Cardiac-Myocyte-Specific Excision of the Vinculin Gene Disrupts Cellular Junctions, Causing Sudden Death or Dilated Cardiomyopathy

REFERENCES

• Angst, B. D., L. U. Khan, N. J. Severs, K. Whitely, S. Rothery, R. P. Thompson, A. I. Magee, and R. G. Gourdie. 1997. Dissociated spatial patterning of gap junctions and cell adhesion junctions during postnatal differentiation of ventricular myocardium. Circ. Res. 80:88–94.
   PubMed Web of Science ®Google Scholar
• Babbitt, C. J., S. Y. Shai, A. E. Harpf, C. G. Pham, and R. S. Ross. 2002. Modulation of integrins and integrin signaling molecules in the pressure-loaded murine ventricle. Histochem. Cell Biol. 118:431–439.
   PubMedGoogle Scholar
• Bakolitsa, C., D. M. Cohen, L. A. Bankston, A. A. Bobkov, G. W. Cadwell, L. Jennings, D. R. Critchley, S. W. Craig, and R. C. Liddington. 2004. Structural basis for vinculin activation at sites of cell adhesion. Nature 430:583–586.
   PubMed Web of Science ®Google Scholar
• Barstead, R. J., and R. H. Waterston. 1991. Vinculin is essential for muscle function in the nematode. J. Cell Biol. 114:715–724.
   PubMed Web of Science ®Google Scholar
• Baurand, A., L. Zelarayan, R. Betney, C. Gehrke, S. Dunger, C. Noack, A. Busjahn, J. Huelsken, M. M. Taketo, W. Birchmeier, R. Dietz, and M. W. Bergmann. 2007. Beta-catenin downregulation is required for adaptive cardiac remodeling. Circ. Res. 100:1353–1362.
   PubMed Web of Science ®Google Scholar
• Bayly, P. V., B. H. KenKnight, J. M. Rogers, R. E. Hillsley, R. E. Ideker, and W. M. Smith. 1998. Estimation of conduction velocity vector fields from epicardial mapping data. IEEE Trans. Biomed. Eng. 45:563–571.
   PubMed Web of Science ®Google Scholar
• Belkin, A. M., O. I. Ornatsky, M. A. Glukhova, and V. E. Koteliansky. 1988. Immunolocalization of meta-vinculin in human smooth and cardiac muscles. J. Cell Biol. 107:545–553.
   PubMedGoogle Scholar
• Belkin, A. M., O. I. Ornatsky, A. E. Kabakov, M. A. Glukhova, and V. E. Koteliansky. 1988. 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. 263:6631–6635.
   PubMedGoogle Scholar
• Birks, E. J., J. L. Hall, P. J. Barton, S. Grindle, N. Latif, J. P. Hardy, J. E. Rider, N. R. Banner, A. Khaghani, L. W. Miller, and M. H. Yacoub. 2005. Gene profiling changes in cytoskeletal proteins during clinical recovery after left ventricular-assist device support. Circulation 112:I57–I64.
   PubMed Web of Science ®Google Scholar
• Borgon, R. A., C. Vonrhein, G. Bricogne, P. R. Bois, and T. Izard. 2004. Crystal structure of human vinculin. Structure 12:1189–1197.
   PubMedGoogle Scholar
• Brancaccio, M., L. Fratta, A. Notte, E. Hirsch, R. Poulet, S. Guazzone, M. De Acetis, C. Vecchione, G. Marino, F. Altruda, L. Silengo, G. Tarone, and G. Lembo. 2003. Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nat. Med. 9:68–75.
   PubMed Web of Science ®Google Scholar
• Byrne, B. J., Y. J. Kaczorowski, M. D. Coutu, and S. W. Craig. 1992. 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. 267:12845–12850.
   PubMedGoogle Scholar
• Chen, H., D. M. Cohen, D. M. Choudhury, N. Kioka, and S. W. Craig. 2005. Spatial distribution and functional significance of activated vinculin in living cells. J. Cell Biol. 169:459–470.
