Tissue cells feel and respond to the stiffness of their substrate

Science

Volumn 310, Issue 5751, 2005, Pages 1139-1143

  Discher, Dennis E ^a   Janmey, Paul ^a   Wang, Yu Li ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOTECHNOLOGY; GELS; MOLECULAR DYNAMICS; SKIN; STIFFNESS; STIFFNESS MATRIX; TISSUE;

MOLECULAR PATHWAYS; PHENOTYPES; TISSUE CELLS; TRANSCELLULAR STRUCTURE;

CELLS;

ACTIN; ADENOSINE TRIPHOSPHATE; MYOSIN; NERVE CELL ADHESION MOLECULE; RAC1 PROTEIN; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

CYTOLOGY;

ACTIN FILAMENT; CELL ADHESION; CELL DIFFERENTIATION; CELL REGENERATION; CELL TYPE; CROSS LINKING; CYTOSKELETON; ENZYME SUBSTRATE; FIBROBLAST; MUSCLE CELL; NERVE CELL; PHYSICAL PARAMETERS; PRIORITY JOURNAL; REVIEW; RIGIDITY; SCANNING ELECTRON MICROSCOPY; SIGNAL TRANSDUCTION; TISSUE CULTURE;

BIOMECHANICS; CELL ADHESION; CELL COMMUNICATION; CELL PHYSIOLOGY; CYTOSKELETON; ELASTICITY; HUMANS; MUSCLE CONTRACTION; ORGANOGENESIS;

EID: 27944497333     PISSN: 00368075     EISSN: 10959203     Source Type: Journal    
DOI: 10.1126/science.1116995     Document Type: Review

References (92)

