Age-related changes in oxidative capacity differ between locomotory muscles and are associated with physical activity behavior

Applied Physiology, Nutrition and Metabolism

Volumn 37, Issue 1, 2012, Pages 88-99

  Larsen, Ryan G ^a   Callahan, Damien M ^a   Foulis, Stephen A ^a   Kent Braun, Jane A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Aging; Bioenergetics; Metabolism; Mitochondria; Physical function; Skeletal muscle

Indexed keywords

ADENOSINE TRIPHOSPHATE; CREATINE PHOSPHATE;

ADULT; AGE; AGED; AGING; ANALYSIS OF VARIANCE; ARTICLE; COMPARATIVE STUDY; ENERGY METABOLISM; FEMALE; FITNESS; HUMAN; LOCOMOTION; MALE; METABOLISM; MUSCLE ISOMETRIC CONTRACTION; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OXIDATION REDUCTION REACTION; QUADRICEPS FEMORIS MUSCLE; SEDENTARY LIFESTYLE; STATISTICAL MODEL; WALKING DIFFICULTY;

ADENOSINE TRIPHOSPHATE; ADULT; AGE FACTORS; AGED; AGED, 80 AND OVER; AGING; ANALYSIS OF VARIANCE; ENERGY METABOLISM; FEMALE; HUMANS; ISOMETRIC CONTRACTION; LINEAR MODELS; LOCOMOTION; MAGNETIC RESONANCE SPECTROSCOPY; MALE; MOBILITY LIMITATION; OXIDATION-REDUCTION; PHOSPHOCREATINE; PHYSICAL FITNESS; QUADRICEPS MUSCLE; SEDENTARY LIFESTYLE; YOUNG ADULT;

EID: 84856569690     PISSN: 17155312     EISSN: 17155320     Source Type: Journal    
DOI: 10.1139/H11-135     Document Type: Article

References (57)

