Nandrolone normalizes determinants of muscle mass and fiber type after spinal cord injury

Journal of Neurotrauma

Volumn 29, Issue 8, 2012, Pages 1663-1675

  Wu, Yong ^a   Zhao, Jingbo ^a   Zhao, Weidong ^a   Pan, Jiangping ^a   Bauman, William A ^a,b   Cardozo, Christopher P ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

muscle atrophy; nandrolone; oxidative metabolism; PGC 1 ; slow twitch muscle; spinal cord injury

Indexed keywords

ACTIVIN RECEPTOR 2; AMOXICILLIN; ENROFLOXACIN; FOLLISTATIN; MESSENGER RNA; NANDROLONE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SMAD2 PROTEIN; SMAD3 PROTEIN; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG MEGADOSE; GASTROCNEMIUS MUSCLE; GENE; GENETIC TRANSCRIPTION; MALE; MUSCLE CELL; MUSCLE MASS; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PARALYSIS; RAT; SIGNAL TRANSDUCTION; SPINAL CORD TRANSSECTION; URINARY TRACT INFECTION;

ANDROGENS; ANIMALS; ATROPHY; MALE; MUSCLE, SKELETAL; MYOSTATIN; NANDROLONE; RATS; RATS, WISTAR; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; SMAD2 PROTEIN; SMAD3 PROTEIN; SPINAL CORD INJURIES; TESTOSTERONE; TRANSCRIPTION FACTORS;

EID: 84861994962     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.2203     Document Type: Article

References (49)

