Melatonin improves cardiovascular function and ameliorates renal, cardiac and cerebral damage in rats with renovascular hypertension

Journal of Pineal Research

Volumn 47, Issue 1, 2009, Pages 97-106

  Erşahin, Mehmet ^b   Öehirli, Özer ^a   Toklu, Hale Z ^a   Süleymanoglu, Selami ^c   Emekli Alturfan, Ebru ^a   Yarat, Ayşen ^a   Tatlidede, Elif ^a   Yěen, Berrak Ç ^d   Şener, Göksel ^a  

^a MARMARA UNIVERSITY   (Turkey)

^b HAYDARPASA NUMUNE EDUCATION AND RESEARCH HOSPITAL   (Turkey)

^c GULHANE SCHOOL OF MEDICINE   (Turkey)

^d MARMARA UNIVERSITY SCHOOL OF MEDICINE   (Turkey)

Author keywords

Asymmetric dimethylarginine; Hypertension; Melatonin; Oxidative stress

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CATALASE; CREATINE KINASE; GLUTATHIONE; LACTATE DEHYDROGENASE; MALONALDEHYDE; MELATONIN; MYELOPEROXIDASE; N(G),N(G) DIMETHYLARGININE; NITRIC OXIDE; SUPEROXIDE DISMUTASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; BLOOD PRESSURE; BRAIN DAMAGE; CARDIOVASCULAR FUNCTION; CONTROLLED STUDY; DRUG EFFECT; ECHOCARDIOGRAPHY; ENZYME ACTIVITY; HEART INJURY; KIDNEY INJURY; MALE; NONHUMAN; RAT; RENOVASCULAR HYPERTENSION;

ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; BLOOD PRESSURE; BRAIN; CARDIOVASCULAR PHYSIOLOGICAL PROCESSES; CATALASE; ECHOCARDIOGRAPHY; GLUTATHIONE; HEART; HYPERTENSION, RENOVASCULAR; KIDNEY; MALE; MALONDIALDEHYDE; MELATONIN; MYOCARDIUM; OXIDATIVE STRESS; PEROXIDASE; RATS; RATS, WISTAR; SUPEROXIDE DISMUTASE;

EID: 67649957803     PISSN: 07423098     EISSN: 1600079X     Source Type: Journal    
DOI: 10.1111/j.1600-079X.2009.00693.x     Document Type: Article

References (73)

