About this Journal Submit a Manuscript Table of Contents
BioMed Research International
Volume 2013 (2013), Article ID 101979, 10 pages
http://dx.doi.org/10.1155/2013/101979
Review Article

Regulation of Tissue Fibrosis by the Biomechanical Environment

Department of Cell Biology and Anatomy, University of South Carolina, School of Medicine, Columbia, SC 29209, USA

Received 6 May 2013; Accepted 10 May 2013

Academic Editor: Mauro S. G. Pavao

Copyright © 2013 Wayne Carver and Edie C. Goldsmith. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. C. A. L. Bassett and I. Herrmann, “Influence of oxygen concentration and mechanical factors on differentiation of connective tissues in vitro,” Nature, vol. 190, no. 4774, pp. 460–461, 1961. View at Publisher · View at Google Scholar · View at Scopus
  2. C. K. Yeh and G. A. Rodan, “Tensile forces enhance prostaglandin E synthesis in osteoblastic cells grown on collagen ribbons,” Calcified Tissue International, vol. 36, supplement 1, pp. S67–S71, 1984. View at Scopus
  3. G. A. Rodan, T. Mensi, and A. Harvey, “A quantitative method for the application of compressive forces to bone in tissue culture,” Calcified Tissue International, vol. 18, no. 2, pp. 125–131, 1975. View at Scopus
  4. D. Y. M. Leung, S. Glagov, and M. B. Matthews, “Cyclic stretching stimulates synthesis of matrix components by arterial smooth muscle cells in vitro,” Science, vol. 191, no. 4226, pp. 475–477, 1976. View at Scopus
  5. D. Y. M. Leung, S. Glagov, and M. B. Mathews, “A new in vitro system for studying cell response to mechanical stimulation. Different effects of cyclic stretching and agitation on smooth muscle cell biosynthesis,” Experimental Cell Research, vol. 109, no. 2, pp. 285–298, 1977. View at Scopus
  6. H. H. Vandenburgh, “Motion into mass: how does tension stimulate muscle growth?” Medicine and Science in Sports and Exercise, vol. 19, no. 5, pp. S142–S149, 1987. View at Scopus
  7. J. L. Samuel, I. Dubus, F. Contard, K. Schwartz, and L. Rappaport, “Biological signals of cardiac hypertrophy,” European Heart Journal, vol. 11, pp. 1–7, 1990. View at Scopus
  8. V. J. Dzau, “Local contractile and growth modulators in the myocardium,” Clinical Cardiology, vol. 16, no. 5, pp. II5–II9, 1993. View at Scopus
  9. T. Yamazaki, I. Komuro, and Y. Yazaki, “Molecular aspects of mechanical stress-induced cardiac hypertrophy,” Molecular and Cellular Biochemistry, vol. 163-164, pp. 197–201, 1996. View at Scopus
  10. J. Löhler, R. Timpl, and R. Jaenisch, “Embryonic lethal mutation in mouse collagen I gene causes rupture of blood vessels and is associated with erythropoietic and mesenchymal cell death,” Cell, vol. 38, no. 2, pp. 597–607, 1984. View at Scopus
  11. T. Bowen, R. H. Jenkins, and D. J. Fraser, “MicroRNAs, transforming growth factor beta-1 and tissue fibrosis,” The Journal of Pathology, vol. 229, pp. 274–285, 2013.
