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Particulate guanylyl cyclases: multiple mechanisms of activation.

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Cyclic GMP (cGMP), a key messenger in several signal transduction pathways, is synthesized from GTP by a family of enzymes termed guanylyl cyclases, which are found in two forms: cytosolic (soluble) and membrane-bound (particulate). The past decade has brought significant progress in understanding the molecular mechanisms that underlie the regulation of particulate guanylyl cyclases and new members of their family have been identified. It has become more evident that the basic mechanism of catalysis of guanylyl cyclases is analogous to that recognized in adenylyl cyclases. Here we review the known basic mechanisms that contribute to the regulation of particulate guanylyl cyclases.

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  • Laboratory of Signaling Proteins, Institute of Immunology and Experimental Therapy, Polish Academy of Sciences, R. Weigla 12, 53-114 Wrocław, Poland
  • Department of Biogenic Amines, Polish Academy of Sciences, Łódź, Poland
  • Aparicio, J.G. & Applebury, M.L. (1996) The photoreceptor guanylate cyclase is an autophosphorylating protein kinase. J. Biol. Chem. 271, 27083-27089.
  • Bakre, M.M., Ghanekar, Y. & Visweswariah, S.S. (2000) Homologous desensitization of the human guanylate cyclase C receptor. Cell specific regulation of catalytic activity. Eur. J. Biochem. 267, 179-187.
  • Beavo, J.A. (1995) Cyclic nucleotide phosphodiesterases: Functional implications of multiple isoforms. Physiol. Rev. 75, 725-748.
  • Braunewell, K.H. & Gundelfinger, E.D. (1999) Intracellular neuronal calcium sensor proteins: A family of EF-hand calcium-binding proteins in search of a function. Cell Tissue Res. 295, 1-12.
  • Chen, H.H. & Burnett, J.C., Jr. (1998) C-type natriuretic peptide: The endothelial component of the natriuretic peptide system. J. Cardiovasc. Pharmacol. 32 (Suppl. 3), S22-S28.
  • Chinkers, M. & Garbers, D.L. (1989) The protein kinase domain of the ANP receptor is required for signalling. Science 245, 1392-1394.
  • Chinkers, M., Garbers, D.L., Chang, M.S., Lowe, D.L., Chin, H., Goeddel, D.V. & Schulz, S. (1989) A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338, 78-83.
  • Chinkers, M., Singh, S. & Garbers, D.L. (1991) Adenine nucleotides are required for activation of rat atrial natriuretic peptide receptor/ guanylyl cyclase expressed in a baculovirus system. J. Biol. Chem. 266, 4088-4093.
  • Dittman, A.H., Quinn, T.P., Nevitt, G.A., Hacker, B. & Storm, D.R. (1997) Sensitization of olfactory guanylyl cyclase to a specific imprinted odorant in coho salmon. Neuron 19, 381-389.
  • Dizhoor, A.M., Lowe, D.G., Olshevskaya, E.V., Laura, R.P. & Hurley, J.B. (1994) The human photoreceptor membrane guanylyl cyclase, RetGC, is present in outer segment and is regulated by calcium and a soluble activator. Neuron 12, 1345-1352.
  • Dizhoor, A.M., Olshevskaya, E.M., Henzel, W.J., Wong, S.C., Stults, J.T., Ankoudinova, I. & Hurley, J.M. (1995) Cloning, sequencing, and expressing of a 24-kDa Ca2+-binding protein activating photoreceptor guanylyl cyclase. J. Biol. Chem. 270, 25200-25206.
  • Drewett, J.G. & Garbers, D.L. (1994) The family of guanylyl cyclase receptors: Their ligands, and functions. Endocr. Rev. 15, 135-162.
  • Drewett, J.G., Fendly, B.M., Garbers, D.L. & Lowe, D.G. (1995) Natriuretic peptide receptor-B (guanylyl cyclase-B) mediates C-type natriuretic peptide relaxation of precontracted rat aorta. J. Biol. Chem. 270, 4668-4674.
  • Duda, T., Goraczniak, R.M. & Sharma, R.K. (1993a) Core sequence of ATP regulatory module in receptor guanylate cyclases. FEBS Lett. 315, 143-148.
  • Duda, T., Goraczniak, R.M., Sitaramayya, A. & Sharma, R.K. (1993b) Cloning and expression of an ATP-regulated human retina C-type natriuretic factor receptor guanylate cyclase. Biochemistry 32, 1391-1395.
  • Duda, T., Goraczniak, R., Surgucheva, I., Rudnicka-Nawrot, M., Gorczyca, W.A., Palczewski, K., Sitaramayya, A., Baehr, W. & Sharma, R.K. (1996) Calcium modulation of bovine photoreceptor guanylate cyclase. Biochemistry 35, 8478-8482.
