Exercise Promotes Healthy Aging of Skeletal Muscle

Cell Metabolism

Volumn 23, Issue 6, 2016, Pages 1034-1047

  Cartee, Gregory D ^a,b,c   Hepple, Russell T ^d,e,f   Bamman, Marcas M ^g,h,i   Zierath, Juleen R ^j,k  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^d MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f MCGILL UNIVERSITY   (Canada)

^g UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^h UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

ⁱ BIRMINGHAM VA MEDICAL CENTER   (United States)

^j KAROLINSKA INSTITUTE   (Sweden)

^k UNIVERSITY OF COPENHAGEN   (Denmark)

more..

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; INSULIN;

AGING; ENDURANCE TRAINING; ENERGY EXPENDITURE; ENVIRONMENTAL FACTOR; EXERCISE; FUNCTIONAL STATUS; GLUCOSE HOMEOSTASIS; GLUCOSE TRANSPORT; HUMAN; INSULIN SENSITIVITY; LIFESTYLE; MITOCHONDRION; MUSCLE ATROPHY; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; PHYSICAL ACTIVITY; PLASTICITY; PRIORITY JOURNAL; RESISTANCE TRAINING; REVIEW; SKELETAL MUSCLE; METABOLISM; PHYSIOLOGY;

AGING; EXERCISE; HUMANS; INSULIN; MITOCHONDRIA; MUSCLE, SKELETAL;

EID: 84975449846     PISSN: 15504131     EISSN: 19327420     Source Type: Journal    
DOI: 10.1016/j.cmet.2016.05.007     Document Type: Review

References (178)

1. G.R. Adams, and M.M. Bamman Characterization and regulation of mechanical loading-induced compensatory muscle hypertrophy Compr. Physiol. 2 2012 2829 2870
2. C.E. Amara, E.G. Shankland, S.A. Jubrias, D.J. Marcinek, M.J. Kushmerick, and K.E. Conley Mild mitochondrial uncoupling impacts cellular aging in human muscles in vivo Proc. Natl. Acad. Sci. USA 104 2007 1057 1062
3. F. Amati, J.J. Dubé, P.M. Coen, M. Stefanovic-Racic, F.G. Toledo, and B.H. Goodpaster Physical inactivity and obesity underlie the insulin resistance of aging Diabetes Care 32 2009 1547 1549
4. G. Annuzzi, G. Riccardi, B. Capaldo, and L. Kaijser Increased insulin-stimulated glucose uptake by exercised human muscles one day after prolonged physical exercise Eur. J. Clin. Invest. 21 1991 6 12
5. E.B. Arias, J. Kim, K. Funai, and G.D. Cartee Prior exercise increases phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle Am. J. Physiol. Endocrinol. Metab. 292 2007 E1191 E1200
6. M.M. Bamman, J.K. Petrella, J.S. Kim, D.L. Mayhew, and J.M. Cross Cluster analysis tests the importance of myogenic gene expression during myofiber hypertrophy in humans J. Appl. Physiol. 102 2007 2232 2239
7. R.N. Baumgartner, K.M. Koehler, D. Gallagher, L. Romero, S.B. Heymsfield, R.R. Ross, P.J. Garry, and R.D. Lindeman Epidemiology of sarcopenia among the elderly in New Mexico Am. J. Epidemiol. 147 1998 755 763
8. C. Beaudart, J.Y. Reginster, J. Slomian, F. Buckinx, M. Locquet, and O. Bruyère Prevalence of sarcopenia: the impact of different diagnostic cut-off limits J. Musculoskelet. Neuronal Interact. 14 2014 425 431
9. C. Beaudart, R. Rizzoli, O. Bruyère, J.Y. Reginster, and E. Biver Sarcopenia: burden and challenges for public health Arch. Public Health 72 2014 45
10. C. Beaudart, J.Y. Reginster, J. Slomian, F. Buckinx, N. Dardenne, A. Quabron, C. Slangen, S. Gillain, J. Petermans, and O. Bruyère Estimation of sarcopenia prevalence using various assessment tools Exp. Gerontol. 61 2015 31 37
11. E. Beregi, O. Regius, T. Hüttl, and Z. Göbl Age-related changes in the skeletal muscle cells Z. Gerontol. 21 1988 83 86
12. P. Bernardi, A. Rasola, M. Forte, and G. Lippe The mitochondrial permeability transition pore: channel formation by F-ATP synthase, integration in signal transduction, and role in pathophysiology Physiol. Rev. 95 2015 1111 1155
13. A.C. Betik, D.J. Baker, D.J. Krause, M.J. McConkey, and R.T. Hepple Exercise training in late middle-aged male Fischer 344 x Brown Norway F1-hybrid rats improves skeletal muscle aerobic function Exp. Physiol. 93 2008 863 871
14. A.C. Betik, M.M. Thomas, K.J. Wright, C.D. Riel, and R.T. Hepple 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. 297 2009 R744 R755
15. C.S. Bickel, J.M. Cross, and M.M. Bamman Exercise dosing to retain resistance training adaptations in young and older adults Med. Sci. Sports Exerc. 43 2011 1177 1187
16. R.S. Biensø, J. Olesen, L. Gliemann, J.F. Schmidt, M.S. Matzen, J.F. Wojtaszewski, Y. Hellsten, and H. Pilegaard Effects of exercise training on regulation of skeletal muscle glucose metabolism in elderly men J. Gerontol. A Biol. Sci. Med. Sci. 70 2015 866 872
17. F.W. Booth, M.V. Chakravarthy, S.E. Gordon, and E.E. Spangenburg Waging war on physical inactivity: using modern molecular ammunition against an ancient enemy J. Appl. Physiol. 93 2002 3 30
