Molecular mechanism of vinculin activation and nanoscale spatial organization in focal adhesions

Nature Cell Biology

Volumn 17, Issue 7, 2015, Pages 880-892

  Case, Lindsay B ^a   Baird, Michelle A ^b   Shtengel, Gleb ^c   Campbell, Sharon L ^d   Hess, Harald F ^c   Davidson, Michael W ^b   Waterman, Clare M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b FLORIDA STATE UNIVERSITY   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; MYOSIN II; PAXILLIN; VINCULIN; INTEGRIN; NANOMATERIAL; PHOTOPROTEIN; PROTEIN BINDING; TALIN;

ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; FOCAL ADHESION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; CELL LINE; CHEMISTRY; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; GENETICS; HUMAN; METABOLISM; MOLECULAR MODEL; MUTATION; NANOTECHNOLOGY; PROCEDURES; PROTEIN TERTIARY STRUCTURE; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING;

ACTINS; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; FLUORESCENCE RESONANCE ENERGY TRANSFER; FOCAL ADHESIONS; HUMANS; INTEGRINS; LUMINESCENT PROTEINS; MICROSCOPY, FLUORESCENCE; MODELS, MOLECULAR; MUTATION; NANOSTRUCTURES; NANOTECHNOLOGY; PAXILLIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA INTERFERENCE; TALIN; VINCULIN;

EID: 84934280727     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb3180     Document Type: Article

References (53)

