Androgen receptor polyglutamine repeat length affects receptor activity and C2C12 cell development

Physiological Genomics

Volumn 43, Issue 20, 2011, Pages 1135-1143

  Sheppard, Ryan L ^a   Spangenburg, Espen E ^a   Chin, Eva R ^a   Roth, Stephen M ^a  

^a UNIVERSITY OF MARYLAND   (United States)

Author keywords

Myoblast; Polymorphism; Skeletal muscle; Testosterone; Transcription

Indexed keywords

ANDROGEN RECEPTOR; CREATINE KINASE; MESSENGER RNA; MYOGENIN; MYOSTATIN; POLYGLUTAMINE; TESTOSTERONE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; COMPARATIVE STUDY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; GENOTYPE; HERITABILITY; MUSCLE FUNCTION; MYONUCLEAR FUSION INDEX; MYOTUBE; NONHUMAN; NUCLEOTIDE REPEAT; PRIORITY JOURNAL; REPEAT LENGTH; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSCRIPTION REGULATION; WILD TYPE;

ANIMALS; CELL DIFFERENTIATION; CELL FUSION; CELL LINE; CELL PROLIFERATION; CELL SHAPE; CULTURE MEDIA; GENE EXPRESSION REGULATION; HUMANS; IMMUNOHISTOCHEMISTRY; MICE; MUSCLE FIBERS, SKELETAL; MYOBLASTS; PEPTIDES; RECEPTORS, ANDROGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TESTOSTERONE; TRANSCRIPTION, GENETIC; TRANSFECTION; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 80054818524     PISSN: 10948341     EISSN: 15312267     Source Type: Journal    
DOI: 10.1152/physiolgenomics.00049.2011     Document Type: Article

References (43)

