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Costamere proteins and their involvement in myopathic processes

Published online by Cambridge University Press:  19 June 2015

Oihane Jaka ,
Leire Casas-Fraile ,
Adolfo López de Munain  and
Amets Sáenz
Oihane Jaka
Affiliation:
Neurosciences Area, BioDonostia Institute, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), Carlos III Health Institute, Spanish Ministry of Economy and Competitiveness, Madrid, Spain
Leire Casas-Fraile
Affiliation:
Neurosciences Area, BioDonostia Institute, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), Carlos III Health Institute, Spanish Ministry of Economy and Competitiveness, Madrid, Spain
Adolfo López de Munain
Affiliation:
Neurosciences Area, BioDonostia Institute, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), Carlos III Health Institute, Spanish Ministry of Economy and Competitiveness, Madrid, Spain Department of Neurology, Donostia University Hospital, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain Department of Neurosciences, University of the Basque Country, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain
Amets Sáenz*
Affiliation:
Neurosciences Area, BioDonostia Institute, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), Carlos III Health Institute, Spanish Ministry of Economy and Competitiveness, Madrid, Spain
*
*Corresponding author: Neurosciences Area, BioDonostia Institute, Paseo Dr. Begiristain s/n, 20014 San Sebastián, Spain. E-mail: amets.saenzpena@osakidetza.net
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Abstract

Muscle fibres are very specialised cells with a complex structure that requires a high level of organisation of the constituent proteins. For muscle contraction to function properly, there is a need for not only sarcomeres, the contractile structures of the muscle fibre, but also costameres. These are supramolecular structures associated with the sarcolemma that allow muscle adhesion to the extracellular matrix. They are composed of protein complexes that interact and whose functions include maintaining cell structure and signal transduction mediated by their constituent proteins. It is important to improve our understanding of these structures, as mutations in various genes that code for costamere proteins cause many types of muscular dystrophy. In this review, we provide a description of costameres detailing each of their constituent proteins, such as dystrophin, dystrobrevin, syntrophin, sarcoglycans, dystroglycans, vinculin, talin, integrins, desmin, plectin, etc. We describe as well the diseases associated with deficiency thereof, providing a general overview of their importance.

Type
Review Article
Information
Expert Reviews in Molecular Medicine , Volume 17 , 2015 , e12
Copyright
Copyright © Cambridge University Press 2015 

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References

1. Pardo, J.V., Siliciano, J.D., and Craig, S.W. (1983) A vinculin-containing cortical lattice in skeletal muscle: transverse lattice elements (“costameres”) mark sites of attachment between myofibrils and sarcolemma. Proceedings of the National Academy of Sciences of the United States of America 80, 1008-1012 Google Scholar
2. Nelson, W.J., Colaco, C.A., and Lazarides, E. (1983) Involvement of spectrin in cell-surface receptor capping in lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 80, 1626-1630 Google Scholar
3. Nelson, W.J. and Lazarides, E. (1984) Goblin (ankyrin) in striated muscle: identification of the potential membrane receptor for erythroid spectrin in muscle cells. Proceedings of the National Academy of Sciences of the United States of America 81, 3292-3296 CrossRefGoogle ScholarPubMed
4. Bloch, R.J. et al. (2002) Costameres: repeating structures at the sarcolemma of skeletal muscle. Clinical Orthopaedics and Related Research S203-S210 Google Scholar
5. Danowski, B.A. et al. (1992) Costameres are sites of force transmission to the substratum in adult rat cardiomyocytes. Journal of Cell Biology 118, 1411-1420 Google Scholar
6. Trimarchi, F. et al. (2006) Culture of human skeletal muscle myoblasts: timing appearance and localization of dystrophin-glycoprotein complex and vinculin–talin–integrin complex. Cells Tissues Organs 183, 87-98 Google Scholar
7. Ervasti, J.M. (2003) Costameres: the Achilles’ heel of Herculean muscle. Journal of Cell Biology 278, 13591-13594 Google Scholar
