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

Volumn 69, Issue 1, 1996, Pages 1-10

  Ohlendieck, Kay ^a  

^a UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

Adhalin; Dystrophin glycoprotein complex; Muscular dystrophy; Syntrophin; Utrophin dystroglycan

Indexed keywords

ACTIN; ADHALIN; CYTOSKELETON PROTEIN; DYSTROGLYCAN; DYSTROPHIN; GLYCOPROTEIN; LAMININ BINDING PROTEIN; UTROPHIN;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CARDIOMYOPATHY; COMPLEX FORMATION; CYTOSKELETON; DUCHENNE MUSCULAR DYSTROPHY; EXTRACELLULAR MATRIX; HEART MUSCLE; HUMAN; MUSCLE CELL; MUSCLE FIBER CONTRACTION; MUSCULAR DYSTROPHY; NEUROMUSCULAR SYNAPSE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REVIEW; SARCOLEMMA; SKELETAL MUSCLE;

EID: 0030026119     PISSN: 01719335     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (107)

1. Adams, M. E., M. H. Butler, T. M. Dwyer, M. F. Peters, A. A. Murnae, S. C. Froehner: Two forms of mouse syntrophin, a 58 kD dystrophin-associated protein, differ in primary structure and tissue distribution. Neuron 11, 531-540 (1993).
2. Ahn, A. H., L. M. Kunkel: The structural and functional diversity of dystrophin. Nature Genet. 3, 283-291 (1993).
3. Ahn, A. H., M. Yoshida, M. S. Anderson, C. A. Feener, S. Selig, Y. Hagiwara, E. Ozawa, L. M. Kunkel: Cloning of human basic Al, a destinct 59-kDa dystrophin-associated protein encoded on chromosome 8q23-24. Proc. Natl. Acad. Sci. USA 91, 4446-4450 (1994).
4. Anderson, M. S., L. M. Kunkel: The molecular and biochemical basis of Duchenne muscular dystrophy. Trends Biochem. Sci. 17, 289-292 (1992).
5. Ascadi, G., G. Dickson, D. R. Love, A. Jani, F. S. Walsh, A. Gurusinghe, J. A. Wolff, K. E. Davies: Human dystrophin expression in mdx mice after intramuscular injection of DNA constructs. Nature 352, 815-818 (1991).
6. Beggs, A. H., E. P. Hoffman, J. R. Snyder, K. Arahata, L. Specht, F. Shapiro. C. Angelini, H. Sugita, L. M. Kunkel: Exploring the molecular basis for variability among patients with Becker muscular dystro-phy: dystrophin gene and protein studies. Am. J. Hum Genet. 49, 54-67 (1991).
7. Bewick, G. S., L. V B Nicholson, C. Young, E. O'Donnell, C. R. Slater: Different distribution of dystrophin and related proteins at nerve-muscle junctions. Neuroreport 3, 857-860 (1992).
8. Bieber, F. R., E. P. Hoffmann: Duchenne and Becker muscular dystrophies: genetics, prenatal diagnosis, and future prospects. Clin. Periantol. 17, 845-865 (1990).
9. Blake, D. J., J. M. Tinsley, K. E. Davies: The emerging family of dystrophin-related proteins. Trends Cell Biol. 4, 19-23 (1994).
10. Bowe, M. A., K. A Deyst, J. D. Leszyk, J. R. Fallon: Identification and purification of an agrin receptor from torpedo postsynaptic membranes: a heteromeric complex related to the dystroglycans. Neuron 12, 1173-1180 (1994).
11. Bulfield, G., W. G Silver, P. A. L. Wight, K. J. Moore: X-chromosome-linked muscular dystrophy (mdx) in the mouse. Proc. Natl. Acad. Sci. USA 81, 1189-1192 (1984).
12. Campanelli, J. T., S. L. Roberds, K. P. Campbell, R. H. Scheller: A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering. Cell 77, 663-674 (1994).
