Cellular response to substrate rigidity is governed by either stress or strain

Biophysical Journal

Volumn 104, Issue 1, 2013, Pages 19-29

  Yip, Ai Kia ^a   Iwasaki, Katsuhiko ^b   Ursekar, Chaitanya ^c   MacHiyama, Hiroaki ^c   Saxena, Mayur ^c   Chen, Huiling ^d   Harada, Ichiro ^b,e   Chiam, Keng Hwee ^c,d   Sawada, Yasuhiro ^a,c,e  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d INSTITUTE OF HIGH PERFORMANCE COMPUTING   (Singapore)

^e Laboratory for Mechanical Medicine   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

AMINOCAPROIC ACID; AZIDE; COLLAGEN; SUCCINIMIDE DERIVATIVE; SULFOSUCCINIMIDYL 6 ((4 AZIDO 2 NITROPHENYL)AMINO)HEXANOATE; SULFOSUCCINIMIDYL 6-((4-AZIDO-2-NITROPHENYL)AMINO)HEXANOATE;

ANIMAL; ANIMAL EMBRYO; ARTICLE; CELL STRAIN 3T3; CYTOLOGY; DRUG EFFECT; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESION; GEL; MECHANICAL STRESS; METABOLISM; MOUSE; YOUNG MODULUS;

6-AMINOCAPROIC ACID; ANIMALS; AZIDES; COLLAGEN; ELASTIC MODULUS; EMBRYO, MAMMALIAN; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; FOCAL ADHESIONS; GELS; MICE; NIH 3T3 CELLS; STRESS, MECHANICAL; SUCCINIMIDES;

EID: 84872170264     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.11.3805     Document Type: Article

References (53)

