Oxidative stress in muscular dystrophy: From generic evidence to specific sources and targets

Journal of Muscle Research and Cell Motility

Volumn 35, Issue 1, 2014, Pages 23-36

  Canton, Marcella ^a   Menazza, Sara ^b   Lisa, Fabio Di ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Mitochondria; Monoamine oxidase; Muscular dystrophy; Myofilament proteins; Oxidative stress

Indexed keywords

MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE;

ANIMAL; HUMAN; METABOLISM; MITOCHONDRION; MUSCLE FIBRIL; MUSCULAR DYSTROPHY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PHYSIOLOGY;

ANIMALS; HUMANS; MEMBRANE PROTEINS; MITOCHONDRIA; MUSCULAR DYSTROPHIES; MYOFIBRILS; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES;

EID: 84899490852     PISSN: 01424319     EISSN: 15732657     Source Type: Journal    
DOI: 10.1007/s10974-014-9380-2     Document Type: Review

References (131)

1. Acharyya S, Villalta SA, Bakkar N, Bupha-Intr T, Janssen PM, Carathers M, Li ZW, Beg AA, Ghosh S, Sahenk Z, Weinstein M, Gardner KL, Rafael-Fortney JA, Karin M, Tidball JG, Baldwin AS, Guttridge DC (2007) Interplay of IKK/NF-kappaB signaling in macrophages and myofibers promotes muscle degeneration in Duchenne muscular dystrophy. J Clin Invest 117(4):889-901. doi:10.1172/JCI30556 (Pubitemid 46556745)
2. Andrade FH, Reid MB, Westerblad H (2001) Contractile response of skeletal muscle to low peroxide concentrations: Myofibrillar calcium sensitivity as a likely target for redox-modulation. FASEB J 15(2):309-311. doi:10.1096/fj.00- 0507fje
3. Angelin A, Tiepolo T, Sabatelli P, Grumati P, Bergamin N, Golfieri C, Mattioli E, Gualandi F, Ferlini A, Merlini L, Maraldi NM, Bonaldo P, Bernardi P (2007) Mitochondrial dysfunction in the pathogenesis of Ullrich congenital muscular dystrophy and prospective therapy with cyclosporins. Proc Natl Acad Sci USA 104(3):991-996. doi:10.1073/pnas.0610270104 (Pubitemid 46154724)
4. Arbogast S, Ferreiro A (2010) Selenoproteins and protection against oxidative stress: Selenoprotein N as a novel player at the crossroads of redox signaling and calcium homeostasis. Antioxid Redox Signal 12(7):893-904. doi:10.1089/ars.2009.2890
5. Arbogast S, Beuvin M, Fraysse B, Zhou H, Muntoni F, Ferreiro A (2009) Oxidative stress in SEPN1-related myopathy: from pathophysiology to treatment. Ann Neurol 65(6):677-686. doi:10.1002/ana.21644
6. Balaban RS, Nemoto S, Finkel T (2005) Mitochondria, oxidants, and aging. Cell 120(4):483-495. doi:10.1016/j.cell.2005.02.001 (Pubitemid 40269763)
7. Bansal D, Miyake K, Vogel SS, Groh S, Chen CC, Williamson R, McNeil PL, Campbell KP (2003) Defective membrane repair in dysferlin-deficient muscular dystrophy. Nature 423(6936): 168-172. doi:10.1038/nature01573 (Pubitemid 36569539)
8. Barbieri E, Sestili P (2012) Reactive oxygen species in skeletal muscle signaling. J Signal Transduct 2012:982794. doi:10.1155/2012/982794
9. Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272(33):20313-20316 (Pubitemid 27355575)
10. Bertini E, Pepe G (2002) Collagen type VI and related disorders: Bethlem myopathy and Ullrich scleroatonic muscular dystrophy. Eur J Paediatr Neurol 6(4):193-198
11. Bhatnagar S, Kumar A (2010) Therapeutic targeting of signaling pathways in muscular dystrophy. J Mol Med 88(2):155-166. doi:10.1007/s00109-009-0550-4
12. Binda C, Newton-Vinson P, Hubalek F, Edmondson DE, Mattevi A (2002) Structure of human monoamine oxidase B, a drug target for the treatment of neurological disorders. Nat Struct Biol 9(1):22-26. doi:10.1038/nsb732 (Pubitemid 34049174)
