PGC-1α buffers ROS-mediated removal of mitochondria during myogenesis

Cell Death and Disease

Volumn 5, Issue 11, 2014, Pages

  Baldelli, S ^a   Aquilano, K ^b   Ciriolo, M R ^b,c  

^a Faculty of Architecture and Industrial Design   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c IRCCS SAN RAFFAELE PISANA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ATROGIN 1; LIGHT CHAIN 3 ALPHA; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PINK1 PROTEIN; PROTEIN; PROTEIN BNIP3; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FKHR; TROLOX C; UNCLASSIFIED DRUG; 6-HYDROXY-2,5,7,8-TETRAMETHYLCHROMAN-2-CARBOXYLIC ACID; ANTIOXIDANT; CHROMAN DERIVATIVE; FBXO32 PROTEIN, MOUSE; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; MAP1LC3 PROTEIN, MOUSE; MICROTUBULE ASSOCIATED PROTEIN; MUSCLE PROTEIN; MYOG PROTEIN, MOUSE; MYOGENIN; PPARGC1A PROTEIN, MOUSE; PROTEIN KINASE; PTEN-INDUCED PUTATIVE KINASE; TRANSCRIPTION FACTOR; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL SIZE; CONTROLLED STUDY; DNA TRANSCRIPTION; MITOCHONDRIAL GENE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; MITOPHAGY; MOUSE; MUSCLE ATROPHY; MUSCLE DEVELOPMENT; MYOBLAST; MYOTUBE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CYTOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MITOCHONDRIAL DYNAMICS; MUSCLE CELL;

ANIMALS; ANTIOXIDANTS; CELL DIFFERENTIATION; CELL LINE; CHROMANS; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MITOCHONDRIA; MITOCHONDRIAL DEGRADATION; MITOCHONDRIAL TURNOVER; MUSCLE CELLS; MUSCLE DEVELOPMENT; MUSCLE PROTEINS; MYOGENIN; OXIDATIVE STRESS; PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION; SKP CULLIN F-BOX PROTEIN LIGASES; TRANSCRIPTION FACTORS;

EID: 84927946082     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2014.458     Document Type: Article

References (52)

