Defective DNA replication impairs mitochondrial biogenesis in human failing hearts

Circulation Research

Volumn 106, Issue 9, 2010, Pages 1541-1548

  Karamanlidis, Georgios ^a,c   Nascimben, Luigino ^a   Couper, Gregory S ^a   Shekar, Prem S ^a   Del Monte, Federica ^b   Tian, Rong ^a,c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Human heart failure; Mitochondrial biogenesis; MtDNA; Oxidative damage; PGC 1

Indexed keywords

BETA ADRENERGIC RECEPTOR BLOCKING AGENT; CATECHOLAMINE; CITRATE SYNTHASE; DIGOXIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ESTROGEN RELATED RECEPTOR ALPHA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; MESSENGER RNA; MITOCHONDRIAL DNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1 RELATED COACTIVATOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1BETA; PHOSPHODIESTERASE INHIBITOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ADULT; AGED; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; DOWN REGULATION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION; HEART FAILURE; HEART MITOCHONDRION; HUMAN; HUMAN TISSUE; MALE; MITOCHONDRIAL DNA DEPLETION; OXIDATIVE STRESS; PRIORITY JOURNAL;

ADULT; AGED; DNA REPLICATION; DNA, MITOCHONDRIAL; DOWN-REGULATION; FEMALE; HEART FAILURE; HEAT-SHOCK PROTEINS; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIA; TRANSCRIPTION FACTORS; YOUNG ADULT;

EID: 77952428203     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.212753     Document Type: Article

References (36)

