Hostname: page-component-586b7cd67f-g8jcs Total loading time: 0 Render date: 2024-11-29T18:59:30.110Z Has data issue: false hasContentIssue false
  • English
  • Français

Skeletal muscle aging

Part of: Bespoke shallow archive Weizmann

Published online by Cambridge University Press:  01 February 2007

Graeme L Close ,
Philippa Haggan  and
Anne McArdle
Graeme L Close
Affiliation:
School of Clinical Sciences, University of Liverpool, UK
Philippa Haggan
Affiliation:
School of Clinical Sciences, University of Liverpool, UK
Anne McArdle*
Affiliation:
School of Clinical Sciences, University of Liverpool, UK
*
Address for correspondence: A McArdle, Division of Metabolic and Cellular Medicine, School of Clinical Science University of Liverpool, Liverpool L69 3GA, UK.
Get access Rights & Permissions [Opens in a new window]

Extract

Average world life expectancy has seen a dramatic rise over the last two centuries although active life expectancy remains relatively unchanged. One reason for this is that aging results in skeletal muscle becoming smaller, weaker and more susceptible to contraction-induced injury. By the age of 70, muscle strength is reduced by around 30–40% and this can have catastrophic effects on quality of life. Despite a vast amount of research into age-related changes in skeletal muscle, the exact mechanisms responsible for this is still unclear and thus treatments to preserve muscle function with aging remain elusive.

Type
Biological gerontology
Information
Reviews in Clinical Gerontology , Volume 17 , Issue 1 , February 2007 , pp. 13 - 23
Copyright
Copyright © Cambridge University Press 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1Close, GL, Kayani, A, Vasilaki, A, McArdle, A. Skeletal muscle damage with exercise and aging. Sports Med 2005; 35:413–27.CrossRefGoogle ScholarPubMed
2McArdle, A, Vasilaki, A, Jackson, M. Exercise and skeletal muscle ageing: cellular and molecular mechanisms. Ageing Res Rev 2002; 1:79–93.CrossRefGoogle ScholarPubMed
3Porter, MM, Vandervoort, AA, Lexell, J. Aging of human muscle: structure, function and adaptability. Scand J Med Sci Sports 1995; 5:129–42.CrossRefGoogle ScholarPubMed
4McCully, KK, Faulkner, JA. Characteristics of lengthening contractions associated with injury to skeletal muscle fibers. J Appl Physiol 1986; 61:293–99.CrossRefGoogle ScholarPubMed
5McArdle, A, Van Der Meulen, JH, Catapano, M, Symons, MCR, Faulkner, JA, Jackson, MJ. Free radical activity following contraction-induced injury to the extensor digitorum longus muscles of rats. Free Radic Biol Med 1999; 26:1085–91.CrossRefGoogle Scholar
6Close, GL, Ashton, T, Cable, T, Doran, D, MacLaren, DP. Eccentric exercise, isokinetic muscle torque and delayed-onset muscle soreness: the role of reactive oxygen species. Eur J Appl Physiol 2004; 91:615–21.CrossRefGoogle ScholarPubMed
7Brooks, SV, Faulkner, JA. Contraction-induced injury: recovery of skeletal muscles in young and old mice. Am J Physiol 1990; 258 (3 Pt 1): C436–42.CrossRefGoogle ScholarPubMed
8McArdle, A, Van Der Meulen, JH, Catapano, M, Symons, MC, Faulkner, JA, Jackson, MJ. Free radical activity following contraction-induced injury to the extensor digitorum longus muscles of rats. Free Radic Biol Med 1999; 26:1085–91.CrossRefGoogle Scholar