18. F.W. Booth, M.J. Laye, and M.D. Roberts Lifetime sedentary living accelerates some aspects of secondary aging J. Appl. Physiol. 111 2011 1497 1504
19. F.W. Booth, C.K. Roberts, and M.J. Laye Lack of exercise is a major cause of chronic diseases Compr. Physiol. 2 2012 1143 1211
20. C. Bouchard, S.N. Blair, and P.T. Katzmarzyk Less sitting, more physical activity, or higher fitness? Mayo Clin. Proc. 90 2015 1533 1540
21. J. Boucher, A. Kleinridders, and C.R. Kahn Insulin receptor signaling in normal and insulin-resistant states Cold Spring Harb. Perspect. Biol. 6 2014 10.1101/cshperspect.a009191
22. D.M. Callahan, N.G. Bedrin, M. Subramanian, J. Berking, P.A. Ades, M.J. Toth, and M.S. Miller Age-related structural alterations in human skeletal muscle fibers and mitochondria are sex specific: relationship to single-fiber function J. Appl. Physiol. 116 2014 1582 1592
23. J. Cannavino, L. Brocca, M. Sandri, B. Grassi, R. Bottinelli, and M.A. Pellegrino The role of alterations in mitochondrial dynamics and PGC-1α over-expression in fast muscle atrophy following hindlimb unloading J. Physiol. 593 2015 1981 1995
24. F. Capel, C. Buffière, P. Patureau Mirand, and L. Mosoni Differential variation of mitochondrial H2O2 release during aging in oxidative and glycolytic muscles in rats Mech. Ageing Dev. 125 2004 367 373
25. F. Capel, V. Rimbert, D. Lioger, A. Diot, P. Rousset, P.P. Mirand, Y. Boirie, B. Morio, and L. Mosoni Due to reverse electron transfer, mitochondrial H2O2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved Mech. Ageing Dev. 126 2005 505 511
26. G.D. Cartee Mechanisms for greater insulin-stimulated glucose uptake in normal and insulin-resistant skeletal muscle after acute exercise Am. J. Physiol. Endocrinol. Metab. 309 2015 E949 E959
27. G.D. Cartee, and E.E. Bohn Growth hormone reduces glucose transport but not GLUT-1 or GLUT-4 in adult and old rats Am. J. Physiol. 268 1995 E902 E909
28. G.D. Cartee, and R.P. Farrar Muscle respiratory capacity and VO2 max in identically trained young and old rats J. Appl. Physiol. 63 1987 257 261
29. G.D. Cartee, and J.O. Holloszy Exercise increases susceptibility of muscle glucose transport to activation by various stimuli Am. J. Physiol. 258 1990 E390 E393
30. G.D. Cartee, D.A. Young, M.D. Sleeper, J. Zierath, H. Wallberg-Henriksson, and J.O. Holloszy Prolonged increase in insulin-stimulated glucose transport in muscle after exercise Am. J. Physiol. 256 1989 E494 E499
31. G.D. Cartee, C. Briggs-Tung, and E.W. Kietzke Persistent effects of exercise on skeletal muscle glucose transport across the life-span of rats J. Appl. Physiol. 75 1993 972 978
32. H.N. Carter, C.C. Chen, and D.A. Hood Mitochondria, muscle health, and exercise with advancing age Physiology (Bethesda) 30 2015 208 223
33. C.J. Caspersen, K.E. Powell, and G.M. Christenson Physical activity, exercise, and physical fitness: definitions and distinctions for health-related research Public Health Rep. 100 1985 126 131
34. C.M. Castorena, E.B. Arias, N. Sharma, and G.D. Cartee Postexercise improvement in insulin-stimulated glucose uptake occurs concomitant with greater AS160 phosphorylation in muscle from normal and insulin-resistant rats Diabetes 63 2014 2297 2308
35. B. Chabi, V. Ljubicic, K.J. Menzies, J.H. Huang, A. Saleem, and D.A. Hood Mitochondrial function and apoptotic susceptibility in aging skeletal muscle Aging Cell 7 2008 2 12
36. D.C. Chan Fusion and fission: interlinked processes critical for mitochondrial health Annu. Rev. Genet. 46 2012 265 287
37. V.S. Chekanov, P. Karakozov, M. Rieder, and G. Zander Age related skeletal muscle response to electrical stimulation ASAIO J. 46 2000 474 481
38. M.E. Cleasby, P. Jamieson, and P.J. Atherton Insulin resistance and sarcopenia: mechanistic links between common co-morbidities J. Endocrinol. 2016 10.1530/JOE-15-0533 Published online March 1, 2016
39. R. Coleman, M. Silbermann, D. Gershon, and A.Z. Reznick Giant mitochondria in the myocardium of aging and endurance-trained mice Gerontology 33 1987 34 39
40. F.S. Collins, and H. Varmus A new initiative on precision medicine N. Engl. J. Med. 372 2015 793 795
41. K.E. Conley, S.A. Jubrias, and P.C. Esselman Oxidative capacity and ageing in human muscle J. Physiol. 526 2000 203 210
42. L.A. Consitt, J. Van Meter, C.A. Newton, D.N. Collier, M.S. Dar, J.F. Wojtaszewski, J.T. Treebak, C.J. Tanner, and J.A. Houmard Impairments in site-specific AS160 phosphorylation and effects of exercise training Diabetes 62 2013 3437 3447
43. C.C. Cowie, K.F. Rust, E.S. Ford, M.S. Eberhardt, D.D. Byrd-Holt, C. Li, D.E. Williams, E.W. Gregg, K.E. Bainbridge, S.H. Saydah, and L.S. Geiss Full accounting of diabetes and pre-diabetes in the U.S. population in 1988-1994 and 2005-2006 Diabetes Care 32 2009 287 294
