Three-dimensional structure of M. tuberculosis dihydrofolate reductase reveals opportunities for the design of novel tuberculosis drugs

Journal of Molecular Biology

Volumn 295, Issue 2, 2000, Pages 307-323

  Li, Rongbao ^a   Sirawaraporn, Rachada ^b   Chitnumsub, Penchit ^b,c   Sirawaraporn, Worachart ^b   Wooden, Jason ^a   Athappilly, Francis ^a   Turley, Stewart ^a   Hol, Wim G J ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

Author keywords

Dihydrofolate reductase; Drug design; Methotrexate; Mycobacterium tuberculosis; Trimethoprim

Indexed keywords

4,6 DIAMINO 1,2 DIHYDRO 2,2 DIMETHYL 1 [3 (2,4,5 TRICHLOROPHENOXY)PROPOXY] 1,3,5 TRIAZINE; AMINO ACID; DIHYDROFOLATE REDUCTASE; GLYCEROL; METHOTREXATE; METHYL GROUP; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TRIMETHOPRIM;

ARTICLE; CRYSTAL STRUCTURE; DRUG DESIGN; DRUG PROTEIN BINDING; ENZYME INHIBITOR COMPLEX; HYDROPHOBICITY; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN QUATERNARY STRUCTURE; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; TUBERCULOSIS CONTROL;

BACTERIA (MICROORGANISMS); MYCOBACTERIUM; MYCOBACTERIUM TUBERCULOSIS;

EID: 0034645774     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1999.3328     Document Type: Article

References (53)

