Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics

Nature

Volumn 466, Issue 7303, 2010, Pages 263-266

  Grashoff, Carsten ^a,b   Hoffman, Brenton D ^a,b   Brenner, Michael D ^c,d   Zhou, Ruobo ^c   Parsons, Maddy ^e   Yang, Michael T ^f   McLean, Mark A ^d   Sligar, Stephen G ^d   Chen, Christopher S ^f   Ha, Taekjip ^c,d,g   Schwartz, Martin A ^a,b,h  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c University of Illinois at Urbana Champaign   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^h University of Virginia   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; F ACTIN; VINCULIN;

ADHESION; BIOCHEMISTRY; FLUORESCENCE SPECTROSCOPY; PATHOLOGY; PROTEIN; TENSION;

ACTIN FILAMENT; ARTICLE; BIOSENSOR; CYTOSKELETON; FLUORESCENCE; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESION; FORCE; MOLECULE; PRIORITY JOURNAL; REGULATORY MECHANISM; TENSION;

ANIMALS; BIOSENSING TECHNIQUES; CALIBRATION; CATTLE; CELL LINE; CELL MOVEMENT; FLUORESCENT DYES; FOCAL ADHESIONS; HUMANS; MICE; MICROSCOPY, CONFOCAL; MOVEMENT; OPTICAL TWEEZERS; SPECTROMETRY, FLUORESCENCE; STRESS, MECHANICAL; VINCULIN;

EID: 77954486800     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature09198     Document Type: Article

References (30)

1. Orr, A. W., Helmke, B. P., Blackman, B. R. & Schwartz, M. A. Mechanisms of mechanotransduction. Dev. Cell 10, 11-20 (2006).
2. Hohng, S. et al. Fluorescence-force spectroscopy maps two-dimensional reaction landscape of the Holliday junction. Science 318, 279-283 (2007).
3. Bershadsky, A. D., Balaban, N. Q. & Geiger, B. Adhesion-dependent cell mechanosensitivity. Annu. Rev. Cell Dev. Biol. 19, 677-695 (2003).
4. Ballestrem, C., Hinz, B., Imhof, B. A. & Wehrle-Haller, B. Marching at the front and dragging behind: differential aVb3-integrin turnover regulates focal adhesion behavior. J. Cell Biol. 155, 1319-1332 (2001).
5. Bakolitsa, C. et al. Structural basis for vinculin activation at sites of cell adhesion. Nature 430, 583-586 (2004).
6. Ziegler, W. H., Gingras, A. R., Critchley, D. R. & Emsley, J. Integrin connections to the cytoskeleton through talin and vinculin. Biochem. Soc. Trans. 36, 235-239 (2008).
7. Galbraith, C. G., Yamada, K. M. & Sheetz, M. P. The relationship between force and focal complex development. J. Cell Biol. 159, 695-705 (2002).
8. Riveline, D. et al. 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 (2001).
9. Xu, W., Baribault, H. & Adamson, E. D. Vinculin knockout results in heart and brain defects during embryonic development. Development 125, 327-337 (1998).
10. Alenghat, F. J. et al. Analysis of cell mechanics in single vinculin-deficient cells using a magnetic tweezer. Biochem. Biophys. Res. Commun. 277, 93-99 (2000).
11. Mierke, C. T. et al. Mechano-coupling and regulation of contractility by the vinculin tail domain. Biophys. J. 94, 661-670 (2008).
12. Hu, K. et al. Differential transmission of actin motion within focal adhesions. Science 315, 111-115 (2007).
13. Ji, L., Lim, J. & Danuser, G. Fluctuations of intracellular forces during cell protrusion. Nature Cell Biol. 10, 1393-1400 (2008).
14. Balaban, N. Q. et al. Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates. Nature Cell Biol. 3, 466-472 (2001).
15. Shemesh, T., Geiger, B., Bershadsky, A. D. & Kozlov, M. M. Focal adhesions as mechanosensors: a physical mechanism. Proc. Natl Acad. Sci. USA 102, 12383-12388 (2005).
16. Tan, J. L. et al. Cells lying on a bed of microneedles: an approach to isolate mechanical force. Proc. Natl Acad. Sci. USA 100, 1484-1489 (2003).
17. Meng, F., Suchyna, T. M. & Sachs, F. A fluorescence energy transfer-based mechanical stress sensor for specific proteins in situ. FEBS J. 275, 3072-3087 (2008).
18. Day, R. N., Booker, C. F. & Periasamy, A. Characterization of an improved donor fluorescent protein for Forster resonance energy transfer microscopy. J. Biomed. Opt. 13, 031203 (2008).
19. Becker, N. et al. Molecular nanosprings in spider capture-silk threads. Nature Mater. 2, 278-283 (2003).
20. Humphries, J. D. et al. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043-1057 (2007).
21. Chen, H. et al. Spatial distribution and functional significance of activated vinculin in living cells. J. Cell Biol. 169, 459-470 (2005).
22. Cohen, D. M. et al. A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions. J. Biol. Chem. 281, 16006-16015 (2006).
23. Parsons, M. et al. Quantification of integrin receptor agonism by fluorescence lifetime imaging. J. Cell Sci. 121, 265-271 (2008).
24. Cai, Y. et al. Nonmuscle myosin IIA-dependent force inhibits cell spreading and drives F-actin flow. Biophys. J. 91, 3907-3920 (2006).
25. Pertz, O., Hodgson, L., Klemke, R. L. & Hahn, K. M. Spatiotemporal dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072 (2006).
26. Kolega, J. Asymmetric distribution of myosin IIB in migrating endothelial cells is regulated by a rho-dependent kinase and contributes to tail retraction. Mol. Biol. Cell 14, 4745-4757 (2003).
27. Periasamy, A., Wallrabe, H., Chen, Y. & Barroso, M. Chapter 22: Quantitation of protein-protein interactions: confocal FRET microscopy. Methods Cell Biol. 89, 569-598 (2008).
28. Zamir, E. et al. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669 (1999).
29. Zaidel-Bar, R., Milo, R., Kam, Z. & Geiger, B. A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J. Cell Sci. 120, 137-148 (2007).
30. Crocker, J. C. & Hoffman, B. D. Multiple-particle tracking and two-point microrheology in cells. Methods Cell Biol. 83, 141-178 (2007).