Mitochondrial metabolic reprogramming induced by calorie restriction

Antioxidants and Redox Signaling

Volumn 19, Issue 3, 2013, Pages 310-320

  Martin Montalvo, Alejandro ^a   De Cabo, Rafael ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SIRTUIN 1;

AGING; APOPTOSIS; BIOGENESIS; CALORIC RESTRICTION; CELL AGING; ENERGY METABOLISM; METABOLIC BALANCE; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN METABOLISM; REVIEW;

ANIMALS; APOPTOSIS; BIOMIMETICS; CALORIC RESTRICTION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MITOCHONDRIAL TURNOVER; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 84879516992     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4866     Document Type: Review

References (94)

1. Algire C, Moiseeva O, Deschenes-Simard X, Amrein L, Petruccelli L, Birman E, Viollet B, Ferbeyre G, and Pollak MN. Metformin reduces endogenous reactive oxygen species and associated DNA damage. Cancer Prev Res (Phila) 5: 536-543, 2012.
2. Andrews ZB and Horvath TL. Uncoupling protein-2 regulates lifespan in mice. Am J Physiol 296: E621-E627, 2009.
3. Anisimov VN, Berstein LM, Egormin PA, Piskunova TS, Popovich IG, Zabezhinski MA, Tyndyk ML, Yurova MV, Kovalenko IG, Poroshina TE, and Semenchenko AV. Metformin slows down aging and extends life span of female SHR mice. Cell Cycle (Georgetown, TX) 7: 2769-2773, 2008.
4. Anisimov VN, Berstein LM, Popovich IG, Zabezhinski MA, Egormin PA, Piskunova TS, Semenchenko AV, Tyndyk ML, Yurova MN, Kovalenko IG, and Poroshina TE. If started early in life, metformin treatment increases life span and postpones tumors in female SHR mice. Aging 3: 148-157, 2011.
5. Baker DJ, Betik AC, Krause DJ, and Hepple RT. No decline in skeletal muscle oxidative capacity with aging in long-term calorically restricted rats: effects are independent of mitochondrial DNA integrity. J Gerontol 61: 675-684, 2006.
6. Barros MH, Bandy B, Tahara EB, and Kowaltowski AJ. Higher respiratory activity decreases mitochondrial reactive oxygen release and increases life span in Saccharomyces cerevisiae. J Biol Chem 279: 49883-49888, 2004.
7. Baur JA, Pearson KJ, Price NL, Jamieson HA, Lerin C, Kalra A, Prabhu VV, Allard JS, Lopez-Lluch G, Lewis K, Pistell PJ, Poosala S, Becker KG, Boss O, Gwinn D, Wang M, Ramaswamy S, Fishbein KW, Spencer RG, Lakatta EG, Le Couteur D, Shaw RJ, Navas P, Puigserver P, Ingram DK, de Cabo R, and Sinclair DA. Resveratrol improves health and survival of mice on a high-calorie diet. Nature 444: 337-342, 2006.
8. Berge RK, Tronstad KJ, Berge K, Rost TH, Wergedahl H, Gudbrandsen OA, and Skorve J. The metabolic syndrome and the hepatic fatty acid drainage hypothesis. Biochimie 87: 15-20, 2005.
9. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, and Harper ME. Effects of short-and medium-term calorie restriction on muscle mitochondrial proton leak and reactive oxygen species production. Am J Physiol 286: E852-E861, 2004.
10. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, Steele AD, Crowe H, Marmor S, Luo J, Gu W, and Guarente L. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell 6: 759-767, 2007.
11. Brown MK, Evans JL, and Luo Y. Beneficial effects of natural antioxidants EGCG and alpha-lipoic acid on life span and age-dependent behavioral declines in Caenorhabditis elegans. Pharmacol, Biochem, Behav 85: 620-628, 2006.
12. Bruce CR, Anderson MJ, Carey AL, Newman DG, Bonen A, Kriketos AD, Cooney GJ, and Hawley JA. Muscle oxidative capacity is a better predictor of insulin sensitivity than lipid status. J Clin Endocrinol Metab 88: 5444-5451, 2003.
