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Cell–Cell Mechanical Communication in Cancer

  • Samantha C. Schwager
  • Paul V. Taufalele
  • Cynthia A. Reinhart-King
Article
  • 153 Downloads

Abstract

Communication between cancer cells enables cancer progression and metastasis. While cell–cell communication in cancer has primarily been examined through chemical mechanisms, recent evidence suggests that mechanical communication through cell–cell junctions and cell–ECM linkages is also an important mediator of cancer progression. Cancer and stromal cells remodel the ECM through a variety of mechanisms, including matrix degradation, cross-linking, deposition, and physical remodeling. Cancer cells sense these mechanical environmental changes through cell–matrix adhesion complexes and subsequently alter their tension between both neighboring cells and the surrounding matrix, thereby altering the force landscape within the microenvironment. This communication not only allows cancer cells to communicate with each other, but allows stromal cells to communicate with cancer cells through matrix remodeling. Here, we review the mechanisms of intercellular force transmission, the subsequent matrix remodeling, and the implications of this mechanical communication on cancer progression.

Keywords

Mechanotransduction Extracellular matrix Mechanosensing Cell mechanics Intercellular force 

Notes

Acknowledgment

This work was supported by awards from the NIH (Award Number HL127499) and NSF (1738345, 1740900) to C.A.R-K.

Animal Studies

No animal studies were carried out by the authors for this article.

Conflict of Interest

Samantha Schwager, Paul Taufalele, and Cynthia Reinhart-King have no conflicts of interest to disclose.

Human Studies

No human studies were carried out by the authors for this article.

