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

Volumn 52, Issue 20, 2013, Pages 3601-3608

  Kumar, Vijay ^a   Martin, Faye ^a   Hahn, Michael G ^b   Schaefer, Martina ^b   Stamler, Jonathan S ^a   Stasch, Johannes Peter ^b   Van Den Akker, Focco ^a  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b BAYER PHARMA AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVITY ASSAYS; BOUND STRUCTURE; DOMAIN COMPLEXES; GUANYLYL CYCLASE; HYDROPHOBIC INTERACTIONS; HYDROPHOBIC TAILS; SOLUBLE GUANYLYL CYCLASE (SGC); STRUCTURAL BASIS;

CARBOXYLATION; HYDROPHOBICITY; NITRIC OXIDE; PORPHYRINS;

CHEMICAL ACTIVATION;

BAY 602770; BINDING PROTEIN; CARBOXYLIC ACID; CINACIGUAT; CYSTEINE; GUANYLATE CYCLASE; GUANYLATE CYCLASE ACTIVATOR; H NOX PROTEIN; HEME; NITRIC OXIDE; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BACTERIAL STRAIN; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; DESENSITIZATION; ENZYME ACTIVITY; ENZYME ASSAY; HYDROPHOBICITY; IN VITRO STUDY; MEDIATOR; NITROSYLATION; NONHUMAN; NOSTOC; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; SUBSTITUTION REACTION;

BACTERIAL PROTEINS; BENZOATES; BIPHENYL COMPOUNDS; CRYSTALLOGRAPHY, X-RAY; GUANYLATE CYCLASE; HYDROCARBONS, FLUORINATED; MODELS, MOLECULAR; NITRIC OXIDE; NOSTOC; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, CYTOPLASMIC AND NUCLEAR;

EID: 84878264090     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi301657w     Document Type: Article

References (52)

