High fructose causes cardiac hypertrophy via mitochondrial signaling pathway

American Journal of Translational Research

Volumn 8, Issue 11, 2016, Pages 4869-4880

  Zhang, Yan Bo ^a   Meng, Yan Hai ^a   Chang, Shuo ^a   Zhang, Rong Yuan ^a   Shi, Chen ^a  

^a FUWAI HOSPITAL   (China)

Author keywords

Cardiac hypertrophy; Cystic fibrosis transmembrane conductance regulator; Fructose; Mitochondria; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CYSTIC FIBROSIS TRANSMEMBRANE CONDUCTANCE REGULATOR; FRUCTOSE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; MITOCHONDRIA TARGETED ANTIOXIDANT SKQ1; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPPLER ECHOCARDIOGRAPHY; FIBROBLAST; HEART EJECTION FRACTION; HEART MITOCHONDRION; HEART VENTRICLE HYPERTROPHY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; MRNA EXPRESSION ASSAY; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 84998880879     PISSN: None     EISSN: 19438141     Source Type: Journal    
DOI: None     Document Type: Article

References (43)

1. Sverdlov AL, Elezaby A, Qin F, Behring JB, Luptak I, Calamaras TD, Siwik DA, Miller EJ, Liesa M, Shirihai OS, Pimentel DR, Cohen RA, Bachschmid MM, Colucci WS. Mitochond-rial Reactive Oxygen Species Mediate Cardiac Structural, Functional, and Mitochondrial Con-sequences of Diet-Induced Metabolic Heart Disease. J Am Heart Assoc 2016; 5.
2. Mells JE, Fu PP, Sharma S, Olson D, Cheng L, Handy JA, Saxena NK, Sorescu D, Anania FA. Glp-1 analog, liraglutide, ameliorates hepatic steatosis and cardiac hypertrophy in C57BL/6J mice fed a Western diet. Am J Physiol Gastro-intest Liver Physiol 2012; 302: G225-235.
3. Zhang J, Zhang BH, Yu YR, Tang CS, Qi YF. Adrenomedullin protects against fructose-induced insulin resistance and myocardial hypertrophy in rats. Peptides 2011; 32: 1415-1421.
4. Bouchard-Thomassin AA, Lachance D, Drolet MC, Couet J, Arsenault M. A high-fructose diet worsens eccentric left ventricular hypertrophy in experimental volume overload. Am J Physiol Heart Circ Physiol 2011; 300: H125-134.
5. Chess DJ, Xu W, Khairallah R, O’Shea KM, Kop WJ, Azimzadeh AM, Stanley WC. The antioxidant tempol attenuates pressure overload-induced cardiac hypertrophy and contractile dysfunction in mice fed a high-fructose diet. Am J Physiol Heart Circ Physiol 2008; 295: H2223-2230.
6. Santos CX, Anilkumar N, Zhang M, Brewer AC, Shah AM. Redox signaling in cardiac myocytes. Free Radic Biol Med 2011; 50: 777-793.
7. Murphy MP. How mitochondria produce reactive oxygen species. Biochem J 2009; 417: 1-13.
8. Ku HJ, Ahn Y, Lee JH, Park KM, Park JW. IDH2 deficiency promotes mitochondrial dysfunction and cardiac hypertrophy in mice. Free Radic Biol Med 2015; 80: 84-92.
9. Sverdlov AL, Elezaby A, Behring JB, Bachschmid MM, Luptak I, Tu VH, Siwik DA, Miller EJ, Liesa M, Shirihai OS, Pimentel DR, Cohen RA, Colucci WS. High fat, high sucrose diet causes car-diac mitochondrial dysfunction due in part to oxidative post-translational modification of mitochondrial complex II. J Mol Cell Cardiol 2015; 78: 165-173.
10. Al-Awwadi NA, Araiz C, Bornet A, Delbosc S, Cristol JP, Linck N, Azay J, Teissedre PL, Cros G. Extracts enriched in different polyphenolic families normalize increased cardiac NADPH oxidase expression while having differential effects on insulin resistance, hypertension, and cardiac hypertrophy in high-fructose-fed rats. J Agric Food Chem 2005; 53: 151-157.
11. Miatello R, Vazquez M, Renna N, Cruzado M, Zumino AP, Risler N. Chronic administration of resveratrol prevents biochemical cardio-vascular changes in fructose-fed rats. Am J Hypertens 2005; 18: 864-870.
12. Adlam VJ, Harrison JC, Porteous CM, James AM, Smith RA, Murphy MP, Sammut IA. Tar-geting an antioxidant to mitochondria de-creases cardiac ischemia-reperfusion injury. FASEB J 2005; 19: 1088-1095.
