Mechanism of the intramolecular claisen condensation reaction catalyzed by MenB, a crotonase superfamily member

Biochemistry

Volumn 50, Issue 44, 2011, Pages 9532-9544

  Li, Huei Jiun ^a   Li, Xiaokai ^a   Liu, Nina ^a   Zhang, Huaning ^a   Truglio, James J ^a   Mishra, Shambhavi ^b   Kisker, Caroline ^b   Garcia Diaz, Miguel ^a   Tonge, Peter J ^a  

^a STONY BROOK UNIVERSITY   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACID-BASE CATALYSTS; ACTIVE SITE; ACTIVE SITE RESIDUES; BENZYLIC; BIOSYNTHESIS PATHWAYS; CARBON-CARBON BOND FORMATION; CATALYTIC MECHANISMS; DIECKMANN REACTION; ELECTROPHILES; ENZYME-SUBSTRATE COMPLEXES; HEXAMERS; HYDRATASE; INTRAMOLECULAR TRANSFER; MECHANISTIC PROBES; MECHANISTIC STUDIES; MYCOBACTERIUM TUBERCULOSIS; OXYANION HOLE; QUATERNARY STRUCTURE; STRUCTURAL DATA; SYNTHASES; TETRAHEDRAL INTERMEDIATES; X-RAY STRUCTURE;

BIOCHEMISTRY; CARBOXYLATION; CARBOXYLIC ACIDS; CATALYSIS; CONDENSATION; ESCHERICHIA COLI; PROTONS; SUBSTRATES;

CONDENSATION REACTIONS;

AMINE; ANION; BACTERIAL ENZYME; CARBON; COENZYME A; ELECTROPHILE; ENOYL COENZYME A HYDRATASE; O SUCCINYLBENZOYL AMINO COENZYME A; OXYANION; PROTEIN MENB; PROTON; TYROSINE; UNCLASSIFIED DRUG;

ACID BASE BALANCE; ACIDITY; ARTICLE; CATALYSIS; CATALYST; CHEMICAL BOND; CHEMICAL STRUCTURE; CLAISEN CONDENSATION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME STABILITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTON TRANSPORT; X RAY ANALYSIS;

AMINO ACID SEQUENCE; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ENOYL-COA HYDRATASE; ESCHERICHIA COLI PROTEINS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MYCOBACTERIUM TUBERCULOSIS; PROTEIN BINDING; SUBSTRATE SPECIFICITY; SUCCINATE-COA LIGASES; VITAMIN K 2;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; MYCOBACTERIUM TUBERCULOSIS;

EID: 80155126202     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200877x     Document Type: Article

References (72)