13. Bonaldo P, Braghetta P, Zanetti M, Piccolo S, Volpin D, Bressan GM (1998) Collagen VI deficiency induces early onset myopathy in the mouse: An animal model for Bethlem myopathy. Hum Mol Genet 7(13):2135-2140 (Pubitemid 28546424)
14. Brigelius-Flohe R, Flohe L (2011) Basic principles and emerging concepts in the redox control of transcription factors. Antioxid Redox Signal 15(8):2335-2381. doi:10.1089/ars2010.3534
15. Burgoyne JR, Madhani M, Cuello F, Charles RL, Brennan JP, Schroder E, Browning DD, Eaton P (2007) Cysteine redox sensor in PKGIa enables oxidant-induced activation. Science 317(5843):1393-1397. doi:10.1126/science. 1144318 (Pubitemid 47417480)
16. Burgoyne JR, Mongue-Din H, Eaton P, Shah AM (2012) Redox signaling in cardiac physiology and pathology. Circ Res 111(8):1091-1106. doi:10.1161/CIRCRESAHA.111.255216
17. BuyseGM, Van derMieren G, ErbM,D'Hooge J, Herijgers P,Verbeken E, Jara A, Van Den Bergh A,Mertens L, Courdier-Fruh I, Barzaghi P, Meier T (2009) 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 30(1):116-124. doi:10.1093/eurheartj/ehn406
18. Buyse GM, Goemans N, van den Hauwe M, Thijs D, de Groot IJ, Schara U, Ceulemans B, Meier T, Mertens L (2011) Idebenone as a novel, therapeutic approach for Duchenne muscular dystrophy: Results from a 12 month, double-blind, randomized placebo-controlled trial. Neuromuscul Disord 21(6):396-405. doi:10.1016/j.nmd.2011.02.016
19. Cadenas E, Davies KJ (2000) Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biol Med 29(3-4):222-230
20. Camacho Vanegas O, Bertini E, Zhang RZ, Petrini S, Minosse C, Sabatelli P, Giusti B, Chu ML, Pepe G (2001) Ullrich scleroatonic muscular dystrophy is caused by recessive mutations in collagen type VI. Proc Natl Acad Sci USA 98(13):7516-7521. doi:10.1073/pnas.121027598 (Pubitemid 32567980)
21. Canton M, Neverova I, Menabo R, Van Eyk J, Di Lisa F (2004) Evidence of myofibrillar protein oxidation induced by postischemic reperfusion in isolated rat hearts. Am J Physiol Heart Circ Physiol 286(3):H870-H877. doi:10.1152/ajpheart.0 0714. 2003 (Pubitemid 38248597)
22. Canton M, Skyschally A, Menabo R, Boengler K, Gres P, Schulz R, Haude M, Erbel R, Di Lisa F, Heusch G (2006) Oxidative modification of tropomyosin and myocardial dysfunction following coronary microembolization. Eur Heart J 27(7):875-881. doi:10.1093/eurheartj/ehi751
23. Canton M, Menazza S, Sheeran FL, Polverino de Laureto P, Di Lisa F, Pepe S (2011) Oxidation of myofibrillar proteins in human heart failure. J Am Coll Cardiol 57(3):300-309. doi:10.1016/j. jacc.2010.06.058
24. Chouchani ET, Methner C, Nadtochiy SM, Logan A, Pell VR, Ding S, James AM, Cocheme HM, Reinhold J, Lilley KS, Partridge L, Fearnley IM, Robinson AJ, Hartley RC, Smith RA, Krieg T, Brookes PS, Murphy MP (2013) Cardioprotection by S-nitrosation of a cysteine switch on mitochondrial complex I. Nat Med 19(6):753-759. doi:10.1038/nm.3212
25. Chung HS, Wang SB, Venkatraman V, Murray CI, Van Eyk JE (2013) Cysteine oxidative posttranslational modifications: Emerging regulation in the cardiovascular system. Circ Res 112(2):382-392. doi:10.1161/CIRCRESAHA.112. 268680
26. Cross JV, Templeton DJ (2006) Regulation of signal transduction through protein cysteine oxidation. Antioxid Redox Signal 8(9-10):1819-1827. doi:10.1089/ars.2006.8.1819 (Pubitemid 44726354)
27. Csordas G, Hajnoczky G (2009) SR/ER-mitochondrial local communication: Calcium and ROS. Biochim Biophys Acta 1787(11):1352-1362. doi:10.1016/j.bbabio. 2009.06.004
