Contractile equilibration of single cells to step changes in extracellular stiffness

Biophysical Journal

Volumn 102, Issue 3, 2012, Pages 443-451

  Crow, Ailey ^a,b   Webster, Kevin D ^a,b   Hohlfeld, Evan ^a   Ng, Win Pin ^a,b   Geissler, Phillip ^a,c   Fletcher, Daniel A ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b University of California at Berkeley   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN;

ANIMAL; ARTICLE; ATOMIC FORCE MICROSCOPY; BIOMECHANICS; CELL SHAPE; CELL STRAIN 3T3; CHEMISTRY; EXTRACELLULAR SPACE; FOCAL ADHESION; HYDROGEL; KINETICS; MECHANICS; METABOLISM; MOUSE; SIGNAL TRANSDUCTION;

ANIMALS; BIOMECHANICS; CELL SHAPE; EXTRACELLULAR SPACE; FOCAL ADHESIONS; HYDROGELS; KINETICS; MECHANICAL PROCESSES; MICE; MICROSCOPY, ATOMIC FORCE; MYOSINS; NIH 3T3 CELLS; SIGNAL TRANSDUCTION;

EID: 84856690892     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.11.4020     Document Type: Article

References (44)

1. S.R. Peyton, and A.J. Putnam Extracellular matrix rigidity governs smooth muscle cell motility in a biphasic fashion J. Cell. Physiol. 204 2005 198 209 (Pubitemid 40776823)
2. 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
3. A.J. Engler, and S. Sen D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689 (Pubitemid 44233625)
4. H.B. Wang, M. Dembo, and Y.L. Wang Substrate flexibility regulates growth and apoptosis of normal but not transformed cells Am. J. Physiol. Cell Physiol. 279 2000 C1345 C1350
5. S. Munevar, Y. Wang, and M. Dembo Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts Biophys. J. 80 2001 1744 1757 (Pubitemid 32280990)
6. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 10 2009 21 33
7. S.W. Moore, P. Roca-Cusachs, and M.P. Sheetz Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing Dev. Cell 19 2010 194 206
8. Y. Cai, and O. Rossier M.P. Sheetz Cytoskeletal coherence requires myosin-IIA contractility J. Cell Sci. 123 2010 413 423
9. A.M. Pasapera, and I.C. Schneider C.M. Waterman Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation J. Cell Biol. 188 2010 877 890
10. Y. Sawada, and M. Tamada M.P. Sheetz Force sensing by mechanical extension of the Src family kinase substrate p130Cas Cell 127 2006 1015 1026 (Pubitemid 44803062)
11. Y. Wang, and E.L. Botvinick S. Chien Visualizing the mechanical activation of Src Nature 434 2005 1040 1045 (Pubitemid 40586054)
12. U.S. Schwarz, T. Erdmann, and I.B. Bischofs Focal adhesions as mechanosensors: the two-spring model Biosystems 83 2006 225 232 (Pubitemid 43199823)
13. C.S. Chen Mechanotransduction-a field pulling together? J. Cell Sci. 121 2008 3285 3292
14. M.J. Paszek, and N. Zahir V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254 (Pubitemid 41317594)
15. A. del Rio, and R. Perez-Jimenez M.P. Sheetz Stretching single talin rod molecules activates vinculin binding Science 323 2009 638 641
16. S. Na, and O. Collin N. Wang Rapid signal transduction in living cells is a unique feature of mechanotransduction Proc. Natl. Acad. Sci. USA 105 2008 6626 6631 (Pubitemid 351754557)
17. K. Hayakawa, H. Tatsumi, and M. Sokabe Actin stress fibers transmit and focus force to activate mechanosensitive channels J. Cell Sci. 121 2008 496 503 (Pubitemid 351405058)
18. M. Shinohara, and K. Sabra M. Tanter Real-time visualization of muscle stiffness distribution with ultrasound shear wave imaging during muscle contraction Muscle Nerve 42 2010 438 441
19. M.T. Frey, and Y.-L. Wang A photo-modulatable material for probing cellular responses to substrate rigidity Soft Matter 5 2009 1918 1924
20. F.X. Jiang, and B. Yurke N.A. Langrana The relationship between fibroblast growth and the dynamic stiffnesses of a DNA crosslinked hydrogel Biomaterials 31 2010 1199 1212
