Sarcospan-deficient mice maintain normal muscle function

Molecular and Cellular Biology

Volumn 20, Issue 5, 2000, Pages 1669-1677

  Lebakken, Connie S ^a,b,c,d   Venzke, David P ^a,b,c,d   Hrstka, Ronald F ^a,b,c,d   Consolino, Christina M ^a,b,c,d   Faulkner, John A ^a,b,c,d   Williamson, Roger A ^a,b,c,d   Campbell, Kevin P ^a,b,c,d  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b Dept of Obstetrics and Gynecology ^*  (United States)

^c UNIVERSITY OF IOWA   (United States)

^d UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DYSTROPHIN; GLYCOPROTEIN; MEMBRANE PROTEIN; MUSCLE PROTEIN;

ARTICLE; MOUSE; MUSCLE FUNCTION; MUSCULAR DYSTROPHY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SARCOLEMMA; SKELETAL MUSCLE; SMOOTH MUSCLE;

ANIMALS; CARRIER PROTEINS; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MUSCLE, SKELETAL; NEOPLASM PROTEINS;

EID: 0033982722     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.5.1669-1677.2000     Document Type: Article

References (73)

1. 2+-calmodulin binds to the carboxyl-terminal domain of dystrophin. J. Biol. Chem. 271: 6605-6610.
2. Araishi, K., T. Sasaoka, M. Imamura, S. Noguchi, H. Hama, E. Wakabayashi, M. Yoshida, T. Hori, and E. Ozawa. 1999. Loss of the sarcoglycan complex and sarcospan leads to muscular dystrophy in beta-sarcoglycandeficient mice. Hum. Mol. Genet. 8:1589-1598.
3. 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. Betasarcoglycan (A3b) mutations cause autosomal recessive muscular dystrophy with loss of the sarcoglycan complex. Nat. Genet. 11:266-273.
4. Brenman, J. E., D. S. Chao, S. H. Gee, A. W. McGee, S. E. Craven, D. R. Santillano, Z. Wu, F. Huang, H. Xia, M. F. Peters, S. C. Froehner, and D. S. Bredt. 1996. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alphal-syntrophin mediated by PDZ domains. Cell 84:757-767.
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. Brooks, S. V., and J. A. Faulkner. 1988. Contractile properties of skeletal muscles from young, adult and aged mice. J. Physiol. (London) 404:71-82.
7. Bushby, K. M. 1999. The limb-girdle muscular dystrophies - multiple genes, multiple mechanisms. Hum. Mol. Genet. 8:1875-1882.
8. Bushhy, K. M. 1999. Making sense of the limb-girdle muscular dystrophies. Brain 122:1403-1420.
9. Byers, T. J., L. M. Kunkel, and S. C. Watkins. 1991. The subcellular distribution of dystrophin in mouse skeletal, cardiac, and smooth muscle. J. Cell Biol. 115:411-421.
10. Campbell, K. P. 1995. Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80:675-679.
11. Cartaud, A., S. Coutant, T. C. Petrucci, and J. Cartaud. 1998. Evidence for in situ and in vitro association between beta-dystroglycan and the subsynaptic 43K rapsyn protein. Consequence for acetylcholine receptor clustering at the synapse. J. Biol. Chem. 273:11321-11326.
12. Chao, D. S., J. R. Gorospe, J. E. Brenman, J. A. Rafael, M. F. Peters, S. C. Froehner, E. P. Hoffman, J. S. Chamberlain, and D. S. Bredt. 1996. Selective loss of sarcolemmal nitric oxide synthase in Becker muscular dystrophy. J. Exp. Med. 184:609-618.
13. Coral-Vazquez, R., R. D. Cohn, S. A. Moore, J. A. Hill, R. M. Weiss, R. L. Davisson, V. Straub, R. Barresi, D. Bansal, R. F. Hrstka, R. Williamson, and K. P. Campbell. 1999. Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: a novel mechanism for cardiomyopathy and muscular dystrophy. Cell 98:465-474.
14. 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.
