Dystrophin and utrophin: Genetic analyses of their role in skeletal muscle

Microscopy Research and Technique

Volumn 48, Issue 3-4, 2000, Pages 155-166

  Rafael, Jill A ^a   Brown, Susan C ^b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DYNAMIC MODE DECOMPOSITION; MAMMALS; MUSCLE;

DUCHENNE MUSCULAR DYSTROPHIES; DYSTROPHIN; GENETIC ANALYSIS; PERIPHERAL PROTEINS; PROTEIN MUTATIONS; SKELETAL MUSCLE; TRANS-MEMBRANE PROTEINS; TRANSGENIC MICE; TRANSMEMBRANE PROTEINS; UTROPHIN;

PROTEINS;

DYSTROPHIN; UTROPHIN;

ANIMAL TISSUE; ARTICLE; DUCHENNE MUSCULAR DYSTROPHY; GENE FUNCTION; GENE MUTATION; GENETIC ANALYSIS; MOUSE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SKELETAL MUSCLE;

ANIMALIA; MUS MUSCULUS;

EID: 0033966105     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0029(20000201/15)48:3/4<155::AID-JEMT4>3.0.CO;2-0     Document Type: Article

References (109)

1. Ahmed N, Nguyen TM, Morris G E. 1998. Flexible hinges in dystrophin. Biochem Soc Trans 26:8310.
2. Ahn AH, Kunkel LM. 1993. The structural and functional diversity of dystrophin. Nat Genet 3:283-291.
3. Ahn AH, Kunkel LM. 1995. Syntrophin binds to an alternatively spliced exon of dystrophin. J Cell Biol 128:363-371.
4. Amann KJ, Renley BA, Ervasti JM. 1998. A cluster of basic repeats in the dystrophin rod domain binds F-actin through an electrostatic interaction. J Biol Chem 273:28419-28423.
5. Beggs AH, Hoffman EP, Snyder JR, Arahata K, Specht L, Shapiro F, Angelini C, Sugita H, Kunkel LM. 1991. Exploring the molecular basis for variability among patients with Becker muscular dystrophy: dystrophin gene and protein studies. Am J Hum Genet 49:54-67.
6. Bewick GS, Nicholson LB, Young C, Odonnell E, Slater CR. 1992. Different distributions of dystrophin and related proteins at nerve muscle junctions. Neuroreport 3:857-860.
7. Bies RD, Caskey CT, Fenwick R. 1992a. An intact cysteine-rich domain is required for dystrophin function. J Clin Invest 90:666-672.
8. Bies RD, Phelps SF, Cortez MD, Roberts R, Caskey CT, Chamberlain JS. 1992b. Human and murine dystrophin mRNA transcripts are differentially expressed during skeletal muscle, heart, and brain development. Nucleic Acids Res 20:1725-1731.
9. Bork P, Sudol M 1994. The WW domain: a signalling site in dystrophin? Trends Biochem Sci 19:531-533.
10. Bowen DC, Sugiyama J, Ferns M, Hall ZW. 1996. Neural agrin activates a high-affinity receptor in c2 muscle-cells that is unresponsive to muscle agrin. J Neurosci 16:3791-3797.
11. Bowen DC, Park JS, Bodine S, Stark JL, Valenzuela DM, Stitt TN, Yancopoulos GD, Lindsay RN, Glass DJ, DiStefano PS. 1998. Localization and regulation of MuSK at the neuromuscular junction. Dev Biol 199:309-319.
12. Bredt DS. 1996. Targeting nitric oxide to its targets. Proc Soc Exp Biol Med 211:41-48.
13. Bredt DS. 1998. No skeletal muscle derived relaxing factor in Duchenne muscular dystrophy. Proc Natl Acad Sci USA 95:14592-14593.
14. Brenman JE, Chao DS, Xia HH, Aldape K, Bredt DS. 1995. Nitricoxide synthase complexed with dystrophin and absent from skeletal-muscle sarcolemma in duchenne muscular-dystrophy. Cell 82:743-752.
15. Brenman JE, Chao DS, Gee SH, Mcgee AW, Craven SE, Santillano DR, Wu Z, Huang F, Xia HH, Peters MF, Froehner SC, Bredt DS. 1996. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and α 1-syntrophin mediated by PDZ domains. Cell 84:757-767.