  • Eckstein, F., Romaniuk, P.J., Heideman, W. & Storm, D.R. (1981) Stereochemistry of the mammalian adenylate cyclase reaction. J. Biol. Chem. 256, 9118-9120.
  • Finn, J.T., Grunwald, M.E. & Yau, K.W. (1996) Cyclic nucleotide-gated channels: An extended family with diverse functions. Annu. Rev. Physiol. 58, 395-426.
  • Fülle, H.J., Vassar, R., Foster, D.C., Yang, R.B., Axel, R. & Garbers, D.L. (1995) A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons. Proc. Natl. Acad. Sci. U.S.A. 92, 3571-3575.
  • Garbers, D.L. & Lowe, D.G. (1994) Guanylyl cyclase receptors. J. Biol. Chem. 269, 30741-30744.
  • Gazzano, H., Wu, H.I. & Waldman, S.A. (1991a) Adenine nucleotide regulation of particulate guanylate cyclase from rat lung. Biochim. Biophys. Acta 1077, 99-106.
  • Gazzano, H., Wu, H.I. & Waldman, S.A. (1991b) Activation of particulate guanylate cyclase by Escherichia coli heat-stable enterotoxin is regulated by adenine nucleotides. Infect. Immun. 59, 1552-1557.
  • Goraczniak, R.M., Duda, T. & Sharma, R.K. (1992) A structural motif that defines the ATP-regulatory module of guanylate cyclase in atrial natriuretic factor signalling. Biochem. J. 282, 533-537.
  • Goraczniak, R.M., Duda, T., Sitaramayya, A. & Sharma, R.K. (1994) Structural and functional characterization of the rod outer segment membrane guanylate cyclase. Biochem. J. 302, 455-461.
  • Goraczniak, R.M., Duda, T. & Sharma, R.K. (1997) Structural and functional characterization of a second subfamily member of the calcium- modulated bovine rod outer segment membrane guanylate cyclase, ROS-GC2. Biochem. Biophys. Res. Commun. 234, 666-670.
  • Gorczyca, W.A. (1999) Role of calcium ions in vertebrate phototransduction. Pol. J. Pharmacol. 51, 167-172.
  • Gorczyca, W.A. (2000) Use of nucleoside a-phosphorothioates in studies of photoreceptor guanylyl cyclase: Purification of guanylyl cyclase- activating proteins. Methods Enzymol. 315, 689-707.
  • Gorczyca, W.A., Gray-Keller, M.P., Detwiler, P.B. & Palczewski, K. (1994a) Purification and physiological evaluation of a guanylate cyclase activating protein from retinal rods. Proc. Natl. Acad. Sci. U.S.A. 91, 4014-4018.
  • Gorczyca, W.A., Van Hooser, J.P. & Palczewski, K. (1994b) Nucleotide inhibitors and activators of retinal guanylyl cyclase. Biochemistry 33, 3217-3222.
  • Gorczyca, W.A., Polans, A.S., Surgucheva, I., Subbaraya, I., Baehr, W. & Palczewski, K. (1995) Guanylyl cyclase-activating protein: A calcium -sensitive regulator of phototransduction. J. Biol. Chem. 270, 22029-22036.
  • Haeseleer, F., Sokal, I., Li, N., Pettenati, M., Rao, N., Bronson, D., Wechter, R., Baehr, W. & Palczewski, K. (1999) Molecular characterization of a third member of the guanylyl cyclase- activating protein subfamily. J. Biol. Chem. 274, 6526-6535.
  • Huo, X., Abe, T. & Misono, K.S. (1999) Ligand binding-dependent limited proteolysis of the atrial natriuretic peptide receptor: Juxtamembrane hinge structure essential for transmembrane signal transduction. Biochemistry 38, 16941-16951.
  • Hurley, J.E. (1998) The adenylyl and guanylyl cyclase superfamily. Curr. Opin. Struct. Biol. 8, 770-777.
  • Khare, S., Wilson, D.M., Tien, X.Y., Wali, R.K., Bissonnette, M. & Brasitus, T.A. (1994) Protein kinase C mediates the calcium-induced activation of rat colonic particulate guanylate cyclase. Arch. Biochem. Biophys. 314, 200- 204.
  • Kiemer, A.K. & Vollmar, A.M. (1998) Autocrine regulation of inducible nitric-oxide synthase in macrophages by atrial natriuretic peptide. J. Biol. Chem. 273, 13444-13451.
