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Role of oxidative stress in the natriuresis induced by central administration of angiotensin II

Laboratory of Neuropeptides, School of Pharmacy, Central University of Venezuela, Caracas, Venezuela, astern60@ hotmail.com

Jorge Arzola

Laboratory of Neuropeptides, School of Pharmacy, Central University of Venezuela, Caracas, Venezuela

Sara De Jesús

Laboratory of Neuropeptides, School of Pharmacy, Central University of Venezuela, Caracas, Venezuela

Maider Varela

Laboratory of Neuropeptides, School of Pharmacy, Central University of Venezuela, Caracas, Venezuela

Introduction. Central administration of angiotensin II (Ang II) is known to reduce urinary volume and to increase sodium and potassium excretion. Recently, a novel signalling mechanism for Ang II in the periphery has been shown to involve reduced nicotinamide adenine dinucleotide phosphate [NAD(P)H] oxidase-derived reactive oxygen species (ROS).Although ROS are now known to be involved in numerous Ang II-regulated processes in peripheral tissues, and are increasingly implicated in CNS neurodegenerative diseases, the role of ROS in central regulation of Ang II-induced hydromineral metabolism remains unexplored.The hypothesis that ROS are involved in central Ang II signalling and in Ang II-dependent antidiuresis, natriuresis and kaliuresis was tested by the use of selective antagonists of the NAD(P)H oxidase cascade. Materials and methods. In intracerebroventricular (ICV)-cannulated rats,Ang II was injected ICV and urinary sodium and potassium excretion was assessed at 1-, 3-, and 6-hour periods of urine collection. Urine sample was analysed for sodium and potassium concentration using a flame photometer. The role of NAD(P)H oxidase-dependent signalling cascade was evaluated using the selective NAD(P)H oxidase inhibitor, apocynin; the superoxide dismutase mimetic, 4-hydroxy-2,2,6,6-tetramethylpiperidine-1-oxyl (tempol); and the protein kinase C inhibitor, chelerythrine. Results. ICV administration of Ang II to conscious hydrated rats resulted in a significant decrease in urinary volume in the first hour, and an increased sodium and potassium excretion during the 6-hour period of urine collection, which was most effective during the 3 and 6 h. Interference with the NAD(P)H oxidase signalling by central administration of apocynin, tempol or chelerythrine, blunted the natriuretic and kaliuretic effect induced by central administration of Ang II, without affecting its antidiuretic action.

Conclusion.This study demonstrates that increases of urinary sodium and potassium excretion elicited by central administration of Ang II are mediated by NAD(P)H oxidase- dependent production of superoxide and protein kinase C activation in conscious hydrated rats.

