Opposite effects of statins on mitochondria of cardiac and skeletal muscles: A 'mitohormesis' mechanism involving reactive oxygen species and PGC-1

European Heart Journal

Volumn 33, Issue 11, 2012, Pages 1397-1407

  Bouitbir, Jamal ^a,b   Charles, Anne Laure ^a,b   Echaniz Laguna, Andoni ^b   Kindo, Michel ^a,b   Daussin, Frédéric ^a,b   Auwerx, Johan ^c   Piquard, François ^a,b   Geny, Bernard ^a,b   Zoll, Joffrey ^a,b  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b HÔPITAL CIVIL   (France)

^c EPFL   (Switzerland)

Author keywords

Heart; Mitochondrial biogenesis; Mitohormesis; ROS; Statin

Indexed keywords

ATORVASTATIN; CHOLESTEROL; CYTOCHROME C OXIDASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MESSENGER RNA; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; QUERCETIN; REACTIVE OXYGEN METABOLITE; SCAVENGER; SUPEROXIDE DISMUTASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CELL CULTURE; CELL FUNCTION; CELLULAR STRESS RESPONSE; CHOLESTEROL BLOOD LEVEL; COMPARATIVE STUDY; CONTROLLED STUDY; DRUG EFFECT; GENE EXPRESSION; HEART MITOCHONDRION; HEART MUSCLE; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MITOHORMESIS; MUSCLE BIOPSY; MUSCLE MITOCHONDRION; MUSCLE WEAKNESS; MYOPATHY; NONHUMAN; OUTCOME ASSESSMENT; OXIDATIVE STRESS; PRIORITY JOURNAL; RHABDOMYOLYSIS; SIGNAL TRANSDUCTION; SKELETAL MUSCLE; TREATMENT DURATION; TREATMENT RESPONSE; WISTAR RAT;

ANIMALS; ANTIOXIDANTS; HEART ATRIA; HEPTANOIC ACIDS; HUMANS; HYDROXYMETHYLGLUTARYL-COA REDUCTASE INHIBITORS; MALE; MITOCHONDRIA, HEART; MITOCHONDRIA, MUSCLE; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; MYOCYTES, CARDIAC; PYRROLES; QUERCETIN; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; RNA, MESSENGER; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS;

EID: 84856108187     PISSN: 0195668X     EISSN: 15229645     Source Type: Journal    
DOI: 10.1093/eurheartj/ehr224     Document Type: Article

References (29)

