NO synthase: Structures and mechanisms

Nitric Oxide - Biology and Chemistry

Volumn 23, Issue 1, 2010, Pages 1-11

  Daff, Simon ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Calmodulin; Flavin; Heme; Monooxygenation; Nitric oxide; NOS

Indexed keywords

ARGININE; CALMODULIN; HEME; ISOENZYME; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDOREDUCTASE; OXYGEN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TETRAHYDROBIOPTERIN;

AMINO TERMINAL SEQUENCE; CARBOXY TERMINAL SEQUENCE; CHEMICAL REACTION; ELECTRON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; REVIEW;

ANIMALS; HUMANS; NITRIC OXIDE SYNTHASE; STRUCTURE-ACTIVITY RELATIONSHIP;

MAMMALIA;

EID: 77952240774     PISSN: 10898603     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.niox.2010.03.001     Document Type: Review

References (136)

1. In: Bothe H., Ferguson S., and Newton W.E. (Eds). Biology of the Nitrogen Cycle (2006), Elsevier pp. 1-452
2. Sudhamsu J., and Crane B.R. Bacterial nitric oxide synthases: what are they good for?. Trends Microbiol. 17 (2009) 212-218
3. Messner S., Leitner S., Bommassar C., Golderer G., Grobner P., Werner E.R., and Werner-Felmayer G. Physarum nitric oxide synthases: genomic structures and enzymology of recombinant proteins. Biochem. J. 418 (2009) 691-700
4. Alderton W.K., Cooper C.E., and Knowles R.G. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357 (2001) 593-615
5. Luckhart S., and Rosenberg R. Gene structure and polymorphism. Of an invertebrate nitric oxide synthase gene. Gene 232 (1999) 25-34
6. Moreau M., Lee G.I., Wang Y., Crane B.R., and Klessig D.F. AtNOS/AtNOA1 is a functional Arabidopsis thaliana cGTPase and not a nitric-oxide synthase. J. Biol. Chem. 283 (2008) 32957-32967
7. In: Balligand J.-L., and Mayer B. (Eds). Nitric Oxide (2000), Springer pp. 1-667
8. In: Ignarro L.J. (Ed). Nitric Oxide - Biology and Pathobiology (2000), Academic Press, San Diego pp. 1-1003
9. Adak S., Aulak K.S., and Stuehr D.J. Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J. Biol. Chem. 277 (2002) 16167-16171
10. Pant K., Bilwes A.M., Adak S., Stuehr D.J., and Crane B.R. Structure of a nitric oxide synthase heme protein from Bacillus subtilis. Biochemistry 41 (2002) 11071-11079
11. Poulos T.L., and Johnson E.F. Structures of cytochrome P450 enzymes. In: Ortiz de Montellano P.R. (Ed). Cytochrome P450: Structure, Mechanism, and Biochemistry (2005), Kluwer Academic/Plenum Publishers, New York 87-111
12. 2+/calmodulin-dependent nitric-oxide synthase from porcine cerebellum - cofactor-role of tetrahydrobiopterin. FEBS Lett. 277 (1990) 215-219
13. Fischmann T.O., Hruza A., Niu X.D., Fossetta J.D., Lunn C.A., Dolphin E., Prongay A.J., Reichert P., Lundell D.J., Narula S.K., and Weber P.C. Structural characterization of nitric oxide synthase isoforms reveals striking active-site conservation. Nat. Struct. Biol. 6 (1999) 233-242
14. Raman C.S., Li H.Y., Martasek P., Kral V., Masters B.S.S., and Poulos T.L. Crystal structure of constitutive endothelial nitric oxide synthase: a paradigm for pterin function involving a novel metal center. Cell 95 (1998) 939-950
15. Crane B.R., Arvai A.S., Ghosh D.K., Wu C.Q., Getzoff E.D., Stuehr D.J., and Tainer J.A. Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 279 (1998) 2121-2126
16. Bredt D.S., Hwang P.M., Glatt C.E., Lowenstein C., Reed R.R., and Snyder S.H. Cloned and expressed nitric-oxide synthase structurally resembles cytochrome-P-450 reductase. Nature 351 (1991) 714-718
