Matrix Mechanics and Cell Contractility in Angiogenesis

Chapter
Part of the Studies in Mechanobiology, Tissue Engineering and Biomaterials book series (SMTEB, volume 12)

Abstract

Angiogenesis is a complex process that relies on the interplay of chemical and mechanical signaling events that ultimately result in the formation of new blood vessels. While much work has uncovered the chemical signaling events that mediate angiogenesis, the role of the mechanical environment is less understood. In this chapter, we will discuss how the mechanical microenvironment regulates angiogenesis by examining how matrix stiffness and cellular contractility mediate endothelial cell behaviors that are necessary for the progression of angiogenesis. Specifically, we will describe the roles of matrix stiffness and cell contractility as regulators of endothelial cell adhesion and shape, migration, growth, cell–cell interactions, and cell–matrix remodeling. Collectively, these findings implicate endogenous cellular forces and matrix stiffness as critical components of the angiogenic microenvironment, and suggest that both are important parameters for tissue engineering applications and a greater understanding of angiogenesis during disease progression.

Keywords

Matrix Stiffness Traction Force Actin Stress Fiber Cell Contractility Ligand Density 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Kalluri, R.: Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer 3(6), 422–433 (2003)CrossRefGoogle Scholar
  2. 2.
    Califano, J.P., Reinhart-King, C.A.: Exogenous and endogenous force regulation of endothelial cell behavior. J. Biomech. 43(1), 79–86 (2010)CrossRefGoogle Scholar
  3. 3.
    Davies, P.F.: Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat. Clin. Pract. Cardiovasc. Med. 6(1), 16–26 (2009)CrossRefGoogle Scholar
  4. 4.
    Davies, P.F.: Flow-mediated endothelial mechanotransduction. Physiol. Rev. 75(3), 519–560 (1995)Google Scholar
  5. 5.
    Kakisis, J.D., Liapis, C.D., Sumpio, B.E.: Effects of cyclic strain on vascular cells. Endothelium 11(1), 17–28 (2004)CrossRefGoogle Scholar
  6. 6.
    Cummins, P.M., von Offenberg Sweeney, N., Killeen, M.T., Birney, Y.A., Redmond, E.M., Cahill, P.A.: Cyclic strain-mediated matrix metalloproteinase regulation within the vascular endothelium: a force to be reckoned with. Am. J. Physiol. Heart Circulatory Physiol. 292(1), H28–H42 (2007)CrossRefGoogle Scholar
  7. 7.
    Vouyouka, A.G., Powell, R.J., Ricotta, J., Chen, H., Dudrick, D.J., Sawmiller, C.J., Dudrick, S.J., Sumpio, B.E.: Ambient pulsatile pressure modulates endothelial cell proliferation. J. Mol. Cell Cardiol. 30(3), 609–615 (1998)CrossRefGoogle Scholar
  8. 8.
    Rabodzey, A., Alcaide, P., Luscinskas, F.W., Ladoux, B.: Mechanical forces induced by the transendothelial migration of human neutrophils. Biophys. J. 95(3), 1428–1438 (2008)CrossRefGoogle Scholar
  9. 9.
    Sheriff, D.: Point: the muscle pump raises muscle blood flow during locomotion. J. Appl. Physiol. 99(1), 371–382; discussion 374–385 (2005)Google Scholar
  10. 10.
    Mahabeleshwar, G.H., Feng, W., Reddy, K., Plow, E.F., Byzova, T.V.: Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis. Circ. Res. 101(6), 570–580 (2007)CrossRefGoogle Scholar
  11. 11.
    Califano, J.P., Reinhart-King, C.A.: A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly. Cell. Mol. Bioeng. 1(2–3), 122–132 (2008)CrossRefGoogle Scholar
  12. 12.
    Reinhart-King, C.A., Dembo, M., Hammer, D.A.: The dynamics and mechanics of endothelial cell spreading. Biophys. J. 89(1), 676–689 (2005)CrossRefGoogle Scholar
  13. 13.
