Thyroid hormone induction of mitochondrial activity is coupled to mitophagy via ROS-AMPKULK1 signaling

Autophagy

Volumn 11, Issue 8, 2015, Pages 1341-1357

  Sinha, Rohit A ^a   Singh, Brijesh K ^a   Zhou, Jin ^a   Wu, Yajun ^b   Farah, Benjamin L ^a   Ohba, Kenji ^a   Lesmana, Ronny ^a,c   Gooding, Jessica ^d   Bay, Boon Huat ^a   Yen, Paul M ^a,b,d  

^a DUKE NUS MEDICAL SCHOOL   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c PADJADJARAN UNIVERSITY   (Indonesia)

^d DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Autophagy; Liver; Mitochondria; Mitophagy; PRKAA1 AMPK; ROS; T3; ULK1

Indexed keywords

ADENYLATE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; LIOTHYRONINE; MEMBRANE PROTEIN; REACTIVE OXYGEN METABOLITE; ULK1 PROTEIN; UNCLASSIFIED DRUG; CALCIUM; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; OXYGEN; PRKAA1 PROTEIN, HUMAN; PROTEIN SERINE THREONINE KINASE; SERINE THREONINE PROTEIN KINASE ULK1; SIGNAL PEPTIDE; SUPEROXIDE; THYROID HORMONE RECEPTOR BETA; ULK1 PROTEIN, HUMAN; ULK1 PROTEIN, MOUSE;

ARTICLE; AUTOPHAGY; CELL STIMULATION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; HORMONAL REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; LIPOPHAGOCYTOSIS; LIVER CELL; MITOCHONDRIAL DYNAMICS; MITOCHONDRION; MITOPHAGY; OXIDATIVE PHOSPHORYLATION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CHEMISTRY; FLUORESCENCE MICROSCOPY; HEP-G2 CELL LINE; MALE; METABOLISM; MOUSE; OXIDATIVE STRESS; REAL TIME POLYMERASE CHAIN REACTION; TRANSMISSION ELECTRON MICROSCOPY;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN-1 HOMOLOG; CALCIUM; HEP G2 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; OXIDATIVE STRESS; OXYGEN; PROTEIN-SERINE-THREONINE KINASES; REACTIVE OXYGEN SPECIES; REAL-TIME POLYMERASE CHAIN REACTION; SUPEROXIDES; THYROID HORMONE RECEPTORS BETA; TRIIODOTHYRONINE;

EID: 84943753597     PISSN: 15548627     EISSN: 15548635     Source Type: Journal    
DOI: 10.1080/15548627.2015.1061849     Document Type: Article

References (55)

