Nicorandil prevents endothelial dysfunction due to antioxidative effects via normalisation of NADPH oxidase and nitric oxide synthase in streptozotocin diabetic rats

Cardiovascular Diabetology

Volumn 10, Issue , 2011, Pages

  Serizawa, Ken ichi ^a   Yogo, Kenji ^a   Aizawa, Ken ^a   Tashiro, Yoshihito ^a   Ishizuka, Nobuhiko ^a  

^a CHUGAI PHARMACEUTICAL CO LTD   (Japan)

Author keywords

Diabetes; Endothelial dysfunction; Enos; Nadph oxidase; Nicorandil; Reactive oxidative species

Indexed keywords

APOCYNIN; DRINKING WATER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; N(G) NITROARGININE METHYL ESTER; NICORANDIL; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; STREPTOZOCIN; TEMPOL; ACETOPHENONE DERIVATIVE; AMINE OXIDE; ANTIOXIDANT; ENZYME INHIBITOR; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; NEUTROPHIL CYTOSOLIC FACTOR 1; NOS3 PROTEIN, RAT; VASODILATOR AGENT;

ANESTHESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTERY DILATATION; ARTICLE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; FEMORAL ARTERY; FLUORESCENCE; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MALE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES; ANIMAL; CELL CULTURE; DIABETIC ANGIOPATHY; DRUG ANTAGONISM; DRUG EFFECT; ECHOGRAPHY; ENZYMOLOGY; EXPERIMENTAL DIABETES MELLITUS; METABOLISM; PATHOPHYSIOLOGY; PROTEIN MULTIMERIZATION; SPIN LABELING; SPRAGUE DAWLEY RAT; TIME; VASCULAR ENDOTHELIUM; VASODILATATION;

ACETOPHENONES; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; CYCLIC N-OXIDES; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; FEMORAL ARTERY; GTP CYCLOHYDROLASE; HUMANS; MALE; NADPH OXIDASE; NG-NITROARGININE METHYL ESTER; NICORANDIL; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PROTEIN MULTIMERIZATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; SPIN LABELS; TIME FACTORS; VASODILATION; VASODILATOR AGENTS;

EID: 81555237210     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/1475-2840-10-105     Document Type: Article

References (61)

