Mechanistic insight into the reaction catalysed by bacterial type II dehydroquinases

Biochemical Journal

Volumn 458, Issue 3, 2014, Pages 547-557

  Coderch, Claire ^a   Lence, Emilio ^b   Peón, Antonio ^b   Lamb, Heather ^c   Hawkins, Alastair R ^c   Gago, Federico ^a   González Bello, Concepcioń ^b  

^a UNIVERSITY OF ALCALÁ   (Spain)

^b s n   (Spain)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Dehydroquinase; Enzymatic mechanism; Essential residue; Helicobacter pylori; MD simulation; Mycobacterium tuberculosis; Quantum mechanics molecular mechanics (QM MM); Solvent isotope effect

Indexed keywords

ARGININE; ASPARTIC ACID; BACTERIAL ENZYME; TYPE II DEHYDROQUINASE; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; CONFORMATIONAL TRANSITION; ENZYME ACTIVE SITE; ENZYME MECHANISM; ENZYME SUBUNIT; HELICOBACTER PYLORI; MOLECULAR DYNAMICS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; SIMULATION; SITE DIRECTED MUTAGENESIS;

ARGININE; ASPARTIC ACID; BACTERIAL PROTEINS; CATALYSIS; HELICOBACTER PYLORI; HYDRO-LYASES; KINETICS; MOLECULAR DYNAMICS SIMULATION; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM TUBERCULOSIS; QUANTUM THEORY; SOLVENTS;

EID: 84896893960     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20131103     Document Type: Article

References (41)

