γ-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin

Journal of Cell Biology

Volumn 142, Issue 5, 1998, Pages 1279-1287

  Hack, Andrew A ^a   Ly, Chantal T ^a   Jiang, Fang ^a   Clendenin, Cynthia J ^a   Sigrist, Kirsten S ^a   Wollmann, Robert L ^a   McNally, Elizabeth M ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

Apoptosis; Dystrophin; Extracellular matrix; Muscular dystrophy; Sarcolemma

Indexed keywords

DYSTROGLYCAN; DYSTROPHIN; GAMMA SARCOGLYCAN; LAMININ; SARCOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DUCHENNE MUSCULAR DYSTROPHY; GENE DISRUPTION; HEART MUSCLE; HISTOPATHOLOGY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; SKELETAL MUSCLE;

ANIMALS; APOPTOSIS; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; DYSTROGLYCANS; DYSTROPHIN; HISTOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; LAMININ; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MUSCLE PROTEINS; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; MYOCARDIUM;

EID: 0032494165     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.142.5.1279     Document Type: Article

References (53)

1. Bönnemann, C.G., E.M. McNally, and L.M. Kunkel. 1996. Beyond dystrophin: current progress in the muscular dystrophies. Curr. Opin. Pediatrics. 8:569-582.
2. Bönnemann, C.G., M.R. Passos-Bueno, E.M. McNally, M. Vainzof, E. de Sa Moreira, S.K. Marie, R.C. Pavanello, S. Noguchi, E. Ozawa, M. Zatz, and L.M. Kunkel. 1996. Genomic screening for beta-sarcoglycan gene mutations: misscnse mutations may cause severe limb-girdle muscular dystrophy type 2E (LGMD 2E). Am. J. Hum. Genet. 59:1040-1047.
3. Burghes, A.H., C. Logan, X. Hu, B. Belfall, R.G. Worton, and P.N. Ray. 1987. A cDNA clone from the Duchenne/Becker muscular dystrophy gene. Nature. 328:434-437.
4. Campbell, K.P. 1995. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell. 80:675-679.
5. Campbell, K.P., and S.D. Kahl. 1989. Association of dystrophin and an integral membrane glycoprotein. Nature. 338:259-262.
6. Cox, G.A., Y. Sunada, K.P. Campbell, and J.S. Chamberlain. 1994. Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nat. Genet. 8:333-339.
7. Deconinck, A.E., J.A. Rafael, J.A. Skinner, S.C. Brown, A.C. Potter, L. Metzinger, D.J. Watt, J.G. Dickson, J.M. Tinsley, and K.E. Davies. 1997. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell. 90:717-727.
8. Dubowitz, V. 1995. Muscle Disorders in Childhood. First edition. W.B. Saunders Co., Ltd., London. 19-50.
9. Duggan, D.J., J.R. Gorospe, M. Fanin, E.P. Hoffman, and C. Angelini. 1997. Mutations in the sarcoglycan genes in patients with myopathy. N. Engl. J. Med. 336:618-624.
10. Ervasti, J.M., and K.P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell. 66:1121-1131.
11. Ervasti, J.M., and K.P. Campbell. 1993. A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122:809-823.
12. Ettinger, A.J., G. Feng, and J.R. Sanes. 1997. Epsilon-sarcoglycan, a broadly expressed homologue of the gene mutated in limb-girdle muscular dystrophy 2D. J. Biol. Chem. 272:32534-32538.
13. Grady, R.M., H. Teng, M.C. Nichol, J.C. Cunningham, R.S. Wilkinson, and J.R. Sanes. 1997. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell. 90:729-738.
14. Greenberg, D.S., Y. Sunada, K.P. Campbell, D. Yaffe, and U. Nudel. 1994. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage In mdx mice. Nat. Genet. 8:340-344.
15. Helbling-Leclerc, A., X. Zhang, H. Topaloglu, C. Cruaud, F. Tesson, J. Weissenbach, F.M. Tomé, K. Schwartz, M. Fardeau, K. Tryggvason, and P. Guicheney. 1995. Mutations in the laminin alpha 2-chain gene (LAMA2) cause merosin- deficient congenital muscular dystrophy. Nat. Genet. 11:216-218.
16. Helliwell, T.R., N.T. Man, G.E. Morris, and K.E. Davies. 1992. The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibres in dystrophies and inflammatory myopathies. Neuromusc. Dis. 2:177-184.