  • Koch, K.W., Eckstein, F. & Stryer, L. (1990) Stereochemical course of the reaction catalysed by guanylate cyclase from bovine retinal rod outer segments. J. Biol. Chem. 265, 9659-9663.
  • Koch, K.W. & Stryer, L. (1988) Highly cooperative feedback control of retinal rod guanylate cyclase by calcium ions. Nature 334, 64-66.
  • Koesling, D. (1998) Modulators of soluble guanylyl cyclase. Naunyn-Schmiedeberg's Arch. Pharmacol. 358, 123-126.
  • Koutalos, Y., Nakatani, K., Tamura, T. & Yau, K.W. (1995) Characterization of guanylate cyclase activity in single retinal rod outer segments. J. Gen. Physiol. 106, 863-890.
  • Krause, W.J., London, R.M., Freeman, R.H. & Forte, L.R. (1997) The guanylin and uroguanylin peptide hormones and their receptors. Acta Anat. 160, 213-231.
  • Krylov, D.M, Niemi, G.A., Dizhoor, A.M. & Hurley, J.B. (1999) Mapping sites in guanylyl cyclase activating-1 required for regulation of photoreceptor membrane guanylyl cyclases. J. Biol. Chem. 274, 10833-10839.
  • Kumar, V.D., Vijaj-Kumar, S., Krishnan, A., Duda, T. & Sharma, R.K. (1999) A second calcium regulator of rod outer segment membrane guanylate cyclase, ROS-GC1: Neurocalcin. Biochemistry 38, 12614-12620.
  • Kurose, H., Inagami, T. & Ui, M. (1987) Participation of adenosine 5'-triphosphate in the activation of membrane-bound guanylate cyclase by the atrial natriuretic factor. FEBS Lett. 219, 375-379.
  • Labrecque, J., Mc Nicoll, N., Marquis, M. & De Lean, A. (1999) A disulfide-bridged mutant of natriuretic peptide receptor-A displays constitutive activity. Role of receptor dimerization in signal transduction. J. Biol. Chem. 274, 9752-9759.
  • Laura, R.P., Dizhoor, A.M. & Hurley, J.B. (1996) The membrane guanylyl cyclase, retinal guanylyl cyclase-1, is activated through its intracellular domain. J. Biol. Chem. 271, 11646-11651.
  • Laura, R.P. & Hurley, J.B. (1998) The kinase homology domain of retinal guanylyl cyclases 1 and 2 specifies the affinity and cooperativity of interaction with guanylyl cyclase activating protein-2. Biochemistry 37, 11264-11271.
  • Lohmann, S.Z., Vaandrager, A.B., Smolenski, A., Walter, U. & De Jonge, H.R. (1997) Distinct and specific functions of cGMP-dependent protein kinases. Trends Biochem. Sci. 22, 307- 312.
  • Lolley, R.N. & Racz, E. (1982) Calcium modulation of cyclic GMP synthesis in rat visual cells. Vision Res. 22, 1481-1486.
  • Lowe, D.G. (1992) Human natriuretic peptide receptor-A guanylyl cyclase is self-associated prior to hormone binding. Biochemistry 31, 10421-10425.
  • Lowe, D.G., Dizhoor, A.M., Liu, K., Gu, Q., Spencer, M., Laura, R., Lu, L. & Hurley, J.B. (1995) Cloning and expression of a second photoreceptor-specific membrane retina guanylyl cyclase (RetGC), RetGC2. Proc. Natl. Acad. Sci. U.S.A. 92, 5535-5539.
  • Margulis, A., Pozdnyakov, N. & Sitaramayya, A. (1996) Activation of bovine photoreceptor guanylate cyclase by S100 proteins. Biochem. Biophys. Res. Commun. 218, 243-247.
  • Moon, C., Jaberi, P., Otto-Bruc, A., Baehr, W., Palczewski, K. & Ronnet, G.V. (1998) Calcium- sensitive particulate cyclase as a modulator of cAMP in olfactory receptor neurons. J. Neurosci. 18, 3195-3205.
  • Müller, D., Olcese, J., Mukhopadhyay, A.K. & Middendorff, R. (2000) Guanylyl cyclase-B represents the predominant natriuretic peptide receptor expressed at exceptionally high levels in the pineal gland. Mol. Brain Res. 75, 321-329.
  • O'Dorisio, M.S., Fertel, R., Finkler, E., Brooks, R. & Vassalo, L. (1984) Characterization of cyclic nucleotide metabolism during human monocyte differentiation. J. Leukoc. Biol. 35, 617- 630.
