The role of free radicals in the pathophysiology of muscular dystrophy

Journal of Applied Physiology

Volumn 102, Issue 4, 2007, Pages 1677-1686

  Tidball, James G ^a,b,c   Wehling Henricks, Michelle ^a  

^a Department of Physiological Science ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Muscle disease; Nitric oxide

Indexed keywords

ALPHA TOCOPHEROL; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; DYSTROPHIN; DYSTROPHIN ASSOCIATED PROTEIN COMPLEX; FREE RADICAL; GLUTATHIONE; GLUTATHIONE PEROXIDASE; GLUTATHIONE TRANSFERASE; HYDROGEN PEROXIDE; MANGANESE SUPEROXIDE DISMUTASE; UBIQUINONE; UBIQUINONE DERIVATIVE;

ANTIOXIDANT ACTIVITY; CARDIOMYOPATHY; CLINICAL TRIAL; DUCHENNE MUSCULAR DYSTROPHY; HOMEOSTASIS; HUMAN; MUSCLE ATROPHY; MUSCLE FATIGUE; MUSCULAR DYSTROPHY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REVIEW;

ANIMALS; FREE RADICALS; HUMANS; MODELS, BIOLOGICAL; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUSCULAR DYSTROPHIES; NITRIC OXIDE; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES;

EID: 34147152905     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.01145.2006     Document Type: Review

References (95)

