Structures of soluble guanylate cyclase: Implications for regulatory mechanisms and drug development

Biochemical Society Transactions

Volumn 42, Issue 1, 2014, Pages 108-113

  Gileadi, Opher ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Allosteric regulation; CGMP; Guanylate cyclase; Hypertension; Nitric oxide; Vasodilation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIC GMP; DIMER; GUANOSINE TRIPHOSPHATE; GUANYLATE CYCLASE; HEME; HETERODIMER; NITRIC OXIDE;

ALLOSTERISM; ANGINA PECTORIS; ARTICLE; CARDIOVASCULAR DISEASE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STRUCTURE; HEART FAILURE; HUMAN; HYPERTENSION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN TARGETING; PULMONARY HYPERTENSION; REGULATORY MECHANISM;

ALLOSTERIC REGULATION; ANIMALS; CARDIOVASCULAR DISEASES; CATALYTIC DOMAIN; DRUG DISCOVERY; GUANYLATE CYCLASE; HUMANS; PROTEIN STRUCTURE, SECONDARY;

EID: 84893299291     PISSN: 03005127     EISSN: 14708752     Source Type: Journal    
DOI: 10.1042/BST20130228     Document Type: Article

References (42)

1. Martin, E., Berka, V., Tsai, A.L. and Murad, F. (2005) Soluble guanylyl cyclase: the nitric oxide receptor. Methods Enzymol. 396, 478-492
2. Murad, F. (2011) Nitric oxide: the coming of the second messenger. Rambam Maimonides Med. J. 2, e0038
3. Mujoo, K., Sharin, V.G., Martin, E., Choi, B.K., Sloan, C., Nikonoff, L.E., Kots, A.Y. and Murad, F. (2010) Role of soluble guanylyl cyclase-cyclic GMP signaling in tumor cell proliferation. Nitric Oxide 22, 43-50
4. Ruiz-Stewart, I., Tiyyagura, S.R., Lin, J.E., Kazerounian, S., Pitari, G.M., Schulz, S., Martin, E., Murad, F. and Waldman, S.A. (2004) Guanylyl cyclase is an ATP sensor coupling nitric oxide signaling to cell metabolism. Proc. Natl. Acad. Sci. U.S.A. 101, 37-42
5. American Gastroenterological Association (2003) American Gastroenterological Association medical position statement: diagnosis and care of patients with anal fissure. Gastroenterology 124, 233-234
6. Follmann, M., Griebenow, N., Hahn, M.G., Hartung, I., Mais, F.J., Mittendorf, J., Schäfer, M., Schirok, H., Stasch, J.P., Stoll, F. and Straub, A. (2013) The chemistry and biology of soluble guanylate cyclase stimulators and activators. Angew. Chem., Int. Ed. 52, 9442-9462
7. Derbyshire, E.R. and Marletta, M.A. (2012) Structure and regulation of soluble guanylate cyclase. Annu. Rev. Biochem. 81, 533-559
8. Linder, J.U. (2006) Class III adenylyl cyclases: molecular mechanisms of catalysis and regulation. Cell. Mol. Life Sci. 63, 1736-1751
9. Allerston, C.K., von Delft, F. and Gileadi, O. (2013) Crystal structures of the catalytic domain of human soluble guanylate cyclase. PLoS ONE 8, e57644
10. Rauch, A., Leipelt, M., Russwurm, M. and Steegborn, C. (2008) Crystal structure of the guanylyl cyclase Cya2. Proc. Natl. Acad. Sci. U.S.A. 105, 15720-15725
11. Winger, J.A., Derbyshire, E.R., Lamers, M.H., Marletta, M.A. and Kuriyan, J. (2008) The crystal structure of the catalytic domain of a eukaryotic guanylate cyclase. BMC Struct. Biol. 8, 42
12. Tesmer, J.J., Sunahara, R.K., Gilman, A.G. and Sprang, S.R. (1997) Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsα·GTPγS. Science 278, 1907-1916
13. Whisnant, R.E., Gilman, A.G. and Dessauer, C.W. (1996) Interaction of the two cytosolic domains of mammalian adenylyl cyclase. Proc. Natl. Acad. Sci. U.S.A. 93, 6621-6625
14. Tesmer, J.J., Sunahara, R.K., Johnson, R.A., Gosselin, G., Gilman, A.G. and Sprang, S.R. (1999) Two-metal-ion catalysis in adenylyl cyclase. Science 285, 756-760
15. Ma, X., Beuve, A. and van den Akker, F. (2010) Crystal structure of the signaling helix coiled-coil domain of the β1 subunit of the soluble guanylyl cyclase. BMC Struct. Biol. 10, 2
16. Fritz, B.G., Roberts, S.A., Ahmed, A., Breci, L., Li, W., Weichsel, A., Brailey, J.L., Wysocki, V.H., Tama, F. and Montfort, W.R. (2013) Molecular model of a soluble guanylyl cyclase fragment determined by small-angle X-ray scattering and chemical cross-linking. Biochemistry 52, 1568-1582
17. Purohit, R., Weichsel, A. and Montfort, W.R. (2013) Crystal structure of the α subunit PAS domain from soluble guanylyl cyclase. Protein Sci. 22, 1439-1444
18. Ma, X.L., Sayed, N., Beuve, A. and van den Akker, F. (2007) NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism. EMBO J. 26, 578-588
19. Winter, M.B., Herzik, M.A., Kuriyan, J. and Marletta, M.A. (2011) Tunnels modulate ligand flux in a heme nitric oxide/oxygen binding (H-NOX) domain. Proc. Natl. Acad. Sci. U.S.A. 108, E881-E889
20. Martin, E., Berka, V., Sharina, I. and Tsai, A.L. (2012) Mechanism of binding of NO to soluble guanylyl cyclase: implication for the second NO binding to the heme proximal site. Biochemistry 51, 2737-2746