13. Lowes DA, Thottakam BM, Webster NR, Murphy MP, Galley HF. The mitochondria-targeted antioxidant MitoQ protects against organ damage in a lipopolysaccharide-peptidoglycan model of sepsis. Free Radic Biol Med 2008; 45: 1559-1565.
14. Gioscia-Ryan RA, LaRocca TJ, Sindler AL, Zigler MC, Murphy MP, Seals DR. Mitochondria-targeted antioxidant (MitoQ) ameliorates age-related arterial endothelial dysfunction in mice. J Physiol 2014; 592: 2549-2561.
15. Demyanenko IA, Popova EN, Zakharova VV, Ilyinskaya OP, Vasilieva TV, Romashchenko VP, Fedorov AV, Manskikh VN, Skulachev MV, Zinovkin RA, Pletjushkina OY, Skulachev VP, Chernyak BV. Mitochondria-targeted antioxidant SkQ1 improves impaired dermal wound healing in old mice. Aging (Albany NY) 2015; 7: 475-485.
16. Plotnikov EY, Silachev DN, Jankauskas SS, Rokitskaya TI, Chupyrkina AA, Pevzner IB, Zorova LD, Isaev NK, Antonenko YN, Skulachev VP, Zorov DB. Mild uncoupling of respir-ation and phosphorylation as a mechanism providing nephro- and neuroprotective effects of penetrating cations of the SkQ family. Bio-chemistry (Mosc) 2012; 77: 1029-1037.
17. Plotnikov EY, Chupyrkina AA, Jankauskas SS, Pevzner IB, Silachev DN, Skulachev VP, Zorov DB. Mechanisms of nephroprotective effect of mitochondria-targeted antioxidants under rhabdomyolysis and ischemia/reperfusion. Biochim Biophys Acta 2011; 1812: 77-86.
18. Velsor LW, Kariya C, Kachadourian R, Day BJ. Mitochondrial oxidative stress in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am J Respir Cell Mol Biol 2006; 35: 579-586.
19. Kelly-Aubert M, Trudel S, Fritsch J, Nguyen-Khoa T, Baudouin-Legros M, Moriceau S, Jeanson L, Djouadi F, Matar C, Conti M, Ollero M, Brouillard F, Edelman A. GSH monoethyl ester rescues mitochondrial defects in cystic fibrosis models. Hum Mol Genet 2011; 20: 2745-2759.
20. Zhou JJ, Wei Y, Zhang L, Zhang J, Guo LY, Gao C, Li DP, Zhang Y. Chronic intermittent hypobaric hypoxia prevents cardiac dysfunction through enhancing antioxidation in fructose-fed rats. Can J Physiol Pharmacol 2013; 91: 332-337.
21. Vinhas M, Araujo AC, Ribeiro S, Rosario LB, Belo JA. Transthoracic echocardiography re-ference values in juvenile and adult 129/Sv mice. Cardiovasc Ultrasound 2013; 11: 12.
22. Pazzini CE, Colpo AC, Poetini MR, Pires CF, de Camargo VB, Mendez AS, Azevedo ML, Soares JC, Folmer V. Effects of Red Wine Tannat on Oxidative Stress Induced by Glucose and Fructose in Erythrocytes in Vitro. Int J Med Sci 2015; 12: 478-486.
23. Zhao L, Guo X, Wang O, Zhang H, Wang Y, Zhou F, Liu J, Ji B. Fructose and glucose combined with free fatty acids induce metabolic disorders in HepG2 cell: A new model to study the impacts of high-fructose/sucrose and high-fat diets in vitro. Mol Nutr Food Res 2016; 60: 909-921.
24. Zhao M, Guo H, Chen J, Fujino M, Ito H, Takahashi K, Abe F, Nakajima M, Tanaka T, Wang J, Huang H, Zheng S, Hei M, Li J, Ma X, Chen Y, Zhao L, Zhuang J, Zhu P, Li XK. 5-aminolevulinic acid combined with sodium ferrous citrate ameliorates H2O2-induced cardiomyocyte hypertrophy via activation of the MAPK/Nrf2/HO-1 pathway. Am J Physiol Cell Physiol 2015; 308: C665-672.
25. Zeng JW, Zeng XL, Li FY, Ma MM, Yuan F, Liu J, Lv XF, Wang GL, Guan YY. Cystic Fibro-sis Transmembrane Conductance Regulator (CFTR) prevents apoptosis induced by hydrogen peroxide in basilar artery smooth muscle cells. Apoptosis 2014; 19: 1317-1329.
26. Elezaby A, Sverdlov AL, Tu VH, Soni K, Luptak I, Qin F, Liesa M, Shirihai OS, Rimer J, Schaffer JE, Colucci WS, Miller EJ. Mitochondrial remodeling in mice with cardiomyocyte-specific lipid overload. J Mol Cell Cardiol 2015; 79: 275-283.
27. Liesa M, Luptak I, Qin F, Hyde BB, Sahin E, Siwik DA, Zhu Z, Pimentel DR, Xu XJ, Ruderman NB, Huffman KD, Doctrow SR, Richey L, Colucci WS, Shirihai OS. Mitochond-rial transporter ATP binding cassette mito-chondrial erythroid is a novel gene required for cardiac recovery after ischemia/reper-fusion. Circulation 2011; 124: 806-813.