1. Abu-Soud HM, Hazen SL. Nitric oxide modulates the catalytic activity of myeloperoxidase. J Biol Chem 275: 5425-5430, 2000.
2. Adams ME, Kramarcy N, Krall SP, Rossi SG, Rotundo RL, Sealock R, Froehner SC. Absence of alpha-syntrophin leads to structurally aberrant neuromuscular synapses deficient in utrophin. J Cell Biol 150: 1385-1398, 2000.
3. Albina JE, Cui S, Mateo RB, Reichner JS. Nitric oxide-mediated apoptosis in murine peritoneal macrophages. J Immunol 150: 5080-5085, 1993.
4. Anderson JE. A role for nitric oxide in muscle repair: nitric oxidemediated activation of muscle satellite cells. Mol Biol Cell 11: 1859-1874, 2000.
5. Asayama K, Hayashibe H, Dobashi K, Kato K. Lipid peroxide and antioxidant enzymes in muscle and nonmuscle of dystrophic mouse. Muscle Nerve 12: 742-748, 1989.
6. Austin L, de Niese M, McGregor A, Arthur H, Gurusinghe A, Gould MK. Potential oxyradical damage and energy status in individual muscle fibres from degenerating muscle diseases. Neuromuscul Disord 2: 27-33, 1992.
7. Bia BL, Cassidy PJ, Young ME, Rafael JA, Leighton B, Davies KE, Radda GK, Clarke K. Decreased myocardial nNOS, increased iNOS and abnormal ECGs in mouse models of Duchenne muscular dystrophy. J Mol Cell Cardiol 31: 1857-1862, 1999.
8. Binder HJ, Herting DC, Hurst V, Finch SC, Sprio HM. Tocopherol deficiency in man. N Engl J Med 273: 1289-1297, 1965.
9. Brenman JE, Chao DS, Xia H, Aldape K, Bredt DS. Nitric oxide synthase complexed with dystrophin and absent from skeletal muscle sarcolemma in Duchenne muscular dystrophy. Cell 82: 743-752, 1995.
10. Camina F, Novo-Rodriguez MI, Rodriguez-Segade S, Castro-Gago M. Purine and carnitine metabolism in muscle of patients with Duchenne muscular dystrophy. Clin Chim Acta 243: 151-164, 1995.
11. Campbell KP, Kahl SD. Association of dystrophin and an integral membrane glycoprotein. Nature 338: 259-262, 1989.
12. Carlson CG, Roshek DM. Adult dystrophin (mdx) endplates exhibit reduced quantal size and enhanced quantal variation. Pflügers Arch 442: 369-375, 2001.
13. Cave A, Grieve D, Johar S, Zhang M, Shah AM. NADPH oxidasederived reactive oxygen species in cardiac pathophysiology. Philos Trans R Soc Lond B Biol Sci 360: 2327-2334, 2005.
14. Chang WJ, Iannaccone ST, Lau KS, Masters BS, McCabe TJ, McMillan K, Padre RC, Spencer MJ, Tidball JG, Stull JT. Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy. Proc Natl Acad Sci USA 93: 9142-9147, 1996.
15. Chao DS, Silvagno F, Xia H, Cornwell TL, Lincoln TM, Bredt DS. Nitric oxide synthase and cyclic GMP-dependent protein kinase concentrated at the neuromuscular endplate. Neuroscience 76: 665-672, 1997.
16. Chi MMY, Hintz CS, McKee D, Felder S, Grant N, Kaiser KK, Lowry OH. Effect of Duchenne muscular dystrophy on enzymes of energy metabolism in individual muscle fibers. Metabolism 36: 761-767, 1987.
17. Chojkier M, Houglum K, Lee KS, Buck M. Long- and short-term D-α-tocopherol supplementation inhibits liver collagen α1(I) gene expression. Am J Physiol Gastrointest Liver Physiol 275: G1480-G1485, 1998.
18. Clancy RM, Leszczynska-Piziak J, Abramson SB. Nitric oxide, an endothelial cell relaxation factor, inhibits neutrophil superoxide anion production via a direct action on the NADPH oxidase. J Clin Invest 90: 1116-1121, 1992.
19. Coral-Vazquez R, Cohn RD, Moore SA, Hill JA, Weiss RM, Davisson RL, Straub V, Barresi R, Bansal D, Hrstka RF, Williamson R, Campbell KP. Disruption of the sarcoglycan-sarcospan complex in vascular smooth muscle: a novel mechanism for cardiomyopathy and muscular dystrophy. Cell 98: 465-474, 1999.
20. Crosbie RH, Straub V, Yun HY, Lee JC, Rafael JA, Chamberlain JS, Dawson VL, Dawson TM, Campbell KP. mdx muscle pathology is independent of nNOS perturbation. Hum Mol Genet 7: 823-829, 1998.
21. Disatnik MH, Dhawan J, Yu Y, Beal MF, Whirl MM, Franco AA, Rando TA. Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state. J Neurol Sci 161: 77-84, 1998.
22. Disatnik MH, Chamberlain JS, Rando TA. Dystrophin mutations predict cellular susceptibility to oxidative stress. Muscle Nerve 23: 784-792, 2000.
23. Duclos F, Straub V, Moore SA, Venzke DP, Hrstka RF, Crosbie RH, Durbeej M, Lebakken CS, Ettinger AJ, van der Meulen J, Holt KH, Lim LE, Sanes JR, Davidson BL, Faulkner JA, Williamson R, Campbell KP. Progressive muscular dystrophy in alpha-sarcoglycan-deficient mice. J Cell Biol 142: 1461-1471, 1998.
