A product analog bound form of 3-oxoadipate-enol-lactonase (PcaD) reveals a multifunctional role for the divergent cap domain

Journal of Molecular Biology

Volumn 406, Issue 5, 2011, Pages 649-658

  Bains, Jasleen ^a   Kaufman, Laura ^a   Farnell, Benjamin ^a   Boulanger, Martin J ^a  

^a UNIVERSITY OF VICTORIA   (Canada)

Author keywords

Burkholderia xenovorans LB400; enol lactonase; PcaD

Indexed keywords

3 OXOADIPATE ENOL LACTONASE; AROMATIC COMPOUND; GLUCONOLACTONASE; LACTONE; LEVULINIC ACID; UNCLASSIFIED DRUG;

ARTICLE; BIOREMEDIATION; BURKHOLDERIA; BURKHOLDERIA XENOVORANS; CATABOLISM; CATALYSIS; ENZYME BINDING; ENZYME METABOLISM; PRIORITY JOURNAL; PROTEIN ENGINEERING; QUORUM SENSING; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS;

BURKHOLDERIA XENOVORANS;

EID: 79951768061     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.01.007     Document Type: Article

References (54)

1. Dong, Y. H. & Zhang, L. H. (2005). Quorum sensing and quorum-quenching enzymes. J. Microbiol. 43, 101-109.
2. Kim, M. H., Choi, W. C., Kang, H. O., Lee, J. S., Kang, B. S., Kim, K. J. et al. (2005). The molecular structure and catalytic mechanism of a quorum-quenching N-acyl-L-homoserine lactone hydrolase. Proc. Natl Acad. Sci. USA, 102, 17606-17611.
3. Lee, S. J., Park, S. Y., Lee, J. J., Yum, D. Y., Koo, B. T. & Lee, J. K. (2002). Genes encoding the N-acyl homoserine lactone-degrading enzyme are widespread in many subspecies of Bacillus thuringiensis. Appl. Environ. Microbiol. 68, 3919-3924.
4. Liu, D., Lepore, B. W., Petsko, G. A., Thomas, P. W., Stone, E. M., Fast, W. & Ringe, D. (2005). Three-dimensional structure of the quorum-quenching N-acyl homoserine lactone hydrolase from Bacillus thuringiensis. Proc. Natl Acad. Sci. USA, 102, 11882-11887.
5. Ulrich, R. L., Deshazer, D., Brueggemann, E. E., Hines, H. B., Oyston, P. C. & Jeddeloh, J. A. (2004). Role of quorum sensing in the pathogenicity of Burkholderia pseudomallei. J. Med. Microbiol. 53, 1053-1064.
6. Lewenza, S., Visser, M. B. & Sokol, P. A. (2002). Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can. J. Microbiol. 48, 707-716.
7. Whitehead, N. A., Byers, J. T., Commander, P., Corbett, M. J., Coulthurst, S. J., Everson, L. et al. (2002). The regulation of virulence in phytopathogenic Erwinia species: quorum sensing, antibiotics and ecological considerations. Antonie Van Leeuwenhoek, 81, 223-231. (Pubitemid 35314611)
8. Kataoka, M., Honda, K., Sakamoto, K. & Shimizu, S. (2007). Microbial enzymes involved in lactone compound metabolism and their biotechnological applications. Appl. Microbiol. Biotechnol. 75, 257-266.
9. Ornston, L. N. (1966). The conversion of catechol and protocatechuate to beta-ketoadipate by Pseudomonas putida. 3. Enzymes of the catechol pathway. J. Biol. Chem. 241, 3795-3799.
10. Canovas, J. L. & Stanier, R. Y. (1967). Regulation of the enzymes of the beta-ketoadipate pathway in Moraxella calcoacetica. 1. General aspects. Eur. J. Biochem. 1, 289-300.
11. Kowalchuk, G. A., Hartnett, G. B., Benson, A., Houghton, J. E., Ngai, K. L. & Ornston, L. N. (1994). Contrasting patterns of evolutionary divergence within the Acinetobacter calcoaceticus pca operon. Gene, 146, 23-30. (Pubitemid 24264817)
12. Shanley, M. S., Harrison, A., Parales, R. E., Kowalchuk, G., Mitchell, D. J. & Ornston, L. N. (1994). Unusual G+C content and codon usage in catIJF, a segment of the ben-cat supra-operonic cluster in the Acinetobacter calcoaceticus chromosome. Gene, 138, 59-65.
13. Delneri, D., Degrassi, G., Rizzo, R. & Bruschi, C. V. (1995). Degradation of trans-ferulic and p-coumaric acid by Acinetobacter calcoaceticus DSM 586. Biochim. Biophys. Acta, 1244, 363-367.
14. Parke, D., Rynne, F. & Glenn, A. (1991). Regulation of phenolic catabolism in Rhizobium leguminosarum biovar trifolii. J. Bacteriol. 173, 5546-5550.