1. Kakkar P, Singh BK. Mitochondria: a hub of redox activities and cellular distress control. Mole Cell Biochem 2007; 305: 235-53; PMID: 17562131; http://dx. doi. org/10. 1007/s11010-007-9520-8.
2. Shokolenko I, Venediktova N, Bochkareva A, Wilson GL, Alexeyev MF. Oxidative stress induces degradation of mitochondrial DNA. Nucleic Acids Res 2009; 37: 2539-48; PMID: 19264794; http://dx. doi. org/; http://dx. doi. org/10. 1093/nar/gkp100.
3. Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011; 36: 30-8; PMID: 20728362; http://dx. doi. org/10. 1016/j. tibs. 2010. 07. 007.
4. Tolkovsky AM. Mitophagy. Biochimica et Biophysica Acta 2009; 1793: 1508-15; PMID: 19289147; http://dx. doi. org/10. 1016/j. bbamcr. 2009. 03. 002.
5. Kurihara Y, Kanki T, Aoki Y, Hirota Y, Saigusa T, Uchiumi T, Kang D. Mitophagy plays an essential role in reducing mitochondrial production of reactive oxygen species and mutation of mitochondrial DNA by maintaining mitochondrial quantity and quality in yeast. J Biol Chem 2012; 287: 3265-72; PMID: 22157017; http://dx. doi. org/10. 1074/jbc. M111. 280156.
6. Dodson M, Darley-Usmar V, Zhang J. Cellular metabolic and autophagic pathways: traffic control by redox signaling. Free Radic Biol Med 2013; 63: 207-21; PMID: 23702245http://dx. doi. org/10. 1016/j. freeradbiomed. 2013. 05. 014.
7. Ashrafi G, Schwarz TL. The pathways of mitophagy for quality control and clearance of mitochondria. Cell Death differ 2013; 20: 31-42; PMID: 22743996; http://dx. doi. org/10. 1038/cdd. 2012. 81.
8. Redmann M, Dodson M, Boyer-Guittaut M, Darley-Usmar V, Zhang J. Mitophagy mechanisms and role in human diseases. Int J Biochem Cell Biol 2014; 53: 127-33; PMID: 24842106; http://dx. doi. org/10. 1016/j. biocel. 2014. 05. 010.
9. Jin SM, Youle RJ. PINK1-and Parkin-mediated mitophagy at a glance. J Cell Sci 2012; 125: 795-9; PMID: 22448035; http://dx. doi. org/10. 1242/jcs. 093849.
10. Sandoval H, Thiagarajan P, Dasgupta SK, Schumacher A, Prchal JT, Chen M, Wang J. Essential role for Nix in autophagic maturation of erythroid cells. Nature 2008; 454: 232-5; PMID: 18454133; http://dx. doi. org/10. 1038/nature07006.
11. Liu L, Sakakibara K, Chen Q, Okamoto K. Receptormediated mitophagy in yeast and mammalian systems. Cell Res 2014; 24: 787-95; PMID: 24903109; http://dx. doi. org/10. 1038/cr. 2014. 75.
12. Melser S, Chatelain EH, Lavie J, Mahfouf W, Jose C, Obre E, Goorden S, Priault M, Elgersma Y, Rezvani HR, et al. Rheb regulates mitophagy induced by mitochondrial energetic status. Cell Metab 2013; 17: 719-30; PMID: 23602449; http://dx. doi. org/10. 1016/j. cmet. 2013. 03. 014.
13. Graef M, Nunnari J. Mitochondria regulate autophagy by conserved signalling pathways. EMBO J 2011; 30: 2101-14; PMID: 21468027; http://dx. doi. org/10. 1038/emboj. 2011. 104.
14. Soleimanpour SA, Gupta A, Bakay M, Ferrari AM, Groff DN, Fadista J, Spruce LA, Kushner JA, Groop L, Seeholzer SH, et al. The diabetes susceptibility gene Clec16a regulates mitophagy. Cell 2014; 157: 1577-90; PMID: 24949970; http://dx. doi. org/10. 1016/j. cell. 2014. 05. 016.
15. Ryter SW, Koo JK, Choi AM. Molecular regulation of autophagy and its implications for metabolic diseases. Curr Opin Clin Nutr Metab Care 2014; 17: 329-37; PMID: 24848530; http://dx. doi. org/10. 1097/MCO. 0000000000000068.