9Lexell, J, Downham, D, Sjostrom, M. Distribution of different fibre types in human skeletal muscles. Fibre type arrangement in m.vastus lateralis from three groups of healthy men between 15 and 83 years. J Neurol Sci 1986; 72:211–22.CrossRefGoogle ScholarPubMed
10Lexell, J, Taylor, CC, Sjostrom, M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 1988; 84:275–94.CrossRefGoogle ScholarPubMed
11Kamel, HK. Sarcopenia and aging. Nutr Rev 2003; 61:157–67.CrossRefGoogle Scholar
12Nakagawa, Y, Hattori, M, Harada, K, Shirase, R, Bando, M, Okano, G. Age-related changes in intramyocellular lipid in humans by in vivo H-MR spectroscopy. Gerontology 2007; 53:218–23.CrossRefGoogle ScholarPubMed
13Conley, KE, Amara, CE, Jubrias, SA, Marcinek, DJ. Mitochondrial function, fibre types and ageing: new insights from human muscle in vivo. Exp Physiol 2007; 92:333–39.CrossRefGoogle ScholarPubMed
14Miller, RA. ‘Accelerated aging’: a primrose path to insight? Aging Cell 2004; 3:47–51.CrossRefGoogle ScholarPubMed
15McArdle, A, Dillmann, WH, Mestril, R, Faulkner, JA, Jackson, MJ. Overexpression of HSP70 in mouse skeletal muscle protects against muscle damage and age-related muscle dysfunction. FASEB J 2004; 18:355–57.CrossRefGoogle ScholarPubMed
16Morse, CI, Thom, JM, Reeves, ND, Birch, KM, Narici, MV. In vivo physiological cross-sectional area and specific force are reduced in the gastrocnemius of elderly men. J Appl Physiol 2005; 99:1050–55.CrossRefGoogle ScholarPubMed
17Zerba, E, Komorowski, TE, Faulkner, JA. Free radical injury to skeletal muscles of young, adult, and old mice. Am J Physiol 1990; 258 (3 Pt 1): C429–35.CrossRefGoogle ScholarPubMed
18Harman, D. Aging: a theory based on free radical and radiation chemistry. J Gerontol 1956; 11:298–300.CrossRefGoogle ScholarPubMed
19Valko, M, Rhodes, CJ, Moncol, J, Izakovic, M, Mazur, M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006; 160:1–40.CrossRefGoogle ScholarPubMed
20St-Pierre, J, Buckingham, JA, Roebuck, SJ, Brand, MD. Topology of superoxide production from different sites in the mitochondrial electron transport chain. J Biol Chem 2002; 277:44784–90.CrossRefGoogle ScholarPubMed
21Ames, BN, Shigenaga, MK, Hagen, TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA 1993; 90:7915–22.CrossRefGoogle ScholarPubMed
22Close, GL, McArdle, F. Antioxidants and free radicals. Nutrition and Sport. Elsevier, London, 2007.Google Scholar
23Halliwell, B. Free radicals and antioxidants: a personal view. Nutr Rev 1994; 52 (8 Pt 1):253–65.CrossRefGoogle ScholarPubMed
24Nohl, H. Involvement of free radicals in ageing: a consequence or cause of senescence. Br Med Bull 1993; 49:653–67.CrossRefGoogle ScholarPubMed
25Biesalski, HK. Free radical theory of aging. Curr Opin Clin Nutr Metab Care 2002; 5:5–10.CrossRefGoogle ScholarPubMed
26Squier, TC. Oxidative stress and protein aggregation during biological aging. Exp Gerontol 2001; 36:1539–50.CrossRefGoogle ScholarPubMed
27Khassaf, M, Child, RB, McArdle, A, Brodie, DA, Esanu, C, Jackson, MJ. Time-course of responses of human skeletal muscle to oxidative stress induced by non-damaging exercise. J Appl Physiol 2001; 90:1031–35.CrossRefGoogle Scholar
28Ji, LL. Exercise-induced modulation of antioxidant defense. Ann N Y Acad Sci 2002; 959:82–92.CrossRefGoogle ScholarPubMed
29McArdle, A, Pattwell, D, Vasilaki, A, Griffiths, RD, Jackson, MJ. Contractile activity-induced oxidative stress: cellular origin and adaptive responses. Am J Physiol Cell Physiol 2001; 280:C621–27.CrossRefGoogle ScholarPubMed