44. J.H. Cox, R.N. Cortright, G.L. Dohm, and J.A. Houmard Effect of aging on response to exercise training in humans: skeletal muscle GLUT-4 and insulin sensitivity J. Appl. Physiol. 86 1999 2019 2025
45. J. Crandall, D. Schade, Y. Ma, W.Y. Fujimoto, E. Barrett-Connor, S. Fowler, S. Dagogo-Jack, R. Andres Diabetes Prevention Program Research Group The influence of age on the effects of lifestyle modification and metformin in prevention of diabetes J. Gerontol. A Biol. Sci. Med. Sci. 61 2006 1075 1081
46. D.F. Dai, Y.A. Chiao, D.J. Marcinek, H.H. Szeto, and P.S. Rabinovitch Mitochondrial oxidative stress in aging and healthspan Longev. Healthspan 3 2014 6
47. R.A. DeFronzo, E. Jacot, E. Jequier, E. Maeder, J. Wahren, and J.P. Felber The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization Diabetes 30 1981 1000 1007
48. F. Dela, T. Ploug, A. Handberg, L.N. Petersen, J.J. Larsen, K.J. Mikines, and H. Galbo Physical training increases muscle GLUT4 protein and mRNA in patients with NIDDM Diabetes 43 1994 862 865
49. P. Demakakos, M. Hamer, E. Stamatakis, and A. Steptoe Low-intensity physical activity is associated with reduced risk of incident type 2 diabetes in older adults: evidence from the English Longitudinal Study of Ageing Diabetologia 53 2010 1877 1885
50. M.J. Drummond, O. Addison, L. Brunker, P.N. Hopkins, D.A. McClain, P.C. LaStayo, and R.L. Marcus Downregulation of E3 ubiquitin ligases and mitophagy-related genes in skeletal muscle of physically inactive, frail older women: a cross-sectional comparison J. Gerontol. A Biol. Sci. Med. Sci. 69 2014 1040 1048
51. B. Egan, and J.R. Zierath Exercise metabolism and the molecular regulation of skeletal muscle adaptation Cell Metab. 17 2013 162 184
52. F. Escrivá, M.L. Gavete, Y. Fermín, C. Pérez, N. Gallardo, C. Alvarez, A. Andrés, M. Ros, and J.M. Carrascosa Effect of age and moderate food restriction on insulin sensitivity in Wistar rats: role of adiposity J. Endocrinol. 194 2007 131 141
53. E.M. Evans, S.B. Racette, L.R. Peterson, D.T. Villareal, J.S. Greiwe, and J.O. Holloszy Aerobic power and insulin action improve in response to endurance exercise training in healthy 77-87 yr olds J. Appl. Physiol. 98 2005 40 45
54. F.S. Facchini, N. Hua, F. Abbasi, and G.M. Reaven Insulin resistance as a predictor of age-related diseases J. Clin. Endocrinol. Metab. 86 2001 3574 3578
55. V.C. Figueiredo, M.K. Caldow, V. Massie, J.F. Markworth, D. Cameron-Smith, and A.J. Blazevich Ribosome biogenesis adaptation in resistance training-induced human skeletal muscle hypertrophy Am. J. Physiol. Endocrinol. Metab. 309 2015 E72 E83
56. R.I. Fink, P. Wallace, and J.M. Olefsky Effects of aging on glucose-mediated glucose disposal and glucose transport J. Clin. Invest. 77 1986 2034 2041
57. M.E. Francois, J.C. Baldi, P.J. Manning, S.J. Lucas, J.A. Hawley, M.J. Williams, and J.D. Cotter 'Exercise snacks' before meals: a novel strategy to improve glycaemic control in individuals with insulin resistance Diabetologia 57 2014 1437 1445
58. C.S. Fry, M.J. Drummond, E.L. Glynn, J.M. Dickinson, D.M. Gundermann, K.L. Timmerman, D.K. Walker, S. Dhanani, E. Volpi, and B.B. Rasmussen Aging impairs contraction-induced human skeletal muscle mTORC1 signaling and protein synthesis Skelet. Muscle 1 2011 11
59. S. Fulle, F. Protasi, G. Di Tano, T. Pietrangelo, A. Beltramin, S. Boncompagni, L. Vecchiet, and G. Fanò The contribution of reactive oxygen species to sarcopenia and muscle ageing Exp. Gerontol. 39 2004 17 24
60. K. Funai, G.G. Schweitzer, N. Sharma, M. Kanzaki, and G.D. Cartee Increased AS160 phosphorylation, but not TBC1D1 phosphorylation, with increased postexercise insulin sensitivity in rat skeletal muscle Am. J. Physiol. Endocrinol. Metab. 297 2009 E242 E251
61. K. Funai, G.G. Schweitzer, C.M. Castorena, M. Kanzaki, and G.D. Cartee In vivo exercise followed by in vitro contraction additively elevates subsequent insulin-stimulated glucose transport by rat skeletal muscle Am. J. Physiol. Endocrinol. Metab. 298 2010 E999 E1010
62. M. Gaster, P. Poulsen, A. Handberg, H.D. Schroder, and H. Beck-Nielsen Direct evidence of fiber type-dependent GLUT-4 expression in human skeletal muscle Am. J. Physiol. Endocrinol. Metab. 278 2000 E910 E916
63. B.H. Goodpaster, C.L. Carlson, M. Visser, D.E. Kelley, A. Scherzinger, T.B. Harris, E. Stamm, and A.B. Newman Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study J. Appl. Physiol. 90 2001 2157 2165
64. B.H. Goodpaster, S.W. Park, T.B. Harris, S.B. Kritchevsky, M. Nevitt, A.V. Schwartz, E.M. Simonsick, F.A. Tylavsky, M. Visser, and A.B. Newman 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 2006 1059 1064
