Demethylation initiated by ROS1 glycosylase involves random sliding along DNA

Nucleic Acids Research

Volumn 40, Issue 22, 2012, Pages 11554-11562

  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

AMINO TERMINAL TELOPEPTIDE; DNA GLYCOSYLASE ROS1; DNA GLYCOSYLTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; DISSOCIATION; DNA METHYLATION; ENZYME ACTIVITY; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TARGETING;

5-METHYLCYTOSINE; BASE PAIR MISMATCH; DIFFUSION; DNA; DNA GLYCOSYLASES; PROTEIN STRUCTURE, TERTIARY;

EID: 84871236510     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks894     Document Type: Article

References (41)

1. Klose, R. J. and Bird, A. P. (2006) Genomic DNA methylation: the mark and its mediators. Trends Biochem. Sci., 31, 89-97.
2. Jones, P. A. (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet., 13, 484-492.
3. Zilberman, D. (2008) The evolving functions of DNA methylation. Curr. Opin. Plant Biol., 11, 554-559.
4. Esteller, M. (2007) Cancer epigenomics: DNA methylomes and histone-modification maps. Nat. Rev. Genet., 8, 286-298.
5. Robertson, K. D. (2005) DNA methylation and human disease. Nat. Rev. Genet., 6, 597-610.
6. Goll, M. G. and Bestor, T. H. (2005) Eukaryotic cytosine methyltransferases. Annu. Rev. Biochem., 74, 481-514.
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. 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.
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. 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.
11. 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.
12. Bhutani, N., Burns, D. M. and Blau, H. M. (2011) DNA demethylation dynamics. Cell, 146, 866-872.
13. 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.
14. Martinez-Macias, M. I., Qian, W., Miki, D., Pontes, O., Liu, Y., Tang, K., Liu, R., Morales-Ruiz, T., Ariza, R. R., Roldan-Arjona, T. et al. (2012) A DNA 3' phosphatase functions in active DNA demethylation in Arabidopsis. Mol. Cell, 45, 357-370.
15. 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.
16. 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.
17. 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.
18. 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.
19. Denver, D. R., Swenson, S. L. and Lynch, M. (2003) An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases. Mol. Biol. Evol., 20, 1603-1611.
20. 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.
21. 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.
22. von Hippel, P. H. and Berg, O. G. (1989) Facilitated target location in biological systems. J. Biol. Chem., 264, 675-678.
23. Loverdo, C., Benichou, O., Voituriez, R., Biebricher, A., Bonnet, I. and Desbiolles, P. (2009) Quantifying hopping and jumping in facilitated diffusion of DNA-binding proteins. Phys. Rev. Lett., 102, 188101.
24. Jeltsch, A., Wenz, C., Stahl, F. and Pingoud, A. (1996) Linear diffusion of the restriction endonuclease EcoRV on DNA is essential for the in vivo function of the enzyme. EMBO J., 15, 5104-5111.
25. Jeltsch, A. (2006) On the enzymatic properties of Dnmt1: specificity, processivity, mechanism of linear diffusion and allosteric regulation of the enzyme. Epigenetics, 1, 63-66.
26. Lloyd, R. S. (2005) Investigations of pyrimidine dimer glycosylases-a paradigm for DNA base excision repair enzymology. Mutat. Res., 577, 77-91.
27. Porecha, R. H. and Stivers, J. T. (2008) Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils. Proc. Natl Acad. Sci. USA, 105, 10791-10796.
28. Blainey, P. C., van Oijen, A. M., Banerjee, A., Verdine, G. L. and Xie, X. S. (2006) A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc. Natl Acad. Sci. USA, 103, 5752-5757.
29. 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.
30. Kampmann, M. (2004) Obstacle bypass in protein motion along DNA by two-dimensional rather than one-dimensional sliding. J. Biol. Chem., 279, 38715-38720.
31. 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.
32. 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.
33. Antao, V. P. and Tinoco, I. Jr (1992) Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res., 20, 819-824.
34. McKinney, K., Mattia, M., Gottifredi, V. and Prives, C. (2004) p53 linear diffusion along DNA requires its C terminus. Mol. Cell, 16, 413-424.
35. Randell, J. C. and Coen, D. M. (2001) Linear diffusion on DNA despite high-affinity binding by a DNA polymerase processivity factor. Mol. Cell, 8, 911-920.
36. Gurland, J. and Tripathi, R. C. (1971) A simple approximation for unbiased estimation of the standard deviation. Am. Stat., 25, 30-32.
37. Zharkov, D. O. and Grollman, A. P. (2005) The DNA trackwalkers: principles of lesion search and recognition by DNA glycosylases. Mutat. Res., 577, 24-54.
38. Vuzman, D. and Levy, Y. (2010) DNA search efficiency is modulated by charge composition and distribution in the intrinsically disordered tail. Proc. Natl Acad. Sci. USA, 107, 21004-21009.
39. Halford, S. E. (2009) An end to 40 years of mistakes in DNA-protein association kinetics? Biochem. Soc. Trans., 37, 343-348.
40. Zaika, E. I., Perlow, R. A., Matz, E., Broyde, S., Gilboa, R., Grollman, A. P. and Zharkov, D. O. (2004) Substrate discrimination by formamidopyrimidine- DNA glycosylase: a mutational analysis. J. Biol. Chem., 279, 4849-4861.
41. Friedman, J. I. and Stivers, J. T. (2010) Detection of damaged DNA bases by DNA glycosylase enzymes. Biochemistry, 49, 4957-4967.