Melatonin improves muscle function of the dystrophic mdx 5Cv mouse, a model for Duchenne muscular dystrophy

Journal of Pineal Research

Volumn 51, Issue 2, 2011, Pages 163-171

  Hibaoui, Youssef ^a   Reutenauer Patte, Julie ^a   Patthey Vuadens, Ophélie ^a   Ruegg, Urs T ^a   Dorchies, Olivier M ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

calcium; Duchenne muscular dystrophy; glutathione; mdx mouse; melatonin; muscle; oxidative stress

Indexed keywords

CREATINE KINASE; MELATONIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CONTROLLED STUDY; CREATINE KINASE BLOOD LEVEL; DUCHENNE MUSCULAR DYSTROPHY; IMPLANT; ISOMETRICS; MALE; MOUSE; MUSCLE FUNCTION; MUSCLE INJURY; MUSCULAR DYSTROPHY; NONHUMAN; TREATMENT RESPONSE; TRICEPS SURAE MUSCLE;

ANIMALS; ANTIOXIDANTS; CREATININE; DISEASE MODELS, ANIMAL; GLUTATHIONE; HUMANS; ISOMETRIC CONTRACTION; MALE; MELATONIN; MICE; MICE, INBRED MDX; MUSCLE RELAXATION; MUSCLE STRENGTH; MUSCLE, SKELETAL; MUSCULAR DYSTROPHY, DUCHENNE; OXIDATION-REDUCTION;

EID: 80051664689     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2011.00871.x     Document Type: Article

References (70)

