Probing the molecular basis of substrate specificity, stereospecificity, and catalysis in the class II pyruvate aldolase, BphI

Biochemistry

Volumn 50, Issue 17, 2011, Pages 3559-3569

  Baker, Perrin ^a   Carere, Jason ^a   Seah, Stephen Y K ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE RESIDUES; ALDOLASES; C-C BONDS; CATALYTIC BASE; CATALYTIC MECHANISMS; CLASS II; DEGRADATION PATHWAYS; ENOLATE INTERMEDIATES; HYDROXIDE CONCENTRATION; MOLECULAR BASIS; NATURAL SUBSTRATES; OXO-ACIDS; PH DEPENDENCE; PROPIONALDEHYDE; PROTON EXCHANGE; PYRUVATES; STEREOCHEMICAL CONTROL; STEREOSPECIFICITY; SUBSTRATE RECOGNITION; SUBSTRATE SPECIFICITY; WILD TYPES; WILD-TYPE ENZYMES;

ACETALDEHYDE; ADDITION REACTIONS; AMINO ACIDS; CATALYSIS; ENZYME ACTIVITY; ENZYMES; ORGANIC POLLUTANTS; POLYCHLORINATED BIPHENYLS; QUANTUM CHEMISTRY;

SUBSTRATES;

4 HYDROXY 2 OXOPENTANOATE; ACETALDEHYDE; ALDEHYDE; ARGININE; CLASS II PYRUVATE ALDOLASE; ENZYME VARIANT; FRUCTOSE BISPHOSPHATE ALDOLASE; HISTIDINE; HYDROXIDE; MUTANT PROTEIN; PENTALDEHYDE; PHENYLALANINE; PROPIONALDEHYDE; PROTEIN BPHI; PROTON; PYRUVIC ACID; SERINE; SOLVENT; UNCLASSIFIED DRUG; VALERIC ACID DERIVATIVE;

ALDOL REACTION; AMINO ACID SUBSTITUTION; ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME KINETICS; ENZYME SPECIFICITY; ENZYME STABILITY; MOLECULAR MODEL; MOLECULAR RECOGNITION; MUTATION; PH; PRIORITY JOURNAL; PROTEIN CLEAVAGE; STEADY STATE; STEREOSPECIFICITY; WILD TYPE;

CATALYSIS; CATALYTIC DOMAIN; KETO ACIDS; KINETICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OXO-ACID-LYASES; PYRUVIC ACID; STEREOISOMERISM; SUBSTRATE SPECIFICITY;

EID: 79955451278     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101947g     Document Type: Article

References (63)

