Crystal Structure of 3-Hydroxybenzoate Hydroxylase from Comamonas testosteroni Has a Large Tunnel for Substrate and Oxygen Access to the Active Site

Journal of Molecular Biology

Volumn 364, Issue 5, 2006, Pages 878-896

  Hiromoto, Takeshi ^a   Fujiwara, Shinsuke ^a   Hosokawa, Keiichi ^b,c   Yamaguchi, Hiroshi ^a  

^a KWANSEI GAKUIN UNIVERSITY   (Japan)

^b Institute of Bio Microbiology   (Japan)

^c Proteomics Research Laboratory   (Japan)

Author keywords

3 hydroxybenzoate hydroxylase; crystal structure; flavoprotein; oxygen binding; substrate recognition

Indexed keywords

3 HYDROXYBENZOATE HYDROXYLASE; ISOENZYME; UNCLASSIFIED DRUG;

ARTICLE; BAY REGION BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; COMAMONAS TESTOSTERONI; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYMOLOGY; HYDROXYLATION; MOLECULAR RECOGNITION; NONHUMAN; OLIGOMERIZATION; OXYGEN TRANSPORT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; STRUCTURAL HOMOLOGY; STRUCTURAL PROTEOMICS;

COMAMONAS TESTOSTERONI;

EID: 33751105570     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.09.031     Document Type: Article

References (70)

