Viscoelastic retraction of single living stress fibers and its impact on cell shape, cytoskeletal organization, and extracellular matrix mechanics

Biophysical Journal

Volumn 90, Issue 10, 2006, Pages 3762-3773

  Kumar, Sanjay ^a,c   Maxwell, Iva Z ^b   Heisterkamp, Alexander ^b,d   Polte, Thomas R ^a   Lele, Tanmay P ^a   Salanga, Matthew ^a   Mazur, Eric ^b   Ingber, Donald E ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c University of California at Berkeley   (United States)

^d LASER ZENTRUM HANNOVER E V   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN LIGHT CHAIN KINASE; RHO KINASE;

ANIMAL CELL; ARTICLE; BLEACHING; CELL ANCHORAGE; CELL CULTURE; CELL DISRUPTION; CELL KINETICS; CELL SHAPE; CYTOSKELETON; ENZYME SUBSTRATE; EXTRACELLULAR MATRIX; LASER; MICROSCOPY; NONHUMAN; STRESS FIBER; TRACTION FORCE MICROSCOPY; VISCOELASTICITY;

ANIMALIA;

EID: 33646179573     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.105.071506     Document Type: Article

References (92)

1. Chen, C. S., M. Mrksich, S. Huang, G. M. Whitesides, and D. E. Ingber. 1997. Geometric control of cell life and death. Science. 276:1425-1428.
2. Parker, K. K., A. L. Brock, C. Brangwynne, R. J. Mannix, N. Wang, E. Ostuni, N. A. Geisse, J. C. Adams, G. M. Whitesides, and D. E. Ingber. 2002. Directional control of lamellipodia extension by constraining cell shape and orienting cell tractional forces. FASEB J. 16:1195-1204.
3. Singhvi, R., A. Kumar, G. P. Lopez, G. N. Stephanopoulos, D. I. C. Wang, G. M. Whitesides, and D. E. Ingber. 1994. Engineering cell-shape and function. Science. 264:696-698.
4. McBeath, R., D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell. 6:483-495.
5. Ridley, A. J., M. A. Schwartz, K. Burridge, R. A. Firtel, M. H. Ginsberg, G. Borisy, J. T. Parsons, and A. R. Horwitz. 2003. Cell migration: integrating signals from front to back. Science. 302:1704-1709.
6. Hoh, J. H., and C. A. Schoenenberger. 1994. Surface-morphology and mechanical-properties of MDCK monolayers by atomic force microscopy. J. Cell Sci. 107:1105-1114.
7. Litniewski, J., and J. Bereiter-Hahn. 1990. Measurements of cells in culture by scanning acoustic microscopy. J. Microsc. 158:95-107.
8. Ingber, D. E. 2003. Tensegrity I. Cell structure and hierarchical systems biology. J. Cell Sci. 116:1157-1173.
9. Wang, N., K. Naruse, D. Stamenovic, J. J. Fredberg, S. M. Mijailovich, I. M. Toric-Norrelykke, T. Polte, R. Mannix, and D. E. Ingber. 2001. Mechanical behavior in living cells consistent with the tensegrity model. Proc. Natl. Acad. Sci. USA. 98:7765-7770.
10. Wang, N., I. M. Tolic-Norrelykke, J. X. Chen, S. M. Mijailovich, J. P. Butler, J. J. Fredberg, and D. Stamenovic. 2002. Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Physiol. 282:C606-C616.
11. Stamenovic, D., Z. L. Liang, J. X. Chen, and N. Wang. 2002. Effect of the cytoskeletal prestress on the mechanical impedance of cultured airway smooth muscle cells. J. Appl. Physiol. 92:1443-1450.
12. Stamenovic, D., B. Suki, B. Fabry, N. Wang, and J. J. Fredberg. 2004. Rheology of airway smooth muscle cells is associated with cytoskeletal contractile stress. J. Appl. Physiol. 96:1600-1605.
13. Heidemann, S. R., and D. Wirtz. 2004. Towards a regional approach to cell mechanics. Trends Cell Biol. 14:160-166.
14. Heidemann, S. R., P. Lamoureux, and R. E. Buxbaum. 2000. Opposing views on tensegrity as a structural framework for understanding cell mechanics. J. Appl. Physiol. 89:1670-1678.
