Cloning and characterization of Rhodotorula glutinis thymine hydroxylase

Chemical Research in Toxicology

Volumn 22, Issue 5, 2009, Pages 885-893

  Neidigh, Jonathan W ^a   Darwanto, Agus ^a   Williams, Adides A ^a   Wall, Nathan R ^a   Sowers, Lawrence C ^a  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; DIOXYGENASE; PYRIMIDINE; THYMINE 2 OXOGLUTARATE DIOXYGENASE; UNCLASSIFIED DRUG; URACIL;

ARTICLE; ENZYME ACTIVITY; ENZYME SUBSTRATE; GENE SEQUENCE; HYDROGEN BOND; MASS SPECTROMETRY; MOLECULAR CLONING; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RHODOTORULA GLUTINIS;

AMINO ACID SEQUENCE; CLONING, MOLECULAR; KETOGLUTARIC ACIDS; MIXED FUNCTION OXYGENASES; MOLECULAR SEQUENCE DATA; RHODOTORULA; SEQUENCE ALIGNMENT; THYMINE;

RHODOTORULA GLUTINIS;

EID: 67649974073     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx8004482     Document Type: Article

References (57)

1. Fink, K., Cline, R. E., Henderson, R. B., and Fink, R. M. (1956) Metabolism of thymine (methyl-C14 or -2-C14) by rat liver in vitro. J. Biol. Chem. 221, 425-433.
2. Schandl, E. K. (1973) Thymine 7-hydroxylase activity in normal and leukemic leukocytes. Biochem. Biophys. Res. Commun. 52, 524-529.
3. Abbott, M. T., Kadner, R. J., and Fink, R. M. (1964) Conversion of thymine to 5-hydroxymethyluracil in a cell-free system. J. Biol. Chem. 239, 156-159.
4. Liu, C. K., Shaffer, P. M., Slaughter, R. S., McCroskey, R. P., and Abbott, M. T. (1972) Stoichiometry of the pyrimidine deoxyribonucleoside 2′-hydroxylase reaction and of the conversions of 5-hydroxymethyluracil to 5-formyluracil and of the latter to uracil-5-carboxylic acid. Biochemistry 11, 2172-2176.
5. Liu, C. K., Hsu, C. A., and Abbott, M. T. (1973) Catalysis of three sequential dioxygenase reactions by thymine 7-hydroxylase. Arch. Biochem. Biophys. 159, 180-187.
6. Abbott, M. T., Schandl, E. K., Lee, R. F., Parker, T. S., and Midgett, R. J. (1967) Cofactor requirements of thymine 7-hydroxylase. Biochim. Biophys. Acta 132, 525-528.
7. McCroskey, R. P., Griswold, W. R., Sokoloff, R. L., Sevier, E. D., Lin, S., Liu, K., Shaffer, P. M., Palmatier, R. D., Parker, T. S., and Abbott, M. T. (1971) Studies pertaining to the purification and properties of thymine 7-hydroxylase. Biochim. Biophys. Acta 227, 264-277.
8. Hausinger, R. P. (2004) FeII/alpha-ketoglutarate-dependent hydroxylases and related enzymes. Crit. Rev. Biochem. Mol. Biol. 39, 21-68.
9. Shaffer, P. M., and Arst, H. N., Jr. (1984) Regulation of pyrimidine salvage in Aspergillus nidulans: A role for the major regulatory gene are A mediating nitrogen metabolite repression. Mol. Gen. Genet. 198, 139-145.
10. Shaffer, P. M., Cairns, J. R., Dorman, D. C., and Lott, A. M. (1984) Separation and characterization of pyrimidine deoxyribonucleoside 2′-hydroxylase and thymine 7-hydroxylase from Aspergillus nidulans. Int. J. Biochem. 16, 429-434.
11. Wondrack, L. M., Hsu, C. A., and Abbott, M. T. (1978) Thymine 7-hydroxylase and pyrimidine deoxyribonucleoside 2′-hydroxylase activities in Rhodotorula glutinis. J. Biol. Chem. 253, 6511-6515.
12. Wondrack, L. M., Warn, B. J., Saewert, M. D., and Abbott, M. T. (1979) Substitution of nucleoside triphosphates for ascorbate in the thymine 7-hydroxylase reaction of Rhodotorula glutinis. J. Biol. Chem. 254, 26-29.
