PGC-1α-mediated adaptations in skeletal muscle

Pflugers Archiv European Journal of Physiology

Volumn 460, Issue 1, 2010, Pages 153-162

  Olesen, Jesper ^a   Kiilerich, Kristian ^a   Pilegaard, Henriette ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Adaptations; Exercise; PGC 1 ; Skeletal muscle

Indexed keywords

CARNITINE PALMITOYLTRANSFERASE I; CITRATE SYNTHASE; GLUCOSE TRANSPORTER 4; MEDIUM CHAIN ACYL COENZYME A DEHYDROGENASE; MYOCYTE ENHANCER FACTOR 2; NUCLEAR RESPIRATORY FACTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PYRUVATE DEHYDROGENASE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FOXO; TRANSCRIPTION FACTOR YY1; ANTIOXIDANT; AUTACOID; HEAT SHOCK PROTEIN; PPARGC1A PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ADAPTATION; ANGIOGENESIS; ANIMAL EXPERIMENT; ANTIOXIDANT ACTIVITY; BROWN ADIPOSE TISSUE; CARBOHYDRATE METABOLISM; CONTROLLED STUDY; ENDURANCE TRAINING; ENZYME REGULATION; ENZYME SUBSTRATE; EXERCISE; GENE CONTROL; GLUCONEOGENESIS; IMMOBILIZATION; INFLAMMATION; LIFESTYLE; LIPID METABOLISM; MOUSE; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; REVIEW; SKELETAL MUSCLE; TISSUE DISTRIBUTION; ANIMAL; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MUSCLE CONTRACTION; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ANTIOXIDANTS; ENERGY METABOLISM; EXERCISE; GENE EXPRESSION REGULATION; HEAT-SHOCK PROTEINS; HUMANS; INFLAMMATION MEDIATORS; MUSCLE CONTRACTION; MUSCLE, SKELETAL; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEDENTARY LIFESTYLE; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 77952892253     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-010-0834-0     Document Type: Review

References (68)

1. PJ Adhihetty G Uguccioni L Leick, et al. 2009 The role of PGC-1{alpha} on mitochondrial function and apoptotic susceptibility in muscle Am J Physiol Cell Physiol 297 C217 C225 10.1152/ajpcell.00070.2009 1:CAS:528:DC%2BD1MXovVKjsbc%3D 19439529
2. Z Arany SY Foo Y Ma, et al. 2008 HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha Nature 451 1008 1012 10.1038/nature06613 1:CAS:528:DC%2BD1cXit1ynsr8%3D 18288196 (Pubitemid 351301733)
3. Z Arany L He J Lin 2005 Transcriptional coactivator PGC-1α controls the energy state and contractile function of cardiac muscle Cell Metabol 1 259 271 10.1016/j.cmet.2005.03.002 1:CAS:528:DC%2BD2MXjvFaqsb8%3D (Pubitemid 43960608)
4. K Baar AR Wende TE Jones, et al. 2002 Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1 FASEB J 16 1879 1886 10.1096/fj.02-0367com 1:CAS:528:DC%2BD38Xps1Ojtbk%3D 12468452 (Pubitemid 35462607)
5. R Barres ME Osler A Rune, et al. 2009 Non-CpG methylation of the PGC-1a promoter through DNMT3B controls mitochondrial density Cell Metabol 10 189 198 10.1016/j.cmet.2009.07.011 1:CAS:528:DC%2BD1MXhsVChtLnO
6. Booth FW, Baldwin KM (1996) Muscle plasticity: energy demand and supply processes. In: Rowell LB, Shepherd JT (eds) The handbook of physiology. Exercise: regulation and integration of multiple systems. American Physiological Society, Bethesda, pp 1075-1123
7. JA Calvo TG Daniels X Wang, et al. 2008 Muscle-specific expression of PPARgamma coactivator-1alpha improves exercise performance and increases peak oxygen uptake J Appl Physiol 104 1304 1312 10.1152/japplphysiol.01231.2007 1:CAS:528:DC%2BD1cXmsFemt7w%3D 18239076
