A biomechanical model for fluidization of cells under dynamic strain

Biophysical Journal

Volumn 108, Issue 1, 2015, Pages 43-52

  Wu, Tenghu ^a   Feng, James J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN;

BIOLOGICAL MODEL; COMPUTER SIMULATION; MECHANICAL STRESS; METABOLISM; MUSCLE CONTRACTION; PHYSIOLOGY; SMOOTH MUSCLE CELL; VISCOSITY; YOUNG MODULUS;

ACTINS; COMPUTER SIMULATION; ELASTIC MODULUS; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MYOCYTES, SMOOTH MUSCLE; MYOSINS; STRESS, MECHANICAL; VISCOSITY;

EID: 84921029371     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2014.11.015     Document Type: Article

References (71)

1. X. Trepat, and L. Deng J.J. Fredberg Universal physical responses to stretch in the living cell Nature 447 2007 592 595
2. B.D. Matthews, and D.R. Overby D.E. Ingber Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels J. Cell Sci. 119 2006 508 518
3. N. Gavara, and P. Roca-Cusachs D. Navajas Mapping cell-matrix stresses during stretch reveals inelastic reorganization of the cytoskeleton Biophys. J. 95 2008 464 471
4. G. Giannone, and G. Jiang M.P. Sheetz Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation J. Cell Biol. 163 2003 409 419
5. R. Krishnan, and C.Y. Park J.J. Fredberg Reinforcement versus fluidization in cytoskeletal mechanoresponsiveness PLoS ONE 4 2009 e5486
6. C. Chen, and R. Krishnan J.J. Fredberg Fluidization and resolidification of the human bladder smooth muscle cell in response to transient stretch PLoS ONE 5 2010 e12035
7. R. Krishnan, and E.P. Canović D. Stamenović Fluidization, resolidification, and reorientation of the endothelial cell in response to slow tidal stretches Am. J. Physiol. Cell Physiol. 303 2012 C368 C375
8. K.I. Morozov, and L.M. Pismen Cytoskeleton fluidization versus resolidification: prestress effect Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 83 2011 051920
9. K.D. Costa, W.J. Hucker, and F.C.P. Yin Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry Cell Motil. Cytoskeleton 52 2002 266 274
10. K. Sato, and T. Adachi Y. Tomita Quantitative evaluation of threshold fiber strain that induces reorganization of cytoskeletal actin fiber structure in osteoblastic cells J. Biomech. 38 2005 1895 1901
11. K. Sato, and T. Adachi Y. Tomita Measurement of local strain on cell membrane at initiation point of calcium signaling response to applied mechanical stimulus in osteoblastic cells J. Biomech. 40 2007 1246 1255
12. M. Soares e Silva, and M. Depken G.H. Koenderink Active multistage coarsening of actin networks driven by myosin motors Proc. Natl. Acad. Sci. USA 108 2011 9408 9413
13. R. Kaunas, and S. Deguchi Multiple roles for myosin II in tensional homeostasis under mechanical loading Cell. Mol. Bioeng. 4 2011 182 191
14. A. Tondon, H.-J. Hsu, and R. Kaunas Dependence of cyclic stretch-induced stress fiber reorientation on stretch waveform J. Biomech. 45 2012 728 735
15. B. Chen, and R. Kemkemer H. Gao Cyclic stretch induces cell reorientation on substrates by destabilizing catch bonds in focal adhesions PLoS ONE 7 2012 e48346
16. K.I. Morozov, and L.M. Pismen Strain dependence of cytoskeleton elasticity Soft Matter 8 2012 9193 9199
17. L. Wolff, P. Fernández, and K. Kroy Resolving the stiffening-softening paradox in cell mechanics PLoS ONE 7 2012 e40063
18. B.T. Marshall, and M. Long C. Zhu Direct observation of catch bonds involving cell-adhesion molecules Nature 423 2003 190 193
19. R. Kaunas, H.-J. Hsu, and S. Deguchi Sarcomeric model of stretch-induced stress fiber reorganization Cell Health Cytoskel. 3 2011 13 22
20. A. Besser, and U.S. Schwarz Coupling biochemistry and mechanics in cell adhesion: a model for inhomogeneous stress fiber contraction New J. Phys. 9 2007 425
