Caloric restriction primes mitochondria for ischemic stress by deacetylating specific mitochondrial proteins of the electron transport chain

Circulation Research

Volumn 109, Issue 4, 2011, Pages 396-406

  Shinmura, Ken ^a   Tamaki, Kayoko ^a   Sano, Motoaki ^a   Nakashima Kamimura, Naomi ^b   Wolf, Alexander M ^b   Amo, Taku ^b,c   Ohta, Shigeo ^b   Katsumata, Yoshinori ^a   Fukuda, Keiichi ^a   Ishiwata, Kyoko ^a   Suematsu, Makoto ^a   Adachi, Takeshi ^a,d  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c NATIONAL DEFENSE ACADEMY   (Japan)

^d NATIONAL DEFENSE MEDICAL COLLEGE   (Japan)

Author keywords

ischemia; mitochondria; nutrition; reactive oxygen species; reperfusion

Indexed keywords

HYDROGEN PEROXIDE; KAEMPFEROL; MANGANESE SUPEROXIDE DISMUTASE; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; MITOCHONDRIAL PROTEIN; NICOTINAMIDE; PROTEOME; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; REACTIVE OXYGEN METABOLITE; RESVERATROL; SIRTUIN; SUCCINATE DEHYDROGENASE; UBIQUINOL CYTOCHROME C REDUCTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANOXIA; ARTICLE; CALORIC RESTRICTION; CELL FUNCTION; CELL HYPOXIA; CONTROLLED STUDY; DRUG EFFECT; ENZYME ACTIVITY; HEART MUSCLE ISCHEMIA; HEART PROTECTION; LOW DRUG DOSE; MALE; MITOCHONDRIAL PERMEABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REOXYGENATION; RESPIRATORY CHAIN; WESTERN BLOTTING;

ACETYLATION; ANIMALS; ANTIOXIDANTS; BLOTTING, WESTERN; CALORIC RESTRICTION; CELLS, CULTURED; DISEASE MODELS, ANIMAL; ELECTRON TRANSPORT CHAIN COMPLEX PROTEINS; ELECTRON TRANSPORT COMPLEX III; HUMANS; HYDROGEN PEROXIDE; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; MYOCYTES, CARDIAC; NAD; NADH DEHYDROGENASE; NIACINAMIDE; OXIDATIVE STRESS; PROTEOMICS; RATS; RATS, INBRED F344; SIRTUINS; STILBENES;

EID: 80051802678     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.243097     Document Type: Article

References (51)