13. Warn-Cramer, B. J., Macrander, L. A., and Abbott, M. T. (1983) Markedly different ascorbate dependencies of the sequential alpha-ketoglutarate dioxygenase reactions catalyzed by an essentially homogeneous thymine 7-hydroxylase from Rhodotorula glutinis. J. Biol. Chem. 258, 10551-10557.
14. Thornburg, L. D., Lai, M. T., Wishnok, J. S., and Stubbe, J. (1993) A non-heme iron protein with heme tendencies: An investigation of the substrate specificity of thymine hydroxylase. Biochemistry 32, 14023-14033.
15. Thornburg, L. D., and Stubbe, J. (1993) Mechanism-based inactivation of thymine hydroxylase, an alpha-ketoglutarate-dependent dioxygenase, by 5-ethynyluracil. Biochemistry 32, 14034-14042.
16. Lai, M., Wu, W., and Stubbe, J. (1995) Characterization of a novel, stable norcaradiene adduct resulting from the inactivation of thymine hydroxylase by 5-ethynyluracil. J. Am. Chem. Soc. 117, 5023-5030.
17. Smiley, J. A., Kundracik, M., Landfried, D. A., Barnes, V. R., Sr., and and Axhemi, A. A. (2005) Genes of the thymidine salvage pathway: Thymine-7-hydroxylase from a Rhodotorula glutinis cDNA library and iso-orotate decarboxylase from Neurospora crassa. Biochim. Biophys. Acta 1723, 256-264.
18. Braun, E. L., Halpern, A. L., Nelson, M. A., and Natvig, D. O. (2000) Large-scale comparison of fungal sequence information: mechanisms of innovation in Neurospora crassa and gene loss in Saccharomyces cerevisiae. Genome Res. 10, 416-430.
19. Galagan, J. E., Calvo, S. E., Borkovich, K. A., Selker, E. U., Read, N. D., Jaffe, D., FitzHugh, W., Ma, L. J., Smirnov, S., Purcell, S., Rehman, B., Elkins, T., Engels, R., Wang, S., Nielsen, C. B., Butler, J., Endrizzi, M., Qui, D., Ianakiev, P., Bell-Pedersen, D., Nelson, M. A., Werner-Washburne, M., Selitrennikoff, C. P., Kinsey, J. A., Braun, E. L., Zelter, A., Schulte, U., Kothe, G. O., Jedd, G., Mewes, W., Staben, C., Marcotte, E., Greenberg, D., Roy, A., Foley, K., Naylor, J., Stange-Thomann, N., Barrett, R., Gnerre, S., Kamal, M., Kamvysselis, M., Mauceli, E., Bielke, C., Rudd, S., Frishman, D., Krystofova, S., Rasmussen, C., Metzenberg, R. L., Perkins, D. D., Kroken, S., Cogoni, C., Macino, G., Catcheside, D., Li, W., Pratt, R. J., Osmani, S. A., DeSouza, C. P., Glass, L., Orbach, M. J., Berglund, J. A., Voelker, R., Yarden, O., Plamann, M., Seiler, S., Dunlap, J., Radford, A., Aramayo, R., Natvig, D. O., Alex, L. A., Mannhaupt, G., Ebbole, D. J., Freitag, M., Paulsen, I., Sachs, M. S., Lander, E. S., Nusbaum, C., and Birren, B. (2003) The genome sequence of the filamentous fungus Neurospora crassa. Nature (London) 422, 859-868.
20. Galagan, J. E., Calvo, S. E., Cuomo, C., Ma, L. J., Wortman, J. R., Batzoglou, S., Lee, S. I., Basturkmen, M., Spevak, C. C., Clutterbuck, J., Kapitonov, V., Jurka, J., Scazzocchio, C., Farman, M., Butler, J., Purcell, S., Harris, S., Braus, G. H., Draht, O., Busch, S., D'Enfert, C., Bouchier, C., Goldman, G. H., Bell-Pedersen, D., Griffiths-Jones, S., Doonan, J. H., Yu, J., Vienken, K., Pain, A., Freitag, M., Selker, E. U., Archer, D. B., Penalva, M. A., Oakley, B. R., Momany, M., Tanaka, T., Kumagai, T., Asai, K., Machida, M., Nierman, W. C., Denning, D. W., Caddick, M., Hynes, M., Paoletti, M., Fischer, R., Miller, B., Dyer, P., Sachs, M. S., Osmani, S. A., and Birren, B. W. (2005) Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 438, 1105-1115.
21. Bankel, L., Lindstedt, G., and Lindstedt, S. (1977) Thymine 7-hydroxylase from Neurospora crassa. Substrate specificity studies. Biochim. Biophys. Acta 481, 431-437.
