Mitochondria, muscle health, and exercise with advancing age

Physiology

Volumn 30, Issue 3, 2015, Pages 208-223

  Carter, Heather N ^a   Chen, Chris C W ^a   Hood, David A ^a  

^a YORK UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MITOCHONDRIAL DNA;

AGE; AGING; ANIMAL; EXERCISE; GENETIC PREDISPOSITION; GENETICS; HUMAN; METABOLISM; MUSCLE CONTRACTION; MUSCLE MITOCHONDRION; MUTATION; PATHOLOGY; PATHOPHYSIOLOGY; RISK FACTOR; SARCOPENIA; SKELETAL MUSCLE;

AGE FACTORS; AGING; ANIMALS; DNA, MITOCHONDRIAL; EXERCISE; GENETIC PREDISPOSITION TO DISEASE; HUMANS; MITOCHONDRIA, MUSCLE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; MUTATION; RISK FACTORS; SARCOPENIA;

EID: 84929580195     PISSN: 15489213     EISSN: 15489221     Source Type: Journal    
DOI: 10.1152/physiol.00039.2014     Document Type: Review

References (179)

1. Adhihetty PJ, Ljubicic V, Hood DA. Effect of chronic contractile activity on SS and IMF mitochondrial apoptotic susceptibility in skeletal muscle. Am J Physiol Endocrinol Metab 292: E748-E755, 2007
2. Adhihetty PJ, Uguccioni G, Leick L, Hidalgo J, Pilegaard H, Hood DA. The role of PGC-1alpha on mitochondrial function and apoptotic susceptibility in muscle. Am J Physiol Cell Physiol 297: C217-C225, 2009
3. Altun M, Edström E, Spooner E, Flores-Moralez A, Bergman E, Tollet-Egnell P, Norstedt G, Kessler BM, Ulfhake B. Iron load and redox stress in skeletal muscle of aged rats. Muscle Nerve 36: 223-233, 2007
4. Alway SE, Siu PM. Nuclear apoptosis contributes to sarcopenia. Exerc Sport Sci Rev 36: 51-57, 2008
5. Andersen JL, Terzis G, Kryger A. Increase in the degree of coexpression of myosin heavy chain isoforms in skeletal muscle fibers of the very old. Muscle Nerve 22: 449-454, 1999
6. Baar K. Epigenetic control of skeletal muscle fiber type. Acta Physiol (Oxf) 199: 477-487, 2010
7. Ballak SB, Degens H, de Haan A, Jaspers RT. Aging related changes in determinants of muscle force generating capacity: A comparison of muscle aging in men and male rodents. Ageing Res Rev 14: 43-55, 2014
8. Baraibar MA, Gueugneau M, Duguez S, Butler-Browne G, Bechet D, Friguet B. Expression and modification proteomics during skeletal muscle ageing. Biogerontology 14: 339-352, 2013
9. Barrès R, Yan J, Egan B, Treebak JT, Rasmussen M, Fritz T, Caidahl K, Krook A, O’Gorman DJ, Zierath JR. Acute exercise remodels promoter methylation in human skeletal muscle. Cell Metab 15: 405-411, 2012
10. Beregi E, Regius O, Hüttl T, Göbl Z. Age-related changes in the skeletal muscle cells. Z Gerontol 21: 83-86, 1988
11. Boffoli D, Scacco SC, Vergari R, Solarino G, Santacroce G, Papa S. Decline with age of the respiratory chain activity in human skeletal muscle. Biochim Biophys Acta 1226: 73-82, 1994
12. Booth FW, Weeden SH, Tseng BS. Effect of aging on human skeletal muscle and motor function. Med Sci Sports Exerc 26: 556-560, 1994
13. Brierley EJ, Johnson MA, James OF, Turnbull DM. Effects of physical activity and age on mitochondrial function. QJM 89: 251-258, 1996
14. Broskey NT, Greggio C, Boss A, Boutant M, Dwyer A, Schlueter L, Hans D, Gremion G, Kreis R, Boesch C, Canto C, Amati F. Skeletal muscle mitochondria in the elderly: Effects of physical fitness and exercise training. J Clin Endocrinol Metab 99: 1852-1861, 2014
15. Bua E, Johnson J, Herbst A, Delong B, McKenzie D, Salamat S, Aiken JM. Mitochondrial DNA-deletion mutations accumulate intracellularly to detrimental levels in aged human skeletal muscle fibers. Am J Hum Genet 79: 469-480, 2006
16. Bua EA, McKiernan SH, Wanagat J, McKenzie D, Aiken JM. Mitochondrial abnormalities are more frequent in muscles undergoing sarcopenia. J Appl Physiol 92: 2617-2624, 2002
17. Capitanio D, Vasso M, Fania C, Moriggi M, Viganò A, Procacci P, Magnaghi V, Gelfi C. Comparative proteomic profile of rat sciatic nerve and gastrocnemius muscle tissues in ageing by 2-D DIGE. Proteomics 9: 2004-2020, 2009
18. Cartee GD, Farrar RP. Muscle respiratory capacity and VO2max in identically trained young and old rats. J Appl Physiol 63: 257-261, 1987
19. Carter HN, Hood DA. Contractile activity-induced mitochondrial biogenesis and mTORC1. Am J Physiol Cell Physiol 303: C540-C547, 2012
20. Centers for Disease Control and Prevention. The State of Aging and Health in America 2013. Atlanta, GA: Centers for Disease Control and Prevention, 2013