17. 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. Structural basis for isozyme-specific regulation of electron transfer in nitric-oxide synthase. J. Biol. Chem. 279 (2004) 37918-37927
18. Wang M., Roberts D.L., Paschke R., Shea T.M., Masters B.S.S., and Kim J.J.P. Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc. Natl. Acad. Sci. USA 94 (1997) 8411-8416
19. Bredt D.S., and Snyder S.H. Isolation of nitric-oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87 (1990) 682-685
20. Kim H.W., Batista L.A., Hoppes J.L., Lee K.J., and Mykles D.L. A crustacean nitric oxide synthase expressed in nerve ganglia, Y-organ, gill and gonad of the tropical land crab, Gecarcinus lateralis. J. Exp. Biol. 207 (2004) 2845-2857
21. Roman L.J., Martasek P., and Masters B.S.S. Intrinsic and extrinsic modulation of nitric oxide synthase activity. Chem. Rev. 102 (2002) 1179-1189
22. Trimmer B.A., Aprille J.R., Dudzinski D.M., Lagace C.J., Lewis S.M., Michel T., Qazi S., and Zayas R.M. Nitric oxide and the control of firefly flashing. Science 292 (2001) 2486-2488
23. Ribeiro J.M.C., and Walker F.A. High-affinity histamine-binding and antihistaminic activity of the salivary nitric oxide-carrying heme protein (Nitrophorin) of Rhodnius prolixus. J. Exp. Med. 180 (1994) 2251-2257
24. Nathan C., and Xie Q.W. Regulation of biosynthesis of nitric-oxide. J. Biol. Chem. 269 (1994) 13725-13728
25. Stuehr D.J., Cho H.J., Kwon N.S., Weise M.F., and Nathan C.F. Purification and characterization of the cytokine-induced macrophage nitric-oxide synthase - an FAD-containing and FMN-containing flavoprotein. Proc. Natl. Acad. Sci. USA 88 (1991) 7773-7777
26. Cho H.J., Xie Q.W., Calaycay J., Mumford R.A., Swiderek K.M., Lee T.D., and Nathan C. Calmodulin is a subunit of nitric-oxide synthase from macrophages. J. Exp. Med. 176 (1992) 599-604
27. Brenman J.E., Chao D.S., Gee S.H., McGee A.W., Craven S.E., Santillano D.R., Wu Z.Q., Huang F., Xia H.H., Peters M.F., Froehner S.C., and Bredt D.S. Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha 1-syntrophin mediated by PDZ domains. Cell 84 (1996) 757-767
28. Daff S. Calmodulin-dependent regulation of mammalian nitric oxide synthase. Biochem. Soc. Trans. 31 (2003) 502-505
29. Stuehr D.J., Kwon N.S., Nathan C.F., Griffith O.W., Feldman P.L., and Wiseman J. N-Omega-hydroxy-l-arginine is an intermediate in the biosynthesis of nitric-oxide from l-arginine. J. Biol. Chem. 266 (1991) 6259-6263
30. Griffith O.W., and Stuehr D.J. Nitric oxides synthases - properties and catalytic mechanism. Annu. Rev. Physiol. 57 (1995) 707-736
31. Stuehr D.J. Mammalian nitric oxide synthases. Biochim. Biophys. Acta Bioenerg. 1411 (1999) 217-230
32. Buga G.M., Singh R., Pervin S., Rogers N.E., Schmitz D.A., Jenkinson C.P., Cederbaum S.D., and Ignarro L.J. Arginase activity in endothelial cells: inhibition by N-G-hydroxy-l-arginine during high-output NO production. Am. J. Physiol. Heart Circ. Physiol. 271 (1996) H1988-H1998
33. Rosen G.M., Tsai P., and Pou S. Mechanism of free-radical generation by nitric oxide synthase. Chem. Rev. 102 (2002) 1191-1199
34. Stuehr D.J., Santolini J., Wang Z.Q., Wei C.C., and Adak S. Update on mechanism and catalytic regulation in the NO synthases. J. Biol. Chem. 279 (2004) 36167-36170
35. In: Ortiz de Montellano P.R. (Ed). Cytochrome P450: Structure, Mechanism, and Biochemistry. third ed. (2005), Kluwer Academic/Plenum Publishers, New York pp. 1-659
