The cytoskeletal protein α-catenin unfurls upon binding to vinculin

Journal of Biological Chemistry

Volumn 287, Issue 22, 2012, Pages 18492-18499

  Rangarajan, Erumbi S ^a   Izard, Tina ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN CYTOSKELETON; ADHERENS JUNCTIONS; BINDING DOMAIN; BINDING STUDIES; CELL-CELL CONTACT; CYTOPLASMIC TAIL; CYTOSKELETAL PROTEINS; DIMER FORMATION; F-ACTIN; FEED-FORWARD; MULTIFUNCTIONAL PROTEIN; VINCULIN;

GLYCOPROTEINS; STABILIZATION;

PROTEINS;

ALPHA CATENIN; CYTOSKELETON PROTEIN; DIMER; F ACTIN; VINCULIN;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE;

ALPHA CATENIN; AMINO ACID SEQUENCE; CHROMATOGRAPHY, GEL; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CRYSTALLIZATION; CYTOSKELETAL PROTEINS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SPECTROPHOTOMETRY, ULTRAVIOLET; VINCULIN;

EUKARYOTA;

EID: 84861562162     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.351023     Document Type: Article

References (56)

1. Braga, V. M., and Balda, M. S. (2004) Regulation of cell-cell adhesion. Semin. Cell Dev. Biol. 15, 631-632 (Pubitemid 39550242)
2. Pokutta, S., and Weis, W. I. (2002) The cytoplasmic face of cell contact sites. Curr. Opin. Struct. Biol. 12, 255-262 (Pubitemid 34327487)
3. Clevers, H. (2006) Wnt/β-Catenin signaling in development and disease. Cell 127, 469-480
4. Wahl, J. K., 3rd, Kim, Y. J., Cullen, J. M., Johnson, K. R., and Wheelock, M. J. (2003) N-cadherin-catenin complexes form prior to cleavage of the proregion and transport to the plasma membrane. J. Biol. Chem. 278, 17269-17276 (Pubitemid 36799609)
5. Haegel, H., Larue, L., Ohsugi, M., Fedorov, L., Herrenknecht, K., and Kemler, R. (1995) Lack of β-catenin affects mouse development at gastrulation. Development 121, 3529-3537 (Pubitemid 3000446)
6. Radice, G. L., Rayburn, H., Matsunami, H., Knudsen, K. A., Takeichi, M., and Hynes, R. O. (1997) Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78 (Pubitemid 27079635)
7. Brault, V., Moore, R., Kutsch, S., Ishibashi, M., Rowitch, D. H., McMahon, A. P., Sommer, L., Boussadia, O., and Kemler, R. (2001) Inactivation of the β-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (Pubitemid 32409648)
8. Huelsken, J., Vogel, R., Erdmann, B., Cotsarelis, G., and Birchmeier, W. (2001) β-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105, 533-545 (Pubitemid 32520858)
9. Pokutta, S., Drees, F., Takai, Y., Nelson, W. J., and Weis, W. I. (2002) Biochemical and structural definition of the l-afadin- and actin-binding sites of α-catenin. J. Biol. Chem. 277, 18868-18874 (Pubitemid 34952446)
10. Pappas, D. J., and Rimm, D. L. (2006) Direct interaction of the C-terminal domain of α-catenin and F-actin is necessary for stabilized cell-cell adhesion. Cell Commun. Adhes. 13, 151-170 (Pubitemid 44349318)
11. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J., and Weis, W. I. (2005) α-Catenin is a molecular switch that binds E-cadherin-β-catenin and regulates actin-filament assembly. Cell 123, 903-915 (Pubitemid 41721035)
12. Yamada, S., Pokutta, S., Drees, F., Weis, W. I., and Nelson, W. J. (2005) Deconstructing the cadherin-catenin-actin complex. Cell 123, 889-901 (Pubitemid 41721034)
13. Weis, W. I., and Nelson, W. J. (2006) Re-solving the cadherin- cateninactin conundrum. J. Biol. Chem. 281, 35593-35597
14. Pokutta, S., Drees, F., Yamada, S., Nelson, W. J., and Weis, W. I. (2008) Biochemical and structural analysis of α-catenin in cell-cell contacts. Biochem. Soc. Trans. 36, 141-147 (Pubitemid 351570583)