28. Sahin E, Colla S, Liesa M, Moslehi J, Muller FL, Guo M, Cooper M, Kotton D, Fabian AJ, Walkey C, Maser RS, Tonon G, Foerster F, Xiong R, Wang YA, Shukla SA, Jaskelioff M, Martin ES, Hefferman TP, Protopopov A, Ivanova E, Mahoney JE, Kost-Alimova M, Perry SR, Bronson R, Liao R, Mulliqan R, Shirihai OS, Chin L, Depinho RA. Telomere dysfunc-tion induces metabolic and mitochondrial compromise. Nature 2011; 470: 359-365.
29. Remig V, Franklin B, Margolis S, Kostas G, Nece T, Street JC. Trans fats in America: a review of their use, consumption, health implications, and regulation. J Am Diet Assoc 2010; 110: 585-592.
30. Mellor K, Ritchie R, Morris M, Delbridge L. Elevated myocardial superoxide production precedes the cardiac hypertrophy response to a high fructose diet in mice. Am J Physiol Renal Physiol 2016; 310: F547-559.
31. Mellor K, Ritchie RH, Meredith G, Woodman OL, Morris MJ, Delbridge LM. High-fructose diet elevates myocardial superoxide generation in mice in the absence of cardiac hyper-trophy. Nutrition 2010; 26: 842-848.
32. Sugden PH, Clerk A. Oxidative stress and growth-regulating intracellular signaling pathways in cardiac myocytes. Antioxid Redox Signal 2006; 8: 2111-2124.
33. Liu L, Li J, Liu J, Yuan Z, Pierre SV, Qu W, Zhao X, Xie Z. Involvement of Na+/K+-ATPase in hydrogen peroxide-induced hypertrophy in cardiac myocytes. Free Radic Biol Med 2006; 41: 1548-1556.
34. Foussal C, Lairez O, Calise D, Pathak A, Guilbeau-Frugier C, Valet P, Parini A, Kunduzova O. Activation of catalase by apelin prevents oxidative stress-linked cardiac hypertrophy. FEBS Lett 2010; 584: 2363-2370.
35. Seenarain V, Viola HM, Ravenscroft G, Casey TM, Lipscombe RJ, Ingley E, Laing NG, Bringans SD, Hool LC. Evidence of altered guinea pig ventricular cardiomyocyte protein expression and growth in response to a 5 min in vitro exposure to H(2)O(2). J Proteome Res 2010; 9: 1985-1994.
36. Chistyakov VA, Prazdnova EV, Gutnikova LV, Sazykina MA, Sazykin IS. Superoxide scav-enging activity of plastoquinone derivative 10-(6’-plastoquinonyl) decyltriphenylphosphonium (SkQ1). Biochemistry (Mosc) 2012; 77: 776-778.
37. Khailova LS, Dedukhova VI, Mokhova EN. Cations SkQ1 and MitoQ accumulated in mitochondria delay opening of ascorbate/FeSO4-induced nonspecific pore in the inner mitochondrial membrane. Biochemistry (Mosc) 2008; 73: 1121-1124.
38. Popova EN, Pletjushkina OY, Dugina VB, Dom-nina LV, Ivanova OY, Izyumov DS, Skulachev VP, Chernyak BV. Scavenging of reactive oxygen species in mitochondria induces myofi-broblast differentiation. Antioxid Redox Sig-nal 2010; 13: 1297-1307.
39. Qin F, Siwik DA, Luptak I, Hou X, Wang L, Higuchi A, Weisbrod RM, Ouchi N, Tu VH, Calamaras TD, Miller EJ, Verbeuren TJ, Walsh K, Cohen RA, Colucci WS. The polyphenols resveratrol and S17834 prevent the structural and functional sequelae of diet-induced metabolic heart disease in mice. Circulation 2012; 125: 1757-1764, S1751-1756.
40. Wu R, Wyatt E, Chawla K, Tran M, Ghanefar M, Laakso M, Epting CL, Ardehali H. Hexokinase II knockdown results in exaggerated cardiac hypertrophy via increased ROS production. EMBO Mol Med 2012; 4: 633-646.
41. Wojtovich AP, Smith CO, Haynes CM, Nehrke KW, Brookes PS. Physiological consequences of complex II inhibition for aging, disease, and the mKATP channel. Biochim Biophys Acta 2013; 1827: 598-611.
42. Yankovskaya V, Horsefield R, Tornroth S, Luna-Chavez C, Miyoshi H, Leger C, Byrne B, Cecchini G, Iwata S. Architecture of succinate dehydrogenase and reactive oxygen species generation. Science 2003; 299: 700-704.
43. Zhang YP, Zhang H, Duan DD. Chloride channels in stroke. Acta Pharmacol Sin 2013; 34: 17-23.