Cardioprotective effects of luteolin on ischemia/reperfusion injury in diabetic rats are modulated by eNOS and the mitochondrial permeability transition pathway

Journal of Cardiovascular Pharmacology

Volumn 65, Issue 4, 2015, Pages 349-356

  Yang, Jin Ting ^a   Qian, Ling Bo ^a   Zhang, Feng Jiang ^a   Wang, Jue ^a   Ai, Heng ^a   Tang, Li Hui ^a   Wang, Hui Ping ^a  

^a ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Diabetes; Endothelial nitric oxide synthase; Luteolin; Mitochondrial permeability transition; Myocardial ischemia reperfusion; Oxidative stress

Indexed keywords

CARDIOTONIC AGENT; CARRIER PROTEIN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; LUTEOLIN; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; NOS3 PROTEIN, HUMAN;

ANIMAL; DISEASE MODEL; DRUG EFFECTS; EXPERIMENTAL DIABETES MELLITUS; HEART MITOCHONDRION; INTRACELLULAR MEMBRANE; METABOLISM; MITOCHONDRIAL MEMBRANE POTENTIAL; MYOCARDIAL REPERFUSION INJURY; OXIDATIVE STRESS; PERMEABILITY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CARDIOTONIC AGENTS; DIABETES MELLITUS, EXPERIMENTAL; DISEASE MODELS, ANIMAL; INTRACELLULAR MEMBRANES; LUTEOLIN; MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA, HEART; MITOCHONDRIAL MEMBRANE TRANSPORT PROTEINS; MYOCARDIAL REPERFUSION INJURY; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PERMEABILITY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84939970590     PISSN: 01602446     EISSN: 15334023     Source Type: Journal    
DOI: 10.1097/FJC.0000000000000202     Document Type: Article

References (48)