1. Cosgrove, S. E. and Carmeli, Y. (2003) The impact of antimicrobial resistance on health and economic outcomes. Clin. Infect. Dis. 36, 1433-1437 (Pubitemid 36702878)
2. Zaoutis, T. E. (2009) Antibiotic resistance: who will pay the bills. Clin. Infect. Dis. 49, 1185-1186
3. Fischbach, M. A. and Walsh, C. T. (2009) Antibiotics for emerging pathogens. Science 325, 1089-1093
4. Lewis, K. (2013) Platforms for antibiotic discovery. Nat. Rev. Drug Discov. 12, 371-387
5. Bush, K., Courvalin, P., Dantas, G., Davies, J., Eisenstein, B., Huovinen, P., Jacoby, G. A., Kishony, R., Kreiswirth, B. N., Kutter, E. et al. (2011) Tackling antibiotic resistance. Nat. Rev. Microbiol. 9, 894-896
6. Lonsdale, R., Harvey, J. N. and Mulholland, A. J. (2012) A practical guide to modelling enzyme-catalysed reactions. Chem. Soc. Rev. 41, 3025-3038
7. van der Kamp, M. W. and Mulholland, A. J. (2013) Combined quantum mechanics/molecular mechanics (QM/MM) methods in computational enzymology. Biochemistry 52, 2708-2728
8. van der Kamp, M. W., Chaudret, R. and Mulholland, A. J. (2013) QM/MM modelling of ketosteroid isomerase reactivity indicates that active site closure is integral to catalysis. FEBS J. 280, 3120-3131
9. Lamichhane, G., Freundlich, J. S., Ekins, S., Wickramaratne, N., Nolan, S. T. and Bisha, W. R. (2011) Essential metabolites of Mycobacterium tuberculosis and their mimics. MBio 2, e00301-10
10. Abell, C. (1999) Enzymology and molecular biology of the shikimate pathway. In Comprehensive Natural Products Chemistry (Meth-Cohn, O., Barton, D. and Nakanishi, K., eds), p. 573, Elsevier Science, Oxford
11. Roberts, F., Roberts, C. W., Johnson, J. J., Kyle, D. E., Krell, T., Coggins, J. R., Coombs, G. H., Milhous, W. K., Tzipori, S., Ferguson, D. J. et al. (1998) Evidence for the shikimate pathway in apicomplexan parasites. Nature 393, 801-805 (Pubitemid 28299493)
12. Price, N. C., Boam, D. J., Kelly, S. M., Duncan, D., Krell, T., Gourley, D. G., Coggins, J. R., Virden, V. and Hawkins, A. R. (1999) The folding and assembly of the dodecameric type II dehydroquinases. Biochem. J. 338, 195-202 (Pubitemid 29097303)
13. Krell, T., Pitt, A. R. and Coggins, J. R. (1995) The use of electrospray mass spectrometry to identify an essential arginine residue in type II dehydroquinases. FEBS Lett. 360, 93-96
14. Krell, T., Horsburgh, M. J., Cooper, A., Kelly, S. M. and Coggins, J. R. (1996) Localization of the active site of type II dehydroquinase. Identification of a common arginine-containing motif in the two classes of dehydroquinases. J. Biol. Chem. 271, 24492-24497 (Pubitemid 26333185)
15. Harris, J., González-Bello, C., Kleanthous, C., Coggins, J. R., Hawkins, A. R. and Abell, C. (1996) Evidence from kinetic isotope studies for an enolate intermediate in the mechanism of type II dehydroquinases. Biochem. J. 319, 333-336 (Pubitemid 26372186)
16. Roszak, A. W., Robinson, D. A., Krell, T., Hunter, I. S., Frederickson, M., Abell, C., Coggins, J. R. and Lapthorn, A. J. (2002) The structure and mechanism of the type II dehydroquinase from Streptomyces coelicolor. Structure 10, 493-503 (Pubitemid 34304228)
17. Peón, A., Otero, J. M., Tizón, L., Prazeres, V. F. V., Llamas-Saiz, A. L., Fox, G. C., van Raaij, M. J., Lamb, H., Hawkins, A. R., Gago, F. et al. (2010) Understanding the key factors that control the inhibition of type II dehydroquinase by (2R)-2-benzyl-3-dehydroquinic acids. ChemMedChem 5, 1726-1733
18. Blomberg, L. M., Mangold, M., Mitchell, J. B. O. and Blumberger, J. (2009) Theoretical study of the reaction mechanism of Streptomyces coelicolor type II dehydroquinase. J. Chem. Theory Comput. 5, 1284-1294
19. Cornell, W. D., Cieplak, P., Bayly, C. I., Gould, I. R., Merz, K. M., Ferguson, D. M., Spellmeyer, D. C., Fox, T., Caldwell, J. W. and Kollman, P. A. (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J. Am. Chem. Soc. 117, 5179-5197
20. Robinson, D. A., Stewart, K. A., Price, N. C., Chalk, P. A., Coggins, J. R. and Lapthorn, A. J. (2006) Crystal structures of Helicobacter pylori type II dehydroquinase inhibitor complexes: new directions for inhibitor design. J. Med. Chem. 49, 1282-1290 (Pubitemid 43271883)
21. Dias, M. V. B., Snee, W. C., Bromfield, K. M., Payne, R. J., Palaninathan, S. K., Ciulli, A., Howard, N. I., Abell, C., Sacchettini, J. C. and Blundell, T. L. (2011) Structural investigation of inhibitor designs targeting 3-dehydroquinate dehydratase from the shikimate pathway of Mycobacterium tuberculosis. Biochem. J. 436, 729-739
22. Lence, E., Tizón, L., Otero, J. M., Peón, A., Prazeres, V. F. V., Llamas-Saiz, A. L., Fox, G. C., van Raaij, M. J., Lamb, H., Hawkins, A. R. and González-Bello, C. (2013) Mechanistic basis of the inhibition of type II dehydroquinase by (2S)- and (2R)-2-benzyl-3-dehydroquinic acids. ACS Chem. Biol. 8, 568-577
23. as and adding missing hydrogens to macromolecules. Nucleic Acids Res. 33, W368-W371
24. as of ionizable groups in proteins: atomic detail from a continuum electrostatic mode. Biochemistry 29, 10219-10225
25. Wang, J., Wolf, R. M., Caldwell, J. W., Kollman, P. A. and Case, D. A. (2004) Development and testing of a general Amber force field. J. Comput. Chem. 25, 1157-1174
26. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. and Klein, M. L. (1983) Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935
27. Aqvist, J. (1990) Ion-water interaction potentials derived from free energy perturbation simulations. J. Phys. Chem. 94, 8021-802
28. Darden, T., York, D. and Pedersen, L. (1993) Particle mesh Ewald: an N·log(N) method for Ewald sums in large systems. J. Chem. Phys. 98, 10089-10092
29. Ryckaert, J.-P., Ciccotti, G. and Berendsen, H. J. C. (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J. Comput. Phys. 23, 327-341
30. Seabra, G. M., Walker, R. C., Elstner, M., Case, D. A. and Roitberg, A. E. (2007) Implementation of the SCC-DFTB method for hybrid QM/MM simulations within the Amber molecular dynamics package. J. Phys. Chem. A 111, 5655-5664 (Pubitemid 47178745)
31. Cui, Q., Elstner, M., Kaxiras, E., Frauenheim, T. and Karplus, M. A. (2000) A QM/MM implementation of the self-consistent charge density functional tight binding (SCC-DFTB) method. J. Phys. Chem. B 105, 569-585
32. Crespo, A., Marti, M. A., Estrin, D. A. and Roitberg, A. E. (2005) Multiple-steering QM-MM calculation of the free energy profile in chorismate mutase. J. Am. Chem. Soc. 127, 6940-6941 (Pubitemid 40676708)
33. Gourley, D. G., Coggins, J. R., Isaacs, N. W., Moore, J. D., Charles, I. G. and Hawkins, A. R. (1994) Crystallization of a type II dehydroquinase from Mycobacterium tuberculosis. J. Mol. Biol. 241, 488-491 (Pubitemid 24266061)
34. Prazeres, V. F. V., Sánchez-Sixto, C., Castedo, L., Shuh, S. W., Lamb, H., Hawkins, A. R., Cañada, F. J., Jiménez-Barbero, J. and González-Bello, C. (2008) Competitive inhibitors of Helicobacter pylori type II dehydroquinase: synthesis, biological evaluation, and NMR studies. ChemMedChem 3, 756-770
35. Schown, K. B. and Schowen, R. L. (1982) Solvent isotope effects of enzyme systems. Methods Enzymol. 87, 551-606
36. Evans, L. D. B., Roszak, A. W., Noble, L. J., Robinson, D. A., Chalk, P. A., Matthews, J. L., Coggins, J. R., Price, N. C. and Lapthorn, A. J. (2002) Specificity of substrate recognition by type II dehydroquinases as revealed by binding of polyanions. FEBS Lett. 530, 24-30 (Pubitemid 35248180)
37. a values of catalytic groups in enzyme active sites. IUBMB Life 53, 85-98
38. a in the active site of ketosteroid isomerase. Biochemistry 52, 7840-7855
39. 5-steroid isomerase. Science 276, 415-418
40. Schwans, J. P., Sunden, F., Lassila, J. K., Gonzalez, A., Tsai, Y. and Herschlag, D. (2013) Use of anion-aromatic interactions to position the general base in the ketosteroid isomerase active site. Proc. Natl. Acad. Sci. U.S.A. 110, 11308-11313
41. 5-ketosteroid isomerase pseudomonas testosterone. Biochemistry 37, 8325-8330