Maintaining PGC-1α expression following pressure overload-induced cardiac hypertrophy preserves angiogenesis but not contractile or mitochondrial function

FASEB Journal

Volumn 28, Issue 8, 2014, Pages 3691-3702

  Pereira, Renata O ^a,b   Wende, Adam R ^b,d   Crum, Ashley ^b   Hunter, Douglas ^b   Olsen, Curtis D ^b   Rawlings, Tenley ^b   Riehle, Christian ^a,b   Ward, Walter F ^c   Abel, E Dale ^a,b  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

Heart failure; Mitochondria

Indexed keywords

ADENOSINE TRIPHOSPHATE; CATALASE; ENDOTHELIN 1; GLUTATHIONE PEROXIDASE 1; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MANGANESE SUPEROXIDE DISMUTASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PROTEIN KINASE B; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA CONSTRICTION; APOPTOSIS; ARTICLE; BACTERIAL ARTIFICIAL CHROMOSOME; BIOSYNTHESIS; CAPILLARY DENSITY; CELL FUNCTION; CONTROLLED STUDY; FATTY ACID OXIDATION; HEART EJECTION FRACTION; HEART LEFT VENTRICLE PRESSURE; HEART MITOCHONDRION; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART PROTECTION; HEART VENTRICLE CONTRACTION; HEART VENTRICLE ENDDIASTOLIC PRESSURE; HEART VENTRICLE FUNCTION; HEART VENTRICLE HYPERTROPHY; HEART VENTRICLE OVERLOAD; HUMAN; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PHYSIOLOGICAL PROCESS; PRESSURE OVERLOAD HYPERTROPHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRANSVERSE AORTIC CONSTRICTION; VASCULARIZATION;

HEART FAILURE; MITOCHONDRIA;

ADENOSINE TRIPHOSPHATE; ANIMALS; AORTA; APOPTOSIS; CAPILLARIES; CARDIOMEGALY; CONSTRICTION; FIBROSIS; HUMANS; HYPERTENSION; MICE; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, TRANSGENIC; MITOCHONDRIA, HEART; MYOCARDIAL CONTRACTION; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATION-REDUCTION; OXIDATIVE PHOSPHORYLATION; PALMITATES; RECOMBINANT PROTEINS; RNA, MESSENGER; STROKE VOLUME; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR REMODELING;

EID: 84905235632     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-253823     Document Type: Article

References (28)