17. Holt, K.H., L.E. Lim, V. Straub, D.P. Venzke, F. Duclos, R.D. Anderson, B.L. Davidson, and K.P. Campbell. 1998. Functional rescue of the sarcoglycan complex in the BIO 14.6 hamster using δ-sarcoglycan gene transfer. Mol. Cell. 1:841-848.
18. Homburger, F., J.R. Baker, C.W. Nixon, and R. Whitney. 1962. Primary, generalized polymyopathy and cardiac necrosis in an inbred line of Syrian hamsters. Med. Exp. 6:339-345.
19. Ibraghimov-Beskrovnaya, O., J.M. Ervasti, C.J. Leveille, C.A. Slaughter, S.W. Sernett, and K.P. Campbell. 1992. Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature. 355:696-702.
20. Karpati, G., S. Carpenter, G.E. Morris, K.E. Davies, C. Guerin, and P. Holland. 1993. Localization and quantitation of the chromosome δ-encoded dystrophin-related protein in normal and pathological human muscle. J. Neuropath. Exp. Neurol. 52:119-128.
21. Koenig. M., E.P. Huffman, C.J. Bertelson, A.P. Monaco, C. Feener, and L.M. Kunkel. 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.
22. Lidov, H.G., T.J. Byers, S.C. Watkins, and L.M. Kunkel. 1990. Localization of dystrophin to postsynaptic regions of central nervous system cortical neurons. Nuture. 348:725-728.
23. Lim, L.E., F. Duclos, O. Broux, N. Bourg, Y. Sunada, V. Allamand, J. Meyer, I. Richard, C. Moomaw, C. Slaughter, et al. 1995. Beta-sarcoglycan: characterization and role in limb-girdle muscular dystrophy linked to 4ql2. Nat. Genet. 11:257-265.
24. Love, D.R., D.F. Hill, G. Dickson, N.K. Spurr, B.C. Byth, R.F. Marsden, F.S. Walsh, Y.H. Edwards, and K.E. Davies. 1989. An autosomal transcript in skeletal muscle with homology to dystrophin. Nature. 339:55-58.
25. Matsuda, R., A. Nishikawa, and H. Tanaka. 1995. Visualization of dystrophic muscle fibers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem. 118:959-964.
26. McArdle, A., R.H.T. Edwards, and M.J. Jackson. 1994. Time course of changes in plasma membrane permeability in the dystrophin-deficient mdx mouse. Musle Nerve. 17:1378-1384.
27. McNally, E.M., D. Duggan, J.R. Gorospe, C.G. Bönnemann, M. Fanin, E. Pegoraro, H.G. Lidov, S. Noguchi, E. Ozawa, R.S. Finkel, et al. 1996. Mutations that disrupt the carboxyl-terminus of gamma-sarcoglycan cause muscular dystrophy. Hum. Mol. Genet. 5:1841-1847.
28. McNally, E.M., C.T. Ly, and L.M. Kunkel. 1998. Human epsilon sarcoglycan is highly related to alpha-sarcoglycan (adhalin), the limb girdle muscular dystrophy type 2D gene. FEBS Lett. 422:27-32.
29. Monaco, A.P., R.L. Neve, F.C. Colletti, C.J. Bertelson, D.M. Kurnit, and L.M. Kunkel. 1986. Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature. 323:646-650.
30. Nicholson, L.V., K. Davison, G. Falkous, C. Harwood, E. O'Donnell, C.R. Slater, and J.B. Harris. 1989. Dystrophin in skeletal muscle. I. Western blot analysis using a monoclonal antibody. J. Neurol. Sci. 94:125-136.
31. Nigro, V., G. Piluso, A. Belsito, L. Politano, A.A. Puca, S. Papparella, E. Rossi, G. Viglietto, M.G. Esposito, C. Abbondanza, et al. 1996. Identification of a novel sarcoglycan gene at 5q33 encoding a sarcolemmal 35 kDa glycoprotein. Hum. Mol. Genet. 5:1179-1186.
32. Nigro, V., Y. Okazaki, A. Belsito, G. Piluso, Y. Matsuda, L. Politano, G. Nigro, C. Ventura, C. Abbondanza, A.M. Molinari, et al. 1997. Identification of the Syrian hamster cardiomyopathy gene. Hum. Mol. Genet. 6:601-607.
33. Nissinen, M., A. Helbling-Leclerc, X. Zhang, T. Evangelista, H. Topaloglu, C. Cruaud, J. Weissenbach, M. Fardeau, P.M. Tomé, et al. 1996. Substitution of a conserved cysteine-996 in a cysteine-rich motif of the laminin alpha2-chain in congenital muscular dystrophy with partial deficiency of the protein. Am. J. Hum. Genet. 58:1177-1184.
