Synergistic activation of soluble guanylate cyclase by CY-1 and carbon monoxide: Implications for the role of cleavage of the iron-histidine bond during activation by nitric oxide

Chemistry and Biology

Volumn 5, Issue 5, 1998, Pages 255-261

  Stone, James R ^a,c   Marletta, Michael A ^b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Allosteric; CGMP; Forskolin; Heme; Stopped flow

Indexed keywords

EID: 0032078245     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/s1074-5521(98)90618-4     Document Type: Article

References (52)

1. Bredt, D.S. & Snyder, S.H. (1994). Nitric oxide: a physiologic messenger molecule. Annu. Rev. Biochem. 63, 175-195.
2. Moncada, S., Palmer, R.M.J. & Higgs, E.A. (1991). Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol. Rev. 43, 109-142.
3. Marletta, M.A. (1993). Nitric oxide synthase structure and mechanism. J. Biol. Chem. 268, 12231-12234.
4. Marletta, M.A. (1994). Nitric oxide synthase: aspects concerning structure and catalysis. Cell 78, 927-930.
5. Waldman, S.A. & Murad, F. (1987). Cyclic GMP synthesis and function. Pharmacol. Rev. 39, 163-196.
6. Garbers, D.L. & Lowe, D.G. (1994). Guanylyl cyclase receptors. J. Biol. Chem. 269, 30741-30744.
7. Goy, M.F. (1991). cGMP: The wayward child of the cyclic nucleotide family. Trends Neurosci. 14, 293-299.
8. Warner, T.D., Mitchell, J.A., Sheng, H. & Murad, F. (1994). Effects of cyclic GMP on smooth muscle relaxation. Adv. Pharmacol. 26, 171-194.
9. Beckman, J.S., Chen, J., Crow, J.P. & Ye, Y.Z. (1994). Reactions of nitric oxide, superoxide and peroxynitrite with superoxide dismutase in neurodegeneration. Prog. Brain Res. 103, 371-380.
10. Roy, B., Lepoivre, M., Henry, Y. & Fontecave, M. (1995). Inhibition of ribonucleotide reductase by nitric oxide derived from thionitrites: reversible modifications of both subunits. Biochemistry 34, 5411-5418.
11. Lancaster, J.R. & Hibbs, J.B. (1990). EPR demonstration of ironnitrosyl complex formation by cytotoxic activated macrophages. Proc. Natl Acad. Sci. USA 87, 1223-1227.
12. Rubbo, H., et al., & Freeman, B.A. (1994). Nitric oxide regulation of superoxide and peroxynitrite-dependent lipid peroxidation. J. Biol. Chem. 269, 26066-26075.
13. Idriss, S.D., Pilz, R.B., Sharma, V.S. & Boss, G.R. (1992). Studies on cytosolic guanylate cyclase from human placenta. Biochem. Biophys. Res. Commun. 183, 312-320.
14. Garbers, D.L. (1979). Purification of soluble guanylate cyclase from rat lung. J. Biol. Chem. 254, 240-243.
15. Mulsch, A. & Gerzer, R (1991). Purification of heme-containing soluble guanylyl cyclase. Meth. Enzymol. 195, 377-383.
16. Stone, J.R. & Marletta, M.A. (1994). Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry 33, 5636-5640.
17. Nakane, M., Arai, K., Saheki, S., Kuno, T., Buechler, W. & Murad, F. (1990). Molecular cloning and expression of cDNAs coding for soluble guanylate cyclase from rat lung. J. Biol. Chem. 265, 16841-16845.
18. Nakane, M., Saheki, S., Kuno, T., Ishii, K. & Murad, F. (1988). Molecular cloning of a cDNA coding for 70 kilodalton subunit of soluble guanylate cyclase from rat lung. Biochem. Biophys. Res. Commun. 157, 1139-1147.
19. Koesling, D., et al., & Bohme, E. (1990). The primary structure of the larger subunit of soluble guanylyl cyclase from bovine lung. FEBS Lett. 266, 128-132.
20. Koesling, D., et al., & Frank, R. (1988). The primary structure of the 70 kDa subunit of bovine soluble guanylate cyclase. FEBS Lett. 239, 29-34.
21. Giuili, G., Scholl, U., Bulle, F. & Guellaen, G. (1992). Molecular cloning of cDNAs coding for the two subunits of soluble guanylyl cyclase from human brain. FEBS Lett. 304, 83-88.
22. Yuen, P.S.T., Potter, L.R. & Garbers, D.L. (1990). A new form of guanylyl cyclase is preferentially expressed in rat kidney. Biochemistry 29, 10872-10878.
23. Harteneck, C., Wedel, B., Koesling, D., Malkewitz, J., Bohme, E. & Schultz, G. (1991). Molecular cloning and expression of a new α-subunit of soluble guanylyl cyclase. FEBS Lett. 292, 217-222.
24. Gerzer, R., Böhme, E., Hofmann, F. & Schultz, G. (1981). Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett. 132, 71-74.
25. Deinum, G., Stone, J.R., Babcock, G.T. & Marietta, M.A. (1996). Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy. Biochemistry 35, 1540-1547.
