The kinetic characterization and X-ray structure of a putative benzoylformate decarboxylase from M. smegmatis highlights the difficulties in the functional annotation of ThDP-dependent enzymes

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1854, Issue 8, 2015, Pages 1001-1009

  Andrews, Forest H ^a   Horton, Joshua D ^a   Shin, Donghyuk ^b   Yoon, Hye Jin ^a   Logsdon, Matthew G ^a   Malik, Ahmed M ^a   Rogers, Megan P ^a   Kneen, Malea M ^a   Suh, Se Won ^c   McLeish, Michael J ^a  

^a INDIANA UNIVERSITY   (United States)

^b Sungkyunkwan University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

Annotation; CD spectroscopy; Crystallography; Enzyme kinetics; Thiamin diphosphate

Indexed keywords

BENZOYLFORMATE DECARBOXYLASE; CARBOXYLYASE; COCARBOXYLASE; PHENYLGLYOXYLIC ACID; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; GLYOXYLIC ACID DERIVATIVE; MANDELIC ACID DERIVATIVE;

ARTICLE; BACTERIAL GENOME; CATALYST; CIRCULAR DICHROISM; CRYSTALLIZATION; DECARBOXYLATION; ENZYME ENGINEERING; ESCHERICHIA COLI; EXPRESSION VECTOR; GEL PERMEATION CHROMATOGRAPHY; MYCOBACTERIUM SMEGMATIS; NONHUMAN; PRIORITY JOURNAL; PSEUDOMONAS PUTIDA; SEQUENCE ALIGNMENT; STEADY STATE; X RAY; CHEMISTRY; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETICS; KINETICS; METABOLISM; X RAY CRYSTALLOGRAPHY;

MYCOBACTERIUM SMEGMATIS; PSEUDOMONAS PUTIDA;

BACTERIAL PROTEINS; CARBOXY-LYASES; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GLYOXYLATES; KINETICS; MANDELIC ACIDS; MYCOBACTERIUM SMEGMATIS; THIAMINE PYROPHOSPHATE;

EID: 84929095961     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2015.04.027     Document Type: Article

References (61)

