Review |
From Abteilung für Pharmakologie, Medizinische Fakultät, Ruhr-Universität Bochum, Bochum, Germany.
Correspondence to Doris Koesling, Abteilung für Pharmakologie, Medizinische Fakultät, Ruhr-Universität Bochum, Universitätsstr. 150, 44780 Bochum, Germany. E-mail doris.koesling{at}ruhr-uni-bochum.de
Rudi Busse Editor This Review is part of a thematic series on Cyclic GMP-Generating Enzymes and Cyclic GMP-Dependent Signaling, which includes the following articles:
Regulation of Nitric Oxide-Sensitive Guanylyl Cyclase
Cyclic GMP Phosphodiesterases and Regulation of Smooth Muscle Function
Structure, Regulation, and Function of Membrane Guanylyl Cyclase Receptors, With a Focus on GC-A
Cyclic GMP-Dependent Protein Kinases and the Cardiovascular System: Insights From Genetically Modified Mice
Regulation of Gene Expression by Cyclic GMP
Explaining the Phenomenon of Nitrate Tolerance
In this review, we outline the current knowledge on the regulation of nitric oxide (NO)-sensitive guanylyl cyclase (GC). Besides NO, the physiological activator that binds to the prosthetic heme group of the enzyme, two novel classes of GC activators have been identified that may have broad pharmacological implications. YC-1 and YC-1-like substances act as NO sensitizers, whereas the substance BAY 58-2667 stimulates NO-sensitive GC NO-independently and preferentially activates the heme-free form of the enzyme. Sensitization and desensitization of NO/cGMP signaling have been reported to occur on the level of NO-sensitive GC; in the present study, an alternative mechanism is introduced explaining the adaptation of the NO-induced cGMP response by a long-term activation of the cGMP-degrading phosphodiesterase 5 (PDE5). Finally, regulation of GC expression and a possible modulation of GC activity by other factors are discussed.
Key Words: cyclic GMP guanylyl cyclase nitric oxide phosphodiesterase sensitization/desensitization
This article has been cited by other articles:
![]() |
G. M. Tozer, V. E. Prise, G. Lewis, S. Xie, I. Wilson, and S. A. Hill Nitric Oxide Synthase Inhibition Enhances the Tumor Vascular-Damaging Effects of Combretastatin A-4 3-O-Phosphate at Clinically Relevant Doses Clin. Cancer Res., June 1, 2009; 15(11): 3781 - 3790. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Mayer, A. L. Kleschyov, H. Stessel, M. Russwurm, T. Munzel, D. Koesling, and K. Schmidt Inactivation of Soluble Guanylate Cyclase by Stoichiometric S-Nitrosation Mol. Pharmacol., April 1, 2009; 75(4): 886 - 891. [Abstract] [Full Text] [PDF] |
||||
![]() |
Z. Zhao, Z. Wang, Y. Gu, R. Feil, F. Hofmann, and L. Ma Regulate Axon Branching by the Cyclic GMP Pathway via Inhibition of Glycogen Synthase Kinase 3 in Dorsal Root Ganglion Sensory Neurons J. Neurosci., February 4, 2009; 29(5): 1350 - 1360. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Pokreisz, S. Vandenwijngaert, V. Bito, A. Van den Bergh, I. Lenaerts, C. Busch, G. Marsboom, O. Gheysens, P. Vermeersch, L. Biesmans, et al. Ventricular Phosphodiesterase-5 Expression Is Increased in Patients With Advanced Heart Failure and Contributes to Adverse Ventricular Remodeling After Myocardial Infarction in Mice Circulation, January 27, 2009; 119(3): 408 - 416. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. P. Stice, J. P. Eiserich, and A. A. Knowlton Role of Aging Versus the Loss of Estrogens in the Reduction in Vascular Function in Female Rats Endocrinology, January 1, 2009; 150(1): 212 - 219. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Antosova, A. Strapkova, and T. Turcan Exogenous Irritant-Induced Airway Hyperreactivity and Inhibition of Soluble Guanylyl Cyclase Biol Res Nurs, October 1, 2008; 10(2): 93 - 101. [Abstract] [PDF] |