1. Nakayama H, Chen X, Baines CP, Klevitsky R, Zhang X, Zhang H, Jaleel N, Chua BH, Hewett TE, Robbins J, Houser SR, Molkentin JD. Ca2 +-and mitochondrial-dependent cardiomyocyte necrosis as a primary mediator of heart failure. J Clin Invest. 2007;117:2431-2444.
2. Marin-Garcia J, Goldenthal MJ. Mitochondrial centrality in heart failure. Heart Fail Rev. 2008;13:137-150.
3. Uldry M, Yang W, St-Pierre J, Lin J, Seale P, Spiegelman BM. Complementary action of the PGC-1 coactivators in mitochondrial biogenesis and brown fat differentiation. Cell Metab. 2006;3:333-341.
4. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 1999;98:115-124.
5. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. A cold-inducible coactivator of nuclear receptors linked to adaptive ther-mogenesis. Cell. 1998;92:829-839.
6. Arany Z, Novikov M, Chin S, Ma Y, Rosenzweig A, Spiegelman BM. Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci USA. 2006;103:10086-10091.
7. Garnier A, Fortin D, Delomenie C, Momken I, Veksler V, Ventura-Clapier R. Depressed mitochondrial transcription factors and oxidative capacity in rat failing cardiac and skeletal muscles. J Physiol. 2003;551:491-501.
8. Arany Z, He H, Lin J, Hoyer K, Handschin C, Toka O, Ahmad F, Matsui T, Chin S, Wu PH, Rybkin II, Shelton JM, Manieri M, Cinti S, Schoen FJ, Bassel-Duby R, Rosenzweig A, Ingwall JS, Spiegelman BM. Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 2005;1:259-271.
9. Lai L, Leone TC, Zechner C, Schaeffer PJ, Kelly SM, Flanagan DP, Medeiros DM, Kovacs A, Kelly DP. Transcriptional coactivators PGC-1alpha and PGC-lbeta control overlapping programs required for perinatal maturation of the heart. Genes Dev. 2008;22:1948-1961.
10. Morgunov I, Srere PA. Interaction between citrate synthase and malate dehydrogenase. Substrate channeling of oxaloacetate. J Biol Chem. 1998; 273:29540-29544.
11. Brown TA, Clayton DA. Release of replication termination controls mitochondrial DNA copy number after depletion with 2',3'-dideoxycytidine. Nucleic Acids Res. 2002;30:2004-2010.
12. Gensler S, Weber K, Schmitt WE, Perez-Martos A, Enriquez JA, Montoya J, Wiesner RJ. Mechanism of mammalian mitochondrial DNA replication: import of mitochondrial transcription factor A into isolated mitochondria stimulates 7S DNA synthesis. Nucleic Acids Res. 2001;29:3657-3663.
13. Kriukiene E. Domain organization and metal ion requirement of the Type IIS restriction endonuclease MnlI. FEBS Lett. 2006;580:6115-6122.
14. Lee DY, Clayton DA. Properties of a primer RNA-DNA hybrid at the mouse mitochondrial DNA leading-strand origin of replication. J Biol Chem. 1996;271:24262-24269.
15. Tsutsui H, Ide T, Kinugawa S. Mitochondrial oxidative stress, DNA damage, and heart failure. Antioxid Redox Signal. 2006;8:1737-1744. (Pubitemid 44726346)
16. Tsutsui H, Ide T, Shiomi T, Kang D, Hayashidani S, Suematsu N, Wen J, Utsumi H, Hamasaki N, Takeshita A. 8-oxo-dGTPase, which prevents oxidative stress-induced DNA damage, increases in the mitochondria from failing hearts. Circulation. 2001;104:2883-2885.
17. Schriner SE, Linford NJ, Martin GM, Treuting P, Ogburn CE, Emond M, Coskun PE, Ladiges W, Wolf N, Van Remmen H, Wallace DC, Rabin-ovitch PS. Extension of murine life span by overexpression of catalase targeted to mitochondria. Science. 2005;308:1909-1911.
18. Finck BN, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 (PGC-1) regulatory cascade in cardiac physiology and disease. Circulation. 2007;115:2540-2548.
19. Ide T, Tsutsui H, Hayashidani S, Kang D, Suematsu N, Nakamura K, Utsumi H, Hamasaki N, Takeshita A. Mitochondrial DNA damage and dysfunction associated with oxidative stress in failing hearts after myocardial infarction. Circ Res. 2001;88:529-535.
20. L'Ecuyer T, Sanjeev S, Thomas R, Novak R, Das L, Campbell W, Heide RV. DNA damage is an early event in doxorubicin-induced cardiac myocyte death. Am J Physiol Heart Circ Physiol. 2006;291: H1273-H1280.
21. Lewis W. Defective mitochondrial DNA replication and NRTIs: pathophysiological implications in AIDS cardiomyopathy. Am J Physiol Heart Circ Physiol. 2003;284:H1-H9.
22. Wang J, Wilhelmsson H, Graff C, Li H, Oldfors A, Rustin P, Bruning JC, Kahn CR, Clayton DA, Barsh GS, Thoren P, Larsson NG. Dilated cardiomyopathy and atrioventricular conduction blocks induced by heart-specific inactivation of mitochondrial DNA gene expression. Nat Genet. 1999;21:133-137.
23. Li H, Wang J, Wilhelmsson H, Hansson A, Thoren P, Duffy J, Rustin P, Larsson NG. Genetic modification of survival in tissue-specific knockout mice with mitochondrial cardiomyopathy. Proc Natl Acad Sci USA. 2000;97:3467-3472.
24. DiMauro S, Schon EA. Mitochondrial respiratory-chain diseases. N Engl J Med. 2003;348:2656-2668.
25. Lebrecht D, Walker UA. Role of mtDNA lesions in anthracycline car-diotoxicity. Cardiovasc Toxicol. 2007;7:108-113.
26. Ikeuchi M, Matsusaka H, Kang D, Matsushima S, Ide T, Kubota T, Fujiwara T, Hamasaki N, Takeshita A, Sunagawa K, Tsutsui H. Overex-pression of mitochondrial transcription factor a ameliorates mitochondrial deficiencies and cardiac failure after myocardial infarction. Circulation. 2005;112:683-690.
27. Williams MD, Van Remmen H, Conrad CC, Huang TT, Epstein CJ, Richardson A. Increased oxidative damage is correlated to altered mito-chondrial function in heterozygous manganese superoxide dismutase knockout mice. J Biol Chem. 1998;273:28510-28515.
28. Matsushima S, Ide T, Yamato M, Matsusaka H, Hattori F, Ikeuchi M, Kubota T, Sunagawa K, Hasegawa Y, Kurihara T, Oikawa S, Kinugawa S, Tsutsui H. Overexpression of mitochondrial peroxiredoxin-3 prevents left ventricular remodeling and failure after myocardial infarction in mice. Circulation. 2006;113:1779-1786. (Pubitemid 43958471)
29. Ventura-Clapier R, Garnier A, Veksler V. Transcriptional control of mitochondrial biogenesis: the central role of PGC-1alpha. Cardiovasc Res. 2008;79:208-217.
30. Sebastiani M, Giordano C, Nediani C, Travaglini C, Borchi E, Zani M, Feccia M, Mancini M, Petrozza V, Cossarizza A, Gallo P, Taylor RW, d'Amati G. Induction of mitochondrial biogenesis is a maladaptive mechanism in mito-chondrial cardiomyopathies. J Am Coll Cardiol. 2007;50:1362-1369.
31. Garnier A, Zoll J, Fortin D, N'Guessan B, Lefebvre F, Geny B, Mettauer B, Veksler V, Ventura-Clapier R. Control by circulating factors of mito-chondrial function and transcription cascade in heart failure: a role for endothelin-1 and angiotensin II. Circ Heart Fail. 2009;2:342-350.
32. Anderson R, Prolla T. PGC-1alpha in aging and anti-aging interventions. Biochim Biophys Acta. 2009;1790:1059-1066.
33. Ling C, Poulsen P, Carlsson E, Ridderstrale M, Almgren P, Wojtaszewski J, Beck-Nielsen H, Groop L, Vaag A. Multiple environmental and genetic factors influence skeletal muscle PGC-1alpha and PGC-1beta gene expression in twins. J Clin Invest. 2004;114:1518-1526.
34. Sihag S, Cresci S, Li AY, Sucharov CC, Lehman JJ. PGC-1alpha and ERRalpha target gene downregulation is a signature of the failing human heart. J Mol Cell Cardiol. 2009;46:201-212.
35. Lehman JJ, Barger PM, Kovacs A, Saffitz JE, Medeiros DM, Kelly DP. Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J Clin Invest. 2000;106:847-856.
36. Russell LK, Mansfield CM, Lehman JJ, Kovacs A, Courtois M, Saffitz JE, Medeiros DM, Valencik ML, McDonald JA, Kelly DP. Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mito-chondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res. 2004;94:525-533.