1887

Abstract

Thymidylate synthase (TS) (EC 2.1.1.45) is essential for the synthesis of dTMP in prokaryotic and eukaryotic organisms. Within the white spot syndrome virus (WSSV) genome, an open reading frame (WSV067) that encodes a 289 amino acid polypeptide showed significant homology to all known TSs from species including mammals, plants, fungi, protozoa, bacteria and DNA viruses. In this study, WSV067 was expressed in , and the purified recombinant protein showed TS activity in dUMP−folate-binding assays using ultraviolet difference spectroscopy. RT-PCR and Western blot analyses showed that WSV067 was a genuine and early gene. Phylogenetic analysis revealed that WSSV-TS was more closely related to the TSs of eukaryotes than to those from prokaryotes.

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2004-07-01
2019-11-14
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References

  1. Adams, M. D., Celniker, S. E., Holt, R. A. & 191 other authors ( 2000; ). The genome sequence of Drosophila melanogaster. Science 287, 2185–2195.[CrossRef]
    [Google Scholar]
  2. Afonso, C. L., Tulman, E. R., Lu, Z., Oma, E., Kutish, G. F. & Rock, D. L. ( 1999; ). The genome of Melanoplus sanguinipes entomopoxvirus. J Virol 73, 533–552.
    [Google Scholar]
  3. Belfort, M., Maley, G. F., Pedersen-Lane, J. & Maley, F. ( 1983a; ). Primary structure of the Escherichia coli thyA gene and its thymidylate synthase product. Proc Natl Acad Sci U S A 80, 4914–4918.[CrossRef]
    [Google Scholar]
  4. Belfort, M., Moelleken, A., Maley, G. F. & Maley, F. ( 1983b; ). Purification and properties of T4 phage thymidylate synthase produced by the cloned gene in an amplification vector. J Biol Chem 258, 2045–2051.
    [Google Scholar]
  5. Beverley, S. M., Ellenberger, T. E. & Cordingley, J. S. ( 1986; ). Primary structure of the gene encoding the bifunctional dihydrofolate reductase-thymidylate synthase of Leishmania major. Proc Natl Acad Sci U S A 83, 2584–2588.[CrossRef]
    [Google Scholar]
  6. Bodemer, W., Niller, H. H., Nitsche, N., Scholz, B. & Fleckenstein, B. ( 1986; ). Organization of the thymidylate synthase gene of herpesvirus saimiri. J Virol 60, 114–123.
    [Google Scholar]
  7. Carreras, C. W. & Santi, D. V. ( 1995; ). The catalytic mechanism and structure of thymidylate synthase. Annu Rev Biochem 64, 721–762.[CrossRef]
    [Google Scholar]
  8. Chen, H. H., Tso, D. J., Yeh, W. B., Cheng, H. J. & Wu, T. F. ( 2001; ). The thymidylate synthase gene of Hz-1 virus: a gene captured from its lepidopteran host. Insect Mol Biol 10, 495–503.[CrossRef]
    [Google Scholar]
  9. Chen, L. L., Wang, H. C., Huang, C. J. & 9 other authors ( 2002; ). Transcriptional analysis of the DNA polymerase gene of shrimp white spot syndrome virus. Virology 301, 136–147.[CrossRef]
    [Google Scholar]
  10. Cheng, Q. & Saul, A. ( 1994; ). The dihydrofolate reductase domain of rodent malarias: point mutations and pyrimethamine resistance. Mol Biochem Parasitol 65, 361–363.[CrossRef]
    [Google Scholar]
  11. Chiericatti, G. & Santi, D. V. ( 1998; ). Aspartate 221 of thymidylate synthase is involved in folate cofactor binding and in catalysis. Biochemistry 37, 9038–9042.[CrossRef]
    [Google Scholar]
  12. Cox, K. M., Robertson, D. & Fites, R. C. ( 1999; ). Mapping and expression of a bifunctional thymidylate synthase, dihydrofolate reductase gene from maize. Plant Mol Biol 41, 733–739.[CrossRef]
    [Google Scholar]
  13. Danenberg, P. V. ( 1977; ). Thymidylate synthetase − a target enzyme in cancer chemotherapy. Biochim Biophys Acta 473, 73–92.