   PubMed Web of Science ®Google Scholar
• Chen, J., S. W. Kubalak, S. Minamisawa, R. L. Price, K. D. Becker, R. Hickey, J. J. Ross, and K. R. Chien. 1998. Selective requirement of myosin light chain 2v in embryonic heart function. J. Biol. Chem. 273:1252–1256.
   PubMedGoogle Scholar
• Chopard, A., F. Pons, and J. F. Marini. 2002. Vinculin and meta-vinculin in fast and slow rat skeletal muscle before and after hindlimb suspension. Pflugers Arch. 444:627–633.
   PubMedGoogle Scholar
• Clark, K. A., A. S. McElhinny, M. C. Beckerle, and C. C. Gregorio. 2002. Striated muscle cytoarchitecture: an intricate web of form and function. Annu. Rev. Cell Dev. Biol. 18:637–706.
   PubMed Web of Science ®Google Scholar
• Cohen, D. M., B. Kutscher, H. Chen, D. B. Murphy, and S. W. Craig. 2006. A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions. J. Biol. Chem. 281:16006–16015.
   PubMedGoogle Scholar
• Critchley, D. R. 2004. Cytoskeletal proteins talin and vinculin in integrin-mediated adhesion. Biochem. Soc. Trans. 32:831–836.
   PubMed Web of Science ®Google Scholar
• Crone, S. A., Y. Y. Zhao, L. Fan, Y. Gu, S. Minamisawa, Y. Liu, K. L. Peterson, J. Chen, R. Kahn, G. Condorelli, J. Ross, Jr., K. R. Chien, and K. F. Lee. 2002. ErbB2 is essential in the prevention of dilated cardiomyopathy. Nat. Med. 8:459–465.
   PubMed Web of Science ®Google Scholar
• Demali, K. A. 2004. Vinculin—a dynamic regulator of cell adhesion. Trends Biochem. Sci. 29:565–567.
   PubMedGoogle Scholar
• DiMichele, L. A., J. T. Doherty, M. Rojas, H. E. Beggs, L. F. Reichardt, C. P. Mack, and J. M. Taylor. 2006. Myocyte-restricted focal adhesion kinase deletion attenuates pressure overload-induced hypertrophy. Circ. Res. 99:636–645.
   PubMed Web of Science ®Google Scholar
• Drees, F., S. Pokutta, S. Yamada, W. J. Nelson, and W. I. Weis. 2005. Alpha-catenin is a molecular switch that binds E-cadherin-beta-catenin and regulates actin-filament assembly. Cell 123:903–915.
   PubMed Web of Science ®Google Scholar
• Ezzell, R. M., W. H. Goldmann, N. Wang, N. Parasharama, and D. E. Ingber. 1997. Vinculin promotes cell spreading by mechanically coupling integrins to the cytoskeleton. Exp. Cell Res. 231:14–26.
   PubMedGoogle Scholar
• Fujimoto, K., A. Nagafuchi, S. Tsukita, A. Kuraoka, A. Ohokuma, and Y. Shibata. 1997. Dynamics of connexins, E-cadherin and alpha-catenin on cell membranes during gap junction formation. J. Cell Sci. 110:311–322.
   PubMed Web of Science ®Google Scholar
• Gallant, N. D., K. E. Michael, and A. J. Garcia. 2005. Cell adhesion strengthening: contributions of adhesive area, integrin binding, and focal adhesion assembly. Mol. Biol. Cell 16:4329–4340.
   PubMed Web of Science ®Google Scholar
• Gates, J., and M. Peifer. 2005. Can 1000 reviews be wrong? Actin, alpha-catenin, and adherens junctions. Cell 123:769–772.
