The structure of adrenodoxin reductase of mitochondrial P450 systems: Electron transfer for steroid biosynthesis

Journal of Molecular Biology

Volumn 289, Issue 4, 1999, Pages 981-990

  Ziegler, Gabriele A ^a   Vonrhein, Clemens ^a   Hanukoglu, Israel ^b   Schulz, Georg E ^a  

^a UNIVERSITY OF FREIBURG   (Germany)

^b ARIEL UNIVERSITY   (Israel)

Author keywords

Crystal structure; Disulfide oxidoreductase; Electron transferase; Flavoenzyme; MAD analysis

Indexed keywords

ADRENODOXIN; CYTOCHROME P450; FERREDOXIN NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE REDUCTASE; FLAVOPROTEIN; MITOCHONDRIAL ENZYME; RECOMBINANT ENZYME;

AMINO ACID SEQUENCE; ARTICLE; CATTLE; CONTROLLED STUDY; ELECTRON TRANSPORT; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; NONHUMAN; PRIORITY JOURNAL; SEQUENCE HOMOLOGY; STEROIDOGENESIS;

BOS TAURUS; BOVINAE;

EID: 0033057396     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.2807     Document Type: Article

References (51)

1. Abrahams J. P., Leslie A. G. W. Methods used in the structure determination of bovine mitochondrial F1 ATPasse. Acta Crystallog. sect. D. 52:1996;30-42.
2. Aoki M., Ishimori K., Morishima I. NMR studies of putidaredoxin: association of putidaredoxin with NADH-putidaredoxin reductase and cytochrome P 450cam. Biochim. Biophys. Acta. 1386:1998;168-178.
3. Bernhardt R. Cytochrome P 450: structure, function and generation of reactive oxygen species. Rev. Phys. Biochem. Pharmacol. 127:1996;137-221.
4. Brünger A. T. X-PLOR version 3. 1 a system for X-ray crystallography and NMR. 1993;Yale University Press, New Haven.
5. Chen Z. W., Koh M., Van Driessche G., Van Beeumen J. J., Bartsch R. G., Meyer T. E., Cusanovich M. A., Mathews F. S. The structure of flavocytochrome c sulfide dehydrogenase from a purple phototrophic bacterium. Science. 266:1994;430-432.
6. Acta Crystallog. sect. D. 50:1994;760-763.
7. Correll C. C., Batie C. J., Ballou D. P., Ludwig M. L. Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S]. Science. 258:1992;1604-1610.
8. Dai S., Saarinen M., Ramaswany S., Meyer Y., Jacquot J.-P., Eklund H. Crystal structure of Arabidopsis thaliana NADPH dependent thioredoxin reductase at 2.5 Å resolution. J. Mol. Biol. 264:1996;1044-1057.
9. de la Fortelle E., Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276:1997;472-493.
10. Gray H. B., Winkler J. R. Electron transfer in proteins. Annu. Rev. Biochem. 65:1996;537-561.
11. Hansen J. E., Lund O., Engelbrecht J., Bohr H., Nielson J. O., Hansen J.-E. S., Brunak S. Prediction of O -glycosylation of mammalian proteins: specificity patterns of UDP-GalNAc:polypeptide N -acetylgalactosaminyltransferase. Biochem. J. 308:1995;801-813.
12. Hanukoglu I. Steroidogenic enzymes: structure, function, and role in regulation of steroid hormone biosynthesis. J. Steroid Biochem. Mol. Biol. 43:1992;779-804.
13. Hanukoglu I., Gutfinger T. cDNA sequence of adrenodoxin reductase. Eur. J. Biochem. 180:1989;479-484.
14. Hanukoglu I., Privalle C. T., Jefcoate C. R. Mechanisms of ionic activation of adrenal mitochondrial cytochromes P-450scc and P-45011β J. Biol. Chem. 256:1981;4329-4335.
15. Hara T., Miyata T. Identification of a cross-linked peptide of a covalent complex between adrenodoxin reductase and adrenodoxin. J. Biochem. 110:1991;261-266.
16. Hasemann C. A., Kurumbail R. G., Boddupalli S. S., Peterson J. A., Deisenhofer J. Structure and function of cytochromes P 450: a comparative analysis of three crystal structures. Structure. 2:1995;41-62.
17. Hiwatashi A., Ichikawa Y., Maruya N., Yamano T., Aki K. Properties of crystalline reduced nicotinamide adenine dinucleotide phosphate-adrenodoxin reductase from bovine adrenocortical mitochondria. Biochemistry. 15:1976;3082-3090.
18. Holm L., Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233:1993;123-138.
19. Ichikawa Y., Hiwatashi A. The role of the sugar regions of components of the cytochrome P 450-linked mixed-function oxidase (monooxygenase) system of bovine adrenocortical mitochondria. Biochim. Biophys. Acta. 705:1982;82-91.
20. Ingelman M., Bianchi V., Eklund H. The three-dimensional structure of flavodoxin reductase from Escherichia coli at 1.7 Å resolution. J. Mol. Biol. 268:1997;147-157.
21. Ishimura K., Fujita H. Light and electron microscopic immunohistochemistry of the localization of adrenal steroidogenic enzymes. Microsc. Res. Tech. 36:1997;445-453.
22. Jones T. A., Zou J.-Y., Cowan S. W., Kjeldgaard M. Improved methods for building models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A. 47:1991;110-119.
