Mitochondrial Dysfunction Launches Dexamethasone-Induced Skeletal Muscle Atrophy via AMPK/FOXO3 Signaling

Molecular Pharmaceutics

Volumn 13, Issue 1, 2016, Pages 73-84

  Liu, Jing ^a   Peng, Yunhua ^a   Wang, Xun ^a   Fan, Yingying ^a   Qin, Chuan ^a   Shi, Le ^a   Tang, Ying ^a   Cao, Ke ^a   Li, Hua ^a   Long, Jiangang ^a   Liu, Jiankang ^a,b  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b TIANJIN UNIVERSITY OF SPORT   (China)

Author keywords

AMPK; Dexamethasone; Mitochondrial dysfunction; Muscle atrophy; Resveratrol

Indexed keywords

ATROGIN 1; DEXAMETHASONE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MUSCLE RING FINGER 1 PROTEIN; RESVERATROL; TRANSCRIPTION FACTOR FKHRL1; STILBENE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVATION; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE ATROPHY; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; METABOLISM; MUSCULAR ATROPHY; PATHOLOGY; SKELETAL MUSCLE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE; DEXAMETHASONE; MALE; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; MUSCULAR ATROPHY; SIGNAL TRANSDUCTION; STILBENES;

EID: 84953378606     PISSN: 15438384     EISSN: 15438392     Source Type: Journal    
DOI: 10.1021/acs.molpharmaceut.5b00516     Document Type: Article

References (59)

