The conserved Trp-Cys hydrogen bond dampens the "push effect" of the heme cysteinate proximal ligand during the first catalytic cycle of nitric oxide synthase

Biochemistry

Volumn 50, Issue 46, 2011, Pages 10069-10081

  Lang, Jérôme ^a   Santolini, Jérôme ^b   Couture, Manon ^a  

^a UNIVERSITÉ LAVAL   (Canada)

^b DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACK-BONDING; CATALYTIC CYCLES; HEME PROTEINS; NH GROUPS; NITRIC OXIDE SYNTHASES; NITRIC-OXIDE SYNTHASE; PUSH EFFECT; REDUCTION POTENTIAL; STAPHYLOCOCCUS AUREUS; THIOLATES;

AMINO ACIDS; BACTERIA; CARRIER CONCENTRATION; ELECTRON DENSITY MEASUREMENT; ELECTRONS; HYDROGEN BONDS; LIGANDS; MOLECULAR OXYGEN; NITRIC OXIDE; OXIDATION; PORPHYRINS; PROTEINS;

COMPLEXATION;

ARGININE; CYSTEINE; ENZYME VARIANT; HEME; HEME CYSTEINATE; LIGAND; NITRIC OXIDE SYNTHASE; OXYGEN; THIOL; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; AUTOOXIDATION; CATALYSIS; CHEMICAL BINDING; CONTROLLED STUDY; ELECTROCHEMISTRY; ELECTRON; ENZYME KINETICS; HYDROGEN BOND; HYDROXYLATION; MOLECULAR INTERACTION; MOLECULAR MODEL; OXIDATION REDUCTION POTENTIAL; POTENTIOMETRY; PRIORITY JOURNAL; RAMAN SPECTROMETRY;

CYSTEINE; HEME; HYDROGEN BONDING; LIGANDS; MUTAGENESIS, SITE-DIRECTED; NITRIC OXIDE SYNTHASE; OXIDATION-REDUCTION; POTENTIOMETRY; SPECTRUM ANALYSIS, RAMAN; STAPHYLOCOCCUS AUREUS;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

EID: 81255151103     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200965e     Document Type: Article

References (77)