||||
![]() |
Z. Zhou, N. Sayed, A. Pyriochou, C. Roussos, D. Fulton, A. Beuve, and A. Papapetropoulos Protein Kinase G Phosphorylates Soluble Guanylyl Cyclase on Serine 64 and Inhibits Its Activity Arterioscler. Thromb. Vasc. Biol., October 1, 2008; 28(10): 1803 - 1810. [Abstract] [Full Text] [PDF] |
||||
![]() |
Z. Zhou, A. Pyriochou, A. Kotanidou, G. Dalkas, M. van Eickels, G. Spyroulias, C. Roussos, and A. Papapetropoulos Soluble guanylyl cyclase activation by HMR-1766 (ataciguat) in cells exposed to oxidative stress Am J Physiol Heart Circ Physiol, October 1, 2008; 295(4): H1763 - H1771. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Roy, E. J. Halvey, and J. Garthwaite An Enzyme-linked Receptor Mechanism for Nitric Oxide-activated Guanylyl Cyclase J. Biol. Chem., July 4, 2008; 283(27): 18841 - 18851. [Abstract] [Full Text] [PDF] |
||||
![]() |
S. W. Rabkin and M. Y. C. Tsang The action of nitric oxide to enhance cell survival in chick cardiomyocytes is mediated through a cGMP and ERK1/2 pathway while p38 mitogen-activated protein kinase-dependent pathways do not alter cell death Exp Physiol, July 1, 2008; 93(7): 834 - 842. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Foller, S. Feil, K. Ghoreschi, S. Koka, A. Gerling, M. Thunemann, F. Hofmann, B. Schuler, J. Vogel, B. Pichler, et al. Anemia and splenomegaly in cGKI-deficient mice PNAS, May 6, 2008; 105(18): 6771 - 6776. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. Martina, A. Masha, V. R. Gigliardi, L. Brocato, E. Manzato, A. Berchio, P. Massarenti, F. Settanni, L. Della Casa, S. Bergamini, et al. Long-Term N-Acetylcysteine and L-Arginine Administration Reduces Endothelial Activation and Systolic Blood Pressure in Hypertensive Patients With Type 2 Diabetes Diabetes Care, May 1, 2008; 31(5): 940 - 944. [Abstract] [Full Text] [PDF] |
||||
![]() |
K. S. Murthy Inhibitory Phosphorylation of Soluble Guanylyl Cyclase by Muscarinic m2 Receptors via G{beta}{gamma}-Dependent Activation of c-Src Kinase J. Pharmacol. Exp. Ther., April 1, 2008; 325(1): 183 - 189. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. D. Cropp, T. Komori, J. E. Shima, T. J. Urban, S. W. Yee, S. S. More, and K. M. Giacomini Organic Anion Transporter 2 (SLC22A7) Is a Facilitative Transporter of cGMP Mol. Pharmacol., April 1, 2008; 73(4): 1151 - 1158. [Abstract] [Full Text] [PDF] |
||||
![]() |
B. Kemp-Harper and R. Feil Meeting Report: cGMP Matters Sci. Signal., March 4, 2008; 1(9): pe12 - pe12. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. N. White, E. J. Hamilton, A. Garcia, D. Wang, K. K. M. Chia, G. A. Figtree, and H. H. Rasmussen Opposing effects of coupled and uncoupled NOS activity on the Na+-K+ pump in cardiac myocytes Am J Physiol Cell Physiol, February 1, 2008; 294(2): C572 - C578. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Mastrodimou, F. Kiagiadaki, and K. Thermos The Role of Nitric Oxide and cGMP in Somatostatin's Protection against Retinal Ischemia Invest. Ophthalmol. Vis. Sci., January 1, 2008; 49(1): 342 - 349. [Abstract] [Full Text] [PDF] |
||||
![]() |
D. B. Frank, J. Lowery, L. Anderson, M. Brink, J. Reese, and M. de Caestecker Increased susceptibility to hypoxic pulmonary hypertension in Bmpr2 mutant mice is associated with endothelial dysfunction in the pulmonary vasculature Am J Physiol Lung Cell Mol Physiol, January 1, 2008; 294(1): L98 - L109. [Abstract] [Full Text] [PDF] |
||||
![]() |
