Vinculin phosphorylation at residues Y100 and Y1065 is required for cellular force transmission

Journal of Cell Science

Volumn 128, Issue 18, 2015, Pages 3435-3443

  Auernheimer, Vera ^a   Lautscham, Lena A ^a   Leidenberger, Maria ^a   Friedrich, Oliver ^a   Kappes, Barbara ^a   Fabry, Ben ^a   Goldmann, Wolfgang H ^a  

^a UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Actin pulldown; Cell stiffness; Focal adhesion; FRAP; Mechanotransduction; Traction; Tyrosine phosphorylation; Vinculin

Indexed keywords

VINCULIN; INTEGRIN; PROTEIN TYROSINE KINASE;

ACTIN FILAMENT; ADHERENT CELL; ARTICLE; CELL SPREADING; CELLS; CYTOPLASM; FOCAL ADHESION; MECHANOTRANSDUCTION; MICROSCOPY; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE; ANIMAL; CELL ADHESION; CYTOSKELETON; ENERGY TRANSFER; FIBROBLAST; KNOCKOUT MOUSE; METABOLISM; MOUSE; PHYSIOLOGY; POINT MUTATION; PROTEIN SECONDARY STRUCTURE; ULTRASTRUCTURE;

ANIMALS; CELL ADHESION; CYTOSKELETON; ENERGY TRANSFER; FIBROBLASTS; INTEGRINS; MICE; MICE, KNOCKOUT; PHOSPHORYLATION; POINT MUTATION; PROTEIN STRUCTURE, SECONDARY; SRC-FAMILY KINASES; VINCULIN;

EID: 84946078409     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.172031     Document Type: Article

References (60)

