The impact of old age on skeletal muscle energetics: Supply and demand

Current Aging Science

Volumn 4, Issue 3, 2011, Pages 234-247

  Russ, David W ^a   Lanza, Ian R ^b  

^a OHIO UNIVERSITY   (United States)

^b Mayo Clinic   (United States)

Author keywords

ATPase; Fatigue; Glycolysis; Mitochondria; Oxidative phosphorylation; SERCA

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE; GLUCOSE; MESSENGER RNA; MITOCHONDRIAL DNA; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN METABOLITE;

AGING; ANAEROBIC GLYCOLYSIS; BIOENERGY; CALORIC RESTRICTION; COPY NUMBER VARIATION; ENERGY METABOLISM; ENERGY RESOURCE; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HUMAN; IMMOBILIZATION; MITOCHONDRION; MORBIDITY; OXIDATIVE PHOSPHORYLATION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; QUALITY OF LIFE; REVIEW; SKELETAL MUSCLE;

EID: 82955246276     PISSN: 18746098     EISSN: 18746128     Source Type: Journal    
DOI: 10.2174/1874609811104030234     Document Type: Review

References (196)

1. Meyer RA, Foley JM. Cellular processes integrating the metabolic response to exercise. In: Handbook of Physiology Exercise: Regulation and Integration of Multiple Systems. Bethesda, MD, USA: American Physiological Society 1996. pp. 841-69.
2. Kent-Braun JA, Ng AV, Doyle JW, Towse TF. Human skeletal muscle responses vary with age and gender during fatigue due to incremental isometric exercise. J Appl Physiol 2002; 93 (5): 1813-23.
3. Walter G, Vandenborne K, Elliott M, Leigh JS. In vivo ATP synthesis rates in single human muscles during high intensity exercise. J Physiol 1999; 519 Pt 3: 901-10.
4. Grimby G, Aniansson A, Hedberg M, Henning GB, Grangard U, Kvist H. Training can improve muscle strength and endurance in 78-to 84-yr-old men. J Appl Physiol 1992; 73 (6): 2517-23.
5. Larsson L, Sjodin B, Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22--65 years. Acta Physiol Scand 1978; 103 (1): 31-9.
6. Pastoris O, Boschi F, Verri M, Baiardi P, Felzani G, Vecchiet J, et al. The effects of aging on enzyme activities and metabolite concentrations in skeletal muscle from sedentary male and female subjects. Exp Gerontol 2000; 35 (1): 95-104.
7. Kaczor JJ, Ziolkowski W, Antosiewicz J, Hac S, Tarnopolsky MA, Popinigis J. The effect of aging on anaerobic and aerobic enzyme activities in human skeletal muscle. J Gerontol A Biol Sci Med Sci 2006; 61 (4): 339-44.
8. Essen-Gustavsson B, Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 1986; 126 (1): 107-14.
9. Grimby G. Muscle performance and structure in the elderly as studied cross-sectionally and longitudinally. J Gerontol A Biol Sci Med Sci 1995; 50 (Spec No): 17-22.
10. Campbell CB, Marsh DR, Spriet LL. Anaerobic energy provision in aged skeletal muscle during tetanic stimulation. J Appl Physiol 1991; 70 (4): 1787-95.
11. Hepple RT, Hagen JL, Krause DJ, Baker DJ. Skeletal muscle aging in F344BN F1-hybrid rats: II. Improved contractile economy in senescence helps compensate for reduced ATP-generating capacity. J Gerontol A Biol Sci Med Sci 2004; 59 (11): 1111-9.
12. Boska M. ATP production rates as a function of force level in the human gastrocnemius/soleus using 31P MRS. Magn Reson Med 1994; 32 (1): 1-10.
13. Crowther GJ, Jubrias SA, Gronka RK, Conley KE. A "functional biopsy" of muscle properties in sprinters and distance runners. Med Sci Sports Exerc 2002; 34 (11): 1719-24.
14. Kemp GJ, Radda GK. Quantitative interpretation of bioenergetic data from 31P and 1H magnetic resonance spectroscopic studies of skeletal muscle: an analytical review. Magn Reson Q 1994; 10 (1): 43-63.
15. Lanza IR, Befroy DE, Kent-Braun JA. Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J Appl Physiol 2005; 99 (5): 1736-44.
16. Lanza IR, Larsen RG, Kent-Braun JA. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J Physiol 2007; 583 (Pt 3): 1093-105.
17. Grimby G, Saltin B. Physiological analysis of physically welltrained middle-aged and old athletes. Acta Med Scand 1966; 179 (5): 513-26.
18. Rogers MA, Hagberg JM, Martin WH, 3rd, Ehsani AA, Holloszy JO. Decline in VO2max with aging in master athletes and sedentary men. J Appl Physiol 1990; 68 (5): 2195-9.
19. Short KR, Bigelow ML, Kahl J, Singh R, Coenen-Schimke J, Raghavakaimal S, et al. Decline in skeletal muscle mitochondrial function with aging in humans. Proc Natl Acad Sci USA 2005; 102 (15): 5618-23.
20. Conley KE, Jubrias SA, Esselman PC. Oxidative capacity and ageing in human muscle. J Physiol 2000; 526 (Pt 1): 203-10.
21. McCully KK, Fielding RA, Evans WJ, Leigh JS, Jr., Posner JD. Relationships between in vivo and in vitro measurements of metabolism in young and old human calf muscles. J Appl Physiol 1993; 75 (2): 813-9.