28. Dalle-Donne I, Giustarini D, Rossi R, Colombo R, Milzani A (2003) Reversible S-glutathionylation of Cys 374 regulates actin filament formation by inducing structural changes in the actin molecule. Free Radical Biol Med 34(1):23-32 (Pubitemid 36043883)
29. Dalmaz Y, Peyrin L, Mamelle JC, Tuil D, Gilly R, Cier JF (1979) The pattern of urinary catecholamines and their metabolites in Duchenne myopathy, in relation to disease evolution. J Neural Transm 46(1):17-34 (Pubitemid 10224593)
30. Davies KE, Nowak KJ (2006) Molecular mechanisms of muscular dystrophies: old and new players. Nat Rev Mol Cell Biol 7(10):762-773. doi:10.1038/nrm2024 (Pubitemid 44450460)
31. Di Lisa F, Canton M, Carpi A, Kaludercic N, Menabo R, Menazza S, Semenzato M (2011) Mitochondrial injury and protection in ischemic pre- and postconditioning. Antioxid Redox Signal 14(5):881-891. doi:10.1089/ars.2010.3375
32. Disatnik MH, Dhawan J, Yu Y, Beal MF, Whirl MM, Franco AA, Rando TA (1998) Evidence of oxidative stress in mdx mouse muscle: Studies of the pre-necrotic state. J Neurol Sci 161(1): 77-84 (Pubitemid 28559187)
33. Dogra C, Changotra H, Wergedal JE, Kumar A (2006) Regulation of phosphatidylinositol 3-kinase (PI3K)/Akt and nuclear factorkappa B signaling pathways in dystrophin-deficient skeletal muscle in response to mechanical stretch. J Cell Physiol 208(3):575-585. doi:10.1002/jcp.20696 (Pubitemid 44141882)
34. Dorchies OM, Wagner S, Vuadens O, Waldhauser K, Buetler TM, Kucera P, Ruegg UT (2006) 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 290(2):C616-C625. doi:10.1152/ajpcell.0. 0425.2005
35. 2+ Binding activity in mutated EF-hands of cardiac troponin C. J Biol Chem 268(32):24067-24073 (Pubitemid 23335387)
36. Du H, Cline MS, Osborne RJ, Tuttle DL, Clark TA, Donohue JP, Hall MP, Shiue L, Swanson MS, Thornton CA, Ares M Jr (2010) Aberrant alternative splicing and extracellular matrix gene expression in mouse models of myotonic dystrophy. Nat Struct Mol Biol 17(2):187-193. doi:10.1038/nsmb.1720
37. Durbeej M, Campbell KP (2002) Muscular dystrophies involving the dystrophin-glycoprotein complex: An overview of current mouse models. Curr Opin Genet Dev 12(3):349-361 (Pubitemid 34669835)
38. Eaton P (2006) Protein thiol oxidation in health and disease: techniques for measuring disulfides and related modifications in complex protein mixtures. Free Radical Biol Med 40(11):1889-1899. doi:10.1016/j.freeradbiomed.2005.12.037 (Pubitemid 43744434)
39. Edmondson DE, Mattevi A, Binda C, Li M, Hubalek F (2004) Structure and mechanism of monoamine oxidase. Curr Med Chem 11(15):1983-1993 (Pubitemid 38967724)
40. El-Shafey AF, Armstrong AE, Terrill JR, Grounds MD, Arthur PG (2011) Screening for increased protein thiol oxidation in oxidatively stressed muscle tissue. Free Radical Res 45(9):991-999. doi:10.3109/10715762.2011.590136
41. Escolar DM, Scacheri CG (2001) Pharmacologic and genetic therapy for childhood muscular dystrophies. Curr Neurol Neurosci Rep 1(2):168-174
42. Esterbauer H, Zollner H (1989) Methods for determination of aldehydic lipid peroxidation products. Free Radical Biol Med 7(2):197-203 (Pubitemid 19220721)
43. Finkel T (2012) Signal transduction by mitochondrial oxidants. J Biol Chem 287(7):4434-4440. doi:10.1074/jbc.R111.271999
44. Fisher-Wellman KH, Neufer PD (2012) Linking mitochondrial bioenergetics to insulin resistance via redox biology. TEM 23(3):142-153. doi:10.1016/j.tem. 2011.12.008
