Role of reactive oxygen species in the defective regeneration seen in aging muscle

Free Radical Biology and Medicine

Volumn 65, Issue , 2013, Pages 317-323

  Vasilaki, Aphrodite ^a   Jackson, Malcolm J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

Aging; Innervation; Neuromuscular junction; Reactive oxygen species; Regeneration; Skeletal muscle

Indexed keywords

CHOLINERGIC RECEPTOR; EARLY PREGNANCY FACTOR; GLUTATHIONE PEROXIDASE 1; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PHOSPHOLIPASE A2; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; XANTHINE OXIDASE;

AGING; CELL ACTIVATION; CELL FUSION; DUCHENNE MUSCULAR DYSTROPHY; EXERCISE; HUMAN; MOTONEURON; MUSCLE CELL; MUSCLE CONTRACTION; MUSCLE DEVELOPMENT; MUSCLE INJURY; MUSCLE INNERVATION; MUSCLE MASS; MUSCLE REGENERATION; MUSCLE REINNERVATION; NERVE CELL DIFFERENTIATION; NEUROMUSCULAR SYNAPSE; NONHUMAN; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUALITY OF LIFE; RESPIRATORY CHAIN; REVIEW; SARCOMERE; SARCOPENIA; SATELLITE CELL; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; PATHOLOGY; PHYSIOLOGY; REGENERATION;

AGING; HUMANS; MUSCLE, SKELETAL; REACTIVE OXYGEN SPECIES; REGENERATION;

EID: 84881013840     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2013.07.008     Document Type: Review

References (73)