1. Lakatta EG, Levy D. Arterial and cardiac aging: major shareholders in cardiovascular disease enterprises, part II: the aging heart in health: links to heart disease. Circulation. 2003;107:346-354. (Pubitemid 36135235)
2. Boersma E, Pieper KS, Steyerberg EW, Wilcox RG, Chang WC, Lee KL, Akkerhuis KM, Harrington RA, Deckers JW, Armstrong PW, Lincoff AM, Califf RM, Topol EJ, Simoons ML. Predictors of outcome in patients with acute coronary syndromes without persistent ST-segment elevation: results from an international trial of 9461 patients: the PURSUIT Investigators. Circulation. 2000;101:2557-2567. (Pubitemid 30350632)
3. Maggioni AP, Maseri A, Fresco C, Franzosi MG, Mauri F, Santoro E, Tognoni G. Age-related increase in mortality among patients with first myocardial infarctions treated with thrombolysis: the Investigators of the Gruppo Italiano per lo Studio della Sopravvivenza nell'Infarto Miocardico (GISSI-2). N Engl J Med. 1993;329:1442-1448.
4. 2+, pHi, and contractility during ischemia and reperfusion. Circulation. 1992;86:II371-II376.
5. Lesnefsky EJ, Gallo DS, Ye J, Whittingham TS, Lust WD. Aging increases ischemia-reperfusion injury in the isolated, buffer-perfused heart. J Lab Clin Med. 1994;124:843-851.
6. Shinmura K, Tamaki K, Bolli R. Short-term caloric restriction improves ischemic tolerance independent of opening of ATP-sensitive K + channels in both young and aged hearts. J Mol Cell Cardiol. 2005;39:285-296. (Pubitemid 40995018)
7. Masoro EJ. Overview of caloric restriction and ageing. Mech Ageing Dev. 2005;126:913-922. (Pubitemid 41033171)
8. Sohal RS, Weindruch R. Oxidative stress, caloric restriction, and aging. Science. 1996;273:59-63. (Pubitemid 26255420)
9. Ungvari Z, Parrado-Fernandez C, Csiszar A, de Cabo R. Mechanisms underlying caloric restriction and lifespan regulation: implications for vascular aging. Circ Res. 2008;102:519-528.
10. Colman RJ, Anderson RM, Johnson SC, Kastman EK, Kosmatka KJ, Beasley TM, Allison DB, Cruzen C, Simmons HA, Kemnitz JW, Weindruch R. Caloric restriction delays disease onset and mortality in rhesus monkeys. Science. 2009;325:201-204.
11. Merry BJ. Oxidative stress and mitochondrial function with aging: the effects of calorie restriction. Aging Cell. 2004;3:7-12. (Pubitemid 40246655)
12. Shinmura K, Tamaki K, Bolli R. Impact of 6-mo caloric restriction on myocardial ischemic tolerance: possible involvement of nitric oxidedependent increase in nuclear Sirt1. Am J Physiol Heart Circ Physiol. 2008;295:H2348- H2355.
13. Shinmura K, Tamaki K, Saito K, Nakano Y, Tobe T, Bolli R. Cardioprotective effects of short-term caloric restriction are mediated by adiponectin via activation of AMP-activated protein kinase. Circulation. 2007;116:2809-2817. (Pubitemid 350291223)
14. Bao J, Sack MN. Protein deacetylation by sirtuins: delineating a posttranslational regulatory program responsive to nutrient and redox stressors. Cell Mol Life Sci. 2010;67:3073-3087.
15. Donmez G, Guarente L. Aging and disease: connections to sirtuins. Aging Cell. 2010;9:285-290.
16. Haigis MC, Sinclair DA. Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol. 2010;5:253-295.
17. Chen Q, Camara AK, Stowe DF, Hoppel CL, Lesnefsky EJ. Modulation of electron transport protects cardiac mitochondria and decreases myocardial injury during ischemia and reperfusion. Am J Physiol Cell Physiol. 2007;292:C137-C147. (Pubitemid 46115127)
18. Di Lisa F, Canton M, Menabo R, Kaludercic N, Bernardi P. Mitochondria and cardioprotection. Heart Fail Rev. 2007;12:249-260. (Pubitemid 350176698)
19. Heusch G, Boengler K, Schulz R. Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation. 2008;118:1915-1919.
20. Wong R, Aponte AM, Steenbergen C, Murphy E. Cardioprotection leads to novel changes in the mitochondrial proteome. Am J Physiol Heart Circ Physiol. 2010;298:H75-H91.
21. Bevilacqua L, Ramsey JJ, Hagopian K, Weindruch R, Harper ME. Long-term caloric restriction increases UCP3 content but decreases proton leak and reactive oxygen species production in rat skeletal muscle mitochondria. Am J Physiol Endocrinol Metab. 2005;289:E429-E438. (Pubitemid 41192698)
22. Colom B, Oliver J, Roca P, Garcia-Palmer FJ. Caloric restriction and gender modulate cardiac muscle mitochondrial H2O2 production and oxidative damage. Cardiovasc Res. 2007;74:456-465. (Pubitemid 46693701)
23. Gredilla R, Sanz A, Lopez-Torres M, Barja G. Caloric restriction decreases mitochondrial free radical generation at complex I and lowers oxidative damage to mitochondrial DNA in the rat heart. FASEB J. 2001;15:1589-1591.
24. Niemann B, Chen Y, Issa H, Silber RE, Rohrbach S. Caloric restriction delays cardiac ageing in rats: role of mitochondria. Cardiovasc Res. 2010;88:267-276.
25. Guarente L. Mitochondria: a nexus for aging, calorie restriction, and sirtuins? Cell. 2008;132:171-176. (Pubitemid 351172441)
26. Chang J, Cornell JE, Van Remmen H, Hakala K, Ward WF, Richardson A. Effect of aging and caloric restriction on the mitochondrial proteome. J Gerontol A Biol Sci Med Sci. 2007;62:223-234. (Pubitemid 47065719)