15. Jenkins, S. 2000. Does tensegrity make the machine work? Scientist. 17:26-27.
16. Costa, K. D., W. J. Hucker, and F. C. P. Yin. 2002. Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil. Cytoskeleton. 52:266-274.
17. Kolodney, M. S., and R. B. Wysolmerski. 1992. Isometric contraction by fibroblasts and endothelial cells in tissue culture - a quantitative study. J. Cell Biol. 117:73-82.
18. Riveline, D., E. Zamir, N. Q. Balaban, U. S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A. D. Bershadsky. 2001. 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. 153:1175-1185.
19. Katoh, K., Y. Kano, M. Masuda, H. Onishi, and K. Fujiwara. 1998. Isolation and contraction of the stress fiber. Mol. Biol. Cell. 9:1919-1938.
20. Deguchi, S., T. Ohashi, and M. Sato. 2005. Tensile properties of single stress fibers isolated from vascular smooth muscle cells. J. Biomech. In press.
21. Gordon, W. E. 1978. Immunofluorescent and ultrastructural studies of sarcomeric units in stress fibers of cultured non-muscle cells. Exp. Cell Res. 117:253-260.
22. Sanger, J. W., B. Mittal, and J. M. Sanger. 1984. Analysis of myofibrillar structure and assembly using fluorescently labeled contractile proteins. J. Cell Biol. 98:825-833.
23. Kreis, T. E., and W. Birchmeier. 1980. Stress fiber sarcomeres of fibroblasts are contractile. Cell. 22:555-561.
24. Anderson, S., L. DiCesare, I. Tan, T. Leung, and N. SundarRaj. 2004. Rho-mediated assembly of stress fibers is differentially regulated in corneal fibroblasts and myofibroblasts. Exp. Cell Res. 298:574-583.
25. Chen, B. H., J. T. C. Tzen, A. R. Bresnick, and H. C. Chen. 2002. Roles of Rho-associated kinase and myosin light chain kinase in morphological and migratory defects of focal adhesion kinase-null cells. J. Biol. Chem. 277:33857-33863.
26. Katoh, K., Y. Kano, M. Amano, K. Kaibuchi, and K. Fujiwara. 2001. Stress fiber organization regulated by MLCK and Rho-kinase in cultured human fibroblasts. Am. J. Physiol. Cell Physiol. 280:C1669-C1679.
27. Sinnett-Smith, J., J. A. Lunn, D. Leopoldt, and E. Rozengurt. 2001. Y-27632, an inhibitor of Rho-associated kinases, prevents tyrosine phosphorylation of focal adhesion kinase and paxillin induced by bombesin: dissociation from tyrosine phosphorylation of p130(cas). Exp. Cell Res. 266:292-302.
28. Yeung, T., P. C. Georges, L. A. Flanagan, B. Marg, M. Ortiz, M. Funaki, N. Zahir, W. Y. Ming, V. Weaver, and P. A. Janmey. 2005. Effects of substrate stiffness on cell morphology, cytoskeletal structure, and adhesion. Cell Motil. Cytoskeleton. 60:24-34.
29. Gupton, S. L., K. L. Anderson, T. P. Kole, R. S. Fischer, A. Ponti, S. E. Hitchcock-DeGregori, G. Danuser, V. M. Fowler, D. Wirtz, D. Hanein, and others. 2005. Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropornyosin. J. Cell Biol. 168:619-631.
30. Stossel, T. P. 1989. From signal to pseudopod - how cells control cytoplasmic actin assembly. J. Biol. Chem. 264:18261-18264.
31. Theriot, J. A., and T. J. Mitchison. 1991. Actin microfilament dynamics in locomoting cells. Nature. 352:126-131.
32. Kolega, J., J. W. Janson, and D. L. Taylor. 1991. The role of solation-contraction coupling in regulating stress fiber dynamics in nonmuscle cells. J. Cell Biol. 114:993-1003.
33. Strohmeier, R., and J. Bereiter-Hahn. 1984. Control of cell-shape and locomotion by external calcium. Exp. Cell Res. 154:412-420.
34. Tseng, Y., K. M. An, and D. Wirtz. 2002. Microheterogeneity controls the rate of gelation of actin filament networks. J. Biol. Chem. 277:18143-18150.
