Nitric oxide synthase stabilizes the tetrahydrobiopterin cofactor radical by controlling its protonation state

Journal of the American Chemical Society

Volumn 132, Issue 33, 2010, Pages 11812-11823

  Stoll, Stefan ^a   Nejatyjahromy, Yaser ^a   Woodward, Joshua J ^b   Ozarowski, Andrew ^c   Marletta, Michael A ^b   Britt, R David ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FLORIDA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; COFACTORS; DENSITY FUNCTIONAL THEORY CALCULATIONS; ELECTRON DONORS; ELECTRON-TRANSFER; ENDOR SPECTROSCOPY; EXPERIMENTAL VALUES; FLAVIN REDUCTASE; G TENSORS; HEME PROPIONATES; HOMODIMERIC ENZYME; HYPERFINE TENSORS; L-ARGININE; MAGNETIC PARAMETERS; MULTIFREQUENCY EPR; NITRIC-OXIDE SYNTHASE; OXYGEN ACTIVATIONS; OXYGENASES; PROTONATED; PROTONATION STATE; SPIN DENSITY DISTRIBUTIONS; SYNTHASES; TETRAHYDROBIOPTERIN; TWO-ELECTRON OXIDATION; TWO-STEP REACTIONS;

AMINO ACIDS; CATALYTIC OXIDATION; COENZYMES; DENSITY FUNCTIONAL THEORY; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYMES; MAGNETIC DOMAINS; NITRIC OXIDE; OXYGEN; PORPHYRINS; PROTONATION; TENSORS;

ELECTRONS;

CYTOCHROME P450; NITRIC OXIDE SYNTHASE; PROPIONIC ACID; TETRAHYDROBIOPTERIN;

ANALYTICAL PARAMETERS; ARTICLE; CATALYSIS; DENSITY FUNCTIONAL THEORY; ELECTRON NUCLEAR DOUBLE RESONANCE; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; FREEZING; OXIDATION REDUCTION REACTION; PREDICTION; PROTEIN EXPRESSION; PROTON TRANSPORT;

ANIMALS; BINDING SITES; BIOCATALYSIS; BIOPTERIN; COMPUTER SIMULATION; ELECTRON SPIN RESONANCE SPECTROSCOPY; FREE RADICALS; MICE; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NITRIC OXIDE SYNTHASE TYPE II; PROTONS; QUANTUM THEORY;

EID: 77955837630     PISSN: 00027863     EISSN: 15205126     Source Type: Journal    
DOI: 10.1021/ja105372s     Document Type: Article

References (109)