  12. K. Lee and C. M. Nelson, “New insights into the regulation of epithelial-mesenchymal transition and tissue fibrosis,” International Review of Cell and Molecular Biology, vol. 294, pp. 171–221, 2012. View at Publisher · View at Google Scholar · View at Scopus
  13. H. Vandenburgh and S. Kaufman, “In vitro model for stretch-induced hypertrophy of skeletal muscle,” Science, vol. 203, no. 4377, pp. 265–268, 1979. View at Scopus
  14. S. F. Hopkins Jr., E. P. McCutcheon, and D. R. Wekstein, “Postnatal changes in rat ventricular function,” Circulation Research, vol. 32, no. 6, pp. 685–691, 1973. View at Scopus
  15. T. K. Borg and J. B. Caulfield, “Collagen in the heart,” Texas Reports on Biology and Medicine, vol. 39, pp. 321–333, 1979. View at Scopus
  16. T. K. Borg, “Development of the connective tissue network in the neonatal hamster heart,” American Journal of Anatomy, vol. 165, no. 4, pp. 435–443, 1982. View at Scopus
  17. W. Carver, L. Terracio, and T. K. Borg, “Expression and accumulation of interstitial collagen in the neonatal rat heart,” Anatomical Record, vol. 236, no. 3, pp. 511–520, 1993. View at Scopus
  18. G. L. Engelmann, “Coordinate gene expression during neonatal rat heart development. A possible role for the myocyte in extracellular matrix biogenesis and capillary angiogenesis,” Cardiovascular Research, vol. 27, no. 9, pp. 1598–1605, 1993. View at Scopus
  19. K. T. Weber, J. S. Janicki, S. G. Shroff, R. Pick, R. M. Chen, and R. I. Bashey, “Collagen remodeling of the pressure-overloaded, hypertrophied nonhuman primate myocardium,” Circulation Research, vol. 62, no. 4, pp. 757–765, 1988. View at Scopus
  20. J. E. Jalil, C. W. Doering, J. S. Janicki, R. Pick, S. G. Shroff, and K. T. Weber, “Fibrillar collagen and myocardial stiffness in the intact hypertrophied rat left ventricle,” Circulation Research, vol. 64, no. 6, pp. 1041–1050, 1989. View at Scopus
  21. P. R. Kollros, S. R. Bates, M. B. Mathews, A. L. Horwitz, and S. Glagov, “Cyclic AMP inhibits increased collagen production by cyclically stretched smooth muscle cells,” Laboratory Investigation, vol. 56, no. 4, pp. 410–417, 1987. View at Scopus
  22. W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circulation Research, vol. 69, no. 1, pp. 116–122, 1991. View at Scopus
  23. A. A. Lee, T. Delhaas, L. K. Waldman, D. A. Mackenna, F. J. Villarreal, and A. D. McCulloch, “An equibiaxial strain system for cultured cells,” American Journal of Physiology, vol. 271, no. 4, pp. C1400–C1408, 1996. View at Scopus
  24. R. P. Butt and J. E. Bishop, “Mechanical load enhances the stimulatory effect of serum growth factors on cardiac fibroblast procollagen synthesis,” Journal of Molecular and Cellular Cardiology, vol. 29, no. 4, pp. 1141–1151, 1997. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Auluck, V. Mudera, N. P. Hunt, and M. P. Lewis, “A three-dimensional in vitro model system to study the adaptation of craniofacial skeletal muscle following mechanostimulation,” European Journal of Oral Sciences, vol. 113, no. 3, pp. 218–224, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. R. K. Birla, Y. C. Huang, and R. G. Dennis, “Development of a novel bioreactor for the mechanical loading of tissue-engineered heart muscle,” Tissue Engineering, vol. 13, no. 9, pp. 2239–2248, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. T. Mammoto and D. E. Ingber, “Mechanical control of tissue and organ development,” Development, vol. 137, no. 9, pp. 1407–1420, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Yin, L. Lian, D. Piao, and J. Nan, “Tetrandrine stimulates the apoptosis of hepatic stellate cells and ameliorates development of fibrosis in a thioacetamide rat model,” World Journal of Gastroenterology, vol. 13, no. 8, pp. 1214–1220, 2007. View at Scopus
  29. W. Tomeno, M. Yoneda, K. Imajo et al., “Evaluation of the liver fibrosis index calculated by using real-time tissue elastography for the non-invasive assessment of liver fibrosis in chronic liver diseases,” Hepatology Research, 2012. View at Publisher · View at Google Scholar
  30. M. J. Paszek, N. Zahir, K. R. Johnson et al., “Tensional homeostasis and the malignant phenotype,” Cancer Cell, vol. 8, no. 3, pp. 241–254, 2005. View at Publisher · View at Google Scholar · View at Scopus
  31. T. A. Ulrich, 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 Research, vol. 69, no. 10, pp. 4167–4174, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. W. A. Lam, L. Cao, V. Umesh, A. J. Keung, S. Sen, and S. Kumar, “Extracellular matrix rigidity modulates neuroblastoma cell differentiation and N-myc expression,” Molecular Cancer, vol. 9, article 35, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Schedin and P. J. Keely, “Mammary gland ECM remodeling, stiffness, and mechanosignaling in normal development and tumor progression,” Cold Spring Harbor Perspectives in Biology, vol. 3, no. 1, p. a003228, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. A. Pathak and S. Kumar, “Independent regulation of tumor cell migration by matrix stiffness and confinement,” Proceedings of the National Academy of Sciences of USA, vol. 109, pp. 10334–10339, 2012.