15. Crosbie, R. H., C. S. Lebakken, K. H. Holt, D. P. Venzke, V. Straub, J. C. Lee, R. M. Grady, J. S. Chamberlain, J. R. Sanes, and K. P. Campbell. 1999. Membrane targeting and stabilization of sarcospan is mediated by the sarcoglycan subcomplex. J. Cell Biol. 145:153-165.
16. D'Amore, P. A., R. H. Brown, Jr., P. T. Ku, E. P. Hoffman, H. Watanabe, K. Arahata, T. Ishihara, and J. Folkman. 1994. Elevated basic fibroblast growth factor in the serum of patients with Duchenne muscular dystrophy. Ann. Neurol. 35:362-365.
17. 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, K. H. Holt, L. E. Lim, J. R. Sanes, B. L. Davidson, J. A. Faulkner, R. Williamson, and K. P. Campbell. 1998. Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice. J. Cell Biol. 142:1461-1471.
18. Durbeej, M., R. D. Cohn, R. F. Hrstka, S. A. Moore, V. Allamand, B. L. Davidson, R. A. Williamson, and K. P. Campbell. Disruption of the β-sarcoglycan gene reveals pathogenetic complexity of limb-girdle muscular dystrophy type 2E. Mol. Cell, in press.
19. Eberst, R., S. Dai, N. Klugbauer, and F. Hofmann. 1997. Identification and functional characterization of a calcium channel gamma subunit. Pfluegers Arch. 433:633-637.
20. Ervasti, J. M., and K. P. Campbell. 1991. Membrane organization of the dystrophin-glycoprotein complex. Cell 66:1121-1131.
21. 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.
22. Froehner, S. C., M. E. Adams, M. F. Peters, and S. H. Gee. 1997. Syntrophins: modular adapter proteins at the neuromuscular junction and the sarcolemma. Soc. Gen. Physiol. Ser. 52:197-207.
23. Furuse, M., K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita. 1998. Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J. Cell Biol. 141:1539-1550.
24. Gee, S. H., R. W. Blacher, P. J. Douville, P. R. Provost, P. D. Yurchenco, and S. Carbonetto. 1993. Laminin-binding protein 120 from brain is closely related to the dystrophin-assodated glycoprotein, dystroglycan, and binds with high affinity to the major heparin binding domain of laminin. J. Biol. Chem. 268:14972-14980.
25. Gee, S. H., R. Madhavan, S. R. Levinson, J. H. Caldwell, R. Sealock, and S. C. Froehner. 1998. Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J. Neurosci. 18:128-137.
26. Grady, R. M., R. W. Grange, K. S. Lau, M. M. Maimone, M. C. Nichol, J. T. Stull, and J. R. Sanes. 1999. Role of α-dystrobrevin in the pathogenesis of dystrophin-dependent muscular dystrophies. Nat. Cell Biol. 1:215-220.
27. Hack, A. A., C. T. Ly, F. Jiang, C. J. Clendenin, K. S. Sigrist, R. L. Wollmann, and E. M. McNally. 1998. Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J. Cell Biol. 142:1279-1287.
28. Hasegawa, M., A. Cuenda, M. G. Spillantini, G. M. Thomas, V. BueeScherrer, P. Cohen, and M. Goedert. 1999. Stress-activated protein kinase-3 interacts with the PDZ domain of alphal-syntrophin. A mechanism for specific substrate recognition. J. Biol. Chem. 274:12626-12631.
29. 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.
30. Henry, M. D., and K. P. Campbell. 1998. A role for dystroglycan in basement membrane assembly. Cell 95:859-870.
31. 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.
32. Holt, K. H., and K. P. Campbell. 1998. Assembly of the sarcoglycan complex. Insights for muscular dystrophy. J. Biol. Chem. 273:34667-34670.
33. Ibraghimov-Beskrovnaya, O., J. M. Ervasti, C. J. Leveille, C. A. Slaughter, S. W. Sernett, and K. P. Campbell. 1992. Primary structure of dystrophinassociated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
