5-methylcytosine recognition by arabidopsis thaliana DNA glycosylases DEMETER and DML3

Biochemistry

Volumn 53, Issue 15, 2014, Pages 2525-2532

  Brooks, Sonja C ^a   Fischer, Robert L ^b   Huh, Jin Hoe ^c   Eichman, Brandt F ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATION; ENZYMES; GENE EXPRESSION;

5-HYDROXYMETHYLCYTOSINE; ARABIDOPSIS THALIANA; DIFFERENT MECHANISMS; ENZYME ACTIVE SITES; HOMOLOGY MODELING; MUTATIONAL ANALYSIS; STRUCTURE-FUNCTION ANALYSIS; X-CHROMOSOME INACTIVATION;

DNA;

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; CYTOSINE; DNA GLYCOSYLTRANSFERASE; DOUBLE STRANDED DNA; PROTEIN DME; PROTEIN DML 3; PROTEIN ROS 1; UNCLASSIFIED DRUG; VEGETABLE PROTEIN;

ARABIDOPSIS THALIANA; ARTICLE; BRASSICACEAE; DNA BINDING; DNA MODIFICATION; ENZYME ACTIVE SITE; EXCISION REPAIR; GENE EXPRESSION; MOLECULAR RECOGNITION; MUTATIONAL ANALYSIS; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

5-METHYLCYTOSINE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; DNA GLYCOSYLASES; DNA PRIMERS; MODELS, MOLECULAR; NUCLEAR PROTEINS; POLYMERASE CHAIN REACTION; SUBSTRATE SPECIFICITY;

EID: 84899410128     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi5002294     Document Type: Article

References (62)