References

  1. 1.
    Aasen, T., M. Mesnil, C. C. Naus, P. D. Lampe, and D. W. Laird. Gap junctions and cancer: communicating for 50 years. Nat. Rev. Cancer 16:775–788, 2016.CrossRefGoogle Scholar
  2. 2.
    Acerbi, I., et al. Human breast cancer invasion and aggression correlates with ECM stiffening and immune cell infiltration. Integr. Biol. Quant. Biosci. Nano Macro 7:1120–1134, 2015.Google Scholar
  3. 3.
    Albinger-Hegyi, A., et al. Lysyl oxidase expression is an independent marker of prognosis and a predictor of lymph node metastasis in oral and oropharyngeal squamous cell carcinoma (OSCC). Int. J. Cancer 126:2653–2662, 2010.Google Scholar
  4. 4.
    Alexander, N. R., et al. Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. CB 18:1295–1299, 2008.CrossRefGoogle Scholar
  5. 5.
    Amano, M., et al. Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 271:20246–20249, 1996.CrossRefGoogle Scholar
  6. 6.
    Amoyel, M., and E. A. Bach. Cell competition: how to eliminate your neighbours. Development 141:988–1000, 2014.CrossRefGoogle Scholar
  7. 7.
    Angelucci, A., et al. Vesicle-associated urokinase plasminogen activator promotes invasion in prostate cancer cell lines. Clin. Exp. Metastasis 18:163, 2000.CrossRefGoogle Scholar
  8. 8.
    Antonyak, M. A., and R. A. Cerione. Microvesicles as Mediators of Intercellular Communication in Cancer. In: Cancer Cell Signaling: Methods and Protocols, edited by M. Robles-Flores. New York: Springer, 2014, pp. 147–173.CrossRefGoogle Scholar
  9. 9.
    Artym, V. V., Y. Zhang, F. Seillier-Moiseiwitsch, K. M. Yamada, and S. C. Mueller. Dynamic interactions of cortactin and membrane type 1 matrix metalloproteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 66:3034–3043, 2006.CrossRefGoogle Scholar
  10. 10.
    Baker, A.-M., D. Bird, G. Lang, T. R. Cox, and J. T. Erler. Lysyl oxidase enzymatic function increases stiffness to drive colorectal cancer progression through FAK. Oncogene 32:1863–1868, 2013.CrossRefGoogle Scholar
  11. 11.
    Balaban, N. Q., et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat. Cell Biol. 3:466–472, 2001.CrossRefGoogle Scholar
  12. 12.
    Bazellières, E., et al. Control of cell–cell forces and collective cell dynamics by the intercellular adhesome. Nat. Cell Biol. 17:409–420, 2015.CrossRefGoogle Scholar
  13. 13.
    Bertocchi, C., et al. Nanoscale architecture of cadherin-based cell adhesions. Nat. Cell Biol. 19:28–37, 2017.CrossRefGoogle Scholar
  14. 14.
    Bordeleau, F., et al. Matrix stiffening promotes a tumor vasculature phenotype. Proc. Natl. Acad. Sci. 114:492–497, 2017.CrossRefGoogle Scholar
  15. 15.
    Brás-Pereira, C., and E. Moreno. Mechanical cell competition. Curr. Opin. Cell Biol. 51:15–21, 2018.CrossRefGoogle Scholar
  16. 16.
    Broussard, J. A., et al. The desmoplakin–intermediate filament linkage regulates cell mechanics. Mol. Biol. Cell 28:3156–3164, 2017.CrossRefGoogle Scholar
  17. 17.
    Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. Turner. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487–525, 1988.CrossRefGoogle Scholar
  18. 18.
    Burridge, K., and K. Wennerberg. Rho and Rac take center stage. Cell 116:167–179, 2004.CrossRefGoogle Scholar
  19. 19.
    Calvo, F., et al. Mechanotransduction and YAP-dependent matrix remodelling is required for the generation and maintenance of cancer-associated fibroblasts. Nat. Cell Biol. 15:637–646, 2013.CrossRefGoogle Scholar
  20. 20.
    Carey, S. P., Z. E. Goldblatt, K. E. Martin, B. Romero, R. M. Williams, and C. A. Reinhart-King. Local extracellular matrix alignment directs cellular protrusion dynamics and migration through Rac1 and FAK. Integr. Biol. Quant. Biosci. Nano Macro 8:821–835, 2016.Google Scholar
  21. 21.
    Carey, S. P., et al. Comparative mechanisms of cancer cell migration through 3D matrix and physiological microtracks. Am. J. Physiol. Cell Physiol. 308:C436–C447, 2015.CrossRefGoogle Scholar
  22. 22.
    Cavalcanti-Adam, E. A., A. Micoulet, J. Blümmel, J. Auernheimer, H. Kessler, and J. P. Spatz. Lateral spacing of integrin ligands influences cell spreading and focal adhesion assembly. Eur. J. Cell Biol. 85:219–224, 2006.CrossRefGoogle Scholar
  23. 23.
    Cawston, T. E., and D. A. Young. Proteinases involved in matrix turnover during cartilage and bone breakdown. Cell Tissue Res. 339:221, 2010.CrossRefGoogle Scholar
  24. 24.
    Chang, H. Y., et al. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc. Natl Acad. Sci. U.S.A. 99:12877–12882, 2002.CrossRefGoogle Scholar
  25. 25.
    Chaudhuri, O., et al. Extracellular matrix stiffness and composition jointly regulate the induction of malignant phenotypes in mammary epithelium. Nat. Mater. 13:970–978, 2014.CrossRefGoogle Scholar
