Voluntary running, skeletal muscle gene expression, and signaling inversely regulated by orchidectomy and testosterone replacement

American Journal of Physiology - Endocrinology and Metabolism

Volumn 300, Issue 2, 2011, Pages

  Ibebunjo, Chikwendu ^a   Eash, John K ^a   Li, Christine ^a   Ma, QiCheng ^a   Glass, David J ^a  

^a NOVARTIS INSTITUTES FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

Aging; Andropause; Pathways; Sarcopenia

Indexed keywords

ATROGIN 1; MUSCLE RING FINGER 1 PROTEIN; SOMATOMEDIN BINDING PROTEIN 1; TESTOSTERONE; UBIQUITIN PROTEIN LIGASE E3;

ANDROGEN THERAPY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION; GENE EXPRESSION REGULATION; MALE; MOUSE; MUSCLE MASS; NONHUMAN; ORCHIECTOMY; PHYSICAL ACTIVITY, CAPACITY AND PERFORMANCE; PRIORITY JOURNAL; RUNNING; SIGNAL TRANSDUCTION; SKELETAL MUSCLE;

ANATOMY, CROSS-SECTIONAL; ANIMALS; BLOTTING, WESTERN; BODY WEIGHT; EATING; ENERGY METABOLISM; GENE EXPRESSION; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; MOTOR ACTIVITY; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; ORCHIECTOMY; ORGAN SIZE; PHYSICAL ENDURANCE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; RUNNING; SIGNAL TRANSDUCTION; TESTOSTERONE;

EID: 79251538909     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00402.2010     Document Type: Article

References (44)