22. McCully KK, Forciea MA, Hack LM, Donlon E, Wheatley RW, Oatis CA, et al. Chance B. Muscle metabolism in older subjects using 31P magnetic resonance spectroscopy. Can J Physiol Pharmacol 1991; 69 (5): 576-80.
23. Petersen KF, Befroy D, Dufour S, Dziura J, Ariyan C, Rothman DL, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science 2003; 300 (5622): 1140-2.
24. Barazzoni R, Short KR, Nair KS. 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 (5): 3343-7.
25. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, et al. Endurance exercise as a countermeasure for aging. Diabetes 2008; 57 (11): 2933-42.
26. Menshikova EV, Ritov VB, Fairfull L, Ferrell RE, Kelley DE, Goodpaster BH. Effects of exercise on mitochondrial content and function in aging human skeletal muscle. J Gerontol A Biol Sci Med Sci 2006; 61 (6): 534-40.
27. Welle S, Bhatt K, Shah B, Needler N, Delehanty JM, Thornton CA. Reduced amount of mitochondrial DNA in aged human muscle. J Appl Physiol 2003; 94 (4): 1479-84.
28. Houmard JA, Weidner ML, Gavigan KE, Tyndall GL, Hickey MS, Alshami A. Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J Appl Physiol 1998; 85 (4): 1337-41.
29. 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 U S A 1996; 93 (26): 15364-9.
30. Welle S, Bhatt K, Thornton CA. High-abundance mRNAs in human muscle: comparison between young and old. J Appl Physiol 2000; 89 (1): 297-304.
31. Tonkonogi M, Fernstrom M, Walsh B, Ji LL, Rooyackers O, Hammarqvist F, et al. Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans. Pflugers Arch 2003; 446 (2): 261-9.
32. 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 1994; 1226 (1): 73-82.
33. Trounce I, Byrne E, Marzuki S. Decline in skeletal muscle mitochondrial respiratory chain function: possible factor in ageing. Lancet 1989; 1 (8639): 637-9.
34. Rasmussen UF, Krustrup P, Kjaer M, Rasmussen HN. Experimental evidence against the mitochondrial theory of aging. A study of isolated human skeletal muscle mitochondria. Exp Gerontol 2003; 38 (8): 877-86.
35. Rasmussen UF, Krustrup P, Kjaer M, Rasmussen HN. Human skeletal muscle mitochondrial metabolism in youth and senescence: no signs of functional changes in ATP formation and mitochondrial oxidative capacity. Pflugers Arch 2003; 446 (2): 270-8.
36. Hutter E, Skovbro M, Lener B, Prats C, Rabol R, Dela F, et al. Oxidative stress and mitochondrial impairment can be separated from lipofuscin accumulation in aged human skeletal muscle. Aging Cell 2007; 6 (2): 245-56.
37. Chance B, Eleff S, Leigh JS, Jr. Noninvasive, nondestructive approaches to cell bioenergetics. Proc Natl Acad Sci U S A 1980; 77 (12): 7430-4.
38. Chilibeck PD, McCreary CR, Marsh GD, Paterson DH, Noble EG, Taylor AW, et al. Evaluation of muscle oxidative potential by 31PMRS during incremental exercise in old and young humans. Eur J Appl Physiol Occup Physiol 1998; 78 (5): 460-5.
39. Kent-Braun JA, Ng AV. Skeletal muscle oxidative capacity in young and older women and men. J Appl Physiol 2000; 89 (3): 1072-8.
40. Taylor DJ, Kemp GJ, Thompson CH, Radda GK. Ageing: effects on oxidative function of skeletal muscle in vivo. Mol Cell Biochem 1997; 174 (1-2): 321-4.
41. Russ DW, Kent-Braun JA. Is skeletal muscle oxidative capacity decreased in old age? Sports Med 2004; 34 (4): 221-9.
42. Lee S, Jeong SY, Lim WC, Kim S, Park YY, Sun X, et al. Mitochondrial fission and fusion mediators, hFis1 and OPA1, modulate cellular senescence. J Biol Chem 2007; 282 (31): 22977-83.
43. Calleja M, Pena P, Ugalde C, Ferreiro C, Marco R, Garesse R. Mitochondrial DNA remains intact during Drosophila aging, but the levels of mitochondrial transcripts are significantly reduced. J Biol Chem 1993; 268 (25): 18891-7.
44. Michikawa Y, Mazzucchelli F, Bresolin N, Scarlato G, Attardi G. Aging-dependent large accumulation of point mutations in the human mtDNA control region for replication. Science 1999; 286 (5440): 774-9.
45. Henderson GC, Dhatariya K, Ford GC, Klaus KA, Basu R, Rizza RA, et al. Higher muscle protein synthesis in women than men across the lifespan, and failure of androgen administration to amend age-related decrements. FASEB J 2009; 23 (2): 631-41.
46. Bota DA, Van Remmen H, Davies KJ. Modulation of Lon protease activity and aconitase turnover during aging and oxidative stress. FEBS Lett 2002; 532 (1-2): 103-6.
47. Hepple RT, Qin M, Nakamoto H, Goto S. Caloric restriction optimizes the proteasome pathway with aging in rat plantaris muscle: implications for sarcopenia. Am J Physiol Regul Integr Comp Physiol 2008; 295 (4): R1231-7.