36. Gorren A.C.F., and Mayer B. Nitric-oxide synthase: a cytochrome P450 family foster child. Biochim. Biophys. Acta Gen. Subj. 1770 (2007) 432-445
37. 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. The novel binding mode of N-alkyl-N′-hydroxyguanidine to neuronal nitric oxide synthase provides mechanistic insights into NO biosynthesis. Biochemistry 41 (2002) 13868-13875
38. Aoyagi M., Arvai A.S., Tainer J.A., and Getzoff E.D. Structural basis for endothelial nitric oxide synthase binding to calmodulin. EMBO J. 22 (2003) 766-775
39. Tochio H., Zhang Q., Mandal P., Li M., and Zhang M.J. Solution structure of the extended neuronal nitric oxide synthase PDZ domain complexed with an associated peptide. Nat. Struct. Biol. 6 (1999) 417-421
40. Panda K., Ghosh S., and Stuehr D.J. Calmodulin activates intersubunit electron transfer in the neuronal nitric-oxide synthase dimer. J. Biol. Chem. 276 (2001) 23349-23356
41. Sagami I., Daff S., and Shimizu T. Intra-subunit and inter-subunit electron transfer in neuronal nitric-oxide synthase - effect of calmodulin on heterodimer catalysis. J. Biol. Chem. 276 (2001) 30036-30042
42. Siddhanta U., Presta A., Fan B.C., Wolan D., Rousseau D.L., and Stuehr D.J. Domain swapping in inducible nitric-oxide synthase - electron transfer occurs between flavin and heme groups located on adjacent subunits in the dimer. J. Biol. Chem. 273 (1998) 18950-18958
43. Adak S., Sharma M., Meade A.L., and Stuehr D.J. A conserved flavin-shielding residue regulates NO synthase electron transfer and nicotinamide coenzyme specificity. Proc. Natl. Acad. Sci. USA 99 (2002) 13516-13521
44. Garnaud P.E., Koetsier M., Ost T.W.B., and Daff S. Redox properties of the isolated flavin mononucleotide- and flavin adenine dinucleotide-binding domains of neuronal nitric oxide synthase. Biochemistry 43 (2004) 11035-11044
45. Hermoso J.A., Mayoral T., Faro M., Gomez-Moreno C., Sanz-Aparicio J., and Medina M. Mechanism of coenzyme recognition and binding revealed by crystal structure analysis of ferredoxin-NADP(+) reductase complexed with NADP(+). J. Mol. Biol. 319 (2002) 1133-1142
46. Deng Z., Aliverti A., Zanetti G., Arakaki A.K., Ottado J., Orellano E.G., Calcaterra N.B., Ceccarelli E.A., Carrilli N., and Karplus P.A. A productive NADP(+) binding mode of ferredoxin-NADP(+) reductase revealed by protein engineering and crystallographic studies. Nat. Struct. Biol. 6 (1999) 847-853
47. Daff S. An appraisal of multiple NADPH binding-site models proposed for cytochrome P450 reductase, NO synthase, and related diflavin reductase systems. Biochemistry 43 (2004) 3929-3932
48. Abusoud H.M., and Stuehr D.J. Nitric-oxide synthases reveal a role for calmodulin in controlling electron-transfer. Proc. Natl. Acad. Sci. USA 90 (1993) 10769-10772
49. 2+/calmodulin-dependent electron transfer. J. Biol. Chem. 274 (1999) 30589-30595
50. Adak S., Ghosh S., Abu-Soud H.M., and Stuehr D.J. Role of reductase domain cluster 1 acidic residues in neuronal nitric-oxide synthase - characterization of the FMN-free enzyme. J. Biol. Chem. 274 (1999) 22313-22320
51. Li H.Y., Das A., Sibhatu H., Jamal J., Sligar S.G., and Poulos T.L. Exploring the electron transfer properties of neuronal nitric-oxide synthase by reversal of the FMN redox potential. J. Biol. Chem. 283 (2008) 34762-34772
52. Noble M.A., Munro A.W., Rivers S.L., Robledo L., Daff S.N., Yellowlees L.J., Shimizu T., Sagami I., Guillemette J.G., and Chapman S.K. Potentiometric analysis of the flavin cofactors of neuronal nitric oxide synthase. Biochemistry 38 (1999) 16413-16418
