Vinculin and metavinculin: Oligomerization and interactions with F-actin

FEBS Letters

Volumn 587, Issue 8, 2013, Pages 1220-1229

  Thompson, Peter M ^a,b   Tolbert, Caitlin E ^a   Campbell, Sharon L ^a,b  

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

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Actin; Metavinculin; Oligomerization; PIP2; Vinculin

Indexed keywords

F ACTIN; METAVINCULIN; OLIGOMER; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; VINCULIN;

DIMERIZATION; HUMAN; MOLECULAR MODEL; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MODEL; REVIEW; STRUCTURE ACTIVITY RELATION;

ACTIN CYTOSKELETON; ACTINS; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; VINCULIN;

EID: 84876026191     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2013.02.042     Document Type: Review

References (89)

1. B. Geiger A 130K protein from chicken gizzard: its localization at the termini of microfilament bundles in cultured chicken cells Cell 18 1979 193 205
2. X.A. Peng, E.S. Nelson, J.L. Maiers, and K.A. DeMali New insights into vinculin function and regulation Int. Rev. Cell Mol. Biol. 287 2011 191 231 http://dx.doi.org/10.1016/B978-0-12-386043-9.00005-0
3. W.H. Ziegler, R.C. Liddington, and D.R. Critchley The structure and regulation of vinculin Trends Cell Biol. 16 2006 453 460 10.1016/j.tcb.2006.07. 004
4. A. Carisey, and C. Ballestrem Vinculin, an adapter protein in control of cell adhesion signalling Eur. J. Cell Biol. 90 2011 157 163 10.1016/j.ejcb.2010. 06.007
5. J.T. Parsons, A.R. Horwitz, and M.A. Schwartz Cell adhesion: integrating cytoskeletal dynamics and cellular tension Nat. Rev. Mol. Cell Biol. 11 2010 633 643 10.1038/nrm2957
6. F. Twiss, Q. Le Duc, S. Van Der Horst, H. Tabdili, G. Van Der Krogt, N. Wang, H. Rehmann, S. Huveneers, D.E. Leckband, and J. De Rooij Vinculin-dependent cadherin mechanosensing regulates efficient epithelial barrier formation Biol. Open 1 2012 1128 1140 10.1242/bio.20122428
7. Q. le Duc, Q. Shi, I. Blonk, A. Sonnenberg, N. Wang, D. Leckband, and J. de Rooij Vinculin potentiates E-cadherin mechanosensing and is recruited to actin-anchored sites within adherens junctions in a myosin II-dependent manner J. Cell Biol. 189 2010 1107 1115 10.1083/jcb.201001149
8. M.P. Maddugoda, M.S. Crampton, A.M. Shewan, and A.S. Yap Myosin VI and vinculin cooperate during the morphogenesis of cadherin cell cell contacts in mammalian epithelial cells J. Cell Biol. 178 2007 529 540 10.1083/jcb.200612042
9. X. Peng, L.E. Cuff, C.D. Lawton, and K.A. DeMali Vinculin regulates cell-surface E-cadherin expression by binding to beta-catenin J. Cell Sci. 123 2010 567 577 10.1242/jcs.056432
10. W. Xu, H. Baribault, and E.D. Adamson Vinculin knockout results in heart and brain defects during embryonic development Development 125 1998 327 337
11. W. Xu, J.L. Coll, and E.D. Adamson Rescue of the mutant phenotype by reexpression of full-length vinculin in null F9 cells; effects on cell locomotion by domain deleted vinculin J. Cell Sci. 111 Pt 11 1998 1535 1544
12. A.E. Zemljic-Harpf, S. Ponrartana, R.T. Avalos, M.C. Jordan, K.P. Roos, N.D. Dalton, V.Q. Phan, E.D. Adamson, and R.S. Ross Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy Am. J. Pathol. 165 2004 1033 1044 10.1016/S0002-9440(10)63364-0
