Apelin regulates FoxO3 translocation to mediate cardioprotective responses to myocardial injury and obesity

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Boal, Frederic ^a,b   Roumegoux, Jessica ^a,b   Alfarano, Chiara ^a,b   Timotin, Andrei ^a,b   Calise, Denis ^b,c   Anesia, Rodica ^a,b   Drougard, Anne ^a,b   Knauf, Claude ^a,b   Lagente, Christine ^d   Roncalli, Jerome ^d   Desmoulin, Franck ^a,b   Tronchere, Helene ^a,b   Valet, Philippe ^a,b   Parini, Angelo ^a,b   Kunduzova, Oksana ^a,b  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b University Hospital of Toulouse   (France)

^c Microsurgery Services   (France)

^d TOULOUSE UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOTONIC AGENT; FORKHEAD TRANSCRIPTION FACTOR; PHOSPHATIDYLINOSITOL 3 KINASE; SIGNAL PEPTIDE;

ADIPOCYTE; ADVERSE EFFECTS; AGED; ANIMAL; BLOOD; C57BL MOUSE; CARDIAC MUSCLE; CARDIAC MUSCLE CELL; CELL CULTURE; CROSS-SECTIONAL STUDY; DISEASE MODEL; FEMALE; HEART FAILURE; HEART LEFT VENTRICLE FUNCTION; HUMAN; LIPID DIET; MALE; METABOLISM; MIDDLE AGED; MOUSE; MYOCARDIAL ISCHEMIA REPERFUSION INJURY; OBESITY; PHYSIOLOGY; PROSPECTIVE STUDY; RAT;

ADIPOCYTES; AGED; ANIMALS; CARDIOTONIC AGENTS; CELLS, CULTURED; CROSS-SECTIONAL STUDIES; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; HEART FAILURE; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MYOCARDIAL REPERFUSION INJURY; MYOCARDIUM; MYOCYTES, CARDIAC; OBESITY; PHOSPHATIDYLINOSITOL 3-KINASES; PROSPECTIVE STUDIES; RATS; VENTRICULAR FUNCTION, LEFT;

EID: 84946887778     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep16104     Document Type: Article

References (51)

