Substrate-ligand interactions in geobacillus stearothermophilus nitric oxide synthase

Biochemistry

Volumn 47, Issue 47, 2008, Pages 12389-12397

  Kabir, Mariam ^a   Sudhamsu, Jawahar ^b   Crane, Brian R ^b   Yeh, Syun Ru ^a   Rousseau, Denis L ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIOLOGY; BOND STRENGTH (MATERIALS); CORRELATION METHODS; ENZYMES; HEMOGLOBIN; MAMMALS; NITRIC OXIDE; OXIDES; OXYGEN; PORPHYRINS; POSITIVE IONS; RAMAN SCATTERING; RAMAN SPECTROSCOPY; RESONANCE; STRENGTH OF MATERIALS;

ACTIVE SITES; BACILLUS SUBTILIS; BOND STRENGTHS; CHEMICAL ENVIRONMENTS; CITRULLINE; DIOXYGEN; ELECTROSTATIC POTENTIALS; FREE FORMS; HEME POCKETS; INVERSE CORRELATIONS; LIGAND INTERACTIONS; MECHANISTIC DIFFERENCES; OXYGEN CHEMISTRIES; RESONANCE RAMAN SPECTROSCOPIES; RESONANCE RAMAN SPECTRUMS; STEAROTHERMOPHILUS; STRETCHING FREQUENCIES; STRETCHING MODES; STRUCTURAL FEATURES; STRUCTURAL PROBES; SUBSTRATE BINDINGS; SUBSTRATE BOUNDS; SYNTHASE;

SUBSTRATES;

ARGININE; CARBON MONOXIDE; CYSTEINE; HEME; IRON; NITRIC OXIDE SYNTHASE; OXYGEN;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; CHEMICAL BOND; CONTROLLED STUDY; ENZYME CONFORMATION; ENZYME STABILITY; ENZYME SUBSTRATE; EXCITATION; GEOBACILLUS STEAROTHERMOPHILUS; MAMMAL; MOLECULAR INTERACTION; MOLECULAR PROBE; PRIORITY JOURNAL; RAMAN SPECTROMETRY;

ABSORPTION; ARGININE; BACILLACEAE; BIOPTERIN; CARBON MONOXIDE; COENZYMES; IRON; LIGANDS; NITRIC OXIDE SYNTHASE; OXYGEN; PROTEIN BINDING; SPECTRUM ANALYSIS, RAMAN; SULFUR;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); GEOBACILLUS STEAROTHERMOPHILUS; MAMMALIA;

EID: 56749134247     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi801491e     Document Type: Article

References (51)

