Effects of 3 days unloading on molecular regulators of muscle size in humans

Journal of Applied Physiology

Volumn 109, Issue 3, 2010, Pages 721-727

  Gustafsson, T ^a   Osterlund, T ^a   Flanagan, J N ^a   Von Walden F ^d   Trappe, T A ^b   Linnehan, R M ^c   Tesch, P A ^d,e  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b BALL STATE UNIVERSITY   (United States)

^c NASA JOHNSON SPACE CENTER   (United States)

^d KAROLINSKA INSTITUTE   (Sweden)

^e MID SWEDEN UNIVERSITY   (Sweden)

Author keywords

Atrophy; Proteasome degradation; Simulated spaceflight; Ubiquitin

Indexed keywords

MESSENGER RNA; MUSCLE PROTEIN;

ADULT; ARTICLE; BIOPSY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMOBILIZATION; MALE; METABOLISM; MUSCLE ATROPHY; ORGAN SIZE; PATHOLOGY; PHOSPHORYLATION; PROTEIN PROCESSING; QUADRICEPS FEMORIS MUSCLE; SIGNAL TRANSDUCTION; TIME; WEIGHTLESSNESS;

ADULT; BIOPSY; GENE EXPRESSION REGULATION; HUMANS; IMMOBILIZATION; MALE; MUSCLE PROTEINS; MUSCULAR ATROPHY; ORGAN SIZE; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; QUADRICEPS MUSCLE; RNA, MESSENGER; SIGNAL TRANSDUCTION; TIME FACTORS; WEIGHTLESSNESS SIMULATION; YOUNG ADULT;

EID: 77957137810     PISSN: 87507587     EISSN: 15221601     Source Type: Journal    
DOI: 10.1152/japplphysiol.00110.2009     Document Type: Article

References (49)