22. Sedgwick, B. (2004) Repairing DNA-methylation damage. Nat. Rev. Mol. Cell Biol. 5, 148-157.
23. Kondo, H., Nakabeppu, Y., Kataoka, H., Kuhara, S., Kawabata, S., and Sekiguchi, M. (1986) Structure and expression of the alkB gene of Escherichia coli related to the repair of alkylated DNA. J. Biol. Chem. 261, 15772-15777.
24. Aravind, L., and Koonin, E. V. (2001) The DNA-repair protein AlkB, EGL-9, and leprecan define new families of 2-oxoglutarate- and iron-dependent dioxygenases. Genome Biol. 2, research0007.10007.8.
25. Trewick, S. C., Henshaw, T. F., Hausinger, R. P., Lindahl, T., and Sedgwick, B. (2002) Oxidative demethylation by Escherichia coli AlkB directly reverts DNA base damage. Nature (London) 419, 174-178.
26. Falnes, P. O., Johansen, R. F., and Seeberg, E. (2002) AlkB-mediated oxidative demethylation reverses DNA damage in Escherichia coli. Nature (London) 419, 178-182.
27. Bhattacharya, S. K., Ramchandani, S., Cervoni, N., and Szyf, M. (1999) A mammalian protein with specific demethylase activity for mCpG DNA. Nature (London) 397, 579-583.
28. Cedar, H., and Verdine, G. L. (1999) Gene expression. The amazing demethylase. Nature (London) 397, 568-569.
29. Wolffe, A. P., Jones, P. L., and Wade, P. A. (1999) DNA demethylation. Proc. Natl. Acad. Sci. U.S.A. 96, 5894-5896.
30. Mayer, W., Niveleau, A., Walter, J., Fundele, R., and Haaf, T. (2000) Demethylation of the zygotic paternal genome. Nature (London) 403, 501-502.
31. Koivisto, P., Robins, P., Lindahl, T., and Sedgwick, B. (2004) Demethylation of 3-methylthymine in DNA by bacterial and human DNA dioxygenases. J. Biol. Chem. 279, 40470-40474.
32. Yu, Z., Genest, P. A., ter Riet, B., Sweeney, K., DiPaolo, C., Kieft, R., Christodoulou, E., Perrakis, A., Simmons, J. M., Hausinger, R. P., van Luenen, H. G., Rigden, D. J., Sabatini, R., and Borst, P. (2007) The protein that binds to DNA base J in trypanosomatids has features of a thymidine hydroxylase. Nucleic Acids Res. 35, 2107-2115.
33. LaFrancois, C. J., Fujimoto, J., and Sowers, L. C. (1998) Synthesis and characterization of isotopically enriched pyrimidine deoxynucleoside oxidation damage products. Chem. Res. Toxicol. 11, 75-83.
34. LaFrancois, C. J., Yu, K., and Sowers, L. C. (1998) Quantification of 5-(hydroxymethyl)uracil in DNA by gas chromatography/mass spectrometry: Problems and solutions. Chem. Res. Toxicol. 11, 786-793.
35. Eng, J. K., McCormack, A. L., and Yates, J. R. (1994) An approach to correlate tandem mass-spectral data of peptides with amino-acid-sequences in a protein database. J. Am. Soc. Mass Spectrom. 5, 976-989.
36. Matsudaira, P. (1990) Limited N-terminal sequence analysis. Methods Enzymol. 182, 602-613.
37. Sauder, J. M., Arthur, J. W., and Dunbrack, R. L., Jr. (2000) Largescale comparison of protein sequence alignment algorithms with structure alignments. Proteins 40, 6-22.
38. Ward, J. J., McGuffin, L. J., Buxton, B. F., and Jones, D. T. (2003) Secondary structure prediction with support vector machines. Bioinformatics 19, 1650-1655.
39. Privat, E., and Sowers, L. C. (1996) Photochemical deamination and demethylation of 5-methylcytosine. Chem. Res. Toxicol. 9, 745-750.
40. Burdzy, A., Noyes, K. T., Valinluck, V., and Sowers, L. C. (2002) Synthesis of stable-isotope enriched 5-methylpyrimidines and their use as probes of base reactivity in DNA. Nucleic Acids Res. 30, 4068-4074.
