, Medzhitov R, Noble PW (2005) Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 11(11):1173–1179. doi: 10.1038/nm1315 PubMedGoogle Scholar
  88. 88.
    Schaefer L, Babelova A, Kiss E, Hausser HJ, Baliova M, Krzyzankova M, Marsche G, Young MF, Mihalik D, Gotte M, Malle E, Schaefer RM, Grone HJ (2005) The matrix component biglycan is proinflammatory and signals through Toll-like receptors 4 and 2 in macrophages. J Clin Invest 115(8):2223–2233. doi: 10.1172/JCI23755 PubMedGoogle Scholar
  89. 89.
    Bunt SK, Clements VK, Hanson EM, Sinha P, Ostrand-Rosenberg S (2009) Inflammation enhances myeloid-derived suppressor cell cross-talk by signaling through Toll-like receptor 4. J Leukoc Biol 85(6):996–1004. doi: 10.1189/jlb.0708446 PubMedGoogle Scholar
  90. 90.
    Friedl P, Brocker EB (2000) T cell migration in three-dimensional extracellular matrix: guidance by polarity and sensations. Dev Immunol 7(2–4):249–266PubMedGoogle Scholar
  91. 91.
    Wolf K, Muller R, Borgmann S, Brocker EB, Friedl P (2003) Amoeboid shape change and contact guidance: T-lymphocyte crawling through fibrillar collagen is independent of matrix remodeling by MMPs and other proteases. Blood 102(9):3262–3269. doi: 10.1182/blood-2002-12-3791 PubMedGoogle Scholar
  92. 92.
    Friedl P, Entschladen F, Conrad C, Niggemann B, Zanker KS (1998) CD4+ T lymphocytes migrating in three-dimensional collagen lattices lack focal adhesions and utilize beta1 integrin-independent strategies for polarization, interaction with collagen fibers and locomotion. Eur J Immunol 28(8):2331–2343. doi: 10.1002/(SICI)1521-4141(199808)28:08<2331:AID-IMMU2331>3.0.CO;2-C PubMedGoogle Scholar
  93. 93.
    Germain RN, Robey EA, Cahalan MD (2012) A decade of imaging cellular motility and interaction dynamics in the immune system. Science 336(6089):1676–1681. doi: 10.1126/science.1221063 PubMedGoogle Scholar
  94. 94.
    Miller MJ, Wei SH, Parker I, Cahalan MD (2002) Two-photon imaging of lymphocyte motility and antigen response in intact lymph node. Science 296(5574):1869–1873. doi: 10.1126/science.1070051 PubMedGoogle Scholar
  95. 95.
    Bajenoff M, Egen JG, Qi H, Huang AY, Castellino F, Germain RN (2007) Highways, byways and breadcrumbs: directing lymphocyte traffic in the lymph node. Trends Immunol 28(8):346–352. doi: 10.1016/j.it.2007.06.005 PubMedGoogle Scholar
  96. 96.
    Asperti-Boursin F, Real E, Bismuth G, Trautmann A, Donnadieu E (2007) CCR7 ligands control basal T cell motility within lymph node slices in a phosphoinositide 3-kinase-independent manner. J Exp Med 204(5):1167–1179. doi: 10.1084/jem.20062079 PubMedGoogle Scholar
  97. 97.
    Okada T, Cyster JG (2007) CC chemokine receptor 7 contributes to Gi-dependent T cell motility in the lymph node. J Immunol 178(5):2973–2978PubMedGoogle Scholar
  98. 98.
    Worbs T, Mempel TR, Bolter J, von Andrian UH, Forster R (2007) CCR7 ligands stimulate the intranodal motility of T lymphocytes in vivo. J Exp Med 204(3):489–495. doi: 10.1084/jem.20061706 PubMedGoogle Scholar
  99. 99.
    Bajenoff M (2012) Stromal cells control soluble material and cellular transport in lymph nodes. Front Immunol 3:304. doi: 10.3389/fimmu.2012.00304 PubMedGoogle Scholar
  100. 100.
    Mempel TR, Junt T, von Andrian UH (2006) Rulers over randomness: stroma cells guide lymphocyte migration in lymph nodes. Immunity 25(6):867–869. doi: 10.1016/j.immuni.2006.11.002 PubMedGoogle Scholar
  101. 101.
    Lee M, Mandl JN, Germain RN, Yates AJ (2012) The race for the prize: T-cell trafficking strategies for optimal surveillance. Blood 120(7):1432–1438. doi: 10.1182/blood-2012-04-424655 PubMedGoogle Scholar
  102. 102.
    Zeng M, Haase AT, Schacker TW (2012) Lymphoid tissue structure and HIV-1 infection: life or death for T cells. Trends Immunol 33(6):306–314. doi: 10.1016/j.it.2012.04.002 PubMedGoogle Scholar
  103. 103.