  26. 26.
    Choquet, D., D. P. Felsenfeld, and M. P. Sheetz. Extracellular matrix rigidity causes strengthening of integrin–cytoskeleton linkages. Cell 88:39–48, 1997.CrossRefGoogle Scholar
  27. 27.
    Collighan, R. J., and M. Griffin. Transglutaminase 2 cross-linking of matrix proteins: biological significance and medical applications. Amino Acids 36:659–670, 2009.CrossRefGoogle Scholar
  28. 28.
    Connell, L. E., and D. M. Helfman. Myosin light chain kinase plays a role in the regulation of epithelial cell survival. J. Cell Sci. 119:2269–2281, 2006.CrossRefGoogle Scholar
  29. 29.
    Costa-Silva, B., et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat. Cell Biol. 17:816–826, 2015.CrossRefGoogle Scholar
  30. 30.
    Cox, T. R., and J. T. Erler. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis. Model. Mech. 4:165–178, 2011.CrossRefGoogle Scholar
  31. 31.
    Das, T., K. Safferling, S. Rausch, N. Grabe, H. Boehm, and J. P. Spatz. A molecular mechanotransduction pathway regulates collective migration of epithelial cells. Nat. Cell Biol. 17:276–287, 2015.CrossRefGoogle Scholar
  32. 32.
    Di Gregorio, A., S. Bowling, and T. A. Rodriguez. Cell competition and its role in the regulation of cell fitness from development to cancer. Dev. Cell 38:621–634, 2016.CrossRefGoogle Scholar
  33. 33.
    Di Vizio, D., et al. Large oncosomes in human prostate cancer tissues and in the circulation of mice with metastatic disease. Am. J. Pathol. 181:1573–1584, 2012.CrossRefGoogle Scholar
  34. 34.
    Edgar, L. T., C. J. Underwood, J. E. Guilkey, J. B. Hoying, and J. A. Weiss. Extracellular matrix density regulates the rate of neovessel growth and branching in sprouting angiogenesis. PLoS ONE 9:e85178, 2014.CrossRefGoogle Scholar
  35. 35.
    Endres, M., S. Kneitz, M. F. Orth, R. K. Perera, A. Zernecke, and E. Butt. Regulation of matrix metalloproteinases (MMPs) expression and secretion in MDA-MB-231 breast cancer cells by LIM and SH3 protein 1 (LASP1). Oncotarget 7:64244–64259, 2016.CrossRefGoogle Scholar
  36. 36.
    Engl, W., B. Arasi, L. L. Yap, J. P. Thiery, and V. Viasnoff. Actin dynamics modulate mechanosensitive immobilization of E-cadherin at adherens junctions. Nat. Cell Biol. 16:587–594, 2014.CrossRefGoogle Scholar
  37. 37.
    Erler, J. T., et al. Lysyl oxidase is essential for hypoxia-induced metastasis. Nature 440:1222–1226, 2006.CrossRefGoogle Scholar
  38. 38.
    Fritz, G., I. Just, and B. Kaina. Rho GTPases are over-expressed in human tumors. Int. J. Cancer 81:682–687, 1999.CrossRefGoogle Scholar
  39. 39.
    Fullár, A., et al. Remodeling of extracellular matrix by normal and tumor-associated fibroblasts promotes cervical cancer progression. BMC Cancer 15:256, 2015.CrossRefGoogle Scholar
  40. 40.
    Fusek, M., J. Vetvickova, and V. Vetvicka. Secretion of cytokines in breast cancer cells: the molecular mechanism of procathepsin D proliferative effects. J. Interferon Cytokine Res. 27:191–199, 2007.CrossRefGoogle Scholar
  41. 41.
    Gaggioli, C., et al. Fibroblast-led collective invasion of carcinoma cells with differing roles for RhoGTPases in leading and following cells. Nat. Cell Biol. 9:1392–1400, 2007.CrossRefGoogle Scholar
  42. 42.
    Ganz, A., et al. Traction forces exerted through N-cadherin contacts. Biol. Cell 98:721–730, 2006.CrossRefGoogle Scholar
  43. 43.
    Georges, P. C., et al. Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 293:G1147–G1154, 2007.CrossRefGoogle Scholar
  44. 44.
    Ghajar, C. M., et al. Mesenchymal cells stimulate capillary morphogenesis via distinct proteolytic mechanisms. Exp. Cell Res. 316:813–825, 2010.CrossRefGoogle Scholar
  45. 45.
    Gialeli, C., A. D. Theocharis, and N. K. Karamanos. Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting. FEBS J. 278:16–27, 2011.CrossRefGoogle Scholar
  46. 46.
    Gjorevski, N., A. S. Piotrowski, V. D. Varner, and C. M. Nelson. Dynamic tensile forces drive collective cell migration through three-dimensional extracellular matrices. Sci. Rep. 5:11458, 2015.CrossRefGoogle Scholar
  47. 47.
    Glentis, A., et al. Cancer-associated fibroblasts induce metalloprotease-independent cancer cell invasion of the basement membrane. Nat. Commun. 8(1):924, 2017.CrossRefGoogle Scholar
  48. 48.
    Gomez, G. A., R. W. McLachlan, and A. S. Yap. Productive tension: force-sensing and homeostasis of cell–cell junctions. Trends Cell Biol. 21:499–505, 2011.CrossRefGoogle Scholar
  49. 49.
    Gudipaty, S. A., et al. Mechanical stretch triggers rapid epithelial cell division through Piezo1. Nature 543:118–121, 2017.CrossRefGoogle Scholar
  50. 50.
