Effects of Resveratrol and SIRT1 on PGC-1α Activity and Mitochondrial Biogenesis: A Reevaluation

PLoS Biology

Volumn 11, Issue 7, 2013, Pages

  Higashida, Kazuhiko ^a   Kim, Sang Hyun ^a   Jung, Su Ryun ^a   Asaka, Meiko ^a   Holloszy, John O ^a   Han, Dong Ho ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RESVERATROL; SIRTUIN 1;

ACETYLATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR PARAMETERS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEACETYLATION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; MALE; MITOCHONDRIAL BIOGENESIS; MOUSE; MYOTUBE; NONHUMAN; PROTEIN EXPRESSION; RAT; TRICEPS BRACHII MUSCLE;

ACETYLATION; ANIMALS; BLOTTING, WESTERN; CELL LINE; MALE; MICE; MICE, INBRED C57BL; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; RATS; RATS, SPRAGUE-DAWLEY; SIRTUIN 1; STILBENES; TRANSCRIPTION FACTORS;

EID: 84880926594     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001603     Document Type: Article

References (58)

1. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, et al. (2006) Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-342.
2. Pearson KJ, Baur JA, Lewis KN, Peshkin L, Price NL, et al. (2008) Resveratrol delays age-related deterioration and mimics transcriptional aspects of dietary restriction without extending life span. Cell Metab 8: 157-168.
3. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, et al. (2006) Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1α. Cell 127: 1109-1122.
4. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, et al. (2011) Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci 66: 191-201.
5. Strong R, Miller RA, Astle CM, Baur JA, de Cabo R, et al. (2012) Evaluation of resveratrol, green tea extract, curcumin, oxaloacetic acid, and medium-chain triglyceride oil on life span of genetically heterogeneous mice. J Gerontol A Biol Sci Med Sci 68: 6-16.
6. Handschin C, Spiegelman BM, (2006) Peroxisome proliferator-activated receptor gamma coactivator 1 coactivators, energy homeostasis, and metabolism. Endocr Rev 27: 728-735.
7. Feige JN, Lagouge M, Canto C, Strehle A, Houten SM, et al. (2008) Specific SIRT1 activation mimics low energy levels and protects against diet-induced metabolic disorders by enhancing fat oxidation. Cell Metab 8: 347-358.
8. Pacholec M, Bleasdale JE, Chrunyk B, Cunningham D, Flynn D, et al. (2010) SRT1720, SRT2183, SRT1460, and resveratrol are not direct activators of SIRT1. J Biol Chem 285: 8340-8351.
9. Howitz KT, Bitterman KJ, Cohen HY, Lamming DW, Lavu S, et al. (2003) Small molecule activators of sirtuins extend Saccharomyces cerevisiae lifespan. Nature 425: 191-196.
10. Kaeberlein M, McDonagh T, Heltweg B, Hixon J, Westman EA, et al. (2005) Substrate-specific activation of sirtuins by resveratrol. J Biol Chem 280: 17038-17045.
11. Borra MT, Smith BC, Denu JM, (2005) Mechanism of human SIRT1 activation by resveratrol. J Biol Chem 280: 17187-17195.
12. Dasgupta B, Milbrandt J, (2007) Resveratrol stimulates AMP kinase activity in neurons. Proc Natl Acad Sci USA 104: 7217-7222.
13. Zang M, Xu S, Maitland-Toolan KA, Zuccollo A, Hou X, et al. (2006) Polyphenols stimulate AMP-activated protein kinase, lower lipids, and inhibit accelerated atherosclerosis in diabetic LDL receptor-deficient mice. Diabetes 55: 2180-2191.
14. Park CE, Kim MJ, Lee JH, Min BI, Bae H, et al. (2007) Resveratrol stimulates glucose transport in C2C12 myotubes by activating AMP-activated protein kinase. Exp Mol Med 39: 222-229.
15. Cantó C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, et al. (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458: 1056-1060.