    Zeng M, Southern PJ, Reilly CS, Beilman GJ, Chipman JG, Schacker TW, Haase AT (2012) Lymphoid tissue damage in HIV-1 infection depletes naive T cells and limits T cell reconstitution after antiretroviral therapy. PLoS Pathog 8(1):e1002437. doi: 10.1371/journal.ppat.1002437 PubMedGoogle Scholar
  104. 104.
    Wilson EH, Harris TH, Mrass P, John B, Tait ED, Wu GF, Pepper M, Wherry EJ, Dzierzinski F, Roos D, Haydon PG, Laufer TM, Weninger W, Hunter CA (2009) Behavior of parasite-specific effector CD8+ T cells in the brain and visualization of a kinesis-associated system of reticular fibers. Immunity 30(2):300–311. doi: 10.1016/j.immuni.2008.12.013 PubMedGoogle Scholar
  105. 105.
    Matheu MP, Beeton C, Garcia A, Chi V, Rangaraju S, Safrina O, Monaghan K, Uemura MI, Li D, Pal S, De la Maza LM, Monuki E, Flugel A, Pennington MW, Parker I, Chandy KG, Cahalan MD (2008) Imaging of effector memory T cells during a delayed-type hypersensitivity reaction and suppression by Kv1.3 channel block. Immunity 29(4):602–614. doi: 10.1016/j.immuni.2008.07.015 PubMedGoogle Scholar
  106. 106.
    Boissonnas A, Fetler L, Zeelenberg IS, Hugues S, Amigorena S (2007) In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med 204(2):345–356PubMedGoogle Scholar
  107. 107.
    Mrass P, Takano H, Ng LG, Daxini S, Lasaro MO, Iparraguirre A, Cavanagh LL, von Andrian UH, Ertl HC, Haydon PG, Weninger W (2006) Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J Exp Med 203(12):2749–2761. doi: 10.1084/jem.20060710 PubMedGoogle Scholar
  108. 108.
    Egeblad M, Ewald AJ, Askautrud HA, Truitt ML, Welm BE, Bainbridge E, Peeters G, Krummel MF, Werb Z (2008) Visualizing stromal cell dynamics in different tumor microenvironments by spinning disk confocal microscopy. Dis Model Mech 1 (2–3):155–167; discussion 165. doi: 10.1242/dmm.000596
  109. 109.
    Engelhardt JJ, Boldajipour B, Beemiller P, Pandurangi P, Sorensen C, Werb Z, Egeblad M, Krummel MF (2012) Marginating dendritic cells of the tumor microenvironment cross-present tumor antigens and stably engage tumor-specific T cells. Cancer Cell 21(3):402–417. doi: 10.1016/j.ccr.2012.01.008 PubMedGoogle Scholar
  110. 110.
    Arrieumerlou C, Donnadieu E, Brennan P, Keryer G, Bismuth G, Cantrell D, Trautmann A (1998) Involvement of phosphoinositide 3-kinase and Rac in membrane ruffling induced by IL-2 in T cells. Eur J Immunol 28(6):1877–1885. doi: 10.1002/(SICI)1521-4141(199806)28:06<1877:AID-IMMU1877>3.0.CO;2-I PubMedGoogle Scholar
  111. 111.
    Lieubeau B, Heymann MF, Henry F, Barbieux I, Meflah K, Gregoire M (1999) Immunomodulatory effects of tumor-associated fibroblasts in colorectal-tumor development. Int J Cancer 81(4):629–636PubMedGoogle Scholar
  112. 112.
    Martin ML, Wall EM, Sandwith E, Girardin A, Milne K, Watson PH, Nelson BH (2010) Density of tumour stroma is correlated to outcome after adoptive transfer of CD4+ and CD8+ T cells in a murine mammary carcinoma model. Breast Cancer Res Treat 121(3):753–763. doi: 10.1007/s10549-009-0559-y PubMedGoogle Scholar
  113. 113.
    Ohno S, Tachibana M, Fujii T, Ueda S, Kubota H, Nagasue N (2002) Role of stromal collagen in immunomodulation and prognosis of advanced gastric carcinoma. Int J Cancer 97(6):770–774PubMedGoogle Scholar
  114. 114.
    Gorter A, Zijlmans HJ, van Gent H, Trimbos JB, Fleuren GJ, Jordanova ES (2010) Versican expression is associated with tumor-infiltrating CD8-positive T cells and infiltration depth in cervical cancer. Mod Pathol 23(12):1605–1615. doi: 10.1038/modpathol.2010.154 PubMedGoogle Scholar
  115. 115.
    Huang JH, Cardenas-Navia LI, Caldwell CC, Plumb TJ, Radu CG, Rocha PN, Wilder T, Bromberg JS, Cronstein BN, Sitkovsky M, Dewhirst MW, Dustin ML (2007) Requirements for T lymphocyte migration in explanted lymph nodes. J Immunol 178(12):7747–7755PubMedGoogle Scholar
  116. 116.