1. Marletta, M. A. J. Biol. Chem. 1993, 268, 12231-12234
2. Alderton, W. K., Cooper, C. E., and Knowles, R. G. Biochem. J. 2001, 357, 593-615
3. Calabrese, V., Mancuso, C., Calvani, M., Rizzarelli, E., Butterfield, D. A., and Stella, A. M. G. Nat. Rev. Neurosci. 2007, 8, 766-775
4. Guix, F. X., Uribesalgo, I., Coma, M., and Muñoz, F. J. Prog. Neurobiol. 2005, 76, 126-152
5. Davydov, R., Ledbetter-Rogers, A., Martásek, P., Larukhin, M., Sono, M., Dawson, J. H., Masters, B. S. S., and Hoffman, B. M. Biochemistry 2002, 41, 10375-10381
6. Davydov, R., Sudhamsu, J., Lees, N. S., Crane, B. R., and Hoffman, B. M. J. Am. Chem. Soc. 2009, 131, 14493-14507
7. Hurshman, A. R., Krebs, C., Edmondson, D. E., Huynh, B. H., and Marletta, M. A. Biochemistry 1999, 38, 15689-15696
8. Wei, C.-C., Wang, Z.-Q., Wang, Q., Meade, A. L., Hemann, C., Hille, R., and Stuehr, D. J. J. Biol. Chem. 2001, 276, 315-219
9. Wei, C.-C., Crane, B. R., and Stuehr, D. J. Chem. Rev. 2003, 103, 2365-2384
10. Wei, C.-C., Wang, Z.-Q., Tejero, J., Yang, Y.-P., Hemann, C., Hille, R., and Stuehr, D. J. J. Biol. Chem. 2008, 283, 11734-11742
11. Woodward, J. J., NejatyJahromy, Y., Britt, R. D., and Marletta, M. A. J. Am. Chem. Soc. 2010, 132, 5105-5113
12. Kappock, T. J. and Caradonna, J. P. Chem. Rev. 1996, 96, 2659-2756
13. Wang, Z.-Q., Wei, C.-C., Santolini, J., Panda, K., Wang, Q., and Stuehr, D. J. Biochemistry 2005, 44, 4676-4690
14. Wang, Z.-Q., Wei, C.-C., Gosh, S., Meade, A. L., Hemann, C., Hille, R., and Stuehr, D. J. Biochemistry 2001, 40, 12819-12825
15. Doukov, T., Seravalli, J., Stezowski, J. J., and Ragsdale, S. W. Structure 2000, 8, 817-830
16. Hoke, K. R. and Crane, B. R. Nitric Oxide 2009, 20, 79-87
17. Bobst, A. Helv. Chim. Acta 1967, 50, 2222-2225
18. Bobst, A. Helv. Chim. Acta 1968, 51, 607-613
19. Patel, K. B., Stratford, M. R. L., Wardman, P., and Everett, S. A. Free Radical Biol. Med. 2002, 32, 203-211
20. Mayer, J. M. Annu. Rev. Phys. Chem. 2004, 55, 363-390
21. Huynh, M. H. V. and Mayer, T. J. Chem. Rev. 2007, 107, 5004-5064
22. Reece, S. Y., Woodward, J. J., and Marletta, M. A. Biochemistry 2009, 48, 5483-5491
23. Schmidt, P. P., Lange, R., Gorren, A. C. F., Werner, E. R., Mayer, B., and Andersson, K. K. J. Biol. Inorg. Chem. 2001, 6, 151-158
24. Hurshman, A. R. and Marletta, M. A. Biochemistry 2002, 41, 3439-3456
25. Woodward, J. J., Martin, N. J., and Marletta, M. A. Nat. Methods 2007, 4, 43-45
26. Hassan, A. K., Pardi, L. A., Krzystek, J., Sienkiewicz, A., Goy, P., Rohrer, M., and Brunel, L.-C. J. Magn. Reson. 2000, 142, 300-312
27. Stoll, S., Ozarowski, A., Britt, R. D., and Angerhofer, A. J. Magn. Reson. 2010, submitted.
28. Iwasaki, M. J. Magn. Reson. 1974, 16, 417-423
29. Stoll, S. and Schweiger, A. J. Magn. Reson. 2006, 178, 42-55
30. Stoll, S. and Britt, R. D. Phys. Chem. Chem. Phys. 2009, 11, 6614-6625
31. Crane, B. R., Arvai, A. S., Ghosh, D. K., Wu, C., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. Science 1998, 279, 2121-2126
32. Neese, F. J. Chem. Phys. 2001, 115, 11080-11096
33. Adamo, C. and Barone, V. J. Chem. Phys. 1999, 110, 6158-6170
34. Barone, V. In Recent Advances in Density Functional Methods, Part I; Chong, D. P., Ed.; World Scientific: Singapore, 1996.
35. Bec, N., Gorren, A. C. F., Mayer, B., Schmidt, P. P., Andersson, K. K., and Lange, R. J. Inorg. Biochem. 2000, 81, 207-211
36. Hurshman, A. R., Krebs, C., Edmondson, D. E., and Marletta, M. A. Biochemistry 2003, 42, 13287-13303
37. Sørlie, M., Gorren, A. C. F., Marchal, S., Shimizu, T., Lange, R., Andersson, K. K., and Mayer, B. J. Biol. Chem. 2003, 278, 48602-48610
