N-terminal domain swapping and metal ion binding in nitric oxide synthase dimerization

EMBO Journal

Volumn 18, Issue 22, 1999, Pages 6271-6281

  Crane, Brian R ^a,b   Rosenfeld, Robin J ^a   Arvai, Andrew S ^a   Ghosh, Dipak K ^c,d   Ghosh, Sanjay ^c   Tainer, John A ^a   Stuehr, Dennis J ^c   Getzoff, Elizabeth D ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^c LERNER RESEARCH INSTITUTE   (United States)

^d DUKE UNIVERSITY   (United States)

Author keywords

hairpin; Disulfide; Domain swapping; X ray structure; Zinc

Indexed keywords

METAL ION; NITRIC OXIDE SYNTHASE; TETRAHYDROBIOPTERIN; ZINC ION;

AMINO TERMINAL SEQUENCE; ARTICLE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTALLOGRAPHY; DIMERIZATION; DISULFIDE BOND; ELECTRON TRANSPORT; ENZYME BINDING; ENZYME CONFORMATION; ENZYME INDUCTION; ENZYME STRUCTURE; ENZYME SUBUNIT; HYDROGEN BOND; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION;

AMINO ACID SEQUENCE; ANIMALS; BINDING SITES; CONSERVED SEQUENCE; CRYSTALLOGRAPHY, X-RAY; CYSTEINE; DIMERIZATION; ELECTROSTATICS; HYDROGEN BONDING; MACROMOLECULAR SUBSTANCES; MICE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SOFTWARE; ZINC;

EID: 0033571222     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.22.6271     Document Type: Article

References (70)

