Heme-coordinating inhibitors of neuronal nitric oxide synthase. Iron-thioether coordination is stabilized by hydrophobic contacts without increased inhibitor potency

Journal of the American Chemical Society

Volumn 132, Issue 2, 2010, Pages 798-806

  Martell, Jeffrey D ^a   Li, Huiying ^b   Doukov, Tzanko ^c   Martásek, Pavel ^d,e   Roman, Linda J ^d   Soltis, Michael ^c   Poulos, Thomas L ^b   Silverman, Richard B ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SLAC NATIONAL ACCELERATOR LABORATORY   (United States)

^d UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

^e CHARLES UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYL GROUPS; BINDING CONFORMATIONS; FERROUS STATE; HEME ENZYME; HEME IRON; HEME LIGATION; HYDROPHOBIC CONTACT; NEURONAL NITRIC-OXIDE SYNTHASE (NNOS); NITRIC-OXIDE SYNTHASE; POTENTIAL INHIBITORS; THIOETHER LIGANDS; THIOETHER SULFUR; THIOETHERS; TYPE II;

CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; HEMOGLOBIN; HYDROPHOBICITY; IRON; LIGANDS; NITRIC OXIDE; SULFUR;

PORPHYRINS;

FERRIC ION; FERROUS ION; HEME; IMIDAZOLE; N(G) NITROARGININE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; SULFIDE;

ARTICLE; CRYSTALLOGRAPHY; DRUG STRUCTURE; HYDROPHOBICITY; SPECTROPHOTOMETRY;

CRYSTALLOGRAPHY, X-RAY; ENZYME INHIBITORS; HEME; HYDROPHOBICITY; IRON; MODELS, MOLECULAR; MOLECULAR STRUCTURE; NITRIC OXIDE SYNTHASE TYPE I; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP; SULFIDES;

EID: 74949117681     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja908544f     Document Type: Article

References (59)

