Denervation atrophy is independent from Akt and mTOR activation and is not rescued by myostatin inhibition

DMM Disease Models and Mechanisms

Volumn 7, Issue 4, 2014, Pages 471-481

  MacDonald, Elizabeth M ^a   Andres Mateos, Eva ^a   Mejias, Rebeca ^a   Simmers, Jessica L ^a   Mi, Ruifa ^a   Park, Jae Sung ^a   Ying, Stephanie ^a   Hoke, Ahmet ^a   Lee, Se Jin ^a   Cohn, Ronald D ^a,b  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOSPITAL FOR SICK CHILDREN   (Canada)

Author keywords

Denervation atrophy; Muscle atrophy pathophysiology; Myostatin; Skeletal muscle; TGF signaling

Indexed keywords

MAMMALIAN TARGET OF RAPAMYCIN; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; MYOSTATIN; PROTEIN KINASE B; RAPAMYCIN; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; TRANSFORMING GROWTH FACTOR BETA; ACTIVIN RECEPTOR 2; ACTIVIN RECEPTOR TYPE II-B; BIOLOGICAL MARKER; PROTEIN SERINE THREONINE KINASE; SERUM-INDUCIBLE KINASE; TARGET OF RAPAMYCIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; CONTROLLED STUDY; DENERVATION ATROPHY; ENZYME ACTIVATION; IMMOBILIZATION; MALE; MOUSE; MUSCLE ATROPHY; MUSCLE DENERVATION; MUSCLE GROWTH; MUSCLE HYPERTROPHY; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PATHOLOGY; PHENOTYPE;

ACTIVIN RECEPTORS, TYPE II; ANIMALS; AUTOPHAGY; BIOLOGICAL MARKERS; ENZYME ACTIVATION; MALE; MICE; MUSCLE DENERVATION; MUSCULAR ATROPHY; MYOSTATIN; PHENOTYPE; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; SIROLIMUS; TOR SERINE-THREONINE KINASES; TRANSFORMING GROWTH FACTOR BETA; UP-REGULATION;

EID: 84897945327     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.014126     Document Type: Article

References (63)