8. Mansour, H. et al. (2004) Restoration of resting sarcomere length after uniaxial static strain is regulated by protein kinase Cepsilon and focal adhesion kinase. Circulation Research 94, 642-649 Google Scholar
9. Rui, Y., Bai, J., and Perrimon, N. (2010) Sarcomere formation occurs by the assembly of multiple latent protein complexes. PLoS Genetics 6, e1001208 Google Scholar
10. Heuson-Stiennon, J. (1965) Morphogenése de la cellule musculaire striée, étudiée au microscope électronique. I. Formation des structures fibrillaires. Journal of Microscopy 4, 657-678 Google Scholar
11. Tokuyasu, K.T. (1989) Immunocytochemical studies of cardiac myofibrillogenesis in early chick embryos. III. Generation of fasciae adherentes and costameres. Journal of Cell Biology 108, 43-53 Google Scholar
12. Fujita, H., Nedachi, T., and Kanzaki, M. (2007) Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Experimental Cell Research 313, 1853-1865 CrossRefGoogle ScholarPubMed
13. Sparrow, J.C. and Schock, F. (2009) The initial steps of myofibril assembly: integrins pave the way. Nature Reviews Molecular Cell Biology 10, 293-298 Google Scholar
14. Ku, N.O. et al. (1999) The cytoskeleton of digestive epithelia in health and disease. American Journal of Physiology 277, G1108-G1137 Google Scholar
15. Omary, M.B., Ku, N.O., and Toivola, D.M. (2002) Keratins: guardians of the liver. Hepatology 35, 251-257 CrossRefGoogle ScholarPubMed
16. Pierobon-Bormioli, S. (1981) Transverse sarcomere filamentous systems: “Z- and M-cables”. Journal of Muscle Research and Cell Motility 2, 401-413 CrossRefGoogle Scholar
17. Shear, C.R. and Bloch, R.J. (1985) Vinculin in subsarcolemmal densities in chicken skeletal muscle: localization and relationship to intracellular and extracellular structures. Journal of Cell Biology 101, 240-256 Google Scholar
18. Street, S.F. (1983) Lateral transmission of tension in frog myofibers: a myofibrillar network and transverse cytoskeletal connections are possible transmitters. Journal of Cellular Physiology 114, 346-364 Google Scholar
19. Li, Z. et al. (1997) Desmin is essential for the tensile strength and integrity of myofibrils but not for myogenic commitment, differentiation, and fusion of skeletal muscle. Journal of Cell Biology 139, 129-144 Google Scholar
20. Lazarides, E. and Hubbard, B.D. (1976) Immunological characterization of the subunit of the 100 A filaments from muscle cells. Proceedings of the National Academy of Sciences of the United States of America 73, 4344-4348 Google Scholar
21. Capetanaki, Y. and Milner, D.J. (1998) Desmin cytoskeleton in muscle integrity and function. Sub-cellular Biochemistry 31, 463-495 Google Scholar
22. Estrella, N.L. and Naya, F.J. (2014) Transcriptional networks regulating the costamere, sarcomere, and other cytoskeletal structures in striated muscle. Cellular and Molecular Life Sciences 71, 1641-1656 Google Scholar
23. Black, B.L. and Olson, E.N. (1998) Transcriptional control of muscle development by myocyte enhancer factor-2 (MEF2) proteins. Annual Review of Cell and Developmental Biology 14, 167-196 Google Scholar
24. Naya, F.J. and Olson, E. (1999) MEF2: a transcriptional target for signaling pathways controlling skeletal muscle growth and differentiation. Current Opinion in Cell Biology 11, 683-688 Google Scholar
25. Potthoff, M.J. and Olson, E.N. (2007) MEF2: a central regulator of diverse developmental programs. Development 134, 4131-4140 Google Scholar
26. Bour, B.A. et al. (1995) Drosophila MEF2, a transcription factor that is essential for myogenesis. Genes & Development 9, 730-741 Google Scholar
27. Lilly, B. et al. (1995) Requirement of MADS domain transcription factor D-MEF2 for muscle formation in Drosophila. Science 267, 688-693 Google Scholar
28. Ewen, E.P. et al. (2011) The Mef2A transcription factor coordinately regulates a costamere gene program in cardiac muscle. Journal of Cell Biology 286, 29644-29653 Google ScholarPubMed
29. Snyder, C.M. et al. (2013) MEF2A regulates the Gtl2–Dio3 microRNA mega-cluster to modulate WNT signaling in skeletal muscle regeneration. Development 140, 31-42 Google Scholar
30. Miano, J.M. (2010) Role of serum response factor in the pathogenesis of disease. Laboratory Investigation 90, 1274-1284 Google Scholar