1. The Japanese Coronary Artery Disease (JCAD) Study Investigators Current status of the background of patients with coronary artery disease in Japan. Circ J 2006, 70(10):1256-1262. 10.1253/circj.70.1256, 16998255, The Japanese Coronary Artery Disease (JCAD) Study Investigators.
2. Kasai T, Miyauchi K, Kajimoto K, Kubota N, Kurata T, Daida H. Influence of diabetes on > 10-year outcomes after percutaneous coronary intervention. Heart Vessels 2008, 23(3):149-154. 10.1007/s00380-007-1021-x, 18484156.
3. Kip KE, Faxon DP, Detre KM, Yeh W, Kelsey SF, Currier JW. Coronary angioplasty in diabetic patients. The National Heart, Lung, and Blood Institute Percutaneous Transluminal Coronary Angioplasty Registry. Circulation 1996, 94(8):1818-1825.
4. Creager MA, Luscher TF, Cosentino F, Beckman JA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part I. Circulation 2003, 108(12):1527-1532. 10.1161/01.CIR.0000091257.27563.32, 14504252.
5. Gryglewski RJ, Palmer RM, Moncada S. Superoxide anion is involved in the breakdown of endothelium-derived vascular relaxing factor. Nature 1986, 320(6061):454-456. 10.1038/320454a0, 3007998.
6. Cai S, Khoo J, Channon KM. Augmented BH4 by gene transfer restores nitric oxide synthase function in hyperglycemic human endothelial cells. Cardiovasc Res 2005, 65(4):823-831. 10.1016/j.cardiores.2004.10.040, 15721862.
7. Laursen JB, Somers M, Kurz S, McCann L, Warnholtz A, Freeman BA, Tarpey M, Fukai T, Harrison DG. Endothelial regulation of vasomotion in apoE-deficient mice: implications for interactions between peroxynitrite and tetrahydrobiopterin. Circulation 2001, 103(9):1282-1288.
8. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 2003, 111(8):1201-1209. 152929, 12697739.
9. Vasquez-Vivar J, Duquaine D, Whitsett J, Kalyanaraman B, Rajagopalan S. Altered tetrahydrobiopterin metabolism in atherosclerosis: implications for use of oxidized tetrahydrobiopterin analogues and thiol antioxidants. Arterioscler Thromb Vasc Biol 2002, 22(10):1655-1661. 10.1161/01.ATV.0000029122.79665.D9, 12377745.
10. d'Uscio LV, Milstien S, Richardson D, Smith L, Katusic ZS. Long-term vitamin C treatment increases vascular tetrahydrobiopterin levels and nitric oxide synthase activity. Circ Res 2003, 92(1):88-95. 10.1161/01.RES.0000049166.33035.62, 12522125.
11. Tiefenbacher CP, Bleeke T, Vahl C, Amann K, Vogt A, Kubler W. Endothelial dysfunction of coronary resistance arteries is improved by tetrahydrobiopterin in atherosclerosis. Circulation 2000, 102(18):2172-2179.
12. Bian K, Doursout MF, Murad F. Vascular system: role of nitric oxide in cardiovascular diseases. J Clin Hypertens (Greenwich) 2008, 10(4):304-310.
13. Nakagawa T, Tanabe K, Croker BP, Johnson RJ, Grant MB, Kosugi T, Li Q. Endothelial dysfunction as a potential contributor in diabetic nephropathy. Nat Rev Nephrol 2011, 7(1):36-44. 10.1038/nrneph.2010.152, 21045790.
14. Landmesser U, Hornig B, Drexler H. Endothelial function: a critical determinant in atherosclerosis?. Circulation 2004, 109(21 Suppl 1):II27-33.
15. IONA study Group Effect of nicorandil on coronary events in patients with stable angina: the Impact Of Nicorandil in Angina (IONA) randomised trial. Lancet 2002, 359(9314):1269-1275. IONA study Group.
16. Sekiya M, Sato M, Funada J, Ohtani T, Akutsu H, Watanabe K. Effects of the long-term administration of nicorandil on vascular endothelial function and the progression of arteriosclerosis. J Cardiovasc Pharmacol 2005, 46(1):63-67. 10.1097/01.fjc.0000162771.00174.a8, 15965356.
17. Ishibashi Y, Takahashi N, Tokumaru A, Karino K, Sugamori T, Sakane T, Yoshitomi H, Sato H, Oyake N, Murakami Y, et al. Effects of long-term nicorandil administration on endothelial function, inflammation, and oxidative stress in patients without coronary artery disease. J Cardiovasc Pharmacol 2008, 51(3):311-316. 10.1097/FJC.0b013e318163a95f, 18356697.
