The crystal structure of phenol hydroxylase in complex with FAD and phenol provides evidence for a concerted conformational change in the enzyme and its cofactor during catalysis

Structure

Volumn 6, Issue 5, 1998, Pages 605-617

  Enroth, Cristofer ^a   Neujahr, Halina ^b   Schneider, Gunter ^a   Lindqvist, Ylva ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b ROYAL INSTITUTE OF TECHNOLOGY   (Sweden)

Author keywords

Crystal structure; Enzyme mechanism; Flavin; Phenol hydroxylase; Trichosporon cutaneum

Indexed keywords

TRICHOSPORON CUTANEUM;

EID: 0032524753     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(98)00062-8     Document Type: Article

References (41)

1. Neujahr, H.Y. & Varga, J.M. (1970). Degradation of phenols by intact cells and cell-free preparations of Trichosporon cutaneum. Eur. J. Biochem. 13, 37-44.
2. Neujahr, H.Y. & Gaal, A. (1973). Phenol hydroxylase from yeast: purification and properties of the enzyme from Trichosporon cutaneum. Eur. J. Biochem. 35, 386-400.
3. Spanning, A. & Neujuahr, H.Y. (1987). Growth and enzyme synthesis during continuous culture of Trichsporon cutaneum on phenol. Biotechnol. Bioeng. 29, 464-468.
4. Kälin, M., et al., & Reiser, J. (1992). Phenol hydroxylase from Trichosporon cutaneum: gene cloning, sequence analysis, and functional expression in Escherichia coli. J. Bacteriol. 174, 7112-7120.
5. Sejlitz, T. & Neujahr, H. (1987). Phenol hydroxylase from yeast. A model for phenol binding and an improved purification procedure. Eur. J. Biochem. 170, 343-349.
6. Waters, S. & Neujahr, H. (1994). A fermentor culture for production of recombinant phenol hydroxylase. Protein Expr. Purif. 5, 534-540.
7. Kjellén, K.G. & Neujahr, H.Y. (1978). Phenol hydroxylase from yeast: reaction with phenol derivatives. J. Biol. Chem. 253, 8835-8841.
8. Neujahr, H.Y. (1990). Phenol hydroxylase. In Chemistry and Biochemistry of Flavoenzymes. (Nuller, F., ed.), vol 2, pp. 65-85, CRC Press Inc., Boca Raton, FL.
9. Mörtberg, M. & Neujahr, H.Y. (1987). In situ and in vitro kinetics of phenol hydroxylase. Biochem. Biophys. Res. Commun. 146, 41-46.
10. Neujahr, H.Y. (1988). Thiol- and pH-modulated slow conformational changes and cooperativity of phenol-binding sites in phenol hydroxylase. Biochemistry 27, 3770-3775.
11. Eppink, M.H.M., Schreuder, H.A. & van Berkel, W.J.H. (1997). Identification of a novel conserved sequence motif in flavoprotein hydroxylases with a putative dual function in FAD/NAD(P)H binding. Protein Sci. 6, 2454-2458.
12. Wierenga, R.K., De Jong, R.J., Kalk., K.H., Hol W.G.J. & Drenth J. (1979). Crystal structure of p-hydroxybenzoate hydroxylase. J. Mol. Biol. 131, 55-73.
13. Schreuder, H.A., et al., & Drenth, J. (1989). Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. J. Mol. Biol. 208, 679-696.
14. Enroth, C., Huang, W., Waters, S., Neujahr, H.Y., Lindqvist, Y. & Schneider, G. (1994). Crystallization and preliminary X-ray analysis of phenol hydroxylase from Trichosporon cutaneum. J. Mol. Biol. 238, 128-130.
15. Enroth, C., Waters, S., Neujahr, H.Y., Lindqvist, Y. & Schneider, G. (1997). Crystallization and preliminary X-ray analysis of phenol hydroxylase from Trichosporon cutaneum. In Flavins and Flavoproteins XII. (Stevenson, K., Massey, V. & Williams, Ch., eds), pp. 337-340, University of Calgary Press, Alberta, Canada.
16. Jones, T.A., Zou, J.Y., Cowan, S.W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Cryst. A 47, 110-119.
17. Manstein, D.J., Pai, E.F., Schopfer, L.M. & Massey, V. (1986). Absolute stereochemistry of flavins in enzyme-catalyzed reactions. Biochemistry 25, 6807-6816.