1. Chan, S. W., Henderson, I. R., and Jacobsen, S. E. (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana Nat. Rev. Genet. 6, 351-360
2. Huh, J. H., Bauer, M. J., Hsieh, T. F., and Fischer, R. L. (2008) Cellular programming of plant gene imprinting Cell 132, 735-744
3. Law, J. A. and Jacobsen, S. E. (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals Nat. Rev. Genet. 11, 204-220
4. Dulac, C. (2010) Brain function and chromatin plasticity Nature 465, 728-735
5. Feinberg, A. P., Ohlsson, R., and Henikoff, S. (2006) The epigenetic progenitor origin of human cancer Nat. Rev. Genet. 7, 21-33
6. Goll, M. G. and Bestor, T. H. (2005) Eukaryotic cytosine methyltransferases Annu. Rev. Biochem. 74, 481-514
7. Piccolo, F. M. and Fisher, A. G. (2013) Getting rid of DNA methylation Trends Cell Biol. 24, 136-143
8. Lindahl, T. (2000) Suppression of spontaneous mutagenesis in human cells by DNA base excision-repair Mutat. Res. 462, 129-135
9. Fromme, J. C., Banerjee, A., Huang, S. J., and Verdine, G. L. (2004) Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase Nature 427, 652-656
10. Huffman, J. L., Sundheim, O., and Tainer, J. A. (2005) DNA base damage recognition and removal: new twists and grooves Mutat. Res. 577, 55-76
11. Brooks, S. C., Adhikary, S., Rubinson, E. H., and Eichman, B. F. (2013) Recent advances in the structural mechanisms of DNA glycosylases Biochim. Biophys. Acta 1834, 247-271
12. Cortellino, S., Xu, J., Sannai, M., Moore, R., Caretti, E., Cigliano, A., Le Coz, M., Devarajan, K., Wessels, A., Soprano, D., Abramowitz, L. K., Bartolomei, M. S., Rambow, F., Bassi, M. R., Bruno, T., Fanciulli, M., Renner, C., Klein-Szanto, A. J., Matsumoto, Y., Kobi, D., Davidson, I., Alberti, C., Larue, L., and Bellacosa, A. (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair Cell 146, 67-79
13. Cortazar, D., Kunz, C., Selfridge, J., Lettieri, T., Saito, Y., MacDougall, E., Wirz, A., Schuermann, D., Jacobs, A. L., Siegrist, F., Steinacher, R., Jiricny, J., Bird, A., and Schar, P. (2011) Embryonic lethal phenotype reveals a function of TDG in maintaining epigenetic stability Nature 470, 419-423
14. Rai, K., Huggins, I. J., James, S. R., Karpf, A. R., Jones, D. A., and Cairns, B. R. (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45 Cell 135, 1201-1212
15. Ito, S., Shen, L., Dai, Q., Wu, S. C., Collins, L. B., Swenberg, J. A., He, C., and Zhang, Y. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine Science 333, 1300-1303
16. 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
17. Veron, N. and Peters, A. H. (2011) Epigenetics: Tet proteins in the limelight Nature 473, 293-294
18. Wu, H. and Zhang, Y. (2011) Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation Genes Dev. 25, 2436-2452
19. Maiti, A. and Drohat, A. C. (2011) Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites J. Biol. Chem. 286, 35334-35338
20. Zhang, L., Lu, X., Lu, J., Liang, H., Dai, Q., Xu, G. L., Luo, C., Jiang, H., and He, C. (2012) Thymine DNA glycosylase specifically recognizes 5-carboxylcytosine-modified DNA Nat. Chem. Biol. 8, 328-330
21. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J. J., Goldberg, R. B., Jacobsen, S. E., and Fischer, R. L. (2002) DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in arabidopsis Cell 110, 33-42
22. 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
23. 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
24. Hsieh, T. F., Shin, J., Uzawa, R., Silva, P., Cohen, S., Bauer, M. J., Hashimoto, M., Kirkbride, R. C., Harada, J. J., Zilberman, D., and Fischer, R. L. (2011) Regulation of imprinted gene expression in Arabidopsis endosperm Proc. Natl. Acad. Sci. U. S. A. 108, 1755-1762
25. Calarco, J. P., Borges, F., Donoghue, M. T., Van Ex, F., Jullien, P. E., Lopes, T., Gardner, R., Berger, F., Feijo, J. A., Becker, J. D., and Martienssen, R. A. (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA Cell 151, 194-205