1. Liesa M, Palacin M, Zorzano A. Mitochondrial dynamics in mammalian health and disease. Physiol Rev 2009; 89: 799-845.
2. Romanello V, Sandri M. Mitochondrial biogenesis and fragmentation as regulators of protein degradation in striated muscles. J Mol Cell Cardiol 2013; 55: 64-72.
3. Benard G, Bellance N, Jose C, Melser S, Nouette-Gaulain K, Rossignol R. Multi-site control and regulation of mitochondrial energy production. Biochim Biophys Acta 2010; 1797: 698-709.
4. Okamoto K, Kondo-Okamoto N. Mitochondria and autophagy: critical interplay between the two homeostats. Biochim Biophys Acta 2012; 1820: 595-600.
5. Sandri M. Signaling in muscle atrophy and hypertrophy. Physiology 2008; 23: 160-170.
6. Aquilano K, Vigilanza P, Baldelli S, Pagliei B, Rotilio G, Ciriolo MR. Peroxisome proliferator-activated receptor gamma co-activator 1alpha (PGC-1alpha) and sirtuin 1 (SIRT1) reside in mitochondria: possible direct function in mitochondrial biogenesis. J Biol Chem 2010; 285: 21590-21599.
7. Safdar A, Little JP, Stokl AJ, Hettinga BP, Akhtar M, Tarnopolsky MA. Exercise increases mitochondrial PGC-1alpha content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J Biol Chem 2011; 286: 10605-10617.
8. Scarpulla RC, Vega RB, Kelly DP. Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol Metab 2012; 23: 459-466.
9. Austin S, St-Pierre J. PGC1alpha and mitochondrial metabolism-emerging concepts and relevance in ageing and neurodegenerative disorders. J Cell Sci 2012; 125(Pt 21): 4963-4971.
10. Pagliei B, Aquilano K, Baldelli S, Ciriolo MR. Garlic-derived diallyl disulfide modulates peroxisome proliferator activated receptor gamma co-activator 1 alpha in neuroblastoma cells. Biochem Pharmacol 2012; 85: 335-344.
11. Aquilano K, Baldelli S, Pagliei B, Ciriolo MR. Extranuclear localization of SIRT1 and PGC-1alpha: an insight into possible roles in diseases associated with mitochondrial dysfunction. Curr Mol Med 2013; 13: 140-154.
12. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006; 127: 397-408.
13. Aquilano K, Baldelli S, Pagliei B, Cannata SM, Rotilio G, Ciriolo MR. p53 orchestrates the PGC-1alpha-mediated antioxidant response upon mild redox and metabolic imbalance. Antioxid Redox Signal 2013; 18: 386-399.
14. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, Rosenberg PB et al. Exercise stimulates Pgc-1alpha transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 2005; 280: 19587-19593.
15. Wright DC, Han DH, Garcia-Roves PM, Geiger PC, Jones TE, Holloszy JO. Exercise-induced mitochondrial biogenesis begins before the increase in muscle PGC-1alpha expression. J Biol Chem 2007; 282: 194-199.
16. Mahoney DJ, Parise G, Melov S, Safdar A, Tarnopolsky MA. Analysis of global mRNA expression in human skeletal muscle during recovery from endurance exercise. FA S E B J 2005; 19: 1498-1500.
17. Lin J, Wu H, Tarr PT, Zhang CY, Wu Z, Boss O et al. Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres. Nature 2002; 418: 797-801.
18. Takikita S, Schreiner C, Baum R, Xie T, Ralston E, Plotz PH et al. Fiber type conversion by PGC-1alpha activates lysosomal and autophagosomal biogenesis in both unaffected and Pompe skeletal muscle. PLoS One 2010; 5: e15239.
19. Brault JJ, Jespersen JG, Goldberg AL. Peroxisome proliferator-activated receptor gamma coactivator 1alpha or 1beta overexpression inhibits muscle protein degradation, induction of ubiquitin ligases, and disuse atrophy. J Biol Chem 2010; 285: 19460-19471.
20. Sandri M, Lin J, Handschin C, Yang W, Arany ZP, Lecker SH et al. PGC-1alpha protects skeletal muscle from atrophy by suppressing FoxO3 action and atrophy-specific gene transcription. Proc Natl Acad Sci USA 2006; 103: 16260-16265.
21. Mammucari C, Milan G, Romanello V, Masiero E, Rudolf R, Del Piccolo P et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab 2007; 6: 458-471.
22. Sengupta A, Molkentin JD, Paik JH, DePinho RA, Yutzey KE. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 2011; 286: 7468-7478.
23. Qi Z, Ding S. Transcriptional regulation by nuclear corepressors and PGC-1alpha: implications for mitochondrial quality control and insulin sensitivity. PPAR Res 2012; 2012: 348245.
24. 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.
25. Alers S, Loffler AS, Wesselborg S, Stork B. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 2012; 32: 2-11.
26. Lee JW, Park S, Takahashi Y, Wang HG. The association of AMPK with ULK1 regulates autophagy. PLoS One 2010; 5: e15394.
27. Azad MB, Chen Y, Gibson SB. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 2009; 11: 777-790.
