Metabolic consequences of muscle disuse atrophy

Journal of Nutrition

Volumn 135, Issue 7, 2005, Pages

  Stein, T P ^a   Wade, C E ^b  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b US ARMY INSTITUTE OF SURGICAL RESEARCH   (United States)

Author keywords

Gluconeogenesis; Liver; Microarrays; Muscle atrophy; Space flight

Indexed keywords

CITRIC ACID CYCLE; CONFERENCE PAPER; DNA MICROARRAY; GLUCONEOGENESIS; GLUCOSE HOMEOSTASIS; GLYCOLYSIS; HUMAN; LIPID OXIDATION; LIPID STORAGE; LIVER METABOLISM; MUSCLE ATROPHY; MUSCLE METABOLISM; NONHUMAN; PATHOPHYSIOLOGY; PHYSICAL ACTIVITY; PROTEIN EXPRESSION; SPACE FLIGHT;

EID: 22144476546     PISSN: 00223166     EISSN: None     Source Type: Journal    
DOI: 10.1093/jn/135.7.1824s     Document Type: Conference Paper

References (87)

1. Thornton, W. & Rummel, J. (1977) Muscular deconditioning and its prevention in space flight. Biomedical results from Skylab (NASA SP-377), pp. 191-197. U.S. Government Printing Office, Washington, DC.
2. Grigoriev, A. I. & Egorov, A. D. (1992) Physiological aspects of adaptation of main human body systems during and after spaceflights. Adv. Space Biol. Med. 2: 43-82.
3. Ilyina-Kakueva, E. I., Portugalov, V. V. & Kirvenkova, N. P. (1976) Spaceflight effects on the skeletal muscle of rats. Aviat. Space Environ. Med. 44: 700-703.
4. Musacchia, X. J., Steffen, J. M., Fell, R. D. & Dombrowski, M. J. (1990) Skeletal muscle response to spaceflight, whole body suspension, and recovery in rats. J. Appl. Physiol. 69: 2248-2253.
5. Morey-Holton, E. R. & Globus, R. K. (2002) Hindlimb unloading rodent model: technical aspects. J. Appl. Physiol. 92: 1367-1377.
6. Musacchia, X. J., Deavers, D. R., Meininger, G. A. & Davis, T. P. (1980) A model for hypokinesia: Effects on muscle atrophy in the rat. J. Appl. Physiol. 48: 479-486.
7. Fortney, S. M., Schneider, V. S. & Greenleaf, J. E. (1996) The physiology of bed rest. In: Handbook of Physiology, Section 4 (Fregly, M. J. & Blatteis, C. M., eds.), pp. 889-942. Oxford University Press, New York, NY.
8. Convertino, V. A. (1990) Physiological adaptations to weightlessness: effects on exercise and work performance. Exer. Sport. Sci. Rev. 18: 119-166.
9. Rogers, M. A. & Evans, W. J. (1993) Changes in skeletal muscle with aging: effects of exercise training. Exerc. Sport. Sci. Rev. 21: 65-102.
10. Roubenoff, R. & Hughes, V. A. (2000) Sarcopenia: current concepts. J. Gerontol. A Biol. Sci. Med. Sci. 55: M716-M724.
11. Caiozzo, V. J., Haddad, F., Baker, M. J., Herrick, R. E., Prietto, N. & Baldwin, K. M. (1996) Microgravity-induced transformations of myosin isoforms and contractile properties of skeletal muscle. J. Appl. Physiol. 81: 123-132.
12. Campione, M., Ausoni, S., Guezennec, C. Y. & Schiaffino, S. (1993) Myosin and troponin changes in rat soleus muscle after hindlimb suspension. J. Appl. Physiol. 74: 1156-1160.
13. Fitts, R. H., Riley, D. R. & Widrick, J. J. (2000) Physiology of a microgravity environment. Invited review: microgravity and skeletal muscle. J. Appl. Physiol. 89: 823-839.
14. Fitts, R. H. (1996) Muscle fatigue: the cellular aspects. Am. J. Sports. Med. 24: S9-S13.
15. Wang, E. (1999) Age-dependent atrophy and microgravity travel: What do they have in common? FASEB J. 13: S167-S174.
16. Biolo, G., Heer, M., Narici, M. & Strollo, F. (2003) Microgravity as a model of ageing. Curr. Opin. Clin. Nutr. Metab. Care 6: 31-40.
