Cyclic Tensile Strain Controls Cell Shape and Directs Actin Stress Fiber Formation and Focal Adhesion Alignment in Spreading Cells

PLoS ONE

Volumn 8, Issue 10, 2013, Pages

  Greiner, Alexandra M ^a   Chen, Hao ^a   Spatz, Joachim P ^b,c   Kemkemer, Ralf ^b,d  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR INTELLIGENT SYSTEMS   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d REUTLINGEN UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN II;

ARTICLE; CELL ACTIVITY; CELL ELONGATION; CELL MATURATION; CELL POLARITY; CELL SHAPE; CELL SIZE; CELL SPREADING; CONTROLLED STUDY; CYCLIC TENSILE STRAIN; EXTRACELLULAR MATRIX; FIBROBLAST; FOCAL ADHESION; INTRACELLULAR SIGNALING; MICROTUBULE; STRESS FIBER;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CELL ADHESION; CELL SHAPE; CELL SIZE; FOCAL ADHESIONS; MECHANOTRANSDUCTION, CELLULAR; MICE; MICROTUBULES; MYOSIN TYPE II; NIH 3T3 CELLS; STRESS, MECHANICAL;

EID: 84886617321     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0077328     Document Type: Article

References (56)

1. Balaban NQ, Schwarz US, Riveline D, Goichberg P, Tzur G, et al. (2001) Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nat Cell Biol 3: 466-472.
2. Cai Y, Sheetz MP, (2009) Force propagation across cells: mechanical coherence of dynamic cytoskeletons. Curr Opin Cell Biol 21: 47-50.
3. McCaig CD, Zhao M, (1997) Physiological electrical fields modify cell behaviour. Bioessays 19: 819-826.
4. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA, (2010) Cell shape, spreading symmetry and the polarization of stress-fibers in cells. J Phys Condens Matter 22: 194110.
5. Vogel V, Sheetz M, (2006) Local force and geometry sensing regulate cell functions. Nat Rev Mol Cell Biol 7: 265-275.
6. Zemel A, Rehfeldt F, Brown AE, Discher DE, Safran SA, (2010) Optimal matrix rigidity for stress fiber polarization in stem cells. Nat Phys 6: 468-473.
7. Thery M, (2010) Micropatterning as a tool to decipher cell morphogenesis and functions. J Cell Sci 123: 4201-4213.
8. Thery M, Pepin A, Dressaire E, Chen Y, Bornens M, (2006) Cell distribution of stress fibres in response to the geometry of the adhesive environment. Cell Motil Cytoskeleton 63: 341-355.
9. De R, Zemel A, Safran SA, (2007) Dynamics of cell orientation. Nature Physics 3: 655-659.
10. Prager-Khoutorsky M, Lichtenstein A, Krishnan R, Rajendran K, Mayo A, et al. (2011) Fibroblast polarization is a matrix-rigidity-dependent process controlled by focal adhesion mechanosensing. Nat Cell Biol 13: 1457-1465.
11. Kaunas R, Nguyen P, Usami S, Chien S, (2005) Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc Natl Acad Sci U S A 102: 15895-15900.
12. Goldyn AM, Rioja BA, Spatz JP, Ballestrem C, Kemkemer R, (2009) Force-induced cell polarisation is linked to RhoA-driven microtubule-independent focal-adhesion sliding. J Cell Sci 122: 3644-3651.
13. Goldyn AM, Kaiser P, Spatz JP, Ballestrem C, Kemkemer R, (2010) The kinetics of force-induced cell reorganization depend on microtubules and actin. Cytoskeleton (Hoboken) 67: 241-250.
14. Engler AJ, Sen S, Sweeney HL, Discher DE, (2006) Matrix elasticity directs stem cell lineage specification. Cell 126: 677-689.
15. Kurpinski K, Chu J, Hashi C, Li S, (2006) Anisotropic mechanosensing by mesenchymal stem cells. Proc Natl Acad Sci U S A 103: 16095-16100.
16. Defilippi P, Olivo C, Venturino M, Dolce L, Silengo L, et al. (1999) Actin cytoskeleton organization in response to integrin-mediated adhesion. Microsc Res Tech 47: 67-78.
17. Zimerman B, Volberg T, Geiger B, (2004) Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil Cytoskeleton 58: 143-159.
18. Lehnert D, Wehrle-Haller B, David C, Weiland U, Ballestrem C, et al. (2004) Cell behaviour on micropatterned substrata: limits of extracellular matrix geometry for spreading and adhesion. J Cell Sci 117: 41-52.
19. Buck RC, (1980) Reorientation response of cells to repeated stretch and recoil of the substratum. Exp Cell Res 127: 470-474.
20. Dartsch PC, Hammerle H, Betz E, (1986) Orientation of cultured arterial smooth muscle cells growing on cyclically stretched substrates. Acta Anat (Basel) 125: 108-113.
21. Jungbauer S, Gao H, Spatz JP, Kemkemer R, (2008) Two characteristic regimes in frequency-dependent dynamic reorientation of fibroblasts on cyclically stretched substrates. Biophys J 95: 3470-3478.
22. Neidlinger-Wilke C, Grood ES, Wang J-C, Brand RA, Claes L, (2001) Cell alignment is induced by cyclic changes in cell length: studies of cells grown in cyclically stretched substrates. J Orthop Res 19: 286-293.
23. Chen B, Kemkemer R, Deibler M, Spatz J, Gao H, (2012) Cyclic stretch induces cell reorientation on substrates by destabilizing catch bonds in focal adhesions. PLoS One 7: e48346.
24. De R, Zemel A, Safran SA, (2008) Do cells sense stress or strain? Measurement of cellular orientation can provide a clue. Biophys J 94: L29-31.