35. Bereiter-Hahn, J., M. Luck, T. Miebach, H. K. Stelzer, and M. Voth. 1990. Spreading of trypsinized cells-cytoskeletal dynamics and energy requirements. J. Cell Sci. 96:171-188.
36. Mooney, D. J., R. Langer, and D. E. Ingber. 1995. Cytoskeletal filament assembly and the control of cell spreading and function by extracellular-matrix. J. Cell Sci. 108:2311-2320.
37. Heisterkamp, A., I. Z. Maxwell, E. Mazur, J. M. Underwood, J. A. Nickerson, S. Kumar, and D. E. Ingber. 2005. Pulse energy dependence of subcellular dissection by femtosecond laser pulses. Opt. Express. 13:3690-3696.
38. Shen, N., D. Datta, C. B. Schaffer, P. LeDuc, D. E. Ingber, and E. Mazur. 2005. Ablation of cytoskeletal filaments and mitochondria in cells using a femtosecond laser nanoscissor. Mech. Chem. Biosyst. 2:17-25.
39. Koonce, M. P., K. R. Strahs, and M. W. Berns. 1982. Repair of laser-severed stress fibers in myocardial non-muscle cells. Exp. Cell Res. 141:375-384.
40. Strahs, K. R., and M. W. Berns. 1979. Laser microirradiation of stress fibers and intermediate filaments in non-muscle cells from cultured ratheart. Exp. Cell Res. 119:31-45.
41. Hu, S., J. Chen, B. Fabry, Y. Numaguchi, A. Gouldstone, D. E. Ingber, J. J. Fredberg, J. P. Butler, and N. Wang. 2003. Intracellular stress tomography reveals stress focusing and structural anisotropy in cytoskeleton of living cells. Am. J. Physiol. Cell Physiol. 285:1082-1090.
42. Alenghat, F. J., S. M. Nauli, R. Kolb, J. Zhou, and D. E. Ingber. 2004. Global cytoskeletal control of mechanotransduction in kidney epithelial cells. Exp. Cell Res. 301:23-30.
43. Munevar, S., Y. L. Wang, and M. Dembo. 2001. Traction force microscopy of migrating normal and h-ras transformed 3t3 fibroblasts. Biophys. J. 80:1744-1757.
44. Polte, T. R., G. S. Eichler, N. Wang, and D. E. Ingber. 2004. Extracellular matrix controls myosin light chain phosphorylation and cell contractility through modulation of cell shape and cytoskeletal prestress. Am. J. Physiol. Cell Physiol. 286:C518-C528.
45. Butler, J. P., I. M. Tolic-Norrelykke, B. Fabry, and J. J. Fredberg. 2002. Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282:C595-C605.
46. Landau, L. D., and E. M. Lifshitz. 1986. Theory of Elasticity. Pergammon, Oxford, UK.
47. Botvinick, E. L., V. Venugopalan, J. V. Shah, L. H. Liaw, and M. W. Berns. 2004. Controlled ablation of microtubules using a picosecond laser. Biophys. J. 87:4203-4212.
48. Clement, S., B. Hinz, V. Dugina, G. Gabbiani, and C. Chaponnier. 2005. The N-terminal Ac-EEED sequence plays a role in alpha-smooth-muscle actin incorporation into stress fibers. J. Cell Sci. 118:1395-1404.
49. McKenna, N. M., and Y. L. Wang. 1986. Possible translocation of actin and alpha-actinin along stress fibers. Exp. Cell Res. 167:95-105.
50. Yoon, K. H., M. Yoon, R. D. Moir, S. Khuon, F. W. Flitney, and R. D. Goldman. 2001. Insights into the dynamic properties of keratin intermediate filaments in living epithelial cells. J. Cell Biol. 153:503-516.
51. Osswald, T. A., and G. Menges. 1995. Materials Science of Polymers for Engineers. Hanser/Gardner, Munich, Germany.
52. Canadas, P., V. M. Laurent, C. Oddou, D. Isabey, and S. Wendling. 2002. A cellular tensegrity model to analyse the structural viscoelasticity of the cytoskeleton. J. Theor. Biol. 218:155-173.
53. Narumiya, S., T. Ishizaki, and M. Uehata. 2000. Use and properties of ROCK-specific inhibitor Y-27632. Methods Enzymol. 325:273-284.