26. Ibarra, C. A., Feng, X., Schoft, V. K., Hsieh, T. F., Uzawa, R., Rodrigues, J. A., Zemach, A., Chumak, N., Machlicova, A., Nishimura, T., Rojas, D., Fischer, R. L., Tamaru, H., and Zilberman, D. (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes Science 337, 1360-1364
27. Zilberman, D., Gehring, M., Tran, R. K., Ballinger, T., and Henikoff, S. (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription Nat. Genet. 39, 61-69
28. Zhang, X., Yazaki, J., Sundaresan, A., Cokus, S., Chan, S. W., Chen, H., Henderson, I. R., Shinn, P., Pellegrini, M., Jacobsen, S. E., and Ecker, J. R. (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis Cell 126, 1189-1201
29. Gong, Z., Morales-Ruiz, T., Ariza, R. R., Roldan-Arjona, T., David, L., and Zhu, J. K. (2002) ROS1, a repressor of transcriptional gene silencing in Arabidopsis, encodes a DNA glycosylase/lyase Cell 111, 803-814
30. Zhu, J., Kapoor, A., Sridhar, V. V., Agius, F., and Zhu, J. K. (2007) The DNA glycosylase/lyase ROS1 functions in pruning DNA methylation patterns in Arabidopsis Curr. Biol. 17, 54-59
31. Penterman, J., Zilberman, D., Huh, J. H., Ballinger, T., Henikoff, S., and Fischer, R. L. (2007) DNA demethylation in the Arabidopsis genome Proc. Natl. Acad. Sci. U. S. A. 104, 6752-6757
32. Penterman, J., Uzawa, R., and Fischer, R. L. (2007) Genetic interactions between DNA demethylation and methylation in Arabidopsis Plant Physiol. 145, 1549-1557
33. Ortega-Galisteo, A. P., Morales-Ruiz, T., Ariza, R. R., and Roldan-Arjona, T. (2008) Arabidopsis DEMETER-LIKE proteins DML2 and DML3 are required for appropriate distribution of DNA methylation marks Plant Mol. Biol. 67, 671-681
34. Kapazoglou, A., Drosou, V., Argiriou, A., and Tsaftaris, A. S. (2013) The study of a barley epigenetic regulator, HvDME, in seed development and under drought BMC Plant Biol. 13, 172
35. Kim, J. Y., Kwak, K. J., Jung, H. J., Lee, H. J., and Kang, H. (2010) MicroRNA402 affects seed germination of Arabidopsis thaliana under stress conditions via targeting DEMETER-LIKE Protein3 mRNA Plant Cell Physiol. 51, 1079-1083
36. Osorio, C., Wen, N., Gemini, R., Zemetra, R., von Wettstein, D., and Rustgi, S. (2012) Targeted modification of wheat grain protein to reduce the content of celiac causing epitopes Funct. Integr. Genomics 12, 417-438
37. Mitea, C., Salentijn, E. M., van Veelen, P., Goryunova, S. V., van der Meer, I. M., van den Broeck, H. C., Mujico, J. R., Montserrat, V., Gilissen, L. J., Drijfhout, J. W., Dekking, L., Koning, F., and Smulders, M. J. (2010) A universal approach to eliminate antigenic properties of alpha-gliadin peptides in celiac disease PLoS One 5, e15637
38. Qi, P. F., Wei, Y. M., Ouellet, T., Chen, Q., Tan, X., and Zheng, Y. L. (2009) The gamma-gliadin multigene family in common wheat (Triticum aestivum) and its closely related species BMC Genomics 10, 168
39. Wen, S., Wen, N., Pang, J., Langen, G., Brew-Appiah, R. A., Mejias, J. H., Osorio, C., Yang, M., Gemini, R., Moehs, C. P., Zemetra, R. S., Kogel, K. H., Liu, B., Wang, X., von Wettstein, D., and Rustgi, S. (2012) Structural genes of wheat and barley 5-methylcytosine DNA glycosylases and their potential applications for human health Proc. Natl. Acad. Sci. U. S. A. 109, 20543-20548
40. Agius, F., Kapoor, A., and Zhu, J. K. (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation Proc. Natl. Acad. Sci. U. S. A. 103, 11796-11801
41. Mok, Y. G., Uzawa, R., Lee, J., Weiner, G. M., Eichman, B. F., Fischer, R. L., and Huh, J. H. (2010) Domain structure of the DEMETER 5-methylcytosine DNA glycosylase Proc. Natl. Acad. Sci. U. S. A. 107, 19225-19230
42. Ponferrada-Marin, M. I., Parrilla-Doblas, J. T., Roldan-Arjona, T., and Ariza, R. R. (2011) A discontinuous DNA glycosylase domain in a family of enzymes that excise 5-methylcytosine Nucleic Acids Res. 39, 1473-1484
