EPR and ENDOR characterization of the reactive intermediates in the generation of NO by cryoreduced oxy-nitric oxide synthase from Geobacillus stearothermophilus

Journal of the American Chemical Society

Volumn 131, Issue 40, 2009, Pages 14493-14507

  Davydov, Roman ^a   Sudhamsu, Jawahar ^b   Lees, Nicholas S ^a   Crane, Brian R ^b   Hoffman, Brian M ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SPECIES; BOUND WATERS; CITRULLINE; COMPOUND I; CRYOREDUCTION; ENDOR SPECTROSCOPY; EPR AND ENDOR; FERROHEME; GEOBACILLUS STEAROTHERMOPHILUS; HYDROXYLATED SUBSTRATES; L-ARGININE; MONOOXYGENASES; NITRIC-OXIDE SYNTHASE; OH GROUP; ONE-ELECTRON REDUCTIONS; PROTON DELIVERY; REACTION PATHWAYS; REACTIVE INTERMEDIATE; SIDE CHAINS; SUBSTRATE COMPLEXES; TETRAHYDROBIOPTERIN;

AMINO ACIDS; ANNEALING; CARBOXYLATION; COORDINATION REACTIONS; ELECTRON RESONANCE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; HEMOGLOBIN; HYDROXYLATION; IRON COMPOUNDS; NITRIC OXIDE; OXIDATION; PARAMAGNETIC RESONANCE; PORPHYRINS; POSITIVE IONS; PROTONS; QUANTUM THEORY;

SUBSTRATES;

ARGININE; CITRULLINE; FERRIC ION; HEMATIN; HEME; N HYDROXY ARGININE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXY NITRIC OXIDE SYNTHASE; UNCLASSIFIED DRUG; WATER;

ABSORPTION SPECTROSCOPY; ARTICLE; CONTROLLED STUDY; CRYOREDUCTION; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; GEOBACILLUS STEAROTHERMOPHILUS; HYDROXYLATION; PROTON TRANSPORT; REDUCTION;

ARGININE; BACILLUS STEAROTHERMOPHILUS; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CITRULLINE; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERROUS COMPOUNDS; HEME; MODELS, MOLECULAR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OXIDATION-REDUCTION;

EID: 70349921627     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja906133h     Document Type: Article

References (67)