45. Flierl MA, Rittirsch D, Nadeau BA, Chen AJ, Sarma JV, Zetoune FS, McGuire SR, List RP, Day DE, Hoesel LM, Gao H, Van Rooijen N, Huber-Lang MS, Neubig RR, Ward PA (2007) Phagocytederived catecholamines enhance acute inflammatory injury. Nature 449(7163):721-725. doi:10.1038/nature06185 (Pubitemid 47552095)
46. Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97-112. doi:10.1146/annurev.bi.64.070195.000525
47. Gatley SJ, Sherratt SA (1976) The effects of diphenyleneiodonium on mitochondrial reactions. Relation of binding of diphenylene[125I]iodonium to mitochondria to the extent of inhibition of oxygen uptake. Biochem J 158(2):307-315
48. Gordon P, Dowben RM (1966) Catecholamine distribution in mice afflicted with muscular dystrophy. Am J Physiol 210(4):728-732
49. Grosso S, Perrone S, Longini M, Bruno C, Minetti C, Gazzolo D, Balestri P, Buonocore G (2008) Isoprostanes in dystrophinopathy: Evidence of increased oxidative stress. Brain Dev 30(6):391-395. doi:10.1016/j.braindev.2007.11.005 (Pubitemid 351602223)
50. Han R, Campbell KP (2007) Dysferlin and muscle membrane repair. Curr Opin Cell Biol 19(4):409-416. doi:10.1016/j.ceb.2007.07.001 (Pubitemid 47277508)
51. Haycock JW, MacNeil S, Jones P, Harris JB, Mantle D (1996) Oxidative damage to muscle protein in Duchenne muscular dystrophy. Neuroreport 8(1):357-361 (Pubitemid 126785588)
52. Haycock JW, Mac Neil S, Mantle D (1998) Differential protein oxidation in Duchenne and Becker muscular dystrophy. Neuroreport 9(10):2201-2207 (Pubitemid 28338206)
53. 2+ sensitivity in human cardiomyocytes. Antioxid Redox Signal 10(7):1175-1184. doi:10.1089/ars.2007.2014 (Pubitemid 351620310)
54. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS (2005) Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol 6(2):150-166. doi:10.1038/nrm1569 (Pubitemid 40215810)
55. Heusch P, Canton M, Aker S, van de Sand A, Konietzka I, Rassaf T, Menazza S, Brodde OE, Di Lisa F, Heusch G, Schulz R (2010) The contribution of reactive oxygen species and p38 mitogenactivated protein kinase to myofilament oxidation and progression of heart failure in rabbits. Br J Pharmacol 160(6):1408-1416. doi:10.1111/j.1476-5381.2010.00793.x
56. Hnia K, Hugon G, Rivier F, Masmoudi A, Mercier J, Mornet D (2007) 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 170(2):633-643. doi:10.2353/ajpath.2007.060344 (Pubitemid 47339400)
57. Hung RJ, Spaeth CS, Yesilyurt HG, Terman JR (2013) SelR reverses Mical-mediated oxidation of actin to regulate F-actin dynamics. Nat Cell Biol. doi:10.1038/ncb2871
58. Hunter MI, Mohamed JB (1986) Plasma antioxidants and lipid peroxidation products in Duchenne muscular dystrophy. Clin Chim Acta 155(2):123-131
59. Irwin WA, Bergamin N, Sabatelli P, Reggiani C, Megighian A, Merlini L, Braghetta P, Columbaro M, Volpin D, Bressan GM, Bernardi P, Bonaldo P (2003) Mitochondrial dysfunction and apoptosis in myopathic mice with collagen VI deficiency. Nat Genet 35(4):367-371. doi:10.1038/ng1270 (Pubitemid 37486921)
60. Iwasaki T, Terrill J, Shavlakadze T, Grounds MD, Arthur PG (2013) Visualizing and quantifying oxidized protein thiols in tissue sections: A comparison of dystrophic mdx and normal skeletal mouse muscles. Free Radical Biol Med 65C:1408-1416. doi:10. 1016/j.freeradbiomed.2013.09.024
61. 2+ signaling in the transverse tubule membrane. Proc Natl Acad Sci USA 110(51):20831-20836. doi:10.1073/pnas.1307960110
62. Khairallah RJ, Shi G, Sbrana F, Prosser BL, Borroto C, Mazaitis MJ, Hoffman EP, Mahurkar A, Sachs F, Sun Y, Chen YW, Raiteri R, Lederer WJ, Dorsey SG, Ward CW (2012) Microtubules underlie dysfunction in duchenne muscular dystrophy. Sci Signal 5(236):ra56. doi:10.1126/scisignal.2002829