   PubMedGoogle Scholar
• Geiger, B., A. H. Dutton, K. T. Tokuyasu, and S. J. Singer. 1981. Immunoelectron microscope studies of membrane-microfilament interactions: distributions of alpha-actinin, tropomyosin, and vinculin in intestinal epithelial brush border and chicken gizzard smooth muscle cells. J. Cell Biol. 91:614–628.
   PubMed Web of Science ®Google Scholar
• Geiger, B., K. T. Tokuyasu, A. H. Dutton, and S. J. Singer. 1980. Vinculin, an intracellular protein localized at specialized sites where microfilament bundles terminate at cell membranes. Proc. Natl. Acad. Sci. USA 77:4127–4131.
   PubMed Web of Science ®Google Scholar
• Geiger, B., T. Volk, and T. Volberg. 1985. Molecular heterogeneity of adherens junctions. J. Cell Biol. 101:1523–1531.
   PubMed Web of Science ®Google Scholar
• Gewillig, M., L. Mertens, P. Moerman, and M. Dumoulin. 1996. Idiopathic restrictive cardiomyopathy in childhood. A diastolic disorder characterized by delayed relaxation. Eur. Heart J. 17:1413–1420.
   PubMed Web of Science ®Google Scholar
• Giepmans, B. N. 2004. Gap junctions and connexin-interacting proteins. Cardiovasc. Res. 62:233–245.
   PubMed Web of Science ®Google Scholar
• Gilmore, A. P., and K. Burridge. 1996. Regulation of vinculin binding to talin and actin by phosphatidyl-inositol-4-5-bisphosphate. Nature 381:531–535.
   PubMed Web of Science ®Google Scholar
• Gingras, A. R., K. P. Vogel, H. J. Steinhoff, W. H. Ziegler, B. Patel, J. Emsley, D. R. Critchley, G. C. Roberts, and I. L. Barsukov. 2006. Structural and dynamic characterization of a vinculin binding site in the talin rod. Biochemistry 45:1805–1817.
   PubMed Web of Science ®Google Scholar
• Goldmann, W. H., R. Galneder, M. Ludwig, W. Xu, E. D. Adamson, N. Wang, and R. M. Ezzell. 1998. Differences in elasticity of vinculin-deficient F9 cells measured by magnetometry and atomic force microscopy. Exp. Cell Res. 239:235–242.
   PubMedGoogle Scholar
• Gutstein, D. E., F. Y. Liu, M. B. Meyers, A. Choo, and G. I. Fishman. 2003. The organization of adherens junctions and desmosomes at the cardiac intercalated disc is independent of gap junctions. J. Cell Sci. 116:875–885.
   PubMed Web of Science ®Google Scholar
• Gutstein, D. E., G. E. Morley, H. Tamaddon, D. Vaidya, M. D. Schneider, J. Chen, K. R. Chien, H. Stuhlmann, and G. I. Fishman. 2001. Conduction slowing and sudden arrhythmic death in mice with cardiac-restricted inactivation of connexin43. Circ. Res. 88:333–339.
   PubMed Web of Science ®Google Scholar
• Gutstein, D. E., G. E. Morley, D. Vaidya, F. Liu, F. L. Chen, H. Stuhlmann, and G. I. Fishman. 2001. Heterogeneous expression of Gap junction channels in the heart leads to conduction defects and ventricular dysfunction. Circulation 104:1194–1199.
   PubMed Web of Science ®Google Scholar
• Hu, K., L. Ji, K. T. Applegate, G. Danuser, and C. M. Waterman-Storer. 2007. Differential transmission of actin motion within focal adhesions. Science 315:111–115.
   PubMedGoogle Scholar
• Izard, T., G. Evans, R. A. Borgon, C. L. Rush, G. Bricogne, and P. R. Bois. 2004. Vinculin activation by talin through helical bundle conversion. Nature 427:171–175.
   PubMed Web of Science ®Google Scholar
• Janssen, M. E., E. Kim, H. Liu, L. M. Fujimoto, A. Bobkov, N. Volkmann, and D. Hanein. 2006. Three-dimensional structure of vinculin bound to actin filaments. Mol. Cell 21:271–281.