Key Words: angiotensin II • apocynin • chelerythrine • natriuresis • tempol

References

• Averill DB, Diz DI Angiotensin peptides and baroreflex control of sympathetic outflow: pathways and mechanisms of the medulla oblongata. Brain Res Bull 2000;51:119-28.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Seltzer A., Bregonzio C., Armando I., Baiardi G., Saavedra JM Oral administration of an AT1 receptor antagonist prevents the central effects of angiotensin II in spontaneously hypertensive rats. Brain Res 2004;1028:9-18.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Veltmar A., Qadri F., Rascher W., Unger T. The angiotensin II induced vasopressin release is mediated through a central catecholaminergic pathway. J Hypertens 1992;10:S23.[Web of Science]
• Severs W., Summy-Long J., Taylor J., Connor J. A central effect of angiotensin: release of pituitary pressor material. J Pharmacol Exp Ther 1970;74:27-34.
• Fitzsimons JT Angiotensin stimulation on the central nervous system. Rev Physiol Biochem Pharmacol 1980;87:117-67.[Medline] [Order article via Infotrieve]
• Sterling GH, Chee O., Riggs RV, Keil LC Effect of chronic intracerebroventricular angiotensin II infusion on vasopressin release in rats. Neuroendocrinology 1980;31:182-8.[Web of Science][Medline] [Order article via Infotrieve]
• Brooks V., Malvin R. Intracerebroventricular infusions of angiotensin II increases sodium excretion. Proc Soc Exp Biol Med 1982;169:532-7.[CrossRef][Medline] [Order article via Infotrieve]
• Barbella Y., Cierco M., Israel A. Effects of losartan, a non-peptide angiotensin II receptor antagonist, on drinking behavior and renal actions of central administered renin. Proc Soc Exp Biol Med 1993;202:401-06.[CrossRef][Medline] [Order article via Infotrieve]
• Saavedra JM, Benicky J., Zhou J. Angiotensin II: multitasking in the brain. J Hypertens Suppl 2006;24:S131-7.[Medline] [Order article via Infotrieve]
• Allen AM, Moeller I., Jenkins TA et al. Angiotensin receptors in the nervous system. Brain Res Bull 1998;47:17-28.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Griendling KK, Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept 2000;91:21-7.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Deng WX, Henati A., Tanier JA Amyotrophic lateral sclerosis and structural defects in Cu, Zn superoxide dismutase. Science 1993;261:1047-51.[Abstract/Free Full Text]
• Smith MA, Richey-Harris PL, Sayre LM, Beckman JS, Perry G. Widespread peroxynitrite-mediated damage in Alzheimer's disease. J Neurosci 1997;17:2653-7.[Abstract/Free Full Text]
• Zimmerman MC, Lazartigues E., Lang JA et al. Superoxide mediates the actions of angiotensin II in the central nervous system. Circ Res 2002;91:1038-45.[Abstract/Free Full Text]
• Sun C., Sellers KW, Sumners C., Raizada MK NAD(P)H oxidase inhibition attenuates neuronal chronotropic actions of angiotensin II. Circ Res 2005;96:659-66.[Abstract/Free Full Text]
• Erdös B., Broxson CS, King MA, Scarpace PJ, Tümer N. Acute pressor effect of central angiotensin II is mediated by NAD(P)H-oxidase-dependent production of superoxide in the hypothalamic cardiovascular regulatory nuclei. J Hypertens 2006;24:109-16.[Medline] [Order article via Infotrieve]
• Schnackenberg CG, Welch WJ, Wilcox CS Normalization of blood pressure and renal vascular resistance in SHR with a membrane-permeable superoxide dismutase mimetic: role of nitric oxide. Hypertension 1998;32:59-64.[Abstract/Free Full Text]
• Zimmerman MC, Lazartigues E., Sharma RV, Davisson RL Hypertension caused by angiotensin II infusion involves increased superoxide production in the central nervous system. Circ Res 2004;95:210-6.[Abstract/Free Full Text]
• Gao L., Wang W., Li YL et al. Superoxide mediates sympathoexcitation in heart failure: roles of angiotensin II and NAD(P)H oxidase. Circ Res 2004;95:937-44.[Abstract/Free Full Text]
• Campese VM, Shaohua Y., Huiquin Z. Oxidative stress mediates angiotensin II-dependent stimulation of sympathetic nerve activity. Hypertension 2005;46:533-9.[Abstract/Free Full Text]
• Lu N., Helwing BG, Fels RJ et al. Central Tempol alters basal sympathetic nerve discharge and attenuates sympathetic excitation to central Ang II. Am J Physiol Heart Circ Physiol 2004;287:H2626-33.[Abstract/Free Full Text]
• Wang G., Anrather J., Huang J., Speth RC, Pickel VM, Iadecola C. NADPH oxidase contributes to angiotensin II signaling in the nucleus tractus solitarius. J Neurosci 2004;24:5516-24.[Abstract/Free Full Text]
• Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res 1994;74:1141-8.[Abstract/Free Full Text]
• Mohazzab KM, Kaminski PM, Wolin MS NADH oxidoreductase is a major source of superoxide anion in bovine coronary artery endothelium. Am J Physiol 1994;266:H2568-72.[Web of Science][Medline] [Order article via Infotrieve]
