Reactivity of the heme-dioxygen complex of the inducible nitric oxide synthase in the presence of alternative substrates

FEBS Journal

Volumn 273, Issue 1, 2006, Pages 180-191

  Lefèvre Groboillot, David ^a,b   Boucher, Jean Luc ^b   Mansuy, Daniel ^b   Stuehr, Dennis J ^a  

^a LERNER RESEARCH INSTITUTE   (United States)

^b CNRS   (France)

Author keywords

Guanidines; Heme dioxygen complex; Hydroxyguanidines; Nitric oxide synthase; Stopped flow visible spectroscopy

Indexed keywords

ARGININE; DIHYDROBIOPTERIN; FERROUS ION; GUANIDINE DERIVATIVE; HEME; INDUCIBLE NITRIC OXIDE SYNTHASE; N(G) HYDROXYARGININE; NITRIC OXIDE SYNTHASE; OXYGEN; TETRAHYDROBIOPTERIN; 5,6,7,8-TETRAHYDROBIOPTERIN; 7,8-DIHYDROBIOPTERIN; BIOPTERIN; DRUG DERIVATIVE;

ARTICLE; CATALYSIS; CONTROLLED STUDY; ENZYME KINETICS; ENZYME SUBSTRATE; HYDROXYLATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; SPECTROSCOPY; ANIMAL; CHEMICAL MODEL; CHEMISTRY; ENZYME SPECIFICITY; KINETICS;

ANIMALS; ARGININE; BIOPTERIN; GUANIDINES; HEME; KINETICS; MICE; MODELS, CHEMICAL; NITRIC OXIDE SYNTHASE TYPE II; OXYGEN; SUBSTRATE SPECIFICITY;

EID: 33644874269     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2005.05056.x     Document Type: Article

References (44)