1. Axell AM, MacLean HE, Plant DR, Harcourt LJ, Davis JA, Jimenez M, Handelsman DJ, Lynch GS, Zajac JD. Continuous testosterone administration prevents skeletal muscle atrophy and enhances resistance to fatigue in orchidectomized male mice. Am J Physiol Endocrinol Metab 291: E506-E516, 2006.
2. Baume N, Schumacher YO, Sottas PE, Bagutti C, Cauderay M, Mangin P, Saugy M. Effect of multiple oral doses of androgenic anabolic steroids on endurance performance and serum indices of physical stress in healthy male subjects. Eur J Appl Physiol 98: 329-340, 2006.
3. Beg S, Al-Khoury L, Cunningham GR. Testosterone replacement in men. Curr Opin Endocrinol Diabetes Obes 15: 364-370, 2008.
4. Brodsky IG, Balagopal P, Nair KS. Effects of testosterone replacement on muscle mass and muscle protein synthesis in hypogonadal men - a clinical research center study. J Clin Endocrinol Metab 81: 3469-3475, 1996.
5. Clarke BA, Drujan D, Willis MS, Murphy LO, Corpina RA, Burova E, Rakhilin SV, Stitt TN, Patterson C, Latres E, Glass DJ. The E3 Ligase MuRF1 degrades myosin heavy chain protein in dexamethasone-treated skeletal muscle. Cell Metab 6: 376-385, 2007.
6. Cohen S, Brault JJ, Gygi SP, Glass DJ, Valenzuela DM, Gartner C, Latres E, Goldberg AL. During muscle atrophy, thick, but not thin, filament components are degraded by MuRF1-dependent ubiquitylation. J Cell Biol 185: 1083-1095, 2009.
7. Copland JA, Pardini AW, Wood TG, Yin D, Green A, Bodenburg YH, Urban RJ, Stuart CA. IGF-1 controls GLUT3 expression in muscle via the transcriptional factor Sp1. Biochim Biophys Acta 1769: 631-640, 2007.
8. Daan S, Damassa D, Pittendrigh CS, Smith ER. An effect of castration and testosterone replacement on a circadian pacemaker in mice (Musmusculus). Proc Natl Acad Sci USA 72: 3744-3747, 1975.
9. Eason JM, Dodd SL, Powers SK. Use of anabolic steroids to attenuate the effects of glucocorticoids on the rat diaphragm. Phys Ther 83: 29-36, 2003.
10. Ferrando AA, Sheffield-Moore M, Yeckel CW, Gilkison C, Jiang J, Achacosa A, Lieberman SA, Tipton K, Wolfe RR, Urban RJ. Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am J Physiol Endocrinol Metab 282: E601-E607, 2002.
11. Freeman ER, Bloom DA, McGuire EJ. A brief history of testosterone. J Urol 165: 371-373, 2001.
12. Gentile MA, Nantermet PV, Vogel RL, Phillips R, Holder D, Hodor P, Cheng C, Dai H, Freedman LP, Ray WJ. Androgen-mediated improvement of body composition and muscle function involves a novel early transcriptional program including IGF1, mechano growth factor, and induction of {beta}-catenin. J Mol Endocrinol 44: 55-73, 2010.
13. Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37: 1974-1984, 2005.
14. Gonzalez-Cadavid NF, Taylor WE, Yarasheski K, Sinha-Hikim I, Ma K, Ezzat S, Shen R, Lalani R, Asa S, Mamita M, Nair G, Arver S, Bhasin S. Organization of the human myostatin gene and expression in healthy men and HIV-infected men with muscle wasting. Proc Natl Acad Sci USA 95: 14938-14943, 1998.
15. Hara H, Nolan PM, Scott MO, Bucan M, Wakayama Y, Fischbeck KH. Running endurance abnormality in mdx mice. Muscle Nerve 25: 207-211, 2002.
16. Hartgens F, Kuipers H. Effects of androgenic-anabolic steroids in athletes. Sports Med 34: 513-554, 2004.
17. Herbst KL, Bhasin S. Testosterone action on skeletal muscle. Curr Opin Clin Nutr Metab Care 7: 271-277, 2004.
18. Hoffman JR, Kraemer WJ, Bhasin S, Storer T, Ratamess NA, Haff GG, Willoughby DS, Rogol AD. Position stand on androgen and human growth hormone use. J Strength Cond Res 23: S1-S59, 2009.
19. Ishihara A, Roy RR, Ohira Y, Ibata Y, Edgerton VR. Hypertrophy of rat plantaris muscle fibers after voluntary running with increasing loads. J Appl Physiol 84: 2183-2189, 1998.
20. Jespersen JG, Nedergaard A, Andersen LL, Schjerling P, Andersen JL. Myostatin expression during human muscle hypertrophy and subsequent atrophy: increased myostatin with detraining. Scand J Med Sci Sports. In press.
21. Kang Z, Janne OA, Palvimo JJ. Coregulator recruitment and histone modifications in transcriptional regulation by the androgen receptor. Mol Endocrinol 18: 2633-2648, 2004.
22. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, Glass DJ. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280: 2737-2744, 2005.