48. Fugere NA, Ferrington DA, Thompson LV. Protein nitration with aging in the rat semimembranosus and soleus muscles. J Gerontol A Biol Sci Med Sci 2006; 61 (8): 806-12.
49. Herndon LA, Schmeissner PJ, Dudaronek JM, Brown PA, Listner KM, Sakano Y, et al. Stochastic and genetic factors influence tissue-specific decline in ageing C. elegans. Nature 2002; 419 (6909): 808-14.
50. Holloszy JO. Mortality rate and longevity of food-restricted exercising male rats: a reevaluation. J Appl Physiol 1997; 82 (2): 399-403.
51. Black AE, Coward WA, Cole TJ, Prentice AM. Human energy expenditure in affluent societies: an analysis of 574 doubly-labelled water measurements. Eur J Clin Nutr 1996; 50 (2): 72-92.
52. Barrientos A, Casademont J, Rotig A, Miro O, Urbano-Marquez A, Rustin P, 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 (2): 536-9.
53. Brierley EJ, Johnson MA, James OF, Turnbull DM. Effects of physical activity and age on mitochondrial function. QJM 1996; 89 (4): 251-8.
54. Meredith CN, Frontera WR, Fisher EC, Hughes VA, Herland JC, Edwards J, et al. Peripheral effects of endurance training in young and old subjects. J Appl Physiol 1989; 66 (6): 2844-9.
55. Levine JA, Lanningham-Foster LM, McCrady SK, Krizan AC, Olson LR, Kane PH, et al. Interindividual variation in posture allocation: possible role in human obesity. Science 2005; 307 (5709): 584-6.
56. Nair KS. Aging muscle. Am J Clin Nutr 2005; 81 (5): 953-63.
57. Coggan AR, Spina RJ, King DS, Rogers MA, Brown M, Nemeth PM, et al. Skeletal muscle adaptations to endurance training in 60-to 70-yr-old men and women. J Appl Physiol 1992; 72 (5): 1780-6.
58. Short KR, Vittone JL, Bigelow ML, Proctor DN, Rizza RA, Coenen-Schimke JM, et al. Impact of aerobic exercise training on age-related changes in insulin sensitivity and muscle oxidative capacity. Diabetes 2003; 52 (8): 1888-96.
59. Jubrias SA, Esselman PC, Price LB, Cress ME, Conley KE. Large energetic adaptations of elderly muscle to resistance and endurance training. J Appl Physiol 2001; 90 (5): 1663-70.
60. Balagopal P, Schimke JC, Ades P, Adey D, Nair KS. Age effect on transcript levels and synthesis rate of muscle MHC and response to resistance exercise. Am J Physiol Endocrinol Metab 2001; 280 (2): E203-8.
61. Proctor DN, Sinning WE, Walro JM, Sieck GC, Lemon PW. Oxidative capacity of human muscle fiber types: effects of age and training status. J Appl Physiol 1995; 78 (6): 2033-8.
62. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, et al. AMPK and PPARdelta agonists are exercise mimetics. Cell 2008; 134 (3): 405-15.
63. Goodyear LJ. The exercise pill--too good to be true? N Engl J Med 2008; 359 (17): 1842-4.
64. Desai VG, Weindruch R, Hart RW, Feuers RJ. Influences of age and dietary restriction on gastrocnemius electron transport system activities in mice. Arch Biochem Biophys 1996; 333 (1): 145-51.
65. Hepple RT, Baker DJ, McConkey M, Murynka T, Norris R. Caloric restriction protects mitochondrial function with aging in skeletal and cardiac muscles. Rejuvenation Res 2006; 9 (2): 219-22.
66. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME. Effects of short-and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol Endocrinol Metab 2004; 286 (5): E852-61.
67. Lass A, Sohal BH, Weindruch R, Forster MJ, Sohal RS. Caloric restriction prevents age-associated accrual of oxidative damage to mouse skeletal muscle mitochondria. Free Radic Biol Med 1998; 25 (9): 1089-97.
68. Haigis MC, Guarente LP. Mammalian sirtuins--emerging roles in physiology, aging, and calorie restriction. Genes Dev 2006; 20 (21): 2913-21.
69. Lin SJ, Ford E, Haigis M, Liszt G, Guarente L. Calorie restriction extends yeast life span by lowering the level of NADH. Genes Dev 2004; 18 (1): 12-6.
70. Bordone L, Guarente L. Calorie restriction, SIRT1 and metabolism: understanding longevity. Nat Rev Mol Cell Biol 2005; 6 (4): 298-305.
71. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci U S A 2008; 105 (9): 3374-9.
72. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005; 434 (7029): 113-8.
73. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, Milne JC, et al. Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 2008; 8 (5): 347-58.
74. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, Wood JG, et al. Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 2003; 425 (6954): 191-6.
75. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, et al. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 2007; 450 (7170): 712-6.
76. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, et al. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 2007; 4 (3): e76.
77. Boirie Y, Short KR, Ahlman B, Charlton M, Nair KS. Tissuespecific regulation of mitochondrial and cytoplasmic protein synthesis rates by insulin. Diabetes 2001; 50 (12): 2652-8.
78. Stump CS, Short KR, Bigelow ML, Schimke JM, Nair KS. Effect of insulin on human skeletal muscle mitochondrial ATP production, protein synthesis, and mRNA transcripts. Proc Natl Acad Sci U S A 2003; 100 (13): 7996-8001.