13. Burnett C, Valentini S, Cabreiro F, Goss M, Somogyvari M, Piper MD, Hoddinott M, Sutphin GL, Leko V, McElwee JJ, Vazquez-Manrique RP, Orfila AM, Ackerman D, Au C, Vinti G, Riesen M, Howard K, Neri C, Bedalov A, Kaeberlein M, Soti C, Partridge L, and Gems D. Absence of effects of Sir2 overexpression on lifespan in C. elegans and Drosophila. Nature 477: 482-485.
14. Canto C and Auwerx J. Calorie restriction: is AMPK a key sensor and effector? Physiology (Bethesda, MD) 26: 214-224.
15. Chan JM and Giovannucci EL. Vegetables, fruits, associated micronutrients, and risk of prostate cancer. Epidemiol Rev 23: 82-86, 2001.
16. Chen C, Yu R, Owuor ED, and Kong AN. Activation of antioxidant-response element (ARE), mitogen-activated protein kinases (MAPKs) and caspases by major green tea polyphenol components during cell survival and death. Arch Pharm Res 23: 605-612, 2000.
17. Civitarese AE, Carling S, Heilbronn LK, Hulver MH, Ukropcova B, Deutsch WA, Smith SR, and Ravussin E. Calorie restriction increases muscle mitochondrial biogenesis in healthy humans. PLoS Med 4: e76, 2007.
18. Colagiuri S. Diabesity: therapeutic options. Diabetes Obes Metab 12: 463-473, 2010.
19. Corradetti MN and Guan KL. Upstream of the mammalian target of rapamycin: do all roads pass through mTOR? Oncogene 25: 6347-6360, 2006.
20. Cui L, Jeong H, Borovecki F, Parkhurst CN, Tanese N, and Krainc D. Transcriptional repression of PGC-1alpha by mutant huntingtin leads to mitochondrial dysfunction and neurodegeneration. Cell 127: 59-69, 2006.
21. Curtis R, O'Connor G, and DiStefano PS. Aging networks in Caenorhabditis elegans: AMP-activated protein kinase (aak-2) links multiple aging and metabolism pathways. Aging Cell 5: 119-126, 2006.
22. Czubryt MP, McAnally J, Fishman GI, and Olson EN. Regulation of peroxisome proliferator-activated receptor gamma coactivator 1 alpha (PGC-1 alpha) and mitochondrial function by MEF2 and HDAC5. Proc Natl Acad Sci USA 100: 1711-1716, 2003.
23. Dali-Youcef N, Lagouge M, Froelich S, Koehl C, Schoonjans K, and Auwerx J. Sirtuins: the 'magnificent seven', function, metabolism and longevity. Ann Med 39: 335-345, 2007.
24. Dhahbi JM, Mote PL, Fahy GM, and Spindler SR. Identification of potential caloric restriction mimetics by microarray profiling. Physiol Genomics 23: 343-350, 2005.
25. Essen-Gustavsson B and Borges O. Histochemical and metabolic characteristics of human skeletal muscle in relation to age. Acta Physiol Scand 126: 107-114, 1986.
26. Fan M, Rhee J, St-Pierre J, Handschin C, Puigserver P, Lin J, Jaeger S, Erdjument-Bromage H, Tempst P, and Spiegelman BM. Suppression of mitochondrial respiration through recruitment of p160 myb binding protein to PGC-1alpha: modulation by p38 MAPK. Genes Dev 18: 278-289, 2004.
27. Faulks SC, Turner N, Else PL, and Hulbert AJ. Calorie restriction in mice: effects on body composition, daily activity, metabolic rate, mitochondrial reactive oxygen species production, and membrane fatty acid composition. J Gerontol 61: 781-794, 2006.
28. Finkel T, Deng CX, and Mostoslavsky R. Recent progress in the biology and physiology of sirtuins. Nature 460: 587-591, 2009.