1. Furukawa, K. and Kimura, N. (1995) Biochemistry and genetics of PCB metabolism Environ. Health Perspect. 103 (Suppl. 5) 21-23
2. Diaz, E. (2004) Bacterial degradation of aromatic pollutants: A paradigm of metabolic versatility Int. Microbiol. 7, 173-180 (Pubitemid 40515129)
3. Furukawa, K., Hirose, J., Suyama, A., Zaiki, T., and Hayashida, S. (1993) Gene components responsible for discrete substrate specificity in the metabolism of biphenyl (bph operon) and toluene (tod operon) J. Bacteriol. 175, 5224-5232 (Pubitemid 23232586)
4. Baker, P., Pan, D., Carere, J., Rossi, A., Wang, W., and Seah, S. Y. (2009) Characterization of an aldolase-dehydrogenase complex that exhibits substrate channeling in the polychlorinated biphenyls degradation pathway Biochemistry 48, 6551-6558
5. Wang, W., Baker, P., and Seah, S. Y. (2010) Comparison of two metal-dependent pyruvate aldolases related by convergent evolution: Substrate specificity, kinetic mechanism, and substrate channeling Biochemistry 49, 3774-3782
6. Takayama, S., McGarvey, G. J., and Wong, C. H. (1997) Microbial aldolases and transketolases: New biocatalytic approaches to simple and complex sugars Annu. Rev. Microbiol. 51, 285-310 (Pubitemid 27433051)
7. Manjasetty, B. A., Powlowski, J., and Vrielink, A. (2003) Crystal structure of a bifunctional aldolase-dehydrogenase: Sequestering a reactive and volatile intermediate Proc. Natl. Acad. Sci. U.S.A. 100, 6992-6997 (Pubitemid 36706381)
8. Forouhar, F., Hussain, M., Farid, R., Benach, J., Abashidze, M., Edstrom, W. C., Vorobiev, S. M., Xiao, R., Acton, T. B., Fu, Z., Kim, J. J., Miziorko, H. M., Montelione, G. T., and Hunt, J. F. (2006) Crystal structures of two bacterial 3-hydroxy-3-methylglutaryl-CoA lyases suggest a common catalytic mechanism among a family of TIM barrel metalloenzymes cleaving carbon-carbon bonds J. Biol. Chem. 281, 7533-7545 (Pubitemid 43847524)
9. Koon, N., Squire, C. J., and Baker, E. N. (2004) Crystal structure of LeuA from Mycobacterium tuberculosis, a key enzyme in leucine biosynthesis Proc. Natl. Acad. Sci. U.S.A. 101, 8295-8300 (Pubitemid 38736569)
10. Prieto, M. A., Diaz, E., and Garcia, J. L. (1996) Molecular characterization of the 4-hydroxyphenylacetate catabolic pathway of Escherichia coli W: Engineering a mobile aromatic degradative cluster J. Bacteriol. 178, 111-120 (Pubitemid 26006072)
11. Dennis, D. A., Chapman, P. J., and Dagley, S. (1973) Degradation of protocatechuate in Pseudomonas testosteroni by a pathway involving oxidation of the product of meta-fission J. Bacteriol. 113, 521-523
12. Wang, W. and Seah, S. Y. (2005) Purification and biochemical characterization of a pyruvate-specific class II aldolase, HpaI Biochemistry 44, 9447-9455 (Pubitemid 40962043)
13. Wang, W., Mazurkewich, S., Kimber, M. S., and Seah, S. Y. (2010) Structural and Kinetic Characterization of 4-Hydroxy-4-methyl-2-oxoglutarate/4- Carboxy-4-hydroxy-2-oxoadipate Aldolase, a Protocatechuate Degradation Enzyme Evolutionarily Convergent with the HpaI and DmpG Pyruvate Aldolases J. Biol. Chem. 285, 36608-36615
14. Ash, D. E., Emig, F. A., Chowdhury, S. A., Satoh, Y., and Schramm, V. L. (1990) Mammalian and avian liver phosphoenolpyruvate carboxykinase. Alternate substrates and inhibition by analogues of oxaloacetate J. Biol. Chem. 265, 7377-7384
15. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular cloning: A laboratory manual, Cold Spring Harbor Laboratory Press, Plainview, NY.
16. Sarkar, G. and Sommer, S. S. (1990) The "megaprimer" method of site-directed mutagenesis BioTechniques 8, 404-407
17. Liu, H. and Naismith, J. H. (2008) An efficient one-step site-directed deletion, insertion, single and multiple-site plasmid mutagenesis protocol BMC Biotechnol. 8, 91
18. Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2002) Multiple sequence alignment using ClustalW and ClustalX, Current Protocols in Bioinformatics, Chapter 2, Unit 2.3, Wiley, New York.
19. Gouet, P., Courcelle, E., Stuart, D. I., and Metoz, F. (1999) ESPript: Analysis of multiple sequence alignments in PostScript Bioinformatics 15, 305-308 (Pubitemid 29213756)
20. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
21. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72, 248-254
22. Cornish-Bowden, A. (1995) Analysis of enzyme kinetic data, Oxford University Press, New York.
23. Cornish-Bowden, A. and Eisenthal, R. (1974) Statistical considerations in the estimation of enzyme kinetic parameters by the direct linear plot and other methods Biochem. J. 139, 721-730