63. Kim JH, Kwak HB, Thompson LV, Lawler JM (2013) Contribution of oxidative stress to pathology in diaphragm and limb muscles with Duchenne muscular dystrophy. J Muscle Res Cell Motil 34(1):1-13. doi:10.1007/s10974-012-9330-9
64. Koenig M, Monaco AP, Kunkel LM (1988) The complete sequence of dystrophin predicts a rod-shaped cytoskeletal protein. Cell 53(2):219-228
65. Kumar A, Boriek AM (2003) Mechanical stress activates the nuclear factor-kappaB pathway in skeletal muscle fibers: A possible role in Duchenne muscular dystrophy. FASEB J 17(3):386-396. doi:10.1096/fj.02-0542com (Pubitemid 36292954)
66. Kumar A, Takada Y, Boriek AM, Aggarwal BB (2004) Nuclear factor-kappaB: Its role in health and disease. J Mol Med 82(7):434-448. doi:10.1007/s00109-004- 0555-y (Pubitemid 39044283)
67. Kuo HJ, Maslen CL, Keene DR, Glanville RW (1997) Type VI collagen anchors endothelial basement membranes by interacting with type IV collagen. J Biol Chem 272(42):26522-26529 (Pubitemid 27458872)
68. Kurz T, Eaton JW, Brunk UT (2010) Redox activity within the lysosomal compartment: Implications for aging and apoptosis. Antioxid Redox Signal 13(4):511-523. doi:10.1089/ars 2009.3005
69. Lawler JM (2011) Exacerbation of pathology by oxidative stress in respiratory and locomotor muscles with Duchenne muscular dystrophy. J Physiol 589(Pt 9):2161-2170. doi:10.1113/jphysiol.2011.207456
70. Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, Dauwerse JG, Snider L, Straasheijm KR, van Ommen GJ, Padberg GW, Miller DG, Tapscott SJ, Tawil R, Frants RR, van der Maarel SM (2010) A unifying genetic model for facioscapulohumeral muscular dystrophy. Science 329(5999):1650-1653. doi:10.1126/science.1189044
71. Levine RL, Wehr N, Williams JA, Stadtman ER, Shacter E (2000) Determination of carbonyl groups in oxidized proteins. Methods Mol Biol 99:15-24. doi:10.1385/1-59259-054-3:15
72. Lo Conte M, Carroll KS (2013) The redox biochemistry of protein sulfenylation and sulfinylation. J Biol Chem 288(37):26480-26488. doi:10.1074/jbc.R113.467738
73. Manoli I, Le H, Alesci S, McFann KK, Su YA, Kino T, Chrousos GP, Blackman MR (2005) Monoamine oxidase-A is a major target gene for glucocorticoids in human skeletal muscle cells. FASEB J 19(10):1359-1361. doi:10.1096/fj.04-3660fje (Pubitemid 41113749)
74. Menazza S, Blaauw B, Tiepolo T, Toniolo L, Braghetta P, Spolaore B, Reggiani C, Di Lisa F, Bonaldo P, Canton M (2010) Oxidative stress by monoamine oxidases is causally involved in myofiber damage in muscular dystrophy. Hum Mol Genet 19(21):4207-4215. doi:10.1093/hmg/ddq339
75. Menazza S, Canton M, Sorato E, Boengler K, Schulz R, Di Lisa F (2014) Old and new biomarkers of oxidative stress in heart failure. Drug Discov Today Ther Strateg (in press
76. Merlini L, Morandi L, Granata C, Ballestrazzi A (1994) Bethlem myopathy: Early-onset benign autosomal dominant myopathy with contractures. Description of two new families. Neuromuscul Disord 4(5-6):503-511 (Pubitemid 24331539)
77. Messina S, Altavilla D, Aguennouz M, Seminara P, Minutoli L, Monici MC, Bitto A, Mazzeo A, Marini H, Squadrito F, Vita G (2006) Lipid peroxidation inhibition blunts nuclear factorkappaB activation, reduces skeletal muscle degeneration, and enhances muscle function in mdx mice. Am J Pathol 168(3):918-926 (Pubitemid 43327744)
78. Millay DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, Sweeney HL, Robbins J, Molkentin JD (2008) Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 14(4):442-447. doi:10.1038/nm1736 (Pubitemid 351499389)