1. Abrahams J. P., Leslie A. G. Methods used in the structure determination of bovine mitochondrial F1 ATPase. Acta Crystallog. Sect. D. 52:1996;30-42.
2. Bass J. B., Farer L. S., Hopewell P. C., O'Brien R., Jacobs R. F., Ruben F., Dixie E., Snider J., Thornton G. Treatment of tuberculosis and tuberculosis infection in adults and children. Am. J. Respir. Crit. Care Med. 149:1994;1359-1374.
3. Blakley R. L. Dihydrofolate reductase. Blakley R. L., Benkovic S. J. Folates and Pterines. 1984;191-253 Wiley, New York.
4. Blakley R. L. Eukaryotic dihydrofolate reductase. Advan. Enzymol. Relat. Areas Mol. Biol. 70:1995;23-102.
5. Bloom B. R., Murray C. J. L. Tuberculosis: commentary on a reemergent killer. Science. 257:1992;1055-1064.
6. Bolin J. T., Filman D. J., Matthews D. A., Hamlin R. C., Kraut J. Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 Å resolution. I. General features and binding of methotrexate. J. Biol. Chem. 257:1982;13650-13662.
7. Brünger A. T. Crystallographic refinement by simulated annealing. Application to a 2.8 Å resolution structure of aspartate aminotransferase. J. Mol. Biol. 203:1988;803-816.
8. Brünger A. T. Free R value: a novel statistical quality for assessing the accuracy of crystal structures. Nature. 355:1992;471-475.
9. Brünger A. T., Nilges M. Computational challenges for macromolecular structure determination by X-ray crystallography and solution NMR-spectroscopy. Quart. Rev. Biophys. 26:1993;49-125.
10. Canfield C. J., Milhous W. K., Ager A. L., Rossan R. N., Sweeney T. R., Lewis N. J., Jacobus D. P. PS-15: a potent, orally active antimalarial from a new class of folic acid antagonists. Am. J. Trop. Med. Hyg. 49:1993;121-126.
11. Cody V., Galitsky N., Luft J. R., Pangborn W., Rosowsky A., Blakley R. L. Comparison of two independent crystal structures of human dihydrofolate reductase ternary complexes reduced with nicotinamide adenine dinucleotide phosphate and the very tight-binding inhibitor PT523. Biochemistry. 36:1997;13897-13903.
12. Acta Crystallog. Sect. D. 50:1994;760-763.
13. Davies J. F. D., Delcamp T. J., Prendergast N. J., Ashford V. A., Freisheim J. H., Kraut J. Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate. Biochemistry. 29:1990;9467-9479.
14. de La Fortelle E., Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276:1997;472-494.
15. Dolin P. J., Raviglione M. D., Kochi A. Global tuberculosis incidence and mortality during 1990-2000. Bull. World Health Org. 72:1994;213-220.
16. Fidock D. A., Wellems T. E. Transformation with human dihydrofolate reductase renders malaria parasites insensitive to WR99210 but does not affect the intrinsic activity of proguanil. Proc. Natl Acad. Sci. USA. 94:1997;10931-10936.
17. Hekmat-Nejad M., Rathod P. K. Plasmodium falciparum: kinetic interactions of WR99210 with pyrimethamine-sensitive and pyrimethamine-resistant dihydrofolate reductase. Expt. Parasitol. 87:1997;222-228.
18. Hol W. G. J. The role of the α-helix dipole in protein structure and function. Prog. Biophys. Mol. Biol. 45:1985;149-195.
19. Hol W. G. J., van Duijnen P. T., Berendsen H. J. C. The α-helix dipole and the properties of proteins. Nature. 273:1978;443-446.
20. Howell E. E., Villafranca J. E., Warren M. S., Oatley S. J., Kraut J. Functional role of aspartic acid-27 in dihydrofolate reductase revealed by mutagenesis. Science. 231:1986;1123-1128.
21. Jiang J. S., Brünger A. T. Protein hydration observed by X-ray diffraction. Solvation properties of penicillopepsin and neuraminidase crystal structures. J. Mol. Biol. 243:1994;100-115.
22. Jones T. A., Zou J. Y., Cowan S. W., Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. Sect. A. 47:1991;110-119.
23. Kolattukudy P. E., Fernandes N. D., Azad A. K., Fitzmaurice A. M., Sirakova T. D. Biochemistry and molecular genetics of cell-wall lipid biosynthesis in mycobacteria. Mol. Microbiol. 24:1997;263-270.
24. Kraulis P. J. MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24:1991;946-950.
25. Kuyper L. F., Baccanari D. P., Jones M. L., Hunter R. N., Tansik R. L., Joyner S. S., Boytos C. M., Rudolph S. K., Knick V., Wilson H. R., Caddell J. M., Friedman H. S., Comley J. C., Stables J. N. High-affinity inhibitors of dihydrofolate reductase: antimicrobial and anticancer activities of 7,8-dialkyl-1,3-diaminopyrrolo[3,2-f]quinazolines with small molecular size. J. Med. Chem. 39:1996a;892-903.
