Stabilization of the second oxyanion intermediate by 1,4-dihydroxy-2- naphthoyl-coenzyme a synthase of the menaquinone pathway: Spectroscopic evidence of the involvement of a conserved aspartic acid

Biochemistry

Volumn 50, Issue 26, 2011, Pages 5893-5904

  Chen, Minjiao ^a   Jiang, Ming ^a,b   Sun, Yueru ^a   Guo, Zu Feng ^a,c   Guo, Zhihong ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b Tufts University   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ASPARTIC ACIDS; BASIC SOLUTIONS; BIOSYNTHETIC PATHWAY; BOUND LIGANDS; CATALYTIC MECHANISMS; CONSERVED POLAR RESIDUES; ELECTRON TRANSPORTER; ENZYME-LIGAND INTERACTIONS; HIGH ENERGY; HYDROGEN BONDING NETWORK; HYDROXYL GROUPS; LIGAND BINDING; OXYANIONS; SIDE-CHAINS; SITE-DIRECTED MUTATION; SMALL MOLECULES; SPECTRAL CHANGE; SPECTROSCOPIC EVIDENCE; SPECTROSCOPIC STUDIES; SYNTHASES;

AMINO ACIDS; CONDENSATION; CONDENSATION REACTIONS; ELECTRON ENERGY LOSS SPECTROSCOPY; ESCHERICHIA COLI; HYDROGEN; HYDROGEN BONDS; LIGANDS; POSITIVE IONS; REACTION INTERMEDIATES; SPECTROSCOPIC ANALYSIS; SPECTROSCOPY;

ENZYME ACTIVITY;

1,4 DIHYDROXY 2 NAPHTHOYL COENZYME A SYNTHASE; 3 HYDROXYBENZOYL COENZYME A; 3,4 DIHYDROXYBENZOYL COENZYME A; 3,5 DIHYDROXYBENZOYL COENZYME A; 4 HYDROXYBENZOYL COENZYME A; ASPARTIC ACID; BACILLUS SUBTILIS MENB PROTEIN; BACTERIAL PROTEIN; COENZYME A; ESCHERICHIA COLI MENB PROTEIN; MENAQUINONE; MYCOBACTERIUM SMEGMATIS MENB PROTEIN; MYCOBACTERIUM TUBERCULOSIS MENB PROTEIN; STAPHYLOCOCCUS AUREUS MENB PROTEIN; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CLAISEN CONDENSATION; ENZYME ACTIVITY; ENZYME BINDING; ENZYME INHIBITION; ENZYME STRUCTURE; HYDROGEN BOND; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; PRIORITY JOURNAL; PROTON TRANSPORT; SPECTROSCOPY; ULTRAVIOLET SPECTROSCOPY;

ABSORPTION; ASPARTIC ACID; BACTERIA; CATALYTIC DOMAIN; COENZYME A; CONSERVED SEQUENCE; ENZYME STABILITY; HYDROGEN BONDING; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; OXO-ACID-LYASES; OXYGEN; PHENOLS; PROTONS; SPECTRUM ANALYSIS; VITAMIN K 2;

ESCHERICHIA COLI;

EID: 79959777970     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi200376x     Document Type: Article

References (57)

