Androgen signaling in myocytes contributes to the maintenance of muscle mass and fiber type regulation but not to muscle strength or fatigue

Endocrinology

Volumn 150, Issue 8, 2009, Pages 3558-3566

  Ophoff, Jill ^a   Van Proeyen, Karen ^b   Callewaert, Filip ^a   De Gendt, Karel ^a   De Bock, Katrien ^b   Vanden Bosch, An ^a   Verhoeven, Guido ^a   Hespel, Peter ^b   Vanderschueren, Dirk ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b University Hospitals Leuven   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; CREATINE KINASE; GLYCOGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BODY WEIGHT; CONTROLLED STUDY; CORTICAL BONE; FEMALE; GLYCOGEN MUSCLE LEVEL; HOMEOSTASIS; INTRAABDOMINAL FAT; LEAN BODY WEIGHT; MALE; MOUSE; MUSCLE CELL; MUSCLE CONTRACTILITY; MUSCLE FATIGUE; MUSCLE FUNCTION; MUSCLE MASS; MUSCLE STRENGTH; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SKELETAL MUSCLE; TRABECULAR BONE;

ABSORPTIOMETRY, PHOTON; ANIMALS; BLOTTING, WESTERN; CREATINE KINASE, MM FORM; FEMALE; GLYCOGEN; IMMUNOHISTOCHEMISTRY; INTRA-ABDOMINAL FAT; MALE; MICE; MICE, KNOCKOUT; MICE, MUTANT STRAINS; MICROSCOPY, FLUORESCENCE; MUSCLE CELLS; MUSCLE FATIGUE; MUSCLE FIBERS, SKELETAL; MUSCLE STRENGTH; MUSCLES; RECEPTORS, ANDROGEN; SATELLITE CELLS, SKELETAL MUSCLE; SUCCINATE DEHYDROGENASE; X-RAY MICROTOMOGRAPHY;

EID: 67651146640     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2008-1509     Document Type: Article

References (52)