1. F.H. Andrews, and M.J. McLeish Substrate specificity in thiamin diphosphate-dependent decarboxylases Bioorg. Chem. 43 2012 26 36
2. R.G. Duggleby Domain relationships in thiamine diphosphate-dependent enzymes Acc. Chem. Res. 39 2006 550 557
3. S.J. Costelloe, J.M. Ward, and P.A. Dalby Evolutionary analysis of the TPP-dependent enzyme family J. Mol. Evol. 66 2008 36 49
4. K. Tittmann, R. Golbik, S. Ghisla, and G. Hübner Mechanism of elementary catalytic steps of pyruvate oxidase from Lactobacillus plantarum Biochemistry 39 2000 10747 10754
5. S.S. Pang, R.G. Duggleby, R.L. Schowen, and L.W. Guddat The crystal structures of Klebsiella pneumoniae acetolactate synthase with enzyme-bound cofactor and with an unusual intermediate J. Biol. Chem. 279 2004 2242 2253
6. A.K. Steinbach, S. Fraas, J. Harder, A. Tabbert, H. Brinkmann, A. Meyer, U. Ermler, and P.M.H. Kroneck Cyclohexane-1,2-dione hydrolase from denitrifying Azoarcus sp. strain 22Lin, a novel member of the thiamine diphosphate enzyme family J. Bacteriol. 193 2011 6760 6769
7. M. Knoll, M. Müller, J. Pleiss, and M. Pohl Factors mediating activity, selectivity, and substrate specificity for the thiamin diphosphate-dependent enzymes, benzaldehyde lyase and benzoylformate decarboxylase ChemBioChem 7 2006 1928 1934
8. B. Lingen, J. Grötzinger, D. Kolter, M.-R. Kula, and M. Pohl Improving the carboligase activity of benzoylformate decarboxylase from Pseudomonas putida by a combination of directed evolution and site-directed mutagenesis Protein Eng. 15 2002 585 593
9. B. Lingen, D. Kolter-Jung, P. Dünkelmann, R. Feldmann, J. Grötzinger, M. Pohl, and M. Müller Alteration of the substrate specificity of benzoylformate decarboxylase from Pseudomonas putida by directed evolution ChemBioChem 4 2003 721 726
10. E.S. Polovnikova, M.J. McLeish, E.A. Sergienko, J.T. Burgner, N.L. Anderson, A.K. Bera, F. Jordan, G.L. Kenyon, and M.S. Hasson Structural and kinetic analysis of catalysis by a thiamin diphosphate-dependent enzyme, benzoylformate decarboxylase Biochemistry 42 2003 1820 1830
11. E.A. Sergienko, J. Wang, L. Polovnikova, M.S. Hasson, M.J. McLeish, G.L. Kenyon, and F. Jordan Spectroscopic detection of transient thiamin diphosphate-bound intermediates on benzoylformate decarboxylase Biochemistry 39 2000 13862 13869
12. P. Siegert, M.J. McLeish, M. Baumann, H. Iding, M.M. Kneen, G.L. Kenyon, and M. Pohl Exchanging the substrate specificities of pyruvate decarboxylase from Zymomonas mobilis and benzoylformate decarboxylase from Pseudomonas putida Protein Eng. Des. Sel. 18 2005 345 357
13. A. Yep, G.L. Kenyon, and M.J. McLeish Saturation mutagenesis of putative catalytic residues of benzoylformate decarboxylase provides a challenge to the accepted mechanism Proc. Natl. Acad. Sci. U. S. A. 105 2008 5733 5738
14. A. Yep, and M.J. McLeish Engineering the substrate binding site of benzoylformate decarboxylase Biochemistry 48 2009 8387 8395
15. M. Widmann, R. Radloff, and J. Pleiss The Thiamine diphosphate-dependent Enzyme Engineering Database: a tool for the systematic analysis of sequence and structure relations BMC Biochem. 11 2010 9
16. C. Vogel, and J. Pleiss The modular structure of ThDP-dependent enzymes Proteins 82 2014 2523 2537
17. G.D. Hegeman Benzoylformate decarboxylase (Pseudomonas putida) Methods Enzymol. 17 1970 674 678
18. +-dependent benzaldehyde dehydrogenase involved in d-phenylglycine metabolism in Pseudomonas stutzeri ST-201 Biochim. Biophys. Acta 1770 2007 1585 1592
19. G.D. Hegeman Synthesis of the enzymes of the mandelate pathway by Pseudomonas putida I. Synthesis of enzymes by the wild type J. Bacteriol. 91 1966 1140 1154
20. M.M. Barrowman, and C.A. Fewson Phenylglyoxylate decarboxylase and phenylpyruvate decarboxylase from Acinetobacter calcoaceticus Curr. Microbiol. 12 1985 235 239
21. G. Engelhardt, W. Ziegler, P.R. Wollnofer, H.J. Jarczyk, and L. Oehlmann Degradation of the triazinone herbicide metamitron by Arthrobacter spec. DSM 20369 J. Agric. Food Chem. 30 1982 278 282
22. H. Henning, C. Leggewie, M. Pohl, M. Müller, T. Eggert, and K.-E. Jaeger Identification of novel benzoylformate decarboxylases by growth selection Appl. Environ. Microbiol. 72 2006 7510 7517
