Crystal structure of deoxycytidylate hydroxymethylase from bacteriophage T4, a component of the deoxyribonucleoside triphosphate-synthesizing complex

EMBO Journal

Volumn 18, Issue 5, 1999, Pages 1104-1113

  Song, Hyun Kyu ^a   Sohn, Se Hui ^a   Suh, Se Won ^a  

^a Seoul National University   (South Korea)

Author keywords

Bacteriophage T4; Deoxycytidylate hydroxymethylase; Deoxyuridylate hydroxymethylase; dNTP synthesizing complex; Thymidylate synthase

Indexed keywords

BACTERIOPHAGE DNA; DEOXYCYTIDINE PHOSPHATE; DEOXYRIBONUCLEOSIDE TRIPHOSPHATE; METHYLTRANSFERASE; MULTIENZYME COMPLEX; PHOSPHATE; SUGAR; THYMIDYLATE SYNTHASE;

ARTICLE; BACTERIOPHAGE T4; BINDING SITE; CRYSTAL STRUCTURE; HYPOTHESIS; MODEL; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL;

T4 BACTERIOPHAGE; UNIDENTIFIED BACTERIOPHAGE;

EID: 0033105429     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.5.1104     Document Type: Article

References (59)

1. Agarwalla, S., LaPorte, S., Liu, L., Finer-Moore, J., Stroud, R.M. and Santi, D.V. (1997) A novel dCMP methylase by engineering thymidylate synthase. Biochemistry, 36, 15909-15917.
2. Allen, J.R., Lasser, G.W., Goldman, D.A., Booth, J.W. and Mathews, C.K. (1983) T4 phage deoxyribonucleotide-synthesizing enzyme complex. Further studies on enzyme composition and regulation. J. Biol. Chem., 258, 5746-5753.
3. Barton, G.J. (1993) ALSCRIPT: a tool to format multiple sequence alignments. Protein Eng., 6, 37-40.
4. Brünger, A.T. (1993) X-PLOR version 3.1. Yale University Press, New Haven, CT.
5. 18O exchange studies for an exocyclic methylene intermediate in the reaction catalyzed by T4 deoxycytidylate hydroxymethylase. Biochemistry, 33, 10521-10526.
6. Carreras, C.W. and Santi, D.V. (1995) The catalytic mechanism and structure of thymidylate synthase. Annu. Rev. Biochem., 64, 721-762.
7. (1994) Collaborative Computational Project Number 4. The CCP4 suite: Programs for protein crystallography. Acta Crystallogr., D50, 760-763.
8. Cohen, F.E., Sternberg, M.J.E. and Taylor, W. (1981) Analysis of the tertiary structure of protein β-sheet sandwiches. J. Mol. Biol., 148, 253-272.
9. Cox, G.S. and Conway, T.W. (1973) Template properties of glucose-deficient T-even bacteriophage DNA. J. Virol, 12, 1279-1287.
10. Elcock, A.H., Potter, M.J., Matthews, D.A., Knighton, D.R. and McCammon, J.A. (1996) Electrostatic channeling in the bifunctional enzyme dihydrofolate reductase-thymidylate synthase. J. Mol. Biol., 262, 370-374.
11. Fauman, E.B., Rutenber, E.E., Maley, G.F., Maley, F. and Stroud, R.M. (1994) Water-mediated substrate/product discrimination: the product complex of thymidylate synthase at 1.83 Å. Biochemistry, 33, 1502-1511.
12. Finer-Moore, J.S., Maley, G.F., Maley, F., Montfort, W.R. and Stroud, R.M. (1994) Crystal structure of thymidylate synthase from T4 phage: component of a deoxynucleoside triphosphate-synthesizing complex. Biochemistry, 33, 15459-15468.
13. Finer-Moore, J.S., Liu, L., Birdsall, D.L., Brem, R., Apfeld, J., Santi, D.V. and Stroud, R.M. (1998) Contributions of orientation and hydrogen bonding to catalysis in Asn229 mutants of thymidylate synthase. J. Mol. Biol., 276, 113-129.
14. Gommers-Ampt, J.H. and Borst, P. (1995) Hypermodified bases in DNA. FASEB J., 9, 1034-1042.
15. Gommers-Ampt, J.H., Van Leeuwen, F., de Beer, A.L.J., Vliegenthart, F.G., Dizdaroglu, M., Kowalak, J.A., Crain, P.F. and Borst, P. (1993) β-D-Glucosyl-hydroxymethyluracil: A novel modified base present in the DNA of the parasitic protozoan T. brucei. Cell, 75, 1129-1136.
16. Graves, K.L., Butler, M.M. and Hardy, L.W. (1992) Roles of Cys148 and Asp179 in catalysis by deoxycytidylate hydroxymethylase from bacteriophage T4 examined by site-directed mutagenesis. Biochemistry, 31, 10315-10321.