    Van Goethem E, Poincloux R, Gauffre F, Maridonneau-Parini I, Le Cabec V (2010) Matrix architecture dictates three-dimensional migration modes of human macrophages: differential involvement of proteases and podosome-like structures. J Immunol 184(2):1049–1061PubMedGoogle Scholar
  117. 117.
    Cougoule C, Van Goethem E, Le Cabec V, Lafouresse F, Dupre L, Mehraj V, Mege JL, Lastrucci C, Maridonneau-Parini I (2012) Blood leukocytes and macrophages of various phenotypes have distinct abilities to form podosomes and to migrate in 3D environments. Eur J Cell Biol 91(11–12):938–949PubMedGoogle Scholar
  118. 118.
    Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, Segall JE, Pollard JW, Condeelis J (2007) Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res 67(6):2649–2656PubMedGoogle Scholar
  119. 119.
    Kobayashi N, Miyoshi S, Mikami T, Koyama H, Kitazawa M, Takeoka M, Sano K, Amano J, Isogai Z, Niida S, Oguri K, Okayama M, McDonald JA, Kimata K, Taniguchi S, Itano N (2010) Hyaluronan deficiency in tumor stroma impairs macrophage trafficking and tumor neovascularization. Cancer Res 70(18):7073–7083. doi: 10.1158/0008-5472.CAN-09-4687 PubMedGoogle Scholar
  120. 120.
    Potter-Perigo S, Johnson PY, Evanko SP, Chan CK, Braun KR, Wilkinson TS, Altman LC, Wight TN (2009) Polyinosine-polycytidylic acid stimulates versican accumulation in the extracellular matrix promoting monocyte adhesion. Am J Respir Cell Mol Biol 43(1):109–120PubMedGoogle Scholar
  121. 121.
    Coombes JL, Han SJ, van Rooijen N, Raulet DH, Robey EA (2012) Infection-induced regulation of natural killer cells by macrophages and collagen at the lymph node subcapsular sinus. Cell Rep 2(1):124–135PubMedGoogle Scholar
  122. 122.
    Barker HE, Cox TR, Erler JT (2012) The rationale for targeting the LOX family in cancer. Nat Rev Cancer 12(8):540–552. doi: 10.1038/nrc3319 PubMedGoogle Scholar
  123. 123.
    Goetz JG, Minguet S, Navarro-Lerida I, Lazcano JJ, Samaniego R, Calvo E, Tello M, Osteso-Ibanez T, Pellinen T, Echarri A, Cerezo A, Klein-Szanto AJ, Garcia R, Keely PJ, Sanchez-Mateos P, Cukierman E, Del Pozo MA (2011) Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 146(1):148–163PubMedGoogle Scholar
  124. 124.
    Brennen WN, Isaacs JT, Denmeade SR (2012) Rationale behind targeting fibroblast activation protein-expressing carcinoma-associated fibroblasts as a novel chemotherapeutic strategy. Mol Cancer Ther 11(2):257–266. doi: 10.1158/1535-7163.MCT-11-0340 PubMedGoogle Scholar
  125. 125.
    Kraman M, Bambrough PJ, Arnold JN, Roberts EW, Magiera L, Jones JO, Gopinathan A, Tuveson DA, Fearon DT (2010) Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-alpha. Science 330(6005):827–830. doi: 10.1126/science.1195300 PubMedGoogle Scholar
  126. 126.
    Akhurst RJ, Hata A (2012) Targeting the TGFbeta signalling pathway in disease. Nat Rev Drug Discov 11(10):790–811. doi: 10.1038/nrd3810 PubMedGoogle Scholar
  127. 127.
    Liu J, Liao S, Diop-Frimpong B, Chen W, Goel S, Naxerova K, Ancukiewicz M, Boucher Y, Jain RK, Xu L (2012) TGF-beta blockade improves the distribution and efficacy of therapeutics in breast carcinoma by normalizing the tumor stroma. Proce Natl Acad Sci USA 109(41):16618–16623. doi: 10.1073/pnas.1117610109 Google Scholar
  128. 128.
    Bierie B, Moses HL (2006) Tumour microenvironment: TGFbeta: the molecular Jekyll and Hyde of cancer. Nat Rev Cancer 6(7):506–520. doi: 10.1038/nrc1926 PubMedGoogle Scholar
  129. 129.
    Flavell RA, Sanjabi S, Wrzesinski SH, Licona-Limon P (2010) The polarization of immune cells in the tumour environment by TGFbeta. Nat Rev Immunol 10(8):554–567. doi: 10.1038/nri2808 PubMedGoogle Scholar
  130. 130.
