Myocardial mitochondrial dysfunction in mice lacking adiponectin receptor 1

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 (2005) Transcriptional coactivator PGC-1 alpha controls the energy state and contractile function of cardiac muscle. Cell Metab 1:259–271. doi: 10.1016/j.cmet.2005.03.002

Arany Z, Novikov M, Chin S, Ma Y, Rosenzweig A, Spiegelman BM (2006) Transverse aortic constriction leads to accelerated heart failure in mice lacking PPAR-gamma coactivator 1alpha. Proc Natl Acad Sci USA 103:10086–10091. doi: 10.1073/pnas.0603615103

Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa J, Hotta K, Shimomura I, Nakamura T, Miyaoka K, Kuriyama H, Nishida M, Yamashita S, Okubo K, Matsubara K, Muraguchi M, Ohmoto Y, Funahashi T, Matsuzawa Y (1999) Paradoxical decrease of an adipose-specific protein, adiponectin, in obesity. Biochem Biophys Res Commun 257:79–83. doi: 10.1006/bbrc.1999.0255

Boardman NT, Aronsen JM, Louch WE, Sjaastad I, Willoch F, Christensen G, Sejersted O, Aasum E (2014) Impaired left ventricular mechanical and energetic function in mice after cardiomyocyte-specific excision of Serca2. Am J Physiol Heart Circ Physiol 306:H1018–H1024. doi: 10.1152/ajpheart.00741.2013

Boudina S, Sena S, O’Neill BT, Tathireddy P, Young ME, Abel ED (2005) Reduced mitochondrial oxidative capacity and increased mitochondrial uncoupling impair myocardial energetics in obesity. Circulation 112:2686–2695. doi: 10.1161/CIRCULATIONAHA.105.554360

Boudina S, Sena S, Theobald H, Sheng X, Wright JJ, Hu XX, Aziz S, Johnson JI, Bugger H, Zaha VG, Abel ED (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. doi: 10.2337/db07-0481

Bugger H, Abel ED (2008) Molecular mechanisms for myocardial mitochondrial dysfunction in the metabolic syndrome. Clin Sci (Lond) 114:195–210. doi: 10.1042/CS20070166

Bugger H, Abel ED (2014) Molecular mechanisms of diabetic cardiomyopathy. Diabetologia 57:660–671. doi: 10.1007/s00125-014-3171-6

Bugger H, Boudina S, Hu XX, Tuinei J, Zaha VG, Theobald HA, Yun UJ, McQueen AP, Wayment B, Litwin SE, Abel ED (2008) Type 1 diabetic akita mouse hearts are insulin sensitive but manifest structurally abnormal mitochondria that remain coupled despite increased uncoupling protein 3. Diabetes 57:2924–2932. doi: 10.2337/db08-0079

Bugger H, Chen D, Riehle C, Soto J, Theobald HA, Hu XX, Ganesan B, Weimer BC, Abel ED (2009) Tissue-specific remodeling of the mitochondrial proteome in type 1 diabetic akita mice. Diabetes 58:1986–1997. doi: 10.2337/db09-0259

Civitarese AE, Ukropcova B, Carling S, Hulver M, DeFronzo RA, Mandarino L, Ravussin E, Smith SR (2006) Role of adiponectin in human skeletal muscle bioenergetics. Cell Metab 4:75–87. doi: 10.1016/j.cmet.2006.05.002

Ding G, Qin Q, He N, Francis-David SC, Hou J, Liu J, Ricks E, Yang Q (2007) Adiponectin and its receptors are expressed in adult ventricular cardiomyocytes and upregulated by activation of peroxisome proliferator-activated receptor gamma. J Mol Cell Cardiol 43:73–84. doi: 10.1016/j.yjmcc.2007.04.014

Echtay KS, Roussel D, St-Pierre J, Jekabsons MB, Cadenas S, Stuart JA, Harper JA, Roebuck SJ, Morrison A, Pickering S, Clapham JC, Brand MD (2002) Superoxide activates mitochondrial uncoupling proteins. Nature 415:96–99. doi: 10.1038/415096a

Fang X, Palanivel R, Cresser J, Schram K, Ganguly R, Thong FS, Tuinei J, Xu A, Abel ED, Sweeney G (2010) An APPL1-AMPK signaling axis mediates beneficial metabolic effects of adiponectin in the heart. Am J Physiol Endocrinol Metab 299:E721–E729. doi: 10.1152/ajpendo.00086.2010

