Thyroid hormone stimulation of autophagy is essential for mitochondrial biogenesis and activity in skeletal muscle

Endocrinology

Volumn 157, Issue 1, 2016, Pages 23-38

  Lesmana, Ronny ^a,b   Sinha, Rohit A ^a   Singh, Brijesh K ^a   Zhou, Jin ^a   Ohba, Kenji ^a   Wu, Yajun ^c   Yau, Winifred WY ^a   Bay, Boon Huat ^c   Yen, Paul M ^a,d  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b PADJADJARAN UNIVERSITY   (Indonesia)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^d DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; AUTOPHAGY PROTEIN 5; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LIOTHYRONINE; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; MITOCHONDRIAL PROTEIN; OXYGEN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEIN KINASE; PROTEIN P62; RAPAMYCIN; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; THYROID HORMONE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; ULK1 PROTEIN; UNCLASSIFIED DRUG; ATG5 PROTEIN, MOUSE; MTOR PROTEIN, MOUSE; PPARGC1A PROTEIN, MOUSE; PROTEIN SERINE THREONINE KINASE; TARGET OF RAPAMYCIN KINASE; THYROXINE; TRANSCRIPTION FACTOR; ULK1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CONTROLLED STUDY; GENE EXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MALE; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL MEMBRANE; MOUSE; MUSCLE CELL; MYOBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; RECEPTOR UPREGULATION; SKELETAL MUSCLE; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; KINETICS; METABOLISM; MITOCHONDRIAL DYNAMICS; MUSCLE MITOCHONDRION; OXYGEN CONSUMPTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SKELETAL MYOBLAST; ULTRASTRUCTURE;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; CELL LINE; GENE EXPRESSION REGULATION; KINETICS; MALE; MICE, INBRED C57BL; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL DYNAMICS; MUSCLE, SKELETAL; MYOBLASTS, SKELETAL; OXYGEN CONSUMPTION; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; RNA INTERFERENCE; SIGNAL TRANSDUCTION; THYROXINE; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; TRIIODOTHYRONINE;

EID: 84954497138     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2015-1632     Document Type: Article

References (56)

1. Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728-741.
2. Tam BT, Pei XM, Yu AP, et al. Autophagic adaptation is associated with exercise-induced fibre-type shifting in skeletal muscle. Acta physiol (Oxf). 2015;214:221-236.
3. Grumati P, Coletto L, Sabatelli P, et al. Autophagy is defective in collagen VI muscular dystrophies, and its reactivation rescues myofiber degeneration. Nat Med. 2010;16:1313-1320.
4. De Palma C, Morisi F, Cheli S, et al. Autophagy as a new therapeutic target in Duchenne muscular dystrophy. Cell Death Dis. 2012;3:e418.
5. Thapaliya S, Runkana A, McMullen MR, et al. Alcohol-induced autophagy contributes to loss in skeletal muscle mass. Autophagy. 2014;10:677-690.
6. Lira VA, Okutsu M, Zhang M, et al. Autophagy is required for exercise training-induced skeletal muscle adaptation and improvement of physical performance. FASEB J. 2013;27:4184-4193.
7. Castets P, Lin S, Rion N, et al. Sustained activation of mTORC1 in skeletal muscle inhibits constitutive and starvation-induced autophagy and causes a severe, late-onset myopathy. Cell Metab. 2013;17:731-744.
8. Masiero E, Sandri M. Autophagy inhibition induces atrophy and myopathy in adult skeletal muscles. Autophagy. 2010;6:307-309.
9. Raben N, Hill V, Shea L, et al. Suppression of autophagy in skeletal muscle uncovers the accumulation of ubiquitinated proteins and their potential role in muscle damage in Pompe disease. Hum Mol Genet. 2008;17:3897-3908.
10. Ma Y, Yang HZ, Xu LM, Huang YR, Dai HL, Kang XN. Testosterone regulates the autophagic clearance of androgen binding protein in rat Sertoli cells. Sci Rep. 2015;5:8894.
11. Zhang Y, Fang F, Goldstein JL, Brown MS, Zhao TJ. Reduced autophagy in livers of fasted, fat-depleted, ghrelin-deficient mice: reversal by growth hormone. Proc Natl Acad Sci USA. 2015;112:1226-1231.
12. Naito T, Kuma A, Mizushima N. Differential contribution of insulin and amino acids to the mTORC1-autophagy pathway in the liver and muscle. J Biol Chem. 2013;288:21074-21081.
13. Sinha RA, You SH, Zhou J, et al. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J Clin Invest. 2012;122:2428-2438.
14. Sinha RA, Singh BK, Zhou J, et al. Thyroid hormone induction of mitochondrial activity is coupled to mitophagy via ROS-AMPKULK1 signaling. Autophagy. 2015;11:1341-1357.
15. Marsili A, Tang D, Harney JW, et al. Type II iodothyronine deiodinase provides intracellular 3, 5, 3'-triiodothyronine to normal and regenerating mouse skeletal muscle. Am J Physiol Endocrinol Metab. 2011;301:E818-E824.
16. Visser WE, Heemstra KA, Swagemakers SM, et al. Physiological thyroid hormone levels regulate numerous skeletal muscle transcripts. J Clin Endocrinol Metab. 2009;94:3487-3496.
17. Clément K, Viguerie N, Diehn M, et al. In vivo regulation of human skeletal muscle gene expression by thyroid hormone. Genome Res. 2002;12:281-291.
18. Weitzel JM, Iwen KA, Seitz HJ. Regulation of mitochondrial biogenesis by thyroid hormone. Exp Physiol. 2003;88:121-128.
19. Short KR, Nygren J, Nair KS. Effect of T (3)-induced hyperthyroidism on mitochondrial and cytoplasmic protein synthesis rates in oxidative and glycolytic tissues in rats. Am J Physiol Endocrinol Metab. 2007;292:E642-E647.
20. Harper ME, Seifert EL. Thyroid hormone effects on mitochondrial energetics. Thyroid. 2008;18:145-156.
21. Mullur R, Liu YY, Brent GA. Thyroid hormone regulation of metabolism. Physiol Rev. 2014;94:355-382.
22. You SH, Liao X, Weiss RE, Lazar MA. The interaction between nuclear receptor corepressor and histone deacetylase 3 regulates both positive and negative thyroid hormone action in vivo. Mol Endocrinol. 2010;24:1359-1367.
23. Koenig RJ, Smith RJ. L6 cells as a tissue culture model for thyroid hormone effects on skeletal muscle metabolism. J Clin Invest. 1985;76:878-881.
24. Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140:313-326.
25. Mizushima N, Yoshimori T. How to interpret LC3 immunoblotting. Autophagy. 2007;3:542-545.
26. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci. 2011;36:30-38.
27. Kakkar P, Singh BK. Mitochondria: a hub of redox activities and cellular distress control. Mol Cell Biochem. 2007;305:235-253.
28. Zhao J, Brault JJ, Schild A, et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 2007;6:472-483.
29. Zhang J, Ng S, Wang J, et al. Histone deacetylase inhibitors induce autophagy through FOXO1-dependent pathways. Autophagy. 2015;11:629-642.
30. Fernandez-Marcos PJ, Auwerx J. Regulation of PGC-1α, a nodal regulator of mitochondrial biogenesis. Am J Clin Nutr 2011;93:884S-890S.
31. Zhu J, Wang KZ, Chu CT. After the banquet: mitochondrial biogenesis, mitophagy, and cell survival. Autophagy. 2013;9:1663-1676.