   PubMed Web of Science ®Google Scholar
• Kostetskii, I., J. Li, Y. Xiong, R. Zhou, V. A. Ferrari, V. V. Patel, J. D. Molkentin, and G. L. Radice. 2005. Induced deletion of the N-cadherin gene in the heart leads to dissolution of the intercalated disc structure. Circ. Res. 96:346–354.
   PubMed Web of Science ®Google Scholar
• Koteliansky, V. E., E. P. Ogryzko, N. I. Zhidkova, P. A. Weller, D. R. Critchley, K. Vancompernolle, J. Vandekerckhove, P. Strasser, M. Way, and M. Gimona. 1992. 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. 205:1218.
   PubMedGoogle Scholar
• Li, J., V. V. Patel, I. Kostetskii, Y. Xiong, A. F. Chu, J. T. Jacobson, C. Yu, G. E. Morley, J. D. Molkentin, and G. L. Radice. 2005. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ. Res. 97:474–481.
   PubMed Web of Science ®Google Scholar
• Maeda, M., E. Holder, B. Lowes, S. Valent, and R. D. Bies. 1997. Dilated cardiomyopathy associated with deficiency of the cytoskeletal protein metavinculin. Circulation 95:17–20.
   PubMedGoogle Scholar
• Malone, P., H. Miao, A. Parker, S. Juarez, and M. R. Hernandez. 2007. Pressure induces loss of gap junction communication and redistribution of connexin 43 in astrocytes. Glia 55:1085–1098.
   PubMed Web of Science ®Google Scholar
• Matsushita, T., M. Oyamada, K. Fujimoto, Y. Yasuda, S. Masuda, Y. Wada, T. Oka, and T. Takamatsu. 1999. Remodeling of cell-cell and cell-extracellular matrix interactions at the border zone of rat myocardial infarcts. Circ. Res. 85:1046–1055.
   PubMed Web of Science ®Google Scholar
• Melo, T. G., D. S. Almeida, M. N. de Meirelles, and M. C. Pereira. 2004. Trypanosoma cruzi infection disrupts vinculin costameres in cardiomyocytes. Eur. J. Cell Biol. 83:531–540.
   PubMedGoogle Scholar
• Miyake, Y., N. Inoue, K. Nishimura, N. Kinoshita, H. Hosoya, and S. Yonemura. 2006. Actomyosin tension is required for correct recruitment of adherens junction components and zonula occludens formation. Exp. Cell Res. 312:1637–1650.
   PubMed Web of Science ®Google Scholar
• Moiseyeva, E. P., P. A. Weller, N. I. Zhidkova, E. B. Corben, B. Patel, I. Jasinska, V. E. Koteliansky, and D. R. Critchley. 1993. Organization of the human gene encoding the cytoskeletal protein vinculin and the sequence of the vinculin promoter. J. Biol. Chem. 268:4318–4325.
   PubMedGoogle Scholar
• O'Connell, T. D., M. C. Rodrigo, and P. C. Simpson. 2006. Isolation and culture of adult mouse cardiac myocytes, p. 271–296. In F. Vivanco (ed.), Cardiovascular proteomics: methods and protocols. Humana Press, Totowa, NJ.
   Google Scholar
• Olson, T. M., S. Illenberger, N. Y. Kishimoto, S. Huttelmaier, M. T. Keating, and B. M. Jockusch. 2002. Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 105:431–437.
   PubMed Web of Science ®Google Scholar
• Pardo, J. V., J. D. Siliciano, and S. W. Craig. 1983. Vinculin is a component of an extensive network of myofibril-sarcolemma attachment regions in cardiac muscle fibers. J. Cell Biol. 97:1081–1088.
