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 Zavala, L. Articles by Israel, A. Search for Related Content PubMed PubMed Citation Articles by Zavala, L. Articles by Israel, A. Social Bookmarking                         What's this?

Neurohumoral mechanism in the natriuretic action of intracerebroventricular administration of renin

School of Medicine, Universidad Experimental Francisco de Miranda, Coro, Estado Falcón

Yarisma Barbella

Laboratory of Neuropeptides, School of Pharmacy, Universidad Central de Venezuela

Anita Israel

Laboratory of Neuropeptides, School of Pharmacy, Universidad Central de Venezuela, astern88{at}hotmail.com

Introduction Intracerebroventricular (IVT) administration of renin (R) decreases urinary volume and increases urinary sodium excretion. We investigated whether IVT-R-induced natriuresis could be associated with the release of atrial natriuretic peptide (ANP), its interaction with renal ANP-A receptors (ANPR-A) and the subsequent increase of urinary cyclic 3'-5' guanosine monophosphate (cGMP).

Methods In IVT cannulated rats, the left carotid artery was catheterised with PE-50 tubing for blood collection, renin was injected IVT and arterial blood samples were collected at 0, 2, 5, 10 and 15 minutes of injection, and urinary sodium and cGMP excretion at 1-, 3- and 6-hour periods of urine collection. Plasma ANP levels and urinary cGMP were determined by radioimmunoassay, and each urine sample was analysed for sodium concentration using a flame photometer.

Results Our results demonstrate that IVT-R administration increases plasma ANP levels after two minutes of injection and urinary cGMP concentration at 1-, 3-and 6 hour period of urine collection. The natriuretic action induced by IVT-R was blunted by peripheral administration of anantin, an ANPR-A antagonist. We assessed the role of brain angiotensin II (Ang II) AT₁-receptors on the IVT-induced antidiuresis, natriuresis and cGMP urinary excretion, the last as an indirect index of ANP secretion. Blockade of brain Ang II AT ₁-receptors with losartan (LOS; 120 µg/3 µl, IVT), inhibited the antidiuretic action and blocked the increased urinary sodium and cGMP excretion induced by IVT-R (7.14 mGU/5 µl). The increase in urinary cGMP was independent of nitric oxide synthase stimulation, since L-NAME pre-treatment did not alter the renal actions induced by IVT-R.

Conclusions Our results suggest that there is a link between the brain and the kidney. The activation of brain angiotensinergic neurons and stimulation of AT₁ receptors may stimulate the release of ANP to the circulation. The released ANP circulates to the kidneys where it acts through renal ANPR-As and the consequent increase in cGMP to produce natriuresis.