21. Chabi B, Ljubicic V, Menzies KJ, Huang JH, Saleem A, Hood DA. Mitochondrial function and apoptotic susceptibility in aging skeletal muscle. Aging Cell 7: 2-12, 2008
22. Chang J, Cornell JE, Van Remmen H, Hakala K, Ward WF, Richardson A. Effect of aging and caloric restriction on the mitochondrial proteome. J Gerontol A Biol Sci Med Sci 62: 223-234, 2007
23. Chaves DFS, Carvalho PC, Lima DB, Nicastro H, Lorenzeti FM, Siqueira-Filho M, Hirabara SM, Alves PHM, Moresco JJ, Yates JR, Lancha AH. Comparative proteomic analysis of the aging soleus and extensor digitorum longus rat muscles using TMT labeling and mass spectrometry. J Proteome Res 12: 4532-4546, 2013
24. Chekanov VS, Karakozov P, Rieder M, Zander G. Age related skeletal muscle response to electrical stimulation. ASAIO J 46: 474-481, 2000
25. Coggan AR, Spina RJ, Rogers MA, King DS, Brown M, Nemeth PM, Holloszy JO. Histochemical and enzymatic characteristics of skeletal muscle in master athletes. J Appl Physiol 68: 1896-1901, 1990
26. Cogswell AM, Stevens RJ, Hood DA. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions. Am J Physiol Cell Physiol 264: C383-C389, 1993
27. Conley KE, Amara CE, Jubrias SA, Marcinek DJ. Mitochondrial function, fiber types and ageing: New insights from human muscle in vivo. Exp Physiol 92: 333-339, 2007
28. Conley KE, Jubrias SA, Cress ME, Esselman PC. Elevated energy coupling and aerobic capacity improves exercise performance in endurance-trained elderly subjects. Exp Physiol 98: 899-907, 2013
29. Conley KE, Jubrias SA, Esselman PC. Oxidative capacity and ageing in human muscle. J Physiol 526: 203-210, 2000
30. Conley KE, Marcinek DJ, Villarin J. Mitochondrial dysfunction and age. Curr Opin Clin Nutr Metab Care 10: 688-692, 2007
31. Cortopassi GA, Arnheim N. Detection of a specific mitochondrial DNA deletion in tissues of older humans. Nucleic Acids Res 18: 6927-6933, 1990
32. Cortopassi GA, Shibata D, Soong NW, Arnheim N. A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc Natl Acad Sci USA 89: 7370-7374, 1992
33. Craig EE, Hood DA. Influence of aging on protein import into cardiac mitochondria. Am J Physiol Heart Circ Physiol 272: H2983-H2988, 1997
34. Deschenes MR. Effects of aging on muscle fiber type and size. Sports Med 34: 809-824, 2004
35. Dirks AJ, Hofer T, Marzetti E, Pahor M, Leeuwenburgh C. Mitochondrial DNA mutations, energy metabolism and apoptosis in aging muscle. Ageing Res Rev 5: 179-195, 2006
36. Dirks AJ, Leeuwenburgh C. The role of apoptosis in age-related skeletal muscle atrophy. Sports Med 35: 473-483, 2005
37. Doherty TJ. Invited review: Aging and sarcopenia. J Appl Physiol 95: 1717-1727, 2003
38. Drummond MJ, Addison O, Brunker L, Hopkins PN, McClain DA, LaStayo PC, Marcus RL. Downregulation of e3 ubiquitin ligases and mitophagyrelated genes in skeletal muscle of physically inactive, frail older women: a cross-sectional comparison. J Gerontol A Biol Sci Med Sci 69: 1040-1048, 2014
39. Falkenberg M, Larsson NG, Gustafsson CM. DNA replication and transcription in mammalian mitochondria. Annu Rev Biochem 76: 679-699, 2007
40. Farrar RP, Martin TP, Ardies CM. The interaction of aging and endurance exercise upon the mitochondrial function of skeletal muscle. J Gerontol 36: 642-647, 1981
41. Fry CS, Drummond MJ, Glynn EL, Dickinson JM, Gundermann DM, Timmerman KL, Walker DK, Dhanani S, Volpi E, Rasmussen BB. Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis. Skelet Muscle 1: 11, 2011
42. Funai K, Parkington JD, Carambula S, Fielding RA. Age-associated decrease in contraction-induced activation of downstream targets of Akt/mTor signaling in skeletal muscle. Am J Physiol Regul Integr Comp Physiol 290: R1080-R1086, 2006
43. Gaugler M, Brown A, Merrell E, DiSanto-Rose M, Rathmacher JA, Reynolds TH. PKB signaling and atrogene expression in skeletal muscle of aged mice. J Appl Physiol 111: 192-199, 2011
44. Gelfi C, Vigano A, Ripamonti M, Pontoglio A, Begum S, Pellegrino MA, Grassi B, Bottinelli R, Wait R, Cerretelli P. The human muscle proteome in aging. J Proteome Res 5: 1344-1353, 2006