Frystyk J, Berne C, Berglund L, Jensevik K, Flyvbjerg A, Zethelius B (2007) Serum adiponectin is a predictor of coronary heart disease: a population-based 10-year follow-up study in elderly men. J Clin Endocrinol Metab 92:571–576. doi: 10.1210/jc.2006-1067

Giorgio M, Migliaccio E, Orsini F, Paolucci D, Moroni M, Contursi C, Pelliccia G, Luzi L, Minucci S, Marcaccio M, Pinton P, Rizzuto R, Bernardi P, Paolucci F, Pelicci PG (2005) Electron transfer between cytochrome c and p66Shc generates reactive oxygen species that trigger mitochondrial apoptosis. Cell 122:221–233. doi: 10.1016/j.cell.2005.05.011

Guo Z, Qin Z, Zhang R, Li J, Yin Y (2012) Effect of rosiglitazone on the expression of cardiac adiponectin receptors and NADPH oxidase in type 2 diabetic rats. Eur J Pharmacol 685:116–125. doi: 10.1016/j.ejphar.2012.04.010

Heusch G (2015) Mitochondria at the heart of cardiovascular protection: p66shc-friend or foe? Eur Heart J 36:469–471. doi: 10.1093/eurheartj/ehu409

Hotta K, Funahashi T, Arita Y, Takahashi M, Matsuda M, Okamoto Y, Iwahashi H, Kuriyama H, Ouchi N, Maeda K, Nishida M, Kihara S, Sakai N, Nakajima T, Hasegawa K, Muraguchi M, Ohmoto Y, Nakamura T, Yamashita S, Hanafusa T, Matsuzawa Y (2000) Plasma concentrations of a novel, adipose-specific protein, adiponectin, in type 2 diabetic patients. Arterioscler Thromb Vasc Biol 20:1595–1599. doi: 10.1161/01.ATV.20.6.1595

Hu E, Liang P, Spiegelman BM (1996) AdipoQ is a novel adipose-specific gene dysregulated in obesity. J Biol Chem 271:10697–10703. doi: 10.1074/jbc.271.18.10697

Hui X, Lam KS, Vanhoutte PM, Xu A (2012) Adiponectin and cardiovascular health: an update. Br J Pharmacol 165:574–590. doi: 10.1111/j.1476-5381.2011.01395.x

Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M, Yamaguchi M, Namiki S, Nakayama R, Tabata M, Ogata H, Kubota N, Takamoto I, Hayashi YK, Yamauchi N, Waki H, Fukayama M, Nishino I, Tokuyama K, Ueki K, Oike Y, Ishii S, Hirose K, Shimizu T, Touhara K, Kadowaki T (2010) Adiponectin and AdipoR1 regulate PGC-1alpha and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 464:1313–1319. doi: 10.1038/nature08991

Janssen AJ, Trijbels FJ, Sengers RC, Smeitink JA, van den Heuvel LP, Wintjes LT, Stoltenborg-Hogenkamp BJ, Rodenburg RJ (2007) Spectrophotometric assay for complex I of the respiratory chain in tissue samples and cultured fibroblasts. Clin Chem 53:729–734. doi: 10.1373/clinchem.2006.078873

Kadowaki T, Yamauchi T (2005) Adiponectin and adiponectin receptors. Endocr Rev 26:439–451. doi: 10.1210/er.2005-0005

Kaludercic N, Carpi A, Nagayama T, Sivakumaran V, Zhu G, Lai EW, Bedja D, De Mario A, Chen K, Gabrielson KL, Lindsey ML, Pacak K, Takimoto E, Shih JC, Kass DA, Di Lisa F, Paolocci N (2014) Monoamine oxidase B prompts mitochondrial and cardiac dysfunction in pressure overloaded hearts. Antioxid Redox Signal 20:267–280. doi: 10.1089/ars.2012.4616

Kawahara Y, Tanonaka K, Daicho T, Nawa M, Oikawa R, Nasa Y, Takeo S (2005) Preferable anesthetic conditions for echocardiographic determination of murine cardiac function. J Pharmacol Sci 99:95–104. doi: 10.1254/jphs.FP0050343

Koenig W, Khuseyinova N, Baumert J, Meisinger C, Lowel H (2006) 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 48:1369–1377. doi: 10.1016/j.jacc.2006.06.053

Kozakova M, Muscelli E, Flyvbjerg A, Frystyk J, Morizzo C, Palombo C, Ferrannini E (2008) Adiponectin and left ventricular structure and function in healthy adults. J Clin Endocrinol Metab 93:2811–2818. doi: 10.1210/jc.2007-2580