Key Words: renin • natriuresis • atrial natriuretic peptide • losartan • GMPc

References

• Veltmar A., Qadri F., Rascher W., Unger T. The angiotensin II induced vasopressin release is mediated through a central catecholaminergic pathway. J Hypertension 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. Neuroendocrinol 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]
• Chang RSL, Lotti VJ, Chen TB, Faust KA Two angiotensin II binding sites in rat brain revealed using [125I]Sar1-Ile-Angiotensin II and selective nonpeptide antagonists. Biochem Biophys Res Commun 1990;171:813-17.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Tsutsumi T., Saavedra JM Characterization and development of angiotensin II receptor subtypes (AT1 and AT2) in rat brain. J Physiol (Regulatory Integrative Com Physiol) 1991;261: R209-16.
• Champion H., Czapla M., Kadowitz P. Responses to angiotensin peptides are mediated by AT1 receptors in the rat. Am J Physiol 1998;274:E115-23.[Web of Science][Medline] [Order article via Infotrieve]
• Barbella Y., Cierco M., Israel A. Effect of losartan a non peptide angiotensin II receptor antagonist, on drinking behavior and renal actions of centrally administered renin. Proc Soc Exp Biol Med 1993;202:401-06.[CrossRef][Medline] [Order article via Infotrieve]
• Sakai RE, Fluharty SJ Intracerebroventricular administration of angiotensin type 1 (AT1) receptor antisense oligonucleotides attenuate thirst in rat. Reg Peptide 1995;59:183-92.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Peng J.-F, Kimura B., Fregly M., Phillips I. Reduction of cold-induced hypertension by antisense oligonucleotides to angiotensin mRNA and AT1-receptor mRNA in brain and blood. Hypertension 1998;31:1317-23.[Abstract/Free Full Text]
• Gohlke P., Kox T., Jurgensen T. et al. Peripheral applied candesartan inhibits central responses to angiotensin II in conscious rats. Naunyn Schmiedebergs Arch Pharmacol 2002;365: 477-83.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Ganten D., Unger T., Lang RE The dual role of angiotensin and vasopressin as plasma hormones and neuropeptides in cardiovascular regulation. J Pharmacol 1985;16:51-68.
• Lang RE,Tholken H., Ganten D., Luft FC, Ruskoaho H., Unger T. Atrial natriuretic factor: a circulating hormone stimulated by volume loading. Nature 1985;314:264-6.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Ruskoaho H. Atrial natriuretic peptide; synthesis, release and metabolism. Pharmacol Rev 1992;44:479-602.[Web of Science][Medline] [Order article via Infotrieve]
• Gutkoswka J., Antunes-Rodrigues J., MacCann SM Atrial natriuretic peptide in brain and pituitary gland. Physiol Rev 1997; 77:465-515.[Abstract/Free Full Text]
• Itoh H., Nakao K., Yamada T. et al. Central interaction of brain atrial natriuretic polypeptide (ANP) system and the brain renin-angiotensin system in ANP secretion from the heart: evidence for possible brain-heart axis. Can J Physiol Pharmacol 1988; 66:255-61.[Web of Science][Medline] [Order article via Infotrieve]
• Soares TJ, Coimbra TM, Martins AR et al. Atrial natriuretic peptide and oxytocin induce natriuresis by release of cGMP. Proc Natl Acad Sci 1999;96:278-83.[Abstract/Free Full Text]
• Kishimoto I., Dubois S., Garbers D. The heart communicates with the kidney exclusively through the guanylyl cyclase-A receptor: acute handling of sodium and water in response to volumen expansion. Proc Natl Acad Sci 1996;93:6215-19.[Abstract/Free Full Text]
• Steiner A., Parker C., Kipnis D. Radioimmunoassay for cyclic nucleotides.JBiol Chem 1972;247:1106-13.[Abstract/Free Full Text]
• Dorn A., Antunes-Rodrigues J., McCann SM Natriuresis in the rat following intraventricular carbachol. American J Physiol 1970;219:1292-8.[Free Full Text]
• McKinley MJ, Denton DA, Coghlan JP et al. Cerebral osmoregulation of renal sodium excretion - a response analogous to thirst and vasopressin release. Canadian J Physiol Pharmacol 1987;65:1724-9.
• McCann SM, Gutkowska J., Antunes-Rodrigues J. Neuroendocrine control of body fluid homeostasis. Brazilian J Med Biol Res 2003;36:165-81.[Web of Science][Medline] [Order article via Infotrieve]
• Antunes-Rodrigues J., Favaretto AL, Ballejo G., Gutkowska J., McCann SMANP as a neuroendocrine modulator of body fluid homeostasis. Rev Bras Biol 1996;56:21-31.[Medline] [Order article via Infotrieve]
• McCann SM, Franci CR, Gutkowska J., Favaretto ALV, Antunes-Rodrigues J. Neural control of atrial natriuretic peptide actions on fluid intake and excretion. Proc Soc Exp Biol Med 1996; 213:117-27.[CrossRef][Medline] [Order article via Infotrieve]
• Favaretto AL, Ballejo GO, Albuquerque-Araujo WIC, Gutkowska J., Antunes-Rodrigues J., McCann M. Oxytocin releases atrial natriuretic peptide from rat atrial in vitro that exerts negative inotropic and chrinotropic action. Peptides 1997; 18:1377-81.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Widecka K., Celibala R., Gozdzik J., Syrenicz A., Ciechanowski K., Czekalski S. Exaggerated natriuresis induced by sodium chloride infusion in essential hypertension is accompanied by an exaggerated urinary 3' 5' guanosine monophosphate excretion. Nephrol Dial Transplant 1993;8:711-15.[Abstract/Free Full Text]
• Valentin JP, Qiu C., Muldowney WP, Ying WZ, Gardner DG, Humphreys MH Cellular basis for blunted volume expansion natriuresis in experimental nephrotic syndrome. J Clin Invest 1992;901:1302-12.
• Anand-Srivastava M., Trachte G. Atrial natriuretic factor receptors and signal transduction mechanisms. Pharmacol Rev 1993;45:455-97.[Web of Science][Medline] [Order article via Infotrieve]
• Wong PC, Hart SD, Zaspel AM et al. Functional studies of nonpeptide angiotensin II receptor subtype-specific ligand: DuP 753 (AII-1) and PD 123177 (AII-2). J Pharm Exp Ther 1990;255:584-92.[Abstract/Free Full Text]
• Gross SS,Wolin MS Nitric oxide: pathophysiological mechanisms. Annu Rev Physiol 1995;57:737-69.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
• Braam B. Renal endothelial and macula densa NOS: integrated response to changes in extracellular fluid volume. Am J Physiol 1999;276:R1551-61.[Web of Science][Medline] [Order article via Infotrieve]

Journal of Renin-Angiotensin-Aldosterone System, Vol. 5, No. 1, 39-44 (2004)
DOI: 10.3317/jraas.2004.007


CiteULike    Complore    Connotea    Del.icio.us    Digg    Reddit    Technorati    Twitter    What's this?

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 Zavala, L. Articles by Israel, A. Search for Related Content PubMed PubMed Citation Articles by Zavala, L. Articles by Israel, A. Social Bookmarking                         What's this?