Oxygen activation in neuronal NO synthase: Resolving the consecutive mono-oxygenation steps

Biochemical Journal

Volumn 443, Issue 2, 2012, Pages 505-514

  Papale, Davide ^a   Bruckmann, Chiara ^a   Gazur, Ben ^a   Miles, Caroline S ^a   Mowat, Christopher G ^a   Daff, Simon ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Electron transfer; Kinetics; Nitric Oxide Synthase (NOS); Oxygen activation; Proton transfer; Tetrahydrobiopterin

Indexed keywords

ARGININE; CITRULLINE; CYTOCHROME P450; HEME; MUTANT PROTEIN; NEURONAL NITRIC OXIDE SYNTHASE; OXYGEN; PROTON; TETRAHYDROBIOPTERIN;

ARTICLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; HYDROGEN BOND; NONHUMAN; OXYGENATION; PRIORITY JOURNAL; WILD TYPE;

CRYSTALLOGRAPHY, X-RAY; IRON; MODELS, MOLECULAR; MUTATION; NITRIC OXIDE SYNTHASE TYPE I; OXIDATION-REDUCTION; PROTEIN STRUCTURE, TERTIARY;

MAMMALIA;

EID: 84859470564     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20111644     Document Type: Article

References (51)

1. Daff, S. (2010) NO synthase: structures and mechanisms. Nitric Oxide 23, 1-11
2. Stuehr, D. J., Santolini, J., Wang, Z. Q., Wei, C. C. and Adak, S. (2004) Update onmechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 279, 36167-36170 (Pubitemid 39128949)
3. Santolini, J. (2011) The molecular mechanism of mammalian NO-synthases: a story of electrons and protons. J. Inorg. Biochem. 105, 127-141
4. 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)
5. Crane, B. R., Arvai, A. S., Ghosh, D. K., Wu, C. Q., 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)
6. Raman, C. S., Li, H. Y., Martasek, P., Kral, V., Masters, B.S.S. and Poulos, T. L. (1998) Crystal structure of constitutive endothelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center. Cell 95, 939-950 (Pubitemid 29019046)
7. Garcin, E. D., Bruns, C. M., Lloyd, S. J., Hosfield, D. J., Tiso, M., Gachhui, R., Stuehr, D. J., Tainer, J. A. and Getzoff, E. D. (2004) Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J. Biol. Chem. 279, 37918-37927 (Pubitemid 39195507)
8. Roman, L. J., Martasek, P. and Masters, B.S.S. (2002) Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem. Rev. 102, 1179-1189 (Pubitemid 35377608)
9. Adak, S., Wang, Q. and Stuehr, D. J. (2000) Arginine conversion tonitroxide by tetrahydrobiopterin-free neuronal nitric-oxide synthase: implications for mechanism. J. Biol. Chem. 275, 33554-33561
10. Wei, C. C., Wang, Z. Q., Hemann, C., Hille, R. and Stuehr, D. J. (2003) A tetra-hydrobiopterin radical forms and then becomes reduced during N-omega-hydroxyarginine oxidation by nitric-oxide synthase. J. Biol. Chem. 278, 46668-46673 (Pubitemid 37452244)
11. 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
12. Ost, T.W.B., 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 P450BM3. J. Am. Chem. Soc. 125, 15010-15020 (Pubitemid 37509664)
13. Bollinger, J. M. and Krebs, C. (2006) Stalking intermediates inoxygen activation by iron enzymes: motivation and method. J. Inorg. Biochem. 100, 586-605
14. Denisov, I. G., Makris, T. M., Sligar, S. G. and Schlichting, I. (2005) Structure and chemistry of cytochrome P450. Chem. Rev. 105, 2253-2277
15. Koppenol, W. H. (2007) Oxygen activation by cytochrome P450: a thermodynamic analysis. J. Am. Chem. Soc. 129, 9686-9690
16. Meunier, B., de Visser, S. P. and Shaik, S. (2004) Mechanism of oxidation reactions catalyzed by cytochrome P450 enzymes. Chem. Rev. 104, 3947-3980