1. Stuehr, D. J. (1999) Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1411, 217-230.
2. Siddhanta, U., Presta, A., Fan, B., Wolan, D., Rousseau, D. L., and Stuehr, D. J. (1998) 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, 18950-18958.
3. Panda, K., Ghosh, S., and Stuehr, D. J. (2001) Calmodulin activates intersubunit electron transfer in the neuronal nitric-oxide synthase dimer. J. Biol. Chem. 276, 23349-23356.
4. Crane, B. R., Arvai, A. S., Gachhui, R., Wu, C., Ghosh, D. K., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. (1997) The structure of nitric oxide synthase oxygenase domain and inhibitor complexes. Science 278, 425-431.
5. Crane, B. R., Arvai, A. S., Ghosh, D. K., Wu, C., Getzoff, E. D., Stuehr, D. J., and Tainer, J. A. (1998) Structure of nitric oxide synthase oxygenase dimer with pterin and substrate. Science 279, 2121-2126.
6. Raman, C. S., Li, H., Martasek, P., Krai, V., Masters, B. S., and Poulos, T. L. (1998) Crystal Structure of Constitutive Endothelial Nitric Oxide Synthase A Paradigm for Pterin Function Involving a Novel Metal Center. Cell 95, 939-950.
7. Li, H., Raman, C. S., Glaser, C. B., Blasko, E., Young, T. A., Parkinson, J. F., Whitlow, M., and Poulos, T. L. (1999) Crystal structures of zinc-free and -bound heme domain of human inducible nitric-oxide synthase. Implications for dimer stability and comparison with endothelial nitric-oxide synthase. J. Biol. Chem. 274, 21276-21284.
8. Li, H., Shimizu, H., Flinspach, M., Jamal, J., Yang, W., Xian, M., Cai, T., Wen, E. Z., Jia, Q., Wang, P. G., and Poulos, T. L. (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.
9. Fedorov, R., Hartmann, E., Ghosh, D. K., and Schlichting, I. (2003) Structural basis for the specificity of the nitric-oxide synthase inhibitors W1400 and Nω-propyl-L-Arg for the inducible and neuronal isoforms. J. Biol. Chem. 278, 45818-45825.
10. Chen, P. F., Tsai, A. L., Berka, V., and Wu, K. K. (1996) Endothelial nitric-oxide synthase. Evidence for bidomain structure and successful reconstitution of catalytic activity from two separate domains generated by a baculovirus expression system. J. Biol. Chem. 271, 14631-14635.
11. Wang, J., Stuehr, D. J., Ikeda-Saito, M., and Rousseau, D. L. (1993) Heme coordination and structure of the catalytic site in nitric oxide synthase. J. Biol. Chem. 268, 22255-22258.
12. Wang, J., Stuehr, D. J., and Rousseau, D. L. (1995) Tetrahydrobiopterin- deficient nitric oxide synthase has a modified heme environment and forms a cytochrome P-420 analogue. Biochemistry 34, 7080-7087.
13. Wang, J., Stuehr, D. J., and Rousseau, D. L. (1997) Interactions between substrate analogues and heme ligands in nitric oxide synthase. Biochemistry 36, 4595-4606.
14. Fan, B., Wang, J., Stuehr, D. J., and Rousseau, D. L. (1997) NO synthase isozymes have distinct substrate binding sites. Biochemistry 36, 12660-12665.
15. Tierney, D. L., Martasek, P., Doan, P. E., Masters, B. S. S., and Hoffman, B. M. (1998) Location of guanidino nitrogen of L-arginine substrate bound to neuronal nitric oxide synthase (nNOS): Determination by Q-band ENDOR spectroscopy. J. Am. Chem. Soc. 120, 2983-2984.
16. Couture, M., Adak, S., Stuehr, D. J., and Rousseau, D. L. (2001) Regulation of the properties of the heme-NO complexes in nitricoxide synthase by hydrogen bonding to the proximal cysteine. J. Biol. Chem. 276, 38280-38288.
17. Adak, S., Crooks, C., Wang, Q., Crane, B. R., Tainer, J. A., Getzoff, E. D., and Stuehr, D. J. (1999) Tryptophan 409 controls the activity of neuronal nitric-oxide synthase by regulating nitric oxide feedback inhibition. J. Biol. Chem. 274, 26907-26911.
18. Adak, S., Wang, Q., and Stuehr, D. J. (2000) Molecular basis for hyperactivity in tryptophan 409 mutants of neuronal NO synthase. J. Biol. Chem. 275, 17434-17439.
19. Adak, S., and Stuehr, D. J. (2001) A proximal tryptophan in NO synthase controls activity by a novel mechanism. J. Inorg. Biochem. 83, 301-308.
20. Voegtle, H. L., Sono, M., Adak, S., Pond, A. E., Tomita, T., Perera, R., Goodin, D. B., Ikeda-Saito, M., Stuehr, D. J., and Dawson, J. H. (2003) Spectroscopic characterization of five- and six-coordinate ferrous-NO heme complexes. Evidence for heme Fe-proximal cysteinate bond cleavage in the ferrous-NO adducts of the Trp-409Tyr/Phe proximal environment mutants of neuronal nitric oxide synthase. Biochemistry 42, 2475-2484.
21. Rousseau, D. L., Li, D., Couture, M., and Yeh, S. R. (2005) Ligand-protein interactions in nitric oxide synthase. J. Inorg. Biochem. 99, 306-323.
22. Kers, J. A., Wach, M. J., Krasnoff, S. B., Widom, J., Cameron, K. D., Bukhalid, R. A., Gibson, D. M., Crane, B. R., and Loria, R. (2004) Nitration of a peptide Phytotoxin by bacterial nitric oxide synthase. Nature 429, 79-82.
23. Chen, Y., and Rosazza, J. P. (1995) Purification and characterization of nitric oxide synthase (NOSNoc) from a Nocardia species. J. Bacteriol. 177, 5122-5128.
24. Buddha, M. R., Keery, K. M., and Crane, B. R. (2004) An unusual tryptophanyl tRNA synthetase interacts with nitric oxide synthase in Deinococcus radiodurans. Proc. Natl. Acad. Sci. U.S.A. 101, 15881-15886.