13. B.J. Byrne, Y.J. Kaczorowski, M.D. Coutu, and S.W. Craig Chicken vinculin and meta-vinculin are derived from a single gene by alternative splicing of a 207-base pair exon unique to meta-vinculin J. Biol. Chem. 267 1992 12845 12850
14. M. Maeda, E. Holder, B. Lowes, S. Valent, and R.D. Bies Dilated cardiomyopathy associated with deficiency of the cytoskeletal protein metavinculin Circulation 95 1997 17 20
15. T.M. Olson, S. Illenberger, N.Y. Kishimoto, S. Huttelmaier, M.T. Keating, and B.M. Jockusch Metavinculin mutations alter actin interaction in dilated cardiomyopathy Circulation 105 2002 431 437
16. J.L. Coll, A. Ben-Ze'ev, R.M. Ezzell, J.L. Rodriguez Fernandez, H. Baribault, R.G. Oshima, and E.D. Adamson Targeted disruption of vinculin genes in F9 and embryonic stem cells changes cell morphology, adhesion, and locomotion Proc. Natl. Acad. Sci. USA 92 1995 9161 9165
17. M.C. Subauste, O. Pertz, E.D. Adamson, C.E. Turner, S. Junger, and K.M. Hahn Vinculin modulation of paxillin-FAK interactions regulates ERK to control survival and motility J. Cell Biol. 165 2004 371 381 10.1083/jcb.200308011
18. C. Bakolitsa, D.M. Cohen, L.A. Bankston, A.A. Bobkov, G.W. Cadwell, L. Jennings, D.R. Critchley, S.W. Craig, and R.C. Liddington Structural basis for vinculin activation at sites of cell adhesion Nature 430 2004 583 586 10.1038/nature02610
19. J. Winkler, H. Lunsdorf, and B.M. Jockusch The ultrastructure of chicken gizzard vinculin as visualized by high-resolution electron microscopy J. Struct. Biol. 116 1996 270 277 http://dx.doi.org/10.1006/jsbi.1996.0042
20. R.P. Johnson, and S.W. Craig An intramolecular association between the head and tail domains of vinculin modulates talin binding J. Biol. Chem. 269 1994 12611 12619
21. E.E. Weiss, M. Kroemker, A.H. Rudiger, B.M. Jockusch, and M. Rudiger Vinculin is part of the cadherin-catenin junctional complex: complex formation between alpha-catenin and vinculin J. Cell Biol. 141 1998 755 764
22. M. Kroemker, A.H. Rudiger, B.M. Jockusch, and M. Rudiger Intramolecular interactions in vinculin control alpha-actinin binding to the vinculin head FEBS Lett. 355 1994 259 262
23. N.P. Brindle, M.R. Holt, J.E. Davies, C.J. Price, and D.R. Critchley The focal-adhesion vasodilator-stimulated phosphoprotein (VASP) binds to the proline-rich domain in vinculin Biochem. J. 318 Pt 3 1996 753 757
24. K. Mandai, H. Nakanishi, A. Satoh, K. Takahashi, K. Satoh, H. Nishioka, A. Mizoguchi, and Y. Takai Ponsin/SH3P12: an l-afadin- and vinculin-binding protein localized at cell-cell and cell-matrix adherens junctions J. Cell Biol. 144 1999 1001 1017
25. N. Kioka, S. Sakata, T. Kawauchi, T. Amachi, S.K. Akiyama, K. Okazaki, C. Yaen, K.M. Yamada, and S. Aota Vinexin: a novel vinculin-binding protein with multiple SH3 domains enhances actin cytoskeletal organization J. Cell Biol. 144 1999 59 69
26. K.A. DeMali, C.A. Barlow, and K. Burridge Recruitment of the Arp2/3 complex to vinculin: coupling membrane protrusion to matrix adhesion J. Cell Biol. 159 2002 881 891 10.1083/jcb.200206043
