Mechanisms of hydrogen peroxide-induced vasoconstriction in the isolated perfused rat kidney

• Autorzy: Moreno J. M. , Rodriguez Gomez I. , Wangensteen R. , Perez-Abud R. , Duarte J. , Osuna A. , Vargas F.
• Języki publikacji: EN

Abstrakty

EN

The vasoconstrictor effect of hydrogen peroxide (H2O2) on isolated perfused rat kidney was investigated. H2O2 induced vasoconstriction in the isolated rat kidney in a concentration-dependent manner. The vasoconstrictor effects of H2O2 were completely inhibited by 1200 U/ml catalase. Endothelium-removal potentiated the renal response to H2O2. The H2O2 dose-response curve was not significantly modified by administration of the NO inhibitor L-NAME (10-4 mol/l), whereas it was increased by the non-specific inhibitor of K+-channels, tetraethylammonium (3·10-3 mol/l). Separately, removal of extracellular Ca2+, administration of a mixture of calcium desensitizing agents (nitroprusside, papaverine, and diazoxide), and administration of a protein kinase C (PKC) inhibitor (chelerythrine, 10-5 mol/l) each significantly attenuated the vasoconstrictor response to H2O2, which was virtually suppressed when they were performed together. The pressor response to H2O2 was not affected by: dimethyl sulfoxide (7·10-3 mol/l) plus mannitol (3·10-3 mol/l); intracellular Ca2+ chelation using BAPTA (10-5 mol/l); calcium store depletion after repeated doses of phenylephrine (10-5 g/g kidney); or the presence of indomethacin (10-5 mol/l), ODYA (2·10-6 mol/l) or genistein (10-5 mol/l). We conclude that the vasoconstrictor response to H2O2 in the rat renal vasculature comprises the following components: 1) extracellular calcium influx, 2) activation of PKC, and 3) stimulation of pathways leading to sensitization of contractile elements to calcium. Moreover, a reduced pressor responsiveness to H2O2 in female kidneys was observed.

Słowa kluczowe

EN

kidney; hydrogen peroxide; mechanism; protein kinase C; sexual dimorphism; renal perfusion pressure; catalase; vasoconstriction; rat

• Wydawca: -
• Czasopismo: Journal of Physiology and Pharmacology
• Rocznik: 2010
• Tom: 61
• Numer: 3
• Opis fizyczny: p.325-332,fig.,ref.

Twórcy

autor

Moreno J. M.

• Departamento de Fisiologia, Facultad de Medicina, E-18012, Granada, Spain

autor

Rodriguez Gomez I.

autor

Wangensteen R.

autor

Perez-Abud R.

autor

Duarte J.

autor

Osuna A.

autor

Vargas F.