    Califano, J.P., Reinhart-King, C.A.: Substrate stiffness and cell area drive cellular traction stresses in single cells and cells in contact. Cell. Mol. Bioeng. 3(1), 68–75 (2010)CrossRefGoogle Scholar
  14. 14.
    Legate, K.R., Fassler, R.: Mechanisms that regulate adaptor binding to beta-integrin cytoplasmic tails. J. Cell Sci. 122(Pt 2), 187–198 (2009)CrossRefGoogle Scholar
  15. 15.
    Chen, C.S., Alonso, J.L., Ostuni, E., Whitesides, G.M., Ingber, D.E.: Cell shape provides global control of focal adhesion assembly. Biochem. Biophys. Res. Commun. 307(2), 355–361 (2003)CrossRefGoogle Scholar
  16. 16.
    Bhadriraju, K., Yang, M., Alom Ruiz, S., Pirone, D., Tan, J., Chen, C.S.: Activation of Rock by RhoA is regulated by cell adhesion, shape, and cytoskeletal tension. Exp. Cell. Res. 313(16), 3616–3623 (2007)Google Scholar
  17. 17.
    Nelson, C.M., Pirone, D.M., Tan, J.L., Chen, C.S.: Vascular endothelial-cadherin regulates cytoskeletal tension, cell spreading, and focal adhesions by stimulating RhoA. Mol. Biol. Cell 15(6), 2943–2953 (2004)CrossRefGoogle Scholar
  18. 18.
    Ko, K.S., Arora, P.D., McCulloch, C.A.: Cadherins mediate intercellular mechanical signaling in fibroblasts by activation of stretch-sensitive calcium-permeable channels. J. Biol. Chem. 276(38), 35967–35977 (2001)CrossRefGoogle Scholar
  19. 19.
    Ganz, A., Lambert, M., Saez, A., Silberzan, P., Buguin, A., Mege, R.M., Ladoux, B.: Traction forces exerted through N-cadherin contacts. Biol. Cell 98(12), 721–730 (2006)CrossRefGoogle Scholar
  20. 20.
    Ladoux, B., Anon, E., Lambert, M., Rabodzey, A., Hersen, P., Buguin, A., Silberzan, P., Mege, R.M.: Strength dependence of cadherin-mediated adhesions. Biophys. J. 98(4), 534–542 (2010)CrossRefGoogle Scholar
  21. 21.
    Liu, Z., Tan, J.L., Cohen, D.M., Yang, M.T., Sniadecki, N.J., Ruiz, S.A., Nelson, C.M., Chen, C.S.: Mechanical tugging force regulates the size of cell–cell junctions. Proc. Natl. Acad. Sci. U S A 107(22), 9944–9949 (2009)CrossRefGoogle Scholar
  22. 22.
    Huynh, J., Nishimura, N., Rana, K., Peloquin, J.M., Califano, J.P., Montague, C.R., King, M.R., Schaffer, C.B., Reinhart-King, C.A.: Age-Related Intimal Stiffening Enhances Endothelial Permeability and Leukocyte Transmigration. Sci. Transl. Med. 3(112), 112ra–122ra (2011)CrossRefGoogle Scholar
  23. 23.
    Ogita, H., Takai, Y.: Cross-talk among integrin, cadherin, and growth factor receptor: roles of nectin and nectin-like molecule. Int. Rev. Cytol. 265, 1–54 (2008)CrossRefGoogle Scholar
  24. 24.
    Beningo, K.A., Dembo, M., Kaverina, I., Small, J.V., Wang, Y.L.: Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153(4), 881–888 (2001)CrossRefGoogle Scholar
  25. 25.
    Mammoto, A., Huang, S., Ingber, D.E.: Filamin links cell shape and cytoskeletal structure to Rho regulation by controlling accumulation of p190RhoGAP in lipid rafts. J. Cell Sci. 120(Pt 3), 456–467 (2007)CrossRefGoogle Scholar
  26. 26.
    Mammoto, A., Connor, K.M., Mammoto, T., Yung, C.W., Huh, D., Aderman, C.M., Mostoslavsky, G., Smith, L.E., Ingber, D.E.: A mechanosensitive transcriptional mechanism that controls angiogenesis. Nature 457(7233), 1103–1108 (2009)CrossRefGoogle Scholar
  27. 27.