1. D.E. Discher, P. Janmey, and Y.-L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143 (Pubitemid 41681732)
2. R.J. Pelham Jr., and Y.-L. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. USA 94 1997 13661 13665 (Pubitemid 28009639)
3. C.M. Lo, and H.B. Wang Y.L. Wang Cell movement is guided by the rigidity of the substrate Biophys. J. 79 2000 144 152
4. H. Delanoë-Ayari, and S. Iwaya J.P. Rieu Changes in the magnitude and distribution of forces at different Dictyostelium developmental stages Cell Motil. Cytoskeleton 65 2008 314 331 (Pubitemid 351458145)
5. P.W. Oakes, and D.C. Patel J.X. Tang Neutrophil morphology and migration are affected by substrate elasticity Blood 114 2009 1387 1395
6. J. Stricker, and Y. Aratyn-Schaus M.L. Gardel Spatiotemporal constraints on the force-dependent growth of focal adhesions Biophys. J. 100 2011 2883 2893
7. M. Ghibaudo, and A. Saez B. Ladoux Traction forces and rigidity sensing regulate cell functions Soft Matter. 4 2008 1836 1843
8. L. Trichet, and J. Le Digabel B. Ladoux Evidence of a large-scale mechanosensing mechanism for cellular adaptation to substrate stiffness Proc. Natl. Acad. Sci. USA 109 2012 6933 6938
9. J.P. Califano, and C.A. Reinhart-King Substrate stiffness and cell area predict cellular traction stresses in single cells and cells in contact Cell Mol. Bioeng 3 2010 68 75
10. M. Prager-Khoutorsky, and A. Lichtenstein A.D. Bershadsky Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing Nat. Cell Biol. 13 2011 1457 1465
11. N.Q. Balaban, and U.S. Schwarz B. Geiger Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates Nat. Cell Biol. 3 2001 466 472 (Pubitemid 32422082)
12. S. Walcott, and S.X. Sun A mechanical model of actin stress fiber formation and substrate elasticity sensing in adherent cells Proc. Natl. Acad. Sci. USA 107 2010 7757 7762
13. A. Zemel, and F. Rehfeldt S.A. Safran Optimal matrix rigidity for stress fiber polarization in stem cells Nat. Phys. 6 2010 468 473
14. A. Nicolas, and S.A. Safran Limitation of cell adhesion by the elasticity of the extracellular matrix Biophys. J. 91 2006 61 73 (Pubitemid 44015308)
15. A. Nicolas, A. Besser, and S.A. Safran Dynamics of cellular focal adhesions on deformable substrates: consequences for cell force microscopy Biophys. J. 95 2008 527 539
16. T. Kobayashi, and M. Sokabe Sensing substrate rigidity by mechanosensitive ion channels with stress fibers and focal adhesions Curr. Opin. Cell Biol. 22 2010 669 676
17. R. De, A. Zemel, and S.A. Safran Do cells sense stress or strain? Measurement of cellular orientation can provide a clue Biophys. J. 94 2008 L29 L31
18. T.M. Freyman, and I.V. Yannas L.J. Gibson Fibroblast contractile force is independent of the stiffness which resists the contraction Exp. Cell Res. 272 2002 153 162 (Pubitemid 34920683)
19. A. Saez, and A. Buguin B. Ladoux Is the mechanical activity of epithelial cells controlled by deformations or forces? Biophys. J. 89 2005 L52 L54
20. M.H. Zaman, and R.D. Kamm D.A. Lauffenburger Computational model for cell migration in 3D matrices Biophys. J. 89 2005 1389 1397 (Pubitemid 41099020)
21. I.V. Dokukina, and M.E. Gracheva A model of fibroblast motility on substrates with different rigidities Biophys. J. 98 2010 2794 2803
22. A.J. Engler, and S. Sen D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689 (Pubitemid 44233625)
23. D.D. Pless, and Y.C. Lee R.L. Schnaar Specific cell adhesion to immobilized glycoproteins demonstrated using new reagents for protein and glycoprotein immobilization J. Biol. Chem. 258 1983 2340 2349 (Pubitemid 13118431)
24. C.E. Kandow, and P.C. Georges K.A. Beningo Polyacrylamide hydrogels for cell mechanics: steps toward optimization and alternative uses Methods Cell Biol. 83 2007 29 46
25. Landau, L. D., and E. M. Lifshitz. 1986. Theory of Elasticity, 3rd ed. J. B. Sykes and W. H. Reid, translators. Pergamon Press, Oxford, UK.
26. K. Araki, K. Kawauchi, and N. Tanaka IKK/NF-kB signaling pathway inhibits cell cycle progression via a novel Rb-independent suppression system for E2F transcription factors Oncogene 27 2008 5696 5705
27. B.-Z. Katz, and E. Zamir B. Geiger Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions Mol. Biol. Cell 11 2000 1047 1060 (Pubitemid 30159321)
28. K.A. Beningo, and K. Hamao H. Hosoya Traction forces of fibroblasts are regulated by the Rho-dependent kinase but not by the myosin light chain kinase Arch. Biochem. Biophys. 456 2006 224 231 (Pubitemid 44880290)
29. M. Dembo, and T. Oliver K. Jacobson Imaging the traction stresses exerted by locomoting cells with the elastic substratum method Biophys. J. 70 1996 2008 2022 (Pubitemid 26103973)
30. J.P. Butler, and I.M. Tolić-Nørrelykke J.J. Fredberg Traction fields, moments, and strain energy that cells exert on their surroundings Am. J. Physiol. Cell Physiol. 282 2002 C595 C605
31. S.A. Maskarinec, and C. Franck G. Ravichandran Quantifying cellular traction forces in three dimensions Proc. Natl. Acad. Sci. USA 106 2009 22108 22113
32. C. Franck, and S. Hong G. Ravichandran Three-dimensional full-field measurements of large deformations in soft materials using confocal microscopy and digital volume correlation Exp. Mech. 47 2007 427 438 (Pubitemid 46767428)
33. M. Dembo, and Y.-L. Wang Stresses at the cell-to-substrate interface during locomotion of fibroblasts Biophys. J. 76 1999 2307 2316 (Pubitemid 29266384)
34. R. Pankov, and E. Cukierman K.M. Yamada Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis J. Cell Biol. 148 2000 1075 1090
35. Z. Avnur, and B. Geiger The removal of extracellular fibronectin from areas of cell-substrate contact Cell 25 1981 121 132 (Pubitemid 11087440)
36. A.D. Rape, W.H. Guo, and Y.-L. Wang The regulation of traction force in relation to cell shape and focal adhesions Biomaterials 32 2011 2043 2051
37. Y. Sawada, and M.P. Sheetz Force transduction by Triton cytoskeletons J. Cell Biol. 156 2002 609 615 (Pubitemid 34839877)
38. A. Saez, and E. Anon B. Ladoux Traction forces exerted by epithelial cell sheets J. Phys. Condens. Matter 22 2010 194119
39. S.J. Han, and K.S. Bielawski N.J. Sniadecki Decoupling substrate stiffness, spread area, and micropost density: a close spatial relationship between traction forces and focal adhesions Biophys. J. 103 2012 640 648
40. T. Tzvetkova-Chevolleau, and A. Stéphanou P. Tracqui The motility of normal and cancer cells in response to the combined influence of the substrate rigidity and anisotropic microstructure Biomaterials 29 2008 1541 1551
41. M.T. Frey, and I.Y. Tsai Y.L. Wang Cellular responses to substrate topography: role of myosin II and focal adhesion kinase Biophys. J. 90 2006 3774 3782
42. J. Solon, and I. Levental P.A. Janmey Fibroblast adaptation and stiffness matching to soft elastic substrates Biophys. J. 93 2007 4453 4461 (Pubitemid 350294491)
43. P. Marcq, N. Yoshinaga, and J. Prost Rigidity sensing explained by active matter theory Biophys. J. 101 2011 L33 L35
44. D. Mitrossilis, and J. Fouchard A. Asnacios Single-cell response to stiffness exhibits muscle-like behavior Proc. Natl. Acad. Sci. USA 106 2009 18243 18248
45. W.H. Guo, and M.T. Frey Y.L. Wang Substrate rigidity regulates the formation and maintenance of tissues Biophys. J. 90 2006 2213 2220
46. K.A. Beningo, and M. Dembo Y.L. Wang Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts J. Cell Biol. 153 2001 881 888
47. M.L. Gardel, and B. Sabass C.M. Waterman Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed J. Cell Biol. 183 2008 999 1005
48. J.P. Califano, and C.A. Reinhart-King A balance of substrate mechanics and matrix chemistry regulates endothelial cell network assembly Cell. Mol. Bioeng. 1 2008 122 132
49. C.A. Reinhart-King, M. Dembo, and D.A. Hammer Endothelial cell traction force on RGD-derivatized polyacrylamide substrata Langmuir 19 2003 1573 1579
50. C.A. Reinhart-King, M. Dembo, and D.A. Hammer Cell-cell mechanical communication through compliant substrates Biophys. J. 95 2008 6044 6051
51. C.A. Reinhart-King, M. Dembo, and D.A. Hammer The dynamics and mechanics of endothelial cell spreading Biophys. J. 89 2005 676 689 (Pubitemid 41098318)
52. J.B. Leach, and X.Q. Brown J.Y. Wong Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity J. Neural Eng. 4 2007 26 34 (Pubitemid 46603794)
53. M.J. Paszek, and N. Zahir V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254 (Pubitemid 41317594)