17. Baldwin, K. M., Herrick, R. E. & McCue, S. A. (1993) Substrate oxidation capacity in rodent skeletal muscle: effects of exposure to zero gravity. J. Appl. Physiol. 75: 2466-2470.
18. Langfort, J., Zernicka, E., Mayet-Sornay, M. H., Dubaniewicz, A. & Desplanches, D. (1997) Effects of acute and chronic hindlimb suspension on sensitivity and responsiveness to insulin in the rat soleus muscle. Biochem. Cell Biol. 75: 41-44.
19. Henriksen, E. J. & Tischler, M. E. (1988) Glucose uptake in rat soleus: effect of acute unloading and subsequent reloading. J. Appl. Physiol. 64: 1428-1432.
20. Stump, C. S., Tipton, C. M. & Henriksen, E. J. (1997) Muscle adaptations to hindlimb suspension in mature and old Fischer 344 rats. J. Appl. Physiol. 82: 1875-1881.
21. Petrova, N. V. & Portugalov, V. V. (1980) Biull. Eksp. Biol. Med. 90: 497-500.
22. Acheson, K. J., Decombaz, J., Piguet-Welsch, C., Montigon, F., Decarli, B., Bartholdi, I. & Fern, E. B. (1995) Energy, protein, and substrate metabolism in simulated microgravity. Am. J. Physiol. (Regul. Integ.) 269: R252-R260.
23. Ritz, P., Acheson, K. J., Gachon, P., Vico, L., Bernard, J. J., Alexandre, C. & Beaufrere, B. (1998) Energy and substrate metabolism during a 42-day bed-rest in a head-down tilt position in humans. Eur. J. Appl. Physiol. Occup. Physiol. 78: 308-314.
24. Edgerton, V. R. & Roy, R. R. (1997) Response of skeletal muscle to spaceflight. In: Fundamentals of Sapce Life Sciences (Churchill, S., ed.), pp. 105-120. Krieger, Malabar, FL.
25. Cartee, G. D. (1994) Aging skeletal muscle: response to exercise. Exerc. Sport. Sci. Rev. 22: 91-120.
26. Beyer, R. E., Starnes, J. W., Edington, D. W., Lipton, R. J., Compton, R. T., 3rd & Kwasman, M. A. (1984) Exercise-induced reversal of age-related declines of oxidative reactions, mitochondrial yield, and flavins in skeletal muscle of the rat. Mech. Ageing Dev. 24: 309-323.
27. Henriksen, E. J., Tischler, M. E. & Johnson, D. G. (1986) Increased response to insulin of glucose-metabolism in the 6-day unloaded rat soleus muscle. J. Biol. Chem. 261: 10707-10712.
28. Stump, C. S., Balon, T. W. & Tipton, C. M. (1992) Effects of insulin and exercise on rat hindlimb muscles after simulated microgravity. J. Appl. Physiol. 73: 2044-2053.
29. Grichko, V. P., Heywood-Cooksey, A., Kidd, K. R. & Fitts, R. H. (2000) Substrate profile in rat soleus muscle fibers after hindlimb unloading and fatigue. J. Appl. Physiol. 88: 473-478.
30. Ferrando, A. A., Lane, H. W., Stuart, C. A., Davis-Street, J. & Wolfe, R. R. (1996) Prolonged bed rest decreases skeletal muscle and whole body protein synthesis. Am. J. Physiol. (Endocrinol. Metab.) 270: E627-E633.
31. Krebs, J. M., Schneider, V. S., Evans, H., Kuo, M. C. & LeBlanc, A. D. (1990) Energy absorption, lean body mass, and total body fat changes during 5 weeks of continuous bed rest. Aviat. Space Environ. Med. 61: 314-318.
32. Blanc, S., Normand, S., Ritz, P., Pachiaudi, C., Vico, L., Gharib, C. & Gauquelin-Koch, G. (1998) Energy and water metabolism, body composition, and hormonal changes induced by 42 days of enforced inactivity and simulated weightlessness. J. Clin. Endocrinol. Metab. 83: 4289-4297.
33. Oganov, V. S., Bakulin, A., Novikov, V., Murashko, L., Kabitskaya, O., Schneider, V. S., Shackelford, L., Evans, H. J. & LeBlanc, A. D. (2001) Results of human bone densitomtery after prolonged space flights. International Scientific Cooperation on board MIR, Lyons, France.
34. Lane, H. W. (1992) Energy requirements for space flight. J. Nutr. 122: 13-18.