1. Harwood C.S., and Parales R.E. The β-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50 (1996) 533-590
2. van Berkel W.J.H., and Müller F. Flavin-dependent monooxygenases with special references to p-hydroxybenzoate hydroxylase. In: Müller F. (Ed). Chemistry and Biochemistry of Flavoenzymes vol. 2 (1991), CRC Press, Boca Raton, FL 1-29
3. Harayama S., Kok M., and Neidle E.L. Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46 (1992) 565-601
4. Moonen M.J.H., Fraaije M.W., Rietjens I.M.C.M., Laane C., and van Berkel W.J.H. Flavoenzyme-catalyzed oxygenations and oxidations of phenolic compounds. Advan. Synth. Catal. 344 (2002) 1023-1035
5. Chen R., Chaen H., and Hosokawa K. Studies on m-hydroxybenzoate 4-hydroxylase from Comamonas testosteroni. I. Purification and characterization. Res. Commun. Biochem. Cell Mol. Biol. 1 (1997) 304-322
6. Chen R., Oki H., Scott Jr. R.P., Yamgaguchi H., Kusunoki M., Matsuura Y., et al. Crystallization and further characterization of meta-hydroxybenzoate 4-hydroxylase from Comamonas testosteroni. Res. Commun. Biochem. Cell Mol. Biol. 2 (1998) 253-274
7. Chen R., Scott Jr. R., Tsugita A., and Hosokawa K. Purification and characterization of p-hydroxybenzoate 3-hydroxylase from Comamonas testosteroni. Res. Commun. Biochem. Cell Mol. Biol. 1 (1997) 51-60
8. Providenti M.A., Mampel J., MacSween S., Cook A.M., and Wyndham R.C. Comamonas testosteroni BR6020 possesses a single genetic locus for extradiol cleavage of protocatechuate. Microbiology 147 (2001) 2157-2167
9. Harpel M.R., and Lipscomb J.D. Gentisate 1,2-dioxygenase from Pseudomonas. Purification, characterization, and comparison of the enzymes from Pseudomonas testosteroni and Pseudomonas acidovorans. J. Biol. Chem. 265 (1990) 6301-6311
10. Harayama S., and Timmis K.N. Aerobic biodegradation of aromatic hydrocarbons by bacteria. In: Sigel H., and Sigel A. (Eds). Metal Ions in Biological Systems vol. 28 (1992), Marcel Dekker Inc, New York, NY 99-156
11. Eppink M.H.M., Schreuder H.A., and van Berkel W.J.H. Identification of a novel conserved sequence motif in flavoprotein hydroxylases with putative dual function in FAD/NAD(P)H binding. Protein Sci. 6 (1997) 2454-2458
12. Dym O., and Eisenberg D. Sequence-structure analysis of FAD-containing proteins. Protein Sci. 10 (2001) 1712-1728
13. Schreuder H.A., Prick P.A.J., Wierenga R.K., Vriend G., Wilson K.S., Hol W.G.J., and Drenth J. Crystal structure of the p-hdyroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution. J. Mol. Biol. 208 (1989) 679-696
14. Schreuder H.A., Mattevi A., Obmolova G., Kalk K.H., Hol W.G.J., van der Bolt F.J.T., and van Berkel W.J.H. Crystal structure of wild-type p-hydroxybenzoate hydroxylase complexed with 4-aminobenzoate, 2,4-dihydroxybenzoate, and 2-hydroxy-4-aminobenzote 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 (1994) 10161-10170
15. Gatti D.L., Palfey B.A., Lah M.S., Entsch B., Massey V., Ballou D.P., and Ludwig M.L. The mobile flavin of 4-OH benzoate hydroxylase. Science 266 (1994) 110-114
16. Wang J., Ortiz-Maldonado M., Entsch B., Massay V., Ballou D., and Gatti D.L. Protein and ligand dynamics in 4-hydroxybenzoate hydroxylase. Proc. Natl Acad. Sci. USA 99 (2002) 608-613
17. Enroth C., Neujahr H., Schneider G., and Lindqvist Y. 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 6 (1998) 605-617
18. Enroth C. High-resolution structure of phenol hydroxylase and correction of sequence errors. Acta. Crystallog. sect. D 59 (2003) 1597-1602
19. Entsch B., and van Berkel W.J.H. Structure and mechanism of para-hydroxybenzoate hydroxylase. FASEB J. 9 (1995) 476-483
20. Xu D., Ballou D.P., and Massey V. Studies of the mechanism of phenol hydroxylase: mutants Tyr289Phe, Asp54Asn and Arg281Met. Biochemistry 40 (2001) 12369-12378
21. Entsch B., Cole L.J., and Ballou D.P. Protein dynamics and electrostatics in the function of p-hydroxybenzoate hydroyxlase. Arch. Biochem. Biophys. 433 (2005) 297-311
22. Ballou D.P., Entsch B., and Cole L.J. Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases. Biochem. Biophys. Res. Commun. 338 (2005) 590-598
23. Brender J.R., Dertouzos J., Ballou D.P., Massey V., Palfey B.A., Entsch B., et al. Conformational dynamics of the isoalloxazine in substrate-free p-hydroxybenzoate hydroxylase: single-molecule studies. J. Am. Chem. Soc. 127 (2005) 18171-18178
