4,675
Views
72
CrossRef citations to date
0
Altmetric
Report

Dexamethasone-induced autophagy mediates muscle atrophy through mitochondrial clearance

, , , , , , , , , , & show all
Pages 2281-2295 | Received 03 Apr 2014, Accepted 17 May 2014, Published online: 04 Jun 2014

References

  • Revollo JR, Cidlowski JA. Mechanisms generating diversity in glucocorticoid receptor signaling. Ann N Y Acad Sci 2009; 1179:167 - 78; http://dx.doi.org/10.1111/j.1749-6632.2009.04986.x; PMID: 19906239
  • Ramamoorthy S, Cidlowski JA. Exploring the molecular mechanisms of glucocorticoid receptor action from sensitivity to resistance. Endocr Dev 2013; 24:41 - 56; http://dx.doi.org/10.1159/000342502; PMID: 23392094
  • Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology (Bethesda) 2008; 23:160 - 70; http://dx.doi.org/10.1152/physiol.00041.2007; PMID: 18556469
  • Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117:399 - 412; http://dx.doi.org/10.1016/S0092-8674(04)00400-3; PMID: 15109499
  • Mammucari C, Schiaffino S, Sandri M. Downstream of Akt: FoxO3 and mTOR in the regulation of autophagy in skeletal muscle. Autophagy 2008; 4:524 - 6; PMID: 18367868
  • Lynch GS, Schertzer JD, Ryall JG. Therapeutic approaches for muscle wasting disorders. Pharmacol Ther 2007; 113:461 - 87; http://dx.doi.org/10.1016/j.pharmthera.2006.11.004; PMID: 17258813
  • Wang X, Blagden C, Fan J, Nowak SJ, Taniuchi I, Littman DR, Burden SJ. Runx1 prevents wasting, myofibrillar disorganization, and autophagy of skeletal muscle. Genes Dev 2005; 19:1715 - 22; http://dx.doi.org/10.1101/gad.1318305; PMID: 16024660
  • Dobrowolny G, Aucello M, Rizzuto E, Beccafico S, Mammucari C, Boncompagni S, Belia S, Wannenes F, Nicoletti C, Del Prete Z, et al. Skeletal muscle is a primary target of SOD1G93A-mediated toxicity. Cell Metab 2008; 8:425 - 36; http://dx.doi.org/10.1016/j.cmet.2008.09.002; PMID: 19046573
  • Deval C, Mordier S, Obled C, Bechet D, Combaret L, Attaix D, Ferrara M. Identification of cathepsin L as a differentially expressed message associated with skeletal muscle wasting. Biochem J 2001; 360:143 - 50; http://dx.doi.org/10.1042/0264-6021:3600143; PMID: 11696001
  • Lokireddy S, Wijesoma IW, Teng S, Bonala S, Gluckman PD, McFarlane C, Sharma M, Kambadur R. The ubiquitin ligase Mul1 induces mitophagy in skeletal muscle in response to muscle-wasting stimuli. Cell Metab 2012; 16:613 - 24; http://dx.doi.org/10.1016/j.cmet.2012.10.005; PMID: 23140641
  • Yamamoto D, Maki T, Herningtyas EH, Ikeshita N, Shibahara H, Sugiyama Y, Nakanishi S, Iida K, Iguchi G, Takahashi Y, et al. Branched-chain amino acids protect against dexamethasone-induced soleus muscle atrophy in rats. Muscle Nerve 2010; 41:819 - 27; http://dx.doi.org/10.1002/mus.21621; PMID: 20169591
  • Lee SR, Kim HK, Song IS, Youm J, Dizon LA, Jeong SH, Ko TH, Heo HJ, Ko KS, Rhee BD, et al. Glucocorticoids and their receptors: insights into specific roles in mitochondria. Prog Biophys Mol Biol 2013; 112:44 - 54; http://dx.doi.org/10.1016/j.pbiomolbio.2013.04.001; PMID: 23603102
  • Verdejo HE, del Campo A, Troncoso R, Gutierrez T, Toro B, Quiroga C, Pedrozo Z, Munoz JP, Garcia L, Castro PF, et al. Mitochondria, myocardial remodeling, and cardiovascular disease. Curr Hypertens Rep 2012; 14:532 - 9; http://dx.doi.org/10.1007/s11906-012-0305-4; PMID: 22972531
