Concentration-dependent processivity of multiple glutamate ligations catalyzed by folylpoly-γ-glutamate synthetase

Biochemistry

Volumn 47, Issue 34, 2008, Pages 9040-9050

  Tomsho, John W ^a   Moran, Richard G ^b   Coward, James K ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b VIRGINIA COMMONWEALTH UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIFOLATES; FOLATES; GLUTAMATE SYNTHETASE; PROCESSIVITY; TETRAHYDROFOLATE;

CONCENTRATION (PROCESS);

FOLIC ACID; FOLYLPOLYGLUTAMATE SYNTHASE; GLUTAMIC ACID;

ARTICLE; CATALYSIS; CHEMICAL INTERACTION; ENZYME KINETICS; ENZYME RELEASE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; PRIORITY JOURNAL; PROTEIN PROCESSING; REACTION TIME;

ANIMALS; BACULOVIRIDAE; CATALYSIS; CELL LINE; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; GLUTAMATES; HUMANS; KINETICS; MOLECULAR STRUCTURE; PEPTIDE SYNTHASES; PTEROYLPOLYGLUTAMIC ACIDS; SPODOPTERA; TETRAHYDROFOLATES; TRANSFECTION;

EID: 50149117379     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi800406w     Document Type: Article

References (45)

1. McGuire, J. J., and Bertino, J. R. (1981) Enzymatic synthesis and function of folylpolyglutamates. Mol. Cell. Biochem. 38, 19-48.
2. McGuire, J. J., and Coward, J. K. (1984) Pteroylpolyglutamates: Biosynthesis, degradation, and function. In Folates and pterins (Blakley, R. L., and Benkovic, S. J., Eds.) pp 135-190, John Wiley & Sons, New York.
3. Shane, B. (1989) Folylpolyglutamate synthesis and role in the regulation of one-carbon metabolism. Vitam. Horm. (San Diego, CA, U.S.) 45, 263-335.
4. Faessel, H. M., Slocum, H. K., Jackson, R. C., Boritzki, T. J., Rustum, Y. M., Nair, M. G., and Greco, W. R. (1998) Super in vitro synergy between inhibitors of dihydrofolate reductase and inhibitors of other folate-requiring enzymes: The critical role of polyglutamylation. Cancer Res. 58, 3036-3050.
5. Mendelsohn, L. G., Worzalla, J. F., and Walling, J. M. (1999) Preclinical and clinical evaluation of the glycinamide ribonucleotide formyltransferase inhibitors Lometrexol and LY309887. In Antifolate Drugs in Cancer Therapy (Jackman, A. L., Ed.) pp 261-280, Humana Press, Totowa, NJ.
6. Adams, J., and Elliott, P. J. (2000) New agents in cancer clinical trials. Oncogene 19, 6687-6692.
7. McGuire, J. J. (2003) Anticancer antifolates: Current status and future directions. Curr. Pharm. Des. 9, 2593-2613.
8. Purcell, W. T., and Ettinger, D. S. (2003) Novel antifolate drugs. Curr. Oncol. Rep. 5, 114-125.
9. Rollins, K. D., and Lindley, C. (2005) Pemetrexed: A multitargeted antifolate. Clin. Ther. 27, 1343-1382.
10. Beardsley, G. P., Moroson, B. A., Taylor, E. C., and Moran, R. G. (1989) A new folate antimetabolite, 5,10-dideaza-5,6,7,8-tetrahydrofolate is a potent inhibitor of de novo purine synthesis. J. Biol. Chem. 264, 328-333.
11. Sanghani, P. C., and Moran, R. G. (2000) Purification and characteristics of recombinant human folylpoly-γ-glutamate synthetase expressed at high levels in insect cells. Protein Expression Purif. 18, 36-45.
12. Pizzorno, G., Sokoloski, J. A., Cashmore, A. R., Moroson, B. A., Cross, A. D., and Beardsley, G. P. (1991) Intracellular metabolism of 5,10-dideazatetrahydrofolic acid in human leukemia cell lines. Mol. Pharmacol. 39, 85-89.
