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Vol. 52, Issue 3, 375-414, September 2000

Guanylyl Cyclases and Signaling by Cyclic GMP

Kimberly A. Lucas, Giovanni M. Pitari, Shiva Kazerounian, Inez Ruiz-Stewart, Jason Park, Stephanie Schulz, Kenneth P. Chepenik and Scott A. Waldman1

Division of Clinical Pharmacology, Departments of Medicine and Biochemistry and Molecular Pharmacology, Thomas Jefferson University, Philadelphia, Pennsylvania (K.A.L., G.M.P., S.K., I.R.-S., J.P., S.S., K.P.C., S.A.W.); and Institute of Pharmacology, University of Catania Medical School, Catania, Italy (G.M.P.)

I. Introduction
II. Guanylyl Cyclases
    A. Molecular Biology
        1. Identification of the Members of the Guanylyl Cyclase Family.
        2. Structure and Location of Guanylyl Cyclase Genes.
        3. Genetic Disorders Associated with Guanylyl Cyclases.
    B. Membrane-Bound Guanylyl Cyclases
        1. Introduction.
        2. Isotypes of Particulate Guanylyl Cyclases.
            a. Natriuretic Peptide Receptors.
            b. Intestinal Peptide Receptor Guanylyl Cyclase.
            c. Orphan Receptor Guanylyl Cyclases.
        3. Structure of Particulate Guanylyl Cyclases.
            a. Extracellular Domain.
                i. Glycosylation of Receptors.
                ii. Cysteines and Oligomerization of Receptors.
            b. Transmembrane Domain.
            c. Juxtamembrane domain.
            d. Kinase Homology Domain.
                i. Structure.
                ii. Kinase Activity.
                iii. Phosphorylation.
            e. Hinge Region.
            f. Catalytic Domain.
                i. Dimerization of Catalytic Domains Is Required for Enzymatic Activity.
                ii. Determinants of Purine Specificity.
                iii. Configuration of the Catalytic Site.
            g. Carboxyl Terminal Tail.
        4. Receptor-Effector Coupling and Particulate Guanylyl Cyclase Function.
            a. Interaction of Ligand and Receptor.
            b. Oligomerization of Receptors.
            c. Regulation by Adenine Nucleotides.
                i. Allosteric Activation of Guanylyl Cyclases by Nucleotides.
                ii. Allosteric Inhibition of Guanylyl Cyclases by Nucleotides.
            d. Kinase Homology Domain.
            e. Phosphorylation and Homologous and Heterologous Desensitization.
            f. Accessory Protein Regulation.
            g. Model for Coupling of Particulate Guanylyl Cyclase Receptor and Effector.
    C. Soluble Guanylyl Cyclase
        1. Subunit Structure and Isotypes of Soluble Guanylyl Cyclase.
        2. Domain Structure.
        3. Regulation of Soluble Guanylyl Cyclase by Ligands.
            a. Nitric Oxide.
            b. Protoporphyrin IX.
            c. Catalytic Mechanism.
            d. Divalent Cations.
III. Cyclic GMP and Cell Signaling
    A. Introduction
    B. Protein Kinases
        1. Cyclic GMP-Dependent Protein Kinases.
        2. Cyclic AMP-Dependent Protein Kinases and Cyclic GMP Signaling.
    C. Cyclic Nucleotide-Gated Channels
    D. Cyclic GMP-Regulated Phosphodiesterases
    E. Cyclic GMP and Cell Physiology
        1. Motility of Vascular Smooth Muscle.
        2. Intestinal Fluid and Electrolyte Homeostasis.
        3. Phototransduction.
IV. Conclusions
Acknowledgments
References