13. Campbell, K. P., S. D. Kahl: Association of dystrophin and an integral glycoprotein. Nature 338, 259-262 (1989).
14. Campbell, K. P.: Three muscular dystrophies: loss of cytoskeleton-extracellular matrix linkage. Cell 80, 675-679 (1995).
15. Cohen, M. W., C. Jacobson, E. W. Godfres, K. P. Campbell, S. Carbonetto: Distribution of alpha-dystroglycan during embryonic nerve-muscle synaptogenesis. J. Cell Biol. 129, 1093-1101 (1995).
16. Cooper, B. J.: Animai models of Duchenne and Becker muscular dystrophy. Brit. Med. Bull. 45, 703-718 (1989).
17. Cox, G. A., N. M. Cole, K. Matsumura, S. F. Phelps, S. D. Hauschka, K. P. Campbell, J. A. Faulkner, J. S. Chamberlain: Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity. Nature 364, 725-729 (1993).
18. Cox, G. A., Y. Sunada, K. P. Campbell, J. S. Chamberlain: Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy. Nature Genet. 8, 333-339 (1994).
19. Dubowitz, V.: Myoblast transfer in muscular dystrophy: panacea or pie in the sky? Neuromusc. Disord. 2, 305-310 (1992).
20. Emery, A. E. H.: Duchenne muscular dystrophy. Oxford Monographs on Medical Genetics No. 24. Oxford University Press. Oxford 1993.
21. Emery, A. E. H.: Some unanswered questions in Duchenne muscular dystrophy. Neuromusc. Disord. 4, 301-303 (1994).
22. Engel, A. G., M. Yamamoto, K. H. Fischbeck: Dystrophinopathies. In: A. G. Engel, M. Yamamoto, K.M.Fischbeck (eds.): Myology. Second edition. Vol. 2. Part. 3. pp. 1133-1187. McGraw-Hill, Inc. New York 1994.
23. Ervasti, J. M., K. Ohlendieck, S. D. Kahl, M. G. Gaver, K. P. Campbell: Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345, 315-319 (1990).
24. Ervasti, J. M., K. P. Campbell: Membrane organization of the dystrophin-glycoprotein complex. Cell 66, 1121-1131 (1991).
25. Ervasti, J. M., K. P. Campbell: Dystrophin and the membrane skeleton. Curr. Opin. Cell Biol. 5, 82-87 (1993).
26. Ervasti, J. M., K. P. Campbell: A role for the dystrophin-glycoprotein complex as a transmembrane linker between laminin and actin. J. Cell Biol. 122, 809-823 (1993).
27. Ervasti, J. M. S. L. Roberds, R. D. Anderson, N. J. H. Sharp, J. N. Kornegay, K. P. Campbell: Alpha-dystroglycan deficiency correlates with elevated serum creatine kinase and decreased muscle contraction tension in golden retriever muscular dystrophy. FEBS Lett. 350, 173-176 (1994).
28. Fardeau, M., K. Matsumura, F. M. Tome, H. Collin, F. Leturcq, J. C. Kaplan, K. P. Campbell: Deficiency of the 50 kDa dystrophin associated glycoprotein (adhalin) in severe autosomal recessive muscular dystrophies in children native from European countries C.R. Acad. Sci. (France) 316, 799-804 (1993).
29. Fong. P., P. R. Turner, W. F. Denetclaw, R. A.Steinhardt: Increased activity of calcium leak channels in myotubes of Duchenne human and mdx mouse origin. Science 250, 673-676 (1990).
30. Gee, S. H., R. W. Blacher, P. J. Douville, P. R. Provost, P. D. Yurchenco, S. Carbonetto: Laminin-binding protein 120 from brain is closely related to the dystrophin-associated glycoprotein, dystroglycan, and binds with high affinity to the major heparin binding domain of laminin. J. Biol. Chem. 268, 14972-14980 (1993).