27. C.K. Wood, C.E. Turner, P. Jackson, and D.R. Critchley Characterisation of the paxillin-binding site and the C-terminal focal adhesion targeting sequence in vinculin J. Cell Sci. 107 Pt 2 1994 709 717
28. S. Huttelmaier, S. Illenberger, I. Grosheva, M. Rudiger, R.H. Singer, and B.M. Jockusch Raver1, a dual compartment protein, is a ligand for PTB/hnRNPI and microfilament attachment proteins J. Cell Biol. 155 2001 775 786 10.1083/jcb.200105044
29. R.P. Johnson, V. Niggli, P. Durrer, and S.W. Craig A conserved motif in the tail domain of vinculin mediates association with and insertion into acidic phospholipid bilayers Biochemistry 37 1998 10211 10222 10.1021/bi9727242
30. S. Huttelmaier, P. Bubeck, M. Rudiger, and B.M. Jockusch Characterization of two F-actin-binding and oligomerization sites in the cell-contact protein vinculin Eur. J. Biochem. 247 1997 1136 1142
31. C. Bakolitsa, J.M. de Pereda, C.R. Bagshaw, D.R. Critchley, and R.C. Liddington Crystal structure of the vinculin tail suggests a pathway for activation Cell 99 1999 603 613
32. T. Izard, G. Evans, R.A. Borgon, C.L. Rush, G. Bricogne, and P.R. Bois Vinculin activation by talin through helical bundle conversion Nature 427 2004 171 175 10.1038/nature02281
33. H. Chen, D.M. Choudhury, and S.W. Craig Coincidence of actin filaments and talin is required to activate vinculin J. Biol. Chem. 281 2006 40389 40398 10.1074/jbc.M607324200
34. C. Grashoff, B.D. Hoffman, M.D. Brenner, R. Zhou, M. Parsons, M.T. Yang, M.A. McLean, S.G. Sligar, C.S. Chen, and T. Ha Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466 2010 263 266 10.1038/nature09198
35. C.G. Galbraith, K.M. Yamada, and M.P. Sheetz The relationship between force and focal complex development J. Cell Biol. 159 2002 695 705 http://dx.doi.org/10.1083/jcb.200204153
36. G. Giannone, G. Jiang, D.H. Sutton, D.R. Critchley, and M.P. Sheetz Talin1 is critical for force-dependent reinforcement of initial integrin-cytoskeleton bonds but not tyrosine kinase activation J. Cell Biol. 163 2003 409 419 10.1083/jcb.200302001
37. D. Riveline, E. Zamir, N.Q. Balaban, U.S. Schwarz, T. Ishizaki, S. Narumiya, Z. Kam, B. Geiger, and A.D. Bershadsky 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 2001 1175 1185 http://dx.doi.org/10.1083/jcb.153.6.1175
38. C. Grashoff, B.D. Hoffman, M.D. Brenner, R.B. Zhou, M. Parsons, M.T. Yang, M.A. McLean, S.G. Sligar, C.S. Chen, and T. Ha Measuring mechanical tension across vinculin reveals regulation of focal adhesion dynamics Nature 466 2010 263-U143 http://dx.doi.org/10.1038/Nature09198
39. J. Golji, T. Wendorff, and M.R.K. Mofrad Phosphorylation primes vinculin for activation Biophys. J. 102 2012 2022 2030 http://dx.doi.org/10.1016/j.bpj. 2012.01.062
40. A.M. Belkin, O.I. Ornatsky, A.E. Kabakov, M.A. Glukhova, and V.E. Koteliansky Diversity of vinculin/meta-vinculin in human tissues and cultivated cells. Expression of muscle specific variants of vinculin in human aorta smooth muscle cells J. Biol. Chem. 263 1988 6631 6635
41. A.M. Belkin, O.I. Ornatsky, M.A. Glukhova, and V.E. Koteliansky Immunolocalization of meta-vinculin in human smooth and cardiac muscles J. Cell Biol. 107 1988 545 553