V. A. Lira, Q. A. Soltow, J. H. D. Long, J. L. Betters, J. E. Sellman, and D. S. Criswell Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle Am J Physiol Endocrinol Metab, October 1, 2007; 293(4): E1062 - E1068. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. E. Teixeira, F. B. M. Priviero, and R. C. Webb Effects of 5-Cyclopropyl-2-[1-(2-fluoro-benzyl)-1H-pyrazolo[3,4-b]pyridine-3-yl]pyrimidin-4-ylamine (BAY 41-2272) on Smooth Muscle Tone, Soluble Guanylyl Cyclase Activity, and NADPH Oxidase Activity/Expression in Corpus Cavernosum from Wild-Type, Neuronal, and Endothelial Nitric-Oxide Synthase Null Mice J. Pharmacol. Exp. Ther., September 1, 2007; 322(3): 1093 - 1102. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. P. Coggins and K. D. Bloch Nitric Oxide in the Pulmonary Vasculature Arterioscler. Thromb. Vasc. Biol., September 1, 2007; 27(9): 1877 - 1885. [Abstract] [Full Text] [PDF] |
||||
![]() |
N. Sayed, P. Baskaran, X. Ma, F. van den Akker, and A. Beuve Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation PNAS, July 24, 2007; 104(30): 12312 - 12317. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Friebe, E. Mergia, O. Dangel, A. Lange, and D. Koesling Fatal gastrointestinal obstruction and hypertension in mice lacking nitric oxide-sensitive guanylyl cyclase PNAS, May 1, 2007; 104(18): 7699 - 7704. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. Glynos, A. Kotanidou, S. E. Orfanos, Z. Zhou, D. C. M. Simoes, C. Magkou, C. Roussos, and A. Papapetropoulos Soluble guanylyl cyclase expression is reduced in LPS-induced lung injury Am J Physiol Regulatory Integrative Comp Physiol, April 1, 2007; 292(4): R1448 - R1455. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Oberholzer, G. Marti, M. Baresic, S. Kunz, A. Hemphill, and T. Seebeck The Trypanosoma brucei cAMP phosphodiesterases TbrPDEB1 and TbrPDEB2: flagellar enzymes that are essential for parasite virulence FASEB J, March 1, 2007; 21(3): 720 - 731. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. A. Winger, E. R. Derbyshire, and M. A. Marletta Dissociation of Nitric Oxide from Soluble Guanylate Cyclase and Heme-Nitric Oxide/Oxygen Binding Domain Constructs J. Biol. Chem., January 12, 2007; 282(2): 897 - 907. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. M. Bevers, E. E. van Faassen, T. D. Vuong, Z. Ni, P. Boer, H. A. Koomans, B. Braam, N. D. Vaziri, and J. A. Joles Low albumin levels increase endothelial NO production and decrease vascular NO sensitivity Nephrol. Dial. Transplant., December 1, 2006; 21(12): 3443 - 3449. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Pyriochou, D. Beis, V. Koika, C. Potytarchou, E. Papadimitriou, Z. Zhou, and A. Papapetropoulos Soluble Guanylyl Cyclase Activation Promotes Angiogenesis J. Pharmacol. Exp. Ther., November 1, 2006; 319(2): 663 - 671. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Ciani, V. Calvanese, C. Crochemore, R. Bartesaghi, and A. Contestabile Proliferation of cerebellar precursor cells is negatively regulated by nitric oxide in newborn rat J. Cell Sci., August 1, 2006; 119(15): 3161 - 3170. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. E. Teixeira, F. B. M. Priviero, and R. C. Webb Molecular Mechanisms Underlying Rat Mesenteric Artery Vasorelaxation Induced by the Nitric Oxide-Independent Soluble Guanylyl Cyclase Stimulators BAY 41-2272 [5-Cyclopropyl-2-[1-(2-fluorobenzyl)-1H-pyrazolo[3,4-b]pyridin-3-yl]pyrimidin-4-ylamine] and YC-1 [3-(5'-Hydroxymethyl-2'-furyl)-1-benzyl Indazole] J. Pharmacol. Exp. Ther., April 1, 2006; 317(1): 258 - 266. [Abstract] [Full Text] [PDF] |
||||
![]() |
