Membrane targeting and stabilization of sarcospan is mediated by the sarcoglycan subcomplex

Journal of Cell Biology

Volumn 145, Issue 1, 1999, Pages 153-165

  Crosbie, Rachelle H ^a   Lebakken, Connie S ^a   Holt, Kathleen H ^a   Venzke, David P ^a   Straub, Volker ^a   Lee, Jane C ^a   Grady, R Mark ^b   Chamberlain, Jeffery S ^c   Sanes, Joshua R ^b   Campbell, Kevin P ^a  

^a UNIVERSITY OF IOWA   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Dystrophin; Muscular dystrophy; Sarcoglycans; Sarcospan; Tetraspans

Indexed keywords

DYSTROGLYCAN; DYSTROPHIN; GLYCOPROTEIN; ISOPROTEIN; MEMBRANE PROTEIN; SARCOGLYCAN; SARCOSPAN; UNCLASSIFIED DRUG; UTROPHIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; MALE; MOLECULAR DYNAMICS; MOUSE; MUSCULAR DYSTROPHY; NEUROMUSCULAR SYNAPSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN ISOLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TARGETING; REGULATORY MECHANISM; SARCOLEMMA; SEQUENCE HOMOLOGY;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CARDIOMYOPATHY, HYPERTROPHIC; CARRIER PROTEINS; CHO CELLS; CRICETINAE; CYTOSKELETAL PROTEINS; DYSTROGLYCANS; DYSTROPHIN; HUMANS; HYDROGEN-ION CONCENTRATION; MACROMOLECULAR SUBSTANCES; MALE; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, ANIMAL; NEOPLASM PROTEINS; NEUROMUSCULAR JUNCTION; RABBITS; SARCOGLYCANS; SARCOLEMMA; SEQUENCE ALIGNMENT; SPECIES SPECIFICITY; TENDONS; TRANSFECTION; UTROPHIN;

ANIMALIA;

EID: 0033526085     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.145.1.153     Document Type: Article

References (78)