53. Gachhui R., Presta A., Bentley D.F., AbuSoud H.M., McArthur R., Brudvig G., Ghosh D.K., and Stuehr D.J. Characterization of the reductase domain of rat neuronal nitric oxide synthase generated in the methylotrophic yeast Pichia pastoris - calmodulin response is complete within the reductase domain itself. J. Biol. Chem. 271 (1996) 20594-20602
54. Stuehr D.J., and Ikedasaito M. Spectral characterization of brain and macrophage nitric-oxide synthases - cytochrome-P-450-like hemeproteins that contain a flavin semiquinone radical. J. Biol. Chem. 267 (1992) 20547-20550
55. Hanley S.C., Ost T.W.B., and Daff S. The unusual redox properties of flavocytochrome P450BM3 flavodoxin domain. Biochem. Biophys. Res. Commun. 325 (2004) 1418-1423
56. Masters B.S.S. The journey from NADPH-cytochrome P450 oxidoreductase to nitric oxide synthases. Biochem. Biophys. Res. Commun. 338 (2005) 507-519
57. Murataliev M.B., Feyereisen R., and Walker A. Electron transfer by diflavin reductases. Biochim. Biophys. Acta Proteins Proteomics 1698 (2004) 1-26
58. Gutierrez A., Grunau A., Paine M., Munro A.W., Wolf C.R., Roberts G.C.K., and Scrutton N.S. Electron transfer in human cytochrome P450 reductase. Biochem. Soc. Trans. 31 (2003) 497-501
59. Hamdane D., Xia C.W., Im S.C., Zhang H.M., Kim J.J.P., and Waskell L. Structure and function of an NADPH-cytochrome P450 oxidoreductase in an open conformation capable of reducing cytochrome P450. J. Biol. Chem. 284 (2009) 11374-11384
60. Welland A., Garnaud P.E., Kitamura M., Miles C.S., and Daff S. Importance of the domain-domain interface to the catalytic action of the NO synthase reductase domain. Biochemistry 47 (2008) 9771-9780
61. Craig D.H., Chapman S.K., and Daff S. Calmodulin activates electron transfer through neuronal nitric-oxide synthase reductase domain by releasing an NADPH-dependent conformational lock. J. Biol. Chem. 277 (2002) 33987-33994
62. Shirran S., Garnaud P., Daff S., McMillan D., and Barran P. The formation of a complex between calmodulin and neuronal nitric oxide synthase is determined by ESI-MS. J. R. Soc. Interface 2 (2005) 465-476
63. Spratt D.E., Taiakina V., Palmer M., and Guillemette J.G. Differential binding of calmodulin domains to constitutive and inducible nitric oxide synthase enzymes. Biochemistry 46 (2007) 8288-8300
64. Jones R.J., Smith S.M.E., Gao Y.T., DeMay B.S., Mann K.J., Salerno K.M., and Salerno J.C. The function of the small insertion in the hinge subdomain in the control of constitutive mammalian nitric-oxide synthases. J. Biol. Chem. 279 (2004) 36876-36883
65. Roman L.J., and Masters B.S.S. Electron transfer by neuronal nitric-oxide synthase is regulated by concerted interaction of calmodulin and two intrinsic regulatory elements. J. Biol. Chem. 281 (2006) 23111-23118
66. Abusoud H.M., Yoho L.L., and Stuehr D.J. Calmodulin controls neuronal nitric-oxide synthase by a dual mechanism - activation of intradomain and interdomain electron-transfer. J. Biol. Chem. 269 (1994) 32047-32050
67. 2+/calmodulin-dependent formation of hydrogen-peroxide by brain nitric-oxide synthase. Biochem. J. 281 (1992) 627-630
68. 2+/calmodulin-independent diaphorase and reductase activities. Biochemistry 31 (1992) 3243-3249
69. Nishida C.R., and Ortiz de Montellano P.R. Control of electron transfer in nitric-oxide synthases - swapping of autoinhibitory elements among nitric-oxide synthase isoforms. J. Biol. Chem. 276 (2001) 20116-20124