17. Greenberg, G.R., He, P., Hilfinger, J. and Tseng, M.J. (1994) Deoxyribonucleoside triphosphate synthesis and phage T4 DNA replication. In Karam, J.D. (ed.), Molecular Biology of Bacteriophage T4. American Society of Microbiology, Washington, DC. pp. 14-27.
18. Grindley, H.M., Artymiuk, P.J., Rice, D.W. and Willett, P. (1993) Identification of tertiary structure resemblance in proteins using a maximal common subgraph isomorphism algorithm. J. Mol. Biol., 229, 707-721.
19. Hardy, L.W., Finer-Moore, J.S., Montfort, W.R., Jones, M.O., Santi, D.V. and Stroud, R.M. (1987) Atomic structure of thymidylate synthase: target for rational drug design. Science, 235, 448-455.
20. Holm, L. and Sander, C. (1993) Protein structure comparison by alignment of distance matrices. J. Mol. Biol., 233, 123-138.
21. Horton, M. and Lewis, M. (1992) Calculation of the free energy of association for protein complexes. Protein Sci., 1, 169-181.
22. Jackson, R.M., Gabb, H.A. and Sternberg, M.J.E. (1998) Rapid refinement of protein interfaces incorporating solvation: application to the docking problem. J. Mol. Biol., 276, 265-285.
23. Janin, J. and Rodier, F. (1995) Protein-protein interaction at crystal contacts. Proteins, 23, 580-587.
24. Jones, S. and Thornton, J.M. (1996) Principles of protein-protein interactions. Proc. Natl Acad. Sci. USA. 93, 13-20.
25. Jones, T.A., Zou, J.-Y., Cowan, S.W. and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr., A47, 110-119.
26. Knighton, D.R., Kan, C.-C., Howland, E., Janson, C.A., Zuzana, H., Welsh, K.M. and Matthews, D.A. (1994) Structure of and kinetic channelling in bifunctional dihydrofolate reductase-thymidylate synthase. Nature Struct. Biol., 1, 186-194.
27. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr., 24, 946-950.
28. Lamm, N., Tomaschewski, J. and Rüger, W. (1987) Nucleotide sequence of the deoxycytidylate hydroxymethylase gene of bacteriophage T4 (g42) and the homology of its gene product with thymidylate synthase of E.coli. Nucleic Acids Res., 15, 3930.
29. Lamm, N., Wang, Y., Mathews, C.K. and Rüger, W. (1988) Deoxycytidylate hydroxymethylase gene of bacteriophage T4. Eur. J. Biochem., 172, 553-563.
30. 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, 283-291.
31. Liu, L. and Santi, D.V. (1993) Exclusion of 2′-deoxycytidine 5′-monophosphate by asparagine 229 of thymidylate synthase. Biochemistry, 32, 9263-9267.
32. Mathews, C.K., Wheeler, L.J., Ungermann, C., Young, J.P. and Ray, N.B. (1993) Enzyme interactions involving T4 phage-coded thymidylate synthase and deoxycytidylate hydroxymethylase. Adv. Exp. Med. Biol., 338, 563-570.
33. Matthews, D.A., Appell, K., Oatley, S.J. and Xuong, N.H. (1990a) Crystal structure of Escherichia coli thymidylate synthase containing bound 5-fluoro-2′-deoxyuridylate and 10-propargyl-5.8-dideazafolate. J. Mol. Biol., 214, 923-936.
34. Matthews, D.A., Villafranca, J.E., Janson, C.A., Smith, W.W., Welsh, K. and Freer, S. (1990b) Stereochemical mechanism of action for thymidylate synthase based on the X-ray structure of the covalent inhibitory ternary complex with 5-fluoro-2′-deoxyuridylate and 5,10-methylenetetrahydrofolate. J. Mol. Biol., 214, 937-948.
35. McGaughey, K.M., Wheeler, L.J., Moore, J.T., Maley, G.F. and Mathews, C.K. (1996) Protein-protein interactions involving T4 phagecoded deoxycytidylate deaminase and thymidylate synthase. J. Biol. Chem., 271, 23037-23042.
36. Merritt, E.A. and Murphy, M.E.P. (1994) Raster3D Version 2.0 - a program for photorealistic molecular graphics. Acta Crystallogr., D50, 869-873.
37. Montfort, W.R., Perry, K.M., Fauman, E.B., Finer-Moore, J.S., Maley, G.F., Hardy, L., Maley, F. and Stroud, R.M. (1990) Structure, multiple site binding and segmental accommodation in thymidylate synthase on binding dUMP and anti-folate. Biochemistry, 29, 6964-6977.