Guanylyl cyclases are a family of enzymes that catalyze the conversion of GTP to cGMP. The family comprises both membrane-bound and soluble isoforms that are expressed in nearly all cell types. They are regulated by diverse extracellular agonists that include peptide hormones, bacterial toxins, and free radicals, as well as intracellular molecules, such as calcium and adenine nucleotides. Stimulation of guanylyl cyclases and the resultant accumulation of cGMP regulates complex signaling cascades through immediate downstream effectors, including cGMP-dependent protein kinases, cGMP-regulated phosphodiesterases, and cyclic nucleotide-gated ion channels. Guanylyl cyclases and cGMP-mediated signaling cascades play a central role in the regulation of diverse (patho)physiological processes, including vascular smooth muscle motility, intestinal fluid and electrolyte homeostasis, and retinal phototransduction. Topics addressed in this review include the structure and chromosomal localization of the genes for guanylyl cyclases, structure and function of the members of the guanylyl cyclase family, molecular mechanisms regulating enzymatic activity, and molecular sequences coupling ligand binding to catalytic activity. A brief overview is presented of the downstream events controlled by guanylyl cyclases, including the effectors that are regulated by cGMP and the role that guanylyl cyclases play in cell physiology and pathophysiology.

1 Address for correspondence: Scott A. Waldman, MD, PhD, FCP, Division of Clinical Pharmacology, Thomas Jefferson University, 132 South 10th St., 1170 Main, Philadelphia, PA 19107. E-mail: scott.waldman{at}mail.tju.edu

0031-6997/00/5203-0375$03.00/0
PHARMACOLOGICAL REVIEWS
Copyright © 2000 by The American Society for Pharmacology and Experimental Therapeutics


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G. M. Pitari, R. I. Baksh, D. M. Harris, P. Li, S. Kazerounian, and S. A. Waldman
Interruption of Homologous Desensitization in Cyclic Guanosine 3',5'-Monophosphate Signaling Restores Colon Cancer Cytostasis by Bacterial Enterotoxins
Cancer Res., December 1, 2005; 65(23): 11129 - 11135.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
P. Krejci, B. Masri, V. Fontaine, P. B. Mekikian, M. Weis, H. Prats, and W. R. Wilcox
Interaction of fibroblast growth factor and C-natriuretic peptide signaling in regulation of chondrocyte proliferation and extracellular matrix homeostasis
J. Cell Sci., November 1, 2005; 118(21): 5089 - 5100.
[Abstract] [Full Text] [PDF]

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 Mol. Pharmacol.Home page
A. Papapetropoulos, Z. Zhou, C. Gerassimou, G. Yetik, R. C. Venema, C. Roussos, W. C. Sessa, and J. D. Catravas
Interaction between the 90-kDa Heat Shock Protein and Soluble Guanylyl Cyclase: Physiological Significance and Mapping of the Domains Mediating Binding
Mol. Pharmacol., October 1, 2005; 68(4): 1133 - 1141.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Meurer, S. Pioch, S. Gross, and W. Muller-Esterl
Reactive Oxygen Species Induce Tyrosine Phosphorylation of and Src Kinase Recruitment to NO-sensitive Guanylyl Cyclase
J. Biol. Chem., September 30, 2005; 280(39): 33149 - 33156.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
M. Christen, B. Christen, M. Folcher, A. Schauerte, and U. Jenal
Identification and Characterization of a Cyclic di-GMP-specific Phosphodiesterase and Its Allosteric Control by GTP
J. Biol. Chem., September 2, 2005; 280(35): 30829 - 30837.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
S. Kazerounian, G. M. Pitari, F. J. Shah, G. S. Frick, M. Madesh, I. Ruiz-Stewart, S. Schulz, G. Hajnoczky, and S. A. Waldman
Proliferative Signaling by Store-Operated Calcium Channels Opposes Colon Cancer Cell Cytostasis Induced by Bacterial Enterotoxins
J. Pharmacol. Exp. Ther., September 1, 2005; 314(3): 1013 - 1022.
[Abstract] [Full Text] [PDF]

