Mycobacterium tuberculosis dihydrofolate reductase is a target for isoniazid

Nature Structural and Molecular Biology

Volumn 13, Issue 5, 2006, Pages 408-413

  Argyrou, Argyrides ^a   Vetting, Matthew W ^a   Aladegbami, Bola ^a,b   Blanchard, John S ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIHYDROFOLATE REDUCTASE; ISONIAZID; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; CONTROLLED STUDY; DRUG TARGETING; GROWTH INHIBITION; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; NUCLEIC ACID SYNTHESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

CELL PROLIFERATION; CLONING, MOLECULAR; CRYSTALLOGRAPHY, X-RAY; FOLIC ACID ANTAGONISTS; GENE EXPRESSION; ISONIAZID; MODELS, MOLECULAR; MYCOBACTERIUM TUBERCULOSIS; NADP; PRODRUGS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; TETRAHYDROFOLATE DEHYDROGENASE;

MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS;

EID: 33745094315     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb1089     Document Type: Article

References (41)

1. Bloom, B.R. & Murray, C.J. Tuberculosis: commentary on a reemergent killer. Science 257, 1055-1064 (1992).
2. Bernstein, J., Lott, W.A., Steinberg, B.A. & Yale, H.L. Chemotherapy of experimental tuberculosis. V. Isonicotinic acid hydrazide (nydrazid) and related compounds. Am. Rev. Tuberc. 65, 357-364 (1952).
3. Youatt, J. A review of the action of isoniazid. Am. Rev. Respir. Dis. 99, 729-749 (1969).
4. Middlebrook, G. Sterilization of tubercle bacilli by isonicotinic acid hydrazide and the incidence of variants resistant to the drug in vitro. Am. Rev. Tuberc. 65, 765-767 (1952).
5. Zhang, Y., Heym, B., Allen, B., Young, D. & Cole, S. The catalase-peroxidase gene and isoniazid resistance of Mycobacterium tuberculosis. Nature 358, 591-593 (1992).
6. Zhao, X. The catalytic mechanism of Mycobacterium tuberculosis catalase-peroxidase (katG) and isoniazid activation. PhD thesis. The Graduate Center, City University of New York, Brooklyn, New York, (2005).
7. Nguyen, M., Claparols, C., Bernadou, J. & Meunier, B. A fast and efficient metal-mediated oxidation of isoniazid and identification of isoniazid-NAD(H) adducts. ChemBioChem 2, 877-883 (2001).
8. Rozwarski, D.A., Grant, G.A., Barton, D.H., Jacobs, W.R., Jr. & Sacchettini, J.C. Modification of the NADH of the isoniazid target (InhA) from Mycobacterium tuberculosis. Science 279, 98-102 (1998).
9. White, S.W., Zheng, J., Zhang, Y.M. & Rock, C.O. The structural biology of type II fatty acid biosynthesis. Annu. Rev. Biochem. 74, 791-831 (2004).
10. Barry, C.E., III. et al. Mycolic acids: structure, biosynthesis and physiological functions. Prog. Lipid Res. 37, 143-179 (1998).
11. Takayama, K., Wang, C. & Besra, G.S. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin. Microbiol. Rev. 18, 81-101 (2005).
12. Lei, B., Wei, C.J. & Tu, S.C. Action mechanism of antitubercular isoniazid. Activation by Mycobacterium tuberculosis KatG, isolation, and characterization of InhA inhibitor. J. Biol. Chem. 275, 2520-2526 (2000).
13. Rawat, R., Whitty, A. & Tonge, P.J. 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. USA 100, 13881-13886 (2003).
14. Zhang, Y., Vilcheze, C. & Jacobs, W.R., Jr. Mechanisms of drug resistance in Mycobacterium tuberculosis, in Tuberculosis and the Tubercle Bacillus (eds. Cole, S.T., Eisenach, K.D., McMurray, D.N. & Jacobs, W.R., Jr.) 115-140 (ASM Press, Washington, DC, 2005).
15. Basso, L.A., Zheng, R., Musser, J.M., Jacobs, W.R., Jr. & Blanchard, J.S. Mechanisms of isoniazid resistance in Mycobacterium tuberculosis: enzymatic characterization of enoyl reductase mutants identified in isoniazid-resistant clinical isolates. J. Infect. Dis. 178, 769-775 (1998).
16. Ducasse-Cabanot, S. et al. In vitro inhibition of the Mycobacterium tuberculosis beta-ketoacyl-acyl carrier protein reductase MabA by isoniazid. Antimicrob. Agents Chemother. 48, 242-249 (2004).
17. Gangadharam, P.R., Harold, F.M. & Schaefer, W.B. Selective inhibition of nucleic acid synthesis in Mycobacterium tuberculosis by isoniazid. Nature 198, 712-714 (1963).