1. Abu-Soud, H.M, Feldman, P.L., Clark, P. and Stuehr, D.J. (1994) Electron transfer in the nitric oxide synthases. J. Biol. Chem., 269, 32318-32326.
2. Beratan, D., Betts, J. and Onuchic, J. (1991) Protein electron-transfer rates set by the bridging secondary and tertiary structure. Science, 252, 1285-1288.
3. Berendji, D., Kolb-Bachofen, V., Meyer, K., Grapenthin, O., Weber, H., Wahn, V. and Kroncke, K. (1997) Nitric oxide mediates intracytoplasmic and intranuclear zinc release. FEBS Lett., 405, 37-41.
4. Berg, J. and Shi, Y. (1996) The galvanization of biology: a growing appreciation for the roles of zinc. Science, 271, 1081-1085.
5. Brünger, A.T., Kuriyan, J. and Karplus, M. (1987) Crystallographic R factor refinement by molecular dynamics. Science, 235, 458-460.
6. Burton, J., Slepnev, V. and DeCamilli, P. (1997) An evolutionarily conserved domain in a subfamily of rabs is crucial for the interaction with the guanyl nucleotide exchange factor mss4. J. Biol. Chem., 272, 3663-3668.
7. Capeillereblandin, C. (1995) Flavocytochrome-b (2) cytochrome c interactions - the electron-transfer reaction revisited. Biochemie, 77, 516-530.
8. Chen, P., Tsai, A. and Wu, K. (1995) Cysteine-99 of endothelial nitric-oxide synthase (NOS-III) is critical for tetrahydrobiopterin-dependent NOS-III stability and activity. Biochem. Biophys. Res. Commun., 215, 1119-1129.
9. Clark-Baldwin, K., Johnson, A., Chen, Y., Dekker, E. and Penner-Hahn, J. (1998) Structural characterization of the zinc site in Escherichia coli L-threonine dehydrogenase using extended X-ray absorption fine structure spectroscopy. Inorg. Chim. Acta, 276, 215-221.
10. Connolly, M.L. (1983) Solvent-accessible surfaces of proteins and nucleic acids. Science, 221, 709-713.
11. 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.
12. 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.
13. Demple, B. (1996) Redox signaling and gene control in the Escherichia coli soxRS oxidative stress regulon - a review. Gene, 179, 53-57.
14. Demple, B., Sedgwick, B., Robins, P., Totty, N., Waterfield, M. and Lindahl, T. (1985) Active-site and complete sequence of the suicidal methyltransferase that counters alkylation mutagenesis. Proc. Natl Acad. Sci. USA, 82, 2688-2692.
15. Eklund, H. et al. (1976) Three-dimensional structure of horse liver alcohol dehyrogenase at 2.4 Å resolution. J. Mol. Biol., 102, 27-59.
16. Fischmann, T. et al. (1999) Structural characterization of nitric oxide synthase isoforms reveals striking active-site conservation. Nature Struct. Biol., 6, 233-242.
17. Garrett, T., McKern, N., Lou, M., Frenkel, M., Bentley, J., Lovrecz, G., Elleman, T., Cosgrove, L. and Ward, C. (1998) Crystal structure of the first three domains of the type-1 insulin-like growth factor receptor. Nature, 394, 395-399.
18. Ghosh, D.K., Wu, C., Pitters, E., Moloney, M., Werner, E.R., Mayer, B. and Stuehr, D.J. (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.
19. Ghosh, D.K. et al. (1999) Inducible nitric oxide synthase: role of the N-terminal β-hairpin hook and pterin-binding segment in dimerization and tetrahydrobiopterin interaction. EMBO J., 18, 6260-6270.
20. Gilson, M.K., Rashin, A., Fine, R. and Honig, B. (1985) On the calculation of electrostatic interactions in proteins. J. Mol. Biol., 183, 503-516.
21. Gray, H.B. and Winkler, J.R. (1996) Electron transfer in proteins. Annu. Rev. Biochem., 65, 537-561.
22. Green, A., Parker, M., Conte, D. and Sarkar, B. (1998) Zinc finger proteins: a bridge between transition metals and gene regulation. J. Trace Elem. Exp. Med., 11, 103-118.
23. Griffith, O.W. and Stuehr, D.J. (1995) Nitric oxide synthases: properties and catalytic mechanism. Annu. Rev. Physiol., 57, 707-736.
24. Harapanhalli, R., Yaghmai, V., Giuliani, D., Howell, R. and Rao, D. (1996) Antioxidant effects of vitamin c in mice following X-irradiation. Res. Commun. Mol. Pathol. Pharmacol., 94, 271-287.
25. Heringa, J. and Taylor, W. (1997) Three-dimensional domain duplication, swapping and stealing. Curr. Opin. Struct. Biol., 7, 416-421.