21. R.J. Russell, and S.L. Xia T.P. Lele Sarcomere mechanics in capillary endothelial cells Biophys. J. 97 2009 1578 1585
22. H.J. Hsu, and C.F. Lee R. Kaunas Stretch-induced stress fiber remodeling and the activations of JNK and ERK depend on mechanical strain rate, but not FAK PLoS ONE 5 2010 e12470
23. J. Bates, and S. Bullimore A. Lauzon Transient oscillatory force-length behavior of activated airway smooth muscle Am. J. Physiol.-. Lung C. 297 2009 L362 L372
24. B.S. Brook Emergence of airway smooth muscle mechanical behavior through dynamic reorganization of contractile units and force transmission pathways J. Appl. Physiol. 116 2014 980 997
25. S. Kumar, and I.Z. Maxwell D.E. Ingber Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics Biophys. J. 90 2006 3762 3773
26. T.S. Matsui, and K. Ito S. Deguchi Actin stress fibers are at a tipping point between conventional shortening and rapid disassembly at physiological levels of MgATP Biochem. Biophys. Res. Commun. 395 2010 301 306
27. T.S. Matsui, and R. Kaunas S. Deguchi Non-muscle myosin II induces disassembly of actin stress fibers independently of myosin light chain dephosphorylation Interface Focus 1 2011 754 766
28. A.P. Pirentis, and E. Peruski D. Stamenović A model for stress fiber realignment caused by cytoskeletal fluidization during cyclic stretching Cell. Mol. Bioeng 4 2011 67 80
29. J.A. Spudich The myosin swinging cross-bridge model Nat. Rev. Mol. Cell Biol. 2 2001 387 392
30. C.M. Hai, and R.A. Murphy Cross-bridge phosphorylation and regulation of latch state in smooth muscle Am. J. Physiol. 254 1988 C99 C106
31. S.M. Mijailovich, J.P. Butler, and J.J. Fredberg Perturbed equilibria of myosin binding in airway smooth muscle: bond-length distributions, mechanics, and ATP metabolism Biophys. J. 79 2000 2667 2681
32. L. Chin, and P. Yue C.Y. Seow Mathematical simulation of muscle cross-bridge cycle and force-velocity relationship Biophys. J. 91 2006 3653 3663
33. I. Wang, and A.Z. Politi J. Sneyd A mathematical model of airway and pulmonary arteriole smooth muscle Biophys. J. 94 2008 2053 2064
34. G.M. Donovan Modeling airway smooth-muscle passive length adaptation via thick-filament length distributions J. Theor. Biol. 333 2013 102 108
35. C. Veigel, and J.E. Molloy J. Kendrick-Jones Load-dependent kinetics of force production by smooth muscle myosin measured with optical tweezers Nat. Cell Biol. 5 2003 980 986
36. C. Veigel, and S. Schmitz J.R. Sellers Load-dependent kinetics of myosin-V can explain its high processivity Nat. Cell Biol. 7 2005 861 869
37. M. Kovács, and K. Thirumurugan J.R. Sellers Load-dependent mechanism of nonmuscle myosin 2 Proc. Natl. Acad. Sci. USA 104 2007 9994 9999
38. R.A. Brown, and R. Prajapati M. Eastwood Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates J. Cell. Physiol. 175 1998 323 332
39. A.V. Hill The heat of shortening and the dynamic constants of muscle Proc. R. Soc. Lond. 126 1938 136 195
40. C.Y. Seow Hill's equation of muscle performance and its hidden insight on molecular mechanisms J. Gen. Physiol. 142 2013 561 573
41. Z. Wei, and V.S. Deshpande A.G. Evans Analysis and interpretation of stress fiber organization in cells subject to cyclic stretch J. Biomech. Eng. 130 2008 031009
42. M.R. Stachowiak, and B. O'Shaughnessy Recoil after severing reveals stress fiber contraction mechanisms Biophys. J. 97 2009 462 471
43. J. Colombelli, and A. Besser E.H. Stelzer Mechanosensing in actin stress fibers revealed by a close correlation between force and protein localization J. Cell Sci. 122 2009 1665 1679
44. D.M. Warshaw, and J.M. Desrosiers K.M. Trybus Smooth muscle myosin cross-bridge interactions modulate actin filament sliding velocity in vitro J. Cell Biol. 111 1990 453 463