42. V.E. Koteliansky, E.P. Ogryzko, N.I. Zhidkova, P.A. Weller, D.R. Critchley, K. Vancompernolle, J. Vandekerckhove, P. Strasser, M. Way, and M. Gimona An additional exon in the human vinculin gene specifically encodes meta-vinculin-specific difference peptide. Cross-species comparison reveals variable and conserved motifs in the meta-vinculin insert Eur. J. Biochem. 205 1992 1218
43. F. Thoss, F. Dietrich, K. Punkt, S. Illenberger, K. Rottner, M. Himmel, and W.H. Ziegler Metavinculin: new insights into functional properties of a muscle adhesion protein Biochem. Biophys. Res. Commun. 430 2013 7 13 10.1016/j.bbrc.2012.11.013
44. S. Witt, A. Zieseniss, U. Fock, B.M. Jockusch, and S. Illenberger Comparative biochemical analysis suggests that vinculin and metavinculin cooperate in muscular adhesion sites J. Biol. Chem. 279 2004 31533 31543 10.1074/jbc.M314245200
45. M.E. Janssen, H. Liu, N. Volkmann, and D. Hanein The C-terminal tail domain of metavinculin, vinculin's splice variant, severs actin filaments J. Cell Biol. 197 2012 585 593 10.1083/jcb.201111046
46. V.E. Koteliansky, A.M. Belkin, M.G. Frid, and M.A. Glukhova Developmental changes in expression of adhesion-mediating proteins in human aortic smooth muscle Biochem. Soc. Trans. 19 1991 1072 1076
47. M.A. Glukhova, A.E. Kabakov, A.M. Belkin, M.G. Frid, O.I. Ornatsky, N.I. Zhidkova, and V.E. Koteliansky Meta-vinculin distribution in adult human tissues and cultured cells FEBS Lett. 207 1986 139 141
48. M. Gimona, M. Herzog, J. Vandekerckhove, and J.V. Small Smooth muscle specific expression of calponin FEBS Lett. 274 1990 159 162
49. V.C. Vasile, M.L. Will, S.R. Ommen, W.D. Edwards, T.M. Olson, and M.J. Ackerman Identification of a metavinculin missense mutation, R975W, associated with both hypertrophic and dilated cardiomyopathy Mol. Genet. Metab. 87 2006 169 174 10.1016/j.ymgme.2005.08.006
50. E.S. Rangarajan, J.H. Lee, S.D. Yogesha, and T. Izard A helix replacement mechanism directs metavinculin functions PLoS ONE 5 2010 e10679 10.1371/journal.pone.0010679
51. R. Dominguez Actin-binding proteins-a unifying hypothesis Trends Biochem. Sci. 29 2004 572 578 10.1016/j.tibs.2004.09.004
52. R. Dominguez, and K.C. Holmes Actin structure and function Annu. Rev. Biophys. 40 2011 169 186 10.1146/annurev-biophys-042910-155359
53. C.A. Schoenenberger, H.G. Mannherz, and B.M. Jockusch Actin: from structural plasticity to functional diversity Eur. J. Cell Biol. 90 2011 797 804 10.1016/j.ejcb.2011.05.002
54. T.D. Pollard, and J.A. Cooper Actin, a central player in cell shape and movement Science 326 2009 1208 1212 10.1126/science.1175862
55. M.E. Janssen, E. Kim, H. Liu, L.M. Fujimoto, A. Bobkov, N. Volkmann, and D. Hanein Three-dimensional structure of vinculin bound to actin filaments Mol. Cell 21 2006 271 281 10.1016/j.molcel.2005.11.020
56. K. Shen, C.E. Tolbert, C. Guilluy, V.S. Swaminathan, M.E. Berginski, K. Burridge, R. Superfine, and S.L. Campbell The vinculin C-terminal hairpin mediates F-actin bundle formation, focal adhesion, and cell mechanical properties J. Biol. Chem. 286 2011 45103 45115 10.1074/jbc.M111.244293
57. S.M. Palmer, M.P. Playford, S.W. Craig, M.D. Schaller, and S.L. Campbell Lipid binding to the tail domain of vinculin: specificity and the role of the N and C termini J. Biol. Chem. 284 2009 7223 7231 10.1074/jbc.M807842200