16. Bulfield G, Siller WG, Wight P A, Moore KJ. 1984. X chromosome-linked muscular dystrophy (mdx) in the mouse. Proc Natl Acad Sci USA 81:1189-1192.
17. Campanelli JT, Roberds SL, Campbell KP, Scheller RH. 1994. Role for dystrophin-associated glycoproteins and utrophin in agrin-induced achr clustering. Cell 77:663-674.
18. Chang WJ, Iannaccone ST, Lau KS, Masters BS, Mccabe TJ, Mcmillan K, Padre RC, Spencer MJ, Tidball JG, Stull JT. 1996. Neuronal nitric-oxide synthase and dystrophin-deficient muscular-dystrophy. Proc Natl Acad Sci USA 93:9142-9147.
19. Cho SI, Ko J, Patton BL, Sanes JR, Chiu AY. 1998. Motor neurons and Schwann cells distinguish between synaptic and extrasynaptic isoforms of laminin. J Neurobiol 37:339-358.
20. Colledge M, Froehner SC. 1998. Signals mediating ion channel clustering at the neuromuscular junction. Curr Opin Neurol 8:357-363.
21. Corrado K, Mills PL, Chamberlain JS. 1994. Deletion analysis of the dystrophin-actin binding domain. FEBS Lett 344:255-260.
22. Corrado K, Rafael JA, Mills PL, Cole NM, Faulkner JA, Wang K, Chamberlain JS. 1996. Transgenic mdx mice expressing dystrophin with a deletion in the actin-binding domain display a mild Becker phenotype. J Cell Biol 134:873-884.
23. Cox GA, Cole NM, Matsumura K, Phelps SF, Hauschka SD, Campbell KP, Faulkner JA, Chamberlain JS. 1993. Overexpression of dystrophin in transgenic mdx mice eliminates dystrophic symptoms without toxicity [see comments]. Nature 364:725-729.
24. Cox GA, Sunada Y, Campbell KP, Chamberlain JS. 1994. Dp71 can restore the dystrophin-associated glycoprotein complex in muscle but fails to prevent dystrophy [see comments]. Nat Genet 8:333-339.
25. Crosbie RH, Straub V, Venzke DP, Yun HY, Chamberlain JS, Dawson VL, Dawson TM, Campbell KP. 1997. Dystrophin and nNOS double knockout mice maintain dystrophic phenotype. Faseb J 11:3281-3281.
26. Crosbie RH, Straub V, Yun HY, Lee JC, Rafael J, Chamberlain JS, Dawson VL, Dawson T, Campbell KP. 1998. mdx muscle pathology is independent of nNOS pertubation. Hum Mol Genet 7:823-829.
27. Crosbie RH, Lebakken CS, Holt KH, Venzke DP, Straub V, Lee JC, Grady RM, Chamberlain JS, Sanes JR, Campbell KP. 1999. Membrane targeting and stabilization of sarcospan is mediated by the sarcoglycan subcomplex. J Cell Biol 145:153-165.
28. Culligan KG, Mackey AJ, Finn DM, Maguire PB, Ohlendieck K. 1998. Role of dystrophin isoforms and associated proteins in muscular dystrophy. Int J Mol Med 2:639-648.
29. Deconinck AE, Potter AC, Tinsley JM, Wood SJ, Vater R, Young C, Metzinger L, Vincent A, Slater CR, Davies KE. 1997a. Postsynaptic abnormalities at the neuromuscular junctions of utrophin-deficient mice. J Cell Biol 136:883-894.
30. Deconinck AE, Rafael JA, Skinner JA, Brown SC, Potter AC, Metzinger L, Watt DJ, Dickson JG, Tinsley JM, Davies KE. 1997b. Utrophin-dystrophin-deficient mice as a model for Duchenne muscular dystrophy. Cell 90:717-727.
31. Deconinck N, Tinsley J, De Backer F, Fisher R, Kahn D, Phelps S, Davies K, Gillis JM. 1997a. Expression of truncated utrophin leads to major functional improvements in dystrophin-deficient muscles of mice. Nat Med 3:1216-1221.
