Bed rest reduces metabolic protein content and abolishes exercise-induced mRNA responses in human skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 4, 2011, Pages

  Ringholm, Stine ^a   Bienso, Rasmus S ^a   Kiilerich, Kristian ^a   Guadalupe Grau, Amelia ^b   Aachmann Andersen, Niels Jacob ^a   Saltin, Bengt ^a   Plomgaard, Peter ^a   Lundby, Carsten ^a   Wojtaszewski, Jorgen F P ^a   Calbet, Jose A ^a,b   Pilegaard, Henriette ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF LAS PALMAS DE GRAN CANARIA   (Spain)

Author keywords

Capillarization; Oxidative capacity; Peroxisome proliferator activated receptor a coactivator 1 ; Physical inactivity

Indexed keywords

CITRATE SYNTHASE; CYTOCHROME C; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; MICRORNA; MICRORNA 133A; MITOCHONDRIAL DNA; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SIRTUIN 1; UNCLASSIFIED DRUG;

ADULT; ARTICLE; BED REST; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; EXERCISE; HUMAN; HUMAN EXPERIMENT; HUMAN TISSUE; INTRACELLULAR SIGNALING; MALE; MUSCLE BIOPSY; NORMAL HUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN METABOLISM; SKELETAL MUSCLE;

ADULT; AMP-ACTIVATED PROTEIN KINASES; BED REST; BODY COMPOSITION; CYTOCHROMES C; ENERGY METABOLISM; EXERCISE; HUMANS; MALE; MITOCHONDRIA; MUSCLE, SKELETAL; OXYGEN CONSUMPTION; RNA, MESSENGER; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 80053270813     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00230.2011     Document Type: Article

References (49)

