Mutual regulation of epicardial adipose tissue and myocardial redox state by PPAR-γ/adiponectin signalling

Circulation Research

Volumn 118, Issue 5, 2016, Pages 842-855

  Antonopoulos, Alexios S ^a   Margaritis, Marios ^a   Verheule, Sander ^b   Recalde, Alice ^a   Sanna, Fabio ^a   Herdman, Laura ^a   Psarros, Costas ^a   Nasrallah, Hussein ^b   Coutinho, Patricia ^a   Akoumianakis, Ioannis ^a   Brewer, Alison C ^d   Sayeed, Rana ^e   Krasopoulos, George ^e   Petrou, Mario ^e   Tarun, Akansha ^a   Tousoulis, Dimitris ^c   Shah, Ajay M ^d   Casadei, Barbara ^a   Channon, Keith M ^a   Antoniades, Charalambos ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Adiponectin; Adipose tissue; Myocardium; Obesity; Oxidative stress

Indexed keywords

4 HYDROXYNONENAL; ACETYL COENZYME A CARBOXYLASE; ADENYLATE KINASE; ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ADIPONECTIN RECEPTOR 2; ANTITHROMBOCYTIC AGENT; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; BRAIN NATRIURETIC PEPTIDE; C REACTIVE PROTEIN; CADHERIN; CADHERIN 13; CALCIUM CHANNEL BLOCKING AGENT; CD36 ANTIGEN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; INTERLEUKIN 6; MALONALDEHYDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PROTEIN KINASE C ALPHA; PROTEIN P47; RAC1 PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; SERINE DERIVATIVE; UNCLASSIFIED DRUG; ADIPOQ PROTEIN, HUMAN;

ADIPOSE TISSUE; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY FAT DISTRIBUTION; BODY MASS; CONTROLLED STUDY; CYTOSOL; DISEASE ASSOCIATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; EPICARDIAL ADIPOSE TISSUE; EX VIVO STUDY; EXPERIMENTAL PIG; FEMALE; GENE CONTROL; GENE LOCUS; GENE OVEREXPRESSION; GENE TRANSLOCATION; HEART ATRIUM PACING; HEART FUNCTION; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE OXYGEN CONSUMPTION; HEART VENTRICLE HYPERTROPHY; HUMAN; HUMAN CELL; HUMAN TISSUE; INCIDENCE; INSULIN RESISTANCE; ISCHEMIC HEART DISEASE; LIPID OXIDATION; MALE; MOUSE; MYOCARDIAL REDOX STATE; NONHUMAN; OBESITY; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PEROXISOME; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; RAT; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; UPREGULATION; WAIST HIP RATIO; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CARDIAC MUSCLE; CELL LINE; CYTOLOGY; METABOLISM; ORGAN CULTURE TECHNIQUE; OXIDATION REDUCTION REACTION; PERICARDIUM; PIG; TRANSGENIC MOUSE;

ADIPONECTIN; ADIPOSE TISSUE; ANIMALS; CELL LINE; FEMALE; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIUM; ORGAN CULTURE TECHNIQUES; OXIDATION-REDUCTION; PERICARDIUM; PPAR GAMMA; RATS; SWINE;

EID: 84957682288     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.115.307856     Document Type: Article

References (42)