1. Meganathan, R. (2001) Biosynthesis of menaquinone (vitamin K2) and ubiquinone (coenzyme Q): A perspective on enzymatic mechanisms Vitam. Horm. 61, 173-218 (Pubitemid 33805695)
2. Forsyth, R. A., Haselbeck, R. J., Ohlsen, K. L., Yamamoto, R. T., Xu, H., Trawick, J. D., Wall, D., Wang, L., Brown-Driver, V., Froelich, J. M., Kedar, G. C., King, P., McCarthy, M., Malone, C., Misiner, B., Robbins, D., Tan, Z., Zhu, Z.-y., Carr, G., Mosca, D. A., Zamudio, C., Foulkes, J. G., and Zyskind, J. W. (2002) A genome-wide strategy for the identification of essential genes in Staphylococcus aureus Mol. Microbiol. 43, 1387-1400 (Pubitemid 34595533)
3. Kobayashi, K., Ehrlich, S. D., Albertini, A., Amati, G., Andersen, K. K., Arnaud, M., Asai, K., Ashikaga, S., Aymerich, S., Bessieres, P., Boland, F., Brignell, S. C., Bron, S., Bunai, K., Chapuis, J., Christiansen, L. C., Danchin, A., Débarbouille, M., Dervyn, E., Deuerling, E., Devine, K., Devine, S. K., Dreesen, O., Errington, J., Fillinger, S., Foster, S. J., Fujita, Y., Galizzi, A., Gardan, R., Eschevins, C., Fukushima, T., Haga, K., Harwood, C. R., Hecker, M., Hosoya, D., Hullo, M. F., Kakeshita, H., Karamata, D., Kasahara, Y., Kawamura, F., Koga, K., Koski, P., Kuwana, R., Imamura, D., Ishimaru, M., Ishikawa, S., Ishio, I., Le Coq, D., Masson, A., Mauël, C., Meima, R., Mellado, R. P., Moir, A., Moriya, S., Nagakawa, E., Nanamiya, H., Nakai, S., Nygaard, P., Ogura, M., Ohanan, T., O'Reilly, M., O'Rourke, M., Pragai, Z., Pooley, H. M., Rapoport, G., Rawlins, J. P., Rivas, L. A., Rivolta, C., Sadaie, A., Sadaie, Y., Sarvas, M., Sato, T., Saxild, H. H., Scanlan, E., Schumann, W., Seegers, J. F., Sekiguchi, J., Sekowska, A., Séror, S. J., Simon, M., Stragier, P., Studer, R., Takamatsu, H., Tanaka, T., Takeuchi, M., Thomaides, H. B., Vagner, V., van Dijl, J. M., Watabe, K., Wipat, A., Yamamoto, H., Yamamoto, M., Yamamoto, Y., Yamane, K., Yata, K., Yoshida, K., Yoshikawa, H., Zuber, U., and Ogasawara, N. (2003) Essential Bacillus subtilis genes Proc. Natl. Acad. Sci. U.S.A. 100, 4678-4683 (Pubitemid 36457789)
4. Akerley, B. J., Rubin, E. J., Novick, V. L., Amaya, K., Judson, N., and Mekalanos, J. J. (2002) A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae Proc. Natl. Acad. Sci. U.S.A. 99, 966-971 (Pubitemid 34106619)
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. Dhiman, R. K., Mahapatra, S., Slayden, R. A., Boyne, M. E., Lenaerts, A., Hinshaw, J. C., Angala, S. K., Chatterjee, D., Biswas, K., Narayanasamy, P., Kurosu, M., and Crick, D. C. (2009) Menaquinone synthesis is critical for maintaining mycobacterial viability during exponential growth and recovery from non-replicating persistence Mol. Microbiol. 72, 85-97
7. 2 biosynthesis J. Biol. Chem. 278, 42352-42360 (Pubitemid 37310505)
8. 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
9. 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)
10. 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. D61, 1199-1206 (Pubitemid 43961291)
11. 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. F63, 908-913 (Pubitemid 350134956)
12. D'Ordine, R. L., Bahnson, B. J., Tonge, P. J., and Anderson, V. E. (1994) Enoyl-coenzyme A hydratase-catalyzed exchange of the α-protons of coenzyme A thiol esters: A model for an enolized intermediate in the enzyme-catalyzed elimination? Biochemistry 33, 14733-14742
13. Müller-Newen, G., Janssen, U., and Stoffel, W. (1995) Enoyl-CoA hydratase and isomerase form a superfamily with a common active-site glutamate residue Eur. J. Biochem. 228, 68-73