16. Holloszy JO, (1967) Biochemical adaptations in muscle. Effects of exercise on mitochondrial O2 uptake and respiratory enzyme activity in skeletal muscle. J Biol Chem 242: 2278-2282.
17. Holloszy JO, (2011) Regulation of mitochondrial biogenesis and GLUT4 expression by exercise. Compr Physiol 1: 921-940.
18. Booth F, Roberts CK, Laye MJ, (2012) Lack of exercise is a major cause of chronic diseases. Compr Physiol 2: 1143-1211.
19. Zheng J, Ramierz VD, (2000) Inhibition of mitochondrial proton F0F1-ATPase/ATP synthase by polyphenolic phytochemicals. British Journal of Pharmacology 130: 1115-1123.
20. Fang N, Casida JE, (1999) New bioactive flavonoids and stilbenes in Cubé resin insecticide. Journal of Natural Products 62: 205-210.
21. Udenigwe CC, Ramprasath VR, Aluko RE, Jones PJ, (2008) Potential of resveratrol in anticancer and anti-inflammatory therapy. Nutr Rev 66: 445-454.
22. Jäger S, Handschin C, St-Pierre J, Spiegelman BM, (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc Natl Acad Sci USA 104: 12017-12022.
23. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1α and SIRT1. Nature 434: 113-118.
24. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, et al. (2001) hSIR2 (SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107: 149-159.
25. Vega R, Huss JM, Kelly DP, (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol Cell Biol 20: 1868-1876.
26. Akimoto T, Pohnert SC, Li P, Zhang M, Gumbs C, et al. (2005) Exercise stimulates Pgc-1α transcription in skeletal muscle through activation of the p38 MAPK pathway. J Biol Chem 280: 19587-19593.
27. Cao W, Daniel KW, Robidoux J, Puigserver P, Medvedev AV, et al. (2004) p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol Cell Biol 24: 3057-3067.
28. Wright DC, Geiger PC, Han D-H, Jones TE, Holloszy JO, (2007) Calcium induces increases in peroxisome proliferator-activated receptor γ coactivator-1α and mitochondrial biogenesis by a pathway leading to p38 mitogen-activated protein kinase activation. J Biol Chem 282: 18793-18799.
29. Kim SH, Asaka M, Higashida K, Takahashi Y, Holloszy JO, et al. (2013) β-Adrenergic stimulation does not activate p38 MAPKinase or induce PGC-1α in skeletal muscle. Am J Physiol Endocrinol Metab 304: E844-E852.
30. Akimoto T, Li P, Yan Z, (2008) Functional interaction of regulatory factors with the Pgc-1α promoter in response to exercise by in vivo imaging. Am J Physiol: Cell Physiol 295: C288-C292.
31. Czubryt MP, McAnnally J, Fishman GI, Olson EN, (2003) Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci USA 100: 1711-1716.
32. McGee SL, van Denderen BJ, Howlett KF, Mollica J, Schertzer JD, et al. (2008) AMP-activated protein kinase regulates GLUT4 transcription by phosphorylating histone deacetylase 5. Diabetes 57: 860-867.
33. Cantó C, Jiang LQ, Deshmukh AS, Mataki C, Coste A, et al. (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell Metabolism 11: 213-219.
34. Bai P, Cantó C, Oudart H, Brunyanszki A, Cen Y, et al. (2011) PARP-1 inhibition increases mitochondrial metabolism through SIRT1 activation. Cell Metabolism 13: 461-468.
35. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, et al. (2007) Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26: 1913-1923.
36. Lerin C, Rodgers JT, Kalume DE, Kim SH, Pandey A, et al. (2006) GCN5 acetyltransferase complex controls glucose metabolism through transcriptional repression of PGC-1α. Cell Metabolism 3: 429-438.
37. Bai P, Cantó C, Brunyanszki A, Huber A, Szanto M, et al. (2011) PARP-2 regulates SIRT1 expression and whole-body energy expenditure. Cell Metab 13: 450-460.
38. Coste A, Louet JF, Lagouge M, Lerin C, Antal MC, et al. (2008) The genetic ablation of SRC-3 protects against obesity and improves insulin sensitivity by reducing the acetylation of PGC-1α. PNAS 105: 17187-17192.