1. Mihm MJ, Yu F, Carnes CA, Reiser PJ, McCarthy PM, Van Wagoner DR, Bauer JA. Impaired myofbrillar energetics and oxidative injury during human atrial fbrillation. Circulation. 2001;104:174-180.
2. Lassègue B, San Martín A, Griendling KK. Biochemistry, physiology, and pathophysiology of NADPH oxidases in the cardiovascular system. Circ Res. 2012;110:1364-1390. doi: 10.1161/CIRCRESAHA.111.243972.
3. Kim YM, Guzik TJ, Zhang YH, Zhang MH, Kattach H, Ratnatunga C, Pillai R, Channon KM, Casadei B. A myocardial Nox2 containing NAD(P) H oxidase contributes to oxidative stress in human atrial fbrillation. Circ Res. 2005;97:629-636. doi: 10.1161/01.RES.0000183735.09871.61.
4. Reilly SN, Jayaram R, Nahar K, Antoniades C, Verheule S, Channon KM, Alp NJ, Schotten U, Casadei B. Atrial sources of reactive oxygen species vary with the duration and substrate of atrial fbrillation: implications for the antiarrhythmic effect of statins. Circulation. 2011;124:1107-1117. doi: 10.1161/CIRCULATIONAHA.111.029223.
5. Antoniades C, Demosthenous M, Reilly S, et al. Myocardial redox state predicts in-hospital clinical outcome after cardiac surgery effects of short-term pre-operative statin treatment. J Am Coll Cardiol. 2012;59:60-70. doi: 10.1016/j.jacc.2011.08.062.
6. Murdoch CE, Zhang M, Cave AC, Shah AM. NADPH oxidase-depen-dent redox signalling in cardiac hypertrophy, remodelling and failure. Cardiovasc Res. 2006;71:208-215. doi: 10.1016/j.cardiores.2006.03.016.
7. Sorescu D, Griendling KK. Reactive oxygen species, mitochondria, and NAD(P)H oxidases in the development and progression of heart failure. Congest Heart Fail. 2002;8:132-140.
8. Montezano AC, Touyz RM. Reactive oxygen species, vascular Noxs, and hypertension: focus on translational and clinical research. Antioxid Redox Signal. 2014;20:164-182. doi: 10.1089/ars.2013.5302.
9. Cosentino F, Eto M, De Paolis P, van der Loo B, Bachschmid M, Ullrich V, Kouroedov A, Delli Gatti C, Joch H, Volpe M, Lüscher TF. High glucose causes upregulation of cyclooxygenase-2 and alters prostanoid profle in human endothelial cells: role of protein kinase C and reactive oxygen species. Circulation. 2003;107:1017-1023.
10. Paneni F, Beckman JA, Creager MA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J. 2013;34:2436-2443. doi: 10.1093/eurheartj/eht149.
11. Paneni F, Costantino S, Cosentino F. Insulin resistance, diabetes, and cardiovascular risk. Curr Atheroscler Rep. 2014;16:419. doi: 10.1007/s11883-014-0419-z.
12. Kjekshus J, Apetrei E, Barrios V, et al; CORONA Group. Rosuvastatin in older patients with systolic heart failure. N Engl J Med. 2007;357:2248-2261. doi: 10.1056/NEJMoa0706201.
13. San Martin A, Griendling KK. NADPH oxidases: progress and opportunities. Antioxid Redox Signal. 2014;20:2692-2694. doi: 10.1089/ars.2014.5947.
14. Antonopoulos AS, Margaritis M, Coutinho P, et al. Reciprocal effects of systemic infammation and brain natriuretic peptide on adiponec-tin biosynthesis in adipose tissue of patients with ischemic heart disease. Arterioscler Thromb Vasc Biol. 2014;34:2151-2159. doi: 10.1161/ATVBAHA.114.303828.
15. Touyz RM. Endothelial cell IL-8, a new target for adiponectin: implications in vascular protection. Circ Res. 2005;97:1216-1219. doi: 10.1161/01.RES.0000196745.09234.36.