  • Olshevskaya, E.V., Boikov, S., Ermilov, A., Krylov, D., Hurley, J.B. & Dizhoor, A.M. (1999a) Mapping functional domains of the guanylate cyclase regulator protein, GCAP-2. J. Biol. Chem. 274, 10823-10832.
  • Olshevskaya, E.V., Ermilov, A.N. & Dizhoor, A.M. (1999b) Dimerization of guanylyl cyclase-activating proteins and mechanism of photoreceptor guanylyl cyclase activation. J. Biol. Chem. 274, 25583-25587.
  • Otto-Bruc, A., Buczyłko, J., Syrgucheva, I., Subbaraya, I., Rudnicka-Nawrot, M., Crabb, J.W., Arendt, A., Hargrave, P.A., Baehr, W. & Palczewski, K. (1997) Functional reconstitution of photoreceptor guanylate cyclase with native and mutant forms of guanylate cyclase- activating protein 1. Biochemistry 36, 4295- 4302.
  • Palczewski, K., Subbaraya, I., Gorczyca, W.A., Helekar, B.S., Ruiz, C.C., Ohguro, H., Huang, J., Zhao, X., Crabb, J.W., Johnson, R.S., Walsh, K.A., Gray-Keller, M.P., Detwiler, P.B. & Baehr, W. (1994) Molecular cloning and characterization of retinal guanylyl cyclase-activating protein. Neuron 13, 395-404.
  • Parkinson, S.J., Carrithers, S.L. & Waldman, S.A. (1994) Opposing adenine nucleotide-dependent pathways regulate guanylyl cyclase C in rat intestine. J. Biol. Chem. 269, 22683-22690.
  • Potter, L.R. (1998) Phosphorylation-dependent regulation of the guanylyl cyclase-linked natriuretic peptide receptor B: Dephosphorylation is a mechanism of desensitization. Biochemistry 37, 2422-2429.
  • Potter, L.R. & Hunter, T. (1998) Phosphorylation of kinase homology domain is essential for activation of the A-type natriuretic receptor. Mol. Cell. Biol. 18, 2164-2172.
  • Pozdnyakov, N., Yoshida, A., Cooper, N.G.F., Margulis, A., Duda, T., Sharma, R.K. & Sitaramayya, A. (1995) A novel calcium-dependent activator of retinal rod outer segment membrane guanylate cyclase. Biochemistry 34, 14279-14283.
  • Pugh, E.N., Duda, T., Sitaramayya, A. & Sharma, R.K. (1997) Photoreceptor guanylate cyclases: A review. Biosci. Rep. 17, 429-473.
  • Rosenzweig, A. & Seidman, C.E. (1991) Atrial natriuretic factor and related peptide hormones. Annu. Rev. Biochem. 60, 229-255.
  • Rudner, X.L., Mandal, K.K., De Sauvage, F.J., Kindman, L.A. & Almenof, J.S. (1995) Regulation of cell signaling by the cytoplasmic domains of the heat-stable enterotoxin receptor: identification of autoinhibitory and activating motifs. Proc. Natl. Acad. Sci. U.S.A. 92, 5169-5173.
  • Schmidt, H.H., Lohmann, S.M. & Walter, U. (1993) The nitric oxide and cGMP signal transduction system: Regulation and mechanism of action. Biochem. Biophys. Acta 1178, 153-175.
  • Schrem, A., Lange, C., Beyermann, M. & Koch, K.W. (1999) Identification of a domain in guanylyl cyclase-activating protein 1 that interacts with a complex of guanylyl cyclase and tubulin in photoreceptors. J. Biol. Chem. 274, 6244-6249.
  • Schulz, S., Green, C.K., Yuen, P.S.T. & Garbers, D.L. (1990) Guanylyl cyclase is a heat-stable enterotoxin receptor. Cell 63, 941-948.
  • Schulz, S., Singh, S., Bellet, R.E., Singh, G., Tubb, D.J., Chin, H. & Garbers, D.L. (1989) The primary structure of a plasma membrane guanylate cyclase demonstrates diversity within this new receptor family. Cell 58, 1155-1162.
  • Schulz, S., Wedel, B.J., Matthews, A. & Garbers, D.L. (1998) The cloning and expression of a new guanylyl cyclase orphan receptor. J. Biol. Chem. 273, 1032-1037.
  • Semple-Rowland, S.L., Larkin, P., Bronson, J.D., Nykamp, K., Streit, W.J. & Baehr, W. (1999) Characterization of the chicken GCAP gene array and analyses of GCAP1, GCAP2, and GC1 gene expression in normal and rd chicken pineal. Molecular Vision 5, 14.
