Mechanism and inhibition of the FabV Enoyl-ACP reductase from Burkholderia mallei

Biochemistry

Volumn 49, Issue 6, 2010, Pages 1281-1289

  Lu, Hao ^a   Tonge, Peter J ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACID-BASE CHEMISTRY; ACTIVE SITE; ACTIVE SITE RESIDUES; ACYL CARRIER PROTEINS; BACTERIAL FATTY ACIDS; BI-BI MECHANISMS; BURKHOLDERIA; DETAILED KINETICS; FLUORESCENCE BINDING; NADH BINDING; PRODUCT COMPLEX; REACTION PATHWAYS; SEQUENCE ALIGNMENTS; SITE DIRECTED MUTAGENESIS; TRICLOSAN; VIBRIO CHOLERAE;

ACIDS; AMINO ACIDS; BIOCHEMISTRY; ENZYME ACTIVITY; ENZYMES; FATTY ACIDS; MUTAGENESIS; PHOSPHATASES; REACTION INTERMEDIATES;

ENZYME INHIBITION;

2 DODECENOYL COENZYME A; BACTERIAL ENZYME; COENZYME A; ENOYL ACYL CARRIER PROTEIN REDUCTASE (NADH); FABV ENOYL (ACYL CARRIER PROTEIN) REDUCTASE (NADH); LYSINE; NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; TRICLOSAN; TYROSINE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BURKHOLDERIA MALLEI; COMPETITIVE INHIBITION; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME KINETICS; FABV GENE; FRANCISELLA TULARENSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REACTION ANALYSIS; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS;

BACTERIAL PROTEINS; BURKHOLDERIA MALLEI; CATALYSIS; CATALYTIC DOMAIN; ENOYL-(ACYL-CARRIER-PROTEIN) REDUCTASE (NADH); GENE EXPRESSION REGULATION, BACTERIAL; HYDROGEN-ION CONCENTRATION; KINETICS; MUTAGENESIS, SITE-DIRECTED; NAD; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TRICLOSAN;

BACTERIA (MICROORGANISMS); BURKHOLDERIA MALLEI; VIBRIO CHOLERAE;

EID: 76749164969     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi902001a     Document Type: Article

References (49)