8. C Canto Z Gerhart-Hines JN Feige, et al. 2009 AMPK regulates energy expenditure by modulating NAD+metabolism and SIRT1 activity Nature 458 1056 1062 10.1038/nature07813 1:CAS:528:DC%2BD1MXivVKltLc%3D 19262508
9. J Chinsomboon J Ruas R Gupta, et al. 2009 The transcriptional coactivator PGC-1alpha mediates exercise-induced angiogenesis in skeletal muscle PNAS 106 21401 21406 10.1073/pnas.0909131106 1:CAS:528:DC%2BC3cXjvFGqtr4%3D 19966219
10. KE Conley SA Jubrias PC Esselman 2000 Oxidative capacity and ageing in human muscle J Physiol 526 203 210 10.1111/j.1469-7793.2000.t01-1-00203.x 1:CAS:528:DC%2BD3cXlsFaltrs%3D 10878112
11. D Constantin-Teodosiu DJ Baker D Constantin PL Greenhaff 2009 PPARdelta agonism inhibits skeletal muscle PDC activity, mitochondrial ATP production and force generation during prolonged contraction J Physiol 587 231 239 10.1113/jphysiol.2008.164210 1:CAS:528:DC%2BD1MXhtVKlsLk%3D 19001043
12. FE De G Alvarez R Berria, et al. 2008 Insulin-resistant muscle is exercise resistant: evidence for reduced response of nuclear-encoded mitochondrial genes to exercise Am J Physiol 294 E607 E614
13. Dominy JE Jr, Lee Y, Gerhart-Hines Z, Puigserver P (2010) Nutrient-dependent regulation of PGC-1alpha's acetylation state and metabolic function through the enzymatic activities of Sirt1/GCN5. Biochem Biophys doi: 10.1016/j.bbapap.2009.11.023
14. T Geng P Li M Okutsu, et al. 2010 PGC-1α plays a functional role in exercise-induced mitochondrial biogenesis and angiogenesis but not fiber-type transformation in mouse skeletal muscle Am J Physiol Cell Physiol 298 C572 C579 10.1152/ajpcell.00481.2009 1:CAS:528:DC%2BC3cXjsFGhu7w%3D 20032509
15. Z Gerhart-Hines JT Rodgers O Bare, et al. 2007 Metabolic control of mitochondrial function and fatty acid oxidation through PGC-1alpha/SIRT1 EMBO J 26 1902 1912 10.1038/sj.emboj.7601633 (Pubitemid 46624046)
16. C Handschin S Chin P Li, et al. 2007 Skeletal muscle fiber-type switching, exercise intolerance, and myopathy in PGC-1alpha muscle-specific knock-out animals J Biol Chem 282 30014 30021 10.1074/jbc.M704817200 1:CAS:528:DC%2BD2sXhtFagtbvF 17702743 (Pubitemid 350035265)
17. C Handschin CS Choi S Chin, et al. 2007 Abnormal glucose homeostasis in skeletal muscle-specific PGC-1α knockout mice reveals skeletal muscle-pancreatic βcell crosstalk J Clin Invest 117 3463 3474 10.1172/JCI31785 1:CAS:528:DC%2BD2sXht12is7%2FN 17932564 (Pubitemid 350097002)
18. C Handschin J Rhee J Lin, et al. 2003 An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle PNAS 100 7111 7116 10.1073/pnas.1232352100 1:CAS:528: DC%2BD3sXkslOnurk%3D 12764228 (Pubitemid 36706401)
19. C Handschin BM Spiegelman 2008 The role of exercise and PGC1α in inflammation and chronic disease Nature 454 463 469 10.1038/nature07206 1:CAS:528:DC%2BD1cXovV2mtbk%3D 18650917
20. I Irrcher JP Adhihetty T Sheehan, et al. 2003 PPARγ coactivator-1α expression during thyroid hormone- and contractile activity-induced mitochondrial adaptations Am J Physiol 284 C1669 C1677 1:CAS:528:DC%2BD3sXltVegsbY%3D
21. S Jager C Handschin J St-Pierre BM Spiegelman 2007 AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1{alpha} PNAS 104 12017 12022 10.1073/pnas.0705070104 17609368 (Pubitemid 47185622)
22. SB Jorgensen JT Treebak B Viollet, et al. 2007 Role of AMPKalpha2 in basal, training-, and AICAR-induced GLUT4, hexokinase II, and mitochondrial protein expression in mouse muscle Am J Physiol 292 E331 E339
