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Soluble guanylyl cyclase: Structure and regulation

  • D. Koesling
  • A. Friebe
Chapter
Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (volume 135)

Keywords

Adenylyl Cyclase Guanylate Cyclase Guanylyl Cyclase Soluble Guanylate Cyclase Soluble Guanylyl Cyclase 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Abiberges N, Hovemadsen L, Fischmeister R, Mery PF (1997) A comparative study of the effects of three guanylyl cyclase inhibitors on the L-type Ca2+ and muscarinic K+ currents in frog. Br J Pharmacol 121:1369–1377Google Scholar
  2. Arnold WP, Mittal CK, Murad F (1977) Nitric oxide activates guanylate cyclase and increases guanosine 3′:5′-cyclic monophosphate levels in various tissue preparations. Proc Natl Acad Sci USA 74:3203–3207Google Scholar
  3. Ashman DF, Lipton R, Melicow MM, Price TD (1963) Isolation of adenosine 3′:5′-monophosphate and guanosine 3′:5′-monophosphate from rat urine. Biochem Biophys Res Commun 11:330–334Google Scholar
  4. Behrends S, Harteneck C, Schultz G, Koesling D (1995) A variant of the α2 subunit of soluble guanylyl cyclase contains an insert homologous to a region within adenylyl cyclases and functions as a dominant negative protein. J Biol Chem 270:21109–21113Google Scholar
  5. Böhme E, Graf H, Schultz G (1978) Effects of sodium nitroprusside and other smooth muscle relaxants on cyclic cGMP formation in smooth muscle and platelets. Adv Cyclic Nucleotide Res 9:131–143Google Scholar
  6. Böhme E, Gerzer R, Grossmann G, Herz J, Mülsch A, Spies C, Schultz G (1983) Regulation of soluble guanylyl cyclase activity. In: Hormones and Cell Regulation Vol. 7 (Dumont JE, Nunez J, Denton RM, eds) Elsevier Biomedical Press, 147–161Google Scholar
  7. Böhme E, Grossmann G, Herz J, Mulsch A, Spies C, Schultz G (1984) Regulation of cyclic GMP formation by soluble guanylate cyclase: stimulation by NO-containing compounds. Adv Cyclic Nucleotide Protein Phosphorylation Res 17:259–266Google Scholar
  8. Brandwein HJ, Lewicki JA, Murad F (1981) Reversible inactivation of guanylate cyclase by mixed disulfide formation. J Biol Chem 256:2958–2962Google Scholar
  9. Braun T, Dods RF (1975) Development of a Mn-2+-sensitive, “soluble” adenylate cyclase in rat testis. Proc Natl Acad Sci USA 72:1097–1101Google Scholar
  10. Brüne B, Ullrich V (1987) Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol Pharmacol 32:497–504Google Scholar
  11. Brüne B, Schmidt K-U, Ullrich V (1990) Activation of soluble guanylate cyclase by carbon monoxide and inhibition by superoxide anion. Eur J Biochem 192:683–686Google Scholar
  12. Brunner F, Schmidt K, Nielsen EB, Mayer B (1996) Novel guanylyl cyclase inhibitor potently inhibits cyclic GMP accumulation in endothelial cells and relaxation of bovine pulmonary artery. J Pharmacol Exp Ther 277:48–53Google Scholar
  13. Buechler WA, Nakane M, Murad F (1991) Expression of soluble guanylate cyclase activity requires both enzyme subunits. Biochem Biophys Res Commun 174:351–357Google Scholar
  14. Burstyn JN, Yu AE, Dierks EA, Hawkins BK, Dawson JH (1995) Studies of the heme coordination and ligand binding properties of soluble guanylyl cyclase (sGC): Characterization of Fe(II)sGC and Fe(II)sGC(CO) by electronic absorption and magnetic circular dichroism spectroscopies and failure of CO to activate the enzyme. Biochemistry 34:5906–5903Google Scholar
  15. Chinkers M, Garbers DL, Chang M-S, Lowe DG, Chin H, Goeddel DV, Schulz S (1989) A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338:78–83Google Scholar