  • Senter, P.D., Eckstein, F., Mülsch, A. & Böme, E. (1983) The stereochemical course of the reaction catalysed by soluble bovine lung guanylate cyclase. J. Biol. Chem. 258, 6741-6745.
  • Shyjan, A.W., de Sauvage, F.J., Gillette, N.A., Goeddel, D.V. & Lowe, D.G. (1992) Molecular cloning of a retina-specific membrane guanylyl cyclase. Neuron 9, 727-737.
  • Singh, S., Lowe, D.G., Thorpe, D.S., Rodriguez, H., Kuang, W.J., Goeddel, D.V. & Garbers, D.L. (1988) Membrane guanylate cyclase is a cell-surface receptor with homology to protein kinases. Nature 334, 708-712.
  • Sokal, I., Haeseleer, F., Arendt, A., Adman, E.T., Hargrave, P.A. & Palczewski, K. (1999) Identification of a guanylyl cyclase-activating protein-binding site within the catalytic domain of retinal guanylyl cyclase 1. Biochemistry 38, 1387-1393.
  • Tang, E.J. & Hurley, J.H. (1998) Catalytic mechanism and regulation of mammalian adenylyl cyclases. Mol. Pharmacol. 54, 231-240.
  • Tucker, C.L., Laura, R.P. & Hurley, J.B. (1997) Domain-specific stabilization of photoreceptor membrane guanylyl cyclase by adenine nucleotides and guanylyl cyclase activating proteins (GCAPs). Biochemistry 36, 11995-12000.
  • Tucker, C.L., Woodcock, S.C., Kelsell, R.E., Ramamurthy, V., Hunt, D.M. & Hurley, J.B. (1999) Biochemical analysis of a dimerization domain mutation in RetGC-1 associated with dominant cone-rod dystrophy. Proc. Natl. Acad. Sci. U.S.A. 96, 9039-9044.
  • Vaandrager, A.B., Van der Wiel, E. & De Jonge, H.R. (1993) Heat-stable enterotoxin activation of immunopurified guanylyl cyclase C. Modulation by adenine nucleotides. J. Biol. Chem. 268, 19598-19603.
  • Vaandrager, A.B., Van der Wiel, E., Hom, M.L., Luthjens, L.H. & De Jonge, H.R. (1994) Heat-stable enterotoxin receptor/guanylyl cyclase C is an oligomer consisting of functionally distinct subunits, which are non-covalently linked in the intestine. J. Biol. Chem. 269, 16409-16415.
  • Venkataraman, V., Duda, T. & Sharma, R.K. (1998) The α2D/A-adrenergic receptor-linked membrane guanylate cyclase: A new signal transduction system in the pineal gland. FEBS Lett. 427, 69-73.
  • Venkataraman, V., Nagele, R., Duda, T. & Sharma, R.K. (2000) Rod outer segment membrane guanylate cyclase type 1-linked stimulatory and inhibitory calcium signaling system in the pineal gland: Biochemical, molecular, and immunohistochemical evidence. Biochemistry 39, 6042-6052.
  • Waldman, S.A., Barber, M., Pearlman, J., Park, J., George, R. & Parkinson, S.J. (1998) Heterogeneity of guanylyl cyclase C expressed by human colorectal cancer cell lines in vitro. Cancer Epidemiol. Biomarkers Prevention 7, 505-514.
  • Wedel, B.J. & Garbers, D.L. (1998) Guanylyl cyclases: Approaching year thirty. Trends Endocrinol. Metabolism 9, 213-219.
  • Wilson, E.M. & Chinkers, M. (1995) Identification of sequences mediating guanylyl cyclase dimerization. Biochemistry 34, 4696-4701.
  • Yang, R.B., Foster, D.C., Garbers, D.L. & Fuelle, H.J. (1995) Two membrane forms of guanylyl cyclase found in the eye. Proc. Natl. Acad. Sci. U.S.A. 92, 602-606.
  • Yang, R.B. & Garbers, D.L. (1997) Two eye guanylyl cyclases are expressed in the same photoreceptor cells and form homomers in preference to heteromers. J. Biol. Chem. 272, 13738-13742.
  • Yu, S., Avery, L., Baude, E. & Garbers, D.L. (1997) Guanylyl cyclase expression in specific sensory neurons: A new family of chemosensory receptors. Proc. Natl. Acad. Sci. U.S.A. 94, 3384-3387.
  • Yu, H., Olshevskaya, E., Duda, T., Seno, K., Hayashi, F., Sharma, R.K., Dizhoor, A.M. & Yamazaki, A. (1999) Activation of retinal guanylyl cyclase-1 by Ca2+-binding proteins involves its dimerization. J. Biol. Chem. 274, 15547-15555.
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