1. Chase, P.J., Davis, P.G. & Bensimhon, D.R. The obesity paradox in chronic heart failure: what does it mean? Curr Heart Fail Rep 11, 111-117 (2014).
2. Clark, A.L., Fonarow, G.C. & Horwich, T.B. Obesity and the obesity paradox in heart failure. Prog Cardiovasc Dis 56, 409-414 (2014).
3. Diercks, D.B. et al. The obesity paradox in non-ST-segment elevation acute coronary syndromes: results from the Can Rapid risk stratification of Unstable angina patients Suppress ADverse outcomes with Early implementation of the American College of Cardiology/American Heart Association Guidelines Quality Improvement Initiative. Am Heart J 152, 140-148 (2006).
4. Ajith, T.A. & Jayakumar, T.G. Mitochondria-targeted agents: Future perspectives of mitochondrial pharmaceutics in cardiovascular diseases. World J Cardiol 6, 1091-1099 (2014).
5. Marin-Garcia, J., Akhmedov, A.T. & Moe, G.W. Mitochondria in heart failure: the emerging role of mitochondrial dynamics. Heart Fail Rev 18, 439-456 (2013).
6. Andreadou, I., Iliodromitis, E.K., Farmakis, D. & Kremastinos, D.T. To prevent, protect and save the ischemic heart: antioxidants revisited. Expert Opin Ther Targets 13, 945-956 (2009).
7. Tsutsui, H., Kinugawa, S. & Matsushima, S. Oxidative stress and heart failure. Am J Physiol Heart Circ Physiol 301, H2181-2190 (2011).
8. Kalogeris, T., Bao, Y. & Korthuis, R.J. Mitochondrial reactive oxygen species: a double edged sword in ischemia/reperfusion vs preconditioning. Redox Biol 2, 702-714 (2014).
9. Bournat, J.C. & Brown, C.W. Mitochondrial dysfunction in obesity. Curr Opin Endocrinol Diabetes Obes 17, 446-452 (2010).
10. Penna, C., Perrelli, M.G. & Pagliaro, P. Mitochondrial pathways, permeability transition pore, and redox signaling in cardioprotection: therapeutic implications. Antioxid Redox Signal 18, 556-599 (2013).
11. Evans-Anderson, H.J., Alfieri, C.M. & Yutzey, K.E. Regulation of cardiomyocyte proliferation and myocardial growth during development by FOXO transcription factors. Circ Res 102, 686-694 (2008).
12. Sengupta, A., Molkentin, J.D., Paik, J.H., DePinho, R.A. & Yutzey, K.E. FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J Biol Chem 286, 7468-7478 (2011).
13. Zhang, S. et al. FoxO3a modulates hypoxia stress induced oxidative stress and apoptosis in cardiac microvascular endothelial cells. PLoS One 8, e80342 (2013).
14. Lu, D. et al. Transcription factor Foxo3a prevents apoptosis by regulating calcium through the apoptosis repressor with caspase recruitment domain. J Biol Chem 288, 8491-8504 (2013).
15. Ferrara, N. et al. Exercise training promotes SIRT1 activity in aged rats. Rejuvenation Res 11, 139-150 (2008).
16. Ponugoti, B., Dong, G. & Graves, D.T. Role of forkhead transcription factors in diabetes-induced oxidative stress. Exp Diabetes Res 2012, 939751 (2012).
17. Nakamura, K., Fuster, J.J. & Walsh, K. Adipokines: a link between obesity and cardiovascular disease. J Cardiol 63, 250-259 (2014).
18. Bluher, M. Adipose tissue dysfunction contributes to obesity related metabolic diseases. Best Pract Res Clin Endocrinol Metab 27, 163-177 (2013).
19. Dray, C. et al. Apelin stimulates glucose utilization in normal and obese insulin-resistant mice. Cell Metab 8, 437-445 (2008).
20. Pchejetski, D. et al. Apelin prevents cardiac fibroblast activation and collagen production through inhibition of sphingosine kinase 1. Eur Heart J 33, 2360-2369 (2012).
21. Kleinz, M.J. & Davenport, A.P. Emerging roles of apelin in biology and medicine. Pharmacol Ther 107, 198-211 (2005).
22. Foussal, C. et al. Activation of catalase by apelin prevents oxidative stress-linked cardiac hypertrophy. FEBS Lett 584, 2363-2370 (2010).
23. Wang, W. et al. Loss of Apelin exacerbates myocardial infarction adverse remodeling and ischemia-reperfusion injury: therapeutic potential of synthetic Apelin analogues. J Am Heart Assoc 2, e000249 (2013).
24. Kuba, K. et al. Impaired heart contractility in Apelin gene-deficient mice associated with aging and pressure overload. Circ Res 101, e32-42 (2007).
25. Kadoglou, N.P. et al. Serum levels of apelin and ghrelin in patients with acute coronary syndromes and established coronary artery disease-KOZANI STUDY. Transl Res 155, 238-246 (2010).