  35. T. Y. Choi, N. Ahmadi, S. Sourayanezhad, I. Zeb, and M. J. Budoff, “Relation of vascular stiffness with epicardial and pericardial adipose tissues and coronary atherosclerosis,” Atherosclerosis, 2013. View at Publisher · View at Google Scholar
  36. R. A. F. Clark, G. S. Ashcroft, M. J. Spencer, H. Larjava, and M. W. J. Ferguson, “Re-epithelialization of normal human excisional wounds is associated with a switch from αvβ5 to αvβ6 integrins,” British Journal of Dermatology, vol. 135, no. 1, pp. 46–51, 1996. View at Scopus
  37. B. Hinz, “Tissue stiffness, latent TGF-β1 Activation, and mechanical signal transduction: implications for the pathogenesis and treatment of fibrosis,” Current Rheumatology Reports, vol. 11, no. 2, pp. 120–126, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. H. Wang, M. Dembo, and Y. Wang, “Substrate flexibility regulates growth and apoptosis of normal but not transformed cells,” American Journal of Physiology, vol. 279, no. 5, pp. C1345–C1350, 2000. View at Scopus
  39. T. Yeung, P. C. Georges, L. A. Flanagan et al., “Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion,” Cell Motility and the Cytoskeleton, vol. 60, no. 1, pp. 24–34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. M. P. Sheetz, D. P. Felsenfeld, and C. G. Galbraith, “Cell migration: regulation of force on extracellular-matrix-integrin complexes,” Trends in Cell Biology, vol. 8, no. 2, pp. 51–54, 1998. View at Scopus
  41. S. R. Peyton and A. J. Putnam, “Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion,” Journal of Cellular Physiology, vol. 204, no. 1, pp. 198–209, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. A. J. Engler, F. Rehfeldt, S. Sen, and D. E. Discher, “Microtissue elasticity: measurements by atomic force microscopy and its influence on cell differentiation,” Methods in Cell Biology, vol. 83, pp. 521–545, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. A. J. Engler, M. A. Griffin, S. Sen, C. G. Bönnemann, H. L. Sweeney, and D. E. Discher, “Myotubes differentiate optimally on substrates with tissue-like stiffness: pathological implications for soft or stiff microenvironments,” Journal of Cell Biology, vol. 166, no. 6, pp. 877–887, 2004. View at Publisher · View at Google Scholar · View at Scopus
  44. C. Mauch, A. Hatamochi, K. Scharffetter, and T. Krieg, “Regulation of collagen synthesis in fibroblasts within a three-dimensional collagen gel,” Experimental Cell Research, vol. 178, no. 2, pp. 493–503, 1988. View at Scopus
  45. C. Mauch, B. Adelmann-Grill, A. Hatamochi, and T. Krieg, “Collagenase gene expression in fibroblasts is regulated by a three-dimensional contact with collagen,” FEBS Letters, vol. 250, no. 2, pp. 301–305, 1989. View at Scopus
  46. L. A. Johnson, E. S. Rodansky, K. L. Sauder et al., “Matrix stiffness corresponding to strictured bowel induces a fibrogenic response in human colonic fibroblasts,” Inflammatory Bowel Diseases, vol. 19, pp. 891–903, 2013.