1. Andres-Mateos, E., Brinkmeier, H., Burks, T. N., Mejias, R., Files, D. C., Steinberger, M., Soleimani, A., Marx, R., Simmers, J. L., Lin, B. et al. (2013). Activation of serum/glucocorticoid-induced kinase 1 (SGK1) is important to maintain skeletal muscle homeostasis and prevent atrophy. EMBO Mol. Med. 5, 80-91.
2. Aoyama, T., Matsui, T., Novikov, M., Park, J., Hemmings, B. and Rosenzweig, A. (2005). Serum and glucocorticoid-responsive kinase-1 regulates cardiomyocyte survival and hypertrophic response. Circulation 111, 1652-1659. (Pubitemid 40525165)
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. Musculoskelet. Neuronal Interact. 3, 8-16. (Pubitemid 36443178)
4. 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. et al. (2001a). Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294, 1704-1708. (Pubitemid 33104839)
5. Bodine, S. C., Stitt, T. N., Gonzalez, M., Kline, W. O., Stover, G. L., Bauerlein, R., Zlotchenko, E., Scrimgeour, A., Lawrence, J. C., Glass, D. J. et al. (2001b). Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat. Cell Biol. 3, 1014-1019. (Pubitemid 34428747)
6. Bonetto, A., Aydogdu, T., Kunzevitzky, N., Guttridge, D. C., Khuri, S., Koniaris, L. G. and Zimmers, T. A. (2011). STAT3 activation in skeletal muscle links muscle wasting and the acute phase response in cancer cachexia. PLoS ONE 6, e22538.
7. Bonetto, A., Aydogdu, T., Jin, X., Zhang, Z., Zhan, R., Puzis, L., Koniaris, L. G. and Zimmers, T. A. (2012). JAK/STAT3 pathway inhibition blocks skeletal muscle wasting downstream of IL-6 and in experimental cancer cachexia. Am. J. Physiol. 303, E410-E421.
8. Brunet, A., Park, J., Tran, H., Hu, L. S., Hemmings, B. A. and Greenberg, M. E. (2001). Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol. Cell. Biol. 21, 952-965. (Pubitemid 32104742)
9. Burks, T. N., Andres-Mateos, E., Marx, R., Mejias, R., Van Erp, C., Simmers, J. L., Walston, J. D., Ward, C. W. and Cohn, R. D. (2011). Losartan restores skeletal muscle remodeling and protects against disuse atrophy in sarcopenia. Sci. Transl. Med. 3, 82ra37.
10. Caron, A. Z., Drouin, G., Desrosiers, J., Trensz, F. and Grenier, G. (2009). A novel hindlimb immobilization procedure for studying skeletal muscle atrophy and recovery in mouse. J. Appl. Physiol. 106, 2049-2059.
11. Cohn, R. D., van Erp, C., Habashi, J. P., Soleimani, A. A., Klein, E. C., Lisi, M. T., Gamradt, M., ap Rhys, C. M., Holm, T. M., Loeys, B. L. et al. (2007). Angiotensin II type 1 receptor blockade attenuates TGF-beta-induced failure of muscle regeneration in multiple myopathic states. Nat. Med. 13, 204-210.
12. Csibi, A., Tintignac, L. A., Leibovitch, M. P. and Leibovitch, S. A. (2008). eIF3-f function in skeletal muscles: to stand at the crossroads of atrophy and hypertrophy. Cell Cycle 7, 1698-1701. (Pubitemid 351988733)
13. Csibi, A., Leibovitch, M. P., Cornille, K., Tintignac, L. A. and Leibovitch, S. A. (2009). MAFbx/Atrogin-1 controls the activity of the initiation factor eIF3-f in skeletal muscle atrophy by targeting multiple C-terminal lysines. J. Biol. Chem. 284, 4413-4421.
14. Da Cruz, S., Parone, P. A., Lopes, V. S., Lillo, C., McAlonis-Downes, M., Lee, S. K., Vetto, A. P., Petrosyan, S., Marsala, M., Murphy, A. N. et al. (2012). Elevated PGC-1́ activity sustains mitochondrial biogenesis and muscle function without extending survival in a mouse model of inherited ALS. Cell Metab. 15, 778-786.
15. Egan, D., Kim, J., Shaw, R. J. and Guan, K. L. (2011). The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 7, 643-644.
16. Fenton, T. R. and Gout, I. T. (2011). Functions and regulation of the 70kDa ribosomal S6 kinases. Int. J. Biochem. Cell Biol. 43, 47-59.
17. Glass, D. J. (2010). Signaling pathways perturbing muscle mass. Curr. Opin. Clin. Nutr. Metab. Care 13, 225-229.
18. Gomes, M. D., Lecker, S. H., Jagoe, R. T., Navon, A. and Goldberg, A. L. (2001). Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy. Proc. Natl. Acad. Sci. USA 98, 14440-14445. (Pubitemid 33121410)
19. Goncalves, M. D., Pistilli, E. E., Balduzzi, A., Birnbaum, M. J., Lachey, J., Khurana, T. S. and Ahima, R. S. (2010). Akt deficiency attenuates muscle size and function but not the response to ActRIIB inhibition. PLoS ONE 5, e12707.