79. Karakelides H, Asmann YW, Bigelow ML, Short KR, Dhatariya K, Coenen-Schimke J, et al. Effect of insulin deprivation on muscle mitochondrial ATP production and gene transcript levels in type 1 diabetic subjects. Diabetes 2007; 56 (11): 2683-9.
80. Paradies G, Ruggiero FM. Effect of hyperthyroidism on the transport of pyruvate in rat-heart mitochondria. Biochim Biophys Acta 1988; 935 (1): 79-86.
81. Paradies G, Ruggiero FM, Petrosillo G, Quagliariello E. Enhanced cytochrome oxidase activity and modification of lipids in heart mitochondria from hyperthyroid rats. Biochim Biophys Acta 1994; 1225 (2): 165-70.
82. Goldenthal MJ, Weiss HR, Marin-Garcia J. Bioenergetic remodeling of heart mitochondria by thyroid hormone. Mol Cell Biochem 2004; 265 (1-2): 97-106.
83. Wooten WL, Cascarano J. The effect of thyroid hormone on mitochondrial biogenesis and cellular hyperplasia. J Bioenerg Biomembr 1980; 12 (1-2): 1-12.
84. Short KR, Nygren J, Barazzoni R, Levine J, Nair KS. T(3) increases mitochondrial ATP production in oxidative muscle despite increased expression of UCP2 and-3. Am J Physiol Endocrinol Metab 2001; 280 (5): E761-9.
85. Short KR, Nygren J, Nair KS. Effect of T(3)-induced hyperthyroidism on mitochondrial and cytoplasmic protein synthesis rates in oxidative and glycolytic tissues in rats. Am J Physiol Endocrinol Metab 2007; 292 (2): E642-7.
86. Wiesner RJ, Kurowski TT, Zak R. Regulation by thyroid hormone of nuclear and mitochondrial genes encoding subunits of cytochrome-c oxidase in rat liver and skeletal muscle. Mol Endocrinol 1992; 6 (9): 1458-67.
87. Short KR, Moller N, Bigelow ML, Coenen-Schimke J, Nair KS. Enhancement of muscle mitochondrial function by growth hormone. J Clin Endocrinol Metab 2008; 93 (2): 597-604.
88. Bentinger M, Dallner G, Chojnacki T, Swiezewska E. Distribution and breakdown of labeled coenzyme Q10 in rat. Free Radic Biol Med 2003; 34 (5): 563-75.
89. Zhang Y, Aberg F, Appelkvist EL, Dallner G, Ernster L. Uptake of dietary coenzyme Q supplement is limited in rats. J Nutr 1995; 125 (3): 446-53.
90. Sohal RS, Kamzalov S, Sumien N, Ferguson M, Rebrin I, Heinrich KR, et al. Effect of coenzyme Q10 intake on endogenous coenzyme Q content, mitochondrial electron transport chain, antioxidative defenses, and life span of mice. Free Radic Biol Med 2006; 40 (3): 480-7.
91. Koopman R, Verdijk L, Manders RJ, Gijsen AP, Gorselink M, Pijpers E, et al. Co-ingestion of protein and leucine stimulates muscle protein synthesis rates to the same extent in young and elderly lean men. Am J Clin Nutr 2006; 84 (3): 623-32.
92. Volpi E, Ferrando AA, Yeckel CW, Tipton KD, Wolfe RR. Exogenous amino acids stimulate net muscle protein synthesis in the elderly. J Clin Invest 1998; 101 (9): 2000-7.
93. Tatpati LL, Irving BA, Tom A, Bigelow ML, Klaus K, Short KR, et al. The effect of branched chain amino acids on skeletal muscle mitochondrial function in young and elderly adults. J Clin Endocrinol Metab 2010; 95 (2): 894-902.
94. Wray DW, Nishiyama SK, Monnet A, Wary C, Duteil SS, Carlier PG, et al. Antioxidants and aging: NMR-based evidence of improved skeletal muscle perfusion and energetics. Am J Physiol Heart Circ Physiol 2009; 297 (5): H1870-5.
95. Ristow M, Zarse K, Oberbach A, Kloting N, Birringer M, Kiehntopf M, et al. Antioxidants prevent health-promoting effects of physical exercise in humans. Proc Natl Acad Sci U S A 2009; 106 (21): 8665-70.
96. Chanseaume E, Bielicki G, Tardy AL, Renou JP, Freyssenet D, Boirie Y, et al. Impaired resting muscle energetics studied by (31)P-NMR in diet-induced obese rats. Obesity (Silver Spring) 2008; 16 (3): 572-7.
97. Meyer RA, Brown TR, Kushmerick MJ. Phosphorus nuclear magnetic resonance of fast-and slow-twitch muscle. Am J Physiol 1985; 248 (3 Pt 1): C279-87.
98. van Pelt RE, Dinneno FA, Seals DR, Jones PP. Age-related decline in RMR in physically active men: relation to exercise volume and energy intake. Am J Physiol Endocrinol Metab 2001; 281 (3): E633-9.
99. Crow MT, Kushmerick MJ. Chemical energetics of slow-and fasttwitch muscles of the mouse. J Gen Physiol 1982; 79 (1): 147-66.
100. Szentesi P, Zaremba R, van Mechelen W, Stienen GJ. ATP utilization for calcium uptake and force production in different types of human skeletal muscle fibres. J Physiol 2001; 531 (Pt 2): 393-403.