28. Marmolino D, Manto M, Acquaviva F, Vergara P, Ravella A, Monticelli A et al. PGC-1alpha down-regulation affects the antioxidant response in Friedreich's ataxia. PLoS One 2010; 5: e10025.
29. Hay N. Interplay between FOXO, TOR, and Akt. Biochim Biophys Acta 2011; 1813: 1965-1970.
30. Tang H, Lee M, Budak MT, Pietras N, Hittinger S, Vu M et al. Intrinsic apoptosis in mechanically ventilated human diaphragm: linkage to a novel Fos/FoxO1/Stat3-Bim axis. FASEB J 2011; 25: 2921-2936.
31. Zhao Y, Yang J, Liao W, Liu X, Zhang H, Wang S et al. Cytosolic FoxO1 is essential for the induction of autophagy and tumour suppressor activity. Nat Cell Biol 2010; 12: 665-675.
32. Yamazaki Y, Kamei Y, Sugita S, Akaike F, Kanai S, Miura S et al. The cathepsin L gene is a direct target of FOXO1 in skeletal muscle. Biochem J 2010; 427: 171-178.
33. Knight JD, Kothary R. The myogenic kinome: protein kinases critical to mammalian skeletal myogenesis. Skelet Muscle 2011; 1: 29.
34. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A et al. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 2004; 117: 399-412.
35. Pagliei B, Aquilano K, Baldelli S, Ciriolo MR. Garlic-derived diallyl disulfide modulates peroxisome proliferator activated receptor gamma co-activator 1 alpha in neuroblastoma cells. Biochem Pharmacol 2013; 85: 335-344.
36. Scott I, Webster BR, Chan CK, Okonkwo JU, Han K, Sack MN. GCN5-like protein 1 (GCN5L1) controls mitochondrial content through coordinated regulation of mitochondrial biogenesis and mitophagy. J Biol Chem 2013; 289: 2864-2872.
37. Neill T, Torres A, Buraschi S, Owens RT, Hoek JB, Baffa R et al. Decorin induces mitophagy in breast carcinoma cells via PGC-1alpha and mitostatin. J Biol Chem 2014; 289: 4952-4968.
38. Masiero E, Agatea L, Mammucari C, Blaauw B, Loro E, Komatsu M et al. Autophagy is required to maintain muscle mass. Cell Metab 2009; 10: 507-515.
39. Li L, Ishdorj G, Gibson SB. Reactive oxygen species regulation of autophagy in cancer: implications for cancer treatment. Free Radic Biol Med 2012; 53: 1399-1410.
40. Desideri E, Filomeni G, Ciriolo MR. Glutathione participates in the modulation of starvation-induced autophagy in carcinoma cells. Autophagy 2012; 8: 1769-1781.
41. Sanchez AM, Csibi A, Raibon A, Cornille K, Gay S, Bernardi H et al. AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J Cell Biochem 2012; 113: 695-710.
42. Mei Y, Zhang Y, Yamamoto K, Xie W, Mak TW, You H. FOXO3a-dependent regulation of Pink1 (Park6) mediates survival signaling in response to cytokine deprivation. Proc Natl Acad Sci USA 2009; 106: 5153-5158.
43. Zhao J, Brault JJ, Schild A, Cao P, Sandri M, Schiaffino S et al. FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab 2007; 6: 472-483.
44. McLoughlin TJ, Smith SM, DeLong AD, Wang H, Unterman TG, Esser KA. FoxO1 induces apoptosis in skeletal myotubes in a DNA-binding-dependent manner. Am J Physiol Cell Physiol 2009; 297: C548-C555.
45. Geng T, Li P, Yin X, Yan Z. PGC-1alpha promotes nitric oxide antioxidant defenses and inhibits FOXO signaling against cardiac cachexia in mice. Am J Pathol 2011; 178: 1738-1748.
46. Handschin C, Chin S, Li P, Liu F, Maratos-Flier E, Lebrasseur NK et al. Skeletal muscle fibertype switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knockout animals. J Biol Chem 2007; 282: 30014-30021.
47. Rowe GC, Patten IS, Zsengeller ZK, El-Khoury R, Okutsu M, Bampoh S et al. Disconnecting mitochondrial content from respiratory chain capacity in PGC-1-deficient skeletal muscle. Cell Rep 2013; 3: 1449-1456.
48. Aquilano K, Vigilanza P, Rotilio G, Ciriolo MR. Mitochondrial damage due to SOD1 deficiency in SH-SY5Y neuroblastoma cells: a rationale for the redundancy of SOD1. FASEB J 2006; 20: 1683-1685.
49. Pellon-Maison M, Montanaro MA, Coleman RA, Gonzalez-Baro MR. Mitochondrial glycerol-3-P acyltransferase 1 is most active in outer mitochondrial membrane but not in mitochondrial associated vesicles (MAV). Biochim Biophys Acta 2007; 1771: 830-838.
50. Aquilano K, Vigilanza P, Filomeni G, Rotilio G, Ciriolo MR. Tau dephosphorylation and microfilaments disruption are upstream events of the anti-proliferative effects of DADS in SH-SY5Y cells. J Cell Mol Med 2010; 14: 564-577.
51. Aquilano K, Baldelli S, Ciriolo MR. Nuclear recruitment of nNOS by alpha-Syntrophin is Crucial for the Induction of Mitochondrial Biogenesis. J Biol Chem 2013; 289: 365-378.
52. Vigilanza P, Aquilano K, Baldelli S, Rotilio G, Ciriolo MR. Modulation of intracellular glutathione affects adipogenesis in 3T3-L1 cells. J Cell Physiol 2011; 226: 2016-2024.