    Huot, J., Houle, F., Rousseau, S., Deschesnes, R.G., Shah, G.M., Landry, J.: SAPK2/p38-dependent F-actin reorganization regulates early membrane blebbing during stress-induced apoptosis. J. Cell Biol. 143(5), 1361–1373 (1998)CrossRefGoogle Scholar
  28. 28.
    van Nieuw Amerongen, G.P., Koolwijk, P., Versteilen, A., van Hinsbergh, V.W.: Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler Thromb. Vasc. Biol. 23(2), 211–217 (2003)CrossRefGoogle Scholar
  29. 29.
    Yang, M.T., Reich, D.H., Chen, C.S.: Measurement and analysis of traction force dynamics in response to vasoactive agonists. Integr. Biol. (Camb) 3(6), 663–674 (2011)CrossRefGoogle Scholar
  30. 30.
    Ezzell, R.M., Goldmann, W.H., Wang, N., Parashurama, N., Ingber, D.E.: Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231(1), 14–26 (1997)CrossRefGoogle Scholar
  31. 31.
    Ingber, D.E.: Fibronectin controls capillary endothelial cell growth by modulating cell shape. Proc. Natl. Acad. Sci. U S A. 87(9), 3579–3583 (1990)CrossRefGoogle Scholar
  32. 32.
    Ingber, D.E., Prusty, D., Sun, Z., Betensky, H., Wang, N.: Cell shape, cytoskeletal mechanics, and cell cycle control in angiogenesis. J. Biomech. 28(12), 1471–1484 (1995)CrossRefGoogle Scholar
  33. 33.
    Roca-Cusachs, P., Alcaraz, J., Sunyer, R., Samitier, J., Farre, R., Navajas, D.: Micropatterning of single endothelial cell shape reveals a tight coupling between nuclear volume in G1 and proliferation. Biophys. J. 94(12), 4984–4995 (2008)CrossRefGoogle Scholar
  34. 34.
    Chen, C.S., Mrksich, M., Huang, S., Whitesides, G.M., Ingber, D.E.: Geometric control of cell life and death. Science 276(5317), 1425–1428 (1997)CrossRefGoogle Scholar
  35. 35.
    Chen, C.S., Mrksich, M., Huang, S., Whitesides, G.M., Ingber, D.E.: Micropatterned surfaces for control of cell shape, position, and function. Biotechnol. Prog. 14(3), 356–363 (1998)CrossRefGoogle Scholar
  36. 36.
    Dike, L.E., Chen, C.S., Mrksich, M., Tien, J., Whitesides, G.M., Ingber, D.E.: Geometric control of switching between growth, apoptosis, and differentiation during angiogenesis using micropatterned substrates. In Vitro Cell. Dev. Biol. Anim. 35(8), 441–448 (1999)CrossRefGoogle Scholar
  37. 37.
    Huang, S., Chen, C.S., Ingber, D.E.: Control of cyclin D1, p27(Kip1), and cell cycle progression in human capillary endothelial cells by cell shape and cytoskeletal tension. Mol. Biol. Cell 9(11), 3179–3193 (1998)CrossRefGoogle Scholar
  38. 38.
    Flusberg, D.A., Numaguchi, Y., Ingber, D.E.: Cooperative control of Akt phosphorylation, bcl-2 expression, and apoptosis by cytoskeletal microfilaments and microtubules in capillary endothelial cells. Mol. Biol. Cell 12(10), 3087–3094 (2001)CrossRefGoogle Scholar
  39. 39.
    Huang, S., Ingber, D.E.: A discrete cell cycle checkpoint in late G(1) that is cytoskeleton-dependent and MAP kinase (Erk)-independent. Exp. Cell Res. 275(2), 255–264 (2002)CrossRefGoogle Scholar
  40. 40.
    Mammoto, A., Huang, S., Moore, K., Oh, P., Ingber, D.E.: Role of RhoA, mDia, and ROCK in cell shape-dependent control of the Skp2-p27kip1 pathway and the G1/S transition. J. Biol. Chem. 279(25), 26323–26330 (2004)CrossRefGoogle Scholar
  41. 41.