41. Kinzie, S. D., Thevis, M., Ngo, K., Whitelegge, J., Loo, J. A., and Abu-Omar, M. M. (2003) Posttranslational hydroxylation of human phenylalanine hydroxylase is a novel example of enzyme self-repair within the second coordination sphere of catalytic iron. J. Am. Chem. Soc. 125, 4710-4711.
42. Muller, I., Stuckl, C., Wakeley, J., Kertesz, M., and Uson, I. (2005) Succinate complex crystal structures of the alpha-ketoglutarate-dependent dioxygenase AtsK: Steric aspects of enzyme self-hydroxylation. J. Biol. Chem. 280, 5716-5723.
43. Ryle, M. J., Koehntop, K. D., Liu, A., Que, L., Jr., and and Hausinger, R. P. (2003) Interconversion of two oxidized forms of taurine/alpha- ketoglutarate dioxygenase, a non-heme iron hydroxylase: Evidence for bicarbonate binding. Proc. Natl. Acad. Sci. U.S.A. 100, 3790-3795.
44. Wilmouth, R. C., Turnbull, J. J., Welford, R.W., Clifton, I. J., Prescott, A. G., and Schofield, C. J. (2002) Structure and mechanism of anthocyanidin synthase from Arabidopsis thaliana. Structure 10, 93-103.
45. Kavli, B., Slupphaug, G., Mol, C. D., Arvai, A. S., Peterson, S. B., Tainer, J. A., and Krokan, H. E. (1996) Excision of cytosine and thymine from DNA by mutants of human uracil-DNA glycosylase. EMBO J. 15, 3442-3447.
46. 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.
47. Handa, P., Acharya, N., and Varshney, U. (2002) Effects of mutations at tyrosine 66 and asparagine 123 in the active site pocket of Escherichia coli uracil DNA glycosylase on uracil excision from synthetic DNA oligomers: Evidence for the occurrence of long-range interactions between the enzyme and substrate. Nucleic Acids Res. 30, 3086-3095.
48. Lindahl, T. (1993) Instability and decay of the primary structure of DNA. Nature (London) 362, 709-715.
49. Mullaart, E., Lohman, P. H., Berends, F., and Vijg, J. (1990) DNA damage metabolism and aging. Mutat. Res. 237, 189-210.
50. Zuo, S., Boorstein, R. J., and Teebor, G. W. (1995) Oxidative damage to 5-methylcytosine in DNA. Nucleic Acids Res. 23, 3239-3243.
51. Burdzy, A., Noyes, K. T., Valinluck, V., and Sowers, L. C. (2002) Synthesis of stable-isotope enriched 5-methylpyrimidines and their use as probes of base reactivity in DNA. Nucleic Acids Res. 30, 4068-4074.
52. Haushalter, K. A., Todd Stukenberg, M. W., Kirschner, M. W., and Verdine, G. L. (1999) Identification of a new uracil-DNA glycosylase family by expression cloning using synthetic inhibitors. Curr. Biol. 9, 174-185.
53. Baker, D., Liu, P., Burdzy, A., and Sowers, L. C. (2002) Characterization of the substrate specificity of a human 5-hydroxymethyluracil glycosylase activity. Chem. Res. Toxicol. 15, 33-39.
54. Cannon-Carlson, S. V., Gokhale, H., and Teebor, G. W. (1989) Purification and characterization of 5-hydroxymethyluracil-DNA glycosylase from calf thymus. Its possible role in the maintenance of methylated cytosine residues. J. Biol. Chem. 264, 13306-13312.
55. Boorstein, R. J., Chiu, L. N., and Teebor, G. W. (1989) Phylogenetic evidence of a role for 5-hydroxymethyluracil-DNA glycosylase in the maintenance of 5-methylcytosine in DNA. Nucleic Acids Res. 17, 7653-7661.
56. Rogstad, D. K., Liu, P., Burdzy, A., Lin, S. S., and Sowers, L. C. (2002) Endogenous DNA lesions can inhibit the binding of the AP-1 (c-Jun) transcription factor. Biochemistry 41, 8093-8102.
57. Valinluck, V., Tsai, H. H., Rogstad, D. K., Burdzy, A., Bird, A., and Sowers, L. C. (2004) Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res. 32, 4100-4108.