101. Narayanan N, Jones DL, Xu A, Yu JC. Effects of aging on sarcoplasmic reticulum function and contraction duration in skeletal muscles of the rat. Am J Physiol 1996; 271 (4 Pt 1): C1032-40.
102. Lowe DA, Husom AD, Ferrington DA, Thompson LV. Myofibrillar myosin ATPase activity in hindlimb muscles from young and aged rats. Mech Ageing Dev 2004; 125 (9): 619-27.
103. Horska A, Fishbein KW, Fleg JL, Spencer RG. The relationship between creatine kinase kinetics and exercise intensity in human forearm is unchanged by age. Am J Physiol Endocrinol Metab 2000; 279 (2): E333-9.
104. Ryschon TW, Fowler MD, Wysong RE, Anthony A, Balaban RS. Efficiency of human skeletal muscle in vivo: comparison of isometric, concentric, and eccentric muscle action. J Appl Physiol 1997; 83 (3): 867-74.
105. Menard MR, Penn AM, Lee JW, Dusik LA, Hall LD. Relative metabolic efficiency of concentric and eccentric exercise determined by 31P magnetic resonance spectroscopy. Arch Phys Med Rehabil 1991; 72 (12): 976-83.
106. Beltman JG, van der Vliet MR, Sargeant AJ, de Haan A. Metabolic cost of lengthening, isometric and shortening contractions in maximally stimulated rat skeletal muscle. Acta Physiol Scand 2004; 182 (2): 179-87.
107. Rall JA. Sense and nonsense about the Fenn effect. Am J Physiol 1982; 242 (1): H1-6.
108. Buschman HP, Elzinga G, Woledge RC. Energetics of shortening depend on stimulation frequency in single muscle fibres from Xenopus laevis at 20 degrees C. Pflugers Arch 1995; 430 (2): 160-7.
109. Wang Y, Kerrick WG. The off rate of Ca(2+) from troponin C is regulated by force-generating cross bridges in skeletal muscle. J Appl Physiol 2002; 92 (6): 2409-18.
110. Fitts RH, McDonald KS, Schluter JM. The determinants of skeletal muscle force and power: their adaptability with changes in activity pattern. J Biomech 1991; 24 (Suppl 1): 111-22.
111. Geiger PC, Cody MJ, Macken RL, Bayrd ME, Fang YH, Sieck GC. Mechanisms underlying increased force generation by rat diaphragm muscle fibers during development. J Appl Physiol 2001; 90 (1): 380-8.
112. Geiger PC, Cody MJ, Macken RL, Sieck GC. Maximum specific force depends on myosin heavy chain content in rat diaphragm muscle fibers. J Appl Physiol 2000; 89 (2): 695-703.
113. Abbate F, De Ruiter CJ, Offringa C, Sargeant AJ, De Haan A. In situ rat fast skeletal muscle is more efficient at submaximal than at maximal activation levels. J Appl Physiol 2002; 92 (5): 2089-96.
114. Bottinelli R, Canepari M, Reggiani C, Stienen GJ. Myofibrillar ATPase activity during isometric contraction and isomyosin composition in rat single skinned muscle fibres. J Physiol 1994; 481 (Pt 3): 663-75.
115. Hilber K, Sun YB, Irving M. Effects of sarcomere length and temperature on the rate of ATP utilisation by rabbit psoas muscle fibres. J Physiol 2001; 531 (Pt 3): 771-80.
116. Kushmerick MJ, Krasner B. Force and ATPase rate in skinned skeletal muscle fibers. Fed Proc 1982; 41 (7): 2232-7.
117. Stienen GJ, Zaremba R, Elzinga G. ATP utilization for calcium uptake and force production in skinned muscle fibres of Xenopus laevis. J Physiol 1995; 482 (Pt 1): 109-22.
118. Han YS, Geiger PC, Cody MJ, Macken RL, Sieck GC. ATP consumption rate per cross bridge depends on myosin heavy chain isoform. J Appl Physiol 2003; 94 (6): 2188-96.
119. He ZH, Bottinelli R, Pellegrino MA, Ferenczi MA, Reggiani C. ATP consumption and efficiency of human single muscle fibers with different myosin isoform composition. Biophys J 2000; 79 (2): 945-61.
120. Rivero JL, Talmadge RJ, Edgerton VR. Interrelationships of myofibrillar ATPase activity and metabolic properties of myosin heavy chain-based fibre types in rat skeletal muscle. Histochem Cell Biol 1999; 111 (4): 277-87.
121. Stienen GJ, Kiers JL, Bottinelli R, Reggiani C. Myofibrillar ATPase activity in skinned human skeletal muscle fibres: fibre type and temperature dependence. J Physiol 1996; 493 (Pt 2): 299-307.
122. Bodine SC, Roy RR, Eldred E, Edgerton VR. Maximal force as a function of anatomical features of motor units in the cat tibialis anterior. J Neurophysiol 1987; 57 (6): 1730-45.
123. Harridge SD, Bottinelli R, Canepari M, Pellegrino MA, Reggiani C, Esbjornsson M, et al. Whole-muscle and single-fibre contractile properties and myosin heavy chain isoforms in humans. Pflugers Arch 1996; 432 (5): 913-20.
124. Hunter GR, Newcomer BR, Larson-Meyer DE, Bamman MM, Weinsier RL. Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 2001; 24 (5): 654-61.
125. Abbate F, Van Der Velden J, Stienen GJ, De Haan A. Post-tetanic potentiation increases energy cost to a higher extent than work in rat fast skeletal muscle. J Muscle Res Cell Motil 2001; 22 (8): 703-10.