15. Petsko, G. A., Kenyon, G. L., Gerlt, J. A., Ringe, D. & Kozarich, J. W. (1993). On the origin of enzymatic species. Trends Biochem. Sci. 18, 372-376.
16. Barnsley, E. A. (1976). Role and regulation of the ortho and meta pathways of catechol metabolism in pseudomonads metabolizing naphthalene and salicylate. J. Bacteriol. 125, 404-408.
17. Dunaway-Mariano, D. & Babbitt, P. C. (1994). On the origins and functions of the enzymes of the 4-chlorobenzoate to 4-hydroxybenzoate converting pathway. Biodegradation, 5, 259-276.
18. Hewetson, L., Dunn, H. M. & Dunn, N. W. (1978). Evidence for a transmissible catabolic plasmid in Pseudomonas putida encoding the degradation of p-cresol via the protocatechuate ortho cleavage pathway. Genet. Res. 32, 249-255.
19. Winstanley, C., Taylor, S. C. & Williams, P. A. (1987). pWW174: a large plasmid from Acinetobacter calcoaceticus encoding benzene catabolism by the beta-ketoadipate pathway. Mol. Microbiol. 1, 219-227.
20. Elmi, F., Lee, H. T., Huang, J. Y., Hsieh, Y. C., Wang, Y. L., Chen, Y. J. et al. (2005). Stereoselective esterase from Pseudomonas putida IFO12996 reveals alpha/beta hydrolase folds for D-beta-acetylthioisobutyric acid synthesis. J. Bacteriol. 187, 8470-8476. (Pubitemid 41780511)
21. Delano, W. L. (2002). The PyMOL Molecular Graphics System. Delano Scientific, San Carlos, CA.
22. Krissinel, E. & Henrick, K. (2007). Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797.
23. Lai, L., Xu, Z., Zhou, J., Lee, K. D. & Amidon, G. L. (2008). Molecular basis of prodrug activation by human valacyclovirase, an alpha-amino acid ester hydrolase. J. Biol. Chem. 283, 9318-9327.
24. Fushinobu, S., Saku, T., Hidaka, M., Jun, S. Y., Nojiri, H., Yamane, H. et al. (2002). Crystal structures of a meta-cleavage product hydrolase from Pseudomonas fluorescens IP01 (CumD) complexed with cleavage products. Protein Sci. 11, 2184-2195. (Pubitemid 34919622)
25. Habe, H., Morii, K., Fushinobu, S., Nam, J. W., Ayabe, Y., Yoshida, T. et al. (2003). Crystal structure of a histidine-tagged serine hydrolase involved in the carbazole degradation (CarC enzyme). Biochem. Biophys. Res. Commun. 303, 631-639.
26. Saku, T., Fushinobu, S., Jun, S. Y., Ikeda, N., Nojiri, H., Yamane, H. et al. (2002). Purification, characterization, and steady-state kinetics of a meta-cleavage compound hydrolase from Pseudomonas fluorescens IPO1. J. Biosci. Bioeng. 93, 568-574.
27. Holmquist, M. (2000). Alpha/Beta-hydrolase fold enzymes: structures, functions and mechanisms. Curr. Protein Pept. Sci. 1, 209-235.
28. Ollis, D. L., Cheah, E., Cygler, M., Dijkstra, B., Frolow, F., Franken, S. M. et al. (1992). The alpha/beta hydrolase fold. Protein Eng. 5, 197-211.
29. Otyepka, M. & Damborsky, J. (2002). Functionally relevant motions of haloalkane dehalogenases occur in the specificity-modulating cap domains. Protein Sci. 11, 1206-1217. (Pubitemid 34441239)
30. Bertrand, T., Auge, F., Houtmann, J., Rak, A., Vallee, F., Mikol, V. et al. (2010). Structural basis for human monoglyceride lipase inhibition. J. Mol. Biol. 396, 663-673.
31. Ashkenazy, H., Erez, E., Martz, E., Pupko, T. & Ben-Tal, N. (2010). ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res. 38, W529-533.
32. Berezin, C., Glaser, F., Rosenberg, J., Paz, I., Pupko, T., Fariselli, P. et al. (2004). ConSeq: the identification of functionally and structurally important residues in protein sequences. Bioinformatics, 20, 1322-1324. (Pubitemid 38807587)
33. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H. et al. (2007). ClustalWand Clustal X version 2.0. Bioinformatics, 23, 2947-2948.
34. Ollis, D. L. & Ngai, K. L. (1985). Crystallization and preliminary x-ray crystallographic data of dienelactone hydrolase from Pseudomonas sp. B13. J. Biol. Chem. 260, 9818-9819.
35. Pathak, D. & Ollis, D. (1990). Refined structure of dienelactone hydrolase at 1.8 A. J. Mol. Biol. 214, 497-525.
