Abstract
(1) The sensitivity of the particulate guanylate cyclase-cyclic guanosine-3',5'-monophosphate (cGMP) system to atrial (ANP) and C-type (CNP) natriuretic peptides was investigated in aortae and mesenteric small arteries from wild-type (WT) and endothelial nitric oxide synthase (eNOS) knockout (KO) mice. (2) ANP and CNP produced concentration-dependent relaxations of mouse aorta that were significantly attenuated by the natriuretic peptide receptor (NPR)-A/B antagonist HS-142-1 (10(-5) M). Both ANP and CNP were more potent in aortae from eNOS KO mice compared to WT. (3) The potency of ANP and CNP in aortae from WT animals was increased in the presence of the NOS inhibitor, N(G)-nitro-L-arginine (3 x 10(-4) M) and the soluble guanylate cyclase inhibitor 1H-[1,2,4]oxadiazolol[4,3,a]quinoxalin-1-one (5 x 10(-6) M). (4) In contrast, the potency of ANP and CNP in aortae from eNOS KO animals was reduced following pretreatment of tissues with supramaximal concentrations of the NO-donor, glyceryl trinitrate (3 x 10(-5) M, 30 min) or ANP (10(-7) M, 30 min). (5) Responses to acetylcholine in aortae from WT mice (dependent on the release of endothelium-derived NO) were significantly reduced following pretreatment of tissues with GTN (3 x 10(-5) M, 30 min) and ANP (10(-7) M, 30 min). (6) CNP and the NO-donor, spermine-NONOate caused concentration-dependent relaxations of mesenteric small arteries from WT animals that were significantly increased in eNOS KO mice compared to WT. ANP was unable to significantly relax mesenteric arteries from WT or eNOS KO animals. (7) In conclusion, both NPR-A- and NPR-B-linked pGC pathways are modulated by NO-cGMP in murine aorta and mesenteric small arteries and crossdesensitisation occurs between NPR subtypes. The biological activity of endothelium-derived NO is also influenced by the ambient concentration of NO and natriuretic peptides. Such an autoregulatory pathway may represent an important physiological homeostatic mechanism and link the paracrine activity of NO and CNP with the endocrine functions of ANP and BNP in the regulation of vascular tone and blood pressure.
MeSH Terms
15-Hydroxy-11 alpha,9 alpha-(epoxymethano)prosta-5,13-dienoic Acid/antagonists & inhibitors,pharmacology
Acetylcholine/pharmacology
Animals
Aorta, Thoracic/drug effects,physiology
Atrial Natriuretic Factor/antagonists & inhibitors,pharmacology
Cyclic GMP/metabolism,physiology
Dose-Response Relationship, Drug
Drug Antagonism
Drug Synergism
Guanylate Cyclase/antagonists & inhibitors,physiology
Male
Mesenteric Arteries/drug effects,physiology
Mice
Mice, Inbred Strains
Mice, Knockout
Muscle Relaxation/drug effects
NG-Nitroarginine Methyl Ester/pharmacology
Natriuretic Peptide, C-Type/antagonists & inhibitors,pharmacology
Nitric Oxide/physiology
Nitric Oxide Synthase/physiology
Nitrogen Oxides
Nitroglycerin/pharmacology
Oxadiazoles/antagonists & inhibitors,pharmacology
Phenylephrine/antagonists & inhibitors,pharmacology
Polysaccharides/pharmacology
Quinoxalines/antagonists & inhibitors,pharmacology
Receptors, Atrial Natriuretic Factor/drug effects,physiology
Signal Transduction/physiology
Spermine/analogs & derivatives,pharmacology
Chemicals
1H-(1,2,4)oxadiazolo(4,3-a)quinoxalin-1-one
HS 142-1
Nitrogen Oxides
Oxadiazoles
Polysaccharides
Quinoxalines
Natriuretic Peptide, C-Type
spermine nitric oxide complex
Phenylephrine
Spermine
Nitric Oxide
15-Hydroxy-11 alpha,9 alpha-(epoxymethano)prosta-5,13-dienoic Acid
Atrial Natriuretic Factor
Nitric Oxide Synthase
Guanylate Cyclase
Receptors, Atrial Natriuretic Factor
Nitroglycerin
Cyclic GMP
Acetylcholine
NG-Nitroarginine Methyl Ester
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Madhani Melanie
Wolfson Institute for Biomedical Research, University College London, Cruciform Building, Gower Street, London WC1E 6AE.
Scotland Ramona S
MacAllister Raymond J
Hobbs Adrian J
References (28)
28 references, click to expand
-
Autoregulation of nitric oxide-soluble guanylate cyclase-cyclic GMP signalling in mouse thoracic aorta.
Br J Pharmacol. 1999 Nov;128(5):1082-8
PMID: 10556946
-
C-type natriuretic peptide: the endothelial component of the natriuretic peptide system.