31. Balza, R.O. Jr and Misra, R.P. (2006) Role of the serum response factor in regulating contractile apparatus gene expression and sarcomeric integrity in cardiomyocytes. Journal of Cell Biology 281, 6498-6510 Google Scholar
32. Fluck, M. et al. (1999) Focal adhesion proteins FAK and paxillin increase in hypertrophied skeletal muscle. American Journal of Physiology 277, C152-C162 Google Scholar
33. Gordon, S.E., Fluck, M., and Booth, F.W. (2001) Selected Contribution: skeletal muscle focal adhesion kinase, paxillin, and serum response factor are loading dependent. Journal of Applied Physiology 90, 1174-1183 Google Scholar
34. Chopard, A., Pons, F., and Marini, J.F. (2002) Vinculin and meta-vinculin in fast and slow rat skeletal muscle before and after hindlimb suspension. Pflugers Archiv-European Journal of Physiology 444, 627-633 Google Scholar
35. Chopard, A. et al. (2005) Changes in dysferlin, proteins from dystrophin glycoprotein complex, costameres, and cytoskeleton in human soleus and vastus lateralis muscles after a long-term bedrest with or without exercise. FASEB Journal 19, 1722-1724 Google Scholar
36. Anastasi, G. et al. (2008) Costameric proteins in human skeletal muscle during muscular inactivity. Journal of Anatomy 213, 284-295 Google Scholar
37. Bozyczko, D. et al. (1989) Integrin on developing and adult skeletal muscle. Experimental Cell Research 183, 72-91 Google Scholar
38. Schroder, R. et al. (1997) Altered distribution of plectin/HD1 in dystrophinopathies. European Journal of Cell Biology 74, 165-171 Google Scholar
39. Williams, M.W., Resneck, W.G., and Bloch, R.J. (2000) Membrane skeleton of innervated and denervated fast- and slow-twitch muscle. Muscle & Nerve 23, 590-599 Google Scholar
40. Fluck, M. et al. (2002) Fibre-type specific concentration of focal adhesion kinase at the sarcolemma: influence of fibre innervation and regeneration. Journal of Experimental Biology 205, 2337-2348 Google Scholar
41. Li, R. et al. (2013) Costamere remodeling with muscle loading and unloading in healthy young men. Journal of Anatomy 223, 525-536 Google Scholar
42. Anastasi, G. et al. (2004) Sarcoglycan and integrin localization in normal human skeletal muscle: a confocal laser scanning microscope study. European Journal of Histochemistry 48, 245-252 Google Scholar
43. Campbell, K.P. (1995) Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80, 675-679 Google Scholar
44. Matsumura, K. and Campbell, K.P. (1994) Dystrophin-glycoprotein complex: its role in the molecular pathogenesis of muscular dystrophies. Muscle & Nerve 17, 2-15 CrossRefGoogle ScholarPubMed
45. Monaco, A.P. et al. (1986) Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 323, 646-650 Google Scholar
46. Suzuki, A. et al. (1994) Molecular organization at the glycoprotein-complex-binding site of dystrophin. Three dystrophin-associated proteins bind directly to the carboxy-terminal portion of dystrophin. European Journal of Biochemistry 220, 283-292 Google Scholar
47. Song, W.K. et al. (1992) H36-alpha 7 is a novel integrin alpha chain that is developmentally regulated during skeletal myogenesis. Journal of Cell Biology 117, 643-657 Google Scholar
48. Song, W.K. et al. (1993) Expression of alpha 7 integrin cytoplasmic domains during skeletal muscle development: alternate forms, conformational change, and homologies with serine/threonine kinases and tyrosine phosphatases. Journal of Cell Science 106 (Pt 4), 1139-1152 Google Scholar
49. Hodges, B.L. and Kaufman, S.J. (1996) Developmental regulation and functional significance of alternative splicing of NCAM and a7b1 integrin in skeletal muscle. Basic and Applied Myology 6, 437-446 Google Scholar
50. Yoshida, M. et al. (1994) Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl beta-D-glucoside. European Journal of Biochemistry 222, 1055-1061 Google Scholar
51. Ohlendieck, K. (1996) Towards an understanding of the dystrophin-glycoprotein complex: linkage between the extracellular matrix and the membrane cytoskeleton in muscle fibers. European Journal of Cell Biology 69, 1-10 Google Scholar
52. Watkins, S.C. et al. (2000) Plasma membrane cytoskeleton of muscle: a fine structural analysis. Microscopy Research and Technique 48, 131-141 Google Scholar
53. Anastasi, G. et al. (2009) Dystrophin–glycoprotein complex and vinculin–talin–integrin system in human adult cardiac muscle. International Journal of Molecular Medicine 23, 149-159 Google Scholar
