Biochemical characterization of recombinant β-glucosyltransferase and analysis of global 5-Hydroxymethylcytosine in unique genomes

Biochemistry

Volumn 51, Issue 5, 2012, Pages 1009-1019

  Terragni, Jolyon ^a   Bitinaite, Jurate ^a   Zheng, Yu ^a   Pradhan, Sriharsa ^a  

^a NEW ENGLAND BIOLABS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINARY COMPLEXES; BIOCHEMICAL CHARACTERIZATION; BOVINE BRAIN; CELL LINES; EPIGENOMES; GENOMIC DNA; GLUCOSYLATE; GLUCOSYLTRANSFERASES; HEALTHY TISSUES; HYPOMETHYLATION; MIXED INHIBITOR; ONCOGENESIS; OXIDATIVE PRODUCTS; PARAMETER ANALYSIS; PRODUCT INHIBITION; STEADY-STATE KINETICS; TARGET SEQUENCES; TURNOVER NUMBER; UDP-GLUCOSE;

CELL CULTURE; DISEASES; ENZYMES; GENES; GLUCOSE; MAMMALS; TISSUE;

DNA;

5 HYDROXYMETHYLCYTOSINE; BETA GLUCOSYLTRANSFERASE; DNA; GLUCOSYLTRANSFERASE; RECOMBINANT ENZYME; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE GLUCOSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL LINE; CONTROLLED STUDY; DNA BINDING; ENZYME GLYCOSYLATION; ENZYME INHIBITION; ENZYME KINETICS; HUMAN; HUMAN CELL; HUMAN TISSUE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; ARABIDOPSIS PROTEINS; BACTERIOPHAGE T4; CATTLE; CYTOSINE; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FEMALE; GENOME, PLANT; GENOME, VIRAL; GLUCOSYLTRANSFERASES; HCT116 CELLS; HEK293 CELLS; HUMANS; MALE; MICE; NIH 3T3 CELLS; RATS; RECOMBINANT PROTEINS; SUBSTRATE SPECIFICITY;

BOVINAE; MAMMALIA; VERTEBRATA;

EID: 84863042219     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi2014739     Document Type: Article

References (37)