1. Adams, C.M., Suneja, M., Dudley-Javoroski, S., and Shields, RK. (2011). Altered mRNA expression after long-term soleus electrical stimulation training in humans with paralysis. Muscle Nerve 43, 65-75.
2. Akimoto, T., Pohnert, S.C., Li, P., Zhang, M., Gumbs, C., Rosenberg, P.B., Williams, R.S., and Yan, Z. (2005). Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J. Biol. Chem. 280, 19587-19593. (Pubitemid 41379480)
3. Baumann, A.P., Ibebunjo, C., Grasser, W.A., and Paralkar, V.M. (2003). Myostatin expression in age and denervation-induced skeletal muscle atrophy. J. Musculoskel. Neuronal Interact. 3, 8-16. (Pubitemid 36443178)
4. Bhasin, S., Woodhouse, L., Casaburi, R., Singh, A.B., Bhasin, D., Berman, N., Chen, X., Yarasheski, K.E., Magliano, L., Dzekov, C., Dzekov, J., Bross, R., Phillips, J., Sinha-Hikim, I., Shen, R., and Storer, T.W. (2001). Testosterone dose-response relationships in healthy young men. Am. J. Physiol. Endocrinol. Metab. 281, E1172-E1181.
5. Blount, A.L., Vaughan, J.M., Vale, W.W., and Bilezikjian, L.M. (2008). A Smad-binding element in intron 1 participates in activin-dependent regulation of the follistatin gene. J. Biol. Chem. 283, 7016-7026.
6. Bodine, S.C., Latres, E., Baumhueter, S., Lai, V.K., Nunez, L., Clarke, B.A., Poueymirou, W.T., Panaro, F.J., Na, E., Dharmarajan, K., Pan, Z.Q., Valenzuela, D.M., DeChiara, T.M., Stitt, T.N., Yancopoulos, G.D., and Glass, D.J. (2001). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708. (Pubitemid 33104839)
7. Demling, R.H., and DeSanti, L. (2003). Oxandrolone induced lean mass gain during recovery from severe burns is maintained after discontinuation of the anabolic steroid. Burns 29, 793-797. (Pubitemid 37433914)
8. Dudley-Javoroski, S., and Shields, R.K. (2008). Muscle and bone plasticity after spinal cord injury: review of adaptations to disuse and to electrical muscle stimulation. J. Rehabil. Res. Dev. 45, 283-296.
9. Ferrando, A.A., Sheffield-Moore, M., Yeckel, C.W., Gilkison, C., Jiang, J., Achacosa, A., Lieberman, S.A, Tipton, K., Wolfe, R.R., and Urban, R.J. (2002). Testosterone administration to older men improves muscle function: molecular and physiological mechanisms. Am. J. Physiol. Endocrinol. Metab. 282, E601-E607. (Pubitemid 34654776)
10. Finck, B.N., and Kelly, D.P. (2006). PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116, 615-622. (Pubitemid 43326866)
11. Furuno, K., Goodman, M.N., and Goldberg, A.L. (1990). Role of different proteolytic systems in the degradation of muscle proteins during denervation atrophy. J. Biol. Chem. 265, 8550-8557.
12. Glass, D.J. (2010). Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 225-229.
13. Gregory, C.M., Vandenborne, K., Huang, H.F., Ottenweller, J.E., and Dudley, G.A. (2003). Effects of testosterone replacement therapy on skeletal muscle after spinal cord injury. Spinal Cord 41, 23-28. (Pubitemid 36132539)
14. Hennebry, A., Berry, C., Siriett, V., O'Callaghan, P., Chau, L., Watson, T., Sharma, M., and Kambadur, R. (2009). Myostatin regulates fiber-type composition of skeletal muscle by regulating MEF2 and MyoD gene expression. Am. J. Physiol. Cell Physiol. 296, C525-C534.
15. Huang, H.F., Linsenmeyer, T.A., Li, M.T., Giglio, W., Anesetti, R., von Hagen, J., Ottenweller, J.E., Serenas, C., and Pogach, L. (1995). Acute effects of spinal cord injury on the pituitary-testicular hormone axis and Sertoli cell functions: a time course study. J. Androl. 16, 148-157.
16. Ibebunjo, C., Eash, J.K., Li, C., Ma, Q., and Glass, D.J. (2011). Voluntary running, skeletal muscle gene expression, and signaling inversely regulated by orchidectomy and testosterone replacement. Am. J. Physiol. Endocrinol. Metab. 300, E327-E340.
17. Jones, A., Hwang, D.J., Narayanan, R., Miller, D.D., and Dalton, J.T. (2010). Effects of a novel selective androgen receptor modulator on dexamethasone-induced and hypogonadism-induced muscle atrophy. Endocrinology 151, 3706-3719.
18. Kovacheva, E.L., Hikim, A.P., Shen, R., Sinha, I., and 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.
19. Lecker, S.H., Jagoe, R.T., Gilbert, A., Gomes, M., Baracos, V., Bailey, J., Price, S.R., Mitch, W.E., and Goldberg, A.L. (2004). Multiple types of skeletal muscle atrophy involve a common program of changes in gene expression. FASEB J. 18, 39-51. (Pubitemid 38076464)
20. Leger, B., Senese, R., Al-Khodairy, A.W., Deriaz, O., Gobelet, C., Giacobino, J.P., and Russell, A.P. (2009). 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.
21. Lima, S.C., Caierao, Q.M., Peviani, S.M., Russo, T.L., Somazz, M.C., Salvini, T.F., Teodori, R.M., and Minamoto, V.B. (2009). Muscle and nerve responses after different intervals of electrical stimulation sessions on denervated rat muscle. Am. J. Phys. Med. Rehabil. 88, 126-135.
22. Lin, J., Handschin, C., and Spiegelman, B.M. (2005). Metabolic control through the PGC-1 family of transcription coactivators. Cell Metab. 1, 361-370. (Pubitemid 43960626)
23. Lin, J., Wu, H., Tarr, P.T., Zhang, C.Y., Wu, Z., Boss, O., Michael, L.F., Puigserver, P., Isotani, E., Olson, E.N., Lowell, B.B., Bassel-Duby, R., and Spiegelman, B.M. (2002). Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 418, 797-801.
24. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. (Pubitemid 34164012)
25. Medina, R., Wing, S.S., Haas, A., and Goldberg, A.L. (1991). Activation of the ubiquitin-ATP-dependent proteolytic system in skeletal muscle during fasting and denervation atrophy. Biomed. Biochim. Acta. 50, 347-356.