1. 31P NMR. Magn. Reson. Med. 1(3): 307-315. doi:10.1002/mrm. 1910010303. PMID:6571561.
2. Barrientos, A., Casademont, J., Rotig, A., Miro, O., Urbano-Marquez, A., Rustin, P., and Cardellach, F. 1996. Absence of relationship between the level of electron transport chain activities and aging in human skeletal muscle. Biochem. Biophys. Res. Commun. 229(2): 536-539. doi:10.1006/bbrc.1996.1839. PMID:8954933.
3. Bass, A., Gutmann, E., and Hanzlikova, V. 1975. Biochemical and histochemical changes in energy supply enzyme pattern of muscles of the rat during old age. Gerontologia, 21(1): 31-45. doi:10.1159/ 000212028. PMID:166901.
4. Brierley, E.J., Johnson, M.A., James, O.F.W., and Turnbull, D.M. 1996. Effects of physical activity and age on mitochondrial function. QJM, 89(4): 251-258. PMID:8733511.
5. Brierley, E.J., Johnson, M.A., Bowman, A., Ford, G.A., Subhan, F., Reed, J.W., et al. 1997. Mitochondrial function in muscle from elderly athletes. Ann. Neurol. 41(1): 114-116. doi:10.1002/ana. 410410120. PMID:9005875.
6. 2 release increases with age in human vastus lateralis muscle although oxidative capacity is preserved. Mech. Ageing Dev. 126(4): 505-511. doi:10.1016/j.mad.2004.11.001. PMID:15722109.
7. Cappellini, G., Ivanenko, Y.P., Poppele, R.E., and Lacquaniti, F. 2006. Motor patterns in human walking and running. J. Neurophysiol. 95(6): 3426-3437. doi:10.1152/jn.00081.2006. PMID:16554517.
8. Chilibeck, P.D., Paterson, D.H., McCreary, C.R., Marsh, G.D., Cunningham, D.A., and Thompson, R.T. 1998. The effects of age on kinetics of oxygen uptake and phosphocreatine in humans during exercise. Exp. Physiol. 83(1): 107-117. PMID:9483424.
9. Chretien, D., Gallego, J., Barrientos, A., Casademont, J., Cardellach, F., Munnich, A., et al. 1998. Biochemical parameters for the diagnosis of mitochondrial respiratory chain deficiency in humans, and their lack of age-related changes. Biochem. J. 329(2): 249-254. PMID:9425106.
10. Coggan, A.R., Spina, R.J., Rogers, M.A., King, D.S., Brown, M., Nemeth, P.M., and Holloszy, J.O. 1990. Histochemical and enzymatic characteristics of skeletal-muscle in master athletes. J. Appl. Physiol. 68(5): 1896-1901. PMID:2361892.
11. Conley, K.E., Jubrias, S.A., and Esselman, P.C. 2000. Oxidative capacity and ageing in human muscle. J. Physiol. 526(1): 203-210. doi:10.1111/j.1469-7793.2000.t01-1-00203.x. PMID:10878112.
12. Cooper, J.M., Mann, V.M., and Schapira, A.H.V. 1992. Analyses of mitochondrial respiratory-chain function and mitochondrial-DNA deletion in human skeletal muscle-effect of aging. J. Neurol. Sci. 113(1): 91-98. doi:10.1016/0022-510X(92)90270-U. PMID: 1469460.
13. Davis, M.G., and Fox, K.R. 2007. Physical activity patterns assessed by accelerometry in older people. Eur. J. Appl. Physiol. 100(5): 581-589. doi:10.1007/s00421-006-0320-8. PMID:17063361.
14. de Boer, M.D., Seynnes, O.R., di Prampero, P.E., Pisot, R., Mekjavić, I.B., Biolo, G., and Narici, M.V. 2008. Effect of 5 weeks horizontal bed rest on human muscle thickness and architecture of weight bearing and non-weight bearing muscles. Eur. J. Appl. Physiol. 104(2): 401-407. doi:10.1007/s00421-008-0703-0. PMID:18320207.
15. den Hoed, M., Hesselink, M.K., van Kranenburg, G.P., and Westerterp, K.R. 2008. Habitual physical activity in daily life correlates positively with markers for mitochondrial capacity. J. Appl. Physiol. 105(2): 561-568. doi:10.1152/japplphysiol.00091. 2008. PMID:18511526.
16. DeVita, P., and Hortobagyi, T. 2000. Age increases the skeletal versus muscular component of lower extremity stiffness during stepping down. J. Gerontol. A Biol. Sci. Med. Sci. 55(12): B593-B600. doi:10.1093/gerona/55.12.B593. PMID:11129389.
17. Dudley, G.A., Abraham, W.M., and Terjung, R.L. 1982. Influence of exercise intensity and duration on biochemical adaptations in skeletal muscle. J. Appl. Physiol. 53(4): 844-850. PMID:6295989.
18. 31P 2-D chemical shift imaging. NMR Biomed. 22(10): 1063-1071. PMID:19579230.
19. Freedson, P.S., Melanson, E., and Sirard, J. 1998. Calibration of the Computer Science and Applications, Inc. accelerometer. Med. Sci. Sports Exerc. 30(5): 777-781. doi:10.1097/00005768-199805000-00021. PMID:9588623.
