Crystal structure of a type II dihydrofolate reductase catalytic ternary complex

Biochemistry

Volumn 46, Issue 51, 2007, Pages 14878-14888

  Krahn, Joseph M ^a   Jackson, Michael R ^b   DeRose, Eugene F ^a   Howell, Elizabeth E ^b   London, Robert E ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF TENNESSEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BINDING SITES; CATALYSIS; CRYSTAL STRUCTURE; DRUG THERAPY; HYDROGEN BONDS;

ANTIFOLATE DRUGS; HOMOTETRAMER; PLASMID-ENCODED ENZYME; SUBSTRATE SPECIFICITY;

ENZYME ACTIVITY;

AMIDE; CARBOXYL GROUP; DIHYDROFOLATE REDUCTASE; DIHYDROFOLIC ACID; FOLIC ACID ANTAGONIST; NICOTINAMIDE; PTERIDINE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE;

ARTICLE; BINDING SITE; CATALYSIS; DRUG SENSITIVITY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME STRUCTURE; EVOLUTION; HYDROGEN BOND; MOLECULAR RECOGNITION; MUTATION; PLASMID; PRIORITY JOURNAL; REACTION ANALYSIS;

CATALYSIS; CRYSTALLOGRAPHY, X-RAY; FOLIC ACID; LIGANDS; MODELS, MOLECULAR; NADP; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY; TETRAHYDROFOLATE DEHYDROGENASE; TRIMETHOPRIM;

BACTERIA (MICROORGANISMS);

EID: 37349009656     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701532r     Document Type: Article

References (67)