54. Kunkel, L.M. et al. (1986) Molecular genetics of Duchenne muscular dystrophy. Cold Spring Harbor Symposia on Quantitative Biology 51 (Pt 1), 349-351 Google Scholar
55. Hoffman, E.P. et al. (1987) Subcellular fractionation of dystrophin to the triads of skeletal muscle. Nature 330, 754-758 Google Scholar
56. Beggs, A.H. and Kunkel, L.M. (1990) Improved diagnosis of Duchenne/Becker muscular dystrophy. Journal of Clinical Investigation 85, 613-619 CrossRefGoogle ScholarPubMed
57. Wagner, K.R., Cohen, J.B., and Huganir, R.L. (1993) The 87 K postsynaptic membrane protein from Torpedo is a protein-tyrosine kinase substrate homologous to dystrophin. Neuron 10, 511-522 Google Scholar
58. Blake, D.J. et al. (1995) Coiled-coil regions in the carboxy-terminal domains of dystrophin and related proteins: potentials for protein–protein interactions. Trends in Biochemical Sciences 20, 133-135 Google Scholar
59. Sadoulet-Puccio, H.M., Rajala, M., and Kunkel, L.M. (1997) Dystrobrevin and dystrophin: an interaction through coiled-coil motifs. Proceedings of the National Academy of Sciences of the United States of America 94, 12413-12418 Google Scholar
60. Yoshida, M. et al. (2000) Biochemical evidence for association of dystrobrevin with the sarcoglycan-sarcospan complex as a basis for understanding sarcoglycanopathy. Human Molelular Genetics 9, 1033-1040 CrossRefGoogle ScholarPubMed
61. Nakamori, M. and Takahashi, M.P. (2011) The role of alpha-dystrobrevin in striated muscle. International Journal of Molecular Sciences 12, 1660-1671 Google Scholar
62. Ichida, F. et al. (2001) Novel gene mutations in patients with left ventricular noncompaction or Barth syndrome. Circulation 103, 1256-1263 CrossRefGoogle ScholarPubMed
63. Piluso, G. et al. (2000) Gamma1- and gamma2-syntrophins, two novel dystrophin-binding proteins localized in neuronal cells. Journal of Cell Biology 275, 15851-15860 Google Scholar
64. Bhat, H.F., Adams, M.E., and Khanday, F.A. (2013) Syntrophin proteins as Santa Claus: role(s) in cell signal transduction. Cellular and Molecular Life Sciences 70, 2533-2554 CrossRefGoogle ScholarPubMed
65. Adams, M.E. et al. (1995) Mouse alpha 1- and beta 2-syntrophin gene structure, chromosome localization, and homology with a discs large domain. Journal of Cell Biology 270, 25859-25865 Google Scholar
66. Ahn, A.H. et al. (1996) The three human syntrophin genes are expressed in diverse tissues, have distinct chromosomal locations, and each bind to dystrophin and its relatives. Journal of Cell Biology 271, 2724-2730 Google Scholar
67. Ueda, K. et al. (2008) Syntrophin mutation associated with long QT syndrome through activation of the nNOS-SCN5A macromolecular complex. Proceedings of the National Academy of Sciences of the United States of America 105, 9355-9360 CrossRefGoogle ScholarPubMed
68. Ozawa, E. et al. (1998) From dystrophinopathy to sarcoglycanopathy: evolution of a concept of muscular dystrophy. Muscle & Nerve 21, 421-438 Google Scholar
69. Crosbie, R.H. et al. (1997) Sarcospan, the 25-kDa transmembrane component of the dystrophin-glycoprotein complex. Journal of Cell Biology 272, 31221-31224 Google Scholar
70. Holt, K.H. and Campbell, K.P. (1998) Assembly of the sarcoglycan complex. Insights for muscular dystrophy. Journal of Cell Biology 273, 34667-34670 Google Scholar
71. Hack, A.A. et al. (2000) Differential requirement for individual sarcoglycans and dystrophin in the assembly and function of the dystrophin–glycoprotein complex. Journal of Cell Science 113 (Pt 14), 2535-2544 Google Scholar
72. Ettinger, A.J., Feng, G., and Sanes, J.R. (1997) epsilon-Sarcoglycan, a broadly expressed homologue of the gene mutated in limb-girdle muscular dystrophy 2D. Journal of Cell Biology 272, 32534-32538 Google ScholarPubMed
73. Noguchi, S. et al. (1995) Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science 270, 819-822 Google Scholar
74. Ozawa, E. et al. (2005) Molecular and cell biology of the sarcoglycan complex. Muscle & Nerve 32, 563-576 Google Scholar
75. Crosbie, R.H. et al. (2000) Molecular and genetic characterization of sarcospan: insights into sarcoglycan-sarcospan interactions. Human Molecular Genetics 9, 2019-2027 Google Scholar
76. Bonnemann, C.G., McNally, E.M., and Kunkel, L.M. (1996) Beyond dystrophin: current progress in the muscular dystrophies. Current Opinion in Pediatrics 8, 569-582 Google Scholar