  47. D. Karamichos, N. Lakshman, and W. M. Petroll, “Regulation of corneal fibroblast morphology and collagen reorganization by extracellular matrix mechanical properties,” Investigative Ophthalmology and Visual Science, vol. 48, no. 11, pp. 5030–5037, 2007. View at Publisher · View at Google Scholar · View at Scopus
  48. F. Liu, J. D. Mih, B. S. Shea et al., “Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression,” Journal of Cell Biology, vol. 190, no. 4, pp. 693–706, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. N. L. Halliday and J. J. Tomasek, “Mechanical properties of the extracellular matrix influence fibronectin fibril assembly in vitro,” Experimental Cell Research, vol. 217, no. 1, pp. 109–117, 1995. View at Publisher · View at Google Scholar · View at Scopus
  50. C. L. Carraher and J. E. Schwarzbauer, “Regulation of matrix assembly through rigidity-dependent fibronectin conformational changes,” The Journal of Biological Chemistry, 2013. View at Publisher · View at Google Scholar
  51. E. Klotzsch, M. L. Smith, K. E. Kubow et al., “Fibronectin forms the most extensible biological fibers displaying switchable force-exposed cryptic binding sites,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 43, pp. 18267–18272, 2009. View at Publisher · View at Google Scholar · View at Scopus
  52. D. A. Brenner, T. Kisseleva, D. Scholten et al., “Origin of myofibroblasts in liver fibrosis,” Fibrogenesis & Tissue Repair, vol. 5, supplement 1, article S17, 2012. View at Publisher · View at Google Scholar
  53. B. Hinz, S. H. Phan, V. J. Thannickal et al., “Recent developments in myofibroblast biology: paradigms for connective tissue remodeling,” American Journal of Pathology, vol. 180, no. 4, pp. 1340–1355, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. B. Hinz, “Mechanical aspects of lung fibrosis: a spotlight on themyofibroblast,” Proceedings of the American Thoracic Society, vol. 9, pp. 137–147, 2012.
  55. P. D. Arora, N. Narani, and C. A. G. McCulloch, “The compliance of collagen gels regulates transforming growth factor-β induction of α-smooth muscle actin in fibroblasts,” American Journal of Pathology, vol. 154, no. 3, pp. 871–882, 1999. View at Scopus
  56. Y. Shi, Y. Dong, Y. Duan, X. Jiang, C. Chen, and L. Deng, “Substrate stiffness influences TGF-ß,1-induced differentiation of bronchial fibroblasts into myofibroblasts in airway remodeling,” Molecular Medicine Reports, vol. 7, pp. 419–424, 2013.
  57. P. A. Galie, M. V. Westfall, and J. P. Stegemann, “Reduced serum content and increased matrix stiffness promote the cardiac myofibroblast transition in 3D collagen matrices,” Cardiovascular Pathology, vol. 20, no. 6, pp. 325–333, 2011. View at Publisher · View at Google Scholar · View at Scopus
  58. S. L. Friedman, “Hepatic stellate cells: protean, multifunctional, and enigmatic cells of the liver,” Physiological Reviews, vol. 88, no. 1, pp. 125–172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. S. L. Friedman, F. J. Roll, J. Boules, D. M. Arenson, and D. M. Bissel, “Maintenance of differentiated phenotype of cultured rat hepatic lipocytes by basement membrane matrix,” Journal of Biological Chemistry, vol. 264, no. 18, pp. 10756–10762, 1989. View at Scopus
  60. M. D. A. Gaça, X. Zhou, R. Issa, K. Kiriella, J. P. Iredale, and R. C. Benyon, “Basement membrane-like matrix inhibits proliferation and collagen synthesis by activated rat hepatic stellate cells: evidence for matrix-dependent deactivation of stellate cells,” Matrix Biology, vol. 22, no. 3, pp. 229–239, 2003. View at Publisher · View at Google Scholar · View at Scopus
  61. A. L. Olsen, S. A. Bloomer, E. P. Chan et al., “Hepatic stellate cells require a stiff environment for myofibroblastic differentiation,” American Journal of Physiology, vol. 301, no. 1, pp. G110–G118, 2011. View at Publisher · View at Google Scholar · View at Scopus
  62. C. Jones and H. P. Ehrlich, “Fibroblast expression of β-smooth muscle actin, β2β1 integrin and βvβ3 integrin: influence of surface rigidity,” Experimental and Molecular Pathology, vol. 91, no. 1, pp. 394–399, 2011. View at Publisher · View at Google Scholar · View at Scopus
  63. M. L. Burgess, L. Terracio, T. Hirozane, and T. K. Borg, “Differential integrin expression by cardiac fibroblasts from hypertensive and exercise-trained rat hearts,” Cardiovascular Pathology, vol. 11, no. 2, pp. 78–87, 2002. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Marinkovic, F. Liu, and D. J. Tschumperlin, “Matrices of physiological stiffnesspotently inactivate idiopathic pulmonary fibrosis fibroblasts,” American Journal of Respiratory Cell and Molecular Biology, vol. 48, pp. 422–430, 2013.