1. Tezcan, F. A.; Winkler, J. R.; Gray, H. B. J. Am. Chem. Soc. 1998, 120, 13383-13388.
2. Voegtle, H. L.; Sono, M.; Adak, S.; Pond, A. E.; Tomita, T.; Perera, R.; Goodin, D. B.; Ikeda-Saito, M.; Stuehr, D. J.; Dawson, J. H. Biochemistry 2003, 42, 2475-2484.
3. Zhong, L.; Wen, X.; Rabinowitz, T. M.; Russell, B. S.; Karan, E. F.; Bren, K. L. Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 8637-8642.
4. Murray, S. G.; Hartley, F. R. Chem. Rev. 1981, 81, 365-414.
5. Smith, M.; McLendon, G. J. Am. Chem. Soc. 1981, 103, 4912-4921.
6. Schejter, A. In Cytochrome c: A Multidisciplinary Approach; Scott, R. A., Mauk, A. G., Eds.; University Science Books: Mill Valley, CA, 1996; pp 335-345.
7. Sono, M.; Andersson, L. A.; Dawson, J. H. J. Biol. Chem. 1982, 14, 8308-8320.
8. Sono, M.; Hager, L. P.; Dawson, J. H. J. Biol. Chem. 1984, 21, 13209-13216.
9. Nastainzcyk, W.; Ruf, H. H.; Ullrich, V. Eur. J. Biochem. 1975, 60, 615-620.
10. Bushnell, G. W.; Louie, G. V.; Brayer, G. D. J. Mol. Biol. 1990, 214, 585-595.
11. Aranda, R.; Worley, C. E.; Liu, M.; Bitto, E.; Cates, M. S.; Olson, J. S.; Lei, B.; Phillips, G. N., Jr. J. Mol. Biol. 2007, 374, 374-383.
12. Griffith, O. W.; Steuhr, D. J. Annu. Rev. Physiol. 1995, 57, 707-736.
13. Kerwin, J. E., Jr.; Heller, M. Med. Res. Rev. 1994, 14, 23-74.
14. Choi, D. W.; Rothman, S. M. Annu. Rev. Neurosci. 1990, 13, 171-182.
15. Crossin, K. L. Trends Biochem. Sci. 1991, 16, 81-2.
16. Ferrendellia, J. A.; Blank, A. C.; Gross, R. A. Brain Res. 1980, 200, 93-103.
17. Das, I.; Khan, N. S.; Puri, B. K.; Sooranna, S. R.; de Belleroche, J.; Hirsch, S. R. Biochem. Biophys. Res. Commun. 1995, 212, 375-80.
18. Thomsen, L. L.; Iversen, H. K.; Lassen, L. H.; Olesen, J. CNS Drugs 1994, 2, 417-22.
19. Dorheim, M.-A.; Tracey, W. R.; Pollock, J. S.; Grammas, P. Biochem. Biophys. Res. Commun. 1994, 205, 659-65.
20. Lee, Y.; Martasek, P.; Roman, L. J.; Masters, B. S. S.; Silverman, R. B. Bioorg. Med. Chem. 1999, 7, 1941-1951.
21. Crane, B. R.; Arvai, A. S.; Ghosh, D. K.; Wu, C.; Getzoff, E. D.; Stuehr, D. J.; Tainer, J. A. Science 1998, 279, 2121-2126.
22. Berghuis, A. M.; Brayer, G. D. J. Mol. Biol. 1992, 223, 959-976.
23. Matsuura, Y.; Takano, T.; Dickerson, R. E. J. Mol. Biol. 1982, 56, 389-409.
24. Narayanan, K.; Spack, L.; McMillan, K.; Kilbourn, R. G.; Hayward, M. A.; Masters, B. S.; Griffith, O. W. J. Biol. Chem. 1995, 270, 11103-11110.
25. Haines, D. C.; Chen, B.; Tomchick, D. R.; Bondlela, M.; Hedge, A.; Machius, M.; Peterson, J. A. Biochemistry 2008, 47, 3662-3670.
26. Rahman, M. N.; Vlahakis, J. Z.; Szarek, W. A.; Nakatsu, K.; Jia, Z. J. Med. Chem. 2008, 51, 5943-5952.
27. Litzinger, E. A.; Martásek, P.; Roman, L. J.; Silverman, R. B. Bioorg. Med. Chem. 2006, 14, 3185-3198.
28. Li, H.; Raman, C. S.; Martásek, P.; Král, V.; Masters, B. S. S.; Poulos, T. L. J. Inorg. Biochem. 2000, 81, 133-139.
29. Li, H.; Shimizu, H.; Flinspach, M.; Jamal, J.; Yang, W.; Xian, M.; Cai, T.; Wen, E. Z.; Jia, Q.; Wang, P. G.; Poulos, T. L. Biochemistry 2002, 41, 13868-13875.