  16. Craven PA, DeRubertis FR (1978) Restoration of the responsiveness of purified guanylate cyclase to nitrosoguanidine, nitric oxide, and related activators by heme and hemeproteins. Evidence for involvement of the paramagnetic nitrosyl-heme complex in enzyme activation. J Biol Chem 253:8433–8443Google Scholar
  17. DeRubertis FR, Craven PA (1977) Activation of hepatic guanylate cyclase by N-methyl-N′-nitro-N-nitrosoguanidine. Effects of thiols, N-ethylmaleimide, and divalent cations. J Biol Chem 252:5804–5814Google Scholar
  18. Dessauer CW, Gilman AG (1996) Purification and characterisation of a soluble form of mammalian adenylyl cyclase. J Biol Chem 271:16967–16974Google Scholar
  19. Dierks EA, Burstyn JN (1996) Nitric oxide (NO), the only nitrogen monoxide redox form capable of activating soluble guanylyl cyclase. Biochem Pharmacol 51:1593–1600Google Scholar
  20. Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D (1996) A functional heme-binding site of soluble guanylyl cyclase requires intact N-termini of a1 and b1 subunits. Eur J Biochem 240:380–386Google Scholar
  21. Friebe A, Malkewitz J, Schultz G, Koesling D (1996a) Positive side-effects of pollution? Nature 382:120Google Scholar
  22. Friebe A, Schultz G, Koesling D (1996b) Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. EMBO J 15:6863–6868Google Scholar
  23. Friebe A, Wedel B, Foerster J, Harteneck C, Malkewitz J, Schultz G, Koesling D (1997) Function of conserved cysteine residues on soluble guanylyl cyclase. Biochemistry 36:1194–1198Google Scholar
  24. Friebe A, Koesling D (1998) Mechanism of YC-1-induced activation of soluble guanylyl cyclase. Mol Pharmacol 53:123–127Google Scholar
  25. Friebe A, Koesling D (1998) Stimulation of soluble guanylyl cyclase by superoxide dismutase is mediated by NO. Biochem 335:527–531Google Scholar
  26. Friebe A, Müllershausen F, Smolenski A, Walter U, Schultz G, Koesling D (1998) YC-1 potentiates NO-and CO-induced cGMP effects in human platelets. Mol Pharmacol 54Google Scholar
  27. Garthwaite J, Charles SL, Chess-Williams R (1988) Endothelium-derived relaxing factor release on activation of NMDA receptors suggests role as intercellular messenger in the brain. Nature 336:385–388Google Scholar
  28. Garthwaite J, Southam E, Boulton CL, Nielsen EB, Schmidt K, Mayer B (1995) Potent and selective inhibition of nitric oxide-sensitive guanylyl cyclase by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ). Mol Pharm 48:185–188Google Scholar
  29. Gerzer R, Böhme E, Hofmann F, Schultz G (1981) Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Letters 132:71–74Google Scholar
  30. Gerzer R, Hofmann F, Schultz G (1981) Purification of a soluble, sodium-nitroprussid-stimulated guanylate cyclase from bovine lung. Eur J Biochem 116:479–486Google Scholar
  31. Giuili G, Scholl U, Bulle F, Guellaen (1992) Molecular cloning of the cDNAs coding for the two subunits of soluble guanylyl cyclase from human brain. FEBS Letters 304:83–88Google Scholar
  32. Goldberg ND, O'Dea RF, Haddox MK (1973) Cyclic GMP. Adv Cycl Nucl Res 3:155–223Google Scholar
  33. Gupta G, Azam M, Yang L, Danziger RS (1997) The β2 subunit inhibits stimulation of the α11 form of soluble guanylyl cyclase by nitric oxide. Potential relevance to regulation of blood pressure. J Clin Invest 100:1488–1492Google Scholar
  34. Hardman JG, Sutherland EW (1969) Guanyl cyclase, an enzyme catalyzing the formation of guanosine 3′,5′-monophosphate from guanosine trihosphate. J Biol Chem 244:6363–6370Google Scholar