14. 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 Å resolution: A spiral fold defines the CoA-binding pocket EMBO J. 15, 5135-5145 (Pubitemid 26336195)
15. 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)
16. 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 Å resolution reveals the importance of aspartate and glutamate side chains for catalysis Structure 6, 957-970 (Pubitemid 28397918)
17. Kiema, T.-R., Engel, C. K., Schmitz, W., Filppula, S. A., Wierenga, R. K., and Hiltunen, J. K. (1999) Mutagenic and enzymological studies of the hydratase and isomerase activities of 2-enoyl-CoA hydratase-1 Biochemistry 38, 2991-2999
18. 2-enoyl- CoA isomerase J. Mol. Biol. 309, 845-853
19. 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
20. Kraut, J. (1977) Serine proteases: Structure and mechanism of catalysis Annu. Rev. Biochem. 46, 331-358
21. Holmquist, M. (2000) α/β-Hydrolase fold enzymes: Structures, functions and mechanisms Curr. Protein Pept. Sci. 1, 209-235
22. Smith, S., Witkowski, A., and Joshi, A. K. (2003) Structural and functional organization of the animal fatty acid synthase Prog. Lipid Res. 42, 289-317 (Pubitemid 36411688)
23. White, S. W., Zheng, J., Zhang, Y.-M., and Rock, C. O. (2005) The structural biology of type II fatty acid biosynthesis Annu. Rev. Biochem. 74, 791-831 (Pubitemid 40995524)
24. Machutta, C. A., Bommineni, G. R., Luckner, S. R., Kapilashrami, K., Ruzsicska, B., Simmerling, C., Kisker, C., and Tonge, P. J. (2010) Slow onset inhibition of bacterial β-ketoacyl-acyl carrier protein synthases by thiolactomycin J. Biol. Chem. 285, 6161-6169
25. Witkowski, A., Joshi, A. K., Lindqvist, Y., and Smith, S. (1999) Conversion of a β-ketoacyl synthase to a malonyl decarboxylase by replacement of the active-site cysteine with glutamine Biochemistry 38, 11643-11650
26. Jiang, M. and Guo, Z. (2007) Effects of macromolecular crowding on the intrinsic catalytic efficiency and structure of enterobactin-specific isochorismate synthase J. Am. Chem. Soc. 129, 730-731 (Pubitemid 46183901)
27. Guo, Z.-F., Jiang, M., Zheng, S., and Guo, Z. (2008) Suppression of linear side products by macromolecular crowding in nonribosomal enterobactin biosynthesis Org. Lett. 10, 649-652
28. 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 (SEPHCHC) as a novel intermediate and re-evaluation of MenD activity Biochemistry 46, 10979-10989 (Pubitemid 47463049)
29. Jiang, M., Chen, M., Cao, Y., Yang, Y., Sze, K. H., Chen, X., and Guo, Z. (2007) Determination of the stereochemistry of 2-succinyl-5-enolpyruvyl-6- hydroxy-3-cyclohexene-1-carboxylic acid, a key intermediate in menaquinone biosynthesis Org. Lett. 9, 4765-4767
30. Jiang, M., Chen, X., Guo, Z.-F., Cao, Y., Chen, M., and Guo, Z. (2008) Identification and characterization of (1 R,6 R)-2-succinyl-6-hydroxy-2,4- cyclohexadiene-1-carboxylate synthase in the menaquinone biosynthesis of Escherichia coli Biochemistry 47, 3426-3434 (Pubitemid 351399231)
31. Jiang, M., Chen, X., Wu, X.-H., Chen, M., Wu, Y., and Guo, Z. (2009) Catalytic mechanism of SHCHC synthase in the menaquinone biosynthesis of Escherichia coli: Identification and mutational analysis of the active site residues Biochemistry 48, 6921-6931
32. Grisostomi, G., Kast, P., Pulido, R., Huynh, J., and Hilvert, D. (1997) Efficient in vivo synthesis and rapid purification of chorismic acid using an engineered Escherichia coli strain Bioorg. Chem. 25, 297-305 (Pubitemid 28218792)
33. Lai, M.-t., Li, D., Oh, E., and Liu, H.-w. (1993) Inactivation of medium-chain acyl-CoA dehydrogenase by a metabolite of hypoglycin: Characterization of the major turnover product and evidence suggesting an alternative flavin modification pathway J. Am. Chem. Soc. 115, 1619-1628