1. Bishop, D. H. L., Pandya, K. P., and King, H. K. (1962) Ubiquinone and Vitamin K in Bacteria Biochem. J. 83, 606-614
2. Collins, M. D., Goodfellow, M., Minnikin, D. E., and Alderson, G. (1985) Menaquinone composition of mycolic acid-containing actinomycetes and some sporoactinomycetes J. Appl. Bacteriol. 58, 77-86 (Pubitemid 15136131)
3. Dowd, P., Ham, S. W., Naganathan, S., and Hershline, R. (1995) The Mechanism of Action of Vitamin K Annu. Rev. Nutr. 15, 419-440
4. Olson, R. E. (1984) The function and metabolism of vitamin K Annu. Rev. Nutr. 4, 281-337
5. Kurosu, M., Narayanasamy, P., Biswas, K., Dhiman, R., and Crick, D. C. (2007) Discovery of 1,4-dihydroxy-2-naphthoate prenyltransferase inhibitors: new drug leads for multidrug-resistant gram-positive pathogens J. Med. Chem. 50, 3973-3975 (Pubitemid 47301729)
6. Li, X., Liu, N., Zhang, H., Knudson, S. E., Slayden, R. A., and Tonge, P. J. (2010) Synthesis and SAR studies of 1,4-benzoxazine MenB inhibitors: novel antibacterial agents against Mycobacterium tuberculosis Bioorg. Med. Chem. Lett. 20, 6306-6309
7. Lu, X., Zhang, H., Tonge, P. J., and Tan, D. S. Mechanism-based inhibitors of MenE, an acyl-CoA synthetase involved in bacterial menaquinone biosynthesis. Bioorg. Med. Chem. Lett. 2008, not supplied.
8. Truglio, J. J., Theis, K., Feng, Y., Gajda, R., Machutta, C., Tonge, P. J., and Kisker, C. (2003) Crystal Structure of Mycobacterium tuberculosis MenB, a Key Enzyme in Vitamin K2 Biosynthesis J. Biol. Chem. 278, 42352-42360 (Pubitemid 37310505)
9. Bentley, R. and Meganathan, R. (1982) Biosynthesis of vitamin K (menaquinone) in bacteria Microbiol. Rev. 46, 241-280 (Pubitemid 13205002)
10. Meganathan, R. (2001) Biosynthesis of menaquinone (vitamin K2) and ubiquinone (coenzyme Q): a perspective on enzymatic mechanisms Vitam. Horm. 61, 173-218 (Pubitemid 33805695)
11. Jiang, M., Cao, Y., Guo, Z. F., Chen, M., Chen, X., and Guo, Z. (2007) Menaquinone biosynthesis in Escherichia coli: identification of 2-succinyl-5-enolpyruvyl-6-hydroxy-3-cyclohexene-1-carboxylate as a novel intermediate and re-evaluation of MenD activity Biochemistry 46, 10979-10989 (Pubitemid 47463049)
12. Jiang, M., Chen, X., Guo, Z. F., Cao, Y., Chen, M., and Guo, Z. (2008) Identification and characterization of (1R,6R)-2-succinyl-6-hydroxy-2,4- cyclohexadiene-1-carboxylate synthase in the menaquinone biosynthesis of Escherichia coli Biochemistry 47, 3426-3434 (Pubitemid 351399231)
13. Bryant, R. W., Jr. and Bentley, R. (1976) Menaquinone biosynthesis: conversion of o-succinylbenzoic acid to 1,4-dihydroxy-2-naphthoic acid and menaquinones by Escherichia coli extracts Biochemistry 15, 4792-4796
14. Meganathan, R. and Bentley, R. (1979) Menaquinone (vitamin K2) biosynthesis: conversion of o-succinylbenzoic acid to 1,4-dihydroxy-2-naphthoic acid by Mycobacterium phlei enzymes J. Bacteriol. 140, 92-98 (Pubitemid 10248472)
15. Heath, R. J. and Rock, C. O. (2002) The Claisen condensation in biology Nat. Prod. Rep. 19, 581-596 (Pubitemid 35259019)
16. Zhang, H., Machutta, C. A., and Tonge, P. J. (2010) Fatty Acid Biosynthesis and Oxidation, in Comprehensive Natural Products Chemistry II Chemistry and Biology (Mander, L. and Lui, H.-W., Eds.) pp 231-275.
17. 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)
18. Holden, H. M., Benning, M. M., Haller, T., and Gerlt, J. A. (2001) The crotonase superfamily: divergently related enzymes that catalyze different reactions involving acyl coenzyme a thioesters Acc. Chem. Res. 34, 145-157 (Pubitemid 32167864)
19. Hamed, R. B., Batchelar, E. T., Clifton, I. J., and Schofield, C. J. (2008) Mechanisms and structures of crotonase superfamily enzymes - how nature controls enolate and oxyanion reactivity Cell. Mol. Life Sci. 65, 2507-2527
