Tonic Stimulation of Renin Gene Expression by Nitric Oxide is Counteracted by Tonic Inhibition Through Angiotensin II

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1995 Aug 15

PMID 7644529

Citations 7

Authors

K Schricker

I Hegyi

M Hamann

B Kaissling

A Kurtz

Affiliations

Soon will be listed here.

Abstract

This study was designed to examine the possible involvement of prostaglandins and nitric oxide (NO) in the renin stimulatory effect of angiotensin II (AngII) antagonists. To this end, plasma renin activities (PRAs) and renal renin mRNA levels were assayed in rats that were treated with the Ang-converting enzyme inhibitor ramipril or with the AngII AT1-receptor antagonist losartan. Ramipril and losartan increased PRA values from 7.5 +/- 1.6 to 86 +/- 6 and 78 +/- 22 ng of AngI per h per ml and renin mRNA levels from 112 +/- 9% to 391 +/- 20% and 317 +/- 10%, respectively. Inhibition of prostaglandin formation with indomethacin did not influence basal or ramipril-affected PRA. Basal renin mRNA levels also were unchanged by indomethacin, while increases in renin mRNA levels after ramipril treatment were slightly reduced by indomethacin. Inhibition of NO synthase by nitro-L-arginine methyl ester (L-NAME) reduced PRA values to 3.2 +/- 0.9, 34 +/- 13, and 12.1 +/- 2.7 ng of AngI per h per ml in control, ramipril-treated, and losartan-treated animals, respectively. Renin mRNA levels were reduced to 77 +/- 14% under basal conditions and ramipril- and losartan-induced increases in renin mRNA levels were completely blunted after addition of L-NAME. The AngII antagonists, furthermore, induced an upstream recruitment of renin-expressing cells in the renal afferent arterioles, which was also blunted by L-NAME. These findings suggest that renin mRNA levels are tonically increased by NO and that the action of NO is counteracted by AngII.

Citing Articles

Endothelium-derived nitric oxide supports renin cell recruitment through the nitric oxide-sensitive guanylate cyclase pathway.

Neubauer B, Machura K, Kettl R, Lopez M, Friebe A, Kurtz A Hypertension. 2013; 61(2):400-7.

PMID: 23297374 PMC: 4037755. DOI: 10.1161/HYPERTENSIONAHA.111.00221.

Regulation of renin secretion by renal juxtaglomerular cells.

Friis U, Madsen K, Stubbe J, Hansen P, Svenningsen P, Bie P Pflugers Arch. 2012; 465(1):25-37.

PMID: 22733355 DOI: 10.1007/s00424-012-1126-7.

Role of cGMP-kinase II in the control of renin secretion and renin expression.

Wagner C, Pfeifer A, Ruth P, Hofmann F, Kurtz A J Clin Invest. 1998; 102(8):1576-82.

PMID: 9788971 PMC: 509008. DOI: 10.1172/JCI4044.

Stimulation of renin secretion by nitric oxide is mediated by phosphodiesterase 3.

Kurtz A, Gotz K, Hamann M, Wagner C Proc Natl Acad Sci U S A. 1998; 95(8):4743-7.

PMID: 9539809 PMC: 22561. DOI: 10.1073/pnas.95.8.4743.

Coordinate changes of renin and brain-type nitric-oxide-synthase (b-NOS) mRNA levels in rat kidneys.

Schricker K, Potzl B, Hamann M, Kurtz A Pflugers Arch. 1996; 432(3):394-400.

PMID: 8765998 DOI: 10.1007/s004240050150.

References

Radermacher J, Forstermann U, Frolich J . Endothelium-derived relaxing factor influences renal vascular resistance. Am J Physiol. 1990; 259(1 Pt 2):F9-17. DOI: 10.1152/ajprenal.1990.259.1.F9. View

Gardes J, Gonzalez M, Alhenc-Gelas F, Menard J . Influence of sodium diet on L-NAME effects on renin release and renal vasoconstriction. Am J Physiol. 1994; 267(5 Pt 2):F798-804. DOI: 10.1152/ajprenal.1994.267.5.F798. View

TAUGNER R, HACKENTHAL E, Helmchen U, Ganten D, Kugler P, Nobiling R . The intrarenal renin-angiotensin-system. An immunocytochemical study on the localization of renin, angiotensinogen, converting enzyme and the angiotensins in the kidney of mouse and rat. Klin Wochenschr. 1982; 60(19):1218-22. DOI: 10.1007/BF01716726. View