58. W.H. Goldmann, Z. Guttenberg, J.X. Tang, K. Kroy, G. Isenberg, and R.M. Ezzell Analysis of the F-actin binding fragments of vinculin using stopped-flow and dynamic light-scattering measurements Eur. J. Biochem. 254 1998 413 419 http://dx.doi.org/10.1046/j.1432-1327.1998.2540413.x
59. R.P. Johnson, and S.W. Craig Actin activates a cryptic dimerization potential of the vinculin tail domain J. Biol. Chem. 275 2000 95 105
60. A.R. Menkel, M. Kroemker, P. Bubeck, M. Ronsiek, G. Nikolai, and B.M. Jockusch Characterization of an F-actin-binding domain in the cytoskeletal protein vinculin J. Cell Biol. 126 1994 1231 1240
61. D.M. Cohen, H. Chen, R.P. Johnson, B. Choudhury, and S.W. Craig Two distinct head-tail interfaces cooperate to suppress activation of vinculin by talin J. Biol. Chem. 280 2005 17109 17117 10.1074/jbc.M414704200
62. V.E. Galkin, A. Orlova, G.F. Schroder, and E.H. Egelman Structural polymorphism in F-actin Nat. Struct. Mol. Biol. 17 2010 1318 1323 10.1038/nsmb.1930
63. K.K. Wen, P.A. Rubenstein, and K.A. DeMali Vinculin nucleates actin polymerization and modifies actin filament structure J. Biol. Chem. 284 2009 30463 30473 10.1074/jbc.M109.021295
64. Thievessen, I.; Berlemont, S.; Plevock, K.M.; Plotnikov, S.V.; Thompson, P.M.; Zemljic-Harpf, A.; Ross, R.S.; Davidson, M.W.; Campbell, S.L.; Danuser, G.; et al. (2013) Vinculin-actin interaction mediates engagement of actin retrograde flow to focal adhesions, but is dispensable for actin-dependent focal adhesion maturation. J. Cell. Biol. Submitted for publication.
65. C. Le Clainche, S.P. Dwivedi, D. Didry, and M.F. Carlier Vinculin is a dually regulated actin filament barbed end-capping and side-binding protein J. Biol. Chem. 285 2010 23420 23432 10.1074/jbc.M110.102830
66. J.D. Humphries, P. Wang, C. Streuli, B. Geiger, M.J. Humphries, and C. Ballestrem Vinculin controls focal adhesion formation by direct interactions with talin and actin J. Cell Biol. 179 2007 1043 1057 10.1083/jcb.200703036
67. S.M. Palmer, M.D. Schaller, and S.L. Campbell Vinculin tail conformation and self-association is independent of pH and H906 protonation Biochemistry 47 2008 12467 12475 10.1021/bi801764a
68. S. Huttelmaier, O. Mayboroda, B. Harbeck, T. Jarchau, B.M. Jockusch, and M. Rudiger The interaction of the cell-contact proteins VASP and vinculin is regulated by phosphatidylinositol-4,5-bisphosphate Curr. Biol. 8 1998 479 488
69. L. Molony, and K. Burridge Molecular shape and self-association of vinculin and metavinculin J. Cell. Biochem. 29 1985 31 36 10.1002/jcb.240290104
70. C. Abe, F. Dietrich, P. Gajula, M. Benz, K.P. Vogel, M. van Gastel, S. Illenberger, W.H. Ziegler, and H.J. Steinhoff Monomeric and dimeric conformation of the vinculin tail five-helix bundle in solution studied by EPR spectroscopy Biophys. J. 101 2011 1772 1780 10.1016/j.bpj.2011.08.048
71. P.A. Steimle, J.D. Hoffert, N.B. Adey, and S.W. Craig Polyphosphoinositides inhibit the interaction of vinculin with actin filaments J. Biol. Chem. 274 1999 18414 18420
72. R.M. Saunders, M.R. Holt, L. Jennings, D.H. Sutton, I.L. Barsukov, A. Bobkov, R.C. Liddington, E.A. Adamson, G.A. Dunn, and D.R. Critchley Role of vinculin in regulating focal adhesion turnover Eur. J. Cell Biol. 85 2006 487 500 10.1016/j.ejcb.2006.01.014
