Purification and characterization of a highly enantioselective epoxide hydrolase from Aspergillus niger

European Journal of Biochemistry

Volumn 263, Issue 2, 1999, Pages 386-395

  Morisseau, Christophe ^a,d   Archelas, Alain ^a   Guitton, Carole ^b   Faucher, Didier ^c   Furstoss, Roland ^a   Baratti, Jacques C ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b SANOFI   (France)

^c CRVA   (France)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Aspergillus niger; Diols; Enantioselectivity; Epoxide hydrolase; Regioselectivity

Indexed keywords

EPOXIDE HYDROLASE;

ARTICLE; ASPERGILLUS NIGER; ENANTIOMER; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME SUBSTRATE COMPLEX; HYDROLYSIS; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ANALYSIS;

AMINO ACID SEQUENCE; AMINO ACIDS; ASPERGILLUS NIGER; BASE SEQUENCE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPOXIDE HYDROLASES; EPOXY COMPOUNDS; HYDROGEN-ION CONCENTRATION; KINETICS; MODELS, CHEMICAL; MOLECULAR SEQUENCE DATA; TEMPERATURE; TIME FACTORS;

ASPERGILLUS NIGER;

EID: 0033565356     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.1999.00519.x     Document Type: Article

References (55)

1. 1. Oesch, F. (1972) Mammalian epoxide hydrases: inducible enzymes catalysing the inactivation of carcinogenic and cytotoxic metabolites derived from aromatic and olefinic compounds. Xenobiotica 3, 305-340.
2. 2. Watabe, T., Kanai, M., Isobe, M. & Ozawa, N. (1981) The hepatic microsomal biotransformation of Δ5-steroids to 5α,6β-glycols via α-and β-epoxides. J. Biol. Chem. 256, 2900-2907.
3. 3. Rädmark, O., Shimizu, T., Jörnvall, H. & Samuelsson, B. (1984) Leukotriene A4 hydrolase in human leukocytes. Purification and properties. J. Biol. Chem. 259, 12339-12345.
4. 4. Pace-Asciak, C.R. & Lee, W.S. (1989) Purification of hepoxilin epoxide hydrolase from rat liver. J. Biol Chem. 264, 9310-9313.
5. 5. Hammock, B.D., Grant, D.F. & Storms, D.H. (1997) Epoxide hydrolases. In Comprehensive Toxicology (Sipes, I., McQueen, C. & Gandolfi, A., eds), pp. 283-305. Pergamon Press, Oxford.
6. 6. Wixtrom, R.N. & Hammock, B.D. (1985) Membrane-bound and soluble-fraction epoxide hydrolases: methodological aspects. In Biochemical Pharmacology and Toxicology (Zakim, D. & Vessey, D.A., eds), pp. 1-93. John Wiley & Sons, New York.
7. 7. Moghaddam, M., Grant, D., Cheek, J., Greene, J.F. & Hammock, B.D. (1997) Bioactivation of leukotoxins to their toxic diols by epoxide hydrolase. Nat. Med. 3, 562-566.
8. 8. Beetham, J.K., Grant, D., Arand, M., Garbarino, J., Kiyosue, T., Pinot, F., Oesch, F., Belknap, W.R., Shinozaki, K. & Hammock, B.D. (1995) Gene evolution of epoxide hydrolases and recommended nomenclature. DNA Cell Biol. 14, 61-71.
9. 9. Arand, M., Grant, D.F., Beetham, J.K., Friedberg, T., Oesch, F. & Hammock, B.D. (1994) Sequence similarity of mammalian epoxide hydrolases to the bacterial haloalkane dehalogenase and other related proteins. Implication for the potential catalytic mechanism of enzymatic epoxide hydrolysis. FEBS Lett. 338, 251-256.
10. 10. Lacourciere, G.M. & Armstrong, R.N. (1994) Microsomal and soluble epoxide hydrolases are members of the same family of C-X bond hydrolase enzymes. Chem. Res. Toxicol. 7, 121-124.
11. 11. Verschueren, K.H.G., Seljée, F., Rozeboom, H.J., Kalk, K.H. & Dijkstra, B.W. (1993) Crystallographic analysis of the catalytic mechanism of haloalkane dehalogenase. Nature (London) 363, 693-698.
12. 12. Lacourciere, G.M. & Armstrong, R.N. (1993) The catalytic mechanism of microsomal epoxide hydrolase involves an ester intermediate. J. Am. Chem. Soc. 115, 10466-10467.
13. 13. Borhan, B., Jones, A.D., Pinot, F., Grant, D.F., Kurth, M.J., Hammock, B. & D. (1995) Mechanism of soluble epoxide hydrolase. Formation of an alpha-hydroxy ester-enzyme intermediate through asp-333. J. Biol. Chem. 270, 26923-26930.
14. 14. Arand, M., Wagner, H. & Oesch, F. (1996) Asp333, Asp495, and His523 form the catalytic triad of rat soluble epoxide hydrolase. J. Biol. Chem. 271, 4223-4229.