30Harman, D. The biologic clock: the mitochondria? J Am Geriatr Soc 1972; 20:145–7.CrossRefGoogle ScholarPubMed
31Reid, MB, Durham, WJ. Generation of reactive oxygen and nitrogen species in contracting skeletal muscle: potential impact on aging. Ann N Y Acad Sci 2002; 959:108–16.CrossRefGoogle ScholarPubMed
32Faragher, RG, Kipling, D. How might replicative senescence contribute to human ageing? Bioessays 1998; 20:985–91.3.0.CO;2-A>CrossRefGoogle ScholarPubMed
33Campisi, J. The biology of replicative senescence. Eur J Cancer 1997; 33:703–09.CrossRefGoogle ScholarPubMed
34Hayflick, L. The limited in vitro lifetime of human diploid cell strains. Exp Cell Res 1965; 37:614–36.CrossRefGoogle ScholarPubMed
35Dimri, GP, Lee, X, Basile, G et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc Natl Acad Sci 1995; 92: 9363–67.CrossRefGoogle ScholarPubMed
36Conboy, IM, Conboy, MJ, Smythe, GM, Rando, TA. Notch-mediated restoration of regenerative potential to aged muscle. Science 2003; 302 (5650):1575–77.CrossRefGoogle ScholarPubMed
37Lee, S, Shin, HS, Shireman, PK, Vasilaki, A, Van Remmen, H, Csete, ME. Glutathione-peroxidase-1 null muscle progenitor cells are globally defective. Free Radic Biol Med 2006; 41:1174–84.CrossRefGoogle ScholarPubMed
38Ehrhardt, J, Morgan, J. Regenerative capacity of skeletal muscle. Curr Opin Neurol 2005; 18:548–53.CrossRefGoogle ScholarPubMed
39Conboy, IM, Rando, TA. Aging, stem cells and tissue regeneration: lessons from muscle. Cell Cycle 2005; 4:407–10.CrossRefGoogle ScholarPubMed
40Carlson, BM, Faulkner, JA. Muscle transplantation between young and old rats: age of host determines recovery. Am J Physiol 1989; 256 (6 Pt 1):C1262–66.CrossRefGoogle Scholar
41Conboy, IM, Conboy, MJ, Wagers, AJ, Girma, ER, Weissman, IL, Rando, TA. Rejuvenation of aged progenitor cells by exposure to a young systemic environment. Nature 2005; 433 (7027):760–64.CrossRefGoogle ScholarPubMed
42Kujoth, GC, Hiona, A, Pugh, TD et al. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 2005; 309 (5733):481–84.CrossRefGoogle ScholarPubMed
43Jacobs, HT. The mitochondrial theory of aging: dead or alive? Aging Cell 2003; 2:11–17.CrossRefGoogle ScholarPubMed
44Mecocci, P, Fano, G, Fulle, S et al. Age-dependent increases in oxidative damage to DNA, lipids, and proteins in human skeletal muscle. Free Radic Biol Med 1999; 26:303–08.CrossRefGoogle ScholarPubMed
45Sanz, A, Pamplona, R, Barja, G. Is the mitochondrial free radical theory of aging intact? Antioxid Redox Signal 2006; 8:582–99.CrossRefGoogle ScholarPubMed
46Sohal, RS, Dubey, A. Mitochondrial oxidative damage, hydrogen peroxide release, and aging. Free Radic Biol Med 1994; 16:621–26.CrossRefGoogle ScholarPubMed
47Lass, A, Sohal, BH, Weindruch, R, Forster, MJ, Sohal, RS. Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria. Free Radic Biol Med 1998; 25:1089–97.CrossRefGoogle ScholarPubMed
48Mansouri, A, Muller, FL, Liu, Y et al. Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging. Mech Ageing Dev 2006; 127:298–306.CrossRefGoogle ScholarPubMed
49Vasilaki, A, Mansouri, A, Remmen, H et al. Free radical generation by skeletal muscle of adult and old mice: effect of contractile activity. Aging Cell 2006; 5:109–17.CrossRefGoogle ScholarPubMed