16. Sinha RA, Singh BK, Yen PM. Thyroid hormone regulation of hepatic lipid and carbohydrate metabolism. Trends Endocrinol Metab: TEM 2014; 25(10): 538-45; PMID: 25127738.
17. Cioffi F, Senese R, Lanni A, Goglia F. Thyroid hormones and mitochondria: with a brief look at derivatives and analogues. Mol Cell Endocrinol 2013; 379: 51-61; PMID: 23769708; http://dx. doi. org/10. 1016/j. mce. 2013. 06. 006.
18. Weitzel JM, Iwen KA. Coordination of mitochondrial biogenesis by thyroid hormone. Mol Cell Endocrinol 2011; 342: 1-7; PMID: 21664416; http://dx. doi. org/10. 1016/j. mce. 2011. 05. 009.
19. Thakran S, Sharma P, Attia RR, Hori RT, Deng X, Elam MB, Park EA. Role of sirtuin 1 in the regulation of hepatic gene expression by thyroid hormone. J Biol Chem 2013; 288: 807-18; PMID: 23209300; http://dx. doi. org/10. 1074/jbc. M112. 437970.
20. Sinha RA, You SH, Zhou J, Siddique MM, Bay BH, Zhu X, Privalsky ML, Cheng SY, Stevens RD, Summers SA, et al. Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J Clin Invest 2012; 122: 2428-38; PMID: 22684107; http://dx. doi. org/10. 1172/JCI60580.
21. Fernandez V, Tapia G, Varela P, Romanque P, Cartier-Ugarte D, Videla LA. Thyroid hormone-induced oxidative stress in rodents and humans: a comparative view and relation to redox regulation of gene expression. Comp Biochem Physiol Toxicol Pharmacol 2006; 142: 231-9; PMID: 16298169; http://dx. doi. org/10. 1016/j. cbpc. 2005. 10. 007.
22. Venditti P, Di Meo S. Thyroid hormone-induced oxidative stress. Cell Mol Life Sci: CMLS 2006; 63: 414-34; PMID: 16389448; http://dx. doi. org/10. 1007/s00018-005-5457-9.
23. Videla LA, Fernandez V, Tapia G, Varela P. Thyroid hormone calorigenesis and mitochondrial redox signaling: upregulation of gene expression. Front Biosci: J virtual library 2007; 12: 1220-8; PMID: 17127375; http://dx. doi. org/10. 2741/2140.
24. Videla LA. Hormetic responses of thyroid hormone calorigenesis in the liver: Association with oxidative stress. IUBMB Life 2010; 62: 460-6; PMID: 20503439.
25. Zambrano A, Garcia-Carpizo V, Gallardo ME, Villamuera R, Gomez-Ferreria MA, Pascual A, Buisine N, Sachs LM, Garesse R, Aranda A. The thyroid hormone receptor b induces DNA damage and premature senescence. J Cell Biol 2014; 204: 129-46; PMID: 24395638; http://dx. doi. org/10. 1083/jcb. 201305084.
26. Gross NJ. Control of mitochondrial turnover under the influence of thyroid hormone. J Cell Biol 1971; 48: 29-40; PMID: 5545111; http://dx. doi. org/10. 1083/jcb. 48. 1. 29.
27. Tseng YH, Ke PY, Liao CJ, Wu SM, Chi HC, Tsai CY, Tseng YH, Ke PY, Liao CJ, Wu SM, Chi HC, Tsai CY. Chromosome 19 open reading frame 80 is upregulated by thyroid hormone and modulates autophagy and lipid metabolism. Autophagy 2014; 10: 20-31; PMID: 24262987; http://dx. doi. org/10. 4161/auto. 26126.
28. Chan IH, Privalsky ML. Isoform-specific transcriptional activity of overlapping target genes that respond to thyroid hormone receptors alpha1 and beta1. Mol Endocrinol (Baltimore, Md) 2009; 23: 1758-75; PMID: 19628582; http://dx. doi. org/10. 1210/me. 2009-0025.
29. Turrens JF. Mitochondrial formation of reactive oxygen species. J physiol 2003; 552: 335-44; PMID: 14561818; http://dx. doi. org/10. 1113/jphysiol. 2003. 049478.