32. Simonides WS, Van Hardeveld C. Thyroid hormone as a determinant of metabolic and contractile phenotype of skeletal muscle. Thyroid. 2008;18:205-216.
33. Jurkuvenaite A, Benavides GA, Komarova S, et al. Upregulation of autophagy decreases chlorine-induced mitochondrial injury and lung inflammation. Free Radic Biol Med. 2015;85:83-94.
34. Sanchez AM, Bernardi H, Py G, Candau RB. Autophagy is essential to support skeletal muscle plasticity in response to endurance exercise. Am J Physiol Regul Integr Comp Physiol. 2014;307:R956-R969.
35. Ferraro E, Giammarioli AM, Chiandotto S, Spoletini I, Rosano G. Exercise-induced skeletal muscle remodeling and metabolic adaptation: redox signaling and role of autophagy. Antioxid Redox Signal. 2014;21:154-176.
36. Milan G, Romanello V, Pescatore F, et al. Regulation of autophagy and the ubiquitin-proteasome system by the FoxO transcriptional network during muscle atrophy. Nat Commun. 2015;6:6670.
37. Zhao J, Brault JJ, Schild A, Goldberg AL. Coordinate activation of autophagy and the proteasome pathway by FoxO transcription factor. Autophagy. 2008;4:378-380.
38. Lo Verso F, Carnio S, Vainshtein A, Sandri M. Autophagy is not required to sustain exercise and PRKAA1/AMPK activity but is important to prevent mitochondrial damage during physical activity. Autophagy. 2014;10:1883-1894.
39. Bahi L, Garnier A, Fortin D, et al. Differential effects of thyroid hormones on energy metabolism of rat slow- and fast-twitch muscles. J Cell Physiol. 2005;203:589-598.
40. Qiao S, Dennis M, Song X, et al. A REDD1/TXNIP pro-oxidant complex regulates ATG4B activity to control stress-induced autophagy and sustain exercise capacity. Nat Commun. 2015;6:7014.
41. Mungai PT, Waypa GB, Jairaman A, et al. Hypoxia triggers AMPK activation through reactive oxygen species-mediated activation of calcium release-activated calcium channels. Mol Cell Biol. 2011;31:3531-3545.
42. Rahman M, Mofarrahi M, Kristof AS, Nkengfac B, Harel S, Hussain SN. Reactive oxygen species regulation of autophagy in skeletal muscles. Antioxid Redox Signal. 2014;20:443-459.
43. Schwalm C, Jamart C, Benoit N, et al. Activation of autophagy in human skeletal muscle is dependent on exercise intensity and AMPK activation. FASEB J. 2015;29:3515-3526.
44. Alers S, Löffler AS, Wesselborg S, Stork B. Role of AMPK-mTORUlk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol. 2012;32:2-11.
45. Kim J, Kundu M, Viollet B, Guan KL. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132-141.
46. Peachey LD, Greif RL. Alterations of mitochondrial structure induced by thyroid hormones in vivo and in vitro. Endocrinology. 1965;77:61-77.
47. Walrand S, Short KR, Heemstra LA, et al. Altered regulation of energy homeostasis in older rats in response to thyroid hormone administration. FASEB J. 2014;28:1499-1510.
48. Gustafson TA, Markham BE, Morkin E. Effects of thyroid hormone on α-actin and myosin heavy chain gene expression in cardiac and skeletal muscles of the rat: measurement of mRNA content using synthetic oligonucleotide probes. Circ Res. 1986;59:194-201.
49. Salvatore D, Simonides WS, Dentice M, Zavacki AM, Larsen PR. Thyroid hormones and skeletal muscle-new insights and potential implications. Nat Rev Endocrinol. 2014;10:206-214.
50. Takikita S, Schreiner C, Baum R, et al. Fiber type conversion by PGC-1α activates lysosomal and autophagosomal biogenesis in both unaffected and Pompe skeletal muscle. PloS One. 2010;5:e15239.
51. Dentice M, Marsili A, Ambrosio R, et al. The FoxO3/type 2 deiodinase pathway is required for normal mouse myogenesis and muscle regeneration. J Clin Invest. 2010;120:4021-4030.
52. Branvold DJ, Allred DR, Beckstead DJ, et al. Thyroid hormone effects on LKB1, MO25, phospho-AMPK, phospho-CREB, and PGC-1α in rat muscle. J Appl Physiol (1985). 2008;105:1218-1227.
53. Wulf A, Harneit A, Kröger M, Kebenko M, Wetzel MG, Weitzel JM. T3-mediated expression of PGC-1α via a far upstream located thyroid hormone response element. Mol Cell Endocrinol. 2008;287:90-95.
54. Palikaras K, Lionaki E, Tavernarakis N. Coupling mitogenesis and mitophagy for longevity. Autophagy. 2015;11:1428-1430.
55. De Palma C, Perrotta C, Pellegrino P, Clementi E, Cervia D. Skeletal muscle homeostasis in duchenne muscular dystrophy: modulating autophagy as a promising therapeutic strategy. Front Aging Neurosci. 2014;6:188.
56. Wenz T, Rossi SG, Rotundo RL, Spiegelman BM, Moraes CT. Increased muscle PGC-1α expression protects from sarcopenia and metabolic disease during aging. Proc Natl Acad Sci USA. 2009;106:20405-20410.