1. Rimbaud, S., Garnier, A., and Ventura-Clapier, R. (2009) Mitochondrial biogenesis in cardiac pathophysiology. Pharmacol. Rep. 61, 131-138
2. Huss, J. M., and Kelly, D. P. (2005) Mitochondrial energy metabolism in heart failure: a question of balance. J. Clin. Invest. 115, 547-555 (Pubitemid 40322224)
3. Huss, J. M., Torra, I. P., Staels, B., Giguere, V., and Kelly, D. P. (2004) Estrogen-related receptor alpha directs peroxisome proliferator-activated receptor alpha signaling in the transcriptional control of energy metabolism in cardiac and skeletal muscle. Mol. Cell. Biol. 24, 9079-9091 (Pubitemid 39313912)
4. Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., and Kelly, D. P. (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106, 847-856
5. Abel, E. D., and Doenst, T. (2011) Mitochondrial adaptations to physiological vs. pathological cardiac hypertrophy. Cardiovasc. Res. 90, 234-242
6. Arany, Z., Novikov, M., Chin, S., Ma, Y., Rosenzweig, A., and Spiegelman, B. M. (2006) Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc. Natl. Acad. Sci. U. S. A. 103, 10086-10091 (Pubitemid 43993627)
7. Riehle, C., Wende, A. R., Zaha, V. G., Pires, K. M., Wayment, B., Olsen, C., Bugger, H., Buchanan, J., Wang, X., Moreira, A. B., Doenst, T., Medina-Gomez, G., Litwin, S. E., Lelliott, C. J., Vidal-Puig, A., and Abel, E. D. (2011) PGC-1beta deficiency accelerates the transition to heart failure in pressure overload hypertrophy. Circ. Res 109, 783-793
8. Huss, J. M., Imahashi, K., Dufour, C. R., Weinheimer, C. J., Courtois, M., Kovacs, A., Giguere, V., Murphy, E., and Kelly, D. P. (2007) The nuclear receptor ERRalpha is required for the bioenergetic and functional adaptation to cardiac pressure overload. Cell Metab. 6, 25-37 (Pubitemid 46995780)
9. Riehle, C., and Abel, E. D. (2012) PGC-1 proteins and heart failure. Trends Cardiovasc. Med. 22, 98-105
10. Arany, Z., He, H., Lin, J., Hoyer, K., Handschin, C., Toka, O., Ahmad, F., Matsui, T., Chin, S., Wu, P. H., Rybkin, I. I., Shelton, J. M., Manieri, M., Cinti, S., Schoen, F. J., Bassel-Duby, R., Rosenzweig, A., Ingwall, J. S., and Spiegelman, B. M. (2005) Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab. 1, 259-271 (Pubitemid 43960608)
11. Lehman, J. J., Boudina, S., Banke, N. H., Sambandam, N., Han, X., Young, D. M., Leone, T. C., Gross, R. W., Lewandowski, E. D., Abel, E. D., and Kelly, D. P. (2008) The transcriptional coactivator PGC-1alpha is essential for maximal and efficient cardiac mitochondrial fatty acid oxidation and lipid homeostasis. Am. J. Physiol. Heart Circ. Physiol. 295, H185-196
12. Leone, T. C., Lehman, J. J., Finck, B. N., Schaeffer, P. J., Wende, A. R., Boudina, S., Courtois, M., Wozniak, D. F., Sambandam, N., Bernal-Mizrachi, C., Chen, Z., Holloszy, J. O., Medeiros, D. M., Schmidt, R. E., Saffitz, J. E., Abel, E. D., Semenkovich, C. F., and Kelly, D. P. (2005) PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol. 3, e101
13. Liang, H., Balas, B., Tantiwong, P., Dube, J., Goodpaster, B. H., O'Doherty, R. M., DeFronzo, R. A., Richardson, A., Musi, N., and Ward, W. F. (2009) Whole body overexpression of PGC-1alpha has opposite effects on hepatic and muscle insulin sensitivity. Am. J. Physiol. Endocrinol. Metab. 296, E945-954
14. Boudina, S., Sena, S., O'Neill, B. T., Tathireddy, P., Young, M. E., and Abel, E. D. (2005) Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112, 2686-2695 (Pubitemid 41532606)
15. Boudina, S., Sena, S., Theobald, H., Sheng, X., Wright, J. J., Hu, X. X., Aziz, S., Johnson, J. I., Bugger, H., Zaha, V. G., and Abel, E. D. (2007) Mitochondrial energetics in the heart in obesity-related diabetes: direct evidence for increased uncoupled respiration and activation of uncoupling proteins. Diabetes 56, 2457-2466 (Pubitemid 47523253)