54. Mammoto, A., S. Huang, K. Moore, P. Oh, and D. E. Ingber. 2004. Role of RhoA, mDia, and ROCK in cell shape-dependent control of the skp2-p27(kip1) pathway and the g(1)/s transition. J. Biol. Chem. 279:26323-26330.
55. Peyton, S. R., and A. J. Putnam. 2005. Extracellular matrix rigidity governs smooth muscle cell rigidity in a biphasic fashion. J. Cell. Physiol. 204:198-209.
56. Shiu, Y. T., S. Li, W. A. Marganski, S. Usami, M. A. Schwartz, Y. L. Wang, M. Dembo, and S. Chien. 2004. Rho mediates the shear-enhancement of endothelial cell migration and traction force generation. Biophys. J. 86:2558-2565.
57. Chen, J., B. Fabry, E. L. Schiffrin, and N. Wang. 2001. Twisting integrin receptors increases endothelin-1 gene expression in endothelial cells. Am. J. Physiol. Cell Physiol. 280:C1475-C1484.
58. Engler, A., L. Bacakova, C. Newman, A. Hategan, M. Griffin, and D. Discher. 2004. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86:617-628.
59. Paszek, M. J., N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozengberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, and others. 2005. Tensional homeostasis and the malignant phenotype. Cancer Cell. 8:241-254.
60. Beningo, K. A., M. Dembo, I. Kaverina, J. V. Small, and Y. L. Wang. 2001. Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153:881-887.
61. Numaguchi, Y., S. Huang, T. R. Polte, G. S. Eichler, N. Wang, and D. E. Ingber. 2003. Caldesmon-dependent switching between capillary endothelial cell growth and apoptosis through modulation of cell shape and contractility. Angiogenesis. 6:55-64.
62. Tolic-Norrelykke, I. M., L. Sacconi, G. Thon, and F. S. Pavone. 2004. Positioning and elongation of the fission yeast spindle by microtubule-based pushing. Curr. Biol. 14:1181-1186.
63. Khodjakov, A., S. La Terra, and F. Chang. 2004. Laser microsurgery in fission yeast: role of the mitotic spindle midzone in anaphase B. Curr. Biol. 14:1330-1340.
64. Watanabe, W., and N. Arakawa. 2004. Femtosecond laser disruption of subcellular organelles in a living cell. Opt. Express. 12:4203-4213.
65. Tirlapur, U. K., and K. Konig. 2002. Femtosecond near-infrared laser pulses as a versatile non-invasive tool for intra-tissue nanoprocessing in plants without compromising viability. Plant J. 31:365-374.
66. Finer, J. T., R. M. Simmons, and J. A. Spudich. 1994. Single myosin molecule mechanics - piconewton forces and nanometer steps. Nature. 368:113-119.
67. Ishii, Y., A. Ishijima, and T. Yanagida. 2001. Single molecule nanomanipulation of biomolecules. Trends Biotechnol. 19:211-216.
68. Kojima, H., A. Ishijima, and T. Yanagida. 1994. Direct measurement of stiffness of single actin-filaments with and without tropomyosin by in-vitro nanomanipulation. Proc. Natl. Acad. Sci. USA. 91:12962-12966.
69. Liu, X. M., and G. H. Pollack. 2002. Mechanics of f-actin characterized with microfabricated cantilevers. Biophys. J. 83:2705-2715.
70. Gardel, M. L., J. H. Shin, F. C. MacKintosh, L. Mahadevan, P. Matsudaira, and D. A. Weitz. 2004. Elastic behavior of cross-linked and bundled actin networks. Science. 304:1301-1305.
71. Linke, W. A., and M. C. Leake. 2004. Multiple sources of passive stress relaxation in muscle fibres. Phys. Med. Biol. 49:3613-3627.
72. Opitz, C. A., M. Kulke, M. C. Leake, C. Neagoe, H. Hinssen, R. J. Hajjar, and W. A. Linke. 2003. Damped elastic recoil of the titin spring in myofibrils of human myocardium. Proc. Natl. Acad. Sci. USA. 100:12688-12693.