45. Ghosh S, Lertwattanarak R, Lefort N, Molina-Carrion M, Joya-Galeana J, Bowen BP, Garduno-Garcia de J J, Abdul-Ghani M, Richardson A, DeFronzo RA, Mandarino L, Van Remmen H, Musi N. Reduction in reactive oxygen species production by mitochondria from elderly subjects with normal and impaired glucose tolerance. Diabetes 60: 2051-2060, 2011
46. Goodpaster BH, Park SW, Harris TB, Kritchevsky SB, Nevitt M, Schwartz AV, Simonsick EM, Tylavsky FA, Visser M, Newman AB. The loss of skeletal muscle strength, mass, and quality in older adults: The health, aging and body composition study. J Gerontol A Biol Sci Med Sci 61: 1059-1064, 2006
47. Gouspillou G, Sgarioto N, Kapchinsky S, Purves-Smith F, Norris B, Pion CH, Barbat-Artigas S, Lemieux F, Taivassalo T, Morais JA, Aubertin-Leheudre M, Hepple RT. Increased sensitivity to mitochondrial permeability transition and myonuclear translocation of endonuclease G in atrophied muscle of physically active older humans. FASEB J 28: 1621-1633, 2014
48. Grumati P, Coletto L, Sabatelli P, Cescon M, Angelin A, Bertaggia E, Blaauw B, Urciuolo A, Tiepolo T, Merlini L, Maraldi NM, Bernardi P, Sandri M, Bonaldo P. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med 16: 1313-1320, 2010
49. Grumati P, Coletto L, Schiavinato A, Castagnaro S, Bertaggia E, Sandri M, Bonaldo P. Physical exercise stimulates autophagy in normal skeletal muscles but is detrimental for collagen VI-deficient muscles. Autophagy 7: 1415-1423, 2011
50. Hämäläinen N, Pette D. Patterns of myosin isoforms in mammalian skeletal muscle fibers. Microsc Res Tech 30: 381-389, 1995
51. Handschin C, Spiegelman BM. Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735, 2006
52. Hardman SE, Hall DE, Cabrera AJ, Hancock CR, Thomson DM. The effects of age and muscle contraction on AMPK activity and heterotrimer composition. Exp Gerontol 55: 120-128, 2014
53. He C, Bassik MC, Moresi V, Sun K, Wei Y, Zou Z, An Z, Loh J, Fisher J, Sun Q, Korsmeyer S, Packer M, May HI, Hill JA, Virgin HW, Gilpin C, Xiao G, Bassel-Duby R, Scherer PE, Levine B. Exerciseinduced BCL2-regulated autophagy is required for muscle glucose homeostasis. Nature 481: 511-515, 2012
54. Hebert SL, Lanza IR, Nair KS. Mitochondrial DNA alterations and reduced mitochondrial function in aging. Mech Ageing Dev 131: 451-462, 2010
55. Herbst A, Johnson CJ, Hynes K, McKenzie D, Aiken JM. Mitochondrial biogenesis drives a vicious cycle of metabolic insufficiency and mitochondrial DNA deletion mutation accumulation in aged rat skeletal muscle fibers. PLos One 8: e59006, 2013
56. Herbst A, Pak JW, McKenzie D, Bua E, Bassiouni M, Aiken JM. Accumulation of mitochondrial DNA deletion mutations in aged muscle fibers: evidence for a causal role in muscle fiber loss. J Gerontol A Biol Sci Med Sci 62: 235-245, 2007
57. Holloszy JO. Exercise, health, and aging: A need for more information. Med Sci Sports Exerc 15: 1-5, 1983
58. Hood DA, Iqbal S. Muscle mitochondrial ultrastructure: new insights into morphological divergences. J Appl Physiol 114: 159-160, 2013
59. Hood DA, Joseph AM. Mitochondrial assembly: Protein import. Proc Nutr Soc 63: 293-300, 2004
60. Hood DA. Invited Review: Contractile activityinduced mitochondrial biogenesis in skeletal muscle. J Appl Physiol 90: 1137-1157, 2001
61. Huang G, Gibson CA, Tran ZV, Osness WH. Controlled endurance exercise training and VO2max changes in older adults: A meta-analysis. Prev Cardiol 8: 217-225, 2005
62. Huang JH, Joseph AM, Ljubicic V, Iqbal S, Hood DA. Effect of age on the processing and import of matrix-destined mitochondrial proteins in skeletal muscle. J Gerontol A Biol Sci Med Sci 65: 138-46, 2010
63. Hughes VA, Frontera WR, Wood M, Evans WJ, Dallal GE, Roubenoff R, Fiatarone Singh MA. Longitudinal muscle strength changes in older adults: Influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci 56: 209-217, 2001
64. Hütter E, Skovbro M, Lener B, Prats C, Rabøl R, Dela F, Jansen-Dürr P. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 6: 245-256, 2007
65. Hwang CY, Kim K, Choi JY, Bahn YJ, Lee SM, Kim YK, Lee C, Kwon KS. Quantitative proteome analysis of age-related changes in mouse gastrocnemius muscle using mTRAQ. Proteomics 14: 121-132, 2014