1. Staffa JA, Chang J, Green L. Cerivastatin and reports of fatal rhabdomyolysis. N Engl J Med 2002;346:539-540.
2. Jasinska M, Owczarek J, Orszulak-Michalak D. Statins: a new insight into their mechanisms of action and consequent pleiotropic effects. Pharmacol Rep 2007; 59:483-499.
3. Giordano N, Senesi M, Mattii G, Battisti E, Villanova M, Gennari C. Polymyositis associated with simvastatin. Lancet 1997;349:1600-1601. (Pubitemid 27229143)
4. Bonetti PO, Lerman LO, Napoli C, Lerman A. Statin effects beyond lipid lowering-are they clinically relevant? Eur Heart J 2003;24:225-248. (Pubitemid 36207079)
5. Echaniz-Laguna A, Mohr M, Tranchant C. Neuromuscular symptoms and elevated creatine kinase after statin withdrawal. N Engl J Med 2010;362:564-565.
6. Jones SP, Teshima Y, Akao M, Marban E. Simvastatin attenuates oxidant-induced mitochondrial dysfunction in cardiac myocytes. Circ Res 2003;93:697-699. (Pubitemid 37288663)
7. Sirvent P, Bordenave S, Vermaelen M, Roels B, Vassort G, Mercier J, Raynaud E, Lacampagne A. Simvastatin induces impairment in skeletal muscle while heart is protected. Biochem Biophys Res Commun 2005;338:1426-1434. (Pubitemid 41608410)
8. Sirvent P, Mercier J, Lacampagne A. New insights into mechanisms of statin-associated myotoxicity. Curr Opin Pharmacol 2008;8:333-338.
9. Kaufmann P, Torok M, Zahno A, Waldhauser KM, Brecht K, Krahenbuhl S. Toxicity of statins on rat skeletal muscle mitochondria. Cell Mol Life Sci 2006;63: 2415-2425. (Pubitemid 44653050)
10. Bindoff L. Mitochondria and the heart. Eur Heart J 2003;24:221-224. (Pubitemid 36207078)
11. Brookes PS. Mitochondrial H(+) leak and ROS generation: an odd couple. Free Radic Biol Med 2005;38:12-23. (Pubitemid 39626904)
12. Lecarpentier Y. Physiological role of free radicals in skeletal muscles. J Appl Physiol 2007;103:1917-1918. (Pubitemid 350232371)
13. Sano M, Fukuda K. Activation of mitochondrial biogenesis by hormesis. Circ Res 2008;103:1191-1193.
14. Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008;103:1232-1240.
15. Michelakis ED, Wilkins MR, Rabinovitch M. Emerging concepts and translational priorities in pulmonary arterial hypertension. Circulation 2008;118:1486-1495.
16. Mettauer B, Zoll J, Sanchez H, Lampert E, Ribera F, Veksler V, Bigard X, Mateo P, Epailly E, Lonsdorfer J, Ventura-Clapier R. Oxidative capacity of skeletal muscle in heart failure patients versus sedentary or active control subjects. J Am Coll Cardiol 2001;38:947-954. (Pubitemid 32912693)
17. 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. (Pubitemid 47076618)
18. Seachrist JL, Loi CM, Evans MG, Criswell KA, Rothwell CE. Roles of exercise and pharmacokinetics in cerivastatin-induced skeletal muscle toxicity. Toxicol Sci 2005; 88:551-561. (Pubitemid 41672163)
19. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res 2008;79:208-217. (Pubitemid 351951611)
20. Schulz TJ, Zarse K, Voigt A, Urban N, Birringer M, Ristow M. Glucose restriction extends Caenorhabditis elegans life span by inducing mitochondrial respiration and increasing oxidative stress. Cell Metab 2007;6:280-293. (Pubitemid 47468090)
21. Gems D, Partridge L. Stress-response hormesis and aging: "that which does not kill us makes us stronger". Cell Metab 2008;7:200-203. (Pubitemid 351285527)
22. Seppet E, Eimre M, Peet N, Paju K, Orlova E, Ress M, Kovask S, Piirsoo A, Saks VA, Gellerich FN, Zierz S, Seppet EK. Compartmentation of energy metabolism in atrial myocardium of patients undergoing cardiac surgery. Mol Cell Biochem 2005;270:49-61. (Pubitemid 40425235)
23. Zheng Z, Chen H, Ke G, Fan Y, Zou H, Sun X, Gu Q, Xu X, Ho PC. Protective effect of perindopril on diabetic retinopathy is associated with decreased vascular endothelial growth factor-to-pigment epithelium-derived factor ratio: involvement of a mitochondria-reactive oxygen species pathway. Diabetes 2009;58: 954-964.
24. Wang W, Wong CW. Statins enhance peroxisome proliferator-activated receptor gamma coactivator-1alpha activity to regulate energy metabolism. J Mol Med (Berlin, Germany) 2010;88:309-317.
25. Draeger A, Sanchez-Freire V, Monastyrskaya K, Hoppeler H, Mueller M, Breil F, Mohaupt MG, Babiychuk EB. Statin therapy and the expression of genes that regulate calcium homeostasis and membrane repair in skeletal muscle. Am J Pathol 2010;177:291-299.
26. Lelliott CJ, Medina-Gomez G, Petrovic N, Kis A, Feldmann HM, Bjursell M, Parker N, Curtis K, Campbell M, Hu P, Zhang D, Litwin SE, Zaha VG, Fountain KT, Boudina S, Jimenez-Linan M, Blount M, Lopez M, Meirhaeghe A, Bohlooly YM, Storlien L, Stromstedt M, Snaith M, Oresic M, Abel ED, Cannon B, Vidal-Puig A. Ablation of PGC-1beta results in defective mitochondrial activity, thermogenesis, hepatic function, and cardiac performance. PLoS Biol 2006; 4:e369.
27. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 2006;127:397-408. (Pubitemid 44572377)
28. Davignon J, Jacob RF, Mason RP. The antioxidant effects of statins. Coron Artery Dis 2004;15:251-258. (Pubitemid 39061608)
29. Bors W, Michel C, Saran M. Flavonoid antioxidants: rate constants for reactions with oxygen radicals. Methods Enzymol 1994;234:420-429.