18. Miller, G.P. & Benkovic, S.J. Stretching exercises - flexibility in dihydrofolate reductase catalysis. Chem. Biol. 5, R105-R113 (1998).
19. Schnell, J.R., Dyson, H.J. & Wright, P.E. Structure, dynamics, and catalytic function of dihydrofolate reductase. Annu. Rev. Biophys. Biomol. Struct. 33, 119-140 (2004).
20. Suling, W.J. et al. Susceptibilities of Mycobacterium tuberculosis and Mycobacterium avium complex to lipophilic deazapteridine derivatives, inhibitors of dihydrofolate reductase. J. Antimicrob. Chemother. 42, 811-815 (1998).
21. Li, R. et al. Three-dimensional structure of Mycobacterium tuberculosis dihydrofolate reductase reveals opportunities for the design of novel tuberculosis drugs. J. Mol. Biol. 295, 307-323 (2000).
22. Daugelat, S. et al. The RD1 proteins of Mycobacterium tuberculosis: expression in Mycobacterium smegmatis and biochemical characterization. Microbes Infect. 5, 1082-1095 (2003).
23. Banerjee, A. et al. InhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 263, 227-230 (1994).
24. Alland, D. et al. Identification of differentially expressed mRNA in prokaryotic organisms by customized amplification libraries (DECAL): the effect of isoniazid on gene expression in Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 95, 13227-13232 (1998).
25. Wilson, M. et al. Exploring drug-induced alterations in gene expression in Mycobacterium tuberculosis by microarray hybridization. Proc. Natl. Acad. Sci. USA 96, 12833-12838 (1999).
26. Betts, J.C. et al. Signature gene expression profiles discriminate between isoniazid-, thiolactomycin-, and triclosan-treated Mycobacterium tuberculosis. Antimicrob. Agents Chemother. 47, 2903-2913 (2003).
27. Boshoff, H.I. et al. The transcriptional responses of Mycobacterium tuberculosis to inhibitors of metabolism: novel insights into drug mechanisms of action. J. Biol. Chem. 279, 40174-40184 (2004).
28. Waddell, S.J. et al. The use of microarray analysis to determine the gene expression profiles of Mycobacterium tuberculosis in response to anti-bacterial compounds. Tuberculosis (Edinb.) 84, 263-274 (2004).
29. Hughes, M.A., Silva, J.C., Geromanos, S.J. & Townsend, C.A. Quantitative proteomic analysis of drug-induced changes in mycobacteria. J. Proteome Res. 5, 54-63 (2006).
30. Wilming, M. & Johnsson, K. Spontaneous formation of the bioactive form of the tuberculosis drug isoniazid. Angew. Chem. Int. Edn Engl. 38, 2588-2590 (1999).
31. Quemard, A. et al. Enzymatic characterization of the target for isoniazid in Mycobacterium tuberculosis. Biochemistry 34, 8235-8241 (1995).
32. Sawaya, M.R. & Kraut, J. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry 36, 586-603 (1997).
33. Cody, V., Luft, J.R., Pangborn, W. & Gangjee, A. Analysis of three crystal structure determinations of a 5-methyl-6-N-methylanilino pyridopyrimidine antifolate complex with human dihydrofolate reductase. Acta Crystallogr. D59, 1603-1609 (2003).
34. Kongsaeree, P. et al. Crystal structure of dihydrofolate reductase from Plasmodium vivax: pyrimethamine displacement linked with mutation-induced resistance. Proc. Natl. Acad. Sci. USA 102, 13046-13051 (2005).
35. Vilcheze, C. et al. Inactivation of the InhA-encoded fatty acid synthase II (FAS II) enoyl-acyl carrier protein reductase induces accumulation of the FAS I end products and cell lysis of Mycobacterium smegmatis. J. Bacteriol. 182, 4059-4067 (2000).
36. Stone, S.R. & Morrison, J.F. Kinetic mechanism of the reaction catalyzed by dihydrofolate reductase from Escherichia coli. Biochemistry 21, 3757-3765 (1982).
37. CCP4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D50, 760-763 (1994).
38. Murshudov, G.N., Vagin, A.A. & Dodson, E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D53, 240-255 (1997).
39. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D60, 2126-2132 (2004).
40. Brunger, A.T. Assessment of phase accuracy by cross validation: the free R value. Methods and applications. Acta Crystallogr. D49, 24-36 (1993).
41. Schuttelkopf, A.W. & van Aalten, D.M. PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. D60, 1355-1363 (2004).