21. J.L. Young, and A.J. Engler Hydrogels with time-dependent material properties enhance cardiomyocyte differentiation in vitro Biomaterials 32 2011 1002 1009
22. H.Y. Yoshikawa, and F.F. Rossetti M. Tanaka Quantitative evaluation of mechanosensing of cells on dynamically tunable hydrogels J. Am. Chem. Soc. 133 2011 1367 1374
23. D. Mitrossilis, and J. Fouchard A. Asnacios Real-time single-cell response to stiffness Proc. Natl. Acad. Sci. USA 107 2010 16518 16523
24. K.D. Webster, A. Crow, and D.A. Fletcher An AFM-based stiffness clamp for dynamic control of rigidity PLoS ONE 6 2011 e17807
25. W.A. Lam, and O. Chaudhuri D.A. Fletcher Mechanics and contraction dynamics of single platelets and implications for clot stiffening Nat. Mater. 10 2011 61 66
26. 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
27. J. Fouchard, D. Mitrossilis, and A. Asnacios Acto-myosin based response to stiffness and rigidity sensing Cell Adh. Migr. 5 2011 16 19
28. P. Marcq, N. Yoshinaga, and J. Prost Rigidity sensing explained by active matter theory Biophys. J. 101 2011 L33 L35
29. 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)
30. C.K. Choi, and M. Vicente-Manzanares A.R. Horwitz Actin and alpha-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner Nat. Cell Biol. 10 2008 1039 1050
31. K.A. Beningo, M. Dembo, and Y.-L. Wang Responses of fibroblasts to anchorage of dorsal extracellular matrix receptors Proc. Natl. Acad. Sci. USA 101 2004 18024 18029 (Pubitemid 40054068)
32. S. Munevar, Y.-L. Wang, and M. Dembo Regulation of mechanical interactions between fibroblasts and the substratum by stretch-activated Ca2+ entry J. Cell Sci. 117 2004 85 92 (Pubitemid 38072123)
33. B.D. Matthews, and C.K. Thodeti D.E. Ingber Ultra-rapid activation of TRPV4 ion channels by mechanical forces applied to cell surface beta1 integrins Integr Biol (Camb) 2 2010 435 442
34. G. Constantinides, and Z.I. Kalcioglu K.J. Van Vliet Probing mechanical properties of fully hydrated gels and biological tissues J. Biomech. 41 2008 3285 3289
35. Y. Aratyn-Schaus, P.W. Oakes, and M.L. Gardel Dynamic and structural signatures of lamellar actomyosin force generation Mol. Biol. Cell 22 2011 1330 1339
36. O. Thoumine, and A. Ott Time scale dependent viscoelastic and contractile regimes in fibroblasts probed by microplate manipulation J. Cell Sci. 110 1997 2109 2116 (Pubitemid 27440434)
37. A.R. Bausch, and F. Ziemann E. Sackmann Local measurements of viscoelastic parameters of adherent cell surfaces by magnetic bead microrheometry Biophys. J. 75 1998 2038 2049 (Pubitemid 28455200)
38. D. Humphrey, and C. Duggan J. Käs Active fluidization of polymer networks through molecular motors Nature 416 2002 413 416 (Pubitemid 34272872)
39. 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
40. B. Guo, and W.H. Guilford Mechanics of actomyosin bonds in different nucleotide states are tuned to muscle contraction Proc. Natl. Acad. Sci. USA 103 2006 9844 9849 (Pubitemid 43993585)
41. A. Hill The heat of shortening and the dynamic constants of muscle Proc. R. Soc. Lond. B Biol. Sci. 126 1938 136 195
42. G. Piazzesi, and M. Reconditi V. Lombardi Skeletal muscle performance determined by modulation of number of myosin motors rather than motor force or stroke size Cell 131 2007 784 795 (Pubitemid 350103598)
43. M. Kovács, and K. Thirumurugan J.R. Sellers Load-dependent mechanism of nonmuscle myosin 2 Proc. Natl. Acad. Sci. USA 104 2007 9994 9999 (Pubitemid 47175251)
44. M.F. Norstrom, P.A. Smithback, and R.S. Rock Unconventional processive mechanics of non-muscle myosin IIB J. Biol. Chem. 285 2010 26326 26334