    Nelson, C.M., Chen, C.S.: VE-cadherin simultaneously stimulates and inhibits cell proliferation by altering cytoskeletal structure and tension. J. Cell Sci. 116(Pt 17), 3571–3581 (2003)CrossRefGoogle Scholar
  42. 42.
    Gray, D.S., Liu, W.F., Shen, C.J., Bhadriraju, K., Nelson, C.M., Chen, C.S.: Engineering amount of cell–cell contact demonstrates biphasic proliferative regulation through RhoA and the actin cytoskeleton. Exp. Cell Res. 314(15), 2846–2854 (2008)CrossRefGoogle Scholar
  43. 43.
    Nelson, C.M., Jean, R.P., Tan, J.L., Liu, W.F., Sniadecki, N.J., Spector, A.A., Chen, C.S.: Emergent patterns of growth controlled by multicellular form and mechanics. Proc. Natl. Acad. Sci. U S A. 102(33), 11594–11599 (2005)CrossRefGoogle Scholar
  44. 44.
    Byfield, F.J., Reen, R.K., Shentu, T.P., Levitan, I., Gooch, K.J.: Endothelial actin and cell stiffness is modulated by substrate stiffness in 2D and 3D. J. Biomech. 42(8), 1114–1119 (2009)CrossRefGoogle Scholar
  45. 45.
    Maniotis, A.J., Chen, C.S., Ingber, D.E.: Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. U S A. 94(3), 849–854 (1997)CrossRefGoogle Scholar
  46. 46.
    Dike, L.E., Ingber, D.E.: Integrin-dependent induction of early growth response genes in capillary endothelial cells. J. Cell Sci. 109(Pt 12), 2855–2863 (1996)Google Scholar
  47. 47.
    Chen, J., Fabry, B., Schiffrin, E.L., Wang, N.: Twisting integrin receptors increases endothelin-1 gene expression in endothelial cells. Am. J. Physiol. Cell Physiol. 280(6), C1475–C1484 (2001)Google Scholar
  48. 48.
    Pourati, J., Maniotis, A., Spiegel, D., Schaffer, J.L., Butler, J.P., Fredberg, J.J., Ingber, D.E., Stamenovic, D., Wang, N.: Is cytoskeletal tension a major determinant of cell deformability in adherent endothelial cells? Am. J. Physiol. 274(5 Pt 1), C1283–C1289 (1998)Google Scholar
  49. 49.
    Kumar, S., Maxwell, I.Z., Heisterkamp, A., Polte, T.R., Lele, T.P., Salanga, M., Mazur, E., Ingber, D.E.: Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics. Biophys. J. 90(10), 3762–3773 (2006)CrossRefGoogle Scholar
  50. 50.
    Lu, L., Oswald, S.J., Ngu, H., Yin, F.C.: Mechanical properties of actin stress fibers in living cells. Biophys. J. 95(12), 6060–6071 (2008)CrossRefGoogle Scholar
  51. 51.
    Wang, N., Ingber, D.E.: Control of cytoskeletal mechanics by extracellular matrix, cell shape, and mechanical tension. Biophys. J. 66(6), 2181–2189 (1994)CrossRefGoogle Scholar
  52. 52.
    Matthews, B.D., Overby, D.R., Mannix, R., Ingber, D.E.: Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell Sci. 119(Pt 3), 508–518 (2006)CrossRefGoogle Scholar
  53. 53.
    Panorchan, P., Lee, J.S., Kole, T.P., Tseng, Y., Wirtz, D.: Microrheology and ROCK signaling of human endothelial cells embedded in a 3D matrix. Biophys. J. 91(9), 3499–3507 (2006)CrossRefGoogle Scholar
  54. 54.
    Stroka, K.M., Aranda-Espinoza, H.: Effects of morphology vs. cell–cell interactions on endothelial cell stiffness. Cell. Mol. Bioeng. 4(1), 9–27 (2011)CrossRefGoogle Scholar
  55. 55.