20. Gollnick, P.D., Armstrong, R.B., Saubert, C.W., IV, Piehl, K., and Saltin, B. 1972. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J. Appl. Physiol. 33(3): 312-319. PMID:4403464.
21. Gregory, C.M., Vandenborne, K., and Dudley, G.A. 2001. Metabolic enzymes and phenotypic expression among human locomotor muscles. Muscle Nerve, 24(3): 387-393. doi:10.1002/1097-4598(200103)24:3<387::AID-MUS1010>3.0.CO;2-M. PMID:11353424.
22. Grimby, L. 1984. Firing properties of single human motor units during locomotion. J. Physiol. 346: 195-202. PMID:6699774.
23. Guralnik, J.M., Simonsick, E.M., Ferrucci, L., Glynn, R.J., Berkman, L.F., Blazer, D.G., et al. 1994. A short physical performance battery assessing lower extremity function: association with selfreported disability and prediction of mortality and nursing home admission. J. Gerontol. 49(2): M85-M94. PMID:8126356.
24. Guralnik, J.M., Ferrucci, L., Simonsick, E.M., Salive, M.E., and Wallace, R.B. 1995. Lower-extremity function in persons over the age of 70 years as a predictor of subsequent disability. N. Engl. J. Med. 332(9): 556-561. doi:10.1056/NEJM199503023320902. PMID:7838189.
25. Harris, J., and Benedict, F. 1919. A biometric study of basal metabolism in man. Carnegie Institute of Washington, Washington D.C., USA.
26. Harris, R.C., Hultman, E., and Nordesjo, L.O. 1974. Glycogen, glycolytic intermediates and high-energy phosphates determined in biopsy samples of musculus quadriceps femoris of man at rest. Methods and variance of values. Scand. J. Clin. Lab. Invest. 33(2): 109-120. doi:10.3109/00365517409082477. PMID:4852173.
27. Holloszy, J.O., Chen, M., Cartee, G.D., and Young, J.C. 1991. Skeletal muscle atrophy in old rats: differential changes in the three fiber types. Mech. Ageing Dev. 60(2): 199-213. doi:10. 1016/0047-6374(91)90131-I. PMID:1745075.
28. Houmard, J.A., Weidner, M.L., Gavigan, K.E., Tyndall, G.L., Hickey, M.S., and Alshami, A. 1998. Fiber type and citrate synthase activity in the human gastrocnemius and vastus lateralis with aging. J. Appl. Physiol. 85(4): 1337-1341. PMID:9760325.
29. Jakobsson, F., Borg, K., Edström, L., and Grimby, L. 1988. Use of motor units in relation to muscle fiber type and size in man. Muscle Nerve, 11(12): 1211-1218. doi:10.1002/mus.880111205. PMID:3070382.
30. Janssen, I., Heymsfield, S.B., and Ross, R. 2002. Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J. Am. Geriatr. Soc. 50(5): 889-896. doi:10.1046/j.1532-5415.2002.50216.x. PMID:12028177.
31. Karakelides, H., Irving, B.A., Short, K.R., O'Brien, P., and Nair, K.S. 2010. Age, obesity, and sex effects on insulin sensitivity and skeletal muscle mitochondrial function. Diabetes, 59(1): 89-97. doi:10.2337/db09-0591. PMID:19833885.
32. Kent-Braun, J.A., and Ng, A.V. 2000. Skeletal muscle oxidative capacity in young and older women and men. J. Appl. Physiol. 89(3): 1072-1078. PMID:10956353.
33. Lanza, I.R., Befroy, D.E., and Kent-Braun, J.A. 2005. Age-related changes in ATP-producing pathways in human skeletal muscle in vivo. J. Appl. Physiol. 99(5): 1736-1744. doi:10.1152/ japplphysiol.00566.2005. PMID:16002769.
34. Lanza, I.R., Larsen, R.G., and Kent-Braun, J.A. 2007. Effects of old age on human skeletal muscle energetics during fatiguing contractions with and without blood flow. J. Physiol. 583(3): 1093-1105. doi:10.1113/jphysiol.2007.138362. PMID:17673506.
35. Lanza, I.R., Short, D.K., Short, K.R., Raghavakaimal, S., Basu, R., Joyner, M.J., et al. 2008. Endurance exercise as a countermeasure for aging. Diabetes, 57(11): 2933-2942. doi:10.2337/db08-0349. PMID:18716044.
36. Larsen, R.G., Callahan, D.M., Foulis, S.A., and Kent-Braun, J.A. 2009. In vivo oxidative capacity varies with muscle and training status in young adults. J. Appl. Physiol. 107(3): 873-879. doi:10. 1152/japplphysiol.00260.2009. PMID:19556459.
37. Levine, J.A., Eberhardt, N.L., and Jensen, M.D. 1999. Role of nonexercise activity thermogenesis in resistance to fat gain in humans. Science, 283(5399): 212-214. doi:10.1126/science.283. 5399.212. PMID:9880251.
38. Matthews, C.E., Ainsworth, B.E., Thompson, R.W., and Bassett, D.R., Jr. 2002. Sources of variance in daily physical activity levels as measured by an accelerometer. Med. Sci. Sports Exerc. 34(8): 1376-1381. doi:10.1097/00005768-200208000-00021. PMID: 12165695.