66. Ibebunjo C, Chick JM, Kendall T, Eash JK, Li C, Zhang Y, Vickers C, Wu Z, Clarke BA, Shi J, Cruz J, Fournier B, Brachat S, Gutzwiller S, Ma Q, Markovits J, Broome M, Steinkrauss M, Skuba E, Galarneau JR, Gygi SP, Glass DJ. Genomic and proteomic profiling reveals reduced mitochondrial function and disruption of the neuromuscular junction driving rat sarcopenia. Mol Cell Biol 33: 194-212, 2013
67. Iosa M, Fusco A, Morone G, Paolucci S. Development and decline of upright gait stability. Front Aging Neurosci 6: 14, 2014
68. Iqbal S, Ostojic O, Singh K, Joseph AM, Hood DA. Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse. Muscle Nerve 48: 963-970, 2013
69. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 89: 81-88, 2000
70. Jeppesen TD, Dunø M, Schwartz M, Krag T, Rafiq J, Wibrand F, Vissing J. Short-and long-term effects of endurance training in patients with mitochondrial myopathy. Eur J Neurol 16: 1336-1339, 2009
71. Johannsen DL, Conley KE, Bajpeyi S, Punyanitya M, Gallagher D, Zhang Z, Covington J, Smith SR, Ravussin E. Ectopic lipid accumulation and reduced glucose tolerance in elderly adults are accompanied by altered skeletal muscle mitochondrial activity. J Clin Endocrinol Metab 97: 242-250, 2012
72. Johnson ML, Robinson MM, Nair KS. Skeletal muscle aging and the mitochondrion. Trends Endocrinol Metab 24: 247-256, 2013
73. Joseph AM, Adhihetty PJ, Buford TW, Wohlgemuth SE, Lees HA, Nguyen LMD, Aranda JM, Sandesara BD, Pahor M, Manini TM, Marzetti E, Leeuwenburgh C. The impact of aging on mitochondrial function and biogenesis pathways in skeletal muscle of sedentary high-and low-functioning elderly individuals. Aging Cell 11: 801-809, 2012
74. Joseph AM, Adhihetty PJ, Wawrzyniak NR, Wohlgemuth SE, Picca A, Kujoth GC, Prolla TA, Leeuwenburgh C. Dysregulation of mitochondrial quality control processes contribute to sarcopenia in a mouse model of premature aging. PLos One 8: e69327, 2013
75. Joseph AM, Ljubicic V, Adhihetty PJ, Hood DA. Biogenesis of the mitochondrial Tom40 channel in skeletal muscle from aged animals and its adaptability to chronic contractile activity. Am J Physiol Cell Physiol 298: C1308-C1314, 2010
76. Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE. Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol 90: 1663-1670, 2001
77. Kadenbach B, Münscher C, Frank V, Müller-Höcker J, Napiwotzki J. Human aging is associated with stochastic somatic mutations of mitochondrial DNA. Mutat Res 338: 161-172, 1995
78. Kang C, Chung E, Diffee G, Ji LL. Exercise training attenuates aging-associated mitochondrial dysfunction in rat skeletal muscle: Role of PGC-1. Exp Gerontol 48: 1343-1350, 2013
79. Kayo T, Allison DB, Weindruch R, Prolla TA. Influences of aging and caloric restriction on the transcriptional profile of skeletal muscle from rhesus monkeys. Proc Natl Acad Sci USA 98: 5093-5098, 2001
80. Kent-Braun JA, Ng AV. Skeletal muscle oxidative capacity in young and older women and men. J Appl Physiol 89: 1072-1078, 2000
81. Kirkwood SP, Munn EA, Brooks GA. Mitochondrial reticulum in limb skeletal muscle. Am J Physiol Cell Physiol 251: C395-C402, 1986
82. Koltai E, Hart N, Taylor AW, Goto S, Ngo JK, Davies KJA, Radak Z. Age-associated declines in mitochondrial biogenesis and protein quality control factors are minimized by exercise training. Am J Physiol Regul Integr Comp Physiol 303: R127-R134, 2012
83. Konopka AR, Douglass MD, Kaminsky LA, Jemiolo B, Trappe TA, Trappe S, Harber MP. Molecular adaptations to aerobic exercise training in skeletal muscle of older women. J Gerontol A Biol Sci Med Sci 65: 1201-1207, 2010
84. Kowald A, Kirkwood TB. Transcription could be the key to the selection advantage of mitochondrial deletion mutants in aging. Proc Natl Acad Sci USA 111: 2972-2977, 2014
85. Kujoth GC, Hiona A, Pugh TD, Someya S, Panzer K, Wohlgemuth SE, Hofer T, Seo AY, Sullivan R, Jobling WA, Morrow JD, Van Remmen H, Sedivy JM, Yamasoba T, Tanokura M, Weindruch R, Leeuwenburgh C, Prolla TA. Mitochondrial DNA mutations, oxidative stress, and apoptosis in mammalian aging. Science 309: 481-484, 2005
86. Kumar V, Selby A, Rankin D, Patel R, Atherton P, Hildebrandt W, Williams J, Smith K, Seynnes O, Hiscock N, Rennie MJ. Age-related differences in the dose-response relationship of muscle protein synthesis to resistance exercise in young and old men. J Physiol 587: 211-217, 2009
87. Lambert CP, Evans WJ. Adaptations to aerobic and resistance exercise in the elderly. Rev Endocr Metab Disord 6: 137-143, 2005