1. Tiao, G.; Fagan, J.; Roegner, V.; Lieberman, M.; Wang, J.-J.; Fischer, J. E.; Hasselgren, P.-O. Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids J. Clin. Invest. 1996, 97 (2) 339-348 10.1172/JCI118421
2. Wing, S. S.; Goldberg, A. L. Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting AJP: Endocrinol. Metab. 1993, 264 (4) E668-E676
3. Braun, T. P.; Zhu, X.; Szumowski, M.; Scott, G. D.; Grossberg, A. J.; Levasseur, P. R.; Graham, K.; Khan, S.; Damaraju, S.; Colmers, W. F.; Baracos, V. E.; Marks, D. L. Central nervous system inflammation induces muscle atrophy via activation of the hypothalamic-pituitary-adrenal axis J. Exp. Med. 2011, 208 (12) 2449-2463 10.1084/jem.20111020
4. Lecker, S. H.; Solomon, V.; Mitch, W. E.; Goldberg, A. L. Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states Journal of Nutrition 1999, 129 (1) 227S-237S
5. Hu, Z.; Wang, H.; Lee, I. H.; Du, J.; Mitch, W. E. Endogenous glucocorticoids and impaired insulin signaling are both required to stimulate muscle wasting under pathophysiological conditions in mice J. Clin. Invest. 2009, 119 (10) 3059-3069 10.1172/JCI38770
6. Schakman, O.; Kalista, S.; Barbé, C.; Loumaye, A.; Thissen, J. Glucocorticoid-induced skeletal muscle atrophy Int. J. Biochem. Cell Biol. 2013, 45, 2163-2172 10.1016/j.biocel.2013.05.036
7. Kostyo, J. L.; Redmond, A. F. Role of protein synthesis in the inhibitory action of adrenal steroid hormones on amino acid transport by muscle Endocrinology 1966, 79 (3) 531-540 10.1210/endo-79-3-531
8. Wang, H.; Kubica, N.; Ellisen, L. W.; Jefferson, L. S.; Kimball, S. R. Dexamethasone represses signaling through the mammalian target of rapamycin in muscle cells by enhancing expression of REDD1 J. Biol. Chem. 2006, 281 (51) 39128-39134 10.1074/jbc.M610023200
9. Liu, Z.; Li, G.; Kimball, S. R.; Jahn, L. A.; Barrett, E. J. Glucocorticoids modulate amino acid-induced translation initiation in human skeletal muscle Am. J. Physiol.: Endocrinol. Metab. 2004, 287 (2) E275-E281 10.1152/ajpendo.00457.2003
10. Shah, O.; Kimball, S.; Jefferson, L. Among translational effectors, p70S6k is uniquely sensitive to inhibition by glucocorticoids Biochem. J. 2000, 347, 389-397 10.1042/bj3470389
11. Armstrong, D. D.; Wong, V. L.; Esser, K. A. Expression of β-catenin is necessary for physiological growth of adult skeletal muscle American Journal of Physiology-Cell Physiology 2006, 291 (1) C185-C188 10.1152/ajpcell.00644.2005
12. Jefferson, L. S.; Fabian, J. R.; Kimball, S. R. Glycogen synthase kinase-3 is the predominant insulin-regulated eukaryotic initiation factor 2B kinase in skeletal muscle Int. J. Biochem. Cell Biol. 1999, 31 (1) 191-200 10.1016/S1357-2725(98)00141-1
13. Cho, J. E.; Fournier, M.; Da, X.; Lewis, M. I. Time course expression of Foxo transcription factors in skeletal muscle following corticosteroid administration J. Appl. Physiol. 2010, 108 (1) 137-145 10.1152/japplphysiol.00704.2009
14. Sandri, M.; Sandri, C.; Gilbert, A.; Skurk, C.; Calabria, E.; Picard, A.; Walsh, K.; Schiaffino, S.; Lecker, S. H.; Goldberg, A. L. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy Cell 2004, 117 (3) 399-412 10.1016/S0092-8674(04)00400-3
15. Verhees, K. J.; Schols, A. M.; Kelders, M. C.; Op den Kamp, C. M. O.; van der Velden, J. L.; Langen, R. C. Glycogen synthase kinase-3β is required for the induction of skeletal muscle atrophy American Journal of Physiology-Cell Physiology 2011, 301 (5) C995-C1007 10.1152/ajpcell.00520.2010