  35. Harteneck C, Koesling D, Söling A, Schultz G, Böhme E (1990) Expression of soluble guanylate cyclase: catalytic activity requires two subunits. FEBS Lett 272:221–223Google Scholar
  36. Harteneck C, Wedel B, Koesling D, Malkewitz J, Böhme E, Schultz G (1991) Molecular cloning and expression of a new a-subunit of soluble guanylyl cyclase. FEBS Lett 292:217–222Google Scholar
  37. Hebeiss K, Kilbinger H (1998) Nitric oxide-sensitive guanylyl cyclase inhibits acetylcholine release and excitatory motor transmission in guinea-pig ileum. Neuroscience 82:623–629Google Scholar
  38. Humbert P, Niroomand F, Fischer G, Mayer B, Koesling D, Hinsch KD, Gausepohl H, Frank R, Schultz G, Böhme E (1990) Purification of soluble guanylyl cyclase from bovine lung by a new immunoaffinity chromatographic method. Eur J Biochem 190:273–278Google Scholar
  39. Ignarro LJ, Degnan JN, Baricos WH, Kadowitz PJ, Wolin MS (1982) Activation of purified guanylate cyclase by nitric oxide requires heme. Comparison of heme-deficient, heme-reconstituted and heme-containing forms of soluble enzyme from bovine lung. Biochim Biophys Acta 718:49–59Google Scholar
  40. Ignarro LJ, Wood KS, Wolin MS (1982) Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc Natl Acad Sci USA 79:2870–2873Google Scholar
  41. Ignarro LJ, Adams JB, Horwitz PM, Wood KS (1986) Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange: comparison of heme-containing and heme-deficient enzyme forms. J Biol Chem 261:4997–5002Google Scholar
  42. Ignarro, LJ, Buga GM, Wood KS, Byrns RE, Chandhuri G (1987): Endotheliumderived relaxing factor produced and released from artery and vein is nitric oxide. Proc Natl Acad Sci USA 84:9265–9269Google Scholar
  43. Ishikawa E, Ishikawa S, Davis JW, Sutherland EW (1969) Determination of guanosine 3′,5′-monophosphate in tissues and of guanyl cyclase in rat intestine. J Biol Chem 244:6371–6376Google Scholar
  44. Kharitonov VG, Russwurm M, Magde D, Sharma VS, Koesling D (1997) Dissociation of nitric oxide from soluble guanylyl cyclase. Biochem Biophys Res Commun 239:284–286Google Scholar
  45. Koesling D, Böhme E, Schultz G (1991) Guanylyl cyclases, a growing family of signal transducing enzymes. FASEB J 5:2785–2791Google Scholar
  46. Lincoln TM (1989) Cyclic GMP and mechanisms of vasodilation. Pharmacol Ther 41:479–502Google Scholar
  47. Liu Y, Ruoho AE, Rao VD, Hurley JH (1997) Catalytic mechanism of the adenylyl and guanylyl cyclase: Modeling and mutational analysis. Proc Natl Acad Sci USA 94:13414–13419Google Scholar
  48. Maines MD (1988) Heme oxygenase: function, multiplicity, regulatory mechanism, and clinical applications. FASEB J 2:2257–2568Google Scholar
  49. Maines MD (1997) The heme oxygenase system: a regulator of second messenger gases. Annu Rev Pharmacol Toxicol 37:517–554Google Scholar
  50. Marks GS, Brien JF, Nakatsu KB and McLaughlin E (1991) Does carbon monoxide have a physiological function? Trends Pharmacol Sci 12:185–188Google Scholar
  51. Mikami T, Kusakabe T, Suzuki N (1998) Molecular cloning of cDNAs and expression of mRNAs encoding alpha and beta subunits of soluble guanylyl cyclase from medaka fish Oryzias latipes. Eur J Biochem 253:42–48Google Scholar
  52. Mittal CK, Murad F (1977) Formation of adenosine 3′:5′-monophosphate by preparations of guanylate cyclase from rat liver and other tissues. J Biol Chem 252:3136–3140Google Scholar
  53. Moncada S, Higgs EA (1995) Molecular mechanisms and therapeutic strategies related to nitric oxide. FASEB J 9:1319–1330Google Scholar