  65. J. L. Balestrini, S. Chaudhry, V. Sarrazy, A. Koehler, and B. Hinz, “The mechanical memory of lung myofibroblasts,” Integrative Biology, vol. 4, no. 4, pp. 410–421, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. H. Wang, S. M. Haeger, A. M. Kloxin, L. A. Leinwand, and K. S. Anseth, “Redirecting valvular myofibroblasts into dormant fibroblasts through light-mediated reduction in substrate modulus,” PLoS One, vol. 7, article e39969, 2012.
  67. G. Garrison, S. K. Huang, K. Okunishi et al., “Reversal of myofibroblast differentiation by prostaglandin e2,” American Journal of Respiratory Cell and Molecular Biology, vol. 48, pp. 550–558, 2013.
  68. J. W. Stone, P. N. Sisco, E. C. Goldsmith, S. C. Baxter, and C. J. Murphy, “Using gold nanorods to probe cell-induced collagen deformation,” Nano Letters, vol. 7, no. 1, pp. 116–119, 2007. View at Publisher · View at Google Scholar · View at Scopus
  69. C. G. Wilson, J. W. Stone, V. Fowlkes et al., “Age-dependent expression of collagen receptors and deformation of type i collagen substrates by rat cardiac fibroblasts,” Microscopy and Microanalysis, vol. 17, no. 4, pp. 555–562, 2011. View at Publisher · View at Google Scholar · View at Scopus
  70. P. N. Sisco, C. G. Wilson, E. Mironova, S. C. Baxter, C. J. Murphy, and E. C. Goldsmith, “The effect of gold nanorods on cell-mediated collagen remodeling,” Nano Letters, vol. 8, no. 10, pp. 3409–3412, 2008. View at Publisher · View at Google Scholar · View at Scopus
  71. C. G. Wilson, P. N. Sisco, F. A. Gadala-Maria, C. J. Murphy, and E. C. Goldsmith, “Polyelectrolyte-coated gold nanorods and their interactions with type I collagen,” Biomaterials, vol. 30, no. 29, pp. 5639–5648, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. S. Wang, E. Cukierman, W. D. Swaim, K. M. Yamada, and B. J. Baum, “Extracellular matrix protein-induced changes in human salivary epithelial cell organization and proliferation on a model biological substratum,” Biomaterials, vol. 20, no. 11, pp. 1043–1049, 1999. View at Publisher · View at Google Scholar · View at Scopus
  73. Y. Zhang, C. Zhao, L. Jiang, and L. Dai, “Substrate stiffness regulates apoptosis and the mRNA expression of extracellular matrix regulatory genes in the rat annular cells,” Matrix Biology, vol. 30, no. 2, pp. 135–144, 2011. View at Publisher · View at Google Scholar · View at Scopus
  74. M. V. Turturro, S. Sokic, J. C. Larson, and G. Papavasiliou, “Effective tuning of ligand incorporation and mechanical properties in visible light photopolymerized poly(ethylene glycol) diacrylate hydrogels dictates cell adhesion and proliferation,” Biomedical Materials, vol. 8, no. 2, article 025001, 2013.