126. Baker AJ, Brandes R, Schendel TM, Trocha SD, Miller RG, Weiner MW. Energy use by contractile and noncontractile processes in skeletal muscle estimated by 31P-NMR. Am J Physiol 1994; 266 (3 Pt 1): C825-31.
127. Barclay CJ. Mechanical efficiency and fatigue of fast and slow muscles of the mouse. J Physiol 1996; 497 (Pt 3): 781-94.
128. Barclay CJ, Lichtwark GA, Curtin NA. The energetic cost of activation in mouse fast-twitch muscle is the same whether measured using reduced filament overlap or N-benzyl-ptoluenesulphonamide. Acta Physiol (Oxf) 2008; 193 (4): 381-91.
129. Homsher E. Muscle enthalpy production and its relationship to actomyosin ATPase. Annu Rev Physiol 1987; 49: 673-90.
130. Walsh B, Howlett RA, Stary CM, Kindig CA, Hogan MC. Measurement of activation energy and oxidative phosphorylation onset kinetics in isolated muscle fibers in the absence of crossbridge cycling. Am J Physiol Regul Integr Comp Physiol 2006; 290 (6): R1707-13.
131. Zhang SJ, Andersson DC, Sandstrom ME, Westerblad H, Katz A. Cross bridges account for only 20% of total ATP consumption during submaximal isometric contraction in mouse fast-twitch skeletal muscle. Am J Physiol Cell Physiol 2006; 291 (1): C147-54.
132. Carroll SL, Klein MG, Schneider MF. Decay of calcium transients after electrical stimulation in rat fast-and slow-twitch skeletal muscle fibres. J Physiol 1997; 501 (Pt 3): 573-88.
133. Eisenberg BR. Quantitative Ultrastructure of Mammalian Skeletal Muscle. Baltimore, M.D.: American Physiololgical Society, 1983.
134. Wu KD, Lytton J. Molecular cloning and quantification of sarcoplasmic reticulum Ca(2+)-ATPase isoforms in rat muscles. Am J Physiol 1993; 264 (2 Pt 1): C333-41.
135. Lytton J, Westlin M, Burk SE, Shull GE, MacLennan DH. Functional comparisons between isoforms of the sarcoplasmic or endoplasmic reticulum family of calcium pumps. J Biol Chem 1992; 267 (20): 14483-9.
136. Sumbilla C, Cavagna M, Zhong L, Ma H, Lewis D, Farrance I, et al. Comparison of SERCA1 and SERCA2a expressed in COS-1 cells and cardiac myocytes. Am J Physiol 1999; 277 (6 Pt 2): H2381-91.
137. Clausen T. The Na+, K+ pump in skeletal muscle: quantification, regulation and functional significance. Acta Physiol Scand 1996; 156 (3): 227-35.
138. Crambert G, Hasler U, Beggah AT, Yu C, Modyanov NN, Horisberger JD, et al. Transport and pharmacological properties of nine different human Na, K-ATPase isozymes. J Biol Chem 2000; 275 (3): 1976-86.
139. Fowles JR, Green HJ, Ouyang J. Na+-K+-ATPase in rat skeletal muscle: content, isoform, and activity characteristics. J Appl Physiol 2004; 96 (1): 316-26.
140. Ng YC, Nagarajan M, Jew KN, Mace LC, Moore RL. Exercise training differentially modifies age-associated alteration in expression of Na+-K+-ATPase subunit isoforms in rat skeletal muscles. Am J Physiol Regul Integr Comp Physiol 2003; 285 (4): R733-40.
141. Thompson CB, McDonough AA. Skeletal muscle Na, K-ATPase alpha and beta subunit protein levels respond to hypokalemic challenge with isoform and muscle type specificity. J Biol Chem 1996; 271 (51): 32653-8.
142. Lavoie L, Levenson R, Martin-Vasallo P, Klip A. The molar ratios of alpha and beta subunits of the Na+-K+-ATPase differ in distinct subcellular membranes from rat skeletal muscle. Biochemistry 1997; 36 (25): 7726-32.
143. Clausen T. Na+-K+ pump regulation and skeletal muscle contractility. Physiol Rev 2003; 83 (4): 1269-324.
144. D'Antona G, Pellegrino MA, Adami R, Rossi R, Carlizzi CN, Canepari M, et al. The effect of ageing and immobilization on structure and function of human skeletal muscle fibres. J Physiol 2003; 552 (Pt 2): 499-511.
145. Haddad F, Adams GR. Aging-sensitive cellular and molecular mechanisms associated with skeletal muscle hypertrophy. J Appl Physiol 2006; 100 (4): 1188-203.
146. Thompson LV, Durand D, Fugere NA, Ferrington DA. Myosin and actin expression and oxidation in aging muscle. J Appl Physiol 2006; 101 (6): 1581-7.
147. Piec I, Listrat A, Alliot J, Chambon C, Taylor RG, Bechet D. Differential proteome analysis of aging in rat skeletal muscle. FASEB J 2005; 19 (9): 1143-5.
148. Klitgaard H, Zhou M, Schiaffino S, Betto R, Salviati G, Saltin B. Ageing alters the myosin heavy chain composition of single fibres from human skeletal muscle. Acta Physiol Scand 1990; 140 (1): 55-62.