Krahenbuhl S, Chang M, Brass EP, Hoppel CL (1991) Decreased activities of ubiquinol:ferricytochrome c oxidoreductase (complex III) and ferrocytochrome c:oxygen oxidoreductase (complex IV) in liver mitochondria from rats with hydroxycobalamin[c-lactam]-induced methylmalonic aciduria. J Biol Chem 266:20998–21003

Lashin OM, Szweda PA, Szweda LI, Romani AM (2006) Decreased complex II respiration and HNE-modified SDH subunit in diabetic heart. Free Radic Biol Med 40:886–896. doi: 10.1016/j.freeradbiomed.2005.10.040

Li J, Su S, Zong X (2014) Analysis of the association between adiponectin, adiponectin receptor 1 and diabetic cardiomyopathy. Exp Ther Med 7:1023–1027. doi: 10.3892/etm.2014.1539

Lindsay RS, Funahashi T, Hanson RL, Matsuzawa Y, Tanaka S, Tataranni PA, Knowler WC, Krakoff J (2002) Adiponectin and development of type 2 diabetes in the Pima Indian population. Lancet 360:57–58. doi: 10.1016/S0140-6736(02)09335-2

Mariappan N, Elks CM, Sriramula S, Guggilam A, Liu Z, Borkhsenious O, Francis J (2010) NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 85:473–483. doi: 10.1093/cvr/cvp305

Okada-Iwabu M, Yamauchi T, Iwabu M, Honma T, Hamagami K, Matsuda K, Yamaguchi M, Tanabe H, Kimura-Someya T, Shirouzu M, Ogata H, Tokuyama K, Ueki K, Nagano T, Tanaka A, Yokoyama S, Kadowaki T (2013) A small-molecule AdipoR agonist for type 2 diabetes and short life in obesity. Nature 503:493–499. doi: 10.1038/nature12656

Palanivel R, Fang X, Park M, Eguchi M, Pallan S, De Girolamo S, Liu Y, Wang Y, Xu A, Sweeney G (2007) Globular and full-length forms of adiponectin mediate specific changes in glucose and fatty acid uptake and metabolism in cardiomyocytes. Cardiovasc Res 75:148–157. doi: 10.1016/j.cardiores.2007.04.011

Pei H, Qu Y, Lu X, Yu Q, Lian K, Liu P, Yan W, Liu J, Ma Y, Liu Y, Li C, Li W, Lau WB, Zhang H, Tao L (2013) Cardiac-derived adiponectin induced by long-term insulin treatment ameliorates myocardial ischemia/reperfusion injury in type 1 diabetic mice via AMPK signaling. Basic Res Cardiol 108:322. doi: 10.1007/s00395-012-0322-0

Pischon T, Girman CJ, Hotamisligil GS, Rifai N, Hu FB, Rimm EB (2004) Plasma adiponectin levels and risk of myocardial infarction in men. JAMA 291:1730–1737. doi: 10.1001/jama.291.14.1730

Rosca MG, Vazquez EJ, Kerner J, Parland W, Chandler MP, Stanley W, Sabbah HN, Hoppel CL (2008) Cardiac mitochondria in heart failure: decrease in respirasomes and oxidative phosphorylation. Cardiovasc Res 80:30–39. doi: 10.1093/cvr/cvn184

Russell LK, Mansfield CM, Lehman JJ, Kovacs A, Courtois M, Saffitz JE, Medeiros DM, Valencik ML, McDonald JA, Kelly DP (2004) Cardiac-specific induction of the transcriptional coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha promotes mitochondrial biogenesis and reversible cardiomyopathy in a developmental stage-dependent manner. Circ Res 94:525–533. doi: 10.1161/01.RES.0000117088.36577.EB

Schrepper A, Schwarzer M, Schope M, Amorim PA, Doenst T (2012) Biphasic response of skeletal muscle mitochondria to chronic cardiac pressure overload—role of respiratory chain complex activity. J Mol Cell Cardiol 52:125–135. doi: 10.1016/j.yjmcc.2011.10.022

Shibata R, Numaguchi Y, Matsushita K, Sone T, Kubota R, Ohashi T, Ishii M, Kihara S, Walsh K, Ouchi N, Murohara T (2008) Usefulness of adiponectin to predict myocardial salvage following successful reperfusion in patients with acute myocardial infarction. Am J Cardiol 101:1712–1715. doi: 10.1016/j.amjcard.2008.02.057

