Structure of Aspergillus niger epoxide hydrolase at 1.8 Å resolution: Implications for the structure and function of the mammalian microsomal class of epoxide hydrolases

Structure

Volumn 8, Issue 2, 2000, Pages 111-122

  Zou, Jinyu ^a   Hallberg, B Martin ^a   Bergfors, Terese ^a   Oesch, Franz ^b   Arand, Michael ^b   Mowbray, Sherry L ^c   Jones, T Alwyn ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

^c SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

Drug metabolism; Epoxide hydrolase; MAD; Microsomal epoxide hydrolases; X ray crystallography

Indexed keywords

EPOXIDE HYDROLASE;

ARTICLE; ASPERGILLUS NIGER; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME STRUCTURE; HYDROGEN BOND; MAMMAL; MICROSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FOLDING; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

ASPERGILLUS; ASPERGILLUS NIGER; MAMMALIA;

EID: 0034651639     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(00)00087-3     Document Type: Article

References (65)

1. Armstrong R.N. Kinetic and chemical mechanism of epoxide hydrolase. Drug Metab. Rev. 31:1999;71-86.
2. Oesch F. Mammalian epoxide hydrases: inducible enzymes catalysing the inactivation of carcinogenic and cytotoxic metabolites derived from aromatic and olefinic compounds. Xenobiotica. 3:1973;305-340.
3. Ota K., Hammock B.D. Cytosolic and microsomal epoxide hydrolases: differential properties in mammalian liver. Science. 207:1980;1479-1481.
4. Knehr M., Thomas H., Arand M., Gebel T., Zeller H.D., Oesch F. Isolation and characterization of a cDNA encoding rat liver cytosolic epoxide hydrolase and its functional expression in Escherichia coli. J. Biol. Chem. 268:1993;17623-17627.
5. Janssen D.B., Fries F., van der Ploeg J., Kazemier B., Terpstra P., Witholt B. Cloning of 1,2-dichloroethane degradation genes of Xanthobacter autotrophicus GJ10 and expression and sequencing of the dhlA gene. J. Bacteriol. 171:1989;6791-6799.
6. Arand M., Grant D.F., Beetham J.K., Friedberg T., Oesch F., Hammock B.D. Sequence similarity of mammalian epoxide hydrolases to the bacterial haloalkane dehalogenase and other related proteins. FEBS Lett. 338:1994;251-256.
7. Ollis D.L., Cheah E., Cygler M., Dijkstra B., Frolow F., Franken S.M., Goldman A.et al. The α/β hydrolase fold. Protein Eng. 5:1992;197-211.
8. Heikinheimo P., Goldman A., Jeffries C., Ollis D.L. Of barn owls and bankers: a lush variety of α/β hydrolases. Structure. 7:1999;141-146.
9. Franken S.M., Rozeboom H.J., Kalk K.H., Dijkstra B.W. Crystal structure of haloalkane dehalogenase: an enzyme to detoxify haolgenated alkanes. EMBO J. 10:1991;1297-1302.
10. Verschueren K.H.G., Seljée F., Rozeboom H.J., Kalk K.H., Dijkstra B.W. Crystallographic analysis of the catalytic mechanism of haloalkane dehalogenase. Nature. 363:1993;693-698.
11. Tsukada H., Blow D.M. Structure of α-chymotrypsin refined at 1.68 Å resolution. J. Mol. Biol. 184:1985;703-711.
12. Lacourciere G.M., Armstrong R.N. Microsomal and soluble epoxide hydrolases are members of the same family of C-X bond hydrolase enzymes. Chem. Res. Toxicol. 7:1994;121-124.
13. Pries F., Janssen D.B.et al. Site-directed mutagenesis and oxygen isotope incorporation studies of the nucleophilic aspartate of haloalkane dehalogenase. Biochemistry. 33:1994;1242-1247.
14. Pinot F., Hammock B.D.et al. Molecular and biochemical evidence for the involvement of the Asp333-His523 pair in catalytic mechanism of soluble epoxide hydrolase. J. Biol. Chem. 270:1995;7968-7974.
15. Arand M., Wagner H., Oesch F. Asp333, Asp495, and His523 form the catalytic triad of rat soluble epoxide hydrolase. J. Biol. Chem. 271:1996;4223-4229.
16. Laughlin L.T., Tzeng H.F., Lin S., Armstrong R.N. Mechanism of microsomal epoxide hydrolase. Semifunctional site-specific mutants affecting the alkylation half-reaction. Biochemistry. 37:1998;2897-2904.
17. Tzeng H.F., Laughlin L.T., Armstrong R.N. Semifunctional site-specific mutants affecting the hydrolytic half-reaction of microsomal epoxide hydrolase. Biochemistry. 37:1998;2905-2911.