1. Gruenewald DA, Matsumoto AM 2003 Testosterone supplementation therapy for older men: potential benefits and risks. J Am Geriatr Soc 51:101-115
2. Bhasin S, Calof OM, Storer TW, Lee ML, Mazer NA, Jasuja R, Montori VM, Gao W, Dalton JT 2006 Drug insight: testosterone and selective androgen receptor modulators as anabolic therapies for chronic illness and aging. Nat Clin Pract Endocrinol Metab 2:146-159
3. Bhasin S, Woodhouse L, Casaburi R, Singh AB, Mac RP, Lee M, Yarasheski KE, Sinha-Hikim I, Dzekov C, Dzekov J, Magliano L, Storer TW 2005 Older men are as responsive as young men to the anabolic effects of graded doses of testosterone on the skeletal muscle. J Clin Endocrinol Metab 90:678-688
4. Bhasin S, Woodhouse L, Casaburi R, Singh AB, Bhasin D, Berman N, Chen X, Yarasheski KE, Magliano L, Dzekov C, Dzekov J, Bross R, Phillips J, Sinha-Hikim I, Shen R, Storer TW 2001 Testosterone dose-response relationships in healthy young men. Am J Physiol Endocrinol Metab 281:E1172-E1181
5. Isidori AM, Giannetta E, Greco EA, Gianfrilli D, Bonifacio V, Isidori A, Lenzi A, Fabbri A 2005 Effects of testosterone on body composition, bone metabolism and serum lipid profile in middle-aged men: a meta-analysis. Clin Endocrinol (Oxf) 63:280-293
6. Storer TW, Magliano L, Woodhouse L, Lee ML, Dzekov C, Dzekov J, Casaburi R, Bhasin S 2003 Testosterone dose-dependently increases maximal voluntary strength and leg power, but does not affect fatigability or specific tension. J Clin Endocrinol Metab 88:1478-1485
7. Ferrando AA, Sheffield-Moore M, Yeckel CW, Gilkison C, Jiang J, Achacosa A, Lieberman SA, Tipton K, Wolfe RR, Urban RJ 2002 Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am J Physiol Endocrinol Metab 282:E601-E607
8. Jasuja R, Ramaraj P, Mac RP, Singh AB, Storer TW, Artaza J, Miller A, Singh R, Taylor WE, Lee ML, Davidson T, Sinha-Hikim I, Gonzalez-Cadavid N, Bhasin S 2005 δ-4-Androstene-3,17-dione binds androgen receptor, promotes myogenesis in vitro, and increases serum testosterone levels, fat-free mass, and muscle strength in hypogonadal men. J Clin Endocrinol Metab 90:855-863
9. Bhasin S, Storer TW, Berman N, Yarasheski KE, Clevenger B, Phillips J, Lee WP, Bunnell TJ, Casaburi R 1997 Testosterone replacement increases fat-free mass and muscle size in hypogonadal men. J Clin Endocrinol Metab 82:407-413
10. Wang C, Eyre DR, Clark R, Kleinberg D, Newman C, Iranmanesh A, Veldhuis J, Dudley RE, Berman N, Davidson T, Barstow TJ, Sinow R, Alexander G, Swerdloff RS 1996 Sublingual testosterone replacement improves muscle mass and strength, decreases bone resorption, and increases bone formation markers in hypogonadal men - a clinical research center study. J Clin Endocrinol Metab 81:3654-3662
11. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A 1996 Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab 81:4358-4365
12. Brodsky IG, Balagopal P, Nair KS 1996 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
13. Brown M, Fisher JS, Hasser EM 2001 Gonadectomy and reduced physical activity: effects on skeletal muscle. Arch Phys Med Rehabil 82:93-97
14. Gao W, Reiser PJ, Coss CC, Phelps MA, Kearbey JD, Miller DD, Dalton JT 2005 Selective androgen receptor modulator treatment improves muscle strength and body composition and prevents bone loss in orchidectomized rats. Endocrinology 146:4887-4897
15. Axell AM, MacLean HE, Plant DR, Harcourt LJ, Davis JA, Jimenez M, Handelsman DJ, Lynch GS, Zajac JD 2006 Continuous testosterone administration prevents skeletal muscle atrophy and enhances resistance to fatigue in orchidectomized male mice. Am J Physiol Endocrinol Metab 291:E506-E516
16. Venken K, De Gendt K, Boonen S, Ophoff J, Bouillon R, Swinnen JV, Verhoeven G, Vanderschueren D 2006 Relative impact of androgen and estrogen receptor activation in the effects of androgens on trabecular and cortical bone in growing male mice: a study in the androgen receptor knockout mouse model. J Bone Miner Res 21:576-585
17. Altuwaijri S, Lee DK, Chuang KH, Ting HJ, Yang Z, Xu Q, Tsai MY, Yeh S, Hanchett LA, Chang HC, Chang C 2004 Androgen receptor regulates expression of skeletal muscle-specific proteins and muscle cell types. Endocrine 25: 27-32
18. Johansen JA, Breedlove SM, Jordan CL 2007 Androgen receptor expression in the levator ani muscle of male mice. J Neuroendocrinol 19:823-826
19. Sinha-Hikim I, Taylor WE, Gonzalez-Cadavid NF, Zheng W, Bhasin S 2004 Androgen receptor in humanskeletal muscle and cultured muscle satellite cells: up-regulation by androgen treatment. J Clin Endocrinol Metab 89:5245-5255
20. Monks DA, O'Bryant EL, Jordan CL 2004 Androgen receptor immunoreactivity in skeletal muscle: enrichment at the neuromuscular junction. J Comp Neurol 473:59-72
21. Singh R, Artaza JN, Taylor WE, Gonzalez-Cadavid NF, Bhasin S 2003 Androgens stimulate myogenic differentiation and inhibit adipogenesis in C3H 10T1/2 pluripotent cells through an androgen receptor-mediated pathway. Endocrinology 144:5081-5088
22. Lee DK 2002 Androgen receptor enhances myogenin expression and accelerates differentiation. Biochem Biophys Res Commun 294:408-413
23. Doumit ME, Cook DR, Merkel RA 1996 Testosterone up-regulates androgen receptors and decreases differentiation of porcine myogenic satellite cells in vitro. Endocrinology 137:1385-1394
24. Antonio J, Wilson JD, George FW 1999 Effects of castration and androgen treatment on androgen-receptor levels in rat skeletal muscles. J Appl Physiol 87:2016-2019