79. 2+ sensitivity in fast-twitch muscle fibres of rats and humans. J Physiol 590(Pt 6):1443-1463. doi:10.1113/jphysiol.2011. 224535
80. Monici MC, Aguennouz M, Mazzeo A, Messina C, Vita G (2003) Activation of nuclear factor-kappaB in inflammatory myopathies and Duchenne muscular dystrophy. Neurology 60(6):993-997 (Pubitemid 36348934)
81. Moylan JS, Reid MB (2007) Oxidative stress, chronic disease, and muscle wasting. Muscle Nerve 35(4):411-429. doi:10.1002/mus.20743 (Pubitemid 46542961)
82. Nakae Y, Stoward PJ, Kashiyama T, Shono M, Akagi A, Matsuzaki T, Nonaka I (2004) Early onset of lipofuscin accumulation in dystrophin-deficient skeletal muscles of DMD patients and mdx mice. J Mol Histol 35(5):489-499 (Pubitemid 41410964)
83. Nguyen HX, Tidball JG (2003) Null mutation of gp91phox reduces muscle membrane lysis during muscle inflammation in mice. J Physiol 553(Pt 3):833-841. doi:10.1113/jphysiol.2003.051912 (Pubitemid 38035625)
84. Nguyen TT, Stevens MV, Kohr M, Steenbergen C, Sack MN, Murphy E (2011) Cysteine 203 of cyclophilin D is critical for cyclophilin D activation of the mitochondrial permeability transition pore. J Biol Chem 286(46):40184-40192. doi:10.1074/jbc.M111.243469
85. Palma E, Tiepolo T, Angelin A, Sabatelli P, Maraldi NM, Basso E, Forte MA, Bernardi P, Bonaldo P (2009) Genetic ablation of cyclophilin D rescues mitochondrial defects and prevents muscle apoptosis in collagen VI myopathic mice. Hum Mol Genet 18(11):2024-2031. doi:10.1093/hmg/ddp126
86. Pantic B, Trevisan E, Citta A, Rigobello MP, Marin O, Bernardi P, Salvatori S, Rasola A (2013) Myotonic dystrophy protein kinase (DMPK) prevents ROS-induced cell death by assembling a hexokinase II-Src complex on the mitochondrial surface. Cell Death Dis 4:e858. doi:10.1038/cddis.2013.385
87. Parker JM, Mendell JR (1974) Proximal myopathy induced by 5-HTimipramine simulates Duchenne dystrophy. Nature 247(436): 103-104
88. Pekovic V, Gibbs-Seymour I, Markiewicz E, Alzoghaibi F, Benham AM, Edwards R, Wenhert M, von Zglinicki T, Hutchison CJ (2011) Conserved cysteine residues in the mammalian lamin A tail are essential for cellular responses to ROS generation. Aging Cell 10(6):1067-1079. doi:10.1111/j.1474-9726.2011.00750.x
89. Pompella A, Maellaro E, Casini AF, Ferrali M, Ciccoli L, Comporti M (1987) Measurement of lipid peroxidation in vivo: A comparison of different procedures. Lipids 22(3):206-211
90. Powers SK, Kavazis AN, McClung JM (2007) Oxidative stress and disuse muscle atrophy. J Appl Physiol 102(6):2389-2397. doi:10.1152/japplphysiol.0 1202.2006 (Pubitemid 47080773)
91. Prosser BL, Ward CW, Lederer WJ (2011) X-ROS signaling: Rapid mechano-chemo transduction in heart. Science 333(6048):1440-1445. doi:10.1126/science.1202768
92. Putkey JA, Dotson DG, Mouawad P (1993) Formation of inter- and intramolecular disulfide bonds can activate cardiac troponin C. J Biol Chem 268(10):6827-6830 (Pubitemid 23105554)
93. Rando TA (2002) Oxidative stress and the pathogenesis of muscular dystrophies. Am J Phys Med Rehabil 81(11 Suppl):S175-S186. doi:10.1097/01.PHM. 0000029774.56528.A6 (Pubitemid 35192977)
94. Rando TA, Disatnik MH, Yu Y, Franco A (1998) Muscle cells from mdx mice have an increased susceptibility to oxidative stress. Neuromuscul Disord 8(1):14-21 (Pubitemid 28174930)
95. Renjini R, Gayathri N, Nalini A, Srinivas Bharath MM (2012) Oxidative damage in muscular dystrophy correlates with the severity of the pathology: Role of glutathione metabolism. Neurochem Res 37(4):885-898. doi:10.1007/s11064-011- 0683-z