20. Bell, A. F., Wu, J., Feng, Y., and Tonge, P. J. (2001) Involvement of glycine 141 in substrate activation by enoyl-CoA hydratase Biochemistry 40, 1725-1733 (Pubitemid 32144043)
21. Jiang, M., Chen, M., Guo, Z. F., and Guo, Z. (2010) A bicarbonate cofactor modulates 1,4-dihydroxy-2-naphthoyl-coenzyme a synthase in menaquinone biosynthesis of Escherichia coli J. Biol. Chem. 285, 30159-30169
22. Johnston, J. M., Arcus, V. L., and Baker, E. N. (2005) Structure of naphthoate synthase (MenB) from Mycobacterium tuberculosis in both native and product-bound forms Acta Crystallogr., Sect. D: Biol. Crystallogr. 61, 1199-1206 (Pubitemid 43961291)
23. Ulaganathan, V., Agacan, M. F., Buetow, L., Tulloch, L. B., and Hunter, W. N. (2007) Structure of Staphylococcus aureus 1,4-dihydroxy-2-naphthoyl-CoA synthase (MenB) in complex with acetoacetyl-CoA Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 63, 908-913 (Pubitemid 350134956)
24. Minasov, G., Wawrzak, Z., Skarina, T., Onopriyenko, O., Peterson, S. N., Savchenko, A., and Anderson, W. F. 2.15 Angstrom Resolution Crystal Structure of Naphthoate Synthase from Salmonella typhimurium. Cent. Struct. Genomics Infect. Dis. 2009, not supplied.
25. Jeyakanthan, J., Kanaujia, S. P., Vasuki Ranjani, C., Sekar, K., BaBa, S., Ebihara, A., Kuramitsu, S., Shinkai, A., Shiro, Y., and Yokoyama, S. Crystal structure of dihydroxynapthoic acid synthetase (GK2873) from Geobacillus kaustophilus HTA426. RIKEN Struct. Genomics/Proteomics Initiative 2006, not supplied.
26. Martin, D. P. and Drueckhammer, D. G. (1992) Combined Chemical and Enzymatic Synthesis of Coenzyme A Analogs J. Am. Chem. Soc. 114, 7287-7288
27. Mishra, P. K. and Drueckhammer, D. G. (2000) Coenzyme A analogues and derivatives: Synthesis and applications as mechanistic probes of coenzyme-A ester utilizing enzymes Chem. Rev. 100, 3283-3310
28. Dai, M., Feng, Y., and Tonge, P. J. (2001) Synthesis of crotonyl-oxyCoA: a mechanistic probe of the reaction catalyzed by enoyl-CoA hydratase J. Am. Chem. Soc. 123, 506-507 (Pubitemid 32105142)
29. Otwinowski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
30. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement J. Appl. Crystallogr. 30, 1022-1025 (Pubitemid 127485985)
31. Moriarty, N. W., Grosse-Kunstleve, R. W., and Adams, P. D. (2009) electronic Ligand Builder and Optimization Workbench (eLBOW): a tool for ligand coordinate and restraint generation Acta Crystallogr., Sect. D: Biol. Crystallogr. 65, 1074-1080
32. Weininger, D. (1990) SMILES. 3. DEPICT. Graphical depiction of chemical structures J. Chem. Inf. Comput. Sci. 30, 237-243
33. Adams, P. D., Afonine, P. V., Bunkoczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., Richardson, J. S., Terwilliger, T. C., and Zwart, P. H. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 213-221
34. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
35. Chen, V. B., Arendall, W. B., Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr., Sect. D: Biol. Crystallogr. 66, 12-21
36. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
37. Beaman, T. W., Vogel, K. W., Drueckhammer, D. G., Blanchard, J. S., and Roderick, S. L. (2002) Acyl group specificity at the active site of tetrahydrodipicolinate N-succinyltransferase Protein Sci. 11, 974-979 (Pubitemid 34241305)
38. Widboom, P. F., Fielding, E. N., Liu, Y., and Bruner, S. D. (2007) Structural basis for cofactor-independent dioxygenation in vancomycin biosynthesis Nature 447, 342-345 (Pubitemid 46788825)
39. Fielding, E. N., Widboom, P. F., and Bruner, S. D. (2007) Substrate recognition and catalysis by the cofactor-independent dioxygenase DpgC Biochemistry 46, 13994-14000 (Pubitemid 350250296)
40. Liu, Y. and Bruner, S. D. (2007) Rational manipulation of carrier-domain geometry in nonribosomal peptide synthetases ChemBioChem 8, 617-621 (Pubitemid 47194852)
