Abstract
In the vascular system, the receptor for the signaling molecule NO, guanylyl cyclase (GC), mediates smooth muscle relaxation and inhibition of platelet aggregation by increasing intracellular cyclic GMP (cGMP) concentration. The heterodimeric GC exists in 2 isoforms (alpha1-GC, alpha2-GC) with indistinguishable regulatory properties. Here, we used mice deficient in either alpha1- or alpha2-GC to dissect their biological functions. In platelets, alpha1-GC, the only isoform present, was responsible for NO-induced inhibition of aggregation. In aortic tissue, alpha1-GC, as the major isoform (94%), mediated vasodilation. Unexpectedly, alpha2-GC, representing only 6% of the total GC content in WT, also completely relaxed alpha1-deficient vessels albeit higher NO concentrations were needed. The functional impact of the low cGMP levels produced by alpha2-GC in vivo was underlined by pronounced blood pressure increases upon NO synthase inhibition. As a fractional amount of GC was sufficient to mediate vasorelaxation at higher NO concentrations, we conclude that the majority of NO-sensitive GC is not required for cGMP-forming activity but as NO receptor reserve to increase sensitivity toward the labile messenger NO in vivo.
MeSH Terms
Animals
Aorta/cytology,enzymology
Blood Pressure/physiology
Brain/enzymology
Cyclic GMP/metabolism
Gene Targeting
Guanylate Cyclase/metabolism
In Vitro Techniques
Isoenzymes/genetics,metabolism
Lung/enzymology
Mice
Mice, Knockout
Nitric Oxide/metabolism
Protein Subunits/genetics,metabolism
Receptors, Guanylate Cyclase-Coupled/genetics,metabolism
Signal Transduction/physiology
Vasodilation
Chemicals
Isoenzymes
Protein Subunits
Nitric Oxide
Guanylate Cyclase
Receptors, Guanylate Cyclase-Coupled
Cyclic GMP
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Mergia Evanthia
Institut für Pharmakologie und Toxikologie, Ruhr-Universität Bochum, Bochum, Germany.
Friebe Andreas
Dangel Oliver
Russwurm Michael
Koesling Doris
References (30)
30 references, click to expand
-
Guanylyl cyclase/PSD-95 interaction: targeting of the nitric oxide-sensitive alpha2beta1 guanylyl cyclase to synaptic membranes.
J Biol Chem. 2001 Nov 30;276(48):44647-52
PMID: 11572861
-
Upregulation of phosphodiesterase 1A1 expression is associated with the development of nitrate tolerance.
Circulation. 2001 Nov 6;104(19):2338-43
PMID: 11696475
-
Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one.
Mol Pharmacol. 1995 Aug;48(2):184-8
PMID: 7544433
-
Increased nitrovasodilator sensitivity in endothelial nitric oxide synthase knockout mice: role of soluble guanylyl cyclase.
Hypertension. 2000 Jan;35(1 Pt 2):231-6
PMID: 10642303
-
Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme.
EMBO J. 1996 Dec 16;15(24):6863-8
PMID: 9003762
-
Radioimmunoassay of cyclic AMP and cyclic GMP.
Adv Cyclic Nucleotide Res. 1979;10:1-33
PMID: 222120
-
Cyclic GMP phosphodiesterases and regulation of smooth muscle function.
Circ Res. 2003 Aug 22;93(4):280-91
PMID: 12933699
-
Isoforms of NO-sensitive guanylyl cyclase.
Mol Cell Biochem. 2002 Jan;230(1-2):159-64
PMID: 11952091
-
Phosphodiesterase-5A dysregulation in penile erectile tissue is a mechanism of priapism.
Proc Natl Acad Sci U S A. 2005 Feb 1;102(5):1661-6
PMID: 15668387
-
Cyclic nucleotide elevating vasodilators inhibit platelet aggregation at an early step of the activation cascade.
Eur J Pharmacol. 1989 Jan 17;159(3):317-20
PMID: 2537741
-
Molecular mechanisms and therapeutic strategies related to nitric oxide.
FASEB J. 1995 Oct;9(13):1319-30
PMID: 7557022
-
Dopaminergic supersensitivity in G protein-coupled receptor kinase 6-deficient mice.
Neuron. 2003 Apr 24;38(2):291-303
PMID: 12718862
-
Vascular consequences of endothelial nitric oxide synthase uncoupling for the activity and expression of the soluble guanylyl cyclase and the cGMP-dependent protein kinase.
Arterioscler Thromb Vasc Biol. 2005 Aug;25(8):1551-7
PMID: 15879305
-
Major occurrence of the new alpha2beta1 isoform of NO-sensitive guanylyl cyclase in brain.
Cell Signal. 2003 Feb;15(2):189-95
PMID: 12464390
-
Cyclic GMP synthesis and function.
Pharmacol Rev. 1987 Sep;39(3):163-96
PMID: 2827195
-
IRAG is essential for relaxation of receptor-triggered smooth muscle contraction by cGMP kinase.
EMBO J. 2004 Oct 27;23(21):4222-31
PMID: 15483626
-
Vascular reactivity in heart failure: role of myosin light chain phosphatase.
Circ Res. 2004 Sep 17;95(6):612-8
PMID: 15321927
-
Defective smooth muscle regulation in cGMP kinase I-deficient mice.
EMBO J. 1998 Jun 1;17(11):3045-51
PMID: 9606187
-
Regulation of nitric oxide-sensitive guanylyl cyclase.
Circ Res. 2003 Jul 25;93(2):96-105
PMID: 12881475
-
Structure, regulation, and function of mammalian membrane guanylyl cyclase receptors, with a focus on guanylyl cyclase-A.
Circ Res. 2003 Oct 17;93(8):700-9
PMID: 14563709
-
Characteristics of 24 h telemetered blood pressure in eNOS-knockout and C57Bl/6J control mice.
J Physiol. 2003 May 15;549(Pt 1):313-25
PMID: 12665600
-
NO-independent regulatory site on soluble guanylate cyclase.
Nature. 2001 Mar 8;410(6825):212-5
PMID: 11242081
-
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
-
Purification and characterization of NO-sensitive guanylyl cyclase.
Methods Enzymol. 2005;396:492-501
PMID: 16291256
-
Cyclic GMP-dependent protein kinases and the cardiovascular system: insights from genetically modified mice.
Circ Res. 2003 Nov 14;93(10):907-16
PMID: 14615494
-
Physiology and pathophysiology of vascular signaling controlled by guanosine 3',5'-cyclic monophosphate-dependent protein kinase [corrected].
Circulation. 2003 Nov 4;108(18):2172-83
PMID: 14597579
-
Effects of endothelium-derived nitric oxide on peripheral arteriolar tone in man.
Lancet. 1989 Oct 28;2(8670):997-1000
PMID: 2572793
-
Efficient in vivo manipulation of mouse genomic sequences at the zygote stage.
Proc Natl Acad Sci U S A. 1996 Jun 11;93(12):5860-5
PMID: 8650183
-
Endothelium-derived relaxing factor. Identification as nitric oxide and role in the control of vascular tone and platelet function.
Biochem Pharmacol. 1988 Jul 1;37(13):2495-501
PMID: 3291879
-
Nitric oxide as a unique signaling molecule in the vascular system: a historical overview.
J Physiol Pharmacol. 2002 Dec;53(4 Pt 1):503-14
PMID: 12512688