24. Cole L.J., Gatti D.L., Entsch B., and Ballou D.P. Removal of a methyl group causes global changes in p-hydroxybenzoate hydroxylase. Biochemistry 44 (2005) 8047-8058
25. Palfey B.A., Moran G.R., Entsch B., Ballou D.P., and Massay V. Substrate recognition by "password" in p-hydroxybenzoate hydroxylase. Biochemistry 38 (1999) 1153-1158
26. Frederick K.K., Ballou D.P., and Palfey B.A. Protein dynamics control proton transfers to the substrate on the His72Asn mutant of p-hydroxybenzoate hydroxylase. Biochemistry 40 (2001) 3891-3899
27. Entsch B., Palfey B.A., Ballou D.P., and Massey V. Catalytic function of tyrosine residues in para-hydroxybenzoate hydroxylase as determinded by the study of site-directed mutants. J. Biol. Chem. 266 (1991) 17341-17349
28. Palfey B.A., Ballou D.P., and Massey V. Flavin conformational changes in the catalytic cycle of p-hydorxybenzoate hydroxylase substituted with 6-azido- and 6-aminoflavin adenine dinucleotide. Biochemistry 36 (1997) 15713-15723
29. Frederick K.K., and Palfey B.A. Kinetics of proton-linked flavin conformational changes in p-hydroxybenzoate hydroxylase. Biochemistry 44 (2005) 13304-13314
30. Moran G.R., Entsch B., Palfey B.A., and Ballou D.P. Electrostatic effects on substrate activation in para-hydroxybenzoate hydroxylase: studies of the mutant lysine 297 methionine. Biochemistry 36 (1997) 7548-7556
31. Ortiz-Maldonado M., Cole L.J., Dumas S.M., Entsh B., and Ballou D.P. Increased positive electrostatic potential in p-hydroxybenzoate hydroxylase accelerates hydroxylation but shows turnover. Biochemistry 43 (2004) 1569-1579
32. Orser C.S., Lange C.C., Xun L., Zahrt T.C., and Schneider B.J. Cloning, sequence analysis, and expression of the Flavobacterium pentachlorophenol-4-monooxygenase gene in Escherichia coli. J. Bacteriol. 175 (1993) 411-416
33. Decker H., Motamedi H., and Hutchinson C.R. Nucleotide sequences and heterologous expression of tcmG and tcmP, biosynthetic genes for tetracenomycin C in Streptomyces glaucescens. J. Bacteriol. 175 (1993) 3876-3886
34. Perkins E.J., Gordon M.P., Caceres O., and Lurquin P.F. Organization and sequence analysis of the 2,4-dichlorophenol hydroxylase and dichlorocatechol oxidative operons of plasmid pJP4. J. Bacteriol. 172 (1990) 2351-2359
35. Nurk A., Kasak L., and Kivisaar M. Sequence of the gene (pheA) encoding phenol monooxygenase from Pseudomonas sp. EST1001: expression in Escherichia coli and Pseudomonas putida. Gene 102 (1991) 13-18
36. Eggink G., Engel H., Vriend G., Terpstra P., and Witholt B. Rubredoxin reductase of Pseudomonas oleovorans. Structural relationship to other flavoprotein oxidoreductases based on one NAD and two FAD fingerprints. J. Mol. Biol. 212 (1990) 135-142
37. Holm L., and Sander C. Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233 (1993) 123-128
38. Orengo C.A., Michie A.D., Jones S., Jones D.T., Swindells M.B., and Thornton J.M. CATH-A hierarchic classification of protein domain structures. Structure 5 (1997) 1093-1108
39. Weichsel A., Gasdaska J.R., Powis G., and Montfort W.R. Crystal structures of reduced, oxidized, and mutated human thioredoxins: evidence for a regulatory homodimer. Structure 4 (1996) 735-751
40. + reductase: prototype for a structurally nobel flavoenzyme family. Science 251 (1991) 60-66
41. Williams Jr. C.H. Lipoamide dehydrogenase, glutathione reductase, thioredoxin reductase, and mercuric ion reductase-A family of flavoenzyme transhydrogenases. In: Müller F. (Ed). Chemistry and Biochemistry of Flavoenzymes vol. 3 (1991), CRC Press, Boca Raton, FL 121-211
42. + reductases. J. Biol. Chem. 276 (2001) 44419-44426
43. Sevrioukova I.F., Li H., and Poulos T.L. Crystal structure of putidaredoxin reductase from Pseudomonas putida, the final structural component of the cytochrome P450cam monooxygenase. J. Mol. Biol. 336 (2004) 889-902
44. Declercq J.-P., Evrard C., Clippe A., Stricht D.V., Bernard A., and Knoops B. Crystal structure of human peroxiredoxin 5, a novel type of mammalian peroxiredoxin at 1.5 Å resolution. J. Mol. Biol. 311 (2001) 751-759
45. Choi H.J., Kang S.W., Yang C.H., Rhee S.G., and Ryu S.E. Crystal structure of a novel human peroxidase enzyme at 2.0 Å resolution. Nature Struct. Biol. 5 (1998) 400-406