    Guo, W., M. T. Frey, N. A. Burnham, and Y. Wang. Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 90:2213–2220, 2006.CrossRefGoogle Scholar
  51. 51.
    Haage, A., and I. C. Schneider. Cellular contractility and extracellular matrix stiffness regulate matrix metalloproteinase activity in pancreatic cancer cells. FASEB J. 28:3589–3599, 2014.CrossRefGoogle Scholar
  52. 52.
    Hakulinen, J., L. Sankkila, N. Sugiyama, K. Lehti, and J. Keski-Oja. Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J. Cell. Biochem. 105:1211–1218, 2008.CrossRefGoogle Scholar
  53. 53.
    Hall, M. S., et al. Fibrous nonlinear elasticity enables positive mechanical feedback between cells and ECMs. Proc. Natl. Acad. Sci. 113:14043–14048, 2016.CrossRefGoogle Scholar
  54. 54.
    Han, W., et al. Oriented collagen fibers direct tumor cell intravasation. Proc. Natl. Acad. Sci. 113:11208–11213, 2016.CrossRefGoogle Scholar
  55. 55.
    Han, Y. L., et al. Cell contraction induces long-ranged stress stiffening in the extracellular matrix. Proc. Natl. Acad. Sci. U.S.A. 115(16):4075–4080, 2018.CrossRefGoogle Scholar
  56. 56.
    Hatte, G., C. Prigent, and J.-P. Tassan. Tight junctions negatively regulate mechanical forces applied to adherens junctions in vertebrate epithelial tissue. J. Cell Sci. 2018.  https://doi.org/10.1242/jcs.208736.CrossRefGoogle Scholar
  57. 57.
    Heino, J., and J. Käpylä. Cellular receptors of extracellular matrix molecules. Curr. Pharm. Des. 15:1309–1317, 2009.CrossRefGoogle Scholar
  58. 58.
    Hellström, M., et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445:776–780, 2007.CrossRefGoogle Scholar
  59. 59.
    Horwitz, A., K. Duggan, C. Buck, M. C. Beckerle, and K. Burridge. Interaction of plasma membrane fibronectin receptor with talin—a transmembrane linkage. Nature 320:531–533, 1986.CrossRefGoogle Scholar
  60. 60.
    Hotchin, N. A., and A. Hall. The assembly of integrin adhesion complexes requires both extracellular matrix and intracellular rho/rac GTPases. J. Cell Biol. 131:1857–1865, 1995.CrossRefGoogle Scholar
  61. 61.
    Humphries, D. L., J. A. Grogan, and E. A. Gaffney. Mechanical cell–cell communication in fibrous networks: the importance of network geometry. Bull. Math. Biol. 79:498–524, 2017.MathSciNetzbMATHCrossRefGoogle Scholar
  62. 62.
    Huveneers, S., and J. de Rooij. Mechanosensitive systems at the cadherin-F–actin interface. J. Cell Sci. 126:403–413, 2013.CrossRefGoogle Scholar
  63. 63.
    Itoh, Y., and H. Nagase. Matrix metalloproteinases in cancer. Essays Biochem. 38:21–36, 2002.CrossRefGoogle Scholar
  64. 64.
    Jaffe, A. B., and A. Hall. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21:247–269, 2005.CrossRefGoogle Scholar
  65. 65.
    Johnson, J. L., N. A. Najor, and K. J. Green. Desmosomes: regulators of cellular signaling and adhesion in epidermal health and disease. Cold Spring Harb. Perspect. Med. 4(11):a015297, 2014.CrossRefGoogle Scholar
  66. 66.
    Kalluri, R., and M. Zeisberg. Fibroblasts in cancer. Nat. Rev. Cancer 6:392–401, 2006.CrossRefGoogle Scholar
  67. 67.
    Kameritsch, P., N. Khandoga, U. Pohl, and K. Pogoda. Gap junctional communication promotes apoptosis in a connexin-type-dependent manner. Cell Death Dis. 4:e584, 2013.CrossRefGoogle Scholar
  68. 68.
    Kaneko-Kawano, T., et al. Dynamic regulation of myosin light chain phosphorylation by Rho-kinase. PLoS ONE 7:e39269, 2012.CrossRefGoogle Scholar
  69. 69.
    Kano, A. Tumor cell secretion of soluble factor(s) for specific immunosuppression. Sci. Rep. 5:8913, 2015.CrossRefGoogle Scholar
  70. 70.
    Kassianidou, E., J. H. Hughes, S. Kumar, and Y.-L. Wang. Activation of ROCK and MLCK tunes regional stress fiber formation and mechanics via preferential myosin light chain phosphorylation. Mol. Biol. Cell 28:3832–3843, 2017.CrossRefGoogle Scholar
  71. 71.
    Katz, B.-Z., E. Zamir, A. Bershadsky, Z. Kam, K. M. Yamada, and B. Geiger. Physical state of the extracellular matrix regulates the structure and molecular composition of cell–matrix adhesions. Mol. Biol. Cell 11:1047–1060, 2000.CrossRefGoogle Scholar
  72. 72.
    Kessenbrock, K., V. Plaks, and Z. Werb. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 141:52–67, 2010.CrossRefGoogle Scholar
  73. 73.
    Kim, J.-H., L. J. Dooling, and A. R. Asthagiri. Intercellular mechanotransduction during multicellular morphodynamics. J. R. Soc. Interface 7:S341–S350, 2010.CrossRefGoogle Scholar
  74. 74.
    Kirschmann, D. A., et al. A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 62:4478–4483, 2002.Google Scholar
  75. 75.
    Klinke, D. J. Eavesdropping on altered cell-to-cell signaling in cancer by secretome profiling. Mol. Cell. Oncol. 3:e1029061, 2015.CrossRefGoogle Scholar
  76. 76.