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 J. Am. Soc. Nephrol.Home page
S. De Frutos, M. Saura, M. Griera, F. J. Rivero-Vilches, C. Zaragoza, D. Rodriguez-Puyol, and M. Rodriguez-Puyol
Differential Regulation of Soluble Guanylyl Cyclase Expression and Signaling by Collagens: Involvement of Integrin-Linked Kinase
J. Am. Soc. Nephrol., September 1, 2005; 16(9): 2626 - 2635.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Cell Physiol.Home page
F. Golin-Bisello, N. Bradbury, and N. Ameen
STa and cGMP stimulate CFTR translocation to the surface of villus enterocytes in rat jejunum and is regulated by protein kinase G
Am J Physiol Cell Physiol, September 1, 2005; 289(3): C708 - C716.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
R. R. Hodges, M. A. Shatos, R. S. Tarko, J. Vrouvlianis, J. Gu, and D. A. Dartt
Nitric Oxide and cGMP Mediate {alpha}1D-Adrenergic Receptor-Stimulated Protein Secretion and p42/p44 MAPK Activation in Rat Lacrimal Gland
Invest. Ophthalmol. Vis. Sci., August 1, 2005; 46(8): 2781 - 2789.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
M. S. Wolin, M. Ahmad, and S. A. Gupte
Oxidant and redox signaling in vascular oxygen sensing mechanisms: basic concepts, current controversies, and potential importance of cytosolic NADPH
Am J Physiol Lung Cell Mol Physiol, August 1, 2005; 289(2): L159 - L173.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
B. Zhu, S. Strada, and T. Stevens
Cyclic GMP-specific phosphodiesterase 5 regulates growth and apoptosis in pulmonary endothelial cells
Am J Physiol Lung Cell Mol Physiol, August 1, 2005; 289(2): L196 - L206.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
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]

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 J. Biol. Chem.Home page
L. K. Antos, S. E. Abbey-Hosch, D. R. Flora, and L. R. Potter
ATP-independent Activation of Natriuretic Peptide Receptors
J. Biol. Chem., July 22, 2005; 280(29): 26928 - 26932.
[Abstract] [Full Text] [PDF]

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 J. Immunol.Home page
R. Morita, T. Uchiyama, and T. Hori
Nitric Oxide Inhibits IFN-{alpha} Production of Human Plasmacytoid Dendritic Cells Partly via a Guanosine 3',5'-Cyclic Monophosphate-Dependent Pathway
J. Immunol., July 15, 2005; 175(2): 806 - 812.
[Abstract] [Full Text] [PDF]

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 J. Neurophysiol.Home page
R. A. Rose, M. B. Anand-Srivastava, W. R. Giles, and J. S. Bains
C-type Natriuretic Peptide Inhibits L-type Ca2+ Current in Rat Magnocellular Neurosecretory Cells by Activating the NPR-C Receptor
J Neurophysiol, July 1, 2005; 94(1): 612 - 621.
[Abstract] [Full Text] [PDF]

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 J. Pharmacol. Exp. Ther.Home page
A. E. Linder, L. P. McCluskey, K. R. Cole III, K. M. Lanning, and R. C. Webb
Dynamic Association of Nitric Oxide Downstream Signaling Molecules with Endothelial Caveolin-1 in Rat Aorta
J. Pharmacol. Exp. Ther., July 1, 2005; 314(1): 9 - 15.
[Abstract] [Full Text] [PDF]

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 J. Cell Sci.Home page
M. Brackmann, S. Schuchmann, R. Anand, and K.-H. Braunewell
Neuronal Ca2+ sensor protein VILIP-1 affects cGMP signalling of guanylyl cyclase B by regulating clathrin-dependent receptor recycling in hippocampal neurons
J. Cell Sci., June 1, 2005; 118(11): 2495 - 2505.
[Abstract] [Full Text] [PDF]

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 Am. J. Respir. Crit. Care Med.Home page
M. R. Wilkins, G. A. Paul, J. W. Strange, N. Tunariu, W. Gin-Sing, W. A. Banya, M. A. Westwood, A. Stefanidis, L. L. Ng, D. J. Pennell, et al.
Sildenafil versus Endothelin Receptor Antagonist for Pulmonary Hypertension (SERAPH) Study
Am. J. Respir. Crit. Care Med., June 1, 2005; 171(11): 1292 - 1297.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Yamamoto and N. Suzuki
Expression and Function of cGMP-dependent Protein Kinase Type I during Medaka Fish Embryogenesis
J. Biol. Chem., April 29, 2005; 280(17): 16979 - 16986.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. M. Barrett, S. M. Black, H. Todor, R. K. Schmidt-Ullrich, K. S. Dawson, and R. B. Mikkelsen
Inhibition of Protein-tyrosine Phosphatases by Mild Oxidative Stresses Is Dependent on S-Nitrosylation
J. Biol. Chem., April 15, 2005; 280(15): 14453 - 14461.
[Abstract] [Full Text] [PDF]