1. Bruckdorfer, R. Mol. Aspects Med. 2005, 26, 3-31.
2. Alderton, W. K.; Cooper, C. E.; Knowles, R. G. Biochem. J. 2001, 357, 593-615.
3. Barbato, J. E.; Tzeng, E. J. Vasc. Surg. 2004, 40, 187-193.
4. Nott, A.; Riccio, A. Cell Cycle 2009, 8, 725-730.
5. Pfeiffer, S.; Mayer, B.; Hemmens, B. Angew. Chem., Int. Ed. 1999, 38, 1715-1731.
6. Yun, H. Y.; Dawson, V. L.; Dawson, T. M. Mol. Psychiatry 1997, 2, 300-310.
7. Marletta, M. A.; Hurshman, A. R.; Rusche, K. M. Curr. Opin. Chem. Biol. 1998, 2, 656-663.
8. Stuehr, D. J.; Santolini, J.; Wang, Z.-Q.; Wei, C.-C.; Adak, S. J. Biol. Chem. 2004, 279, 36167-36170.
9. Zhu, Y.; Silverman, R. B. Biochemistry 2008, 47, 2231-2243.
10. Sudhamsu, J.; Crane, B. R. Trends Microbiol. 2009, 17, 212-218.
11. Sudhamsu, J.; Crane, B. R. J. Biol. Chem. 2006, 281, 9623-9632.
12. Pant, K.; Crane, B. R. Biochemistry 2006, 45, 2537-2544.
13. Davydov, R.; Makris, T. M.; Kofman, V.; Werst, D. W.; Sligar, S. G.; Hoffman, B. M. J. Am. Chem. Soc. 2001, 123, 1403-1415.
14. Cho, K.-B.; Carvajal, M. A.; Shaik, S. J. Phys. Chem. B 2009, 113, 336-346.
15. Wei, C.-C.; Wang, Z.-Q.; Hemann, C.; Hille, R.; Stuehr, D. J. J. Biol. Chem. 2003, 278, 46668-46673.
16. Stuehr, D. J.; Wei, C.-C.; Wang, Z.; Hille, R. Dalton Trans. 2005, 3427-3435.
17. Woodward, J. J.; Chang, M. M.; Martin, N. I.; Marletta, M. A. J. Am. Chem. Soc. 2009, 131, 297-305.
18. Cai, T.; Xian, M.; Wang, P. G. Bioorg. Med. Chem. Lett. 2002, 12, 1507-1510.
19. Mukherjee, M.; Ray, A. R. Catal. Commun. 2007, 8, 1431-1437.
20. Clague, M. A.; Wishnok, J. S.; Marletta, M. A. Biochemistry 1997, 36, 14465-14473.
21. Robinet, J. J.; Cho, K.-B.; Gauld, J. W. J. Am. Chem. Soc. 2008, 130, 3328-3334.
22. Tejero, J.; Biswas, A.; Wang, Z.-Q.; Page, R. C.; Haque, M. M.; Hemann, C.; Zweier, J. L.; Misra, S.; Stuehr, D. J. J. Biol. Chem. 2008, 283, 33498-33507.
23. Davydov, R.; Kofman, V.; Fujii, H.; Yoshida, T.; Ikeda-Saito, M.; Hoffman, B. J. Am. Chem. Soc. 2002, 124, 1798-1808.
24. Davydov, R.; Ledbetter-Rogers, A.; Martasek, P.; Larukhin, M.; Sono, M.; Dawson, J. H.; Masters, B. S. S.; Hoffman, B. M. Biochemistry 2002, 41, 10375-10381.
25. Davydov, R.; Matsui, T.; Fujii, H.; Ikeda-Saito, M.; Hoffman, B. M. J. Am. Chem. Soc. 2003, 125, 16208-16209.
26. Davydov, R.; Razeghifard, R.; Im, S.-C.; Waskell, L.; Hoffman, B. M. Biochemistry 2008, 47, 9661-9666.
27. Marchal, S.; Gorren, A. C. F.; Sorlie, M.; Andersson, K. K.; Mayer, B.; Lange, R. J. Biol. Chem. 2004, 279, 19824-19831.
28. Glasoe, P. K.; Long, F. A. J. Phys. Chem. 1960, 64, 188-190.
29. Dixon, M. Biochim. Biophys. Acta, Bioenerg. 1971, 226, 241-258.
30. Adak, S.; Wang, Q.; Stuehr, D. J. J. Biol. Chem. 2000, 275, 17434-17439.
31. Hoffman, B. M. Acc. Chem. Res. 1991, 24, 164-170.
32. Salerno, J. C.; Martasek, P.; Williams, R. F.; Masters, B. S. S. Biochemistry 1997, 36, 11821-11827.
33. Kominami, S.; Yamazaki, T.; Koga, T.; Hori, H. J. Biochem. (Tokyo) 1999, 126, 756-761.
34. Salerno, J. C.; McMillan, K.; Masters, B. S. S. Biochemistry 1996, 35, 11839-11845.
35. Davydov, R.; Chemerisov, S.; Werst, D. E.; Rajh, T.; Matsui, T.; Ikeda- Saito, M.; Hoffman, B. M. J. Am. Chem. Soc. 2004, 126, 15960-15961.
36. Davydov, R.; Behrouzian, B.; Smoukov, S.; Stubbe, J.; Hoffman, B. M.; Shanklin, J. Biochemistry 2005, 44, 1309-1315.