   PubMed Web of Science ®Google Scholar
• Peng, X., M. S. Kraus, H. Wei, T. L. Shen, R. Pariaut, A. Alcaraz, G. Ji, L. Cheng, Q. Yang, M. I. Kotlikoff, J. Chen, K. Chien, H. Gu, and J. L. Guan. 2006. Inactivation of focal adhesion kinase in cardiomyocytes promotes eccentric cardiac hypertrophy and fibrosis in mice. J. Clin. Investig. 116:217–227.
   PubMed Web of Science ®Google Scholar
• Perriard, J. C., A. Hirschy, and E. Ehler. 2003. Dilated cardiomyopathy: a disease of the intercalated disc? Trends Cardiovasc. Med. 13:30–38.
   PubMed Web of Science ®Google Scholar
• Pham, C. G., A. E. Harpf, R. S. Keller, H. T. Vu, S. Y. Shai, J. C. Loftus, and R. S. Ross. 2000. Striated muscle-specific beta(1D)-integrin and FAK are involved in cardiac myocyte hypertrophic response pathway. Am. J. Physiol. Heart Circ. Physiol. 279:H2916–H2926.
   PubMedGoogle Scholar
• Polontchouk, L., J. A. Haefliger, B. Ebelt, T. Schaefer, D. Stuhlmann, U. Mehlhorn, F. Kuhn-Regnier, E. R. De Vivie, and S. Dhein. 2001. Effects of chronic atrial fibrillation on gap junction distribution in human and rat atria. J. Am. Coll. Cardiol. 38:883–891.
   PubMed Web of Science ®Google Scholar
• Rivenes, S. M., D. L. Kearney, E. O. Smith, J. A. Towbin, and S. W. Denfield. 2000. Sudden death and cardiovascular collapse in children with restrictive cardiomyopathy. Circulation 102:876–882.
   PubMedGoogle Scholar
• Rodriguez, C. I., F. Buchholz, J. Galloway, R. Sequerra, J. Kasper, R. Ayala, A. F. Stewart, and S. M. Dymecki. 2000. High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat. Genet. 25:139–140.
   PubMed Web of Science ®Google Scholar
• Rudiger, M., N. Korneeva, C. Schwienbacher, E. E. Weiss, and B. M. Jockusch. 1998. Differential actin organization by vinculin isoforms: implications for cell type-specific microfilament anchorage. FEBS Lett. 431:49–54.
   PubMedGoogle Scholar
• Saffitz, J. E., and A. G. Kleber. 2004. Effects of mechanical forces and mediators of hypertrophy on remodeling of gap junctions in the heart. Circ. Res. 94:585–591.
   PubMedGoogle Scholar
• Sakurai, A., S. Fukuhara, A. Yamagishi, K. Sako, Y. Kamioka, M. Masuda, Y. Nakaoka, and N. Mochizuki. 2006. MAGI-1 is required for Rap1 activation upon cell-cell contact and for enhancement of vascular endothelial cadherin-mediated cell adhesion. Mol. Biol. Cell 17:966–976.
   PubMed Web of Science ®Google Scholar
• Samarel, A. M. 2005. Costameres, focal adhesions, and cardiomyocyte mechanotransduction. Am. J. Physiol. Heart Circ. Physiol. 289:H2291–H2301.
   PubMed Web of Science ®Google Scholar
• Saunders, R. M., 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. 2006. Role of vinculin in regulating focal adhesion turnover. Eur. J. Cell Biol. 85:487–500.
   PubMedGoogle Scholar
• Shai, S. Y., A. E. Harpf, C. J. Babbitt, M. C. Jordan, M. C. Fishbein, J. Chen, M. Omura, T. A. Leil, K. D. Becker, M. Jiang, D. J. Smith, S. R. Cherry, J. C. Loftus, and R. S. Ross. 2002. Cardiac myocyte-specific excision of the beta1 integrin gene results in myocardial fibrosis and cardiac failure. Circ. Res. 90:458–464.