1. Alibegovic AC, Sonne MP, Højbjerre L, Bork-Jensen J, Jacobsen S, Nilsson E, Færch K, Hiscock N, Mortensen B, Friedrichsen M, Stallknecht B, Dela F, Vaag A. Insulin resistance induced by physical inactivity is associated with multiple transcriptional changes in skeletal muscle in young men. Am J Physiol Endocrinol Metab 299: E752-E763, 2010.
2. Alibegovic AC, Højbjerre L, Sonne MP, van Hall G, Stallknecht B, Dela F, Vaag A. Impact of 9 days of bed rest on hepatic and peripheral insulin action, insulin secretion, and whole-body lipolysis in healthy young male offspring of patients with type 2 diabetes. Diabetes 58: 2749-2756, 2009.
3. Allen DL, Bandstra ER, Harrison BC, Thorng S, Stodieck LS, Kostenuik PJ, Morony S, Lacey DL, Hammond TG, Leinwand LL, Argraves WS, Bateman TA, Barth JL. Effects of spaceflight on murine skeletal muscle gene expression. J Appl Physiol 106: 582-595, 2009.
4. Allred JB, Reilly KE. Short-term regulation of acetyl CoA carboxylase in tissues of higher animals. Prog Lipid Res 35: 371-385, 1996.
5. Andersen P. Capillary density in skeletal muscle of man. Acta Physiol Scand 95: 203-205, 1975.
6. Arany Z, Foo SY, Ma Y, Ruas JL, Bommi-Reddy A, Girnun G, Cooper M, Laznik D, Chinsomboon J, Rangwala SM, Baek KH, Rosenzweig A, Spiegelman BM. HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451: 1008-1012, 2008.
7. Barres R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 10: 189-198, 2009.
8. Bergström J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
9. Bienso RS, Ringholm S, Lundby C, Achman-Andersen NJ, Plomgaard P, Krogh-Madsen R, Kiilerich K, Guerra B, Treebak JT, Calbet JA, Pilegaard H, Wojtaszewski JJ. Bed rest-induced changes in TBC1D4 phosphorylation and glycogen synthase activity. Effects of acute exercise (Abstract). Diabetes 59: A365, 2010.
10. Birk JB, Wojtaszewski JF. Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 577: 1021-1032, 2006.
11. Brooke MH, Kaiser KK. Three "myosin adenosine triphosphatase" systems: the nature of their pH lability and sulfhydryl dependence. J Histochem Cytochem 18: 670-672, 1970.
12. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. AMPK regulates energy expenditure by modulating NAD metabolism and SIRT1 activity. Nature 458: 1056-1060, 2009.
13. Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162: 156-159, 1987.
14. De Filippis E, Alvarez G, Berria R, Cusi K, Everman S, Meyer C, Mandarino LJ. Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise. Am J Physiol Endocrinol Metab 294: E607-E614, 2008.
15. Gallagher IJ, Scheele C, Keller P, Nielsen AR, Remenyi J, Fischer CP, Roder K, Babraj J, Wahlestedt C, Hutvagner G, Pedersen BK, Timmons JA. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med 2: 9, 2010.
16. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26: 1913-1923, 2007.
17. Gollnick PD, Saltin B. Significance of skeletal muscle oxidative enzyme enhancement with endurance training. Clin Physiol 2: 1-12, 1982.
18. Henriksson J, Reitman JS. Time course of changes in human skeletal muscle succinate dehydrogenase and cytochrome oxidase activities and maximal oxygen uptake with physical activity and inactivity. Acta Physiol Scand 99: 91-97, 1977.
19. Hiscock N, Fischer CP, Pilegaard H, Pedersen BK. Vascular endothelial growth factor mRNA expression and arteriovenous balance in response to prolonged, submaximal exercise in humans. Am J Physiol Heart Circ Physiol 285: H1759-H1763, 2003.
20. Hudlicka O, Brown M, Egginton S. Angiogenesis in skeletal and cardiac muscle. Physiol Rev 72: 369-417, 1992.
21. Jager S, Handschin C, St-Pierre J, Spiegelman BM. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc Natl Acad Sci USA 104: 12017-12022, 2007.
22. Jensen L, Pilegaard H, Neufer PD, Hellsten Y. Effect of acute exercise and exercise training on VEGF splice variants in human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 287: R397-R402, 2004.
23. Jeppesen TD, Schwartz M, Olsen DB, Wibrand F, Krag T, Dunø M, Hauerslev S, Vissing J. Aerobic training is safe and improves exercise capacity in patients with mitochondrial myopathy. Brain 129: 3402-3412, 2006.
24. Jørgensen SB, Richter EA, Wojtaszewski JFP. Role of AMPK in skeletal muscle metabolic regulation and adaptation in relation to exercise. J Physiol 574: 17-31, 2006.
25. Jørgensen SB, Wojtaszewski JF, Viollet B, Andreelli F, Birk JB, Hellsten Y, Schjerling P, Vaulont S, Neufer PD, Richter EA, Pilegaard H. Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle. FASEB J 19: 1146-1148, 2005.
26. Kiens B, Essen-Gustavsson B, Christensen NJ, Saltin B. Skeletal muscle substrate utilization during submaximal exercise in man: effect of endurance training. J Physiol 469: 459-478, 1993.