15. Abe, K., and Takeichi, M. (2008) EPLIN mediates linkage of the cadherin catenin complex to F-actin and stabilizes the circumferential actin belt. Proc. Natl. Acad. Sci. U.S.A. 105, 13-19
16. Weiss, E. E., Kroemker, M., Rüdiger, A. H., Jockusch, B. M., and Rüdiger, M. (1998) Vinculin is part of the cadherin-catenin junctional complex: complex formation between α-catenin and vinculin. J. Cell Biol. 141, 755-764 (Pubitemid 28217919)
17. Vasioukhin, V., Bauer, C., Yin, M., and Fuchs, E. (2000) Directed actin polymerization is the driving force for epithelial cell-cell adhesion. Cell 100, 209-219 (Pubitemid 30064909)
18. Maddugoda, M. P., Crampton, M. S., Shewan, A. M., and Yap, A. S. (2007) Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell-cell contacts in mammalian epithelial cells. J. Cell Biol. 178, 529-540 (Pubitemid 47196159)
19. 1(E)-Catenin is an actin-binding and -bundling protein mediating the attachment of F-actin to the membrane adhesion complex. Proc. Natl. Acad. Sci. U.S.A. 92, 8813-8817
20. Pokutta, S., and Weis, W. I. (2000) Structure of the dimerization and β-catenin-binding region of α-catenin. Mol. Cell 5, 533-543
21. Yang, J., Dokurno, P., Tonks, N. K., and Barford, D. (2001) Crystal structure of the M-fragment of α-catenin: implications for modulation of cell adhesion. EMBO J. 20, 3645-3656 (Pubitemid 32691776)
22. Izard, T., Evans, G., Borgon, R. A., Rush, C. L., Bricogne, G., and Bois, P. R. (2004) Vinculin activation by talin through helical bundle conversion. Nature 427, 171-175 (Pubitemid 38094959)
23. Borgon, R. A., Vonrhein, C., Bricogne, G., Bois, P. R., and Izard, T. (2004) Crystal structure of human vinculin. Structure 12, 1189-1197 (Pubitemid 38900761)
24. Ylänne, J., Scheffzek, K., Young, P., and Saraste, M. (2001) Crystal structure of the α-actinin rod reveals an extensive torsional twist. Structure 9, 597-604 (Pubitemid 32695584)
25. del Rio, A., Perez-Jimenez, R., Liu, R., Roca-Cusachs, P., Fernandez, J. M., and Sheetz, M. P. (2009) Stretching single talin rod molecules activates vinculin binding. Science 323, 638-641
26. Lecuit, T. (2010) α-Catenin mechanosensing for adherens junctions. Nat. Cell Biol. 12, 522-524
27. Park, H., Rangarajan, E. S., Sygusch, J., and Izard, T. (2010) Dramatic improvement of crystal quality for low-temperature-grown rabbit muscle aldolase. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 66, 595-600
28. Yogesha, S. D., Sharff, A., Bricogne, G., and Izard, T. (2011) Intermolecular versus intramolecular interactions of the vinculin binding site 33 of talin. Protein Sci. 20, 1471-1476
29. Vonrhein, C., Flensburg, C., Keller, P., Sharff, A., Smart, O., Paciorek, W., Womack, T., and Bricogne, G. (2011) Data processing and analysis with the autoPROC toolbox. Acta Crystallogr. D. Biol. Crystallogr. 67, 293-302
30. Kabsch, W. (1993) Automatic processing of rotation diffraction data from crystals of initially unknown symmetry and cell constants. J. Appl. Crystallogr. 26, 795-800
31. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr. D. Biol. Crystallogr. 62, 72-82
32. Nhieu, G. T., and Izard, T. (2007) Vinculin binding in its closed conformation by a helix addition mechanism. EMBO J. 26, 4588-4596
33. Vagin, A., and Teplyakov, A. (1997) MOLREP: an Automated Program for Molecular Replacement. J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
34. Bricogne, G., Blanc, E., Brandl, M., Flensburg, C., Keller, P., Paciorek, P., Roversi, P., Sharff, A., Smart, O. S., Vonrhein, C., and Womack, T. O. (2011) BUSTER, Global Phasing Ltd., Cambridge, UK
35. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D. Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