1. Alenghat, F. J., Fabry, B., Tsai, K. Y., Goldmann, W. H. and Ingber, D. E. (2000). Analysis of cell mechanics in single vinculin-deficient cells using a magnetic tweezer. Biochem. Biophys. Res. Commun. 277, 93-99.
2. Auernheimer, V. and Goldmann, W. H. (2014). Serine phosphorylation on position 1033 of vinculin impacts cellular mechanics. Biochem. Biophys. Res. Commun. 450, 1095-1098.
3. Bakolitsa, C., Cohen, D. M., Bankston, L. A., Bobkov, A. A., Cadwell, G. W., Jennings, L., Critchley, D. R., Craig, S. W. and Liddington, R. C. (2004). Structural basis for vinculin activation at sites of cell adhesion. Nature 430, 583-586.
4. Bass, M. D., Patel, B., Barsukov, I. G., Fillingham, I. J., Mason, R., Smith, B. J., Bagshaw, C. R. and Critchley, D. R. (2002). Further characterization of the interaction between the cytoskeletal proteins talin and vinculin. Biochem. J. 362, 761-768.
5. Bays, J. L., Peng, X., Tolbert, C. E., Guilluy, C., Angell, A. E., Pan, Y., Superfine, R., Burridge, K. and DeMali, K. A. (2014). Vinculin phosphorylation differentially regulates mechanotransduction at cell-cell and cell-matrix adhesions. J. Cell Biol. 205, 251-263.
6. Beningo, K. A., Dembo, M., Kaverina, I., Small, J. V. and Wang, Y.-L. (2001). Nascent focal adhesions are responsible for the generation of strong propulsive forces in migrating fibroblasts. J. Cell Biol. 153, 881-888.
7. Bershadsky, A. D., Ballestrem, C., Carramusa, L., Zilberman, Y., Gilquin, B., Khochbin, S., Alexandrova, A. Y., Verkhovsky, A. B., Shemesh, T. and Kozlov, M. M. (2006). Assembly and mechanosensory function of focal adhesions: experiments and models. Eur. J. Cell Biol. 85, 165-173.
8. Bois, P. R. J., O'Hara, B. P., Nietlispach, D., Kirkpatrick, J. and Izard, T. (2006). The vinculin binding sites of talin and alpha-actinin are sufficient to activate vinculin. J. Biol. Chem. 281, 7228-7236.
9. Butler, J. P., Tolic-Norrelykke, I. M., Fabry, B. and Fredberg, J. J. (2002). Traction fields, moments, and strain energy that cells exert on their surroundings. Am. J. Physiol. Cell Physiol. 282, C595-C605.
10. Chandrasekar, I., Stradal, T. E. B., Holt, M. R., Entschladen, F., Jockusch, B. M. and Ziegler, W. H. (2005). Vinculin acts as a sensor in lipid regulation of adhesionsite turnover. J. Cell Sci. 118, 1461-1472.
11. Chen, X., Yang, Y., Wang, F., Chen, Y. and Xia, Y. (2005). Generation and evolution of quadratic dark spatial solitons using the wavefront modulation method. Opt. Expr. 13, 8699-8707.
12. Chen, H., Choudhury, D. M. and Craig, S. W. (2006). Coincidence of actin filaments and talin is required to activate vinculin. J. Biol. Chem. 281, 40389-40398.
13. Choquet, D., Felsenfeld, D. P. and Sheetz, M. P. (1997). Extracellular matrix rigidity causes strengthening of integrin-cytoskeleton linkages. Cell 88, 39-48.
14. Cohen, D. M., Chen, H., Johnson, R. P., Choudhury, B. and Craig, S. W. (2005). Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin. J. Biol. Chem. 280, 17109-17117.
15. Cohen, D. M., Kutscher, B., Chen, H., Murphy, D. B. and Craig, S. W. (2006). A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions. J. Biol. Chem. 281, 16006-16015.
16. Damsky, C. H., Knudsen, K. A., Bradley, D., Buck, C. A. and Horwitz, A. F. (1985). Distribution of the cell substratum attachment (CSAT) antigen on myogenic and fibroblastic cells in culture. J. Cell Biol. 100, 1528-1539.
17. Diez, G., Kollmannsberger, P., Mierke, C. T., Koch, T. M., Vali, H., Fabry, B. and Goldmann, W. H. (2009). Anchorage of vinculin to lipid membranes influences cell mechanical properties. Biophys. J. 97, 3105-3112.
18. Diez, G., Auernheimer, V., Fabry, B. and Goldmann, W. H. (2011). Head/tail interaction of vinculin influences cell mechanical behavior. Biochem. Biophys. Res. Commun. 406, 85-88.
19. Dumbauld, D. W., Lee, T. T., Singh, A., Scrimgeour, J., Gersbach, C. A., Zamir, E. A., Fu, J., Chen, C. S., Curtis, J. E., Craig, S. W. et al. (2013). How vinculin regulates force transmission. Proc. Natl. Acad. Sci. USA 110, 9788-9793.