34. Iwata, Y., Y. Pan, T. Yoshida, H. Kanada, and M. Shigekawa. 1998. Alphalsyntrophin has distinct binding sites for actin and calmodulin. FEBS Lett. 423:173-177.
35. Jay, S. D., S. B. Ellis, A. F. McCue, M. E. Williams, T. S. Vedvick, M. M. Harpold, and K. P. Campbell. 1990. Primary structure of the gamma subunit of the DHP-sensitive calcium channel from skeletal muscle. Science 248: 490-492.
36. Jung, D., F. Duclos, B. Apostol, V. Straub, J. C. Lee, V. Allamand, D. P. Venzke, Y. Sunada, C. R. Moomaw, C. J. Leveille, C. A. Slaughter, T. O. Crawford, J. D. McPherson, and K. P. Campbell. 1996. Characterization of delta-sarcoglycan, a novel component of the oligomeric sarcoglycan complex involved in limb-girdle muscular dystrophy. J. Biol. Chem. 271:32321-32329.
37. Jung, D., B. Yang, J. Meyer, J. S. Chamberlain, and K. P. Campbell. 1995. Identification and characterization of the dystrophin anchoring site on beta-dystroglycan. J. Biol. Chem. 270:27305-27310.
38. Kameya, S., Y. Miyagoe, I. Nonaka, T. Ikemoto, M. Endo, K. Hanaoka, Y. Nabeshima, and S. Takeda. 1999. Alpha1-syntrophin gene disruption results in the absence of neuronal-type nitric-oxide synthase at the sarcolemma but does not induce muscle degeneration. J. Biol. Chem. 274:2193-2200.
39. Kaye, D., D. Pimental, S. Prasad, T. Maki, H. J. Berger, P. L. McNeil, T. W. Smith, and R. A. Kelly. 1996. Role of transiently altered sarcolemmal membrane permeability and basic fibroblast growth factor release in the hypertrophic response of adult rat ventricular myocytes to increased mechanical activity in vitro. J. Clin. Investig. 97:281-291.
40. 2+-channel gamma subunit. Nat. Genet. 19:340-347.
41. Lim, L. E., and K. P. Campbell. 1998. The sarcoglycan complex in limbgirdle muscular dystrophy. Curr. Opin. Neurol. 11:443-452.
42. 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.
43. Lo, C. W. 1999. Genes, gene knockouts, and mutations in the analysis of gap junctions. Dev. Genet. 24:1-4.
44. Lumeng, C., S. Phelps, G. E. Crawford, P. D. Waiden, K. Barald, and J. S. Chamberlain. 1999. Interactions between beta 2-syntrophin and a family of microtubule-associated serine/threonine kinases. Nat. Neurosci. 2:611-617.
45. Maecker, H. T., S. C. Todd, and S. Levy. 1997. The tetraspanin superfamily: molecular facilitators. FASEB J. 11:428-442.
46. Matsuda, R., A. Nishikawa, and H. Tanaka. 1995. Visualization of dystrophic muscle libers in mdx mouse by vital staining with Evans blue: evidence of apoptosis in dystrophin-deficient muscle. J. Biochem. (Tokyo) 118:959-964.
47. Mayer, U., G. Saher, R. Fassler, A. Bornemann, F. Echtermeyer, H. von der Mark, N. Miosge, E. Poschl, and K. von der Mark. 1997. Absence of integrin alpha 7 causes a novel form of muscular dystrophy. Nat. Genet. 17:318-323.
48. McNally, E. M., M. Yoshida, Y. Mizuno, E. Ozawa, and L. M. Kunkel. 1994 Human adhalin is alternatively spliced and the gene is located on chromosome 17q21. Proc. Natl. Acad. Sci. USA 91:9690-9694.
49. Morita, K., M. Furuse, K. Fujimoto, and S. Tsukita. 1999. Claudin multigene family encoding four-transmembrane domain protein components of tight junction strands. Proc. Natl. Acad. Sci. USA 96:511-516.
50. Nigro, V., G. Piluso, A. Belsito, L. Politano, A. A. Puca, S. Papparella, E. Rossi, G. Viglietto, M. G. Esposito, C. Abbondanza, N. Medici, A. M. Molinari, G. Nigro, and G. A. Puca. 1996. Identification of a novel sarcoglycan gene at 5q33 encoding a sarcolemmal 35 kDa glycoprotein. Hum. Mol. Genet. 5:1179-1186.
