Skeletal muscle aging and the mitochondrion

Trends in Endocrinology and Metabolism

Volumn 24, Issue 5, 2013, Pages 247-256

  Johnson, Matthew L ^a   Robinson, Matthew M ^a   Nair, Sreekumaran K ^a  

^a MAYO CLINIC   (United States)

Author keywords

Aging; Mitochondria; Protein metabolism; Protein synthesis; Sarcopenia

Indexed keywords

MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN;

AGING; BIOGENESIS; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; HUMAN; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

AGING; ANIMALS; HUMANS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DISEASES; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; OXIDATIVE STRESS; PROTEIN STABILITY; SARCOPENIA; SIGNAL TRANSDUCTION;

EID: 84876959937     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2012.12.003     Document Type: Review

References (103)

1. Herndon L.A., et al. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002, 419:808-814.
2. Guarente L., Kenyon C. Genetic pathways that regulate ageing in model organisms. Nature 2000, 408:255-262.
3. Anderson R.M., et al. Caloric restriction and aging: studies in mice and monkeys. Toxicol. Pathol. 2009, 37:47-51.
4. 2max with aging in master athletes and sedentary men. J. Appl. Physiol. 1990, 68:2195-2199.
5. Short K.R., et al. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:5618-5623.
6. Morley J.E., et al. Sarcopenia with limited mobility: an international consensus. J. Am. Med. Dir. Assoc. 2011, 12:403-409.
7. Nair K.S. Aging muscle. Am. J. Clin. Nutr. 2005, 81:953-963.
8. Irving B.A., et al. Age effect on myocellular remodeling: response to exercise and nutrition in humans. Ageing Res. Rev. 2012, 11:374-389.
9. 2max in trained older subjects. J. Appl. Physiol. 1997, 82:1411-1415.
10. Julius S., et al. Influence of age on the hemodynamic response to exercise. Circulation 1967, 36:222-230.
11. Ogawa T., et al. Effects of aging, sex, and physical training on cardiovascular responses to exercise. Circulation 1992, 86:494-503.
12. Rooyackers O.E., et al. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:15364-15369.
13. Tonkonogi M., et al. Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans. Pflugers Arch. 2003, 446:261-269.
14. McCully K.K., et al. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J. Appl. Physiol. 1993, 75:813-819.
15. Barazzoni R., et al. Effects of aging on mitochondrial DNA copy number and cytochrome c oxidase gene expression in rat skeletal muscle, liver, and heart. J. Biol. Chem. 2000, 275:3343-3347.
16. Lanza I.R., et al. Endurance exercise as a countermeasure for aging. Diabetes 2008, 57:2933-2942.
17. Conley K.E., et al. Oxidative capacity and ageing in human muscle. J. Physiol. 2000, 526:203-210.
18. Short K.R., et al. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am. J. Physiol. Endocrinol. Metab. 2004, 286:E92-E101.
19. Petersen K.F. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003, 300:1140-1142.
20. Coggan A.R., et al. Skeletal muscle adaptations to endurance training in 60- to 70-yr-old men and women. J. Appl. Physiol. 1992, 72:1780-1786.
21. Bass A., et al. Biochemical and histochemical changes in energy supply enzyme pattern of muscles of the rat during old age. Gerontologia 1975, 21:31-45.
22. Picard M., et al. Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles. Aging Cell 2011, 10:1047-1055.
23. Houmard J.A., et al. Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J. Appl. Physiol. 1998, 85:1337-1341.
24. Larsen R.G., et al. Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior. Appl. Physiol. Nutr. Metab. 2012, 37:88-99.
25. Balagopal P., et al. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am. J. Physiol. 1997, 273:E790-E800.
26. Troiano R.P., et al. Physical activity in the United States measured by accelerometer. Med. Sci. Sports Exerc. 2008, 40:181-188.
27. Balagopal P., et al. Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise. Am. J. Physiol. Endocrinol. Metab. 2001, 280:E203-E208.
28. Scelsi R., et al. Histochemical and ultrastructural aspects of m. vastus lateralis in sedentary old people (age 65-89 years). Acta Neuropathol. 1980, 51:99-105.
29. Andersen J.L. Muscle fibre type adaptation in the elderly human muscle. Scand. J. Med. Sci. Sports 2003, 13:40-47.
30. Mai S., et al. Autophagy proteins LC3B, ATG5 and ATG12 participate in quality control after mitochondrial damage and influence lifespan. Autophagy 2012, 8:47-62.
31. Baker B.M., et al. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem. Sci. 2011, 36:254-261.
32. Joseph A-M., et al. Plasticity of TOM complex assembly in skeletal muscle mitochondria in response to chronic contractile activity. Mitochondrion 2012, 12:305-312.
33. Bota D.A., et al. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 2002, 4:674-680.
34. Twig G., et al. Fission and selective fusion govern mitochondrial segregation and elimination by autophagy. EMBO J. 2008, 27:433-446.