70. Chen P.F., and Wu K.K. Characterization of the roles of the 594-645 region in human endothelial nitric-oxide synthase in regulating calmodulin binding and electron transfer. J. Biol. Chem. 275 (2000) 13155-13163
71. Montgomery H.J., Romanov V., and Guillemette J.G. Removal of a putative inhibitory element reduces the calcium-dependent calmodulin activation of neuronal nitric-oxide synthase. J. Biol. Chem. 275 (2000) 5052-5058
72. Nishida C.R., and Ortiz de Montellano P.R. Autoinhibition of endothelial nitric-oxide synthase - identification of an electron transfer control element. J. Biol. Chem. 274 (1999) 14692-14698
73. Nishida C.R., and Ortiz de Montellano P.R. Electron transfer and catalytic activity of nitric oxide synthases - chimeric constructs of the neuronal, inducible, and endothelial isoforms. J. Biol. Chem. 273 (1998) 5566-5571
74. Harris D.E., Roman L.J., Martasek P., Shea T.M., and Masters B.S.S. Regulation of the constitutive nitric oxide synthases through their reductase domains. Biochemistry 40 (2001) 225
75. Roman L.J., Martasek P., Miller R.T., Harris D.E., de la Garza M.A., Shea T.M., Kim J.J.P., and Masters B.S.S. The C termini of constitutive nitric-oxide synthases control electron flow through the flavin and heme domains and affect modulation by calmodulin. J. Biol. Chem. 275 (2000) 29225-29232
76. Tiso M., Tejero J., Panda K., Aulak K.S., and Stuehr D.J. Versatile regulation of neuronal nitric oxide synthase by specific regions of its C-terminal tail. Biochemistry 46 (2007) 14418-14428
77. Haque M.M., Panda K., Tejero J., Aulak K.S., Fadlalla M.A., Mustovich A.T., and Stuehr D.J. A connecting hinge represses the activity of endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. USA 104 (2007) 9254-9259
78. Ilagan R.P., Tejero J., Aulak K.S., Ray S.S., Hemann C., Wang Z.Q., Gangoda M., Zweier J.L., and Stuehr D.J. Regulation of FMN subdomain interactions and function in neuronal nitric oxide synthase. Biochemistry 48 (2009) 3864-3876
79. Ilagan R.P., Tiso M., Konas D.W., Hemann C., Durra D., Hille R., and Stuehr D.J. Differences in a conformational equilibrium distinguish catalysis by the endothelial and neuronal nitric-oxide synthase flavoproteins. J. Biol. Chem. 283 (2008) 19603-19615
80. Feng C.J., Tollin G., Hazzard J.T., Nahm N.J., Guillemette J.G., Salerno J.C., and Ghosh D.K. Direct measurement by laser flash photolysis of intraprotein electron transfer in a rat neuronal nitric oxide synthase. J. Am. Chem. Soc. 129 (2007) 5621-5629
81. Feng C.J., Tollin G., Holliday M.A., Thomas C., Salerno J.C., Enemark J.H., and Ghosh D.K. Intraprotein electron transfer in a two-domain construct of neuronal nitric oxide synthase: the output state in nitric oxide formation. Biochemistry 45 (2006) 6354-6362
82. 2+) values for calmodulin binding and enzyme activation. J. Biol. Chem. 284 (2009) 11892-11899
83. 2+ concentrations required for calmodulin to bind and activate the enzyme. Biochemistry 47 (2008) 7557-7566
84. Panda K., Haque M.M., Garcin-Hosfield E.D., Durra D., Getzoff E.D., and Stuehr D.J. Surface charge interactions of the FMN module govern catalysis by nitric-oxide synthase. J. Biol. Chem. 281 (2006) 36819-36827
85. Knight K., and Scrutton N.S. Stopped-flow kinetic studies of electron transfer in the reductase domain of neuronal nitric oxide synthase: re-evaluation of the kinetic mechanism reveals new enzyme intermediates and variation with cytochrome P450 reductase. Biochem. J. 367 (2002) 19-30