  75. P. F. Lee, Y. Bai, R. L. Smith, K. J. Bayless, and A. T. Yeh, “Angiogenic responses are enhanced in mechanically and microscopically characterized, microbial transglutaminase crosslinked collagen matrices with increased stiffness,” Acta Biomaterialia, 2013. View at Publisher · View at Google Scholar
  76. R. L. Saunders and D. A. Hammer, “Assembly of human umbilical vein endothelial cells on compliant hydrogels,” Cellular and Molecular Bioengineering, vol. 3, no. 1, pp. 60–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  77. C. C. Dufort, M. J. Paszek, and V. M. Weaver, “Balancing forces: architectural control of mechanotransduction,” Nature Reviews Molecular Cell Biology, vol. 12, no. 5, pp. 308–319, 2011. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Zhang and M. Labouesse, “Signaling through mechanical inputs: a coordinated process,” Journal of Cell Science, vol. 125, pp. 3039–3049, 2012.
  79. D. A. MacKenna, F. Dolfi, K. Vuori, and E. Ruoslahti, “Extracellular signal-regulated kinase and c-Jun NH2-terminal kinase activation by mechanical stretch is integrin-dependent and matrix-specific in rat cardiac fibroblasts,” Journal of Clinical Investigation, vol. 101, no. 2, pp. 301–310, 1998. View at Scopus
  80. C. A. Buck and A. F. Horwitz, “Cell surface receptors for extracellular matrix molecules,” Annual Review of Cell Biology, vol. 3, pp. 179–205, 1987. View at Scopus
  81. M. J. Humphries, Y. Yasuda, K. Olden, and K. M. Yamada, “The cell interaction sites of fibronectin in tumour metastasis,” Ciba Foundation symposium, vol. 141, pp. 75–93, 1988. View at Scopus
  82. E. Ruoslahti, “Fibronectin and its receptors,” Annual Review of Biochemistry, vol. 57, pp. 375–413, 1988. View at Scopus
  83. J. Atance, M. J. Yost, and W. Carver, “Influence of the extracellular matrix on the regulation of cardiac fibroblast behavior by mechanical stretch,” Journal of Cellular Physiology, vol. 200, no. 3, pp. 377–386, 2004. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Roca-Cusachs, T. Iskratsch, and M. P. Sheetz, “Finding the wekest link: exploring integrin-mediated mechanical molecular pathways,” Journal of Cell Science, vol. 125, pp. 3025–3038, 2012.
  85. R. Zaidel-Bar, S. Itzkovitz, A. Ma'ayan, R. Iyengar, and B. Geiger, “Functional atlas of the integrin adhesome,” Nature Cell Biology, vol. 9, no. 8, pp. 858–867, 2007. View at Publisher · View at Google Scholar · View at Scopus
  86. A. M. Pasapera, I. C. Schneider, E. Rericha, D. D. Schlaepfer, and C. M. Waterman, “Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation,” Journal of Cell Biology, vol. 188, no. 6, pp. 877–890, 2010. View at Publisher · View at Google Scholar · View at Scopus
  87. D. E. Ingber, “Control of capillary growth and differentiation by extracellular matrix: use of a tensegrity (tensional integrity) mechanism for signal processing,” Chest, vol. 99, no. 3, pp. 34S–40S, 1991. View at Scopus
  88. D. E. Ingber, “Integrins, tensegrity, and mechanotransduction,” Gravitational and Space Biology Bulletin, vol. 10, no. 2, pp. 49–55, 1997. View at Scopus
  89. K. Burridge and P. Mangeat, “An interaction between vinculin and talin,” Nature, vol. 308, no. 5961, pp. 744–746, 1984. View at Scopus