26. Hillier, B., Christopherson, K., Prehods, K., Bredt, D. and Lim, W. (1999) Unexpected modes of PDZ domain scaffolding revealed by structure of nNOS-syntrophin complex. Science, 284, 812-815.
27. Holm, R., Kennepohl, P. and Solomon, E.I. (1996) Structural and functional aspects of metal sites in biology. Chem. Rev., 96, 2239-2314.
28. Honig, B. and Nicholls, A. (1995) Classical electrostatics in biology and chemistry. Science, 268, 1144-1149.
29. Iwasaki, T., Hori, H., Hayashi, Y. and Nishino, T. (1999) Modulation of the remote heme site geometry of recombinant neuronal nitric-oxide synthase by the N-terminal hook region. J. Biol. Chem., 274, 7705-7713.
30. Jacob, C., Maret, W. and Vallee, B. (1998) Control of zinc transfer between thionein, metallothionein and zinc proteins. Proc. Natl Acad. Sci. USA, 95, 3489-3494.
31. Jiang, L., Maret, W. and Vallee, B. (1998) The glutathione redox couple modulates zinc transfer from metallothionein to zinc-depleted sorbitol dehydrogenase. Proc. Natl Acad. Sci. USA, 95, 3483-3488.
32. Jones, G., Les, J., Symons, M. and Taiwo, F. (1987) Electron spin resonance studies of radiation damage to DNA and to proteins. Nature, 330, 727-773.
33. Jörnvall, H. (1973) Differences in thiol groups and multiple forms of rat liver alcohol dehydrogenase. Biochem. Biophys. Res. Commun., 53, 1096-1101.
34. Kroncke, K. and Kolb-Bachofen, V. (1999) Measurement of nitric oxide-mediated effects on zinc homeostasis and zinc finger transcription factors. Methods Enzymol., 301, 126-135.
35. Li, H., Raman, C., Glaser, C., Blasko, E., Young, T., Parkinson, J., Whitlow, M. and Poulos, T. (1999) Crystal structure of zinc-free and -bound heme domain of human inducible nitric-oxide synthase. J. Biol. Chem., 30, 21276-21284.
36. Lipinski, P. and Drapier, J. (1997) Interplay between ferritin metabolism, reactive oxygen species and nitric oxide. J. Biol. Inorg. Chem., 2, 559-566.
37. Lipscomb, W. (1994) Aspartate-transcarbamylase from Escherichia coli -activity and regulation. Adv. Enzymol. Mol. Biol., 68, 67-151.
38. Maret, W. and Vallee, B. (1998) Thiolate ligands in metallothionein confer redox activity on zinc clusters. Proc. Natl Acad. Sci. USA, 95, 3478-3482.
39. Marletta, M. (1994) Nitric oxide synthase: aspects concerning structure and catalysis. Cell, 78, 927-930.
40. Martasek, P. et al. (1998) The C331A mutant of neuronal nitric-oxide synthase is defective in arginine binding. J. Biol. Chem., 273, 34799-34805.
41. Masters, B.S.S., McMillan, K., Sheta, E.A., Nishimura, J.S., Roman, L.J. and Martasek, P. (1996) Neuronal nitric oxide synthase, a modular enzyme formed by convergent evolution: structure studies of a cysteine thiolate-liganded heme protein that hydroxylates L-arginine to produce NO as a cellular signal. FASEB J., 10, 552-558.
42. McRee, D.E. (1992) A visual protein crystallographic software system for XII/Xview. J. Mol. Graph., 10, 44-46.
43. McRee, D.E. (1999) XtalView/Xfit - A versatile program manipulating atomic coordinates and electron density. J. Struct. Biol., 125, 156-165.
44. Mines, G.A., Bjerrum, M.J., Hill, M.G., Casimiro, D.R., Chang, I., Winkler, J.R. and Gray, H.B. (1996) Rates of heme oxidation and reduction in Ru (His33)cytochrome c at very high driving forces. J. Am. Chem. Soc., 118, 1961-1965.
45. Mol, C., Parikh, S. and Tainer, J. (1998) Structural Phylogenetics of DNA Base Excision Repair. Springer, Berlin, Germany, Vol. 12, pp. 283-438.
46. Mouesca, J., Chen, J., Noodleman, L., Bashford, D. and Case, D. (1994) Density-functional Poisson-Boltzmann calculations of redox potentials for iron-sulfur clusters. J. Am. Chem. Soc., 116, 11898-11914.
47. Nurizzo, D. et al. (1997) N-terminal arm exchange is observed in the 2.15 Å crystal structure of oxidized nitrite reductase from Pseudomonas aeruginosa. Structure, 5, 1157-1171.
48. Ortiz de Montellano, P., Nishida, C., Rodriguez-Crespo, I. and Gerber, N. (1998) Nitric oxide synthase structure and electron transfer. Drug Metab. Disp., 26, 1185-1189.