65. G. Gouspillou, I. Bourdel-Marchasson, R. Rouland, G. Calmettes, J.M. Franconi, V. Deschodt-Arsac, and P. Diolez Alteration of mitochondrial oxidative phosphorylation in aged skeletal muscle involves modification of adenine nucleotide translocator Biochim. Biophys. Acta 1797 2010 143 151
66. G. Gouspillou, I. Bourdel-Marchasson, R. Rouland, G. Calmettes, M. Biran, V. Deschodt-Arsac, S. Miraux, E. Thiaudiere, P. Pasdois, D. Detaille, and et al. Mitochondrial energetics is impaired in vivo in aged skeletal muscle Aging Cell 13 2014 39 48
67. G. Gouspillou, N. Sgarioto, S. Kapchinsky, F. Purves-Smith, B. Norris, C.H. Pion, S. Barbat-Artigas, F. Lemieux, T. Taivassalo, J.A. Morais, and et al. Increased sensitivity to mitochondrial permeability transition and myonuclear translocation of endonuclease G in atrophied muscle of physically active older humans FASEB J. 28 2014 1621 1633
68. M. Gram, A. Vigelsø, T. Yokota, J.W. Helge, F. Dela, and M. Hey-Mogensen Skeletal muscle mitochondrial H2 O2 emission increases with immobilization and decreases after aerobic training in young and older men J. Physiol. 593 2015 4011 4027
69. E.A. Gulve, K.J. Rodnick, E.J. Henriksen, and J.O. Holloszy Effects of wheel running on glucose transporter (GLUT4) concentration in skeletal muscle of young adult and old rats Mech. Ageing Dev. 67 1993 187 200
70. S.M. Haffner Epidemiology of insulin resistance and its relation to coronary artery disease Am. J. Cardiol. 84 1A 1999 11J 14J
71. D.H. Han, P.A. Hansen, M.M. Chen, and J.O. Holloszy DHEA treatment reduces fat accumulation and protects against insulin resistance in male rats J. Gerontol. A Biol. Sci. Med. Sci. 53 1998 B19 B24
72. P.A. Hansen, L.A. Nolte, M.M. Chen, and J.O. Holloszy Increased GLUT-4 translocation mediates enhanced insulin sensitivity of muscle glucose transport after exercise J. Appl. Physiol. 85 1998 1218 1222
73. D. Heber, S. Ingles, J.M. Ashley, M.H. Maxwell, R.F. Lyons, and R.M. Elashoff Clinical detection of sarcopenic obesity by bioelectrical impedance analysis Am. J. Clin. Nutr. 64 Suppl 1996 472S 477S
74. S.L. Hebert, P. Marquet-de Rougé, I.R. Lanza, S.K. McCrady-Spitzer, J.A. Levine, S. Middha, R.E. Carter, K.A. Klaus, T.M. Therneau, E.W. Highsmith, and K.S. Nair Mitochondrial aging and physical decline: insights from three generations of women J. Gerontol. A Biol. Sci. Med. Sci. 70 2015 1409 1417
75. R.T. Hepple Mitochondrial involvement and impact in aging skeletal muscle Front. Aging Neurosci. 6 2014 211 10.1016/j.freeradbiomed.2016.03.017
76. R.T. Hepple Impact of aging on mitochondrial function in cardiac and skeletal muscle Free Radic. Biol. Med. 2016 10.1016/j.freeradbiomed.2016.03.017 Published online March 24, 2016
77. J.O. Holloszy The biology of aging Mayo Clin. Proc. 75 Suppl 2000 S3 S8
78. J.O. Holloszy, W.M. Kohrt, and P.A. Hansen The regulation of carbohydrate and fat metabolism during and after exercise Front. Biosci. 3 1998 D1011 D1027
79. J.A. Houmard, M.D. Weidner, P.L. Dolan, N. Leggett-Frazier, K.E. Gavigan, M.S. Hickey, G.L. Tyndall, D. Zheng, A. Alshami, and G.L. Dohm Skeletal muscle GLUT4 protein concentration and aging in humans Diabetes 44 1995 555 560
80. J.A. Houmard, M.L. Weidner, K.E. Gavigan, G.L. Tyndall, M.S. Hickey, and A. Alshami Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging J. Appl. Physiol. 85 1998 1337 1341
81. D.M. Huffman, and N. Barzilai Role of visceral adipose tissue in aging Biochim. Biophys. Acta 1790 2009 1117 1123
82. V.A. Hughes, M.A. Fiatarone, R.A. Fielding, B.B. Kahn, C.M. Ferrara, P. Shepherd, E.C. Fisher, R.R. Wolfe, D. Elahi, and W.J. Evans Exercise increases muscle GLUT-4 levels and insulin action in subjects with impaired glucose tolerance Am. J. Physiol. 264 1993 E855 E862
83. G.R. Hunter, J.P. McCarthy, and M.M. Bamman Effects of resistance training on older adults Sports Med. 34 2004 329 348
84. E. Hütter, M. Skovbro, B. Lener, C. Prats, R. Rabøl, F. Dela, and P. Jansen-Dürr Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle Aging Cell 6 2007 245 256
85. S. Iqbal, O. Ostojic, K. Singh, A.M. Joseph, and D.A. Hood Expression of mitochondrial fission and fusion regulatory proteins in skeletal muscle during chronic use and disuse Muscle Nerve 48 2013 963 970
86. I. Irrcher, V. Ljubicic, A.F. Kirwan, and D.A. Hood AMP-activated protein kinase-regulated activation of the PGC-1alpha promoter in skeletal muscle cells PLoS ONE 3 2008 e3614
87. 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, and et al. Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration FASEB J. 24 2010 1376 1390
88. I. Janssen, S.B. Heymsfield, and R. Ross Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability J. Am. Geriatr. Soc. 50 2002 889 896