1. Textor SC, Wilcox CS. Renal artery stenosis: a common, treatable cause of renal failure? Annu Rev Med 2001 52 : 421 442. (Pubitemid 32195333)
2. Magrini F, Reggiani P, Roberts N, Meazza R, Ciulla M, Zanchetti A. Effects of angiotensin and angiotensin blockade on coronary circulation and coronary reserve. Am J Med 1988 84 : 55 60.
3. Kim S, Iwao H. Molecular and cellular mechanisms of angiotensin-II mediated cardiovascular and renal diseases. Pharmacol Rev 2000 52 : 11 34. (Pubitemid 30127593)
4. Minuz P, Patrignani P, Gaino S et al. Increased oxidative stress and platelet activation in patients with hypertension and renovascular disease. Circulation 2002 106 : 2800 2805. (Pubitemid 35396979)
5. Ushio-Fukai M, Zafari AM, Fukui T, Ishizaka N, Griendling KK. p22phox is a critical component of the superoxide-generating NADH/NADPH oxidase system and regulates angiotensin II-induced hypertrophy in vascular smooth muscle cells. J Biol Chem 1996 271 : 23317 23321. (Pubitemid 26314775)
6. 2 in angiotensin II-induced vascular hypertrophy. Hypertension 1998 32 : 488 495. (Pubitemid 28429138)
7. Laursen JB, Rajagopalan S, Galis Z, Tarpey M, Freeman BA, Harrison DG. Role of superoxide in angiotensin-II-induced but not catecholamine-induced hypertension. Circulation 1997 95 : 588 593. (Pubitemid 27063033)
8. Somers MJ, Mavromatis K, Galis ZS, Harrison DG. Vascular superoxide production and vasomotor function in hypertension induced by deoxycorticosterone acetate-salt. Circulation 2000 101 : 1722 1728. (Pubitemid 30196634)
9. Touyz RM, Tabet F, Schiffrin EL. Redox-dependent signalling by angiotensin II and vascular remodelling in hypertension. Clin Exp Pharmacol Physiol 2003 30 : 860 866. (Pubitemid 37506154)
10. Diep QN, Amiri F, Touyz RM et al. PPAR alpha activator effects on Ang II-induced vascular oxidative stress and inflammation. Hypertension 2002 40 : 866 871. (Pubitemid 35434908)
11. Rajagopalan S, Kurz S, Munzel T et al. Angiotensin II-mediated hypertension in the rat increases vascular superoxide production via membrane NADH/NADPH oxidase activation: contribution to alterations of vasomotor tone. J Clin Invest 1996 97 : 1916 1923.
12. Cohuet G, Struijker-Boudier H. Mechanisms of target organ damage caused by hypertension: therapeutic potential. Pharm Ther 2006 111 : 81 98. (Pubitemid 43765539)
13. Lerner AB, Case JD, Takahashi Y et al. Isolation of melatonin, a pineal factor that lightens melanocytes. J Am Chem Soc 1958 80 : 2587 2589.
14. Tengattini S, Reiter RJ, Tan DX, Terron MP, Rodella LF, Rezzani R. Cardiovascular diseases: protective effects of melatonin. J Pineal Res 2008 44 : 16 25. (Pubitemid 350231106)
15. Simko F, Paulis L. Melatonin as a potential antihypertensive treatment. J Pineal Res 2007 42 : 319 322. (Pubitemid 46581667)
16. Arangino S, Cagnacci A, Angiolucci M et al. Effects of melatonin on vascular reactivity, catecholamine levels, and blood pressure in healthy men. Am J Cardiol 1999 83 : 1417 1419. (Pubitemid 29205758)
17. Pechánová O, Zicha J, Paulis L et al. The effect of N-acetylcysteine and melatonin in adult spontaneously hypertensive rats with established hypertension. Eur J Pharmacol 2007 561 : 129 136. (Pubitemid 46435853)
18. Girouard H, Denault C, Chulak C, De Champlain J. Treatment by n-acetylcysteine and melatonin increases cardiac baroreflex and improves antioxidant reserve. Am J Hypertens 2004 17 : 947 954. (Pubitemid 39361668)
19. Sahna E, Deniz E, Bay-Karabulut A, Burma O. Melatonin protects myocardium from ischemia-reperfusion injury in hypertensive rats: role of myeloperoxidase activity. Clin Exp Hypertens 2008 30 : 673 681.
20. Abete P, Bianco S, Calabrese C et al. Effects of melatonin in isolated rat papillary muscle. FEBS Lett 1997 412 : 79 85. (Pubitemid 27310004)
21. Pang CS, Xi SC, Brown GM, Pang SF, Shiu SY. 2[125I] Iodomelatonin binding and interaction with beta-adrenergic signaling in chick heart/coronary artery physiology. J Pineal Res 2002 32 : 243 252. (Pubitemid 34478286)
22. Masana MI, Doolen S, Ersahin C et al. MT(2) melatonin receptors are present and functional in rat caudal artery. J Pharmacol Exp Ther 2002 302 : 1295 1302. (Pubitemid 34920255)
23. Peyrot F, Ducrocq C. Potential role of tryptophan derivatives in stress responses characterized by the generation of reactive oxygen and nitrogen species. J Pineal Res 2008 45 : 235 246.
24. Reiter RJ, Tan DX, Pilar Terron M, Flores LJ, Czarnocki Z. Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochim Pol 2007 54 : 1 9. (Pubitemid 46481811)