  • Romanello V, Guadagnin E, Gomes L, Roder I, Sandri C, Petersen Y, Milan G, Masiero E, Del Piccolo P, Foretz M, et al. Mitochondrial fission and remodelling contributes to muscle atrophy. EMBO J 2010; 29:1774 - 85; http://dx.doi.org/10.1038/emboj.2010.60; PMID: 20400940
  • Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, Chan DC. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 2010; 141:280 - 9; http://dx.doi.org/10.1016/j.cell.2010.02.026; PMID: 20403324
  • Hernández-Alvarez MI, Paz JC, Sebastián D, Muñoz JP, Liesa M, Segalés J, Palacín M, Zorzano A. Glucocorticoid modulation of mitochondrial function in hepatoma cells requires the mitochondrial fission protein Drp1. Antioxid Redox Signal 2013; 19:366 - 78; http://dx.doi.org/10.1089/ars.2011.4269; PMID: 22703557
  • Xia X, Kar R, Gluhak-Heinrich J, Yao W, Lane NE, Bonewald LF, Biswas SK, Lo WK, Jiang JX. Glucocorticoid-induced autophagy in osteocytes. J Bone Miner Res 2010; 25:2479 - 88; http://dx.doi.org/10.1002/jbmr.160; PMID: 20564240
  • Grandér D, Kharaziha P, Laane E, Pokrovskaja K, Panaretakis T. Autophagy as the main means of cytotoxicity by glucocorticoids in hematological malignancies. Autophagy 2009; 5:1198 - 200; http://dx.doi.org/10.4161/auto.5.8.10122; PMID: 19855186
  • Klionsky DJ, Abdalla FC, Abeliovich H, Abraham RT, Acevedo-Arozena A, Adeli K, Agholme L, Agnello M, Agostinis P, Aguirre-Ghiso JA, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy 2012; 8:445 - 544; http://dx.doi.org/10.4161/auto.19496; PMID: 22966490
  • Lavandero S, Troncoso R, Rothermel BA, Martinet W, Sadoshima J, Hill JA. Cardiovascular autophagy: concepts, controversies, and perspectives. Autophagy 2013; 9:1455 - 66; http://dx.doi.org/10.4161/auto.25969; PMID: 23959233
  • Kadmiel M, Cidlowski JA. Glucocorticoid receptor signaling in health and disease. Trends Pharmacol Sci 2013; 34:518 - 30; http://dx.doi.org/10.1016/j.tips.2013.07.003; PMID: 23953592
  • Kewalramani G, Puthanveetil P, Wang F, Kim MS, Deppe S, Abrahani A, Luciani DS, Johnson JD, Rodrigues B. AMP-activated protein kinase confers protection against TNF-alpha-induced cardiac cell death. Cardiovasc Res 2009; 84:42 - 53; http://dx.doi.org/10.1093/cvr/cvp166; PMID: 19477967
  • del Campo A, Parra V, Vásquez-Trincado C, Gutiérrez T, Morales PE, López-Crisosto C, Bravo-Sagua R, Navarro-Marquez MF, Verdejo HE, Contreras-Ferrat A, et al. Mitochondrial fragmentation impairs insulin-dependent glucose uptake by modulating Akt activity through mitochondrial Ca2+ uptake. Am J Physiol Endocrinol Metab 2014; 306:E1 - 13; PMID: 24085037
  • Chan DC. Fusion and fission: interlinked processes critical for mitochondrial health. Annu Rev Genet 2012; 46:265 - 87; http://dx.doi.org/10.1146/annurev-genet-110410-132529; PMID: 22934639
  • Schakman O, Kalista S, Barbé C, Loumaye A, Thissen JP. Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol 2013; 45:2163 - 72; http://dx.doi.org/10.1016/j.biocel.2013.05.036; PMID: 23806868
  • Mizushima N, Levine B, Cuervo AM, Klionsky DJ. Autophagy fights disease through cellular self-digestion. Nature 2008; 451:1069 - 75; http://dx.doi.org/10.1038/nature06639; PMID: 18305538
  • Levine B, Kroemer G. Autophagy in aging, disease and death: the true identity of a cell death impostor. Cell Death Differ 2009; 16:1 - 2; http://dx.doi.org/10.1038/cdd.2008.139; PMID: 19079285