24. Dudley RW, Danialou G, Govindaraju K, Lands L, Eidelman DE, Petrof BJ. Sarcolemmal damage in dystrophin deficiency is modulated by synergistic interactions between mechanical and oxidative/nitrosative stresses. Am J Pathol 168: 1276-1287, 2006.
25. Durbeej M, Cohn RD, Hrstka RF, Moore SA, Allamand V, Davidson BL, Williamson RA, Campbell KP. Disruption of the beta-sarcoglycan gene reveals pathogenic complexity of limb-girdle muscular dystrophy type 2E. Mol Cell 5: 141-151, 2000.
26. Edwards RH, Chapman SJ, Newham DJ, Jones DA. Practical analysis of variability of muscle function measurements in Duchenne muscular dystrophy. Muscle Nerve 10: 6-14, 1987.
27. Emery AE. Clinical and molecular studies in Duchenne muscular dystrophy. Prog Clin Biol Res 306: 15-28, 1989.
28. Fenoglio JJ Jr, Pham TD, Harken AH, Horowitz LN, Josephson ME, Wit AL. Recurrent sustained ventricular tachycardia: structure and ultrastructure of subendocardial regions in which tachycardia originates. Circulation 68: 518-533, 1983.
29. Finsterer J, Stollberger C. The heart in human dystrophinopathies. Cardiology 99: 1-19, 2003.
30. Fitzgerald G, McArdle B. Vitamins E and B6 in the treatment of muscular dystrophy and motor neuron disease. Brain 64: 19-42, 1954.
31. Frascarelli M, Rocchi L, Feola I. EMG computerized analysis of localized fatigue in Duchenne muscular dystrophy. Muscle Nerve 11: 757-761, 1988.
32. Gebre-Medhin M, Gustavson KH, Gamstorp I, Plantin LO. Selenium supplementation in X-linked muscular dystrophy. Effects on erythrocyte and serum selenium and on erythrocyte glutathione peroxidase activity. Acta Paediatr Scand 74: 886-890, 1985.
33. Girten B, Oloff C, Plato P, Eveland E, Merola AJ, Kazarian L. Skeletal muscle antioxidant enzyme levels in rats after simulated weightlessness, exercise and dobutamine. Physiologist 32: S59-S60, 1989.
34. Godfrey EW, Schwarte RC. The role of nitric oxide signaling in the formation of the neuromuscular junction. J Neurocytol 32: 591-602, 2003.
35. Grady RM, Zhou H, Cunningham JM, Henry MD, Campbell KP, Sanes JR. Maturation and maintenance of the neuromuscular synapse: genetic evidence for roles of the dystrophin-glycoprotein complex. Neuron 25: 279-293, 2000.
36. Grinio LP, Orlov ON, Prilipko LL, Kagan VE. Lipid peroxidation in children with Duchenne's hereditary myopathy. Biull Eksp Biol Med 98: 423-425, 1984.
37. Hack AA, Ly CT, Jiang F, Clendenin CJ, Sigrist KS, Wollmann RL, McNally EM. Gamma-sarcoglycan deficiency leads to muscle membrane defects and apoptosis independent of dystrophin. J Cell Biol 142: 1279-1287, 1998.
38. Hampton MB, Kettle AJ, Winterbourn CC. Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92: 3007-3017, 1998.
39. Harper SQ, Hauser MA, DelloRusso C, Duan D, Crawford RW, Phelps SF, Harper HA, Robinson AS, Engelhardt JF, Brooks SV, Chamberlain JS. Modular flexibility of dystrophin: implications for gene therapy of Duchenne muscular dystrophy. Nat Med 8: 253-261, 2002.
40. Heydemann A, Huber JM, Kakkar R, Wheeler MT, McNally EM. Functional nitric oxide synthase mislocalization in cardiomyopathy. J Mol Cell Cardiol 36: 213-223, 2004.
41. Hosaka Y, Yokata T, Miyagoe-Suzuki Y, Yuasa K, Imamura M, Matsuda R, Ikemoto T, Kameya S, Takeda S. Alpha1-syntrophindeficient skeletal muscle exhibits hypertrophy and aberrant formation of neuromuscular junctions during regeneration. J Cell Biol 158: 1097-1107, 2002.
42. Hunter MI, Mohamed JB. Plasma antioxidants and lipid peroxidation products in Duchenne muscular dystrophy. Clin Chim Acta 155: 123-131, 1986.
43. Ishimoto S, Goto I, Ohta M, Kuroiwa Y. A quantitative study of the muscle satellite cells in various neuromuscular disorders. J Neurol Sci 62: 303-314, 1983.
44. Jackson MJ, Jones DA, Edwards RH. Techniques for studying free radical damage in muscular dystrophy. Med Biol 62: 135-138, 1984.
45. Jones MA, Werle MJ. Nitric oxide is a downstream mediator of agrininduced acetylcholine receptor aggregation. Mol Cell Neurosci 16: 649-660, 2000.
46. Judge LM, Haraguchi M, Chamberlain JS. Dissecting the signaling and mechanical functions of the dystrophin-glycoprotein complex. J Cell Sci 119: 1537-1546, 2006.
47. Kar NC, Pearson CM. Catalase, superoxide dismutase, glutathione reductase and thiobarbituric acid-reactive products in normal and dystrophin human muscle. Clin Chim Acta 94: 277-280, 1979.