31. Gee, S. H., F. Montanaro, M. H. Lindenbaum, S. Carbonetto: Dystroglycan-alpha, a dystrophin-associated glycoprotein, is a functional agrin receptor. Cell 77, 675-686 (1994).
32. Griggs, R. C., R. T. Moxley, J. R. Mendell, G. M.Fenichel, M. H. Brooke, A. Pestronk, J. P. Miller, V. A. Cwik, S. Pandya, J. Robinson, W. King, L. Signore, J. Schierbecker, J. Florence, N. Matheson-Burden, B. Wilson: Duchenne dystrophy: randomized, controlled trial of prednisone (18 month) and azathioprine (12 months). Neurology 43, 520-527 (1993).
33. Gussoni. E., G. K. Pavlath, A. M. Lanctot, K. R. Sharma, R. G. Miller, L. Steinman, H. M. Blau: Normal dystrophin transcripts detected in Duchenne muscular dystrophy patients after myoblast transplantation. Nature 356, 435-438 (1992).
34. Hardiman, O.: Dystrophin deficiency, altered cell signaling and fibre hypertrophy. Neuromusc. Disord. 4, 305-315 (1994).
35. Helliwell, T. R., N. T. Man, G. E. Morris, K. E. Davies: The dystrophin-related protein, utrophin, is expressed on the sarcolemma of regenerating human skeletal muscle fibers in dystrophies and inflammatory myopathies. Neuromusc. Disord. 2, 177-184 (1992).
36. Hoch, W., J. T. Campanelli, R. H. Scheller: Agrin-induced clustering of acetylcholine receptors; a cytoskeletal link. J. Cell Biol. 126, 1-4 (1994).
37. Hoffman, E. P., K. H. Fischbeck, R. H. Brown, M. Johson, R. Medori. J. D. Loike, J. B. Harris, R. Waterston, M. Brooke, L. Specht, W. Kupsky, J. Chamberlain, C. T. Caskey, F. Shapiro, L. M. Kunkel: Characterization of dystrophin in muscle-biopsy specimens from patients with Duchenne's or Becker's muscular dystrophy. N. Engl. J. Med. 318, 1363-1368 (1988).
38. Hutter, O. F.: The membrane hypothesis of Duchenne muscular dystrophy: quest for functional evidence. J. Inher. Metab. Dis. 15, 565-577 (1992).
39. Ibraghimov-Beskrovnaya, O., J. M. Ervasti, C. J. Leveille, C. A. Slaughter, S. W. Sernett, K. P. Campbell: Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696-702 (1992).
40. Jennekens, F. G. I., L. P. ten Kate, M. de Visser. A. R. Wintzen. Duchenne and Becker muscular dystrophies. In: A. E. H. Emery (ed.): Diagnostic Criteria for Neuromuscular Disorders. pp. 9-13 European Neuro Muscular Centre. Baarn 1994.
41. Karparti, G., G. Acsadi: The potential for gene therapy in Duchenne muscular dystrophy and other genetic diseases. Muscle & Nerve 16, 1141-1153 (1993).
42. Karparti, G., D. Ajdukovic, D. Arnold, R. B. Gledhill, R. Guttmann, P. Holland, P. A. Koch, E. Shoubridge, D. Spence, M. Vanasse, G. V. Watters, M. Abrahamowicz, C. Duff, R. G. Worton: Myoblast transfer in Duchenne muscular dystrophy. Ann, Neurol. 34. 8-17 (1993).
43. Karparti, G., S. Carpenter, G. E. Morris, K. E. Davies, C Guerin, P. Holland: Localization and quantitation of the chromosome 6-encoded dystrophin-related protein in normal and pathological human muscle. J. Neuropathol. Exp. Neurol. 52, 119-128 (1993).
44. Khurana, T. S., E. P. Hofman, L. M. Kunkel: Identification of a chromosome 6-encoded dystrophin-related protein. J. Biol. Chem. 265, 16717-16720 (1990).