43. Ponferrada-Marin, M. I., Martinez-Macias, M. I., Morales-Ruiz, T., Roldan-Arjona, T., and Ariza, R. R. (2010) Methylation-independent DNA binding modulates specificity of Repressor of Silencing 1 (ROS1) and facilitates demethylation in long substrates J. Biol. Chem. 285, 23032-23039
44. Ponferrada-Marin, M. I., Roldan-Arjona, T., and Ariza, R. R. (2009) ROS1 5-methylcytosine DNA glycosylase is a slow-turnover catalyst that initiates DNA demethylation in a distributive fashion Nucleic Acids Res. 37, 4264-4274
45. Parrilla-Doblas, J. T., Ponferrada-Marin, M. I., Roldan-Arjona, T., and Ariza, R. R. (2013) Early steps of active DNA demethylation initiated by ROS1 glycosylase require three putative helix-invading residues Nucleic Acids Res. 41, 8654-8664
46. Jang, H., Shin, H., Eichman, B. F., and Huh, J. H. Excision of 5-hydroxymethylcytosine by DEMETER family DNA glycosylases, Biochem. Biophys. Res. Commun. 2014, 10.1016/j.bbrc2014.03.060.
47. Guex, N. and Peitsch, M. C. (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18, 2714-2723
48. Fromme, J. C. and Verdine, G. L. (2003) Structure of a trapped endonuclease III-DNA covalent intermediate EMBO J. 22, 3461-3471
49. Dalhus, B., Laerdahl, J. K., Backe, P. H., and Bjoras, M. (2009) DNA base repair - recognition and initiation of catalysis FEMS Microbiol. Rev. 33, 1044-1078
50. David, S. S., O'Shea, V. L., and Kundu, S. (2007) Base-excision repair of oxidative DNA damage Nature 447, 941-950
51. Friedman, J. I. and Stivers, J. T. (2010) Detection of damaged DNA bases by DNA glycosylase enzymes Biochemistry 49, 4957-4967
52. Li, G. M. (2010) Novel molecular insights into the mechanism of GO removal by MutM Cell Res. 20, 116-118
53. Maiti, A., Michelson, A. Z., Armwood, C. J., Lee, J. K., and Drohat, A. C. (2013) Divergent mechanisms for enzymatic excision of 5-formylcytosine and 5-carboxylcytosine from DNA J. Am. Chem. Soc. 135, 15813-15822
54. Otani, J., Arita, K., Kato, T., Kinoshita, M., Kimura, H., Suetake, I., Tajima, S., Ariyoshi, M., and Shirakawa, M. (2013) Structural basis of the versatile DNA recognition ability of the methyl-CpG binding domain of methyl-CpG binding domain protein 4 J. Biol. Chem. 288, 6351-6362
55. Manvilla, B. A., Maiti, A., Begley, M. C., Toth, E. A., and Drohat, A. C. (2012) Crystal structure of human methyl-binding domain IV glycosylase bound to abasic DNA J. Mol. Biol. 420, 164-175
56. Morera, S., Grin, I., Vigouroux, A., Couve, S., Henriot, V., Saparbaev, M., and Ishchenko, A. A. (2012) Biochemical and structural characterization of the glycosylase domain of MBD4 bound to thymine and 5-hydroxymethyuracil- containing DNA Nucleic Acids Res. 40, 9917-9926
57. Banerjee, A., Santos, W. L., and Verdine, G. L. (2006) Structure of a DNA glycosylase searching for lesions Science 311, 1153-1157
58. Baldwin, M. R. and O'Brien, P. J. (2010) Nonspecific DNA binding and coordination of the first two steps of base excision repair Biochemistry 49, 7879-7891
59. Waters, T. R., Gallinari, P., Jiricny, J., and Swann, P. F. (1999) Human thymine DNA glycosylase binds to apurinic sites in DNA but is displaced by human apurinic endonuclease 1 J. Biol. Chem. 274, 67-74
60. Fitzgerald, M. E. and Drohat, A. C. (2008) Coordinating the initial steps of base excision repair. Apurinic/apyrimidinic endonuclease 1 actively stimulates thymine DNA glycosylase by disrupting the product complex J. Biol. Chem. 283, 32680-32690
61. Sidorenko, V. S., Nevinsky, G. A., and Zharkov, D. O. (2007) Mechanism of interaction between human 8-oxoguanine-DNA glycosylase and AP endonuclease DNA Repair 6, 317-328
62. Wu, H. and Zhang, Y. (2014) Reversing DNA methylation: mechanisms, genomics, and biological functions Cell 156, 45-68