    [Google Scholar]
  14. Davison, A. J. & Scott, J. E. ( 1986; ). The complete DNA sequence of varicella-zoster virus. J Gen Virol 67, 1759–1816.[CrossRef]
    [Google Scholar]
  15. Eastwood, D. C., Bains, N. K., Henderson, J. & Burton, K. S. ( 2000; ). Genomic sequencing of superoxide dismutase in Agaricus bisporus. Submitted to the EMBL/GenBank/DDBJ databases.
  16. Edgell, D. R. & Shub, D. A. ( 2001; ). Related homing endonucleases I-BmoI and I-TevI use different strategies to cleave homologous recognition sites. Proc Natl Acad Sci U S A 98, 7898–7903.[CrossRef]
    [Google Scholar]
  17. Eldin de Pecoulas, P., Basco, L. K., Tahar, R., Ouatas, T. & Mazabraud, A. ( 1998; ). Analysis of the Plasmodium vivax dihydrofolate reductase-thymidylate synthase gene sequence. Gene 211, 177–185.[CrossRef]
    [Google Scholar]
  18. Gamarro, F., Yu, P. L., Zhao, J., Edman, U., Greene, P. J. & Santi, D. ( 1995; ). Trypanosoma brucei dihydrofolate reductase-thymidylate synthase gene isolation and expression and characterization of the enzyme. Mol Biochem Parasitol 72, 11–22.[CrossRef]
    [Google Scholar]
  19. Hardy, L. W. & Nalivaika, E. ( 1992; ). Asn177 in Escherichia coli thymidylate synthase is a major determinant of pyrimidine specificity. Proc Natl Acad Sci U S A 89, 9725–9729.[CrossRef]
    [Google Scholar]
  20. Honess, R. W., Bodemer, W., Cameron, K. R., Niller, H. H., Fleckenstein, B. & Randall, R. E. ( 1986; ). The A-rich genome of herpesvirus saimiri contains a highly conserved gene for thymidylate synthase. Proc Natl Acad Sci U S A 83, 3604–3608.[CrossRef]
    [Google Scholar]
  21. Huang, C., Zhang, X., Lin, Q., Xu, X., Hu, Z. & Hew, C. L. ( 2002; ). Proteomic analysis of shrimp white spot syndrome viral proteins and characterization of a novel envelope protein VP466. Mol Cell Proteomics 1, 223–231.[CrossRef]
    [Google Scholar]
  22. Hughes, D. E., Shonekan, O. A. & Simpson, L. ( 1989; ). Structure, genomic organization and transcription of the bifunctional dihydrofolate reductase-thymidylate synthase gene from Crithidia fasciculata. Mol Biochem Parasitol 34, 155–166.[CrossRef]
    [Google Scholar]
  23. Ivanova, N., Anderson, I., Bhattacharyya, A. & 16 other authors ( 2002; ). The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc Natl Acad Sci U S A 99, 443–448.[CrossRef]
    [Google Scholar]
  24. Ivanova, N., Sorokin, A., Anderson, I. & 20 other authors ( 2003; ). Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 423, 87–91.[CrossRef]
    [Google Scholar]
  25. Kaneda, S., Nalbantoglu, J., Takeishi, K., Shimizu, K., Gotoh, O., Seno, T. & Ayusawa, D. ( 1990; ). Structural and functional analysis of the human thymidylate synthase gene. J Biol Chem 265, 20277–20284.
    [Google Scholar]
  26. Kenny, E., Atkinson, T. & Hartley, B. S. ( 1985; ). Nucleotide sequence of the thymidylate synthetase gene (thyP3) from the Bacillus subtilis phage phi 3T. Gene 34, 335–342.[CrossRef]
    [Google Scholar]
  27. Kozak, M. ( 1989; ). The scanning model for translation: an update. J Cell Biol 108, 229–234.[CrossRef]
    [Google Scholar]
  28. Lockshin, A., Mondal, K. & Danenberg, P. V. ( 1984; ). Spectroscopic studies of ternary complexes of thymidylate synthase, deoxyribonucleotides, and folate analogs. J Biol Chem 259, 11346–11352.