48. Kitaoka K, Matsuda Y, Desaki J, Oki S, Nagano Y, Shibata T. Topographic comparison of subneural apparatuses at neuromuscular junctions in normal and dystrophic (mdx) mice: a scanning electron microscope study. J Electron Microsc (Tokyo) 46: 193-197, 1997.
49. Lawler JM, Song W, Demaree SR. Hindlimb unloading increases oxidative stress and distrupts antioxidant capacity in skeletal muscle. Free Radic Biol Med 35: 9-16, 2003.
50. Lee KH, Baek MY, Moon KY, Song WK, Chung CH, Ha DB, Kang MS. Nitric oxide as a messenger molecule for myoblast fusion. J Biol Chem 269: 14371-14374, 1994.
51. Liu P, Xu B, Hock CE, Nagele R, Sun FF, Wong PY. NO modulates P-selectin and ICAM-1 mRNA expression and hemodynamic alterations in hepatic I/R. Am J Physiol Heart Circ Physiol 275: H2191-H2198, 1998.
52. Lyons PR, Slater CR. Structure and function of the neuromuscular junction in young adult mdx mice. J Neurocytol 20: 969-981, 1991.
53. Mendell JR, Engel WK, Derrer EC. Duchenne muscular dystrophy: functional ischemia reproduces its characteristic lesions. Science 172: 1143-1145, 1971.
54. Miles AM, Bohle DS, Glassbrenner PA, Hansart B, Wink DA, Grisham MB. Modulation of superoxide-dependent oxidation and hydroxylation reactions by nitric oxide. J Biol Chem 271: 40-47, 1996.
55. Miyoshi K. Echocardiographic evaluation of fibrous replacement in the myocardium of patients with Duchenne muscular dystrophy. Br Heart J 66: 452-455, 1991.
56. Mohr S, Hallak H, de Boitte A, Lapetina EG, Brune B. Nitric oxideinduced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274: 9427-9430, 1999.
57. Nguyen HX, Tidball JG. Interactions between neutrophils and macrophages promote macrophage killing of rat muscle cells in vitro. J Physiol 547: 125-132, 2003.
58. Park JB, Schiffrin EL. Cardiac and vascular fibrosis and hypertrophy in aldosterone-infused rats: the role of endothelin-1. Am J Hypertens 15: 164-169, 2002.
59. Petrof BJ, Shrager JB, Stedman HH, Kelly AM, Sweeney HL. Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci USA 90: 3710-3714, 1993.
60. Pisconti A, Brunelli S, Di Padova M, De Palma C, Deponti D, Baesso S, Sartorelli V, Cossu G, Clementi E. Follistatin induction by nitric oxide through cyclic GMP: a tightly regulated signaling pathway that controls myoblast fusion. J Cell Biol 172: 233-244, 2006.
61. Poli G, Parola M. Oxidative damage and fibrogenesis. Free Radic Biol Med 22: 287-305, 1997.
62. Rafael JA, Townsend ER, Squire SE, Potter AC, Chamberlain JS, Davies KE. Dystrophin and utrophin influence fiber type composition and post-synaptic membrane structure. Hum Mol Genet 9: 1357-1367, 2000.
63. Ragusa RJ, Chow CK, St. Clair DK, Porter JD. Extraocular, limb and diaphragm muscle group-specific antioxidant enzyme activity patterns in control and mdx mice. J Neurol Sci 139: 180-186, 1996.
64. Ragusa RJ, Chow CK, Porter JD. Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromuscul Disord 7: 379-386, 1997.
65. Rando TA, Disatnik MH, Yu Y, Franco A. Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 8: 14-21, 1998.
66. Rando TA, Crowley RS, Carlson EJ, Epstein CJ, Mohapatra PK. Overexpression of copper/zinc superoxide dismutase: a novel cause of murine muscular dystrophy. Ann Neurol 44: 381-386, 1998.
67. Rando TA. Role of nitric oxide in the pathogenesis of muscular dystrophies: a "two hit" hypothesis of the cause of muscle necrosis. Microsc Res Tech 55: 223-235, 2001.
68. Rapoport RM, Draznin MB, Murad F. Endothelium-dependent relaxation in rat aorta may be mediated through cyclic GMP-dependent protein phosphorylation. Nature 306: 174-176, 1983.
69. Sander M, Chavoshan B, Harris SA, Iannaccone S, Stull JT, Thomas GD, Victor RG. Functional muscle ischemia in neuronal nitric oxide synthase-deficient skeletal muscle of children with Duchenne muscular dystrophy. Proc Natl Acad Sci USA 97: 13818-13823, 2000.
70. Schoser BG, Behrends S. Soluble guanylyl cyclase is localized at the neuromuscular junction in human skeletal muscle. Neuroreport 12: 979-981, 2001.
71. Schwarte RC, Godfrey EW. Nitric oxide synthase activity is required for postsynaptic differentiation of the embryonic neuromuscular junction. Dev Biol 273: 276-284, 2004.
72. Scott OM, Vrbova G, Hyde SA, Dubowitz V. Responses of muscles of patients with Duchenne muscular dystrophy to chronic electrical stimulation. J Neurol Neurosurg Psychiatry 49: 1427-1434, 1986.
73. Scott OM, Hyde SA, Vrbova G, Dubowitz V. Therapeutic possibilities of chronic low frequency stimulation in children with Duchenne muscular dystrophy. J Neurol Sci 95: 171-182, 1990.