• Lindenau J., Noack H., Possel H., Asayarna K., Wolf G. Cellular distribution of superoxide dismutases in the rat CNS. Glia 2000;29:25-34.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Babior BM NADPH oxidase: an update. Blood 1999;93:1464-76.[Free Full Text]
• Pou S., Pou WS, Bredt DS, Snyder SH, Rosen GM Generation of superoxide by purified brain nitric oxide synthase. J Biol Chem 1992;267:24173-6.[Abstract/Free Full Text]
• Atlante A., Calissano P., Bobba A., Giannattasio S., Marra E., Passarella S. Glutamate neurotoxicity, oxidative stress and mitochondria. FEBS Lett 2001;497:1-5.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Gao L., Wang W., Li YL et al. Sympatho-excitation by central Ang II: the roles for AT1 receptor upregulation and NAD(P)H oxidase in the RVLM. Am J Physiol Heart Circ Physiol 2005;288:H2271-9.[Abstract/Free Full Text]
• Richards EM, Raizada MK, Gelband CH, Sumners C. Angiotensin II type 1 receptor-modulated signaling pathways in neurons. Mol Neurobiol 1999;19:25-41.[Web of Science][Medline] [Order article via Infotrieve]
• Sumners C., Fleegal MA, Zhu MY Angiotensin AT-1 receptor signalling pathways in neurons. Clin Exp Pharmacol Physiol 2002;29:483-90.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Chan SH, Hsu KS, Huang CC, Wang LL, Ou CC, Chan JY NADPH oxidase-derived superoxide anion mediates angiotensin II-induced pressor effect via activation of p38 mitogenactivated protein kinase in the rostral ventrolateral medulla. Circ Res 2005;97:772-80.[Abstract/Free Full Text]
• Zimmerman MC, Sharma RV, Davisson RL Superoxide mediates angiotensin II-induced influx of extracellular calcium in neural cells. Hypertension 2005;45:717-23.[Abstract/Free Full Text]
• Mayorov DN, Head GA, De Matteo R. Tempol attenuates excitatory actions of angiotensin II in the rostral ventrolateral medulla during emotional stress. Hypertension 2004;44:101-6.[Abstract/Free Full Text]
• Iannone A., Bini A., Swartz HM, Tomasi A., Vannini V. Metabolism in rat liver microsomes of the nitroxide spin probe tempol. Biochem Pharmacol 1989;38:2581-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Nilsson UA, Olsson LI, Carlin G., Bylund-Fellenius AC Inhibition of lipid peroxidation by spin labels: relationships between structure and function. J Biol Chem 1989; 19:11131-5.
• Mok JS, Paisley K., Martin W. Inhibition of nitrergic neurotransmission in the bovine retractor penis muscle by an oxidant stress: effects of superoxide dismutase mimetics. Br J Pharmacol 1998;124:111-8.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Nishiyama A., Fukui T., Fujisawa Y. et al. Systemic and regional hemodynamic responses to tempol in angiotensin II-infused hypertensive rats. Hypertension 2001;37:77-83.[Abstract/Free Full Text]
• Simpson J., Routtenberg A. Subfornical organ: a dipsogenic site action of angiotensin II. Science 1978;201:379-81.[Free Full Text]
• Sun C., Sumners C., Raizada MK Chronotropic action of angiotensin II in neurons via protein kinase C and CaMKII. Hypertension 2002;39:562-6.[Abstract/Free Full Text]
• Wang D., Gelband CH, Sumners C., Posner P. Mechanisms underlying the chronotropic effect of angiotensin II on cultured neurons from rat hypothalamus and brain stem. J Neurophysiol 1997;78:1013-20.[Abstract/Free Full Text]
• Wang D., Sumners C., Posner P., Gelband CH A-type K+ current in neurons cultured from neonatal rat hypothalamus and brain stem: modulation by angiotensin II. J Neurophysiol 1997;78:1021-9.[Abstract/Free Full Text]
• Sumners C., Zhu M., Gelband CH, Posner P. Angiotensin II type 1 receptor modulation of neuronal K+ and Ca2+ currents: intracellular mechanisms. Am J Physiol Cell Physiol 1996;271:C154-63.[Abstract/Free Full Text]
• Fleegal MA, Sumners C. Drinking behavior elicited by central injection of angiotensin II: roles for protein kinase C and Ca2+/calmodulin dependent protein kinase II. Am J Physiol Regul Integr Comp Physiol 2003;285:632-40.
• Zhu M., Gelband CH, Posner P., Sumners C. Angiotensin II decreases neuronal delayed rectifier potassium current: role of calcium/calmodulin-dependent protein kinase II. J Neurophysiol 1999;82:1560-8.[Abstract/Free Full Text]

Journal of Renin-Angiotensin-Aldosterone System, Vol. 10, No. 1, 9-14 (2009)
DOI: 10.1177/1470320309102946


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This Article Abstract Free Full Text (Free PDF) Free Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Saved Citations Download to citation manager Request Permissions Request Reprints Add to My Marked Citations Citing Articles Citing Articles via Google Scholar Citing Articles via Scopus Google Scholar Articles by Israel, A. Articles by Varela, M. Search for Related Content PubMed PubMed Citation Articles by Israel, A. Articles by Varela, M. Pubmed/NCBI databases Compound via MeSH Substance via MeSH Hazardous Substances DB POTASSIUM SODIUM Social Bookmarking                         What's this?