18. Arand M., Oesch F.et al. Catalytic triad of microsomal epoxide hydrolase: replacement of Glu404 with Asp leads to a strongly increased turnover rate. Biochem. J. 337:1999;37-43.
19. Barbirato F., Verdoes J.C., de Bont J.A., van der Werf M.J. The Rhodococcus erythropolis DCL14 limonene-1,2-epoxide hydrolase gene encodes an enzyme belonging to a novel class of epoxide hydrolases. FEBS Lett. 438:1998;293-296.
20. Nardini M., Dijkstra B.W.et al. The X-ray structure of epoxide hydrolase from Agrobacterium radiobacter AD1. An enzyme to detoxify harmful epoxides. J. Biol. Chem. 274:1999;14579-14586.
21. Arand M., Oesch F. Cloning and molecular characterization of a soluble epoxide hydrolase from Aspergillus niger that is related to mammalian microsomal epoxide hydrolase. Biochem. J. 344:1999;273-280.
22. Morisseau C., Archelas A., Guitton C., Faucher D., Furstoss R., Baratti J.C. Purification and characterization of a highly enantioselective epoxide hydrolase from Aspergillus niger. Eur. J. Biochem. 263:1999;386-395.
23. Brünger A.T. Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature. 355:1992;472-475.
24. Lacourciere G.M., Armstrong R.N. The catalytic mechanism of microsomal epoxide hydrolase involves an ester intermediate. J. Am. Chem. Soc. 115:1993;10466-10467.
25. McGaughey G.B., Gagne M., Rappe A.K. pi-Stacking interactions. Alive and well in proteins. J. Biol. Chem. 273:1998;15458-15463.
26. Pedragosa-Moreau S., Archelas A., Furstoss R. Microbiological transformations. 32. Use of epoxide hydrolase mediated biohydrolysis as a way to enantiopure epoxides and vicinal diols: application to substituted styrene oxide derivatives. Tetrahedron. 52:1996;4593-4606.
27. Wang P., Meijer J., Guengerich F.P. Purification of human liver cytosolic epoxide hydrolase and comparison to the microsomal enzyme. Biochemistry. 21:1982;5769-5776.
28. Blée E., Schuber F. Occurrence of fatty acid epoxide hydrolases in soybean (Glycine max). Purification and characterization of the soluble form. Biochem. J. 282:1992;711-714.
29. Argiriadi M.A., Morisseau C., Hammock B.D., Christianson D.W. Detoxification of environmental mutagens and carcinogens: structure, mechanism, and evolution of liver epoxide hydrolase. Proc. Natl Acad. Sci. USA. 96:1999;10637-10642.
30. Puente X.S., Lopez-Otin C. The PLEES proteins: a family of structurally related enzymes widely distributed from bacteria to humans. Biochem. J. 322:1997;947-949.
31. Bernstein F.C., Tasumi M.et al. The Protein Data Bank: a computer-based archival file for macromolecular structures. J. Mol. Biol. 112:1977;535-542.
32. Pacifici G.M., Franchi M., Bencini C., Rane A. Valpromide inhibits human epoxide hydrolase. Brit. J. Clin. Pharmacol. 22:1986;269-274.
33. Oesch F., Daly J. Conversion of naphthalene to trans-naphthalene dihydrodiol: evidence for the presence of a coupled aryl monooxygenase-epoxide hydrase system in hepatic microsomes. Biochem. Biophys. Res. Commun. 46:1972;1713-1720.
34. Etter H.U., Richter C., Ohta Y., Winterhalter K.H., Sasabe H., Kawato S. Rotation and interaction with epoxide hydrolase of cytochrome P-450 in proteoliposomes. J. Biol. Chem. 266:1991;18600-18605.
35. Alves C., von Dippe P., Amoui M., Levy D. Bile acid transport into hepatocyte smooth endoplasmic reticulum vesicles is mediated by microsomal epoxide hydrolase, a membrane protein exhibiting two distinct topological orientations. J. Biol. Chem. 268:1993;20148-20155.
36. Honscha W., Platte H.D., Oesch F., Friedberg T. Relationship between the microsomal epoxide hydrolase and the hepatocellular transport of bile acids and xenobiotics. Biochem. J. 311:1995;975-979.
37. von Dippe P., Amoui M., Stellwagen R.H., Levy D. The functional expression of sodium-dependent bile acid transport in Madin-Darby canine kidney cells transfected with the cDNA for microsomal epoxide hydrolase. J. Biol. Chem. 271:1996;18176-18180.