29. Franke TF. PI3K/Akt: getting it right matters. Oncogene 27: 6473-6488, 2008.
30. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, and Sartorelli V. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev Cell 14: 661-673, 2008.
31. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, Franke TF, Papapetropoulos A, and Sessa WC. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 399: 597-601, 1999.
32. Gates AC, Bernal-Mizrachi C, Chinault SL, Feng C, Schneider JG, Coleman T, Malone JP, Townsend RR, Chakravarthy MV, and Semenkovich CF. Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease. Cell Metab 6: 497-505, 2007.
33. Genova ML, Pich MM, Bernacchia A, Bianchi C, Biondi A, Bovina C, Falasca AI, Formiggini G, Castelli GP, and Lenaz G. The mitochondrial production of reactive oxygen species in relation to aging and pathology. Ann N Y Acad Sci 1011: 86-100, 2004.
34. Gerhart-Hines Z, Rodgers JT, Bare O, Lerin C, Kim SH, Mostoslavsky R, Alt FW, Wu Z, and Puigserver P. Metabolic control of muscle mitochondrial function and fatty acid oxidation through SIRT1/PGC-1alpha. EMBO J 26: 1913-1923, 2007.
35. Gonzalez AA, Kumar R, Mulligan JD, Davis AJ, Weindruch R, and Saupe KW. Metabolic adaptations to fasting and chronic caloric restriction in heart, muscle, and liver do not include changes in AMPK activity. Am J Physiol 287: E1032-E1037, 2004.
36. Gupta S, Mathur R, and Dwarakanath BS. The glycolytic inhibitor 2-deoxy-D-glucose enhances the efficacy of etoposide in ehrlich ascites tumor-bearing mice. Cancer Biol Ther 4: 87-94, 2005.
37. Halicka HD, Zhao H, Li J, Traganos F, Zhang S, Lee M, and Darzynkiewicz Z. Genome protective effect of metformin as revealed by reduced level of constitutive DNA damage signaling. Aging (Albany, NY) 3: 1028-1038.
38. Hansen BC, Ortmeyer HK, and Bodkin NL. Prevention of obesity in middle-aged monkeys: food intake during body weight clamp. Obes Res 3 Suppl 2: 199s-204s, 1995.
39. Hansen M, Taubert S, Crawford D, Libina N, Lee SJ, and Kenyon C. Lifespan extension by conditions that inhibit translation in Caenorhabditis elegans. Aging Cell 6: 95-110, 2007.
40. Hariharakrishnan J, Satpute RM, Prasad GB, and Bhattacharya R. Oxidative stress mediated cytotoxicity of cyanide in LLC-MK2 cells and its attenuation by alpha-ketoglutarate and N-acetyl cysteine. Toxicol Lett 185: 132-141, 2009.
41. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, and Miller RA. Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460: 392-395, 2009.
42. Hepple RT, Baker DJ, Kaczor JJ, and Krause DJ. Long-term caloric restriction abrogates the age-related decline in skeletal muscle aerobic function. FASEB J 19: 1320-1322, 2005.
43. Herranz D, Munoz-Martin M, Canamero M, Mulero F, Martinez-Pastor B, Fernandez-Capetillo O, and Serrano M. Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nat Commun 1: 3, 2010.
44. Holloszy JO and Fontana L. Caloric restriction in humans. Exp Gerontol 42: 709-712, 2007.
45. Hou X, Song J, Li XN, Zhang L, Wang X, Chen L, and Shen YH. Metformin reduces intracellular reactive oxygen species levels by upregulating expression of the antioxidant thioredoxin via the AMPK-FOXO3 pathway. Biochem Biophys Res Commun 396: 199-205.
46. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, and Vanfleteren JR. No reduction of metabolic rate in food restricted Caenorhabditis elegans. Exp Gerontol 37: 1359-1369, 2002.
47. Howell TH. The art of living long by Luigi Cornaro. Age Ageing 16: 194-195, 1987.
48. Kapahi P, Zid BM, Harper T, Koslover D, Sapin V, and Benzer S. Regulation of lifespan in Drosophila by modulation of genes in the TOR signaling pathway. Curr Biol 14: 885-890, 2004.