74. Shiao T, Fond A, Deng B, Wehling-Henricks M, Adams ME, Froehner SC, Tidball JG. Defects in neuromuscular junction structure in dystrophic muscle are corrected by expression of a NOS transgene in dystrophindeficient muscles, but not in muscles lacking alpha- and beta1-syntrophins. Hum Mol Genet 13: 1873-1884, 2004.
75. Souza JM, Radi R. Glyceraldehyde-3-phosphate dehydrogenase inactivation by peroxynitrite. Arch Biochem Biophys 360: 187-194, 1998.
76. Stamler JS, Meissner G. Physiology of nitric oxide in skeletal muscle. Physiol Rev 81: 209-237, 2001.
77. Stern LZ, Ringel SP, Ziter FA, Menander-Huber KB, Ionasescu V, Pellegrino RJ, Snyder RD. Drug trial of superoxide dismutase in Duchenne's muscular dystrophy. Arch Neurol 39: 342-346, 1982.
78. Tatsumi R, Hattori A, Ikeuchi Y, Anderson JE, Allen RE. Release of hepatocyte growth factor from mechanically stretched skeletal muscle satellite cells and role of pH and nitric oxide. Mol Biol Cell 13: 2909-2918, 2002.
79. Thomas GD, Sander M, Lau KS, Huang PL, Stuff JT, Victor RG. Impaired metabolic modulation of alpha-adrenergic vasoconstriction in dystrophin-deficient skeletal muscle. Proc Natl Acad Sci USA 95: 15090-15095, 1998.
80. Tidball JG, Lavernge E, Lau KS, Spencer MJ, Stull JT, Wehling M. Mechanical loading regulates NOS expression and activity in developing and adults skeletal muscle. Am J Physiol Cell Physiol 275: C260-C266, 1998.
81. Tidball JG, Wehling-Henricks M. Evolving therapeutic strategies for Duchenne muscular dystrophy: targeting downstream events. Pediatr Res 56: 831-841, 2004.
82. Torres LF, Duchen LW. The mutant mdx: inherited myopathy in the mouse. Morphological studies of nerves, muscles and end-plates. Brain 110: 269-299, 1987.
83. Touboul D, Brunelle A, Halgand F, De La Porte S, Laprevote O. Lipid imaging by gold cluster time-of-flight secondary ion mass spectrometry: application to Duchenne muscular dystrophy. J Lipid Res 46: 1388-1395, 2005.
84. Trejo-Solis C, Chagoya De Sanchez V, Aranda-Fraustro A, Sanchez-Sevilla L, Gomez-Ruiz C, Hernandez-Munoz R. Inhibitory effect of vitamin E administration on the progression of liver regeneration induced by partial hepatectomy in rats. Lab Invest 83: 1669-1679, 2003.
85. Wakayama Y, Schotland DL, Bonilla E, Orecchio E. Quantitative ultrastructural study of muscle satellite cells in Duchenne dystrophy. Neurology 29: 401-407, 1979.
86. Walton JN, Nattrass FJ. On the classification, natural history and treatment of myopathies. Brain 77: 169-231, 1954.
87. Warner LE, DelloRusso C, Crawford RW, Rybakova IN, Patel JR, Ervasti JM, Chamberlain JS. Expression of Dp260 in muscle tethers the actin cytoskeleton to the dystrophin-glycoprotein complex and partially prevents dystrophy. Hum Mol Genet 11: 1095-1105, 2002.
88. Watkins SC, Cullen MJ. A quantitative study of myonuclear and satellite cell nuclear size in Duchenne's muscular dystrophy, polymyositis and normal human skeletal muscle. Anat Rec 222: 6-11, 1988.
89. Wehling M, Spencer MJ, Tidball JG. A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155: 123-131, 2001.
90. Wehling-Henricks M, Jordan MC, Roos KP, Deng B, Tidball JG. Cardiomyopathy in dystrophin-deficient hearts is prevented by expression of a neuronal nitric oxide synthase transgene in the myocardium. Hum Mol Genet 14: 1921-1933, 2005.
91. Wheeler MT, Allikian MJ, Heydemann A, Hadhazy M, Zarnegar S, McNally EM. Smooth muscle cell-extrinsic vascular spasm arises from cardiomyocyte degeneration in sarcoglycan-deficient cardiomyopathy. J Clin Invest 113: 668-75, 2004.
92. Wineinger MA, Walsh SA, Abresch RT. The effect of age and temperature on mdx muscle fatigue. Muscle Nerve 21: 1075-1077, 1998.
93. Yoshikawa T, Yoshida N, Manabe H, Terasawa Y, Takemura T, Kondo M. alpha-Tocopherol protects against expression of adhesion molecules on neutrophils and endothelial cells. Biofactors 7: 15-19, 1998.
94. Zhuang W, Eby JC, Cheong M, Mohapatra PK, Bredt DS, Distnik MH, Rando TA. The susceptibility of muscle cells to oxidative stress is independent of nitric oxide synthase expression. Muscle Nerve 24: 502-511, 2001.
95. Zubrzycka-Gaarn EE, Bulman DE, Karpati G, Burghes AH, Belfall B, Klamut HJ, Talbot J, Hodges RS, Ray PN, Worton RG. The Duchenne muscular dystrophy gene product is localized in sarcolemma of human skeletal muscle. Nature 333: 466-469, 1988.