73. I. Chandrasekar, T.E. Stradal, M.R. Holt, F. Entschladen, B.M. Jockusch, and W.H. Ziegler Vinculin acts as a sensor in lipid regulation of adhesion-site turnover J. Cell Sci. 118 2005 1461 1472 10.1242/jcs.01734
74. S. Ito, D.K. Werth, N.D. Richert, and I. Pastan Vinculin phosphorylation by the src kinase. Interaction of vinculin with phospholipid vesicles J. Biol. Chem. 258 1983 14626 14631
75. S. Ito, N. Richert, and I. Pastan Phospholipids stimulate phosphorylation of vinculin by the tyrosine-specific protein kinase of Rous sarcoma virus Proc. Natl. Acad. Sci. USA 79 1982 4628 4631
76. A.P. Gilmore, and K. Burridge Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate Nature 381 1996 531 535 10.1038/381531a0
77. J. Weekes, S.T. Barry, and D.R. Critchley Acidic phospholipids inhibit the intramolecular association between the N- and C-terminal regions of vinculin, exposing actin-binding and protein kinase C phosphorylation sites Biochem. J. 314 Pt 3 1996 827 832
78. W.H. Ziegler, U. Tigges, A. Zieseniss, and B.M. Jockusch A lipid-regulated docking site on vinculin for protein kinase C J. Biol. Chem. 277 2002 7396 7404 10.1074/jbc.M110008200
79. V.F. Wirth, F. List, G. Diez, and W.H. Goldmann Vinculin's C-terminal region facilitates phospholipid membrane insertion Biochem. Biophys. Res. Commun. 398 2010 433 437 10.1016/j.bbrc.2010.06.094
80. G. Diez, P. Kollmannsberger, C.T. Mierke, T.M. Koch, H. Vali, B. Fabry, and W.H. Goldmann Anchorage of vinculin to lipid membranes influences cell mechanical properties Biophys. J. 97 2009 3105 3112 10.1016/j.bpj.2009.09.039
81. G. Diez, F. List, J. Smith, W.H. Ziegler, and W.H. Goldmann Direct evidence of vinculin tail-lipid membrane interaction in beta-sheet conformation Biochem. Biophys. Res. Commun. 373 2008 69 73 10.1016/j.bbrc.2008.05.182
82. B.M. Jockusch, and G. Isenberg Interaction of alpha-actinin and vinculin with actin-opposite effects on filament network formation Proc. Natl. Acad. Sci. Biol. 78 1981 3005 3009 http://dx.doi.org/10.1073/pnas.78.5.3005
83. R.P. Johnson, and S.W. Craig F-actin binding site masked by the intramolecular association of vinculin head and tail domains Nature 373 1995 261 264 10.1038/373261a0
84. H. Chen, D.M. Cohen, D.M. Choudhury, N. Kioka, and S.W. Craig Spatial distribution and functional significance of activated vinculin in living cells J. Cell Biol. 169 2005 459 470 10.1083/jcb.200410100
85. M. Rudiger, N. Korneeva, C. Schwienbacher, E.E. Weiss, and B.M. Jockusch Differential actin organization by vinculin isoforms: implications for cell type-specific microfilament anchorage FEBS Lett. 431 1998 49 54
86. B. Zimerman, T. Volberg, and B. Geiger Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading Cell Motil. Cytoskeleton 58 2004 143 159 10.1002/cm.20005
87. C.E. Tolbert, K. Burridge, and S.L. Campbell Vinculin regulation of F-actin bundle formation: what does it mean for the cell? Cell Adhes. Migr. 7 2013 142
88. The PyMOL Molecular Graphics System, Version 1.5.0.4 Schrödinger, LLC. Inc.
89. Reprinted from Molecular Cell: 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, 21(2), 271-281, with permission from Elsevier.