1. Alen P, Claessens F, Verhoeven G, Rombauts W, Peeters B. The androgen receptor amino-terminal domain plays a key role in p160 coactivator-stimulated gene transcription. Mol Cell Biol 19: 6085-6097, 1999.
2. Allan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI. Testosterone therapy prevents gain in visceral adipose tissue and loss of skeletal muscle in nonobese aging men. J Clin Endocrinol Metab 93: 139-146, 2008.
3. Beilin J, Ball EM, Favaloro JM, Zajac JD. Effect of the androgen receptor CAG repeat polymorphism on transcriptional activity: specificity in prostate and non-prostate cell lines. J Mol Endocrinol 25: 85-96, 2000.
4. Bhasin S, Storer TW, Berman N, Callegari C, Clevenger B, Phillips J, Bunnell TJ, Tricker R, Shirazi A, Casaburi R. The effects of supraphysiologic doses of testosterone on muscle size and strength in normal men. N Engl J Med 335: 1-7, 1996.
5. 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. Testosterone doseresponse relationships in healthy young men. Am J Physiol Endocrinol Metab 281: E1172-E1181, 2001.
6. Bhasin S, Woodhouse L, Storer TW. Proof of the effect of testosterone on skeletal muscle. J Endocrinol 170: 27-38, 2001.
7. 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.
8. Burd CJ, Petre CE, Moghadam H, Wilson EM, Knudsen KE. Cyclin D1 binding to the androgen receptor (AR) NH2-terminal domain inhibits activation function 2 association and reveals dual roles for AR corepression. Mol Endocrinol 19: 607-620, 2005.
9. Campbell BC, Gray PB, Eisenberg DT, Ellison P, Sorenson MD. Androgen receptor CAG repeats and body composition among Ariaal men. Int J Androl 32: 140-148, 2009.
10. Caravatti M, Perriard JC, Eppenberger HM. Developmental regulation of creatine kinase isoenzymes in myogenic cell cultures from chicken. Biosynthesis of creatine kinase subunits M and B. J Biol Chem 254: 1388-1394, 1979.
11. Chamberlain NL, Driver ED, Miesfeld RL. The length and location of CAG trinucleotide repeats in the androgen receptor N-terminal domain affect transactivation function. Nucl Acids Res 22: 3181-3186, 1994.
12. Chamberlain NL, Whitacre DC, Miesfeld RL. Delineation of two distinct type 1 activation functions in the androgen receptor aminoterminal domain. J Biol Chem 271: 26772-26778, 1996.
13. Chambon C, Duteil D, Vignaud A, Ferry A, Messaddeq N, Malivindi R, Kato S, Chambon P, Metzger D. Myocytic androgen receptor controls the strength but not the mass of limb muscles. Proc Natl Acad Sci USA 107: 14327-14332, 2010.
14. Dejager S, Bry-Gauillard H, Bruckert E, Eymard B, Salachas F, LeGuern E, Tardieu S, Chadarevian R, Giral P, Turpin G. A comprehensive endocrine description of Kennedy's disease revealing androgen insensitivity linked to CAG repeat length. J Clin Endocrinol Metab 87: 3893-3901, 2002.
15. Diel P, Baadners D, Schlupmann K, Velders M, Schwarz JP. C2C12 myoblastoma cell differentiation and proliferation is stimulated by androgens and associated with a modulation of myostatin and Pax7 expression. J Mol Endocrinol 40: 231-241, 2008.
16. Diel P, Friedel A, Geyer H, Kamber M, Laudenbach-Leschowsky U, Schanzer W, Thevis M, Vollmer G, Zierau O. Characterisation of the pharmacological profile of desoxymethyltestosterone (Madol), a steroid misused for doping. Toxicol Lett 169: 64-71, 2007.
17. Edwards A, Hammond HA, Jin L, Caskey CT, Chakraborty R. Genetic variation at five trimeric and tetrameric tandem repeat loci in four human population groups. Genomics 12: 241-253, 1992.
18. Fu R, Liu J, Fan J, Li R, Li D, Yin J, Cui S. Novel evidence that testosterone promotes cell proliferation and differentiation via G proteincoupled receptors in the rat L6 skeletal muscle myoblast cell line. J Cell Physiol [Epub ahead of print].
19. Giovannucci E, Platz EA, Stampfer MJ, Chan A, Krithivas K, Kawachi I, Willett WC, Kantoff PW. The CAG repeat within the androgen receptor gene and benign prostatic hyperplasia. Urology 53: 121-125, 1999.
20. Giovannucci E, Stampfer MJ, Krithivas K, Brown M, Dahl D, Brufsky A, Talcott J, Hennekens CH, Kantoff PW. The CAG repeat within the androgen receptor gene and its relationship to prostate cancer. Proc Natl Acad Sci USA 94: 3320-3323, 1997.
21. Hong MH, Sun H, Jin CH, Chapman M, Hu J, Chang W, Burnett K, Rosen J, Negro-Vilar A, Miner JN. Cell-specific activation of the human skeletal alpha-actin by androgens. Endocrinology 149: 1103-1112, 2008.
22. Janne OA, Moilanen AM, Poukka H, Rouleau N, Karvonen U, Kotaja N, Hakli M, Palvimo JJ. Androgen-receptor-interacting nuclear proteins. Biochem Soc Trans 28: 401-405, 2000.