30. Kim SJ, Khan M, Quan J, Till A, Subramani S, Siddiqui A. Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathogens 2013; 9: e1003722; PMID: 24339771; http://dx. doi. org/10. 1371/journal. ppat. 1003722.
31. Kim SJ, Syed GH, Khan M, Chiu WW, Sohail MA, Gish RG, Siddiqui A. Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc Natl Acad Sci USA 2014; 111: 6413-8; PMID: 24733894; http://dx. doi. org/10. 1073/pnas. 1321114111.
32. Katayama H, Kogure T, Mizushima N, Yoshimori T, Miyawaki A. A sensitive and quantitative technique for detecting autophagic events based on lysosomal delivery. Chem Biol 2011; 18: 1042-52; PMID: 21867919; http://dx. doi. org/10. 1016/j. chembiol. 2011. 05. 013.
33. Ding WX, Yin XM. Mitophagy: mechanisms, pathophysiological roles, and analysis. Biol Chem 2012; 393: 547-64; PMID: 22944659.
34. Li L, Chen Y, Gibson SB. Starvation-induced autophagy is regulated by mitochondrial reactive oxygen species leading to AMPK activation. Cell Signal 2013; 25: 50-65; PMID: 23000343; http://dx. doi. org/10. 1016/j. cellsig. 2012. 09. 020.
35. 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: 443-59; PMID: 24180497; http://dx. doi. org/10. 1089/ars. 2013. 5410.
36. Vargas R, Ortega Y, Bozo V, Andrade M, Minuzzi G, Cornejo P, Fernandez V, Videla LA. Thyroid hormone activates rat liver adenosine 5,-monophosphate-activated protein kinase: relation to CaMKKb, TAK1 and LKB1 expression and energy status. J Biol Regul Homeost Agents 2013; 27: 989-99; PMID: 24382180.
37. Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ. AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 2008; 30: 214-26; PMID: 18439900; http://dx. doi. org/10. 1016/j. molcel. 2008. 03. 003.
38. Ruderman NB, Carling D, Prentki M, Cacicedo JM. AMPK, insulin resistance, and the metabolic syndrome. J Clin Invest 2013; 123: 2764-72; PMID: 23863634; http://dx. doi. org/10. 1172/JCI67227.
39. Mungai PT, Waypa GB, Jairaman A, Prakriya M, Dokic D, Ball MK, Schumacker PT. Hypoxia triggers AMPK activation through reactive oxygen speciesmediated activation of calcium release-activated calcium channels. Mol Cell Biol 2011; 31: 3531-45; PMID: 21670147; http://dx. doi. org/10. 1128/MCB. 05124-11.
40. Itakura E, Kishi-Itakura C, Koyama-Honda I, Mizushima N. Structures containing Atg9A and the ULK1 complex independently target depolarized mitochondria at initial stages of Parkin-mediated mitophagy. J Cell Sci 2012; 125: 1488-99; PMID: 22275429; http://dx. doi. org/10. 1242/jcs. 094110.
41. Wu W, Tian W, Hu Z, Chen G, Huang L, Li W, Zhang X, Xue P, Zhou C, Liu L, et al. ULK1 translocates to mitochondria and phosphorylates FUNDC1 to regulate mitophagy. EMBO Rep 2014; 15(5): 566-75; PMID: 24671035.
42. Egan DF, Shackelford DB, Mihaylova MM, Gelino S, Kohnz RA, Mair W, Vasquez DS, Joshi A, Gwinn DM, Taylor R, et al. Phosphorylation of ULK1 (hATG1) by AMP-activated protein kinase connects energy sensing to mitophagy. Science 2011; 331: 456-61.; PMID: 21205641; http://dx. doi. org/10. 1126/science. 1196371.