1. Campbell, J. W., and Cronan, J. E., Jr. (2001) Bacterial fatty acid biosynthesis: Targets for antibacterial drug discovery. Annu. Rev. Microbiol. 55, 305-332.
2. Heath, R. J., White, S. W., and Rock, C. O. (2001) Lipid biosynthesis as a target for antibacterial agents. Prog. Lipid Res. 40, 467-497.
3. Egan, A. F., and Russell, R. R. (1973) Conditional mutations affecting the cell envelope of Escherichia coli K-12. Genet. Res. 21, 139-152.
4. Turnowsky, F., Fuchs, K., Jeschek, C., and Hogenauer, G. (1989) envM genes of Salmonella typhimurium and Escherichia coli. J. Bacteriol. 171, 6555-6565.
5. 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.
6. Magnuson, K., Jackowski, S., Rock, C. O., and Cronan, J. E., Jr. (1993) Regulation of fatty acid biosynthesis in Escherichia coli. Microbiol. Rev. 57, 522-542.
7. Rock, C. O., and Cronan, J. E. (1996) Escherichia coli as a model for the regulation of dissociable (type II) fatty acid biosynthesis. Biochim. Biophys. Acta 1302, 1-16.
8. Heath, R. J., and Rock, C. O. (2004) Fatty acid biosynthesis as a target for novel antibacterials. Curr. Opin. Invest. Drugs 5, 146-153.
9. 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.
10. McMurry, L. M., Oethinger, M., and Levy, S. B. (1998) Triclosan targets lipid synthesis. Nature 394, 531-532.
11. Heath, R. J., Yu, Y. T., Shapiro, M. A., Olson, E., and Rock, C. O. (1998) Broad spectrum antimicrobial biocides target the FabI component of fatty acid synthesis. J. Biol. Chem. 273, 30316-30320.
12. Musser, J. M., Kapur, V., Williams, D. L., Kreiswirth, B. N., van Soolingen, D., and van Embden, J. D. (1996) Characterization of the catalase-peroxidase gene (katG) and inhA locus in isoniazid-resistant and -susceptible strains of Mycobacterium tuberculosis by automated DNA sequencing: Restricted array of mutations associated with drug resistance. J. Infect. Dis. 173, 196-202.
13. Tonge, P. J., Kisker, C., and Slayden, R. A. (2007) Development of modern InhA inhibitors to combat drug resistant strains of Mycobacterium tuberculosis. Curr. Top. Med. Chem. 7, 489-498.
14. Bergler, H., Wallner, P., Ebeling, A., Leitinger, B., Fuchsbichler, S., Aschauer, H., Kollenz, G., Hogenauer, G., and Turnowsky, F. (1994) Protein EnvM is the NADH-dependent enoyl-ACP reductase (FabI) of Escherichia coli. J. Biol. Chem. 269, 5493-5496.
15. Lu, H., and Tonge, P. J. (2008) Inhibitors of FabI, an enzyme drug target in the bacterial fatty acid biosynthesis pathway. Acc. Chem. Res. 41, 11-20.
16. Zhang, Y. M., White, S. W., and Rock, C. O. (2006) Inhibiting bacterial fatty acid synthesis. J. Biol. Chem. 281, 17541-17544.
17. Heath, R. J., and Rock, C. O. (2000) A triclosan-resistant bacterial enzyme. Nature 406, 145-146.
18. Heath, R. J., Su, N., Murphy, C. K., and Rock, C. O. (2000) The enoyl-[acyl-carrier-protein] reductases FabI and FabL from Bacillus subtilis. J. Biol. Chem. 275, 40128-40133.
19. Massengo-Tiasse, R. P., and Cronan, J. E. (2008) Vibrio cholerae FabV defines a new class of enoyl-acyl carrier protein reductase. J. Biol. Chem. 283, 1308-1316.
20. Srinivasan, A., Kraus, C. N., DeShazer, D., Becker, P. M., Dick, J. D., Spacek, L., Bartlett, J. G., Byrne, W. R., and Thomas, D. L. (2001) Glanders in a military research microbiologist. N. Engl. J. Med. 345, 256-258.
21. Parikh, S., Moynihan, D. P., Xiao, G., and Tonge, P. J. (1999) Roles of tyrosine 158 and lysine 165 in the catalytic mechanism of InhA, the enoyl-ACP reductase from Mycobacterium tuberculosis. Biochemistry 38, 13623-13634.
22. Marcinkeviciene, J., Jiang, W., Kopcho, L. M., Locke, G., Luo, Y., and Copeland, R. A. (2001) Enoyl-ACP reductase (FabI) of Haemophilus influenzae: Steady-state kinetic mechanism and inhibition by triclosan and hexachlorophene. Arch. Biochem. Biophys. 390, 101-108.
23. Kapoor, M., Dar, M. J., Surolia, A., and Surolia, N. (2001) Kinetic determinants of the interaction of enoyl-ACP reductase from Plasmodium falciparum with its substrates and inhibitors. Biochem. Biophys. Res. Commun. 289, 832-837.
24. Xu, H., Sullivan, T. J., Sekiguchi, J., Kirikae, T., Ojima, I., Stratton, C. F., Mao, W., Rock, F. L., Alley, M. R., Johnson, F., Walker, S. G., and Tonge, P. J. (2008) Mechanism and inhibition of saFabI, the enoyl reductase from Staphylococcus aureus. Biochemistry 47, 4228-4236.
25. Fawcett, T., Copse, C. L., Simon, J. W., and Slabas, A. R. (2000) Kinetic mechanism of NADH-enoyl-ACP reductase from Brassica napus. FEBS Lett. 484, 65-68.
26. Ward, W. H., Holdgate, G. A., Rowsell, S., McLean, E. G., Pauptit, R. A., Clayton, E., Nichols, W. W., Colls, J. G., Minshull, C. A., Jude, D. A., Mistry, A., Timms, D., Camble, R., Hales, N. J., Britton, C. J., and Taylor, I. W. (1999) Kinetic and structural characteristics of the inhibition of enoyl (acyl carrier protein) reductase by triclosan. Biochemistry 38, 12514-12525.
27. Roujeinikova, A., Levy, C. W., Rowsell, S., Sedelnikova, S., Baker, P. J., Minshull, C. A., Mistry, A., Colls, J. G., Camble, R., Stuitje, A. R., Slabas, A. R., Rafferty, J. B., Pauptit, R. A., Viner, R., and Rice, D. W. (1999) Crystallographic analysis of triclosan bound to enoyl reductase. J. Mol. Biol. 294, 527-535.