25. Asarian L, Geary N 2006 Modulation of appetite by gonadal steroid hormones. Philos Trans R Soc Lond B Biol Sci 361:1251-1263
26. Borst SE, Conover CF 2006 Orchiectomized Fischer 344 male rat models body composition in hypogonadal state. Life Sci 79:411-415
27. Urban RJ, Bodenburg YH, Gilkison C, Foxworth J, Coggan AR, Wolfe RR, Ferrando A 1995 Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am J Physiol 269(5 Pt 1):E820-E826
28. Lewis MI, Horvitz GD, Clemmons DR, Fournier M 2002 Role of IGF-I and IGF-binding proteins within diaphragm muscle in modulating the effects of nandrolone. Am J Physiol Endocrinol Metab 282:E483-E490
29. Mauras N, Hayes V, Welch S, Rini A, Helgeson K, Dokler M, Veldhuis JD, Urban RJ 1998 Testosterone deficiency in young men: marked alterations in whole body protein kinetics, strength, and adiposity. J Clin Endocrinol Metab 83:1886-1892
30. Li H, Wang J, Wilhelmsson H, Hansson A, Thoren P, Duffy J, Rustin P, Larsson NG 2000 Genetic modification of survival in tissue-specific knockout mice with mitochondrial cardiomyopathy. Proc Natl Acad Sci USA 97:3467-3472
31. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, Rustin P, Brüning JC, Kahn CR, Clayton DA, Barsh GS, Thorén P, Larsson NG 1999 Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet 21:133-137
32. De Gendt K, Swinnen JV, Saunders PT, Schoonjans L, Dewerchin M, Devos A, Tan K, Atanassova N, Claessens F, Lécureuil C, Heyns W, Carmeliet P, Guillou F, Sharpe RM, Verhoeven G 2004 A Sertoli cell-selective knockout of the androgen receptor causes spermatogenic arrest in meiosis. Proc Natl Acad Sci USA 101:1327-1332
33. Brüning JC, Michael MD, Winnay JN, Hayashi T, Hörsch D, Accili D, Goodyear LJ, Kahn CR 1998 A muscle-specific insulin receptor knockout exhibits features of the metabolic syndrome of NIDDM without altering glucose tolerance. Mol Cell 2:559-569
34. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, Rudnicki MA 2000 Pax7 is required for the specification of myogenic satellite cells. Cell 102:777-786
35. Callewaert F, Venken K, Ophoff J, De Gendt K, Torcasio A, van Lenthe GH, Van Oosterwyck H, Boonen S, Bouillon R, Verhoeven G, Vanderschueren D 2009 Differential regulation of bone and body composition in male mice with combined inactivation of androgen and estrogen receptor-α. FASEB J 23:232-240
36. Lowry O, Passoneau J 1972 A flexible system of enzymatic analysis. New York: Academic Press
37. Snyder PJ, Peachey H, Berlin JA, Hannoush P, Haddad G, Dlewati A, Santanna J, Loh L, Lenrow DA, Holmes JH, Kapoor SC, Atkinson LE, Strom BL 2000 Effects of testosterone replacement in hypogonadal men. J Clin Endocrinol Metab 85:2670-2677
38. Frost HM 2003 Bone's mechanostat: a 2003 update. Anat Rec A Discov Mol Cell Evol Biol 275:1081-1101
39. Hayes A, Williams DA 1996 Beneficial effects of voluntary wheel running on the properties of dystrophic mouse muscle. J Appl Physiol 80:670-679
40. Ryder JW, Bassel-Duby R, Olson EN, Zierath JR 2003 Skeletal muscle reprogramming by activation of calcineurin improves insulin action on metabolic pathways. J Biol Chem 278:44298-44304
41. Hickey MS, Carey JO, Azevedo JL, Houmard JA, Pories WJ, Israel RG, Dohm GL 1995 Skeletal muscle fiber composition is related to adiposity and in vitro glucose transport rate in humans. Am J Physiol 268(3 Pt 1):E453-E457
42. Tanner CJ, Barakat HA, Dohm GL, Pories WJ, MacDonald KG, Cunningham PR, Swanson MS, Houmard JA 2002 Muscle fiber type is associated with obesity and weight loss. Am J Physiol Endocrinol Metab 282:E1191-E1196
43. Sinha-Hikim I, Artaza J, Woodhouse L, Gonzalez-Cadavid N, Singh AB, Lee MI, Storer TW, Casaburi R, Shen R, Bhasin S 2002 Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am J Physiol Endocrinol Metab 283:E154-E164
44. Snyder PJ, Peachey H, Hannoush P, Berlin JA, Loh L, Lenrow DA, Holmes JH, Dlewati A, Santanna J, Rosen CJ, Strom BL 1999 Effect of testosterone treatment on body composition and muscle strength in men over 65 years of age. J Clin Endocrinol Metab 84:2647-2653
45. MacLean HE, Chiu WS, Notini AJ, Axell AM, Davey RA, McManus JF, Ma C, Plant DR, Lynch GS, Zajac JD 2008 Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J 22:2676-2689
46. Andrechek ER, Hardy WR, Girgis-Gabardo AA, Perry RL, Butler R, Graham FL, Kahn RC, Rudnicki MA, Muller WJ 2002 ErbB2 is required for muscle spindle and myoblast cell survival. Mol Cell Biol 22:4714-4722
47. Gu H, Marth JD, Orban PC, Mossmann H, Rajewsky K 1994 Deletion of a DNA polymerase β gene segment in T cells using cell type-specific gene targeting. Science 265:103-106
48. Campion DR 1984 The muscle satellite cell: a review. Int Rev Cytol 87:225-251
49. Stickland NC, O'Shaughnessy PJ 1994 The influence of male-specific genes on female muscle fiber types: studies on the sex-reversed (Sxr) mouse. J Exp Zool 269:378-382
50. Simoneau JA, Bouchard C 1989 Human variation in skeletal muscle fiber-type proportion and enzyme activities. Am J Physiol 257(4 Pt 1):E567-E572
51. Staron RS, Hagerman FC, Hikida RS, Murray TF, Hostler DP, Crill MT, Ragg KE, Toma K 2000 Fiber type composition of the vastus lateralis muscle of young men and women. J Histochem Cytochem 48:623-629
52. Fan W, Yanase T, Nomura M, Okabe T, Goto K, Sato T, Kawano H, Kato S, Nawata H 2005 Androgen receptor null male mice develop late-onset obesity caused by decreased energy expenditure and lipolytic activity but show normal insulin sensitivity with high adiponectin secretion. Diabetes 54:1000-1008