Mapping cell-matrix stresses during stretch reveals inelastic reorganization of the cytoskeleton

Biophysical Journal

Volumn 95, Issue 1, 2008, Pages 464-471

  Gavara, Núria ^a   Roca Cusachs, Pere ^a   Sunyer, Raimon ^a   Farré, Ramon ^a,b   Navajas, Daniel ^a,b,c,d  

^a UNIVERSITY OF BARCELONA   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c INSTITUTE FOR BIOENGINEERING OF CATALONIA IBEC   (Spain)

^d UNIVERSITY OF BARCELONA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BIOLOGICAL MODEL; CELL LINE; COMPUTER SIMULATION; CYTOSKELETON; ELASTICITY; EPITHELIUM CELL; EXTRACELLULAR MATRIX; HUMAN; MECHANICAL STRESS; MECHANOTRANSDUCTION; PHYSIOLOGY;

CELL LINE; COMPUTER SIMULATION; CYTOSKELETON; ELASTICITY; EPITHELIAL CELLS; EXTRACELLULAR MATRIX; HUMANS; MECHANOTRANSDUCTION, CELLULAR; MODELS, BIOLOGICAL; STRESS, MECHANICAL;

EID: 46749108441     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1529/biophysj.107.124180     Document Type: Article

References (40)