26. Stone, J.R., Sands, R.H., Dunham, W.R. & Marletta, M.A. (1996). Spectral and ligand-binding properties of an unusual hemoprotein, the ferric form of soluble guanylate cyclase. Biochemistry 35, 3258-3262.
27. Stone, J.R. & Marletta, M.A. (1995). Heme stoichiometry of heterodimeric soluble guanylate cyclase. Biochemistry 34, 14668-14674.
28. Craven, P.A. & DeRubertis, F.R. (1978). Restoration of the responsiveness of purified guanylate cyclase to nitrosoguanidine, nitric oxide, and related activators by heme and hemeproteins. J. Biol. Chem. 253, 8433-8443.
29. Ignarro, L.J., Wood, K.S. & Wolin, M.S. (1984). Regulation of purified soluble guanylate cyclase by porphyrins and metalloporphyrins: A unifying concept. Adv. Cyclic Nucleotide Prot. Phosphor. Res. 17, 267-274.
30. Ignarro, L.J., Degnan, J.N., Baricos, W.H., Kadowitz, P.J. & Wolin, M.S. (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, 49-59.
31. Ignarro, L.J., Wood, K.S. & Wolin, M.S. (1982). Activation of purified soluble guanylate cyclase by protoporphyrin IX. Proc. Natl Acad. Sci. USA 79, 2870-2873.
32. Stone, J.R., Sands, R.H., Dunham, W.R. & Marietta, M.A. (1995). Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cylcase. Biochem. Biophys. Res. Comm. 207, 572-577.
33. Stone, J.R. & Marletta, M.A. (1996). Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry 35, 1093-1099.
34. Stone, J.R. & Marletta, M.A. (1995). The ferrous heme of soluble guanylate cyclase: formation of hexacoordinate complexes with carbon monoxide and nitrosomethane. Biochemistry 34, 16397-16403.
35. Mulsch, A., Bauersachs, J., Schafer, A., Stasch, J., 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. Pharmacol. 120, 681-689.
36. Wu, C., Ko, F., Kuo, S., Lee, F. & Teng, C. (1995). YC-1 inhibited human platelet aggregation through NO-independent activation of soluble guanylate cyclase. Br. J. Pharmacol. 116, 1973-1978.
37. Teng, C., Wu, C., Ko, F., Lee, F. & Kuo, S. (1997). YC-1, a nitric oxide-independent activator of soluble guanylate cyclase, inhibits platelet-rich thrombosis in mice. Eur. J. Pharmacol. 320, 161-166.
38. Ko, F., Wu, C., Kuo, S., Lee, F. & Teng, C. (1994). YC-1, a novel activator of platelet guanylate cyclase. Blood 84, 4226-4233.
39. Friebe, A., Schultz, G. & Koesling, D. (1996). Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. EMBO J. 15, 6863-6868.
40. Marks, G.S., Brien, J.F., Nakatsu, K. & McLaughlin, B.E. (1991). Does carbon monoxide have a physiological function? Trends Physiolog. Sci. 12, 185-188.
41. Verma, A., Hirsch, D.J., Glatt, C.E., Ronnett, G.V. & Snyder, S.H. (1993). Carbon monoxide: a putative neural messenger. Science 259, 381-384.
42. Geibel, J., Cannon, J., Campell, D., & Traylor, T.G. (1978). Model compounds for R-state and T-state hemoglobins, J. Am. Chem. Soc. 100, 3575-3585.
43. Zhao, Y., Schelvis, J.P.M., Babcock, G.T. & Marletta, M.A. (1998). Identification of histidine 105 in the β1 subunit of soluble guanylate cyclase as the heme proximal ligand. Biochemistry 37, 4502-4509.
44. Zhao, Y. & Marletta, M.A. (1997). Localization of the heme binding region in soluble guanylate cyclase. Biochemistry 36, 15959-15964.
45. Wedel, B., et al. & Koesling, D. (1994). Mutation of His-105 in the β1 subunit yields a nitric oxide-insensitive form of soluble guanylyl cyclase. Proc. Natl Acad. Sci. USA 91, 2592-2596.
46. Friebe, A. & Koesling, D. (1998). Mechanism of YC-1-induced activation of soluble guanylyl cyclase. Mol. Pharmacol. 53, 123-127.
47. Zhang, G., Liu, Y., Ruoho, A.E. & Hurley, J.H. (1997). Structure of the adenylyl cyclase catalytic core. Nature 386, 247-253.
48. sα-GTPγS. Science 278, 1907-1916.
49. sα with the cytosolio domains of mammalian adenylyl cyclase. J. Biol. Chem. 272, 22265-22271.
50. Graser, T., Vedernikov, Y.P. & Li, D.S. (1990). Study on the mechanism of carbon monoxide induced endothelium-independent relaxation in porcine coronary artery and vein. Biomed. Biochim. Acta 49, 293-296.
51. Brüne, B. & Ullrich, V. (1987). Inhibition of platelet aggregation by carbon monoxide is mediated by activation of guanylate cyclase. Mol. Pharmacol. 32, 497-504.
52. Dean, J.A. (1992). Lange's Handbook of Chemistry. McGraw-Hill, New York.