Sub-atomic resolution crystal structure of cholesterol oxidase: What atomic resolution crystallography reveals about enzyme mechanism and the role of the FAD cofactor in redox activity

Journal of Molecular Biology

Volumn 326, Issue 5, 2003, Pages 1635-1650

  Lario, Paula I ^a,b   Sampson, Nicole ^c   Vrielink, Alice ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MCGILL UNIVERSITY   (Canada)

^c STONY BROOK UNIVERSITY   (United States)

Author keywords

Atomic resolution crystallography; Cholesterol oxidase; Flavoenzyme; Oxygen tunnel; Protein flexibility

Indexed keywords

CHOLESTEROL OXIDASE; ENZYME; FLAVIN OXIDASE; FLAVINE ADENINE NUCLEOTIDE; OXIDOREDUCTASE; OXYGEN; UNCLASSIFIED DRUG;

ARTICLE; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ENZYME LOCALIZATION; ENZYME MECHANISM; ENZYME STRUCTURE; HYDROGEN BOND; HYDROPHOBICITY; MOLECULAR DYNAMICS; OPTICAL RESOLUTION; OXIDATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; R FACTOR;

EID: 0037424631     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(03)00054-8     Document Type: Article

References (56)

1. Ohta T., Fujishiro K., Yamaguchi K., Tamura Y., Aisaka K., Uwajima T., Hasegawa M. Sequence of gene choB encoding cholesterol oxidase of Brevibacterium sterolicum: comparison with choA of Streptomyces sp. SA-COO. Gene. 103:1991;93-96.
2. Uwajima T., Yagi H., Nakamurs S., Terada O. Isolation and crystallization of extracellular 3β-hydroxysteroid oxidase of Brevibacterium sterolicum nov. sp. Agric. Biol. Chem. 37:1973;2345-2350.
3. MacLachlan J., Wotherspoon A.T.L., Ansell R.O., Brooks C.J.W. Cholesterol oxidase: sources, physical properties and analytical applications. J. Steroid Biochem. Mol. Biol. 72:2000;169-195.
4. Aparicio J.F., Fouces R., Mendes M.V., Olivera N., Martin J.F. A complex multienzyme system encoded by five polyketide synthase genes is involved in the biosynthesis of the 26-membered polyene macrolide pimaricin in Streptomyces natalensis. Chem. Biol. 7:2000;895-905.
5. Navas J., Gonzalez-Zorn B., Ladron N., Garrido P., Vazquez-Boland J.A. Identification and mutagenesis by allelic exchange of choE, encoding a cholesterol oxidase from the intracellular pathogen Rhodococcus equi. J. Bacteriol. 183:2001;4796-4805.
6. Corbin D.R., Grebenok R.J., Ohnmeiss T.E., Greenplate J.T., Purcell J.P. Expression and chloroplast targeting of cholesterol oxidase in transgenic tobacco plants. Plant Physiol. 126:2001;1116-1128.
7. Shen Z., Corbin D.R., Greenplate J.T., Grebenok R.J., Galbraith D.W., Purcell J.P. Studies on the mode of action of cholesterol oxidase on insect midgut membranes. Arch. Insect Biochem. Physiol. 34:1997;429-442.
8. Ishizaki R., Hirayama N., Shinkawa H., Nimi O., Murooka Y. Nucleotide sequence of the gene for cholesterol oxidase from a Streptomyces sp. J. Bacteriol. 171:1989;596-601.
9. Yue Q.K., Kass I.J., Sampson N.S., Vrielink A. Crystals structure determination of cholesterol oxidase from Streptomyces and structural characterization of key active site mutants. Biochemistry. 38:1999;4277-4286.
10. Li J., Vrielink A., Brick P., Blow D.M. Crystal structure of cholesterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry. 32:1993;11507-11515.
11. Vrielink A., Lloyd L.F., Blow D.M. Crystal structure of cholesterol oxidase from Brevibacterium sterolicum refined at 1.8 Å resolution. J. Mol. Biol. 219:1991;533-554.
12. Yamashita M., Toyama M., Ono H., Fujii I., Hirayama N., Murooka Y. Separation of the two reactions, oxidation and isomerization, catalyzed by Streptomyces cholesterol oxidase. Protein Eng. 11:1998;1075-1081.
13. Yin Y., Sampson N.S., Vrielink A., Lario P.I. The presence of a hydrogen bond between asparagine 485 and the pi system of FAD modulates the redox potential in the reaction catalyzed by cholesterol oxidase. Biochemistry. 40:2001;13779-13787.