36. Schuttelkopf, A. W. & van Aalten, D. M. (2004). PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363. (Pubitemid 41079731)
37. Cheah, E., Ashley, G. W., Gary, J. & Ollis, D. (1993). Catalysis by dienelactone hydrolase: a variation on the protease mechanism. Proteins, 16, 64-78. (Pubitemid 23129874)
38. Cheah, E., Austin, C., Ashley, G. W. & Ollis, D. (1993). Substrate-induced activation of dienelactone hydrolase: an enzyme with a naturally occurring Cys-His-Asp triad. Protein Eng. 6, 575-583. (Pubitemid 23246508)
39. McCulloch, K. M., Mukherjee, T., Begley, T. P. & Ealick, S. E. (2010). Structure determination and characterization of the vitamin B6 degradative enzyme (E)-2-(acetamidomethylene)succinate hydrolase. Biochemistry, 49, 1226-1235.
40. Dunn, G., Montgomery, M. G., Mohammed, F., Coker, A., Cooper, J. B., Robertson, T. et al. (2005). The structure of the C-C bond hydrolase MhpC provides insights into its catalytic mechanism. J. Mol. Biol. 346, 253-265.
41. Lack, N. A., Yam, K. C., Lowe, E. D., Horsman, G. P., Owen, R. L., Sim, E. & Eltis, L. D. (2010). Characterization of a carbon-carbon hydrolase from Mycobacterium tuberculosis involved in cholesterol metabolism. J. Biol. Chem. 285, 434-443.
42. Loening, A. M., Fenn, T. D. & Gambhir, S. S. (2007). Crystal structures of the luciferase and green fluorescent protein from Renilla reniformis. J. Mol. Biol. 374, 1017-1028.
43. Marek, J., Vevodova, J., Smatanova, I. K., Nagata, Y., Svensson, L. A., Newman, J. et al. (2000). Crystal structure of the haloalkane dehalogenase from Sphingomonas paucimobilis UT26. Biochemistry, 39, 14082-14086.
44. Newman, J., Peat, T. S., Richard, R., Kan, L., Swanson, P. E., Affholter, J. A. et al. (1999). Haloalkane dehalogenases: structure of a Rhodococcus enzyme. Biochemistry, 38, 16105-16114. (Pubitemid 129520531)
45. Schanstra, J. P., Kingma, J. & Janssen, D. B. (1996). Specificity and kinetics of haloalkane dehalogenase. J. Biol. Chem. 271, 14747-14753.
46. Goettig, P., Groll, M., Kim, J. S., Huber, R. & Brandstetter, H. (2002). Structures of the tricorn-interacting aminopeptidase F1 with different ligands explain its catalytic mechanism. EMBO J. 21, 5343-5352. (Pubitemid 35231014)
47. Kim, H. K., Liu, J. W., Carr, P. D. & Ollis, D. L. (2005). Following directed evolution with crystallography: structural changes observed in changing the substrate specificity of dienelactone hydrolase. Acta Crystallogr., Sect. D: Biol. Crystallogr. 61, 920-931. (Pubitemid 43943155)
48. Robinson, A., Edwards, K. J., Carr, P. D., Barton, J. D., Ewart, G. D. & Ollis, D. L. (2000). Structure of the C123S mutant of dienelactone hydrolase (DLH) bound with the PMS moiety of the protease inhibitor phenylmethylsulfonyl fluoride (PMSF). Acta Crystallogr., Sect. D: Biol. Crystallogr. 56, 1376-1384.
49. Yin de, L. T., Bernhardt, P., Morley, K. L., Jiang, Y., Cheeseman, J. D., Purpero, V. et al. (2010). Switching catalysis from hydrolysis to perhydrolysis in Pseudomonas fluorescens esterase. Biochemistry, 49, 1931-1942.
50. Steiner, R. A., Janssen, H. J., Roversi, P., Oakley, A. J. & Fetzner, S. (2010). Structural basis for cofactor-independent dioxygenation of N-heteroaromatic compounds at the alpha/beta-hydrolase fold. Proc. Natl Acad. Sci. USA, 107, 657-662.
51. Harwood, C. S. & Parales, R. E. (1996). The beta-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50, 553-590.
52. Schlomann, M. (1994). Evolution of chlorocatechol catabolic pathways. Conclusions to be drawn from comparisons of lactone hydrolases. Biodegradation, 5, 301-321.
53. Schlomann, M., Schmidt, E. & Knackmuss, H. J. (1990). Different types of dienelactone hydrolase in 4-fluorobenzoate-utilizing bacteria. J. Bacteriol. 172, 5112-5118. (Pubitemid 20281960)
54. Pathak, D., Ngai, K. L. & Ollis, D. (1988). X-ray crystallographic structure of dienelactone hydrolase at 2.8 A. J. Mol. Biol. 204, 435-445.