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. 1995 Mar 28;92(7):2568–2571. doi: 10.1073/pnas.92.7.2568

Basis of guanylate cyclase activation by carbon monoxide.

V G Kharitonov 1, V S Sharma 1, R B Pilz 1, D Magde 1, D Koesling 1
PMCID: PMC42259  PMID: 7708686

Abstract

Kinetics of CO association with guanylate cyclase [GTP pyrophosphate-lyase (cyclizing), EC 4.6.1.2] and dissociation from carboxy guanylate cyclase have been studied at pH 7.5 by flash photolysis, yielding rate constants at 23 degrees C of 1.2 +/- 0.1 x 10(5) M-1.sec-1 and 28 +/- 2 sec-1, respectively. While the CO combination rate constant is the same as for the T state of hemoglobin, the CO dissociation rate constant is much higher than expected for a six-coordinate carboxyheme protein; yet the absorption spectrum is indicative of a six-coordinate heme. The two observations are reconciled by a reaction mechanism in which CO dissociation proceeds via a five-coordinate intermediate. This intermediate is structurally very similar to the five-coordinate nitrosyl heme derivative of guanylate cyclase and is presumably responsible for the observed 4-fold activation of guanylate cyclase by CO. Thus, we provide a model that explains enzyme activities of the nitrosyl and carboxy forms of the enzyme on the basis of a common mechanism.

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Selected References

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  1. Beaven G. H., Chen S. H., d' Albis A., Gratzer W. B. A spectroscopic study of the haemin--human-serum-albumin system. Eur J Biochem. 1974 Feb 1;41(3):539–546. doi: 10.1111/j.1432-1033.1974.tb03295.x. [DOI] [PubMed] [Google Scholar]
  2. Coletta M., Ascoli F., Brunori M., Traylor T. G. pH dependence of carbon monoxide binding to ferrous horseradish peroxidase. J Biol Chem. 1986 Jul 25;261(21):9811–9814. [PubMed] [Google Scholar]
  3. Friedman J. M., Rousseau D. L., Ondrias M. R., Stepnoski R. A. Transient Raman study of hemoglobin: structural dependence of the iron-histidine linkage. Science. 1982 Dec 17;218(4578):1244–1246. doi: 10.1126/science.7146910. [DOI] [PubMed] [Google Scholar]
  4. Gerzer R., Böhme E., Hofmann F., Schultz G. Soluble guanylate cyclase purified from bovine lung contains heme and copper. FEBS Lett. 1981 Sep 14;132(1):71–74. doi: 10.1016/0014-5793(81)80429-2. [DOI] [PubMed] [Google Scholar]
  5. Humbert P., Niroomand F., Fischer G., Mayer B., Koesling D., Hinsch K. D., Gausepohl H., Frank R., Schultz G., Böhme E. Purification of soluble guanylyl cyclase from bovine lung by a new immunoaffinity chromatographic method. Eur J Biochem. 1990 Jun 20;190(2):273–278. doi: 10.1111/j.1432-1033.1990.tb15572.x. [DOI] [PubMed] [Google Scholar]
  6. Ignarro L. J., Adams J. B., Horwitz P. M., Wood K. S. Activation of soluble guanylate cyclase by NO-hemoproteins involves NO-heme exchange. Comparison of heme-containing and heme-deficient enzyme forms. J Biol Chem. 1986 Apr 15;261(11):4997–5002. [PubMed] [Google Scholar]
  7. Ignarro L. J. Heme-dependent activation of soluble guanylate cyclase by nitric oxide: regulation of enzyme activity by porphyrins and metalloporphyrins. Semin Hematol. 1989 Jan;26(1):63–76. [PubMed] [Google Scholar]
  8. Makinen M. W., Houtchens R. A., Caughey W. S. Structure of carboxymyoglobin in crystals and in solution. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6042–6046. doi: 10.1073/pnas.76.12.6042. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Maxwell J. C., Caughey W. S. An infrared study of NO bonding to heme B and hemoglobin A. Evidence for inositol hexaphosphate induced cleavage of proximal histidine to iron bonds. Biochemistry. 1976 Jan 27;15(2):388–396. doi: 10.1021/bi00647a023. [DOI] [PubMed] [Google Scholar]
  10. Moore E. G., Gibson Q. H. Cooperativity in the dissociation of nitric oxide from hemoglobin. J Biol Chem. 1976 May 10;251(9):2788–2794. [PubMed] [Google Scholar]
  11. Perutz M. F. Regulation of oxygen affinity of hemoglobin: influence of structure of the globin on the heme iron. Annu Rev Biochem. 1979;48:327–386. doi: 10.1146/annurev.bi.48.070179.001551. [DOI] [PubMed] [Google Scholar]
  12. Senter P. D., Eckstein F., Mülsch A., Böhme E. The stereochemical course of the reaction catalyzed by soluble bovine lung guanylate cyclase. J Biol Chem. 1983 Jun 10;258(11):6741–6745. [PubMed] [Google Scholar]
  13. Sharma V. S., Geibel J. F., Ranney H. M. "Tension" on heme by the proximal base and ligand reactivity: conclusions drawn from model compounds for the reaction of hemoglobin. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3747–3750. doi: 10.1073/pnas.75.8.3747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Sharma V. S., Ranney H. M., Geibel J. F., Traylor T. G. A new method for the determination of ligand dissociation rate constant of carboxyhemoglobin. Biochem Biophys Res Commun. 1975 Oct 27;66(4):1301–1306. doi: 10.1016/0006-291x(75)90501-x. [DOI] [PubMed] [Google Scholar]
  15. Sharma V. S., Schmidt M. R., Ranney H. M. Dissociation of CO from carboxyhemoglobin. J Biol Chem. 1976 Jul 25;251(14):4267–4272. [PubMed] [Google Scholar]
  16. Stone J. R., Marletta M. A. Soluble guanylate cyclase from bovine lung: activation with nitric oxide and carbon monoxide and spectral characterization of the ferrous and ferric states. Biochemistry. 1994 May 10;33(18):5636–5640. doi: 10.1021/bi00184a036. [DOI] [PubMed] [Google Scholar]
  17. Szabo A., Perutz M. F. Equilibrium between six- and five-coordinated hemes in nitrosylhemoglobin: interpretation of electron spin resonance spectra. Biochemistry. 1976 Oct 5;15(20):4427–4428. doi: 10.1021/bi00665a013. [DOI] [PubMed] [Google Scholar]
  18. Traylor T. G., Sharma V. S. Why NO? Biochemistry. 1992 Mar 24;31(11):2847–2849. doi: 10.1021/bi00126a001. [DOI] [PubMed] [Google Scholar]
  19. Walda K. N., Liu X. Y., Sharma V. S., Magde D. Geminate recombination of diatomic ligands CO, O2, and NO with myoglobin. Biochemistry. 1994 Mar 1;33(8):2198–2209. doi: 10.1021/bi00174a029. [DOI] [PubMed] [Google Scholar]
  20. Yoshimura T., Ozaki T. Electronic spectra for nitrosyl(protoporphyrin IX dimethyl ester)iron(II) and its complexes with nitrogenous bases as model systems for nitrosylhemoproteins. Arch Biochem Biophys. 1984 Feb 15;229(1):126–135. doi: 10.1016/0003-9861(84)90137-1. [DOI] [PubMed] [Google Scholar]

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