Crystal Structure of Putidaredoxin Reductase from Pseudomonas putida, the Final Structural Component of the Cytochrome P450cam Monooxygenase

Journal of Molecular Biology

Volumn 336, Issue 4, 2004, Pages 889-902

  Sevrioukova, Irina F ^a   Li, Huiying ^a   Poulos, Thomas L ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BphA4 like proteins; Crystal structure; NAD binding; Putidaredoxin reductase; Redox partner interaction

Indexed keywords

APOPTOSIS INDUCING FACTOR; ARGININE; BACTERIAL PROTEIN; CAMPHOR 5 MONOOXYGENASE; DISULFIDE; FLAVINE ADENINE NUCLEOTIDE; FLAVOPROTEIN; OXIDOREDUCTASE; OXYGENASE; PUTIDAREDOXIN; PUTIDAREDOXIN REDUCTASE; PYROPHOSPHATE; RECOMBINANT PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TYROSINE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON TRANSPORT; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PSEUDOMONAS PUTIDA; SEQUENCE HOMOLOGY;

ESCHERICHIA COLI; MAMMALIA; PSEUDOMONAS; PSEUDOMONAS PUTIDA; PYRONIA TITHONUS;

EID: 1042264042     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2003.12.067     Document Type: Article

References (65)

1. Katagiri M., Ganguli B.N., Gunsalus I.C. A soluble cytochrome P450 functional in methylene hydroxylation. J. Biol. Chem. 243:1968;3543-3546.
2. Poulos T.L., Finzel B.C., Howard A.J. High-resolution crystal structure of cytochrome P450cam. J. Mol. Biol. 195:1987;687-700.
3. Pochapsky T.C., Ye X.M., Ratnaswamy G., Lyons T.A. An NMR-derived model for the solution structure of oxidized putidaredoxin, a 2Fe, 2S ferredoxin from Pseudomonas. Biochemistry. 33:1994;6424-6432.
4. Pochapsky T.C., Lyons T.A., Kazanis S., Arakaki T., Ratnaswamy G. A structure-based model for cytochrome P450cam-putidaredoxin interactions. Biochimie. 78:1996;723-733.
5. Aoki M., Ishimori K., Morishima I. NMR studies of putidaredoxin: associations of putidaredoxin with NADH-putidaredoxin reductase and cytochrome P450cam. Biochim. Biophys. Acta. 1386:1998;168-178.
6. Unger B.P., Gunsalus I.C., Sligar S.G. Nucleotide sequence of the Pseudomonas putida cytochrome P450cam gene and its expression in Escherichia coli. J. Biol. Chem. 261:1986;1158-1163.
7. Peterson J.A., Lorence M.C., Amarneh B. Putidaredoxin reductase and putidaredoxin. Cloning, sequence determination, and heterologous expression of the proteins. J. Biol. Chem. 265:1990;6066-6073.
8. Gunsalus I.C., Wagner G.C. Bacterial P450cam methylene monooxygenase components: cytochrome m, putidaredoxin, and putidaredoxin reductase. Methods Enzymol. 52:1978;166-188.
9. Roome P.W., Peterson J.A. The reduction of putidaredoxin reductase by reduced pyridine nucleotides. Arch. Biochem. Biophys. 266:1988;32-40.
10. Roome P.W., Peterson J.A. The oxidation of reduced putidaredoxin reductase by oxidized putidaredoxin. Arch. Biochem. Biophys. 266:1988;41-50.
11. Sevrioukova I.F., Hazzard J.T., Tollin G., Poulos T.L. Laser flash induced electron transfer in P450cam monooxygenase: putidaredoxin reductase-putidaredoxin interaction. Biochemistry. 40:2001;10592-10600.
12. Holden M., Mayhew M., Bunk D., Roitberg A., Vilker V. Probing the interactions of putidaredoxin with redox partners in camphor P450 5-monooxygenase by mutagenesis of surface residues. J. Biol. Chem. 272:1997;21720-21725.
13. Roome P.W. Jr, Philley J.C., Peterson J.A. Purification and properties of putidaredoxin reductase. J. Biol. Chem. 258:1983;2593-2598.
14. Geren L., Tuls J., O'Brien P., Millett F., Peterson J.A. The involvement of carboxylate groups of putidaredoxin in the reaction with putidaredoxin reductase. J. Biol. Chem. 261:1986;15491-15495.
15. Aoki M., Ishimori K., Fukada H., Takahashi K., Morishima I. Isothermal titration calorimetric studies on the associations of putidaredoxin to NADH-putidaredoxin reductase and P450cam. Biochim. Biophys. Acta. 1384:1998;180-188.
16. Aoki M., Ishimori K., Morishima I. Roles of negatively charged surface residues of putidaredoxin in interactions with redox partners in P450cam monooxygenase system. Biochim. Biophys. Acta. 1386:1998;157-167.