88. Lambertucci RH, Levada-Pires AC, Rossoni LV, Curi R, Pithon-Curi TC. Effects of aerobic exercise training on antioxidant enzyme activities and mRNA levels in soleus muscle from young and aged rats. Mech Ageing Dev 128: 267-275, 2007
89. Larsen RG, Callahan DM, Foulis SA, Kent-Braun JA. Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior. Appl Physiol Nutr Metab 37: 88-99, 2012
90. Lee CM, Lopez ME, Weindruch R, Aiken JM. Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy. Free Radic Biol Med 25: 964-972, 1998
91. Leick L, Lyngby SS, Wojtaszewski JFP, Wojtasewski JFP, Pilegaard H. PGC-1alpha is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp Gerontol 45: 336-342, 2010
92. Lexell J, Taylor CC, Sjöström 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-yearold men. J Neurol Sci 84: 275-294, 1988
93. Lexell J, Taylor CC. Variability in muscle fiber areas in whole human quadriceps muscle: effects of increasing age. J Anat 174: 239-249, 1991
94. Lezza AM, Pesce V, Cormio A, Fracasso F, Vecchiet J, Felzani G, Cantatore P, Gadaleta MN. Increased expression of mitochondrial transcription factor A and nuclear respiratory factor-1 in skeletal muscle from aged human subjects. FEBS Lett 501: 74-78, 2001
95. Linnane AW, Baumer A, Maxwell RJ, Preston H, Zhang CF, Marzuki S. Mitochondrial gene mutation: the ageing process and degenerative diseases. Biochem Int 22: 1067-1076, 1990
96. Lira VA, Okutsu M, Zhang M, Greene NP, Laker RC, Breen DS, Hoehn KL, Yan Z. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J 27: 4184-4193, 2013
97. Liu D, Sartor MA, Nader GA, Pistilli EE, Tanton L, Lilly C, Gutmann L, IglayReger HB, Visich PS, Hoffman EP, Gordon PM. Microarray analysis reveals novel features of the muscle aging process in men and women. J Gerontol A Biol Sci Med Sci 68: 1035-1044, 2013
98. Ljubicic V, Adhihetty PJ, Hood DA. Application of animal models: chronic electrical stimulation-induced contractile activity. Can J Appl Physiol 30: 625-643, 2005
99. Ljubicic V, Hood DA. Kinase-specific responsiveness to incremental contractile activity in skeletal muscle with low and high mitochondrial content. Am J Physiol Endocrinol Metab 295: E195-E204, 2008
100. Ljubicic V, Hood DA. Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle. Aging Cell 8: 394-404, 2009
101. Ljubicic V, Hood DA. Specific attenuation of protein kinase phosphorylation in muscle with a high mitochondrial content. Am J Physiol Endocrinol Metab 297: E749-E758, 2009
102. Ljubicic V, Joseph AM, Adhihetty PJ, Huang JH, Saleem A, Uguccioni G, Hood DA. Molecular basis for an attenuated mitochondrial adaptive plasticity in aged skeletal muscle. Aging (Milano) 1: 818-830, 2009
103. Lombardi A, Silvestri E, Cioffi F, Senese R, Lanni A, Goglia F, de Lange P, Moreno M. Defining the transcriptomic and proteomic profiles of rat ageing skeletal muscle by the use of a cDNA array, 2D-and Blue native-PAGE approach. J Proteomics 72: 708-721, 2009
104. Lopez ME, Van Zeeland NL, Dahl DB, Weindruch R, Aiken JM. Cellular phenotypes of age-associated skeletal muscle mitochondrial abnormalities in rhesus monkeys. Mutat Res 452: 123-138, 2000
105. López-Otín C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 153: 1194-1217, 2013
106. Lowell BB, Spiegelman BM. Towards a molecular understanding of adaptive thermogenesis. Nature 404: 652-660, 2000
107. Marcinek DJ, Schenkman KA, Ciesielski WA, Lee D, Conley KE. Reduced mitochondrial coupling in vivo alters cellular energetics in aged mouse skeletal muscle. J Physiol 569: 467-473, 2005
108. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. Autophagy is required to maintain muscle mass. Cell Metab 10: 507-515, 2009
109. Masuyama M, Iida R, Takatsuka H, Yasuda T, Matsuki T. Quantitative change in mitochondrial DNA content in various mouse tissues during aging. Biochim Biophys Acta 1723: 302-308, 2005
110. Melov S, Shoffner JM, Kaufman A, Wallace DC. Marked increase in the number and variety of mitochondrial DNA rearrangements in aging human skeletal muscle. Nucleic Acids Res 23: 4122-4126, 1995
111. Melov S, Tarnopolsky MA, Beckman K, Felkey K, Hubbard A. Resistance exercise reverses aging in human skeletal muscle. PLos One 2: e465, 2007