1. C.E. Lee, A. McArdle, and R.D. Griffiths The role of hormones, cytokines and heat shock proteins during age-related muscle loss Clin. Nutr. 26 2007 524 534 (Pubitemid 47618317)
2. L. Larsson, and T. Ansved Effects of ageing on the motor unit Prog. Neurobiol. 45 1995 397 458
3. S.V. Brooks, and J.A. Faulkner Contraction-induced injury: recovery of skeletal muscles in young and old mice Am. J. Physiol. 258 1990 C436 C442
4. J. Ehrhardt, and J. Morgan Regenerative capacity of skeletal muscle Curr. Opin. Neurol. 18 2005 548 553 (Pubitemid 41476141)
5. X. Shi, and D.J. Garry Muscle stem cells in development, regeneration, and disease Genes Dev. 20 2006 1692 1708 (Pubitemid 43992877)
6. J. Sastre, F.V. Pallardo, and J. Vina The role of mitochondrial oxidative stress in aging Free Radic. Biol. Med. 35 2003 1 8 (Pubitemid 36782332)
7. A. Vasilaki, D. Simpson, F. McArdle, L. McLean, R.J. Beynon, H. Van Remmen, A.G. Richardson, A. McArdle, J.A. Faulkner, and M.J. Jackson Formation of 3-nitrotyrosines in carbonic anhydrase III is a sensitive marker of oxidative stress in skeletal muscle Proteomics Clin. Appl. 1 2007 362 372
8. C.S. Broome, A.C. Kayani, J. Palomero, W.H. Dillmann, R. Mestril, M.J. Jackson, and A. McArdle Effect of lifelong overexpression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after nondamaging contractile activity FASEB J 20 2006 1549 1551
9. Palomero, J.; Vasilaki, A.; Pye, D.; McArdle, A.; Jackson, M.J. Aging increases the oxidation of dichlorohydrofluorescein in single isolated skeletal muscle fibers at rest, but not during contractionsAm. J. Physiol. Regul. Integr. Comp. Physiol.; 2013.
10. S.B. Charge, and M.A. Rudnicki Cellular and molecular regulation of muscle regeneration Physiol. Rev. 84 2004 209 238 (Pubitemid 38049880)
11. A.B. Borisov, E.I. Dedkov, and B.M. Carlson Abortive myogenesis in denervated skeletal muscle: differentiative properties of satellite cells, their migration, and block of terminal differentiation Anat. Embryol. 209 2005 269 279 (Pubitemid 40674818)
12. T. Kobayashi, V. Askanas, and W.K. Engel Human muscle cultured in monolayer and cocultured with fetal rat spinal cord: importance of dorsal root ganglia for achieving successful functional innervation J. Neurosci 7 1987 3131 3141
13. I.M. Conboy, and T.A. Rando Aging, stem cells and tissue regeneration: lessons from muscle Cell Cycle 4 2005 407 410 (Pubitemid 41359725)
14. M.E. Carlson, H.S. Silva, and I.M. Conboy Aging of signal transduction pathways, and pathology Exp. Cell Res. 314 2008 1951 1961 (Pubitemid 351649367)
15. H. Degens Age-related skeletal muscle dysfunction: causes and mechanisms J. Musculoskeletal Neuronal Interact 7 2007 246 252 (Pubitemid 350238152)
16. A. McArdle, W.H. Dillmann, R. Mestril, J.A. Faulkner, and M.J. Jackson Overexpression of HSP70 in mouse skeletal muscle protects against muscle damage and age-related muscle dysfunction FASEB J 18 2004 355 357
17. G. Valdez, J.C. Tapia, H. Kang, G.D. Clemenson Jr, F.H. Gage, J.W. Lichtman, and J.R. Sanes Attenuation of age-related changes in mouse neuromuscular synapses by caloric restriction and exercise Proc. Natl. Acad. Sci. USA 107 2010 14863 14868
18. E. Verdu, D. Ceballos, J.J. Vilches, and X. Navarro Influence of aging on peripheral nerve function and regeneration J. Peripher. Nerv. Syst. 5 2000 191 208 (Pubitemid 32037991)
19. M. Kawabuchi, Z. Chongjian, A.T. Islam, K. Hirata, and O. Nada The effect of aging on the morphological nerve changes during muscle reinnervation after nerve crush Restor. Neurol. Neurosci. 13 1998 117 127 (Pubitemid 29015948)
20. M. Kawabuchi, C.J. Zhou, S. Wang, K. Nakamura, W.T. Liu, and K. Hirata The spatiotemporal relationship among Schwann cells, axons and postsynaptic acetylcholine receptor regions during muscle reinnervation in aged rats Anat. Rec. 264 2001 183 202 (Pubitemid 32976820)