149. Sullivan VK, Powers SK, Criswell DS, Tumer N, Larochelle JS, Lowenthal D. Myosin heavy chain composition in young and old rat skeletal muscle: effects of endurance exercise. J Appl Physiol 1995; 78 (6): 2115-20.
150. Carlsen RC, Walsh DA. Decrease in force potentiation and appearance of alpha-adrenergic mediated contracture in aging rat skeletal muscle. Pflugers Arch 1987; 408 (3): 224-30.
151. Petrella RJ, Cunningham DA, Vandervoort AA, Paterson DH. Comparison of twitch potentiation in the gastrocnemius of young and elderly men. Eur J Appl Physiol Occup Physiol 1989; 58 (4): 395-9.
152. Russ DW, Towse TF, Wigmore DM, Lanza IR, Kent-Braun JA. Contrasting influences of age and sex on muscle fatigue. Med Sci Sports Exerc 2008; 40 (2): 234-41.
153. Larsson L. Morphological and functional characteristics of the ageing skeletal muscle in man. A cross-sectional study. Acta Physiol Scand Suppl 1978; 457: 1-36.
154. Lexell J, Henriksson-Larsen K, Winblad B, Sjostrom M. Distribution of different fiber types in human skeletal muscles: effects of aging studied in whole muscle cross sections. Muscle Nerve 1983; 6 (8): 588-95.
155. Lexell J, Taylor CC, Sjostrom M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15-to 83-year-old men. J Neurol Sci 1988; 84 (2-3): 275-94.
156. Deschenes MR. Effects of aging on muscle fibre type and size. Sports Med 2004; 34 (12): 809-24.
157. Tomlinson BE, Irving D. The numbers of limb motor neurons in the human lumbosacral cord throughout life. J Neurol Sci 1977; 34 (2): 213-9.
158. Ulfhake B, Bergman E, Edstrom E, Fundin BT, Johnson H, Kullberg S, et al. Regulation of neurotrophin signaling in aging sensory and motoneurons: dissipation of target support? Mol Neurobiol 2000; 21 (3): 109-35.
159. Tevald MA, Foulis SA, Lanza IR, Kent-Braun JA. Lower energy cost of skeletal muscle contractions in older humans. Am J Physiol Regul Integr Comp Physiol 2010; 298 (3): R729-39.
160. Larsson L, Li X, Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 1997; 272 (2 Pt 1): C638-49.
161. Hook P, Larsson L. Actomyosin interactions in a novel single muscle fiber in vitro motility assay. J Muscle Res Cell Motil 2000; 21 (4): 357-65.
162. Hook P, Li X, Sleep J, Hughes S, Larsson L. In vitro motility speed of slow myosin extracted from single soleus fibres from young and old rats. J Physiol 1999; 520 Pt 2: 463-71.
163. Lowe DA, Surek JT, Thomas DD, Thompson LV. Electron paramagnetic resonance reveals age-related myosin structural changes in rat skeletal muscle fibers. Am J Physiol Cell Physiol 2001; 280 (3): C540-7.
164. Lowe DA, Thomas DD, Thompson LV. Force generation, but not myosin ATPase activity, declines with age in rat muscle fibers. Am J Physiol Cell Physiol 2002; 283 (1): C187-92.
165. Lowe DA, Warren GL, Snow LM, Thompson LV, Thomas DD. Muscle activity and aging affect myosin structural distribution and force generation in rat fibers. J Appl Physiol 2004; 96 (2): 498-506.
166. Balagopal P, Rooyackers OE, Adey DB, Ades PA, Nair KS. Effects of aging on in vivo synthesis of skeletal muscle myosin heavy-chain and sarcoplasmic protein in humans. Am J Physiol 1997; 273 (4 Pt 1): E790-800.
167. Short KR, Vittone JL, Bigelow ML, Proctor DN, Nair KS. Age and aerobic exercise training effects on whole body and muscle protein metabolism. Am J Physiol Endocrinol Metab 2004; 286 (1): E92-101.
168. Welle S, Thornton C, Statt M. Myofibrillar protein synthesis in young and old human subjects after three months of resistance training. Am J Physiol 1995; 268 (3 Pt 1): E422-7.
169. Damiani E, Larsson L, Margreth A. Age-related abnormalities in regulation of the ryanodine receptor in rat fast-twitch muscle. Cell Calcium 1996; 19 (1): 15-27.
170. Ferrington DA, Jones TE, Qin Z, Miller-Schlyer M, Squier TC, Bigelow DJ. Decreased conformational stability of the sarcoplasmic reticulum Ca-ATPase in aged skeletal muscle. Biochim Biophys Acta 1997; 1330 (2): 233-47.
171. Hunter SK, Thompson MW, Ruell PA, Harmer AR, Thom JM, Gwinn TH, et al. Human skeletal sarcoplasmic reticulum Ca2+ uptake and muscle function with aging and strength training. J Appl Physiol 1999; 86 (6): 1858-65.
172. Klitgaard H, Ausoni S, Damiani E. Sarcoplasmic reticulum of human skeletal muscle: age-related changes and effect of training. Acta Physiol Scand 1989; 137 (1): 23-31.
173. Larsson L, Salviati G. Effects of age on calcium transport activity of sarcoplasmic reticulum in fast-and slow-twitch rat muscle fibres. J Physiol 1989; 419: 253-64.