73. Cortes, P., M. Mendez, B. L. Riser, C. J. Guerin, A. Rodriguez-Barbero, C. Hassett, and J. Yee. 2000. F-actin fiber distribution in glomerular cells: structural and functional implications. Kidney Int. 58:2452-2461.
74. Satcher, R. L., and C. F. Dewey. 1996. Theoretical estimates of mechanical properties of the endothelial cell cytoskeleton. Biophys. J. 71:109-118.
75. Lo, C. M., H. B. Wang, M. Dembo, and Y. L. Wang. 2000. Cell movement is guided by the rigidity of the substrate. Biophys. J. 79:144-152.
76. Lele, T. P., J. Pendse, S. Kumar, M. Salanga, J. Karavitis, and D. E. Ingber. 2005. Mechanical forces alter zyxin unbinding kinetics within focal adhesions of living cells. J. Cell. Physiol. In press.
77. 2+ sensitivity in the bovine middle cerebral artery. Br. J. Pharmacol. 140:871-880.
78. Nobe, H., K. Nobe, F. Fazal, P. deLanerolle, and R. J. Paul. 2003. Rho kinase mediates serum-induced contraction in fibroblast fibers independent of myosin lc20 phosphorylation. Am. J. Physiol. Cell Physiol. 284:C599-C606.
79. Kureishi, Y., S. Kobayashi, M. Amano, K. Kimura, H. Kanaide, T. Nakano, K. Kaibuchi, and M. Ito. 1997. Rho-associated kinase directly induces smooth muscle contraction through myosin light chain phosphorylation. J. Biol. Chem. 272:12257-12260.
80. Dudek, S. M., and J. G. Garcia. 2001. Cytoskeletal regulation of pulmonary vascular permeability. J. Appl. Physiol. 91:1487-1500.
81. Totsukawa, G., Y. Yamakita, S. Yamashiro, D. J. Hartshorne, Y. Sasaki, and F. Matsumura. 2000. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150:797-806.
82. Kaunas, R., P. Nguyen, S. Usami, and S. Chien. 2005. Cooperative effects of Rho and mechanical stretch on stress fiber organization. Proc. Natl. Acad. Sci. USA. 102:15895-15900.
83. Marek, L. F., R. O. Kelley, and B. D. Perdue. 1982. Organization of the cytoskeleton in square fibroblasts. Cell Motil. Cytoskeleton. 2:115-130.
84. Seifert, G. J., D. Lawson, and G. Wiche. 1992. Immunolocalization of the intermediate filament-associated protein plectin at focal contacts and actin stress fibers. Eur. J. Cell Biol. 59:138-147.
85. Peterson, L. J., Z. Rajfur, A. S. Maddox, C. D. Freel, Y. Chen, M. Edlund, C. Otey, and K. Burridge. 2004. Simultaneous stretching and contraction of stress fibers in vivo. Mol. Biol. Cell. 15:3497-3508.
86. Maniotis, A. J., C. S. Chen, and D. E. Ingber. 1997. Demonstration of mechanical connections between integrins cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA. 94:849-854.
87. Helmke, B. P., A. B. Rosen, and P. F. Davies. 2003. Mapping mechanical strain of an endogenous cytoskeletal network in living endothelial cells. Biophys. J. 84:2691-2699.
88. Choquet, D., D. P. Felsenfeld, and M. P. Sheetz. 1997. Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell. 88:39-48.
89. Engler, A., L. Bacakova, C. Newman, A. Hategan, M. Griffin, and D. Discher. 2004. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86:617-628.
90. Pelham, R. J., and Y. L. Wang. 1997. Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA. 94:13661-13665.
91. Moore, K. A., T. Polte, S. Huang, B. Shi, E. Alsberg, M. E. Sunday, and D. E. Ingber. 2005. Control of basement membrane remodeling and epithelial branching morphogenesis in embryonic lung by Rho and cytoskeletal tension. Dev. Dyn. 232:268-281.
92. Hayes, A. J., M. Benjamin, and J. R. Ralphs. 1999. Role of actin stress fibres in the development of the intervertebral disc: cytoskeletal control of extracellular matrix assembly. Dev. Dyn. 215:179-189.