Early steps of active DNA demethylation initiated by ROS1 glycosylase require three putative helix-invading residues

Nucleic Acids Research

Volumn 41, Issue 18, 2013, Pages 8654-8664

  Parrilla Doblas, Jara Teresa ^a   Ponferrada Marín, María Isabel ^a   Roldán Arjona, Teresa ^a   Ariza, Rafael R ^a  

^a UNIVERSITY OF CÓRDOBA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DNA; DNA GLYCOSYLTRANSFERASE; GUANINE; PEPTIDES AND PROTEINS; PROTEIN M905G; PROTEIN Q607A; PROTEIN R903A; PROTEIN ROS1; UNCLASSIFIED DRUG;

ARTICLE; BASE MISPAIRING; BASE PAIRING; CONTROLLED STUDY; DEMETHYLATION; DNA DEMETHYLATION; DNA HELIX; DNA METHYLATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; HUMAN; INTERCALATION COMPLEX; MOLECULAR RECOGNITION; MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN MODIFICATION;

5-METHYLCYTOSINE; AMINO ACID SEQUENCE; ARABIDOPSIS PROTEINS; BASE PAIRING; DNA; DNA GLYCOSYLASES; DNA METHYLATION; DNA-BINDING PROTEINS; GUANINE; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; NUCLEAR PROTEINS; SEQUENCE ALIGNMENT;

EID: 84885906394     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt625     Document Type: Article

References (48)