86. Guan Z.W., Kamatani D., Kimura S., and Iyanagi T. Mechanistic studies on the intramolecular one-electron transfer between the two flavins in the human neuronal nitric-oxide synthase and inducible nitric-oxide synthase flavin domains. J. Biol. Chem. 278 (2003) 30859-30868
87. Matsuda H., and Iyanagi T. Calmodulin activates intramolecular electron transfer between the two flavins of neuronal nitric oxide synthase flavin domain. Biochim. Biophys. Acta Gen. Subj. 1473 (1999) 345-355
88. Konas D.W., Zhu K., Sharma M., Aulak K.S., Brudvig G.W., and Stuehr D.J. The FAD-shielding residue Phe(1395) regulates neuronal nitric-oxide synthase catalysis by controlling NADP(+) affinity and a conformational equilibrium within the flavoprotein domain. J. Biol. Chem. 279 (2004) 35412-35425
89. Batie C.J., and Kamin H. Association of ferredoxin-NADP+ reductase with NADP(H) specificity and oxidation-reduction properties. J. Biol. Chem. 261 (1986) 1214-1223
90. Page C.C., Moser C.C., and Dutton P.L. Mechanism for electron transfer within and between proteins. Curr. Opin. Chem. Biol. 7 (2003) 551-556
91. Gao Y.T., Smith S.M.E., Weinberg J.B., Montgomery H.J., Newman E., Guillemette J.G., Ghosh D.K., Roman L.J., Martasek P., and Salerno J.C. Thermodynamics of oxidation-reduction reactions in mammalian nitric-oxide synthase isoforms. J. Biol. Chem. 279 (2004) 18759-18766
92. Ilagan R.P., Tiso M., Konas D.W., Hemann C., Durra D., Hille R., and Stuehr D.J. Differences in a conformational equilibrium distinguish catalysis by the endothelial and neuronal nitric-oxide synthase flavoproteins. J. Biol. Chem. 283 (2008) 19603-19615
93. Dunford A.J., Rigby S.E.J., Hay S., Munro A.W., and Scrutton N.S. Conformational and thermodynamic control of electron transfer in neuronal nitric oxide synthase. Biochemistry 46 (2007) 5018-5029
94. Shimanuki T., Sato H., Daff S., Sagami I., and Shimizu T. Crucial role of Lys(423) in the electron transfer of neuronal nitric-oxide synthase. J. Biol. Chem. 274 (1999) 26956-26961
95. Crane B.R., Arvai A.S., Gachhui R., Wu C.Q., Ghosh D.K., Getzoff E.D., Stuehr D.J., and Tainer J.A. The structure of nitric oxide synthase oxygenase domain and inhibitor complexes. Science 278 (1997) 425-431
96. Feng C.J., Dupont A.L., Nahm N.J., Spratt D.E., Hazzard J.T., Weinberg J.B., Guillemette J.G., Tollin G., and Ghosh D.K. Intraprotein electron transfer in inducible nitric oxide synthase holoenzyme. J. Biol. Inorg. Chem. 14 (2009) 133-142
97. Feng C.J., Roman L.J., Hazzard J.T., Ghosh D.K., Tollin G., and Masters B.S.S. Deletion of the autoregulatory insert modulates intraprotein electron transfer in rat neuronal nitric oxide synthase. FEBS Lett. 582 (2008) 2768-2772
98. Leys D., Basran J., Talfournier F., Sutcliffe M.J., and Scrutton N.S. Extensive conformational sampling in a ternary electron transfer complex. Nat. Struct. Biol. 10 (2003) 219-225
99. Darrouzet E., Valkova-Valchanova M., Moser C.C., Dutton P.L., and Daldal F. Uncovering the [2Fe2S] domain movement in cytochrome bc(1) and its implications for energy conversion. Proc. Natl. Acad. Sci. USA 97 (2000) 4567-4572
100. Denisov I.G., Makris T.M., Sligar S.G., and Schlichting I. Structure and chemistry of cytochrome P450. Chem. Rev. 105 (2005) 2253-2277
101. Ost T.W.B., Clark J., Mowat C.G., Miles C.S., Walkinshaw M.D., Reid G.A., Chapman S.K., and Daff S. Oxygen activation and electron transfer in flavocytochrome P450BM3. J. Am. Chem. Soc. 125 (2003) 15010-15020