35. Chkottova, N. & Makko, L. (1982) Spaceflight effects lipogenesis and lipolyisis in rats. Kosm. Biol. Aviakosm. Med. 16: 82-83.
36. Musacchia, X. J., Steffen, J. M., Fell, R. D., Dombrowski, M. J., Oganov, V. W. & Ilyina-Kakueva, E. I. (1992) Skeletal muscle atrophy in response to 14 days of weightlessness: vastus medialis. J. Appl. Physiol. 73: 44S-50S.
37. Morley, J. E., Baumgartner, R. N., Roubenoff, R., Mayer, J. & Nair, K. S. (2001) Sarcopenia. J. Lab. Clin. Med. 137: 231-243.
38. Poggi, P., Marchetti, C. & Scelsi, R. (1987) Automatic morphometric analysis of skeletal muscle fibers in the aging man. Anat. Rec. 217: 30-34.
39. Greenleaf, J. E., Bernauer, E. M., Ertl, A. C., Trowbridge, T. S. & Wade, C. E. (1989) Work capacity during 30 days of bed rest with isotonic and isokinetic exercise training. J. Appl. Physiol. 67: 1820-1826.
40. Edgerton, V. R. & Roy, R. R., eds. (1994) Neuromuscular adaptation to actual and simulated spaceflight. In: Handbook of Physiology, Vol. 4, pp. 721-763. Oxford University Press, New York, NY.
41. Riley, D. A., Thompson, J. L., Prippendorf, B. & Slocum, G. R. (1995) Review of spaceflight and hindlimb suspension unloading induced sarcomere damage and repair. Bas. Appl. Myol. 5: 139-145.
42. Stauber, W. T., Clarkson, P. M., Fritz, V. K. & Evans, W. J. (1990) Extracellular matrix disruption and pain after eccentric muscle action. J. Appl. Physiol. 69: 868-874.
43. Fitts, R. H., Riley, D. R. & Widrick, J. J. (2001) Functional and structural adaptations of skeletal muscle to microgravity. J. Exp. Biol. 204: 3201-3208.
44. Blanc, S., Normand, S., Pachiaudi, C., Fortrat, J. O., Laville, M. & Gharib, C. (2000) Fuel homeostasis during physical inactivity induced by bed rest. J. Clin. Endocrinol. Metab. 85: 2223-2233.
45. Morio, B., Hocquette, J. F., Montaurier, C., Boirie, Y., Bouteloup-Demange, C., McCormack, C., Fellmann, N., Beaufrere, B. & Ritz, P. (2001) Muscle fatty acid oxidative capacity is a determinant of whole body fat oxidation in elderly people. Am. J. Physiol. Endocrinol. Metab. 280: E143-E149.
46. Essen-Gustavsson, B. & Borges, O. (1986) Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol. Scand. 126: 107-114.
47. Sial, S., Coggan, A. R., Carroll, R., Goodwin, J. & Klein, S. (1996) Fat and carbohydrate metabolism during exercise in elderly and young subjects. Am. J. Physiol. 271: E983-E989.
48. Calles-Escandon, J., Poehlman, E. T. & Garcia-Rubi, E. (1997) Lipolysis in elderly postmenopausal women. Metabolism 46: 1312-1315.
49. Ferretti, G., Antonutto, G., Denis, C., Hoppeler, H., Minetti, A. E., Narici, M. V. & Desplanches, D. (1997) The interplay of central and peripheral factors in limiting maximal O2 consumption in man after prolonged bed rest. J. Physiol. 501: 677-686.
50. Hikida, R. S., Gollnick, P. D., Dudley, G. A., Convertino, V. A. & Buchanan, P. (1989) Structural and metabolic characteristics of human skeletal muscle following 30 days of simulated microgravity. Aviat. Space Environ. Med. 60: 664-670.
51. Stein, T. P., Schluter, M. D., Galante, A. T., Soteropoulos, P., Tolias, P. P., Grindeland, R. E., Moran, M. M., Wang, T. J., Polansky, M. & Wade, C. E. (2002) Energy metabolism pathways in rat muscle under conditions of simulated microgravity. Nutr. Biochem. 13: 471-478.
52. Wittwer, M., Fluck, M., Hoppeler, H., Muller, S., Desplanches, D. & Billeter, R. (2002) Prolonged unloading of rat soleus muscle causes distinct adaptations of the gene profile. FASEB J. 16: 884-886.