23. Lee SJ, McPherron AC. Myostatin and the control of skeletal muscle mass. Curr Opin Genet Dev 9: 604-607, 1999.
24. Leger B, Senese R, Al-Khodairy AW, Deriaz O, Gobelet C, Giacobino JP, Russell AP. Atrogin-1, MuRF1, and FoXO, as well as phosphorylated GSK-3beta and 4E-BP1 are reduced in skeletal muscle of chronic spinal cord-injured patients. Muscle Nerve 40: 69-78, 2009.
25. Mendler L, Baka Z, Kovacs-Simon A, Dux L. Androgens negatively regulate myostatin expression in an androgen-dependent skeletal muscle. Biochem Biophys Res Commun 361: 237-242, 2007.
26. Milan G, Dalla Nora E, Pilon C, Pagano C, Granzotto M, Manco M, Mingrone G, Vettor R. Changes in muscle myostatin expression in obese subjects after weight loss. J Clin Endocrinol Metab 89: 2724-2727, 2004. (Pubitemid 38766356)
27. Montano M, Flanagan JN, Jiang L, Sebastiani P, Rarick M, LeBrasseur NK, Morris CA, Jasuja R, Bhasin S. Transcriptional profiling of testosterone- regulated genes in the skeletal muscle of human immunodeficiency virus-infected men experiencing weight loss. J Clin Endocrinol Metab 92: 2793-2802, 2007.
28. Noirez P, Ferry A. Effect of anabolic/androgenic steroids on myosin heavy chain expression in hindlimb muscles of male rats. Eur J Appl Physiol 81: 155-158, 2000.
29. Pitteloud N, Mootha VK, Dwyer AA, Hardin M, Lee H, Eriksson KF, Tripathy D, Yialamas M, Groop L, Elahi D, Hayes FJ. Relationship between testosterone levels, insulin sensitivity, and mitochondrial function in men. Diabetes Care 28: 1636-1642, 2005.
30. 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.
31. 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.
32. Shao C, Liu M, Wu X, Ding F. Time-dependent expression of myostatin RNA transcript and protein in gastrocnemius muscle of mice after sciatic nerve resection. Microsurgery 27: 487-493, 2007.
33. Singh R, Artaza JN, Taylor WE, Braga M, Yuan X, Gonzalez-Cadavid NF, Bhasin S. Testosterone inhibits adipogenic differentiation in 3T3-L1 cells: nuclear translocation of androgen receptor complex with beta-catenin and T-cell factor 4 may bypass canonical Wnt signaling to down-regulate adipogenic transcription factors. Endocrinology 147: 141-154, 2006.
34. Singh R, Bhasin S, Braga M, Artaza JN, Pervin S, Taylor WE, Krishnan V, Sinha SK, Rajavashisth TB, Jasuja R. Regulation of myogenic differentiation by androgens: cross talk between androgen receptor/beta-catenin and follistatin/transforming growth factor-beta signaling pathways. Endocrinology 150: 1259-1268, 2009.
35. 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.
36. Szustakowski JD, Lee JH, Marrese CA, Kosinski PA, Nirmala NR, Kemp DM. Identification of novel pathway regulation during myogenic differentiation. Genomics 87: 129-138, 2006.
37. Tamaki T, Uchiyama S, Uchiyama Y, Akatsuka A, Roy RR, Edgerton VR. Anabolic steroids increase exercise tolerance. Am J Physiol Endocrinol Metab 280: E973-E981, 2001.
38. Van Zyl CG, Noakes TD, Lambert MI. Anabolic-androgenic steroid increases running endurance in rats. Med Sci Sports Exerc 27: 1385-1389, 1995.
39. Vermeulen A, Goemaere S, Kaufman JM. Testosterone, body composition and aging. J Endocrinol Invest 22: 110-116, 1999.
40. Witte AV, Floel A, Stein P, Savli M, Mien LK, Wadsak W, Spindelegger C, Moser U, Fink M, Hahn A, Mitterhauser M, Kletter K, Kasper S, Lanzenberger R. Aggression is related to frontal serotonin-1A receptor distribution as revealed by PET in healthy subjects. Hum Brain Mapp 30: 2558-2570, 2009.
41. Wu MV, Manoli DS, Fraser EJ, Coats JK, Tollkuhn J, Honda S, Harada N, Shah NM. Estrogen masculinizes neural pathways and sex-specific behaviors. Cell 139: 61-72, 2009.
42. Yarasheski KE, Bhasin S, Sinha-Hikim I, Pak-Loduca J, Gonzalez-Cadavid NF. Serum myostatin-immunoreactive protein is increased in 60-92 year old women and men with muscle wasting. J Nutr Health Aging 6: 343-348, 2002. (Pubitemid 36118984)
43. Zachwieja JJ, Smith SR, Sinha-Hikim I, Gonzalez-Cadavid N, Bhasin S. Plasma myostatin-immunoreactive protein is increased after prolonged bed rest with low-dose T3 administration. J Gravit Physiol 6: 11-15, 1999.
44. Zhao W, Pan J, Zhao Z, Wu Y, Bauman WA, Cardozo CP. Testosterone protects against dexamethasone-induced muscle atrophy, protein degradation and MAFbx upregulation. J Steroid Biochem Mol Biol 110: 125-129, 2008.