50Anderson, EJ, Neufer, PD. Type II skeletal myofibers possess unique properties that potentiate mitochondrial H(2)O(2) generation. Am J Physiol Cell Physiol 2006; 290:C844–51.CrossRefGoogle Scholar
51Close, GL, Kayani, AC, Ashton, T, McArdle, A, Jackson, MJ. Release of superoxide from skeletal muscle of adult and old mice: an experimental test of the reductive hotspot hypothesis. Aging Cell 2007; 6:189–95.CrossRefGoogle ScholarPubMed
52Pansarasa, O, Bertorelli, L, Vecchiet, J, Felzani, G, Marzatico, F. Age-dependent changes of antioxidant activities and markers of free radical damage in human skeletal muscle. Free Radic Biol Med 1999; 27:617–22.CrossRefGoogle ScholarPubMed
53Sundaram, K, Panneerselvam, KS. Oxidative stress and DNA. Single-strand breaks in skeletal muscle of aged rats: role of carnitine and lipoicacid. Biogerentology 2006; 7:111–18.CrossRefGoogle ScholarPubMed
54Broome, CS, Kayani, AC, Palomero, J et al. Effect of lifelong over-expression of HSP70 in skeletal muscle on age-related oxidative stress and adaptation after non-damaging contractile activity. FASEB J 2006; 20:1549–51.CrossRefGoogle Scholar
55Vasilaki, A, Simpson, D, McArdle, F et al. Formation of 3-nitrotyrosines in carbonic anhydrase III is a sensitive marker of oxidative stress in skeletal muscle. Proteomics–Clin Appl 2007; 1:362–72.CrossRefGoogle ScholarPubMed
56Stadtman, ER. Protein oxidation and aging. Science 1992; 257 (5074):1220–24.CrossRefGoogle ScholarPubMed
57Lee, C-K, Klopp, RG, Weindruch, R, Prolla, TA. Gene expression profile of aging and its retardation by caloric restriction. Science 1999; 285 (5432):1390–93.CrossRefGoogle ScholarPubMed
58Mecocci, P, MacGarvey, U, Kaufman, AE et al. Oxidative damage to mitochondrial DNA shows marked age-dependent increases in human brain. Ann Neurol 1993; 34:609–16.CrossRefGoogle ScholarPubMed
59De Flora, S, Izzotti, A, Randerath, K et al. DNA adducts and chronic degenerative disease. Pathogenetic relevance and implications in preventive medicine. Mutat Res 1996; 366:197–238.CrossRefGoogle ScholarPubMed
60Lezza, AM, Boffoli, D, Scacco, S, Cantatore, P, Gadaleta, MN. Correlation between mitochondrial DNA 4977-bp deletion and respiratory chain enzyme activities in aging human skeletal muscles. Biochem Biophys Res Commun 1994; 205:772–79.CrossRefGoogle ScholarPubMed
61Kirkwood, TBL. Understanding the odd science of aging. Cell 2005; 120: 437–47.CrossRefGoogle ScholarPubMed
62Halliwell, B. Oxidants and human disease: some new concepts. FASEB J 1987; 1:358–64.CrossRefGoogle ScholarPubMed
63Ji, LL, Dillon, D, Wu, E. Alteration of antioxidant enzymes with aging in rat skeletal muscle and liver. Am J Physiol 1990; 258:R918–23.Google ScholarPubMed
64Vasilaki, A, McArdle, F, Iwanejko, LM, McArdle, A. Adaptive responses of mouse skeletal muscle to contractile activity: the effect of age. Mech Ageing Dev 2006; 127:830–39.CrossRefGoogle ScholarPubMed
65McBride, TA, Gorin, FA, Carlsen, RC. Prolonged recovery and reduced adaptation in aged rat muscle following eccentric exercise. Mech Ageing Dev 1995; 83:185–200.CrossRefGoogle ScholarPubMed
66Li, YP, Reid, MB. NF-kB mediates the protein loss induced by TNF-alpha in differentiated skeletal muscle myotubes. Am J Physiol 2000; 279:R1165–R70.Google ScholarPubMed
67Beckman, KB, Ames, BN. The free radical theory of aging matures. Physiol Rev 1998; 78:547–81.CrossRefGoogle ScholarPubMed