25. Faust U, Hampe N, Rubner W, Kirchgessner N, Safran S, et al. (2011) Cyclic stress at mHz frequencies aligns fibroblasts in direction of zero strain. PLoS One 6: e28963.
26. Deibler M, Spatz JP, Kemkemer R, (2011) Actin fusion proteins alter the dynamics of mechanically induced cytoskeleton rearrangement. PLoS One 6: e22941.
27. Ahmed WW, Wolfram T, Goldyn AM, Bruellhoff K, Rioja BA, et al. (2010) Myoblast morphology and organization on biochemically micro-patterned hydrogel coatings under cyclic mechanical strain. Biomaterials 31: 250-258.
28. Hayakawa K, Sato N, Obinata T, (2001) Dynamic reorientation of cultured cells and stress fibers under mechanical stress from periodic stretching. Exp Cell Res 268: 104-114.
29. Lee CF, Haase C, Deguchi S, Kaunas R, (2010) Cyclic stretch-induced stress fiber dynamics- dependence on strain rate, Rho-kinase and MLCK. Biochem Biophys Res Commun 401: 344-349.
30. Hynes RO, (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110: 673-687.
31. Bershadsky AD, Balaban NQ, Geiger B, (2003) Adhesion-dependent cell mechanosensitivity. Annu Rev Cell Dev Biol 19: 677-695.
32. Puklin-Faucher E, Sheetz MP, (2009) The mechanical integrin cycle. J Cell Sci 122: 179-186.
33. Katsumi A, Orr AW, Tzima E, Schwartz MA, (2004) Integrins in mechanotransduction. J Biol Chem 279: 12001-12004.
34. Aratyn-Schaus Y, Gardel ML, (2010) Transient Frictional Slip between Integrin and the ECM in Focal Adhesions under Myosin II Tension. Current Biology 20: 1145-1153.
35. Cai Y, Rossier O, Gauthier NC, Biais N, Fardin MA, et al. (2010) Cytoskeletal coherence requires myosin-IIA contractility. J Cell Sci 123: 413-423.
36. Zhang X, Jiang G, Cai Y, Monkley SJ, Critchley DR, et al. (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nat Cell Biol 10: 1062-1068.
37. Galbraith CG, Yamada KM, Sheetz MP, (2002) The relationship between force and focal complex development. J Cell Biol 159: 695-705.
38. Oakes PW, Beckham Y, Stricker J, Gardel ML, (2012) Tension is required but not sufficient for focal adhesion maturation without a stress fiber template. J Cell Biol 196: 363-374.
39. Costa KD, Hucker WJ, Yin FC, (2002) Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil Cytoskeleton 52: 266-274.
40. Brown RA, Prajapati R, McGrouther DA, Yannas IV, Eastwood M, (1998) Tensional homeostasis in dermal fibroblasts: mechanical responses to mechanical loading in three-dimensional substrates. J Cell Physiol 175: 323-332.
41. Mizutani T, Haga H, Kawabata K, (2004) Cellular stiffness response to external deformation: tensional homeostasis in a single fibroblast. Cell Motil Cytoskeleton 59: 242-248.
42. Wei Z, Deshpande VS, McMeeking RM, Evans AG, (2008) Analysis and interpretation of stress fiber organization in cells subject to cyclic stretch. J Biomech Eng 130: 031009.
43. Kaunas R, Hsu H, Deguchi S, (2011) Sarcomeric model of stretch-induced stress fiber reorganization. Cell Health and Cytoskeleton 3: 13-22.
44. Alenghat FJ, Ingber DE, (2002) Mechanotransduction: all signals point to cytoskeleton, matrix, and integrins. Sci STKE 2002: PE6.
45. Cai Y, Biais N, Giannone G, Tanase M, Jiang G, et al. (2006) Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys J 91: 3907-3920.
46. Tojkander S, Gateva G, Lappalainen P, (2012) Actin stress fibers-assembly, dynamics and biological roles. J Cell Sci 125: 1855-1864.
47. Betapudi V, (2010) Myosin II motor proteins with different functions determine the fate of lamellipodia extension during cell spreading. PLoS One 5: e8560.
48. Rehfeldt F, Discher DE, (2007) Biophysics: Cell dipoles feel their way. Nature Physics 3: 592-593.
49. Dobereiner HG, Dubin-Thaler BJ, Giannone G, Sheetz MP, (2005) Force sensing and generation in cell phases: analyses of complex functions. J Appl Physiol 98: 1542-1546.
50. Pierres A, Benoliel AM, Touchard D, Bongrand P, (2008) How cells tiptoe on adhesive surfaces before sticking. Biophys J 94: 4114-4122.
51. Suter DM, Errante LD, Belotserkovsky V, Forscher P, (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J Cell Biol 141: 227-240.
52. Kaverina I, Krylyshkina O, Beningo K, Anderson K, Wang YL, et al. (2002) Tensile stress stimulates microtubule outgrowth in living cells. J Cell Sci 115: 2283-2291.
53. Schmoranzer J, Kreitzer G, Simon SM, (2003) Migrating fibroblasts perform polarized, microtubule-dependent exocytosis towards the leading edge. J Cell Sci 116: 4513-4519.
54. Wehrle-Haller B, Imhof BA, (2003) Actin, microtubules and focal adhesion dynamics during cell migration. Int J Biochem Cell Biol 35: 39-50.
55. Ingber DE, (2008) Tensegrity-based mechanosensing from macro to micro. Prog Biophys Mol Biol 97: 163-179.
56. Cuvelier D, Thery M, Chu YS, Dufour S, Thiery JP, et al. (2007) The universal dynamics of cell spreading. Curr Biol 17: 694-699.