14. Coulombe R., Yue K.Q., Ghisla S., Vrielink A. Oxygen access to the active site of cholesterol oxidase through a narrow channel is gated by an Arg-Glu pair. J. Biol. Chem. 2001;276.
15. Iwata S., Ostermeier C., Ludwig B., Michel H. Structure at 2.8-Angstrom resolution of cytochrome C oxidase from Paracoccus Denitrificans. Nature. 376:1995;660-669.
16. Riistama S., Puustinen A., Garciahorsman A., Iwata S., Michel H., Wikstrom M. Channelling of dioxygen into the respiratory enzyme. Biochim. Biophys. Acta-Bioenerg. 1275:1996;1-4.
17. Soulimane T., Buse G., Bourenkov G.P., Bartunik H.D., Huber R., Than M.E. Structure and mechanism of the aberrant ba(3)-cytochrome c oxidase from Thermus thermophilus. EMBO J. 19:2000;1766-1776.
18. Eriksson M., Jordan A., Eklund H. Structure of Salmonella typhimurium nrdF ribonucleotide reductase in its oxidized and reduced forms. Biochemistry. 37:1998;13359-13369.
19. Stillman T.J., Hempstead P.D., Artymiuk P.J., Andrews S.C., Hudson A.J., Treffry A., et al. The high-resolution X-ray crystallographic structure of the ferritin (EcFtnA) of Escherichia coli; comparison with human H ferritin (HuHF) and the structures of the Fe(3+) and Zn(2+) derivatives. J. Mol. Biol. 307:2001;587-603.
20. Kass I.J., Sampson N.S. The isomerization catalyzed by Brevibacterium sterolicum cholesterol oxidase proceeds stereospecifically with one base. Biochem. Biophys. Res. Commun. 206:1995;688-693.
21. Kass I.J., Sampson N.S. Evaluation of the role of His447 in the reaction catalyzed by cholesterol oxidase. Biochemistry. 37:1998;17990-18000.
22. Sampson N.S., Kass I.J. Isomerization, but not oxidation, is suppressed by a single point mutation, E361Q, in the reaction catalyzed by cholesterol oxidase. J. Am. Chem. Soc. 119:1997;855-862.
23. Medina M., Vrielink A., Cammack R. ESR and electron nuclear double resonance characterization of the cholesterol oxidase from Brevibacterium sterolicum in its semiquinone state. Eur. J. Biochem. 222:1994;941-947.
24. Medina M., Vrielink A., Cammack R. Electron spin echo envelope modulation studies of the semiquinone anion radical of cholesterol oxidase from Brevibacterium sterolicum. FEBS Letters. 400:1997;247-251.
25. Breinlinger E.C., Keenan C.J., Rotello V.M. Modulation of flavin recognition and redox properties through donor atom-interactions. J. Am. Chem. Soc. 120:1998;8606-8609.
26. Cavelier G., Amzel L.M. Mechanism of NAD(P)H:quinone reductase: ab initio studies of reduced flavin. Proteins: Struct. Funct. Genet. 43:2001;420-432.
27. Trickey P., Basran J., Lian L.Y., Chen Z., Barton J.D., Sutcliffe M.J., et al. Structural and biochemical characterization of recombinant wild type and a C30A mutant of trimethylamine dehydrogenase from Methylophilus methylotrophus (sp. W(3)A(1)). Biochemistry. 39:2000;7678-7688.
28. Fraaije M.W., Mattevi A. Flavoenzymes: diverse catalysts with recurrent features. Trends Biochem. Sci. 25:2000;126-132.
29. Mesecar A.D., Stoddard B.L., Koshland D.E. Jr. Orbital steering in the catalytic power of enzymes: small structural changes with large catalytic consequences. Science. 277:1997;202-206.
30. Shan S.O., Herschlag D. The change in hydrogen bond strength accompanying charge rearrangement: implications for enzymatic catalysis. Proc. Natl Acad. Sci. USA. 93:1993;14474-14479.
31. Warshel A., Aqvist J. Electrostatic energy and macromolecular function. Annu. Rev. Biophys. Biophys. Chem. 20:1981;267-298.
32. Cavener D. GMC oxidoreuctases. A newly defined family of homologous proteins with diverse catalytic activities. J. Mol. Biol. 223:1992;811-814.
33. Wohlfahrt G., Witt S., Hendle J., Schomburg D., Kalisz H.M., Hecht H.J. 1.8 and 1.9 Å resolution structures of the Penicillium amagasakiense and Aspergillus niger glucose oxidases as a basis for modelling substrate complexes. Acta Crystallog. sect. D, Biol. Crystallog. 55:1999;969-977.
34. Su Q., Klinman J.P. Nature of oxygen activation in glucose oxidase from Aspergillus niger: the importance of electrostatic stabilization in superoxide formation. Biochemistry. 38:1999;8572-8581.