1. Alderton, W. K., Cooper, C. E., and Knowles, R. G. (2001) Nitric oxide synthases: Structure, function and inhibition Biochem. J. 357, 593-615 (Pubitemid 32735142)
2. Li, H. and Poulos, T. L. (2005) Structure-function studies on nitric oxide synthases J. Inorg. Biochem. 99, 293-305 (Pubitemid 39642983)
3. Gorren, A. C. and Mayer, B. (2007) Nitric-oxide synthase: A cytochrome P450 family foster child Biochim. Biophys. Acta 1770, 432-445 (Pubitemid 46136746)
4. Stuehr, D. J. (1999) Mammalian nitric oxide synthases Biochim. Biophys. Acta 1411, 217-230 (Pubitemid 29221951)
5. Daff, S., Noble, M. A., Craig, D. H., Rivers, S. L., Chapman, S. K., Munro, A. W., Fujiwara, S., Rozhkova, E., Sagami, I., and Shimizu, T. (2001) Control of electron transfer in neuronal NO synthase Biochem. Soc. Trans. 29, 147-152 (Pubitemid 32587494)
6. Stuehr, D. J., Tejero, J., and Haque, M. M. (2009) Structural and mechanistic aspects of flavoproteins: Electron transfer through the nitric oxide synthase flavoprotein domain FEBS J. 276, 3959-3974
7. Stuehr, D. J. (1997) Structure-function aspects in the nitric oxide synthases Annu. Rev. Pharmacol. Toxicol. 37, 339-359 (Pubitemid 27238880)
8. Crane, B. R., Sudhamsu, J., and Patel, B. A. (2010) Bacterial nitric oxide synthases Annu. Rev. Biochem. 79, 445-470
9. Sudhamsu, J. and Crane, B. R. (2009) Bacterial nitric oxide synthases: What are they good for? Trends Microbiol. 17, 212-218
10. Crane, B. R. (2008) The enzymology of nitric oxide in bacterial pathogenesis and resistance Biochem. Soc. Trans. 36, 1149-1154
11. Crane, B. R., Arvai, A. S., Ghosh, D. K., Wu, C., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. (1998) Structure of nitric oxide synthase oxygenase dimer with pterin and substrate Science 279, 2121-2126 (Pubitemid 28196359)
12. Bird, L. E., Ren, J., Zhang, J., Foxwell, N., Hawkins, A. R., Charles, I. G., and Stammers, D. K. (2002) Crystal structure of SANOS, a bacterial nitric oxide synthase oxygenase protein from Staphylococcus aureus Structure 10, 1687-1696 (Pubitemid 35447979)
13. Pant, K., Bilwes, A. M., Adak, S., Stuehr, D. J., and Crane, B. R. (2002) Structure of a Nitric Oxide Synthase Heme Protein from Bacillus subtilis Biochemistry 41, 11071-11079 (Pubitemid 35034008)
14. Sudhamsu, J. and Crane, B. R. (2006) Structure and reactivity of a thermostable prokaryotic nitric-oxide synthase that forms a long-lived oxy-heme complex J. Biol. Chem. 281, 9623-9632 (Pubitemid 43864681)
15. Crane, B. R., Arvai, A. S., Gachhui, R., Wu, C., Ghosh, D. K., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. (1997) The structure of nitric oxide synthase oxygenase domain and inhibitor complexes Science 278, 425-431 (Pubitemid 27454419)
16. Gusarov, I., Starodubtseva, M., Wang, Z. Q., McQuade, L., Lippard, S. J., Stuehr, D. J., and Nudler, E. (2008) Bacterial nitric-oxide synthases operate without a dedicated redox partner J. Biol. Chem. 283, 13140-13147
17. Agapie, T., Suseno, S., Woodward, J. J., Stoll, S., Britt, R. D., and Marletta, M. A. (2009) NO formation by a catalytically self-sufficient bacterial nitric oxide synthase from Sorangium cellulosum Proc. Natl. Acad. Sci. U.S.A. 106, 16221-16226
18. Adak, S., Aulak, K. S., and Stuehr, D. J. (2002) Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis J. Biol. Chem. 277, 16167-16171 (Pubitemid 34967904)
19. Adak, S., Bilwes, A. M., Panda, K., Hosfield, D., Aulak, K. S., McDonald, J. F., Tainer, J. A., Getzoff, E. D., Crane, B. R., and Stuehr, D. J. (2002) Cloning, expression, and characterization of a nitric oxide synthase protein from Deinococcus radiodurans Proc. Natl. Acad. Sci. U.S.A. 99, 107-112 (Pubitemid 34060324)
20. Reece, S. Y., Woodward, J. J., and Marletta, M. A. (2009) Synthesis of nitric oxide by the NOS-like protein from Deinococcus radiodurans: A direct role for tetrahydrofolate Biochemistry 48, 5483-5491