  54. Mülsch A, Bauersachs J, Schäfer A, Stasch JP, Kast R, Busse R (1997) Effect of YC-1, an NO-independent, superoxide-sensitive stimulator of soluble guanylyl cyclase, on smooth muscle responsiveness to nitrovasodilators. Br J Pharmacology 120:681–689Google Scholar
  55. Nakane M, Arai K, Saheki S, Kuno T, Buechler W, Murad F (1990) Molecular cloning and expression of cDNAs coding for soluble guanylyl cyclase from rat lung. J Biol Chem 265:16841–16845Google Scholar
  56. O'Dell TJ, Hawkins RD, Kandel ER, Arancio O (1991) Tests of the roles of two diffusible substances in long-term potentiation: evidence for nitric oxide as a possible early retrograde messenger. Proc Natl Acad Sci USA 88:11285–11289Google Scholar
  57. Ohlstein EH, Wood KS, Ignarro LJ (1982) Purification and properties of heme-deficient hepatic soluble guanylate cyclase: effects of heme and other factors on enzyme activation by NO, NO-heme, and protoporphyrin IX. Arch Biochem Biophys 218:187–198Google Scholar
  58. Olesen SP, Drejer J, Axelsson O, Moldt P, Bang L, Nielsen-Kudsk JE, Busse R, Mülsch A (1998) Characterization of NS 2028 as a specific inhibitor of soluble guanylyl cyclase. Br J Pharmacol 123:299–309Google Scholar
  59. Palmer RMJ, Ferrige AG, Moncada S (1987) Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327:524–526Google Scholar
  60. Prabhakar S, Short DB, Scholz NL, Goy MF (1997) Identification of nitric oxide-sensitive and-insensitive forms of cytoplasmatic guanylate cyclase. J Neurochem 69:1650–1660Google Scholar
  61. Russwurm M, Behrends S, Harteneck C, Koesling D (1998) Functional properties of a naturally occurring isoform of soluble guanylyl cyclase. Biochem 335:125–130Google Scholar
  62. Schmidt H, Walter U (1994) NO at work. Cell 78:919–925Google Scholar
  63. Schrammel A, Behrends S, Schmidt K, Koesling D, Mayer B (1996) Characterisation of 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ) as a heme site inhibitor of nitric oxide-sensitive guanylyl cyclase. Mol Pharmacol 50:1–5Google Scholar
  64. Schultz G, Böhme E, Munske K (1969) Guanyl cyclase. Determination of enzyme activity. Life Sci 8:1323–1332Google Scholar
  65. Shah S, Hyde DR (1995) Two Drosophila genes that encode the a and b subunits of the brain soluble guanylyl cyclase. J Biol Chem 270:15368–15376Google Scholar
  66. Stone JR, Marletta MA (1994) Soluble guanylyl cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterisation of the ferrous and ferric states. Biochemistry 33:5636–5640Google Scholar
  67. Stone JR, Marletta MA (1995) Heme stoichiometry of heterodimeric soluble guanylate cyclase. Biochemistry 34:14668–14674Google Scholar
  68. Stone JR, Marletta MA (1998) Synergistic activation of soluble guanylate cyclase by YC-1 and carbon monoxide: implications for the role of cleavage of the iron-histidine bond during activation by nitric oxide. Chem Biol 5:255–261Google Scholar
  69. Sunahara RK, Dessauer CW, Gilman AG (1996) Complexity and diversity of mammalian adenylyl cyclases. Annu Rev Pharmacol Toxicol 36:461–480Google Scholar
  70. Sunahara RK, Beuve A, Tesmer JJG, Sprang SR, Garbers DL, Gilman AG (1998) Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem 273:16332–16338Google Scholar
  71. Tang WJ, Stanzel M, Gilman AG (1995) Truncation and alanine-scanning mutants of type I adenylyl cyclase. Biochemistry 34:14563–14572Google Scholar
  72. Tawata M, Aida K, Noguchi T, Ozaki Y, Kume S, Sasaki H, Chin M, Onaya T (1992) Anti-platelet action of isoliquiritigenin, an aldose reductase inhibitor in licorice. Eur J Pharmacol 212:87–92Google Scholar