21. M.J. Jackson Reactive oxygen species and redox-regulation of skeletal muscle adaptations to exercise Philos. Trans. R. Soc. London B Biol. Sci 360 2005 2285 2291 (Pubitemid 46682147)
22. L.L. Ji Oxidative stress during exercise: implication of antioxidant nutrients Free Radic. Biol. Med. 18 1995 1079 1086
23. 2+ in mitochondrial myopathy Hum. Mol. Genet 18 2009 278 288
24. J. St-Pierre, J.A. Buckingham, S.J. Roebuck, and M.D. Brand Topology of superoxide production from different sites in the mitochondrial electron transport chain J. Biol. Chem. 277 2002 44784 44790 (Pubitemid 36159072)
25. G.K. Sakellariou, A. Vasilaki, J. Palomero, A. Kayani, L. Zibrik, A. McArdle, and M.J. Jackson Studies of mitochondrial and nonmitochondrial sources implicate nicotinamide adenine dinucleotide phosphate oxidase(s) in the increased skeletal muscle superoxide generation that occurs during contractile activity Antioxid. Redox Signal. 18 2013 603 621
26. S.K. Powers, and M.J. Jackson Exercise-induced oxidative stress: cellular mechanisms and impact on muscle force production Physiol. Rev. 88 2008 1243 1276
27. M.C. Gomez-Cabrera, C. Borras, F.V. Pallardo, J. Sastre, L.L. Ji, and J. Vina Decreasing xanthine oxidase-mediated oxidative stress prevents useful cellular adaptations to exercise in rats J. Physiol. 567 2005 113 120 (Pubitemid 41167309)
28. A. McArdle, D. Pattwell, A. Vasilaki, R.D. Griffiths, and M.J. Jackson Contractile activity-induced oxidative stress: cellular origin and adaptive responses Am. J. Physiol. Cell Physiol. 280 2001 C621 C627
29. M.B. Reid, T. Shoji, M.R. Moody, and M.L. Entman Reactive oxygen in skeletal muscle. II. Extracellular release of free radicals J. Appl. Physiol. 73 1992 1805 1809
30. A. Vasilaki, A. Mansouri, H. Remmen, J.H. van der Meulen, L. Larkin, A.G. Richardson, A. McArdle, J.A. Faulkner, and M.J. Jackson Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity Aging Cell 5 2006 109 117 (Pubitemid 44056502)
31. T.W. Balon, and J.L. Nadler Nitric oxide release is present from incubated skeletal muscle preparations J. Appl. Physiol. 77 1994 2519 2521
32. L. Kobzik, M.B. Reid, D.S. Bredt, and J.S. Stamler Nitric oxide in skeletal muscle Nature 372 1994 546 548 (Pubitemid 24368535)
33. B. Halliwell Oxidative stress in skeletal muscle 1998 Birkhauser Verlag Basel, Switzerland
34. J. Bejma, and L.L. Ji Aging and acute exercise enhance free radical generation in rat skeletal muscle J. Appl. Physiol. 87 1999 465 470 (Pubitemid 29330715)
35. M.J. Jackson, and A. McArdle Age-related changes in skeletal muscle reactive oxygen species generation and adaptive responses to reactive oxygen species J. Physiol. 589 2011 2139 2145
36. Talbert, E.E.; Smuder, A.J.; Min, K.; Kwon, O.S.; Szeto, H.H.; Powers, S.K. Immobilization-induced activation of key proteolytic systems in skeletal muscles is prevented by a mitochondria-targeted antioxidant. J. Appl. Physiol.; 2013.
37. Y.J. Piao, Y.H. Seo, F. Hong, J.H. Kim, Y.J. Kim, M.H. Kang, B.S. Kim, S.A. Jo, I. Jo, D.M. Jue, I. Kang, J. Ha, and S.S. Kim Nox 2 stimulates muscle differentiation via NF-kappaB/iNOS pathway Free Radic. Biol. Med. 38 2005 989 1001 (Pubitemid 40386545)
38. F. Hong, J. Lee, J.W. Song, S.J. Lee, H. Ahn, J.J. Cho, J. Ha, and S.S. Kim Cyclosporin A blocks muscle differentiation by inducing oxidative stress and inhibiting the peptidyl-prolyl-cis-trans isomerase activity of cyclophilin A: cyclophilin A protects myoblasts from cyclosporin A-induced cytotoxicity FASEB J. 16 2002 1633 1635
39. J.M. Hansen, M. Klass, C. Harris, and M. Csete A reducing redox environment promotes C2C12 myogenesis: implications for regeneration in aged muscle Cell Biol. Int. 31 2007 546 553 (Pubitemid 46660641)