36. Folta-Stogniew, E., and Williams, K. R. (1999) Determination of molecular masses of proteins in solution: implementation of an HPLC size exclusion chromatography and laser light scattering service in a core laboratory. J. Biomol. Tech. 10, 51-63
37. Bois, P. R., O'Hara, B. P., Nietlispach, D., Kirkpatrick, J., and Izard, T. (2006) The vinculin binding sites of talin and α-actinin are sufficient to activate vinculin. J. Biol. Chem. 281, 7228-7236 (Pubitemid 43847490)
38. Imamura, Y., Itoh, M., Maeno, Y., Tsukita, S., and Nagafuchi, A. (1999) Functional domains of α-catenin required for the strong state of cadherin-based cell adhesion. J. Cell Biol. 144, 1311-1322 (Pubitemid 29157307)
39. 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 (Pubitemid 38998634)
40. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A., and Shibata, M. (2010) α-Catenin as a tension transducer that induces adherens junction development. Nat. Cell Biol. 12, 533-542
41. Peng, X., Maiers, J. L., Choudhury, D., Craig, S. W., and DeMali, K. A. (2012) α-Catenin uses a novel mechanism to activate vinculin. J. Biol.Chem. 287, 7728-7737
42. Kelley, L. A., and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4, 363-371
43. Matthews, B. W. (1968) Solvent content of protein crystals. J. Mol. Biol. 33, 491-497
44. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D. Biol. Crystallogr. 66, 12-21
45. Izard, T., and Vonrhein, C. (2004) Structural basis for amplifying vinculin activation by talin. J. Biol. Chem. 279, 27667-27678 (Pubitemid 38812608)
46. Gingras, A. R., Ziegler, W. H., Frank, R., Barsukov, I. L., Roberts, G. C., Critchley, D. R., and Emsley, J. (2005) Mapping and consensus sequence identification for multiple vinculin binding sites within the talin rod. J. Biol. Chem. 280, 37217-37224 (Pubitemid 41587806)
47. Fillingham, I., Gingras, A. R., Papagrigoriou, E., Patel, B., Emsley, J., Critchley, D. R., Roberts, G. C., and Barsukov, I. L. (2005) A vinculin binding domain from the talin rod unfolds to form a complex with the vinculin head. Structure 13, 65-74 (Pubitemid 40092475)
48. Yogesha, S. D., Rangarajan, E. S., Vonrhein, C., Bricogne, G., and Izard, T. (2012) Crystal structure of vinculin in complex with vinculin binding site 50 (VBS50), the integrin binding site 2 (IBS2) of talin. Protein Sci. 21, 583-588
49. Bois, P. R., Borgon, R. A., Vonrhein, C., and Izard, T. (2005) Structural dynamics of α-actinin-vinculin interactions. Mol. Cell. Biol. 25, 6112-6122
50. Izard, T., Tran Van Nhieu, G., and Bois, P. R. (2006) Shigella applies molecular mimicry to subvert vinculin and invade host cells. J. Cell Biol. 175, 465-475
51. Park, H., Valencia-Gallardo, C., Sharff, A., Tran Van Nhieu, G., and Izard, T. (2011) Novel vinculin binding site of the IpaA invasin of Shigella. J. Biol. Chem. 286, 23214-23221
52. Park, H., Lee, J. H., Gouin, E., Cossart, P., and Izard, T. (2011) The Rickettsia surface cell antigen 4 applies mimicry to bind to and activate vinculin. J. Biol. Chem. 286, 35096-35103
53. Benjamin, J. M., Kwiatkowski, A. V., Yang, C., Korobova, F., Pokutta, S., Svitkina, T., Weis, W. I., and Nelson, W. J. (2010) αE-Catenin regulates actin dynamics independently of cadherin-mediated cell-cell adhesion. J. Cell Biol. 189, 339-352
54. Janssen, M. E., 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 (Pubitemid 43099942)
55. Lawrence, M. C., and Colman, P. M. (1993) Shape complementarity at protein/protein interfaces. J. Mol. Biol. 234, 946-950 (Pubitemid 24027225)
56. 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 (Pubitemid 41389175)