21. Johnson, E. G., Sparks, J. P., Dzikovski, B., Crane, B. R., Gibson, D. M., and Loria, R. (2008) Plant-pathogenic Streptomyces species produce nitric oxide synthase-derived nitric oxide in response to host signals Chem. Biol. 15, 43-50
22. Shatalin, K., Gusarov, I., Avetissova, E., Shatalina, Y., McQuade, L. E., Lippard, S. J., and Nudler, E. (2008) Bacillus anthracis -derived nitric oxide is essential for pathogen virulence and survival in macrophages Proc. Natl. Acad. Sci. U.S.A. 105, 1009-1013 (Pubitemid 351282072)
23. Patel, B. A., Moreau, M., Widom, J., Chen, H., Yin, L., Hua, Y., and Crane, B. R. (2009) Endogenous nitric oxide regulates the recovery of the radiation-resistant bacterium Deinococcus radiodurans from exposure to UV light Proc. Natl. Acad. Sci. U.S.A. 106, 18183-18188
24. Gusarov, I. and Nudler, E. (2005) NO-mediated cytoprotection: Instant adaptation to oxidative stress in bacteria Proc. Natl. Acad. Sci. U.S.A. 102, 13855-13860 (Pubitemid 41377668)
25. Gusarov, I., Shatalin, K., Starodubtseva, M., and Nudler, E. (2009) Endogenous nitric oxide protects bacteria against a wide spectrum of antibiotics Science 325, 1380-1384
26. Pant, K. and Crane, B. R. (2006) Nitrosyl-heme structures of Bacillus subtilis nitric oxide synthase have implications for understanding substrate oxidation Biochemistry 45, 2537-2544
27. Cho, K.-B. and Gauld, J. W. (2005) Second half-reaction of the nitric oxide synthase: Computational insights into the initial step and key proposed intermediate J. Phys. Chem. B 109, 23706-23714 (Pubitemid 43081546)
28. 2 binding and implications for the catalytic mechanism J. Am. Chem. Soc. 126, 10267-10270 (Pubitemid 39100778)
29. Li, H., Igarashi, J., Jamal, J., Yang, W., and Poulos, T. L. (2006) Structural studies of constitutive nitric oxide synthases with diatomic ligands bound J. Biol. Inorg. Chem. 11, 753-768 (Pubitemid 44100470)
30. Davydov, R., Sudhamsu, J., Lees, N. S., Crane, B. R., and Hoffman, B. M. (2009) EPR and ENDOR characterization of the reactive intermediates in the generation of NO by cryoreduced oxy-nitric oxide synthase from Geobacillus stearothermophilus J. Am. Chem. Soc. 131, 14493-14507
31. Santolini, J. (2011) The molecular mechanism of mammalian NO-synthases: A story of electrons and protons J. Inorg. Biochem. 105, 127-141
32. Zhu, Y. and Silverman, R. B. (2008) Revisiting heme mechanisms. A perspective on the mechanisms of nitric oxide synthase (NOS), heme oxygenase (HO) and cytochrome P450s (CYP450s) Biochemistry 47, 2231-2243 (Pubitemid 351304531)
33. Auclair, K., Moenne-Loccoz, P., and Ortiz de Montellano, P. R. (2001) Roles of the proximal heme thiolate ligand in cytochrome p450(cam) J. Am. Chem. Soc. 123, 4877-4885 (Pubitemid 32905644)
34. Yoshioka, S., Takahashi, S., Ishimori, K., and Morishima, I. (2000) Roles of the axial push effect in cytochrome P450cam studied with the site-directed mutagenesis at the heme proximal site J. Inorg. Biochem. 81, 141-151
35. Brunel, A., Wilson, A., Henry, L., Dorlet, P., and Santolini, J. (2011) The proximal hydrogen bond network modulates Bacillus subtilis nitric-oxide synthase electronic and structural properties J. Biol. Chem. 286, 11997-12005
36. Lang, J., Driscoll, D., Gelinas, S., Rafferty, S. P., and Couture, M. (2009) Trp180 of endothelial NOS and Trp56 of bacterial saNOS modulate σ bonding of the axial cysteine to the heme J. Inorg. Biochem. 103, 1102-1112
37. Adak, S., Crooks, C., Wang, Q., Crane, B. R., Tainer, J. A., Getzoff, E. D., and Stuehr, D. J. (1999) Tryptophan 409 controls the activity of neuronal nitric-oxide synthase by regulating nitric oxide feedback inhibition J. Biol. Chem. 274, 26907-26911
38. Adak, S. and Stuehr, D. J. (2001) A proximal tryptophan in NO synthase controls activity by a novel mechanism J. Inorg. Biochem. 83, 301-308 (Pubitemid 32186415)
39. Adak, S., Wang, Q., and Stuehr, D. J. (2000) Molecular basis for hyperactivity in tryptophan 409 mutants of neuronal NO synthase J. Biol. Chem. 275, 17434-17439 (Pubitemid 30430781)