45. T. Luo, and K. Mohan D.N. Robinson Understanding the cooperative interaction between myosin II and actin cross-linkers mediated by actin filaments during mechanosensation Biophys. J. 102 2012 238 247
46. T. Luo, and K. Mohan D.N. Robinson Molecular mechanisms of cellular mechanosensing Nat. Mater. 12 2013 1064 1071
47. J.-W. Shin, and A. Buxboim D.E. Discher Contractile forces sustain and polarize hematopoiesis from stem and progenitor cells Cell Stem Cell 14 2014 81 93
48. S.S. Rosenfeld, and J. Xing H.L. Sweeney Myosin IIb is unconventionally conventional J. Biol. Chem. 278 2003 27449 27455
49. M.A. Conti, S. Kawamoto, and R.S. Adelstein Non-muscle myosin II A.J. Ridley, J. Frampton, Proteins and Cell Regulation Vol. 7 2008 Springer Berlin 223 264
50. F. Wang, and M. Kovács J.R. Sellers Kinetic mechanism of non-muscle myosin IIB: functional adaptations for tension generation and maintenance J. Biol. Chem. 278 2003 27439 27448
51. E.P. Debold, J.B. Patlak, and D.M. Warshaw Slip sliding away: load-dependence of velocity generated by skeletal muscle myosin molecules in the laser trap Biophys. J. 89 2005 L34 L36
52. S. Deguchi, T. Ohashi, and M. Sato Tensile properties of single stress fibers isolated from cultured vascular smooth muscle cells J. Biomech. 39 2006 2603 2610
53. Q. Wang, J.J. Feng, and L.M. Pismen A cell-level biomechanical model of Drosophila dorsal closure Biophys. J. 103 2012 2265 2274
54. J.W. Sanger, J.M. Sanger, and B.M. Jockusch Differences in the stress fibers between fibroblasts and epithelial cells J. Cell Biol. 96 1983 961 969
55. L. Lu, and Y. Feng F.C.P. Yin Actin stress fiber pre-extension in human aortic endothelial cells Cell Motil. Cytoskeleton 65 2008 281 294
56. K. Katoh, and Y. Kano K. Fujiwara Isolation and contraction of the stress fiber Mol. Biol. Cell 9 1998 1919 1938
57. K. Katoh, and Y. Kano K. Fujiwara Rho-kinase - mediated contraction of isolated stress fibers J. Cell Biol. 153 2001 569 584
58. J. Kolega Cytoplasmic dynamics of myosin IIA and IIB: spatial 'sorting' of isoforms in locomoting cells J. Cell Sci. 111 1998 2085 2095
59. J. Kolega Asymmetric distribution of myosin IIB in migrating endothelial cells is regulated by a rho-dependent kinase and contributes to tail retraction Mol. Biol. Cell 14 2003 4745 4757
60. M. Vicente-Manzanares, and J. Zareno A.F. Horwitz Regulation of protrusion, adhesion dynamics, and polarity by myosins IIA and IIB in migrating cells J. Cell Biol. 176 2007 573 580
61. M. Vicente-Manzanares, and M.A. Koach A.F. Horwitz Segregation and activation of myosin IIB creates a rear in migrating cells J. Cell Biol. 183 2008 543 554
62. J. Pourati, and A. Maniotis N. Wang Is cytoskeletal tension a major determinant of cell deformability in adherent endothelial cells? Am. J. Physiol. 274 1998 C1283 C1289
63. T. Mizutani, H. Haga, and K. Kawabata Cellular stiffness response to external deformation: tensional homeostasis in a single fibroblast Cell Motil. Cytoskeleton 59 2004 242 248
64. 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
65. N. Wang, and I.M. Tolić-Nørrelykke D. Stamenović Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells Am. J. Physiol. Cell Physiol. 282 2002 C606 C616
66. R. Kaunas, and P. Nguyen S. Chien Cooperative effects of Rho and mechanical stretch on stress fiber organization Proc. Natl. Acad. Sci. USA 102 2005 15895 15900
67. R. Kaunas, and H.-J. Hsu A kinematic model of stretch-induced stress fiber turnover and reorientation J. Theor. Biol. 257 2009 320 330
68. 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
69. 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
70. S.-Y. Tee, and J. Fu P.A. Janmey Cell shape and substrate rigidity both regulate cell stiffness Biophys. J. 100 2011 L25 L27
71. R.A. Jannat, M. Dembo, and D.A. Hammer Traction forces of neutrophils migrating on compliant substrates Biophys. J. 101 2011 575 584