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 and Development

Volumn 25, Issue 2, 2011, Pages 137-152

  Rajakumara, Eerappa ^a   Law, Julie A ^b   Simanshu, Dhirendra K ^a   Voigt, Philipp ^c   Johnson, Lianna M ^b   Reinberg, Danny ^c   Patel, Dinshaw J ^a   Jacobsen, Steven E ^b  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5mC binding pocket; DNA methylation; Dual base flip out; Epigenetics; H3K9 methylation; SET domain

Indexed keywords

DNA;

ARABIDOPSIS; ARTICLE; CALORIMETRY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DEMETHYLATION; DNA BINDING; DNA METHYLATION; GEL MOBILITY SHIFT ASSAY; GENE MUTATION; IN VIVO STUDY; MOLECULAR RECOGNITION; NONHUMAN; PLANT GENE; PRIORITY JOURNAL;

5-METHYLCYTOSINE; ARABIDOPSIS; CALORIMETRY; DNA; DNA METHYLATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HISTONES; METHYLTRANSFERASES; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

ARABIDOPSIS; EUKARYOTA; MAMMALIA;

EID: 78651515883     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1980311     Document Type: Article

References (38)

1. Arita K, Ariyoshi M, Tochio H, Nakamura Y, Shirakawa M. 2008. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455: 818-821.
2. Avvakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, Arrowsmith CH, Dhe-Paganon S. 2008. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455: 822-825.
3. Bernatavichute YV, Zhang X, Cokus S, Pellegrini M, Jacobsen SE. 2008. Genome-wide association of histone H3 lysine nine methylation with CHG DNA methylation in Arabidopsis thaliana. PLoS One 3: e3156. doi: 10.1371/journal.pone.0003156.
4. Bostick M, Kim JK, Esteve PO, Clark A, Pradhan S, Jacobsen SE. 2007. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science 317: 1760-1764.
5. Cheng X, Blumenthal RM. 2008. Mammalian DNA methyltransferases: A structural perspective. Structure 16: 341-350.
6. Ebbs ML, Bender J. 2006. Locus-specific control of DNA methylation by the Arabidopsis SUVH5 histone methyltransferase. Plant Cell 18: 1166-1176.
7. Ebbs ML, Bartee L, Bender J. 2005. H3 lysine 9 methylation is maintained on a transcribed inverted repeat by combined action of SUVH6 and SUVH4 methyltransferases. Mol Cell Biol 25: 10507-10515.
8. Ehrlich M, Gama-Sosa MA, Huang LH, Midgett RM, Kuo KC, McCune RA, Gehrke C. 1982. Amount and distribution of 5-methylcytosine in human DNA from different types of tissues of cells. Nucleic Acids Res 10: 2709-2721.
9. Feng S, Cokus SJ, Zhang X, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, et al. 2010. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci 107: 8689-8694.
10. Goll MG, Bestor TH. 2005. Eukaryotic cytosine methyltransferases. Annu Rev Biochem 74: 481-514.
11. Hashimoto H, Horton JR, Zhang X, Bostick M, Jacobsen SE, Cheng X. 2008. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455: 826-829.
12. Henderson IR, Jacobsen SE. 2007. Epigenetic inheritance in plants. Nature 447: 418-424.
13. Ho KL, McNae IW, Schmiedeberg L, Klose RJ, Bird AP, Walkinshaw MD. 2008. MeCP2 binding to DNA depends upon hydration at methyl-CpG. Mol Cell 29: 525-531.
14. Huffman JL, Sundheim O, Tainer JA. 2005. DNA base damage recognition and removal: New twists and grooves. Mutat Res 577: 55-76.
15. Jackson JP, Lindroth AM, Cao X, Jacobsen SE. 2002. Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416: 556-560.
16. Jackson JP, Johnson L, Jasencakova Z, Zhang X, PerezBurgos L, Singh PB, Cheng X, Schubert I, Jenuwein T, Jacobsen SE. 2004. Dimethylation of histone H3 lysine 9 is a critical mark for DNA methylation and gene silencing in Arabidopsis thaliana. Chromosoma 112: 308-315.