J Cardiovasc Pharmacol. 1998;32 Suppl 3:S22-8
PMID: 9883743
-
Nitric oxide-sensitive guanylyl cyclase activity inhibition through cyclic GMP-dependent dephosphorylation.
J Neurochem. 2000 Nov;75(5):2029-39
PMID: 11032892
-
Reciprocal regulation of cGMP-mediated vasorelaxation by soluble and particulate guanylate cyclases.
Am J Physiol Heart Circ Physiol. 2001 Mar;280(3):H1151-9
PMID: 11179059
-
Molecular biology of natriuretic peptides and nitric oxide synthases.
Cardiovasc Res. 2001 Aug 15;51(3):429-41
PMID: 11476733
-
The renal urodilatin system: clinical implications.
Cardiovasc Res. 2001 Aug 15;51(3):450-62
PMID: 11476735
-
Identification of the G protein-activating domain of the natriuretic peptide clearance receptor (NPR-C).
J Biol Chem. 1999 Jun 18;274(25):17587-92
PMID: 10364194
-
Contractile properties of small arterial resistance vessels in spontaneously hypertensive and normotensive rats.
Circ Res. 1977 Jul;41(1):19-26
PMID: 862138
-
Evidence for phosphorylation of rat brain guanylate cyclase by cyclic AMP-dependent protein kinase.
Biochem Biophys Res Commun. 1981 Aug 31;101(4):1381-7
PMID: 6118147
-
Atrial natriuretic factor elicits an endothelium-independent relaxation and activates particulate guanylate cyclase in vascular smooth muscle.
Proc Natl Acad Sci U S A. 1984 Dec;81(23):7661-4
PMID: 6150486
-
Protein kinase C catalyzes phosphorylation of guanylate cyclase in vitro.
J Biol Chem. 1985 Feb 10;260(3):1350-3
PMID: 2857174
-
Physiological role of silent receptors of atrial natriuretic factor.
Science. 1987 Oct 30;238(4827):675-8
PMID: 2823385
-
A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor.
Nature. 1989 Mar 2;338(6210):78-83
PMID: 2563900
-
Microbial polysaccharide, HS-142-1, competitively and selectively inhibits ANP binding to its guanylyl cyclase-containing receptor.
Biochem Biophys Res Commun. 1991 May 15;176(3):949-57
PMID: 1674870
-
Nitric oxide: physiology, pathophysiology, and pharmacology.
Pharmacol Rev. 1991 Jun;43(2):109-42
PMID: 1852778
-
Dephosphorylation of the guanylyl cyclase-A receptor causes desensitization.
J Biol Chem. 1992 Jul 25;267(21):14531-4
PMID: 1353076
-
Endothelial production of C-type natriuretic peptide and its marked augmentation by transforming growth factor-beta. Possible existence of "vascular natriuretic peptide system".
J Clin Invest. 1992 Sep;90(3):1145-9
PMID: 1522222
-
Presence of C-type natriuretic peptide in cultured human endothelial cells and plasma.
Am J Physiol. 1992 Oct;263(4 Pt 2):H1318-21
PMID: 1384363
-
Natriuretic peptide receptor-B (guanylyl cyclase-B) mediates C-type natriuretic peptide relaxation of precontracted rat aorta.
J Biol Chem. 1995 Mar 3;270(9):4668-74
PMID: 7876238
-
Hypertension in mice lacking the gene for endothelial nitric oxide synthase.
Nature. 1995 Sep 21;377(6546):239-42
PMID: 7545787
-
Role of atrial natriuretic factor in volume control.
Kidney Int. 1996 Jun;49(6):1732-7
PMID: 8743487
-
Soluble guanylate cyclase: the forgotten sibling.
Trends Pharmacol Sci. 1997 Dec;18(12):484-91
PMID: 9458697
-
Phosphorylation-dependent regulation of the guanylyl cyclase-linked natriuretic peptide receptor B: dephosphorylation is a mechanism of desensitization.
Biochemistry. 1998 Feb 24;37(8):2422-9
PMID: 9485390
-
Identification and characterization of the major phosphorylation sites of the B-type natriuretic peptide receptor.
J Biol Chem. 1998 Jun 19;273(25):15533-9
PMID: 9624142
-
Nitric oxide in the human cardiovascular system--SKB lecture 1997.
Br J Clin Pharmacol. 1998 May;45(5):433-9
PMID: 9643614
-
Natriuretic peptides.
N Engl J Med. 1998 Jul 30;339(5):321-8
PMID: 9682046
-
Chronic regulation of arterial blood pressure by ANP: role of endogenous vasoactive endothelial factors.
Am J Physiol. 1998 Nov;275(5 Pt 2):H1826-33
PMID: 9815091
-
G(i-1)/G(i-2)-dependent signaling by single-transmembrane natriuretic peptide clearance receptor.
Am J Physiol Gastrointest Liver Physiol. 2000 Jun;278(6):G974-80
PMID: 10859228