23. R. Shrivastava, A. Basu, and P. Phale Purification and characterization of benzyl alcohol- and benzaldehyde-dehydrogenase from Pseudomonas putida CSV86 Arch. Microbiol. 193 2011 553 563
24. +-dependent benzaldehyde dehydrogenase from Pseudomonas putida ATCC 12633 J. Bacteriol. 185 2003 2451 2456
25. M.S. Hasson, A. Muscate, M.J. McLeish, L.S. Polovnikova, J.A. Gerlt, G.L. Kenyon, G.A. Petsko, and D. Ringe The crystal structure of benzoylformate decarboxylase at 1.6 Å resolution: diversity of catalytic residues in thiamin diphosphate-dependent enzymes Biochemistry 37 1998 9918 9930
26. M. Bruning, M. Berheide, D. Meyer, R. Golbik, H. Bartunik, A. Liese, and K. Tittmann Structural and kinetic studies on native intermediates and an intermediate analogue in benzoylformate decarboxylase reveal a least motion mechanism with an unprecedented short-lived predecarboxylation intermediate Biochemistry 48 2009 3258 3268
27. A.K. Bera, L.S. Polovnikova, J. Roestamadji, T.S. Widlanski, G.L. Kenyon, M.J. McLeish, and M.S. Hasson Mechanism-based inactivation of benzoylformate decarboxylase, a thiamin diphosphate-dependent enzyme J. Am. Chem. Soc. 129 2007 4120 4121
28. F.H. Andrews, A.R. Tom, P.R. Gunderman, W.R.P. Novak, and M.J. McLeish A bulky hydrophobic residue is not required to maintain the V-conformation of enzyme-bound thiamin diphosphate Biochemistry 52 2013 3028 3030
29. S.B. Snapper, R.E. Melton, S. Mustafa, T. Kieser, and W.R. Jacobs Jr. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis Mol. Microbiol. 4 1990 1911 1919
30. K.J. Ellis, and J.F. Morrison Buffers of constant ionic strength for studying pH-dependent processes Methods Enzymol. 87 1982 405 426
31. Z. Otwinowski, and W. Minor Processing of X-ray Diffraction Data Collected in Oscillation Mode 1997 Elsevier 307 326
32. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. Sect. D 60 2004 2126 2132
33. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. Sect. D 67 1997 355 367
34. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, A.J. McCoy, N.W. Moriarty, R. Oeffner, R.J. Read, D.C. Richardson, J.S. Richardson, T.C. Terwilliger, and P.H. Zwart PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. Sect. D 66 2010 213 221
35. V.B. Chen, W.B. Arendall III, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. Sect. D 66 2010 12 21
36. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, X. Wang, L.W. Murray, W.B. Arendall, J. Snoeyink, J.S. Richardson, and D.C. Richardson MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res. 35 2007 W375 W383
37. H. Iding, T. Dünnwald, L. Greiner, A. Liese, M. Müller, P. Siegert, J. Grötzinger, A.S. Demir, and M. Pohl Benzoylformate decarboxylase from Pseudomonas putida as stable catalyst for the synthesis of chiral 2-hydroxy ketones Chem. Eur. J. 6 2000 1483 1495
38. C. Abreu-Goodger, and E. Merino RibEx: a web server for locating riboswitches and other conserved bacterial regulatory elements Nucleic Acids Res. 33 2005 W690 W692
39. A. Yep, G.L. Kenyon, and M.J. McLeish Determinants of substrate specificity in KdcA, a thiamin diphosphate-dependent decarboxylase Bioorg. Chem. 34 2006 325 336
40. M.M. Kneen, R. Stan, A. Yep, R.P. Tyler, C. Saehuan, and M.J. McLeish Characterization of a thiamin diphosphate-dependent phenylpyruvate decarboxylase from Saccharomyces cerevisiae FEBS J. 278 2011 1842 1853
41. N. Nemeria, A. Baykal, E. Joseph, S. Zhang, Yan, W. Furey, and F. Jordan Tetrahedral intermediates in thiamin diphosphate-dependent decarboxylations exist as a 1′,4′-imino tautomeric form of the coenzyme, unlike the Michaelis complex or the free coenzyme Biochemistry 43 2004 6565 6575
42. N. Nemeria, S. Chakraborty, A. Baykal, L.G. Korotchkina, M.S. Patel, and F. Jordan The 1′,4′-iminopyrimidine tautomer of thiamin diphosphate is poised for catalysis in asymmetric active centers on enzymes Proc. Natl. Acad. Sci. U. S. A. 104 2007 78 82
43. N. Nemeria, L. Korotchkina, M.J. McLeish, G.L. Kenyon, M.S. Patel, and F. Jordan Elucidation of the chemistry of enzyme-bound thiamin diphosphate prior to substrate binding: defining internal equilibria among tautomeric and ionization states Biochemistry 46 2007 10739 10744
