Aging Increases Neuronal Nitric Oxide Release and Superoxide Anion Generation in Mesenteric Arteries from Spontaneously Hypertensive Rats

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Abstract

We hypothesized that neuronal NO release as well as its bioavailability and vasomotor response could be affected when aging and hypertension are present simultaneously. The neuronal nitric oxide (NO) release, its metabolism and vasomotor response induced by electrical field stimulation was analyzed in isolated segments of endothelium-denuded mesenteric arteries from young and old spontaneously hypertensive rats (SHR). The nitric oxide synthase (NOS) inhibitor NG-nitro-arginine-methyl ester ( L-NAME) and NOS inhibitor 7-nitroindazole both strengthened electrical field stimulation-elicited contractions more in arteries from young than aged SHR rats. Superoxide dismutase (SOD) potentiated the L-NAME effect in segments from old rats, whereas catalase decreased the contractions induced by electrical field stimulation and noradrenaline but did not modify the L-NAME effect. In noradrenaline-precontracted segments, sodium nitroprusside induced a similar relaxation in arteries from both experimental groups. This relaxation was increased by SOD in old SHR. 8Br cGMP induced greater relaxation in segments from old than from young SHR. Electrical field stimulation induced a tritium release in arteries preincubated with [3H]-noradrenaline, that was similar in both young and old SHR rats. Electrical field stimulation induced NO2– formation, which was greater in segments from old than young SHR rats. Basal cGMP levels and those stimulated with sodium nitroprusside were similar in segments from both groups. Superoxide anion production was greater from old than young SHR rats. Peroxynitrite production induced by electrical field stimulation was only detected in segments from old SHR. The results obtained in mesenteric arteries from old SHR showed increased neuronal NO release and superoxide anion production with respect to those observed in arteries from young SHR rats. This induced decreased NO bioavailability through peroxynitrite formation. The final effect is to decrease the involvement of neuronal NO in electrical field stimulation-induced vasomotor response in arteries from old SHR rats.

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Most cited references 22

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Oxidative pathways in cardiovascular disease: roles, mechanisms, and therapeutic implications.

Suvara K. Wattanapitayakul, Ashley Bauer (2001)

Despite some recent declines, cardiovascular disease (CVD) remains the major cause of death in the United States and worldwide. Most recent advances in the treatment of CVD states have been produced by inhibition of mechanisms involved in disease progress. Many studies conducted in the last decade have illustrated increased biological oxidative pathways during CVD in animals and humans. Thus, increased production of reactive oxygen species may be a unifying mechanism in CVD progression, and antioxidants may have therapeutic value in this setting. In this review we address the following questions: Do oxidative mechanisms play a role in CVD? Where do the oxidants come from? What are the relevant oxidative events? What are the therapeutic implications?

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NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling.

Petra Rocic, R. Hanna, Katalin Szöcs … (2002)

Angiotensin II has been shown to participate in both physiological processes, such as sodium and water homeostasis and vascular contraction, and pathophysiological processes, including atherosclerosis and hypertension. The effects of this molecule on vascular tissue are mediated at least in part by the modification of the redox milieu of its target cells. Angiotensin II has been shown to activate the vascular NAD(P)H oxidase(s) resulting in the production of reactive oxygen species, namely superoxide and hydrogen peroxide. In this article, we review what is known about the molecular steps that link angiotensin II and its receptor to production of reactive oxygen species and subsequent redox-mediated events, focusing on the structural and functional properties of the vascular NAD(P)H oxidases and their downstream mediators. As such, we provide a framework linking angiotensin II to crucial vascular pathologies, such as hypertension, atherosclerosis, and restenosis after angioplasty, by means of the NAD(P)H-dependent oxidases and their effector molecules.

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Vasodilator dysfunction in aged spontaneously hypertensive rats: changes in NO synthase III and soluble guanylyl cyclase expression, and in superoxide anion production.

G Wiemer, R. Busse, Nicholas Fleming … (1998)

Genetic hypertension is associated with an apparent endothelial dysfunction and impaired endothelium-dependent vasodilatation in response to increased flow and receptor-dependent agonists. However, the link between impaired vasodilatation and nitric oxide (NO) synthase expression is still unclear. In the present study, dilator responses were determined in the aorta and coronary circulation of 16 month old spontaneously hypertensive (SHR) and Wistar Kyoto rats (WKY). Changes in vascular reactivity were compared with alterations in superoxide anion production as well as endothelial NO synthase (NOS III) and soluble guanylyl cyclase expression. In the isolated perfused heart both the bradykinin- and sodium nitroprusside-induced vasodilator responses were attenuated in SHR compared to WKY. Western blot analysis revealed a parallel reduction in NOS III expression in coronary microvascular endothelial cells from SHR. Superoxide anion production in aortae from SHR was markedly elevated over that of aortae from WKY, and was almost completely abolished by pretreatment with superoxide dismutase. Superoxide dismutase induced similar relaxations in phenylephrine-preconstricted aortic rings from both SHR and WKY, but failed to restore the attenuated acetylcholine- and sodium nitroprusside-induced relaxations in SHR. No difference in NOS III expression was detected in the aortae from either strain whereas soluble guanylyl cyclase expression was markedly decreased in SHR. These results demonstrate that NOS III expression in different tissues is differentially affected by hypertension. Moreover, although an elevated superoxide anion production is apparent in the aorta, a reduced soluble guanylyl cyclase expression appears to account for the observed vasodilator dysfunction in SHR.

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Author and article information

Journal

Journal ID (publisher-id): JVR

Journal ID (nlm-ta): J Vasc Res

Journal ID (doi): 10.1159/issn.1018-1172

Title: Journal of Vascular Research

Publisher: S. Karger AG

ISSN (Print): 1018-1172

ISSN (Electronic): 1423-0135

Publication date Subscription-year: 2003

Publication date (Print): December 2003

Publication date (Electronic): 29 January 2004

Volume: 40

Issue: 6

Pages: 509-519

Affiliations

Departamentos de ^aFisiología and ^bFarmacología y Terapeútica, Facultad de Medicina, Universidad Autónoma de Madrid, Madrid, Spain

Article

Publisher ID: 75183 Other ID: J Vasc Res 2003;40:509–519

DOI: 10.1159/000075183

PubMed ID: 14646371

SO-VID: 3cef0239-e9f2-46cc-a1b3-2b7d21f3e8c5

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Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher. Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug. Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.

History

Date received : 15 November 2002

Date accepted : 04 September 2003

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Figures: 8, Tables: 1, References: 63, Pages: 11

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Aging Increases Neuronal Nitric Oxide Release and Superoxide Anion Generation in Mesenteric Arteries from Spontaneously Hypertensive Rats

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Karger: Cardiovascular System

Most cited references 22

Oxidative pathways in cardiovascular disease: roles, mechanisms, and therapeutic implications.

NAD(P)H oxidase-derived reactive oxygen species as mediators of angiotensin II signaling.

Vasodilator dysfunction in aged spontaneously hypertensive rats: changes in NO synthase III and soluble guanylyl cyclase expression, and in superoxide anion production.

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