1. Guariguata L, Whiting DR, Hambleton I, et al. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract. 2014;103:137-149.
2. Miki T, Yuda S, Kouzu H, et al. Diabetic cardiomyopathy: pathophysiology and clinical features. Heart Fail Rev. 2013;18:149-166.
3. Szuszkiewicz-Garcia MM, Davidson JA. Cardiovascular disease in diabetes mellitus: risk factors and medical therapy. Endocrinol Metab Clin North Am. 2014;43:25-40.
4. Alserius T, Hammar N, Nordqvist T, et al. Risk of death or acute myocardial infarction 10 years after coronary artery bypass surgery in relation to type of diabetes. Am Heart J. 2006;152:599-605.
5. Kvan E, Pettersen KI, Sandvik L, et al. High mortality in diabetic patients with acute myocardial infarction: cardiovascular co-morbidities contribute most to the high risk. Int J Cardiol. 2007;121:184-188.
6. Yin T, Hou R, Liu S, et al. Nitrative inactivation of thioredoxin-1 increases vulnerability of diabetic hearts to ischemia/reperfusion injury. J Mol Cell Cardiol. 2010;49:354-361.
7. Boudina S, Abel ED. Diabetic cardiomyopathy revisited. Circulation. 2007;115:3213-3223.
8. Yellon DM, Hausenloy DJ. Myocardial reperfusion injury. N Engl J Med. 2007;357:1121-1135.
9. Brunner F, Maier R, Andrew P, et al. Attenuation of myocardial ischemia/ reperfusion injury in mice with myocyte-specific overexpression of endothelial nitric oxide synthase. Cardiovasc Res. 2003;57:55-62.
10. Jones SP, Greer JJ, Kakkar AK, et al. Endothelial nitric oxide synthase overexpression attenuates myocardial reperfusion injury. Am J Physiol Heart Circ Physiol. 2004;286:H276-H282.
11. Jugdutt BI. Nitric oxide and cardioprotection during ischemia-reperfusion. Heart Fail Rev. 2002;7:391-405.
12. Burwell LS, Brookes PS. Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia-reperfusion injury. Antioxid Redox Signal. 2008;10:579-599.
13. Walters AM, Porter GA Jr, Brookes PS. Mitochondria as a drug target in ischemic heart disease and cardiomyopathy. Circ Res. 2012;111:1222-1236.
14. Whittington HJ, Babu GG, Mocanu MM, et al. The diabetic heart: too sweet for its own good? Cardiol Res Pract. 2012;2012:845698.
15. Ansley DM, Wang B. Oxidative stress and myocardial injury in the diabetic heart. J Pathol. 2013;229:232-241.
16. Hoang HH, Padgham SV, Meininger CJ. L-arginine, tetrahydrobiopterin, nitric oxide and diabetes. Curr Opin Clin Nutr Metab Care. 2013;16:76-82.
17. Thirunavukkarasu M, Penumathsa SV, Koneru S, et al. Resveratrol alleviates cardiac dysfunction in streptozotocin-induced diabetes: role of nitric oxide, thioredoxin, and heme oxygenase. Free Radic Biol Med. 2007;43:720-729.
18. Shimoi K, Okada H, Furugori M, et al. Intestinal absorption of luteolin and luteolin 7-O-[beta]-glucoside in rats and humans. FEBS Lett. 1998; 438:220-224.
19. López-Lázaro M. Distribution and biological activities of the flavonoid luteolin. Mini Rev Med Chem. 2009;9:31-59.
20. Middleton E Jr, Kandaswami C, Theoharides TC. The effects of plant flavonoids on mammalian cells: implications for inflammation, heart disease, and cancer. Pharmacol Rev. 2000;52:673-751.
21. Fang F, Li D, Pan H, et al. Luteolin inhibits apoptosis and improves cardiomyocyte contractile function through the PI3K/Akt pathway in simulated ischemia/reperfusion. Pharmacology. 2011;88:149-158.
22. Wu X, Xu T, Li D, et al. ERK/PP1a/PLB/SERCA2a and JNK pathways are involved in luteolin-mediated protection of rat hearts and cardiomyocytes following ischemia/reperfusion. PLoS One. 2013;8:e82957.
23. Qian LB, Lu JF, Ye ZG, et al. Luteolin reduces cardiac dysfunctions in streptozotocin-induced diabetic rats [in Chinese]. Zhongguo Ying Yong Sheng Li Xue Za Zhi. 2011;27:409-414.
24. Qian LB, Wang HP, Chen Y, et al. Luteolin reduces high glucose-mediated impairment of endothelium-dependent relaxation in rat aorta by reducing oxidative stress. Pharmacol Res. 2010;61:281-287.
25. Wang G, Li W, Lu X, et al. Luteolin ameliorates cardiac failure in type I diabetic cardiomyopathy. J Diabetes Complications. 2012;26:259-265.
26. Ghaboura N, Tamareille S, Ducluzeau PH, et al. Diabetes mellitus abrogates erythropoietin-induced cardioprotection against ischemicreperfusion injury by alteration of the RISK/GSK-3beta signaling. Basic Res Cardiol. 2011;106:147-162.
27. Gao Q, Yang B, Ye ZG, et al. Opening the calcium-activated potassium channel participates in the cardioprotective effect of puerarin. Eur J Pharmacol. 2007;574:179-184.
28. Gao Q, Pan HY, Qiu S, et al. Atractyloside and 5-hydroxydecanoate block the protective effect of puerarin in isolated rat heart. Life Sci. 2006;79:217-224.
29. Ghosh S, Standen NB, Galinanes M. Preconditioning the human myocardium by simulated ischemia: studies on the early and delayed protection. Cardiovasc Res. 2000;45:339-350.
30. Yao YY, Zhu MH, Zhang FJ, et al. Activation of Akt and cardioprotection against reperfusion injury are maximal with only five minutes of sevoflurane postconditioning in isolated rat hearts. J Zhejiang Univ Sci B. 2013;14:511-517.
31. Zhang FJ, Ma LL, Wang WN, et al. Hypercholesterolemia abrogates sevoflurane-induced delayed preconditioning against myocardial infarct in rats by alteration of nitric oxide synthase signaling. Shock. 2012;37:485-491.
32. Zheng Z, Yang M, Zhang F, et al. Gender-related difference of sevoflurane postconditioning in isolated rat hearts: focus on phosphatidylinositol-3-kinase/Akt signaling. J Surg Res. 2011;170:e3-e9.
33. Cui J, Li Z, Qian LB, et al. Reducing the oxidative stress mediates the cardioprotection of bicyclol against ischemia-reperfusion injury in rats. J Zhejiang Univ Sci B. 2013;14:487-495.
34. Zhang SZ, Wang NF, Xu J, et al. Kappa-opioid receptors mediate cardioprotection by remote preconditioning. Anesthesiology. 2006;105:550-556.
35. Petronilli V, Miotto G, Canton M, et al. Transient and long-lasting openings of the mitochondrial permeability transition pore can be monitored directly in intact cells by changes in mitochondrial calcein fluorescence. Biophys J. 1999;76:725-734.
36. Rodriguez-Sinovas A, Garcia-Dorado D, Pina P, et al. Effect of sarcolemmal rupture on myocardial electrical impedance during oxygen deprivation. Am J Physiol Heart Circ Physiol. 2005;288:H1396-H1403.
37. Diaz RJ, Fernandes K, Lytvyn Y, et al. Enhanced cell-volume regulation in cyclosporin A cardioprotection. Cardiovasc Res. 2013;98:411-419.
38. Shahzad T, Kasseckert SA, Iraqi W, et al. Mechanisms involved in postconditioning protection of cardiomyocytes against acute reperfusion injury. J Mol Cell Cardiol. 2013;58:209-216.
39. Qi L, Pan H, Li D, et al. Luteolin improves contractile function and attenuates apoptosis following ischemia-reperfusion in adult rat cardiomyocytes. Eur J Pharmacol. 2011;668:201-207.
40. Sun D, Huang J, Zhang Z, et al. Luteolin limits infarct size and improves cardiac function after myocardium ischemia/reperfusion injury in diabetic rats. PLoS One. 2012;7:e33491.
41. Falé PL, Ascensão L, Serralheiro ML. Effect of luteolin and apigenin on rosmarinic acid bioavailability in Caco-2 cell monolayers. Food Funct. 2013;4:426-431.
42. Hausenloy DJ, Yellon DM. Myocardial ischemia-reperfusion injury: a neglected therapeutic target. J Clin Invest. 2013;123:92-100.
43. Rubbo H, Radi R, Trujillo M, et al. Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. Formation of novel nitrogen-containing oxidized lipid derivatives. J Biol Chem. 1994;269:26066-26075.
44. Shen X, Zheng S, Metreveli NS, et al. Protection of cardiac mitochondria by overexpression of MnSOD reduces diabetic cardiomyopathy. Diabetes. 2006;55:798-805.
45. Jones SP, Bolli R. The ubiquitous role of nitric oxide in cardioprotection. J Mol Cell Cardiol. 2006;40:16-23.
46. Kim JS, Ohshima S, Pediaditakis P, et al. Nitric oxide: a signaling molecule against mitochondrial permeability transition-and ph-dependent cell death after reperfusion. Free Radic Biol Med. 2004;37:1943-1950.
47. Murphy E, Steenbergen C. Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev. 2008;88:581-609.
48. Morin D, Assaly R, Paradis S, et al. Inhibition of mitochondrial membrane permeability as a putative pharmacological target for cardioprotection. Curr Med Chem. 2009;16:4382-4398.