46. Montet Y., Amara P., Volbeda A., Vernede X., Hatchikian E.C., Field M.J., et al. Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nature Struct. Biol. 4 (1997) 523-526
47. Wentworth Jr. P., Jones L.H., Wentworth A.D., Zhu X., Larsen N.A., Wilson I.A., et al. Antibody catalysis of the oxidation of water. Science 293 (2001) 1806-1811
48. Svensson-Ek M., Abramson J., Larsson G., Törnroth S., Brzezinski P., Iwata, and So. The X-ray crystal structures of wild-type and EQ(I-286) mutant cytochrome c oxidases from Rhodobacter sphaeroides. J. Mol. Biol. 321 (2002) 329-339
49. Duff A.P., Trambaiolo D.M., Cohen A.E., Ellis P.J., Juda G.A., Shepard E.M., et al. Using xenon as a probe for dioxygen-binding sites in copper amine oxidases. J. Mol. Biol. 344 (2004) 599-607
50. Cruickshank D.W.J. Remarks about protein structure precision. Acta. Crystallog. sect. D 55 (1999) 583-601
51. Xu D., Enroth C., Lindqvist Y., Ballou D.P., and Massey V. Studies of the mechanism of phenol hydroxylase: effect of mutation of proline 364 to serine. Biochemistry 41 (2002) 13627-13636
52. Ridder, L., Mulholland, A. J., Rietjens, I. M., & Vervoort, J. (1999). Combined quantum mechanical and molecular mechanical reaction pathway calculation for aromatic hydroxylation by p-hydroxybenzoate hydroxylase. J. Mol. Graph. Model. 17, 163-175, 214.
53. Palfey B.A., Basu R., Frederick K.K., Entsch B., and Ballou D.P. Role of protein flexibility in the catalytic cycle of p-hydroxybenzoate hydroxylase elucidated by the Pro293Ser mutant. Biochemistry 41 (2002) 8438-8446
54. Rappoport Z. Table XXVIII. Acid dissociation constants of phenols in aqueous solution. In: Rappoport Z. (Ed). Hand-Book of Tables for Organic Compound Identification (1967), CRC Press, Cleveland, OH 434
55. Vervoort J., Rietjens I.M.C.M., van Berkel W.J.H., and Veeger C. Frontier orbital study on the 4-hydroxybenzoate-3-hydroxylase-dependent activity with benzoate derivatives. Eur. J. Biochem. 206 (1992) 479-484
56. van Berkel W., Westphal A., Eschrich K., Eppink M., and de Kok A. Substitution of Arg214 at the substrate-binding site of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens. Eur. J. Biochem. 210 (1992) 411-419
57. Ridder L., Palfey B.A., Vervoort J., and Rietjens I.M.C.M. Modeling flavin and substrate substituent effects on the activation barrier and rate of oxygen transfer by p-hydroxybenzoate hydroxylase. FEBS Letters 478 (2000) 197-201
58. Bach R.D., and Dmitrenko O. Model studies on p-hydroxybenzoate hydroxylase. The catalytic role of Arg-214 and Tyr-201in the hydroxylation step. J. Am. Chem. Soc. 126 (2003) 127-142
59. Sambrook J., and Russell D.W. Molecular Cloning: A Laboratory Manual. 3rd edit., (2001), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
60. Imanaka T., Tanaka T., Tsunekawa H., and Aiba S. Cloning of the genes for penicillinase, penP and penI, of Bacillus licheniformis in some vector plasmids and their expression in Escherichia coli, Bacillus subtilis and Bacillus licheniformis. J. Bacteriol. 147 (1981) 776-786
61. Leslie A.G.W. Molecular data processing. In: Moras D., Podjarny A.D., and Thierry J.C. (Eds). Crystallographic Computing (1991), IUC Oxford University Press, Oxford, UK 50-61
62. Powell H.R. The Rossmann Fourier autoindexing algorithm in MOSFLM. Acta Crystallog. sect. D 55 (1999) 1690-1695
63. Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta. Crystallog. sect. D 50 (1994) 760-763
64. McRee D.E. XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
65. Brünger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., et al. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta. Crystallog. sect. D 54 (1998) 905-921
66. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
67. Kraulis P.J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24 (1991) 946-950
68. Merritt E.A., and Bacon D.J. Raster3D: photorealistic molecular graphics. In: Carter C.W., and Sweet R.M. (Eds). Methods in Enzymology vol. 277 (1997), Academic Press, San Diego, CA 505-524
69. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 (1994) 4673-4680
70. Hutchinson E.G., and Thornton J.M. PROMOTIF: a program to identify and analyze structural motifs in proteins. Protein Sci. 5 (1996) 212-220