    Ghosh, K., Thodeti, C.K., Dudley, A.C., Mammoto, A., Klagsbrun, M., Ingber, D.E.: Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. PNAS 105(32), 11305–11310 (2008)CrossRefGoogle Scholar
  56. 56.
    Folkman, J., Haudenschild, C.: Angiogenesis in vitro. Nature 288(5791), 551–556 (1980)CrossRefGoogle Scholar
  57. 57.
    Chicurel, M.E., Chen, C.S., Ingber, D.E.: Cellular control lies in the balance of forces. Curr. Opin. Cell Biol. 10(2), 232–239 (1998)CrossRefGoogle Scholar
  58. 58.
    Vernon, R.B., Lara, S.L., Drake, C.J., Iruela-Arispe, M.L., Angello, J.C., Little,C.D., Wight, T.N., Sage,E.H.: Organized type I collagen influences endothelial patterns during “spontaneous angiogenesis in vitro”: planar cultures as models of vascular development. In Vitro Cell. Dev. Biol. Anim. 31(2), 120–131 (1995)Google Scholar
  59. 59.
    Ingber, D.E., Folkman, J.: Mechanochemical switching between growth and differentiation during fibroblast growth factor-stimulated angiogenesis in vitro: role of extracellular matrix. J. Cell Biol. 109(1), 317–330 (1989)CrossRefGoogle Scholar
  60. 60.
    Vailhe, B., Ronot, X., Tracqui, P., Usson, Y., Tranqui, L. In: vitro angiogenesis is modulated by the mechanical properties of fibrin gels and is related to alpha(v)beta3 integrin localization. In: Vitro Cell. Dev Biol. Anim. 33(10), 763–773 (1997)Google Scholar
  61. 61.
    Deroanne, C.F., Lapiere, C.M., Nusgens, B.V.: In vitro tubulogenesis of endothelial cells by relaxation of the coupling extracellular matrix-cytoskeleton. Cardiovasc. Res. 49(3), 647–658 (2001)CrossRefGoogle Scholar
  62. 62.
    Kuzuya, M., Satake, S., Ai, S., Asai, T., Kanda, S., Ramos, M.A., Miura, H., Ueda, M., Iguchi, A.: Inhibition of angiogenesis on glycated collagen lattices. Diabetologia 41(5), 491–499 (1998)CrossRefGoogle Scholar
  63. 63.
    Nehls, V., Herrmann, R.: The configuration of fibrin clots determines capillary morphogenesis and endothelial cell migration. Microvasc. Res. 51(3), 347–364 (1996)CrossRefGoogle Scholar
  64. 64.
    Sieminski, A.L., Hebbel, R.P., Gooch, K.J.: The relative magnitudes of endothelial force generation and matrix stiffness modulate capillary morphogenesis in vitro. Exp. Cell Res. 297(2), 574–584 (2004)CrossRefGoogle Scholar
  65. 65.
    Guo, W.H., Frey, M.T., Burnham, N.A., Wang, Y.L.: Substrate rigidity regulates the formation and maintenance of tissues. Biophys. J. 90(6), 2213–2220 (2006)CrossRefGoogle Scholar
  66. 66.
    Ghajar, C.M., Blevins, K.S., Hughes, C.C., George, S.C., Putnam, A.J.: Mesenchymal stem cells enhance angiogenesis in mechanically viable prevascularized tissues via early matrix metalloproteinase upregulation. Tissue Eng. 12(10), 2875–2888 (2006)CrossRefGoogle Scholar
  67. 67.
    Shamloo, A., Heilshorn, S.C.: Matrix density mediates polarization and lumen formation of endothelial sprouts in VEGF gradients. Lab. Chip. 10(22), 3061–3068 (2010)CrossRefGoogle Scholar
  68. 68.
    Parker, K.K., Brock, A.L., Brangwynne, C., Mannix, R.J., Wang, N., Ostuni, E., Geisse, N.A., Adams, J.C., Whitesides, G.M., Ingber, D.E.: Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB J 16(10), 1195–1204 (2002)CrossRefGoogle Scholar
  69. 69.