44. G.S. Brandt, M.M. Kneen, S. Chakraborty, A.T. Baykal, N. Nemeria, A. Yep, D.I. Ruby, G.A. Petsko, G.L. Kenyon, M.J. McLeish, F. Jordan, and D. Ringe Snapshot of a reaction intermediate: analysis of benzoylformate decarboxylase in complex with a benzoylphosphonate inhibitor Biochemistry 48 2009 3247 3257
45. K. Chandrasekhar, P. Arjunan, M. Sax, N. Nemeria, F. Jordan, and W. Furey Active-site changes in the pyruvate dehydrogenase multienzyme complex E1 apoenzyme component from Escherichia coli observed at 2.32 Å resolution Acta Crystallogr. Sect. D 62 2006 1382 1386
46. R.A.W. Frank, A.J. Price, F.D. Northrop, R.N. Perham, and B.F. Luisi Crystal structure of the E1 component of the Escherichia coli 2-oxoglutarate dehydrogenase multienzyme complex J. Mol. Biol. 368 2007 639 651
47. J. Li, R.M. Wynn, M. Machius, J.L. Chuang, S. Karthikeyan, D.R. Tomchick, and D.T. Chuang Cross-talk between thiamin diphosphate binding and phosphorylation loop conformation in human branched-chain α-keto acid decarboxylase/dehydrogenase J. Biol. Chem. 279 2004 32968 32978
48. T. Nakai, N. Nakagawa, N. Maoka, R. Masui, S. Kuramitsu, and N. Kamiya Ligand-induced conformational changes and a reaction intermediate in branched-chain 2-oxo acid dehydrogenase (E1) from Thermus thermophilus HB8, as revealed by X-ray crystallography J. Mol. Biol. 337 2004 1011 1033
49. X.-Y. Pei, K.M. Erixon, B.F. Luisi, and F.J. Leeper Structural insights into the prereaction state of pyruvate decarboxylase from Zymomonas mobilis Biochemistry 49 2010 1727 1736
50. M. Sundstrom, Y. Lindqvist, and G. Schneider Three-dimensional structure of apotransketolase. Flexible loops at the active site enable cofactor binding FEBS Lett. 313 1992 229 231
51. U. Nilsson, L. Meshalkina, Y. Lindqvist, and G. Schneider Examination of substrate binding in thiamin diphosphate-dependent transketolase by protein crystallography and site-directed mutagenesis J. Biol. Chem. 272 1997 1864 1869
52. F. Guo, D. Zhang, A. Kahyaoglu, R.S. Farid, and F. Jordan Is a hydrophobic amino acid required to maintain the reactive V conformation of thiamin at the active center of thiamin diphosphate-requiring enzymes? Experimental and computational studies of isoleucine 415 of yeast pyruvate decarboxylase Biochemistry 37 1998 13379 13391
53. N. Furnham, T.A. de Beer, and J.M. Thornton Current challenges in genome annotation through structural biology and bioinformatics Curr. Opin. Struct. Biol. 22 2012 594 601
54. K.R. Ramkissoon, J.K. Miller, S. Ojha, D.S. Watson, M.G. Bomar, A.K. Galande, and A.G. Shearer Rapid identification of sequences for orphan enzymes to power accurate protein annotation PLoS One 8 2013 e84508
55. D. Frishman Protein annotation at genomic scale: the current status Chem. Rev. 107 2007 3448 3466
56. A.M. Schnoes, S.D. Brown, I. Dodevski, and P.C. Babbitt Annotation error in public databases: misannotation of molecular function in enzyme superfamilies PLoS Comput. Biol. 5 2009 e1000605
57. K. Tittmann, R. Golbik, K. Uhlemann, L. Khailova, G. Schneider, M. Patel, F. Jordan, D.M. Chipman, R.G. Duggleby, and G. Hübner NMR analysis of covalent intermediates in thiamin diphosphate enzymes Biochemistry 42 2003 7885 7891
58. S. Harayama, M. Rekik, K.L. Ngai, and L.N. Ornston Physically associated enzymes produce and metabolize 2-hydroxy-2,4-dienoate, a chemically unstable intermediate formed in catechol metabolism via meta cleavage in Pseudomonas putida J. Bacteriol. 171 1989 6251 6258
59. S.C. Wang, W.H. Johnson, R.M. Czerwinski, S.L. Stamps, and C.P. Whitman Kinetic and stereochemical analysis of YwhB, a 4-oxalocrotonate tautomerase homologue in Bacillus subtilis: mechanistic implications for the YwhB- and 4-oxalocrotonate tautomerase-catalyzed reactions Biochemistry 46 2007 11919 11929
60. B.J. Baas, E. Zandvoort, A.A. Wasiel, W.J. Quax, and G.J. Poelarends Characterization of a newly identified mycobacterial tautomerase with promiscuous dehalogenase and hydratase activities reveals a functional link to a recently diverged cis-3-chloroacrylic acid dehalogenase Biochemistry 50 2011 2889 2899
61. J.A. Gerlt, K.N. Allen, S.C. Almo, R.N. Armstrong, P.C. Babbitt, J.E. Cronan, D. Dunaway-Mariano, H.J. Imker, M.P. Jacobson, W. Minor, C.D. Poulter, F.M. Raushel, A. Sali, B.K. Shoichet, and J.V. Sweedler The Enzyme Function Initiative Biochemistry 50 2011 9950 9962