40. S. Lee, H.S. Shin, P.K. Shireman, A. Vasilaki, H. Van Remmen, and M.E. Csete Glutathione-peroxidase-1 null muscle progenitor cells are globally defective Free Radic. Biol. Med. 41 2006 1174 1184 (Pubitemid 44331577)
41. A. Vasilaki, F. McArdle, L.M. Iwanejko, and A. McArdle Adaptive responses of mouse skeletal muscle to contractile activity: the effect of age Mech. Ageing Dev. 127 2006 830 839 (Pubitemid 44602139)
42. H. Kawamata, and G. Manfredi Import, maturation, and function of SOD1 and its copper chaperone CCS in the mitochondrial intermembrane space Antioxid. Redox Signal 13 2010 1375 1384
43. F.L. Muller, W. Song, Y. Liu, A. Chaudhuri, S. Pieke-Dahl, R. Strong, T.T. Huang, C.J. Epstein, and L.J. Roberts 2nd; Csete, M.; Faulkner, J. A.; Van Remmen, H. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy Free Radic. Biol. Med. 40 2006 1993 2004 (Pubitemid 43728860)
44. I. Dalle-Donne, R. Rossi, D. Giustarini, A. Milzani, and R. Colombo Protein carbonyl groups as biomarkers of oxidative stress Clin. Chim. Acta 329 2003 23 38 (Pubitemid 36187411)
45. P. Ghezzi, and V. Bonetto Redox proteomics: identification of oxidatively modified proteins Proteomics 3 2003 1145 1153 (Pubitemid 36929536)
46. R.L. Levine, and E.R. Stadtman Oxidative modification of proteins during aging Exp. Gerontol. 36 2001 1495 1502 (Pubitemid 32768727)
47. A. Vasilaki, J.H. van der Meulen, L. Larkin, D.C. Harrison, T. Pearson, H. Van Remmen, A. Richardson, S.V. Brooks, M.J. Jackson, and A. McArdle The age-related failure of adaptive responses to contractile activity in skeletal muscle is mimicked in young mice by deletion of Cu,Zn superoxide dismutase Aging Cell 9 2010 979 990
48. D.G. Flood, A.G. Reaume, J.A. Gruner, E.K. Hoffman, J.D. Hirsch, Y.G. Lin, K.S. Dorfman, and R.W. Scott Hindlimb motor neurons require Cu/Zn superoxide dismutase for maintenance of neuromuscular junctions Am. J. Pathol. 155 1999 663 672 (Pubitemid 29370416)
49. Y.C. Jang, M.S. Lustgarten, Y. Liu, F.L. Muller, A. Bhattacharya, H. Liang, A.B. Salmon, S.V. Brooks, L. Larkin, C.R. Hayworth, A. Richardson, and H. Van Remmen Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration FASEB J 24 2010 1376 1390
50. L.M. Larkin, C.S. Davis, C. Sims-Robinson, T.Y. Kostrominova, H.V. Remmen, A. Richardson, E.L. Feldman, and S.V. Brooks Skeletal muscle weakness due to deficiency of CuZn-superoxide dismutase is associated with loss of functional innervation Am. J. Physiol. Regul. Integr. Comp. Physiol 301 2011 R1400 R1407
51. J.M. Shefner, A.G. Reaume, D.G. Flood, R.W. Scott, N.W. Kowall, R.J. Ferrante, D.F. Siwek, M. Upton-Rice, and R.H. Brown Jr. Mice lacking cytosolic copper/zinc superoxide dismutase display a distinctive motor axonopathy Neurology 53 1999 1239 1246 (Pubitemid 29480082)
52. C.D. Smith, J.M. Carney, P.E. Starke-Reed, C.N. Oliver, E.R. Stadtman, R.A. Floyd, and W.R. Markesbery Excess brain protein oxidation and enzyme dysfunction in normal aging and in Alzheimer disease Proc. Natl. Acad. Sci. USA 88 1991 10540 10543 (Pubitemid 21915871)
53. A. Navarro, M.J. Sanchez Del Pino, C. Gomez, J.L. Peralta, and A. Boveris Behavioral dysfunction, brain oxidative stress, and impaired mitochondrial electron transfer in aging mice Am. J. Physiol. Regul. Integr. Comp. Physiol 282 2002 R985 R992
54. T.M. Manini, S.L. Hong, and B.C. Clark Aging and muscle: a neuron′s perspective Curr. Opin. Clin. Nutr. Metab. Care 16 2013 21 26
55. K. Opalach, S. Rangaraju, I. Madorsky, C. Leeuwenburgh, and L. Notterpek Lifelong calorie restriction alleviates age-related oxidative damage in peripheral nerves Rejuvenation Res 13 2010 65 74