89. I. Janssen, R.N. Baumgartner, R. Ross, I.H. Rosenberg, and R. Roubenoff Skeletal muscle cutpoints associated with elevated physical disability risk in older men and women Am. J. Epidemiol. 159 2004 413 421
90. I. Janssen, D.S. Shepard, P.T. Katzmarzyk, and R. Roubenoff The healthcare costs of sarcopenia in the United States J. Am. Geriatr. Soc. 52 2004 80 85
91. A.M. Joseph, P.J. Adhihetty, N.R. Wawrzyniak, S.E. Wohlgemuth, A. Picca, G.C. Kujoth, T.A. Prolla, and C. Leeuwenburgh Dysregulation of mitochondrial quality control processes contribute to sarcopenia in a mouse model of premature aging PLoS ONE 8 2013 e69327
92. P.P. Karunadharma, N. Basisty, Y.A. Chiao, D.F. Dai, R. Drake, N. Levy, W.J. Koh, M.J. Emond, S. Kruse, D. Marcinek, and et al. Respiratory chain protein turnover rates in mice are highly heterogeneous but strikingly conserved across tissues, ages, and treatments FASEB J. 29 2015 3582 3592
93. J.A. Kent-Braun, and A.V. Ng Skeletal muscle oxidative capacity in young and older women and men J. Appl. Physiol. 89 2000 1072 1078
94. M. Kern, P.L. Dolan, R.S. Mazzeo, J.A. Wells, and G.L. Dohm Effect of aging and exercise on GLUT-4 glucose transporters in muscle Am. J. Physiol. 263 1992 E362 E367
95. J.S. Kim, D.J. Kosek, J.K. Petrella, J.M. Cross, and M.M. Bamman Resting and load-induced levels of myogenic gene transcripts differ between older adults with demonstrable sarcopenia and young men and women J. Appl. Physiol. 99 2005 2149 2158
96. J.P. Kirwan, W.M. Kohrt, D.M. Wojta, R.E. Bourey, and J.O. Holloszy Endurance exercise training reduces glucose-stimulated insulin levels in 60- to 70-year-old men and women J. Gerontol. 48 1993 M84 M90
97. W.M. Kohrt, J.P. Kirwan, M.A. Staten, R.E. Bourey, D.S. King, and J.O. Holloszy Insulin resistance in aging is related to abdominal obesity Diabetes 42 1993 273 281
98. A.R. Konopka, M.K. Suer, C.A. Wolff, and M.P. Harber Markers of human skeletal muscle mitochondrial biogenesis and quality control: effects of age and aerobic exercise training J. Gerontol. A Biol. Sci. Med. Sci. 69 2014 371 378
99. D.J. Kosek, J.S. Kim, J.K. Petrella, J.M. Cross, and M.M. Bamman Efficacy of 3 days/wk resistance training on myofiber hypertrophy and myogenic mechanisms in young vs. older adults J. Appl. Physiol. 101 2006 531 544
100. M. Kumari, E. Brunner, and R. Fuhrer Minireview: mechanisms by which the metabolic syndrome and diabetes impair memory J. Gerontol. A Biol. Sci. Med. Sci. 55 2000 B228 B232
101. H. Kuwahara, T. Horie, S. Ishikawa, C. Tsuda, S. Kawakami, Y. Noda, T. Kaneko, S. Tahara, T. Tachibana, M. Okabe, and et al. Oxidative stress in skeletal muscle causes severe disturbance of exercise activity without muscle atrophy Free Radic. Biol. Med. 48 2010 1252 1262
102. A.V. Kuznetsov, J. Troppmair, R. Sucher, M. Hermann, V. Saks, and R. Margreiter Mitochondrial subpopulations and heterogeneity revealed by confocal imaging: possible physiological role? Biochim. Biophys. Acta 1757 2006 686 691
103. K.A. Landers, G.R. Hunter, C.J. Wetzstein, M.M. Bamman, and R.L. Weinsier The interrelationship among muscle mass, strength, and the ability to perform physical tasks of daily living in younger and older women J. Gerontol. A Biol. Sci. Med. Sci. 56 2001 B443 B448
104. I.R. Lanza, D.E. Befroy, and J.A. Kent-Braun Age-related changes in ATP-producing pathways in human skeletal muscle in vivo J. Appl. Physiol. 99 2005 1736 1744
105. J. Lapointe, and S. Hekimi Early mitochondrial dysfunction in long-lived Mclk1+/- mice J. Biol. Chem. 283 2008 26217 26227
106. J.P. Leduc-Gaudet, M. Picard, F. St-Jean Pelletier, N. Sgarioto, M.J. Auger, J. Vallée, R. Robitaille, D.H. St-Pierre, and G. Gouspillou Mitochondrial morphology is altered in atrophied skeletal muscle of aged mice Oncotarget 6 2015 17923 17937
107. D. Leto, and A.R. Saltiel Regulation of glucose transport by insulin: traffic control of GLUT4 Nat. Rev. Mol. Cell Biol. 13 2012 383 396
108. J. Lexell Human aging, muscle mass, and fiber type composition J. Gerontol. A Biol. Sci. Med. Sci. 50 1995 11 16
109. J. Lexell, K. Henriksson-Larsén, B. Winblad, and M. Sjöström Distribution of different fiber types in human skeletal muscles: effects of aging studied in whole muscle cross sections Muscle Nerve 6 1983 588 595
110. J. Lexell, D. Downham, and M. Sjöström 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. 72 1986 211 222
111. J. Lexell, C.C. Taylor, and M. Sjöström 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. 84 1988 275 294
112. V. Ljubicic, and D.A. Hood Diminished contraction-induced intracellular signaling towards mitochondrial biogenesis in aged skeletal muscle Aging Cell 8 2009 394 404