38. Dalton, L. R. and Kwiram, A. L. J. Chem. Phys. 1972, 57, 1132-1145
39. Schweiger, A. Electron Nuclear Double Resonance of Transition Metal Complexes with Organic Ligands; Springer: Berlin, 1982; Vol. 51.
40. Thomann, H. and Bernardo, M. Methods Enzymol. 1993, 227, 118-189
41. Singel, D. J., van der Poel, W. A. J. A., Schnmidt, J., and van der Waals, J. H. J. Chem. Phys. 1984, 81, 5453-5461
42. Morton, J. R. and Preston, K. F. J. Magn. Reson. 1978, 30, 577-582
43. Koh, A. K. and Miller, D. J. At. Data Nucl. Data Tables 1985, 33, 235-253
44. Gordy, W. Theory and applications of electron spin resonance; Wiley: New York, 1980.
45. McConnell, H. M. and Strathdee, J. Mol. Phys. 1959, 2, 129-138
46. Beveridge, D. L. and McIver, J. W. J. Chem. Phys. 1971, 54, 4681-4690
47. Barfield, M. J. Chem. Phys. 1970, 53, 3836-3843
48. Edlund, O., Lund, A., Shiotani, M., Sohma, J., and Thuomas, K.-Å. Mol. Phys. 1976, 32, 49-69
49. Himo, F. and Eriksson, L. A. J. Phys. Chem. B 1997, 101, 9811-9819
50. Schleicher, E., Bittl, R., and Weber, S. FEBS J. 2009, 276, 4290-4303
51. Stoll, S., Gunn, A., Brynda, M., Sughrue, W., Kohler, A. C., Ozarowski, A., Fisher, A. J., Lagarias, J. C., and Britt, R. D. J. Am. Chem. Soc. 2009, 131, 1986-1995
52. Galander, M., Uppsten, M., Uhlin, U., and Lendzian, F. J. Biol. Chem. 2006, 281, 31743-31752
53. Fuchs, M. R., Schleicher, E., Schnegg, A., Kay, C. W. M., Törring, J., Bittl, R., Bacher, A., Richter, G., Möbius, K., and Weber, S. J. Phys. Chem. B. 2002, 106, 8885-8890
54. Schnegg, A., Kay, C. W. M., Schleicher, E., Hitomi, K., Todo, T., Möbius, K., and Weber, S. Mol. Phys. 2006, 140, 1627-1633
55. Okafuji, A., Schnegg, A., Schleicher, E., Möbius, K., and Weber, S. J. Phys. Chem. B 2008, 112, 3568-3574
56. Weber, S., Kay, C. W. M., Bacher, A., Richter, G., and Bittl, R. ChemPhysChem 2005, 6, 292-299
57. Ehrenberg, A., Hemmerich, P., Müller, F., Okada, T., and Viscontini, M. Helv. Chim. Acta 1967, 50, 411-416
58. Ehrenberg, A., Hemmerich, P., Müller, F., and Pfleiderer, W. Eur. J. Biochem. 1970, 16, 584-591
59. Westerling, J., Mager, H. I. X., and Berends, W. Tetrahedron 1977, 33, 2587-2594
60. Funahashi, Y., Kohzuma, T., Odani, A., and Yamauchi, O. Chem. Lett. 1994, 385-388
61. Vásquez-Vivar, J., Whitsett, J., Martásek, P., Hogg, N., and Kalyanaraman, B. Free Radical Biol. Med. 2001, 31, 975-985
62. Kuzkaya, N., Weissmann, N., Harrison, D. G., and Dikalov, S. J. Biol. Chem. 2003, 278, 22546-22554
63. Mansuy, D., Mathieu, D., Battioni, P., and Boucher, J.-L. J. Porphyrins Phthalocyanines 2004, 8, 265-278
64. Mathieu, D., Frapart, Y.-M., Bartoli, J. F., Boucher, J.-L., Battioni, P., and Mansuy, D. Chem. Commun. 2004, 54-55
65. Adhikary, A., Khanduri, D., and Sevilla, M. D. J. Am. Chem. Soc. 2009, 131, 8614-8619
66. Adhikary, A., Kumar, A., Becker, D., and Sevilla, M. D. J. Phys. Chem. B 2006, 110, 24171-24180s
67. Kacprzak, S. and Kaupp, M. J. Phys. Chem. B 2004, 108, 2464-2469
68. Sinnecker, S., Rajendran, A., Klamt, A., Diedenhofen, M., and Neese, F. J. Phys. Chem. A 2006, 110, 2235-2245
69. Ményhard, D. Chem. Phys. Lett. 2004, 392, 439-443
70. Morao, I., Periyasamy, G., Hillier, I. H., and Joule, J. A. Chem. Commun. 2006, 3525-3527
71. Ményhard, D. J. Phys. Chem. B 2009, 113, 3151-3159
72. Luykx, D. M. A. M., Duine, J. A., and de Vries, S. Biochemistry 1998, 37, 11366-11375
73. Kay, C. W. M., Schleicher, E., Hitomi, K., Todo, T., Bittl, R., and Weber, S. Magn. Reson. Chem. 2005, 43, S96-S102
74. Raman, C. S., Li, H., Martásek, P., Král, V., Masters, B. S. S., and Poulos, T. L. Cell 1998, 95, 939-950