16. Evenson, A. R.; Fareed, M. U.; Menconi, M. J.; Mitchell, J. C.; Hasselgren, P.-O. GSK-3β inhibitors reduce protein degradation in muscles from septic rats and in dexamethasone-treated myotubes Int. J. Biochem. Cell Biol. 2005, 37 (10) 2226-2238 10.1016/j.biocel.2005.06.002
17. Imae, M.; Fu, Z.; Yoshida, A.; Noguchi, T.; Kato, H. Nutritional and hormonal factors control the gene expression of FoxOs, the mammalian homologues of DAF-16 J. Mol. Endocrinol. 2003, 30 (2) 253-262 10.1677/jme.0.0300253
18. Gilson, H.; Schakman, O.; Combaret, L.; Lause, P.; Grobet, L.; Attaix, D.; Ketelslegers, J.; Thissen, J. Myostatin gene deletion prevents glucocorticoid-induced muscle atrophy Endocrinology 2007, 148 (1) 452-460 10.1210/en.2006-0539
19. 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.; Glass, D. J. Identification of ubiquitin ligases required for skeletal muscle atrophy Science 2001, 294 (5547) 1704-1708 10.1126/science.1065874
20. Glass, D. J. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy Nat. Cell Biol. 2003, 5 (2) 87-90 10.1038/ncb0203-87
21. Romanello, V.; Sandri, M. Mitochondrial biogenesis and fragmentation as regulators of protein degradation in striated muscles J. Mol. Cell. Cardiol. 2013, 55, 64-72 10.1016/j.yjmcc.2012.08.001
22. Romanello, V.; Guadagnin, E.; Gomes, L.; Roder, I.; Sandri, C.; Petersen, Y.; Milan, G.; Masiero, E.; Del Piccolo, P.; Foretz, M.; Scorrano, L.; Rudolf, R.; Sandri, M. Mitochondrial fission and remodelling contributes to muscle atrophy EMBO J. 2010, 29 (10) 1774-1785 10.1038/emboj.2010.60
23. Siu, P. M.; Alway, S. E. Mitochondria-associated apoptotic signalling in denervated rat skeletal muscle J. Physiol. 2005, 565 (1) 309-323 10.1113/jphysiol.2004.081083
24. Liu, J.; Peng, Y.; Cui, Z.; Wu, Z.; Qian, A.; Shang, P.; Qu, L.; Li, Y.; Liu, J.; Long, J. Depressed mitochondrial biogenesis and dynamic remodeling in mouse tibialis anterior and gastrocnemius induced by 4-week hindlimb unloading IUBMB Life 2012, 64 (11) 901-910 10.1002/iub.1087
25. Liu, J.; Peng, Y.; Feng, Z.; Shi, W.; Qu, L.; Li, Y.; Liu, J.; Long, J. Reloading functionally ameliorates disuse-induced muscle atrophy by reversing mitochondrial dysfunction, and similar benefits are gained by administering a combination of mitochondrial nutrients Free Radical Biol. Med. 2014, 69, 116-128 10.1016/j.freeradbiomed.2014.01.003
26. Lee, C. M.; Lopez, M. E.; Weindruch, R.; Aiken, J. M. Association of age-related mitochondrial abnormalities with skeletal muscle fiber atrophy Free Radical Biol. Med. 1998, 25 (8) 964-972 10.1016/S0891-5849(98)00185-3
27. Liu, J.; Ames, B. N. Reducing mitochondrial decay with mitochondrial nutrients to delay and treat cognitive dysfunction, Alzheimer's disease, and Parkinson's disease Nutr. Neurosci. 2005, 8 (2) 67-89 10.1080/10284150500047161
28. Liu, J.; Shen, W.; Zhao, B.; Wang, Y.; Wertz, K.; Weber, P.; Zhang, P. Targeting mitochondrial biogenesis for preventing and treating insulin resistance in diabetes and obesity: Hope from natural mitochondrial nutrients Adv. Drug Delivery Rev. 2009, 61 (14) 1343-52 10.1016/j.addr.2009.06.007
29. Tischler, M. E. Effect of the antiglucocorticoid RU38486 on protein metabolism in unweighted soleus muscle Metab., Clin. Exp. 1994, 43 (11) 1451-5 10.1016/0026-0495(94)90044-2
30. Watson, M. L.; Baehr, L. M.; Reichardt, H. M.; Tuckermann, J. P.; Bodine, S. C.; Furlow, J. D. A cell-autonomous role for the glucocorticoid receptor in skeletal muscle atrophy induced by systemic glucocorticoid exposure Am. J. Physiol Endocrinol Metab 2012, 302 (10) E1210-20 10.1152/ajpendo.00512.2011
31. Martens, M.; Peterson, P.; Lee, C. In vitro effects of glucocorticoid on mitochondrial energy metabolism Biochim. Biophys. Acta, Bioenerg. 1991, 1058 (2) 152-160 10.1016/S0005-2728(05)80232-4