1. Kuo, J-C. C., Han, X., Hsiao, C-T. T., Yates Iii, J. R., Waterman, C. M. Analysis of the myosin-II-responsive focal adhesion proteome reveals a role for-Pix in negative regulation of focal adhesion maturation. Nat. Cell Biol. 13, 383-393 (2011).
2. Byron, A., Humphries, J. D., Bass, M. D., Knight, D., Humphries, M. J. Proteomic analysis of integrin adhesion complexes. Sci. Signal. 4, pt2 (2011).
3. Schiller, H. B., Friedel, C. C., Boulegue, C., Fässler, R. Quantitative proteomics of the integrin adhesome show a myosin II-dependent recruitment of LIM domain proteins. EMBO Rep. 12, 259-266 (2011).
4. Kanchanawong, P. et al. Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584 (2010).
5. Choi, C. K. et al. Actin and-actinin orchestrate the assembly and maturation of nascent adhesions in a myosin II motor-independent manner. Nat. Cell Biol. 10, 1039-1050 (2008).
6. Zaidel-Bar, R., Ballestrem, C., Kam, Z., Geiger, B. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J. Cell Sci. 116, 4605-4613 (2003).
7. 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).
8. Zamir, E. et al. Molecular diversity of cell-matrix adhesions. J. Cell Sci. 112, 1655-1669 (1999).
9. Wolfenson, H. et al. A role for the juxtamembrane cytoplasm in the molecular dynamics of focal adhesions. PLoS ONE 4, e4304 (2009).
10. Diez, G., Auernheimer, V., Fabry, B., Goldmann, W. H. Head/tail interaction of vinculin influences cell mechanical behavior. Biochem. Biophys. Res. Commun. 406, 85-88 (2011).
11. Dumbauld, D. W. et al. How vinculin regulates force transmission. Proc. Natl Acad. Sci. USA 110, 9788-9793 (2013).
12. Saunders, R. M. et al. Role of vinculin in regulating focal adhesion turnover. Eur. J. Cell Biol. 85, 487-500 (2006).
13. Humphries, J. D. et al. Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043-1057 (2007).
14. Carisey, A. et al. Vinculin regulates the recruitment and release of core focal adhesion proteins in a force-dependent manner. Curr. Biol. 23, 271-281 (2013).
15. Plotnikov, S. V., Pasapera, A. M., Sabass, B., Waterman, C. M. Force fluctuations within focal adhesions mediate ECM-rigidity sensing to guide directed cell migration. Cell 151, 1513-1527 (2012).
16. Thievessen, I. et al. Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J. Cell Biol. 202, 163-177 (2013).
17. Subauste, M. C. et al. Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility. J. Cell Biol. 165, 371-381 (2004).
18. Burridge, K., Mangeat, P. An interaction between vinculin and talin. Nature 308, 744-746 (1984).
19. Jockusch, B. M., Isenberg, G. Interaction of-actinin and vinculin with actin: opposite effects on filament network formation. Proc. Natl Acad. Sci. USA 78, 3005-3009 (1981).
20. Turner, C. E., Glenney, J. R., Burridge, K. Paxillin: a new vinculin-binding protein present in focal adhesions. J. Cell Biol. 111, 1059-1068 (1990).
21. Gilmore, A. P., Burridge, K. Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381, 531-535 (1996).
22. DeMali, K. A., Barlow, C. A., Burridge, K. Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion. J. Cell Biol. 159, 881-891 (2002).
23. Kioka, N. et al. Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organization. J. Cell Biol. 144, 59-69 (1999).
24. Johnson, R. P., Craig, S. W. An intramolecular association between the head and tail domains of vinculin modulates talin binding. J. Biol. Chem. 269, 12611-12619 (1994).
25. Johnson, R. P., Craig, S. W. F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature 373, 261-264 (1995).
26. Chen, H., Choudhury, D. M., Craig, S. W. Coincidence of actin filaments and talin is required to activate vinculin. J. Biol. Chem. 281, 40389-40398 (2006).
27. Calderwood, D. A. et al. The talin head domain binds to integrin subunit cytoplasmic tails and regulates integrin activation. J. Biol. Chem. 274, 28071-28074 (1999).
28. Goldmann, W. H. et al. Examining F-actin interaction with intact talin and talin head and tail fragment using static and dynamic light scattering. Eur. J. Biochem. 250, 447-450 (1997).
29. Critchley, D. R. Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annu. Rev. Biophys. 38, 235-254 (2009).
30. Rubashkin, M. G. et al. Force engages vinculin and promotes tumor progression by enhancing PI3K activation of phosphatidylinositol (3, 4, 5)-triphosphate. Cancer Res. 74, 4597-4611 (2014).
31. Bakolitsa, C. et al. Structural basis for vinculin activation at sites of cell adhesion. Nature 430, 583-586 (2004).
32. Cohen, D. M., Chen, H., Johnson, R. P., Choudhury, B., Craig, S. W. Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J. Biol. Chem. 280, 17109-17117 (2005).
33. Cohen, D. M., Kutscher, B., Chen, H., Murphy, D. B., Craig, S. W. A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions. J. Biol. Chem. 281, 16006-16015 (2006).
34. Ciobanasu, C., Faivre, B., Le Clainche, C. Actomyosin-dependent formation of the mechanosensitive talin-vinculin complex reinforces actin anchoring. Nat. Commun. 5, 3095 (2014).
35. Del Rio, A. et al. Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641 (2009).
36. Chen, H., Cohen, D. M., Choudhury, D. M., Kioka, N., Craig, S. W. Spatial distribution and functional significance of activated vinculin in living cells. J. Cell Biol. 169, 459-470 (2005).
37. Shaner, N. C. et al. A bright monomeric green fluorescent protein derived from Branchiostoma lanceolatum. Nat. Methods 10, 407-409 (2013).
38. Pasapera, A. M., Schneider, I. C., Rericha, E., Schlaepfer, D. D., Waterman, C. M. Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation. J. Cell Biol. 188, 877-890 (2010).
39. Brown, M. C., Perrotta, J. A., Turner, C. E. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135, 1109-1023 (1996).
40. Thompson, P. M. et al. Identification of an actin binding surface on vinculin that mediates mechanical cell and focal adhesion properties. Structure 22, 697-706 (2014).
41. Gardel, M. L. et al. Traction stress in focal adhesions correlates biphasically with actin retrograde flow speed. J. Cell Biol. 183, 999-1005 (2008).
42. Bachir, A. I. et al. Integrin-associated complexes form hierarchically with variable stoichiometry in nascent adhesions. Curr. Biol. 24, 1845-1853 (2014).
43. Wolfenson, H., Bershadsky, A., Henis, Y. I., Geiger, B. Actomyosin-generated tension controls the molecular kinetics of focal adhesions. J. Cell Sci. 124, 1425-1432 (2011).
44. Schneider, I. C., Hays, C. K., Waterman, C. M. Epidermal growth factorinduced contraction regulates paxillin phosphorylation to temporally separate traction generation from de-adhesion. Mol. Biol. Cell 20, 3155-3167 (2009).
45. Tadokoro, S. et al. Talin binding to integrin-tails: a final common step in integrin activation. Science 302, 103-106 (2003).
46. Astrof, N. S., Salas, A., Shimaoka, M., Chen, J., Springer, T. A. Importance of force linkage in mechanochemistry of adhesion receptors. Biochemistry 45, 15020-15028 (2006).
47. Jiang, G., Giannone, G., Critchley, D. R., Fukumoto, E., Sheetz, M. P. Twopiconewton slip bond between fibronectin and the cytoskeleton depends on talin. Nature 424, 334-337 (2003).
48. Friedland, J. C., Lee, M. H., Boettiger, D. Mechanically activated integrin switch controls-5-1 function. Science 323, 642-644 (2009).
49. Yao, M. et al. Mechanical activation of vinculin binding to talin locks talin in an unfolded conformation. Sci. Rep. 4, 4610 (2014).
50. Hoffmann, J-E., Fermin, Y., Stricker, R. L., Ickstadt, K., Zamir, E. Symmetric exchange of multi-protein building blocks between stationary focal adhesions and the cytosol. eLife 3, e02257-e02257 (2014).
51. Shin, W. et al. in Live Cell Imaging: A Laboratory Manual (eds Goldman, R., Swedlow, J., Spector, D.) 2nd edn (Cold Spring Harbor Press, 2010).
52. Thévenaz, P., Ruttimann, U. E., Unser, M. A pyramid approach to subpixel registration based on intensity. IEEE Trans. Image Process. 7, 27-41 (1998).
53. Shtengel, G. et al. Imaging cellular ultrastructure by PALM, iPALM, and correlative iPALM-EM. Methods Cell Biol. 123, 273-294 (2014).