1. E. Ruoslahti, M. D. Pierschbacher, Science 238, 491 (1987).
2. H. L. Hadden, C. A. Henke, Am. J. Respir. Crit. Care Med. 162, 1553 (2000).
3. For example, classic palpation self-exam reveals that tumor stiffening can be quantitated by both MRI (4) and ultrasound elastography (5).
4. A. L. McKnight et al., AJR Am. J. Roentgenol. 178, 1411 (2002).
5. J. Bercoff et al., Ultrasound Med. Biol. 29, 1387 (2003).
6. D. R. Welch et al., Cancer Res. 60, 1552 (2000).
7. A. K. Harris, P. Wild, D. Stopak, Science 208, 177 (1980).
8. Since (7), methods for measuring traction force have become more quantitative by embedding beads in either films (9) or gels (10) or by using deformable patterns (11) or posts (12).
9. T. Oliver, M. Dembo, K. Jacobson, J. Cell Biol. 145, 589 (1999).
10. W. A. Marganski, M. Dembo, Y. Wang, Methods Enzymol. 361, 197 (2003).
11. N. Q. Balaban et al., Nat. Cell Biol. 3, 466 (2001).
12. J. L. Tan et al., Proc. Natl. Acad. Sci. U.S.A. 100, 1484 (2003).
13. F. J. Alenghat, D. E. Ingber, Sci. STKE 119, pe6 (2002).
14. (Fibroblasts and epithelial cells) R. J. Pelham, Y. Wang. Proc. Natl. Acad. Sci. U.S.A. 94, 13661 (1997) with Erratum 95, 12070a (1998).
15. (Endothelial cells) C. F. Deroanne, C. M. Lapiere, B. V. Nusgens., Cardiovasc. Res. 49, 647 (2001).
16. (Transformed cells) H. B. Wang, M. Dembo, Y. Wang., Am. J. Physiol. Cell Physiol. 279, C1345 (2000).
17. (Smooth muscle cells) A. Engler et al. Biophys. J. 86, 617 (2004).
18. R. E. Mahaffy, C. K. Shih, F. C. Macintosh, J. Kas, Phys. Rev. Lett. 85, 880 (2000).
19. 1/2 where the force f indents to a depth d. The shear modulus, G, of an isotropic, incompressible material is G ≈ E/3, reflecting the fact that shearing and tensile extension are related by a rotation of frame.
20. C. M. Lo, H. B. Wang, M. Dembo, Y. Wang, Biophys. J. 79, 144 (2000).
21. C. Storm, J. J. Pastore, F. C. Macintosh, T. C. Lubensky, P. A. Janmey, Nature 435, 191 (2005).
22. Y. C. Fung, A First Course in Continuum Mechanics: For Physical and Biological Engineers and Scientists (Prentice Hall, Englewood Cliffs, NJ, ed. 3, 1994).
23. M. M. Stevens, J. George, Science 310, 1135 (2005).
24. A. Gefen, S. S. Margulies, J. Biomech. 37, 1339 (2004).
25. S. Hu et al., Am. J. Physiol. Cell Physiol. 287, C1184 (2004).
26. G. Bao, S. Suresh, Nat. Mater. 2, 715 (2003).
27. F. Wottawah et al., Phys. Rev. Lett. 94, 098103 (2005).
28. (Skeletal Muscle Cells) A. J. Engler et al., J. Cell Biol. 166, 877 (2004).
29. Y. Yoshikawa, T. Yasuike, A. Yagi, T. Yamada, Biochem. Biophys. Res. Commun. 256, 13 (1999).
30. S. Diridollou et al., Skin Res. Technol. 6, 214 (2000).
31. W. M. Leader, D. Stopak, A. K. Harris, J. Cell Sci. 64, 1 (1983).
32. E. Cukierman, R. Pankov, D. R. Stevens, K. M. Yamada, Science 294, 1708 (2001).
33. M. Chrzanowska-Wodnicka, K. Burridge, J. Cell Biol. 133, 1403 (1996).
34. O. J. Pletjushkina et al., Cell Motil. Cytoskeleton 48, 235 (2001).
35. N. Wang et al., Proc. Natl. Acad. Sci. U.S.A. 98, 7765 (2001).
36. P. C. Bridgman, S. Dave, C. F. Asnes, A. N. Tullio, R. S. Adelstein, J. Neurosci. 21, 6159 (2001).
37. (Neurons) L. A. Flanagan, Y. E. Ju, B. Marg, M. Osterfield, P. A. Janmey, Neuroreport 13, 2411 (2002).
38. M. A. Griffin, S. Sen, H. L. Sweeney, D. E. Discher, J. Cell Sci. 117, 5855 (2004).
39. P. C. Georges, P. A. Janmey, in preparation.
40. T. Yeung et al., Cell Motil. Cytoskeleton 60, 24 (2005).
41. Y. Wang, in preparation.
42. P. C. Georges, P. A. Janmey, J. Appl. Physiol. 98, 1547 (2005).
43. G. P. Raeber, M. P. Lutolf, J. A. Hubbell. Biophys. J. 89, 1374 (2005).
44. A. Saez, A. Buguin, P. Silberzan, B. Ladoux, Biophys J., in press.
45. A. Engler, L. Richert, J. Wong, C. Picart, D. E. Discher, Surf. Sci. 570, 142 (2004).