39. Kelly TJ, Lerin C, Haas W, Gygi SP, Puigserver P, (2009) GCN5-mediated transcriptional control of the metabolic coactivator PGC-1β through lysine acetylation. J Biol Chem 284: 19945-19952.
40. Bouras T, Sauve AA, Wang F, Quong AA, Perkins ND, et al. (2005) SIRT1 deacetylation and repression of p300 involves lysine residues 1020/1024 within the cell cycle regulatory domain 1. J Biol Chem 280: 10264-10276.
41. Nemoto S, Fergusson MM, Finkel T, (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α. J Biol Chem 280: 16456-16460.
42. Puigserver P, Adelmant G, Wu Z, Fan M, Xu J, et al. (1999) Activation of PPARgamma coactivator-1 through transcription factor docking. Science 286: 1368-1371.
43. Gurd BJ, Yoshida Y, Lally J, Holloway GP, Bonen A, (2009) The deacetylase enzyme SIRT1 is not associated with oxidative capacity in rat heart and skeletal muscle and its overexpression reduces mitochondrial biogenesis. J Physiol 587 (8) (): 1817-1828.
44. Chen D, Bruno J, Easlon E, Lin SJ, Cheng HL, et al. (2008) Tissue-specific regulation of SIRT1 by calorie restriction. Genes & Development 22: 1753-1757.
45. Cohen DE, Supinski AM, Bonkowski MS, Donmez G, Guarente LP, (2009) Neuronal SIRT1 regulates endocrine and behavioral responses to calorie restriction. Genes Dev 23: 2812-2817.
46. Longo VD, (2009) Linking sirtuins, IGF-I signaling, and starvation. Exp Gerontol 44: 70-74.
47. Satoh A, Brace CS, Ben-Josef G, West T, Wozniak DF, et al. (2010) SIRT1 promotes the central adaptive response to diet restriction through activation of the dorsomedial and lateral nuclei of the hypothalamus. J Neurosci 30: 10220-10232.
48. Soare A, Cangemi R, Omodei D, Holloszy JO, Fontana L, (2011) Long-term calorie restriction, but not endurance exercise, lowers core body temperature in humans. Aging 3: 374-379.
49. Forsum E, Hillman PE, Nesheim MC, (1981) Effect of energy restriction on total heat production, basal metabolic rate, and specific dynamic action of food in rats. J Nutr 111: 1691-1697.
50. Duffy PH, Feuers RJ, Leakey JA, Nakamura K, Turturro A, et al. (1989) Effect of chronic caloric restriction on physiological variables related to energy metabolism in the male Fischer 344 rat. Mech Ageing Dev 48: 117-133.
51. Gonzales-Pacheco DM, Buss WC, Koehler KM, Woodside WF, Alpert SS, (1993) Energy restriction reduces metabolic rate in adult male Fisher-344 rats. J Nutr 123: 90-97.
52. Boily G, Seifert EL, Bevilacqua L, He XH, Sabourin G, et al. (2008) SirT1 regulates energy metabolism and response to caloric restriction in mice. PLoS ONE 3: e1759 doi:10.1371/journal.pone.0001759.
53. Puigserver P, Wu Z, Park CW, Graves R, Wright M, et al. (1998) A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92: 829-839.
54. Mu J, Brozinick JT Jr, Valladares O, Bucan M, Birnbaum MJ, (2001) A role for AMP-activated protein kinase in contraction- and hypoxia-regulated glucose transport in skeletal muscle. Mol Cell 7: 1085-1094.
55. He TC, Zhou S, da Costa LT, Yu J, Kinzler KW, et al. (1998) A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA 95: 2509-2514.
56. Akimoto T, Sorg BS, Yan Z, (2004) Real-time imaging of peroxisome proliferator-activated receptor-gamma coactivator-1α promoter activity in skeletal muscles of living mice. Am J Physiol: Cell Physiol 287: C790-C796.
57. Han D-H, Hancock CR, Jung SR, Higashida K, Kim SH, et al. (2011) Deficiency of the mitochondrial electron transport chain in muscle does not cause insulin resistance. PLoS ONE 6: e19739 doi:10.1371/journal.pone.0019739.
58. Hancock CR, Han D-H, Higashida K, Kim SH, Holloszy JO, (2011) Does calorie restriction induce mitochondrial biogenesis? A reevaluation. FASEB J 25: 785-791.