    Fainaru, O., Almog, N., Yung, C.W., Nakai, K., Montoya-Zavala, M., Abdollahi, A., D’Amato, R., Ingber, D.E.: Tumor growth and angiogenesis are dependent on the presence of immature dendritic cells. FASEB J 24(5), 1411–1418 (2010)CrossRefGoogle Scholar
  70. 70.
    Ghajar, C.M., Kachgal, S., Kniazeva, E., Mori, H., Costes, S.V., George, S.C., Putnam, A.J.: Mesenchymal cells stimulate capillary morphogenesis via distinct proteolytic mechanisms. Exp. Cell Res. 316(5), 813–825 (2010)CrossRefGoogle Scholar
  71. 71.
    Kachgal, S., Putnam, A.J.: Mesenchymal stem cells from adipose and bone marrow promote angiogenesis via distinct cytokine and protease expression mechanisms. Angiogenesis 14(1), 47–59 (2011)CrossRefGoogle Scholar
  72. 72.
    Grainger, S.J., Putnam, A.J.: Assessing the permeability of engineered capillary networks in a 3D culture. PLoS ONE 6(7), e22086 (2011)CrossRefGoogle Scholar
  73. 73.
    Chen, X., Aledia, A.S., Ghajar, C.M., Griffith, C.K., Putnam, A.J., Hughes, C.C., George, S.C.: Prevascularization of a fibrin-based tissue construct accelerates the formation of functional anastomosis with host vasculature. Tissue Eng. Part A 15(6), 1363–1371 (2009)CrossRefGoogle Scholar
  74. 74.
    Kniazeva, E., Putnam, A.J.: Endothelial cell traction and ECM density influence both capillary morphogenesis and maintenance in 3-D. Am. J. Physiol. Cell Physiol. 297(1), C179–C187 (2009)CrossRefGoogle Scholar
  75. 75.
    Kniazeva, E., Kachgal, S., Putnam, A.J.: Effects of extracellular matrix density and mesenchymal stem cells on neovascularization in vivo. Tissue Eng. Part A 17(7–8), 905–914 (2011)CrossRefGoogle Scholar
  76. 76.
    Oliver, T., Dembo, M., Jacobson, K.: Separation of propulsive and adhesive traction stresses in locomoting keratocytes. J. Cell Biol. 145(3), 589–604 (1999)CrossRefGoogle Scholar
  77. 77.
    Palecek, S.P., Loftus, J.C., Ginsberg, M.H., Lauffenburger, D.A., Horwitz, A.F.: Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature 385(6616), 537–540 (1997)CrossRefGoogle Scholar
  78. 78.
    Peyton, S.R., Putnam, A.J.: Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion. J. Cell Physiol. 204(1), 198–209 (2005)CrossRefGoogle Scholar
  79. 79.
    Jannat, R.A., Dembo, M., Hammer, D.A.: Neutrophil adhesion and chemotaxis depend on substrate mechanics. J. Phys.: Condens. Matter 22(19), 194117 (2010)Google Scholar
  80. 80.
    Lo, C.M., Wang, H.B., Dembo, M., Wang, Y.L.: Cell movement is guided by the rigidity of the substrate. Biophys. J. 79(1), 144–152 (2000)CrossRefGoogle Scholar
  81. 81.
    Reinhart-King, C.A., Dembo, M., Hammer, D.A.: Cell–cell mechanical communication through compliant substrates. Biophys. J. 95(12), 6044–6051 (2008)CrossRefGoogle Scholar
  82. 82.
    Isenberg, B.C., Dimilla, P.A., Walker, M., Kim, S., Wong, J.Y.: Vascular smooth muscle cell durotaxis depends on substrate stiffness gradient strength. Biophys. J. 97(5), 1313–1322 (2009)CrossRefGoogle Scholar
  83. 83.
    Tse, J.R., Engler, A.J.: Stiffness gradients mimicking in vivo tissue variation regulate mesenchymal stem cell fate. PLoS ONE 6(1), e15978 (2011)CrossRefGoogle Scholar
  84. 84.