1. Alderton WK Cooper CE Knowles RG 2001 Nitric oxide synthases: structure, function and inhibition Biochem J 357 593 615
2. Gorren AC Mayer B 2002 Tetrahydrobiopterin in nitric oxide synthesis: a novel biological role for pteridines Curr Drug Metab 3 133 157
3. Roman LJ Martasek P Masters BS 2002 Intrisic and extrinsic modulation of nitric oxide synthase activity Chem Rev 102 1179 1190
4. Boggs S Huang L Stuehr DJ 2000 Formation and reactions of the heme-dioxygen intermediate in the first and second steps of nitric oxide synthesis as studied by stopped-flow spectroscopy under single-turnover conditions Biochemistry 39 2332 2339
5. Wei CC Wang ZQ Wang Q Meade AL Hemann C Hille R Stuehr DJ 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
6. Hurshman AR Marletta MA 2002 Reactions catalyzed by the heme domain of inducible nitric oxide synthase: evidence for the involvement of tetrahydrobiopterin in electron transfer Biochemistry 41 3439 3456
7. Bec N Gorren AC Voelker C Mayer B 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
8. Gorren AC Bec N Schrammel A Werner ER Lange R Mayer B 2000 Low temperature optical absorption spectra suggest a redox role for tetrahydrobiopterin in both steps of nitric oxide synthase catalysis Biochemistry 39 11763 11770
9. Bec N Gorren AFC Mayer B Schmidt PP Andersson KK Lange R 2000 The role of tetrahydrobiopterin in the activation of oxygen by nitric oxide synthase J Inorg Biochem 81 207 211
10. Wang ZQ Wei CC Stuehr DJ 2002 A conserved tryptophan 457 modulates the kinetics and extent of N-hydroxy- l -arginine oxidation by inducible nitric oxide synthase J Biol Chem 277 12830 12837
11. Schmidt PP Lange R Gorren AC Werner ER Mayer B Andersson KK 2001 Formation of a protonated trihydrobiopterin radical cation in the first reaction cycle of neuronal and endothelial nitric oxide synthase detected by electron paramagnetic resonance spectroscopy J Biol Inorg Chem 6 151 158
12. Hurshman AR Krebs C Edmondson DE Huynh BH Marletta MA 1999 Formation of a pterin radical in the reaction of the heme domain of inducible nitric oxide synthase with oxygen Biochemistry 38 15689 15696
13. Wei CC Wang ZQ Arvai AS Hemann C Hille R Getzoff ED Stuehr DJ 2003 Structure of tetrahydrobiopterin tunes its electron transfer to the heme-dioxy intermediate in nitric oxide synthase Biochemistry 42 1969 1977
14. Abu-Soud HM Gachhui R Raushel FM Stuehr DJ 1997 The ferrous-dioxy complex of neuronal nitric oxide synthase: divergent effects of 1-arginine and tetrahydrobiopterin on its stability J Biol Chem 272 17349 17353
15. Sato H Sagami I Daff S Shimizu T 1998 Autoxidation rates of neuronal nitric oxide synthase: effects of the substrates, inhibitors, and modulators Biochem Biophys Res Commum 253 845 849
16. Couture M Stuehr DJ Rousseau DL 2000 The ferrous dioxygen complex of the oxygenase domain of neuronal nitric oxide synthase J Biol Chem 275 3201 3205
17. Ledbetter AP McMillan K Roman LJ Masters BS Dawson JH Sono M 1999 Low-temperature stabilization and spectroscopic characterization of the dioxygen complex of the ferrous neuronal nitric oxide synthase oxygenase domain Biochemistry 38 8014 8021
18. ω- hydroxyarginine J Med Chem 44 3199 3202
19. Xian M Fujiwara N Wen Z Cai T Kazuma S Janczuk A Tang X Telyatnikov V Zhang Y Chen X et al. 2002 Novel substrates for nitric oxide synthases Bioorg Med Chem 10 3049 3055
20. Renodon-Corniere A Boucher JL Dijols S Stuehr DJ Mansuy D 1999 Efficient formation of nitric oxide from selective oxidation of N-aryl-N'- hydroxyguanidines by inducible nitric oxide synthase Biochemistry 38 4663 4668
21. Jia Q Cai T Huang M Li H Xian M Poulos TL Wang PG 2003 Isoform-selective substrates of nitric oxide synthase J Med Chem 46 2271 2274
22. Dijols S Boucher JL Lepoivre M Lefevre-Groboillot D Moreau M Frapart Y Rekka E Meade AL Stuehr DJ Mansuy D 2002 First non α-amino acid guanidines acting as efficient NO precursors upon oxidation by NO-synthase II or activated mouse macrophages Biochemistry 41 9286 9292
23. Renodon-Corniere A Dijols S Perollier C Lefevre-Groboillot D Boucher JL Attias R Sari MA Stuehr D Mansuy D 2002 N-Aryl-N'-hydroxyguanidines, a new class of NO-donors after selective oxidation by nitric oxide synthases: structure activity relationship J Med Chem 45 944 954
24. Mansuy D Boucher JL 2004 Alternative nitric oxide-producing substrates for NO synthases Free Rad Biol Med 37 1105 1121
25. Presta A Siddhanta U Wu C Sennequier N Huang L Abu-Soud HM Erzurum S Stuehr DJ 1998 Comparative functioning of dihydro- and tetrahydropterins in supporting electron transfer, catalysis, and subunit dimerization in inducible nitric oxide synthase Biochemistry 37 298 310
26. Wang ZQ Wei CC Ghosh S Meade AL Hemann C Hille R Stuehr DJ 2001 A conserved tryptophan in nitric oxide synthase regulates heme-dioxy reduction by tetrahydrobiopterin Biochemistry 40 12819 12825
27. Sorlie M Gorren A Marchal S Shimizu T Lange R Anderson KK Mayer B 2003 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 48602 48610
28. ω-hydroxy- l -arginine complex of inducible nitric oxide synthase oxygenase dimer with active and inactive pterins Biochemistry 39 4608 4621
29. Li H Shimizu H Flinspach M Jamal J Yang W Xian M Cai T Wen EZ Jia Q Wang PG et al. 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
30. Raman CS Li H Martasek P Southan G Masters BS Poulos TL 2001 Crystal structure of nitric oxide synthase bound to nitro indazole reveals a novel inactivation mechanism Biochemistry 40 13448 13455
31. Li H Raman CS Martasek P Masters BS Poulos TL 2001 Crystallographic studies on endothelial nitric oxide synthase complexed with nitric oxide and mechanism-based inhibitors Biochemistry 40 5399 5406
32. Fedorov R Ghosh DK Schlichting I 2003 Crystal structures of cyanide complexes of P450cam and the oxygenase domain of inducible nitric oxide synthase-structural models of the short-lived oxygen complexes Arch Biochem Biophys 409 25 31
33. Crane BR Arvai AS Ghosh DK Wu C Getzoff ED Stuehr DJ Tainer JA 1998 Structure of nitric oxide synthase oxygenase dimer with pterin and substrate Science 279 2121 2126
34. Lefevre-Groboillot D Boucher JL Stuehr DJ Mansuy D 2005 Relationship between the structure of guanidines and N-hydroxyguanidines, their binding to inducible nitric oxide synthase (iNOS) and their iNOS-catalysed oxidation to FEBS J 272 3172 3183
35. Berka V Yeh HC Gao D Kiran F Tsai AL 2004 Redox function of tetrahydrobiopterin and effect of 1-arginine on oxygen binding in endothelial nitric oxide synthase Biochemistry 43 13137 13148
36. Marchal S Gorren ACF Sorlie M Andersson KK Mayer B Lange R 2004 Evidence of two distinct oxygen complexes of reduced endothelial nitric oxide synthase J Biol Chem 279 19824 19831
37. Marchal S Lange R Sorlie M Andersson KK Gorren ACF Mayer B 2004 CO Exchange of the oxyferrous complexes of endothelial nitric oxide synthase oxygenase domain in the presence of 4-amino-tetrahydrobiopterin J Inorg Biochem 98 1217 1222
38. Yamamoto Y Kojima S 1991 The Chemistry of Amidines and Imidates Patai S Rappoport Z, eds), pp. 485 526 John Wiley and Sons Ltd Chichester, UK
39. Wei CC Crane BR Stuehr DJ 2003 Tetrahydrobiopterin radical enzymology Chem Rev 103 2365 2383
40. Stuehr DJ Santolini J Wang ZQ Wei CC Adak S 2004 Update on mechanism and catalytic regulation in the NO synthases J Biol Chem 279 36167 36170
41. ω-hydroxyarginine oxidation by nitric oxide synthase J Biol Chem 278 46668 46673
42. Patel KB Stratford MRL Wardman P Everett SA 2002 Oxidation of tetrahydrobiopterin by biological radicals and scavenging of the tetrahydrobiopterin radical by ascorbate Free Rad Biol Med 32 203 211
43. Ghosh DK Wu C Pitters E Moloney M Werner ER Mayer B Stuehr DJ 1997 Characterization of the inducible nitric oxide synthase oxygenase domain identifies a 49 amino acid segment required for subunit dimerization and tetrahydrobiopterin interaction Biochemistry 36 10609 10619
44. 2 intermediate in early catalysis Methods Enzymol 354 320 338