  73. Teng CM, Wu CC, Ko FN, Lee FY, Kuo SC (1997) YC-1, a nitric oxide-independent activator of soluble guanylate cyclase, inhibits platelet-rich thrombosis in mice. Eur J Pharmacol 320:161–166Google Scholar
  74. Tesmer JJG, Sunahara RK, Gilman AG, Sprang SR (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with G8α · GTPγS. Science 278:1907–1916Google Scholar
  75. Thompson DK, Garbers DL (1995) Dominant negative mutations of the guanylyl cyclase-A receptor. J Biol Chem 270:425–430Google Scholar
  76. Tomita T, Tsuyama S, Imai Y, Kitagawa T (1997) Purification of bovine soluble guanylate cyclase and ADP-ribosylation on its small subunit by bacterial toxins. J Biochemistry 122:531–536Google Scholar
  77. Tucker CL, Hurley JH, Miller TR, Hurley JB (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci USA 95:5993–5997Google Scholar
  78. Waldman SA, Murad F (1987) Cyclic GMP synthesis and function. Pharmacol Rev 39:163–196Google Scholar
  79. Walter U (1989) Physiological role of cGMP and cGMP-dependent protein kinase in the cardiovascular system. Rev Physiol Biochem Pharmacol 113:42–88Google Scholar
  80. Wedel B, Humbert P, Harteneck C, Foerster J, Malkewitz J, Böhme E, Schultz G, Koesling D (1994) Mutation of His-105 of the β1 subunit yields a nitric oxideinsensitive form of soluble guanylyl cyclase. Proc Natl Acad Sci USA 91:2592–2596Google Scholar
  81. Wedel B, Harteneck C, Foerster J, Friebe A, Schultz G, Koesling D (1995) Functional domains of soluble guanylyl cyclase. J Biol Chem 270:24871–24875Google Scholar
  82. Wegener JW, Nawrath H (1997) Differentiell effects of isoliquiritigenin and YC-1 in rat aortic smooth muscle. Eur J Pharmacol 3203:89–91Google Scholar
  83. White AA, Aurbach GD (1969) Detection of guanyl cyclase in mammalian tissues. Biochim Biophys Acta 191:686–697Google Scholar
  84. Wilson EM, Chinkers M (1995) Identification of sequences mediating guanylyl cyclase dimerisation. Biochemistry 34:4696–4701Google Scholar
  85. Wu CC, Ko FN, Kuo SC, Lee FY, Teng CM (1995) YC-1 inhibited human platelet aggregation through NO-independent activation of soluble guanylate cyclase. Br J Pharmacol 116:1973–1978Google Scholar
  86. Yoshikawa S, Miyamoto I, Aruga J, Furuichi T, Okano H, Mikoshiba K (1993) Isolation of a Drosophila gene encoding a head-specific guanylyl cyclase. J Neurochem 60:1570–1573Google Scholar
  87. Yu S, Avery L, Baude E, Garbers DL (1997) Guanylyl cyclase expression in specific sensory neurons: a new family of chemosensory receptors. Proc Natl Acad Sci USA 94:3384–3387Google Scholar
  88. Yuen PST, Potter LR, Garbers DL (1990) A new form of guanylyl cyclase is preferentially expressed in rat kidney. Biochemistry 29:10872–10878Google Scholar
  89. Zhao Y, Marletta MA (1997) Localization of the heme binding region in soluble guanylate cyclase. Biochemistry 36:15959–15964Google Scholar
  90. Zhao Y, Schelvis JP, Babcock GT, Marletta MA (1998) Identification of histidine 105 in the β1 subunit of soluble guanylate cyclase as the heme proximal ligand. Biochemistry 37:4502–4509Google Scholar
  91. Zhuo M, Hawkins RD (1995) Long-term depression: a learning-related type of synaptic plasticity in the mammalian central nervous system. Rev Neurosci 6:259–277Google Scholar

Copyright information

© Springer-Verlag 1999

Authors and Affiliations

  • D. Koesling
    • 1
  • A. Friebe
    • 1
  1. 1.Institut für PharmakologieFreie Universität BerlinBerlinGermany

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