37. Denisov, I. G.; Makris, T. M.; Sligar, S. G. J. Biol. Chem. 2001, 276, 11648-11652.
38. Migita, C. T.; Salerno, J. C.; Masters, B. S. S.; Martásek, P.; Ikeda-Saito, M. Biochemistry 1997, 36, 10987-10992.
39. Frauenfelder, H.; Young, R. D. Comments Mol. Cell. Biophys. 1986, 3, 347-372.
40. Tierney, D. L.; Huang, H.; Martásek, P.; Masters, B. S. S.; Silverman, R. B.; Hoffman, B. M. Biochemistry 1999, 38, 3704-3710.
41. Lefevre-Groboillot, D.; Frapart, Y.; Desbois, A.; Zimmermann, J.-L.; Boucher, J.-L.; Gorren, A. C. F.; Mayer, B.; Stuehr, D. J.; Mansuy, D. Biochemistry 2003, 42, 3858-3867.
42. Davydov, R.; Perera, R.; Jin, S.; Yang, T.-C.; Bryson, T. A.; Sono, M.; Dawson, J. H.; Hoffman, B. M. J. Am. Chem. Soc. 2005, 127, 1403-1413.
43. Davydov, R.; Kofman, V.; Nocek, J.; Noble, R. W.; Hui, H.; Hoffman, B. M. Biochemistry 2004, 43, 6330-6338.
44. Davydov, R.; Satterlee, J. D.; Fujii, H.; Sauer-Masarwa, A.; Busch, D. H.; Hoffman, B. M. J. Am. Chem. Soc. 2003, 125, 16340-16346.
45. Unno, M.; Chen, H.; Kusama, S.; Shaik, S.; Ikeda-Saito, M. J. Am. Chem. Soc. 2007, 129, 13394-13395.
46. Hersleth, H.-P.; Hsiao, Y.-W.; Ryde, U.; Goerbitz, C. H.; Andersson, K. K. Biochem. J. 2008, 412, 257-264.
47. Li, H.; Igarashi, J.; Jamal, J.; Yang, W.; Poulos, T. L. JBIC, J. Biol. Inorg. Chem. 2006, 11, 753-768.
48. Schlichting, I.; Berendzen, J.; Chu, K.; Stock, A. M.; Maves, S. A.; Benson, D. E.; Sweet, B. M.; Ringe, D.; Petsko, G. A.; Sligar, S. G. Science 2000, 287, 1615-1622.
49. Makris, T. M.; von Koenig, K.; Schlichting, I.; Sligar, S. G. Biochemistry 2007, 46, 14129-14140.
50. Kappl, R.; Höhn-Berlage, M.; Hüttermann, J.; Bartlett, N.; Symons, M. C. R. Biochim. Biophys. Acta 1985, 827, 327-343.
51. Cho, K.-B.; Derat, E.; Shaik, S. J. Am. Chem. Soc. 2007, 129, 3182-3188.
52. Chen, H.; Hirao, H.; Derat, E.; Schlichting, I.; Shaik, S. J. Phys. Chem. B 2008, 112, 9490-9500.
53. de Visser, S. P.; Tan, L. S. J. Am. Chem. Soc. 2008, 130, 12961-12974.
54. Li, H.; Raman, C. S.; Martásek, P.; Masters, B. S. S.; Poulos, T. L. Biochemistry 2001, 40, 5399-5406.
55. Gorren, A. C. F.; Schmidt, K.; Mayer, B. Biochemistry 2002, 41, 7819-7829.
56. Rousseau, D. L.; Li, D.; Couture, M.; Yeh, S.-R. J. Inorg. Biochem. 2005, 99, 306-323.
57. Li, D.; Kabir, M.; Stuehr, D. J.; Rousseau, D. L.; Yeh, S.-R. J. Am. Chem. Soc. 2007, 129, 6943-6951.
58. Kabir, M.; Sudhamsu, J.; Crane, B. R.; Yeh, S.-R.; Rousseau, D. L. Biochemistry 2008, 47, 12389-12397.
59. Feldman, P. L.; Griffith, O. W.; Hong, H.; Stuehr, D. J. J. Med. Chem. 1993, 36, 491-496.
60. Li, H.; Poulos, T. L. J. Inorg. Biochem. 2005, 99, 293-305.
61. Abu-Soud, H. M.; Wu, C.; Ghosh, D. K.; Stuehr, D. J. Biochemistry 1998, 37, 3777-3786.
62. Renodon, A.; Boucher, J.-L.; Wu, C.; Gachhui, R.; Sari, M.-A.; Mansuy, D.; Stuehr, D. Biochemistry 1998, 37, 6367-6374.
63. Gerber, N. C.; Rodriguez-Crespo, I.; Nishida, C. R.; Ortiz de Montellano, P. R. J. Biol. Chem. 1997, 272, 6285-6290.
64. Sorlie, M.; Gorren, A. C. F.; Marchal, S.; Shimizu, T.; Lange, R.; Andersson, K. K.; Mayer, B. J. Biol. Chem. 2003, 278, 48602-48610.
65. Cho, K.-B.; Gauld, J. W. J. Am. Chem. Soc. 2004, 126, 10267-10270.
66. Pufahl, R. A.; Wishnok, J. S.; Marletta, M. A. Biochemistry 1995, 34, 1930-1941.
67. Fukuto, J. M. Methods Enzymol. 1996, 268, 365-375.