Distal-to-proximal NO conversion in hemoproteins: The role of the proximal pocket

Journal of Molecular Biology

Volumn 405, Issue 2, 2011, Pages 395-409

  Hough, Michael A ^a   Antonyuk, Svetlana V ^a   Barbieri, Sonia ^b   Rustage, Neil ^a,c   McKay, Alison L ^d   Servid, Amy E ^d   Eady, Robert R ^a   Andrew, Colin R ^d   Hasnain, S Samar ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b BANGOR UNIVERSITY   (United Kingdom)

^c LIVERPOOL JOHN MOORES UNIVERSITY   (United Kingdom)

^d EASTERN OREGON UNIVERSITY   (United States)

Author keywords

cytochrome; kinetics; ligand discrimination; NO; resonance Raman

Indexed keywords

ALANINE; ARGININE; CARDIOLIPIN; CYTOCHROME C; GUANYLATE CYCLASE; HEMOPROTEIN; IRON; NITRIC OXIDE;

ACHROMOBACTER XYLOSOXIDANS; ARTICLE; BINDING KINETICS; BINDING SITE; CRYSTAL STRUCTURE; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL;

ACHROMOBACTER XYLOSOXIDANS; EUKARYOTA;

EID: 78650899877     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.10.035     Document Type: Article

References (32)