68Melov, S, Ravenscroft, J, Malik, S. Extension of lifespan with superoxide ismutase/catalase mimetics. Science 2000; 289 (5484):1567–69.CrossRefGoogle ScholarPubMed
69Keaney, M, Matthijssens, F, Sharpe, M, Vanfleteren, J, Gems, D. Superoxide dismutase mimetics elevate superoxide dismutase activity in vivo but do not retard aging in the nematode. Free Radic Biol Med 2004; 37:239–50.CrossRefGoogle Scholar
70Huang, TT, Carlson, EJ, Raineri, I, Gillespie, AM, Kozy, H, Epstein, CJ. The use of transgenic and mutant mice to study oxygen free radical metabolism. Ann NY Acad Sci 1999; 893:95–112.CrossRefGoogle ScholarPubMed
71Muller, FL, Song, W, Liu, Y et al. Absence of CuZn superoxide dismutase leads to elevated oxidative stress and acceleration of age-dependent skeletal muscle atrophy. Free Radic Biol Med 2006; 40:1993–2004.CrossRefGoogle ScholarPubMed
72Sumien, N, Forster, MJ, Sohal, RS. Supplementation with vitamin E fails to attenuate oxidative damage in aged mice. Exp Gerontol 2003; 38:699–704.CrossRefGoogle ScholarPubMed
73Van Der Meulen, JH, McArdle, A, Jackson, MJ, Faulkner, JA. Contraction-induced injury to the extensor digitorum longus muscles of rats: the role of vitamin E. J Appl Physiol 1997; 83:817–23.CrossRefGoogle Scholar
74Ikemoto, M, Okamura, Y, Kano, M et al. A relative high dose of vitamin E does not attenuate unweighting-induced oxidative stress and ubiquitination in rat skeletal muscle. J Physiol Anthropol Appl Human Sci 2002; 21:257–63.CrossRefGoogle Scholar
75Meydani, M, Lipman, RD, Han, SN et al. The effect of long-term dietary supplementation with antioxidants. Ann NY Acad Sci 1998; 854:352–60.CrossRefGoogle ScholarPubMed
76Finkel, T, Holbrook, NJ. Oxidants, oxidative stress and the biology of ageing. Nature 2000; 408:239–47.CrossRefGoogle ScholarPubMed
77Sohal, RS, Mockett, RJ, Orr, WC. Mechanisms of aging: an appraisal of the oxidative stress hypothesis. Free Radic Biol Med 2002; 33:575–86.CrossRefGoogle ScholarPubMed
78Rafique, R, Schapira, AH, Coper, JM. Mitochondrial respiratory chain dysfunction in ageing; influence of vitamin E deficiency. Free Radic Res 2004; 38:157–65.CrossRefGoogle ScholarPubMed
79Ji, L. Exercise at old age: does it increase or alleviate oxidative stress? Ann NY Acad Sci 2001; 928:236–47.CrossRefGoogle ScholarPubMed
80Paffenbarger, RS, Hyde, RT, Wing, AL, Lee, IM, Jung, DL, Kampert, JB. The association of changes in physical-activity level and other lifestyle characteristics with mortality among men. N Engl J Med 1993; 328:538–45.CrossRefGoogle ScholarPubMed
81Morton, JP, MacLaren, DP, Cable, NT et al. Time-course and differential responses of the major heat-shock protein families in human skeletal muscle following acute non-damaging treadmill exercise. J Appl Physiol 2006; 101:176–82.CrossRefGoogle Scholar
82Close, GL, Ashton, T, McArdle, A, Jackson, MJ. Microdialysis studies of extracellular reactive oxygen species in skeletal muscle: factors influencing the reduction of cytochrome c and hydroxylation of salicylate. Free Radic Biol Med 2005; 39:1460–67.CrossRefGoogle ScholarPubMed
83Vasilaki, A, Csete, M, Pye, D et al. Genetic modification of the manganese superoxide dismutase/glutathione peroxidase 1 pathway influences intracellular ROS generation in quiescent, but not contracting, skeletal muscle cells. Free Radic Biol Med 2006; 41:1719– 25.CrossRefGoogle Scholar