1. Fleming, M. P., Datta, N., and Gruneberg, R. N. (1972) Trimethoprim resistance determined by R factors, Br. Med. J. 1, 726-728.
2. Pattishall, K. H., Acar, J., Burchall, J. J., Goldstein, F. W., and Harvey, R. J. (1977) Two distinct types of trimethoprim-resistant dihydrofolate reductase specified by R-plasmids of different compatibility groups, J. Biol. Chem. 252, 2319-2323.
3. Stone, D., and Smith, S. L. (1979) The amino acid sequence of the trimethoprim-resistant dihydrofolate reductase specified in Escherichia coli by R-plasmid R67, J. Biol. Chem. 254, 10857-10861.
4. Smith, S. L., Stone, D., Novak, P., Baccanari, D. P., and Burchall, J. J. (1979) R plasmid dihydrofolate reductase with subunit structure, J. Biol. Chem. 254, 6222-6225.
5. Narayana, N., Matthews, D. A., Howell, E. E., and Nguyen-huu, X. (1995) A plasmid-encoded dihydrofolate reductase from trimethoprim-resistant bacteria has a novel D2-symmetric active site, Nat. Struct. Biol. 2, 1018-1025.
6. + bound to a type II dihydrofolate reductase, Biochemistry 30, 1461-1469.
7. Li, D., Levy, L. A., Gabel, S. A., Lebetkin, M. S., DeRose, E. F., Wall, M. J., Howell, E. E., and London, R. E. (2001) Interligand Overhauser effects in type II dihydrofolate reductase, Biochemistry 40, 4242-4252.
8. Pitcher, W. H., 3rd, DeRose, E. F., Mueller, G. A., Howell, E. E., and London, R. E. (2003) NMR studies of the interaction of a type II dihydrofolate reductase with pyridine nucleotides reveal unexpected phosphatase and reductase activity, Biochemistry 42, 11150-11160.
9. 2 symmetric protein, Biochemistry 35, 11414-11424.
10. Alonso, H., Gillies, M. B., Cummins, P. L., Bliznyuk, A. A., and Gready, J. E. (2005) Multiple ligand-binding modes in bacterial R67 dihydrofolate reductase, J. Comput.-Aided Mol. Des. 19, 165-187.
11. Xu, Q., Guo, H., Wlodawer, A., and Guo, H. (2006) The importance of dynamics in substrate-assisted catalysis and specificity, J. Am. Chem. Soc. 128, 5994-5995.
12. a of N5 of dihydrofolate bound to dihydrofolate reductase: mechanistic implications, Biochemistry 33, 7021-7026.
13. Deng, H., and Callender, R. (1998) Structure of dihydrofolate when bound to DHFR, J. Am. Chem. Soc. 120, 7730-7737.
14. Rod, T. H., and Brooks, C. L., 3rd. (2003) How dihydrofolate reductase facilitates protonation of dihydrofolate, J. Am. Chem. Soc. 125, 8718-8719.
15. Deng, H., Callender, R., and Howell, E. (2001) Vibrational structure of dihydrofolate bound to R67 dihydrofolate reductase, J. Biol. Chem. 276, 48956-48960.
16. Cannon, W., Garrison, B., and Benkovic, S. (1997) Electrostatic Characterization of Enzyme Complexes: Evaluation of the Mechanism of Catalysis of Dihydrofolate Reductase, J. Am. Chem. Soc. 119, 2386-2395.
17. Reece, L. J., Nichols, R., Ogden, R. C., and Howell, E. E. (1991) Construction of a synthetic gene for an R-plasmid-encoded dihydrofolate reductase and studies on the role of the N-terminus in the protein, Biochemistry 30, 10895-10904.
18. Brunger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., and Pannu, N. S. e. a. (1998) Crystallography and NMR system: a new software suite for macromolecular structure determination, Acta Crystallogr. Sect., D: Biol. Crystallogr. 54, 905-921.
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 2nd generation force-field for the simulation of proteins, nucleic-acids, and organic-molecules, J. Am. Chem. Soc. 117, 5179-5197.
20. Bruno, I. J., Cole, J. C., Kessler, M., Luo, J., Motherwell, W. D. S., Purkis, L. H., Smith, B. R., Taylor, R., Cooper, R. I., Harris, S. E., and Orpen, A. G. (2004) Retrieval of Crystallographically-Derived Molecular Geometry Information, J. Chem. Inf. Comput. Sci. 44, 2133-2144.
21. Vagin, A. A., Steiner, R. A., Lebedev, A. A., Potterton, L., McNicholas, S., Long, F., and Murshudov, G. N. (2004) REF-MAC5 dictionary: organization of prior chemical knowledge and guidelines for its use, Acta Crystallogr., Sect. D: Biol. Crystallogr. 60, 2184-2195.
22. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) Procheck: a program to check the stereochemical quality of protein structures, J. Appl. Crystallogr. 26, 283-291a
23. Lovell, S. C., Davis, I. W., Arendall, W. B., 3rd, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Calpha geometry: phi,psi and Cbeta deviation, Proteins 50, 437-450.
24. West, F. W., Seo, H. S., Bradrick, T. D., and Howell, E. E. (2000) Effects of single-tryptophan mutations on R67 dihydrofolate reductase, Biochemistry 39, 3678-3689.