1. Chicurel, M. E., C. S. Chen, and D. E. Ingber. 1998. Cellular control lies in the balance of forces. Curr. Opin. Cell Biol. 10:232-239.
2. Janmey, P. A. 1998. The cytoskeleton and cell signaling: component localization and mechanical coupling. Physiol. Rev. 78:763-781.
3. Huang, S., and D. E. Ingber. 1999. The structural and mechanical complexity of cell-growth control. Nat. Cell Biol. 1:E131-E138.
4. Ingber, D. E. 2006. Cellular mechanotransduction: putting all the pieces together again. FASEB J. 20:811-827.
5. Vogel, V., and M. P. Sheetz. 2006. Local force and geometry sensing regulate cell functions. Nat. Rev. Mol. Cell Biol. 7:265-275.
6. Ingber, D. E. 2003. Tensegrity I. Cell structure and hierarchical systems biology. J. Cell Sci. 116:1157-1173.
7. Bausch, A. R., and K. Kroy. 2006. A bottom-up approach to cell mechanics. Nat. Phys. 2:231-238.
8. An, S. S., R. E. Laudadio, J. Lai, R. A. Rogers, and J. J. Fredberg. 2002. Stiffness changes in cultured airway smooth muscle cells. Am. J. Physiol. Cell Physiol. 283:C792-C801.
9. Sylvester, J. T. 2004. The tone of pulmonary smooth muscle: ROK and Rho music? Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L624-L630.
10. Wang, N., J. P. Butler, and D. E. Ingber. 1993. Mechanotransduction across the cell surface and through the cytoskeleton. Science. 260: 1124-1127.
11. 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. 153:1175-1186.
12. Yoshigi, M., E. B. Clark, and H. J. Yost. 2003. Quantification of stretch-induced cytoskeletal remodeling in vascular endothelial cells by image processing. Cytometry A. 55:109-118.
13. Mack, P. J., M. R. Kaazempur-Mofrad, H. Karcher, R. T. Lee, and R. D. Kamm. 2004. Force-induced focal adhesion translocation: effects of force amplitude and frequency. Am. J. Physiol. Cell Physiol. 287: C954-C962.
14. 2+ entry. J. Cell Sci. 117:85-92.
15. Sniadecki, N. J., A. Anguelouch, M. T. Yang, C. M. Lamb, Z. Liu, S. B. Kirschner, Y. Liu, D. H. Reich, and C. S. Chen. 2007. Magnetic microposts as an approach to apply forces to living cells. Proc. Natl. Acad. Sci. USA. 104:14553-14558.
16. 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.
17. Storm, C., J. J. Pastore, F. C. MacKintosh, T. C. Lubensky, and P. A. Janmey. 2005. Nonlinear elasticity in biological gels. Nature. 435: 191-194.
18. Gardel, M. L., F. Nakamura, J. H. Hartwig, J. C. Crocker, T. P. Stossel, and D. A. Weitz. 2006. Prestressed F-actin networks cross-linked by hinged filamins replicate mechanical properties of cells. Proc. Natl. Acad. Sci. USA. 103:1762-1767.
19. Pourati, J., A. Maniotis, D. Spiegel, J. L. Schaffer, J. P. Butler, J. J. Fredberg, D. E. Ingber, D. Stamenovic, and N. Wang. 1998. Is cytoskeletal tension a major determinant of cell deformability in adherent endothelial cells? Am. J. Physiol. 274:C1283-C1289.
20. Trepat, X., M. Grabulosa, F. Puig, G. N. Maksym, D. Navajas, and R. Farre. 2004. Viscoelasticity of human alveolar epithelial cells subjected to stretch. Am. J. Physiol. Lung Cell. Mol. Physiol. 287:L1025-L1034.
21. Fernandez, P., P. A. Pullarkat, and A. Ott. 2006. A master relation defines the nonlinear viscoelasticity of single fibroblasts. Biophys. J. 90:3796-3805.
22. Matthews, B. D., D. R. Overby, R. Mannix, and D. E. Ingber. 2006. Cellular adaptation to mechanical stress: role of integrins, Rho, cytoskeletal tension and mechanosensitive ion channels. J. Cell Sci. 119:508-518.
23. Rosenblatt, N., S. Hu, B. Suki, N. Wang, and D. Stamenovic. 2007. Contributions of the active and passive components of the cytoskeletal prestress to stiffening of airway smooth muscle cells. Ann. Biomed. Eng. 35:224-234.
24. Trepat, X., L. Deng, S. S. An, D. Navajas, D. J. Tschumperlin, W. T. Gerthoffer, J. P. Butler, and J. J. Fredberg. 2007. Universal physical responses to stretch in the living cell. Nature. 447:592-595.
25. 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.
26. Dembo, M., and Y. L. Wang. 1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307-2316.
27. Tolic-Norrelykke, I. M., J. P. Butler, J. Chen, and N. Wang. 2002. Spatial and temporal traction response in human airway smooth muscle cells. Am. J. Physiol. Cell Physiol. 283:C1254-C1266.
28. Gavara, N., R. Sunyer, P. Roca-Cusachs, R. Farre, M. Rotger, and D. Navajas. 2006. Thrombin-induced contraction in alveolar epithelial cells probed by traction microscopy. J. Appl. Physiol. 101:512-520.
29. Alcaraz, J., L. Buscemi, M. Grabulosa, X. Trepat, B. Fabry, R. Farre, and D. Navajas. 2003. Microrheology of human lung epithelial cells measured by atomic force microscopy. Biophys. J. 84:2071-2079.
30. Burnham, N. A., X. Chen, C. S. Hodges, G. A. Matei, E. J. Thoreson, C. J. Roberts, M. C. Davis, and S. J. B. Tendler. 2003. Comparison of calibration methods for atomic-force microscopy cantilevers. Nanotechnology. 14:1-6.
31. Rico, F., P. Roca-Cusachs, N. Gavara, R. Farre, M. Rotger, and D. Navajas. 2005. Probing mechanical properties of living cells by atomic force microscopy with blunted pyramidal cantilever tips. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 72:021914.
32. Marganski, W. A., V. M. De Biase, M. L. Burgess, and M. Dembo. 2003. Demonstration of altered fibroblast contractile activity in hypertensive heart disease. Cardiovasc. Res. 60:547-556.
33. Hirshman, C. A., H. Togashi, D. Shao, and C. W. Emala. 1998. Gi-2 is required for carbachol-induced stress fiber formation in human airway smooth muscle cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 275: L911-L916.
34. Yuan, H., S. Kononov, F. S. Cavalcante, K. R. Lutchen, E. P. Ingenito, and B. Suki. 2000. Effects of collagenase and elastase on the mechanical properties of lung tissue strips. J. Appl. Physiol. 89:3-14.
35. Sheetz, M. P. 2001. Cell control by membrane-cytoskeleton adhesion. Nat. Rev. Mol. Cell Biol. 2:392-396.
36. Yap, B., and R. D. Kamm. 2005. Cytoskeletal remodeling and cellular activation during deformation of neutrophils into narrow channels. J. Appl. Physiol. 99:2323-2330.
37. Costa, K. D., W. J. Hucker, and F. C. Yin. 2002. Buckling of actin stress fibers: a new wrinkle in the cytoskeletal tapestry. Cell Motil. Cytoskeleton. 52:266-274.
38. Trepat, X., F. Puig, N. Gavara, J. J. Fredberg, R. Farre, and D. Navajas. 2006. Effect of stretch on structural integrity and micromechanics of human alveolar epithelial cell monolayers exposed to thrombin. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L1104-L1110.
39. Wang, N., I. M. Tolic-Norrelykke, J. 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.
40. Sawada, Y., M. Tamada, B. J. Dubin-Thaler, O. Cherniavskaya, R. Sakai, S. Tanaka, and M. P. Sheetz. 2006. Force sensing by mechanical extension of the Src family kinase substrate p130Cas. Cell. 127: 1015-1026.