1. Blake DJ, Weir A, Newey SE, et al., Function and genetics of dystrophin and dystrophin-related proteins in muscle. Physiol Rev 2002; 82: 291-329. (Pubitemid 34654455)
2. Petrof BJ, Shrager JB, Stedman HH, et al., Dystrophin protects the sarcolemma from stresses developed during muscle contraction. Proc Natl Acad Sci U S A 1993; 90: 3710-3714. (Pubitemid 23111437)
3. Dorchies OM, Wagner S, Vuadens O, et al., Green tea extract and its major polyphenol (-)-epigallocatechin gallate improve muscle function in a mouse model for Duchenne muscular dystrophy. Am J Physiol Cell Physiol 2006; 290: C616-C625.
4. Hopf FW, Turner PR, Steinhardt RA,. Calcium misregulation and the pathogenesis of muscular dystrophy. Subcell Biochem 2007; 45: 429-464.
5. Gailly P, De Backer F, Van Schoor M, et al., In situ measurements of calpain activity in isolated muscle fibres from normal and dystrophin-lacking mdx mice. J Physiol 2007; 582: 1261-1275. (Pubitemid 47104353)
6. Ragusa RJ, Chow CK, Porter JD,. Oxidative stress as a potential pathogenic mechanism in an animal model of Duchenne muscular dystrophy. Neuromuscul Disord 1997; 7: 379-386. (Pubitemid 27445322)
7. Rodriguez MC, Tarnopolsky MA,. Patients with dystrophinopathy show evidence of increased oxidative stress. Free Radic Biol Med 2003; 34: 1217-1220. (Pubitemid 36423371)
8. Nakae Y, Stoward P, Kashiyama T, et al., Early onset of Lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice. J Mol Histol 2004; 35: 489-499. (Pubitemid 41410964)
9. Disatnik MH, Dhawan J, Yu Y, et al., Evidence of oxidative stress in mdx mouse muscle: studies of the pre-necrotic state. J Neurol Sci 1998; 161: 77-84. (Pubitemid 28559187)
10. Rando TA,. Oxidative stress and the pathogenesis of muscular dystrophies. Am J Phys Med Rehabil 2002; 81: S175-S186. (Pubitemid 35192977)
11. Rando TA, Disatnik MH, Yu Y, et al., Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 1998; 8: 14-21. (Pubitemid 28174930)
12. Dudley RWR, Khairallah M, Mohammed S, et al., Dynamic responses of the glutathione system to acute oxidative stress in dystrophic mouse (mdx) muscles. Am J Physiol Regul Integr Comp Physiol 2006; 291: R704-R710. (Pubitemid 44352353)
13. Whitehead NP, Pham C, Gervasio OL, et al., N-Acetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J Physiol 2008; 586: 2003-2014. (Pubitemid 351997524)
14. Buetler TM, Renard M, Offord EA, et al., Green tea extract decreases muscle necrosis in mdx mice and protects against reactive oxygen species. Am J Clin Nutr 2002; 75: 749-753. (Pubitemid 34250689)
15. Dorchies OM, Wagner S, Buetler TM, et al., Protection of dystrophic muscle cells with polyphenols from green tea correlates with improved glutathione balance and increased expression of 67LR, a receptor for (-)-epigallocatechin gallate. BioFactors 2009; 35: 279-294.
16. Nakae Y, Hirasaka K, Goto J, et al., Subcutaneous injection, from birth, of epigallocatechin-3-gallate, a component of green tea, limits the onset of muscular dystrophy in mdx mice: a quantitative histological, immunohistochemical and electrophysiological study. Histochem Cell Biol 2008; 129: 489-501.
17. Messina S, Bitto A, Aguennouz MH, et al., Nuclear factor kappa-B blockade reduces skeletal muscle degeneration and enhances muscle function in Mdx mice. Exp Neurol 2006; 198: 234-241. (Pubitemid 43243761)
18. Burdi R, Rolland JF, Fraysse B, et al., Multiple pathological events in exercised dystrophic mdx mice are targeted by pentoxifylline: outcome of a large array of in vivo and ex vivo tests. J Appl Physiol 2009; 106: 1311-1324.
19. Buyse GM, Van Der Mieren G, Erb M, et al., Long-term blinded placebo-controlled study of SNT-MC17/idebenone in the dystrophin deficient mdx mouse: cardiac protection and improved exercise performance. Eur Heart J 2009; 30: 116-124.
20. Radley HG, De Luca A, Lynch GS, et al., Duchenne muscular dystrophy: focus on pharmaceutical and nutritional interventions. Int J Biochem Cell Biol 2007; 39: 469-477. (Pubitemid 46096791)
21. Smith MA, Reid MB,. Redox modulation of contractile function in respiratory and limb skeletal muscle. Respir Physiol Neurobiol 2006; 151: 229-241.
22. Van Der Poel C, Edwards JN, Macdonald WA, et al., Mitochondrial superoxide production in skeletal muscle fibers of the rat and decreased fiber excitability. Am J Physiol Cell Physiol 2007; 292: C1353-C1360. (Pubitemid 46631722)