20. Ezzell, R. M., Goldmann, W. H., Wang, N., Parashurama, N. and Ingber, D. E. (1997). Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231, 14-26.
21. Fabry, B., Maksym, G. N., Butler, J. P., Glogauer, M., Navajas, D. and Fredberg, J. J. (2001). Scaling the microrheology of living cells. Phys. Rev. Lett. 87, 148102.
22. Fabry, B., Klemm, A. H., Kienle, S., Schäffer, T. E. and Goldmann, W. H. (2011). Focal adhesion kinase stabilizes the cytoskeleton. Biophys. J. 101, 2131-2138.
23. Gallant, N. D., Michael, K. E. and Garcia, A. J. (2005). Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol. Biol. Cell 16, 4329-4340.
24. Goldmann, W. H. and Ezzell, R. M. (1996). Viscoelasticity in wild-type and vinculindeficient (5.51) mouse F9 embryonic carcinoma cells examined by atomic force microscopy and rheology. Exp. Cell Res. 226, 234-237.
25. Goldmann, W. H., Schindl, M., Cardozo, T. J. and Ezzell, R. M. (1995). Motility of vinculin-deficient F9 embryonic carcinoma cells analyzed by video, laser confocal, and reflection interference contrast microscopy. Exp. Cell Res. 221, 311-319.
26. Goldmann, W. H., Galneder, R., Ludwig, M., Xu, W., Adamson, E. D., Wang, N. and Ezzell, R. M. (1998). Differences in elasticity of vinculin-deficient F9 cells measured by magnetometry and atomic force microscopy. Exp. Cell Res. 239, 235-242.
27. Goldmann, W. H., Auernheimer, V., Thievessen, I. and Fabry, B. (2013). Vinculin, cell mechanics and tumour cell invasion. Cell Biol. Int. 37, 397-405.
28. Golji, J., Lam, J. and Mofrad, M. R. K. (2011). Vinculin activation is necessary for complete talin binding. Biophys. J. 100, 332-340.
29. Golji, J., Wendorff, T. and Mofrad, M. R. K. (2012). Phosphorylation primes vinculin for activation. Biophys. J. 102, 2022-2030.
30. Grashoff, C., Hoffman, B. D., Brenner, M. D., Zhou, R., Parsons, M., Yang, M. T., McLean, M. A., Sligar, S. G., Chen, C. S., Ha, T. et al. (2010). Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics. Nature 466, 263-266.
31. Harburger, D. S. and Calderwood, D. A. (2009). Integrin signalling at a glance. J. Cell Sci. 122, 159-163.
32. Hildebrandt, J. (1969). Comparison of mathematical models for cat lung and viscoelastic balloon derived by Laplace transform methods from pressure-volume data. Bull. Math. Biophy. 31, 651-667.
33. Huang, Y., Zhang, W. and Gunst, S. J. (2011). Activation of vinculin induced by cholinergic stimulation regulates contraction of tracheal smooth muscle tissue. J. Biol. Chem. 286, 3630-3644.
34. Huang, Y., Day, R. N. and Gunst, S. J. (2014). Vinculin phosphorylation at Tyr1065 regulates vinculin conformation and tension development in airway smooth muscle tissues. J. Biol. Chem. 289, 3677-3688.
35. Humphries, J. D., Wang, P., Streuli, C., Geiger, B., Humphries, M. J. and Ballestrem, C. (2007). Vinculin controls focal adhesion formation by direct interactions with talin and actin. J. Cell Biol. 179, 1043-1057.
36. Ito, S., Werth, D. K., Richert, N. D. and Pastan, I. (1983). Vinculin phosphorylation by the src kinase. Interaction of vinculin with phospholipid vesicles. J. Biol. Chem. 258, 14626-14631.
37. Izard, T. and Vonrhein, C. (2004). Structural basis for amplifying vinculin activation by talin. J. Biol. Chem. 279, 27667-27678.
38. Izard, T., Evans, G., Borgon, R. A., Rush, C. L., Bricogne, G. and Bois, P. R. J. (2004). Vinculin activation by talin through helical bundle conversion. Nature 427, 171-175.
39. Janssen, M. E. W., Kim, E., Liu, H., Fujimoto, L. M., Bobkov, A., Volkmann, N. and Hanein, D. (2006). Three-dimensional structure of vinculin bound to actin filaments. Mol. Cell 21, 271-281.
40. Jockusch, B. M. and Rüdiger, M. (1996). Crosstalk between cell adhesion molecules: vinculin as a paradigm for regulation by conformation. Trends Cell Biol. 6, 311-315.
41. Johnson, R. P. and Craig, S. W. (1995). F-actin binding site masked by the intramolecular association of vinculin head and tail domains. Nature 373, 261-264.
42. Kanchanawong, P., Shtengel, G., Pasapera, A. M., Ramko, E. B., Davidson, M. W., Hess, H. F. and Waterman, C. M. (2010). Nanoscale architecture of integrin-based cell adhesions. Nature 468, 580-584.