17. Jasencakova Z, Soppe WJ, Meister A, Gernand D, Turner BM, Schubert I. 2003. Histone modifications in Arabidopsis - High methylation of H3 lysine 9 is dispensable for constitutive heterochromatin. Plant J 33: 471-480.
18. Johnson L, Cao X, Jacobsen S. 2002. Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr Biol 12: 1360-1367.
19. Johnson LM, Bostick M, Zhang X, Kraft E, Henderson I, Callis J, Jacobsen SE. 2007. The SRA methyl-cytosine-binding domain links DNA and histone methylation. Curr Biol 17: 379-384.
20. Johnson LM, Law JA, Khattar A, Henderson IR, Jacobsen SE. 2008. SRA-domain proteins required for DRM2-mediated de novo DNA methylation. PLoS Genet 4: e1000280. doi: 10.1371/journal.pgen.1000280.
21. Kim JK, Samaranayake M, Pradhan S. 2009. Epigenetic mechanisms in mammals. Cell Mol Life Sci 66: 596-612.
22. Klimasauskas S, Roberts RJ. 1995. M.HhaI binds tightly to substrates containing mismatches at the target base. Nucleic Acids Res 23: 1388-1395.
23. Klimasauskas S, Kumar S, Roberts RJ, Cheng X. 1994. HhaI methyltransferase flips its target base out of the DNA helix. Cell 76: 357-369. (Pubitemid 24046697)
24. Kraft E, Bostick M, Jacobsen SE, Callis J. 2008. ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J 56: 704-715.
25. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-220.
26. Li CF, Pontes O, El-Shami M, Henderson IR, Bernatavichute YV, Chan SW, Lagrange T, Pikaard CS, Jacobsen SE. 2006. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana. Cell 126: 93-106.
27. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. 2009. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462: 315-322.
28. Malagnac F, Bartee L, Bender J. 2002. An Arabidopsis SET domain protein required for maintenance but not establishment of DNA methylation. EMBO J 21: 6842-6852.
29. Min JH, Pavletich NP. 2007. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449: 570-575.
30. O'Gara M, Horton JR, Roberts RJ, Cheng X. 1998. Structures of HhaI methyltransferase complexed with substrates containing mismatches at the target base. Nat Struct Biol 5: 872-877.
31. Ohki I, Shimotake N, Fujita N, Jee J, Ikegami T, Nakao M, Shirakawa M. 2001. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell 105: 487-497.
32. Phillips K, Luisi B. 2000. The virtuoso of versatility: POU proteins that flex to fit. J Mol Biol 302: 1023-1039.
33. Qian C, Li S, Jakoncic J, Zeng L, Walsh MJ, Zhou MM. 2008. Structure and hemimethylated CpG binding of the SRA domain from human UHRF1. J Biol Chem 283: 34490-34494.
34. Reinisch KM, Chen L, Verdine GL, Lipscomb WN. 1995. The crystal structure of HaeIII methyltransferase convalently complexed to DNA: An extrahelical cytosine and rearranged base pairing. Cell 82: 143-153.
35. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, Shinga J, Mizutani-Koseki Y, Toyoda T, Okamura K, et al. 2007. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature 450: 908-912.
36. Woo HR, Pontes O, Pikaard CS, Richards EJ. 2007. VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev 21: 267-277.
37. Woo HR, Dittmer TA, Richards EJ. 2008. Three SRA-domain methylcytosine-binding proteins cooperate to maintain global CpG methylation and epigenetic silencing in Arabidopsis. PLoS Genet 4: e1000156. doi: 10.1371/journal.pgen.1000156.
38. Zhang X, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, et al. 2006. Genome-wide high-resolution mapping and functional analysis of DNA methylation in arabidopsis. Cell 126: 1189-1201.