23. Ferreira LF, Reid MB,. Muscle-derived ROS and thiol regulation in muscle fatigue. J Appl Physiol 2008; 104: 853-860. (Pubitemid 351468816)
24. Allen DG, Lamb GD, Westerblad H,. Skeletal muscle fatigue: cellular mechanisms. Physiol Rev 2008; 88: 287-332.
25. Powers SK, Jackson MJ,. Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production. Physiol Rev 2008; 88: 1243-1276.
26. Whitehead NP, Yeung EW, Allen DG,. Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species. Clin Exp Pharmacol Physiol 2006; 33: 657-662. (Pubitemid 43894030)
27. Petrosillo G, Colantuono G, Moro N, et al., Melatonin protects against heart ischemia-reperfusion injury by inhibiting mitochondrial permeability transition pore opening. Am J Physiol Heart Circ Physiol 2009; 297: H1487-H1493.
28. Tengattini S, Reiter RJ, Tan DX, et al., Cardiovascular diseases: protective effects of melatonin. J Pineal Res 2008; 44: 16-25. (Pubitemid 350231106)
29. Erkanli K, Kayalar N, Erkanli G, et al., Melatonin protects against ischemia/reperfusion injury in skeletal muscle. J Pineal Res 2005; 39: 238-242. (Pubitemid 41337803)
30. Wang WZ, Fang XH, Stephenson LL, et al., Melatonin reduces ischemia/reperfusion-induced superoxide generation in arterial wall and cell death in skeletal muscle. J Pineal Res 2006; 41: 255-260. (Pubitemid 44337721)
31. Yeung HM, Hung MW, Fung ML,. Melatonin ameliorates calcium homeostasis in myocardial and ischemia-reperfusion injury in chronically hypoxic rats. J Pineal Res 2008; 45: 373-382.
32. Escames G, López LC, Tapias V, et al., Melatonin counteracts inducible mitochondrial nitric oxide synthase-dependent mitochondrial dysfunction in skeletal muscle of septic mice. J Pineal Res 2006; 40: 71-78.
33. Hibaoui Y, Roulet E, Ruegg UT,. Melatonin prevents oxidative stress-mediated mitochondrial permeability transition and death in skeletal muscle cells. J Pineal Res 2009; 47: 238-252.
34. Schaefer M, Hardeland R,. The melatonin metabolite N1-acetyl-5- methoxykynuramine is a potent singlet oxygen scavenger. J Pineal Res 2009; 46: 49-52.
35. Hardeland R, Tan D-X, Reiter RJ,. Kynuramines, metabolites of melatonin and other indoles: the resurrection of an almost forgotten class of biogenic amines. J Pineal Res 2009; 47: 109-126.
36. Urata Y, Honma S, Goto S, et al., Melatonin induces gamma- glutamylcysteine synthetase mediated by activator protein-1 in human vascular endothelial cells. Free Radic Biol Med 1999; 27: 838-847. (Pubitemid 29454587)
37. Rodriguez C, Mayo JC, Sainz RM, et al., Regulation of antioxidant enzymes: a significant role for melatonin. J Pineal Res 2004; 36: 1-9. (Pubitemid 38130283)
38. Acuna-Castroviejo D, Escames G, Rodriguez MI, et al., Melatonin role in the mitochondrial function. Front Biosci 2007; 12: 947-963. (Pubitemid 46846869)
39. Paradies G, Petrosillo G, Paradies V, et al., Melatonin, cardiolipin and mitochondrial bioenergetics in health and disease. J Pineal Res 2010; 48: 297-310.
40. Gomez-Pinilla PJ, Gomez MF, Swärd K, et al., Melatonin restores impaired contractility in aged guinea pig urinary bladder. J Pineal Res 2008; 44: 416-425. (Pubitemid 351533526)
41. 2+ homeostasis and contractility in acute cholecystitis. J Pineal Res 2008; 44: 250-260. (Pubitemid 351392938)
42. Passaquin AC, Renard R, Kay L, et al., Creatine supplementation reduces skeletal muscle degeneration and enhances mitochondrial function in mdx mice. Neuromuscul Disord 2002; 12: 174-182. (Pubitemid 33152736)
43. Tanabe Y, Esaki K, Nomura T,. Skeletal muscle pathology in X chromosome-linked muscular dystrophy (mdx) mouse. Acta Neuropathol 1986; 69: 91-95. (Pubitemid 16146255)
44. Williams AH, Mcphee SR, Reeve JL, et al., Optimum use of subcutaneous melatonin implants to enhance the reproductive performance of seasonal and non-seasonal sheep joined in spring and early summer. Anim Reprod Sci 1992; 30: 225-258.
45. Staples LD, Mcphee S, Kennaway DJ, et al., The influence of exogenous melatonin on the seasonal patterns of ovulation and oestrus in sheep. Anim Reprod Sci 1992; 30: 185-223.
46. Willis GL, Armstrong SMA,. Therapeutic role for melatonin antagonism in experimental models of Parkinson's disease. Physiol Behav 1999; 66: 785-795. (Pubitemid 29281640)