    Kraning-Rush, C. M., J. P. Califano, and C. A. Reinhart-King. Cellular traction stresses increase with increasing metastatic potential. PLoS ONE 7(2):e32572, 2012.CrossRefGoogle Scholar
  77. 77.
    Kraning-Rush, C. M., S. P. Carey, M. C. Lampi, and C. A. Reinhart-King. Microfabricated collagen tracks facilitate single cell metastatic invasion in 3D. Integr. Biol. Quant. Biosci. Nano Macro 5:606–616, 2013.Google Scholar
  78. 78.
    Labernadie, A., et al. A mechanically active heterotypic E-cadherin/N-cadherin adhesion enables fibroblasts to drive cancer cell invasion. Nat. Cell Biol. 19:224–237, 2017.CrossRefGoogle Scholar
  79. 79.
    Laghezza Masci, V., A. R. Taddei, G. Gambellini, F. Giorgi, and A. M. Fausto. Microvesicles shed from fibroblasts act as metalloproteinase carriers in a 3-D collagen matrix. J. Circ. Biomark. 2016.  https://doi.org/10.1177/1849454416663660.CrossRefGoogle Scholar
  80. 80.
    Larsen, M., V. V. Artym, J. A. Green, and K. M. Yamada. The matrix reorganized: extracellular matrix remodeling and integrin signaling. Curr. Opin. Cell Biol. 18:463–471, 2006.CrossRefGoogle Scholar
  81. 81.
    le Duc, Q., et al. Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner. J. Cell Biol. 189:1107–1115, 2010.CrossRefGoogle Scholar
  82. 82.
    Levental, K. R., et al. Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139:891–906, 2009.CrossRefGoogle Scholar
  83. 83.
    Li, L., et al. E-cadherin plays an essential role in collective directional migration of large epithelial sheets. Cell. Mol. Life Sci. 69:2779–2789, 2012.CrossRefGoogle Scholar
  84. 84.
    Lo, C. M., H. B. Wang, M. Dembo, and Y. L. Wang. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144–152, 2000.CrossRefGoogle Scholar
  85. 85.
    Ma, L.-J., et al. Expression of LOX and MMP-2 in gastric cancer tissue and the effects of LOX and MMP-2 on tumor invasion and metastasis. Chin. J. Oncol. 33:37–41, 2011.Google Scholar
  86. 86.
    Maia, J., S. Caja, M. C. Strano Moraes, N. Couto, and B. Costa-Silva. Exosome-based cell–cell communication in the tumor microenvironment. Front. Cell Dev. Biol. 6:18, 2018.CrossRefGoogle Scholar
  87. 87.
    Martin, A. C., M. Gelbart, R. Fernandez-Gonzalez, M. Kaschube, and E. F. Wieschaus. Integration of contractile forces during tissue invagination. J. Cell Biol. 188:735–749, 2010.CrossRefGoogle Scholar
  88. 88.
    Martin, A. C., M. Kaschube, and E. F. Wieschaus. Pulsed contractions of an actin-myosin network drive apical constriction. Nature 457:495–499, 2009.CrossRefGoogle Scholar
  89. 89.
    Maruthamuthu, V., B. Sabass, U. S. Schwarz, and M. L. Gardel. Cell–ECM traction force modulates endogenous tension at cell–cell contacts. Proc. Natl. Acad. Sci. U.S.A. 108:4708–4713, 2011.CrossRefGoogle Scholar
  90. 90.
    Maruyama, T., and Y. Fujita. Cell competition in mammals—novel homeostatic machinery for embryonic development and cancer prevention. Curr. Opin. Cell Biol. 48:106–112, 2017.CrossRefGoogle Scholar
  91. 91.
    McWhorter, F. Y., C. T. Davis, and W. F. Liu. Physical and mechanical regulation of macrophage phenotype and function. Cell. Mol. Life Sci. 72:1303–1316, 2015.CrossRefGoogle Scholar
  92. 92.
    Mekhdjian, A. H., et al. Integrin-mediated traction force enhances paxillin molecular associations and adhesion dynamics that increase the invasiveness of tumor cells into a three-dimensional extracellular matrix. Mol. Biol. Cell 28:1467–1488, 2017.CrossRefGoogle Scholar
  93. 93.
    Monsky, W. L., et al. A potential marker protease of invasiveness, separase, is localized on invadopodia of human malignant melanoma cells. Cancer Res. 54:5702–5710, 1994.Google Scholar
  94. 94.
    Mulligan, J. A., F. Bordeleau, C. A. Reinhart-King, and S. G. Adie. Measurement of dynamic cell-induced 3D displacement fields in vitro for traction force optical coherence microscopy. Biomed. Opt. Express 8:1152–1171, 2017.CrossRefGoogle Scholar
  95. 95.
    Muranen, T., et al. Starved epithelial cells uptake extracellular matrix for survival. Nat. Commun. 8:13989, 2017.CrossRefGoogle Scholar
  96. 96.
    Naba, A., K. R. Clauser, S. Hoersch, H. Liu, S. A. Carr, and R. O. Hynes. The matrisome: in silico definition and in vivo characterization by proteomics of normal and tumor extracellular matrices. Mol. Cell. Proteomics (MCP) 11:M111.014647, 2012.CrossRefGoogle Scholar
  97. 97.
    Nabeshima, K., T. Inoue, Y. Shimao, and T. Sameshima. Matrix metalloproteinases in tumor invasion: role for cell migration. Pathol. Int. 52:255–264, 2002.CrossRefGoogle Scholar
  98. 98.
    Namy, P., J. Ohayon, and P. Tracqui. Critical conditions for pattern formation and in vitro tubulogenesis driven by cellular traction fields. J. Theor. Biol. 227:103–120, 2004.MathSciNetCrossRefGoogle Scholar