  90. D. R. Critchley, “Biochemical and structural properties of the integrin-associated cytoskeletal protein talin,” Annual Review of Biophysics, vol. 38, no. 1, pp. 235–254, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. M. D. Schaller, C. A. Borgman, B. S. Cobb, R. R. Vines, A. B. Reynolds, and J. T. Parsons, “pp125(FAK), a structurally distinctive protein-tyrosine kinase associated with focal adhesions,” Proceedings of the National Academy of Sciences of the United States of America, vol. 89, no. 11, pp. 5192–5196, 1992. View at Publisher · View at Google Scholar · View at Scopus
  92. T. M. Weiner, E. T. Liu, R. J. Craven, and W. G. Cance, “Expression of focal adhesion kinase gene and invasive cancer,” The Lancet, vol. 342, no. 8878, pp. 1024–1025, 1993. View at Publisher · View at Google Scholar · View at Scopus
  93. A. J. Pelletier, T. Kunicki, Z. M. Ruggeri, and V. Quaranta, “The activation state of the integrin α(IIb)β3 affects outside-in signals leading to cell spreading and focal adhesion kinase phosphorylation,” Journal of Biological Chemistry, vol. 270, no. 30, pp. 18133–18140, 1995. View at Publisher · View at Google Scholar · View at Scopus
  94. H. Chen, P. A. Appeddu, H. Isoda, and J. Guan, “Phosphorylation of tyrosine 397 in focal adhesion kinase is required for binding phosphatidylinositol 3-kinase,” Journal of Biological Chemistry, vol. 271, no. 42, pp. 26329–26334, 1996. View at Publisher · View at Google Scholar · View at Scopus
  95. K. E. Michael, D. W. Dumbauld, K. L. Burns, S. K. Hanks, and A. J. García, “Focal adhesion kinase modulates cell adhesion strengthening via integrin activation,” Molecular Biology of the Cell, vol. 20, no. 9, pp. 2508–2519, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Mammoto, T. Mammoto, and D. E. Ingber, “Mechanosensitive mechanisms in transcriptional regulation,” Journal of Cell Science, vol. 125, pp. 3061–3073, 2012.
  97. D. R. Carter, G. S. Beaupré, N. J. Giori, and J. A. Helms, “Mechanobiology of skeletal regeneration,” Clinical Orthopaedics and Related Research, no. 355, pp. S41–S55, 1998. View at Scopus
  98. W. Carver, M. L. Nagpal, M. Nachtigal, T. K. Borg, and L. Terracio, “Collagen expression in mechanically stimulated cardiac fibroblasts,” Circulation Research, vol. 69, no. 1, pp. 116–122, 1991. View at Scopus
  99. W. Zheng, L. P. Christensen, and R. J. Tomanek, “Differential effects of cyclic and static stretch on coronary microvascular endothelial cell receptors and vasculogenic/angiogenic responses,” American Journal of Physiology, vol. 295, no. 2, pp. H794–H800, 2008. View at Publisher · View at Google Scholar · View at Scopus
  100. S. Lehoux, B. Esposito, R. Merval, and A. Tedgui, “Differential regulation of vascular focal adhesion kinase by steady stretch and pulsatility,” Circulation, vol. 111, no. 5, pp. 643–649, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. S. Dupont, L. Morsut, M. Aragona et al., “Role of YAP/TAZ in mechanotransduction,” Nature, vol. 474, no. 7350, pp. 179–184, 2011. View at Publisher · View at Google Scholar · View at Scopus
  102. G. Halder, S. Dupont, and S. Piccolo, “Tranduction of mechanical and cytoskeletal cues by YAP and TAZ,” Nature Reviews Molecular Cell Biology, vol. 13, pp. 591–600, 2012.
  103. V. Raghunathan, C. T. McKee, W. Cheung et al., “Influence of extracellular matrix proteins and substratum topography on corneal epithelial alignment and migration,” Tissue Engineering A, 2013. View at Publisher · View at Google Scholar
  104. S. M. Thomasy, J. A. Wood, P. H. Kass, C. J. Murphy, and P. Russell, “Substratum stiffness and latrunculin B regulate matrix gene and protein expression in human trabecular meshwork cells,” Investigative Ophthalmology & Visual Science, vol. 53, no. 2, pp. 952–958, 2012. View at Scopus