113. V. Ljubicic, and D.A. Hood Specific attenuation of protein kinase phosphorylation in muscle with a high mitochondrial content Am. J. Physiol. Endocrinol. Metab. 297 2009 E749 E758
114. M.S. Lustgarten, Y.C. Jang, Y. Liu, W. Qi, Y. Qin, P.L. Dahia, Y. Shi, A. Bhattacharya, F.L. Muller, T. Shimizu, and et al. MnSOD deficiency results in elevated oxidative stress and decreased mitochondrial function but does not lead to muscle atrophy during aging Aging Cell 10 2011 493 505
115. C.N. Lyons, O. Mathieu-Costello, and C.D. Moyes Regulation of skeletal muscle mitochondrial content during aging J. Gerontol. A Biol. Sci. Med. Sci. 61 2006 3 13
116. A. Mansouri, F.L. Muller, Y. Liu, R. Ng, J. Faulkner, M. Hamilton, A. Richardson, T.T. Huang, C.J. Epstein, and H. Van Remmen Alterations in mitochondrial function, hydrogen peroxide release and oxidative damage in mouse hind-limb skeletal muscle during aging Mech. Ageing Dev. 127 2006 298 306
117. D.J. Marcinek, K.A. Schenkman, W.A. Ciesielski, D. Lee, and K.E. Conley Reduced mitochondrial coupling in vivo alters cellular energetics in aged mouse skeletal muscle J. Physiol. 569 2005 467 473
118. R.L. Marcus, O. Addison, P.C. LaStayo, R. Hungerford, A.R. Wende, J.M. Hoffman, E.D. Abel, and D.A. McClain Regional muscle glucose uptake remains elevated one week after cessation of resistance training independent of altered insulin sensitivity response in older adults with type 2 diabetes J. Endocrinol. Invest. 36 2013 111 117
119. E. Marzetti, J.C. Hwang, H.A. Lees, S.E. Wohlgemuth, E.E. Dupont-Versteegden, C.S. Carter, R. Bernabei, and C. Leeuwenburgh Mitochondrial death effectors: relevance to sarcopenia and disuse muscle atrophy Biochim. Biophys. Acta 1800 2010 235 244
120. E. Marzetti, R. Calvani, M. Cesari, T.W. Buford, M. Lorenzi, B.J. Behnke, and C. Leeuwenburgh Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials Int. J. Biochem. Cell Biol. 45 2013 2288 2301
121. O. Mathieu-Costello, Y. Ju, M. Trejo-Morales, and L. Cui Greater capillary-fiber interface per fiber mitochondrial volume in skeletal muscles of old rats J. Appl. Physiol. 99 2005 281 289
122. D.L. Mayhew, T.A. Hornberger, H.C. Lincoln, and M.M. Bamman Eukaryotic initiation factor 2B epsilon induces cap-dependent translation and skeletal muscle hypertrophy J. Physiol. 589 2011 3023 3037
123. G.S. Meneilly, T. Elliott, D. Tessier, L. Hards, and H. Tildesley NIDDM in the elderly Diabetes Care 19 1996 1320 1325
124. K.J. Menzies, K. Singh, A. Saleem, and D.A. Hood Sirtuin 1-mediated effects of exercise and resveratrol on mitochondrial biogenesis J. Biol. Chem. 288 2013 6968 6979
125. E.K. Merritt, M.J. Stec, A. Thalacker-Mercer, S.T. Windham, J.M. Cross, D.P. Shelley, S. Craig Tuggle, D.J. Kosek, J.S. Kim, and M.M. Bamman Heightened muscle inflammation susceptibility may impair regenerative capacity in aging humans J. Appl. Physiol. 115 2013 937 948
126. P. Mishra, V. Carelli, G. Manfredi, and D.C. Chan Proteolytic cleavage of Opa1 stimulates mitochondrial inner membrane fusion and couples fusion to oxidative phosphorylation Cell Metab. 19 2014 630 641
127. J. Nagasawa, Y. Sato, and T. Ishiko Time course of in vivo insulin sensitivity after a single bout of exercise in rats Int. J. Sports Med. 12 1991 399 402
128. M. Navratil, A. Terman, and E.A. Arriaga Giant mitochondria do not fuse and exchange their contents with normal mitochondria Exp. Cell Res. 314 2008 164 172
129. P.D. Neufer, M.M. Bamman, D.M. Muoio, C. Bouchard, D.M. Cooper, B.H. Goodpaster, F.W. Booth, W.M. Kohrt, R.E. Gerszten, M.P. Mattson, and et al. Understanding the cellular and molecular mechanisms of physical activity-induced health benefits Cell Metab. 22 2015 4 11
130. T. Ogata, and Y. Yamasaki Ultra-high-resolution scanning electron microscopy of mitochondria and sarcoplasmic reticulum arrangement in human red, white, and intermediate muscle fibers Anat. Rec. 248 1997 214 223
131. J.R. Pauli, E.R. Ropelle, D.E. Cintra, C.T. De Souza, A.S. da Silva, J.C. Moraes, P.O. Prada, J.A. de Almeida Leme, E. Luciano, L.A. Velloso, and et al. Acute exercise reverses aged-induced impairments in insulin signaling in rodent skeletal muscle Mech. Ageing Dev. 131 2010 323 329
132. C. Pehmøller, N. Brandt, J.B. Birk, L.D. Høeg, K.A. Sjøberg, L.J. Goodyear, B. Kiens, E.A. Richter, and J.F. Wojtaszewski Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4 Diabetes 61 2012 2743 2752
133. G. Perseghin, T.B. Price, K.F. Petersen, M. Roden, G.W. Cline, K. Gerow, D.L. Rothman, and G.I. Shulman Increased glucose transport-phosphorylation and muscle glycogen synthesis after exercise training in insulin-resistant subjects N. Engl. J. Med. 335 1996 1357 1362