75. Brown, D. H. Fused Pyrimidines. Part Three: Pteridines; Wiley: New York, 1988.
76. Eberlein, G., Bruice, T. C., Lazarus, R. A., Henrie, R., and Benkovic, S. J. J. Am. Chem. Soc. 1984, 106, 7916-7924
77. Kallen, R. G. and Jencks, W. P. J. Biol. Chem. 1966, 241, 5845-5850
78. Crane, B. R., Arvai, A. S., Ghosh, S., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. Biochemistry 2000, 39, 4608-4621
79. Werner, E. R., Pitters, E., Schmidt, K., Wachter, H., Werner-Felmayer, G., and Mayer, B. Biochem. J. 1996, 320, 193-196
80. Wei, C.-C., Wang, Z.-Q., Arvai, A. S., Hemann, C., Hille, R., Getzoff, E. D., and Stuehr, D. J. Biochemistry 2003, 42, 1969-1977
81. Evans, J. C., Huddler, D. P., Hilgers, M. T., Romanchuk, G., Matthews, R. G., and Ludwig, M. L. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 3729-3736
82. Smith, A. E. and Matthews, R. G. Biochemistry 2000, 39, 13880-13890
83. Alonso, H., Cummins, P. L., and Gready, J. E. J. Phys. Chem. B. 2009, 113, 14787-14796
84. Doukov, T. I., Hemmi, H., Drennan, C. L., and Ragsdale, S. W. J. Biol. Chem. 2007, 282, 6609-6618
85. Dixon, W. T. and Murphy, P. J. Chem. Soc., Faraday Trans. 1976, 72, 1221-1230
86. Bordwell, F. G. and Cheng, J.-P. J. Am. Chem. Soc. 1991, 113, 1736-1743
87. Das, T. N. J. Phys. Chem. A 2005, 109, 3344-3351
88. Faller, P., Coussias, C., Rutherford, A. W., and Un, S. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 8732-8735
89. Solar, S., Getoff, N., Surdhar, P. S., Armstrong, D. A., and Singh, A. J. Phys. Chem. 1991, 95, 3639-3643
90. Shafaat, H. S., Leigh, B. S., Tauber, M. J., and Kim, J. E. J. Phys. Chem. B 2009, 113, 382-388
91. Bent, D. V. and Hayon, E. J. Am. Chem. Soc. 1975, 97, 2612-2619
92. Aubert, C., Vos, M. H., Mathis, P., Eker, A. P. M., and Brettel, K. Nature 2000, 405, 586-590s
93. Langenbacher, T., Immeln, D., Dick, B., and Kottke, T. J. Am. Chem. Soc. 2009, 131, 14274-14280
94. Kiryutin, A. S., Morozova, O. B., Kuhn, L. T., Yurkovskaya, A. V., and Hore, P. J. J. Phys. Chem. B 2007, 111
95. Connor, H. D., Sturgeon, B. E., Mottley, C., Sipe, H. J., Jr., and Mason, R. P. J. Am. Chem. Soc. 2008, 130, 6381-6387
96. Jang, Y. H., Goddard, W. A., III, Noyes, K. T., Sowers, L. C., Hwang, S., and Chung, D. S. J. Phys. Chem. B. 2003, 107, 344-357
97. Kay, C. W. M., El Mkami, H., Molla, G., Pollegioni, L., and Ramsay, R. R. J. Am. Chem. Soc. 2007, 129, 16091-16097
98. Barquera, B., Morgan, J. E., Lukoyanov, D., Scholes, C. P., Gennis, R. B., and Nilges, M. J. J. Am. Chem. Soc. 2003, 125, 265-275
99. Blair, J. A. and Pearson, A. J. J. Chem. Soc., Perkin Trans. 2 1974, 80-88
100. Presta, A., Siddhanta, U., Wu, C., Sennequier, N., Huang, L., Abu-Soud, H. M., Erzurum, S., and Stuehr, D. J. Biochemistry 1998, 37, 298-310
101. Poulos, T. L. Nat. Prod. Rep. 2007, 24, 504-510
102. Guallar, V. J. Phys. Chem. B 2008, 112, 13460-13464
103. Brändén, G., Brändén, M., Schmidt, B., Mills, D. A., Ferguson-Miller, S., and Brzezinski, P. Biochemistry 2005, 44, 10466-10474
104. Battistuzzi, G., Borsari, M., Cowan, J. A., Eicken, C., Loschi, L., and Sola, M. Biochemistry 1999, 38, 5553-5562
105. Gorren, A. C. F., Sørlie, M., Andersson, K. K., Marchal, S., Lange, R., and Mayer, B. Methods Enzymol. 2005, 396, 456-466
106. Gorren, A. C. F. and Mayer, B. Curr. Drug Metab. 2002, 3, 133-157
107. de Visser, S. P. and Tan, L. S. J. Am. Chem. Soc. 2008, 130, 12961-12974
108. de Visser, S. P. Biochem. Soc. Trans. 2009, 37, 373-377
109. Cho, K.-B., Carvajal, M. A., and Shaik, S. J. Phys. Chem. B 2009, 113, 336-346