17. Senda T., Yamada T., Sakurai N., Kubota M., Nashizaki T., Masai T., et al. Crystal structure of NADH-dependent ferredoxin reductase component in biphenyl dioxygenase. J. Mol. Biol. 304:2000;397-410.
18. Harayama S., Kok M., Neidle E.L. Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46:1992;565-601.
19. Keseru G.M. A virtual high throughput screen for high affinity cytochrome P450cam substrates. Implications for in silico prediction of drug metabolism. J. Comput. Mol. Des. 15:2001;649-657.
20. French K.J., Strickler M.D., Rock D.A., Bennett G.A., Wahlstrom J.L., Goldstein B.M., et al. Benign synthesis of 2-ethylhexanoic acid by cytochrome P450cam: enzymatic, crystallographic, and theoretical studies. Biochemistry. 40:2001;9532-9538.
21. Manchester J.I., Ornstein R.L. Enzyme-catalyzed dehalogenation of pentachloroethane: why F87W-cytochrome P450cam is faster than wild type. Protein Eng. 8:1995;801-807.
22. Boyd D.R., Sheldrake G.N. The dioxygenase-catalyzed formation of vicinal cis-diols. Nature Prod. Rep. 15:1998;309-325.
23. Butler C.S., Mason J.R. Structure-function analysis of the bacterial aromatic ring-hydroxylating dioxygenases. Advan. Microb. Physiol. 38:1997;47-84.
24. Gibson D.T., Parales R.E. Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr. Opin. Biotechnol. 11:2000;236-243.
25. + reductase: prototype for a structurally novel flavoenzyme family. Science. 251:1991;60-66.
26. Schierbeek A.J., Swarte M.B., Dijkstra B.W., Vriend G., Read R.J., Hol W.G., et al. X-ray structure of lipoamide dehydrogenase from Azotobacter vilneladii determined by a combination of molecular and isomorphous replacement techniques. J. Mol. Biol. 206:1989;365-379.
27. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., et al. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-446.
28. Cande C., Cecconi F., Dessen P., Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115:2002;4727-4734.
29. Miramar M.D., Costantini P., Ravagnan L., Saraiva L.M., Haouzi D., Brothers G., et al. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol. Chem. 276:2001;16391-16398.
30. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., et al. The harlequin mouse mutation down-regulates apoptosis-inducing factor. Nature. 419:2002;367-374.
31. Mate M.J., Ortiz-Lombardia M., Boitel B., Haouz A., Tello D., Susin S.A., et al. Crystal structure of the mouse apoptosis-inducing factor AIF. Nature Struct. Biol. 9:2002;442-446.
32. Ye H., Cande C., Stephanoou N.C., Jiang S., Gurbuxani S., Larochette N., et al. DNA binding is required for the apoptogenic action of apoptosis inducing factor. Nature Struct. Biol. 9:2002;680-684.
33. Karplus P.A., Schulz G.E. Substrate binding and catalysis by glutathione reductase as derived from refined enzyme: substrate crystal structures at 2 Å resolution. J. Mol. Biol. 210:1989;163-180.
34. Sevrioukova I.F., Poulos T.L. Putidaredoxin reductase: a new function for an old protein. J. Biol. Chem. 277:2002;25831-25839.
35. Williams C.H. Jr. Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase, and mercuric ion reductase - a family of flavoenzyme transhydrogenases. Müller F. Chemistry and Biochemistry of Flavoenzymes. vol. 3:1991;121-211 CRC Press, Boca Raton.
36. Berry A., Scrutton N., Perham R. Switching kinetic mechanism and putative proton donor by directed mutagenesis of glutathione reductase. Biochemistry. 28:1989;1264-1269.
37. Krauth-Siegel R.L., Arscott L.D., Schonleben-Janas A., Schirmer R.H., Williams C.H. Jr. Role of active site tyrosine residues in catalysis by human glutathione reductase. Biochemistry. 37:1998;13968-13977.
38. Pai E.F., Schulz G.E. The catalytic mechanism of glutathione reductase as derived from x-ray diffraction analyses of reaction intermediates. J. Biol. Chem. 258:1983;1752-1757.
39. + at 2.45-Å resolution. Proteins: Struct. Funct. Genet. 13:1992;336-351.
40. Bailey S., Smith K., Fairlamb A.H., Hunter W.N. Substrate interactions between trypanothione reductase and N1-glutathionylspermidine disulphide at 0.28-nm resolution. Eur. J. Biochem. 213:1993;67-75.
41. Rice D.W., Schulz G.E., Guest J.R. Structural relationship between glutathione reductase and lipoamide dehydrogenase. J. Mol. Biol. 174:1984;483-496.