17. Kellner, D. G., Hung, S. C., Weiss, K. E. and Sligar, S. G. (2002) Kinetic characterization of Compound I formation in the thermostable cytochrome P450 CYP119. J. Biol. Chem. 277, 9641-9644 (Pubitemid 34968061)
18. Rittle, J. and Green, M. T. (2010) Cytochrome P450 Compound I: capture, characterization, and C-H bond activation ainetics. Science 330, 933-937
19. Davydov, R., Makris, T. M., Kofman, V., Werst, D. E., Sligar, S. G. and Hoffman, B. M. (2001) Hydroxylation of camphor by-reduced oxy-cytochrome P450cam: mechanistic implications of EPR and ENDOR studies of catalytic intermediates in native and mutant enzymes. J. Am. Chem. Soc. 123, 1403-1415 (Pubitemid 32167333)
20. Davydov, R., Ledbetter-Rogers, A., Martasek, P., Larukhin, M., Sono, M., Dawson, J. H., Masters, B.S.S. and Hoffman, B. M. (2002) EPR and ENDOR characterization of intermediates in the cryoreduced oxy-nitric oxide synthase heme domain with bound L-arginine or N-G-hydroxyarginine. Biochemistry 41, 10375-10381
21. Hurshman, A. R., Krebs, C., Edmondson, D. E., Huynh, B. H. and Marletta, M. A. (1999) Formation of apterin radical in the reaction of the heme domain of inducible nitric oxide synthase with oxygen. Biochemistry 38, 15689-15696
22. Bec, N., Gorren, A. C. F., Voelker, C., Mayer, B. and Lange, R. (1998) Reaction of neuronal nitric-oxide synthase with oxygen at low temperature: evidence for reductive activation of the oxy-ferrous complex by tetrahydrobiopterin. J. Biol. Chem. 273, 13502-13508 (Pubitemid 28268391)
23. Ost, T. W. B. and Daff, S. (2005) Thermodynamic and kinetic analysis of the nitrosyl, carbonyl, and dioxy heme complexes of neuronal nitric-oxide synthase: the roles of substrate and tetrahydrobiopterin in oxygen activation. J. Biol. Chem. 280, 965-973
24. Crane, B. R., Sudhamsu, J. and Patel, B. A. (2010) Bacterial nitric oxide synthases. Annu. Rev. Biochem. 79, 445-470
25. Sagami, I., Daff, S. and Shimizu, T. (2001) Intra-subunit and inter-subunit electron transfer in neuronal nitric-oxide synthase: effect of calmodulin on heterodimer catalysis. J. Biol. Chem. 276, 30036-30042
26. Kunkel, T. A. (1985) Rapid and efficient site-specific mutagenesis without phenotypic selection. Proc. Natl. Acad. Sci, U.S.A. 82, 488-492
27. Sagami, I. and Shimizu, T. (1998) The crucial roles of Asp-314 and Thr-315 in the catalytic activation of molecular oxygen by neuronal nitric-oxide synthase: a site-directed mutagenesis study. J. Biol. Chem. 273, 2105-2108 (Pubitemid 28069259)
28. Ghosh, D. K., Holliday, M. A., Thomas, C., Weinberg, J. B., Smith, S. M. E. and Salerno, J. C. (2006) Nitric-oxide synthase output state: design and properties of nitric-oxide synthase oxygenase/FMN domain constructs. J. Biol. Chem. 281, 14173-14183 (Pubitemid 43848345)
29. Woodward, J. J., Chang, M. M., Martin, N. I. and Marletta, M. A. (2009) The second step of the nitric oxide synthase reaction: evidence for ferric-peroxo as the active oxidant. J. Am. Chem. Soc. 131, 297-305
30. d binding sites: binding of arginine analogs to nitric oxide synthases. Nitric Oxide 5, 442-452
31. ω-hydroxyarginine to nitric oxide and citrulline. Biochemistry 36, 10811-10816
32. Collaborative Computational Project, N. (1994) The CCP4 Suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
33. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