1. Ashman, D. F., Lipton, R., Melicow, M. M., and Rice, T. D. (1963) Isolation of adenosine 3′, 5′-monophosphate and guanosine 3′, 5′-monophosphate from rat urine Biochem. Biophys. Res. Commun. 11, 330-334
2. 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
3. Bohme, E., Munske, K., and Schultz, G. (1969) [Formation of cyclic guanosine-3′,5′-monophosphate in various rat tissues] Naunyn Schmiedebergs Arch. Pharmakol. 264, 220-221
4. 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
5. Chan, N. L., Rogers, P. H., and Arnone, A. (1998) Crystal structure of the S-nitroso form of liganded human hemoglobin Biochemistry 37, 16459-16464
6. Chen, Y. Y., Chu, H. M., Pan, K. T., Teng, C. H., Wang, D. L., Wang, A. H., Khoo, K. H., and Meng, T. C. (2008) Cysteine S-nitrosylation protects protein-tyrosine phosphatase 1B against oxidation-induced permanent inactivation J. Biol. Chem. 283, 35265-35272
7. Chung, K. K., Thomas, B., Li, X., Pletnikova, O., Troncoso, J. C., Marsh, L., Dawson, V. L., and Dawson, T. M. (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function Science 304, 1328-1331
8. Derewenda, Z. S. (2004) Rational protein crystallization by mutational surface engineering Structure (Cambridge) 12, 529-535
9. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
10. Evgenov, O. V., Pacher, P., Schmidt, P. M., Hasko, G., Schmidt, H. H., and Stasch, J. P. (2006) NO-independent stimulators and activators of soluble guanylate cyclase: discovery and therapeutic potential Nat. Rev. Drug Discovery 5, 755-768
11. Fernhoff, N. B., Derbyshire, E. R., Underbakke, E. S., and Marletta, M. A. (2012) Heme-assisted S-Nitrosation Desensitizes Ferric Soluble Guanylate Cyclase (sGC) to Nitric Oxide J. Biol. Chem. 287, 43053-43062
12. Forconi, M., Schwans, J. P., Porecha, R. H., Sengupta, R. N., Piccirilli, J. A., and Herschlag, D. (2011) 2′-Fluoro substituents can mimic native 2′-hydroxyls within structured RNA Chem. Biol. 18, 949-954
13. Foster, M. W., McMahon, T. J., and Stamler, J. S. (2003) S-nitrosylation in health and disease Trends Mol. Med. 9, 160-168
14. Gaston, B., Reilly, J., Drazen, J. M., Fackler, J., Ramdev, P., Arnelle, D., Mullins, M. E., Sugarbaker, D. J., Chee, C., and Singel, D. J. (1993) Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc. Natl. Acad. Sci. U. S. A. 90, 10957-10961.
15. Gheorghiade, M., Marti, C. N., Sabbah, H. N., Roessig, L., Greene, S. J., Bohm, M., Burnett, J. C., Campia, U., Cleland, J. G., Collins, S. P., Fonarow, G. C., Levy, P. D., Metra, M., Pitt, B., Ponikowski, P., Sato, N., Voors, A. A., Stasch, J. P., and Butler, J. (2013) Soluble guanylate cyclase: a potential therapeutic target for heart failure Heart Fail. Rev. 18, 123-134
16. Hardman, J. G. and Sutherland, E. W. (1969) Guanyl cyclase, an enzyme catalyzing the formation of guanosine 3′,5′-monophosphate from guanosine trihosphate J. Biol. Chem. 244, 6363-6370
17. Helbo, S. and Fago, A. (2011) Allosteric modulation by S-nitrosation in the low-O(2) affinity myoglobin from rainbow trout Am. J. Physiol. Regul. Integr. Comp. Physiol. 300, R101-R108
18. Hess, D. T., Matsumoto, A., Kim, S. O., Marshall, H. E., and Stamler, J. S. (2005) Protein S-nitrosylation: purview and parameters Nat. Rev. Mol. Cell Biol. 6, 150-166
19. Hoffmann, L. S., Schmidt, P. M., Keim, Y., Hoffmann, C., Schmidt, H. H., and Stasch, J. P. (2011) Fluorescence dequenching makes haem-free soluble guanylate cyclase detectable in living cells PLoS One 6, e23596
20. Knorr, A., Hirth-Dietrich, C., Alonso-Alija, C., Harter, M., Hahn, M., Keim, Y., Wunder, F., and Stasch, J. P. (2008) Nitric oxide-independent activation of soluble guanylate cyclase by BAY 60-2770 in experimental liver fibrosis Arzneimittelforschung 58, 71-80
21. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (2001) PROCHECK-a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26, 283-291
22. Lima, B., Forrester, M. T., Hess, D. T., and Stamler, J. S. (2010) S-nitrosylation in cardiovascular signaling Circ. Res. 106, 633-646
23. Liu, L., Yan, Y., Zeng, M., Zhang, J., Hanes, M. A., Ahearn, G., McMahon, T. J., Dickfeld, T., Marshall, H. E., Que, L. G., and Stamler, J. S. (2004) Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock Cell 116, 617-628
24. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation Proteins 50, 437-450
25. Luchsinger, B. P., Rich, E. N., Gow, A. J., Williams, E. M., Stamler, J. S., and Singel, D. J. (2003) Routes to S-nitroso-hemoglobin formation with heme redox and preferential reactivity in the beta subunits Proc. Natl. Acad. Sci. U. S. A. 100, 461-466
26. Ma, X., 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
27. 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