U. Schindler, H. Strobel, K. Schonafinger, W. Linz, M. Lohn, P. A. Martorana, H. Rutten, P. W. Schindler, A. E. Busch, M. Sohn, et al. Biochemistry and Pharmacology of Novel Anthranilic Acid Derivatives Activating Heme-Oxidized Soluble Guanylyl Cyclase Mol. Pharmacol., April 1, 2006; 69(4): 1260 - 1268. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Fischmeister Is cAMP Good or Bad?: Depends on Where It's Made Circ. Res., March 17, 2006; 98(5): 582 - 584. [Full Text] [PDF] |
||||
![]() |
M. J. Burkitt and A. Raafat Nitric oxide generation from hydroxyurea: significance and implications for leukemogenesis in the management of myeloproliferative disorders Blood, March 15, 2006; 107(6): 2219 - 2222. [Abstract] [Full Text] [PDF] |
||||
![]() |
C. J. Mingone, S. A. Gupte, N. Ali, R. A. Oeckler, and M. S. Wolin Thiol oxidation inhibits nitric oxide-mediated pulmonary artery relaxation and guanylate cyclase stimulation Am J Physiol Lung Cell Mol Physiol, March 1, 2006; 290(3): L549 - L557. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Godecke On the impact of NO-globin interactions in the cardiovascular system Cardiovasc Res, February 1, 2006; 69(2): 309 - 317. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Pisconti, S. Brunelli, M. Di Padova, C. De Palma, D. Deponti, S. Baesso, V. Sartorelli, G. Cossu, and E. Clementi Follistatin induction by nitric oxide through cyclic GMP: a tightly regulated signaling pathway that controls myoblast fusion J. Cell Biol., January 17, 2006; 172(2): 233 - 244. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Hofmann, R. Feil, T. Kleppisch, and J. Schlossmann Function of cGMP-Dependent Protein Kinases as Revealed by Gene Deletion Physiol Rev, January 1, 2006; 86(1): 1 - 23. [Abstract] [Full Text] [PDF] |
||||
![]() |
A. Papapetropoulos, D. C. M. Simoes, G. Xanthou, C. Roussos, and C. Gratziou Soluble guanylyl cyclase expression is reduced in allergic asthma Am J Physiol Lung Cell Mol Physiol, January 1, 2006; 290(1): L179 - L184. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Deruelle, T. R. Grover, and S. H. Abman Pulmonary vascular effects of nitric oxide-cGMP augmentation in a model of chronic pulmonary hypertension in fetal and neonatal sheep Am J Physiol Lung Cell Mol Physiol, November 1, 2005; 289(5): L798 - L806. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Munzel, A. Daiber, and A. Mulsch Explaining the Phenomenon of Nitrate Tolerance Circ. Res., September 30, 2005; 97(7): 618 - 628. [Abstract] [Full Text] [PDF] |
||||
![]() |
T. Munzel, A. Daiber, V. Ullrich, and A. Mulsch 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., August 1, 2005; 25(8): 1551 - 1557. [Abstract] [Full Text] [PDF] |
||||
![]() |
C.A. Gunnett, D.D. Lund, A.K. McDowell, F.M. Faraci, and D.D. Heistad Mechanisms of Inducible Nitric Oxide Synthase-Mediated Vascular Dysfunction Arterioscler. Thromb. Vasc. Biol., August 1, 2005; 25(8): 1617 - 1622. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Yang, J. W. Clark, R. M. Bryan, and C. S. Robertson Mathematical modeling of the nitric oxide/cGMP pathway in the vascular smooth muscle cell Am J Physiol Heart Circ Physiol, August 1, 2005; 289(2): H886 - H897. [Abstract] [Full Text] [PDF] |
||||
![]() |
S.-L. Pan, J.-H. Guh, C.-Y. Peng, S.-W. Wang, Y.-L. Chang, F.-C. Cheng, J.-H. Chang, S.-C. Kuo, F.-Y. Lee, and C.-M. Teng YC-1 [3-(5'-Hydroxymethyl-2'-furyl)-1-benzyl Indazole] Inhibits Endothelial Cell Functions Induced by Angiogenic Factors in Vitro and Angiogenesis in Vivo Models J. Pharmacol. Exp. Ther., July 1, 2005; 314(1): 35 - 42. [Abstract] [Full Text] [PDF] |
||||
![]() |
R M McAllister, I Albarracin, E M Price, T K Smith, J R Turk, and K D Wyatt Thyroid status and nitric oxide in rat arterial vessels J. Endocrinol., April 1, 2005; 185(1): 111 - 119. [Abstract] [Full Text] [PDF] |