34. Adams, P. D., Grosse-Kunstleve, R. W., Hung, L. W., Ioerger, T. R., McCoy, A. J., Moriarty, N. W., Read, R. J., Sacchettini, J. C., Sauter, N. K. and Terwilliger, T. C. (2002) PHENIX: building new software for automated crystallographic structure determination. Acta Crystallogr. Sect. D Biol. Crystallogr. 58, 1948-1954 (Pubitemid 35337293)
35. Li, H. Y., Shimizu, H., Flinspach, M., Jamal, J., Yang, W. P., Xian, M., Cai, T. W., Wen, E. Z., Jia, Q. A., Wang, P. G. and Poulos, T. L. (2002) The novel binding mode of N-alkyl-N′-hydroxyguanidine to neuronal nitric oxide synthase provides mechanistic insights into NO biosynthesis. Biochemistry 41, 13868-13875 (Pubitemid 35364860)
36. Wei, C. C., Crane, B. R. and Stuehr, D. J. (2003) Tetrahydrobiopterin radical enzymology. Chem. Rev. 103, 2365-2383
37. Crane, B. R., Arvai, A. S., Ghosh, S., Getzoff, E. D., Stuehr, D. J. and Tainer, J. A. (2000) Structures of the N-ω-hydroxy-L-arginine complex of inducible nitric oxide synthase oxygenase dimer with active and inactive pterins. Biochemistry 39, 4608-4621 (Pubitemid 30225324)
38. Moser, C. C., Keske, J. M., Warncke, K., Farid, R. S. and Dutton, P. L. (1992) Nature of biological electron transfer. Nature 355, 796-802
39. Groves, J. T. and Wang, C. C. Y. (2000) Nitric oxide synthase: models and mechanisms. Curr. Opin. Chem. Biol. 4, 687-695
40. Wei, C. C., Wang, Z. Q., Wang, Q., Meade, A. L., Hemann, C., Hille, R. and Stuehr, D. J. (2001) Rapid kinetic studies link tetrahydrobiopterin radical formation to heme-dioxy reduction and arginine hydroxylation in inducible nitric-oxide synthase. J. Biol. Chem. 276, 315-319 (Pubitemid 32050321)
41. 2 and NO bonding to heme from ab initio multireference/multiconfiguration and DFT calculations. J. Biol. Inorg. Chem. 16, 841-855
42. Zhu, Y. Q. 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
43. de Visser, S. P. and Tan, L. S. (2008) Is the bound substrate in nitric oxide synthase protonated or neutral and what is the active oxidant that performs substrate hydroxylation? J. Am. Chem. Soc. 130, 12961-12974
44. Robinet, J. J., Cho, K.-B. and Gauld, J. W. (2008) A density functional theory investigation on the mechanism of the second half-reaction of nitric oxide synthase. J. Am. Chem. Soc. 130, 3328-3334 (Pubitemid 351456037)
45. 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
46. 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
47. Giroud, C., Moreau, M., Mattioli, T. A., Balland, V., Boucher, J. L., Yun, X. L., Stuehr, D. J. and Santolini, J. (2010) Role of a arginine guanidinium moiety in nitric-oxide synthase mechanism of oxygen activation. J. Biol. Chem. 285, 7233-7245
48. Sligar, S. G., Makris, T. M. and Denisov, I. G. (2005) Thirty years of microbial P450 monooxygenase research: peroxo-heme intermediates, the central bus station in heme oxygenase catalysis. Biochem. Biophys. Res. Commun. 338, 346-354 (Pubitemid 41541971)
49. Spolitak, T., Dawson, J. H. and Ballou, D. P. (2005) Reaction of ferric cytochrome P450cam with peracids: kinetic characterization of intermediates on the reaction pathway. J. Biol. Chem. 280, 20300-20309 (Pubitemid 40776727)
50. Jung, C., Lendzian, F., Schunemann, V., Richter, M., Bottger, L. H., Trautwein, A. X., Contzen, J., Galander, M., Ghosh, D. K. and Barra, A. L. (2005) Multi-frequency EPR and Mossbauer spectroscopic studies on freeze-quenched reaction intermediates of nitric oxide synthase. Magn. Reson. Chem. 43, S84-S95 (Pubitemid 41578505)
51. Tejero, J. S., 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