Mechanisms of mechanical signaling in development and disease

Journal of Cell Science

Volumn 124, Issue 1, 2011, Pages 9-18

  Janmey, Paul A ^a   Miller, R Tyler ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cell mechanics; Matrix stiffness; Mechanosensing

Indexed keywords

CARDIOVASCULAR DISEASE; CELL COMMUNICATION AND CELL CONTACT; CELL CONTACT; CELL FUNCTION; CELL MOTILITY; CELL PROLIFERATION; CELL STRUCTURE; CELL SURVIVAL; DISEASE COURSE; EXTRACELLULAR MATRIX; GLOMERULOPATHY; HUMAN; LIVER DISEASE; MOLECULAR MECHANICS; NEOPLASM; NONHUMAN; NOTE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ANIMALS; BIOMECHANICS; DISEASE PROGRESSION; HUMANS; MECHANOTRANSDUCTION, CELLULAR;

ANIMALIA;

EID: 78651063200     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.071001     Document Type: Note

References (76)

1. Assoian, R. K. and Klein, E. A. (2008). Growth control by intracellular tension and extracellular stiffness. Trends Cell. Biol. 18, 347-352.
2. Baker, E. L., Bonnecaze, R. T. and Zaman, M. H. (2009). Extracellular matrix stiffness and architecture govern intracellular rheology in cancer. Biophys. J. 97, 1013-1021.
3. Beningo, K. A. and Wang, Y. L. (2007). Double-hydrogel substrate as a model system for three-dimensional cell culture. Methods Mol. Biol. 370, 203-212.
4. Beningo, K. A., Dembo, M. and Wang, Y. L. (2004). Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors. Proc. Natl. Acad. Sci. USA 101, 18024-18029.
5. Brown, A. E. and Discher, D. E. (2009). Conformational changes and signaling in cell and matrix physics. Curr. Biol. 19, R781-R789.
6. Buxboim, A., Ivanovska, I. L. and Discher, D. E. (2010). Matrix elasticity, cytoskeletal forces and physics of the nucleus: how deeply do cells 'feel' outside and in? J. Cell Sci. 123, 297-308.
7. Byfield, F. J., Reen, R. K., Shentu, T. P., Levitan, I. and Gooch, K. J. (2009a). Endothelial actin and cell stiffness is modulated by substrate stiffness in 2D and 3D. J. Biomech. 42, 1114-1119.
8. Byfield, F. J., Wen, Q., Levental, I., Nordstrom, K., Arratia, P. E., Miller, R. T. and Janmey, P. A. (2009b). Absence of filamin A prevents cells from responding to stiffness gradients on gels coated with collagen but not fibronectin. Biophys. J. 96, 5095-5102.
9. Cecelja, M. and Chowienczyk, P. (2009). Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: a systematic review. Hypertension 54, 1328-1336.
10. Chan, C. E. and Odde, D. J. (2008). Traction dynamics of filopodia on compliant substrates. Science 322, 1687-1691.
11. Chaturvedi, R. R., Herron, T., Simmons, R., Shore, D., Kumar, P., Sethia, B., Chua, F., Vassiliadis, E. and Kentish, J. C. (2010). Passive stiffness of myocardium from congenital heart disease and implications for diastole. Circulation 121, 979-988.
12. Chen, C. S. (2008). Mechanotransduction-a field pulling together? J. Cell Sci. 121, 3285-3292.
13. Choquet, D., Felsenfeld, D. P. and Sheetz, M. P. (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48.
14. del Rio, A., Perez-Jimenez, R., Liu, R., Roca-Cusachs, P., Fernandez, J. M. and Sheetz, M. P. (2009). Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641.
15. DeLoach, S. S. and Townsend, R. R. (2008). Vascular stiffness: its measurement and significance for epidemiologic and outcome studies. Clin. J. Am. Soc. Nephrol. 3, 184-192.
16. Didonna, B. and Lubensky, T. (2005). Nonaffinity and nonlinearity in random elastic networks. Phys. Rev. E 72, 066619.
17. Engler, A. J., Sweeney, H. L., Discher, D. E. and Schwarzbauer, J. E. (2007). Extracellular matrix elasticity directs stem cell differentiation. J. Musculoskelet. Neuronal Interact. 7, 335.