32. Deconinck N, Rafael JA, Beckers-Bleukx G, Kahn D, Deconinck AE, Davies KE, Gillis JM. 1997b. Consequences of the combined deficiency in dystrophin and utrophin on the mechanical properties and myosin composition of some limb and respiratory muscles of the mouse. Nueromusc Disord 8:364-370.
33. England SB, Nicholson LV, Johnson MA, Forrest SM, Love DR, Zubrzycka-Gaarn EE, Bulman DE, Harris JB, Davies KE. 1990. Very mild muscular dystrophy associated with the deletion of 46% of dystrophin. Nature 343:180-182.
34. Ervasti JM, Ohlendieck K, Kahl SD, Gaver MG, Campbell KP. 1990. Deficiency of a glycoprotein component of the dystrophin complex in dystrophic muscle. Nature 345:315-319.
35. Fabbrizio E, Bonet-Kerrache A, Leger JJ, Mornet D. 1993. Actin-dystrophin interface. Biochemistry, 32:10457-10463.
36. Feener CA, Koenig M, Kunkel LM. 1989. Alternative splicing of human dystrophin mRNA generates isoforms at the carboxy terminus. Nature 338:509-511.
37. + channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43kD protein. Neuron 3:163-175.
38. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP. 1995, Failure of postsynaptic specialization to develop at neuromuscular-junctions of rapsyn-deficient mice. Nature 377:232-236.
39. Gee SH, Madhavan RS, Levinson SR, Caldwell JH, Sealock R, Froehnor SC. 1998. Interaction of muscle and brain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18:128-137.
40. Glass DJ, Yancopoulos GD. 1997. Sequential roles of agrin MuSK and rapsyn during neuromuscular junction formation. Curr Opin Neurol 7:379-384.
41. Grady R M, Merlie J P, Sanes J R. 1997a. Subtle neuromuscular defects in utrophin-deficient mice. J Cell Biol 136:871-882.
42. Grady RM, Teng H, Nichol MC, Cunningham JC, Wilkinson RS, Sanes JR. 1997b. Skeletal and cardiac myopathies in mice lacking utrophin and dystrophin: a model for Duchenne muscular dystrophy. Cell 90:729-738.
43. Gramolini AO, Dennis CL, Tinsley JM, Robertson GS, Cartaud J, Davies KE, Jasmin BJ. 1997. Local transcriptional control of utrophin expression at the neuromuscular synapse. J Biol Chem 272:8117-8120.
44. Greenberg DS, Sunada Y, Campbell KP, Yaffe D, Nudel U. 1994. Exogenous Dp71 restores the levels of dystrophin associated proteins but does not alleviate muscle damage in mdx mice [see comments]. Nat Genet 8:340-344.
45. Hall ZW. and Sanes JR. 1993. Synaptic structure and development -the neuromuscular-junction. Cell 72:99-121.
46. Henry MD, Williamson RA, Campbell KP. 1998. Analysis of the role of dystroglycan in early postimplantation mouse development. Ann NY Acad Sci 857:256-259.
47. Hoffman EP, Brown RH, Kunkel LM. 1987. Dystrophin: the protein product of the duchenne muscular-dystrophy locus. Cell 51:919-928.
48. Hoffman EP, Garcia CA, Chamberlain JS, Angelini C, Lupski JR, Fenwick R. 1991. Is the carboxyl-terminus of dystrophin required for membrane association? A novel, severe case of Duchenne muscular dystrophy. Ann Neurol 30:605-610.
49. Jarrett HW, Foster J L. 1995. Alternate binding of actin and calmodulin to multiple sites on dystrophin. J Biol Chem 270:5578-5586.
50. Jung D, Yang B, Meyer J, Chamberlain JS, Campbell KP. 1995. Identification and characterization of the dystrophin anchoring site on beta-dystroglycan. J Biol Chem 270:27305-27310.
51. Kameya S, Miyagoe Y, Nonaka I, Ikemoto T, Endo M, Hanaoka K, Nabeshima Y, Takeda S. 1999. a1-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.