20. Guo, T., Jou, W., Chanturiya, T., Portas, J., Gavrilova, O. and McPherron, A. C. (2009). Myostatin inhibition in muscle, but not adipose tissue, decreases fat mass and improves insulin sensitivity. PLoS ONE 4, e4937.
21. Guo, T., Bond, N. D., Jou, W., Gavrilova, O., Portas, J. and McPherron, A. C. (2012). Myostatin inhibition prevents diabetes and hyperphagia in a mouse model of lipodystrophy. Diabetes 61, 2414-2423.
22. Inoki, K., Ouyang, H., Li, Y. and Guan, K. L. (2005). Signaling by target of rapamycin proteins in cell growth control. Microbiol. Mol. Biol. Rev. 69, 79-100. (Pubitemid 40358068)
23. Koncarevic, A., Kajimura, S., Cornwall-Brady, M., Andreucci, A., Pullen, A., Sako, D., Kumar, R., Grinberg, A. V., Liharska, K., Ucran, J. A. et al. (2012). A novel therapeutic approach to treating obesity through modulation of TGFβ signaling. Endocrinology 153, 3133-3146.
24. Lamming, D. W., Ye, L., Katajisto, P., Goncalves, M. D., Saitoh, M., Stevens, D. M., Davis, J. G., Salmon, A. B., Richardson, A., Ahima, R. S. et al. (2012). Rapamycin-induced insulin resistance is mediated by mTORC2 loss and uncoupled from longevity. Science 335, 1638-1643.
25. Langley, B., Thomas, M., Bishop, A., Sharma, M., Gilmour, S. and Kambadur, R. (2002). Myostatin inhibits myoblast differentiation by down-regulating MyoD expression. J. Biol. Chem. 277, 49831-49840. (Pubitemid 36014431)
26. Laplante, M. and Sabatini, D. M. (2012). mTOR signaling in growth control and disease. Cell 149, 274-293.
27. Lecker, S. H. and Goldberg, A. L. (2002). Slowing muscle atrophy: putting the brakes on protein breakdown. J. Physiol. 545, 729. (Pubitemid 36024415)
28. 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)
29. Lee, S. J. (2004). Regulation of muscle mass by myostatin. Annu. Rev. Cell Dev. Biol. 20, 61-86.
30. Lee, S. J., Reed, L. A., Davies, M. V., Girgenrath, S., Goad, M. E., Tomkinson, K. N., Wright, J. F., Barker, C., Ehrmantraut, G., Holmstrom, J. et al. (2005). Regulation of muscle growth by multiple ligands signaling through activin type II receptors. Proc. Natl. Acad. Sci. USA 102, 18117-18122. (Pubitemid 41798511)
31. Lee, S. B., Kim, S., Lee, J., Park, J., Lee, G., Kim, Y., Kim, J. M. and Chung, J. (2007). ATG1, an autophagy regulator, inhibits cell growth by negatively regulating S6 kinase. EMBO Rep. 8, 360-365. (Pubitemid 46511036)
32. Liu, M., Zhang, D., Shao, C., Liu, J., Ding, F. and Gu, X. (2007). Expression pattern of myostatin in gastrocnemius muscle of rats after sciatic nerve crush injury. Muscle Nerve 35, 649-656. (Pubitemid 46676854)
33. Ma, X. M. and Blenis, J. (2009). Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell Biol. 10, 307-318.
34. MacDonald, E. M. and Cohn, R. D. (2012). TGFβ signaling: its role in fibrosis formation and myopathies. Curr. Opin. Rheumatol. 24, 628-634.
35. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J. et al. (2007). FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6, 458-471. (Pubitemid 350163055)
36. McKinnell, I. W. and Rudnicki, M. A. (2004). Molecular mechanisms of muscle atrophy. Cell 119, 907-910. (Pubitemid 40037604)
37. McPherron, A. C. and Lee, S. J. (1997). Double muscling in cattle due to mutations in the myostatin gene. Proc. Natl. Acad. Sci. USA 94, 12457-12461. (Pubitemid 27492550)
38. Morine, K. J., Bish, L. T., Selsby, J. T., Gazzara, J. A., Pendrak, K., Sleeper, M. M., Barton, E. R., Lee, S. J. and Sweeney, H. L. (2010). Activin IIB receptor blockade attenuates dystrophic pathology in a mouse model of Duchenne muscular dystrophy. Muscle Nerve 42, 722-730.
39. Morissette, M. R., Cook, S. A., Buranasombati, C., Rosenberg, M. A. and Rosenzweig, A. (2009). Myostatin inhibits IGF-I-induced myotube hypertrophy through Akt. Am. J. Physiol. 297, C1124-C1132.
40. Morrison, B. M., Lachey, J. L., Warsing, L. C., Ting, B. L., Pullen, A. E., Underwood, K. W., Kumar, R., Sako, D., Grinberg, A., Wong, V. et al. (2009). A soluble activin type IIB receptor improves function in a mouse model of amyotrophic lateral sclerosis. Exp. Neurol. 217, 258-268.