25. Santolini, J., Roman, M., Steuhr, D. J., and Mattioli, T. A. (2006) Resonance Raman Study of Bacillus subtilis NO synthase-like protein: Similarities and differences with mammalian NO synthases. Biochemistry 45, 1489-1489.
26. Salard, I., Mercey, E., Rekka, E., Boucher, J. L., Nioche, P., Mikula, I., Martasek, P., Raman, C. S., and Mansuy, D. (2006) Analogies and surprising differences between recombinant nitric oxide synthase-like proteins from Staphylococcus aureus and Bacillus anthracis in their interactions with L-arginine analogs and iron ligands. J. Inorg. Biochem. 100, 2024-2033.
27. Chartier, F. J., and Couture, M. (2004) Stability of the heme environment of the nitric oxide synthase from Staphylococcus aureus in the absence of pterin cofactor. Biophys. J. 87, 1939-1950.
28. Sudhamsu, J., and Crane, B. R. (2006) Structure and reactivity of a thermostable prokaryotic nitric-oxide synthase that forms a long-lived oxy-heme complex. J. Biol. Chem. 281, 9623-9632.
29. Pant, K., Bilwes, A. M., Adak, S., Stuehr, D. J., and Crane, B. R. (2002) Structure of a nitric oxide synthase heme protein from Bacillus subtilis. Biochemistry 41, 11071-11079.
30. Bird, L. E., Ren, J., Zhang, J., Foxwell, N., Hawkins, A. R., Charles, I. G., and Stammers, D. K. (2002) Crystal Structure of SANOS, a Bacterial Nitric Oxide Synthase Oxygenase Protein from Staphylococcus aureus. Structure 10, 1687-1696.
31. Crane, B. R., Rosenfeld, R. J., Arvai, A. S., Ghosh, D. K., Ghosh, S., Tainer, J. A., Stuehr, D. J., and Getzoff, E. D. (1999) N-Terminal domain swapping and metal ion binding in nitric oxide synthase dimerization. EMBO J. 18, 6271-6281.
32. Li, D., Kabir, M., Stuehr, D. J., Rousseau, D. L., and Yeh, S. R. (2007) Substrate- and isoform-specific dioxygen complexes of nitric oxide synthase. J. Am. Chem. Soc. 129, 6943-6951.
33. Rousseau, D. L., Li, D., Hayden, E. Y., Deng, H., and Yeh, S. R. (2008) Ligand-Protein Interactions in Mammalian Nitric Oxide Synthase. In The Smallest Biomolecules: Diatomics and their Interactions with Hemeproteins (Ghosh, A., Ed.) pp 465-497, Elsevier, Amsterdam.
34. Griffith, O. W., and Stuehr, D. J. (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu. Rev. Physiol. 57, 707-736.
35. Pufahl, R. A., Wishnok, J. S., and Marietta, M. A. (1995) Hydrogen peroxide-supported oxidation of NG-hydroxy-L-arginine by nitric oxide synthase. Biochemistry 34, 1930-1941.
36. Li, H., Igarashi, J., Jamal, J., Yang, W., and Poulos, T. L. (2006) Structural studies of constitutive nitric oxide synthases with diatomic ligands bound. J. Biol. Inorg. Chem. 11, 753-768.
37. Pant, K., and Crane, B. R. (2006) Nitrosyl-heme structures of Bacillus subtilis nitric oxide synthase have implications for understanding substrate oxidation. Biochemistry 45, 2537-2544.
38. Li, D., Stuehr, D. J., Yeh, S. R., and Rousseau, D. L. (2004) Heme distortion modulated by ligand-protein interactions in inducible nitric-oxide synthase. J. Biol. Chem. 279, 26489-26499.
39. Rousseau, D. L., Li, D., Couture, M., and Yeh, S. R. (2005) Ligand-protein interactions in nitric oxide synthase. J. Inorg. Biochem. 99, 306-323.
40. Yu, N.-T., and Kerr, E. A. (1987) in Biological Applications of Raman Spectroscopy: Resonance Raman Spectra of Hemes and Metalloproteins (Spiro, T. G., Ed.) pp 39-96, Wiley, New York.
41. Egawa, T., and Yeh, S. R. (2005) Structural and functional properties of hemoglobins from unicellular organisms as revealed by resonance Raman spectroscopy. J. Inorg. Biochem. 99, 72-96.
42. Spiro, T. G., and Wasbotten, I. H. (2005) CO as a vibrational probe of heme protein active sites. J. Inorg. Biochem. 99, 34-44.
43. Xu, C., Ibrahim, M., and Spiro, T. G. (2008) DFT analysis of axial and equatorial effects on heme-CO vibrational modes: Applications to CooA and H-NOX heme sensor proteins. Biochemistry 47, 2379-2387.
44. cam. J. Chem. Phys. 87, 4273-4284.
45. Champion, P. M., Stallard, B. R., Wagner, G. C., and Gunsalus, I. C. (1982) Resonance Raman detection of an iron-sulfur bond in cytochrome P450cam. J. Am. Chem. Soc. 104, 5469-5472.
46. Unno, M., Christian, J. F., Sjodin, T., Benson, D. E., Macdonald, I. D., Sligar, S. G., and Champion, P. M. (2002) Complex formation of cytochrome P450cam with putidaredoxin. Evidence for protein-specific interactions involving the proximal thiolate ligand. J. Biol. Chem. 277, 2547-2553.
47. Schelvis, J. P., Berka, V., Babcock, G. T., and Tsai, A. L. (2002) Resonance Raman detection of the Fe-S bond in endothelial nitric oxide synthase. Biochemistry 41, 5695-5701.
48. Dawson, J. H. (1988) Probing structure-function relations in heme-containing oxygenases and peroxidases. Science 240, 433-439.
49. Pant, K., and Crane, B. R. (2005) Structure of a loose dimer: An intermediate in nitric oxide synthase assembly. J. Mol. Biol. 352, 932-940.
50. Couture, M., Stuehr, D. J., and Rousseau, D. L. (2000) The ferrous dioxygen complex of the oxygenase domain of neuronal nitric-oxide synthase. J. Biol. Chem. 275, 3201-3205.
51. Unno, M., Christian, J. F., Benson, D. E., Gerber, N. C., Sligar, S. G., and Champion, P. M. (1997) Resonance Raman Investigations of Cytochrome P450cam Complexed with Putidaredoxin. J. Am. Chem. Soc. 119, 6614-6620.