16. Antoniades C, Antonopoulos AS, Tousoulis D, Stefanadis C. Adiponectin: from obesity to cardiovascular disease. Obes Rev. 2009;10:269-279. doi: 10.1111/j.1467-789X.2009.00571.x.
17. Shibata R, Sato K, Pimentel DR, Takemura Y, Kihara S, Ohashi K, Funahashi T, Ouchi N, Walsh K. Adiponectin protects against myocar-dial ischemia-reperfusion injury through AMPK-and COX-2-dependent mechanisms. Nat Med. 2005;11:1096-1103. doi: 10.1038/nm1295.
18. Koenig W, Khuseyinova N, Baumert J, Meisinger C, Löwel H. Serum concentrations of adiponectin and risk of type 2 diabetes mellitus and coronary heart disease in apparently healthy middle-aged men: results from the 18-year follow-up of a large cohort from southern Germany. J Am Coll Cardiol. 2006;48:1369-1377. doi: 10.1016/j. jacc.2006.06.053.
19. Schnabel R, Messow CM, Lubos E, Espinola-Klein C, Rupprecht HJ, Bickel C, Sinning C, Tzikas S, Keller T, Genth-Zotz S, Lackner KJ, Münzel TF, Blankenberg S. Association of adiponectin with adverse outcome in coronary artery disease patients: results from the AtheroGene study. Eur Heart J. 2008;29:649-657. doi: 10.1093/eurheartj/ehn009.
20. Margaritis M, Antonopoulos AS, Digby J, et al. Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adi-ponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation. 2013;127:2209-2221. doi: 10.1161/CIRCULATIONAHA.112.001133.
21. Wingler K, Altenhoefer SA, Kleikers PW, Radermacher KA, Kleinschnitz C, Schmidt HH. VAS2870 is a pan-NADPH oxidase inhibitor. Cell Mol Life Sci. 2012;69:3159-3160. doi: 10.1007/s00018-012-1107-1.
22. Antoniades C, Bakogiannis C, Tousoulis D, et al. Preoperative ator-vastatin treatment in CABG patients rapidly improves vein graft redox state by inhibition of Rac1 and NADPH-oxidase activity. Circulation. 2010;122:S66-S73. doi: 10.1161/CIRCULATIONAHA.109.927376.
23. Brewer AC, Murray TV, Arno M, Zhang M, Anilkumar NP, Mann GE, Shah AM. Nox4 regulates Nrf2 and glutathione redox in cardiomyo-cytes in vivo. Free Radic Biol Med. 2011;51:205-215. doi: 10.1016/j. freeradbiomed.2011.04.022.
24. Heid IM, Henneman P, Hicks A, et al. Clear detection of ADIPOQ locus as the major gene for plasma adiponectin: results of genome-wide association analyses including 4659 European individuals. Atherosclerosis. 2010;208:412-420. doi: 10.1016/j.atherosclerosis.2009.11.035.
25. Richards JB, Waterworth D, O'Rahilly S, et al; GIANT Consortium. A genome-wide association study reveals variants in ARL15 that infuence adiponectin levels. PLoS Genet. 2009;5:e1000768. doi: 10.1371/journal. pgen.1000768.
26. Zhang M, Prosser BL, Bamboye MA, Gondim AN, Santos CX, Martin D, Ghigo A, Perino A, Brewer AC, Ward CW, Hirsch E, Lederer WJ, Shah AM. Contractile Function During Angiotensin-II Activation: Increased Nox2 Activity Modulates Cardiac Calcium Handling via Phospholamban Phosphorylation. J Am Coll Cardiol. 2015;66:261-272. doi: 10.1016/j. jacc.2015.05.020.
27. Kohr MJ, Traynham CJ, Roof SR, Davis JP, Ziolo MT. cAMP-independent activation of protein kinase A by the peroxynitrite generator SIN-1 elicits positive inotropic effects in cardiomyocytes. J Mol Cell Cardiol. 2010;48:645-648. doi: 10.1016/j.yjmcc.2010.01.007.
28. Park M, Youn B, Zheng XL, Wu D, Xu A, Sweeney G. Globular adipo-nectin, acting via AdipoR1/APPL1, protects H9c2 cells from hypoxia/re-oxygenation-induced apoptosis. PLoS One. 2011;6:e19143. doi: 10.1371/journal.pone.0019143.
