Testosterone enables growth and hypertrophy in fusion impaired myoblasts that display myotube atrophy: deciphering the role of androgen and IGF-I receptors

Biogerontology

Volumn 17, Issue 3, 2016, Pages 619-639

  Hughes, David C ^a,b   Stewart, Claire E ^a   Sculthorpe, Nicholas ^c   Dugdale, Hannah F ^a   Yousefian, Farzad ^a   Lewis, Mark P ^d   Sharples, Adam P ^a  

^a LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF THE WEST OF SCOTLAND   (United Kingdom)

^d LOUGHBOROUGH UNIVERSITY   (United Kingdom)

Author keywords

Aging; Akt; Androgens; IGF I; Muscle; Satellite cell; Testosterone

Indexed keywords

AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; ANDROGEN RECEPTOR; FLUTAMIDE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PICROPODOPHYLLIN; PROTEIN KINASE B; SOMATOMEDIN C RECEPTOR; TESTOSTERONE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; GENE; GENE EXPRESSION; IGF IR GENE; MOUSE; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MYOD GENE; MYOGENIN GENE; MYOSTATIN GENE; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; SKELETAL MYOBLAST; TRANSCRIPTION REGULATION; ANIMAL; CELL FUSION; CELL LINE; CELL PROLIFERATION; HYPERTROPHY; METABOLISM; MYOBLAST; PATHOLOGY; PHYSIOLOGY; SKELETAL MUSCLE CELL;

ANIMALS; CELL FUSION; CELL LINE; CELL PROLIFERATION; HYPERTROPHY; MICE; MUSCLE FIBERS, SKELETAL; MYOBLASTS; RECEPTOR, IGF TYPE 1; RECEPTORS, ANDROGEN; TESTOSTERONE;

EID: 84946145691     PISSN: 13895729     EISSN: 15736768     Source Type: Journal    
DOI: 10.1007/s10522-015-9621-9     Document Type: Article

References (51)

