Lateral communication between stress fiber sarcomeres facilitates a local remodeling response

Biophysical Journal

Volumn 103, Issue 10, 2012, Pages 2082-2092

  Chapin, Laura M ^a   Blankman, Elizabeth ^a   Smith, Mark A ^a   Shiu, Yan Ting ^b   Beckerle, Mary C ^a  

^a UNIVERSITY OF UTAH   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ANIMAL; ARTICLE; BIOLOGICAL MODEL; BIOMECHANICS; CELL SURVIVAL; CYTOLOGY; FIBROBLAST; HOMEOSTASIS; MECHANICAL STRESS; METABOLISM; MOUSE; SARCOMERE; STRESS FIBER;

ACTINS; ANIMALS; BIOMECHANICS; CELL SURVIVAL; FIBROBLASTS; HOMEOSTASIS; MICE; MODELS, BIOLOGICAL; SARCOMERES; STRESS FIBERS; STRESS, MECHANICAL;

EID: 84869448333     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.09.038     Document Type: Article

References (48)

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
2. A. Hall Rho GTPases and the actin cytoskeleton Science 279 1998 509 514
3. A.B. Jaffe, and A. Hall Rho GTPases: biochemistry and biology Annu. Rev. Cell Dev. Biol. 21 2005 247 269
4. V. Vogel, and M. Sheetz Local force and geometry sensing regulate cell functions Nat. Rev. Mol. Cell Biol. 7 2006 265 275
5. B.M. Friedrich, and A. Buxboim S.A. Safran Striated acto-myosin fibers can reorganize and register in response to elastic interactions with the matrix Biophys. J. 100 2011 2706 2715
6. G.M. O'Neill The coordination between actin filaments and adhesion in mesenchymal migration Cell Adhes. Migr. 3 2009 355 357
7. G. Isenberg, and P.C. Rathke K.E. Wohlfarth-Bottermann Cytoplasmic actomyosin fibrils in tissue culture cells: direct proof of contractility by visualization of ATP-induced contraction in fibrils isolated by laser micro-beam dissection Cell Tissue Res. 166 1976 427 443
8. K. Katoh, and Y. Kano K. Fujiwara Isolation and contraction of the stress fiber Mol. Biol. Cell 9 1998 1919 1938
9. E. Lazarides, and K. Burridge Alpha-actinin: immunofluorescent localization of a muscle structural protein in nonmuscle cells Cell 6 1975 289 298
10. K. Weber, and U. Groeschel-Stewart Antibody to myosin: the specific visualization of myosin-containing filaments in nonmuscle cells Proc. Natl. Acad. Sci. USA 71 1974 4561 4564
11. 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
12. N. Endlich, and C.A. Otey K. Endlich Movement of stress fibers away from focal adhesions identifies focal adhesions as sites of stress fiber assembly in stationary cells Cell Motil. Cytoskeleton 64 2007 966 976
13. L.J. Peterson, and Z. Rajfur K. Burridge Simultaneous stretching and contraction of stress fibers in vivo Mol. Biol. Cell 15 2004 3497 3508
14. O.M. Rossier, and N. Gauthier M.P. Sheetz Force generated by actomyosin contraction builds bridges between adhesive contacts EMBO J. 29 2010 1055 1068
15. B. Russell, and M.W. Curtis A.M. Samarel Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width J. Mol. Cell. Cardiol. 48 2010 817 823
16. M.A. Smith, and E. Blankman M.C. Beckerle A zyxin-mediated mechanism for actin stress fiber maintenance and repair Dev. Cell 19 2010 365 376
17. W.H. Guo, and Y.L. Wang Retrograde fluxes of focal adhesion proteins in response to cell migration and mechanical signals Mol. Biol. Cell 18 2007 4519 4527
18. P. Hotulainen, and P. Lappalainen Stress fibers are generated by two distinct actin assembly mechanisms in motile cells J. Cell Biol. 173 2006 383 394
19. T. Usui Actin- and microtubule-targeting bioprobes: their binding sites and inhibitory mechanisms Biosci. Biotechnol. Biochem. 71 2007 300 308
20. S. Deguchi, and M. Sato Biomechanical properties of actin stress fibers of non-motile cells Biorheology 46 2009 93 105
21. 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