51. Noguchi, S., E. M. McNally, K. Ben Othmane, Y. Hagiwara, Y. Mizuno, M. Yoshida, H. Yamamoto, C. G. Bonnemann, E. Gussoni, P. H. Denton, et al. 1995. Mutations in the dystrophin-associated protein gamma-sarcoglycan in chromosome 13 muscular dystrophy. Science 270:819-822.
52. 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.
53. Ohlendieck, K., J. M. Ervasti, J. B. Snook, and K. P. Campbell. 1991. Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemnia. J. Cell Biol. 112:135-148.
54. Ozawa, E., S. Noguchi, Y. Mizuno, Y. Hagiwara, and M. Yoshida. 1998. From dystrophinopathy to sarcoglycanopathy: evolution of a concept of muscular dystrophy. Muscle Nerve 21:421-438.
55. Roberts, 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.
56. Roberts, S. L., F. Leturcq, V. Allamand, F. Piccolo, M. Jeanpierre, R. D. Anderson, L. E. Lim, J. C. Lee, F. M. Tome, N. B. Romero, et al. 1994. Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell 78:625-633.
57. Rosalki, S. B. 1989. Serum enzymes in disease of skeletal muscle. Clin. Lab. Med. 9:767-781.
58. 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.
59. 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.
60. Schultz, J., U. Hoffmuller, G. Krause, J. Ashurst, M. J. Macias, P. Schmieder, J. Schneider-Mergener, and H. Oschkinat. 1998. Specific interactions between the syntrophin PDZ domain and voltage-gated sodium channels. Nat. Struct. Biol. 5:19-24.
61. 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.
62. Straub, V., and K. P. Campbell. 1997. Muscular dystrophies and the dystrophin-glycoprotein complex, Curr. Opin. Neurol. 10:168-175.
63. Straub, V., F. Duclos, D. P. Venzke, J. C. Lee, S. Cutshall, C. J. Leveille, and K. P. Campbell. 1998. Molecular pathogenesis of muscle degeneration in the delta-sarcoglycan-deficient hamster. Am. J. Pathol. 153:1623-1630.
64. Straub, V., A. J. Ettinger, M. Durneej, D. P. Venzke, S. Cutshall, J. R. Sanes, and K. P. Campbell. 1999. Epsilon-sarcoglycan replaces alpha-sarcoglycan in smooth muscle to form a unique dystrophin-glycoprotein complex. J. Biol. Chem. 274:27989-27996.
65. 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.
66. Taverna, D., M. H. Disatnik, H. Rayburn, R. T. Bronson, J. Yang, T. A. Rando, and R. O. Hynes. 1998. Dystrophic muscle in mice chimeric for expression of alpha5 integrin. J. Cell Biol. 143:849-859.
67. Tybulewicz, V. L., C. E. Crawford, P. K. Jackson, R. T. Bronson, and R. C. Mulligan. 1991. Neonatal lethality and lymphopenia in mice with a homozygous disruption of the c-abl proto-oncogene. Cell 65:1153-1163.
68. 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.
69. Wissenbach, U., E. Bosse-Doenecke, D. Kreise, A. Ludwig, M. Murakami, F. Hofmann, and V. Flockerzi. 1998. The structure of the murine calcium channel gamma-subunit gene and protein. Biol. Chem. 379:45-50.
70. Wright, M. D., and M. G. Tomlinson. 1994. The ins and outs of the transmembrane 4 superfamily. Immunol. Today 15:588-594.
71. Yang, B., D. Jung, D. Motto, J. Meyer, G. Korelzty, and K. P. Campbell. 1995. SH3 domain-mediated interaction of dystroglycan and Grb2. J. Biol. Chem. 270:11711-11714.
72. Yeager, M. 1998. Structure of cardiac gap junction intercellular channels. J. Struct. Biol. 121:231-245.
73. Yeager, M., V. M. Unger, and M. M. Falk. 1998. Synthesis, assembly and structure of gap junction intercellular channels. Curr. Opin. Struct. Biol. 8:517-524.