52. Khurana TS, Watkins SC, Chafey P, Chelly J, Tome FM, Fardeau M, Kaplan JC, Kunkel LM. 1991. Immunolocalization and developmental expression of dystrophin related protein in skeletal muscle. Neuromusc Disord 1:185-194.
53. Kim TW, Wu K, Black IB. 1995. Deficiency of brain synaptic dystrophin in human duchenne muscular dystrophy. Ann Neurol 38:446-449.
54. Kobzik L, Reid MB, Bredt DS, Stamler JS. 1994. Nitric-oxide in skeletal-muscle. Nature 372:546-548.
55. Koenig M, Kunkel LM. 1990. Detailed analysis of the repeat domain of dystrophin reveals four potential hinge segments that may confer flexibility. J Biol Chem 265:4560-4566.
56. Koenig M, Monaco AP, Kunkel LM. 1988. The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53:219-226.
57. Love DR, Morris GE, Ellis JM, Fairbrother U, Marsden RF, Bloomfield JF, Edwards YH, Slater CP, Parry DJ, Davies KE. 1991. Tissue distribution of the dystrophin-related gene product and expression in the mdx and dy mouse. Proc Natl Acad Sci USA 88:3243-3247.
58. Lynch GS, Rafael JA, Hinkle RT, Cole NM, Chamberlain JS, Faulkner JA. 1997. Contractile properties of diaphragm muscle segments from old mdx and old transgenic mdx mice. Am J Physiol 272: C2063-C2068.
59. Lyons PR, Slater CR. 1991. Structure and function of the neuromuscular-junction in young-adult mdx mice. J Neurocytol 20:969-981.
60. Martin AR. 1994. Amplification of neuromuscular transmission by postjunctional folds. Proc Royal Soc B 258:321-326.
61. Matsumura K, Ervasti JM, Ohlendieck K, Kahl SD, Campbell KP. 1992. Association of dystrophin-related protein with dystrophin-associated proteins in mdx mouse muscle. Nature 360:588-591.
62. Matsumura K, Shasby DM, Campbell KP. 1993. Purification of dystrophin-related protein (utrophin) from lung and its identification in pulmonary artery endothelial cells. FEBS Lett 326:289-293.
63. Menke A, Jockusch H. 1991. Decreased osmotic stability of dystrophin-less muscle-cells from the mdx mouse. Nature 349:69-71.
64. Menke A, Brinkmeier H, Naumann T, Rudel R, Jockusch H. 1993. Duchenne myotubes are more susceptible to hypoosmotic shock than dystrophin expressing human controls. J Mus Res Cell Motil 14:258-259.
65. Nagel A, Lehmann-Horn F, Engel AG. 1990. Neuromuscular-transmission in the mdx mouse. Muscle Nerve 13:742-749.
66. Ohlendieck K, Campbell KP. 1991. Dystrophin-associated proteins are greatly reduced in skeletal muscle from mdx mice. J Cell Biol 115:1685-1694.
67. Ohlendieck K, Ervasti JM, Matsumura K, Kahl SD, Leveille CJ, Campbell KP. 1991. Dystrophin-related protein is localized to neuromuscular junctions of adult skeletal muscle. Neuron 7:499-508.
68. Ozawa E, Noguchi S, Mizuno Y, Hagiwara Y, Yoshida M. 1998. From dystrophinopathy to sarcoglycanopathy: evolution of a concept of muscular dystrophy. Muscle Nerve 21:421-438.
69. Pasternak C, Wong S, Elson EL. 1995. Mechanical function of dystrophin in muscle-cells. J Cell Biol 128:355-361.
70. Patel TJ, Lieber RL. 1997. Force transmission in skeletal muscle: from actomyosin to external tendons. Exerc Sport Sci Rev 25:321-363.
71. Patton BL, Chiu AY, Sanes JR. 1998. Synaptic laminin prevents glial entry into the synaptic cleft. Nature 393:698-701.
72. Pearce M, Blake DJ, Tinsley JM, Byth BC, Campbell L, Monaco AP, Davies KE. 1993. The utrophin and dystrophin genes share similarities in genomic structure. Hum Mol Genet 2:1765-1772.