102. Green M.T. C-H bond activation in heme proteins: the role of thiolate ligation in cytochrome P450. Curr. Opin. Chem. Biol. 13 (2009) 84-88
103. Groves J.T. High-valent iron in chemical and biological oxidations. J. Inorg. Biochem. 100 (2006) 434-447
104. Makris T.M., von Koenig K., Schlichting I., and Sligar S.G. The status of high-valent metal oxo complexes in the P450 cytochromes. J. Inorg. Biochem. 100 (2006) 507-518
105. Sheng X., Zhang H.M., Im S.C., Horner J.H., Waskell L., Hollenberg P.F., and Newcomb M. Kinetics of oxidation of benzphetamine by compounds I of cytochrome P450 2B4 and its mutants. J. Am. Chem. Soc. 131 (2009) 2971-2976
106. Sheng X., Horner J.H., and Newcomb M. Spectra and kinetic studies of the compound I derivative of cytochrome P450 119. J. Am. Chem. Soc. 130 (2008) 13310-13320
107. Newcomb M., Zhang R., Chandrasena R.E.P., Halgrimson J.A., Horner J.H., Makris T.M., and Sligar S.G. Cytochrome P450 compound I. J. Am. Chem. Soc. 128 (2006) 4580-4581
108. Schlichting I., Berendzen J., Chu K., Stock A.M., Maves S.A., Benson D.E., Sweet B.M., Ringe D., Petsko G.A., and Sligar S.G. The catalytic pathway of cytochrome P450cam at atomic resolution. Science 287 (2000) 1615-1622
109. Zhu Y.Q., and Silverman R.B. Revisiting heme mechanisms. A perspective on the mechanisms of nitric oxide synthase (NOS), heme oxygenase (HO), and cytochrome p450s (CYP450s). Biochemistry 47 (2008) 2231-2243
110. de Visser S.P., and Tan L.S. 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 (2008) 12961-12974
111. Cho K.B., Carvajal M.A., and Shaik S. First half-reaction mechanism of nitric oxide synthase: the role of proton and oxygen coupled electron transfer in the reaction by quantum mechanics/molecular mechanics. J. Phys. Chem. B 113 (2009) 336-346
112. Robinet J.J., Cho K.B., and Gauld J.W. A density functional theory investigation on the mechanism of the second half-reaction of nitric oxide synthase. J. Am. Chem. Soc. 130 (2008) 3328-3334
113. Wei C.C., Crane B.R., and Stuehr D.J. Tetrahydrobiopterin radical enzymology. Chem. Rev. 103 (2003) 2365-2383
114. Bec N., Gorren A.C.F., Voelker C., Mayer B., and Lange R. 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 (1998) 13502-13508
115. AbuSoud H.M., Gachhui R., Raushel F.M., and Stuehr D.J. The ferrous-dioxy complex of neuronal nitric oxide synthase - divergent effects of l-arginine and tetrahydrobiopterin on its stability. J. Biol. Chem. 272 (1997) 17349-17353
116. Berka V., Yeh H.C., Gao D., Kiran F., and Tsai A.L. Redox function of tetrahydrobiopterin and effect of l-arginine on oxygen binding in endothelial nitric oxide synthase. Biochemistry 43 (2004) 13137-13148
117. Ost T.W.B., and Daff S. 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 (2005) 965-973
118. Hurshman A.R., Krebs C., Edmondson D.E., and Marletta M.A. Ability of tetrahydrobiopterin analogues to support catalysis by inducible nitric oxide synthase: formation of a pterin radical is required for enzyme activity. Biochemistry 42 (2003) 13287-13303
119. Suckling C.J., Gibson C.L., Huggan J.K., Morthala R.R., Clarke B., Kununthur S., Wadsworth R.M., Daff S., and Papale D. 6-Acetyl-7,7-dimethyl-5,6,7,8-tetrahydropterin is an activator of nitric oxide synthases. Bioorg. Med. Chem. Lett. 18 (2008) 1563-1566
120. Wei C.C., Wang Z.Q., Hemann C., Hille R., and Stuehr D.J. A tetrahydrobiopterin radical forms and then becomes reduced during N-omega-hydroxyarginine oxidation by nitric-oxide synthase. J. Biol. Chem. 278 (2003) 46668-46673