    Gray, D.S., Tien, J., Chen, C.S.: Repositioning of cells by mechanotaxis on surfaces with micropatterned Young’s modulus. J. Biomed. Mater. Res. A 66(3), 605–614 (2003)CrossRefGoogle Scholar
  85. 85.
    Davis, G.E., Senger, D.R.: Endothelial extracellular matrix: biosynthesis, remodeling, and functions during vascular morphogenesis and neovessel stabilization. Circ. Res. 97(11), 1093–1107 (2005)CrossRefGoogle Scholar
  86. 86.
    Saunders, R.L., Hammer, D.A.: Assembly of human umbilical vein endothelial cells on compliant hydrogels. Cell. Mol. Bioeng. 3(1), 60–67 (2010)CrossRefGoogle Scholar
  87. 87.
    de Rooij, J., Kerstens, A., Danuser, G., Schwartz, M.A., Waterman-Storer, C.M.: Integrin-dependent actomyosin contraction regulates epithelial cell scattering. J. Cell Biol. 171(1), 153–164 (2005)CrossRefGoogle Scholar
  88. 88.
    du Roure, O., Saez, A., Buguin, A., Austin, R.H., Chavrier, P., Silberzan, P., Ladoux, B.: Force mapping in epithelial cell migration. Proc. Natl. Acad. Sci. U S A 102(7), 2390–2395 (2005)CrossRefGoogle Scholar
  89. 89.
    Trepat, X., Wasserman, M.R., Angelini, T.E., Millet, E., Weitz, D.A., Butler, J.P., Fredberg, J.J.: Physical forces during collective cell migration. Nat. Phys. 5(6), 426–430 (2009)CrossRefGoogle Scholar
  90. 90.
    Saez, A., Ghibaudo, M., Buguin, A., Silberzan, P., Ladoux, B.: Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc. Natl. Acad. Sci. U S A 104(20), 8281–8286 (2007)CrossRefGoogle Scholar
  91. 91.
    Krishnan, L., Hoying, J.B., Nguyen, H., Song, H., Weiss, J.A.: Interaction of angiogenic microvessels with the extracellular matrix. Am. J. Physiol. Heart. Circ. Physiol. 293(6), H3650–H3658 (2007)CrossRefGoogle Scholar
  92. 92.
    Reinhart-King, C.A., Dembo, M., Hammer, D.A.: Endothelial cell traction forces on RGD-derivatized polyacrylamide substrata. Langmuir 19(5), 1573–1579 (2003)CrossRefGoogle Scholar
  93. 93.
    Vernon, R.B., Angello, J.C., Iruela-Arispe, M.L., Lane, T.F., Sage, E.H.: Reorganization of basement membrane matrices by cellular traction promotes the formation of cellular networks in vitro. Lab. Invest. 66(5), 536–547 (1992)Google Scholar
  94. 94.
    Zhou, X., Rowe, R.G., Hiraoka, N., George, J.P., Wirtz, D., Mosher, D.F., Virtanen, I., Chernousov, M.A., Weiss, S.J.: Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev. 22(9), 1231–1243 (2008)CrossRefGoogle Scholar
  95. 95.
    Magnusson, M.K., Mosher, D.F.: Fibronectin: structure, assembly, and cardiovascular implications. Arterioscler. Thromb. Vasc. Biol. 18(9), 1363–1370 (1998)CrossRefGoogle Scholar
  96. 96.
    Lemmon, C.A., Chen, C.S., Romer, L.H.: Cell traction forces direct fibronectin matrix assembly. Biophys. J. 96(2), 729–738 (2009)CrossRefGoogle Scholar
  97. 97.
    Dzamba, B.J., Jakab, K.R., Marsden, M., Schwartz, M.A., DeSimone, D.W.: Cadherin adhesion, tissue tension, and noncanonical wnt signaling regulate fibronectin matrix organization. Dev. Cell 16(3), 421–432 (2009)CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Joseph P. Califano
    • 1
  • Cynthia A. Reinhart-King
    • 1
  1. 1.Department of Biomedical EngineeringCornell University 302 Weill HallIthacaUSA

Personalised recommendations