Characterization of two different five-coordinate soluble guanylate cyclase ferrous-nitrosyl complexes

Biochemistry

Volumn 47, Issue 12, 2008, Pages 3892-3899

  Derbyshire, Emily R ^a   Gunn, Alexander ^c   Ibrahim, Mohammed ^d   Spiro, Thomas G ^d   Britt, R David ^c   Marletta, Michael A ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOSYNTHESIS; NITRIC OXIDE; PARAMAGNETIC RESONANCE; SOLUBILITY;

GUANYLATE CYCLASE FERROUS-NITROSYL COMPLEXES; HEMOPROTEINS;

PROTEINS;

1 BENZYL 3 (5 HYDROXYMETHYL 2 FURYL)INDAZOLE; 4 AMINO 5 CYCLOPROPYL 2 [1 (2 FLUOROBENZYL) 1H PYRAZOLO[3,4 B]PYRIDIN 3 YL]PYRIMIDINE; CYCLIC GMP; FERROUS ION; GUANOSINE TRIPHOSPHATE; GUANYLATE CYCLASE; HEME; NITRIC OXIDE;

ARTICLE; CHEMICAL STRUCTURE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ENZYME ACTIVATION; ENZYME ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; RAMAN SPECTROMETRY;

ALLOSTERIC REGULATION; ANIMALS; COMPUTER SIMULATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERROUS COMPOUNDS; GUANOSINE TRIPHOSPHATE; GUANYLATE CYCLASE; HEME; NITRIC OXIDE; RATS; SOLUBILITY; SPECTRUM ANALYSIS, RAMAN;

EUKARYOTA;

EID: 41149159119     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi7022943     Document Type: Article

References (38)