   PubMed Web of Science ®Google Scholar
• Sharp, W. W., D. G. Simpson, T. K. Borg, A. M. Samarel, and L. Terracio. 1997. Mechanical forces regulate focal adhesion and costamere assembly in cardiac myocytes. Am. J. Physiol. 273:H546–H556.
   PubMedGoogle Scholar
• Shaw, R. M., A. J. Fay, M. A. Puthenveedu, M. von Zastrow, Y. N. Jan, and L. Y. Jan. 2007. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128:547–560.
   PubMed Web of Science ®Google Scholar
• Sheikh, F., Y. Chen, X. Liang, A. Hirschy, A. E. Stenbit, Y. Gu, N. D. Dalton, T. Yajima, Y. Lu, K. U. Knowlton, K. L. Peterson, J. C. Perriard, and J. Chen. 2006. alpha-E-catenin inactivation disrupts the cardiomyocyte adherens junction, resulting in cardiomyopathy and susceptibility to wall rupture. Circulation 114:1046–1055.
   PubMed Web of Science ®Google Scholar
• Shiraishi, I., D. G. Simpson, W. Carver, R. Price, T. Hirozane, L. Terracio, and T. K. Borg. 1997. Vinculin is an essential component for normal myofibrillar arrangement in fetal mouse cardiac myocytes. J. Mol. Cell. Cardiol. 29:2041–2052.
   PubMedGoogle Scholar
• Siliciano, J. D., and S. W. Craig. 1982. Meta-vinculin—a vinculin-related protein with solubility properties of a membrane protein. Nature 300:533–535.
   PubMedGoogle Scholar
• Subauste, M. C., P. Nalbant, E. D. Adamson, and K. M. Hahn. 2005. Vinculin controls PTEN protein level by maintaining the interaction of the adherens junction protein beta-catenin with the scaffolding protein MAGI-2. J. Biol. Chem. 280:5676–5681.
   PubMed Web of Science ®Google Scholar
• Sung, D., J. S. J. P. Cosman, R. Mills, and A. D. McCulloch. 2001. Phase shifting prior to spatial filtering enhances optical recordings of cardiac action potential propagation. Ann. Biomed. Eng. 29:854–861.
   PubMedGoogle Scholar
• Tansey, E. E., K. F. Kwaku, P. E. Hammer, D. B. Cowan, M. Federman, S. Levitsky, and J. D. McCully. 2006. Reduction and redistribution of gap and adherens junction proteins after ischemia and reperfusion. Ann. Thorac. Surg. 82:1472–1479.
   PubMedGoogle Scholar
• Terracio, L., D. G. Simpson, L. Hilenski, W. Carver, R. S. Decker, N. Vinson, and T. K. Borg. 1990. Distribution of vinculin in the Z-disk of striated muscle: analysis by laser scanning confocal microscopy. J. Cell. Physiol. 145:78–87.
   PubMed Web of Science ®Google Scholar
• Thibault, G., M. J. Lacombe, L. M. Schnapp, A. Lacasse, F. Bouzeghrane, and G. Lapalme. 2001. Upregulation of alpha(8)beta(1)-integrin in cardiac fibroblast by angiotensin II and transforming growth factor-beta1. Am. J. Physiol. Cell Physiol. 281:C1457–C1467.
   PubMed Web of Science ®Google Scholar
• Tokuyasu, K. T., A. H. Dutton, B. Geiger, and S. J. Singer. 1981. Ultrastructure of chicken cardiac muscle as studied by double immunolabeling in electron microscopy. Proc. Natl. Acad. Sci. USA 78:7619–7623.
   PubMedGoogle Scholar
• Vasile, V. C., S. R. Ommen, W. D. Edwards, and M. J. Ackerman. 2006. A missense mutation in a ubiquitously expressed protein, vinculin, confers susceptibility to hypertrophic cardiomyopathy. Biochem. Biophys. Res. Commun. 345:998–1003.