40. Couture, M., Adak, S., Stuehr, D. J., and Rousseau, D. L. (2001) Regulation of the properties of the heme-NO complexes in nitric-oxide synthase by hydrogen bonding to the proximal cysteine J. Biol. Chem. 276, 38280-38288
41. Wilson, D. J. and Rafferty, S. P. (2001) A structural role for tryptophan 188 of inducible nitric oxide synthase Biochem. Biophys. Res. Commun. 287, 126-129 (Pubitemid 32912473)
42. Yumoto, T., Sagami, I., Daff, S., and Shimizu, T. (2000) Roles of the heme proximal side residues tryptophan409 and tryptophan421 of neuronal nitric oxide synthase in the electron transfer reaction J. Inorg. Biochem. 82, 163-170
43. Chartier, F. J. and Couture, M. (2004) Stability of the heme environment of the nitric oxide synthase from Staphylococcus aureus in the absence of pterin cofactor Biophys. J. 87, 1939-1950 (Pubitemid 39167048)
44. Chartier, F. J. M. and Couture, M. (2007) Interactions between substrates and the haem-bound nitric oxide of ferric and ferrous bacterial nitric oxide synthases Biochem. J. 401, 235-245 (Pubitemid 46115899)
45. Chartier, F. J., Blais, S. P., and Couture, M. (2006) A Weak Fe-O Bond in the Oxygenated Complex of the Nitric-oxide Synthase of Staphylococcus aureus J. Biol. Chem. 281, 9953-9962 (Pubitemid 43869904)
46. Chartier, F. J. and Couture, M. (2007) Substrate-specific interactions with the heme-bound oxygen molecule of nitric-oxide synthase J. Biol. Chem. 282, 20877-20886 (Pubitemid 47099919)
47. Tejero, J., Biswas, A., Wang, Z. Q., Page, R. C., Haque, M. M., Hemann, C., Zweier, J. L., Misra, S., and Stuehr, D. J. (2008) Stabilization and characterization of a heme-oxy reaction intermediate in inducible nitric oxide synthase J. Biol. Chem. 283, 33498-33507
48. Zheng, L., Baumann, U., and Reymond, J. L. (2004) An efficient one-step site-directed and site-saturation mutagenesis protocol Nucleic Acids Res. 32, e115
49. Appleby, C. A. (1978) Purification of Rhizobium cytochromes P-450 Methods Enzymol. 52, 157-166
50. Copeland, R. A. (2000) Enzymes. A practical introduction to structure, mechanism, and data analysis, 2nd ed., Wiley-VCH, New York.
51. Gorren, A. C., Schmidt, K., and Mayer, B. (2002) Binding of l -arginine and imidazole suggests heterogeneity of rat brain neuronal nitric oxide synthase Biochemistry 41, 7819-7829 (Pubitemid 34627809)
52. Benson, B. B. and Krause, D. (1980) The Concentration and Isotopic Fractionation of Gases Dissolved in Fresh-Water in Equilibrium with the Atmosphere. 1. Oxygen Limnol. Oceanogr. 25, 662-671
53. Balland, V., Hureau, C., Cusano, A. M., Liu, Y., Tron, T., and Limoges, B. (2008) Oriented immobilization of a fully active monolayer of histidine-tagged recombinant laccase on modified gold electrodes Chemistry 14, 7186-7192
54. Giroud, C., Moreau, M., Mattioli, T. A., Balland, V., Boucher, J. L., Xu-Li, Y., Stuehr, D. J., and Santolini, J. (2010) Role of arginine guanidinium moiety in nitric-oxide synthase mechanism of oxygen activation J. Biol. Chem. 285, 7233-7245
55. Sabat, J., Stuehr, D. J., Yeh, S. R., and Rousseau, D. L. (2009) Characterization of the proximal ligand in the P420 form of inducible nitric oxide synthase J. Am. Chem. Soc. 131, 12186-12192
56. Suzuki, N., Higuchi, T., Urano, Y., Kikuchi, K., Uekusa, H., Ohashi, Y., Uchida, T., Kitagawa, T., and Nagano, T. (1999) Novel iron porphyrin- alkanethiolate complex with intramolecular NH•••S hydrogen bond: Synthesis, spectroscopy, and reactivity J. Am. Chem. Soc. 121, 11571-11572 (Pubitemid 30010491)
57. Ost, T. W., Miles, C. S., Munro, A. W., Murdoch, J., Reid, G. A., and Chapman, S. K. (2001) Phenylalanine 393 exerts thermodynamic control over the heme of flavocytochrome P450 BM3 Biochemistry 40, 13421-13429 (Pubitemid 33130769)
58. 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 (Pubitemid 46032759)
59. Rousseau, D. L., Li, D., Couture, M., and Yeh, S. R. (2005) Ligand-protein interactions in nitric oxide synthase J. Inorg. Biochem. 99, 306-323
60. Spiro, T. G. and Wasbotten, I. H. (2005) CO as a vibrational probe of heme protein active sites J. Inorg. Biochem. 99, 34-44 (Pubitemid 39642970)