25. Mayo JC, Sainz RM, Tan DX et al. Anti-inflammatory actions of melatonin and its metabolites, N1-acetyl-N2-formyl-5-methoxykynuramine (AFMK) and N1-acetyl-5-methoxykynuramine(AMK), in macrophages. J Neuroimmunol 2005 165 : 139 149. (Pubitemid 40984631)
26. Carrillo-Vico A, Guerrero JM, Lardone PJ, Reiter RJ. A review of the multiple actions of melatonin on the immune system. Endocr 2005 27 : 189 200. (Pubitemid 41558451)
27. Navar LG, Harrison-Bernard LM, Nishiyama A, Kobori H. Regulation of intrarenal angiotensin II in hypertension. Hypertension 2002 39 : 316 322. (Pubitemid 34165142)
28. Goldblatt H, Lynch J, Hanzal RF, Summerville MD. Studies on Experimental Hypertension I. The production of persistent elevation of the systolic blood pressure by means of renal ischemia. J Exper Med 1934 59 : 347 379.
29. Schiller NB, Shah PM, Crawford M et al. Recommendations for quantitation of the left ventricle by two-dimensional echocardiography. American Society of Echocardiography Committee on Standards, Subcommittee on Quantitation of Two-Dimensional Echocardiograms. J Am Soc Echocardiogr 1989 2 : 358 367.
30. Mylorie AA, Collins H, Umbles C, Kyle J. Erythrocyte superoxide dismutase activity and other parameters of cupper status in rats ingesting lead acetate. Toxicol Appl Pharmacol 1986 82 : 512 520. (Pubitemid 16162421)
31. Aebi H. Catalase in vitro. In : Methods of Enzymatic Analysis, 2nd edn, Vol. 2. Bergmeyer HU (ed FL, 1974 pp. 121 126.
32. Beuge JA, Aust SD. Microsomal lipid peroxidation. Meth Enzymol 1978 52 : 302 311.
33. Beutler E. Glutathione in red blood cell metabolism. A Manuel of Biochemical Methods. Grune & Stratton, New York, 1975, pp. 112 114.
34. Hillegass LM, Griswold DE, Brickson B, Albrightson-Winslow C. Assessment of myeloperoxidase activity in whole rat kidney. J Pharmacol Meth 1990 24 : 285 295.
35. Kim YK, Lee SH, Goldinger JM, Hong SK. Effect of ethanol on organic ion transport in rabbit kidney. Toxicol Appl Pharmacol 1986 86 : 411 420. (Pubitemid 17224953)
36. Reading HW, Isbir T. The role of cation activated ATPase in transmitter release from the rat iris. Q J Exp Physiol 1980 65 : 105 116.
37. Fiske CH, Subbarow Y. The colorimetric determination of phosphorus. J Biol Chem 1925 66 : 375 400.
38. Lowry OH, Rosenbrough NJ, Farr AL, Randall RJ. Protein measurements with the folin phenol reagent. J Biol Chem 1951 193 : 265 275.
39. Russo C, Olivieri O, Girelli D et al. Anti-oxidant status and lipid peroxidation in patients with essential hypertension. J Hypertens 1998 16 : 1267 1271. (Pubitemid 28408409)
40. Schnackenberg CG, Welch WJ, Wilcox CS. Normalization of blood pressure and renal vascular resistance in SHR with a membranepermeable superoxide dismutase mimetic: role of nitric oxide. Hypertension 1998 32 : 59 64. (Pubitemid 28324125)
41. Swei A, Lacy F, Delano FA, Parks DA, Schmid-Schonbein GW. A mechanism of oxygen free radical production in the Dahl hypertensive rat. Microcirculation 1999 6 : 179 187. (Pubitemid 129671257)
42. Vaziri ND, Wang XQ, Oveisi F, Rad B. Induction of oxidative stress by glutathione depletion causes severe hypertension in normal rats. Hypertension 2000 36 : 142 146. (Pubitemid 30602167)
43. Cosentino F, Sill JC, Katusic ZS. Role of superoxide anions in the mediation of endothelium-dependent contractions. Hypertension 1994 23 : 229 235. (Pubitemid 24050286)
44. Martinez ML, Castro MM, Rizzi E et al. Lercanidipine reduces matrix metalloproteinase-2 activity and reverses vascular dysfunction in renovascular hypertensive rats. Eur J Pharmacol 2008 591 : 224 230.
45. Reckelhoff JF, Romero JC. Role of oxidative stress in angiotensin-induced hypertension. Am J Physiol Regul Integr Comp Physiol 2003 284 : R893 912.
46. Kielstein JT, Bode-Böger SM, Frölich JC, Ritz E, Haller H, Fliser D. Asymmetric dimethylarginine, blood pressure, and renal perfusion in elderly subjects. Circulation 2003 107 : 1891 1895. (Pubitemid 36444130)
47. Veresh Z, Racz A, Lotz G, Koller A. ADMA impairs nitric oxide-mediated arteriolar function due to increased superoxide production by angiotensin II-NAD(P)H oxidase pathway. Hypertension 2008 52 : 960 966.
48. Miyazaki H, Matsuoka H, Cooke JP et al. Endogenous nitric oxide synthase inhibitor: a novel marker of atherosclerosis. Circulation 1999 99 : 1141 1146. (Pubitemid 29120084)
49. Jacobi J, Maas R, Cordasic N et al. Role of asymmetric dimethylarginine for angiotensin II-induced target organ damage in mice. Am J Physiol Heart Circ Physiol 2008 294 : H1058 1066.