1. Adi S, Bin-Abbas B, Wu N-Y, Rosenthal SM (2002) Early stimulation and late inhibition of extracellular signal-regulated kinase 1/2 phosphorylation by IGF-I: a potential mechanism mediating the switch in IGF-I action on skeletal muscle cell differentiation. Endocrinology 143:511–516
2. Altuwaijri S, Lee DK, Chuang K-H, Ting H-J, Yang Z, Xu Q, Tsai M-Y, Yeh S, Hanchett LA, Chang H-C (2004) Androgen receptor regulates expression of skeletal muscle-specific proteins and muscle cell types. Endocrine 25:27–32
3. Amthor H, Nicholas G, McKinnell I, Kemp CF, Sharma M, Kambadur R, Patel K (2004) Follistatin complexes Myostatin and antagonises Myostatin-mediated inhibition of myogenesis. Dev Biol 270:19–30
4. Atkinson RA, Srinivas-Shankar U, Roberts SA, Connolly MJ, Adams JE, Oldham JA, Wu FC, Seynnes OR, Stewart CE, Maganaris CN (2010) Effects of testosterone on skeletal muscle architecture in intermediate-frail and frail elderly men. J Gerontol Ser A 65:1215–1219
5. Baar K, Esser K (1999) Phosphorylation of p70S6 k correlates with increased skeletal muscle mass following resistance exercise. Am J Physiology-Cell Physiol 276:C120–C127
6. Basualto-Alarcón C, Jorquera G, Altamirano F, Jaimovich E, Estrada M (2013) Testosterone signals through mTOR and androgen receptor to induce muscle hypertrophy. Med Sci Sports Exerc 45:1712–1720
7. Bhasin S, Storer TW, Javanbakht M, Berman N, Yarasheski KE, Phillips J, Dike M, Sinha-Hikim I, Shen R, Hays RD (2000) Testosterone replacement and resistance exercise in HIV-infected men with weight loss and low testosterone levels. J Am Med Assoc 283:763–770
8. Bigot A, Jacquemin V, Debacq-Chainiaux F, Butler-Browne GS, Toussaint O, Furling D, Mouly V (2008) Replicative aging down-regulates the myogenic regulatory factors in human myoblasts. Biol Cell 100:189–199
9. Blau HM, Pavlath GK, Hardeman EC, Chiu C-P, Silberstein L, Webster SG, Miller SC, Webster C (1985) Plasticity of the differentiated state. Science 230:758–766
10. Braga M, Bhasin S, Jasuja R, Pervin S, Singh R (2012) Testosterone inhibits transforming growth factor-β signaling during myogenic differentiation and proliferation of mouse satellite cells: potential role of follistatin in mediating testosterone action. Mol Cell Endocrinol 350:39–52
11. Brodsky I, 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
12. Casaburi R, Bhasin S, Cosentino L, Porszasz J, Somfay A, Lewis MI, Fournier M, Storer TW (2004) Effects of testosterone and resistance training in men with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 170:870–878
13. De Naeyer H, Lamon S, Russell A, Everaert I, De Spaey A, Vanheel B, Taes Y, Derave W (2014) Androgenic and estrogenic regulation of Atrogin-1, MuRF1 and myostatin expression in different muscle types of male mice. Eur J Appl Physiol 114:1–11
14. Deane CS, Hughes DC, Sculthorpe N, Lewis MP, Stewart CE, Sharples AP (2013) Impaired hypertrophy in myoblasts is improved with testosterone administration. J Steroid Biochem Mol Biol 138:152–161
15. Dillon EL, Basra G, Horstman AM, Casperson SL, Randolph KM, Durham WJ, Urban RJ, Diaz-Arrastia C, Levine L, Hatch SS (2012) Cancer cachexia and anabolic interventions: a case report. J Cachexia Sarcopenia Muscle 3:253–263
16. Dubois V, Laurent MR, Sinnesael M, Cielen N, Helsen C, Clinckemalie L, Spans L, Gayan-Ramirez G, Deldicque L, Hespel P, Carmeliet G, Vanderschueren D, Claessens F (2014) A satellite cell-specific knockout of the androgen receptor reveals myostatin as a direct androgen target in skeletal muscle. FASEB J 26:26
17. 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
18. Jones NC, Fedorov YV, Rosenthal RS, Olwin BB (2001) ERK1/2 is required for myoblast proliferation but is dispensable for muscle gene expression and cell fusion. J Cell Physiol 186:104–115
19. Kawada S, Okuno M, Ishii N (2006) Testosterone causes decrease in the content of skeletal muscle myostatin. Int J Sport Health Sci 4:44–48
20. Kovacheva EL, Hikim APS, Shen R, Sinha I, Sinha-Hikim I (2010) Testosterone supplementation reverses sarcopenia in aging through regulation of myostatin, c-Jun NH2-terminal kinase, Notch, and Akt signaling pathways. Endocrinology 151:628–638
21. Lee DK (2002) Androgen receptor enhances myogenin expression and accelerates differentiation. Biochem Biophys Res Commun 294:408–413
22. Lees SJ, Rathbone CR, Booth FW (2006) Age-associated decrease in muscle precursor cell differentiation. Am J Physiol Cell Physiol 290:C609–C615
23. Lees SJ, Zwetsloot KA, Booth FW (2009) Muscle precursor cells isolated from aged rats exhibit an increased tumor necrosis factor- alpha response. Aging Cell 8:26–35
24. Leger B, Derave W, De Bock K, Hespel P, Russell AP (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res 11:163B–175B
25. −ΔΔCT method. Methods 25:402–408
26. MacLean HE, Chiu WM, Notini AJ, Axell A-M, 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