96. Requena JR, Chao CC, Levine RL, Stadtman ER (2001) Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc Natl Acad Sci USA 98(1):69-74. doi:10.1073/pnas. 011526698 (Pubitemid 32095865)
97. Riganti C, Gazzano E, Polimeni M, Costamagna C, Bosia A, Ghigo D (2004) Diphenyleneiodonium inhibits the cell redox metabolism and induces oxidative stress. J Biol Chem 279(46):47726-47731. doi:10.1074/jbc.M406314200 (Pubitemid 39540920)
98. Sampaolesi M, Torrente Y, Innocenzi A, Tonlorenzi R, D'Antona G, Pellegrino MA, Barresi R, Bresolin N, De Angelis MG, Campbell KP, Bottinelli R, Cossu G (2003) Cell therapy of alpha-sarcoglycan null dystrophic mice through intra-arterial delivery of mesoangioblasts. Science 301(5632):487-492. doi:10.1126/science.1082254 (Pubitemid 36900300)
99. Shih JC, Wu JB, Chen K (2011) Transcriptional regulation and multiple functions of MAO genes. J Neural Transm 118(7):979-986. doi:10.1007/s00702-010- 0562-9
100. Shin J, Tajrishi MM, Ogura Y, Kumar A (2013) Wasting mechanisms in muscular dystrophy. Int J Biochem Cell Biol 45(10):2266-2279. doi:10.1016/j.biocel.2013.05.001
101. Sieprath T, Darwiche R, De Vos WH (2012) Lamins as mediators of oxidative stress. Biochem Biophys Res Commun 421(4):635-639. doi:10.1016/j.bbrc.2012.04. 058
102. Smith MA, Reid MB (2006) Redox modulation of contractile function in respiratory and limb skeletal muscle. Respir Physiol Neurobiol 151(2-3):229-241. doi:10.1016/j.resp.2005.12.011
103. Spurney CF, Knoblach S, Pistilli EE, Nagaraju K, Martin GR, Hoffman EP (2008) Dystrophin-deficient cardiomyopathy in mouse: Expression of Nox4 and Lox are associated with fibrosis and altered functional parameters in the heart. Neuromuscul Disord 18(5):371-381. doi:10.1016/j.nmd.2008.03.008
104. Stadtman ER, Berlett BS (1991) Fenton chemistry. Amino acid oxidation. J Biol Chem 266(26):17201-17211 (Pubitemid 21907925)
105. Stadtman ER, Berlett BS (1997) Reactive oxygen-mediated protein oxidation in aging and disease. Chem Res Toxicol 10(5):485-494. doi:10.1021/tx960133r (Pubitemid 27217204)
106. Stadtman ER, Van Remmen H, Richardson A, Wehr NB, Levine RL (2005) Methionine oxidation and aging. Biochim Biophys Acta 1703(2):135-140. doi:10.1016/j.bbapap.2004.08.010 (Pubitemid 40170436)
107. 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(6335):536-539. doi:10.1038/352536a0
108. Steinberg SF (2013) Oxidative stress and sarcomeric proteins. Circ Res 112(2):393-405. doi:10.1161/CIRCRESAHA.111.300496
109. Stuehr DJ, Fasehun OA, Kwon NS, Gross SS, Gonzalez JA, Levi R, Nathan CF (1991) Inhibition of macrophage and endothelial cell nitric oxide synthase by diphenyleneiodonium and its analogs. FASEB J 5(1):98-103 (Pubitemid 21892842)
110. Suzuki YJ, Carini M, Butterfield DA (2010) Protein carbonylation. Antioxid Redox Signal 12(3):323-325. doi:10.1089/ars.2009.2887
111. Terman A, Brunk UT (2006) Oxidative stress, accumulation of biological 'garbage', and aging. Antioxid Redox Signal 8(1-2):197-204. doi:10.1089/ars. 2006.8.197 (Pubitemid 43324546)
112. Terrill JR, Radley-Crabb HG, Iwasaki T, Lemckert FA, Arthur PG, Grounds MD (2013) Oxidative stress and pathology in muscular dystrophies: focus on protein thiol oxidation and dysferlinopathies. FEBS J 280(17):4149-4164. doi:10.1111/febs.12142
113. Tew DG (1993) Inhibition of cytochrome P450 reductase by the diphenyliodonium cation. Kinetic analysis and covalent modifications. Biochemistry 32(38):10209-10215 (Pubitemid 23312452)