45. Klitsch, R., J. M. Ervasti, W. Arnold, K. P. Campbell, A. O. Jorgensen: Dystrophin-glycoprotein complex and Iaminin colocalize to the sarcolemma and transverse tubules of cardiac muscle. Circ. Res. 72, 349-360 (1993).
46. Koenig, M., A. P. Monaco, L. M. Kunkel: The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53. 219-228 (1988).
47. Levine, B. A., A. J. G. Moir, V. B. Pathell, S. V. Perry: Binding sites involved in the interaction of actin with the N-terminal region of dystrophin. FEBS Lett. 298, 44-48 (1992).
48. Lindenbaum, M. H., S. Carbonetto: Dystrophin and partners at the ceil surface. Curr. Biol. 3, 109-111 (1993).
49. Love, D. R., D. F. Hill, G. Dickson, N. K. Spurr, B. C. Byth, R. F. Marsden, F. S. Walsh, Y. H. Edwards, K. E. Davies: An autosomal transcript in skeletal muscle with homology to dystrophin. Nature 339, 55-58 (1989).
50. Love, D. R., B. C. Byth, J. M. Tinsley, D. J. Blake, K. E. Davies: Dystrophin and dystrophin-related proteins: a review of protein and RNA studies. Neuromus. Disord. 3, 5-21 (1993).
51. Matsumura, K., J. M. Ervasti, K. Ohlendieck, S. D. Kahi, K. P. Campbell: Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse. Nature 360, 588-591 (1992).
52. Matsumura, K., F. M. S. Tome, H. Collin, K. Azibi, M. Chaouch. J. C. Kaplan, M. Fardeau, K. P. Campbell: Deficiency of the 50K dystrophin-associated glycoprotein in severe childhood autosomal recessive muscular dystrophy. Nature 359, 320-322 (1992).
53. Matsumura, K., K. P. Campbell: Deficiency of dystrophin-associated proteins: A common mechanism leading to muscle cell necrosis in severe childhood muscular dystrophies. Neuromusc. Disord. 3, 109-118 (1993).
54. Matsumura, K., I. Nonaka, K. Arahata, K. P. Campbell: Partial deficiency of dystrophin-associated proteins in a young girl with sporadic myopathy and normal karyotype. Neurology 43, 1267-1268 (1993).
55. Matsumura, K., I. Nonaka, K. P. Campbell: Abnormal expression of dystrophin-associated proteins in Fukuyma-type cogenital muscular dystrophy. Lancet 341, 521-522 (1993).
56. Matsumura, K., I. Nonaka, F. M. S. Tome, K. Arahata, H. Collin, F Leturcq. D. Recan, J. C. Kaplan, M. Fardeau, K. P. Campbell: Mild deficiency of dystrophin-associated proteins in Becker muscular dystrophy patients having in-frame deletions in the rod domain of dystrophin. Am. J. Hum. Genet. 53, 409-416 (1993).
57. Matsumura, K., F. M. S. Tome, H. Collin, F. Leturcq, M. Jeanpierre, J.-C. Kaplan, M. Fardeau, K. P. Campbell: Expression of dystrophin-associated proteins in dystrophin-positive muscle fibers (revertants) in Duchenne muscular dystrophy. Neuromusc. Disord. 4, 115-120 (1994).
58. Menke, A., H. Jockusch: Decreased osmotic stability of dystrophin-less muscle cells from mdx mouse. Nature 349, 69-71 (1991).
59. Mizuno, Y., S. Noguchi, H. Yamamoto, M. Yoshida, A. Suzuki, Y. Hagiwara, Y. K. Hayashi, K. Arahata, I. Nonaka, S. Hirai, E. Ozawa: Selective defect of sarcoglycan complex in severe childhood autosomal recessive muscular dystrophy muscle. Biochem. Biophys. Res. Commun. 203, 979-983 (1994).
60. Monaco, A. P., R. L. Neve, C. Coletti-Feener, C. J. Bertelson, D. M. Kurnit, L. M. Kunkel: Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 323, 646-650 (1986).