47. Yeleswaram K, Mclaughlin LG, Knipe JO, et al., Pharmacokinetics and oral bioavailability of exogenous melatonin in preclinical animal models and clinical implications. J Pineal Res 1997; 22: 45-51. (Pubitemid 127731790)
48. Pertsov SS,. Effect of melatonin on the thymus, adrenal glands, and spleen in rats during acute stress. Bull Exp Biol Med 2006; 141: 292-295. (Pubitemid 43905092)
49. Reutenauer J, Dorchies OM, Patthey-Vuadens O, et al., Investigation of Debio 025, a cyclophilin inhibitor, in the dystrophic mdx mouse, a model for Duchenne muscular dystrophy. Br J Pharmacol 2008; 155: 574-584.
50. Kumar A, Boriek AM,. Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: a possible role in Duchenne muscular dystrophy. FASEB J 2003; 17: 386-396. (Pubitemid 36292954)
51. Messina S, Altavilla D, Aguennouz MH, et al., Lipid peroxidation inhibition blunts nuclear factor-kappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am J Pathol 2006; 168: 918-926. (Pubitemid 43327744)
52. Tan D, Chen L, Poeggeler B, et al., Melatonin: a potent, endogenous hydroxyl radical scavenger. Endocr J 1993; 1: 57-60.
53. Tan DX, Manchester LC, Terron LJ, et al., One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007; 42: 28-42. (Pubitemid 44924323)
54. Peyrot F, Ducrocq C,. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008; 45: 235-246.
55. García JJ, Reiter RJ, Guerrero JM, et al., Melatonin prevents changes in microsomal membrane fluidity during induced lipid peroxidation. FEBS Lett 1997; 408: 297-300. (Pubitemid 27227019)
56. Martín M, Macías M, Escames G, et al., Melatonin but not vitamins C and E maintains glutathione homeostasis in t-butyl hydroperoxide-induced mitochondrial oxidative stress. FASEB J 2000; 14: 1677-1679.
57. Hnia K, Hugon G, Rivier F, et al., Modulation of p38 mitogen-activated protein kinase cascade and metalloproteinase activity in diaphragm muscle in response to free radical scavenger administration in dystrophin-deficient Mdx mice. Am J Pathol 2007; 170: 633-643. (Pubitemid 47339400)
58. Bottinelli R, Reggiani C,. Human skeletal muscle fibres: molecular and functional diversity. Prog Biophys Mol Biol 2000; 73: 195-262.
59. Khawli FA, Reid MB,. N-acetylcysteine depresses contractile function and inhibits fatigue of diaphragm in vitro. J Appl Physiol 1994; 77: 317-324. (Pubitemid 24226152)
60. Reid MB, Khawli FA, Moody MR,. Reactive oxygen in skeletal muscle. III. Contractility of unfatigued muscle. J Appl Physiol 1993; 75: 1081-1087. (Pubitemid 23289594)
61. Ruegg UT, Nicolas-Métral V, Challet C, et al., Pharmacological control of cellular calcium handling in dystrophic skeletal muscle. Neuromuscul Disord 2002; 12: S155-S161. (Pubitemid 36158786)
62. Bruton J, Tavi P, Aydin J, et al., Mitochondrial and myoplasmic Ca2+ in single fibres from mouse limb muscles during repeated tetanic contractions. J Physiol 2003; 551: 179-190. (Pubitemid 37062921)
63. 2+ uptake into mitochondria of mouse skeletal muscle during contraction. J Cell Biol 2004; 166: 527-536. (Pubitemid 39097172)
64. Kargacin ME, Kargacin GJ,. The sarcoplasmic reticulum calcium pump is functionally altered in dystrophic muscle. Biochim Biophys Acta 1996; 1290: 4-8. (Pubitemid 26173321)
65. Gailly P,. New aspects of calcium signaling in skeletal muscle cells: implications in Duchenne muscular dystrophy. Biochim Biophys Acta 2002; 1600: 38-44. (Pubitemid 38224396)
66. Hidalgo C, Donoso P,. Crosstalk between calcium and redox signaling: from molecular mechanisms to health implications. Antioxid Redox Signal 2008; 10: 1275-1312. (Pubitemid 351634396)
67. Sun J, Xu L, Eu JP, et al., Classes of thiols that influence the activity of the skeletal muscle calcium release channel. J Biol Chem 2001; 276: 15625-15630.
68. Zable AC, Favero TG, Abramson JJ,. Glutathione modulates ryanodine receptor from skeletal muscle sarcoplasmic reticulum. J Biol Chem 1997; 272: 7069-7077.
69. Chahbouni M, Escames G, Venegas C, et al., Melatonin treatment normalizes plasma pro-inflammatory cytokines and nitrosative/oxidative stress in patients suffering from Duchenne muscular dystrophy. J Pineal Res 2010; 48: 282-289.
70. Alonso M, Collado PS, González-Gallego J,. Melatonin inhibits the expression of the inducible isoform of nitric oxide synthase and nuclear factor kappa B activation in rat skeletal muscle. J Pineal Res 2006; 41: 8-14. (Pubitemid 43980689)