1. Allamand, V., Y. Sunada, M.A. Salih, V. Straub, C.O. Ozo, M.H. Al-Turaiki, M. Akbar, T. Kolo, H. Colognato, X. Zhang, et al. 1997. Mild congenital muscular dystrophy in two patients with an internally deleted laminin alpha-2-chain. Hum. Mol. Genet. 6:747-752.
2. Amann, K.J., B.A. Renley, and J.M. Ervasti. 1998. A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction. J. Biol. Chem. 273:28419-28423.
3. Arahata, K., Y.K. Hayashi, R. Koga, K. Goto, J.H. Lee, Y. Miyagoe, H. Ishii, T. Tsukahara, S. Takeda, M. Woo, et al. 1993. Laminin in animal models for muscular dystrophy: defect of laminin M in skeletal and cardiac muscles and peripheral nerve of the homozygous dystrophic dy/dy mice. Proc. Jpn. Acad. 69B:259-264.
4. Bönnemann, C.G., R. Modi, S. Noguchi, Y. Mizuno, M. Yoshida, E. Gussoni, E.M. McNally, D.J. Duggan, C. Angelini, and E.P. Hoffman. 1995. Beta-sarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat. Genet. 11:266-273.
5. Brenman, J.E., D.S. Chao, H. Xia, K. Aldape, and D.S. Bredt. 1995. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell. 82:743-752.
6. Bulfield, G., W.G. Siller, P.A. Wright, and K.J. Moore. 1984. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA. 81:1189-1192.
7. Campbell, K.P. 1995. Three muscular dystrophies: loss of cytoskeleton-extra-cellular matrix linkage. Cell. 80:675-679.
8. Campbell, K.P., and S.D. Kahl. 1989. Association of dystrophin and an integral membrane glycoprotein. Nature. 338:259-262.
9. Chamberlain, J.S., J.A. Pearlman, D.M. Muzny, R.A. Gibbs, J.E. Ranier, C.T. Caskey, and A.A. Reeves. 1988. Expression of the murine Duchenne muscular dystrophy gene in muscle and brain. Science. 239:1416-1418.
10. Chang, W.J., S.T. Iannaccone, K.S. Lau, B.S.S. Masters, T.J. McCabe, K. McMillan, R.C. Padre, M.J. Spencer, J.G. Tidball, and J.T. Stull. 1996. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc. Natl. Acad. Sci. USA. 93:9142-9147.
11. 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.
12. Crosbie, R.H., J. Heighway, D.P. Venzke, J.C. Lee, and K.P. Campbell. 1997. Sarcospan: the 25 kDa transmembrane component of the dystrophin-glycoprotein complex. J. Biol. Chem. 272:31221-31224.
13. Crosbie, R.H., H. Yamada, D.P. Venzke, M.P. Lisanti, and K.P. Campbell. 1998. Caveolin-3 is not an integral component of the dystrophin-glycoprotein complex. FEBS Lett. 427:279-282.
14. 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.
15. Duclos, F., O. Broux, N. Bourg, V. Straub, O.L. Feldman, Y. Sunada, L.E. Lim, F. Piccolo, S. Cutshall, F. Gary, et al. 1998a. β-Sarcoglycan: genomic analysis and identification of a novel missense mutation in the LGMD2E Amish isolate. Neuromuscul. Disord. 8:30-38.
16. Duclos, F., V. Straub, S.A. Moore, D.P. Venzke, R.F. Hrstka, R.H. Crosbie, M. Durbeej, C.S. Lebakken, A.J. Ettinger, J. van der Meulen, et al. 1998b. Progressive muscular dystrophy in α-sarcoglycan deficient mice. J. Cell Biol. 142:1461-1471.
17. Ervasti, J.M., and K.P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell. 66:1121-1131.
18. 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.
19. Ervasti, J.M., K. Ohlendieck, S.D. Kahl, M.G. Gaver, and K.P. Campbell. 1990. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature. 345:315-319.
20. Ervasti, J.M., S.D. Kahl, and K.P. Campbell. 1991. Purification of dyslrophin from skeletal muscle. J. Biol. Chem. 266:9161-9165.
21. Ettinger, A.J., G. Feng, and J.R. Sanes. 1997. ∈-Sarcoglycan, a broadly expressed homologue of the gene mutated in limb-girdle muscular dystrophy 2D. J. Biol. Chem. 272:32534-32538.
22. Grady, R.M., J.P. Merlie, and J.R. Sanes. 1997a. Subtle neuromuscular defects in utrophin-deficient mice. J. Cell Biol. 136:871-881.
23. Grady, R.M., H. Teng, M.C. Nichol, J.C. Cuttingham, R.S. Wilkinson, and J.R. Sanes. 1997b. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell. 90:729-738.
24. 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.
25. Hack, A.A., C.T. Ly, F. Jiang, C.J. Clendenin, K.S. Sigrist, R.L. Wollmann, and E.M. McNally. 1998. γ-Sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol. 142:1279-1287.
26. Heighway, J., D.C. Betticher, P.R. Hoban, H.J. Altermatt, and R. Cowen. 1996. Coamplification in tumors of KRAS2, type 2 inositol 1,4,5 triphosphate receptor gene, and a novel human gene, KRAG. Genomics. 35:207-214.