42. Wierenga R.K., Terpstra P., Hol W.G. Prediction of the occurrence of the ADP-binding beta alpha beta-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:1986;101-107.
43. Hanukoglu I., Gutfinger T. cDNA sequence of adrenodoxin reductase. Identification of NADP-binding sites in oxidoreductases. Eur. J. Biochem. 180:1989;479-484.
44. Scrutton N.S., Berry A., Perham R.N. Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature. 343:1990;38-43.
45. Yu S.W., Wang H.M., Poitras M.F., Coombs C., Bowers W.J., Federoff V.L., et al. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 297:2002;259-263.
46. Matthews R.G., Ballou D.P., Williams C.H. Jr. Reactions of pig heart lipoamide dehydrogenase with pyridine nucleotides. Evidence for an effector role for bound oxidized pyridine nucleotide. J. Biol. Chem. 254:1979;4974-4981.
47. O'Donnell M.E., Williams C.H. Jr. Reconstitution of Escherichia coli thioredoxin reductase with 1-deazaFAD. Evidence for 1-deazaFAD C4(a) adduct formation linked to the ionization of an active site base. J. Biol. Chem. 259:1984;2243-2251.
48. Miller S.M., Massey V., Ballou D., Williams C.H. Jr, Distefano M.D., Moore M.J., et al. Use of a site-directed triple mutant to trap intermediates: demonstration that the flavin C(4a)-thiol adduct and reduced flavin are kinetically competent intermediates in mercuric ion reductase. Biochemistry. 29:1990;2831-2841.
49. Sevrioukova I.F., Garsia C., Li H., Bhaskar B., Poulos T.L. Crystal structure of putidaredoxin, the [2Fe-2S] component of the P450cam monooxygenase system from Pseudomonas putida. J. Mol. Biol. 333:2003;377-392.
50. Bernhardt R., Gunsalus I.C. Reconstitution of cytochrome P4502B4 (LM2) activity with camphor and linalool monooxygenase electron donors. Biochem. Biophys. Res. Commun. 187:1992;310-317.
51. Ziegler G.A., Vonrhein C., Hanukoglu I., Schulz G.E. The structure of adrenodoxin reductase of mitochondrial P450 systems: electron transfer for steroid biosynthesis. J. Mol. Biol. 289:1999;981-990.
52. Lambeth J.D., Seybert D.W., Kamin H. Ionic effects on adrenal steroidogenic electron transport. The role of adrenodoxin as an electron shuttle. J. Biol. Chem. 254:1979;7255-7264.
53. Hanukoglu I., Privalle C.T., Jefcoate C.R. Mechanisms of ionic activation of adrenal mitochondrial cytochromes P450scc and P45011 beta. J. Biol. Chem. 256:1981;4329-4335.
54. Lambeth J.D., Geren L.M., Millett F. Adrenodoxin interaction with adrenodoxin reductase and cytochrome P450scc. Cross-linking of protein complexes and effects of adrenodoxin modification by 1-ethyl-3-(3- dimethylaminopropyl)carbodiimide. J. Biol. Chem. 259:1984;10025-10029.
55. Bernhardt R. Cytochrome P450: structure, function, and generation of reactive oxygen species. Rev. Physiol. Biochem. Pharmacol. 127:1996;137-221.
56. Vickery L.E. Molecular recognition and electron transfer in mitochondrial steroid hydroxylase systems. Steroids. 62:1997;124-127.
57. Muller J.J., Lapko A., Bourenkov G., Ruckpaul K., Heinemann U. Adrenodoxin reductase-adrenodoxin complex structure suggests electron transfer path in steroid biosynthesis. J. Biol. Chem. 276:2001;2786-2789.
58. Lambeth J.D., Kamin H. Adrenodoxin reductase.adrenodoxin complex. Flavin to iron-sulfur electron transfer as the rate-limiting step in the NADPH-cytochrome c reductase reaction. J. Biol. Chem. 254:1979;2766-2774.
59. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
60. The CCP4 suite: programs for protein crystallography. Acta Crystallog. sect. D. 50:1994;760-763.
61. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
62. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., GrosseKunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallog. sect. D. 54:1998;905-921.
63. Jeanmougin F., Thompson J.D., Gouy M., Higgins D.G., Gibson T.J. Multiple sequence alignment with Clustal X. Trends Biochem. Sci. 23:1998;403-405.
64. Pikuleva I.A., Tesh K., Waterman M.R., Kim Y.C. The tertiary structure of full-length bovine adrenodoxin suggests functional dimers. Arch. Biochem. Biophys. 373:2000;44-55.
65. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.