77. Ibraghimov-Beskrovnaya, O. et al. (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696-702 Google Scholar
78. Barresi, R. and Campbell, K.P. (2006) Dystroglycan: from biosynthesis to pathogenesis of human disease. Journal of Cell Science 119, 199-207 Google Scholar
79. Hara, Y. et al. (2011) A dystroglycan mutation associated with limb-girdle muscular dystrophy. New England Journal of Medicine 364, 939-946 Google Scholar
80. Michele, D.E. et al. (2002) Post-translational disruption of dystroglycan-ligand interactions in congenital muscular dystrophies. Nature 418, 417-422 Google Scholar
81. Schwartz, M.A. (1992) Transmembrane signalling by integrins. Trends in Cell Biology 2, 304-308 Google Scholar
82. Hynes, R.O. (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69, 11-25 Google Scholar
83. Schwartz, M.A., Schaller, M.D., and Ginsberg, M.H. (1995) Integrins: emerging paradigms of signal transduction. Annual Review of Cell and Developmental Biology 11, 549-599 Google Scholar
84. Lu, M.H. et al. (1992) The vinculin/sarcomeric-alpha-actinin/alpha-actin nexus in cultured cardiac myocytes. Journal of Cell Biology 117, 1007-1022 Google Scholar
85. Burridge, K. and Mangeat, P. (1984) An interaction between vinculin and talin. Nature 308, 744-746 Google Scholar
86. Weiss, E.E. et al. (1998) Vinculin is part of the cadherin-catenin junctional complex: complex formation between alpha-catenin and vinculin. Journal of Cell Biology 141, 755-764 Google Scholar
87. Peng, X. et al. (2011) New insights into vinculin function and regulation. International Review of Cell and Molecular Biology 287, 191-231 Google Scholar
88. Olson, T.M. et al. (2002) Metavinculin mutations alter actin interaction in dilated cardiomyopathy. Circulation 105, 431-437 Google Scholar
89. Vasile, V.C. et al. (2006) A missense mutation in a ubiquitously expressed protein, vinculin, confers susceptibility to hypertrophic cardiomyopathy. Biochemical and Biophysical Research Communications 345, 998-1003 Google Scholar
90. Critchley, D.R. (2009) Biochemical and structural properties of the integrin-associated cytoskeletal protein talin. Annual Review of Biophysics 38, 235-254 Google Scholar
91. Zemljic-Harpf, A., Manso, A.M., and Ross, R.S. (2009) Vinculin and talin: focus on the myocardium. Journal of Investigative Medicine 57, 849-855 CrossRefGoogle ScholarPubMed
92. Zhang, X. et al. (2008) Talin depletion reveals independence of initial cell spreading from integrin activation and traction. Nature Cell Biology 10, 1062-1068 Google Scholar
93. Yamada, K.M. and Miyamoto, S. (1995) Integrin transmembrane signaling and cytoskeletal control. Current Opinion in Cell Biology 7, 681-689 Google Scholar
94. Legate, K.R., Wickstrom, S.A., and Fassler, R. (2009) Genetic and cell biological analysis of integrin outside-in signaling. Genes & Development 23, 397-418 Google Scholar
95. Wiesner, S., Legate, K.R., and Fassler, R. (2005) Integrin-actin interactions. Cellular and Molecular Life Sciences 62, 1081-1099 Google Scholar
96. Belkin, A.M. et al. (1996) Beta 1D integrin displaces the beta 1A isoform in striated muscles: localization at junctional structures and signaling potential in nonmuscle cells. Journal of Cell Biology 132, 211-226 Google Scholar
97. Belkin, A.M. et al. (1997) Muscle beta1D integrin reinforces the cytoskeleton-matrix link: modulation of integrin adhesive function by alternative splicing. Journal of Cell Biology 139, 1583-1595 Google Scholar
98. Tadokoro, S. et al. (2003) Talin binding to integrin beta tails: a final common step in integrin activation. Science 302, 103-106 Google Scholar
99. Hayashi, Y.K. et al. (1998) Mutations in the integrin alpha7 gene cause congenital myopathy. Nature Genetics 19, 94-97 Google Scholar
100. Tetreault, M. et al. (2006) A new form of congenital muscular dystrophy with joint hyperlaxity maps to 3p23-21. Brain 129, 2077-2084 Google Scholar
101. De Palma, S. et al. (2013) Changes in muscle cell metabolism and mechanotransduction are associated with myopathic phenotype in a mouse model of collagen VI deficiency. PLoS ONE 8, e56716 Google Scholar
102. De Palma, S. et al. (2014) Muscle proteomics reveals novel insights into the pathophysiological mechanisms of collagen VI myopathies. Journal of Proteome Research 13, 5022-5030 Google Scholar