41. Kelley, L. A. and Sternberg, M. J. E. (2009) Protein structure prediction on the Web: a case study using the Phyre server Nature Protocols 4, 363-371
42. Benning, M. M., Taylor, K. L., Liu, R. Q., Yang, G., Xiang, H., Wesenberg, G., DunawayMariano, D., and Holden, H. M. (1996) Structure of 4-chlorobenzoyl coenzyme A dehalogenase determined to 1.8 angstrom resolution: An enzyme catalyst generated via adaptive mutation Biochemistry 35, 8103-8109 (Pubitemid 26234908)
43. Engel, C. K., Mathieu, M., Zeelen, J. P., Hiltunen, J. K., and Wierenga, R. K. (1996) Crystal structure of enoyl-coenzyme A (CoA) hydratase at 2.5 angstrom resolution: A spiral fold defines the CoA-binding pocket EMBO J. 15, 5135-5145 (Pubitemid 26336195)
44. Wu, W. J., Anderson, V. E., Raleigh, D. P., and Tonge, P. J. (1997) Structure of hexadienoyl-CoA bound to enoyl-CoA hydratase determined by transferred nuclear Overhauser effect measurements: mechanistic predictions based on the X-ray structure of 4-(chlorobenzoyl)-CoA dehalogenase Biochemistry 36, 2211-2220 (Pubitemid 27104714)
45. Benning, M. M., Haller, T., Gerlt, J. A., and Holden, H. M. (2000) New reactions in the crotonase superfamily: Structure of methylmalonyl CoA decarboxylase from Escherichia coli Biochemistry 39, 4630-4639 (Pubitemid 30225326)
46. Bell, A. F., Feng, Y. G., Hofstein, H. A., Parikh, S., Wu, J. Q., Rudolph, M. J., Kisker, C., Whitty, A., and Tonge, P. J. (2002) Stereoselectivity of enoyl-CoA hydratase results from preferential activation of one of two bound substrate conformers Chem. Biol. 9, 1247-1255 (Pubitemid 35352772)
47. Hall, P. R., Wang, Y. F., Rivera-Hainaj, R. E., Zheng, X. J., Pustai-Carey, M., Carey, P. R., and Yee, V. C. (2003) Transcarboxylase 12S crystal structure: hexamer assembly and substrate binding to a multienzyme core EMBO J. 22, 2334-2347 (Pubitemid 36604973)
48. Bennett, J. P., Bertin, L., Moulton, B., Fairlamb, I. J. S., Brzozowski, A. M., Walton, N. J., and Grogan, G. (2008) A ternary complex of hydroxycinnamoyl-CoA hydratase-lyase (HCHL) with acetyl-CoA and vanillin gives insights into substrate specificity and mechanism Biochem. J. 414, 281-289
49. Thoden, J. B., Ringia, E. A. T., Garrett, J. B., Gerlt, J. A., Holden, H. M., and Rayment, I. (2004) Evolution of enzymatic activity in the enolase superfamily: Structural studies of the promiscuous o-succinylbenzoate synthase from Amycolatopsis Biochemistry 43, 5716-5727 (Pubitemid 38623606)
50. Sugadev, R., Burley, S. K., and Swaminathan, S. Crystal structure of O-succinylbenzoate synthase complexed with O-succinyl benzoate (OSB). N. Y. SGX Res. Center Struct. Genomics 2007, not supplied.
51. Thompson, T. B., Garrett, J. B., Taylor, E. A., Meganathan, R., Gerlt, J. A., and Rayment, I. (2000) Evolution of enzymatic activity in the enolase superfamily: structure of o-succinylbenzoate synthase from Escherichia coli in complex with Mg2+ and o-succinylbenzoate Biochemistry 39, 10662-10676
52. Schuttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 1355-1363 (Pubitemid 41079731)
53. Gandour, R. D. (1981) On the importance of orientation in general base catalysis by carboxylate Bioorg. Chem. 10, 169-176
54. Ramanadham, M., Jakkal, V. S., and Chidambaram, R. (1993) Carboxyl group hydrogen bonding in X-ray protein structures analysed using neutron studies on amino acids FEBS Lett. 323, 203-206 (Pubitemid 23153469)
55. Wong, B. J. and Gerlt, J. A. (2004) Evolution of function in the crotonase superfamily: (3S)-methylglutaconyl-CoA hydratase from Pseudomonas putida Biochemistry 43, 4646-4654 (Pubitemid 38509084)
56. Pelletier, D. A. and Harwood, C. S. (1998) 2-Ketocyclohexanecarboxyl coenzyme A hydrolase, the ring cleavage enzyme required for anaerobic benzoate degradation by Rhodopseudomonas palustris J. Bacteriol. 180, 2330-2336 (Pubitemid 28217344)