73. Peng HB, Xie H, Rossi S, Rotundo R. 1999. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J Cell Biol 145:911-921.
74. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. 1993. Dystrophin protects the sarcolemma from stresses developed during muscle-contraction. Proc Natl Acad Sci USA 90:3710-3714.
75. Phelps SF, Hauser MA, Cole NM, Rafael JA, Hinkle RT, Faulkner JA, Chamberlain JS. 1995. Expression of full-length and truncated dystrophin mini-genes in transgenic mdx mice. Hum Mol Genet 4:1251-1258.
76. Phillips WD, Noakes PG, Roberds SL, Campbell KP, Merlie JP. 1993. Clustering and immobilization of acetylcholine-receptors by the 43-kd protein: a possible role for dystrophin-related protein. J Cell Biol 123:729-740.
77. Porter JD, Rafael JA, Ragusa RJ, Brueckner JK, Trickett JI, Davies KE. 1998. The sparing of extraocular muscle in dystrophinopathy is lost in mice lacking utrophin and dystrophin. J Cell Sci 111:1801-1811.
78. Rafael JA, Sunada Y, Cole NM, Campbell KP, Faulkner JA, Chamberlain JS. 1994. Prevention of dystrophic pathology in mdx mice by a truncated dystrophin isoform. Hum Mol Genet, 3:1725-1733.
79. Rafael JA, Cox GA, Corrado K, Jung D, Campbell KP, Chamberlain JS. 1996. Forced expression of dystrophin deletion constructs reveals structure-function correlations. J Cell Biol 134:93-102.
80. Rafael JA, Tinsley JM, Potter AC, Deconinck AE, Davies KE. 1998. Skeletal muscle-specific expression of a utrophin transgene rescues utrophin-dystrophin deficient mice. Nat Genet 19:79-82.
81. Ragusa RJ, Porter JD. 1994. Extraocular-muscle is highly protected from dystrophic changes in the mdx mouse. Investigative Ophthalmol Vis Sci ISUAL:2198-2198.
82. Ruegg MA, Bixby JL. 1998. Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction. TINS 21:22-27.
83. Rybakova IN, Ervasti JM. 1997. Dystrophin-glycoprotein complex is monomeric and stabilizes actin filaments in vitro through a lateral association. J Biol Chem 272:28771-28778.
84. Rybakova IN, Amann KJ, Ervasti JM. 1996. A new model for the interaction of dystrophin with F-actin. J Cell Biol 135:661-672.
85. Sealock R, Butler MH, Kramarcy NR, Gao KX, Murnane AA, Douville K, Froehner SC. 1991. Localization of dystrophin relative to acetylcholine-receptor domains in electric tissue and adult and cultured skeletal-muscle. J Cell Biol 113:1133-1144.
86. Sicinski P, Geng Y, Ryder-Cook AS, Barnard EA, Darlison MG, Barnard PJ. 1989. The molecular basis of muscular dystrophy in the mdx mouse: a point mutation. Science 244:1578-1580.
87. Sketelj J, Crne-Finderle N, Strukelj B, Trontelj JV, Pette D. 1998. Acetylcholinesterase mRNAlevel and synaptic activity in rat muscles depend on nerve-induced pattern of muscle activation. J Neurosci 18:1944-1952.
88. Stedman HH, Sweeney HL, Shrager JB, Maguire HC, Panettieri RA, Petrof B, Narusawa M, Leferovich JM, Sladky JT, Kelly AM. 1991. The mdx mouse diaphragm reproduces the degenerative changes of Duchenne muscular dystrophy. Nature 352:536-539.
89. Straub V, Campbell KP. 1997. Muscular dystrophies and the dystrophin-glycoprotein complex. Curr Opin Neurol 10:168-175.
90. Sugiyama J, Bowen DC, Hall ZW. 1994. Dystroglycan binds nerve and muscle agrin. Neuron 13:103-115.