18. Zhao JL, Yang YJ, Chen JL, Kang LM, Wu Y, Gao RL. Nicorandil reduces myocardial no-reflow by protection of endothelial function via the activation of KATP channel. Clin Chim Acta 2006, 374(1-2):100-105. 10.1016/j.cca.2006.05.039, 16824503.
19. Date T, Taniguchi I, Inada K, Matsuo S, Miyanaga S, Yamane T, Abe Y, Sugimoto K, Mochizuki S. Nicorandil inhibits serum starvation-induced apoptosis in vascular endothelial cells. J Cardiovasc Pharmacol 2005, 46(6):721-726. 10.1097/01.fjc.0000184466.37951.76, 16306793.
20. Kasono K, Yasu T, Kakehashi A, Kinoshita N, Tamemoto H, Namai K, Ohno R, Ueba H, Kuroki M, Ishikawa S, et al. Nicorandil improves diabetes and rat islet beta-cell damage induced by streptozotocin in vivo and in vitro. Eur J Endocrinol 2004, 151(2):277-285. 10.1530/eje.0.1510277, 15296485.
21. Heiss C, Sievers RE, Amabile N, Momma TY, Chen Q, Natarajan S, Yeghiazarians Y, Springer ML. In vivo measurement of flow-mediated vasodilation in living rats using high-resolution ultrasound. Am J Physiol Heart Circ Physiol 2008, 294(2):H1086-1093.
22. Corretti MC, Anderson TJ, Benjamin EJ, Celermajer D, Charbonneau F, Creager MA, Deanfield J, Drexler H, Gerhard-Herman M, Herrington D, et al. Guidelines for the ultrasound assessment of endothelial-dependent flow-mediated vasodilation of the brachial artery: a report of the International Brachial Artery Reactivity Task Force. J Am Coll Cardiol 2002, 39(2):257-265. 10.1016/S0735-1097(01)01746-6, 11788217.
23. Griendling KK, Sorescu D, Ushio-Fukai M. NAD(P)H oxidase: role in cardiovascular biology and disease. Circ Res 2000, 86(5):494-501.
24. Muller G, Morawietz H. NAD(P)H oxidase and endothelial dysfunction. Horm Metab Res 2009, 41(2):152-158. 10.1055/s-0028-1086023, 18816427.
25. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RA, Warnholtz A, et al. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 2001, 88(2):E14-22.
26. Ojaimi C, Kinugawa S, Recchia FA, Hintze TH. Oxidant-NO dependent gene regulation in dogs with type I diabetes: impact on cardiac function and metabolism. Cardiovasc Diabetol 2010, 9:43. 2936363, 20735837.
27. Gupte S, Labinskyy N, Gupte R, Csiszar A, Ungvari Z, Edwards JG. Role of NAD(P)H oxidase in superoxide generation and endothelial dysfunction in Goto-Kakizaki (GK) rats as a model of nonobese NIDDM. PLoS One 2010, 5(7):e11800. 10.1371/journal.pone.0011800, 2909910, 20668682.
28. Mishra PK, Tyagi N, Sen U, Joshua IG, Tyagi SC. Synergism in hyperhomocysteinemia and diabetes: role of PPAR gamma and tempol. Cardiovasc Diabetol 2010, 9:49. 10.1186/1475-2840-9-49, 2944245, 20828387.
29. Tajima M, Ishizuka N, Saitoh K, Sakagami H. Nicorandil enhances the effect of endothelial nitric oxide under hypoxia-reoxygenation: role of the KATP channel. Eur J Pharmacol 2008, 579(1-3):86-92. 10.1016/j.ejphar.2007.10.074, 18045588.
30. Ohshiro Y, Ma RC, Yasuda Y, Hiraoka-Yamamoto J, Clermont AC, Isshiki K, Yagi K, Arikawa E, Kern TS, King GL. Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase Cbeta-null mice. Diabetes 2006, 55(11):3112-3120. 10.2337/db06-0895, 17065350.
31. Mariappan N, Elks CM, Sriramula S, Guggilam A, Liu Z, Borkhsenious O, Francis J. NF-kappaB-induced oxidative stress contributes to mitochondrial and cardiac dysfunction in type II diabetes. Cardiovasc Res 2010, 85(3):473-483. 10.1093/cvr/cvp305, 2860708, 19729361.
32. Iliodromitis EK, Aggeli IK, Gaitanaki C, Tsiafoutis I, Zoga A, Beis I, Kremastinos DT. p38-MAPK is involved in restoration of the lost protection of preconditioning by nicorandil in vivo. Eur J Pharmacol 2008, 579(1-3):289-297. 10.1016/j.ejphar.2007.10.026, 18031732.