Shibata R, Ouchi N, Ito M, Kihara S, Shiojima I, Pimentel DR, Kumada M, Sato K, Schiekofer S, Ohashi K, Funahashi T, Colucci WS, Walsh K (2004) Adiponectin-mediated modulation of hypertrophic signals in the heart. Nat Med 10:1384–1389. doi: 10.1038/nm1137

Shibata R, Sato K, Pimentel DR, Takemura Y, Kihara S, Ohashi K, Funahashi T, Ouchi N, Walsh K (2005) Adiponectin protects against myocardial ischemia-reperfusion injury through AMPK- and COX-2-dependent mechanisms. Nat Med 11:1096–1103. doi: 10.1038/nm1295

Starkov AA (2010) Measurement of mitochondrial ROS production. Methods Mol Biol 648:245–255. doi: 10.1007/978-1-60761-756-3_16

Stumvoll M, Tschritter O, Fritsche A, Staiger H, Renn W, Weisser M, Machicao F, Haring H (2002) Association of the T-G polymorphism in adiponectin (exon 2) with obesity and insulin sensitivity: interaction with family history of type 2 diabetes. Diabetes 51:37–41. doi: 10.2337/diabetes.51.1.37

Tsuchida A, Yamauchi T, Ito Y, Hada Y, Maki T, Takekawa S, Kamon J, Kobayashi M, Suzuki R, Hara K, Kubota N, Terauchi Y, Froguel P, Nakae J, Kasuga M, Accili D, Tobe K, Ueki K, Nagai R, Kadowaki T (2004) Insulin/Foxo1 pathway regulates expression levels of adiponectin receptors and adiponectin sensitivity. J Biol Chem 279:30817–30822. doi: 10.1074/jbc.M402367200

Tzagoloff A, Wharton DC (1965) Studies on the electron transfer system. Lxii. The reaction of cytochrome oxidase with carbon monoxide. J Biol Chem 240:2628–2633

Villeneuve C, Guilbeau-Frugier C, Sicard P, Lairez O, Ordener C, Duparc T, De Paulis D, Couderc B, Spreux-Varoquaux O, Tortosa F, Garnier A, Knauf C, Valet P, Borchi E, Nediani C, Gharib A, Ovize M, Delisle MB, Parini A, Mialet-Perez J (2013) p53-PGC-1alpha pathway mediates oxidative mitochondrial damage and cardiomyocyte necrosis induced by monoamine oxidase-A upregulation: role in chronic left ventricular dysfunction in mice. Antioxid Redox Signal 18:5–18. doi: 10.1089/ars.2011.4373

Weibel ER (1979) Steriological principles for morphometry in electron microscopic cytology. Int Rev Cytol 26:235–302

Westenbrink BD, Ling H, Divakaruni AS, Gray CB, Zambon AC, Dalton ND, Peterson KL, Gu Y, Matkovich SJ, Murphy AN, Miyamoto S, Dorn GW 2nd, Heller Brown J (2015) Mitochondrial reprogramming induced by CaMKIIdelta mediates hypertrophy decompensation. Circ Res 116:e28–e39. doi: 10.1161/CIRCRESAHA.116.304682

Wittig I, Braun HP, Schagger H (2006) Blue native PAGE. Nat Protoc 1:418–428. doi: 10.1038/nprot.2006.62

Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M, Murakami K, Ohteki T, Uchida S, Takekawa S, Waki H, Tsuno NH, Shibata Y, Terauchi Y, Froguel P, Tobe K, Koyasu S, Taira K, Kitamura T, Shimizu T, Nagai R, Kadowaki T (2003) Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423:762–769. doi: 10.1038/nature01705

Yamauchi T, Nio Y, Maki T, Kobayashi M, Takazawa T, Iwabu M, Okada-Iwabu M, Kawamoto S, Kubota N, Kubota T, Ito Y, Kamon J, Tsuchida A, Kumagai K, Kozono H, Hada Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Awazawa M, Takamoto I, Froguel P, Hara K, Tobe K, Nagai R, Ueki K, Kadowaki T (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat Med 13:332–339. doi: 10.1038/nm1557

Yan W, Zhang H, Liu P, Wang H, Liu J, Gao C, Liu Y, Lian K, Yang L, Sun L, Guo Y, Zhang L, Dong L, Lau WB, Gao E, Gao F, Xiong L, Wang H, Qu Y, Tao L (2013) Impaired mitochondrial biogenesis due to dysfunctional adiponectin-AMPK-PGC-1alpha signaling contributing to increased vulnerability in diabetic heart. Basic Res Cardiol 108:329. doi: 10.1007/s00395-013-0329-1