   PubMed Web of Science ®Google Scholar
• Vasile, V. C., M. L. Will, S. R. Ommen, W. D. Edwards, T. M. Olson, and M. J. Ackerman. 2006. Identification of a metavinculin missense mutation, R975W, associated with both hypertrophic and dilated cardiomyopathy. Mol. Genet. Metab. 87:169–174.
   PubMed Web of Science ®Google Scholar
• Volk, T., and B. Geiger. 1984. A 135-kd membrane protein of intercellular adherens junctions. EMBO J. 3:2249–2260.
   PubMed Web of Science ®Google Scholar
• Wei, C. J., R. Francis, X. Xu, and C. W. Lo. 2005. Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J. Biol. Chem. 280:19925–19936.
   PubMed Web of Science ®Google Scholar
• Weis, W. I., and W. J. Nelson. 2006. Re-solving the cadherin-catenin-actin conundrum. J. Biol. Chem. 281:35593–35597.
   PubMedGoogle Scholar
• Weiss, E. E., M. Kroemker, A. H. Rudiger, B. M. Jockusch, and M. Rudiger. 1998. Vinculin is part of the cadherin-catenin junctional complex: complex formation between alpha-catenin and vinculin. J. Cell Biol. 141:755–764.
   PubMedGoogle Scholar
• Weller, P. A., E. P. Ogryzko, E. B. Corben, N. I. Zhidkova, B. Patel, G. J. Price, N. K. Spurr, V. E. Koteliansky, and D. R. Critchley. 1990. Complete sequence of human vinculin and assignment of the gene to chromosome 10. Proc. Natl. Acad. Sci. USA 87:5667–5671.
   PubMedGoogle Scholar
• White, D. E., P. Coutu, Y. F. Shi, J. C. Tardif, S. Nattel, R. St. Arnaud, S. Dedhar, and W. J. Muller. 2006. Targeted ablation of ILK from the murine heart results in dilated cardiomyopathy and spontaneous heart failure. Genes Dev. 20:2355–2360.
   PubMed Web of Science ®Google Scholar
• Witt, S., A. Zieseniss, U. Fock, B. M. Jockusch, and S. Illenberger. 2004. Comparative biochemical analysis suggests that vinculin and metavinculin cooperate in muscular adhesion sites. J. Biol. Chem. 279:31533–31543.
   PubMedGoogle Scholar
• Wu, J. C., R. Y. Tsai, and T. H. Chung. 2003. Role of catenins in the development of gap junctions in rat cardiomyocytes. J. Cell. Biochem. 88:823–835.
   PubMed Web of Science ®Google Scholar
• Xu, W., H. Baribault, and E. D. Adamson. 1998. Vinculin knockout results in heart and brain defects during embryonic development. Development 125:327–337.
   PubMed Web of Science ®Google Scholar
• Yamada, S., S. Pokutta, F. Drees, W. I. Weis, and W. J. Nelson. 2005. Deconstructing the cadherin-catenin-actin complex. Cell 123:889–901.
   PubMed Web of Science ®Google Scholar
• Zemljic-Harpf, A. E., S. Ponrartana, R. T. Avalos, M. C. Jordan, K. P. Roos, N. D. Dalton, V. Q. Phan, E. D. Adamson, and R. S. Ross. 2004. Heterozygous inactivation of the vinculin gene predisposes to stress-induced cardiomyopathy. Am. J. Pathol. 165:1033–1044.
   PubMedGoogle Scholar
• Zhou, J., J. Qu, X. P. Yi, K. Graber, L. Huber, X. Wang, A. M. Gerdes, and F. Li. 2007. Upregulation of gamma-catenin compensates for the loss of beta-catenin in adult cardiomyocytes. Am. J. Physiol. Heart Circ. Physiol. 292:H270–H276.
   PubMed Web of Science ®Google Scholar
• Ziegler, W. H., R. C. Liddington, and D. R. Critchley. 2006. The structure and regulation of vinculin. Trends Cell Biol. 16:453–460.
   PubMed Web of Science ®Google Scholar