27. Hoffman, E.P., R.H. Brown, Jr., and L.M. Kunkel. 1987. Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell. 51:919-928.
28. Holt, K.H., and K.P. Campbell. 1998. Assembly of the sarcoglycan complex: insights for LGMD. J. Biol Chem. 273:34667-34670.
29. Holt, K.H., S.B. Waters, S. Okada, K. Yamauchi, S.J. Decker, A.R. Saltiel, D.G. Motto, G.A. Koretzky, and J.E. Pessin. 1996. Epidermal growth factor receptor targeting prevents uncoupling of the Grb2-SOS complex. J. Biol. Chem. 271:8300-8306.
30. 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.
31. 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.
32. Iwata, Y., H. Nakamura, Y. Mizuno, M. Yoshida, E. Ozawa, and M. Shigekawa. 1993. Defective association of dystrophin with sarcolemmal glycoproteins in the cardiomyopathic hamster heart. FEBS Lett. 329:227-231.
33. Jung, D., B. Yang, J. Meyer, J.S. Chamberlain, and K.P. Campbell. 1995. Identification and characterization of the dystrophin anchoring site on β-dystroglycan. J. Biol. Chem. 270:27305-27310.
34. Jung, D., F. Leturcq, Y. Sunada, F. Duclos, P.M. Tome, C. Moomaw, L. Merlini, K. Azibi, M. Chaouch, C. Slaughter, et al. 1996. Absence of gamma-sarcoglycan (35 DAG) in autosomal recessive muscular dystrophy linked to chromosome 13q12. FEBS Lett. 381:15-20.
35. Karpati, G., S. Carpenter, G.E. Morris, K.E. Davies, C. Guerin, and P. Holland. 1993. Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J. Neuropathol. Exp. Neurol. 52:119-128.
36. Khurana, T.S., S.C. Watkins, P. Chafey, J. Chelly, F.M. Tome, M. Fardeau, J.C. Kaplan, and L.M. Kunkel. 1991. Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromuscul. Disord. 1:185-194.
37. Lim, L.E., and K.P. Campbell. 1998. The sarcoglycan complex in limb-girdle muscular dystrophy. Curr. Opin. Neurol. 11:443-452.
38. 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 4q12. Nat. Genet. 11:257-265.
39. Maecker, H.T., S.C. Todd, and S. Levy. 1997. The tetraspanin superfamily: molecular facilitators. FASEB J. 11:428-442.
40. Matsumura, K., J.M. Ervasti, K. Ohlendieck, S.D. Kahl, and K.P. Campbell. 1992. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature. 360:588-591.
41. 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 2D gene. FEBS Lett. 422:27-32.
42. Mizuno, Y., S. Noguchi, H. Yamamoto, M. Yoshida, I. Nonaka, S. Hirai, and E. Ozawa. 1995. Sarcoglycan complex is selectively lost in dystrophic hamster muscle. Am. J. Pathol. 146:530-536.
43. Nguyen, T.M., J.M. Ellis, D.R. Love, K.E. Davies, K.C. Gatter, G. Dickson, and G.E. Morris. 1991. Localization of the DMDL gene-encoded dystrophin-related protein using a panel of nineteen monoclonal antibodies: presence at neuromuscular junctions, in the sarcolemma of dystrophic skeletal muscle, in vascular and other smooth muscles, and in proliferating brain cell lines. J. Cell Biol. 115:1695-1700.
44. Nigro, V., E. de Sa Moreira, G. Piluso, M. Vainzof, A. Belsito, L. Politano, A.A. Puca, M.R. Passos-Bueno, and M. Zatz. 1996a. Autosomal recessive limb-girdle muscular dystrophy, LGMD2F, is caused by a mutation in the delta-sarcoglycan gene. Nat. Genet. 14:195-198.
45. Nigro, V., G. Piluso, A. Belsito, L. Politano, A.A. Puca, S. Papparella, E. Rossi, G. Viglietto, M.G. Esposito, C. Abbondanza, et al. 1996b. Identification of a novel sarcoglycan gene at 5q33 encoding a sarcolemmal 35 kDa glycoprotein. Hum. Mol. Genet. 5:1179-1186.
46. 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.
47. Noguchi, S., E.M. McNally, K. Ben Othmane, Y. Hagiwara, Y. Mizuno, M. Yoshida, H. Yamamoto, C.G. Bönnemann, E. Gussoni, P.H. Demon, et al. 1995. Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science. 270:819-822.
48. Ohlendieck, K., and K.P. Campbell. 1991. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J. Cell Biol. 115:1685-1694.
49. Ohlendieck, K., J.M. Ervasti, K. Matsumura, S.D. Kahl, C.J. Leveille, and K.P. Campbell. 1991. Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron. 7:499-508.
50. Okazaki, Y., H. Okuizumi, T. Ohsumi, O. Nomura, S. Takada, M. Kamiya, N. Sasaki, Y. Matsuda, M. Nishimura, O. Tagaya, et al. 1996. A genetic linkage map of the Syrian hamster and localization of cardiomyopathy locus on chromosome 9qa2.1-b1 using RLGS spot-mapping. Nat. Genet. 13:87-90.
51. Passos-Bueno, M.R., E.S. Moreira, M. Vainzof, S.K. Marie, and M. Zatz. 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. Hum. Mol. Genet. 5:815-820.