27. Kiilerich K, Ringholm S, Biensø RS, Fisher JP, Iversen N, van Hall G, Wojtaszewski JF, Saltin B, Lundby C, Calbet JA, Pilegaard H. Exercise-induced Pyruvate Dehydrogenase Activation Is Not Affected by Seven Days of Bed Rest. J Appl Physiol. First published June 16, 2011; doi:10.1152/japplphysiol.00063.2011.
28. Krogh-Madsen R, Thyfault JP, Broholm C, Mortensen OH, Olsen RH, Mounier R, Plomgaard P, van Hall G, Booth FW, Pedersen BK. A 2-wk reduction of ambulatory activity attenuates peripheral insulin sensitivity. J Appl Physiol 108: 1034-1040, 2010.
29. Leick L, Hellsten Y, Fentz J, Lyngby SS, Wojtaszewski JF, Hidalgo J, Pilegaard H. PGC-1α mediates exercise-induced skeletal muscle VEGF expression in mice. Am J Physiol Endocrinol Metab 297: E92-E103, 2009.
30. Leick L, Plomgaard P, Grønløkke L, Al-Abaiji F, Wojtaszewski JF, Pilegaard H. Endurance exercise induces mRNA expression of oxidative enzymes in human skeletal muscle late in recovery. Scand J Med Sci Sports 20: 593-599, 2010.
31. Leick L, Wojtaszewski JF, Johansen ST, Kiilerich K, Comes G, Hellsten Y, Hidalgo J, Pilegaard H. PGC-1α is not mandatory for exercise-and training-induced adaptive gene responses in mouse skeletal muscle. Am J Physiol Endocrinol Metab 294: E463-E474, 2008.
32. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O, Michael LF, Puigserver P, Isotani E, Olson EN, Lowell BB, Bassel-Duby R, Spiegelman BM. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418: 797-801, 2002.
33. Little JP, Safdar A, Cermak N, Tarnopolsky MA, Gibala MJ. Acute endurance exercise increases the nuclear abundance of PGC-1α in trained human skeletal muscle. Am J Physiol Regul Integr Comp Physiol 298: R912-R917, 2010.
34. Little JP, Safdar A, Wilkin GP, Tarnopolsky MA, Gibala MJ. A practical model of low-volume high-intensity interval training induces mitochondrial biogenesis in human skeletal muscle: potential mechanisms. J Physiol 588: 1011-1022, 2010.
35. Lowry OH, Passonneau JV. A Flexible System of Enzymatic Analysis. London: Academic, 1972.
36. Lundby C, Nordsborg N, Kusuhara K, Kristensen KM, Neufer PD, Pilegaard H. Gene expression in human skeletal muscle: alternative normalization method and effect of repeated biopsies. Eur J Appl Physiol 95: 351-360, 2005.
37. MacDonald C, Wojtaszewski JF, Pedersen BK, Kiens B, Richter EA. Interleukin-6 release from human skeletal muscle during exercise: relation to AMPK activity. J Appl Physiol 95: 2273-2277, 2003.
38. Mikines KJ, Dela F, Tronier B, Galbo H. Effect of 7 days of bed rest on dose-response relation between plasma glucose and insulin secretion. Am J Physiol Endocrinol Metab 257: E43-E48, 1989.
39. Mikines KJ, Richter EA, Dela F, Galbo H. Seven days of bed rest decrease insulin action on glucose uptake in leg and whole body. J Appl Physiol 70: 1245-1254, 1991.
40. Nielsen S, Scheele C, Yfanti C, Akerström T, Nielsen AR, Pedersen BK, Laye M. Muscle specific microRNAs are regulated by endurance exercise in human skeletal muscle. J Physiol 588: 4029-4037, 2010.
41. Pilegaard H, Ordway GA, Saltin B, Neufer PD. Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise. Am J Physiol Endocrinol Metab 279: E806-E814, 2000.
42. Pilegaard H, Saltin B, Neufer PD. Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle. J Physiol 546: 851-858, 2003.
43. Safdar A, Abadi A, Akhtar M, Hettinga BP, Tarnopolsky MA. miRNA in the regulation of skeletal muscle adaptation to acute endurance exercise in C57Bl/6J male mice. PLoS One 4: e5610, 2009.
44. Saltin B, Blomqvist G, Mitchell JH, Johnson RL Jr, Wildenthal K, Chapman CB. Response to exercise after bed rest and after training. Circulation 38: VII1-VII78, 1968.
45. Seip RL, Mair K, Cole TG, Semenkovich CF. Induction of human skeletal muscle lipoprotein lipase gene expression by short-term exercise is transient. Am J Physiol Endocrinol Metab 272: E255-E261, 1997.
46. Wang H, Garzon R, Sun H, Ladner KJ, Singh R, Dahlman J, Cheng A, Hall BM, Qualman SJ, Chandler DS, Croce CM, Guttridge DC. NF-kappaB-YY1-miR-29 regulatory circuitry in skeletal myogenesis and rhabdomyosarcoma. Cancer Cell 14: 369-381, 2008.
47. Williams RS, Neufer PD. Regulation of gene expression in skeletal muscle by contractile activity. In: Handbook of Physiology. Exercise: Regulation and Integration of Multiple Systems. Am. Physiol. Soc., 1996, sect. 12, vol. III, chapt. 25, p. 1124-1150.
48. Yeo WK, Paton CD, Garnham AP, Burke LM, Carey AL, Hawley JA. Skeletal muscle adaptation and performance responses to once a day versus twice every second day endurance training regimens. J Appl Physiol 105: 1462-1470, 2008.
49. Yfanti C, Akerström T, Nielsen S, Nielsen AR, Mounier R, Mortensen OH, Lykkesfeldt J, Rose AJ, Fischer CP, Pedersen BK. Antioxidant supplementation does not alter endurance training adaptation. Med Sci Sports Exerc 42: 1388-1395, 2010.