27. Shinmura K, Tamaki K, Sano M, Murata M, Yamakawa H, Ishida H, Fukuda K. Impact of long-term caloric restriction on cardiac senescence: caloric restriction ameliorates cardiac diastolic dysfunction associated with aging. J Mol Cell Cardiol. 2011;50:117-127.
28. Pillai VB, Sundaresan NR, Jeevanandam V, Gupta MP. Mitochondrial SIRT3 and heart disease. Cardiovasc Res. 2010;88:250-256.
29. Bolli R, Marban E. Molecular and cellular mechanisms of myocardial stunning. Physiol Rev. 1999;79:609-634. (Pubitemid 29210931)
30. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135.
31. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem. 2003;278:36027-36031. (Pubitemid 37139922)
32. Paradies G, Petrosillo G, Pistolese M, Ruggiero FM. Reactive oxygen species affect mitochondrial electron transport complex I activity through oxidative cardiolipin damage. Gene. 2002;286:135-141. (Pubitemid 34273870)
33. Petrosillo G, Ruggiero FM, Di Venosa N, Paradies G. Decreased complex III activity in mitochondria isolated from rat heart subjected to ischemia and reperfusion: role of reactive oxygen species and cardiolipin. FASEB J. 2003;17:714-716.
34. Tompkins AJ, Burwell LS, Digerness SB, Zaragoza C, Holman WL, Brookes PS. Mitochondrial dysfunction in cardiac ischemia-reperfusion injury: ROS from complex I, without inhibition. Biochim Biophys Acta. 2006;1762:223-231. (Pubitemid 43006028)
35. 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, Auwerx J. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127:1109-1122. (Pubitemid 44894520)
36. Nisoli E, Tonello C, Cardile A, Cozzi V, Bracale R, Tedesco L, Falcone S, Valerio A, Cantoni O, Clementi E, Moncada S, Carruba MO. Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science. 2005;310:314-317. (Pubitemid 41457197)
37. Tanno M, Kuno A, Yano T, Miura T, Hisahara S, Ishikawa S, Shimamoto K, Horio Y. Induction of manganese superoxide dismutase by nuclear translocation and activation of SIRT1 promotes cell survival in chronic heart failure. J Biol Chem. 2010;285:8375-8382.
38. Huang JY, Hirschey MD, Shimazu T, Ho L, Verdin E. Mitochondrial sirtuins. Biochim Biophys Acta. 2010;1804:1645-1651.
39. Broderick TL, Belke T, Driedzic WR. Effects of chronic caloric restriction on mitochondrial respiration in the ischemic reperfused rat heart. Mol Cell Biochem. 2002;233:119-125. (Pubitemid 34746117)
40. Heusch G, Boengler K, Schulz R. Inhibition of mitochondrial permeability transition pore opening: the Holy Grail of cardioprotection. Basic Res Cardiol. 2010;105:151-154.
41. Drew B, Phaneuf S, Dirks A, Selman C, Gredilla R, Lezza A, Barja G, Leeuwenburgh C. Effects of aging and caloric restriction on mitochondrial energy production in gastrocnemius muscle and heart. Am J Physiol Regul Integr Comp Physiol. 2003;284:R474-R480. (Pubitemid 36120164)
42. Lambert AJ, Wang B, Yardley J, Edwards J, Merry BJ. The effect of aging and caloric restriction on mitochondrial protein density and oxygen consumption. Exp Gerontol. 2004;39:289-295. (Pubitemid 38264359)
43. Iuso A, Scacco S, Piccoli C, Bellomo F, Petruzzella V, Trentadue R, Minuto M, Ripoli M, Capitanio N, Zeviani M, Papa S. Dysfunctions of cellular oxidative metabolism in patients with mutations in the NDUFS1 and NDUFS4 genes of complex I. J Biol Chem. 2006;281:10374-10380. (Pubitemid 43864576)
44. Liu B, Tewari AK, Zhang L, Green-Church KB, Zweier JL, Chen YR, He G. Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: mitochondria as the major target. Biochim Biophys Acta. 2009;1794:476-485.
45. Sundaresan NR, Gupta M, Kim G, Rajamohan SB, Isbatan A, Gupta MP. Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3adependent antioxidant defense mechanisms in mice. J Clin Invest. 2009;119:2758-2771.
46. Marfe G, Tafani M, Indelicato M, Sinibaldi-Salimei P, Reali V, Pucci B, Fini M, Russo MA. Kaempferol induces apoptosis in two different cell lines via Akt inactivation, Bax and SIRT3 activation, and mitochondrial dysfunction. J Cell Biochem. 2009;106:643-650.
47. Boengler K, Buechert A, Heinen Y, Roeskes C, Hilfiker-Kleiner D, Heusch G, Schulz R. Cardioprotection by ischemic postconditioning is lost in aged and STAT3-deficient mice. Circ Res. 2008;102:131-135.
48. Boengler K, Konietzka I, Buechert A, Heinen Y, Garcia-Dorado D, Heusch G, Schulz R. Loss of ischemic preconditioning's cardioprotection in aged mouse hearts is associated with reduced gap junctional and mitochondrial levels of connexin 43. Am J Physiol Heart Circ Physiol. 2007;292:H1764-H1769. (Pubitemid 46572399)
49. Boengler K, Schulz R, Heusch G. Loss of cardioprotection with ageing. Cardiovasc Res. 2009;83:247-261.
50. Riva A, Tandler B, Loffredo F, Vazquez E, Hoppel C. Structural differences in two biochemically defined populations of cardiac mitochondria. Am J Physiol Heart Circ Physiol. 2005;289:H868-H872. (Pubitemid 41129405)
51. Boengler K, Stahlhofen S, van de Sand A, Gres P, Ruiz-Meana M, Garcia-Dorado D, Heusch G, Schulz R. Presence of connexin 43 in subsarcolemmal, but not in interfibrillar cardiomyocyte mitochondria. Basic Res Cardiol. 2009;104:141-147.