33. Kawamura T, Kadosaki M, Nara N, Wei J, Endo S, Inada K. Nicorandil attenuates NF-kappaB activation, adhesion molecule expression, and cytokine production in patients with coronary artery bypass surgery. Shock 2005, 24(2):103-108. 10.1097/01.shk.0000168874.83401.3f, 16044078.
34. Wenzel P, Daiber A, Oelze M, Brandt M, Closs E, Xu J, Thum T, Bauersachs J, Ertl G, Zou MH, et al. Mechanisms underlying recoupling of eNOS by HMG-CoA reductase inhibition in a rat model of streptozotocin-induced diabetes mellitus. Atherosclerosis 2008, 198(1):65-76. 10.1016/j.atherosclerosis.2007.10.003, 2889614, 18061195.
35. Eguchi Y, Takahari Y, Higashijima N, Ishizuka N, Tamura N, Kawamura Y, Ishida H. Nicorandil attenuates FeCl(3)-induced thrombus formation through the inhibition of reactive oxygen species production. Circ J 2009, 73(3):554-561. 10.1253/circj.CJ-08-0843, 19179768.
36. Wenzel P, Schulz E, Oelze M, Muller J, Schuhmacher S, Alhamdani MS, Debrezion J, Hortmann M, Reifenberg K, Fleming I, et al. AT1-receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med 2008, 45(5):619-626. 10.1016/j.freeradbiomed.2008.05.009, 18539157.
37. Satoh M, Fujimoto S, Arakawa S, Yada T, Namikoshi T, Haruna Y, Horike H, Sasaki T, Kashihara N. Angiotensin II type 1 receptor blocker ameliorates uncoupled endothelial nitric oxide synthase in rats with experimental diabetic nephropathy. Nephrol Dial Transplant 2008, 23(12):3806-3813. 10.1093/ndt/gfn357, 2639062, 18596126.
38. Pieper GM. Acute amelioration of diabetic endothelial dysfunction with a derivative of the nitric oxide synthase cofactor, tetrahydrobiopterin. J Cardiovasc Pharmacol 1997, 29(1):8-15. 10.1097/00005344-199701000-00002, 9007664.
39. Heitzer T, Krohn K, Albers S, Meinertz T. Tetrahydrobiopterin improves endothelium-dependent vasodilation by increasing nitric oxide activity in patients with Type II diabetes mellitus. Diabetologia 2000, 43(11):1435-1438. 10.1007/s001250051551, 11126415.
40. Horinaka S, Kobayashi N, Higashi T, Hara K, Hara S, Matsuoka H. Nicorandil enhances cardiac endothelial nitric oxide synthase expression via activation of adenosine triphosphate-sensitive K channel in rat. J Cardiovasc Pharmacol 2001, 38(2):200-210. 10.1097/00005344-200108000-00005, 11483869.
41. Xu J, Nagata K, Obata K, Ichihara S, Izawa H, Noda A, Nagasaka T, Iwase M, Naoe T, Murohara T, et al. Nicorandil promotes myocardial capillary and arteriolar growth in the failing heart of Dahl salt-sensitive hypertensive rats. Hypertension 2005, 46(4):719-724. 10.1161/01.HYP.0000185189.46698.15, 16172417.
42. Horinaka S, Kobayashi N, Yagi H, Mori Y, Matsuoka H. Nicorandil but not ISDN upregulates endothelial nitric oxide synthase expression, preventing left ventricular remodeling and degradation of cardiac function in Dahl salt-sensitive hypertensive rats with congestive heart failure. J Cardiovasc Pharmacol 2006, 47(5):629-635. 10.1097/01.fjc.0000211741.47960.c2, 16775500.
43. Horinaka S, Kobayashi N, Yabe A, Asakawa H, Yagi H, Mori Y, Tsubokou Y, Yoshida K, Nakano S, Matsuoka H. Nicorandil protects against lethal ischemic ventricular arrhythmias and up-regulates endothelial nitric oxide synthase expression and sulfonylurea receptor 2 mRNA in conscious rats with acute myocardial infarction. Cardiovasc Drugs Ther 2004, 18(1):13-22.
44. Hongo M, Mawatari E, Sakai A, Ruan Z, Koizumi T, Terasawa F, Yazaki Y, Kinoshita O, Ikeda U, Shibamoto T. Effects of nicorandil on monocrotaline-induced pulmonary arterial hypertension in rats. J Cardiovasc Pharmacol 2005, 46(4):452-458. 10.1097/01.fjc.0000176728.74690.09, 16160596.
45. Liou JY, Hong HJ, Sung LC, Chao HH, Chen PY, Cheng TH, Chan P, Liu JC. Nicorandil inhibits angiotensin-II-induced proliferation of cultured rat cardiac fibroblasts. Pharmacology 2011, 87(3-4):144-151. 10.1159/000323555, 21346392.
46. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP, et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 2000, 404(6779):787-790. 10.1038/35008121, 10783895.
47. Ozcan C, Bienengraeber M, Dzeja PP, Terzic A. Potassium channel openers protect cardiac mitochondria by attenuating oxidant stress at reoxygenation. Am J Physiol Heart Circ Physiol 2002, 282(2):H531-539.
48. Serizawa K, Yogo K, Aizawa K, Koike N, Ishizuka N, Ishida H. Nicorandil, a KATP channel opener, prevents paclitaxel-induced endothelial dysfunction in rats. Eur J Cardiol 2010, 31(supple 1):99.
49. Wilcox CS, Pearlman A. Chemistry and antihypertensive effects of tempol and other nitroxides. Pharmacol Rev 2008, 60(4):418-469. 10.1124/pr.108.000240, 2739999, 19112152.
50. Simonsen U, Christensen FH, Buus NH. The effect of tempol on endothelium-dependent vasodilatation and blood pressure. Pharmacol Ther 2009, 122(2):109-124. 10.1016/j.pharmthera.2009.02.002, 19268689.
51. Leo CH, Hart JL, Woodman OL. 3',4'-Dihydroxyflavonol restores endothelium-dependent relaxation in small mesenteric artery from rats with type 1 and type 2 diabetes. Eur J Pharmacol 2011, 659(2-3):193-198. 10.1016/j.ejphar.2011.03.018, 21453697.
52. Rodriguez F, Lopez B, Perez C, Fenoy FJ, Hernandez I, Stec DE, Li Volti G, Salom MG. Chronic tempol treatment attenuates the renal hemodynamic effects induced by a heme oxygenase inhibitor in streptozotocin diabetic rats. Am J Physiol Regul Integr Comp Physiol 2011, 301(5):R1540-1548. 10.1152/ajpregu.00847.2010, 21849637.
53. Pieper GM, Moore-Hilton G, Roza AM. Evaluation of the mechanism of endothelial dysfunction in the genetically-diabetic BB rat. Life Sci 1996, 58(9):PL147-152. 10.1016/0024-3205(95)02360-7, 8632717.
54. Inoguchi T, Li P, Umeda F, Yu HY, Kakimoto M, Imamura M, Aoki T, Etoh T, Hashimoto T, Naruse M, et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C--dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000, 49(11):1939-1945. 10.2337/diabetes.49.11.1939, 11078463.
55. Kobayashi T, Matsumoto T, Kamata K. Mechanisms underlying the chronic pravastatin treatment-induced improvement in the impaired endothelium-dependent aortic relaxation seen in streptozotocin-induced diabetic rats. Br J Pharmacol 2000, 131(2):231-238. 10.1038/sj.bjp.0703572, 1572325, 10991915.
56. Kanie N, Matsumoto T, Kobayashi T, Kamata K. Relationship between peroxisome proliferator-activated receptors (PPAR alpha and PPAR gamma) and endothelium-dependent relaxation in streptozotocin-induced diabetic rats. Br J Pharmacol 2003, 140(1):23-32. 10.1038/sj.bjp.0705414, 1574012, 12967931.
57. Jones ID, Luis Fuentes V, Wrigglesworth D, Mort E, Elliott J. Comparison of flow-mediated vasodilation in femoral and brachial arteries in healthy dogs. Am J Vet Res 2011, 72(8):1029-1037. 10.2460/ajvr.72.8.1029, 21801059.
58. Weber LP, Al-Dissi A, Marit JS, German TN, Terletski SD. Role of carbon monoxide in impaired endothelial function mediated by acute second-hand tobacco, incense, and candle smoke exposures. Environ Toxicol Pharmacol 2011, 31(3):453-459. 10.1016/j.etap.2011.02.008, 21787716.
59. Potenza MA, Gagliardi S, Nacci C, Carratu MR, Montagnani M. Endothelial dysfunction in diabetes: from mechanisms to therapeutic targets. Curr Med Chem 2009, 16(1):94-112. 10.2174/092986709787002853, 19149564.
60. IONA study Group Impact of nicorandil in angina: subgroup analyses. Heart 2004, 90(12):1427-1430. 1768587, 15547020, IONA study Group.
61. Horinaka S, Yabe A, Yagi H, Ishimitsu T, Yamazaki T, Suzuki S, Kohro T, Nagai R. Effects of nicorandil on cardiovascular events in patients with coronary artery disease in the Japanese Coronary Artery Disease (JCAD) study. Circ J 2010, 74(3):503-509. 10.1253/circj.CJ-09-0649, 20081320.