49. Keipert S, Klaus S, Heldmaier G, and Jastroch M. UCP1 ectopically expressed in murine muscle displays native function and mitigates mitochondrial superoxide production. Biochim Biophys Acta 1797: 324-330, 2010.
50. Kitani K, Osawa T, and Yokozawa T. The effects of tetrahydrocurcumin and green tea polyphenol on the survival of male C57BL/6 mice. Biogerontology 8: 567-573, 2007.
51. Klaassen CD and Slitt AL. Regulation of hepatic transporters by xenobiotic receptors. Curr Drug Metab 6: 309-328, 2005.
52. Klenow H. Inhibition by cordycepin and 2-deoxyglucose of the incorporation of (32p)orthophosphate into the nucleic acids of ehrlich ascites-tumor cells in vitro. Biochim Biophys Acta 76: 354-365, 1963.
53. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, and Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 127: 1109-1122, 2006.
54. Larsson L, Sjodin B, and Karlsson J. Histochemical and biochemical changes in human skeletal muscle with age in sedentary males, age 22-65 years. Acta Physiol Scand 103: 31-39, 1978.
55. Lee KS, Lee BS, Semnani S, Avanesian A, Um CY, Jeon HJ, Seong KM, Yu K, Min KJ, and Jafari M. Curcumin extends life span, improves health span, and modulates the expression of age-associated aging genes in Drosophila melanogaster. Rejuvenation Res 13: 561-570.
56. Liao VH, Yu CW, Chu YJ, Li WH, Hsieh YC, and Wang TT. Curcumin-mediated lifespan extension in Caenorhabditis elegans. Mech Ageing Dev 132: 480-487.
57. Lin SJ, Kaeberlein M, Andalis AA, Sturtz LA, Defossez PA, Culotta VC, Fink GR, and Guarente L. Calorie restriction extends Saccharomyces cerevisiae lifespan by increasing respiration. Nature 418: 344-348, 2002.
58. Lopez-Lluch G, Hunt N, Jones B, Zhu M, Jamieson H, Hilmer S, Cascajo MV, Allard J, Ingram DK, Navas P, and de Cabo R. Calorie restriction induces mitochondrial biogenesis and bioenergetic efficiency. Proc Natl Acad Sci USA 103: 1768-1773, 2006.
59. Mandlekar S, Hong JL, and Kong AN. Modulation of metabolic enzymes by dietary phytochemicals: a review of mechanisms underlying beneficial versus unfavorable effects. Cur Drug Metab 7: 661-675, 2006.
60. Martin-Montalvo A, Villalba JM, Navas P, and de Cabo R. NRF2, cancer and calorie restriction. Oncogene 30: 505-520.
61. Marzetti E, Lees HA, Wohlgemuth SE, and Leeuwenburgh C. Sarcopenia of aging: underlying cellular mechanisms and protection by calorie restriction. BioFactors (Oxford, England) 35: 28-35, 2009.
62. Marzetti E, Wohlgemuth SE, Lees HA, Chung HY, Giovannini S, and Leeuwenburgh C. Age-related activation of mitochondrial caspase-independent apoptotic signaling in rat gastrocnemius muscle. Mech Ageing Dev 129: 542-549, 2008.
63. Metter EJ, Talbot LA, Schrager M, and Conwit R. Skeletal muscle strength as a predictor of all-cause mortality in healthy men. J Gerontol 57: B359-B365, 2002.
64. Miller RA, Harrison DE, Astle CM, Baur JA, Boyd AR, de Cabo R, Fernandez E, Flurkey K, Javors MA, Nelson JF, Orihuela CJ, Pletcher S, Sharp ZD, Sinclair D, Starnes JW, Wilkinson JE, Nadon NL, and Strong R. Rapamycin, but not resveratrol or simvastatin, extends life span of genetically heterogeneous mice. J Gerontol A: Biol Sci Med Sci 66: 191-201, 2011.