103. Demir, E. et al. (2002) Mutations in COL6A3 cause severe and mild phenotypes of Ullrich congenital muscular dystrophy. American Journal of Human Genetics 70, 1446-1458 Google Scholar
104. Bethlem, J. and Wijngaarden, G.K. (1976) Benign myopathy, with autosomal dominant inheritance. A report on three pedigrees. Brain 99, 91-100 Google Scholar
105. Merlini, L. et al. (2008) Autosomal recessive myosclerosis myopathy is a collagen VI disorder. Neurology 71, 1245-1253 Google Scholar
106. Legate, K.R. et al. (2006) ILK, PINCH and parvin: the tIPP of integrin signalling. Nature Reviews Molecular Cell Biology 7, 20-31 Google Scholar
107. Hannigan, G.E. et al. (1996) Regulation of cell adhesion and anchorage-dependent growth by a new beta 1-integrin-linked protein kinase. Nature 379, 91-96 Google Scholar
108. Tu, Y. et al. (2001) A new focal adhesion protein that interacts with integrin-linked kinase and regulates cell adhesion and spreading. Journal of Cell Biology 153, 585-598 Google Scholar
109. Rearden, A. (1994) A new LIM protein containing an autoepitope homologous to “senescent cell antigen”. Biochemical and Biophysical Research Communications 201, 1124-1131 Google Scholar
110. Zhang, Y. et al. (2002) Characterization of PINCH-2, a new focal adhesion protein that regulates the PINCH-1-ILK interaction, cell spreading, and migration. Journal of Cell Biology 277, 38328-38338 Google ScholarPubMed
111. Fukuda, T. et al. (2003) PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and survival. Journal of Cell Biology 278, 51324-51333 Google Scholar
112. Nikolopoulos, S.N. and Turner, C.E. (2000) Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. Journal of Cell Biology 151, 1435-1448 Google Scholar
113. Yamaji, S. et al. (2001) A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell-substrate interaction. Journal of Cell Biology 153, 1251-1264 Google Scholar
114. Olski, T.M., Noegel, A.A., and Korenbaum, E. (2001) Parvin, a 42 kDa focal adhesion protein, related to the alpha-actinin superfamily. Journal of Cell Science 114, 525-538 Google Scholar
115. Brancaccio, M. et al. (1999) Melusin is a new muscle-specific interactor for beta(1) integrin cytoplasmic domain. Journal of Cell Biology 274, 29282-29288 Google Scholar
116. Brancaccio, M. et al. (2003) Melusin, a muscle-specific integrin beta1-interacting protein, is required to prevent cardiac failure in response to chronic pressure overload. Nature Medicine 9, 68-75 Google Scholar
117. Nigro, V. and Savarese, M. (2014) Genetic basis of limb-girdle muscular dystrophies: the 2014 update. Acta Myologica 33, 1-12 Google Scholar
118. Knoll, R. et al. (2007) Laminin-alpha4 and integrin-linked kinase mutations cause human cardiomyopathy via simultaneous defects in cardiomyocytes and endothelial cells. Circulation 116, 515-525 Google Scholar
119. Ruppert, V. et al. (2013) Identification of a missense mutation in the melusin-encoding ITGB1BP2 gene in a patient with dilated cardiomyopathy. Gene 512, 206-210 Google Scholar
120. Nadruz, W. et al. (2005) Focal adhesion kinase mediates MEF2 and c-Jun activation by stretch: role in the activation of the cardiac hypertrophic genetic program. Cardiovascular Research 68, 87-97 Google Scholar
121. Quach, N.L. and Rando, T.A. (2006) Focal adhesion kinase is essential for costamerogenesis in cultured skeletal muscle cells. Developmental Biology 293, 38-52 Google Scholar
122. Ussar, S. et al. (2006) The Kindlins: subcellular localization and expression during murine development. Experimental Cell Research 312, 3142-3151 Google Scholar
123. Dowling, J.J. et al. (2008) Kindlin-2 is required for myocyte elongation and is essential for myogenesis. BMC Cell Biology 9, 36 Google Scholar
124. O'Neill, A. et al. (2002) Sarcolemmal organization in skeletal muscle lacking desmin: evidence for cytokeratins associated with the membrane skeleton at costameres. Molecular Biology of the Cell 13, 2347-2359 Google Scholar
125. Kouloumenta, A., Mavroidis, M., and Capetanaki, Y. (2007) Proper perinuclear localization of the TRIM-like protein myospryn requires its binding partner desmin. Journal of Cell Biology 282, 35211-35221 Google Scholar
126. Goldfarb, L.G. and Dalakas, M.C. (2009) Tragedy in a heartbeat: malfunctioning desmin causes skeletal and cardiac muscle disease. Journal of Clinical Investigation 119, 1806-1813 Google Scholar