61. Moreau, M., Boucher, J. L., Mattioli, T. A., Stuehr, D. J., Mansuy, D., and Santolini, J. (2006) Differential effects of alkyl- and arylguanidines on the stability and reactivity of inducible NOS heme-dioxygen complexes Biochemistry 45, 3988-3999
62. Fe-O2 J. Am. Chem. Soc. 113, 4815-4822
63. Oertling, W. A., Kean, R. T., Wever, R., and Babcock, G. T. (1990) Factors Affecting the Iron Oxygen Vibrations of Ferrous Oxy and Ferryl Oxo Heme-Proteins and Model Compounds Inorg. Chem. 29, 2633-2645
64. Galinato, M. G., Spolitak, T., Ballou, D. P., and Lehnert, N. (2011) Elucidating the role of the proximal cysteine hydrogen-bonding network in ferric cytochrome P450cam and corresponding mutants using magnetic circular dichroism spectroscopy Biochemistry 50, 1053-1069
65. Voegtle, H. L., Sono, M., Adak, S., Pond, A. E., Tomita, T., Perera, R., Goodin, D. B., Ikeda-Saito, M., Stuehr, D. J., and Dawson, J. H. (2003) Spectroscopic characterization of five- and six-coordinate ferrous-NO heme complexes. Evidence for heme Fe-proximal cysteinate bond cleavage in the ferrous-NO adducts of the Trp-409Tyr/Phe proximal environment mutants of neuronal nitric oxide synthase Biochemistry 42, 2475-2484 (Pubitemid 36255220)
66. Giroud, C., Moreau, M., Sagami, I., Shimizu, T., Frapart, Y., Mansuy, D., and Boucher, J. L. (2010) Comparison of wild type neuronal nitric oxide synthase and its Tyr588Phe mutant towards various l -arginine analogues J. Inorg. Biochem. 104, 1043-1050
67. Li, D., Kabir, M., Stuehr, D. J., Rousseau, D. L., and Yeh, S. R. (2007) Substrate- and isoform-specific dioxygen complexes of nitric oxide synthase J. Am. Chem. Soc. 129, 6943-6951 (Pubitemid 46847539)
68. Ost, T. W., Munro, A. W., Mowat, C. G., Taylor, P. R., Pesseguiero, A., Fulco, A. J., Cho, A. K., Cheesman, M. A., Walkinshaw, M. D., and Chapman, S. K. (2001) Structural and spectroscopic analysis of the F393H mutant of flavocytochrome P450 BM3 Biochemistry 40, 13430-13438 (Pubitemid 33130770)
69. Ost, T. W., Clark, J., Mowat, C. G., Miles, C. S., Walkinshaw, M. D., Reid, G. A., Chapman, S. K., and Daff, S. (2003) Oxygen activation and electron transfer in flavocytochrome P450 BM3 J. Am. Chem. Soc. 125, 15010-15020 (Pubitemid 37509664)
70. Chen, Z., Ost, T. W., and Schelvis, J. P. (2004) Phe393 mutants of cytochrome P450 BM3 with modified heme redox potentials have altered heme vinyl and propionate conformations Biochemistry 43, 1798-1808 (Pubitemid 38233243)
71. Varadarajan, R., Zewert, T. E., Gray, H. B., and Boxer, S. G. (1989) Effects of buried ionizable amino acids on the reduction potential of recombinant myoglobin Science 243, 69-72
72. Dutton, P. L., Shifman, J. M., Gibney, B. R., and Sharp, R. E. (2000) Heme redox potential control in de novo designed four-α-helix bundle proteins Biochemistry 39, 14813-14821
73. Olea, C., Jr., Kuriyan, J., and Marletta, M. A. (2010) Modulating heme redox potential through protein-induced porphyrin distortion J. Am. Chem. Soc. 132, 12794-12795
74. Gray, H. B., Tezcan, F. A., and Winkler, J. R. (1998) Effects of ligation and folding on reduction potentials of heme proteins J. Am. Chem. Soc. 120, 13383-13388 (Pubitemid 29025203)
75. Okamura, T., Takamizawa, S., Ueyama, N., and Nakamura, A. (1998) Novel rubredoxin model tetrathiolato iron(II) and cobalt(II) complexes containing intramolecular single and double NH•••S hydrogen bonds Inorg. Chem. 37, 18-28 (Pubitemid 128487961)
76. Ueno, T., Nishikawa, N., Moriyama, S., Adachi, S., Lee, K., Okamura, T., Ueyama, N., and Nakamura, A. (1999) Role of the invariant peptide fragment forming NH•••S hydrogen bonds in the active site of cytochrome P-450 and chloroperoxidase: Synthesis and properties of Cys-containing peptide Fe(III) and Ga(III) (octaethylporphinato) complexes as models Inorg. Chem. 38, 1199-1210
77. 2-: Protection of the Fe-S bond by double NH•••S hydrogen bonds Inorg. Chem. 35, 6473-6484 (Pubitemid 126452646)