174. Schertzer JD, Plant DR, Ryall JG, Beitzel F, Stupka N, Lynch GS. Beta2-agonist administration increases sarcoplasmic reticulum Ca2+-ATPase activity in aged rat skeletal muscle. Am J Physiol Endocrinol Metab 2005; 288 (3): E526-33.
175. Viner RI, Ferrington DA, Williams TD, Bigelow DJ, Schoneich C. Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle. Biochem J 1999; 340 (Pt 3): 657-69.
176. Schoneich C, Viner RI, Ferrington DA, Bigelow DJ. Age-related chemical modification of the skeletal muscle sarcoplasmic reticulum Ca-ATPase of the rat. Mech Ageing Dev 1999; 107 (3): 221-31.
177. Sharov VS, Galeva NA, Kanski J, Williams TD, Schoneich C. Age-associated tyrosine nitration of rat skeletal muscle glycogen phosphorylase b: characterization by HPLC-nanoelectrospraytandem mass spectrometry. Exp Gerontol 2006; 41 (4): 407-16.
178. Jimenez-Moreno R, Wang ZM, Gerring RC, Delbono O. Sarcoplasmic reticulum Ca2+ release declines in muscle fibers from aging mice. Biophys J 2008; 94 (8): 3178-88.
179. Thomas MM, Vigna C, Betik AC, Tupling AR, Hepple RT. Initiating treadmill training in late middle age offers modest adaptations in Ca2+ handling but enhances oxidative damage in senescent rat skeletal muscle. Am J Physiol Regul Integr Comp Physiol 2010.
180. Weisleder N, Brotto M, Komazaki S, Pan Z, Zhao X, Nosek T, et al. Muscle aging is associated with compromised Ca2+ spark signaling and segregated intracellular Ca2+ release. J Cell Biol 2006; 174 (5): 639-45.
181. Margreth A, Damiani E, Bortoloso E. Sarcoplasmic reticulum in aged skeletal muscle. Acta Physiol Scand 1999; 167 (4): 331-8.
182. O'Connell K, Gannon J, Doran P, Ohlendieck K. Reduced expression of sarcalumenin and related Ca2+-regulatory proteins in aged rat skeletal muscle. Exp Gerontol 2008; 43 (10): 958-61.
183. Cai DQ, Li M, Lee KK, Lee KM, Qin L, Chan KM. Parvalbumin expression is downregulated in rat fast-twitch skeletal muscles during aging. Arch Biochem Biophys 2001; 387 (2): 202-8.
184. Sun X, Nagarajan M, Beesley PW, Ng YC. Age-associated differential expression of Na(+)-K(+)-ATPase subunit isoforms in skeletal muscles of F-344/BN rats. J Appl Physiol 1999; 87 (3): 1132-40.
185. Zhang L, Morris KJ, Ng YC. Fiber type-specific immunostaining of the Na+, K+-ATPase subunit isoforms in skeletal muscle: ageassociated differential changes. Biochim Biophys Acta 2006; 1762 (9): 783-93.
186. Zhang L, Ng YC. Fiber specific differential phosphorylation of the alpha1-subunit of the Na(+), K (+)-ATPase in rat skeletal muscle: the effect of aging. Mol Cell Biochem 2007; 303 (1-2): 231-7.
187. Juel C. Na+-K+-ATPase in rat skeletal muscle: muscle fiberspecific differences in exercise-induced changes in ion affinity and maximal activity. Am J Physiol Regul Integr Comp Physiol 2009; 296 (1): R125-32.
188. Klitgaard H, Clausen T. Increased total concentration of Na-K pumps in vastus lateralis muscle of old trained human subjects. J Appl Physiol 1989; 67 (6): 2491-4.
189. Hikida RS, Staron RS, Hagerman FC, Walsh S, Kaiser E, Shell S, et al. Effects of high-intensity resistance training on untrained older men. II. Muscle fiber characteristics and nucleo-cytoplasmic relationships. J Gerontol A Biol Sci Med Sci 2000; 55 (7): B347-54.
190. Inashima S, Matsunaga S, Yasuda T, Wada M. Effect of endurance training and acute exercise on sarcoplasmic reticulum function in rat fast-and slow-twitch skeletal muscles. Eur J Appl Physiol 2003; 89 (2): 142-9.
191. Hagerman FC, Walsh SJ, Staron RS, Hikida RS, Gilders RM, Murray TF, et al. Effects of high-intensity resistance training on untrained older men. I. Strength, cardiovascular, and metabolic responses. J Gerontol A Biol Sci Med Sci 2000; 55 (7): B336-46.
192. Tracy BL, Ivey FM, Hurlbut D, Martel GF, Lemmer JT, Siegel EL, et al. Muscle quality. II. Effects Of strength training in 65-to 75-yr-old men and women. J Appl Physiol 1999; 86 (1): 195-201.
193. Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol 2001; 535 (Pt 1): 301-11.
194. Gregory CM, Williams RH, Vandenborne K, Dudley GA. Metabolic and phenotypic characteristics of human skeletal muscle fibers as predictors of glycogen utilization during electrical stimulation. Eur J Appl Physiol 2005; 95 (4): 276-82.
195. Sieck GC, Zhan WZ, Prakash YS, Daood MJ, Watchko JF. SDH and actomyosin ATPase activities of different fiber types in rat diaphragm muscle. J Appl Physiol 1995; 79 (5): 1629-39.
196. Kent-Braun JA. Skeletal muscle fatigue in old age: whose advantage? Exerc Sport Sci Rev 2009; 37 (1): 3-9.