Bibliografia

• Halliwell B, Clement MV, Long LH. Hydrogen peroxide in the human body. FEBS Lett 2000; 486: 10-13.
• Ardanaz N, Pagano PJ. Hydrogen peroxide as a paracrine vascular mediator: regulation and signaling leading to dysfunction. Exp Biol Med 2006; 231: 237-251.
• Droge W. Free radicals in the physiological control of cell function. Physiol Rev 2001; 82: 47-95.
• Faraci FM. Hydrogen peroxide: watery fuel for change in vascular biology. Arteriocler Thromb Vasc Biol 2006; 26: 1931-1933.
• Wolin MS, Gupte SA, Oeckler RA. Superoxide in the vascular system. J Vasc Res 2002; 39: 191-207.
• Gil-Longo J, Gonzalez-Vazquez C. Characterization of four different effects elicited by H2O2 in rat aorta. Vascul Pharmacol 2005; 43: 128-138.
• Thakali K, Davenport L, Fink GD, Watts SW. Pleiotropic effects of hydrogen peroxide in arteries and veins from normotensive and hypertensive rats. Hypertension 2006; 47: 482–487.
• Rodriguez-Martinez MA, Garcia-Cohen EC, Baena AB, Gonzalez R, Salaices M, Marin J. Contractile responses elicited by hydrogen peroxide in aorta from normotensive and hypertensive rats. Endothelial modulation and mechanism involved. Br J Pharmacol 1998; 125: 1329-1335.
• Yang ZW, Zheng T, Zhang A, Altura BT, Altura BM. Mechanisms of hydrogen peroxide-induced contraction of rat aorta. Eur J Pharmacol 1998; 344: 169-181.
• Thakali K, Davenport L, Fink GD, Watts SW. Cyclooxygenase, p38 mitogen-activated protein kinase (MAPK), extracellular signal-regulated kinase MAPK, Rho kinase, and Src mediate hydrogen peroxide-induced contraction of rat thoracic aorta and vena cava. J Pharmacol Exp Ther 2007; 320: 236-243.
• Jin N, Rhoades RA. Activation of tyrosine kinases in H2O2-induced contraction in pulmonary artery. Am J Physiol 1997; 272: H2686-H2692.
• Katusic ZS, Schugel J, Cosentino F, Vanhoutte PM. Endothelium-dependent contractions to oxygen-derived free radicals in the canine basilar artery. Am J Physiol 1993; 264: H859-H864.
• Omar HA, Figueroa R, Omar RA, Tejani N, Wolin MS. Hydrogen peroxide and reoxygenation cause prostaglandin-mediated contraction of human placental arteries and veins. Am J Obstet Gynecol 1992; 167: 201-207.
• Horowitz A, Menice CB, Laporte R, Morgan KG. Mechanisms of smooth muscle contraction. Physiol Rev 1996; 76: 967-1003.
• Yang ZW, Zheng T, Wang J, Zhang A, Altura BT, Altura BM. Hydrogen peroxide induces contraction and raises [Ca2+]i in canine cerebral arterial smooth muscle: participation of cellular signaling pathways. Naunyn Schmiedebergs Arch Pharmacol 1999; 360: 646-653.
• Robert M, Morris HG, Schreoder WR, Repine JE. Oxygen metabolites stimulate thromboxane production and vasoconstriction in isolated saline-perfused rabbit lungs. J Clin Invest 1984; 74: 608-613.
• Rao GN, Runge MS, Alexander RW. Hydrogen peroxide activation of cytosolic phospholipase A2 in vascular smooth muscle cells. Biochim Biophys Acta 1995; 1265: 67-72.
• Sheehan DW, Giese EC, Gugino SF, Russel JA. Characterization and mechanisms of H2O2-induced contractions of pulmonary arteries. Am J Physiol 1993; 264: H1542-H1547.
• Boyer CS, Bannenberg GL, Neve EPA, Ryrfeldt A, Moldeus P. Evidence for the activation of the signal-responsive phospholipase A2 by exogenous hydrogen peroxide. Biochem Pharmacol 1995; 50: 753-761.
• Swei A, Lacy F, DeLano FA, Schmid-Schonbein GW. Oxidative stress in the Dahl hypertensive rat. Hypertension 1997; 30: 1628-1633.
• Wolin MS. Activated oxygen metabolites as regulators of vascular tone. Klin Wochenschr 1991; 69: 1046-1049.
• Yang H, Shi M, VanRemmen H, et al. Reduction of pressor response to vasoconstrictor agents by overexpression of catalase in mice. Am J Hypertens 2003; 16: 1-5.
• Suvorava T, Lauer N, Kumpf S, Jacob R, Meyer W, Kojda G. Endogenous vascular hydrogen peroxide regulates arteriolar tension in vivo. Circulation 2005; 112: 2487-2495.
• Cowley AW. Long-term control of arterial pressure. Physiol Rev 1992; 72: 211-300.
• Chen YF, Cowley AW, Zou AP. Increased H2O2 counteracts the vasodilator and natriuretic effects of superoxide dismutation by tempol in renal medulla. Am J Physiol Regul Integr Comp Physiol 2003; 285: R827-R833.
• Makino A, Skelton MM, Zou AP, Cowley AW. Increased renal medullary H2O2 leads to hypertension. Hypertension 2003; 42: 25-30.