91. Sugiyama JE, Glass DJ, Yancopoulos GD, Hall ZW. 1997. Laminin-induced acetylcholine receptor clustering: an alternative pathway. J Cell Biol 139:181-191.
92. Suzuki A, Yoshida M, Hayashi K, Mizuno Y, Hagiwara Y, Ozawa E. 1994. 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.
93. Suzuki A, Yoshida M, Ozawa E. 1995. Mammalian a 1-and beta 1-syntrophin bind to the alternative splice-prone region of the dystrophin COOH terminus. J Cell Biol 128:373-381.
94. Takemitsu M, Ishiura S, Koga B, Kamakura K, Arahata K, Nonaka I, Sugita H. 1991. Dystrophin-related protein in the fetal and denervated skeletal muscles of normal and mdx mice. Biochem Biophys Res Commun 180:1179-1186.
95. Thomas GD, Sander M, Lau KS, Huang PL, Stull JT, Victor RG. 1998. Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci USA 95:15090-15095.
96. Tinsley JM, Blake DJ, Roche A, Fairbrother U, Riss J, Byth BC, Knight AE, Kendrick-Jones J, Suthers GK, Love DR, Edwards YH, Davies KE. 1992. Primary structure of dystrophin-related protein. Nature 360:591-593.
97. Tinsley JM, Potter AC, Phelps SR, Fisher R, Trickett JI, Davies KE. 1996. Amelioration of the dystrophic phenotype of mdx mice using a truncated utrophin transgene. Nature 384:349-353.
98. Tinsley J, Deconinck N, Fisher R, Kahn D, Phelps S, Gillis JM, Davies K. 1998. Expression of full-length utrophin prevents muscular dystrophy in mdx mice. Nat Med 4:1441-1444.
99. Torres LFB, Duchen LW. 1987. The mutant mdx-inherited myopathy in the mouse: morphological studies of nerves, muscles, and end-plates. Brain 110:269-299
100. Way M, Pope B, Cross RA, Kendrick-Jones J, Weeds AG. 1992. Expression of the N-terminal domain of dystrophin in E. coli and demonstration of binding to F-actin. FEBS Lett 301:243-245.
101. Wehling M, Lavergne E, Lau KS, Stull JT, Spencer MS, Tidball JG. 1998. nNOS expression and activity in skeletal muscle are positive-lyregulated by mechanical and electrical stimulation. Faseb J 12:2408.
102. Wells DJ, Wells KE, Asante EA, Turner G, Sunada Y, Campbell KP, Walsh FS, Dickson G. 1995. Expression of human full-length and minidystrophin in transgenic mdx mice: implications for gene therapy of Duchenne muscular dystrophy. Hum Mol Genet 4:1245-1250.
103. Wilson SJ, McEwan JC, Sheard PW, Harris AJ. 1992. Early stages of myogenesis in a large mammal-formation of successive generations of myotubes in sheep tibialis cranialis muscle. J Mus Res Cell Motil 13:534-550.
104. Winnard AV, Mendell JR, Prior TW, Florence J, Burghes AH. 1995. Frameshift deletions of exons 3-7 and revertant fibers in Duchenne muscular dystrophy: mechanisms of dystrophin production. Am J Hum Genet 56:158-166.
105. Wood SJ, Slater CR. 1997. The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast-and slow-twitch muscles. J Physiol Lond 500:165-176.
106. Wood SJ, Slater CR. 1998. beta-spectrin is colocalized with both voltage-gated sodium channels and ankyrin(G) at the adult rat neuromuscular junction. J Cell Biol 140:675-684.
107. Worton R. 1995. Muscular dystrophies: diseases of the dystrophin-glycoprotein complex. Science 270:755-756.
108. Yang B, Jung D, Rafael JA, Chamberlain JS, Campbell KP. 1995. Identification of a-syntrophin binding to syntrophin triplet, dystrophin, and utrophin. J Biol Chem 270:4975-4978.
109. Yoshida M, Ozawa E. 1990. Glycoprotein complex anchoring dystrophin to sarcolemma. J Biochem (Tokyo) 108:748-752.