34. Guo, Z.-F., Sun, Y., Zheng, S., and Guo, Z. (2009) Preferential hydrolysis of aberrant precursors suggests an active proofreading mechanism for the type II thioesterase in Escherichia coli enterobactin biosynthesis Biochemistry 48, 1712-1722
35. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, DeLano Scientific, San Carlos, CA.
36. Emsley, P. and Cowtan, K. (2004) Coot: Model-building tools for molecular graphics Acta Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
37. Gibson, R. E. (1976) Ligand interactions with the acetylcholine receptor from Torpedo californica. Extensions of the allosteric model for cooperativity to half-of-site activity Biochemistry 15, 3890-3901
38. Brown, J. H. (2006) Breaking symmetry in protein dimers: Designs and functions Protein Sci. 15, 1-13 (Pubitemid 43004228)
39. 1 complex: Enzyme with one inactive monomer is fully active but unable to activate the second ubiquinol oxidation site in response to ligand binding at the ubiquinone reduction site J. Biol. Chem. 285, 502-510
40. 5-3-ketosteroid isomerase reaction: Absorption and fluorescence spectra of enzyme-steroid complexes J. Biol. Chem. 238, 576-585
41. Eames, T. M., Pollack, R. M., and Steiner, R. F. (1989) Orientation, accessibility, and mobility of equilenin bound to the active site of steroid isomerase? Biochemistry 28, 6269-6275 (Pubitemid 19202016)
42. 5-steroid isomerase yeaction? Biochemistry 31, 1521-1528
43. 5-steroid isomerase. A probe for the nature of hydrogen bonding to the intermediate Biochemistry 37, 700-705 (Pubitemid 28123805)
44. 5-steroid isomerase: Variation of ligand ionization state with the nature of the electrophilic component Biochemistry 39, 110-116 (Pubitemid 30033325)
45. 5-3-ketosteroid isomerase Biochemistry 28, 149-159 (Pubitemid 19046732)
46. 5-3-ketosteroid isomerase Biochemistry 34, 426-434
47. 5-3-ketosteroid isomerase revisited: Substrate polarization by active-site residues Biochemistry 34, 4441-4447
48. 5-3-ketosteroid isomerase Proc. Natl. Acad. Sci. U.S.A. 93, 8220-8224 (Pubitemid 26269537)
49. 5-steroid isomerase Science 276, 415-418
50. 5-3-ketosteroid isomerase from Pseudomonas testosterone Biochemistry 37, 8325-8330 (Pubitemid 28275451)
51. 5-3-ketosteroid isomerase from Pseudomonas testosteroni in complex with equilenin settles the correct hydrogen bonding scheme for transition state stabilization J. Biol. Chem. 274, 32863-32868 (Pubitemid 129535321)
52. 5-3-ketosteroid isomerase from Pseudomonas putida biotype B Biochemistry 39, 903-909 (Pubitemid 30075316)
53. Kraut, D. A., Sigala, P. A., Pybus, B., Liu, C. W., Ringe, D., Petsko, G. A., and Herschlag, D. (2006) Testing electrostatic complementarity in enzyme catalysis: Hydrogen bonding in the ketosteroid isomerase oxyanion hole PLoS Biol. 4, 0501-0519
54. Childs, W. and Boxer, S. G. (2010) Proton affinity of the oxyanion hole in the active site of ketosteroid isomerase Biochemistry 49, 2725-2731
55. Krauta, D. A., Sigalaa, P. A., Fennb, T. D., and Herschlag, D. (2010) Dissecting the paradoxical effects of hydrogen bond mutations in the ketosteroid isomerase oxyanion hole Proc. Natl. Acad. Sci. U.S.A. 107, 1960-1965
56. Hanoian, P., Sigala, P. A., Herschlag, D., and Hammes-Schiffer, S. (2010) Hydrogen bonding in the active site of ketosteroid isomerase: Electronic inductive effects and hydrogen bond coupling Biochemistry 49, 10339-10348
57. 5-steroid isomerase Biochemistry 37, 10499-10506 (Pubitemid 28357574)