1. Buechler, W. A., Ivanova, K., Wolfram, G., Drummer, C., Heim, J. M., and Gerzer, R. (1994) Soluble guanylyl cyclase and platelet function. Ann. N.Y. Acad. Sci. 714, 151-157.
2. Denninger, J. W., and Marletta, M. A. (1999) Guanylate cyclase and the NO/cGMP signaling pathway. Biochim. Biophys. Acta 1411, 334-350.
3. 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.
4. 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.
5. 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.
6. 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.
7. Harteneck, C., Wedel, B., Koesling, D., Malkewitz, J., Bohme, E., and Schultz, G. (1991) Molecular cloning and expression of a new α-subunit of soluble guanylyl cyclase. Interchangeability of the α-subunits of the enzyme. FEBS Lett. 292, 217-222.
8. Yuen, P. S., Potter, L. R., and Garbers, D. L. (1990) A new form of guanylyl cyclase is preferentially expressed in rat kidney. Biochemistry 29, 10872-10878.
9. Karow, D. S., Pan, D., Davis, J. H., Behrends, S., Mathies, R. A., and Marletta, M. A. (2005) Characterization of functional heme domains from soluble guanylate cyclase. Biochemistry 44, 16266-16274.
10. 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.
11. Koglin, M., Vehse, K., Budaeus, L., Scholz, H., and Behrends, S. (2001) Nitric oxide activates the β1 subunit of soluble guanylyl cyclase in the absence of a second subunit. J. Biol. Chem. 276, 30737-30743.
12. Stone, J. R., and Marletta, M. A. (1996) Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide. Biochemistry 35, 1093-1099.
13. Zhao, Y., Brandish, P. E., Ballou, D. P., and Marletta, M. A. (1999) A molecular basis for nitric oxide sensing by soluble guanylate cyclase. Proc. Natl. Acad. Sci. U.S.A. 96, 14753-14758.
14. Derbyshire, E. R., Tran, R., Mathies, R. A., and Marletta, M. A. (2005) Characterization of nitrosoalkane binding and activation of soluble guanylate cyclase. Biochemistry 44, 16257-16265.
15. Friebe, A., Schultz, G., and Koesling, D. (1996) Sensitizing soluble guanylyl cyclase to become a highly CO-sensitive enzyme. EMBO J. 15, 6863-6868.
16. Stasch, J. P., Becker, E. M., Alonso-Alija, C., Apeler, H., Dembowsky, K., Feurer, A., Gerzer, R., Minuth, T., Perzborn, E., Pleiss, U., Schroder, H., Schroeder, W., Stahl, E., Steinke, W., Straub, A., and Schramm, M. (2001) NO-independent regulatory site on soluble guanylate cyclase. Nature 410, 212-215.
17. Makino, R., Obayashi, E., Homma, N., Shiro, Y., and Hori, H. (2003) YC-1 facilitates release of the proximal His residue in the NO and CO complexes of soluble guanylate cyclase. J. Biol. Chem. 278, 11130-11137.
18. Martin, E., Czarnecki, K., Jayaraman, V., Murad, F., and Kincaid, J. (2005) Resonance Raman and infrared spectroscopic studies of high-output forms of human soluble guanylyl cyclase. J. Am. Chem. Soc. 127, 4625-4631.
19. Pal, B., and Kitagawa, T. (2005) Interactions of soluble guanylate cyclase with diatomics as probed by resonance Raman spectroscopy. J. Inorg. Biochem. 99, 267-279.
20. Russwurm, M., and Koesling, D. (2004) NO activation of guanylyl cyclase. EMBO J. 23, 4443-4450.
21. Stone, J. R., Sands, R. H., Dunham, W. R., and Marletta, M. A. (1995) Electron paramagnetic resonance spectral evidence for the formation of a pentacoordinate nitrosyl-heme complex on soluble guanylate cyclase. Biochem. Biophys. Res. Commun. 207, 572-577.
22. Yazawa, S., Tsuchiya, H., Hori, H., and Makino, R. (2006) Functional characterization of two nucleotide-binding sites in soluble guanylate cyclase. J. Biol. Chem. 281, 21763-21770.
23. Ibrahim, M., Xu, C., and Spiro, T. G. (2006) Differential sensing of protein influences by NO and CO vibrations in heme adducts. J. Am. Chem. Soc. 128, 16834-16845.
24. Winger, J. A., Derbyshire, E. R., and Marletta, M. A. (2006) Dissociation of nitric oxide from soluble guanylate cyclase and H-NOX domain constructs. J. Biol Chem. 292, 897-907.
25. Stoll, S., and Schweiger, A. (2006) EasySpin, a comprehensive software package for spectral simulation and analysis in EPR. J. Magn. Reson. 178, 42-55.
26. Czernuszewicz, R. S. (1986) Closed-cycle refrigerator solution and rotating solid sample cells for anaerobic resonance Raman spectroscopy. Appl. Spectrosc. 40, 571-573.
27. Tomita, T., Hirota, S., Ogura, T., Olson, J. S., and Kitagawa, T. (1999) Resonance Raman investigation of Fe-N-O structure of nitrosylheme in myoglobin and its mutants. J. Phys. Chem. B 103, 7044-7054.
28. Deinum, G., Stone, J. R., Babcock, G. T., and Marletta, M. A. (1996) Binding of nitric oxide and carbon monoxide to soluble guanylate cyclase as observed with resonance Raman spectroscopy. Biochemistry 35, 1540-1547.
29. Schelvis, J. P., Zhao, Y., Marletta, M. A., and Babcock, G. T. (1998) Resonance Raman characterization of the heme domain of soluble guanylate cyclase. Biochemistry 37, 16289-16297.
30. Wayland, B. B., and Olson, L. W. (1974) Spectroscopic studies and bonding model for nitric oxide complexes of iron porphyrins. J. Am. Chem. Soc. 96, 6037-6041.
31. Denninger, J. W., Schelvis, J. P. M., Brandish, P. E., Zhao, Y., Babcock, G. T., and Marletta, M. A. (2000) Interaction of soluble guanylate cyclase with YC-1: Kinetic and resonance Raman studies. Biochemistry 39, 4191-4198.
32. Li, Z. Q., Pal, B., Takenaka, S., Tsuyama, S., and Kitagawa, T. (2005) Resonance Raman evidence for the presence of two heme pocket conformations with varied activities in CO-bound bovine soluble guanylate cyclase and their conversion. Biochemistry 44, 939-946.
33. 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.
34. Lamothe, M., Chang, F. J., Balashova, N., Shirokov, R., and Beuve, A. (2004) Functional characterization of nitric oxide and YC-1 activation of soluble guanylyl cyclase: Structural implication for the YC-1 binding site? Biochemistry 43, 3039-3048.
35. More, C., Belle, V., Asso, M., Fournel, A., Roger, G., Guigliarelli, B., and Bertrand, P. (1999) EPR spectroscopy: A powerful technique for the structural and functional investigation of metalloproteins. Biospectroscopy 5, S3-S18.
36. Ubbink, M., Worrall, J. A., Canters, G. W., Groenen, E. J., and Huber, M. (2002) Paramagnetic resonance of biological metal centers. Annu. Rev. Biophys. Biomol. Struct. 31, 393-422.
37. Tomita, T., Ogura, T., Tsuyama, S., Imai, Y., and Kitagawa, T. (1997) Effects of GTP on bound nitric oxide of soluble guanylate cyclase probed by resonance Raman spectroscopy. Biochemistry 36, 10155-10160.
38. Derbyshire, E. R., and Marletta, M. A. (2007) Butyl isocyanide as a probe of the activation mechanism of soluble guanylate cyclase. Investigating the role of non-heme nitric oxide. J. Biol. Chem. 282, 35741-35748.