23. SB Jorgensen JFP Wojtaszewski B Viollet, et al. 2005 Effects of alpha-AMPK knockout on exercise-induced gene activation in mouse skeletal muscle FASEB J 19 1146 1148 15878932
24. DP Kelly RC Scarpulla 2007 Transcriptional regulatory circuits controlling mitochondrial biogenesis and function Genes Dev 18 357 368 10.1101/gad.1177604
25. Kiilerich K, Adser H, Jakobsen AH et al (2009) Role of PGC-1α in PDH regulation in mouse skeletal muscle. Biochem Exerc (in press)
26. JA Koval RA DeFronzo RM O'Doherty, et al. 1998 Regulation of hexokinase II activity and expression in human muscle by moderate exercise Am J Physiol 274 E304 E308 1:CAS:528:DyaK1cXis1yqsbo%3D 9486162
27. Y Kraniou D Cameron-Smith M Misso, et al. 2000 Effects of exercise on GLUT-4 and glycogenin gene expression in human skeletal muscle J Appl Physiol 88 794 796 10.1063/1.373804 1:CAS:528:DC%2BD3cXht12isLo%3D 10658052
28. K Kusuhara K Madsen L Jensen, et al. 2007 Calcium signalling in the regulation of PGC-1alpha, PDK4 and HKII mRNA expression Biol Chem 388 481 488 10.1515/BC.2007.052 1:CAS:528:DC%2BD2sXlsVWnsLk%3D 17516843 (Pubitemid 46800257)
29. L Leick Y Hellsten J Fentz, et al. 2009 PGC-1{alpha} mediates exercise-induced skeletal muscle VEGF expression in mice Am J Physiol 297 E92 E103 1:CAS:528:DC%2BD1MXovVKjt78%3D
30. Leick L, Lyngby SS, Wojtaszewski JFP, Pilegaard H (2010) PGC-1α is required for training-induced prevention of age-associated decline in mitochondrial enzymes in mouse skeletal muscle. Exp Gerontol 45:336-342
31. Leick L, Plomgaard P, Wojtaszewski JFP, Pilegaard H (2009) Endurance exercise induces mRNA of oxidative proteins in human skeletal muscle late in recovery. Scan J Sports Med (in press)
32. L Leick JF Wojtaszewski ST Johansen, et al. 2008 PGC-1alpha is not mandatory for exercise- and training-induced adaptive gene responses in mouse skeletal muscle Am J Physiol 294 E463 E474 1:CAS:528:DC%2BD1cXit1ykurY%3D
33. TC Leone JJ Lehman BN Finck, et al. 2005 PGC-1α deficiency causes multi-system energy metabolic dearrangements: muscle dysfunction, abnormal weight control and hepatic steatosis PLoS Biol 3 e101 10.1371/journal.pbio. 0030101 15760270 (Pubitemid 40721160)
34. C Lerin JT Rodgers DE Kalume, et al. 2006 GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1alpha Cell Metabol 3 429 438 10.1016/j.cmet.2006.04.013 1:CAS:528:DC%2BD28Xmt1eku7s%3D (Pubitemid 43811779)
35. J Lin C Handschin BM Spiegelman 2005 Metabolic control through the PGC-1 family of transcription coactivators Cell Metabol 1 361 370 10.1016/j.cmet.2005. 05.004 (Pubitemid 43960626)
36. J Lin H Wu PT Tarr, et al. 2002 Transcriptional co-activator PGC-1 alpha drives the formation of slow-twitch muscle fibres Nature 418 797 801 10.1038/nature00904 1:CAS:528:DC%2BD38XmtV2gu7o%3D 12181572
37. J Lin PH Wu PT Tarr, et al. 2004 Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice Cell 119 121 135 10.1016/j.cell.2004.09.013 1:CAS:528:DC%2BD2cXotlyqu7s%3D 15454086 (Pubitemid 39349325)
38. C Ling P Poulsen E Carlsson, et al. 2004 Multiple environmental and genetic factors influence skeletal muscle PGC-1alpha and PGC-1beta gene expression in twins J Clin Invest 114 1518 1526 1:CAS:528:DC%2BD2cXpvFOqsb0%3D 15546003
39. LF Michael Z Wu RB Cheatham, et al. 2001 Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1 PNAS 98 3820 3825 10.1073/pnas.061035098 1:CAS:528:DC%2BD3MXis1Khsrg%3D 11274399 (Pubitemid 32249855)