50. Wang D, Strandgaard S, Iversen J, Wilcox CS. Asymmetric dimethylarginine, oxidative stress, and vascular nitric oxide synthase in essential hypertension. Am J Physiol Regul Integr Comp Physiol 2009 296 : R195 200.
51. Schnackenberg CG, Wilcox CS. Two-week administration of tempol attenuates both hypertension and renal excretion of 8-Iso prostaglandin F2 alpha. Hypertension 1999 33 : 424 428. (Pubitemid 29065696)
52. Atarashi K, Ishiyama A, Takagi M et al. Vitamin E ameliorates the renal injury of Dahl salt-sensitive rats. Am J Hypertens 1997 10 : 116S 119S. (Pubitemid 27239844)
53. Girouard H, Chulak C, Lejossec M, Lamontagne D, De Champlain J. Vasorelaxant effects of the chronic treatment with melatonin on mesenteric artery and aorta of spontaneously hypertensive rats. J Hypertens 2001 19 : 1369 1377. (Pubitemid 32730453)
54. Kojsová S, Jendeková L, Zicha J, Kunes J, Andriantsitohaina R, Pechánová O. The effect of different antioxidants on nitric oxide production in hypertensive rats. Physiol Res 2006 55 (Suppl 1 S3 16.
55. Paulis L, Matuskova J, Adamcova M et al. Regression of left ventricular hypertrophy and aortic remodelling in NO-deficient hypertensive rats: effect of L-arginine and spironolactone. Acta Physiol (Oxf) 2008 194 : 45 55.
56. Cunnane SC, Manku MS, Oka M, Horrobin DF. Enhanced vascular reactivity to various vasoconstrictor agents following pinealectomy in the rat: role of melatonin. Can J Physiol Pharmacol 1980 58 : 287 293. (Pubitemid 10135051)
57. Kawashima K, Miwa Y, Fujimoto K, Oohata H, Nishino H, Koike H. Antihypertensive action of melatonin in the spontaneously hypertensive rat. Clin Exp Hypertens A 1987 9 : 1121 1131.
58. Gradman AH, Alfayoumi F. From left ventricular hypertrophy to congestive heart failure: management of hypertensive heart disease. Prog Cardiovasc Dis 2006 48 : 326 341.
59. Higashi Y, Sasaki S, Nakagawa K, Matsuura H, Oshima T, Chayama K. Endothelial function and oxidative stress in renovascular hypertension. N Engl J Med 2002 346 : 1954 1962. (Pubitemid 34651355)
60. De Nigris F, Lerman LO, Condorelli M, Lerman A, Napoli C. Oxidationsensitive transcription factors and molecular mechanisms in the arterial wall. Antioxid Redox Signal 2001 3 : 1119 1130. (Pubitemid 34027367)
61. Dubocovich M, Markowska M. Functional MT1 and MT2 melatonin receptors in mammals. Endocr 2005 27 : 101 110.
62. Tan DX, Manchester LC, Terron MP, Flores LJ, Reiter RJ. One molecule, many derivatives: a never-ending interaction of melatonin with reactive oxygen and nitrogen species? J Pineal Res 2007 42 : 28 42. (Pubitemid 44924323)
63. Ghosh G, De K, Maity S et al. Melatonin protects against oxidative damage and restores expression of GLUT4 gene in the hyperthyroid rat heart. J Pineal Res 2007 42 : 71 82. (Pubitemid 44924328)
64. Jonas M, Garfinkel D, Zisapel N, Laudon M, Grossman E. Impaired nocturnal melatonin secretion in non-dipper hypertensive patients. Blood Press 2003 12 : 19 24. (Pubitemid 36416949)
65. Girotti L, Lago M, Ianovsky O et al. Low urinary 6-sulfatoxymelatonin levels in patients with severe congestive heart failure. Endocr 2003 22 : 245 248. (Pubitemid 38183700)
66. Brugger P, Marktl W, Herold M. Impaired nocturnal secretion of melatonin in coronary heart disease. Lancet 1995 345 : 1408.
67. Domínguez-Rodríguez A, Abreu-González P, García MJ, Sanchez J, Marrero F, De Armas-Trujillo D. Decreased nocturnal melatonin levels during acute myocardial infarction. J Pineal Res 2002 33 : 248 252. (Pubitemid 35252997)
68. Lerman L, Textor SC. Pathophysiology of ischemic nephropathy. Urol Clin North Am 2001 28 : 793 803. (Pubitemid 34028042)
69. Chade AR, Rodriguez-Porcel M, Herrmann J et al. Antioxidant Intervention Blunts Renal Injury in Experimental Renovascular Disease. J Am Soc Nephrol 2004 15 : 958 966. (Pubitemid 38375315)
70. ++)-ATPase activities in high glucose-treated human erythrocytes. Free Radic Biol Med 2000 29 : 1122 1128. (Pubitemid 30838455)
71. Korkmaz A, Reiter RJ, Topal T, Manchester LC, Oter S, Tan DX. Melatonin: an established antioxidant worthy of use in clinical trials. Mol Med 2009 15 : 43 50.
72. Kettle AJ, Winterbourn CC. Myeloperoxidase: a key regulator of neutrophil oxidant production. Redox Rep 1997 3 : 3 15. (Pubitemid 27199160)
73. Galijasevic S, Abdulhamid I, Abu-Soud HM. Melatonin is a potent inhibitor for myeloperoxidase. Biochemistry 2008 47 : 2668 2677. (Pubitemid 351304572)