21. Martin, F., Baskaran, P., Ma, X., Dunten, P.W., Schaefer, M., Stasch, J.P., Beuve, A. and van den Akker, F. (2010) Structure of cinaciguat (BAY 58-2667) bound to Nostoc H-NOX domain reveals insights into heme-mimetic activation of the soluble guanylyl cyclase. J. Biol. Chem. 285, 22651-22657
22. Baskaran, P., Heckler, E.J., van den Akker, F. and Beuve, A. (2011) Identification of residues in the heme domain of soluble guanylyl cyclase that are important for basal and stimulated catalytic activity. PLoS ONE 6, e26976
23. Friebe, A., Wedel, B., Harteneck, C., Foerster, J., Schultz, G. and Koesling, D. (1997) Functions of conserved cysteines of soluble guanylyl cyclase. Biochemistry 36, 1194-1198
24. Martin, E., Sharina, I., Kots, A. and Murad, F. (2003) A constitutively activated mutant of human soluble guanylyl cyclase (sGC): implication for the mechanism of sGC activation. Proc. Natl. Acad. Sci. U.S.A. 100, 9208-9213
25. Winger, J.A. and Marletta, M.A. (2005) Expression and characterization of the catalytic domains of soluble guanylate cyclase: interaction with the heme domain. Biochemistry 44, 4083-4090
26. Friebe, A., Russwurm, M., Mergia, E. and Koesling, D. (1999) A point-mutated guanylyl cyclase with features of the YC-1-stimulated enzyme: implications for the YC-1 binding site? Biochemistry 38, 15253-15257
27. Cary, S.P., Winger, J.A., Derbyshire, E.R. and Marletta, M.A. (2006) Nitric oxide signaling: no longer simply on or off. Trends Biochem. Sci. 31, 231-239
28. Cary, S.P., Winger, J.A. and Marletta, M.A. (2005) Tonic and acute nitric oxide signaling through soluble guanylate cyclase is mediated by nonheme nitric oxide, ATP, and GTP. Proc. Natl. Acad. Sci. U.S.A. 102, 13064-13069
29. Fernhoff, N.B., Derbyshire, E.R. and Marletta, M.A. (2009) A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 106, 21602-21607
30. Schmidt, P., Schramm, M., Schroder, H. and Stasch, J.P. (2003) Mechanisms of nitric oxide independent activation of soluble guanylyl cyclase. Eur. J. Pharmacol. 468, 167-174
31. Kumar, V., Martin, F., Hahn, M.G., Schaefer, M., Stamler, J.S., Stasch, J.P. and van den Akker, F. (2013) Insights into BAY 60-2770 activation and S-nitrosylation-dependent desensitization of soluble guanylyl cyclase via crystal structures of homologous Nostoc H-NOX domain complexes. Biochemistry 52, 3601-3608
32. Robinson, J.W. and Potter, L.R. (2012) Guanylyl cyclases A and B are asymmetric dimers that are allosterically activated by ATP binding to the catalytic domain. Sci. Signaling 5, ra65
33. Duda, T., Yadav, P. and Sharma, R.K. (2010) ATP allosteric activation of atrial natriuretic factor receptor guanylate cyclase. FEBS J. 277, 2550-2553
34. Duda, T., Yadav, P. and Sharma, R.K. (2011) Allosteric modification, the primary ATP activation mechanism of atrial natriuretic factor receptor guanylate cyclase. Biochemistry 50, 1213-1225
35. Ruiz-Stewart, I., Kazerounian, S., Pitari, G.M., Schulz, S. and Waldman, S.A. (2002) Soluble guanylate cyclase is allosterically inhibited by direct interaction with 2-substituted adenine nucleotides. Eur. J. Biochem. 269, 2186-2193
36. Derbyshire, E.R., Fernhoff, N.B., Deng, S. and Marletta, M.A. (2009) Nucleotide regulation of soluble guanylate cyclase substrate specificity. Biochemistry 48, 7519-7524
37. Beste, K.Y., Burhenne, H., Kaever, V., Stasch, J.P. and Seifert, R. (2012) Nucleotidyl cyclase activity of soluble guanylyl cyclase α1β1. Biochemistry 51, 194-204
38. Stasch, J.P., Pacher, P. and Evgenov, O.V. (2011) Soluble guanylate cyclase as an emerging therapeutic target in cardiopulmonary disease. Circulation 123, 2263-2273
39. Voors, A.A. and van Veldhuisen, D.J. (2012) Why do drugs for acute heart failure fail? Eur. J. Heart Fail. 14, 955-956
40. Gheorghiade, M., Greene, S.J., Filippatos, G., Erdmann, E., Ferrari, R., Levy, P.D., Maggioni, A., Nowack, C. and Mebazaa, A. (2012) Cinaciguat, a soluble guanylate cyclase activator: results from the randomized, controlled, phase IIb COMPOSE programme in acute heart failure syndromes. Eur. J. Heart Fail. 14, 1056-1066
41. Ghofrani, H.A., D'Armini, A.M., Grimminger, F., Hoeper, M.M., Jansa, P., Kim, N.H., Mayer, E. and Simonneau, G. (2013) Riociguat for the treatment of chronic thromboembolic pulmonary hypertension. N. Engl. J. Med. 369, 319-329
42. Ghofrani, H.A., Galiè, N., Grimminger, F., Grünig, E., Humbert, M., Jing, Z.C., Keogh, A.M., Langleben, D., Kilama, M.O., Fritsch, A. et al. (2013) Riociguat for the treatment of pulmonary arterial hypertension. N. Engl. J. Med. 369, 330-340