49. Otwinowski, Z. (1993) In Sawyer, L., Isaacs, N. and Bailey, S. (eds), Data Collection and Processing. Science and Engineering Research Council, Warrington, UK, pp. 56-62.
50. Perry, J. and Marletta, M. (1998) Effects of transition metals on nitric oxide synthase catalysis. Proc. Natl Acad. Sci. USA, 95, 11101-11106.
51. Pfeiffer, S., Mayer, B. and Hemmens, B. (1999) Nitric oxide: chemical puzzles posed by a biological messenger. Angew. Chem. Int. Ed. Engl., 38, 1715-1731.
52. Piedrafita, D. and Liew, F. (1998) Nitric oxide: a protective or pathogenic molecule? Rev. Med. Microbiol., 9, 179-189.
53. Platzer, I. and Getoff, N. (1998) Vitamin C acts as radiation-protecting agent. Radiat. Phys. Chem., 51, 73-76.
54. Presta, A., Siddhanta, U., Wu, C., Sennequier, N., Huang, L., Abu-Soud, H.M., Erzurum, S. and Stuehr, D.J. (1997) Comparative functioning of dihydro- and tetrahydropterins in supporting electron transfer, catalysis and subunit dimerization in inducible nitric oxide synthase. Biochemistry, 37, 298-310.
55. Presta, A., Weber-Main, A., Stankovich, M. and Stuehr, D. (1998) Comparative effects of substrates and pterin cofactor on the heme midpoint potential in inducible and neuronal nitric oxide synthases. J. Am. Chem. Soc., 120, 9460-9465.
56. Raman, C., Li, H., Martasek, P., Kral, 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.
57. Samson, L. (1992) The suicidal DNA-repair methyltransferases of microbes. Mol. Microbiol., 6, 825-831.
58. Schlunegger, M., Bennett, M.J. and Eisenberg, D. (1997) Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. Adv. Protein Chem., 50, 61-122.
59. Sevrioukova, I., Li, H., Zhang, H., Peterson, J. and Poulos, T. (1999) Structure of a cytochrome p450-redox partner electron-transfer complex. Proc. Natl Acad. Sci. USA, 96, 1863-1868.
60. Siddhanta, U., Presta, A. Fan, B., Wolan, D., Rousseau, D. and Stuehr, D. (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.
61. Stuehr, D. (1997) Structure-function aspects in the nitric oxide synthases. Annu. Rev. Pharmacol. Toxicol., 18, 707-736.
62. Svoboda, P. and Harms-Ringdahl, M. (1999) Protection or sensitization by thiols or ascorbate in irradiated solutions of DNA or deoxyguanosine. Radiat. Res., 151, 605-616.
63. Symons, M. (1995) Electron spin resonance studies of radiation damage to DNA and to proteins. Radiat. Phys. Chem., 45, 837-845.
64. Tsukihara, T., Aoyama, H., Yamashita, E., Tomizaki, T., Yamaguchi, H., Shinzawaltoh, K., Nakashima, R., Yaono, R. and Yoshikawa, S. (1996) The whole structure of the 13-subunit oxidized cytochrome c oxidase at 2.8 Å. Science, 272, 1136-1144.
65. Vermilion, J., Ballou, D., Massey, V. and Coon, M. (1981) Separate roles for FMN and FAD in catalysis by liver microsomal NADPH-cytochrome P-450 reductase. J. Biol. Chem., 56, 266-277.
66. Wang, M., Roberts, D.L., Paschke, R., Shea, T.M., Masters, B.S.S. and Kim, J.J. (1997) Three-dimensional structure of NADPH-cytochrome P450 reductase: prototype for FMN- and FAD-containing enzymes. Proc. Natl Acad. Sci. USA, 94, 8411-8416.
67. Weiner, P.K. and Kollman, P.A. (1981) AMBER: assisted model building with energy refinement. A general program for modeling molecules and their interactions. J. Comput. Chem., 2, 287-303.
68. Wilker, J. and Lippard, S. (1995) Modeling the DNA methylphosphotriester repair site in Escherichia coli ada: why zinc and 4 cysteines. J. Am. Chem. Soc., 117, 8682-8683.
69. Wink, D. and Mitchell, J. (1998) Chemical biology of nitric oxide: insights into regulatory, cytotoxic and cytoprotective mechanisms of nitric oxide. Free Radic. Biol. Med., 25, 434-456.
70. Witteveen, C. Giovanelli, J., Yim, M., Gachhui, R., Stuehr, D. and Kaufman, S. (1998) Reactivity of the flavin semiquinone of nitric oxide synthase in the oxygenation of arginine to N-G-hydroxyarginine, the first step of nitric oxide synthesis. Biochem. Biophys. Res. Commun., 250, 36-42.