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 IOVSHome page
I. Sokal, W. J. Dupps, M. A. Grassi, J. Brown Jr, L. M. Affatigato, N. Roychowdhury, L. Yang, S. Filipek, K. Palczewski, E. M. Stone, et al.
A Novel GCAP1 Missense Mutation (L151F) in a Large Family with Autosomal Dominant Cone-Rod Dystrophy (adCORD)
Invest. Ophthalmol. Vis. Sci., April 1, 2005; 46(4): 1124 - 1132.
[Abstract] [Full Text] [PDF]

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 Exp. Biol. Med.Home page
J. Su, P. M. Scholz, and H. R. Weiss
Differential Effects of cGMP Produced by Soluble and Particulate Guanylyl Cyclase on Mouse Ventricular Myocytes
Experimental Biology and Medicine, April 1, 2005; 230(4): 242 - 250.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
A. Weichsel, E. M. Maes, J. F. Andersen, J. G. Valenzuela, T. Kh. Shokhireva, F. A. Walker, and W. R. Montfort
Heme-assisted S-nitrosation of a proximal thiolate in a nitric oxide transport protein
PNAS, January 18, 2005; 102(3): 594 - 599.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. B. Morton
Atypical Soluble Guanylyl Cyclases in Drosophila Can Function as Molecular Oxygen Sensors
J. Biol. Chem., December 3, 2004; 279(49): 50651 - 50653.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Wicher, S. Messutat, C. Lavialle, and B. Lapied
A New Regulation of Non-capacitative Calcium Entry in Insect Pacemaker Neurosecretory Neurons: INVOLVEMENT OF ARACHIDONIC ACID, NO-GUANYLYL CYCLASE/cGMP, AND cAMP
J. Biol. Chem., November 26, 2004; 279(48): 50410 - 50419.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
K. A. Hanafy, E. Martin, and F. Murad
CCT{eta}, a Novel Soluble Guanylyl Cyclase-interacting Protein
J. Biol. Chem., November 5, 2004; 279(45): 46946 - 46953.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
M. M. Gironacci, M. S. Valera, I. Yujnovsky, and C. Pena
Angiotensin-(1-7) Inhibitory Mechanism of Norepinephrine Release in Hypertensive Rats
Hypertension, November 1, 2004; 44(5): 783 - 787.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
D. D. Mruk and C. Y. Cheng
Sertoli-Sertoli and Sertoli-Germ Cell Interactions and Their Significance in Germ Cell Movement in the Seminiferous Epithelium during Spermatogenesis
Endocr. Rev., October 1, 2004; 25(5): 747 - 806.
[Abstract] [Full Text] [PDF]

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 J. Neurosci.Home page
J. C. Ayoob, H.-H. Yu, J. R. Terman, and A. L. Kolodkin
The Drosophila Receptor Guanylyl Cyclase Gyc76C Is Required for Semaphorin-1a-Plexin A-Mediated Axonal Repulsion
J. Neurosci., July 28, 2004; 24(30): 6639 - 6649.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Renal Physiol.Home page
S. Notenboom, D. S. Miller, P. Smits, F. G. M. Russel, and R. Masereeuw
Involvement of guanylyl cyclase and cGMP in the regulation of Mrp2-mediated transport in the proximal tubule
Am J Physiol Renal Physiol, July 1, 2004; 287(1): F33 - F38.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Z. Zhou, S. Gross, C. Roussos, S. Meurer, W. Muller-Esterl, and A. Papapetropoulos
Structural and Functional Characterization of the Dimerization Region of Soluble Guanylyl Cyclase
J. Biol. Chem., June 11, 2004; 279(24): 24935 - 24943.
[Abstract] [Full Text] [PDF]