121. Wei C.C., Wang Z.Q., Tejero J., Yang Y.P., Hemann C., Hille R., and Stuehr D.J. Catalytic reduction of a tetrahydrobiopterin radical within nitric-oxide synthase. J. Biol. Chem. 283 (2008) 11734-11742
122. Wei C.C., Wang Z.Q., Wang Q., Meade A.L., Hemann C., Hille R., and Stuehr D.J. Rapid kinetic studies link tetrahydrobiopterin radical formation to heme-dioxy reduction and arginine hydroxylation in inducible nitric-oxide synthase. J. Biol. Chem. 276 (2001) 315-319
123. Hurshman A.R., Krebs C., Edmondson D.E., Huynh B.H., and Marletta M.A. Formation of a pterin radical in the reaction of the heme domain of inducible nitric oxide synthase with oxygen. Biochemistry 38 (1999) 15689-15696
124. Sorlie M., Gorren A.C.F., Marchal S., Shimizu T., Lange R., Andersson K.K., and Mayer B. Single-turnover of nitric-oxide synthase in the presence of 4-amino-tetrahydrobiopterin - proposed role for tetrahydrobiopterin as a proton donor. J. Biol. Chem. 278 (2003) 48602-48610
125. Davydov R., Ledbetter-Rogers A., Martasek P., Larukhin M., Sono M., Dawson J.H., Masters B.S.S., and Hoffman B.M. 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 (2002) 10375-10381
126. Woodward J.J., Chang M.M., Martin N.I., and Marletta M.A. The second step of the nitric oxide synthase reaction: evidence for ferric-peroxo as the active oxidant. J. Am. Chem. Soc. 131 (2009) 297-305
127. Klatt P., Schmidt K., Lehner D., Glatter O., Bachinger H.P., and Mayer B. Structural-analysis of porcine brain nitric-oxide synthase reveals a role for tetrahydrobiopterin and l-arginine in the formation of an Sds-resistant dimer. EMBO J. 14 (1995) 3687-3695
128. Moser C.C., Keske J.M., Warncke K., Farid R.S., and Dutton P.L. Nature of biological electron-transfer. Nature 355 (1992) 796-802
129. Crane B.R., Arvai A.S., Ghosh S., Getzoff E.D., Stuehr D.J., and Tainer J.A. Structures of the N-omega-hydroxy-l-arginine complex of inducible nitric oxide synthase oxygenase dimer with active and inactive pterins. Biochemistry 39 (2000) 4608-4621
130. Menyhard D.K. Comparative computational analysis of active and inactive cofactors of nitric oxide synthase. J. Phys. Chem. B 113 (2009) 3151-3159
131. Morao I., Periyasamy G., Hillier I.H., and Joule J.A. The role of tetrahydrobiopterin in catalysis by nitric oxide synthase. Chem. Commun. (2006) 3525-3527
132. Spolitak T., Dawson J.H., and Ballou D.P. Rapid kinetics investigations of peracid oxidation of ferric cytochrome P450cam: nature and possible function of compound ES. J. Inorg. Biochem. 100 (2006) 2034-2044
133. Homer R.B., and Alwis K.W. Kinetics and mechanism of alkaline-hydrolysis of guanidine, hexamethylguanidinium perchlorate, and tetramethylurea. J. Chem. Soc. Perkin Trans. 2 (1976) 781-784
134. Papale D., Miles C.C., and Daff S.N. A stabilised intermediate observed during oxygen activation by nNOS. J. Biol. Inorg. Chem. 12 (2007) S199
135. 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. Stabilization and characterization of a heme-oxy reaction intermediate in inducible nitric-oxide synthase. J. Biol. Chem. 283 (2008) 33498-33507
136. Matter H., Kumar H.S.A., Fedorov R., Frey A., Kotsonis P., Hartmann E., Frohlich L.G., Reif A., Pfleiderer W., Scheurer P., Ghosh D.K., Schlichting M., and Schmidt H. Structural analysis of isoform-specific inhibitors targeting the tetrahydrobiopterin binding site of human nitric oxide synthases. J. Med. Chem. 48 (2005) 4783-4792