26. Kuyper L. F., Garvey J. M., Baccanari D. P., Champness J. N., Stammers D. K., Beddell C. R. Pyrrolo[2,3-d]pyrimidines and pyrido[2,3-d]pyrimidines as conformationally restricted analogues of the antibacterial agent trimethoprim. Bioorg. Med. Chem. 4:1996b;593-602.
27. Laskowski R. A., MacArthur M. W., Moss D. S., Thornton J. M. PROCHECK: a program to check the sterochemical quality of protein structures. J. Appl. Crystallog. 26:1993;283-291.
28. Lee R. E., Brennan P. J., Besra G. S. Mycobacterium tuberculosis cell envelope. Curr. Top. Mycrobiol. Immunol. 215:1996;1-27.
29. Matthews D. A., Alden R. A., Bolin J. T., Freer S. T., Hamlin R., Xuong N., Kraut J., Poe M., Williams M., Hoogsteen K. Dihydrofolate reductase: X-ray structure of the binary complex with methotrexate. Science. 197:1977;452-455.
30. Merritt E. A., Bacon D. J. Raster3D: Photorealistic molecular graphics. Methods Enzymol. 277:1997;505-524.
31. Merritt E. A., Murphy M. E. P. Raster3D version 2.0. A program for photorealistic molecular graphics. Acta Crystallog. Sect. D. 50:1994;869-873.
32. Miller G. P., Benkovic S. J. Stretching exercises - flexibility in dihydrofolate reductase catalysis. Chem. Biol. 5:1998;R105-R113.
33. Morris A. L., MacArthur M. W., Hutchinson E. G., Thornton J. M. Sterochemical quality of protein structure coordinates. Proteins: Struct. Funct. Genet. 12:1992;345-364.
34. Nakajima H. Tuberculosis: a global emergency. World Health. 46:1993;3.
35. Navaza J. AMoRe: an automated package for molecular replacement. Acta Crystallog. Sect. A. 50:1994;157-163.
36. Nicholls A., Sharp K. A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of chydrocarbons. Proteins: Struct. Funct. Genet. 11:1991;281-296.
37. Nunn P., Kochi A. A deadly duo - TB and AIDS. World Health. 46:1993;7-8.
38. Otwinowski Z., Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276:1997;307-326.
39. Ramachandran G. N., Venkatchalam C. M., Krimm S. Stereochemical criteria for polypeptide and protein chain conformations, 3. Helical and hydrogen-bonded polypeptide chains. Biophys. J. 6:1966;849-872.
40. Read R. J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta. Crystallog. Sect. A. 42:1986;140-149.
41. Roth B., Stammers D. K. Drug interactions with target enzymes of known structure. Beddell C. R. The Design of Drugs to Macromolecular Targets. 1992;85-118 Wiley, Chichester.
42. Rouhi A. M. Tuberculosis: a tough adversary. Chem. Eng. News. 77:1999;52-69.
43. Sawaya M. R., Kraut J. Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence. Biochemistry. 36:1997;586-603.
44. Schweitzer B. I., Dicker A. P., Bertino J. R. Dihydrofolate reductase as a therapeutic target. FASEB J. 4:1990;2441-2452.
45. Snider D. E. J., Roper W. L. The new tuberculosis. New Engl. J. Med. 326:1992;703-705.
46. Snider D. E. J., Raviglione M., Kochi A. Tuberculosis: pathogenesis, protection, and control. Bloom B. R. Tuberculosis: Pathogenesis, Protection, and Control. 1994;2-11 American Society of Microbiology, Washington DC.
47. Suling W. J., Reynolds R. C., Barrow E. W., Wilson L. N., Piper J. R., Barrow W. W. Susceptibilities of Mycobacterium tuberculosis and Mycobacterium avium complex to lipophilic deazapteridine derivaties, inhibitors of dihydrofolate reductase. J. Antimicrob. Chemother. 42:1998;811-815.
48. Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22:1994;4673-4680.
49. van den Akker F., Hol W. G. Difference density quality (DDQ): a method to assess the global and local correctness of macromolecular crystal structures. Acta Crystallog. Sect. D. 55:1999;206-218.
50. Wallace A. C., Laskowski R. A., Thornton J. M. LIGPLOT: a program to generate schematic diagrams of protein-ligand interactions. Protein Eng. 8:1995;127-134.
51. Wiktor S. Z., Sassan-Morokro M., Grant A. D., Abouya L., Karon J. M., Marice C., Djomand G., Ackah A., Domoua K., Kadio A., Yapi A., Combe P., Tossou O., Roels T. H., Lackritz E. M. et al. Efficacy of trimethoprim-sulphamethoxazole prophylaxis to decrease morbidity and mortality in HIV-1-infected patients with tuberculosis in Abijian, Cote d'Ivoire: a randomised controlled trial. Lancet. 353:1999;1469-1475.
52. Yeo A. E., Seymour K. K., Rieckmann K. H., Christopherson R. I. Effects of folic and folinic acids in the activities of cycloguanil and WR99210 against Plasmodium falciparum in erythrocytic culture. Ann. Trop. Med. Parasitol. 91:1997;17-23.
53. Zuccotto F., Martin A. C., Laskowski R. A., Thornton J. M., Gilbert I. H. Dihydrofolate reductase: a potential drug target in trypanosomes and leishmania. J. Comput. Aided Mol. Des. 12:1998;241-257.