40. PD Neufer GL Dohm 1993 Exercise induces a transient increase in transcription of the GLUT-4 gene in skeletal muscle Am J Physiol 265 C1597 C1603 1:CAS:528:DyaK2cXhsF2ru7c%3D 7506491
41. RM O'Doherty DP Bracy DK Granner DH Wasserman 1996 Transcription of the rat skeletal muscle hexokinase II gene is increased by acute exercise J Appl Physiol 81 789 793 8872647
42. EO Ojuka TE Jones DH Han, et al. 2003 Raising Ca2+ in L6 myotubes mimics effects of exercise on mitochondrial biogenesis in muscle FASEB J 17 675 681 10.1096/fj.02-0951com 1:CAS:528:DC%2BD3sXislKls7Y%3D 12665481 (Pubitemid 37221153)
43. H Pilegaard GA Ordway B Saltin PD Neufer 2000 Transcriptional regulation of gene expression in human skeletal muscle during recovery from exercise Am J Physiol 279 E806 E814 1:CAS:528:DC%2BD3cXnsFOrtLc%3D
44. H Pilegaard T Osada L Andersen, et al. 2005 Influence of substrate availability on transcriptional regulation of metabolic genes in human skeletal muscle Metab 54 1048 1055 10.1016/j.metabol.2005.03.008 1:CAS:528: DC%2BD2MXmvVGiurY%3D (Pubitemid 41033106)
45. H Pilegaard B Saltin PD Neufer 2003 Exercise induces transient transcriptional activation of the PGC-1alpha gene in human skeletal muscle J Physiol 546 851 858 10.1113/jphysiol.2002.034850 1:CAS:528:DC%2BD3sXitlSmtrg%3D 12563009 (Pubitemid 36204518)
46. P Puigserver J Rhee J Lin, et al. 2001 Cytokine stimulation of energy expenditure through p38 MAP kinase activation of PPARgamma coactivator-1 Mol Cell 8 971 982 10.1016/S1097-2765(01)00390-2 1:CAS:528:DC%2BD3MXovFOit78%3D 11741533 (Pubitemid 34031800)
47. P Puigserver Z Wu CW Park R Graves M Wright BM Spiegelman 1998 A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis Cell 92 6 829 839 10.1016/S0092-8674(00)81410-5 1:CAS:528:DyaK1cXit1Klsb8%3D 9529258 (Pubitemid 28155321)
48. KSC Röckl CA Witczak LJ Goodyear 2008 Signaling mechanisms in skeletal muscle: acute responses and chronic adaptations to exercise Life 60 145 153 18380005
49. JT Rodgers C Lerin Z Gerhart-Hines P Puigserver 2008 Metabolic adaptations through the PGC-1α and SIRT1 pathways FEBS Lett 582 46 53 10.1016/j.febslet.2007.11.034 1:CAS:528:DC%2BD2sXhsVOltb3J 18036349 (Pubitemid 350297246)
50. JT Rodgers C Lerin W Haas, et al. 2005 Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1 Nature 434 113 118 10.1038/nature03354 1:CAS:528:DC%2BD2MXhslClsb0%3D 15744310 (Pubitemid 40349395)
51. P Seale S Kajumuras W Yang, et al. 2007 Transcriptional control of brown fat determination by PRDM16 Cell Metabol 6 38 54 10.1016/j.cmet.2007.06.001 1:CAS:528:DC%2BD2sXotlCitLo%3D (Pubitemid 47008902)
52. RL Seip K Mair TG Cole CF Semenkovich 1997 Induction of human skeletal muscle lipoprotein lipase gene expression by short-term exercise is transient Am J Physiol 272 E255 E261 1:CAS:528:DyaK2sXhvVCrtrY%3D 9124332
53. LR Silveira H Pilegaard K Kusuhara, et al. 2006 The effect of reactive oxygen species and antioxidants on basal and contraction-induced gene expression of PGC-1α, UCP3 and HKII in primary rat skeletal muscle cells Biochem Biophys Acta 1763 969 976 10.1016/j.bbamcr.2006.06.010 1:CAS:528: DC%2BD28XptlyrtLY%3D 16916551 (Pubitemid 44332599)
54. J St-Pierre S Drori M Uldry, et al. 2006 Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators Cell 127 397 408 10.1016/j.cell.2006.09.024 1:CAS:528:DC%2BD28XhtFOkt7rM 17055439 (Pubitemid 44572377)