23. Kabsch W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Crystallog. 21:1988;916-924.
24. +reductase: prototype for a structurally novel flavoenzyme family. Science. 251:1991;60-66.
25. +as studied by pulse radiolysis. Biochemistry. 34:1995;12932-12936.
26. Kuban R.-J., Marg A., Resch M., Ruckpaul K. Crystallization of bovine adrenodoxin reductase in a new unit cell and its crystallographic characterization. J. Mol. Biol. 234:1993;245-248.
27. Lambeth J. D., Seybert D. W., Kamin H. Ionic effects on adrenal steroidogenic electron transport. J. Biol. Chem. 254:1979;7255-7264.
28. Lambeth J. D., Seybert D. W., Lancaster J. R. Jr, Salerno J. C., Kamin H. Steroidogenic electron transport in adrenal cortex mitochondria. Mol. Cell. Biochem. 45:1982;13-31.
29. Lapko A., Müller A., Heese O., Ruckpaul K., Heinemann U. Preparation and crystallization of a cross-linked complex of bovine adrenodoxin and adrenodoxin reductase. Proteins: Struct. Funct. Genet. 28:1997;289-292.
30. Leslie A. G. W. Molecular data processing. Moras D., Podgarny A. D., Thierry J. C. Crystallographic Computing 5. 1990;50-61 Oxford University Press, Oxford.
31. Lu G., Campbell W. H., Schneider G., Lindqvist Y. Crystal structure of the FAD-containing fragment of corn nitrate reductase at 2.5 Å resolution: relationship to other flavoprotein reductases. Structure. 2:1994;809-821.
32. Massey V. Introduction: flavoprotein structure and mechanism. FASEB J. 9:1995;473-475.
33. +and adrenoferredoxin. J. Biol. Chem. 269:1994;8001-8006.
34. Müller A., Müller J. J., Muller Y. A., Uhlmann H., Bernhardt R., Heinemann U. New aspects of electron transfer revealed by the crystal structure of truncated bovine adrenodoxin, Adx(4-108). Structure. 6:1998;269-280.
35. 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.
36. 5reductase from pig liver at 2.4 Å resolution. Biochemistry. 34:1995;2763-2767.
37. Nonaka Y., Aibara S., Sugiyama T., Yamano T., Morita Y. A crystallographic investigation on NADPH-adrenodoxin oxidoreductase. J. Biochem. 98:1985;257-260.
38. Omura T., Sanders E., Estabrook R. W., Cooper D. Y., Rosenthal O. Isolation from adrenal cortex of a nonheme iron protein and a flavoprotein functional as a reduced triphosphopyridine nucleotide-cytochrome P-450 reductase. Archives Biochem. Biophys. 117:1966;660-673.
39. Pochapsky T. C., Ye X. M., Ratnaswamy G., Lyons T. A. An NMR-derived model for the solution structure of oxidized putidaredoxin, a 2-Fe, 2-S ferredoxin fromPseudomonas. Biochemistry. 33:1994;6424-6432.
40. Sagara Y., Wada A., Takata Y., Waterman M. R., Sekimizu K., Horiuchi T. Direct expression of adrenodoxin reductase in Escherichia coli and the functional characterization. Biol. Pharm. Bull. 16:1993;627-630.
41. Schulz G. E. Gene duplication in glutathione reductase. J. Mol. Biol. 138:1980;335-347.
42. Schulz G. E. Binding of nucleotides by proteins. Curr. Opin. Struct. Biol. 2:1992;61-67.
43. Schulz G. E., Schirmer R. H., Sachsenheimer W., Pai E. F. The structure of the flavoenzyme glutathione reductase. Nature. 273:1978;120-124.
44. Stehle T., Ahmed S. A., Claiborne A., Schulz G. E. Structure of NADH peroxidase from Streptococcus faecalis 10C1 refined at 2.16 Å resolution. J. Mol. Biol. 221:1991;1325-1344.
45. Suhara K., Nakayama K., Takikawa O., Katagiri M. Two forms of adrenodoxin reductase from mitochondria of bovine adrenal cortex. Eur. J. Biochem. 125:1982;659-664.
46. Uhlmann H., Kraft R., Bernhardt R. C-terminal region of adrenodoxin affects its structural integrity and determines differences in its electron transfer function to cytochrome P-450. J. Biol. Chem. 269:1994;22557-22564.
47. Vickery L. E. Molecular recognition and electron transfer in the mitochondrial steroid hydroxylase system. Steroids. 62:1997;124-127.
48. Vonrhein C., Schmidt U., Ziegler G. A., Schweiger S., Hanukoglu I., Schulz G. E. Chaperone-assisted expression of authentic bovine adrenodoxin reductase in Escherichia coli. FEBS Letters. 443:1999;167-169.
49. Waksmann G., Krishnan T. S. R., Williams C. H. Jr, Kuriyan J. Crystal structure of Escherichia coli thioredoxin reductase refined at 2 Å resolution. J. Mol. Biol. 236:1994;800-816.
50. Wang M., Roberts D. L., Paschke R., Shea T. M., Masters B. S. S., Kim J.-J. P. Three-dimensional structure of NADPH-cytochrome P 450 reductase: prototype for FMN- and FAD-containing enzymes. Proc. Natl Acad. Sci. USA. 94:1997;8411-8416.
51. Wartburton R. J., Seybert D. W. Structural and functional characterization of bovine adrenodoxin reductase by limited proteolysis. Biochim. Biophys. Acta. 1246:1995;39-46.