McIntyre T, Zimmerman G, Satoh K, Prescott S . Cultured endothelial cells synthesize both platelet-activating factor and prostacyclin in response to histamine, bradykinin, and adenosine triphosphate. J Clin Invest. 1985; 76(1):271-80. PMC: 423763. DOI: 10.1172/JCI111957. View

Nakamura N, Soubrier F, Menard J, Panthier J, Rougeon F, Corvol P . Nonproportional changes in plasma renin concentration, renal renin content, and rat renin messenger RNA. Hypertension. 1985; 7(6 Pt 1):855-9. DOI: 10.1161/01.hyp.7.6.855. View

MOFFETT R, McGowan R, Gross K . Modulation of kidney renin messenger RNA levels during experimentally induced hypertension. Hypertension. 1986; 8(10):874-82. DOI: 10.1161/01.hyp.8.10.874. View

Scherf H, PIETSCH R, Landsberg G, Kramer H, Dusing R . Converting enzyme inhibitor ramipril stimulates prostacyclin synthesis by isolated rat aorta: evidence for a kinin-dependent mechanism. Klin Wochenschr. 1986; 64(16):742-5. DOI: 10.1007/BF01734341. View

Ludwig G, Ganten D, Murakami K, Fasching U, HACKENTHAL E . Relationship between renin mRNA and renin secretion in adrenalectomized, salt-depleted, or converting enzyme inhibitor-treated rats. Mol Cell Endocrinol. 1987; 50(3):223-9. DOI: 10.1016/0303-7207(87)90020-7. View

Chomczynski P, Sacchi N . Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987; 162(1):156-9. DOI: 10.1006/abio.1987.9999. View

10.

Burnham C, Frank B, Lynch K . Molecular cloning of rat renin cDNA and its gene. Proc Natl Acad Sci U S A. 1987; 84(16):5605-9. PMC: 298911. DOI: 10.1073/pnas.84.16.5605. View

11.

Gomez R, Lynch K, Chevalier R, Everett A, Johns D, Wilfong N . Renin and angiotensinogen gene expression and intrarenal renin distribution during ACE inhibition. Am J Physiol. 1988; 254(6 Pt 2):F900-6. DOI: 10.1152/ajprenal.1988.254.6.F900. View

12.

Vidal M, Romero J, Vanhoutte P . Endothelium-derived relaxing factor inhibits renin release. Eur J Pharmacol. 1988; 149(3):401-2. DOI: 10.1016/0014-2999(88)90679-6. View

13.

Makrides S, Mulinari R, Zannis V, Gavras H . Regulation of renin gene expression in hypertensive rats. Hypertension. 1988; 12(4):405-10. DOI: 10.1161/01.hyp.12.4.405. View

14.

Dawson T, Gandhi R, Le Hir M, Kaissling B . Ecto-5'-nucleotidase: localization in rat kidney by light microscopic histochemical and immunohistochemical methods. J Histochem Cytochem. 1989; 37(1):39-47. DOI: 10.1177/37.1.2535703. View

15.

Luckhoff A, Pohl U, Mulsch A, Busse R . Differential role of extra- and intracellular calcium in the release of EDRF and prostacyclin from cultured endothelial cells. Br J Pharmacol. 1988; 95(1):189-96. PMC: 1854120. DOI: 10.1111/j.1476-5381.1988.tb16564.x. View

16.

Samani N, Godfrey N, Major J, Brammar W, Swales J . Kidney renin mRNA levels in the early and chronic phases of two-kidney, one clip hypertension in the rat. J Hypertens. 1989; 7(2):105-12. View

17.

Nakamura A, Iwao H, Fukui K, Kimura S, Tamaki T, Nakanishi S . Regulation of liver angiotensinogen and kidney renin mRNA levels by angiotensin II. Am J Physiol. 1990; 258(1 Pt 1):E1-6. DOI: 10.1152/ajpendo.1990.258.1.E1. View

18.

Todd P, Benfield P . Ramipril. A review of its pharmacological properties and therapeutic efficacy in cardiovascular disorders. Drugs. 1990; 39(1):110-35. DOI: 10.2165/00003495-199039010-00009. View

19.

Johns D, Peach M, Gomez R, Inagami T, Carey R . Angiotensin II regulates renin gene expression. Am J Physiol. 1990; 259(6 Pt 2):F882-7. DOI: 10.1152/ajprenal.1990.259.6.F882. View

20.

Rees D, Palmer R, Schulz R, HODSON H, Moncada S . Characterization of three inhibitors of endothelial nitric oxide synthase in vitro and in vivo. Br J Pharmacol. 1990; 101(3):746-52. PMC: 1917753. DOI: 10.1111/j.1476-5381.1990.tb14151.x. View