112. Menzies KJ, Singh K, Saleem A, Hood DA. Sirtuin 1-mediated effects of exercise and resveratrol on mitochondrial biogenesis. J Biol Chem 288: 6968-6979, 2013
113. Murias JM, Kowalchuk JM, Paterson DH. Mechanisms for increases in VO2max with endurance training in older and young women. Med Sci Sports Exerc 42: 1891-1898, 2010
114. Murias JM, Kowalchuk JM, Ritchie D, Hepple RT, Doherty TJ, Paterson DH. Adaptations in capillarization and citrate synthase activity in response to endurance training in older and young men. J Gerontol A Biol Sci Med Sci 66: 957-964, 2011
115. Murphy JL, Blakely EL, Schaefer AM, He L, Wyrick P, Haller RG, Taylor RW, Turnbull DM, Taivassalo T. Resistance training in patients with single, large-scale deletions of mitochondrial DNA. Brain 131: 2832-2840, 2008
116. Navratil M, Terman A, Arriaga EA. Giant mitochondria do not fuse and exchange their contents with normal mitochondria. Exp Cell Res 314: 164-172, 2008
117. Nilwik R, Snijders T, Leenders M, Groen BBL, van Kranenburg J, Verdijk LB, van Loon LJC. The decline in skeletal muscle mass with aging is mainly attributed to a reduction in type II muscle fiber size. Exp Gerontol 48: 492-498, 2013
118. O’Connell K, Ohlendieck K. Proteomic DIGE analysis of the mitochondria-enriched fraction from aged rat skeletal muscle. Proteomics 9: 5509-5524, 2009
119. O’Leary MF, Vainshtein A, Iqbal S, Ostojic O, Hood DA. Adaptive plasticity of autophagic proteins to denervation in aging skeletal muscle. Am J Physiol Cell Physiol 304: C422-C430, 2013
120. Ogata T, Yamasaki Y. High-resolution scanning electron-microscopic studies on the three-dimensional structure of mitochondria and sarcoplasmic reticulum in the different twitch muscle fibers of the frog. Cell Tissue Res 250: 489-497, 1987
121. Ogura Y, Naito H, Kakigi R, Ichinoseki-Sekine N, Kurosaka M, Yoshihara T, Akema T. Effects of ageing and endurance exercise training on alphaactinin isoforms in rat plantaris muscle. Acta Physiol (Oxf) 202: 683-690, 2011
122. Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong SE, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thorburn DR, Carr SA, Mootha VK. A mitochondrial protein compendium elucidates complex I disease biology. Cell 134: 112-123, 2008
123. Pattison JS, Folk LC, Madsen RW, Childs TE, Booth FW. Transcriptional profiling identifies extensive downregulation of extracellular matrix gene expression in sarcopenic rat soleus muscle. Physiol Genomics 15: 34-43, 2003
124. Pesce V, Cormio A, Fracasso F, Lezza AMS, Cantatore P, Gadaleta MN. Age-related changes of mitochondrial DNA content and mitochondrial genotypic and phenotypic alterations in rat hindlimb skeletal muscles. J Gerontol A Biol Sci Med Sci 60: 715-723, 2005
125. Pette D, Skorjanc D. Adaptive potentials of skeletal muscle in young and aging rats. Int J Sport Nutr Exerc Metab 11, Suppl: S3-S8, 2001
126. Phillips BE, Williams JP, Gustafsson T, Bouchard C, Rankinen T, Knudsen S, Smith K, Timmons JA, Atherton PJ. Molecular networks of human muscle adaptation to exercise and age. PLoS Genet 9: e1003389, 2013
127. Picard M, Ritchie D, Thomas MM, Wright KJ, Hepple RT. Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles. Aging Cell 10: 1047-1055, 2011
128. Picard M, Shirihai OS, Gentil BJ, Burelle Y. Mitochondrial morphology transitions and functions: implications for retrograde signaling? Am J Physiol Regul Integr Comp Physiol 304: R393-R406, 2013
129. Picard M, White K, Turnbull DM. Mitochondrial morphology, topology, and membrane interactions in skeletal muscle: A quantitative three-dimensional electron microscopy study. J Appl Physiol 114: 161-171, 2013
130. Piec I, Listrat A, Alliot J, Chambon C, Taylor RG, Bechet D. Differential proteome analysis of aging in rat skeletal muscle. FASEB J 19: 1143-1145, 2005
131. Purves-Smith FM, Sgarioto N, Hepple RT. Fiber typing in aging muscle. Exerc Sport Sci Rev 42: 45-52, 2014
132. Purves-Smith FM, Solbak NM, Rowan SL, Hepple RT. Severe atrophy of slow myofibers in aging muscle is concealed by myosin heavy chain coexpression. Exp Gerontol 47: 913-918, 2012
133. Quadrilatero J, Alway SE, Dupont-Versteegden EE. Skeletal muscle apoptotic response to physical activity: potential mechanisms for protection. Appl Physiol Nutr Metab 36: 608-617, 2011