24. Eisenthal, R. and Cornish-Bowden, A. (1974) The direct linear plot. A new graphical procedure for estimating enzyme kinetic parameters Biochem. J. 139, 715-720
25. Schowen, K. B. and Schowen, R. L. (1982) Solvent isotope effects of enzyme systems Methods Enzymol. 87, 551-606
26. Harayama, S. and Rekik, M. (1993) Comparison of the nucleotide sequences of the meta-cleavage pathway genes of TOL plasmid pWW0 from Pseudomonas putida with other meta-cleavage genes suggests that both single and multiple nucleotide substitutions contribute to enzyme evolution Mol. Gen. Genet. 239, 81-89 (Pubitemid 23167485)
27. Vallee, B. L. and Galdes, A. (1984) The metallobiochemistry of zinc enzymes Adv. Enzymol. Relat. Areas Mol. Biol. 56, 283-430
28. Derbyshire, V., Grindley, N. D., and Joyce, C. M. (1991) The 3′-5′ exonuclease of DNA polymerase I of Escherichia coli: Contribution of each amino acid at the active site to the reaction EMBO J. 10, 17-24 (Pubitemid 21905262)
29. Legler, P. M., Massiah, M. A., and Mildvan, A. S. (2002) Mutational, kinetic, and NMR studies of the mechanism of E. coli GDP-mannose mannosyl hydrolase, an unusual Nudix enzyme Biochemistry 41, 10834-10848 (Pubitemid 34971061)
30. Dahm, S. C., Derrick, W. B., and Uhlenbeck, O. C. (1993) Evidence for the role of solvated metal hydroxide in the hammerhead cleavage mechanism Biochemistry 32, 13040-13045 (Pubitemid 24005910)
31. Hall, D. R., Bond, C. S., Leonard, G. A., Watt, C. I., Berry, A., and Hunter, W. N. (2002) Structure of tagatose-1,6-bisphosphate aldolase. Insight into chiral discrimination, mechanism, and specificity of class II aldolases J. Biol. Chem. 277, 22018-22024 (Pubitemid 34952356)
32. Lee, J. H., Bae, J., Kim, D., Choi, Y., Im, Y. J., Koh, S., Kim, J. S., Kim, M. K., Kang, G. B., Hong, S. I., Lee, D. S., and Eom, S. H. (2006) Stereoselectivity of fructose-1,6-bisphosphate aldolase in Thermus caldophilus Biochem. Biophys. Res. Commun. 347, 616-625 (Pubitemid 44092629)
33. Williams, G. J., Domann, S., Nelson, A., and Berry, A. (2003) Modifying the stereochemistry of an enzyme-catalyzed reaction by directed evolution Proc. Natl. Acad. Sci. U.S.A. 100, 3143-3148 (Pubitemid 36356553)
34. Corina, D. L. and Wilton, D. C. (1976) An apparent lack of stereospecificity in the reaction catalysed by deoxyribose 5-phosphate aldolase due to methyl-group rotation and enolization before product release Biochem. J. 157, 573-576
35. Bolt, A., Berry, A., and Nelson, A. (2008) Directed evolution of aldolases for exploitation in synthetic organic chemistry Arch. Biochem. Biophys. 474, 318-330
36. Jennewein, S., Schurmann, M., Wolberg, M., Hilker, I., Luiten, R., Wubbolts, M., and Mink, D. (2006) Directed evolution of an industrial biocatalyst: 2-Deoxy- d -ribose 5-phosphate aldolase Biotechnol. J. 1, 537-548
37. Wymer, N., Buchanan, L. V., Henderson, D., Mehta, N., Botting, C. H., Pocivavsek, L., Fierke, C. A., Toone, E. J., and Naismith, J. H. (2001) Directed evolution of a new catalytic site in 2-keto-3-deoxy-6-phosphogluconate aldolase from Escherichia coli Structure 9, 1-9 (Pubitemid 32064344)
38. Williams, G. J., Woodhall, T., Farnsworth, L. M., Nelson, A., and Berry, A. (2006) Creation of a pair of stereochemically complementary biocatalysts J. Am. Chem. Soc. 128, 16238-16247 (Pubitemid 44936617)
39. Smith, B. J., Lawrence, M. C., and Barbosa, J. A. (1999) Substrate-Assisted Catalysis in Sialic Acid Aldolase J. Org. Chem. 64, 945-949 (Pubitemid 29098020)
40. Barbosa, J. A., Smith, B. J., DeGori, R., Ooi, H. C., Marcuccio, S. M., Campi, E. M., Jackson, W. R., Brossmer, R., Sommer, M., and Lawrence, M. C. (2000) Active site modulation in the N-acetylneuraminate lyase sub-family as revealed by the structure of the inhibitor-complexed Haemophilus influenzae enzyme J. Mol. Biol. 303, 405-421
41. Kruger, D., Schauer, R., and Traving, C. (2001) Characterization and mutagenesis of the recombinant N-acetylneuraminate lyase from Clostridium perfringens: Insights into the reaction mechanism Eur. J. Biochem. 268, 3831-3839 (Pubitemid 32862923)
42. Theodossis, A., Walden, H., Westwick, E. J., Connaris, H., Lamble, H. J., Hough, D. W., Danson, M. J., and Taylor, G. L. (2004) The structural basis for substrate promiscuity in 2-keto-3-deoxygluconate aldolase from the Entner-Doudoroff pathway in Sulfolobus solfataricus J. Biol. Chem. 279, 43886-43892 (Pubitemid 39390696)