  99. 99.
    Ng, M. R., A. Besser, J. S. Brugge, and G. Danuser. Mapping the dynamics of force transduction at cell–cell junctions of epithelial clusters. eLife 3:e03282, 2014.CrossRefGoogle Scholar
  100. 100.
    Oria, R., et al. Force loading explains spatial sensing of ligands by cells. Nature 552:219–224, 2017.Google Scholar
  101. 101.
    Oster, G. F., J. D. Murray, and A. K. Harris. Mechanical aspects of mesenchymal morphogenesis. J. Embryol. Exp. Morphol. 78:83–125, 1983.zbMATHGoogle Scholar
  102. 102.
    Page-McCaw, A., A. J. Ewald, and Z. Werb. Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8:221–233, 2007.CrossRefGoogle Scholar
  103. 103.
    Panorchan, P., M. S. Thompson, K. J. Davis, Y. Tseng, K. Konstantopoulos, and D. Wirtz. Single-molecule analysis of cadherin-mediated cell–cell adhesion. J. Cell Sci. 119:66–74, 2006.CrossRefGoogle Scholar
  104. 104.
    Parsons, J. T., A. R. Horwitz, and M. A. Schwartz. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat. Rev. Mol. Cell Biol. 11:633–643, 2010.CrossRefGoogle Scholar
  105. 105.
    Pascalis, C. D., et al. Intermediate filaments control collective migration by restricting traction forces and sustaining cell–cell contacts. J. Cell Biol. 217(9):3031–3044, 2018.CrossRefGoogle Scholar
  106. 106.
    Pasdar, M., and W. J. Nelson. Kinetics of desmosome assembly in Madin–Darby canine kidney epithelial cells: temporal and spatial regulation of desmoplakin organization and stabilization upon cell–cell contact. II. Morphological analysis. J. Cell Biol. 106:687–695, 1988.CrossRefGoogle Scholar
  107. 107.
    Paszek, M. J., et al. Tensional homeostasis and the malignant phenotype. Cancer Cell 8:241–254, 2005.CrossRefGoogle Scholar
  108. 108.
    Pawlizak, S., et al. Testing the differential adhesion hypothesis across the epithelial–mesenchymal transition. New J. Phys. 17:083049, 2015.CrossRefGoogle Scholar
  109. 109.
    Peinado, H., et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18:883–891, 2012.CrossRefGoogle Scholar
  110. 110.
    Pelham, R. J., and Y. Wang. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol. Biol. Cell 10:935–945, 1999.CrossRefGoogle Scholar
  111. 111.
    Plotnikov, S. V., A. M. Pasapera, B. Sabass, and C. M. Waterman. Force fluctuations within focal adhesions mediate ECM-Rigidity sensing to guide directed cell migration. Cell 151:1513–1527, 2012.CrossRefGoogle Scholar
  112. 112.
    Potente, M., H. Gerhardt, and P. Carmeliet. Basic and therapeutic aspects of angiogenesis. Cell 146:873–887, 2011.CrossRefGoogle Scholar
  113. 113.
    Prakasam, A. K., V. Maruthamuthu, and D. E. Leckband. Similarities between heterophilic and homophilic cadherin adhesion. Proc. Natl. Acad. Sci. 103:15434–15439, 2006.CrossRefGoogle Scholar
  114. 114.
    Provenzano, P. P., K. W. Eliceiri, J. M. Campbell, D. R. Inman, J. G. White, and P. J. Keely. Collagen reorganization at the tumor-stromal interface facilitates local invasion. BMC Med. 4:38, 2006.CrossRefGoogle Scholar
  115. 115.
    Provenzano, P. P., D. R. Inman, K. W. Eliceiri, and P. J. Keely. Matrix density-induced mechanoregulation of breast cell phenotype, signaling, and gene expression through a FAK-ERK linkage. Oncogene 28:4326–4343, 2009.CrossRefGoogle Scholar
  116. 116.
    Provenzano, P. P., D. R. Inman, K. W. Eliceiri, S. M. Trier, and P. J. Keely. Contact guidance mediated three-dimensional cell migration is regulated by Rho/ROCK-dependent matrix reorganization. Biophys. J. 95:5374–5384, 2008.CrossRefGoogle Scholar
  117. 117.
    Provenzano, P. P., et al. Collagen density promotes mammary tumor initiation and progression. BMC Med. 6:11, 2008.CrossRefGoogle Scholar
  118. 118.
    Reffay, M., et al. Interplay of RhoA and mechanical forces in collective cell migration driven by leader cells. Nat. Cell Biol. 16:217–223, 2014.CrossRefGoogle Scholar
  119. 119.
    Reid, S. E., et al. Tumor matrix stiffness promotes metastatic cancer cell interaction with the endothelium. EMBO J. 36:2373–2389, 2017.CrossRefGoogle Scholar
  120. 120.
    Reinhart-King, C. A., M. Dembo, and D. A. Hammer. Cell–cell mechanical communication through compliant substrates. Biophys. J. 95:6044–6051, 2008.CrossRefGoogle Scholar
  121. 121.
    Riching, K. M., et al. 3D collagen alignment limits protrusions to enhance breast cancer cell persistence. Biophys. J. 107:2546–2558, 2014.CrossRefGoogle Scholar
  122. 122.
    Riveline, D., et al. Focal contacts as mechanosensors: externally applied local mechanical force induces growth of focal contacts by an mDia1-dependent and ROCK-independent mechanism. J. Cell Biol. 153:1175–1186, 2001.CrossRefGoogle Scholar
  123. 123.