32. Mitsui, T.; Azuma, H.; Nagasawa, M.; Iuchi, T.; Akaike, M.; Odomi, M.; Matsumoto, T. Chronic corticosteroid administration causes mitochondrial dysfunction in skeletal muscle J. Neurol. 2002, 249 (8) 1004-1009 10.1007/s00415-002-0774-5
33. Qin, W.; Pan, J.; Wu, Y.; Bauman, W. A.; Cardozo, C. Protection against dexamethasone-induced muscle atrophy is related to modulation by testosterone of FOXO1 and PGC-1alpha Biochem. Biophys. Res. Commun. 2010, 403 (3-4) 473-8 10.1016/j.bbrc.2010.11.061
34. Pouw, E.; Koerts-de Lang, E.; Gosker, H.; Freling, G.; Van Der Vusse, G.; Wouters, E.; Schols, A. Muscle metabolic status in patients with severe COPD with and without long-term prednisolone Eur. Respir. J. 2000, 16 (2) 247-252 10.1034/j.1399-3003.2000.16b11.x
35. Cao, K.; Zheng, A.; Xu, J.; Li, H.; Liu, J.; Peng, Y.; Long, J.; Zou, X.; Li, Y.; Chen, C.; Liu, J.; Feng, Z. AMPK activation prevents prenatal stress-induced cognitive impairment: Modulation of mitochondrial content and oxidative stress Free Radical Biol. Med. 2014, 75, 156-166 10.1016/j.freeradbiomed.2014.07.029
36. Long, J.; Gao, H.; Sun, L.; Liu, J.; Zhao-Wilson, X. Grape extract protects mitochondria from oxidative damage and improves locomotor dysfunction and extends lifespan in a Drosophila Parkinson's disease model Rejuvenation Res. 2009, 12 (5) 321-331 10.1089/rej.2009.0877
37. Palmer, J. W.; Tandler, B.; Hoppel, C. L. Biochemical properties of subsarcolemmal and interfibrillar mitochondria isolated from rat cardiac muscle J. Biol. Chem. 1977, 252 (23) 8731-8739
38. Sahin, E.; Colla, S.; Liesa, M.; Moslehi, J.; Müller, F. L.; Guo, M.; Cooper, M.; Kotton, D.; Fabian, A. J.; Walkey, C. et al. Telomere dysfunction induces metabolic and mitochondrial compromise Nature 2011, 470 (7334) 359-365 10.1038/nature09787
39. Wang, X.; Li, H.; Zheng, A.; Yang, L.; Liu, J.; Chen, C.; Tang, Y.; Zou, X.; Li, Y.; Long, J.; Liu, J.; Zhang, Y.; Feng, Z. Mitochondrial dysfunction-associated OPA1 cleavage contributes to muscle degeneration: preventative effect of hydroxytyrosol acetate Cell Death Dis. 2014, 5 (11) e1521 10.1038/cddis.2014.473
40. Twig, G.; Hyde, B.; Shirihai, O. S. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view Biochim. Biophys. Acta, Bioenerg. 2008, 1777 (9) 1092-7 10.1016/j.bbabio.2008.05.001
41. Chen, H.; Vermulst, M.; Wang, Y. E.; Chomyn, A.; Prolla, T. A.; McCaffery, J. M.; Chan, D. C. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations Cell 2010, 141 (2) 280-289 10.1016/j.cell.2010.02.026
42. Mitsui, T.; Umaki, Y.; Nagasawa, M.; Akaike, M.; Aki, K.; Azuma, H.; Ozaki, S.; Odomi, M.; Matsumoto, T. Mitochondrial damage in patients with long-term corticosteroid therapy: development of oculoskeletal symptoms similar to mitochondrial disease Acta neuropathologica 2002, 104 (3) 260-266
43. Weber, K.; Brück, P.; Mikes, Z.; Küpper, J.-H.; Klingenspor, M.; Wiesner, R. J. Glucocorticoid hormone stimulates mitochondrial biogenesis specifically in skeletal muscle Endocrinology 2002, 143 (1) 177-184 10.1210/endo.143.1.8600
44. Manoli, I. Monoamine oxidase-A is a major target gene for glucocorticoids in human skeletal muscle cells FASEB J. 2005, 19 (10) 1359-1361 10.1096/fj.04-3660fje
45. Duclos, M.; Gouarne, C.; Martin, C.; Rocher, C.; Mormède, P.; Letellier, T. Effects of corticosterone on muscle mitochondria identifying different sensitivity to glucocorticoids in Lewis and Fischer rats American Journal of Physiology-Endocrinology and Metabolism 2004, 286 (2) E159-E167 10.1152/ajpendo.00281.2003