15. 15. Croteau, R. & Kolattukudy, P.E. (1975) Biosynthesis of hydroxyfatty acid polymers. Enzymatic hydration of 18-hydroxy-cis-9,10-epoxystearic acid to threo 9,10,18-trihydroxystearic acid by a particulate preparation from apple (Malus pumila). Arch. Biochem. Biophys. 170, 73-81.
16. 16. Blée, E. & Schuber, F. (1992) Occurrence of fatty acid epoxide hydrolases in soybean (glycine max). Purification and characterization of the soluble form. Biochem. J. 282, 711-714.
17. 17. Stapleton, A., Beetham, J.K., Pinot, F., Gabarino, J.E., Rockhold, D.R., Friedman, M., Hammock, B.D. & Belknap, W.R. (1994) Cloning and expression of soluble epoxide hydrolase from potato. Plant J. 6, 251-258.
18. 18. Kiyosue, T., Beelham, J.K., Pinot, F., Hammock, B.D., Yamaguchi-Shinozaki, K. & Shinozaki, K. (1994) Characterisation of an Arabidopsis cDNA for a soluble epoxide gene that is inducible by auxin and water stress. Plant J. 6, 259-269.
19. 19. Roe, R.M., Kallapur, V., Linderman, R.J., Viviani, F., Harris, S.V., Walker, E.A. & Thompson, D.M. (1996) Mechanism of action and cloning of epoxide hydrolase from the cabbage looper, Trichoplusia ni. Arch. Insect Biochem. Physiol. 32, 527-535.
20. 20. Roe, R.M. & Venkatesh, K. (1990). Metabolism of juvenile hormones: degradation and titer regulation. In Morphogenetic Hormones of Arthropods (Gupta, A., ed.), pp. 126-179. Rutgers University Press, New Brunswick.
21. 21. Touhara, K. & Prestwich, G.D. (1993) Juvenile hormone epoxide hydrolase. Photoaffinity labeling, purification, and characterization from tobacco hornworm eggs. J. Biol. Chem. 268, 19604-19609.
22. 22. Wojtasek, H. & Prestwich, G.D. (1996) An insect juvenile hormone-specific epoxide hydrolase is related to vertebrate microsomal epoxide hydrolases. Biochem. Biophys. Res. Commun. 220, 323-329.
23. 23. Faber, K., Mischtiz, M. & Kroutil, W. (1996) Microbial epoxide hydrolases. Acta Chem. Scand. 50, 249-258.
24. 24. Archelas, A. & Furstoss, R. (1997) Synthesis of enantiopure epoxides through biocatalytic approaches. Annu. Rev. Microbiol. 51, 491-525.
25. 25. Archer, I.V.J. (1997) Epoxide hydrolases as asymmetric catalysts. Tetrahedron 53, 15617-15662.
26. 26. Archelas, A. & Furstoss, R. (1998) Epoxide hydrolases: new tools for the synthesis of fine organic chemicals. Trends Biotechnol. 16, 108-116.
27. 27. Allen, R.H. & Jakoby, W.B. (1969) Tartaric acid metabolism IX. Synthesis with tartrate epoxidase. J. Biol. Chem. 244, 2078-2084.
28. 28. Rink, R., Fennema, M., Smids, M., Dehmel, U. & Janssen, D.B. (1997) Primary structure and catalytic mechanism of the epoxide hydrolase from Agrobacterium radiobacter AD1. J. Biol. Chem. 272, 14650-14657.
29. 29. Nakamura, T., Nagasawa, T., Watanabe, I. & Yamade, H. (1994) Purification and characterization of two epoxide hydrolases from corynebacterium sp. Strain n-1074. Appl. Environ. Microbiol. 60, 4630-4633.
30. 30. Mischitz, M., Faber, K. & Willetts, A. (1995) Isolation of a highly enantioselective epoxide hydrolase from Rhodococcus sp. NCIMB 11216. Biotechnol. Lett. 17, 893-898.
31. 31. Misawa, E., Chan Kwo Chion, C.K.C., Archer, I.V., Woodland, M.P., Zhou, N.Y., Carter, S.F., Widdowson, D.A. & Leak, D.A. (1998) Characterisation of a catabolic epoxide hydrolase from a Corynebacterium sp. Eur. J. Biochem. 253, 173-183.
32. 32. Barbirato, F., Verdoes, J.C., de Bont, J.A.M. & van der Werf (1998) The Rhodococcus erythropolis DCL14 limonene-1,2-epoxide hydrolase gene encodes an enzyme belonging to a novel class of epoxide hydrolases. FEBS Lett. 438, 293-296.
33. 33. Kolb, H.C., Van Nieuwenhze, M.S. & Sharpless, K.B. (1994) Catalytic asymmetric dihydroxylation. Chem. Rev. 94, 2483-2587.
34. 34. Katsuki, T. (1995) Catalytic asymmetric oxidations using optically active (salen) manganese (III) complexes as catalysis. Coord. Chem. Rev. 140, 189-214.
35. 35. De Bont, J.A.M. (1993) Bioformation of optically pure epoxides. Tetrahedron Asymmetry 4, 1331-1340.
36. 36. Archelas, A. & Furstoss, R. (1998) Biocatalytic approaches for the synthesis of enantiopure epoxides. Topics Curr. Chem. 200, 159-191.