    Roca-Cusachs, P., N. C. Gauthier, A. Del Rio, and M. P. Sheetz. Clustering of alpha(5)beta(1) integrins determines adhesion strength whereas alpha(v)beta(3) and talin enable mechanotransduction. Proc. Natl Acad. Sci. U. S. A. 106:16245–16250, 2009.CrossRefGoogle Scholar
  124. 124.
    Rodemann, H. P., and G. A. Müller. Characterization of human renal fibroblasts in health and disease: II. In vitro growth, differentiation, and collagen synthesis of fibroblasts from kidneys with interstitial fibrosis. Am. J. Kidney Dis. 17:684–686, 1991.CrossRefGoogle Scholar
  125. 125.
    Salameh, A., and S. Dhein. Effects of mechanical forces and stretch on intercellular gap junction coupling. Biochim. Biophys. Acta (BBA) 1828:147–156, 2013.CrossRefGoogle Scholar
  126. 126.
    Sawada, Y., et al. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell 127:1015–1026, 2006.CrossRefGoogle Scholar
  127. 127.
    Schrader, J., et al. Matrix stiffness modulates proliferation, chemotherapeutic response and dormancy in hepatocellular carcinoma cells. Hepatology 53:1192–1205, 2011.CrossRefGoogle Scholar
  128. 128.
    Schwarz, U. S., and M. L. Gardel. United we stand: integrating the actin cytoskeleton and cell–matrix adhesions in cellular mechanotransduction. J. Cell Sci. 125:3051–3060, 2012.CrossRefGoogle Scholar
  129. 129.
    Seong, J., N. Wang, and Y. Wang. Mechanotransduction at focal adhesions: from physiology to cancer development. J. Cell Mol. Med. 17:597–604, 2013.CrossRefGoogle Scholar
  130. 130.
    Sewell-Loftin, M. K., et al. Cancer-associated fibroblasts support vascular growth through mechanical force. Sci. Rep. 7:12574, 2017.CrossRefGoogle Scholar
  131. 131.
    Shi, Q., et al. Rapid disorganization of mechanically interacting systems of mammary acini. Proc. Natl. Acad. Sci. 111:658–663, 2014.CrossRefGoogle Scholar
  132. 132.
    Sica, A., et al. Macrophage polarization in tumour progression. Semin. Cancer Biol. 18:349–355, 2008.CrossRefGoogle Scholar
  133. 133.
    Sivasankar, S., B. Gumbiner, and D. Leckband. Direct measurements of multiple adhesive alignments and unbinding trajectories between cadherin extracellular domains. Biophys. J. 80:1758–1768, 2001.CrossRefGoogle Scholar
  134. 134.
    Sluysmans, S., E. Vasileva, D. Spadaro, J. Shah, F. Rouaud, and S. Citi. The role of apical cell–cell junctions and associated cytoskeleton in mechanotransduction. Biol. Cell 109:139–161, 2017.CrossRefGoogle Scholar
  135. 135.
    Stachowiak, M. R., et al. A mechanical-biochemical feedback loop regulates remodeling in the actin cytoskeleton. Proc. Natl Acad. Sci. U.S.A. 111:17528–17533, 2014.CrossRefGoogle Scholar
  136. 136.
    Sunyer, R., et al. Collective cell durotaxis emerges from long-range intercellular force transmission. Science 353:1157–1161, 2016.CrossRefGoogle Scholar
  137. 137.
    Tamada, M., M. P. Sheetz, and Y. Sawada. Activation of a signaling cascade by cytoskeleton stretch. Dev. Cell 7:709–718, 2004.CrossRefGoogle Scholar
  138. 138.
    Tambe, D. T., et al. Collective cell guidance by cooperative intercellular forces. Nat. Mater. 10:469–475, 2011.CrossRefGoogle Scholar
  139. 139.
    Tan, J. L., J. Tien, D. M. Pirone, D. S. Gray, K. Bhadriraju, and C. S. Chen. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. 100:1484–1489, 2003.CrossRefGoogle Scholar
  140. 140.
    Tornavaca, O., et al. ZO-1 controls endothelial adherens junctions, cell–cell tension, angiogenesis, and barrier formation. J. Cell Biol. 208:821–838, 2015.CrossRefGoogle Scholar
  141. 141.
    Trepat, X., and J. J. Fredberg. Plithotaxis and emergent dynamics in collective cellular migration. Trends Cell Biol. 21:638–646, 2011.CrossRefGoogle Scholar
  142. 142.
    Ulrich, T. A., E. M. de Juan Pardo, and S. Kumar. The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Res. 69:4167–4174, 2009.CrossRefGoogle Scholar
  143. 143.
    van Helvert, S., and P. Friedl. Strain stiffening of fibrillar collagen during individual and collective cell migration identified by AFM nanoindentation. ACS Appl. Mater. Interfaces. 8:21946–21955, 2016.CrossRefGoogle Scholar
  144. 144.
    van Oers, R. F. M., E. G. Rens, D. J. LaValley, C. A. Reinhart-King, and R. M. H. Merks. Mechanical cell–matrix feedback explains pairwise and collective endothelial cell behavior in vitro. PLoS Comput. Biol. 10(8):e1003774, 2014.CrossRefGoogle Scholar
  145. 145.
    Vasquez, C. G., and A. C. Martin. Force transmission in epithelial tissues. Dev. Dyn. 245:361–371, 2016.CrossRefGoogle Scholar
  146. 146.
    Vishwakarma, M., J. D. Russo, D. Probst, U. S. Schwarz, T. Das, and J. P. Spatz. Mechanical interactions among followers determine the emergence of leaders in migrating epithelial cell collectives. Nat. Commun. 9:3469, 2018.CrossRefGoogle Scholar