    McKee TD, Grandi P, Mok W, Alexandrakis G, Insin N, Zimmer JP, Bawendi MG, Boucher Y, Breakefield XO, Jain RK (2006) Degradation of fibrillar collagen in a human melanoma xenograft improves the efficacy of an oncolytic herpes simplex virus vector. Cancer Res 66(5):2509–2513. doi: 10.1158/0008-5472.CAN-05-2242 PubMedGoogle Scholar
  131. 131.
    Hurst LC, Badalamente MA, Hentz VR, Hotchkiss RN, Kaplan FT, Meals RA, Smith TM, Rodzvilla J (2009) Injectable collagenase clostridium histolyticum for Dupuytren’s contracture. N Engl J Med 361(10):968–979. doi: 10.1056/NEJMoa0810866 PubMedGoogle Scholar
  132. 132.
    Syed F, Thomas AN, Singh S, Kolluru V, Emeigh Hart SG, Bayat A (2012) In vitro study of novel collagenase (XIAFLEX(R)) on Dupuytren’s disease fibroblasts displays unique drug related properties. PLoS One 7(2):e31430. doi: 10.1371/journal.pone.0031430PONE-D-11-15575 PubMedGoogle Scholar
  133. 133.
    Bollyky PL, Wu RP, Falk BA, Lord JD, Long SA, Preisinger A, Teng B, Holt GE, Standifer NE, Braun KR, Xie CF, Samuels PL, Vernon RB, Gebe JA, Wight TN, Nepom GT (2011) ECM components guide IL-10 producing regulatory T-cell (TR1) induction from effector memory T-cell precursors. Proc Natl Acad Sci USA 108(19):7938–7943. doi: 10.1073/pnas.1017360108 PubMedGoogle Scholar
  134. 134.
    Provenzano PP, Cuevas C, Chang AE, Goel VK, Von Hoff DD, Hingorani SR (2012) Enzymatic targeting of the stroma ablates physical barriers to treatment of pancreatic ductal adenocarcinoma. Cancer Cell 21(3):418–429PubMedGoogle Scholar
  135. 135.
    Lukashev M, LePage D, Wilson C, Bailly V, Garber E, Lukashin A, Ngam-ek A, Zeng W, Allaire N, Perrin S, Xu X, Szeliga K, Wortham K, Kelly R, Bottiglio C, Ding J, Griffith L, Heaney G, Silverio E, Yang W, Jarpe M, Fawell S, Reff M, Carmillo A, Miatkowski K, Amatucci J, Crowell T, Prentice H, Meier W, Violette SM, Mackay F, Yang D, Hoffman R, Browning JL (2006) Targeting the lymphotoxin-beta receptor with agonist antibodies as a potential cancer therapy. Cancer Res 66(19):9617–9624. doi: 10.1158/0008-5472.CAN-06-0217 PubMedGoogle Scholar
  136. 136.
    Schrama D, Thor Straten P, Fischer WH, McLellan AD, Brocker EB, Reisfeld RA, Becker JC (2001) Targeting of lymphotoxin-alpha to the tumor elicits an efficient immune response associated with induction of peripheral lymphoid-like tissue. Immunity 14(2):111–121PubMedGoogle Scholar
  137. 137.
    Shields JD, Kourtis IC, Tomei AA, Roberts JM, Swartz MA (2010) Induction of lymphoidlike stroma and immune escape by tumors that express the chemokine CCL21. Science 328(5979):749–752. doi: 10.1126/science.1185837 PubMedGoogle Scholar
  138. 138.
    Mellman I, Coukos G, Dranoff G (2011) Cancer immunotherapy comes of age. Nature 480(7378):480–489. doi: 10.1038/nature10673 PubMedGoogle Scholar
  139. 139.
    DuFort CC, Paszek MJ, Weaver VM (2011) Balancing forces: architectural control of mechanotransduction. Nat Rev Mol Cell Biol 12(5):308–319. doi: 10.1038/nrm3112 PubMedGoogle Scholar

Copyright information

© Springer Basel 2013

Authors and Affiliations

  • Elisa Peranzoni
    • 1
    • 2
    • 3
  • Ana Rivas-Caicedo
    • 4
  • Houcine Bougherara
    • 1
    • 2
    • 3
  • Hélène Salmon
    • 5
  • Emmanuel Donnadieu
    • 1
    • 2
    • 3
    • 6
    Email author
  1. 1.Inserm, U1016, Institut CochinParisFrance
  2. 2.Cnrs UMR8104ParisFrance
  3. 3.Université Paris DescartesSorbonne Paris CitéFrance
  4. 4.Alta Tecnología en Laboratorios SA de CVMexicoMexico
  5. 5.Department of Oncological SciencesMount Sinai School of MedicineNew YorkUSA
  6. 6.Département d’Immunologie et d’HématologieInstitut CochinParisFrance

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