134. K.F. Petersen, K. Morino, T.C. Alves, R.G. Kibbey, S. Dufour, S. Sono, P.S. Yoo, G.W. Cline, and G.I. Shulman Effect of aging on muscle mitochondrial substrate utilization in humans Proc. Natl. Acad. Sci. USA 112 2015 11330 11334
135. J.K. Petrella, J.S. Kim, S.C. Tuggle, S.R. Hall, and M.M. Bamman Age differences in knee extension power, contractile velocity, and fatigability J. Appl. Physiol. 98 2005 211 220
136. J.K. Petrella, J.S. Kim, D.L. Mayhew, J.M. Cross, and M.M. Bamman Potent myofiber hypertrophy during resistance training in humans is associated with satellite cell-mediated myonuclear addition: a cluster analysis J. Appl. Physiol. 104 2008 1736 1742
137. A.H. Pham, J.M. McCaffery, and D.C. Chan Mouse lines with photo-activatable mitochondria to study mitochondrial dynamics Genesis 50 2012 833 843
138. S.K. Phillips, K.M. Rook, N.C. Siddle, S.A. Bruce, and R.C. Woledge Muscle weakness in women occurs at an earlier age than in men, but strength is preserved by hormone replacement therapy Clin. Sci. 84 1993 95 98
139. M. Picard, D. Ritchie, K.J. Wright, C. Romestaing, M.M. Thomas, S.L. Rowan, T. Taivassalo, and R.T. Hepple Mitochondrial functional impairment with aging is exaggerated in isolated mitochondria compared to permeabilized myofibers Aging Cell 9 2010 1032 1046
140. M. Picard, D. Ritchie, M.M. Thomas, K.J. Wright, and R.T. Hepple Alterations in intrinsic mitochondrial function with aging are fiber type-specific and do not explain differential atrophy between muscles Aging Cell 10 2011 1047 1055
141. M. Picard, T. Taivassalo, G. Gouspillou, and R.T. Hepple Mitochondria: isolation, structure and function J. Physiol. 589 2011 4413 4421
142. M. Picard, T. Taivassalo, D. Ritchie, K.J. Wright, M.M. Thomas, C. Romestaing, and R.T. Hepple Mitochondrial structure and function are disrupted by standard isolation methods PLoS ONE 6 2011 e18317
143. S.J. Prior, A.P. Goldberg, H.K. Ortmeyer, E.R. Chin, D. Chen, J.B. Blumenthal, and A.S. Ryan Increased skeletal muscle capillarization independently enhances insulin sensitivity in older adults after exercise training and detraining Diabetes 64 2015 3386 3395
144. U. Raue, D. Slivka, K. Minchev, and S. Trappe Improvements in whole muscle and myocellular function are limited with high-intensity resistance training in octogenarian women J. Appl. Physiol. 106 2009 1611 1617
145. K.F. Reid, and R.A. Fielding Skeletal muscle power: a critical determinant of physical functioning in older adults Exerc. Sport Sci. Rev. 40 2012 4 12
146. E.A. Richter, and M. Hargreaves Exercise, GLUT4, and skeletal muscle glucose uptake Physiol. Rev. 93 2013 993 1017
147. M.A. Rogers, J.M. Hagberg, W.H. Martin 3rd, A.A. Ehsani, and J.O. Holloszy Decline in VO2max with aging in master athletes and sedentary men J. Appl. Physiol. 68 1990 2195 2199
148. M.A. Rogers, D.S. King, J.M. Hagberg, A.A. Ehsani, and J.O. Holloszy Effect of 10 days of physical inactivity on glucose tolerance in master athletes J. Appl. Physiol. 68 1990 1833 1837
149. V. Romanello, E. Guadagnin, L. Gomes, I. Roder, C. Sandri, Y. Petersen, G. Milan, E. Masiero, P. Del Piccolo, M. Foretz, and et al. Mitochondrial fission and remodelling contributes to muscle atrophy EMBO J. 29 2010 1774 1785
150. I.H. Rosenberg Sarcopenia: origins and clinical relevance J. Nutr. 127 Suppl 1997 990S 991S
151. S.L. Rowan, K. Rygiel, F.M. Purves-Smith, N.M. Solbak, D.M. Turnbull, and R.T. Hepple Denervation causes fiber atrophy and myosin heavy chain co-expression in senescent skeletal muscle PLoS ONE 7 2012 e29082
152. J.W. Rowe, K.L. Minaker, J.A. Pallotta, and J.S. Flier Characterization of the insulin resistance of aging J. Clin. Invest. 71 1983 1581 1587
153. C.E. Schaar, D.J. Dues, K.K. Spielbauer, E. Machiela, J.F. Cooper, M. Senchuk, S. Hekimi, and J.M. Van Raamsdonk Mitochondrial and cytoplasmic ROS have opposing effects on lifespan PLoS Genet. 11 2015 e1004972
154. G.G. Schweitzer, E.B. Arias, and G.D. Cartee Sustained postexercise increases in AS160 Thr642 and Ser588 phosphorylation in skeletal muscle without sustained increases in kinase phosphorylation J. Appl. Physiol. 113 2012 1852 1861
155. N. Sharma, E.B. Arias, M.P. Sajan, J.G. MacKrell, A.D. Bhat, R.V. Farese, and G.D. Cartee Insulin resistance for glucose uptake and Akt2 phosphorylation in the soleus, but not epitrochlearis, muscles of old vs. adult rats J. Appl. Physiol. 108 2010 1631 1640
156. N. Sharma, H. Wang, E.B. Arias, C.M. Castorena, and G.D. Cartee Mechanisms for independent and combined effects of calorie restriction and acute exercise on insulin-stimulated glucose uptake by skeletal muscle of old rats Am. J. Physiol. Endocrinol. Metab. 308 2015 E603 E612