1. Zilberman, D. (2008) The evolving functions of DNA methylation. Curr. Opin. Plant Biol., 11, 554-559.
2. Roldan-Arjona, T. and Ariza, R.R. (2009) In: Grosjean, H. (ed.), DNA and RNA modification Enzymes: Comparative Structure, Mechanism, Functions, Cellular Interactions and Evolution. Landes Bioscience, Austin, TX, pp. 149-161.
3. Wu, S.C. and Zhang, Y. (2010) Active DNA demethylation: many roads lead to Rome. Nat. Rev. Mol. Cell Biol., 11, 607-620.
4. Zhu, J.K. (2009) Active DNA demethylation mediated by DNA glycosylases. Annu. Rev. Genet., 43, 143-166.
5. Bhutani, N., Burns, D.M. and Blau, H.M. (2011) DNA demethylation dynamics. Cell, 146, 866-872.
6. Gong, Z. and Zhu, J.K. (2011) Active DNA demethylation by oxidation and repair. Cell Res., 21, 1649-1651.
7. 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.
8. 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. USA, 103, 6853-6858.
9. 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. USA, 103, 11796-11801.
10. 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.
11. 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. USA, 104, 6752-6757.
12. 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.
13. 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.
14. 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 selfimprinting by allele-specific demethylation. Cell, 124, 495-506.
15. 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. et al. (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell, 151, 194-205.
16. Ibarra, C.A., Feng, X., Schoft, V.K., Hsieh, T.F., Uzawa, R., Rodrigues, J.A., Zemach, A., Chumak, N., Machlicova, A., Nishimura, T. et al. (2012) Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science, 337, 1360-1364.
17. Mart́nez-Maćas, M.I., Qian, W., Miki, D., Pontes, O., Liu, Y., Tang, K., Liu, R., Morales-Ruiz, T., Ariza, R.R., Roldán-Arjona, T. et al. (2012) A DNA 30 phosphatase functions in active DNA demethylation in Arabidopsis. Mol. Cell, 45, 357-370.
18. Martinez-Maćas, M.I., Cordoba-Can? ero, D., Ariza, R.R. and Roldan-Arjona, T. (2013) The DNA repair protein XRCC1 functions in the plant DNA demethylation pathway by stimulating cytosine methylation (5-meC) excision, gap tailoring, and DNA ligation. J. Biol. Chem., 288, 5496-5505.
19. Nash, H.M., Bruner, S.D., Scharer, O.D., Kawate, T., Addona, T.A., Spooner, E., Lane, W.S. and Verdine, G.L. (1996) Cloning of a yeast 8-oxoguanine DNA glycosylase reveals the existence of a base-excision DNA-repair protein superfamily. Curr. Biol., 6, 968-980.
20. Ponferrada-Maŕn, M.I., Parrilla-Doblas, J.T., Roldá n-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.
21. Ponferrada-Maŕn, M.I., Mart́nez-Maćas, M.I., Morales-Ruiz, T., Roldá n-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.
22. Ponferrada-Maŕn, M.I., Roldá n-Arjona, T. and Ariza, R.R. (2012) Demethylation initiated by ROS1 glycosylase involves random sliding along DNA. Nucleic Acids Res., 40, 11554-11562.
23. 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.
24. 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.
25. 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.
26. Ponferrada-Maŕn, M.I., Roldán-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.
27. Hardeland, U., Bentele, M., Jiricny, J. and Schar, P. (2000) Separating substrate recognition from base hydrolysis in human thymine DNA glycosylase by mutational analysis. J. Biol. Chem., 275, 33449-33456.
28. Fromme, J.C. and Verdine, G.L. (2003) Structure of a trapped endonuclease III-DNA covalent intermediate. EMBO J., 22, 3461-3471.
29. Pope, M.A. and David, S.S. (2005) DNA damage recognition and repair by the murine MutY homologue. DNA Repair (Amst), 4, 91-102.
30. Dalhus, B., Forsbring, M., Helle, I.H., Vik, E.S., Forstrom, R.J., Backe, P.H., Alseth, I. and Bjoras, M. (2011) Separation-of-function mutants unravel the dual-reaction mode of human 8-oxoguanine DNA glycosylase. Structure, 19, 117-127.
31. Sung, R.J., Zhang, M., Qi, Y. and Verdine, G.L. (2013) Structural and biochemical analysis of DNA helix-invasion by the bacterial 8-oxoguanine DNA glycosylase MutM. J. Biol. Chem., 288, 10012-10023.
32. Francis, A.W., Helquist, S.A., Kool, E.T. and David, S.S. (2003) Probing the requirements for recognition and catalysis in Fpg and MutY with nonpolar adenine isosteres. J. Am. Chem. Soc., 125, 16235-16242.
33. Krosky, D.J., Song, F. and Stivers, J.T. (2005) The origins of highaffinity enzyme binding to an extrahelical DNA base. Biochemistry, 44, 5949-5959.
34. Vallur, A.C., Feller, J.A., Abner, C.W., Tran, R.K. and Bloom, L.B. (2002) Effects of hydrogen bonding within a damaged base pair on the activity of wild type and DNA-intercalating mutants of human alkyladenine DNA glycosylase. J. Biol. Chem., 277, 31673-31678.
35. Cao, C., Jiang, Y.L., Stivers, J.T. and Song, F. (2004) Dynamic opening of DNA during the enzymatic search for a damaged base. Nat. Struct. Mol. Biol., 11, 1230-1236.
36. Maiti, A., Morgan, M.T. and Drohat, A.C. (2009) Role of two strictly conserved residues in nucleotide flipping and N-glycosylic bond cleavage by human thymine DNA glycosylase. J. Biol. Chem., 284, 36680-36688.
37. Slupphaug, G., Mol, C.D., Kavli, B., Arvai, A.S., Krokan, H.E. and Tainer, J.A. (1996) A nucleotide-flipping mechanism from the structure of human uracil-DNA glycosylase bound to DNA. Nature, 384, 87-92.
38. Banerjee, A., Santos, W.L. and Verdine, G.L. (2006) Structure of a DNA glycosylase searching for lesions. Science, 311, 1153-1157.
39. Qi, Y., Spong, M.C., Nam, K., Banerjee, A., Jiralerspong, S., Karplus, M. and Verdine, G.L. (2009) Encounter and extrusion of an intrahelical lesion by a DNA repair enzyme. Nature, 462, 762-766.
40. Dunn, A.R., Kad, N.M., Nelson, S.R., Warshaw, D.M. and Wallace, S.S. (2011) Single Qdot-labeled glycosylase molecules use a wedge amino acid to probe for lesions while scanning along DNA. Nucleic Acids Res., 39, 7487-7498.
41. Qi, Y., Nam, K., Spong, M.C., Banerjee, A., Sung, R.J., Zhang, M., Karplus, M. and Verdine, G.L. (2012) Strandwise translocation of a DNA glycosylase on undamaged DNA. Proc. Natl Acad. Sci. USA, 109, 1086-1091.
42. Qi, Y., Spong, M.C., Nam, K., Karplus, M. and Verdine, G.L. (2010) Entrapment and structure of an extrahelical guanine attempting to enter the active site of a bacterial DNA glycosylase, MutM. J. Biol. Chem., 285, 1468-1478.
43. Verdine, G.L. and Bruner, S.D. (1997) How do DNA repair proteins locate damaged bases in the genome? Chem. Biol., 4, 329-334.
44. Mirau, P.A. and Kearns, D.R. (1984) Effect of environment, conformation, sequence and base substituents on the imino proton exchange rates in guanine and inosine-containing DNA, RNA, and DNA-RNA duplexes. J. Mol. Biol., 177, 207-227.
45. Derreumaux, S., Chaoui, M., Tevanian, G. and Fermandjian, S. (2001) Impact of CpG methylation on structure, dynamics and solvation of cAMP DNA responsive element. Nucleic Acids Res., 29, 2314-2326.
46. Sukackaite, R., Grazulis, S., Tamulaitis, G. and Siksnys, V. (2012) The recognition domain of the methyl-specific endonuclease McrBC flips out 5-methylcytosine. Nucleic Acids Res., 40, 7552-7562.
47. Hashimoto, H., Horton, J.R., Zhang, X., Bostick, M., Jacobsen, S.E. and Cheng, X. (2008) The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature, 455, 826-829.
48. Rajakumara, E., Law, J.A., Simanshu, D.K., Voigt, P., Johnson, L.M., Reinberg, D., Patel, D.J. and Jacobsen, S.E. (2011) A dual flip-out mechanism for 5mC recognition by the Arabidopsis SUVH5 SRA domain and its impact on DNA methylation and H3K9 dimethylation in vivo. Genes Dev., 25, 137-152.