53. Ohira, Y., Jiang, B., Roy, R. R., Oganov, V., Ilyina-Kakueva, E., Marini, J. F. & Edgerton, V. R. (1992) Rat soleus muscle fiber responses to 14 days of spaceflight and hindlimb suspension. J. Appl. Physiol. 73: 51S-57S.
54. Fitts, R. H., Brimmer, C. J., Heywood-Cooksey, A. & Timmerman, R. J. (1989) Single muscle fiber enzyme shifts with hindlimb suspension and immobilization. Am. J. Physiol. Circul. 256: C1082-C1091.
55. Chi, M. M., Choksi, R., Nemeth, P., Krasnov, I., Ilyina-Kakueva, E., Manchester, J. K. & Lowry, O. H. (1992) Effects of microgravity and tail suspension on enzymes of individual soleus and tibialis anterior fibers. J. Appl. Physiol. 73: 66S-73S.
56. Henriksen, E. J. & Tischler, M. E. (1988) Time course of the response of carbohydrate metabolism to unloading of the soleus. Metabolism 37: 201-208.
57. Desplanches, D. (1997) Structural and functional adaptations of skeletal muscle to weightlessness. Int. J. Sports. Med. 18 (suppl. 4): S259-S264.
58. Martin, I. P., Edgerton, V. R. & Grindeland, R. E. (1988) Influence of spaceflight on rat skeletal muscle. J. Appl. Physiol. 65: 2318-2325.
59. Manchester, J. K., Chi, M. M., Norris, B., Ferrier, B., Krasnov, I., Nemeth, P. M., McDougal, D. B., Jr. & Lowry, O. H. (1990) Effect of microgravity on metabolic enzymes of individual muscle fibers. FASEB J. 4: 55-63.
60. Simard, C., Lacaille, M. & Vallieres, J, (1985) Enzymatic adaptations to suspension hypokinesia in skeletal muscle of young and old rats. Mech. Ageing Dev. 33: 1-9.
61. Kell, R., Pierce, H. & Swoap, S. J. (1999) PGAM-M expression is regulated pretranslationally in hindlimb muscles and under altered loading conditions. J. Appl. Physiol. 86: 236-242.
62. Desplanches, D., Mayet, M. H., Ilyina-Kakueva, E. I., Sempore, B. & Flandrois, R. (1990) Skeletal muscle adaptation in rats flown on Cosmos 1667. J. Appl. Physiol. 68: 48-52.
63. Woodman, C. R., Tipton, C. M., Evans, J., Linderman, J. K., Gosselink, K. & Grindeland, R. E. (1993) Metabolic responses to head-down suspension in hypophysectomized rats. J. Appl. Physiol. 75: 2718-2726.
64. Baldwin, K. M., White, T. P., Arnaud, S. B., Edgerton, V. R., Kraemer, W. J., Kram, R., Raab-Cullen, D. & Snow, C. M. (1996) Musculoskeletal adaptations to weightlessness and development of effective countermeasures. Med. Sci. Sports Exerc. 28: 1247-1253.
65. Morey-Holton, E. & Wronski, T. J. (1981) Animal models for simulating weightlessness. Physiologist 14: S45-S48.
66. Stein, T. P. & Wade, C. E. (2003) Protein turnover in atrophying muscle: from nutritional intervention to microarray analysis. Curr. Opin. Clin. Nutr. Metab. Care 6: 95-102.
67. Ojala, B. E., Page, L. A., Moore, M. A. & Thompson, L. V. (2001) Effects of inactivity on glycolytic capacity of single skeletal muscle fibers in adult and aged rats. Biol. Res. Nurs. 3: 88-95.
68. Young, V. R. & Marchini, J. S. (1990) Mechanisms and nutritional significance of metabolic responses to altered intakes of protein and amino acids, with reference to nutritional adaptation in humans. Am. J. Clin. Nutr. 51: 270-289.
69. Waterlow, J. C. (1995) Whole-body protein turnover in humans-past, present, and future. Annu. Rev. Nutr. 15: 57-92.
70. Cortes, C. W., Thompson, P. D., Moyna, N. M., Schluter, M. D., Leskiw, M. J., Donaldson, M. R., Duncan, B. H. & Stein, T. P. (2003) Protein kinetics in stable heart failure patients. J. Appl. Physiol. 94: 295-300.