35. Bota D.A., et al. Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett. 2002, 532:103-106.
36. Kubica N., et al. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bepsilon mRNA in a mammalian target of rapamycin-dependent manner. J. Biol. Chem. 2005, 280:7570-7580.
37. Perry C.G.R., et al. Repeated transient mRNA bursts precede increases in transcriptional and mitochondrial proteins during training in human skeletal muscle. J. Physiol. 2010, 588:4795-4810.
38. Menshikova E.V., et al. Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J. Gerontol. A: Biol. Sci. Med. Sci. 2006, 61:534-540.
39. Slivka D., et al. Single muscle fiber adaptations to resistance training in old (>80 yr) men: evidence for limited skeletal muscle plasticity. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 295:R273-R280.
40. Raue U., et al. Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women. J. Appl. Physiol. 2009, 106:1611-1617.
41. Betik A.C., et al. Exercise training from late middle age until senescence does not attenuate the declines in skeletal muscle aerobic function. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009, 297:R744-R755.
42. Guillet C., et al. Impaired anabolic response of muscle protein synthesis is associated with S6K1 dysregulation in elderly humans. FASEB J. 2004, 18:1586-1587.
43. Miller B.F., et al. A comprehensive assessment of mitochondrial protein synthesis and cellular proliferation with age and caloric restriction. Aging Cell 2012, 11:150-161.
44. Henderson G.C., et al. Effects of adiposity and 30 days of caloric restriction upon protein metabolism in moderately vs. severely obese women. Obesity 2009, 18:1135-1142.
45. Glynn E.L., et al. Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 299:R533-R540.
46. Zhang X-J., et al. Measurement of muscle protein fractional synthesis and breakdown rates from a pulse tracer injection. Am. J. Physiol. Endocrinol. Metab. 2002, 283:E753-E764.
47. Demontis F., et al. FOXO/4E-BP signaling in Drosophila muscles regulates organism-wide proteostasis during aging. Cell 2010, 143:813-825.
48. Zhang C., Cuervo A.M. Restoration of chaperone-mediated autophagy in aging liver improves cellular maintenance and hepatic function. Nat. Med. 2008, 14:959-965.
49. Wohlgemuth S.E., et al. Skeletal muscle autophagy and apoptosis during aging: effects of calorie restriction and life-long exercise. Exp. Gerontol. 2010, 45:138-148.
50. Ferrington D.A., et al. Altered proteasome structure, function, and oxidation in aged muscle. FASEB J. 2005, 19:644-646.
51. Cuervo A.M., Dice J.F. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 2000, 275:31505-31513.
52. Wohlgemuth S.E., et al. An exploratory analysis of the effects of a weight loss plus exercise program on cellular quality control mechanisms in older overweight women. Rejuvenation Res. 2011, 14:315-324.
53. Handschin C., et al. Abnormal glucose homeostasis in skeletal muscle-specific PGC-1alpha knockout mice reveals skeletal muscle-pancreatic beta cell crosstalk. J. Clin. Invest. 2007, 117:3463-3474.
54. Leick L., et al. PGC-1alpha is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 2008, 294:E463-E474.
55. Wenz T., et al. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:20405-20410.
56. Brault J.J., et al. Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J. Biol. Chem. 2010, 285:19460-19471.
57. Wu J., et al. The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1α/ATF6α complex. Cell Metab. 2011, 13:160-169.
58. Ghosh S., et al. Reduction in reactive oxygen species production by mitochondria from elderly subjects with normal and impaired glucose tolerance. Diabetes 2011, 60:2051-2060.
59. Chabi B., et al. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 2008, 7:2-12.
60. Koltai E., et al. Age-associated declines in mitochondrial biogenesis and protein quality control factors are minimized by exercise training. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2012, 303:R127-R134.
61. + intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 2011, 14:528-536.
62. Herranz D., et al. Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nat. Commun. 2010, 1:3.
63. Park S-J., et al. Resveratrol ameliorates aging-related metabolic phenotypes by inhibiting cAMP phosphodiesterases. Cell 2012, 148:421-433.
64. Aquilano K., et al. Peroxisome proliferator-activated receptor gamma co-activator 1alpha (PGC-1alpha) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J. Biol. Chem. 2010, 285:21590-21599.
65. Cantó C., et al. Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metab. 2010, 11:213-219.
66. Hirschey M.D., et al. SIRT3 deficiency and mitochondrial protein hyperacetylation accelerate the development of the metabolic syndrome. Mol. Cell 2011, 44:177-190.
67. Jing E., et al. Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:14608-14613.
68. Lee H-Y., et al. Targeted expression of catalase to mitochondria prevents age-associated reductions in mitochondrial function and insulin resistance. Cell Metab. 2010, 12:668-674.