39. McCully, K.K., Fielding, R.A., Evans, W.J., Leigh, J.S., Jr, and Posner, J.D. 1993. Relationships between in-vivo and in-vitro measurements of metabolism in young and old human calf muscles. J. Appl. Physiol. 75(2): 813-819. PMID:8226486.
40. McDermott, M.M., Greenland, P., Liu, K., Guralnik, J.M., Criqui, M.H., Dolan, N.C., et al. 2001. Leg symptoms in peripheral arterial disease: associated clinical characteristics and functional impairment. JAMA, 286(13): 1599-1606. doi:10.1001/jama.286.13. 1599. PMID:11585483.
41. Meyer, R.A. 1988. A linear model of muscle respiration explains monoexponential phosphocreatine changes. Am. J. Physiol. 254(4): C548-C553. PMID:3354652.
42. Meyer, R.A. 1989. Linear dependence of muscle phosphocreatine kinetics on total creatine content. Am. J. Physiol. 257(6): C1149-C1157. PMID:2610252.
43. Moon, R.B., and Richards, J.H. 1973. Determination of intracellular pH by 31P magnetic resonance. J. Biol. Chem. 248(20): 7276-7278. PMID:4743524.
44. Pastoris, O., Boschi, F., Verri, M., Baiardi, P., Felzani, G., Vecchiet, J., et al. 2000. The effects of aging on enzyme activities and metabolite concentrations in skeletal muscle from sedentary male and female subjects. Exp. Gerontol. 35(1): 95-104. doi:10.1016/ S0531-5565(99)00077-7. PMID:10705043.
45. 2max in trained older subjects. J. Appl. Physiol. 82(5): 1411-1415. PMID:9134886.
46. Proctor, D.N., Sinning, W.E., Walro, J.M., Sieck, G.C., and Lemon, P.W.R. 1995. Oxidative capacity of human muscle fiber types-effects of age and training status. J. Appl. Physiol. 78(6): 2033-2038. PMID:7665396.
47. Quistorff, B., Johansen, L., and Sahlin, K. 1993. Absence of phosphocreatine resynthesis in human calf muscle during ischaemic recovery. Biochem. J. 291(3): 681-686. PMID: 8489495.
48. Rasmussen, U.F., Krustrup, P., Kjaer, M., and Rasmussen, H.N. 2003. Experimental evidence against the mitochondrial theory of aging. A study of isolated human skeletal muscle mitochondria. Exp. Gerontol. 38(8): 877-886. doi:10.1016/S0531-5565(03) 00092-5. PMID:12915209.
49. Rimbert, V., Boirie, Y., Bedu, M., Hocquette, J.F., Ritz, P., and Morio, B. 2004. Muscle fat oxidative capacity is not impaired by age but by physical inactivity: association with insulin sensitivity. FASEB J. 18(6): 737-739. PMID:14977873.
50. Rooyackers, O.E., Adey, D., Ford, G.C., Ades, P., and Nair, K.S. 1996. Effect of aging on skeletal muscle mitochondrial protein synthesis rates in humans. J. Investig. Med. 44: A317.
51. Russ, D.W., and Kent-Braun, J.A. 2004. Is skeletal muscle oxidative capacity decreased in old age? Sports Med. 34(4): 221-229. doi:10.2165/00007256-200434040-00002. PMID:15049714.
52. Sanchez, J., Bastien, C., and Monod, H. 1983. Enzymatic adaptations to treadmill training in skeletal muscle of young and old rats. Eur. J. Appl. Physiol. Occup. Physiol. 52(1): 69-74. doi:10.1007/ BF00429028. PMID:6686132.
53. Short, K.R., Bigelow, M.L., Kahl, J., Singh, R., Coenen-Schimke, J., Raghavakaimal, S., and Nair, K.S. 2005. Decline in skeletal muscle mitochondrial function with aging in humans. Proc. Natl. Acad. Sci. U.S.A. 102(15): 5618-5623. doi:10.1073/pnas. 0501559102. PMID:15800038.
54. Stephens, B.R., Granados, K., Zderic, T.W., Hamilton, M.T., and Braun, B. 2011. Effects of 1 day of inactivity on insulin action in healthy men and women: interaction with energy intake. Metabolism, 60(7): 941-949. doi:10.1016/j.metabol.2010.08.014. PMID:21067784.
55. Theou, O., Jones, G.R., Vandervoort, A.A., and Jakobi, J.M. 2010. Daily muscle activity and quiescence in non-frail, pre-frail, and frail older women. Exp. Gerontol. 45(12): 909-917. doi:10.1016/j. exger.2010.08.008. PMID:20736056.
56. Tonkonogi, M., Fernstrom, M., Walsh, B., Ji, L.L., Rooyackers, O., Hammarqvist, F., et al. 2003. Reduced oxidative power but unchanged antioxidative capacity in skeletal muscle from aged humans. Pflugers Arch. 446(2): 261-269. PMID:12684796.
57. Troiano, R.P., Berrigan, D., Dodd, K.W., Masse, L.C., Tilert, T., and Mcdowell, M. 2008. Physical activity in the United States measured by accelerometer. Med. Sci. Sports Exerc. 40(1): 181-188. PMID:18091006.