57. Bahnson, B. J., Anderson, V. E., and Petsko, G. A. (2002) Structural mechanism of enoyl-CoA hydratase: Three atoms from a single water are added in either an E1cb stepwise or concerted fashion Biochemistry 41, 2621-2629 (Pubitemid 34168931)
58. Engel, C. K., Kiema, T. R., Hiltunen, J. K., and Wierenga, R. K. (1998) The crystal structure of enoyl-CoA hydratase complexed with octanoyl-CoA reveals the structural adaptations required for binding of a long chain fatty acid-CoA molecule J. Mol. Biol. 275, 847-859 (Pubitemid 28077700)
59. Mursula, A. M., Hiltunen, J. K., and Wierenga, R. K. (2004) Structural studies on Delta(3)-Delta(2)-enoyl-CoA isomerase: the variable mode of assembly of the trimeric disks of the crotonase superfamily FEBS Lett. 557, 81-87 (Pubitemid 38115873)
60. Xiang, H., Luo, L., Taylor, K. L., and Dunaway-Mariano, D. (1999) Interchange of Catalytic Activity within the 2-Enoyl-Coenzyme A Hydratase/Isomerase Superfamily Based on a Common Active Site Template Biochemistry 38, 7638-7652
61. Bennett, M. J., Schlunegger, M. P., and Eisenberg, D. (1995) 3D Domain swapping-a mechanism for oligomer assembly Protein Sci. 4, 2455-2468
62. Hofstein, H. A., Feng, Y., Anderson, V. E., and Tonge, P. J. (1999) Role of Glutamate 144 and Glutamate 164 in the Catalytic Mechanism of Enoyl-CoA Hydratase Biochemistry 38, 9508-9516
63. Modis, Y., Filppula, S. A., Novikov, D. K., Norledge, B., Hiltunen, J. K., and Wierenga, R. K. (1998) The crystal structure of dienoyl-CoA isomerase at 1.5 A resolution reveals the importance of aspartate and glutamate sidechains for catalysis Structure 6, 957-970 (Pubitemid 28397918)
64. Muller-Newen, G. and Stoffel, W. (1993) Site-directed mutagenesis of putative active-site amino acid residues of 3,2-trans-enoyl-CoA isomerase, conserved within the low-homology isomerase/hydratase enzyme family Biochemistry 32, 11405-11412 (Pubitemid 23332053)
65. Igbavboa, U. and Leistner, E. (1990) Sequence of proton abstraction and stereochemistry of the reaction catalyzed by naphthoate synthase, an enzyme involved in menaquinone (vitamin K2) biosynthesis Eur. J. Biochem. 192, 441-449 (Pubitemid 20283513)
66. Eberhard, E. D. and Gerlt, J. A. (2004) Evolution of function in the crotonase superfamily: the stereochemical course of the reaction catalyzed by 2-ketocyclohexanecarboxyl-CoA hydrolase J. Am. Chem. Soc. 126, 7188-7189 (Pubitemid 38747764)
67. Laskowski, R. A., Hutchinson, E. G., Michie, A. D., Wallace, A. C., Jones, M. L., and Thornton, J. M. (1997) PDBsum: a Web-based database of summaries and analyses of all PDB structures Trends Biochem. Sci. 22, 488-490 (Pubitemid 27515917)
68. Delano, W. L. (2002) The PyMOL Molecular Graphics System http://www.pymol.org.
69. Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004) The Jalview Java alignment editor Bioinformatics 20, 426-427 (Pubitemid 38262778)
70. Waterhouse, A. M., Procter, J. B., Martin, D. M. A., Clamp, M., and Barton, G. J. (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench Bioinformatics 25, 1189-1191
71. Leonard, P. M. and Grogan, G. (2004) Structure of 6-oxo camphor hydrolase H122A mutant bound to its natural product, (2 S,4 S)-alpha-campholinic acid-Mutant structure suggests an atypical mode of transition state binding for a crotonase homolog J. Biol. Chem. 279, 31312-31317 (Pubitemid 39037797)
72. Bennett, J. P., Whittingham, J. L., Brzozowski, A. M., Leonard, P. M., and Grogan, G. (2007) Structural characterization of a beta-diketone hydrolase from the cyanobacterium Anabaena sp PCC 7120 in native and product-bound forms, a coenzyme A-independent member of the crotonase suprafamily Biochemistry 46, 137-144 (Pubitemid 46067743)