18. Engler, A. J., Carag-Krieger, C., Johnson, C. P., Raab, M., Tang, H. Y., Speicher, D. W., Sanger, J. W., Sanger, J. M. and Discher, D. E. (2008). Embryonic cardiomyocytes beat best on a matrix with heart-like elasticity: scar-like rigidity inhibits beating. J. Cell Sci. 121, 3794-3802.
19. Ezzell, R. M., Goldmann, W. H., Wang, N., Parashurama, N. and Ingber, D. E. (1997). Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231, 14-26.
20. Flanagan, L. A., Ju, Y. E., Marg, B., Osterfield, M. and Janmey, P. A. (2002). Neurite branching on deformable substrates. NeuroReport 13, 2411-2415.
21. Friedland, J. C., Lee, M. H. and Boettiger, D. (2009). Mechanically activated integrin switch controls alpha5beta1 function. Science 323, 642-644.
22. Fu, J., Wang, Y.-K., Yang, M. T., Desai, R. A., Yu, X., Liu, Z. and Chen, C. S. (2010). Mechanical regulation of cell function with geometrically modulated elastomeric substrates. Nat. Methods 7, 733-736.
23. Gehler, S., Baldassarre, M., Lad, Y., Leight, J. L., Wozniak, M. A., Riching, K. M., Eliceiri, K. W., Weaver, V. M., Calderwood, D. A. and Keely, P. J. (2009). Filamin A-beta1 integrin complex tunes epithelial cell response to matrix tension. Mol. Biol. Cell 20, 3224-3238.
24. Georges, P. C., Miller, W. J., Meaney, D. F., Sawyer, E. S. and Janmey, P. A. (2006). Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys. J. 90, 3012-3018.
25. Georges, P. C., Hui, J. J., Gombos, Z., McCormick, M. E., Wang, A. Y., Uemura, M., Mick, R., Janmey, P. A., Furth, E. E. and Wells, R. G. (2007). Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 293, G1147-G1154.
26. Ghibaudo, M., Saez, A., Trichet, L., Xayaphoummine, A., Browaeys, J., Silberzan, P., Buguin, A. and Ladoux, B. (2008). Traction forces and rigidity sensing regulate cell functions. Soft Matter 4, 1836-1843.
27. Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P. and Blau, H. M. (2010). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081.
28. Glogauer, M., Arora, P., Yao, G., Sokholov, I., Ferrier, J. and McCulloch, C. A. (1997). Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J. Cell Sci. 110, 11-21.
29. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., McLean, M. A., Sligar, S. G., Chen, C. S., Ha, T. et al. (2010). Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266.
30. Harris, A. K., Wild, P. and Stopak, D. (1980). Silicone rubber substrata: a new wrinkle in the study of cell locomotion. Science 208, 177-179.
31. Heil, P. and Spatz, J. P. (2010). Lateral shear forces applied to cells with single elastic micropillars to influence focal adhesion dynamics. J. Phys. Condens. Matter 22, 194108.
32. Janmey, P. A. and Schliwa, M. (2008). Rheology. Curr. Biol. 18, R639-R641.
33. Ju, Y. E., Janmey, P. A., McCormick, M. E., Sawyer, E. S. and Flanagan, L. A. (2007). Enhanced neurite growth from mammalian neurons in three-dimensional salmon fibrin gels. Biomaterials 28, 2097-2108.
34. Kang, H., Wen, Q., Janmey, P. A., Tang, J. X., Conti, E. and MacKintosh, F. C. (2009). Nonlinear elasticity of stiff filament networks: strain stiffening, negative normal stress, and filament alignment in fibrin gels. J. Phys. Chem. B 113, 3799-3805.
35. Kasza, K. E., Nakamura, F., Hu, S., Kollmannsberger, P., Bonakdar, N., Fabry, B., Stossel, T. P., Wang, N. and Weitz, D. A. (2009). Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys. J. 96, 4326-4335.
36. Katzberg, A. A. (1951). Distance as a factor in the development of attraction fields between growing tissues in culture. Science 114, 431-432.