27. McCroskery S, Thomas M, Maxwell L, Sharma M, Kambadur R (2003) Myostatin negatively regulates satellite cell activation and self-renewal. The Journal of cell biology. 162:1135–1147
28. Mendler L, Baka Z, Kovács-Simon A, Dux L (2007) Androgens negatively regulate myostatin expression in an androgen-dependent skeletal muscle. Biochem Biophys Res Commun 361:237–242
29. Pietrangelo T, Puglielli C, Mancinelli R, Beccafico S, Fanò G, Fulle S (2009) Molecular basis of the myogenic profile of aged human skeletal muscle satellite cells during differentiation. Exp Gerontol 44:523–531
30. Rommel C, Bodine SC, Clarke BA, Rossman R, Nunez L, Stitt TN, Yancopoulos GD, Glass DJ (2001) 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
31. Sattler F, Bhasin S, He J, Chou C-P, Castaneda-Sceppa C, Yarasheski K, Binder E, Schroeder ET, Kawakubo M, Zhang A (2011) Testosterone threshold levels and lean tissue mass targets needed to enhance skeletal muscle strength and function: the HORMA trial. J Gerontol Ser A 66:122–129
32. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101–1108
33. Sculthorpe N, Solomon AM, Sinanan AC, Bouloux PM, Grace F, Lewis MP (2012) Androgens affect myogenesis in vitro and increase local IGF-1 expression. Med Sci Sports Exerc 44:610–615
34. Serra C, Bhasin S, Tangherlini F, Barton ER, Ganno M, Zhang A, Shansky J, Vandenburgh HH, Travison TG, Jasuja R (2011) The role of GH and IGF-I in mediating anabolic effects of testosterone on androgen-responsive muscle. Endocrinology 152:193–206
35. Serra C, Sandor NL, Jang H, Lee D, Toraldo G, Guarneri T, Wong S, Zhang A, Guo W, Jasuja R, Bhasin S (2013a) The effects of testosterone deprivation and supplementation on proteasomal and autophagy activity in the skeletal muscle of the male mouse: differential effects on high-androgen responder and low-androgen responder muscle groups. Endocrinology 154:4594–4606
36. Serra C, Tangherlini F, Rudy S, Lee D, Toraldo G, Sandor NL, Zhang A, Jasuja R, Bhasin S (2013b) Testosterone improves the regeneration of old and young mouse skeletal muscle. J Gerontol Ser A 68:17–26
37. Sharples AP, Al-Shanti N, Stewart CE (2010) C2 and C2C12 murine skeletal myoblast models of atrophic and hypertrophic potential: relevance to disease and ageing? J Cell Physiol 225:240–250
38. Sharples AP, Al-Shanti N, Lewis MP, Stewart CE (2011) Reduction of myoblast differentiation following multiple population doublings in mouse C2C12 cells: a model to investigate ageing? J Cell Biochem 112:3773–3785
39. Sharples AP, Player DJ, Martin NR, Mudera V, Stewart CE, Lewis MP (2012) Modelling in vivo skeletal muscle ageing in vitro using three-dimensional bioengineered constructs. Aging Cell 11:986–995
40. Sharples AP, Polydorou I, Hughes DC, Owens DJ, Hughes TM, Stewart CE (2015) Skeletal muscle cells possess a ‘memory’ of acute early life TNF-α exposure: role of epigenetic adaptation. Biogerontology. doi:10.1007/s10522-015-9604-x
41. Sheffield-Moore M, Urban RJ, Wolf SE, Jiang J, Catlin DH, Herndon DN, Wolfe RR, Ferrando AA (1999) Short-term oxandrolone administration stimulates net muscle protein synthesis in young men. J Clin Endocrinol Metab 84:2705–2711
42. Sinha I, Sinha-Hikim AP, Wagers AJ, Sinha-Hikim I (2014) Testosterone is essential for skeletal muscle growth in aged mice in a heterochronic parabiosis model. Cell Tissue Res 24:24
43. Sinha-Hikim I, Cornford M, Gaytan H, Lee ML, Bhasin S (2006) Effects of testosterone supplementation on skeletal muscle fiber hypertrophy and satellite cells in community-dwelling older men. J Clin Endocrinol Metab 91:3024–3033
44. Stevenson EJ, Koncarevic A, Giresi PG, Jackman RW, Kandarian SC (2005) Transcriptional profile of a myotube starvation model of atrophy. J Appl Physiol 98:1396–1406
45. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ (2009) Myostatin reduces Akt/TORC1/p70S6 K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiology-Cell Physiol 296:C1258–C1270
46. Wagner KR, Liu X, Chang X, Allen RE (2005) Muscle regeneration in the prolonged absence of myostatin. Proc Natl Acad Sci USA 102:2519–2524
47. Wannenes F, Caprio M, Gatta L, Fabbri A, Bonini S, Moretti C (2008) Androgen receptor expression during C2C12 skeletal muscle cell line differentiation. Mol Cell Endocrinol 292:11–19
48. Welle S, Brooks AI, Delehanty JM, Needler N, Thornton CA (2003) Gene expression profile of aging in human muscle. Physiol Genomics 14:149–159
49. White JP, Gao S, Puppa MJ, Sato S, Welle SL, Carson JA (2012) Testosterone regulation of Akt/mTORC1/FoxO3a signaling in skeletal muscle. Mol Cell Endocrinol 365:174–186
50. Wu Y, Bauman WA, Blitzer RD, Cardozo C (2010) Testosterone-induced hypertrophy of L6 myoblasts is dependent upon Erk and mTOR. Biochem Biophys Res Commun 400:679–683
51. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270:725–727