26. Tycinska, A.M. et al. The value of apelin-36 and brain natriuretic peptide measurements in patients with first ST-elevation myocardial infarction. Clin Chim Acta 411, 2014-2018 (2010).
27. Weir, R.A. et al. Plasma apelin concentration is depressed following acute myocardial infarction in man. Eur J Heart Fail 11, 551-558 (2009).
28. Dray, C. et al. Apelin and APJ regulation in adipose tissue and skeletal muscle of type 2 diabetic mice and humans. Am J Physiol Endocrinol Metab 298, E1161-1169 (2010).
29. Kleinz, M.J., Skepper, J.N. & Davenport, A.P. Immunocytochemical localisation of the apelin receptor, APJ, to human cardiomyocytes, vascular smooth muscle and endothelial cells. Regul Pept 126, 233-240 (2005).
30. Brunet, A. et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868 (1999).
31. Alfarano, C. et al. Transition from metabolic adaptation to maladaptation of the heart in obesity: role of apelin. Int J Obes 39, 312-20 (2015).
32. Drougard, A. et al. Hypothalamic apelin/reactive oxygen species signaling controls hepatic glucose metabolism in the onset of diabetes. Antioxid Redox Signal 20, 557-573 (2013).
33. Pchejetski, D. et al. Oxidative stress-dependent sphingosine kinase-1 inhibition mediates monoamine oxidase A-associated cardiac cell apoptosis. Circ Res 100, 41-49 (2007).
34. Boal, F. et al. LG186: An inhibitor of GBF1 function that causes Golgi disassembly in human and canine cells. Traffic 11, 1537-1551 (2010).
35. Attane, C. et al. Apelin treatment increases complete Fatty Acid oxidation, mitochondrial oxidative capacity, and biogenesis in muscle of insulin-resistant mice. Diabetes 61, 310-320 (2012).
36. Nahrendorf, M., Pittet, M.J. & Swirski, F.K. Monocytes: protagonists of infarct inflammation and repair after myocardial infarction. Circulation 121, 2437-2445 (2010).
37. Van Der Heide, L.P., Hoekman, M.F. & Smidt, M.P. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J 380, 297-309 (2004).
38. Calnan, D.R. & Brunet, A. The FoxO code. Oncogene 27, 2276-2288 (2008).
39. Kops, G.J. et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 419, 316-321 (2002).
40. Medema, R.H., Kops, G.J., Bos, J.L. & Burgering, B.M. AFX-like Forkhead transcription factors mediate cell-cycle regulation by Ras and PKB through p27kip1. Nature 404, 782-787 (2000).
41. Kowluru, A. & Matti, A. Hyperactivation of protein phosphatase 2A in models of glucolipotoxicity and diabetes: potential mechanisms and functional consequences. Biochem Pharmacol 84, 591-597 (2012).
42. Awad, H., Nolette, N., Hinton, M. & Dakshinamurti, S. AMPK and FoxO1 regulate catalase expression in hypoxic pulmonary arterial smooth muscle. Pediatr Pulmonol (2013).
43. Battiprolu, P.K. et al. Metabolic stress-induced activation of FoxO1 triggers diabetic cardiomyopathy in mice. J Clin Invest 122, 1109-1118 (2013).
44. Raju, I., Kannan, K. & Abraham, E.C. FoxO3a Serves as a Biomarker of Oxidative Stress in Human Lens Epithelial Cells under Conditions of Hyperglycemia. PLoS One 8, e67126 (2013).
45. Wang, X. The expanding role of mitochondria in apoptosis. Genes Dev 15, 2922-2933 (2001).
46. Ferber, E.C. et al. FOXO3a regulates reactive oxygen metabolism by inhibiting mitochondrial gene expression. Cell Death Differ 19, 968-979 (2011).
47. Artham, S.M., Lavie, C.J., Milani, R.V. & Ventura, H.O. Obesity and hypertension, heart failure, and coronary heart disease-risk factor, paradox, and recommendations for weight loss. Ochsner J 9, 124-132 (2009).
48. De Schutter, A., Lavie, C.J. & Milani, R.V. The impact of obesity on risk factors and prevalence and prognosis of coronary heart disease-the obesity paradox. Prog Cardiovasc Dis 56, 401-408 (2014).
49. Curtis, J.P. et al. The obesity paradox: body mass index and outcomes in patients with heart failure. Arch Intern Med 165, 55-61 (2005).
50. Horwich, T.B. et al. The relationship between obesity and mortality in patients with heart failure. J Am Coll Cardiol 38, 789-795 (2001).
51. Fonarow, G.C. et al. An obesity paradox in acute heart failure: analysis of body mass index and inhospital mortality for 108,927 patients in the Acute Decompensated Heart Failure National Registry. Am Heart J 153, 74-81 (2007).