52. Petrof, B.J., J.B. Shrager, H.H. Stedman, A.M. Kelly, and H.L. Sweeney. 1993. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA. 90:3710-3714.
53. Phelps, S.F., M.A. Mauser, N.M. Cole, J.A. Rafael, R.T. Hinkle, J.A. Faulkner, and J.S. Chamberlain. 1995. Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum. Mol. Genet. 4:1251-1258.
54. Piccolo, F., S.L. Roberds, M. Jeanpierre, F. Leturcq, K. Azibi, C. Belford, A. Carrie, and D. Recan. 1995. Primary adhalinopathy: a common cause of autosomal recessive muscular dystrophy of variable severity. Nat. Genet. 5:1963-1969.
55. Pons, F., N. Augier, J.O. Leger, A. Robert, P.M. Tome, M. Fardeau, T. Voit, L.V. Nicholson, D. Mornet, and J.J. Leger. 1991. A homologue of dystrophin is expressed at the neuromuscular junctions of normal individuals and DMD patients, and of normal and mdx mice. Immunological evidence. FEBS Lett. 282:161-165.
56. Porter, J.D., J.A. Rafael, R.J. Ragusa, J.K. Brueckner, J.I. Trickett, and K.E. Davies. 1998. The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J. Cell Sci. 111:1801-1811.
57. Rafael, J.A., Y. Sunada, N.M. Cole, K.P. Campbell, J.A. Faulkner, and J.S. Chamberlain. 1994. Prevention of dystrophic pathology in mdx mice by a truncated dystrophin isoform. Hum. Mol. Genet. 3:1725-1733.
58. Rafael, J.A., G.A. Cox, K. Corrado, D. Jung, K.P. Campbell, and J.S. Chamberlain. 1996. Forced expression of dystrophin deletion constructs reveals structure-function correlations. J. Cell Biol. 134:93-102.
59. Roberds, S.L., J.M. Ervasli, R.D. Anderson, K. Ohlendieck, S.D. Kahl, D. Zoloto, and K.P. Campbell. 1993. Disruption of the dystrophin-glycoprotein complex in the cardiomyopathic hamster. J. Biol. Chem. 268:11496-11499.
60. Roberds, S.L., F. Leturcq, V. Allamand, F. Piccolo, M. Jeanpierre, R.D. Anderson, L.E. Lim, J.C. Lee, F.M.S. Tome, N.B. Romero, et al. 1994. Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell. 78:625-633.
61. Rybakova, I.N., and J.M. Ervasti. 1997. Dystrophin-glycoprotein complex is monomeric and stabilizes actin filaments in vitro through a lateral association. J. Biol. Chem. 272:28771-28778.
62. Rybakova, I.N., K.J. Amann, and J.M. Ervasti. 1996. A new model for the interaction of dystrophin with F-actin. J. Biol. Chem. 135:661-672.
63. 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.
64. Scott, A.F., A. Elizaga, J. Morrell, A. Bergen, and M.B. Penno. 1994. Characterization of a gene coamplified with Ki-ras in Y1 murine adrenal carcinoma cells that codes for a putative membrane protein. Genomics. 20:227-230.
65. Straub, V., and K.P. Campbell. 1997. Muscular dystrophies and the dystrophin-glycoprotein complex. Curr. Opin. Neurol. 10:168-175.
66. 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.
67. Straub, V., F. Duclos, D.P. Venzke, J.C. Lee, S. Cutshall, C.J. Leveille, and K.P. Campbell. 1998. Molecular palhogenesis of muscle degeneration in the δ-sarcoglycan-deficient hamster. Am. J. Pathol. 153:1623-1630.
68. 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.
69. 21 mice. Hum. Mol. Genet. 4:1055-1061.
70. Tinsley, J., N. Deconinck, R. Fisher, D. Kahn, S. Phelps, J.M. Gillis, and K. Davies. 1998. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat. Med. 4:1441-1444.
71. Tinsley, J.M., A.C. Potter, S.R. Phelps, R. Fisher, J.I. Trickett, and K.E. Davies. 1996. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature. 384:349-353.
72. Weller, B., G. Karpati, and S. Carpenter. 1990. Dystrophin-deficient mdx muscle fibers are preferentially vulnerable to necrosis induced by experimental lengthening contractions. J. Neurol. Sci. 100:9-13.
73. Wright, M.D., and M.G. Tomlinson. 1994. The ins and outs of the transmembrane 4 superfamily. Immunol. Today. 15:588-594.
74. Xu, H., P. Christmas, X.-R. Wu, U.M. Wewer, and E. Engvall. 1994a. Defective muscle basement membrane and lack of M-laminin in the dystrophic dy/dy mouse. Proc. Natl. Acad. Sci. USA. 91:5572-5576.
75. Xu, H., X.-R. Wu, U.M. Wewer, and E. Engvall. 1994b. Murine muscular dystrophy caused by a mutation in the laminin α2 (Lamα2) gene. Nat. Genet. 8:297-302.
76. Yang, B., D. Jung, D. Motto, J. Meyer, G. Koretzky, and K.P. Campbell. 1995. SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270:11711-11714.
77. Yoshida, M., and E. Ozawa. 1990. Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. (Tokyo). 108:748-752.
78. 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.