37. Keese, C. R. and Giaever, I. (1991). Substrate mechanics and cell spreading. Exp. Cell Res. 195, 528-532.
38. Klein, E. A., Yin, L. Q., Kothapalli, D., Castagnino, P., Byfield, F. J., Xu, T. N., Levental, I., Hawthorne, E., Janmey, P. A. and Assoian, R. K. (2009). Cell-cycle control by physiological matrix elasticity and in vivo tissue stiffening. Curr. Biol. 19, 1511-1518.
39. Koivusalo, M., Kapus, A. and Grinstein, S. (2009). Sensors, transducers, and effectors that regulate cell size and shape. J. Biol. Chem. 284, 6595-6599.
40. Kumar, S. and Weaver, V. M. (2009). Mechanics, malignancy, and metastasis: the force journey of a tumor cell. Cancer Metastasis Rev. 28, 113-127.
41. Lacolley, P., Challande, P., Osborne-Pellegrin, M. and Regnault, V. (2009). Genetics and pathophysiology of arterial stiffness. Cardiovasc. Res. 81, 637-648.
42. le Digabel, J., Ghibaudo, M., Trichet, L., Richert, A. and Ladoux, B. (2010). Microfabricated substrates as a tool to study cell mechanotransduction. Med. Biol. Eng. Comput. 48, 965-976.
43. Levental, I., Georges, P. C. and Janmey, P. A. (2007). Soft biological materials and their impact on cell function. Soft Matter 1, 299-306.
44. Levental, K. R., Yu, H., Kass, L., Lakins, J. N., Egeblad, M., Erler, J. T., Fong, S. F., Csiszar, K., Giaccia, A., Weninger, W. et al. (2009). Matrix crosslinking forces tumor progression by enhancing integrin signaling. Cell 139, 891-906.
45. Li, Z., Dranoff, J. A., Chan, E. P., Uemura, M., Sevigny, J. and Wells, R. G. (2007). Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture. Hepatology 46, 1246-1256.
46. Liu, J., Koenderink, G. H., Kasza, K. E., Mackintosh, F. C. and Weitz, D. A. (2007). Visualizing the strain field in semiflexible polymer networks: strain fluctuations and nonlinear rheology of F-actin gels. Phys. Rev. Lett. 98, 198304.
47. Lu, Y. B., Franze, K., Seifert, G., Steinhauser, C., Kirchhoff, F., Wolburg, H., Guck, J., Janmey, P., Wei, E. Q., Kas, J. et al. (2006). Viscoelastic properties of individual glial cells and neurons in the CNS. Proc. Natl. Acad. Sci. USA 103, 17759-17764.
48. Ma, Z. and Finkel, T. H. (2010). T cell receptor triggering by force. Trends Immunol. 31, 1-6.
49. Mammoto, T. and Ingber, D. E. (2010). Mechanical control of tissue and organ development. Development 137, 1407-1420.
50. Mitchell, G. F., Hwang, S. J., Vasan, R. S., Larson, M. G., Pencina, M. J., Hamburg, N. M., Vita, J. A., Levy, D. and Benjamin, E. J. (2010). Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation 121, 505-511.
51. Na, S., Collin, O., Chowdhury, F., Tay, B., Ouyang, M., Wang, Y. and Wang, N. (2008). Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl. Acad. Sci. USA 105, 6626-6631.
52. Nicolas, A., Besser, A. and Safran, S. A. (2008). Dynamics of cellular focal adhesions on deformable substrates: consequences for cell force microscopy. Biophys. J. 95, 527-539.
53. Nicolle, S., Lounis, M. and Willinger, R. (2004). Shear properties of brain tissue over a frequency range relevant for automotive impact situations: new experimental results. Stapp Car Crash J. 48, 239-258.
54. Onck, P. R., Koeman, T., van Dillen, T. and van der Giessen, E. (2005). Alternative explanation of stiffening in cross-linked semiflexible networks. Phys. Rev. Lett. 95, 178102.
55. Paszek, M. J., Zahir, N., Johnson, K. R., Lakins, J. N., Rozenberg, G. I., Gefen, A., Reinhart-King, C. A., Margulies, S. S., Dembo, M., Boettiger, D. et al. (2005). Tensional homeostasis and the malignant phenotype. Cancer Cell 8, 241-254.
56. Paszek, M. J., Boettiger, D., Weaver, V. M. and Hammer, D. A. (2009). Integrin clustering is driven by mechanical resistance from the glycocalyx and the substrate. PLoS Comput. Biol. 5, e1000604.