13. Habeck, L. L., Chay, S. H., Pohland, R. C., Worzalla, J. F., Shih, C., and Mendelsohn, L. G. (1998) Whole-body disposition and polyglutamate distribution of the GAR formyltransferase inhibitors LY309887 and lometrexol in mice: Effect of a low folate diet. Cancer Chemother. Pharmacol. 41, 201-209.
14. Sanghani, S. P., and Moran, R. G. (1997) Tight binding of folate substrates and inhibitors to recombinant mouse glycinamide ribonucleotide formyltransferase. Biochemistry 36, 10506-10516.
15. McGuire, J. J. (1999) Antifolate polyglutamylation in preclinical and clinical antifolate resistance. In Antifolate drugs in cancer therapy (Jackman, A. L., Ed.) pp 339-363, Humana Press, Totowa, NJ.
16. Zhao, R. B., Titus, S., Gao, F., Moran, R. G., and Goldman, I. D. (2000) Molecular analysis of murine leukemia cell lines resistant to 5,10-dideazatetrahydrofolate identifies several amino acids critical to the function of folylpolyglutamate synthetase. J. Biol. Chem. 275, 26599-26606.
17. Liani, E., Rothem, L., Bunni, M. A., Smith, C. A., Jansen, G., and Assaraf, Y. G. (2003) Loss of folylpoly-γ-glutamate synthetase activity is a dominant mechanism of resistance to polyglutamylation-dependent novel antifolates in multiple human leukemia sublines. Int. J. Cancer 103, 587-599.
18. Banerjee, R., McGuire, J. J., Shane, B., and Coward, J. K. (1988) Dihydrofolate synthetase and folylpolyglutamate synthetase: Direct evidence for intervention of acyl phosphate intermediates. Biochemistry 27, 9062-9070.
19. McBurney, M. W., and Whitmore, G. F. (1974) Isolation and biochemical characterization of folate deficient mutants of Chinese-hamster cells. Cell 2, 173-182.
20. McGuire, J. J., Hsieh, P., Coward, J. K., and Bertino, J. R. (1980) Enzymatic synthesis of folylpolyglutamates: Characterization of the reaction and its products. J. Biol. Chem. 255, 5776-5788.
21. McClure, W. R., and Chow, Y. (1980) The kinetics and processivity of nucleic acid polymerases. Methods Enzymol. 64, 277-297.
22. Capson, T. L., Peliska, J. A., Kaboord, B. F., Frey, M. W., Lively, C., Dahlberg, M., and Benkovic, S. J. (1992) Kinetic characterization of the polymerase and exonuclease activities of the gene 43 protein of bacteriophage T4. Biochemistry 31, 10984-10994.
23. Yuan, Y., Barrett, D., Zhang, Y., Kahne, D., Sliz, P., and Walker, S. (2007) Crystal structure of a peptidoglycan glycosyltransferase suggests a model for processive glycan chain synthesis. Proc. Natl. Acad. Sci. U.S.A. 104, 5348-5353.
24. Barrett, D., Wang, T. A., Yuan, Y., Zhang, Y., Kahne, D., and Walker, S. (2007) Analysis of glycan polymers produced by peptidoglycan glycosyltransferases. J. Biol. Chem. 287, 31964-31971.
25. Shane, B. (1980) Pteroylpoly(γ-glutamate) synthesis by Corynebacterium species: Studies on the mechanism of folylpoly(γ- glutamate) synthetase. J. Biol. Chem. 255, 5663-5667.
26. Bognar, A. L., and Shane, B. (1983) Purification and properties of Lactobacillus casei folylpoly-γ-glutamate synthetase. J. Biol. Chem. 258, 12574-12581.
27. Cichowicz, D. J., and Shane, B. (1987) Mammalian folylpoly-γ- glutamate synthetase. 2. Substrate specificity and kinetic properties. Biochemistry 26, 513-521.