43. Kasza, K. E., Nakamura, F., Hu, S., Kollmannsberger, P., Bonakdar, N., Fabry, B., Stossel, T. P., Wang, N. and Weitz, D. A. (2009). Filamin A is essential for active cell stiffening but not passive stiffening under external force. Biophys. J. 96, 4326-4335.
44. Kollmannsberger, P. and Fabry, B. (2007). High-force magnetic tweezers with force feedback for biological applications. Rev. Sci. Instrum. 78, 114301.
45. Kollmannsberger, P., Mierke, C. T. and Fabry, B. (2011). Nonlinear viscoelasticity of adherent cells is controlled by cytoskeletal tension. Soft Matter 7, 3127-3132.
46. Küpper, K., Lang, N., Möhl, C., Kirchgessner, N., Born, S., Goldmann, W. H., Merkel, R. and Hoffmann, B. (2010). Tyrosine phosphorylation of vinculin at position 1065 modifies focal adhesion dynamics and cell tractions. Biochem. Biophys. Res. Commun. 399, 560-564.
47. Marg, S., Winkler, U., Sestu, M., Himmel, M., Schönherr, M., Bär, J., Mann, A., Moser, M., Mierke, C. T., Rottner, K. et al. (2010). The vinculin-DeltaIn20/21 mouse: characteristics of a constitutive, actin-binding deficient splice variant of vinculin. PLoS ONE 5, e11530.
48. Mierke, C. T., Kollmannsberger, P., Paranhos Zitterbart, D., Smith, J., Fabry, B. and Goldmann, W. H. (2008). Mechano-coupling and regulation of contractility by the vinculin tail domain. Biophys. J. 94, 661-670.
49. Mierke, C. T., Kollmannsberger, P., Zitterbart, D. P., Diez, G., Koch, T. M., Marg, S., Ziegler, W. H., Goldmann, W. H. and Fabry, B. (2010). Vinculin facilitates cell invasion into three-dimensional collagen matrices. J. Biol. Chem. 285, 13121-13130.
50. Moese, S., Selbach, M., Brinkmann, V., Karlas, A., Haimovich, B., Backert, S. and Meyer, T. F. (2007). The Helicobacter pylori CagA protein disrupts matrix adhesion of gastric epithelial cells by dephosphorylation of vinculin. Cell. Microbiol. 9, 1148-1161.
51. Pelham, R. J., Jr and Wang, Y.-L. (1997). Cell locomotion and focal adhesions are regulated by substrate flexibility. Proc. Natl. Acad. Sci. USA 94, 13661-13665.
52. Peng, X., Maiers, J. L., Choudhury, D., Craig, S. W. and DeMali, K. A. (2012). alpha-Catenin uses a novel mechanism to activate vinculin. J. Biol. Chem. 287, 7728-7737.
53. Riveline, D., Zamir, E., Balaban, N. Q., Schwarz, U. S., Ishizaki, T., Narumiya, S., Kam, Z., Geiger, B. and Bershadsky, A. D. (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.
54. Subauste, M. C., Pertz, O., Adamson, E. D., Turner, C. E., Junger, S. and Hahn, K. M. (2004). Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility. J. Cell Biol. 165, 371-381.
55. Thievessen, I., Thompson, P. M., Berlemont, S., Plevock, K. M., Plotnikov, S. V., Zemljic-Harpf, A., Ross, R. S., Davidson, M. W., Danuser, G., Campbell, S. L. et al. (2013). Vinculin-actin interaction couples actin retrograde flow to focal adhesions, but is dispensable for focal adhesion growth. J. Cell Biol. 202, 163-177.
56. Tolbert, C. E., Thompson, P. M., Superfine, R., Burridge, K. and Campbell, S. L. (2014). Phosphorylation at Y1065 in vinculin mediates actin bundling, cell spreading, and mechanical responses to force. Biochemistry 53, 5526-5536.
57. Wang, N., Tolic-Norrelykke, I. M., Chen, J., Mijailovich, S. M., Butler, J. P., Fredberg, J. J. and Stamenovic, D. (2002). Cell prestress. I. Stiffness and prestress are closely associated in adherent contractile cells. Am. J. Physiol. Cell Phsiol. 282, C606-C616.
58. Winkler, J., Lünsdorf, H. and Jockusch, B. M. (1996). The ultrastructure of chicken gizzard vinculin as visualized by high-resolution electron microscopy. J. Struct. Biol. 116, 270-277.
59. Zhang, Z., Izaguirre, G., Lin, S.-Y., Lee, H. Y., Schaefer, E. and Haimovich, B. (2004). The phosphorylation of vinculin on tyrosine residues 100 and 1065, mediated by SRC kinases, affects cell spreading. Mol. Biol. Cell 15, 4234-4247.
60. Ziegler, W. H., Liddington, R. C. and Critchley, D. R. (2006). The structure and regulation of vinculin. Trends Cell Biol. 16, 453-460.