38. Nicholls, A., Sharp, K.A. and Honig, B. (1991) Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins. 11, 281-293.
39. Perry, K.M., Carreras, C.W., Chang, L.C., Santi, D.V. and Stroud, R.M. (1993) Structures of thymidylate synthase with a C-terminal deletion: role of the C-terminus in alignment of 2′-deoxyuridine 5′-monophosphate and 5.10-methylenetetrahydrofolate. Biochemistry, 32, 7116-7125.
40. Rice, P.A. and Steitz, T.A. (1994) Model for a DNA-mediated synaptic complex suggested by crystal packing of γδ resolvase subunits. EMBO J., 13, 1514-1524.
41. Rüger, W. (1978) Transcription of bacteriophage T4 DNA in vitro: Selective initiation with dinucleotides. Eur. J. Biochem., 88, 109-117.
42. Rutenber, E.E. and Stroud, R.M. (1996) Binding of the anticancer drug ZDI694 to E.coli thymidylate synthase: assessing specificity and affinity. Structure, 4, 1317-1324.
43. Sack, J.S. (1988) CHAIN - A crystallographic modelling program. J. Mol. Graph., 6, 244-245.
44. Sage, C.R., Rutenber, E.E., Stout, T.J. and Stroud, R.M. (1996) An essential role for water in an enzyme reaction mechanism: The crystal structure of the thymidylate synthase mutant E58Q. Biochemistry, 35, 16270-16281.
45. Schellenberger, U., Livi, L.L. and Santi, D.V. (1995) Cloning, expression, purification and characterization of 2′-deoxyuridylate hydroxymethylase from phage SPO1, Protein Expr. Purif., 6, 423-430.
46. Shapiro, L. et al. (1995) Structural basis of cell-cell adhesion by cadherins. Nature, 374, 327-337.
47. Sohn, S.H. et al. (1999) Crystallization and preliminary X-ray crystallographic analysis of deoxycytidylate hydroxymethylase from bacteriophage T4. Acta Crystallogr., D55, in press.
48. Story, R.M., Weber, I.T. and Steitz, T.A. (1992) The structure of the E.coli recA protein monomer and polymer. Nature, 335, 318-325.
49. Stout, T.J., Schellenberger, U., Santi, D.V. and Stroud, R.M. (1998) Crystal structure of a unique thermal-stable thymidylate synthase from Bacillus subtilis. Biochemistry, 37, 14736-14747.
50. Stroud, R.M. and Finer-Moore, J.S. (1993) Stereochemistry of a multistep/bipartite methyl transfer reaction: thymidylate synthase. FASEB J., 7, 671-677.
51. Stroud, R.M. (1994) An electrostatic highway. Nature Struct. Biol., 1, 131-134.
52. Terwilliger, T.C. and Berendzen, J. (1996) Correlated phasing of multiple isomorphous replacement data. Acta Crystallogr., D52, 749-757.
53. Thylen, C. (1988) Expression and DNA sequence of the cloned bacteriophage T4 dCMP hydroxymethylase gene. J. Bacteriol., 170, 1994-1998.
54. Vrielink, A. Rüger, W., Driessen, H.P.C. and Freemont, P.S. (1994) Crystal structure of the DNA modifying enzyme β-D-glucosyltransferase in the presence and absence of the substrate uridine diphosphoglucose. EMBO J., 13, 3413-3422.
55. Warren, R.A.J. (1980) Modified bases in bacteriophage DNAs. Annu. Rev. Microbiol., 34, 137-158.
56. Wheeler, L., Wang, Y. and Mathews, C.K. (1992) Specific associations of T4 bacteriophage proteins with immobilized deoxycytidylate hydroxymethylase. J. Biol. Chem., 267, 7664-7670.
57. Wheeler, L., Ray, N.B., Ungermann, C., Hendricks, S.P., Bernard, M.A., Hanson, E.S. and Mathews, C.K. (1996) T4 phage gene 32 protein as a candidate organizing factor for the deoxyribonucleoside triphosphate synthetase complex. J. Biol. Chem., 271, 11156-11162.
58. Wilhelm, K. and Rüger, W. (1992) Deoxyuridylate-hydroxymethylase of bacteriophage SPO1. Virology, 189, 640-646.
59. Young, J.P. and Mathews, C.K. (1992) Interactions between T4 phagecoded deoxycytidylate hydroxymethylase and thymidylate synthase as revealed with an anti-idiotypic antibody. J. Biol. Chem., 267, 10786-10790.