  147. 147.
    Wagstaff, L., et al. Mechanical cell competition kills cells via induction of lethal p53 levels. Nat. Commun. 7:11373, 2016.CrossRefGoogle Scholar
  148. 148.
    Wang, H., A. S. Abhilash, C. S. Chen, R. G. Wells, and V. B. Shenoy. Long-range force transmission in fibrous matrices enabled by tension-driven alignment of fibers. Biophys. J. 107:2592–2603, 2014.CrossRefGoogle Scholar
  149. 149.
    Wang, K., R. C. Andresen Eguiluz, F. Wu, B. R. Seo, C. Fischbach, and D. Gourdon. Stiffening and unfolding of early deposited-fibronectin increase proangiogenic factor secretion by breast cancer-associated stromal cells. Biomaterials 54:63–71, 2015.CrossRefGoogle Scholar
  150. 150.
    Wang, N., J. P. Butler, and D. E. Ingber. Mechanotransduction across the cell surface and through the cytoskeleton. Science 260:1124–1127, 1993.CrossRefGoogle Scholar
  151. 151.
    Wang, T.-H., S.-M. Hsia, and T.-M. Shieh. Lysyl oxidase and the tumor microenvironment. Int. J. Mol. Sci. 18(1):100, 2016.  https://doi.org/10.3390/ijms18010062.CrossRefGoogle Scholar
  152. 152.
    Wang, S., J. Sun, Y. Xiao, Y. Lu, D. D. Zhang, and P. K. Wong. Intercellular tension negatively regulates angiogenic sprouting of endothelial tip cells via Notch1-Dll4 signaling. Adv. Biosyst. 1:1600019, 2017.CrossRefGoogle Scholar
  153. 153.
    Webb, D. J., J. T. Parsons, and A. F. Horwitz. Adhesion assembly, disassembly and turnover in migrating cells—over and over and over again. Nat. Cell Biol. 4:E97–100, 2002.CrossRefGoogle Scholar
  154. 154.
    Wheelock, M. J., Y. Shintani, M. Maeda, Y. Fukumoto, and K. R. Johnson. Cadherin switching. J. Cell Sci. 121:727–735, 2008.CrossRefGoogle Scholar
  155. 155.
    Winer, J. P., S. Oake, and P. A. Janmey. Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS ONE 4:e6382, 2009.CrossRefGoogle Scholar
  156. 156.
    Wolf, K., et al. Compensation mechanism in tumor cell migration: mesenchymal–amoeboid transition after blocking of pericellular proteolysis. J. Cell Biol. 160:267–277, 2003.CrossRefGoogle Scholar
  157. 157.
    Wozniak, M. A., R. Desai, P. A. Solski, C. J. Der, and P. J. Keely. ROCK-generated contractility regulates breast epithelial cell differentiation in response to the physical properties of a three-dimensional collagen matrix. J. Cell Biol. 163:583–595, 2003.CrossRefGoogle Scholar
  158. 158.
    Wyckoff, J. B., S. E. Pinner, S. Gschmeissner, J. S. Condeelis, and E. Sahai. ROCK- and myosin-dependent matrix deformation enables protease-independent tumor-cell invasion in vivo. Curr. Biol. 16:1515–1523, 2006.CrossRefGoogle Scholar
  159. 159.
    Xu, X., Y. Wang, Z. Chen, M. D. Sternlicht, M. Hidalgo, and B. Steffensen. Matrix metalloproteinase-2 contributes to cancer cell migration on collagen. Cancer Res. 65:130–136, 2005.Google Scholar
  160. 160.
    Xu, W. W., et al. Cancer cell-secreted IGF2 instigates fibroblasts and bone marrow-derived vascular progenitor cells to promote cancer progression. Nat. Commun. 8:14399, 2017.CrossRefGoogle Scholar
  161. 161.
    Yeh, Y.-C., J.-Y. Ling, W.-C. Chen, H.-H. Lin, and M.-J. Tang. Mechanotransduction of matrix stiffness in regulation of focal adhesion size and number: reciprocal regulation of caveolin-1 and β1 integrin. Sci. Rep. 7:15008, 2017.CrossRefGoogle Scholar
  162. 162.
    Zaidel-Bar, R., M. Cohen, L. Addadi, and B. Geiger. Hierarchical assembly of cell–matrix adhesion complexes. Biochem. Soc. Trans. 32:416–420, 2004.CrossRefGoogle Scholar
  163. 163.
    Zamir, E., et al. Dynamics and segregation of cell–matrix adhesions in cultured fibroblasts. Nat. Cell Biol. 2:191–196, 2000.CrossRefGoogle Scholar
  164. 164.
    Zegers, M. M., and P. Friedl. Rho GTPases in collective cell migration. Small GTPases 5:e983869, 2014.CrossRefGoogle Scholar
  165. 165.
    Zhang, W., W. T. Couldwell, M. F. Simard, H. Song, J. H.-C. Lin, and M. Nedergaard. Direct gap junction communication between malignant glioma cells and astrocytes. Cancer Res. 59:1994–2003, 1999.Google Scholar
  166. 166.
    Zhou, G., et al. The role of desmosomes in carcinogenesis. Onco Targets Ther. 10:4059–4063, 2017.CrossRefGoogle Scholar
  167. 167.
    Zhu, X., et al. Galectin-1 knockdown in carcinoma-associated fibroblasts inhibits migration and invasion of human MDA-MB-231 breast cancer cells by modulating MMP-9 expression. Acta Biochim. Biophys. Sin. 48:462–467, 2016.CrossRefGoogle Scholar

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© Biomedical Engineering Society 2018

Authors and Affiliations

  1. 1.Department of Biomedical EngineeringVanderbilt UniversityNashvilleUSA

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