127. Wiche, G. et al. (1983) Occurrence and immunolocalization of plectin in tissues. Journal of Cell Biology 97, 887-901 Google Scholar
128. Wiche, G. (1989) Plectin: general overview and appraisal of its potential role as a subunit protein of the cytomatrix. Critical Reviews in Biochemistry and Molecular Biology 24, 41-67 Google Scholar
129. Herrmann, H. and Wiche, G. (1987) Plectin and IFAP-300 K are homologous proteins binding to microtubule-associated proteins 1 and 2 and to the 240-kilodalton subunit of spectrin. Journal of Cell Biology 262, 1320-1325 Google Scholar
130. Svitkina, T.M., Verkhovsky, A.B., and Borisy, G.G. (1996) Plectin sidearms mediate interaction of intermediate filaments with microtubules and other components of the cytoskeleton. Journal of Cell Biology 135, 991-1007 Google Scholar
131. Rezniczek, G.A. et al. (1998) Linking integrin alpha6beta4-based cell adhesion to the intermediate filament cytoskeleton: direct interaction between the beta4 subunit and plectin at multiple molecular sites. Journal of Cell Biology 141, 209-225 Google Scholar
132. Konieczny, P. and Wiche, G. (2008) Muscular integrity–a matter of interlinking distinct structures via plectin. Advances in Experimental Medicine and Biology 642, 165-175 Google Scholar
133. Cetin, N. et al. (2013) A novel desmin mutation leading to autosomal recessive limb-girdle muscular dystrophy: distinct histopathological outcomes compared with desminopathies. Journal of Medical Genetics 50, 437-443 Google Scholar
134. Goldfarb, L.G. et al. (1998) Missense mutations in desmin associated with familial cardiac and skeletal myopathy. Nature Genetics 19, 402-403 Google Scholar
135. Gundesli, H. et al. (2010) Mutation in exon 1f of PLEC, leading to disruption of plectin isoform 1f, causes autosomal-recessive limb-girdle muscular dystrophy. American Journal of Human Genetics 87, 834-841 Google Scholar
136. Gabellini, D. et al. (2006) Facioscapulohumeral muscular dystrophy in mice overexpressing FRG1. Nature 439, 973-977 Google Scholar
137. Liu, Q. et al. (2010) Facioscapulohumeral muscular dystrophy region gene-1 (FRG-1) is an actin-bundling protein associated with muscle-attachment sites. Journal of Cell Science 123, 1116-1123 Google Scholar
138. Lecroisey, C., Segalat, L., and Gieseler, K. (2007) The C. elegans dense body: anchoring and signaling structure of the muscle. Journal of Muscle Research and Cell Motility 28, 79-87 Google Scholar
139. Compton, A.G. et al. (2008) Mutations in contactin-1, a neural adhesion and neuromuscular junction protein, cause a familial form of lethal congenital myopathy. American Journal of Human Genetics 83, 714-724 Google Scholar
140. Malik, V., Rodino-Klapac, L.R., and Mendell, J.R. (2012) Emerging drugs for Duchenne muscular dystrophy. Expert Opinion on Emerging Drugs 17, 261-277 Google Scholar
141. Li, H.L. et al. (2015) Precise correction of the dystrophin gene in duchenne muscular dystrophy patient induced pluripotent stem cells by TALEN and CRISPR-Cas9. Stem Cell Reports 4, 143-154 Google Scholar
142. Herson, S. et al. (2012) A phase I trial of adeno-associated virus serotype 1-γ-sarcoglycan gene therapy for limb girdle muscular dystrophy type 2C. Brain 135, 483-492 Google Scholar
143. Merlini, L. and Bernardi, P. (2008) Therapy of collagen VI-related myopathies (Bethlem and Ullrich). Neurotherapeutics 4, 613-618 Google Scholar
144. Zulian, A. et al. (2014) NIM811, a cyclophilin inhibitor without immunosuppressive activity, is beneficial in collagen VI congenital muscular dystrophy models. Human Molecular Genetics 23, 5353-5363 Google Scholar
145. Koenig, M. et al. (1987) Complete cloning of the Duchenne muscular dystrophy (DMD) cDNA and preliminary genomic organization of the DMD gene in normal and affected individuals. Cell 50, 509-517 Google Scholar
146. Burghes, A.H. et al. (1987) A cDNA clone from the Duchenne/Becker muscular dystrophy gene. Nature 328, 434-437 Google Scholar
147. Monaco, A.P. et al. (1988) An explanation for the phenotypic differences between patients bearing partial deletions of the DMD locus. Genomics 2, 90-95 Google Scholar
148. Muntoni, F. et al. (1993) Brief report: deletion of the dystrophin muscle-promoter region associated with X-linked dilated cardiomyopathy. New England Journal of Medicine 329, 921-925 Google Scholar