65. Milne JC, Lambert PD, Schenk S, Carney DP, Smith JJ, Gagne DJ, Jin L, Boss O, Perni RB, Vu CB, Bemis JE, Xie R, Disch JS, Ng PY, Nunes JJ, Lynch AV, Yang H, Galonek H, Israelian K, Choy W, Iffland A, Lavu S, Medvedik O, Sinclair DA, Olefsky JM, Jirousek MR, Elliott PJ, and Westphal CH. Small molecule activators of SIRT1 as therapeutics for the treatment of type 2 diabetes. Nature 450: 712-716, 2007.
66. Minor RK, Baur JA, Gomes AP, Ward TM, Csiszar A, Mercken EM, Abdelmohsen K, Shin Y-K, Canto C, Scheibye-Knudsen M, Krawczyk M, Irusta PM, Martin-Montalvo A, Hubbard BP, Zhang Y, Lehrmann E, White AA, Price NL, Swindell WR, Pearson KJ, Becker KG, Bohr VA, Gorospe M, Egan JM, Talan MI, Auwerx J, Westphal CH, Ellis JL, Ungvari Z, Vlasuk GP, Elliott PJ, Sinclair DA, and de Cabo R. SRT1720 improves survival and healthspan of obese mice. Sci Rep 1: 70, 2011.
67. Minor RK, Smith DL, Jr., Sossong AM, Kaushik S, Poosala S, Spangler EL, Roth GS, Lane M, Allison DB, de Cabo R, Ingram DK, and Mattison JA. Chronic ingestion of 2-deoxy-Dglucose induces cardiac vacuolization and increases mortality in rats. Toxicol Appl Pharmacol 243: 332-339, 2010.
68. Miyagi S, Iwama N, Kawabata T, and Hasegawa K. Longevity and diet in Okinawa, Japan: the past, present and future. Asia Pac J Public Health 15 Suppl: S3-S9, 2003.
69. Motohashi H and Yamamoto M. Nrf2-Keap1 defines a physiologically important stress response mechanism. Trends Mol Med 10: 549-557, 2004.
70. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, Banayo E, Mihaylova MM, Nelson MC, Zou Y, Juguilon H, Kang H, Shaw RJ, and Evans RM. AMPK and PPARdelta agonists are exercise mimetics. Cell 134: 405-415, 2008.
71. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, and Carruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science (New York, NY) 310: 314-317, 2005.
72. Onken B and Driscoll M. Metformin induces a dietary restriction-like state and the oxidative stress response to extend C. elegans Healthspan via AMPK, LKB1, and SKN-1. PloS One 5: e8758, 2010.
73. Pearson KJ, Lewis KN, Price NL, Chang JW, Perez E, Cascajo MV, Tamashiro KL, Poosala S, Csiszar A, Ungvari Z, Kensler TW, Yamamoto M, Egan JM, Longo DL, Ingram DK, Navas P, and de Cabo R. Nrf2 mediates cancer protection but not prolongevity induced by caloric restriction. Proc Natl Acad Sci USA 105: 2325-2330, 2008.
74. Reznick RM, Zong H, Li J, Morino K, Moore IK, Yu HJ, Liu ZX, Dong J, Mustard KJ, Hawley SA, Befroy D, Pypaert M, Hardie DG, Young LH, and Shulman GI. Aging-associated reductions in AMP-activated protein kinase activity and mitochondrial biogenesis. Cell Metab 5: 151-156, 2007.
75. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, and Puigserver P. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434: 113-118, 2005.
76. Rooyackers OE, Adey DB, Ades PA, and Nair KS. Effect of age on in vivo rates of mitochondrial protein synthesis in human skeletal muscle. Proc Natl Acad Sci USA 93: 15364-15369, 1996.
77. Scarpello JH. Improving survival with metformin: the evidence base today. Diabetes Metab 29: 6S36-6S43, 2003.
78. Schmeisser S, Zarse K, and Ristow M. Lonidamine extends lifespan of adult Caenorhabditis elegans by increasing the formation of mitochondrial reactive oxygen species. Horm Metab Res 43: 687-692.
79. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, and Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 6: 280-293, 2007.
80. Smith JJ, Kenney RD, Gagne DJ, Frushour BP, Ladd W, Galonek HL, Israelian K, Song J, Razvadauskaite G, Lynch AV, Carney DP, Johnson RJ, Lavu S, Iffland A, Elliott PJ, Lambert PD, Elliston KO, Jirousek MR, Milne JC, and Boss O. Small molecule activators of SIRT1 replicate signaling pathways triggered by calorie restriction in vivo. BMC Syst Biol 3: 31, 2009.
81. Speakman JR, Talbot DA, Selman C, Snart S, McLaren JS, Redman P, Krol E, Jackson DM, Johnson MS, and Brand MD. Uncoupled and surviving: individual mice with high metabolism have greater mitochondrial uncoupling and live longer. Aging Cell 3: 87-95, 2004.
82. Stuart JA, Bourque BM, de Souza-Pinto NC, and Bohr VA. No evidence of mitochondrial respiratory dysfunction in OGG1-null mice deficient in removal of 8-oxodeoxyguanine from mitochondrial DNA. Free Radic Biol Med 38: 737-745, 2005.
83. Tassa A, Roux MP, Attaix D, and Bechet DM. Class III phosphoinositide 3-kinase-Beclin1 complex mediates the amino acid-dependent regulation of autophagy in C2C12 myotubes. Biochem J 376: 577-586, 2003.
84. Testa CM, Sherer TB, and Greenamyre JT. Rotenone induces oxidative stress and dopaminergic neuron damage in organotypic substantia nigra cultures. Brain Res Mol Brain Res 134: 109-118, 2005.
85. Tuveson D and Hanahan D. Translational medicine: Cancer lessons from mice to humans. Nature 471: 316-317, 2011.
86. Ungvari Z, Labinskyy N, Mukhopadhyay P, Pinto JT, Bagi Z, Ballabh P, Zhang C, Pacher P, and Csiszar A. Resveratrol attenuates mitochondrial oxidative stress in coronary arterial endothelial cells. Am J Physiol Heart Circ Physiol 297: H1876-H1881, 2009.
87. van Gurp M, Festjens N, van Loo G, Saelens X, and Vandenabeele P. Mitochondrial intermembrane proteins in cell death. Biochem Biophys Res Commun 304: 487-497, 2003.
88. Wanagat J, Cao Z, Pathare P, and Aiken JM. Mitochondrial DNA deletion mutations colocalize with segmental electron transport system abnormalities, muscle fiber atrophy, fiber splitting, and oxidative damage in sarcopenia. FASEB J 15: 322-332, 2001.
89. White R, Morganstein D, Christian M, Seth A, Herzog B, and Parker MG. Role of RIP140 in metabolic tissues: connections to disease. FEBS Lett 582: 39-45, 2008.
90. Wu Z, Huang X, Feng Y, Handschin C, Feng Y, Gullicksen PS, Bare O, Labow M, Spiegelman B, and Stevenson SC. Transducer of regulated CREB-binding proteins (TORCs) induce PGC-1alpha transcription and mitochondrial biogenesis in muscle cells. Proc Natl Acad Sci USA 103: 14379-14384, 2006.
91. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, and Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98: 115-124, 1999.
92. Zarse K, Bossecker A, Muller-Kuhrt L, Siems K, Hernandez MA, Berendsohn WG, Birringer M, and Ristow M. The phytochemical glaucarubinone promotes mitochondrial metabolism, reduces body fat, and extends lifespan of Caenorhabditis elegans. Horm Metab Res 43: 241-243.
93. Zarse K, Schmeisser S, Birringer M, Falk E, Schmoll D, and Ristow M. Differential effects of resveratrol and SRT1720 on lifespan of adult Caenorhabditis elegans. Horm Metab Res 42: 837-839, 2010.
94. Zhu Z, Jiang W, Thompson MD, McGinley JN, and Thompson HJ. Metformin as an energy restriction mimetic agent for breast cancer prevention. J Carcinog 10: 17, 2011.