16. Riehle, C., Wende, A. R., Sena, S., Pires, K. M., Pereira, R. O., Zhu, Y., Bugger, H., Frank, D., Bevins, J., Chen, D., Perry, C. N., Dong, X. C., Valdez, S., Rech, M., Sheng, X., Weimer, B. C., Gottlieb, R. A., White, M. F., and Abel, E. D. (2013) Insulin receptor substrate signaling suppresses neonatal autophagy in the heart. J. Clin. Invest. 123, 5319-5333
17. Mazumder, P. K., O'Neill, B. T., Roberts, M. W., Buchanan, J., Yun, U. J., Cooksey, R. C., Boudina, S., and Abel, E. D. (2004) Impaired cardiac efficiency and increased fatty acid oxidation in insulin-resistant ob/ob mouse hearts. Diabetes 53, 2366-2374 (Pubitemid 39145591)
18. Pereira, R. O., Wende, A. R., Olsen, C., Soto, J., Rawlings, T., Zhu, Y., Anderson, S. M., and Abel, E. D. (2013) Inducible overexpression of GLUT1 prevents mitochondrial dysfunction and attenuates structural remodeling in pressure overload but does not prevent left ventricular dysfunction. J. Am. Heart Assoc. 2, e000301
19. Sena, S., Rasmussen, I. R., Wende, A. R., McQueen, A. P., Theobald, H. A., Wilde, N., Pereira, R. O., Litwin, S. E., Berger, J. P., and Abel, E. D. (2007) Cardiac hypertrophy caused by peroxisome proliferator- activated receptor-gamma agonist treatment occurs independently of changes in myocardial insulin signaling. Endocrinology 148, 6047-6053 (Pubitemid 350146163)
20. Gundersen, H. J., and Osterby, R. (1977) Glomerular size and structure in diabetes mellitus. II. Late abnormalities. Diabetologia 13, 43-48 (Pubitemid 8032037)
21. Arany, Z., Foo, S. Y., Ma, Y., Ruas, J. L., Bommi-Reddy, A., Girnun, G., Cooper, M., Laznik, D., Chinsomboon, J., Rangwala, S. M., Baek, K. H., Rosenzweig, A., and Spiegelman, B. M. (2008) HIF-independent regulation of VEGF and angiogenesis by the transcriptional coactivator PGC-1alpha. Nature 451, 1008-1012 (Pubitemid 351301733)
22. Mettauer, B., Zoll, J., Garnier, A., and Ventura-Clapier, R. (2006) Heart failure: a model of cardiac and skeletal muscle energetic failure. Pflügers Archiv. 452, 653-666 (Pubitemid 44337900)
23. Hu, X., Xu, X., Huang, Y., Fassett, J., Flagg, T. P., Zhang, Y., Nichols, C. G., Bache, R. J., and Chen, Y. (2008) Disruption of sarcolemmal ATP-sensitive potassium channel activity impairs the cardiac response to systolic overload. Circ. Res. 103, 1009-1017
24. Hu, X., Xu, X., Lu, Z., Zhang, P., Fassett, J., Zhang, Y., Xin, Y., Hall, J. L., Viollet, B., Bache, R. J., Huang, Y., and Chen, Y. (2011) AMP activated protein kinase-alpha2 regulates expression of estrogen-related receptor-alpha, a metabolic transcription factor related to heart failure development. Hypertension 58, 696-703
25. Karamanlidis, G., Nascimben, L., Couper, G. S., Shekar, P. S., del Monte, F., and Tian, R. (2010) Defective DNA replication impairs mitochondrial biogenesis in human failing hearts. Circ. Res. 106, 1541-1548
26. Patten, I. S., and Arany, Z. (2012) PGC-1 coactivators in the cardiovascular system. Trends Endocrinol. Metab. 23, 90-97
27. Lu, Z., Xu, X., Hu, X., Fassett, J., Zhu, G., Tao, Y., Li, J., Huang, Y., Zhang, P., Zhao, B., and Chen, Y. (2010) PGC-1 alpha regulates expression of myocardial mitochondrial antioxidants and myocardial oxidative stress after chronic systolic overload. Antioxid. Redox Signal. 13, 1011-1022
28. Patten, I. S., Rana, S., Shahul, S., Rowe, G. C., Jang, C., Liu, L., Hacker, M. R., Rhee, J. S., Mitchell, J., Mahmood, F., Hess, P., Farrell, C., Koulisis, N., Khankin, E. V., Burke, S. D., Tudorache, I., Bauersachs, J., del Monte, F., Hilfiker-Kleiner, D., Karumanchi, S. A., and Arany, Z. (2012) Cardiac angiogenic imbalance leads to peripartum cardiomyopathy. Nature 485, 333-338