61. Muligan, R. C.: The basic science of gene therapy. Science 260, 926-932 (1993).
62. Mutoni, F. M. Cau, A. Ganau, R. Congui, G. Arvedi, A. Mateddu, M. G. Marrosu, C. Cianchetti, G. Realdi, A. Cao: Brief report: deletion of the dystrophin muscle-promoter region associated with X-linked dilated cardiomyopathy. N. Engl. J. Med 329, 960-961 (1993).
63. Mutoni, F., M. A. Melis, A. Ganau, V. Dubowitz: Transcription of the dystrophin gene in normal tissues and in skeletal muscle of a family with X-linked dilated cardiomyopathy. Am. J. Hum. Genet. 56, 151-157 (1995).
64. Nguyen, T. M., J. M. Ellis, D. R. Love, K. E. Davies, K. C. Gatter, G. E. Morris: 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 (1991).
65. Ohlendieck. K., K. P. Campbell: Dystrophin constitutes 5% of membrane cytoskeleton in skeletal muscle. FEBS Lett. 283, 230-234 (1991).
66. Ohlendieck, K , K. P. Campbell: Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J. Cell Biol. 115, 1685-1694 (1991).
67. Ohlendieck, K., J. M. Ervasti, K. Matsumura. S. D. Kahl, C. J. Leveille, K. P. Campbell: Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7, 499-508 (1991).
68. Ohlendieck, K., J. M. Ervasti, J. B. Snook, K. P. Campbell: Dystrophin-glycoprotein complex is highly enriched in isolated skeletal muscle sarcolemma. J. Cell Biol. 112, 135-148 (1991).
69. Ohlendieck, K., K. Matsumura, V. V. Ionasescu, J. A. Towbin, E. P. Bosch, S. L. Weinstein, S. W. Sernett, K. P. Campbell: Duchenne muscular dystrophy: deficiency of dystrophin-associated proteins in the sarcolamma. Neurology 43, 795-800 (1993).
70. Partridge, T. A., J. E. Morgan, G. R. Coulton, E. P. Hoffman, L. M. Kunkel: Conversion of mdx myofibres from dystrophin-negative to positive by injection of normal myoblasts. Nature 337, 176-179 (1989).
71. Partridge, T. A.: Invited review: Myoblast tranfser: a possible therapy for inherited myopathies? Muscle & Nerve 14, 197-212 (1991).
72. Peters, M. F., N. R. Kramarcy, R. Sealock, S. C. Froehner. Beta 2-syntrophin: localization at the neuromuscular junction in skeletal muscle. Neuroreport 5, 1577-1580 (1994).
73. Petrof, B. J., J. B. Schrager, H. H. Stedman, A. M. Kelly, H. L. Sweeney: Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc. Natl. Acad. Sci. USA 90, 3710-3714 (1993).
74. Pons, F., N. Augier, J. O. C. Leger, A. Roberts, F. M. S. Tome, M Fardeau, T. Voit, L. V. B. Nicholson, D. Mornet, J. J. Leger: A homologue of dystrophin is expressed at the neuromuscular junctions of normal individuals and DMD patients, and of normal and mdx mice. FEBS Lett. 282. 161-165 (1991).
75. Roberds, S. L., R. D. Anderson, O. Ibraghimov-Beskrovnaya, K. P. Campbell: Primary structure and muscle-specific expression of the 50-kDa dystrophin-associated glycoprotein (adhalin), J. Biol. Chem. 268, 23739-23742 (1993).
76. Roberds, S. L., J. M. Ervasti, R. D. Anderson, K. Ohlendieck, S. D. Kahl, D. Zoloto, K. P. Campbell: Disruption of the dystrophin-glycoprotein complex in the cardiomyopathic hamster. J. Biol. Chem. 268, 11496-11499 (1993).
77. 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, M. Fardeau, J. S. Beckmann, J.-C. Kaplan, K. P. Campbell: Missense mutations in the adhalin gene linked to autosomal recessive muscular dystrophy. Cell 78, 625-633 (1994).