41. O'Leary, M. F. and Hood, D. A. (2009). Denervation-induced oxidative stress and autophagy signaling in muscle. Autophagy 5, 230-231.
42. Ohsawa, Y., Hagiwara, H., Nakatani, M., Yasue, A., Moriyama, K., Murakami, T., Tsuchida, K., Noji, S. and Sunada, Y. (2006). Muscular atrophy of caveolin-3-deficient mice is rescued by myostatin inhibition. J. Clin. Invest. 116, 2924-2934. (Pubitemid 44684477)
43. Rahimi, R. A. and Leof, E. B. (2007). TGF-beta signaling: a tale of two responses. J. Cell. Biochem. 102, 593-608. (Pubitemid 47557414)
44. Ramos, F. J., Chen, S. C., Garelick, M. G., Dai, D. F., Liao, C. Y., Schreiber, K. H., MacKay, V. L., An, E. H., Strong, R., Ladiges, W. C. et al. (2012). Rapamycin reverses elevated mTORC1 signaling in lamin A/C-deficient mice, rescues cardiac and skeletal muscle function, and extends survival. Sci. Transl. Med. 4, 144ra103.
45. Rebbapragada, A., Benchabane, H., Wrana, J. L., Celeste, A. J. and Attisano, L. (2003). Myostatin signals through a transforming growth factor beta-like signaling pathway to block adipogenesis. Mol. Cell. Biol. 23, 7230-7242. (Pubitemid 37211004)
46. Richter, J. D. and Sonenberg, N. (2005). Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature 433, 477-480. (Pubitemid 40204297)
47. Rommel, C., Bodine, S. C., Clarke, B. A., Rossman, R., Nunez, L., Stitt, T. N., Yancopoulos, G. D. and Glass, D. J. (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. (Pubitemid 34428746)
48. Rüegg, M. A. and Glass, D. J. (2011). Molecular mechanisms and treatment options for muscle wasting diseases. Annu. Rev. Pharmacol. Toxicol. 51, 373-395.
49. 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)
50. 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)
51. Sarbassov, D. D., Ali, S. M., Sengupta, S., Sheen, J. H., Hsu, P. P., Bagley, A. F., Markhard, A. L. and Sabatini, D. M. (2006). Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22, 159-168.
52. 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. 296, C1248-C1257.
53. Schiaffino, S. and Mammucari, C. (2011). Regulation of skeletal muscle growth by the IGF1-Akt/PKB pathway: insights from genetic models. Skelet Muscle 1, 4.
54. Serrano, A. L., Mann, C. J., Vidal, B., Ardite, E., Perdiguero, E. and Muñoz-Cánoves, P. (2011). Cellular and molecular mechanisms regulating fibrosis in skeletal muscle repair and disease. Curr. Top. Dev. Biol. 96, 167-201.
55. Shao, C., Liu, M., Wu, X. and Ding, F. (2007). Time-dependent expression of myostatin RNA transcript and protein in gastrocnemius muscle of mice after sciatic nerve resection. Microsurgery 27, 487-493. (Pubitemid 47255166)
56. Sumner, C. J., Wee, C. D., Warsing, L. C., Choe, D. W., Ng, A. S., Lutz, C. and Wagner, K. R. (2009). Inhibition of myostatin does not ameliorate disease features of severe spinal muscular atrophy mice. Hum. Mol. Genet. 18, 3145-3152.
57. Trendelenburg, A. U., Meyer, A., Rohner, D., Boyle, J., Hatakeyama, S. and Glass, D. J. (2009). Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am. J. Physiol. 296, C1258-C1270.
58. Wagner, K. R., McPherron, A. C., Winik, N. and Lee, S. J. (2002). Loss of myostatin attenuates severity of muscular dystrophy in mdx mice. Ann. Neurol. 52, 832-836. (Pubitemid 35403195)
59. Wenz, T., Rossi, S. G., Rotundo, R. L., Spiegelman, B. M. and Moraes, C. T. (2009). Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging. Proc. Natl. Acad. Sci. USA 106, 20405-20410.
60. Ye, L., Varamini, B., Lamming, D. W., Sabatini, D. M. and Baur, J. A. (2012). Rapamycin has a biphasic effect on insulin sensitivity in C2C12 myotubes due to sequential disruption of mTORC1 and mTORC2. Front. Genet. 3, 177.
61. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H. and Goldberg, A. L. (2007). FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483. (Pubitemid 350163056)
62. Zhao, J., Brault, J. J., Schild, A. and Goldberg, A. L. (2008). Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy 4, 378-380. (Pubitemid 351458106)
63. Zhou, X., Wang, J. L., Lu, J., Song, Y., Kwak, K. S., Jiao, Q., Rosenfeld, R., Chen, Q., Boone, T., Simonet, W. S. et al. (2010). Reversal of cancer cachexia and muscle wasting by ActRIIB antagonism leads to prolonged survival. Cell 142, 531-543.