30. Pinner, A.; Klein, F. Ber. Dtsch. Chem. Ges. 1877, 10, 1889-1897.
31. McMillan, K.; Masters, B. S. S. Biochemistry 1993, 32, 9875-9880.
32. Roman, L. J.; Sheta, E. A.; Martásek, P.; Gross, S. S.; Liu, Q.; Masters, B. S. S. Proc. Natl. Acad. Sci. U.S.A. 1995, 92, 8428-8432.
33. Frey, C.; Narayana, K.; McMillan, K.; Spack, L.; Gross, S. S.; Masters, B. S.; Griffith, O. W. J. Biol. Chem. 1994, 269, 26083-26091.
34. Hevel, J. M.; Marletta, M. A. Methods Enzymol. 1994, 233, 250-258.
35. Segel, I. H. Enzyme Kinetics; John Wiley and Sons: New York, 1975; p 105.
36. Babu, B. R.; Griffith, O. W. Curr. Opin. Chem. Biol. 1998, 2, 491-500.
37. Cowan, J. A.; Gray, H. B. Inorg. Chem. 1989, 28, 4554-4556.
38. Dawson, J. H.; Andersson, L. A.; Sono, M. J. Biol. Chem. 1983, 258, 13637-13645.
39. Nastainczyk, W.; Ruf, H.-H.; Ullrich, V. Chem.-Biol. Interact. 1976, 14, 251-263.
40. Beitlich, T.; Kuhnel, K.; Schulze-Briese, C.; Shoeman, R. L.; Schlichting, I. J. Synchrotron Radiat. 2007, 14, 11-23.
41. Narayanan, K.; Griffith, O. W. J. Med. Chem. 1994, 37, 885-887.
42. (a) Suzuki, N.; Higuchi, T.; Urano, Y.; Kikuchi, K.; Uekusa, H.; Ohashi, Y.; Uchida, T.; Kitagawa, T.; Nagano, T. J. Am. Chem. Soc. 1999, 121, 11571-11572.
43. (b) Ueyama, N.; Nishikawa, N.; Yamada, Y.; Okamura, T.; Nakamura, A. J. Am. Chem. Soc. 1996, 118, 12826-12827.
44. Yoshioka, S.; Takahashi, S.; Ishimori, K.; Morishima, I. J. Inorg. Biochem. 2000, 81, 141-151.
45. (a) Goodin, D. B. J. Biol. Inorg. Chem. 1996, 1, 360-363.
46. (b) Poulos, T. L. J. Biol. Inorg. Chem. 1996, 1, 356-359.
47. Paulat, F.; Lehnert, N. Inorg. Chem. 2007, 46, 1547-1549.
48. Xu, N.; Powell, D. R.; Cheng, L.; Richter-Addo, G. B. Chem. Commun. 2006, 19, 2030-2032.
49. Ellison, M. K.; Scheidt, W. R. J. Am. Chem. Soc. 1999, 121, 5210-5219.
50. Ohno, T.; Suzuki, N.; Dokoh, T.; Urano, Y.; Kikuchi, K.; Hirobe, M.; Higuchi, T.; Nagano, T. Inorg. Biochem. 2000, 82, 123-125.
51. McPhillips, T. M.; McPhillips, S. E.; Chiu, H. J.; Cohen, A. E.; Deacon, A. M.; Ellis, P. J.; Garman, E.; Gonzalez, A.; Sauter, N. K.; Phizackerley, R. P.; Soltis, S. M.; Kuhn, P. J. Synchrotron Radiat. 2002, 9, 401-406.
52. Otwinowski, Z.; Minor, W. Methods Enzymol. 1997, 276, 307-326.
53. Brunger, A. T.; Adams, P. D.; Clore, G. M.; DeLano, W. L.; Gros, P.; Grosse-Kunstleve, R. W.; Jiang, J.-S.; Kuszewski, J.; Nilges, M.; Pannu, N. S.; Read, R. J.; Rice, L. M.; Simonson, T.; Warren, G. L. Acta Crystallogr. 1998, D54, 905-921.
54. Jones, T. A.; Zou, J.-Y.; Cowan, S. W.; Kjeldgaarrd, M. Acta Crystallogr. 1991, A47, 110-119.
55. Emsley, P.; Cowtan, K. Acta Crystallogr. 2004, D60, 2126-2132.
56. Murshudov, G. N.; Vagin, A. A.; Dodson, E. J. Acta Crystallogr. 1997, D53, 240-255.
57. Winn, M. D.; Isupov, M. N.; Murshudov, G. N. Acta Crystallogr. 2001, D57, 122-133.
58. Hevel, J. M.; White, K. A.; Marletta, M. J. Biol. Chem. 1991, 266, 22789-22791.
59. Martasek, P.; Liu, Q.; Roman, L. J.; Gross, S. S.; Sessa, W. C.; Masters, B. S. S. Biochem. Biophys. Res. Commun. 1996, 219, 359-365.