29. Parajuli N, Patel VB, Wang W, Basu R, Oudit GY. Loss of NOX2 (gp-91phox) prevents oxidative stress and progression to advanced heart failure. Clin Sci (Lond). 2014;127:331-340. doi: 10.1042/CS20130787.
30. Brown DI, Griendling KK. Nox proteins in signal transduc-tion. Free Radic Biol Med. 2009;47:1239-1253. doi: 10.1016/j. freeradbiomed.2009.07.023.
31. Mizrahi A, Berdichevsky Y, Casey PJ, Pick E. A prenylated p47phox-p67phox-Rac1 chimera is a Quintessential NADPH oxidase activator: membrane association and functional capacity. J Biol Chem. 2010;285:25485-25499. doi: 10.1074/jbc.M110.113779.
32. Kim YM, Kattach H, Ratnatunga C, Pillai R, Channon KM, Casadei B. Association of atrial nicotinamide adenine dinucleotide phosphate oxidase activity with the development of atrial fbrillation after cardiac surgery. J Am Coll Cardiol. 2008;51:68-74. doi: 10.1016/j. jacc.2007.07.085.
33. Greulich S, Maxhera B, Vandenplas G, de Wiza DH, Smiris K, Mueller H, Heinrichs J, Blumensatt M, Cuvelier C, Akhyari P, Ruige JB, Ouwens DM, Eckel J. Secretory products from epicardial adipose tissue of patients with type 2 diabetes mellitus induce cardiomyocyte dysfunction. Circulation. 2012;126:2324-2334. doi: 10.1161/CIRCULATIONAHA.111.039586.
34. Konishi M, Sugiyama S, Sato Y, et al. Pericardial fat infammation correlates with coronary artery disease. Atherosclerosis. 2010;213:649-655. doi: 10.1016/j.atherosclerosis.2010.10.007.
35. Wang Y, Tao L, Yuan Y, Lau WB, Li R, Lopez BL, Christopher TA, Tian R, Ma XL. Cardioprotective effect of adiponectin is partially mediated by its AMPK-independent antinitrative action. Am J Physiol Endocrinol Metab. 2009;297:E384-E391. doi: 10.1152/ajpendo.90975.2008.
36. Tsukamoto O, Fujita M, Kato M, et al. Natriuretic peptides enhance the production of adiponectin in human adipocytes and in patients with chronic heart failure. J Am Coll Cardiol. 2009;53:2070-2077. doi: 10.1016/j. jacc.2009.02.038.
37. George J, Patal S, Wexler D, Sharabi Y, Peleg E, Kamari Y, Grossman E, Sheps D, Keren G, Roth A. Circulating adiponectin concentrations in patients with congestive heart failure. Heart. 2006;92:1420-1424. doi: 10.1136/hrt.2005.083345.
38. Ayala A, Muñoz MF, Argüelles S. Lipid peroxidation: production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxid Med Cell Longev. 2014;2014:360438. doi: 10.1155/2014/360438.
39. Viollet B, Horman S, Leclerc J, Lantier L, Foretz M, Billaud M, Giri S, Andreelli F. AMPK inhibition in health and disease. Crit Rev Biochem Mol Biol. 2010;45:276-295. doi: 10.3109/10409238.2010.488215.
40. Park L, Anrather J, Zhou P, Frys K, Wang G, Iadecola C. Exogenous NADPH increases cerebral blood fow through NADPH oxidase-dependent and-independent mechanisms. Arterioscler Thromb Vasc Biol. 2004;24:1860-1865. doi: 10.1161/01.ATV.0000142446.75898.44.
41. Didion SP, Faraci FM. Effects of NADH and NADPH on superox-ide levels and cerebral vascular tone. Am J Physiol Heart Circ Physiol. 2002;282:H688-H695. doi: 10.1152/ajpheart.00576.2001.
42. Guzik TJ, West NE, Black E, McDonald D, Ratnatunga C, Pillai R, Channon KM. Vascular superoxide production by NAD(P)H oxidase: association with endothelial dysfunction and clinical risk factors. Circ Res. 2000;86:E85-E90.