56. E. Mariani, M.C. Polidori, A. Cherubini, and P. Mecocci Oxidative stress in brain aging, neurodegenerative and vascular diseases: an overview J. Chromatogr. B Analyt. Technol.Biomed. Life Sci. 827 2005 65 75 (Pubitemid 41551598)
57. M. Buck, and M. Chojkier Muscle wasting and dedifferentiation induced by oxidative stress in a murine model of cachexia is prevented by inhibitors of nitric oxide synthesis and antioxidants EMBO J 15 1996 1753 1765 (Pubitemid 26119211)
58. D.G. Allen, and N.P. Whitehead Duchenne muscular dystrophy - what causes the increased membrane permeability in skeletal muscle? Int. J. Biochem. Cell Biol. 43 2011 290 294
59. N.P. Whitehead, E.W. Yeung, and D.G. Allen Muscle damage in mdx (dystrophic) mice: role of calcium and reactive oxygen species Clin. Exp. Pharmacol. Physiol. 33 2006 657 662 (Pubitemid 43894030)
60. S.K. Powers, A.J. Smuder, and A.R. Judge Oxidative stress and disuse muscle atrophy: cause or consequence? Curr. Opin. Clin. Nutr. Metab. Care 15 2012 240 245
61. A.C. Kayani, G.L. Close, W.H. Dillmann, R. Mestril, M.J. Jackson, and A. McArdle Overexpression of HSP10 in skeletal muscle of transgenic mice prevents the age-related fall in maximum tetanic force generation and muscle cross-sectional area Am. J. Physiol. Regul. Integr. Comp. Physiol 299 2010 R268 R276
62. D.C. Guttridge, C. Albanese, J.Y. Reuther, R.G. Pestell, and A.S. Baldwin Jr. NF-kappaB controls cell growth and differentiation through transcriptional regulation of cyclin D1 Mol. Cell. Biol. 19 1999 5785 5799 (Pubitemid 29339933)
63. D.C. Guttridge, M.W. Mayo, L.V. Madrid, C.Y. Wang, and A.S. Baldwin Jr. NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia Science 289 2000 2363 2366
64. D. Thaloor, K.J. Miller, J. Gephart, P.O. Mitchell, and G.K. Pavlath Systemic administration of the NF-kappaB inhibitor curcumin stimulates muscle regeneration after traumatic injury Am. J. Physiol. 277 1999 C320 C329
65. F. Mourkioti, P. Kratsios, T. Luedde, Y.H. Song, P. Delafontaine, R. Adami, V. Parente, R. Bottinelli, M. Pasparakis, and N. Rosenthal Targeted ablation of IKK2 improves skeletal muscle strength, maintains mass, and promotes regeneration J. Clin. Invest. 116 2006 2945 2954 (Pubitemid 44684479)
66. E.W. Petersen, K. Ostrowski, T. Ibfelt, M. Richelle, E. Offord, J. Halkjaer-Kristensen, and B.K. Pedersen Effect of vitamin supplementation on cytokine response and on muscle damage after strenuous exercise Am. J. Physiol. Cell Physiol 280 2001 C1570 C1575
67. A.C. Howard, A.K. McNeil, and P.L. McNeil Promotion of plasma membrane repair by vitamin E Nat. Commun 2 2011 597
68. K. Nakazato, H. Song, and T. Waga Dietary apple polyphenols enhance gastrocnemius function in Wistar rats Med. Sci. Sports Exerc. 39 2007 934 940 (Pubitemid 46883463)
69. K. Nakazato, E. Ochi, and T. Waga Dietary apple polyphenols have preventive effects against lengthening contraction-induced muscle injuries Mol. Nutr. Food Res. 54 2010 364 372
70. J. Kaminski, A. Lancon, V. Aires, E. Limagne, E. Tili, J.J. Michaille, and N. Latruffe Resveratrol initiates differentiation of mouse skeletal muscle-derived C2C12 myoblasts Biochem. Pharmacol. 84 2012 1251 1259
71. K.H. Myburgh, M.J. Kruger, and C. Smith Accelerated skeletal muscle recovery after in vivo polyphenol administration J. Nutr. Biochem. 23 2012 1072 1079
72. M.J. Kruger, and C. Smith Postcontusion polyphenol treatment alters inflammation and muscle regeneration Med. Sci. Sports Exerc. 44 2012 872 880
73. A.L. Charles, A. Meyer, S. Dal-Ros, C. Auger, N. Keller, T.G. Ramamoorthy, J. Zoll, D. Metzger, V. Schini-Kerth, and B. Geny Polyphenols prevent ageing-related impairment in skeletal muscle mitochondrial function through decreased reactive oxygen species production Exp. Physiol. 98 2013 536 545