134. Ratbehavior.org. How Old is a Rat in Human Years? [Online]. http://www.ratbehavior.org/RatYears.htm [29 Jul. 2014].
135. Raue U, Trappe TA, Estrem ST, Qian HR, Helvering LM, Smith RC, Trappe S. Transcriptome signature of resistance exercise adaptations: mixed muscle and fiber type specific profiles in young and old adults. J Appl Physiol 112: 1625-1636, 2012
136. Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, Liu ZX, Dong J, Mustard KJ, Hawley SA, Befroy D, Pypaert M, Hardie DG, Young LH, Shulman GI. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 5: 151-156, 2007
137. Rivas DA, Lessard SJ, Rice NP, Lustgarten MS, So K, Goodyear LJ, Parnell LD, Fielding RA. Diminished skeletal muscle microRNA expression with aging is associated with attenuated muscle plasticity and inhibition of IGF-1 signaling. FASEB J. In press.
138. Rönn T, Poulsen P, Hansson O, Holmkvist J, Almgren P, Nilsson P, Tuomi T, Isomaa B, Groop L, Vaag A, Ling C. Age influences DNA methylation and gene expression of COX7A1 in human skeletal muscle. Diabetologia 51: 1159-1168, 2008
139. Rooyackers OE, Adey DB, Ades PA, Nair KS. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc Natl Acad Sci USA 93: 15364-15369, 1996
140. Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr 127: 990-991, 1997
141. Rossiter HB, Howlett RA, Holcombe HH, Entin PL, Wagner HE, Wagner PD. Age is no barrier to muscle structural, biochemical and angiogenic adaptations to training up to 24 months in female rats. J Physiol 565: 993-1005, 2005
142. Safdar A, Bourgeois JM, Ogborn DI, Little JP, Hettinga BP, Akhtar M, Thompson JE, Melov S, Mocellin NJ, Kujoth GC, Prolla TA, Tarnopolsky MA. Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc Natl Acad Sci USA 108: 4135-4140, 2011
143. Safdar A, Hamadeh MJ, Kaczor JJ, Raha S, Debeer J, Tarnopolsky MA. Aberrant mitochondrial homeostasis in the skeletal muscle of sedentary older adults. PLos One 5: e10778, 2010
144. Saleem A, Carter HN, Hood DA. p53 is necessary for the adaptive changes in cellular milieu subsequent to an acute bout of endurance exercise. Am J Physiol Cell Physiol 306: C241-C249, 2014
145. Satlin B, Gollnick PD. Skeletal muscle adaptability: significance for metabolism and performance. In: Handbook of Physiology: Skeletal Muscle. Bethesda, MD: Am. Physiol. Soc., 1983, sect. 10, chapt 19, p. 555-632
146. Scarpulla RC. Transcriptional paradigms in mammalian mitochondrial biogenesis and function. Physiol Rev 88: 611-638, 2008
147. Scarpulla RC. Nuclear control of respiratory chain expression by nuclear respiratory factors and PGC-1-related coactivator. Ann NY Acad Sci 1147: 321-334, 2008
148. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, Nair KS. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci USA 102: 5618-5623, 2005
149. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, Nair KS. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 52: 1888-1896, 2003
150. Singh K, Hood DA. Effect of denervation-induced muscle disuse on mitochondrial protein import. Am J Physiol Cell Physiol 300: C138-C145, 2011
151. Skorjanc D, Traub I, Pette D. Identical responses of fast muscle to sustained activity by low-frequency stimulation in young and aging rats. J Appl Physiol 85: 437-441, 1998
152. Sokol AM, Sztolsztener ME, Wasilewski M, Heinz E, Chacinska A. Mitochondrial protein translocases for survival and wellbeing. FEBS Lett 588: 2484-2495, 2014
153. Song W, Kwak HB, Lawler JM. Exercise training attenuates age-induced changes in apoptotic signaling in rat skeletal muscle. Antioxid Redox Signal 8: 517-528, 2006
154. Staunton L, O’Connell K, Ohlendieck K. Proteomic profiling of mitochondrial enzymes during skeletal muscle aging. J Aging Res 2011: 908035, 2011
155. Staunton L, Zweyer M, Swandulla D, Ohlendieck K. Mass spectrometry-based proteomic analysis of middle-aged vs. aged vastus lateralis reveals increased levels of carbonic anhydrase isoform 3 in senescent human skeletal muscle. Int J Mol Med 30: 723-733, 2012
156. Taivassalo T, Fu K, Johns T, Arnold D, Karpati G, Shoubridge EA. Gene shifting: a novel therapy for mitochondrial myopathy. Hum Mol Genet 8: 1047-1052, 1999
157. Taivassalo T, Gardner JL, Taylor RW, Schaefer AM, Newman J, Barron MJ, Haller RG, Turnbull DM. Endurance training and detraining in mitochondrial myopathies due to single large-scale mtDNA deletions. Brain 129: 3391-3401, 2006