25. Nichols, R., Weaver, C. D., Eisenstein, E., Blakley, R. L., Appleman, J., Huang, T. H., Huang, F. Y., and Howell, E. E. (1993) Titration of histidine 62 in R67 dihydrofolate reductase is linked to a tetramer to two-dimers equilibrium, Biochemistry 32, 1695-1706.
26. Narayana, N. (2006) High-resolution structure of a plasmid-encoded dihydrofolate reductase: pentagonal network of water molecules in the D2-symmetric active site, Acta Crystallogr., Sect. D: Biol. Crystallogr. 62, 695-706.
27. Sawaya, M. R., and Kraut, J. (1997) Loop and subdomain movements in the mechanism of Escherichia coli dihydrofolate reductase: crystallographic evidence, Biochemistry 36, 586-603.
28. Bystroff, C., Oatley, S. J., and Kraut, J. (1990) Crystal structures of Escherichia coli dihydrofolate reductase: the NADP+ holoenzyme and the folate.NADP+ ternary complex. Substrate binding and a model for the transition state, Biochemistry 29, 3263-3277.
29. Filman, D. J., Bolin, J. T., Matthews, D. A., and Kraut, J. (1982) Crystal structures of Escherichia coli and Lactobacillus casei dihydrofolate reductase refined at 1.7 A resolution. II. Environment of bound NADPH and implications for catalysis, J. Biol. Chem. 257, 13663-13672.
30. Jackson, M., Chopra, S., Smiley, R. D., Maynord, P. O., Rosowsky, A., London, R. E., Levy, L., Kalman, T. I., and Howell, E. E. (2005) Calorimetric studies of ligand binding in R67 dihydrofolate reductase, Biochemistry 44, 12420-12433.
31. Andres, J., Moliner, V., Safont, B. S., Domingo, L. R., Picher, M. T., and Krechl, J. (1996) On Transition Structures for Hydride Transfer Step: A Theoretical Study of the Reaction Catalyzed by Dihydrofolate Reductase Enzyme, Bioorg. Chem. 24, 10-18.
32. Smith, S. L., and Burchall, J. J. (1983) Alpha-pyridine nucleotides as substrates for a plasmid-specified dihydrofolate reductase, Proc. Natl. Acad. Sci. U.S.A. 80, 4619-4623.
33. Hicks, S. N., Smiley, R. D., Hamilton, J. B., and Howell, E. E. (2003) Role of ionic interactions in ligand binding and catalysis of R67 dihydrofolate reductase, Biochemistry 42, 10569-10578.
34. Divya, N., Grifith, E., and Narayana, N. (2007) Structure of the Q67H mutant of R67 dihydrofolate reductase-NADP+ complex reveals a novel cofactor binding mode, Protein Sci. 16, 1063-1068.
35. Chopra, S., Lynch, R., Kim, S. H., Jackson, M., and Howell, E. E. (2006) Effects of temperature and viscosity on R67 dihydrofolate reductase catalysis, Biochemistry 45, 6596-6605.
36. Wilkinson, T. A., Botuyan, M. V., Kaplan, B. E., Rossi, J. J., and Chen, Y. (2000) Arginine side-chain dynamics in the HIV-1 rev-RRE complex, J. Mol. Biol. 303, 515-529.
37. Schneider, H. J., Blatter, T., and Simova, S. (1991) Host guest chemistry. 26. NMR and fluorescence studies of cyclodextrin complexes with guest molecules containing both phenyl and naphthyl units, J. Am. Chem. Soc. 113, 1996-2000.
38. Garel, L., Lozach, B., Dutasta, J. P., and Collet, A. (1993) Remarkable effect of the receptor size in the binding of acetylcholine and related ammonium ions to water-soluble cryptophanes, J. Am. Chem. Soc. 115, 11652-11653.
39. Brito, R. M., Reddick, R., Bennett, G. N., Rudolph, F. B., and Rosevear, P. R. (1990) Characterization and stereochemistry of cofactor oxidation by a type II dihydrofolate reductase, Biochemistry 29, 9825-9831.
40. Gourley, D. G., Schuttelkopf, A. W., Leonard, G. A., Luba, J., Hardy, L. W., Beverley, S. M., and Hunter, W. N. (2001) Pteridine reductase mechanism correlates pterin metabolism with drug resistance in trypanosomatid parasites, Nat. Struct. Biol. 8, 521-525.
41. Castillo, R., Andres, J., and Moliner, V. (1999) Catalytic Mechanism of Dihydrofolate Reductase Enzyme. A Combined Quantum-Mechanical/Molecular- Mechanical Characterizaton of Transition State Structure for the Hydride Transfer Step, J. Am. Chem. Soc. 121, 12140-12147.
42. Wu, Y. D., and Houk, K. N. (1987) Transition structures for hydride transfers, J. Am. Chem. Soc. 109, 906-908.
43. Wu, Y. D., and Houk, K. N. (1987) Theoretical transition structures for hydride transfer to methyleniminium ion from methylamine and dihydropyridine. On the nonlinearity of hydride transfers, J. Am. Chem. Soc. 109, 226-227.
44. Davies, J. F., 2nd, Delcamp, T. J., Prendergast, N. J., Ashford, V. A., Freisheim, J. H., and Kraut, J. (1990) Crystal structures of recombinant human dihydrofolate reductase complexed with folate and 5-deazafolate, Biochemistry 29, 9467-9479.