157. K.R. Short, J.L. Vittone, M.L. Bigelow, D.N. Proctor, R.A. Rizza, J.M. Coenen-Schimke, and K.S. Nair Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity Diabetes 52 2003 1888 1896
158. K.R. Short, M.L. Bigelow, J. Kahl, R. Singh, J. Coenen-Schimke, S. Raghavakaimal, and K.S. Nair Decline in skeletal muscle mitochondrial function with aging in humans Proc. Natl. Acad. Sci. USA 102 2005 5618 5623
159. D. Skorjanc, G. Dünstl, and D. Pette Mitochondrial enzyme defects in normal and low-frequency-stimulated muscles of young and aging rats J. Gerontol. A Biol. Sci. Med. Sci. 56 2001 B503 B509
160. D. Slivka, U. Raue, C. Hollon, K. Minchev, and S. Trappe 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. 295 2008 R273 R280
161. J.R. Speakman, D.A. Talbot, C. Selman, S. Snart, J.S. McLaren, P. Redman, E. Krol, D.M. Jackson, M.S. Johnson, and M.D. Brand Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer Aging Cell 3 2004 87 95
162. M.J. Stec, D.L. Mayhew, and M.M. Bamman The effects of age and resistance loading on skeletal muscle ribosome biogenesis J. Appl. Physiol. 119 2015 851 857
163. M.J. Stec, N.A. Kelly, G.M. Many, S.T. Windham, S.C. Tuggle, and M.M. Bamman Ribosome biogenesis may augment resistance training-induced myofiber hypertrophy and is required for myotube growth in vitro Am. J. Physiol. Endocrinol. Metab. 310 2016 E652 E661
164. M. Tonkonogi, M. Fernström, B. Walsh, L.L. Ji, O. Rooyackers, F. Hammarqvist, J. Wernerman, and K. Sahlin Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans Pflugers Arch. 446 2003 261 269
165. E.Q. Toyama, S. Herzig, J. Courchet, T.L. Lewis Jr., O.C. Losón, K. Hellberg, N.P. Young, H. Chen, F. Polleux, D.C. Chan, and R.J. Shaw Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress Science 351 2016 275 281
166. J.T. Treebak, C. Frøsig, C. Pehmøller, S. Chen, S.J. Maarbjerg, N. Brandt, C. MacKintosh, J.R. Zierath, D.G. Hardie, B. Kiens, and et al. Potential role of TBC1D4 in enhanced post-exercise insulin action in human skeletal muscle Diabetologia 52 2009 891 900
167. J.D. van der Berg, C.D. Stehouwer, H. Bosma, J.H. van der Velde, P.J. Willems, H.H. Savelberg, M.T. Schram, S.J. Sep, C.J. van der Kallen, R.M. Henry, and et al. Associations of total amount and patterns of sedentary behaviour with type 2 diabetes and the metabolic syndrome: The Maastricht Study Diabetologia 59 2016 709 718
168. H. Wallberg-Henriksson, S.H. Constable, D.A. Young, and J.O. Holloszy Glucose transport into rat skeletal muscle: interaction between exercise and insulin J. Appl. Physiol. 65 1988 909 913
169. X. Wang, B.W. Patterson, G.I. Smith, J. Kampelman, D.N. Reeds, S.A. Sullivan, and B. Mittendorfer A ∼60-min brisk walk increases insulin-stimulated glucose disposal but has no effect on hepatic and adipose tissue insulin sensitivity in older women J. Appl. Physiol. 114 2013 1563 1568
170. P.E. Willis, S.G. Chadan, V. Baracos, and W.S. Parkhouse Restoration of insulin-like growth factor I action in skeletal muscle of old mice Am. J. Physiol. 275 1998 E525 E530
171. R.R. Wing, R.F. Hamman, G.A. Bray, L. Delahanty, S.L. Edelstein, J.O. Hill, E.S. Horton, M.A. Hoskin, A. Kriska, J. Lachin, et al. Diabetes Prevention Program Research Group Achieving weight and activity goals among diabetes prevention program lifestyle participants Obes. Res. 12 2004 1426 1434
172. J.F. Wojtaszewski, B.F. Hansen, B. Kiens, and E.A. Richter Insulin signaling in human skeletal muscle: time course and effect of exercise Diabetes 46 1997 1775 1781
173. J.F. Wojtaszewski, Y. Higaki, M.F. Hirshman, M.D. Michael, S.D. Dufresne, C.R. Kahn, and L.J. Goodyear Exercise modulates postreceptor insulin signaling and glucose transport in muscle-specific insulin receptor knockout mice J. Clin. Invest. 104 1999 1257 1264
174. J.F. Wojtaszewski, B.F. Hansen, Gade, B. Kiens, J.F. Markuns, L.J. Goodyear, and E.A. Richter Insulin signaling and insulin sensitivity after exercise in human skeletal muscle Diabetes 49 2000 325 331
175. Y. Xiao, N. Sharma, E.B. Arias, C.M. Castorena, and G.D. Cartee A persistent increase in insulin-stimulated glucose uptake by both fast-twitch and slow-twitch skeletal muscles after a single exercise session by old rats Age (Dordr.) 35 2013 573 582
176. A. Young, and D.A. Skelton Applied physiology of strength and power in old age Int. J. Sports Med. 15 1994 149 151
177. J.C. Young, M. Chen, and J.O. Holloszy Maintenance of the adaptation of skeletal muscle mitochondria to exercise in old rats Med. Sci. Sports Exerc. 15 1983 243 246
178. J.R. Zierath, and H. Wallberg-Henriksson Looking ahead perspective: where will the future of exercise biology take us? Cell Metab. 22 2015 25 30