78. Romero, N. B., F. M. S. Tome, F. Leturcq, F. E. Kerch, K. Azibi, L. Bachner, R. D. Anderson, S. L. Roberds, K. P. Campbell, M. Fardeau, J.-C. Kaplan: Genetic heterogeneity of severe childhood autosomal recessive muscular dystrophy with adhalin (50 kDa dystrophinassociated glycoprotein) deficiency. C.R. Acad. Sci. (France) 317, 70-76 (1994).
79. Sealock, R., S. C. Froehner: Dystrophin-associated proteins and synapse formation: is alpha-dystroglycan the agrin receptor? Cell 77, 617-619 (1994).
80. Sewry, C. A., K. Matsumura, K. P. Campbell, V. Dubowitz: Expression of dystrophin-associated glycoproteins and utrophin in carriers of Duchenne muscular dystrophy. Neuromusc. Disord. 4, 401-409 (1994).
81. Sewry, C. A., K. Matsumura, A. Sansome, K. P. Campbell, V. Dubowitz: Deficiency of the 50 kDa dystrophin-associated glycoprotein and abnormal expression of utrophin in two asian cousins with variable expression of severe childhood autosomal recessive muscular dystrophy. Neuromusc. Disord. 4, 121-129 (1994).
82. Sharma, K. R., M. A. Mynhier, R. G. Miller: Cyclosporine increases muscle force generation in Duchenne muscular dystrophy. Neurology 43, 527-532 (1993).
83. Sicinski, P., Y. Geng. A. S. Ryder-Cook, E. A. Barnard, M. G. Darlison. P. J. Barnard: The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244, 1578-1580 (1989).
84. Stedman, H. H., H. L. Sweeney, J. B. Shrager, H. C. Maguire, R. A. Panettieri, B. Petrof, M. Narusawa, J. M. Leferovich, J. T. Sladky, A. M. Kelly: The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352, 536-539 (1991).
85. Sunada, Y., S. M. Bernier, C. A. Kozak, Y. Yamada, K. P. Campbell: Deficiency of merosin in dystrophic dy mice and genetic linkage of laminin M chain gene to dy locus. J. Biol. Chem. 269, 13729-13732 (1994).
86. Suzuki, A., M. Yoshida, H. Yamamoto, E. Ozawa: Glycoprotein-binding site of dystrophin is confined to the cystein-rich domain and the first half of the carboxy-terminal domain. FEBS Lett. 308, 154-160 (1992).
87. Suzuki, A., M. Yoshida, K. Hayashi, Y. Mizuno, Y. Hagiwara, E. Ozawa: Molecular organization at the glycoprotein-complex binding site of dystrophin: Three dystrophin-associated proteins bind directly to the carboxy-terminal portion of dystrophin. Eur. J. Biochem. 220, 283-292 (1994).
88. Tinsley, J. M., D. J. Blake, A. Roche, U. Fairbrother, J. Riss, B. C. Byth, A. E. Knight, J. Kendrick-Jones, G. K. Suthers, D. R. Love, Y. H. Edwards, K. E. Davies: Primary structure of dystrophin-related protein. Nature 360, 591-593 (1992).
89. Tinsley, J. M., D. J. Blake, M. Pearce, A. E. Knight, J. Kendrick-Jones, K. E. Davies: Dystrophin and related proteins. Curr. Opin. Genet. Dev. 3, 484-490 (1993).
90. Tinsley, J. M., K. E. Davies: Utrophin: a potential replacement for dystrophin? Neuromusc. Disord. 3, 537-539 (1993).
91. Tinsley, J. M., D. J. Blake, R. A. Zuellig, K. E. Davies: Increasing complexity of the dystrophin-associated protein complex. Proc. Natl. Acad. Sci. USA 91, 8307-8313 (1994).
92. Toescu, V., R. H. T. Edwards. M. J. Jackson: Treatment of Duchenne muscular dystrophy: history and future directions. Bas. Appl. Myol. 4, 217-227 (1994).