    [Google Scholar]
  29. Luo, M., Piffanelli, P., Rastelli, L. & Cella, R. ( 1993; ). Molecular cloning and analysis of a cDNA coding for the bifunctional dihydrofolate reductase-thymidylate synthase of Daucus carota. Plant Mol Biol 22, 427–435.[CrossRef]
    [Google Scholar]
  30. McLauchlan, J., Gaffney, D., Whitton, J. L. & Clements, J. B. ( 1985; ). The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3′ termini. Nucleic Acids Res 13, 1347–1368.[CrossRef]
    [Google Scholar]
  31. Muller, K., Tidona, C. A., Bahr, U. & Darai, G. ( 1998; ). Identification of a thymidylate synthase gene within the genome of Chilo iridescent virus. Virus Genes 17, 243–258.[CrossRef]
    [Google Scholar]
  32. Nelson, K., Alonso, G., Langer, P. J. & Beverley, S. M. ( 1990; ). Sequence of the dihydrofolate reductase-thymidylate synthase (DHFR-TS) gene of Leishmania amazonensis. Nucleic Acids Res 18, 2819.[CrossRef]
    [Google Scholar]
  33. Nierman, W. C., Feldblyum, T. V., Laub, M. T. & 34 other authors ( 2001; ). Complete genome sequence of Caulobacter crescentus. Proc Natl Acad Sci U S A 98, 4136–4141.[CrossRef]
    [Google Scholar]
  34. Nishio, Y., Nakamura, Y., Kawarabayasi, Y. & 8 other authors ( 2003; ). Comparative complete genome sequence analysis of the amino acid replacements responsible for the thermostability of Corynebacterium efficiens. Genome Res 13, 1572–1579.[CrossRef]
    [Google Scholar]
  35. Noelling, J., Breton, G., Omelchenko, M. V. & 16 other authors ( 2001; ). Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183, 4823–4838.[CrossRef]
    [Google Scholar]
  36. Perry, K. M., Fauman, E. B., Finer-Moore, J. S., Montfort, W. R., Maley, G. F., Maley, F. & Stroud, R. M. ( 1990; ). Plastic adaptation toward mutations in proteins: structural comparison of thymidylate synthases. Proteins 8, 315–333.[CrossRef]
    [Google Scholar]
  37. Perryman, S. M., Rossana, C., Deng, T. L., Vanin, E. F. & Johnson, L. F. ( 1986; ). Sequence of a cDNA for mouse thymidylate synthase reveals striking similarity with the prokaryotic enzyme. Mol Biol Evol 3, 313–321.
    [Google Scholar]
  38. Read, T. D., Peterson, S. N., Tourasse, N. & 49 other authors ( 2003; ). The genome sequence of Bacillus anthracis Ames and comparison to closely related bacteria. Nature 423, 81–86.[CrossRef]
    [Google Scholar]
  39. Reche, P., Arrebola, R., Olmo, A., Santi, D. V., Gonzalez-Pacanowska, D. & Ruiz-Perez, L. M. ( 1994; ). Cloning and expression of the dihydrofolate reductase-thymidylate synthase gene from Trypanosoma cruzi. Mol Biochem Parasitol 65, 247–258.[CrossRef]
    [Google Scholar]
  40. Richter, J., Puchtler, I. & Fleckenstein, B. ( 1988; ). Thymidylate synthase gene of herpesvirus ateles. J Virol 62, 3530–3535.
    [Google Scholar]
  41. Roos, D. S. ( 1993; ). Primary structure of the dihydrofolate reductase-thymidylate synthase gene from Toxoplasma gondii. J Biol Chem 268, 6269–6280.
    [Google Scholar]
  42. Russo, J. J., Bohenzky, R. A., Chien, M. C. & 8 other authors ( 1996; ). Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc Natl Acad Sci U S A 93, 14862–14867.[CrossRef]
    [Google Scholar]
  43. Schiffer, C. A., Clifton, I. J., Davisson, V. J., Santi, D. V. & Stroud, R. M. ( 1995; ). The crystal structure of human thymidylate synthase: a structural mechanism for guiding substrates into the active site. Biochemistry 34, 16279–16287.[CrossRef]
    [Google Scholar]
  44. Schlichtherle, I. M., van Houten, J. L. & Roos, D. S. ( 1996; ). Cloning and molecular analysis of the bifunctional dihydrofolate reductase-thymidylate synthase gene in the ciliated protozoan Paramecium tetraurelia. Mol Genet Gen 250, 665–673.
