Traction stresses and translational distortion of the nucleus during fibroblast migration on a physiologically relevant ECM mimic

Biophysical Journal

Volumn 96, Issue 10, 2009, Pages 4286-4298

  Pan, Zhi ^a   Ghosh, Kaustabh ^b   Liu, Yajie ^a   Clark, Richard A F ^b   Rafailovich, Miriam H ^a  

^a USA   (United States)

^b Stony Brook University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CELL CULTURE; CELL MIGRATION; CELL SURFACE; EXTRACELLULAR MATRIX; FEMALE; FIBROBLAST; HUMAN; HUMAN CELL; MOLECULAR DYNAMICS; ADULT; ANIMAL; BIOMIMETICS; CELL MOTION; CELL NUCLEUS; CHEMISTRY; CYTOLOGY; MECHANICAL STRESS; METABOLISM; MOVEMENT (PHYSIOLOGY); PROTEIN TERTIARY STRUCTURE; SURFACE PROPERTY;

FIBRONECTIN; HYALURONIC ACID; LIGAND; THIOL DERIVATIVE;

ADULT; ANIMALS; BIOMIMETICS; CELL MOVEMENT; CELL NUCLEUS; EXTRACELLULAR MATRIX; FEMALE; FIBROBLASTS; FIBRONECTINS; HUMANS; HYALURONIC ACID; LIGANDS; MOVEMENT; PROTEIN STRUCTURE, TERTIARY; STRESS, MECHANICAL; SULFHYDRYL COMPOUNDS; SURFACE PROPERTIES;

EID: 68049148544     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.02.039     Document Type: Article

References (31)

1. Lauffenburger, D., and A. Horwitz. 1996. Cell migration: a physically integrated molecular process. Cell. 84:359-369.
2. Mitchison, T., and L. Cramer. 1996. Actin-based cell motility and cell locomotion. Cell. 84:371-379.
3. Sheetz, M., D. Felsenfeld, and C. Galbraith. 1998. Cell migration: regulation of force on extracellular-matrix-integrin complexes. Trends Cell Biol. 8:51-54.
4. Geiger, B., and A. Bershadsky. 2001. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13:584-592.
5. Smilenov, L. B., A. Mikhailov, R. J. Pelham, E. E. Marcantonio, and G. G. Gundersen. 1999. Focal adhesion motility revealed in stationary fibroblasts. Science. 286:1172-1174.
6. Wehrle-Haller, B., and B. A. Imhof. 2003. Actin, microtubules and focal adhesion dynamics during cell migration. Int. J. Biochem. Cell Biol. 35:39-50.
7. Beningo, K., and Y. Wang. 2002. Flexible substrata for the detection of cellular traction forces. Trends Cell Biol. 12:79-84.
8. Dembo, M., T. Oliver, A. Ishihara, and K. Jacobson. 1996. Imaging the traction stresses exerted by locomoting cells with the elastic substratum method. Biophys. J. 70:2008-2022.
9. Dembo, M., and Y. Wang. 1999. Stresses at the cell-to-substrate interface during locomotion of fibroblasts. Biophys. J. 76:2307-2316.
10. Pelham, R., and Y. Wang. 1999. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol. Biol. Cell. 10:935-945.
11. Tan, J., J. Tien, D. Pirone, D. Gray, K. Bhadriraju, et al. 2003. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl. Acad. Sci. USA. 100:1484-1489.
12. Buguin, A., P. Chavrier, B. Ladoux, O. du Roure, A. Saez, et al. 2005. An array of microfabricated pillars to study cell migration. Med. Sci. (Paris). 21:765-767.
13. 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.
14. Munevar, S., Y. Wang, and M. Dembo. 2001. Distinct roles of frontal and rear cell-substrate adhesions in fibroblast migration. Mol. Biol. Cell. 12:3947-3954.
15. du Roure, O., A. Saez, A. Buguin, R. Austin, P. Chavrier, et al. 2005. Force mapping in epithelial cell migration. Proc. Natl. Acad. Sci. USA. 102:2390-2395.
16. Harris, A., P. Wild, and D. Stopak. 1980. Silicone-rubber substrata. New wrinkle in the study of cell locomotion. Science. 208:177-179.
17. Ghosh, K., Z. Pan, E. Guan, S. Ge, Y. Liu, et al. 2007. Cell adaptation to a physiologically relevant ECM mimic with different viscoelastic properties. Biomaterials. 28:671-679.
18. Ghosh, K., X. Ren, X. Shu, G. Prestwich, and R. Clark. 2006. Fibronectin functional domains coupled to hyaluronan stimulate adult human dermal fibroblast responses critical for wound healing. Tissue Eng. 12:601-613.
19. Palecek, S., J. Loftus, M. Ginsberg, D. Lauffenburger, and A. Horwitz. 1997. Integrin-ligand binding properties govern cell migration speed through cell-substratum adhesiveness. Nature. 385:537-540.
20. Engler, A., L. Bacakova, C. Newman, A. Hategan, M. Griffin, et al. 2004. Substrate compliance versus ligand density in cell on gel responses. Biophys. J. 86:617-628.
21. Ghosh, K., X. Shu, R. Mou, J. Lombardi, G. Prestwich, et al. 2005. Rheological characterization of in situ cross-linkable hyaluronan hydrogels. Biomacromolecules. 6:2857-2865.
22. Clark, R., J. An, D. Greiling, A. Khan, and J. Schwarzbauer. 2003. Fibroblast migration on fibronectin requires three distinct functional domains. J. Invest. Dermatol. 121:695-705.
23. Guan, E., S. Smilow, M. Rafailovich, and J. Sokolov. 2004. Determining the mechanical properties of rat skin with digital image speckle correlation. Dermatology. 208:112-119.
24. Munevar, S., Y. Wang, and M. Dembo. 2001. Traction force microscopy of migrating normal and H-ras transformed 3T3 fibroblasts. Biophys. J. 80:1744-1757.
25. Palecek, S., A. Huttenlocher, A. Horwitz, and D. Lauffenburger. 1998. Physical and biochemical regulation of integrin release during rear detachment of migrating cells. J. Cell Sci. 111:929-940.
26. Hautaniemi, S., S. Kharait, A. Iwabu, A. Wells, and D. A. Lauffenburger. 2005. Modeling of signal-response cascades using decision tree analysis. Bioinformatics. 21:2027-2035.
27. Dahl, K. N., A. J. Engler, J. D. Pajerowski, and D. E. Discher. 2005. Power-law rheology of isolated nuclei with deformation mapping of nuclear substructures. Biophys. J. 89:2855-2864.
28. Ingber, D. E. 2003. Mechanosensation through integrins: cells act locally but think globally. Proc. Natl. Acad. Sci. USA. 100:1472-1474.
29. Maniotis, A., C. Chen, and D. Ingber. 1997. Demonstration of mechanical connections between integrins cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure. Proc. Natl. Acad. Sci. USA. 94:849-854.
30. Ridley, A., M. Schwartz, K. Burridge, R. Firtel, M. Ginsberg, et al. 2003. Cell migration: integrating signals from front to back. Science. 302:1704-1709.
31. Ji, Y., K. Ghosh, X. Shu, B. Li, J. Sokolov, et al. 2006. Electrospun three-dimensional hyaluronic acid nanofibrous scaffolds. Biomaterials. 27:3782-3792.