1. Josse, J. and Kornberg, A. (1962) Glucosylation of deoxyribonucleic acid. III. α- and β-glucosyl transferases from T4-infected Escherichia coli J. Biol. Chem. 237, 1968-1976
2. Kornberg, S. R., Zimmerman, S. B., and Kornberg, A. (1961) Glucosylation of deoxyribonucleic acid by enzymes from bacteriophage-infected Escherichia coli J. Biol. Chem. 236, 1487-1493
3. Dharmalingam, K. and Goldberg, E. B. (1979) Restriction in vivo. III. General effects of glucosylation and restriction on phage T4 gene expression and replication Virology 96, 393-403 (Pubitemid 9236679)
4. Cox, G. S. and Conway, T. W. (1973) Template properties of glucose-deficient T-even bacteriophage DNA J. Virol. 12, 1279-1287
5. Ruger, W. (1978) Transcription of bacteriophage T4 DNA in vitro: Selective initiation with dinucleotides Eur. J. Biochem. 88, 109-117 (Pubitemid 8367845)
6. Penn, N. W. (1976) Modification of brain deoxyribonucleic acid base content with maturation in normal and malnourished rats Biochem. J. 155, 709-712
7. Tahiliani, M., Koh, K. P., Shen, Y., Pastor, W. A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L. M., Liu, D. R., Aravind, L., and Rao, A. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1 Science 324, 930-935
8. Kriaucionis, S. and Heintz, N. (2009) The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain Science 324, 929-930
9. Ko, M., Huang, Y., Jankowska, A. M., Pape, U. J., Tahiliani, M., Bandukwala, H. S., An, J., Lamperti, E. D., Koh, K. P., Ganetzky, R., Liu, X. S., Aravind, L., Agarwal, S., Maciejewski, J. P., and Rao, A. (2010) Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2 Nature 468, 839-843
10. Guo, J. U., Su, Y., Zhong, C., Ming, G. L., and Song, H. (2011) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain Cell 145, 423-434
11. Koh, K. P., Yabuuchi, A., Rao, S., Huang, Y., Cunniff, K., Nardone, J., Laiho, A., Tahiliani, M., Sommer, C. A., Mostoslavsky, G., Lahesmaa, R., Orkin, S. H., Rodig, S. J., Daley, G. Q., and Rao, A. (2011) Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells Cell Stem Cell 8, 200-213
12. Wu, H., DAlessio, A. C., Ito, S., Xia, K., Wang, Z., Cui, K., Zhao, K., Eve Sun, Y., and Zhang, Y. (2011) Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells Nature 473, 389-393
13. Stroud, H., Feng, S., Morey Kinney, S., Pradhan, S., and Jacobsen, S. E. (2011) 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells Genome Biol. 12, R54
14. Iqbal, K., Jin, S. G., Pfeifer, G. P., and Szabo, P. E. (2011) Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine Proc. Natl. Acad. Sci. U.S.A. 108, 3642-3647
15. Wossidlo, M., Nakamura, T., Lepikhov, K., Marques, C. J., Zakhartchenko, V., Boiani, M., Arand, J., Nakano, T., Reik, W., and Walter, J. (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming Nat. Commun. 2, 241
16. Ficz, G., Branco, M. R., Seisenberger, S., Santos, F., Krueger, F., Hore, T. A., Marques, C. J., Andrews, S., and Reik, W. (2011) Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation Nature 473, 398-402
17. Pastor, W. A., Pape, U. J., Huang, Y., Henderson, H. R., Lister, R., Ko, M., McLoughlin, E. M., Brudno, Y., Mahapatra, S., Kapranov, P., Tahiliani, M., Daley, G. Q., Liu, X. S., Ecker, J. R., Milos, P. M., Agarwal, S., and Rao, A. (2011) Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells Nature 473, 394-397
18. Szwagierczak, A., Bultmann, S., Schmidt, C. S., Spada, F., and Leonhardt, H. (2010) Sensitive enzymatic quantification of 5-hydroxymethylcytosine in genomic DNA Nucleic Acids Res. 38, e181
19. Chin, H. G., Patnaik, D., Esteve, P. O., Jacobsen, S. E., and Pradhan, S. (2006) Catalytic properties and kinetic mechanism of human recombinant Lys-9 histone H3 methyltransferase SUV39H1: Participation of the chromodomain in enzymatic catalysis Biochemistry 45, 3272-3284 (Pubitemid 43376346)
20. Gehring, M., Huh, J. H., Hsieh, T. F., Penterman, J., Choi, Y., Harada, J. J., Goldberg, R. B., and Fischer, R. L. (2006) DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation Cell 124, 495-506 (Pubitemid 43199436)
21. Morales-Ruiz, T., Ortega-Galisteo, A. P., Ponferrada-Marin, M. I., Martinez-Macias, M. I., Ariza, R. R., and Roldan-Arjona, T. (2006) DEMETER and REPRESSOR OF SILENCING 1 encode 5-methylcytosine DNA glycosylases Proc. Natl. Acad. Sci. U.S.A. 103, 6853-6858
22. Georgopoulos, C. P. and Revel, H. R. (1971) Studies with glucosyl transferase mutants of the T-even bacteriophages Virology 44, 271-285
23. Penn, N. W., Suwalski, R., ORiley, C., Bojanowski, K., and Yura, R. (1972) The presence of 5-hydroxymethylcytosine in animal deoxyribonucleic acid Biochem. J. 126, 781-790
24. Kinney, S. M., Chin, H. G., Vaisvila, R., Bitinaite, J., Zheng, Y., Esteve, P. O., Feng, S., Stroud, H., Jacobsen, S. E., and Pradhan, S. (2011) Tissue-specific Distribution and Dynamic Changes of 5-Hydroxymethylcytosine in Mammalian Genomes J. Biol. Chem. 286, 24685-24693
25. Holz-Schietinger, C. and Reich, N. O. (2010) The inherent processivity of the human de novo methyltransferase 3A (DNMT3A) is enhanced by DNMT3L J. Biol. Chem. 285, 29091-29100
26. Morera, S., Imberty, A., Aschke-Sonnenborn, U., Ruger, W., and Freemont, P. S. (1999) T4 phage β-glucosyltransferase: Substrate binding and proposed catalytic mechanism J. Mol. Biol. 292, 717-730 (Pubitemid 29457331)
27. Morera, S., Lariviere, L., Kurzeck, J., Aschke-Sonnenborn, U., Freemont, P. S., Janin, J., and Ruger, W. (2001) High resolution crystal structures of T4 phage β-glucosyltransferase: Induced fit and effect of substrate and metal binding J. Mol. Biol. 311, 569-577 (Pubitemid 32816590)
28. Patnaik, D., Chin, H. G., Esteve, P. O., Benner, J., Jacobsen, S. E., and Pradhan, S. (2004) Substrate specificity and kinetic mechanism of mammalian G9a histone H3 methyltransferase J. Biol. Chem. 279, 53248-53258 (Pubitemid 40051828)
29. Bacolla, A., Pradhan, S., Roberts, R. J., and Wells, R. D. (1999) Recombinant human DNA (cytosine-5) methyltransferase. II. Steady-state kinetics reveal allosteric activation by methylated DNA J. Biol. Chem. 274, 33011-33019 (Pubitemid 129535341)
30. Wu, J. C. and Santi, D. V. (1987) Kinetic and catalytic mechanism of HhaI methyltransferase J. Biol. Chem. 262, 4778-4786 (Pubitemid 17102852)
31. Lindstrom, W. M., Jr., Malygin, E. G., Ovechkina, L. G., Zinoviev, V. V., and Reich, N. O. (2003) Functional analysis of BamHI DNA cytosine-N4 methyltransferase J. Mol. Biol. 325, 711-720 (Pubitemid 36268693)
32. McKenna, E. S. and Roberts, C. W. (2009) Epigenetics and cancer without genomic instability Cell Cycle 8, 23-26
33. Kinney, S. R. and Pradhan, S. (2011) Regulation of expression and activity of DNA (cytosine-5) methyltransferases in mammalian cells Prog. Mol. Biol. Transl. Sci. 101, 311-333
34. Gama-Sosa, M. A., Slagel, V. A., Trewyn, R. W., Oxenhandler, R., Kuo, K. C., Gehrke, C. W., and Ehrlich, M. (1983) The 5-methylcytosine content of DNA from human tumors Nucleic Acids Res. 11, 6883-6894
35. Kurzeck, J. (2002) Functional and Structural Research on the β-Glucosyltransferase of Bacteriophage T4. Ph.D. Dissertation, Ruhr-Universität Bochum, Bochum, Germany.
36. Cerutti, P. A. (1976) in DNA base damage induced by ionizing radiation (Wang, S. Y., Ed.) Vol. II, Academic Press, New York.
37. Hollstein, M. C., Brooks, P., Linn, S., and Ames, B. N. (1984) Hydroxymethyluracil DNA glycosylase in mammalian cells Proc. Natl. Acad. Sci. U.S.A. 81, 4003-4007 (Pubitemid 14054512)