43. Frank M, Duvezin-Caubet S, Koob S, Occhipinti A, Jagasia R, Petcherski A, Ruonala MO, Priault M, Salin B, Reichert AS. Mitophagy is triggered by mild oxidative stress in a mitochondrial fission dependent manner. Biochim Biophys Acta 2012; 1823: 2297-310; PMID: 22917578; http://dx. doi. org/10. 1016/j. bbamcr. 2012. 08. 007.
44. Springer W, Kahle PJ. Regulation of PINK1-Parkinmediated mitophagy. Autophagy 2011; 7: 266-78; PMID: 21187721; http://dx. doi. org/10. 4161/auto. 7. 3. 14348.
45. Lemasters JJ. Selective mitochondrial autophagy, or mitophagy, as a targeted defense against oxidative stress, mitochondrial dysfunction, and aging. Rejuvenation Res 2005; 8: 3-5; PMID: 15798367; http://dx. doi. org/10. 1089/rej. 2005. 8. 3.
46. Wikstrom JD, Mahdaviani K, Liesa M, Sereda SB, Si Y, Las G, Twig G, Petrovic N, Zingaretti C, Graham A, et al. Hormone-induced mitochondrial fission is utilized by brown adipocytes as an amplification pathway for energy expenditure. EMBO J 2014; 33: 418-36; PMID: 24431221.
47. Glick D, Zhang W, Beaton M, Marsboom G, Gruber M, Simon MC, Hart J, Dorn GW 2nd, Brady MJ, Macleod KF. BNip3 regulates mitochondrial function and lipid metabolism in the liver. Mol Cell Biol 2012; 32: 2570-84; PMID: 22547685; http://dx. doi. org/10. 1128/MCB. 00167-12.
48. Carchman EH, Whelan S, Loughran P, Mollen K, Stratamirovic S, Shiva S, Rosengart MR, Zuckerbraun BS. Experimental sepsis-induced mitochondrial biogenesis is dependent on autophagy, TLR4, and TLR9 signaling in liver. FASEB J 2013; 27: 4703-11; PMID: 23982147; http://dx. doi. org/10. 1096/fj. 13-229476.
49. Bin-Umer MA, McLaughlin JE, Butterly MS, McCormick S, Tumer NE. Elimination of damaged mitochondria through mitophagy reduces mitochondrial oxidative stress and increases tolerance to trichothecenes. Proc Natl Acad Sci USA 2014; 111(32): 11798-803; PMID: 25071194.
50. Zhu H, Foretz M, Xie Z, Zhang M, Zhu Z, Xing J, Leclerc J, Gaudry M, Viollet B, Zou MH. PRKAA1/AMPKalpha1 is required for autophagy-dependent mitochondrial clearance during erythrocyte maturation. Autophagy 2014; 10: 1522-34; PMID: 24988326.
51. Czaja MJ, Ding WX, Donohue TM, Jr., Friedman SL, Kim JS, Komatsu M, Lemasters JJ, Lemoine A, Lin JD, Ou JH, et al. Functions of autophagy in normal and diseased liver. Autophagy 2013; 9: 1131-58; PMID: 23774882; http://dx. doi. org/10. 4161/auto. 25063.
52. Blake R, Trounce IA. Mitochondrial dysfunction and complications associated with diabetes. Biochim Biophys Acta 2014; 1840: 1404-12; PMID: 24246956; http://dx. doi. org/10. 1016/j. bbagen. 2013. 11. 007.
53. Cable EE, Finn PD, Stebbins JW, Hou J, Ito BR, van Poelje PD, Linemeyer DL, Erion MD. Reduction of hepatic steatosis in rats and mice after treatment with a liver-targeted thyroid hormone receptor agonist. Hepatology 2009; 49: 407-17; PMID: 19072834; http://dx. doi. org/10. 1002/hep. 22572.
54. Andreux PA, Houtkooper RH, Auwerx J. Pharmacological approaches to restore mitochondrial function. Nat Rev Drug Discov 2013; 12: 465-83; PMID: 23666487; http://dx. doi. org/10. 1038/nrd4023.
55. Sinha RA, Farah BL, Singh BK, Siddique MM, Li Y, Wu Y, Ilkayeva OR, Gooding J, Ching J, Zhou J, et al. Caffeine stimulates hepatic lipid metabolism by the autophagy-lysosomal pathway in mice. Hepatology 2014; 59: 1366-80; PMID: 23929677; http://dx. doi. org/10. 1002/hep. 26667.