158. Taivassalo T, Shoubridge EA, Chen J, Kennaway NG, DiMauro S, Arnold DL, Haller RG. Aerobic conditioning in patients with mitochondrial myopathies: physiological, biochemical, and genetic effects. Ann Neurol 50: 133-141, 2001
159. Terman A, Kurz T, Navratil M, Arriaga EA, Brunk UT. Mitochondrial turnover and aging of longlived postmitotic cells: The mitochondrial-lysosomal axis theory of aging. Antioxid Redox Signal 12: 503-535, 2010
160. Théron L, Gueugneau M, Coudy C, Viala D, Bijlsma A, Butler-Browne G, Maier A, Béchet D, Chambon C. Label-free quantitative protein profiling of vastus lateralis muscle during human aging. Mol Cell Proteomics 13: 283-294, 2014
161. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly YM, Gidlöf S, Oldfors A, Wibom R, Törnell J, Jacobs HT, Larsson NG. Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429: 417-423, 2004
162. Trounce I, Byrne E, Marzuki S. Decline in skeletal muscle mitochondrial respiratory chain function: Possible factor in ageing. Lancet 1: 637-639, 1989
163. Wallace DC. Mitochondrial DNA mutations in disease and aging. Environ Mol Mutagen 51: 440-450, 2010
164. Walters TJ, Sweeney HL, Farrar RP. Influence of electrical stimulation on a fast-twitch muscle in aging rats. J Appl Physiol 71: 1921-1928, 1991
165. Wanagat J, Cao Z, Pathare P, Aiken JM. Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J 15: 322-332, 2001
166. Wang Y, Michikawa Y, Mallidis C, Bai Y, Woodhouse L, Yarasheski KE, Miller CA, Askanas V, Engel WK, Bhasin S, Attardi G. Muscle-specific mutations accumulate with aging in critical human mtDNA control sites for replication. Proc Natl Acad Sci USA 98: 4022-4027, 2001
167. Welle S, Bhatt K, Shah B, Needler N, Delehanty JM, Thornton CA. Reduced amount of mitochondrial DNA in aged human muscle. J Appl Physiol 94: 1479-1484, 2003
168. Welle S, Bhatt K, Thornton CA. High-abundance mRNAs in human muscle: Comparison between young and old. J Appl Physiol 89: 297-304, 2000
169. Welle S, Brooks AI, Delehanty JM, Needler N, Bhatt K, Shah B, Thornton CA. Skeletal muscle gene expression profiles in 20-29 year old and 65-71 year old women. Exp Gerontol 39: 369-377, 2004
170. Welle S, Brooks AI, Delehanty JM, Needler N, Thornton CA. Gene expression profile of aging in human muscle. Physiol Genomics 14: 149-159, 2003
171. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, Moraes CT. Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA 106: 20405-20410, 2009
172. Wohlgemuth SE, Seo AY, Marzetti E, Lees HA, Leeuwenburgh C. Skeletal muscle autophagy and apoptosis during aging: Effects of calorie restriction and life-long exercise. Exp Gerontol 45: 138-148, 2010
173. Wu JJ, Quijano C, Chen E, Liu H, Cao L, Fergusson MM, Rovira II, Gutkind S, Daniels MP, Komatsu M, Finkel T. Mitochondrial dysfunction and oxidative stress mediate the physiological impairment induced by the disruption of autophagy. Aging (Milano) 1: 425-437, 2009
174. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999
175. Zampieri S, Pietrangelo L, Loefler S, Fruhmann H, Vogelauer M, Burggraf S, Pond A, Grim-Stieger M, Cvecka J, Sedliak M, Tirpáková V, Mayr W, Sarabon N, Rossini K, Barberi L, De Rossi M, Romanello V, Boncompagni S, Musarò A, Sandri M, Protasi F, Carraro U, Kern H. Lifelong physical exercise delays age-associated skeletal muscle decline. J Gerontol A Biol Sci Med Sci 70: 163-173, 2015
176. Zhang Y, Iqbal S, O’Leary MFN, Menzies KJ, Saleem A, Ding S, Hood DA. Altered mitochondrial morphology and defective protein import reveal novel roles for Bax and/or Bak in skeletal muscle. Am J Physiol Cell Physiol 305: C502-C511, 2013
177. Zhang Y, Uguccioni G, Ljubicic V, Irrcher I, Iqbal S, Singh K, Ding S, Hood DA. Multiple signaling pathways regulate contractile activity-mediated PGC-1gene expression and activity in skeletal muscle cells. Physiol Rep 2: e12008, 2014
178. Zhao L, Zou X, Feng Z, Luo C, Liu J, Li H, Chang L, Wang H, Li Y, Long J, Gao F, Liu J. Evidence for association of mitochondrial metabolism alteration with lipid accumulation in aging rats. Exp Gerontol 56: 3-12, 2014
179. Zykovich A, Hubbard A, Flynn JM, Tarnopolsky M, Fraga MF, Kerksick C, Ogborn D, MacNeil L, Mooney SD, Melov S. Genome-wide DNA methylation changes with age in disease-free human skeletal muscle. Aging Cell 13: 360-366, 2014.