23. Jimenez A, Davies J. Expression of a transposable antibiotic resistance element in Saccharomyces. Nature 287: 869-871, 1980.
24. Kasper S, Rennie PS, Bruchovsky N, Lin L, Cheng H, Snoek R, Dahlman-Wright K, Gustafsson JA, Shiu RP, Sheppard PC, Matusik RJ. Selective activation of the probasin androgen-responsive region by steroid hormones. J Mol Endocrinol 22: 313-325, 1999.
25. Katznelson L, Finkelstein JS, Schoenfeld DA, Rosenthal DI, Anderson EJ, Klibanski A. Increase in bone density and lean body mass during testosterone administration in men with acquired hypogonadism. J Clin Endocrinol Metab 81: 4358-4365, 1996.
26. Krithivas K, Yurgalevitch SM, Mohr BA, Wilcox CJ, Batter SJ, Brown M, Longcope C, McKinlay JB, Kantoff PW. Evidence that the CAG repeat in the androgen receptor gene is associated with the agerelated decline in serum androgen levels in men. J Endocrinol 162: 137-142, 1999.
27. MacLean HE, Chiu WS, Notini AJ, Axell AM, Davey RA, McManus JF, Ma C, Plant DR, Lynch GS, Zajac JD. Impaired skeletal muscle development and function in male, but not female, genomic androgen receptor knockout mice. FASEB J 22: 2676-2689, 2008.
28. Markus SM, Taneja SS, Logan SK, Li W, Ha S, Hittelman AB, Rogatsky I, Garabedian MJ. Identification and characterization of ART-27, a novel coactivator for the androgen receptor N terminus. Mol Biol Cell 13: 670-682, 2002.
29. Megeney LA, Rudnicki MA. Determination versus differentiation and the MyoD family of transcription factors. Biochem Cell Biol 73: 723-732, 1995.
30. 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.
31. Miller KK, Biller BM, Beauregard C, Lipman JG, Jones J, Schoenfeld D, Sherman JC, Swearingen B, Loeffler J, Klibanski A. Effects of testosterone replacement in androgen-deficient women with hypopituitarism: a randomized, double-blind, placebo-controlled study. J Clin Endocrinol Metab 91: 1683-1690, 2006.
32. Nenonen H, Bjork C, Skjaerpe PA, Giwercman A, Rylander L, Svartberg J, Giwercman YL. CAG repeat number is not inversely associated with androgen receptor activity in vitro. Mol Hum Reprod 16: 153-157, 2010.
33. Nielsen TL, Hagen C, Wraae K, Bathum L, Larsen R, Brixen K, Andersen M. The impact of the CAG repeat polymorphism of the androgen receptor gene on muscle and adipose tissues in 20-29-year-old Danish men: Odense Androgen Study. Eur J Endocrinol 162: 795-804, 2010.
34. Perriard JC, Caravatti M, Perriard ER, Eppenberger HM. Quantitation of creatine kinase isoenzyme transition in differentiating chicken embryonic breast muscle and myogenic cell cultures by immunoadsorption. Arch Biochem Biophys 191: 90-100, 1978.
35. Rogozkin V. Metabolic effects of anabolic steroid on skeletal muscle. Med Sci Sports 11: 160-163, 1979.
36. Sabourin LA, Girgis-Gabardo A, Seale P, Asakura A, Rudnicki MA. Reduced differentiation potential of primary MyoD-/- myogenic cells derived from adult skeletal muscle. J Cell Biol 144: 631-643, 1999.
37. Sabourin LA, Rudnicki MA. The molecular regulation of myogenesis. Clin Genet 57: 16-25, 2000.
38. Sattler FR, Castaneda-Sceppa C, Binder EF, Schroeder ET, Wang Y, Bhasin S, Kawakubo M, Stewart Y, Yarasheski KE, Ulloor J, Colletti P, Roubenoff R, Azen SP. Testosterone and growth hormone improve body composition and muscle performance in older men. J Clin Endocrinol Metab 94: 1991-2001, 2009.
39. Shank LC, Paschal BM. Nuclear transport of steroid hormone receptors. Crit Rev Eukaryot Gene Expr 15: 49-73, 2005.
40. Tut TG, Ghadessy FJ, Trifiro MA, Pinsky L, Yong EL. Long polyglutamine tracts in the androgen receptor are associated with reduced transactivation, impaired sperm production, and male infertility. J Clin Endocrinol Metab 82: 3777-3782, 1997.
41. Vlahopoulos S, Zimmer WE, Jenster G, Belaguli NS, Balk SP, Brinkmann AO, Lanz RB, Zoumpourlis VC, Schwartz RJ. Recruitment of the androgen receptor via serum response factor facilitates expression of a myogenic gene. J Biol Chem 280: 7786-7792, 2005.
42. Walsh S, Zmuda JM, Cauley JA, Shea PR, Metter EJ, Hurley BF, Ferrell RE, Roth SM. Androgen receptor CAG repeat polymorphism is associated with fat-free mass in men. J Appl Physiol 98: 132-137, 2005.
43. Zhou ZX, Sar M, Simental JA, Lane MV, Wilson EM. A liganddependent bipartite nuclear targeting signal in the human androgen receptor. Requirement for the DNA-binding domain and modulation by NH2- terminal and carboxyl-terminal sequences. J Biol Chem 269: 13115-13123, 1994.