18. Pai, E.F. (1991). Variations on a theme: the family of FAD-dependent NAD(P)H-(disulphide)-oxidoreductases. Curr. Opin. Struct. Biol. 1, 796-803.
19. 2. Proc. Natl. Acad. Sci. USA 93, 7496-7501.
20. Hecht, H.J., Kalisz, H.M., Hendle, J., Schmid, R.D. & Schomburg, D. (1993). Crystal structure of glucose oxidase from Aspergillus niger refined to 2.3 Å resolution. J. Mol. Biol. 229, 153-172.
21. Li, J., Vrielink, A., Brick., P. & Blow, D.M. (1993). Crystal structure of cholesterol oxidase complexed with a steroid substrate: implications for flavin adenine dinucleotide dependent alcohol oxidases. Biochemistry 32, 11507-11515.
22. Gatti, D.L., et al., & Ludwig, M. (1994). The mobile flavin of 4-OH benzoate hydroxylase. Science 266, 110-114.
23. Schreuder, H.A., et al., & van Berkel, W.J.H. (1994). Crystal structures of wild-type p-hydroxybenzoate hydroxylase complexed with 4-aminobenzoate, 2,4-dihydroxybenzoate, and 2-hydroxy-4-aminobenzoate and of the Tyr222Ala mutant complexed with 2-hydroxy-4-aminobenzoate. Evidence for a proton channel and a new binding mode of the flavin ring. Biochemistry 33, 10161-10170.
24. Lu, G. (1996). A WWW service system for automatic comparison of protein structures. Protein Data Bank Quart. Newslett. 78, 10-11.
25. Weichsel, A., Gasdaska, J.R., Powis, G. & Montfort W.R. (1996). Crystal structures of reduced, oxidized and mutated human thioredoxins: evidence for a regulatory homodimer. Structure 4, 735-751.
26. Cleland, W.W. (1970). Steady state kinetics. In The Enzymes, 3rd Edition. Volume 2, (Boyer, P., ed.), Academic Press, New York.
27. Detmer, K. & Massey, V. (1984). Effects of monovalent anions on the mechanism of phenol hydroxylase. J. Biol. Chem. 259, 11265-11272.
28. Waters, S. & Neujahr, H.Y. (1997). Sources and nature of heterogeneity in recombinant phenol hydroxylase derived from the basidiomycetous soil yeast Trichosporon cutaneum. Biotechnol. Appl. Biochem. 25, 235-242.
29. Matthews, B.W. (1968). Solvent content of protein crystals. J. Mol. Biol. 33, 491-497.
30. Otwinowski, Z. (1993). Data collection and processing. In Proceedings of the CCP4 Study Weekend (Sawyer, L., Isaacs, N., Biley, S., eds) p. 56, SERC Laboratory, Daresbury, UK.
31. Minor, W. (1993). XDISPLAYF Program. Purdue University, USA.
32. Collaborative Computational Project No4. (1994). The CCP4 Suite: Programs for Protein Crystallography. Acta Cryst. D 50, 760-763.
33. Cowtan, K. (1994). Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography. 31, 34-38.
34. Cowtan, K. & Main, P. (1996). Phase combination and cross validation in iterated density-modification calculations. Acta Cryst. D 52, 43-48.
35. Brünger, A.T. (1992). Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475.
36. Brünger, AT., Kuriyan, J. & Karplus, M. (1987). Crystallographic R factor refinement by molecular dynamics. Science 235, 458-460.
37. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. (1997). Refinement of macromolecular structures by the maximum-likelihood method. Acta Cryst. D 53, 240-255.
38. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the quality of protein structures J. Appl. Cryst. 26, 282-291.
39. Ramachandran, G.N. & Sasisekharan, V. (1968). Conformations of polypeptides and proteins. Adv. Prot. Chem. 23, 325-347.
40. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
41. Merrit, E.A. & Murphy, M.E.P. (1994). Raster 3D version 2.0: a program for photorealistic molecular graphics. Acta Cryst. D 50, 869-873.