37. 37. Moussou, P., Archelas, A. & Furstoss, R. (1998) Microbiological transformations 40. Use of fungal epoxide hydrolases for the synthesis of enantiopure alkyl epoxides. Tetrahedron 54, 1563-1572.
38. 38. Nellaiah, H., Morisseau, C., Archelas, A., Furstoss, R. & Baratti, J.C. (1996) Enantioselective hydrolysis of p-nitrostyrene oxide by an epoxide hydrolase preparation from Aspergillus niger. Biotechnol. Bioeng. 49, 70-77.
39. 39. Morisseau, C., Nellaiah, H., Archelas, A., Furstoss, R. & Baratti, J.C. (1997) Asymmetric hydrolysis of racemic para-nitrostyrene oxide using an epoxide hydrolase preparation from Aspergillus niger. Enzyme Microb. Technol. 20, 446-452.
40. 40. Pedragosa-Moreau, S., Morisseau, C., Baratti, J.C., Zylber, J., Archelas, A. & Furstoss, R. (1997) Microbiological transformations. Part 37: an enantioconvergent synthesis of the beta-blocker (R)-Nifenalol using a combined chemoenzymatic approach. Tetrahedron 53, 9707-9714.
41. 41. Cleij, M., Archelas, A. & Furstoss, R. (1998) Microbiological transformations. Part 42: a two-liquid-phase preparative scale process for an epoxide hydrolase catalysed resolution of para-bromo-α-methyl styrene oxide. Occurrence of a surprising enantioselectivity enhancement. Tetrahedron Asymmetry 9, 1839-1842.
42. 42. Westkaemper, R.B. & Hanzlik, R.P. (1980) A convenient reverse-phase liquid chromatographic assay for epoxide hydrolase. Anal. Biochem. 102, 63-67.
43. 43. Pedragosa-Moreau, S., Archelas, A. & Furstoss, R. (1996) Microbial transformations. Part 32: use of epoxide hydrolase mediated biohydrolysis as a way to enantiopure epoxides and vicinal diols: application to substituted styrene oxide derivatives. Tetrahedron 52, 4593-4606.
44. 44. Chen, X.-J., Archelas, A. & Furstoss, R. (1993) Microbial transformations. Part 27: the first examples for preparative-scale enantioselective or diastereoselective epoxides hydrolyses using microorganisms. An unequivocal access to all four bisabolol stereoisomers. J. Org. Chem. 58, 5528-5532.
45. 45. Pedragosa-Moreau, S., Archelas, A. & Furstoss, R. (1993) Microbiological transformations. Part 28: enantiocomplementary epoxide hydrolyses as a preparative access to both enantiomers of styrene oxide. J. Org. Chem. 58, 5533-5536.
46. 46. Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with Folin phenol reagent. J. Biol. Chem. 193, 265-275.
47. 47. Audier, H.E., Dupin, J.F. & Jullien, J. (1968) Etude cinétique des réactions d'hydratation catalysées par l'ion hydroxyle d'une série d'époxydes phénylées. Bull. Chem. Soc. Fr. 9, 3844-3847.
48. 48. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature (London) 227, 680-685.
49. 49. Delaage, M. (1968) On the determination of the most coherent molecular weight with analysis of the amino acids of a protein. Biochim. Biophys. Acta 168, 573-575.
50. 50. Meijer, J. & DePierre, J.W. (1983) Cytosolic epoxide hydrolases. Chem. Biol. Interact. 64, 207-249.
51. 51. Dubois, G.C., Appella, E., Levin, W., Lu, A.Y.H. & Jerina, D.M. (1978) Hepatic microsomal epoxide hydrase. J. Biol. Chem. 253, 2932-2939.
52. 52. Borhan, B., Jones, A.D., Pinot, F., Grant, D.F., Kurth, M.J. & Hammock, B.D. (1995) Mechanism of soluble epoxide hydrolase. Formation of an α-hydroxy ester-enzyme intermediate through Asp-333. J. Biol. Chem. 270, 26923-26930.
53. 53. Pedragosa-Moreau, S., Archelas, A. & Furstoss, R. (1994) Microbiological transformations. Part 24: enantioselective hydrolysis of epoxides using microorganisms: a mechanistic study. Bioorg. Med. Chem. 2, 609-616.
54. 54. Pedragosa-Moreau, S., Morisseau, C., Zylber, J., Archelas, A., Baratti, J.C. & Furstoss, R. (1996) Microbiological transformations. Part 33: fungal epoxide hydrolases applied to the synthesis of enantiopure para-substituted styrene oxides. A mechanistic approach. J. Org. Chem. 61, 7402-7407.
55. 55. Chen, C.S., Fujimoto, Y., Giraukas, G. & Sih, C. (1982) Quantitative analyses of biochemical kinetic resolutions of enantiomers. J. Am. Chem. Soc. 104, 7294-7297.