71. Gibson, J. N., Halliday, D., Morrison, W. L., Stoward, P. J., Hornsby, G. A., Watt, P. W., Murdoch, G. & Rennie, A. J. (1987) Decrease in human quadriceps muscle protein turnover consequent upon leg immobilization. Clin. Sci. 72: 503-509.
72. Schonhyder, F., Heilskov, N. S. & Olesen, K. (1954) Isotopic studies on the negative nitrogen balance produced by immobilization. Scand. J. Clin. Lab. Invest. 6: 178-188.
73. Tucker, K. R., Seider, M. J. & Booth, F. W. (1981) Protein synthesis rates in atrophied gastrocnemius muscles after limb immobilization. J. Appl. Physiol. 51: 73-77.
74. Welle, S. & Nair, K. S. (1990) Relationship of resting metabolic rate to body composition and protein turnover. Am. J. Physiol. 258: E990-E998.
75. Tappy, L. & Minehira, K. (2001) New data and new concepts on the role of the liver in glucose homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 4: 273-277.
76. Corssmit, E. P., Romijn, J. A. & Sauerwein, H. P. (2001) Review article: Regulation of glucose production with special attention to nonclassical regulatory mechanisms: a review. Metabolism 50: 742-755.
77. Bizeau, M. E., Short, C., Thresher, J. S., Commerford, S. R., Willis, W. T. & Pagliassotti, M. J. (2001) Increased pyruvate flux capacities account for diet-induced increases in gluconeogenesis in vitro. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281: R427-R433.
78. Bisschop, P. H., Pereira Arias, A. M., Ackermans, M. T., Endert, E., Pijl, H., Kuipers, F., Meijer, A. J., Sauerwein, H. P. & Romijn, J. A. (2000) The effects of carbohydrate variation in isocaloric diets on glycogenolysis and gluconeogenesis in healthy men. J. Clin. Endocrinol. Metab. 85: 1963-1967.
79. Linn, T., Santosa, B., Gronemeyer, D., Aygen, S., Scholz, N., Busch, M. & Bretzel, R. G. (2000) Effect of long-term dietary protein intake on glucose metabolism in humans. Diabetologia 43: 1257-1265.
80. Stein, T. P., Leskiw, M. J., Schluter, M. D., Hoyt, R. W., Lane, H. W., Gretebeck, R. E. & LeBlanc, A. D. (1999) Energy expenditure and balance during space flight on the shuttle: the LMS mission. Am. J. Physiol. (Endocrinol. Metab.) 276: R1739-R1748.
81. Stein, T. P., Leskiw, M. J., Schluter, M. D., Donaldson, M. R. & Larina, I. (1999) Protein kinetics during and after long term space flight on MIR. Am. J. Physiol. (Endocrinol. Metab.) 276: E1014-E1012.
82. Stein, T. P. & Leskiw, M. J. (2000) Oxidant damage during and after space flight. Am. J. Physiol. (Endocrinol. Metab). 278: E375-E382.
83. Ruderman, N. B., Saha, A. K., Vavvas, D. & Witters, L. A. (1999) Malonyl-CoA, fuel sensing, and insulin resistance. Am. J. Physiol. 276: E1-E18.
84. Laybutt, D. R., Chisholm, D. J. & Kraegen, E. W. (1997) Specific adaptations in muscle and adipose tissue in response to chronic systemic glucose oversupply in rats. Am. J. Physiol. 273: E1-E9.
85. Laybutt, D. R., Schmitz-Peiffer, G., Saha, A. K., Ruderman, N. B., Biden, T. J. & Kraegen, E. W. (1999) Muscle lipid accumulation and protein kinase C activation in the insulin-resistant chronically glucose-infused rat. Am. J. Physiol. 277: E1070-E1076.
86. Rossetti, L., Giaccari, A. & DeFronzo, R. A. (1990) Glucose toxicity. Diabetes Care 13: 610-630.
87. Prentki, M. & Corkey, B. E. (1996) Are the beta-cell signaling molecules malonyl-CoA and cystolic long-chain acyl-CoA implicated in multiple tissue defects of obesity and NIDDM? Diabetes 45: 273-283.