1. Lawson D.M., Stevenson C.E., Andrew C.R., and Eady R.R. Unprecedented proximal binding of nitric oxide to heme: implications for guanylate cyclase EMBO J. 19 2000 5661 5671
2. Choi P.S., Grigoryants V.M., Abruna H.D., Scholes C.P., and Shapleigh J.P. Regulation and function of cytochrome c′ in Rhodobacter sphaeroides 2.4.3 J. Bacteriol. 187 2005 4077 4085
3. Cross R., Aish J., Paston S.J., Poole R.K., and Moir J.W. Cytochrome c′ from Rhodobacter capsulatus confers increased resistance to nitric oxide J. Bacteriol. 182 2000 1442 1447
4. Pletneva E.V., Zhao Z., Kimura T., Petrova K., Gray H., and Winkler J. Probing the cytochrome c′ folding landscape J. Inorg. Biochem. 101 2007 1768 1775
5. Benini S., Rypniewski W.R., Wilson K.S., and Ciurli S. High resolution crystal structure of Rubrivivax gelatinosus cytochrome c′ J. Inorg. Biochem. 102 2008 1322 1328
6. Weiss R., Gold A., and Terner J. Cytochromes c′: biological models for the S = 3/2, 5/2 spin-state admixture? Chem. Rev. 106 2006 2550 2579
7. Zhao Y., Brandish P.E., Ballou D.P., and Marletta M.A. A molecular basis for nitric oxide sensing by soluble guanylate cyclase Proc. Natl Acad. Sci. USA 96 1999 14753 14758
8. Pixton D.A., Petersen C.A., Franke A., van Eldik R., Garton E.M., and Andrew C.R. Activation parameters for heme-NO binding in Alcaligenes xylosoxidans cytochrome c′: the putative dinitrosyl intermediate forms via a dissociative mechanism J. Am. Chem. Soc. 131 2009 4846 4853
9. Sharma V.S., and Magde D. Activation of soluble guanylate cyclase by carbon monoxide and nitric oxide: a mechanistic model Methods 19 1999 494 505
10. Derbyshire E.R., Gunn A., Ibrahim M., Spiro T., Britt R.D., and Marletta M.A. Characterization of two different five-coordinate soluble guanylate cyclase ferrous-nitrosyl complexes Biochemistry 47 2008 3892 3899
11. Ballou D.P., Zhao Y., Brandish P.E., and Marletta M.A. Revisiting the kinetics of nitric oxide (NO) binding to soluble guanylate cyclase: the simple NO-binding model is incorrect Proc. Natl Acad. Sci. USA 99 2002 12097 12101
12. Fernhoff N.B., Derbyshire E.R., and Marletta M.A. A nitric oxide/cysteine interaction mediates the activation of soluble guanylate cyclase Proc. Natl Acad. Sci. USA 106 2009 21602 21607
13. Ma X., Sayed N., Beuve A., and van den Akker F. NO and CO differentially activate soluble guanylyl cyclase via a heme pivot-bend mechanism EMBO J. 26 2007 578 588
14. Silkstone G., Kapetanaki S.M., Husu I., Vos M.H., and Wilson M.T. Nitric oxide binds to the proximal heme coordination site of the ferrocytochrome c/cardiolipin complex: formation mechanism and dynamics J. Biol. Chem. 285 2010 19785 19792
15. Andrew C.R., Green E.L., Lawson D.M., and Eady R.R. Resonance Raman studies of cytochrome c′ support the binding of NO and CO to opposite sides of the heme: implications for ligand discrimination in heme-based sensors Biochemistry 40 2001 4115 4122
16. Andrew C.R., George S.J., Lawson D.M., and Eady R.R. Six- to five-coordinate heme-nitrosyl conversion in cytochrome c′ and its relevance to guanylate cyclase Biochemistry 41 2002 2353 2360
17. Andrew C.R., Kemper L.J., Busche T.L., Tiwari A.M., Kecskes M.C., Stafford J.M. Accessibility of the distal heme face, rather than Fe-His bond strength, determines the heme-nitrosyl coordination number of cytochromes c′: evidence from spectroscopic studies Biochemistry 44 2005 8664 8672
18. Marti M.A., Capece L., Crespo A., Doctorovich F., and Estrin D.A. Nitric oxide interaction with cytochrome c′ and its relevance to guanylate cyclase. Why does the iron histidine bond break? J. Am. Chem. Soc. 127 2005 7721 7728
19. Kruglik S.G., Lambry J.C., Cianetti S., Martin J.L., Eady R.R., Andrew C.R., and Negrerie M. Molecular basis for nitric oxide dynamics and affinity with Alcaligenes xylosoxidans cytochrome c J. Biol. Chem. 282 2007 5053 5062
20. Lee B., Usov O.M., Grigoryants V.M., Myers W.K., Shapleigh J.P., and Scholes C.P. The role of arginine-127 at the proximal NO-binding site in determining the electronic structure and function of 5-coordinate NO-heme in cytochrome c′ of Rhodobacter sphaeroides Biochemistry 48 2009 8985 8993
21. Huston W.M., Andrew C.R., Servid A.E., McKay A.L., Leech A.P., Butler C.S., and Moir J.W. Heterologous overexpression and purification of cytochrome c′ from Rhodobacter capsulatus and a mutant (K42E) in the dimerization region. Mutation does not alter oligomerization but impacts the heme iron spin state and nitric oxide binding properties Biochemistry 45 2006 4388 4395
22. Barbieri S., Murphy L.M., Sawers R.G., Eady R.R., and Hasnain S.S. Modulation of NO binding to cytochrome c′ by distal and proximal haem pocket residues J. Biol. Inorg. Chem. 13 2008 531 540
23. Martin E., Berka V., Bogatenkova E., Murad F., and Tsai A.L. Ligand selectivity of soluble guanylyl cyclase: effect of the hydrogen-bonding tyrosine in the distal heme pocket on binding of oxygen, nitric oxide, and carbon monoxide J. Biol. Chem. 281 2006 27836 27845
24. Russworm M., and Koesling D. NO activation of guanylyl cyclase EMBO J. 23 2004 4443 4450
25. Otwinowski, Z. (1993). Oscillation Data Reduction Program. Proceedings of the CCP4 Study Weekend: "Data Collection and Processing", 29-30 January 1993, ed England. SDLNILSSB, 56-62.
26. Kabsch W. Automatic indexing of rotation diffraction patterns J. Appl. Crystallogr. 21 1988 67 71
27. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 1997 240 255
28. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 50 1994 760 763
29. Sheldrick G.M., and Schneider T.R. SHELXL: high-resolution refinement Methods Enzymol. 277 1997 319 343
30. Morris R.J., Perrakis A., and Lamzin V.S. ARP/wARP and automatic interpretation of protein electron density maps Methods Enzymol. 374 2003 229 244
31. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132
32. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. Procheck-a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 25 1993 283 291