149. Roberts, R.G., Bobrow, M., and Bentley, D.R. (1992) Point mutations in the dystrophin gene. Proceedings of the National Academy of Sciences of the United States of America 89, 2331-2335 Google Scholar
150. Emery, A.E. (1969) Abnormalities of the electrocardiogram in female carriers of Duchenne muscular dystrophy. British Medical Journal 2, 418-420 Google Scholar
151. Hoogerwaard, E.M. et al. (1999) Signs and symptoms of Duchenne muscular dystrophy and Becker muscular dystrophy among carriers in The Netherlands: a cohort study. Lancet 353, 2116-2119 Google Scholar
152. Requena, T. et al. (2014) Identification of two novel mutations in FAM136A and DTNA genes in autosomal-dominant familial Meniere's disease. Human Molecular Genetics 24, 1119-1126 Google Scholar
153. Ben, O.K. et al. (1992) Linkage of Tunisian autosomal recessive Duchenne-like muscular dystrophy to the pericentromeric region of chromosome 13q. Nature Genetics 2, 315-317 Google Scholar
154. Azibi, K. et al. (1993) Severe childhood autosomal recessive muscular dystrophy with the deficiency of the 50 kDa dystrophin-associated glycoprotein maps to chromosome 13q12. Human Molecular Genetics 2, 1423-1428 Google Scholar
155. Piccolo, F. et al. (1996) A founder mutation in the gamma-sarcoglycan gene of gypsies possibly predating their migration out of India. Human Molecular Genetics 5, 2019-2022 Google Scholar
156. Roberds, S.L. et al. (1994) Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell 78, 625-633 Google Scholar
157. Bonnemann, C.G. et al. (1995) Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nature Genetics 11, 266-273 Google Scholar
158. Lim, L.E. et al. (1995) Beta-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4q12. Nature Genetics 11, 257-265 Google Scholar
159. Passos-Bueno, M.R. et al. (1996) Linkage analysis in autosomal recessive limb-girdle muscular dystrophy (AR LGMD) maps a sixth form to 5q33-34 (LGMD2F) and indicates that there is at least one more subtype of AR LGMD. Human Molecular Genetics 5, 815-820 Google Scholar
160. Tsubata, S. et al. (2000) Mutations in the human delta-sarcoglycan gene in familial and sporadic dilated cardiomyopathy. Journal of Clinical Investigation 106, 655-662 Google Scholar
161. Zimprich, A. et al. (2001) Mutations in the gene encoding epsilon-sarcoglycan cause myoclonus-dystonia syndrome. Nature Genetics 29, 66-69 Google Scholar
162. Wheeler, M.T., Zarnegar, S., and McNally, E.M. (2002) Zeta-sarcoglycan, a novel component of the sarcoglycan complex, is reduced in muscular dystrophy. Human Molecular Genetics 11, 2147-2154 Google Scholar
163. Beggs, H.E. et al. (2003) FAK deficiency in cells contributing to the basal lamina results in cortical abnormalities resembling congenital muscular dystrophies. Neuron 40, 501-514 Google Scholar
164. Jobard, F. et al. (2003) Identification of mutations in a new gene encoding a FERM family protein with a pleckstrin homology domain in Kindler syndrome. Human Molecular Genetics 12, 925-935 Google Scholar
165. Malinin, N.L. et al. (2009) A point mutation in KINDLIN3 ablates activation of three integrin subfamilies in humans. Nature Medicine 15, 313-318 Google Scholar
166. Greenberg, S.A. et al. (2012) Etiology of limb girdle muscular dystrophy 1D/1E determined by laser capture microdissection proteomics. Annals of Neurology 71, 141-145 Google Scholar
167. Li, D. et al. (1999) Desmin mutation responsible for idiopathic dilated cardiomyopathy. Circulation 100, 461-464 Google Scholar
168. Walter, M.C. et al. (2007) Scapuloperoneal syndrome type Kaeser and a wide phenotypic spectrum of adult-onset, dominant myopathies are associated with the desmin mutation R350P. Brain 130, 1485-1496 Google Scholar
169. Gache, Y. et al. (1996) Defective expression of plectin/HD1 in epidermolysis bullosa simplex with muscular dystrophy. Journal of Clinical Investigation 97, 2289-2298 Google Scholar
170. Koss-Harnes, D. et al. (2002) A site-specific plectin mutation causes dominant epidermolysis bullosa simplex Ogna: two identical de novo mutations. Journal of Investigative Dermatology 118, 87-93 Google Scholar
171. Charlesworth, A. et al. (2003) Identification of a lethal form of epidermolysis bullosa simplex associated with a homozygous genetic mutation in plectin. Journal of Investigative Dermatology 121, 1344-1348 Google Scholar