  • Raben N, Wong A, Ralston E, Myerowitz R. Autophagy and mitochondria in Pompe disease: nothing is so new as what has long been forgotten. Am J Med Genet C Semin Med Genet 2012; 160C:13 - 21; http://dx.doi.org/10.1002/ajmg.c.31317; PMID: 22253254
  • Nishino I, Fu J, Tanji K, Yamada T, Shimojo S, Koori T, Mora M, Riggs JE, Oh SJ, Koga Y, et al. Primary LAMP-2 deficiency causes X-linked vacuolar cardiomyopathy and myopathy (Danon disease). Nature 2000; 406:906 - 10; http://dx.doi.org/10.1038/35022604; PMID: 10972294
  • Suzuki T, Nakagawa M, Yoshikawa A, Sasagawa N, Yoshimori T, Ohsumi Y, Nishino I, Ishiura S, Nonaka I. The first molecular evidence that autophagy relates rimmed vacuole formation in chloroquine myopathy. J Biochem 2002; 131:647 - 51; http://dx.doi.org/10.1093/oxfordjournals.jbchem.a003147; PMID: 11983070
  • Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M, Metzger D, Reggiani C, Schiaffino S, Sandri M. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10:507 - 15; http://dx.doi.org/10.1016/j.cmet.2009.10.008; PMID: 19945408
  • Buttgereit F, Krauss S, Brand MD. Methylprednisolone inhibits uptake of Ca2+ and Na+ ions into concanavalin A-stimulated thymocytes. Biochem J 1997; 326:329 - 32; PMID: 9291100
  • Croxtall JD, Choudhury Q, Flower RJ. Glucocorticoids act within minutes to inhibit recruitment of signalling factors to activated EGF receptors through a receptor-dependent, transcription-independent mechanism. Br J Pharmacol 2000; 130:289 - 98; http://dx.doi.org/10.1038/sj.bjp.0703272; PMID: 10807665
  • Buttgereit F, Scheffold A. Rapid glucocorticoid effects on immune cells. Steroids 2002; 67:529 - 34; http://dx.doi.org/10.1016/S0039-128X(01)00171-4; PMID: 11960631
  • Buttgereit F, Wehling M, Burmester GR. A new hypothesis of modular glucocorticoid actions: steroid treatment of rheumatic diseases revisited. Arthritis Rheum 1998; 41:761 - 7; http://dx.doi.org/10.1002/1529-0131(199805)41:5<761::AID-ART2>3.0.CO;2-M; PMID: 9588727
  • Ayroldi E, Cannarile L, Migliorati G, Nocentini G, Delfino DV, Riccardi C. Mechanisms of the anti-inflammatory effects of glucocorticoids: genomic and nongenomic interference with MAPK signaling pathways. FASEB J 2012; 26:4805 - 20; http://dx.doi.org/10.1096/fj.12-216382; PMID: 22954589
  • Lee SR, Kim HK, Youm JB, Dizon LA, Song IS, Jeong SH, Seo DY, Ko KS, Rhee BD, Kim N, et al. Non-genomic effect of glucocorticoids on cardiovascular system. Pflugers Arch 2012; 464:549 - 59; http://dx.doi.org/10.1007/s00424-012-1155-2; PMID: 23001133
  • Bellavance MA, Rivest S. The neuroendocrine control of the innate immune system in health and brain diseases. Immunol Rev 2012; 248:36 - 55; http://dx.doi.org/10.1111/j.1600-065X.2012.01129.x; PMID: 22725953
  • Pérez MH, Cormack J, Mallinson D, Mutungi G. A membrane glucocorticoid receptor mediates the rapid/non-genomic actions of glucocorticoids in mammalian skeletal muscle fibres. J Physiol 2013; 591:5171 - 85; http://dx.doi.org/10.1113/jphysiol.2013.256586; PMID: 23878367
  • Nishimura M, Mikura M, Hirasaka K, Okumura Y, Nikawa T, Kawano Y, Nakayama M, Ikeda M. Effects of dimethyl sulphoxide and dexamethasone on mRNA expression of myogenesis- and muscle proteolytic system-related genes in mouse myoblastic C2C12 cells. J Biochem 2008; 144:717 - 24; http://dx.doi.org/10.1093/jb/mvn126; PMID: 18835828