46. Phagocytosis of rigid yeast particles by neutrophils involves a large contractile stress (∼1 kPa) and implicates myosin (47), consistent with stiffness sensitivity of phagocytosis by macrophages (48).
47. E. A. Evans, A. Leung, D. Zhelev, J. Cell Biol. 122, 1295 (1993).
48. (Macrophages) K. A. Beningo, Y. Wang, J. Cell Sci. 115, 849 (2002).
49. M. Jin, I. Andricioaei, T. A. Springer, Structure (Cambridge) 12, 2137 (2004).
50. A. F. Straight et al., Science 299, 1743 (2003).
51. B. Hinz, G. Celetta, J. J. Tomasek, G. Gabbiani, C. Chaponnier, Mol. Biol. Cell 12, 2730 (2001).
52. A. Katsumi et al., J. Cell Biol. 158, 153 (2002).
53. (Smooth muscle cells) S. R. Peyton, A. J. Putnam, J. Cell. Physiol, 204, 198 (2005).
54. N. Zaari, P. Rajagopalan, S. K. Kim, A. J. Engler, J. Y. Wong, Adv. Mater. 16, 2133 (2004).
55. S. L. Goodman, G. Risse, K. von der Mark, J. Cell Biol. 109, 799 (1989).
56. M. H. Zaman, R. D. Kamm, P. Matsudaira, D. A. Lauffenburger, Biophys. J. 89, 1389 (2005).
57. P. Y. Jay, P. A. Pham, S. A. Wong, E. L Elson, J. Cell Sci. 108, 387 (1995).
58. D. Riveline et al., J. Cell Biol. 153, 1175 (2001).
59. L. P. Cramer, T. J. Mitchison, J. Cell Biol. 131, 179 (1995).
60. A. Doyle, W. Marganski, J. Lee, J. Cell Sci. 117, 2203 (2004).
61. M. Tamada, M. P. Sheetz, Y. Sawada, Dev. Cell 7, 709 (2004).
62. I. Fillingham et al., Structure (Cambridge) 13, 65 (2005).
63. Recent unfolding of spectrin helical bundles at force levels that myosins can generate are described in (64).
64. R. Law et al., Biophys. J. 85, 3286 (2003).
65. Y. T. Shiu et al., Biophys. J. 86, 2558 (2004).
66. A. R. Asthagiri, C. A. Reinhart, A. F. Horwitz, D. A. Lauffenburger, J. Cell Sci. 113, 4499 (2000).
67. T. Wakatsuki, R. B. Wysolmerski, E. L. Elson, J. Cell Sci. 116, 1617 (2003).
68. A. Nicolas, B. Geiger, S. A. Safran, Proc. Natl. Acad. Sci. U.S.A. 101, 12520 (2004).
69. I. B. Bischofs, U. S. Schwarz, Proc. Natl. Acad. Sci. U.S.A. 100, 9274 (2003).
70. M. S. Steinberg, Science 137, 762 (1962).
71. J. P. Trinkaus, J. P. Lentz, Dev. Biol. 89, 115 (1964).
72. K. Jakab, A. Neagu, V. Mironov, R. R. Markwald, G. Forgacs, Proc. Natl. Acad. Sci. U.S.A. 101, 2864 (2004).
73. R. A. Foty, M. S. Steinberg, Dev. Biol. 278, 255 (2005).
74. S. E. Zalik, E. Lewandowski, Z. Kam, B. Geiger, Biochem. Cell Biol. 77, 527 (1999).
75. E. A. Evans, V. Heinrich, F. Ludwig, W. Rawicz, Biophys, J. 85, 2342 (2003).
76. N. K. Noren, W. T. Arthur, K. Burridge, J Biol. Chem. 278, 13615 (2003).
77. W. T. Arthur, N. K. Noren, K. Burridge, Biol. Res. 35. 239 (2002).
78. In vitro studies of cadherin-coated surfaces show no cytoskeleton assembly and no response to contractile inhibitors (79).
79. H. Delanoe-Ayari, R. Al Kurdi, M. Vallade, D. Gulino-Debrac, D. Riveline, Proc. Natl. Acad. Sci. U.S.A. 101. 2229 (2004).
80. A. K. Harris, J. Theor. Biol. 61, 267 (1976).
81. A. Engler, S. Sen, H. L. Sweeney, D. E. Discher, in preparation.
82. R. G. Wells, J. Clin. Gastroenterol. 39, S158 (2005).
83. M. A. Griffin et al., J. Cell Sci. 118, 1405 (2005).
84. E. J. Semler, P. A. Lancin, A. Dasgupta, P. V. Moghe, Biotechnol. Bioeng. 89, 296 (2005).
85. H. J. Kong et al., Nat. Mater. 4, 460 (2005).
86. K. A. Beningo, M. Dembo, Y. Wang, Proc. Natl. Acad. Sci. U.S.A. 101, 18024 (2004).
87. G. Baneyx, L. Baugh, V. Vogel, Proc. Natl. Acad. Sci. U.S.A. 99, 5139 (2002).
88. A. L. Sieminski, R. P. Hebbel, K. J. Gooch, Exp. Cell Res. 297, 574 (2004).
89. Y. Shikinami, M. Okuno, Biomaterials 24, 3161 (2003).
90. P. F. Gratzer, J. P. Santerre, J. M. Lee, Biomaterials. 25, 2081 (2004).
91. K. Rottner, A. Hall, J. V. Small, Curr. Biol. 9, 640 (1999).
92. Support was provided by NIH, NSF-PECASE (D.E.D.), and Penn's NSF-MRSEC.