||||
![]() |
P. Deruelle, T. R. Grover, L. Storme, and S. H. Abman Effects of BAY 41-2272, a soluble guanylate cyclase activator, on pulmonary vascular reactivity in the ovine fetus Am J Physiol Lung Cell Mol Physiol, April 1, 2005; 288(4): L727 - L733. [Abstract] [Full Text] [PDF] |
||||
![]() |
F.-J. Chang, S. Lemme, Q. Sun, R. K. Sunahara, and A. Beuve Nitric Oxide-dependent Allosteric Inhibitory Role of a Second Nucleotide Binding Site in Soluble Guanylyl Cyclase J. Biol. Chem., March 25, 2005; 280(12): 11513 - 11519. [Abstract] [Full Text] [PDF] |
||||
![]() |
L. Moreno, G. Gonzalez-Luis, A. Cogolludo, F. Lodi, A. Lopez-Farre, J. Tamargo, E. Villamor, and F. Perez-Vizcaino Soluble guanylyl cyclase during postnatal porcine pulmonary maturation Am J Physiol Lung Cell Mol Physiol, January 1, 2005; 288(1): L125 - L130. [Abstract] [Full Text] [PDF] |
||||
![]() |
J. Li, X. Hu, P. Selvakumar, R. R. Russell III, S. W. Cushman, G. D. Holman, and L. H. Young Role of the nitric oxide pathway in AMPK-mediated glucose uptake and GLUT4 translocation in heart muscle Am J Physiol Endocrinol Metab, November 1, 2004; 287(5): E834 - E841. [Abstract] [Full Text] [PDF] |
||||
![]() |
O. V. Evgenov, F. Ichinose, N. V. Evgenov, M. J. Gnoth, G. E. Falkowski, Y. Chang, K. D. Bloch, and W. M. Zapol Soluble Guanylate Cyclase Activator Reverses Acute Pulmonary Hypertension and Augments the Pulmonary Vasodilator Response to Inhaled Nitric Oxide in Awake Lambs Circulation, October 12, 2004; 110(15): 2253 - 2259. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Stocker and J. F. Keaney Jr. Role of Oxidative Modifications in Atherosclerosis Physiol Rev, October 1, 2004; 84(4): 1381 - 1478. [Abstract] [Full Text] [PDF] |
||||
![]() |
F. Mullershausen, M. Russwurm, D. Koesling, and A. Friebe In Vivo Reconstitution of the Negative Feedback in Nitric Oxide/cGMP Signaling: Role of Phosphodiesterase Type 5 Phosphorylation Mol. Biol. Cell, September 1, 2004; 15(9): 4023 - 4030. [Abstract] [Full Text] [PDF] |
||||
![]() |
Y. Stasiv, B. Kuzin, M. Regulski, T. Tully, and G. Enikolopov Regulation of multimers via truncated isoforms: a novel mechanism to control nitric-oxide signaling Genes & Dev., August 1, 2004; 18(15): 1812 - 1823. [Abstract] [Full Text] [PDF] |
||||
![]() |
E. Mo, H. Amin, I. H. Bianco, and J. Garthwaite Kinetics of a Cellular Nitric Oxide/cGMP/Phosphodiesterase-5 Pathway J. Biol. Chem., June 18, 2004; 279(25): 26149 - 26158. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Schulz and G. Heusch Connexin 43 and ischemic preconditioning Cardiovasc Res, May 1, 2004; 62(2): 335 - 344. [Abstract] [Full Text] [PDF] |
||||
![]() |
M. Craven, G. P. Sergeant, M. A. Hollywood, N. G. McHale, and K. D. Thornbury Modulation of spontaneous Ca2+-activated Cl- currents in the rabbit corpus cavernosum by the nitric oxide-cGMP pathway J. Physiol., April 15, 2004; 556(2): 495 - 506. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Schulz, M. Kelm, and G. Heusch Nitric oxide in myocardial ischemia/reperfusion injury Cardiovasc Res, February 15, 2004; 61(3): 402 - 413. [Abstract] [Full Text] [PDF] |
||||
![]() |
R. Feil, S. M. Lohmann, H. de Jonge, U. Walter, and F. Hofmann Cyclic GMP-Dependent Protein Kinases and the Cardiovascular System: Insights From Genetically Modified Mice Circ. Res., November 14, 2003; 93(10): 907 - 916. [Abstract] [Full Text] [PDF] |
||||
|
Circulation Research Home | Subscriptions | Archives | Feedback | Authors | Help | AHA Journals Home | Search Copyright © 2003 American Heart Association, Inc. All rights reserved. Unauthorized use prohibited. |