  • Waddell DS, Baehr LM, van den Brandt J, Johnsen SA, Reichardt HM, Furlow JD, Bodine SC. The glucocorticoid receptor and FOXO1 synergistically activate the skeletal muscle atrophy-associated MuRF1 gene. Am J Physiol Endocrinol Metab 2008; 295:E785 - 97; http://dx.doi.org/10.1152/ajpendo.00646.2007; PMID: 18612045
  • Kuo T, Lew MJ, Mayba O, Harris CA, Speed TP, Wang JC. Genome-wide analysis of glucocorticoid receptor-binding sites in myotubes identifies gene networks modulating insulin signaling. Proc Natl Acad Sci U S A 2012; 109:11160 - 5; http://dx.doi.org/10.1073/pnas.1111334109; PMID: 22733784
  • Yu CY, Mayba O, Lee JV, Tran J, Harris C, Speed TP, Wang JC. Genome-wide analysis of glucocorticoid receptor binding regions in adipocytes reveal gene network involved in triglyceride homeostasis. PLoS One 2010; 5:e15188; http://dx.doi.org/10.1371/journal.pone.0015188; PMID: 21187916
  • Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S, Lecker SH, Goldberg AL. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6:472 - 83; http://dx.doi.org/10.1016/j.cmet.2007.11.004; PMID: 18054316
  • Dodson S, Baracos VE, Jatoi A, Evans WJ, Cella D, Dalton JT, Steiner MS. Muscle wasting in cancer cachexia: clinical implications, diagnosis, and emerging treatment strategies. Annu Rev Med 2011; 62:265 - 79; http://dx.doi.org/10.1146/annurev-med-061509-131248; PMID: 20731602
  • Emery AE. The muscular dystrophies. Lancet 2002; 359:687 - 95; http://dx.doi.org/10.1016/S0140-6736(02)07815-7; PMID: 11879882
  • Evans WJ. Skeletal muscle loss: cachexia, sarcopenia, and inactivity. Am J Clin Nutr 2010; 91:1123S - 7S; http://dx.doi.org/10.3945/ajcn.2010.28608A; PMID: 20164314
  • Lecker SH. Ubiquitin-protein ligases in muscle wasting: multiple parallel pathways?. Curr Opin Clin Nutr Metab Care 2003; 6:271 - 5; http://dx.doi.org/10.1097/01.mco.0000068963.34812.e5; PMID: 12690258
  • Cárdenas C, Miller RA, Smith I, Bui T, Molgó J, Müller M, Vais H, Cheung KH, Yang J, Parker I, et al. Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 2010; 142:270 - 83; http://dx.doi.org/10.1016/j.cell.2010.06.007; PMID: 20655468
  • Rambold AS, Lippincott-Schwartz J. Mechanisms of mitochondria and autophagy crosstalk. Cell Cycle 2011; 10:4032 - 8; http://dx.doi.org/10.4161/cc.10.23.18384; PMID: 22101267
  • Pi H, Xu S, Zhang L, Guo P, Li Y, Xie J, Tian L, He M, Lu Y, Li M, et al. Dynamin 1-like-dependent mitochondrial fission initiates overactive mitophagy in the hepatotoxicity of cadmium. Autophagy 2013; 9:1780 - 800; http://dx.doi.org/10.4161/auto.25665; PMID: 24121705
  • Kroemer G, Mariño G, Levine B. Autophagy and the integrated stress response. Mol Cell 2010; 40:280 - 93; http://dx.doi.org/10.1016/j.molcel.2010.09.023; PMID: 20965422
  • East DA, Campanella M. Ca2+ in quality control: an unresolved riddle critical to autophagy and mitophagy. Autophagy 2013; 9:1710 - 9; http://dx.doi.org/10.4161/auto.25367; PMID: 24121708
  • Tiao G, Fagan J, Roegner V, Lieberman M, Wang JJ, Fischer JE, Hasselgren PO. Energy-ubiquitin-dependent muscle proteolysis during sepsis in rats is regulated by glucocorticoids. J Clin Invest 1996; 97:339 - 48; http://dx.doi.org/10.1172/JCI118421; PMID: 8567953
  • Fang CH, James HJ, Ogle C, Fischer JE, Hasselgren PO. Influence of burn injury on protein metabolism in different types of skeletal muscle and the role of glucocorticoids. J Am Coll Surg 1995; 180:33 - 42; PMID: 8000653