114. Tidball JG (2005) Inflammatory processes in muscle injury and repair. Am J Physiol Reg I 288(2):R345-R353. doi:10.1152/ajpregu.0.0454.2004 (Pubitemid 40129595)
115. Tidball JG, Wehling-Henricks M (2007) The role of free radicals in the pathophysiology of muscular dystrophy. J Appl Physiol 102(4):1677-1686. doi:10.1152/japplphysiol.01145.2006 (Pubitemid 46571068)
116. Tonks NK (2013) Protein tyrosine phosphatases-from housekeeping enzymes to master regulators of signal transduction. FEBS J 280(2):346-378. doi:10.1111/febs.12077
117. Turki A, Hayot M, Carnac G, Pillard F, Passerieux E, Bommart S, Raynaud de Mauverger E, Hugon G, Pincemail J, Pietri S, Lambert K, Belayew A, Vassetzky Y, Juntas Morales R, Mercier J, Laoudj-Chenivesse D (2012) Functional muscle impairment in facioscapulohumeral muscular dystrophy is correlated with oxidative stress and mitochondrial dysfunction. Free Radic Biol Med 53(5):1068-1079. doi:10.1016/j.freeradbiomed.2012.06.041
118. Turrens JF (2003) Mitochondrial formation of reactive oxygenspecies. J Physiol 552(Pt 2):335-344. doi:10.1113/jphysiol.2003.049478 (Pubitemid 37321833)
119. Villalta SA, Nguyen HX, Deng B, Gotoh T, Tidball JG (2009) Shifts in macrophage phenotypes and macrophage competition for arginine metabolism affect the severity of muscle pathology in muscular dystrophy. Hum Mol Genet 18(3):482-496. doi:10.1093/hmg/ddn376
120. Wang SB, Foster DB, Rucker J, O'Rourke B, Kass DA, Van Eyk JE (2011) Redox regulation of mitochondrial ATP synthase: Implications for cardiac resynchronization therapy. Circ Res 109(7):750-757. doi:10.1161/CIRCRESAHA.111. 246124
121. Ward CW, Prosser BL, Lederer WJ (2013) Mechanical stretch induced activation of ROS/RNS signaling in striated muscle. Antioxid Redox Signal 20(6):929-936. doi:10.1089/ars.2013.5517
122. Wehling M, Spencer MJ, Tidball JG (2001) A nitric oxide synthase transgene ameliorates muscular dystrophy in mdx mice. J Cell Biol 155(1):123-131. doi:10.1083/jcb.200105110 (Pubitemid 34286213)
123. Weir EK, Wyatt CN, Reeve HL, Huang J, Archer SL, Peers C (1994) Diphenyleneiodonium inhibits both potassium and calcium currents in isolated pulmonary artery smooth muscle cells. J Appl Physiol 76(6):2611-2615 (Pubitemid 24184785)
124. Whitehead NP, Pham C, Gervasio OL, Allen DG (2008) Nacetylcysteine ameliorates skeletal muscle pathophysiology in mdx mice. J Physiol 586(7):2003-2014. doi:10.1113/jphysiol.2007.148338 (Pubitemid 351997524)
125. Whitehead NP, Yeung EW, Froehner SC, Allen DG (2010) Skeletal muscle NADPH oxidase is increased and triggers stretchinduced damage in the mdx mouse. PLoS One 5(12):e15354. doi:10.1371/journal.pone.0015354
126. Williams IA, Allen DG (2007) The role of reactive oxygen species in the hearts of dystrophin-deficient mdx mice. Am J Physiol Heart Circ Physiol 293(3):H1969-H1977. doi:10.1152/ajpheart.00489.2007 (Pubitemid 47367249)
127. Williams DL Jr, Swenson CA (1982) Disulfide bridges in tropomyosin. Effect on ATPase activity of actomyosin. Eur J Biochem 127(3):495-499 (Pubitemid 13214664)
128. Wright TL, O'Neill JA, Olson WH (1973) Abnormal intrafibrillar monoamines in sex-linked muscular dystrophy. Neurology 23(5):510-517
129. 2+ currents in type I cells isolated from the neonatal rat carotid body. Neurosci Lett 172(1-2):63-66
130. Youdim MB, Edmondson D, Tipton KF (2006) The therapeutic potential of monoamine oxidase inhibitors. Nat Rev Neurosci 7(4):295-309. doi:10.1038/nrn1883
131. Zima AV, Blatter LA (2006) Redox regulation of cardiac calcium channels and transporters. Cardiovasc Res 71(2):310-321. doi:10.1016/j.cardiores.2006.02. 019