26. Qin, W., Bauman, W.A., and Cardozo, C. (2010a). Bone and muscle loss after spinal cord injury: organ interactions. Ann. NY Acad. Sci. 1211, 66-84.
27. Qin, W., Pan, J., Bauman, W.A., and Cardozo, C.P. (2010b). Differential alterations in gene expression profiles contribute to time-dependent effects of nandrolone to prevent denervation atrophy. BMC Genomics 22, 596.
28. Qin, W., Pan, J., Wu, Y., Bauman, W.A., and Cardozo, C. (2010c). Protection against dexamethasone-induced muscle atrophy is related to modulation by testosterone of FOXO1 and PGC-1alpha. Biochem. Biophys. Res. Commun. 403, 473-478.
29. Ruegg, M.A., and Glass, D.J. (2011). Molecular mechanisms and treatment options for muscle wasting diseases. Annu. Rev. Pharmacol. Toxicol. 51, 373-395.
30. Ryan, A.S., Ivey, F.M., Prior, S., Li, G., and Hafer-Macko, C. (2011). Skeletal muscle hypertrophy and muscle myostatin reduction after resistive training in stroke survivors. Stroke 42, 416-420.
31. Sacheck, J.M., Hyatt, J.P., Raffaello, A., Jagoe, R.T., Roy, R.R., Edgerton, V.R., Lecker, S.H., and Goldberg, A.L. (2007). Rapid disuse and denervation atrophy involve transcriptional changes similar to those of muscle wasting during systemic diseases. FASEB J. 21, 140-155. (Pubitemid 46052553)
32. Sandri, M., Sandri, C., Gilbert, A., Skurk, C., Calabria, E., Picard, A., Walsh, K., Schiaffino, S., Lecker, S.H., and Goldberg, A.L. (2004). Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117, 399-412. (Pubitemid 38534545)
33. Sartori, R., Milan, G., Patron, M., Mammucari, C., Blaauw, B., Abraham, R., and Sandri, M. (2009). Smad2 and 3 transcription factors control muscle mass in adulthood. Am. J. Physiol. Cell Physiol. 296, C1248-C1257.
34. Schopp, L.H., Clark, M., Mazurek, M.O., Hagglund, K.J., Acuff, M.E., Sherman, A.K., and Childers, M.K. (2006). Testosterone levels among men with spinal cord injury admitted to inpatient rehabilitation. Am. J. Phys. Med. Rehabil. 85, 678-684; quiz 685-677.
35. Schroeder, E.T., Zheng, L., Yarasheski, K.E., Qian, D., Stewart, Y., Flores, C., Martinez, C., Terk, M., and Sattler, F.R. (2004). Treatment with oxandrolone and the durability of effects in older men. J. Appl. Physiol. 96, 1055-1062. (Pubitemid 38248683)
36. Singh, R., Bhasin, S., Braga, M., Artaza, J.N., Pervin, S., Taylor, W.E., Krishnan, V., Sinha, S.K., Rajavashisth, T.B., and Jasuja, R. (2009). 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.
37. Stitt, T.N., Drujan, D., Clarke, B.A., Panaro, F., Timofeyva, Y., Kline, W.O., Gonzalez, M., Yancopoulos, G.D., and Glass, D.J. (2004). The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol. Cell. 14, 395-403. (Pubitemid 38591410)
38. Taylor, D.C., Brooks, D.E., and Ryan, J.B. (1999). Anabolic-androgenic steroid administration causes hypertrophy of immobilized and nonimmobilized skeletal muscle in a sedentary rabbit model. Am. J. Sports Med. 27, 718-727.
39. Tsitouras, P.D., Zhong, Y.G., Spungen, A.M., and Bauman, W.A. (1995). Serum testosterone and growth hormone/insulin-like growth factor-I in adults with spinal cord injury. Horm. Metab. Res. 27, 287-292.
40. Ung, R.V., Rouleau, P., and Guertin, P.A. (2010). Effects of co-administration of clenbuterol and testosterone propionate on skeletal muscle in paraplegic mice. J. Neurotrauma 27, 1129-1142.
41. Urban, R.J., Bodenburg, Y.H., Gilkison, C., Foxworth, J., Coggan, A.R., Wolfe, R.R., and Ferrando, A. (1995). Testosterone administration to elderly men increases skeletal muscle strength and protein synthesis. Am. J. Physiol. 269, E820-E826. (Pubitemid 3005899)
42. Waddell, D.S., Baehr, L.M., van den Brandt, J., Johnsen, S.A., Reichardt, H.M., Furlow, J.D., and Bodine, S.C. (2008). The glucocorticoid receptor and Foxo1 synergistically activate the skeletal muscle atrophy associated Murf1 gene. Am. J. Physiol. Endocrinol. Metab. 295, E785-E797.
43. Wheeler, T.L., and Koohmaraie, M. (1999). The extent of proteolysis is independent of sarcomere length in lamb longissimus and psoas major. J. Anim. Sci. 77, 2444-2451. (Pubitemid 129558869)
44. Wimalawansa, S.M., Chapa, M.T., Wei, J.N., Westlund, K.N., Quast, M.J., and Wimalawansa, S.J. (1999). Reversal of weightlessness-induced musculoskeletal losses with androgens: quantification by MRI. J. Appl. Physiol. 86, 1841-1846. (Pubitemid 29275557)
45. Wu, Y., Zhao, W., Zhao, J., Zhang, Y., Qin, W., Pan, J., Bauman, W.A., Blitzer, R.D., and Cardozo, C. (2010). REDD1 is a major target of testosterone action in preventing dexamethasone-induced muscle loss. Endocrinology 151, 1050-1059.
46. Xu, T., Shen, Y., Pink, H., Triantafillou, J., Stimpson, S.A., Turnbull, P., and Han, B. (2004). Phosphorylation of p70s6 kinase is implicated in androgen-induced levator ani muscle anabolism in castrated rats. J. Steroid Biochem. Mol. Biol. 92, 447-454. (Pubitemid 40192528)
47. Zeman, R.J., Zhao, J., Zhang, Y., Zhao, W., Wen, X., Wu, Y., Pan, J., Bauman, W.A., and Cardozo, C. (2009). Differential skeletal muscle gene expression after upper or lower motor neuron transection. Pflugers Arch. 458, 525-535.
48. Zhao, W., Pan, J., Zhao, Z., Wu, Y., Bauman, W.A., and Cardozo, C.P. (2008a). Testosterone protects against dexamethasone-induced muscle atrophy, protein degradation and MAFbx upregulation. J. Steroid Biochem. Mol. Biol. 110, 125-129.
49. Zhao, J., Zhang, Y., Zhao, W., Wu, Y., Pan, J., Bauman, W.A., and Cardozo, C. (2008b). Effects of nandrolone on denervation atrophy depend upon time after nerve transection. Muscle Nerve 37, 42-49.