28. 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 activatio Proc. Natl. Acad. Sci. U. S. A. 100, 9208-9213
29. 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
30. Mayer, B., Kleschyov, A. L., Stessel, H., Russwurm, M., Munzel, T., Koesling, D., and Schmidt, K. (2009) Inactivation of soluble guanylate cyclase by stoichiometric S-nitrosation Mol. Pharmacol. 75, 886-891
31. Munzel, T., Feil, R., Mulsch, A., Lohmann, S. M., Hofmann, F., and Walter, U. (2003) Physiology and pathophysiology of vascular signaling controlled by guanosine 3′,5′-cyclic monophosphate-dependent protein kinase [corrected] Circulation 108, 2172-2183
32. Olea, C., Jr., Herzik, M. A., Jr., Kuriyan, J., and Marletta, M. A. (2010) Structural insights into the molecular mechanism of H-NOX activation Protein Sci. 19, 881-887
33. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326
34. Pankey, E. A., Bhartiya, M., Badejo, A. M., Jr., Haider, U., Stasch, J. P., Murthy, S. N., Nossaman, B. D., and Kadowitz, P. J. (2011) Pulmonary and systemic vasodilator responses to the soluble guanylyl cyclase activator, BAY 60-2770, are not dependent on endogenous nitric oxide or reduced heme Am. J. Physiol. Heart Circ. Physiol. 300, H792-H802
35. Sanders, K. M., Ward, S. M., Thornbury, K. D., Dalziel, H. H., Westfall, D. P., and Carl, A. (1992) Nitric oxide as a non-adrenergic, non-cholinergic neurotransmitter in the gastrointestinal tract Jpn. J. Pharmacol. 58 (Suppl 2) 220P-225P
36. Sayed, N., Baskaran, P., Ma, X., van den Akker, F., and Beuve, A. (2007) Desensitization of soluble guanylyl cyclase, the NO receptor, by S-nitrosylation Proc. Natl. Acad. Sci. U. S. A. 104, 12312-12317
37. Schmidt, P. M., Rothkegel, C., Wunder, F., Schroder, H., and Stasch, J. P. (2005) Residues stabilizing the heme moiety of the nitric oxide sensor soluble guanylate cyclase Eur. J. Pharmacol. 513, 67-74
38. Schreiter, E. R., Rodriguez, M. M., Weichsel, A., Montfort, W. R., and Bonaventura, J. (2007) S-nitrosylation-induced conformational change in blackfin tuna myoglobin J. Biol. Chem. 282, 19773-19780
39. Schultz, G., Bohme, E., and Munske, K. (1969) Guanyl cyclase. Determination of enzyme activity Life Sci 8, 1323-1332
40. Singel, D. J. and Stamler, J. S. (2005) Chemical physiology of blood flow regulation by red blood cells: the role of nitric oxide and S-nitrosohemoglobin Annu. Rev. Physiol. 67, 99-145
41. Smith, B. C. and Marletta, M. A. (2012) Mechanisms of S-nitrosothiol formation and selectivity in nitric oxide signaling Curr. Opin. Chem. Biol. 16, 498-506
42. Stasch, J. P., Schmidt, P., Alonso-Alija, C., Apeler, H., Dembowsky, K., Haerter, M., Heil, M., Minuth, T., Perzborn, E., Pleiss, U., Schramm, M., Schroeder, W., Schroder, H., Stahl, E., Steinke, W., and Wunder, F. (2002) NO- and haem-independent activation of soluble guanylyl cyclase: molecular basis and cardiovascular implications of a new pharmacological principle Br. J. Pharmacol. 136, 773-783
43. Stasch, J. P., Schmidt, P. M., Nedvetsky, P. I., Nedvetskaya, T. Y., AK, H. S., Meurer, S., Deile, M., Taye, A., Knorr, A., Lapp, H., Muller, H., Turgay, Y., Rothkegel, C., Tersteegen, A., Kemp-Harper, B., Muller-Esterl, W., and Schmidt, H. H. (2006) Targeting the heme-oxidized nitric oxide receptor for selective vasodilatation of diseased blood vessels J. Clin. Invest. 116, 2552-2561
44. van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., and Vriend, G. (1996) PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules J. Comput.-Aided Mol. Des. 10, 255-262
45. Warner, T. D., Mitchell, J. A., Sheng, H., and Murad, F. (1994) Effects of cyclic GMP on smooth muscle relaxation Adv. Pharmacol. 26, 171-194
46. Weichsel, A., Brailey, J. L., and Montfort, W. R. (2007) Buried S-nitrosocysteine revealed in crystal structures of human thioredoxin Biochemistry 46, 1219-1227
47. White, A. A. and Aurbach, G. D. (1969) Detection of guanyl cyclase in mammalian tissues Biochim. Biophys. Acta 191, 686-697
48. 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
49. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions Methods Enzymol 374, 300-321
50. Wunder, F., Stasch, J. P., Hutter, J., Alonso-Alija, C., Huser, J., and Lohrmann, E. (2005) A cell-based cGMP assay useful for ultra-high-throughput screening and identification of modulators of the nitric oxide/cGMP pathway Anal. Biochem. 339, 104-112
51. Xie, G., Wang, X., Wang, L., Wang, L., Atkinson, R. D., Kanel, G. C., Gaarde, W. A., and Deleve, L. D. (2012) Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats Gastroenterology 142, 918-927
52. Yeates, T. O. (1997) Detecting and overcoming crystal twinning Methods Enzymol. 276, 344-358