93. Tome, F. M. S., T. Evangelista, A. Leclerc, Y. Sunada, E. Manole, B. Estournet, A. Barois, K. P. Campbell, M. Fardeau: Congenital muscular dystrophy with merosin deficiency. C.R. Acad. Sci. (France) 317, 351-357 (1994).
94. Torres, L. F. B., L. W. Duchen: The mutant mdx: inherited myopathy in the mouse. Brain 110, 269-299 (1987).
95. Towbin, J. A., J. F. Hejtmancik, P. Brink, B. Gelb, X. M. Zhu, J. S. Chamberlain, E. R. B. McCabe, M. Swift: X-linked dilated cardiomyopathy: molecular genetic evidence of linkage to the Duchenne muscular dystrophy (dystrophin) gene at Xp21 locus. Circulation 87, 1854-1865 (1993).
96. Turner, P. R., P. Fong, W. F. Denetclaw, R. A. Steinhardt: Increased calcium influx in dystrophic muscle. J. Cell Biol. 115, 1701-1712 (1991).
97. Watkins, B. C., E. P. Hoffman, H. S. Slayter, L. M. Kunkel: Immunoelectron microscopic localization of dystrophin in myofibers. Nature 333, 863-866 (1988).
98. Way, M., B. Pope, R. A. Cross, J. Kendrick-Jones, A. G. Weeds: Expression of the N-terminal domain of dystrophin in E.coli and demonstration of binding to F-actin. FEBS Lett. 301, 243-245 (1992).
99. Yamada, H., T. Shimizu, T. Tanaka, K. P. Campbell, M. Matsumura: Dystroglycan is a binding protein of laminin and merosin in peripheral nerve. FEBS Lett. 352, 49-53 (1994).
100. Yamamoto, H., Y. Hagiwara, Y. Mizuno, M. Yoshida, E. Ozawa: Heterogeneity of dystrophin-associated proteins. J. Biochem. 114, 132-139 (1993).
101. Yamanouchi, Y., Y. Mizuno, H. Yamamoto, M. Takemitsu, M. Yoshida, I. Nonaka, E. Ozawa; Selective defect in dystrophin-associated glycoproteins 50DAG (A2) and 35DAG (A4) in the dystrophic hamster: an animal model for severe childhood autosomal recessive muscular dystrophy (SCARMD). Neuromus. Disord. 4. 49-54 (1994).
102. Yang, B., O. Ibraghimov-Beskrovnaya, C. R. Moomav, C. A. Slaughter. K. P. Campbell: Heterogeneity of the 59-kDa dystrophin-associated protein revealed by cDNA cloning and expression. J. Biol. Chem. 269, 6040-6044 (1994).
103. Yang, B., D. Jung, J. A. Rafael, J. S. Chamberlain, K. P. Campbell: Identification of alpha-syntrophin binding to syntrophin triplet, dystrophin and utrophin. J. Biol. Chem. 270, 4975-4978 (1995).
104. Yoshida, M., E. Ozawa: Glycoprotein complex anchoring dystrophin to sarcolemma. J. Biochem. 108, 748-752 (1990).
105. Yoshida, M., Y. Mizuno, K. Hayashi, I. Nonaka, E. Ozawa: A dystrophin-associated glycoprotein, A3a (One of 43DAG Doublets), is retained in Duchenne muscular dystrophy. J. Biochem. 114, 634-639 (1993).
106. Yoshida, M., A. Suzuki, H. Yamamoto, S. Noguchi, Y. Mizuno. E. Ozawa: 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 (1994).
107. Zatz, M., K. Mutsumura, M. Vainzof, M. R. Passos-Bueno, R. C. Pavanello, S. K. Marie, K. P. Campbell: Assessment of the 50-kDa dystrophin-associated glycoprotein in Brazilian patients with severe childhood autosomal recessive muscular dystrophy. J. Neurol. Sci. 123, 122-128 (1994).