35. Lodi P.J., Knowles J.R. Neutral imidazole is the electrophile in the reaction catalyzed by triosephosphate isomerase: structural origins and catalytic implications. Biochemistry. 30:1991;6948-6956.
36. Zhao G., Song H., Chen Z.W., Mathews F.S., Jorns M.S. Monomeric sarcosine oxidase: role of histidine 269 in catalysis. Biochemistry. 41:2002;9751-9764.
37. Yin Y., Liu P., Anderson R.G., Sampson N.S. Construction of a catalytically inactive cholesterol oxidase mutant: investigation of the interplay between active site-residues glutamate 361 and histidine 447. Arch. Biochem. Biophys. 402:2002;235-242.
38. Umhau S., Pollegioni L., Molla G., Diederichs K., Welte W., Pilone M.S., Ghisla S. The X-ray structure of D-amino acid oxidase at very high resolution identifies the chemical mechanism of flavin-dependent substrate dehydrogenation. Proc. Natl Acad. Sci. USA. 97:2000;12463-12468.
39. Ghisla S., Thorpe C., Massey V. Mechanistic studies with general acyl-CoA dehydrogenase and butyryl-CoA dehydrogenase: evidence for the transfer of the beta-hydrogen to the flavin N(5)-position as a hydride. Biochemistry. 23:1984;3154-3161.
40. Pohl B., Raichle T., Ghisla S. Studies on the reaction mechanism of general acyl-CoA dehydrogenase. Determination of selective isotope effects in the dehydrogenation of butyryl-CoA. Eur. J. Biochem. 160:1986;109-115.
41. Basran J., Sutcliffe M.J., Scrutton N.S. Optimizing the Michaelis complex of trimethylamine dehydrogenase: identification of interactions that perturb the ionization of substrate and facilitate catalysis with trimethylamine base. J. Biol. Chem. 276:2001;42887-42892.
42. Dreveny I., Gruber K., Glieder A., Thompson A., Kratky C. The hydroxynitrile lyase from almond: a lyase that looks like an oxidoreductase. Structure. 9:2001;803-815.
43. Hecht H.J., Kalisz H.M., Hendle J., Schmid R.D., Schomburg D. Crystal structure of glucose oxidase from Aspergillus niger refined at 2.3 Å resolution. J. Mol. Biol. 229:1993;153-172.
44. 361 position in the reaction catalyzed by cholesterol oxidase. Bioorg. Med. Chem. Letters. 8:1998;2663-2668.
45. Thorpe C., Kim J.J. Structure and mechanism of action of the acyl-CoA dehydrogenases. Faseb J. 9:1995;718-725.
46. Vock P., Engst S., Eder M., Ghisla S. Substrate activation by acyl-CoA dehydrogenases: transition-state stabilization and pKs of involved functional groups. Biochemistry. 37:1998;1848-1860.
47. Rowland P., Bjornberg O., Nielsen F.S., Jensen K.F., Larsen S. The crystal structure of Lactococcus lactis dihydroorotate dehydrogenase A complexed with the enzyme reaction product throws light on its enzymatic function. Protein Sci. 7:1998;1269-1279.
48. 5-3-ketosteroid isomerase from Pseudomonas testosteroni. Biochemistry. 37:1998;8325-8330.
49. Pollegioni L., Wels G., Pilone M.S., Ghisla S. Kinetic mechanisms of cholesterol oxidase from Streptomyces hygroscopicus and Brevibacterium sterolicum. Eur. J. Biochem. 263:1999;1-13.
50. Otwinowski Z., Minor W. Carter C.W.J., Sweet R.M. Methods in Enzymology. Methods in Enzymology. vol. 276:1997;307-325 Academic Press, Boston.
51. Sheldrick G.M., Schneider T.R. Carter C.W.J., Sweet R.M. Methods in Enzymology. Methods in Enzymology. vol. 277:1997;319-343 Academic Press, Boston.
52. McRee D.E. XtalView/Xfit - a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125:1999;156-165.
53. Kraulis P. MOLSCRIPT:a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
54. Christopher, J.A. (1998). SPOCK: the structural properties observation and calculation kit (Program Manual). Texas A&M University.
55. Merritt E.A., Bacon D.J. Carter C.W.J., Sweet R.M. Methods in Enzymology. Methods in Enzymology. vol. 277:1997;505-525 Academic Press, New York.
56. Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., et al. The Protein Data Bank. Nucl. Acids Res. 28:2000;235-242.