1. Alkner BA, Tesch PA. Knee extensor and plantar flexor muscle size and function following 90 days of bed rest with or without resistance exercise. Eur J Appl Physiol 93:294-305, 2004.
2. 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.
3. Amirouche A, Durieux AC, Banzet S, Koulmann N, Bonnefoy R, Mouret C, Bigard X, Peinnequin A, Freyssenet D. Down-regulation of Akt/mammalian target of rapamycin signaling pathway in response to myostatin overexpression in skeletal muscle. Endocrinology 150:286-294, 2009.
4. Attaix D, Ventadour S, Codran A, Bechet D, Taillandier D, Combaret L. The ubiquitin-proteasome system and skeletal muscle wasting. Essays Biochem 41:173-186, 2005.
5. Berg HE, Dudley GA, Haggmark T, Ohlsen H, Tesch PA. Effects of lower limb unloading on skeletal muscle mass and function in humans. J Appl Physiol 70:1882-1885, 1991.
6. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704-1708, 2001.
7. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3:1014-1019, 2001.
8. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868, 1999.
9. Carlson CJ, Booth FW, Gordon SE. Skeletal muscle myostatin mRNA expression is fiber-type specific and increases during hindlimb unloading. Am J Physiol Regul Integr Comp Physiol 277: R601-R606, 1999.
10. Chelh I, Meunier B, Picard B, Reecy MJ, Chevalier C, Hocquette JF, Cassar-Malek I. Molecular profiles of Quadriceps muscle in myostatinnull mice reveal PI3K and apoptotic pathways as myostatin targets. BMC Genomics 10:196, 2009.
11. Coffey VG, Pilegaard H, Garnham AP, O'Brien BJ, Hawley JA. Consecutive bouts of diverse contractile activity alter acute responses in human skeletal muscle. J Appl Physiol 106:1187-1197, 2009.
12. Coffey VG, Zhong Z, Shield A, Canny BJ, Chibalin AV, Zierath JR, Hawley JA. Early signaling responses to divergent exercise stimuli in skeletal muscle from well-trained humans. FASEB J 20:190-192, 2006.
13. de Boer MD, Maganaris CN, Seynnes OR, Rennie MJ, Narici MV. Time course of muscular, neural and tendinous adaptations to 23 day unilateral lower-limb suspension in young men. J Physiol 583:1079-1091, 2007.
14. Du J, Wang X, Miereles C, Bailey JL, Debigare R, Zheng B, Price SR, Mitch WE. Activation of caspase-3 is an initial step triggering accelerated muscle proteolysis in catabolic conditions. J Clin Invest 113:115-123, 2004.
15. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37:1974-1984, 2005.
16. Glover EI, Phillips SM, Oates BR, Tang JE, Tarnopolsky MA, Selby A, Smith K, Rennie MJ. Immobilization induces anabolic resistance in human myofibrillar protein synthesis with low and high dose amino acid infusion. J Physiol 586:6049-6061, 2008.
17. Goll DE, Thompson VF, Li H, Wei W, Cong J. The calpain system. Physiol Rev 83:731-801, 2003.
18. Gomes MD, Lecker SH, Jagoe RT, Navon A, Goldberg AL. Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc Natl Acad Sci USA 98:14440-14445, 2001.
19. Haddad F, Baldwin KM, Tesch PA. Pretranslational markers of contractile protein expression in human skeletal muscle: effect of limb unloading plus resistance exercise. J Appl Physiol 98:46-52, 2005.
20. Huang J, Forsberg NE. Role of calpain in skeletal-muscle protein degradation. Proc Natl Acad Sci USA 95:12100-12105, 1998.
21. Jespersen J, Kjaer M, Schjerling P. The possible role of myostatin in skeletal muscle atrophy and cachexia. Scand J Med Sci Sports 16:74-82, 2006.
22. Jin B, Li YP. Curcumin prevents lipopolysaccharide-induced atrogin-1/MAFbx upregulation and muscle mass loss. J Cell Biochem 100:960-969, 2007.
23. Jones SW, Hill RJ, Krasney PA, O'Conner B, Peirce N, Greenhaff PL. Disuse atrophy and exercise rehabilitation in humans profoundly affects the expression of genes associated with the regulation of skeletal muscle mass. FASEB J 18:1025-1027, 2004.
24. Kambadur R, Sharma M, Smith TP, Bass JJ. Mutations in myostatin (GDF8) in double-muscled Belgian Blue and Piedmontese cattle. Genome Res 7:910-916, 1997.
25. Kramerova I, Kudryashova E, Venkatraman G, Spencer MJ. Calpain 3 participates in sarcomere remodeling by acting upstream of the ubiquitin-proteasome pathway. Hum Mol Genet 14:2125-2134, 2005.
26. Lecker SH, Jagoe RT, Gilbert A, Gomes M, Baracos V, Bailey J, Price SR, Mitch WE, Goldberg AL. Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J 18:39-51, 2004.
27. Lee SJ. Regulation of muscle mass by myostatin. Annu Rev Cell Dev Biol 20:61-86, 2004.
28. Leger B, Cartoni R, Praz M, Lamon S, Deriaz O, Crettenand A, Gobelet C, Rohmer P, Konzelmann M, Luthi F, Russell AP. Akt signalling through GSK-3beta, mTOR and Foxo1 is involved in human skeletal muscle hypertrophy and atrophy. J Physiol 576:923-933, 2006.
29. Li YP, Chen Y, John J, Moylan J, Jin B, Mann DL, Reid MB. TNF-alpha acts via p38 MAPK to stimulate expression of the ubiquitin ligase atrogin1/MAFbx in skeletal muscle. FASEB J 19:362-370, 2005.
30. Louis E, Raue U, Yang Y, Jemiolo B, Trappe S. Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103:1744-1751, 2007.
31. Machida S, Booth FW. Changes in signalling molecule levels in 10-day hindlimb immobilized rat muscles. Acta Physiol Scand 183:171-179, 2005.
32. Mamane Y, Petroulakis E, Rong L, Yoshida K, Ler LW, Sonenberg N. eIF4E-from translation to transformation. Oncogene 23:3172-3179, 2004.
33. Mascher H, Tannerstedt J, Brink-Elfegoun T, Ekblom B, Gustafsson T, Blomstrand E. Repeated resistance exercise training induces different changes in mRNA expression of MAFbx and MuRF-1 in human skeletal muscle. Am J Physiol Endocrinol Metab 294: E43-E51, 2008.
34. McFarlane C, Plummer E, Thomas M, Hennebry A, Ashby M, Ling N, Smith H, Sharma M, Kambadur R. Myostatin induces cachexia by activating the ubiquitin proteolytic system through an NF-kappaB-independent, FoxO1-dependent mechanism. J Cell Physiol 209:501-514, 2006.
35. Phillips SM, Glover EI, Rennie MJ. Alterations of protein turnover underlying disuse atrophy in human skeletal muscle. J Appl Physiol 107:645-654, 2009.
36. Reardon KA, Davis J, Kapsa RM, Choong P, Byrne E. Myostatin, insulin-like growth factor-1, and leukemia inhibitory factor mRNAs are upregulated in chronic human disuse muscle atrophy. Muscle Nerve 24:893-899, 2001.
37. Rhoads RE. Signal transduction pathways that regulate eukaryotic protein synthesis. J Biol Chem 274:30337-30340, 1999.
38. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ. Mediation of IGF-1-induced skeletal myotube hypertrophy by PI (3) K/Akt/mTOR and PI (3) K/Akt/GSK3 pathways. Nat Cell Biol 3:1009-1013, 2001.
39. Sacheck JM, Hyatt JP, Raffaello A, Jagoe RT, Roy RR, Edgerton VR, Lecker SH, Goldberg AL. Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J 21:140-155, 2007.
40. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399-412, 2004.
41. Schuelke M, Wagner KR, Stolz LE, Hubner C, Riebel T, Komen W, Braun T, Tobin JF, Lee SJ. Myostatin mutation associated with gross muscle hypertrophy in a child. N Engl J Med 350:2682-2688, 2004.
42. Stevenson EJ, Giresi PG, Koncarevic A, Kandarian SC. Global analysis of gene expression patterns during disuse atrophy in rat skeletal muscle. J Physiol 551:33-48, 2003.
43. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395-403, 2004.
44. Tesch PA, Trieschmann JT, Ekberg A. Hypertrophy of chronically unloaded muscle subjected to resistance exercise. J Appl Physiol 96:1451-1458, 2004.
45. Tesch PA, von Walden F, Gustafsson T, Linnehan RM, Trappe TA. Skeletal muscle proteolysis in response to short-term unloading in humans. J Appl Physiol 105:902-906, 2008.
46. Trappe TA, Burd NA, Louis ES, Lee GA, Trappe SW. Influence of concurrent exercise or nutrition countermeasures on thigh and calf muscle size and function during 60 days of bed rest in women. Acta Physiol (Oxf) 191:147-159, 2007.
47. Urso ML, Scrimgeour AG, Chen YW, Thompson PD, Clarkson PM. Analysis of human skeletal muscle after 48 h immobilization reveals alterations in mRNA and protein for extracellular matrix components. J Appl Physiol 101:1136-1148, 2006.
48. Wehling M, Cai B, Tidball JG. Modulation of myostatin expression during modified muscle use. FASEB J 14:103-110, 2000.
49. Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, McPherron AC, Wolfman NM, Lee SJ. Induction of cachexia in mice by systemically administered myostatin. Science 296:1486-1488, 2002.