    [Google Scholar]
  45. Shigenobu, S., Watanabe, H., Hattori, M., Sakaki, Y. & Ishikawa, H. ( 2000; ). Genome sequence of the endocellular bacterial symbiont of aphids Buchnera sp. APS. Nature 407, 81–86.[CrossRef]
    [Google Scholar]
  46. Singer, S. C., Richards, C. A., Ferone, R., Benedict, D. & Ray, P. ( 1989; ). Cloning, purification, and properties of Candida albicans thymidylate synthase. J Bacteriol 171, 1372–1378.
    [Google Scholar]
  47. Tamas, I., Klasson, L., Canbaeck, B., Naeslund, A. K., Eriksson, A. S., Wernegreen, J. J., Sandstroem, J. P., Moran, N. A. & Andersson, S. G. E. ( 2002; ). 50 million years of genomic stasis in endosymbiotic bacteria. Science 296, 2376–2379.[CrossRef]
    [Google Scholar]
  48. Taylor, G. R., Lagosky, P. A., Storms, R. K. & Haynes, R. H. ( 1987; ). Molecular characterization of the cell cycle-regulated thymidylate synthase gene of Saccharomyces cerevisiae. J Biol Chem 262, 5298–5307.
    [Google Scholar]
  49. Telford, E. A. R., Watson, M. S., Aird, H. C., Perry, J. & Davison, A. J. ( 1995; ). The DNA sequence of equine herpesvirus 2. J Mol Biol 249, 520–528.[CrossRef]
    [Google Scholar]
  50. Tian, L. & Tam, J. W. O. ( 1998; ). Molecular cloning of thymidylate synthase from Ascaris suum. Submitted to the EMBL/GenBank/DDBJ databases.
  51. Tong, Y. ( 1998; ). Thymidylate synthase (TS) that contain single residue substitutions within the highly conserved Arg50-loop, which binds the pyrimidine substrate. J Biol Chem 273, 11611–11618.[CrossRef]
    [Google Scholar]
  52. Tsai, M. F., Yu, H. T., Tzeng, H. F. & 7 other authors ( 2000; ). Identification and characterization of a shrimp white spot syndrome virus (WSSV) gene that encodes a novel chimeric polypeptide of cellular-type thymidine kinase and thymidylate kinase. Virology 277, 100–110.[CrossRef]
    [Google Scholar]
  53. Van Dijk, M. R., McConkey, G. A., Vinkenoog, R., Waters, A. P. & Janse, C. J. ( 1994; ). Mechanisms of pyrimethamine resistance in two different strains of Plasmodium berghei. Mol Biochem Parasitol 68, 167–171.[CrossRef]
    [Google Scholar]
  54. Van Ham, R. C. H. J., Kamerbeek, J., Palacios, C. & 13 other authors ( 2003; ). Reductive genome evolution in Buchnera aphidicola. Proc Natl Acad Sci U S A 100, 581–586.[CrossRef]
    [Google Scholar]
  55. Van Hulten, M. C. W., Tsai, M. F., Schipper, C. A., Lo, C. F., Kou, G. H. & Vlak, J. M. ( 2000; ). Analysis of a genomic segment of white spot syndrome virus of shrimp containing ribonucleotide reductase genes and repeat regions. J Gen Virol 81, 307–316.
    [Google Scholar]
  56. Van Hulten, M. C. W., Wittenberg, M., Goodall, S. D. & Vlak, J. M. ( 2001; ). Identification of two major virion protein genes of white spot syndrome virus of shrimp. Virology 266, 227–236.
    [Google Scholar]
  57. Wang, M., Ratnam, S. & Freisheim, J. H. ( 1995; ). Cloning, nucleotide sequence and expression of the bifunctional dihydrofolate reductase-thymidylate synthase from Glycine max. Biochim Biophys Acta 1261, 325–336.[CrossRef]
    [Google Scholar]
  58. Yang, F., He, J., Lin, X., Li, Q., Pan, D., Zhang, X. & Xu, X. ( 2001; ). Complete genome sequence of the shrimp white spot syndrome virus. J Virol 75, 11811–11820.[CrossRef]
    [Google Scholar]
  59. Zhang, X., Huang, C., Xu, X. & Hew, C. L. ( 2002; ). Transcription and identification of an envelope protein gene (p22) from shrimp white spot syndrome virus. J Gen Virol 83, 471–477.
    [Google Scholar]
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