28. + at 2.1 Å resolution. J. Mol. Biol. 284, 1529-1546.
29. + and a C16 fatty acyl substrate. J. Biol. Chem. 274, 15582-15589.
30. Rafferty, J. B., Simon, J. W., Baldock, C., Artymiuk, P. J., Baker, P. J., Stuitje, A. R., Slabas, A. R., and Rice, D. W. (1995) Common themes in redox chemistry emerge from the X-ray structure of oilseed rape (Brassica napus) enoyl acyl carrier protein reductase. Structure 3, 927-938.
31. Jörnvall, H., Persson, B., Krook, M., Atrian, S., Gonzàlez-Duarte, R., Jeffery, J., and Ghosh, D. (1995) Short-chain dehydrogenases/ reductases (SDR). Biochemistry 34, 6003-6013.
32. Sivaraman, S., Zwahlen, J., Bell, A. F., Hedstrom, L., and Tonge, P. J. (2003) Structure-Activity Studies of the Inhibition of FabI, the Enoyl Reductase from Escherichia coli, by Triclosan: Kinetic Analysis of Mutant FabIs. Biochemistry 42, 4406-4413.
33. Rafi, S., Novichenok, P., Kolappan, S., Zhang, X., Stratton, C. F., Rawat, R., Kisker, C., Simmerling, C., and Tonge, P. J. (2006) Structure of acyl carrier protein bound to Fabi, the FASII enoyl reductase from Escherichia coli. J. Biol. Chem. 281, 39285-39293.
34. Fillgrove, K. L., and Anderson, V. E. (2001) The mechanism of dienoyl-CoA reduction by 2,4-dienoyl-CoA reductase is stepwise: Observation of a dienolate intermediate. Biochemistry 40, 12412-12421.
35. Filling, C., Berndt, K. D., Benach, J., Knapp, S., Prozorovski, T., Nordling, E., Ladenstein, R., Jornvall, H., and Oppermann, U. (2002) Critical residues for structure and catalysis in short-chain dehydrogenases/ reductases. J. Biol. Chem. 277, 25677-25684.
36. Perozzo, R., Kuo, M., Sidhu, A. S., Valiyaveettil, J. T., Bittman, R., Jacobs, W. R., Jr., Fidock, D. A., and Sacchettini, J. C. (2002) Structural elucidation of the specificity of the antibacterial agent triclosan for malarial enoyl acyl carrier protein reductase. J. Biol. Chem. 277, 13106-13114.
37. Stewart,M. J., Parikh, S., Xiao, G., Tonge, P. J., and Kisker, C. (1999) Structural basis and mechanism of enoyl reductase inhibition by triclosan. J. Mol. Biol. 290, 859-865.
38. Pidugu, L. S., Kapoor, M., Surolia, N., Surolia, A., and Suguna, K. (2004) Structural basis for the variation in triclosan affinity to enoyl reductases. J. Mol. Biol. 343, 147-155.
39. Sivaraman, S., Sullivan, T. J., Johnson, F., Novichenok, P., Cui, G., Simmerling, C., and Tonge, P. J. (2004) Inhibition of the bacterial enoyl reductase FabI by triclosan: A structure-reactivity analysis of FabI inhibition by triclosan analogues. J. Med. Chem. 47, 509-518.
40. Parikh, S. L., Xiao, G., and Tonge, P. J. (2000) Inhibition of InhA, the enoyl-reductase from Mycobacterium tuberculosis, by triclosan and isoniazid. Biochemistry 39, 7645-7650.
41. Lu, H., England, H., am Ende, C. W., Truglio, J. J., Luckner, S., Reddy, B. G., Marlenee, N., Knudson, S. E., Knudson,D. L., Bowen, R. A., Kisker, C., Slayden, R. A., and Tonge, P. J. (2009) Slow-Onset Inhibition of the FabI Enoyl Reductase from Francisella Tularensis: Residence Time and In Vivo Activity. ACS Chem. Biol. 4, 221-231.
42. Sullivan, T. J., Truglio, J. J., Boyne, M. E., Novichenok, P., Zhang, X., Stratton, C. F., Li, H. J., Kaur, T., Amin, A., Johnson, F., Slayden, R. A., Kisker, C., and Tonge, P. J. (2006) High affinity InhA inhibitors with activity against drug-resistant strains of Mycobacterium tuberculosis. ACS Chem. Biol. 1, 43-53.
43. Tonge, P. J. Unpublished work.
44. Rawat, R., Whitty, A., and Tonge, P. J. (2003) The isoniazid-NAD adduct is a slow, tight-binding inhibitor of InhA, the Mycobacterium tuberculosis enoyl reductase: Adduct affinity and drug resistance. Proc. Natl. Acad. Sci. U.S.A. 100, 13881-13886.
45. Zhu, L., Lin, J., Ma, J., Cronan, J. E., and Wang, H. (2009) The Triclosan Resistance of Pseudomonas aeruginosa PA01 is Due to FabV, a Triclosan-Resistant Enoyl-Acyl Carrier Protein Reductase. Antimicrob. Agents Chemother. (in press).
46. Nierman, W. C., DeShazer, D., Kim, H. S., Tettelin, H., Nelson, K. E., Feldblyum, T., Ulrich, R. L., Ronning, C. M., Brinkac, L. M., Daugherty, S. C., Davidsen, T. D., Deboy, R. T., Dimitrov, G., Dodson, R. J., Durkin, A. S., Gwinn,M. L., Haft, D. H., Khouri, H., Kolonay, J. F., Madupu, R., Mohammoud, Y., Nelson, W. C., Radune, D., Romero, C. M., Sarria, S., Selengut, J., Shamblin, C., Sullivan, S. A., White, O., Yu, Y., Zafar, N., Zhou, L., and Fraser, C. M. (2004) Structural flexibility in the Burkholderia mallei genome. Proc. Natl. Acad. Sci. U.S.A. 101, 14246-14251.
47. Cheng, A. C., and Currie, B. J. (2005) Melioidosis: Epidemiology, pathophysiology, and management. Clin. Microbiol. Rev. 18, 383-416.
48. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994) CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
49. Waterhouse, A. M., Procter, J. B., Martin, D. M., Clamp, M., and Barton, G. J. (2009) Jalview Version 2: Amultiple sequence alignment editor and analysis workbench. Bioinformatics 25, 1189-1191.