45. Morrison, J., and Stone, S. (1988) Mechanism of the reaction catalyzed by DHFR from E. coli: pH and deuterium isotope effects with NADPH as the variable substrate, Biochemistry 27, 5499-5506.
46. Pu, J., Ma, S., Garcia-Viloca, M., Gao, J., Truhlar, D. G., and Kohen, A. (2005) Nonperfect synchronization of reaction center rehybridization in the transition state of the hydride transfer catalyzed by dihydrofolate reductase, J. Am. Chem. Soc. 127, 14879-14886.
47. Garcia-Viloca, M., Truhlar, D. G., and Gao, J. (2003) Reaction-path energetics and kinetics of the hydride transfer reaction catalyzed by dihydrofolate reductase, Biochemistry 42, 13558-13575.
48. Casarotto, M. G., Basran, J., Badii, R., Sze, K. H., and Roberts, G. C. (1999) Direct measurement of the pKa of aspartic acid 26 in Lactobacillus casei dihydrofolate reductase: implications for the catalytic mechanism, Biochemistry 38, 8038-8044.
49. Cummins, P. L., and Gready, J. E. (2001) Energetically most likely substrate and active-site protonation sites and pathways in the catalytic mechanism of dihydrofolate reductase, J. Am. Chem. Soc. 123, 3418-3428.
50. Poe, M. (1977) Acidic dissociation constants of folic acid, dihydrofolic acid, and methotrexate, J. Biol. Chem. 252, 3724-3728.
51. Kallen, R. G., and Jencks, W. P. (1966) The dissociation constants of tetrahydrofolic acid, J. Biol. Chem. 241, 5845-5850.
52. Maharaj, G., Selinsky, B. S., Appleman, J. R., Perlman, M., London, R. E., and Blakley, R. L. (1990) Dissociation constants for dihydrofolic acid and dihydrobiopterin and implications for mechanistic models for dihydrofolate reductase, Biochemistry 29, 4554-4560.
53. Strader, M. B., Chopra, S., Jackson, M., Smiley, R. D., Stinnett, L., Wu, J., and Howell, E. E. (2004) Defining the binding site of homotetrameric R67 dihydrofolate reductase and correlating binding enthalpy with catalysis, Biochemistry 43, 7403-7412.
54. Strader, M. B., Smiley, R. D., Stinnett, L. G., VerBerkmoes, N. C., and Howell, E. E. (2001) Role of S65, Q67, 168, and Y69 residues in homotetrameric R67 dihydrofolate reductase, Biochemistry 40, 11344-11352.
55. Kosloff, M., and Selinger, Z. (2001) Substrate assisted catalysis - application to G proteins, Trends Biochem. Sci. 26, 161-166.
56. Dall'Acqua, W., and Carter, P. (2000) Substrate-assisted catalysis: molecular basis and biological significance, Protein Sci. 9, 1-9.
57. Fersht, A. (1999) Structure and Mechanism in Protein Science, W.H. Freeman and Company, New York.
58. Ranaghan, K. E., Ridder, L., Szefczyk, B., Sokalski, W. A., Hermann, J. C., and Mulholland, A. J. (2004) Transition state stabilization and substrate strain in enzyme catalysis: ab initio QM/MM modelling of the chorismate mutase reaction, Org. Biomol. Chem. 2, 968-980.
59. Bruice, T. C., and Benkovic, S. J. (2000) Chemical basis for enzyme catalysis, Biochemistry 39, 6267-6274.
60. Schramm, V. L. (2001) Transition state variation in enzymatic reactions, Curr. Opin. Chem. Biol. 5, 556-563.
61. Schmitzer, A. R., Lepine, F., and Pelletier, J. N. (2004) Combinatorial exploration of the catalytic site of a drug-resistant dihydrofolate reductase: creating alternative functional configurations, Protein Eng. Des. Sel. 17, 809-819.
62. Howell, E. E. (2005) Searching sequence space: two different approaches to dihydrofolate reductase catalysis, ChemBioChem 6, 590-600.
63. Amyes, S. G., and Smith, J. T. (1976) The purification and properties of the trimethoprim-resistant dihydrofolate reductase mediated by the R-factor, R388, Eur. J. Biochem. 61, 597-603.
64. Coco, L., Groff, J., Temple, C., Jr., Montgomery, J., London. R., and Blakley, R. (1981) Carbon-13 nuclear magnetic resonance study of protonation of methotrexate and aminopterin bound to dihydrofolate reductase, Biochemistry 20, 3972-3978.
65. Coco, L., Temple, C., Jr., Montgomery, J., London, R., and Blakley, R. (1981) Protonation of methotrexate bound to the catalytic site of dihydrofolate from Lactobacillus casei, Biochem. Biophys. Res. Commun. 100, 413-419.
66. Coco, L., Roth, B., Temple, C., Jr., Montgomery, J., London. R., and Blakley, R. (1983) Protonated state of methotrexate, trimethoprim, and pyrimethamine bound to dihydrofolate reductase, Arch. Biochem. Biophys. 226, 567-577.
67. Schuttelkopf, A. W., Hardy, L. W., Beverley, S. M., and Hunter, W. N. (2005) Structures of Leishmania major pteridine reductase complexes reveal the active site features important for ligand binding and to guide inhibitor design, J. Mol. Biol. 352, 105-116.