38. Sprengart M.L., Fuchs E., Porter A.G. The downstream box: an efficient and independent translation initiation signal in Escherichia coli. EMBO J. 15:1996;665-674.
39. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989). Molecular cloning: a laboratory manual. 2nd ed. Vol. 1-3. Cold Spring Harbour Laboratory Press, Cold Spring Harbour.
40. McPherson A.J. Preparation and Analysis of Protein Crystals. 1982;John Wiley and Sons, New York.
41. Harlos K. Micro-bridges for sitting-drop crystallizations. J Appl. Crystallogr. 25:1992;536-538.
42. Jancarik J., Kim S.-H. Sparse matrix sampling: a screening method for crystallization of proteins. J. Appl. Crystallogr. 24:1991;409-411.
43. Bergfors, T. (1998). Crystallization of Proteins: Techniques, Strategies, and Tips. A Laboratory Manual. IUL Biotechnology Series, (Bergfors, T.M. ed) La Jolla, CA: International University Line.
44. Stura E., Wilson I. Seeding techniques. Ducruix A., Giegé R. Crystallization of Nucleic Acids and Proteins. 1992;IRL Press, Oxford.
45. Hendrickson W.A., Horton J.R., LeMaster D.M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three-dimensional structure. EMBO J. 9:1990;1665-1672.
46. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
47. Terwilliger T.C., Berendzen J. Automated structure solution for MIR and MAD. Acta Crystallogr. D. 55:1999;849-861.
48. Cowtan K. An automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallogr. 31:1994;34-38.
49. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D. 50:1994;760-763.
50. Jones T.A., Kjeldgaard M.O. Electron-density map interpretation. Methods Enzymol. 277:1997;173-208.
51. Kleywegt G.J., Jones T.A. Halloween... Masks and Bones. Bailey S., Hubbard R., Waller D. From First Map to Final Model. 1994;59-66 SERC Daresbury Laboratory, Warrington, UK.
52. 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 Crystallogr. A. 47:1991;110-119.
53. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W.et al., Warren G.L. Crystallography and NMR system (CNS): a new software suite for macromolecular structure determination. Acta Crystallogr. D. 54:1998;905-921.
54. Engh R.A., Huber R. Accurate bond and angle parameters for X-ray protein structure refinement. Acta Crystallogr. A. 47:1991;392-400.
55. Perrakis A., Sixma T.K., Wilson K.S., Lamzin V.S. wARP: improvement and extension of crystallographic phases by weighted averaging of multiple-refined dummy atomic models. Acta Crystallogr. D. 53:1997;448-455.
56. Lee B., Richards F.M. The interpretation of protein structures: estimation of static accessibility. J. Mol. Biol. 55:1971;379-400.
57. Shindyalov I.N., Bourne P.E. Protein structure alignment by incremental combinatorial extension (CE) of the optimal path. Protein Eng. 11:1998;739-747.
58. Kleywegt G.J. Use of non-crystallographic symmetry in protein structure refinement. Acta Crystallogr. D. 52:1996;842-857.
59. Kleywegt G.J., Jones T.A. Detecting folding motifs and similarities in protein structures. Methods Enzymol. 277:1997;525-545.
60. Kleywegt G.J., Jones T.A. Phi/Psi-cology: Ramachandran revisited. Structure. 4:1996;1395-1400.
61. Hecht H.J., Sobek H., Haag T., Pfeifer O., van Pée K.-H. The metal-ion-free oxidoreductase from Streptomyces aureofaciens has an α/β hydrolase fold. Nat. Struct. Biol. 1:1994;532-537.
62. Hofmann B., Tolzer S., Pelletier I., Altenbuchner J., van Pee K.H., Hecht H.J. Structural investigation of the cofactor-free chloroperoxidases. J. Mol. Biol. 279:1998;889-900.
63. Wagner U.G., Hasslacher M., Griengl H., Schwab H., Kratky C. Mechanism of cyanogenesis: the crystal structure of hydroxynitrile lyase from Hevea brasiliensis. Structure. 4:1996;811-822.
64. Medrano F.J., Alonso J., Garcia J.L., Romero A., Bode W., Gomis-Ruth F.X. Structure of proline iminopeptidase from Xanthomonas campestris pv. citri: a prototype for the prolyl oligopeptidase family. EMBO J. 17:1998;1-9.
65. Uppenberg J., Hansen M.T., Patkar S., Jones T.A. The sequence, crystal structure determination and refinement of two crystal forms of lipase B from Candida antarctica. Structure. 2:1994;293-308.