43. 8 barrel proteins J. Biol. Chem. 278, 47253-47260 (Pubitemid 37452313)
44. Lorentzen, E., Siebers, B., Hensel, R., and Pohl, E. (2005) Mechanism of the Schiff base forming fructose-1,6-bisphosphate aldolase: Structural analysis of reaction intermediates Biochemistry 44, 4222-4229 (Pubitemid 40403962)
45. Quinn, D. M. and Sutton, L. D. (1991) in Enzyme Mechanism from Isotope Effects (Cook, P. F., Ed.) CRC Press, Inc., Boca Raton, FL.
46. Wang, Y., Li, Y., and Yan, H. (2006) Mechanism of dihydroneopterin aldolase: Functional roles of the conserved active site glutamate and lysine residues Biochemistry 45, 15232-15239 (Pubitemid 46032450)
47. Fullerton, S. W., Griffiths, J. S., Merkel, A. B., Cheriyan, M., Wymer, N. J., Hutchins, M. J., Fierke, C. A., Toone, E. J., and Naismith, J. H. (2006) Mechanism of the Class I KDPG aldolase Bioorg. Med. Chem. 14, 3002-3010
48. Heine, A., DeSantis, G., Luz, J. G., Mitchell, M., Wong, C. H., and Wilson, I. A. (2001) Observation of covalent intermediates in an enzyme mechanism at atomic resolution Science 294, 369-374 (Pubitemid 32963404)
49. de Carvalho, L. P. and Blanchard, J. S. (2006) Kinetic and chemical mechanism of α-isopropylmalate synthase from Mycobacterium tuberculosis Biochemistry 45, 8988-8999 (Pubitemid 44100695)
50. Morris, A. J. and Tolan, D. R. (1993) Site-directed mutagenesis identifies aspartate 33 as a previously unidentified critical residue in the catalytic mechanism of rabbit aldolase A J. Biol. Chem. 268, 1095-1100 (Pubitemid 23019747)
51. Qamar, S., Marsh, K., and Berry, A. (1996) Identification of arginine 331 as an important active site residue in the class II fructose-1,6-bisphosphate aldolase of Escherichia coli Protein Sci. 5, 154-161 (Pubitemid 26022078)
52. Plater, A. R., Zgiby, S. M., Thomson, G. J., Qamar, S., Wharton, C. W., and Berry, A. (1999) Conserved residues in the mechanism of the E. coli Class II FBP-aldolase J. Mol. Biol. 285, 843-855 (Pubitemid 29041812)
53. Rea, D., Fulop, V., Bugg, T. D., and Roper, D. I. (2007) Structure and mechanism of HpcH: A metal ion dependent class II aldolase from the homoprotocatechuate degradation pathway of Escherichia coli J. Mol. Biol. 373, 866-876 (Pubitemid 47500169)
54. Wang, W. and Seah, S. Y. (2008) The role of a conserved histidine residue in a pyruvate-specific Class II aldolase FEBS Lett. 582, 3385-3388
55. Joerger, A. C., Gosse, C., Fessner, W. D., and Schulz, G. E. (2000) Catalytic action of fuculose 1-phosphate aldolase (class II) as derived from structure-directed mutagenesis Biochemistry 39, 6033-6041 (Pubitemid 30327077)
56. Kroemer, M., Merkel, I., and Schulz, G. E. (2003) Structure and catalytic mechanism of l -rhamnulose-1-phosphate aldolase Biochemistry 42, 10560-10568 (Pubitemid 37102094)
57. Choi, K. H., Shi, J., Hopkins, C. E., Tolan, D. R., and Allen, K. N. (2001) Snapshots of catalysis: The structure of fructose-1,6-(bis)phosphate aldolase covalently bound to the substrate dihydroxyacetone phosphate Biochemistry 40, 13868-13875 (Pubitemid 33078855)
58. Maurady, A., Zdanov, A., de Moissac, D., Beaudry, D., and Sygusch, J. (2002) A conserved glutamate residue exhibits multifunctional catalytic roles in d -fructose-1,6-bisphosphate aldolases J. Biol. Chem. 277, 9474-9483 (Pubitemid 34953035)
59. Gerlt, J. A. and Babbitt, P. C. (2001) Divergent evolution of enzymatic function: Mechanistically diverse superfamilies and functionally distinct suprafamilies Annu. Rev. Biochem. 70, 209-246 (Pubitemid 32662210)
60. Gherardini, P. F., Wass, M. N., Helmer-Citterich, M., and Sternberg, M. J. (2007) Convergent evolution of enzyme active sites is not a rare phenomenon J. Mol. Biol. 372, 817-845 (Pubitemid 47321792)
61. Tuinstra, R. L., Wang, C. Z., Mitchell, G. A., and Miziorko, H. M. (2004) Evaluation of 3-hydroxy-3-methylglutaryl-coenzyme A lyase arginine-41 as a catalytic residue: use of acetyldithio-coenzyme A to monitor product enolization Biochemistry 43, 5287-5295 (Pubitemid 38620920)
62. Fu, Z., Runquist, J. A., Montgomery, C., Miziorko, H. M., and Kim, J. J. (2010) Functional insights into human HMG-CoA lyase from structures of Acyl-CoA-containing ternary complexes J. Biol. Chem. 285, 26341-26349
63. Fu, Z., Runquist, J. A., Forouhar, F., Hussain, M., Hunt, J. F., Miziorko, H. M., and Kim, J. J. (2006) Crystal structure of human 3-hydroxy-3-methylglutaryl-CoA Lyase: Insights into catalysis and the molecular basis for hydroxymethylglutaric aciduria J. Biol. Chem. 281, 7526-7532 (Pubitemid 43847523)