69. Reznick R.M., et al. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab. 2007, 5:151-156.
70. Lantier L., et al. Coordinated maintenance of muscle cell size control by AMP-activated protein kinase. FASEB J. 2010, 24:3555-3561.
71. Winder W.W., et al. Activation of AMP-activated protein kinase increases mitochondrial enzymes in skeletal muscle. J. Appl. Physiol. 2000, 88:2219-2226.
72. Picard M., et al. Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers. Aging Cell 2010, 9:1032-1046.
73. Chomentowski P., et al. Skeletal muscle mitochondria in insulin resistance: differences in intermyofibrillar versus subsarcolemmal subpopulations and relationship to metabolic flexibility. J. Clin. Endocrinol. Metab. 2011, 96:494-503.
74. Lanza I.R., Nair K.S. Functional assessment of isolated mitochondria in vitro. Methods Enzymol. 2009, 457:349-372.
75. Capel F., et al. Due to reverse electron transfer, mitochondrial H2O2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mech. Ageing Dev. 2005, 126:505-511.
76. Fanó G., et al. Age and sex influence on oxidative damage and functional status in human skeletal muscle. J. Muscle Res. Cell. Motil. 2001, 22:345-351.
77. Aiken J., et al. Mitochondrial DNA deletion mutations and sarcopenia. Ann. N. Y. Acad. Sci. 2002, 959:412-423.
78. Bua E.A., et al. Mitochondrial abnormalities are more frequent in muscles undergoing sarcopenia. J. Appl. Physiol. 2002, 92:2617-2624.
79. Bua E., et al. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am. J. Hum. Genet. 2006, 79:469-480.
80. Wanagat J., et al. Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J. 2001, 15:322-332.
81. Gianni P., et al. Oxidative stress and the mitochondrial theory of aging in human skeletal muscle. Exp. Gerontol. 2004, 39:1391-1400.
82. Edris W., et al. Detection and quantitation by competitive PCR of an age-associated increase in a 4.8-kb deletion in rat mitochondrial DNA. Mutat. Res. 1994, 316:69-78.
83. Simonetti S., et al. Accumulation of deletions in human mitochondrial DNA during normal aging: analysis by quantitative PCR. Biochim. Biophys. Acta 1992, 1180:113-122.
84. Schwarze S.R., et al. High levels of mitochondrial DNA deletions in skeletal muscle of old rhesus monkeys. Mech. Ageing Dev. 1995, 83:91-101.
85. Safdar A., et al. Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLoS ONE 2010, 5:e10778.
86. Souza J.M., et al. Protein tyrosine nitration - functional alteration or just a biomarker?. Free Radic. Biol. Med. 2008, 45:357-366.
87. Safdar A., et al. Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:4135-4140.
88. Trounce I., et al. Decline in skeletal muscle mitochondrial respiratory chain function: possible factor in ageing. Lancet 1989, 1:637-639.
89. Boffoli D., et al. Decline with age of the respiratory chain activity in human skeletal muscle. Biochim. Biophys. Acta 1994, 1226:73-82.
90. Proctor D.N., et al. Oxidative capacity of human muscle fiber types: effects of age and training status. J. Appl. Physiol. 1995, 78:2033-2038.
91. Barrientos A., et al. Absence of relationship between the level of electron transport chain activities and aging in human skeletal muscle. Biochem. Biophys. Res. Commun. 1996, 229:536-539.
92. Brierley E.J., et al. Effects of physical activity and age on mitochondrial function. QJM 1996, 89:251-258.
93. Rasmussen U.F., et al. Experimental evidence against the mitochondrial theory of aging. A study of isolated human skeletal muscle mitochondria. Exp. Gerontol. 2003, 38:877-886.
94. Hütter E., et al. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 2007, 6:245-256.
95. Chretien D., et al. Biochemical parameters for the diagnosis of mitochondrial respiratory chain deficiency in humans, and their lack of age-related changes. Biochem. J. 1998, 329:249-254.
96. Kent-Braun J.A., Ng A.V. Skeletal muscle oxidative capacity in young and older women and men. J. Appl. Physiol. 2000, 89:1072-1078.
97. Lanza I.R. Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J. Appl. Physiol. 2005, 99:1736-1744.
98. Lanza I.R., et al. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J. Physiol. 2007, 583:1093-1105.
99. Amara C.E., et al. Mild mitochondrial uncoupling impacts cellular aging in human muscles in vivo. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:1057-1062.
100. Ross-Inta C., et al. The mitochondrial pool of free amino acids reflects the composition of mitochondrial DNA-encoded proteins: indication of a post- translational quality control for protein synthesis. Biosci. Rep. 2008, 28:239-249.
101. Liu X., et al. Mitochondrial 'kiss-and-run': interplay between mitochondrial motility and fusion-fission dynamics. EMBO J. 2009, 28:3074-3089.
102. Scheckhuber C.Q., et al. Unopposed mitochondrial fission leads to severe lifespan shortening. Cell Cycle 2011, 10:3105-3110.
103. Romanello V., et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J. 2010, 29:1774-1785.