34. Noguchi, S., E.M. McNally, K. Ben Othmane, Y. Hagiwara, Y. Mizuno, M. Yoshida, H. Yamamoto, C.G. Bönnemann, E. Gussoni, et al. 1995. Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science. 270:819-822.
35. Ohlendieck, K., and K.P. Campbell. 1992. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J. Cell Biol. 115:1685-1694.
36. Ohlendieck. K., K. Matsumura, V.V. Ionasescu, J.A. Towbin, E.P. Bosch, S.L. Weinstein, S.W. Sernett, and K.P. Campbell. 1993. Duchennc muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolemma. Neurology. 43:795-800.
37. Ozawa, E., M. Yoshida, A. Suzuki, Y. Mizuno, Y. Hagiwara, and S. Noguchi. 1995. Dystrophin-associated proteins in muscular dystrophy. Hum. Mol. Genet. 4:1711-1716.
38. Roberds, S.L., R.D. Anderson, O. Ibraghimov-Beskrovnaya, and K.P. Campbell. 1993. Primary structure and muscle-specific expression of the 50-kDa dystrophin-associated glycoprotein (adhalin). J. Biol. Chem. 268:23739-23742.
39. Rybakova, I.N., K.J. Amann, and J.M. Ervasti. 1996. A new model for the interaction of dystrophin with F-actin. J. Cell Biol. 135:661-672.
40. Sakamoto, A., K. Ono, M. Abe, G. Jasmin, T. Eki, Y. Murakami, T. Masaki, T. Toyo-oka, and F. Hanaoka. 1997. Both hypertrophic and dilated cardiomyopathies are caused by mutation of the same gene, delta-sarcoglycan, in hamster: an animal model of disrupted dystrophin-associated glycoprotein complex. Proc. Natl. Acad. Sci. USA. 94:13873-13878.
41. Scott, E., M.C. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science. 265:1573-1577.
42. Sicinski, P., Y. Geng, C. Ryder, E. Barnard, M. Darlison, and P. Barnard. 1989. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science. 244:1578-1580.
43. Straub, V., and K.P. Campbell. 1997. Muscular dystrophies and the dystrophinglycoprotein complex. Curr. Opin. Neural. 10:168-175.
44. Straub, V., J.A. Rafael, J.S. Chamberlain, and K.P. Campbell. 1997. Animal models for muscular dystrophy show different patterns of sarcolemmal disruption. J. Cell Biol. 139:375-385.
45. Sunada, Y., S.M. Bernier, C.A. Kozak, Y. Yamada, and K.P. Campbell. 1994. Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. J. Biol. Chem. 269:13729-13732.
46. Tybulewicz, V., C. Crawford, P. Jackson, R. Bronson, and R. Mulligan, 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell. 65:1153-1163.
47. Vainzof, M., M.R. Passos-Bueno, M. Canovas, E.S. Moreira, R.C. Pavanello, S.K. Marie, L.V. Anderson, C.G. Bonnemann, E.M. McNally, V. Nigro, et al. 1996. The sarcoglycan complex in the six autosomal recessive limb-girdle muscular dystrophies. Hum. Mol. Genet. 5:1963-1969.
48. Williamson, R.A., M.D. Henry, K.J. Daniels, R.F. Hrstka, J.C Lee, Y. Sunada, O. Ibraghimov-Beskrovnaya, and K.P. Campbell. 1997. Dystroglycan is essential for early embryonic development: disruption of Reichert's membrane in Dag1-null mice. Hum. Mol. Genet. 6:831-841.
49. Xu, H., P. Christmas, X.R. Wu, U.M. Wewer, and E. Engvall. 1994. Defective muscle basement membrane and lack of M-laminin in the dystrophic dy/dy mouse. Proc. Natl. Acad. Sci. USA. 91:5572-5576.
50. Yamada, H., T. Shimizu, T. Tanaka, K.P. Campbell, and K. Matsumura. 1994. Dystroglycan is a binding protein of laminin and merosin in peripheral nerve. FEBS Lett. 352:49-53.
51. Yoshida, M., and E. Ozawa. 1990. Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. 108:748-752.
52. Yoshida, M., A. Suzuki, H. Yamamoto, S. Noguchi, Y. Mizuno, and E. Ozawa. 1994. Dissociation of the complex of dystrophin and its associated proteins into several unique groups by n-octyl beta-D-glucoside. Eur. J. Biochem. 222:1055-1061.
53. Yoshida, T., Y. Pan, H. Hanada, Y. Iwata, and M. Shigekawa. 1998. Bidirectional Signaling between Sarcoglycans and the Integrin Adhesion System in Cultured L6 Myocytes. J. Biol. Chem. 273:1583-1590.