55. J St-Pierre J Lin S Krauss, et al. 2003 Bioenergetic analysis of peroxisome proliferator-activated receptor gamma coactivators 1alpha and 1beta (PGC-1alpha and PGC-1beta) in muscle cells J Biol Chem 278 26597 26603 10.1074/jbc.M301850200 1:CAS:528:DC%2BD3sXltlKqsL0%3D 12734177 (Pubitemid 36876804)
56. MC Sugden MJ Holness 2003 Recent advances in mechanisms regulating glucose oxidation at the level of the pyruvate dehydrogenase complex by PDK's Am J Physiol 284 E855 E862 1:CAS:528:DC%2BD3sXjvFGqt7c%3D
57. M Suwa H Nakano Z Radak S Kumagai 2008 Endurance exercise increases the SIRT1 and peroxisome proliferator-activated receptor gamma coactivator-1alpha protein expression in rat skeletal muscle Metab 57 986 998 10.1016/j.metabol. 2008.02.017 1:CAS:528:DC%2BD1cXnt1egsr4%3D (Pubitemid 351814692)
58. S Terada M Goto M Kato, et al. 2002 Effects of low-intensity prolonged exercise on PGC-1 mRNA expression in rat epitrochlearis muscle Biochem Biophys Res Commun 296 350 354 10.1016/S0006-291X(02)00881-1 1:CAS:528: DC%2BD38XlvF2gtro%3D 12163024
59. RB Vega JM Huss DP Kelly 2000 The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor alpha in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes Mol Cell Biol 20 1868 1876 10.1128/MCB.20.5.1868-1876.2000 1:CAS:528:DC%2BD3cXhtF2ntb8%3D 10669761 (Pubitemid 30100203)
60. AE Wallberg S Yamamurra D Malik, et al. 2003 Coordination of p300-mediated chromatin remodelling and TRAP/mediator function through coactivator PGC-1α Mol Cell 12 1137 1149 10.1016/S1097-2765(03)00391-5 1:CAS:528:DC%2BD3sXpvVGhtb4%3D 14636573 (Pubitemid 37487924)
61. KE Wellen GS Hotamisligil 2005 Inflammation, stress, and diabetes J Clin Invest 115 1111 1119 1:CAS:528:DC%2BD2MXktFSksbY%3D 15864338
62. AR Wende JM Huss PJ Schaeffer, et al. 2005 PGC-1α coactivates PDK4 gene expression via the orphan nuclear receptor ERRα: a mechanism for transcriptional control of muscle glucose metabolism Mol Cell Biol 25 10684 10694 10.1128/MCB.25.24.10684-10694.2005 1:CAS:528:DC%2BD2MXhtleksbfJ 16314495 (Pubitemid 41747115)
63. AR Wende PJ Schaeffer GJ Parker, et al. 2007 A role for the transcriptional coactivator PGC-1α in muscle refueling J Biol Chem 50 36642 36651 10.1074/jbc.M707006200
64. T Wenz S Rossi RL Rotundo, et al. 2009 Increased muscle PGC-1alpha expression protects from sarcopenia and metabolic disease during aging PNAS 106 20405 20410 10.1073/pnas.0911570106 1:CAS:528:DC%2BC3cXjtFWjtw%3D%3D 19918075
65. Williams RS, Neufer PD (1996) Regulation of gene expression in skeletal muscle by contractile activity. In: Rowell LB, Shepherd JT (eds) The handbook of physiology. Exercise: regulation and integration of multiple systems. American Physiological Society, Bethesda, pp 1124-1150
66. DC Wright PC Geiger DH Han, et al. 2007 Calcium induces increases in peroxisome proliferator-activated receptor gamma coactivator-1alpha and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation J Biol Chem 282 18793 18799 10.1074/jbc.M611252200 1:CAS:528:DC%2BD2sXmvVarsLw%3D 17488713 (Pubitemid 47100154)
67. H Wu SB Kanatous FA Thurmond, et al. 2002 Regulation of mitochondrial biogenesis in skeletal muscle by CaMK Science 296 349 352 10.1126/science. 1071163 1:CAS:528:DC%2BD38XjtVWhs7w%3D 11951046 (Pubitemid 34303690)
68. Z Wu P Puigserver U Andersson, et al. 1999 Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1 Cell 98 115 124 10.1016/S0092-8674(00)80611-X 1:CAS:528:DyaK1MXks1Kktrs%3D 10412986 (Pubitemid 29331201)