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 J. Exp. Biol.Home page
K. K. Langlais, J. A. Stewart, and D. B. Morton
Preliminary characterization of two atypical soluble guanylyl cyclases in the central and peripheral nervous system of Drosophila melanogaster
J. Exp. Biol., June 1, 2004; 207(13): 2323 - 2338.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
F. Shi, R. L. Stewart Jr, E. Perez, J. Y.-H. Chen, and P. S. LaPolt
Cell-Specific Expression and Regulation of Soluble Guanylyl Cyclase {alpha}1 and {beta}1 Subunits in the Rat Ovary
Biol Reprod, June 1, 2004; 70(6): 1552 - 1561.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. Gille, G. H. Lushington, T.-C. Mou, M. B. Doughty, R. A. Johnson, and R. Seifert
Differential Inhibition of Adenylyl Cyclase Isoforms and Soluble Guanylyl Cyclase by Purine and Pyrimidine Nucleotides
J. Biol. Chem., May 7, 2004; 279(19): 19955 - 19969.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Dhakshinamoorthy and A. G. Porter
Nitric Oxide-induced Transcriptional Up-regulation of Protective Genes by Nrf2 via the Antioxidant Response Element Counteracts Apoptosis of Neuroblastoma Cells
J. Biol. Chem., May 7, 2004; 279(19): 20096 - 20107.
[Abstract] [Full Text] [PDF]

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 Am. J. Physiol. Heart Circ. Physiol.Home page
R. A. Rose, A. E. Lomax, C. S. Kondo, M. B. Anand-Srivastava, and W. R. Giles
Effects of C-type natriuretic peptide on ionic currents in mouse sinoatrial node: a role for the NPR-C receptor
Am J Physiol Heart Circ Physiol, May 1, 2004; 286(5): H1970 - H1977.
[Abstract] [Full Text] [PDF]

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 HypertensionHome page
X.-H. Jin, H. E. McGrath, J. J. Gildea, H. M. Siragy, R. A. Felder, and R. M. Carey
Renal Interstitial Guanosine Cyclic 3', 5'-Monophosphate Mediates Pressure-Natriuresis Via Protein Kinase G
Hypertension, May 1, 2004; 43(5): 1133 - 1139.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
R. M. Fritsch, D. Saur, M. Kurjak, D. Oesterle, J. Schlossmann, A. Geiselhoringer, F. Hofmann, and H.-D. Allescher
InsP3R-associated cGMP Kinase Substrate (IRAG) Is Essential for Nitric Oxide-induced Inhibition of Calcium Signaling in Human Colonic Smooth Muscle
J. Biol. Chem., March 26, 2004; 279(13): 12551 - 12559.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
Q. Huai, Y. Liu, S. H. Francis, J. D. Corbin, and H. Ke
Crystal Structures of Phosphodiesterases 4 and 5 in Complex with Inhibitor 3-Isobutyl-1-methylxanthine Suggest a Conformation Determinant of Inhibitor Selectivity
J. Biol. Chem., March 26, 2004; 279(13): 13095 - 13101.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. Muller, A. K. Mukhopadhyay, R. C. Speth, G. Guidone, R. Potthast, L. R. Potter, and R. Middendorff
Spatiotemporal Regulation of the Two Atrial Natriuretic Peptide Receptors in Testis
Endocrinology, March 1, 2004; 145(3): 1392 - 1401.
[Abstract] [Full Text] [PDF]

Home page
 Mol. Pharmacol.Home page
S. H. H. Chan, K.-F. Chang, C.-C. Ou, and J. Y. H. Chan
Nitric Oxide Regulates c-fos Expression in Nucleus Tractus Solitarii Induced by Baroreceptor Activation via cGMP-Dependent Protein Kinase and cAMP Response Element-Binding Protein Phosphorylation
Mol. Pharmacol., February 1, 2004; 65(2): 319 - 325.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
N. P.Y. Lee and C. Y. Cheng
Nitric Oxide/Nitric Oxide Synthase, Spermatogenesis, and Tight Junction Dynamics
Biol Reprod, February 1, 2004; 70(2): 267 - 276.
[Abstract] [Full Text] [PDF]


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