  • Hu Z, Wang H, Lee IH, Du J, Mitch WE. Endogenous glucocorticoids and impaired insulin signaling are both required to stimulate muscle wasting under pathophysiological conditions in mice. J Clin Invest 2009; 119:3059 - 69; PMID: 19759515
  • Fitts RH, Romatowski JG, Peters JR, Paddon-Jones D, Wolfe RR, Ferrando AA. The deleterious effects of bed rest on human skeletal muscle fibers are exacerbated by hypercortisolemia and ameliorated by dietary supplementation. Am J Physiol Cell Physiol 2007; 293:C313 - 20; http://dx.doi.org/10.1152/ajpcell.00573.2006; PMID: 17409123
  • Lecker SH, Goldberg AL, Mitch WE. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 2006; 17:1807 - 19; http://dx.doi.org/10.1681/ASN.2006010083; PMID: 16738015
  • Castillero E, Alamdari N, Lecker SH, Hasselgren PO. Suppression of atrogin-1 and MuRF1 prevents dexamethasone-induced atrophy of cultured myotubes. Metabolism 2013; 62:1495 - 502; http://dx.doi.org/10.1016/j.metabol.2013.05.018; PMID: 23866982
  • Givvimani S, Munjal C, Tyagi N, Sen U, Metreveli N, Tyagi SC. Mitochondrial division/mitophagy inhibitor (Mdivi) ameliorates pressure overload induced heart failure. PLoS One 2012; 7:e32388; http://dx.doi.org/10.1371/journal.pone.0032388; PMID: 22479323
  • Ong SB, Subrayan S, Lim SY, Yellon DM, Davidson SM, Hausenloy DJ. Inhibiting mitochondrial fission protects the heart against ischemia/reperfusion injury. Circulation 2010; 121:2012 - 22; http://dx.doi.org/10.1161/CIRCULATIONAHA.109.906610; PMID: 20421521
  • Zhang X, Yan H, Yuan Y, Gao J, Shen Z, Cheng Y, Shen Y, Wang RR, Wang X, Hu WW, et al. Cerebral ischemia-reperfusion-induced autophagy protects against neuronal injury by mitochondrial clearance. Autophagy 2013; 9:1321 - 33; http://dx.doi.org/10.4161/auto.25132; PMID: 23800795
  • Parra V, Eisner V, Chiong M, Criollo A, Moraga F, Garcia A, Härtel S, Jaimovich E, Zorzano A, Hidalgo C, et al. Changes in mitochondrial dynamics during ceramide-induced cardiomyocyte early apoptosis. Cardiovasc Res 2008; 77:387 - 97; http://dx.doi.org/10.1093/cvr/cvm029; PMID: 18006463
  • Troncoso R, Vicencio JM, Parra V, Nemchenko A, Kawashima Y, Del Campo A, Toro B, Battiprolu PK, Aranguiz P, Chiong M, et al. Energy-preserving effects of IGF-1 antagonize starvation-induced cardiac autophagy. Cardiovasc Res 2012; 93:320 - 9; http://dx.doi.org/10.1093/cvr/cvr321; PMID: 22135164
  • Munoz JP, Chiong M, García L, Troncoso R, Toro B, Pedrozo Z, Diaz-Elizondo J, Salas D, Parra V, Núñez MT, et al. Iron induces protection and necrosis in cultured cardiomyocytes: Role of reactive oxygen species and nitric oxide. Free Radic Biol Med 2010; 48:526 - 34; http://dx.doi.org/10.1016/j.freeradbiomed.2009.11.017; PMID: 19969068
  • Marambio P, Toro B, Sanhueza C, Troncoso R, Parra V, Verdejo H, García L, Quiroga C, Munafo D, Díaz-Elizondo J, et al. Glucose deprivation causes oxidative stress and stimulates aggresome formation and autophagy in cultured cardiac myocytes. Biochim Biophys Acta 2010; 1802:509 - 18; http://dx.doi.org/10.1016/j.bbadis.2010.02.002; PMID: 20176105
  • Bravo R, Vicencio JM, Parra V, Troncoso R, Munoz JP, Bui M, Quiroga C, Rodriguez AE, Verdejo HE, Ferreira J, et al. Increased ER-mitochondrial coupling promotes mitochondrial respiration and bioenergetics during early phases of ER stress. J Cell Sci 2011; 124:2143 - 52; http://dx.doi.org/10.1242/jcs.080762; PMID: 21628424

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.