• Wangensteen R, Moreno JM, Sainz J, et al. Gender difference in the role of endothelial-derived relaxing factors modulating renal vascular reactivity. Eur J Pharmacol 2004; 486: 281-288.
• Vargas F. Osuna A. Modulatory role of endothelium-derived relaxing factors on the response to vasoconstrictors and on flow-pressure curve in the isolated perfused rat kidney. J Vasc Res 1996; 33: 119-123.
• Snedecor GW, Cochran WG. Statistical methods. Iowa: The Iowa State University Press 1980, 507.
• Thakali K, Demel SL, Fink GD, Watts SW. Endothelin-1-induced contraction in veins is independent of hydrogen peroxide. Am J Physiol Heart Circ Physiol 2005; 289: H1115-H11122.
• Suematsu M, Schmid-Schonbein GW, Chavez-Chavez RH, et al. in vivo visualization of oxidative changes in microvessels during neutrophil activation. Am J Physiol 1993; 264: H881-H891.
• Lacy F, Kailasam MT, O’Connor DT, Schmid-Schonbein GW, Parmer RJ. Plasma hydrogen peroxide production in human essential hypertension: role of heredity, gender, and ethnicity. Hypertension 2000; 36: 878-884.
• Lacy F, O’Connor DT, Schmid-Schonbein GW. Plasma hydrogen peroxide production in hypertensives and normotensive subjects at genetic risk of hypertension. J Hypertens 1998; 16: 291-303.
• Brandes RP, Mugge A. Gender differences in the generation of superoxide anions in the rat aorta. Life Sci 1997; 60: 391-396.
• Sullivan JC, Sasser JM, Pollock JS. Male SHR had enhanced urinary excretion of H2O2 compared with female SHR. Am J Physiol 2007; 92: R764-R768.
• Pelaez NJ, Braun TR, Paul RJ, Meiss RA, Packer S. H2O2 mediates Ca2+- and MLC20 phosphorylation-independent contraction in intact and permeabilized vascular muscle. Am J Physiol 2000; 279: H1185-H1193.
• Baas AS, Berk BC. Differential activation of mitogen-activated protein kinases by H2O2 and O2·- in vascular smooth muscle cells. Circ Res 1995; 77: 29-36.
• Salamanca DA, Khalil RA. Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem Pharmacol 2005; 70: 1537-1547.
• Lopez-Ongil S, Torrecillas G, Perez-Sala D, Gonzalez-Santiago L, Rodriguez-Puyol M, Rodriguez-Puyol D. Mechanisms involved in the contraction of endothelial cells by hydrogen peroxide. Free Radic Biol Med 1999; 26: 501-510.
• Kompanowska-Jezierska E, Kuczeriszka M. Cytochrome P-450 metabolites in renal circulation and excretion-interaction with the nitric oxide (NO) system. J Physiol Pharmacol 2008; 59: 137-149.
• Sadowski J, Badzynska B. Intrarenal vasodilator systems: NO, prostaglandins and bradykinin. An integrative approach. J Physiol Pharmacol 2008; 59: 105-119.
• Thomas SR, Schulz E, Keaney JF. Hydrogen peroxide restrains endothelium- derived nitric oxide bioactivity - role for iron-dependent oxidative stress. Free Radic Biol Med 2006; 41: 681-688.
• Li WG, Miller FJ, Zhang HJ, Spitz DR, Oberley LW, Weintraub NL. H2O2-induced O2– production by a non-phagocytic NAD(P)H oxidase causes oxidant injury. J Biol Chem 2001; 276: 29251-29256.
• Chalupsky K, Cai H. Endothelial dihydrofolate reductase: critical for nitric oxide bioavailability and role in angiotensin II uncoupling of endothelial nitric oxide synthase. Proc Natl Acad Sci USA 2005; 102: 9056-9061.
• Thengchaisri N, Hein TW, Wang W, et al. Upregulation of arginase by H2O2 impairs endothelium-dependent nitric oxide-mediated dilation of coronary arterioles. Arterioscler Thromb Vasc Biol 2006; 26: 2035-2042.
• Jaimes EA, Sweeney C, Raij L. Effects of the reactive oxygen species hydrogen peroxide and hypochlorite on endothelial nitric oxide production. Hypertension 2001; 38: 877-883.
• Li L, Wu J, Jiang C. Differential expression of Kir6.1 and SUR2B mRNAs in the vasculature of various tissues in rats. J Membr Biol 2003; 196: 61-69.
• Leffler CW, Busija DW, Armstead WM, Mirro R. H2O2 effects on cerebral prostanoids and pial arteriolar diameter in piglets. Am J Physiol 1990; 258: H1382-H1387.
• Gao Y, Vanhoutte PM. Products of cyclooxygenase mediate the responses of guinea pig trachea to hydrogen peroxide. J Appl Physiol 1993; 74: 2105-2111.
• Shen JZ, Zheng XF, Kwan CY. Differential contractile actions of reactive oxygen species on rat aorta: selective activation of ATP receptor by H2O2. Life Sci 2000; 66: 291-296.