28. Tomsho, J. W., McGuire, J. J., and Coward, J. K. (2005) Synthesis and biological evaluation of (6S)- and (6R)-5,10-dideaza-5,6,7,8- tetrahydropteroyl poly-γ-glutamates as substrates for human folylpoly-γ-glutamate synthetase. Org. Biomol. Chem. 3, 3388-3398.
29. Rose, I. A. (1980) The isotope trapping method: Desorption rates of productive E-S complexes. Methods Enzymol. 64, 47-59.
30. Rose, I. A. (1995) Partition analysis: Detecting enzyme reaction cycle intermediates. Methods Enzymol. 249, 315-340.
31. Moran, R. G., Baldwin, S. W., Taylor, E. C., and Shih, C. (1989) The 6S-diastereomer and 6R-diastereomer of 5,10-dideaza-5,6,7,8- tetrahydrofolate are equiactive inhibitors of de novo purine synthesis. J. Biol. Chem. 264, 21047-21051.
32. Chen, L., Qi, H., Korenberg, J., Garrow, T. A., Choi, Y. J., and Shane, B. (1996) Purification and properties of human cytosolic folylpoly-γ- glutamate synthetase and organization, localization, and differential splicing of its gene. J. Biol. Chem. 271, 13077-13087.
33. Gangjee, A., Yu, J., Kisliuk, R. L., Haile, W. H., Sobrero, G., and McGuire, J. J. (2003) Design, synthesis, and biological activities of classical N-[4-[2-(2-amino-4-ethylpyrrolo[2,3-d]pyrimidin-5-yl)ethyl]benzoyl] -L-glutamic acid and its 6-methyl derivative as
34. potential dual inhibitors of thymidylate synthetase and dihydrofolate reductase and as potential antitumor agents. J. Med. Chem. 46, 591-600.
35. Bradford, M. M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248-254.
36. Kuzmic, P. (1996) Analysis and simulation of chemical kinetic, biochemical kinetic, and pharmacokinetic data. Anal. Biochem. 237, 260-273.
37. Segel, I. H. (1975) Enzyme Kinetics, John Wiley & Sons, New York.
38. Moran, R. G., Colman, P. D., Forsch, R. A., and Rosowsky, A. (1984) A mechanism for the addition of multiple moles of glutamate by folylpolyglutamate synthetase. J. Med. Chem. 27, 1263-1267.
39. Tomsho, J. W. (2005) Folylpoly-γ-glutamate Synthetase: Kinetics of Multiple Glutamate Ligations. Ph.D. Thesis, University of Michigan, Ann Arbor, MI.
40. Chen, X.-Y., Berti, P. J., and Schramm, V. J. (2000) Ricin A-chain: Kinetic isotope effects and transition state structure with stem-loop RNA. J. Am. Chem. Soc. 122, 1609-1617.
41. Tan, X.-J., and Carlson, H. A. (2005) Docking studies and ligand recognition in folylpolyglutamate synthetase. J. Med. Chem. 48, 7764-7772.
42. Sun, X., Cross, J. A., Bognar, A. L., Baker, E. N., and Smith, C. A. (2001) Folate binding triggers the activation of folylpoly-glutamate synthetase. J. Mol. Biol. 310, 1067-1078.
43. Mathieu, M., Debousker, G., Vincent, S., Viviani, F., Bamas-Jacques, N., and Mikol, V. (2005) Escherichia coli FolC structure reveals an unexpected dihydrofolate binding site providing an attractive target for anti-microbial therapy. J. Biol. Chem. 280, 18916-18922.
44. Sheng, Y., Nurussaba, K., Tsaksis, Y., Shi, X., Lu, Q., and Bognar, A. L. (2008) Mutagenesis of folylpolyglutamate synthetase indicates that dihydropteroate and tetrahydrofolate bind to the same site. Biochemistry 47, 2388-2396.
45. Pai, C. H., Chiang, B. Y., Ko, T. P., Chou, C. C., Chong, C. M., Yen, F. J., Chen, S., Coward, J. K., Wang, H. J., and Lin, C. H. (2006) Dual binding sites for translocation catalysis by Escherichia coli glutathionylspermidine synthetase. EMBO J. 25, 5970-5982.