22. R.J. Russell, and S.L. Xia T.P. Lele Sarcomere mechanics in capillary endothelial cells Biophys. J. 97 2009 1578 1585
23. L.M. Hoffman, and C.C. Jensen M.C. Beckerle Genetic ablation of zyxin causes Mena/VASP mislocalization, increased motility, and deficits in actin remodeling J. Cell Biol. 172 2006 771 782
24. E.E. Bragina, J.M. Vasiliev, and I.M. Gelfand Formation of bundles of microfilaments during spreading of fibroblasts on the substrate Exp. Cell Res. 97 1976 241 248
25. K. Burridge Are stress fibers contractile? Nature 294 1981 691 692
26. L. Guolla, and M. Bertrand A.E. Pelling Force transduction and strain dynamics in actin stress fibers in response to nanoNewton forces J. Cell Sci. 125 2012 603 613
27. O. Esue, Y. Tseng, and D. Wirtz Alpha-actinin and filamin cooperatively enhance the stiffness of actin filament networks PLoS ONE 4 2009 e4411
28. K. Burridge, and J.R. Feramisco Non-muscle α-actinins are calcium-sensitive actin-binding proteins Nature 294 1981 565 567
29. D.L. Morgan New insights into the behavior of muscle during active lengthening Biophys. J. 57 1990 209 221
30. G.T. Charras, and M.A. Horton Determination of cellular strains by combined atomic force microscopy and finite element modeling Biophys. J. 83 2002 858 879
31. H. Haga, and S. Sasaki T. Sambongi Elasticity mapping of living fibroblasts by AFM and immunofluorescence observation of the cytoskeleton Ultramicroscopy 82 2000 253 258
32. D.E. Rassier The mechanisms of the residual force enhancement after stretch of skeletal muscle: non-uniformity in half-sarcomeres and stiffness of titin Proc. Biol. Sci. R. Soc. B. 2012 10.1098/rspb.2012.0467
33. 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
34. D. Riveline, and E. Zamir A.D. Bershadsky 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 2001 1175 1186
35. V.E. Galkin, A. Orlova, and E.H. Egelman Actin filaments as tension sensors Curr. Biol. 22 2012 R96 R101
36. Y. Sawada, and M.P. Sheetz Force transduction by Triton cytoskeletons J. Cell Biol. 156 2002 609 615
37. J. Solon, and I. Levental P.A. Janmey Fibroblast adaptation and stiffness matching to soft elastic substrates Biophys. J. 93 2007 4453 4461
38. B.D. Hoffman, C. Grashoff, and M.A. Schwartz Dynamic molecular processes mediate cellular mechanotransduction Nature 475 2011 316 323
39. K.D. Costa, W.J. Hucker, and F.C. Yin Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry Cell Motil. Cytoskeleton 52 2002 266 274
40. S. Deguchi, T.S. Matsui, and M. Sato Simultaneous contraction and buckling of stress fibers in individual cells J. Cell. Biochem. 113 2012 824 832
41. L. Lu, and S.J. Oswald F.C. Yin Mechanical properties of actin stress fibers in living cells Biophys. J. 95 2008 6060 6071
42. 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
43. P.J. Cavnar, S.G. Olenych, and T.C. Keller 3rd Molecular identification and localization of cellular titin, a novel titin isoform in the fibroblast stress fiber Cell Motil. Cytoskeleton 64 2007 418 433
44. M. Gautel Cytoskeletal protein kinases: titin and its relations in mechanosensing Pflugers Archiv. Eur. J. Physiol. 462 2011 119 134
45. D. Frank, and N. Frey Cardiac Z-disc signaling network J. Biol. Chem. 286 2011 9897 9904
46. K. Tanner, and A. Boudreau S. Kumar Dissecting regional variations in stress fiber mechanics in living cells with laser nanosurgery Biophys. J. 99 2010 2775 2783
47. G. Totsukawa, and Y. Wu F. Matsumura Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts J. Cell Biol. 164 2004 427 439
48. D. Kirchenbuchler, and S. Born R. Merkel Substrate, focal adhesions, and actin filaments: a mechanical unit with a weak spot for mechanosensitive proteins J. Phys. Cond. Matter 22 2010 194109