46. Marone, J. R.; Falduto, M. T.; Essig, D. A.; Hickson, R. C. Effects of glucocorticoids and endurance training on cytochrome oxidase expression in skeletal muscle J. Appl. Physiol. 1994, 77 (4) 1685-1690
47. Alesci, S.; Manoli, I.; Michopoulos, V.; Brouwers, F.; Le, H.; Gold, P.; Blackman, M.; Rennert, O.; Su, Y.; Chrousos, G. Development of a human mitochondria-focused cDNA microarray (hMitChip) and validation in skeletal muscle cells: implications for pharmaco-and mitogenomics Pharmacogenomics J. 2006, 6 (5) 333-342 10.1038/sj.tpj.6500377
48. Oshima, Y.; Kuroda, Y.; Kunishige, M.; Matsumoto, T.; Mitsui, T. Oxidative stress-associated mitochondrial dysfunction in corticosteroid-treated muscle cells Muscle Nerve 2004, 30 (1) 49-54 10.1002/mus.20036
49. Cogswell, A. M.; Stevens, R. J.; Hood, D. A. Properties of skeletal muscle mitochondria isolated from subsarcolemmal and intermyofibrillar regions AJP: Cell Physiol. 1993, 264 (2) C383-C389
50. Roussel, D.; Dumas, J.-F.; Augeraud, A.; Douay, O.; Foussard, F.; Malthiéry, Y.; Simard, G.; Ritz, P. Dexamethasone treatment specifically increases the basal proton conductance of rat liver mitochondria FEBS Lett. 2003, 541 (1) 75-79 10.1016/S0014-5793(03)00307-7
51. Dumas, J.-F.; Simard, G.; Roussel, D.; Douay, O.; Foussard, F.; Malthiery, Y.; Ritz, P. Mitochondrial energy metabolism in a model of undernutrition induced by dexamethasone Br. J. Nutr. 2003, 90 (5) 969-978 10.1079/BJN2003980
52. Dumas, J.-F.; Bielicki, G.; Renou, J.-P.; Roussel, D.; Ducluzeau, P.-H.; Malthièry, Y.; Simard, G.; Ritz, P. Dexamethasone impairs muscle energetics, studied by 31P NMR, in rats Diabetologia 2005, 48 (2) 328-335 10.1007/s00125-004-1631-0
53. Twig, G.; Hyde, B.; Shirihai, O. S. Mitochondrial fusion, fission and autophagy as a quality control axis: the bioenergetic view Biochim. Biophys. Acta, Bioenerg. 2008, 1777 (9) 1092-1097 10.1016/j.bbabio.2008.05.001
54. Troncoso, R.; Paredes, F.; Parra, V.; Gatica, D.; Vásquez-Trincado, C.; Quiroga, C.; Bravo-Sagua, R.; López-Crisosto, C.; Rodriguez, A. E.; Oyarzún, A. P.; Kroemer, G.; Lavandero, S. Dexamethasone-induced autophagy mediates muscle atrophy through mitochondrial clearance Cell Cycle 2014, 13 (14) 2281-2295 10.4161/cc.29272
55. Kim, J.; Kundu, M.; Viollet, B.; Guan, K.-L. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1 Nat. Cell Biol. 2011, 13 (2) 132-141 10.1038/ncb2152
56. Jäger, S.; Handschin, C.; St.-Pierre, J.; Spiegelman, B. M. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α Proc. Natl. Acad. Sci. U. S. A. 2007, 104 (29) 12017-12022 10.1073/pnas.0705070104
57. Greer, E. L.; Oskoui, P. R.; Banko, M. R.; Maniar, J. M.; Gygi, M. P.; Gygi, S. P.; Brunet, A. The Energy Sensor AMP-activated Protein Kinase Directly Regulates the Mammalian FOXO3 Transcription Factor J. Biol. Chem. 2007, 282 (41) 30107-30119 10.1074/jbc.M705325200
58. Momken, I.; Stevens, L.; Bergouignan, A.; Desplanches, D.; Rudwill, F.; Chery, I.; Zahariev, A.; Zahn, S.; Stein, T. P.; Sebedio, J. L. et al. Resveratrol prevents the wasting disorders of mechanical unloading by acting as a physical exercise mimetic in the rat FASEB J. 2011, 25 (10) 3646-3660 10.1096/fj.10-177295
59. Alamdari, N.; Aversa, Z.; Castillero, E.; Gurav, A.; Petkova, V.; Tizio, S.; Hasselgren, P.-O. Resveratrol prevents dexamethasone-induced expression of the muscle atrophy-related ubiquitin ligases atrogin-1 and MuRF1 in cultured myotubes through a SIRT1-dependent mechanism Biochem. Biophys. Res. Commun. 2012, 417 (1) 528-533 10.1016/j.bbrc.2011.11.154