57. Pelham, R. J., Jr and Wang, Y. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94, 13661-13665.
58. Provenzano, P. P., Inman, D. R., Eliceiri, K. W. and Keely, P. J. (2009). Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK-ERK linkage. Oncogene 28, 4326-4343.
59. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. D. (2001). 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.
60. Sack, I., Beierbach, B., Hamhaber, U., Klatt, D. and Braun, J. (2008). Non-invasive measurement of brain viscoelasticity using magnetic resonance elastography. NMR Biomed. 21, 265-271.
61. Saez, A., Ghibaudo, M., Buguin, A., Silberzan, P. and Ladoux, B. (2007). Rigidity-driven growth and migration of epithelial cells on microstructured anisotropic substrates. Proc. Natl. Acad. Sci. USA 104, 8281-8286.
62. Schwarz, U. S. and Safran, S. A. (2002). Elastic interactions of cells. Phys. Rev. Lett. 88, 048102.
63. Tan, J. L., Tien, J., Pirone, D. M., Gray, D. S., Bhadriraju, K. and Chen, C. S. (2003). Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. USA 100, 1484-1489. (Pubitemid 36254472)
64. Tandon, R., Levental, I., Huang, C., Byfield, F. J., Ziembicki, J., Schelling, J. R., Bruggeman, L. A., Sedor, J. R., Janmey, P. A. and Miller, R. T. (2006). HIV infection changes glomerular podocyte cytoskeletal composition and results in distinct cellular mechanical properties. Am. J. Physiol. Renal. Physiol. 292, F701-F710.
65. Tenney, R. M. and Discher, D. E. (2009). Stem cells, microenvironment mechanics, and growth factor activation. Curr. Opin. Cell Biol. 21, 630-635.
66. Vogel, V. and Sheetz, M. P. (2009). Cell fate regulation by coupling mechanical cycles to biochemical signaling pathways. Curr. Opin Cell Biol. 21, 38-46.
67. Wang, N., Butler, J. P. and Ingber, D. E. (1993). Mechanotransduction across the cell surface and through the cytoskeleton. Science 260, 1124-1127.
68. Wang, N., Tytell, J. D. and Ingber, D. E. (2009). Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat. Rev. Mol. Cell Biol. 10, 75-82.
69. Weiss, P. and Garber, B. (1952). Shape and movement of mesenchyme cells as functions of the physical structure of the medium: contributions to a quantitative morphology. Proc. Natl. Acad. Sci. USA 38, 264-280.
70. Weiss, P. and Katzberg, A. A. (1952). "Attraction fields" between growing tissue cultures. Science 115, 293-296.
71. Wells, R. G. (2008). The role of matrix stiffness in regulating cell behavior. Hepatology 47, 1394-1400.
72. Winer, J. P., Janmey, P. A., McCormick, M. E. and Funaki, M. (2009a). Bone marrow-derived human mesenchymal stem cells become quiescent on soft substrates but remain responsive to chemical or mechanical stimuli. Tissue Eng. Part A 15, 147-154.
73. Winer, J. P., Oake, S. and Janmey, P. A. (2009b). Non-linear elasticity of extracellular matrices enables contractile cells to communicate local position and orientation. PLoS ONE 4, e6382.
74. Wyss, H. M., Henderson, J. M., Byfield, F. J., Bruggeman, L. A., Ding, Y., Huang, C., Suh, J.-H., Franke, T., Mele, E., Pollak, M. R. et al. (2011). Biophysical properties of normal and diseased renal glomeruli. Am. J. Physiol. (Cell), in press.
75. Yeung, T., Georges, P. C., Flanagan, L. A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V. and Janmey, P. A. (2005). Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton 60, 24-34.
76. Zemel, A., Rehfeldt, F., Brown, A. E., Discher, D. E. and Safran, S. A. (2010). Optimal matrix rigidity for stress fiber polarization in stem cells. Nat. Phys. 6, 468-473.