Dual functions of the RFTS domain of dnmt1 in replication-coupled DNA methylation and in protection of the genome from aberrant methylation

PLoS ONE

Volumn 10, Issue 9, 2015, Pages

  Garvilles, Ronald Garingalao ^a   Hasegawa, Takashi ^a   Kimura, Hironobu ^a   Sharif, Jafar ^b   Muto, Masahiro ^b   Koseki, Haruhiko ^b   Takahashi, Saori ^a   Suetake, Isao ^a,c   Tajima, Shoji ^a  

^a OSAKA UNIVERSITY   (Japan)

^b RIKEN   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLINE; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA METHYLATION; DNA REPLICATION; EMBRYO; EMBRYONIC STEM CELL; GENE; GENOME; KCNQ1OT1 GENE; MOUSE; NONHUMAN; PEG3 GENE; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RASGRF1 GENE; REPLICATION FOCI TARGETING SEQUENCE DOMAIN; STRUCTURE ACTIVITY RELATION; WILD TYPE; ANIMAL; BINDING SITE; CELL CULTURE; GENE DELETION; GENETICS; GENOME IMPRINTING; METABOLISM; MOUSE EMBRYONIC STEM CELL; PROTEIN TERTIARY STRUCTURE;

ANIMALS; BINDING SITES; CELLS, CULTURED; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA REPLICATION; GENE DELETION; GENOMIC IMPRINTING; MICE; MOUSE EMBRYONIC STEM CELLS; PROTEIN STRUCTURE, TERTIARY;

EID: 84946599736     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0137509     Document Type: Article

References (55)

1. Okano M, Xie S, Li E. Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet. 1998; 19: 219-220. PMID: 9662389
2. Aoki A, Suetake I, Miyagawa J, Fujio T, Chijiwa T, Sasaki H, et al. Enzymatic properties of de novo-type mouse DNA (cytosine-5) methyltransferases. Nucl Acids Res. 2001; 29: 3506-3512. PMID: 11522819
3. Goll MG, Bestor TH. Eukaryotic cytosine methyltransferases. Annu Rev Biochem. 2005; 74: 481-514. PMID: 15952895
4. Vilkaitis G, Suetake I, Klimasauskas S, Tajima S. Processive methylation of hemimethylated CpG sites by mouse Dnmt1 DNA methyltransferase. J Biol Chem. 2005; 280: 63-72.
5. Suetake I, Hayata D, Tajima S. The amino-terminus of mouse DNA methyltransferase 1 forms an independent domain and binds to DNA with the sequence involving PCNA binding motif. J Biochem. 2006; 140: 763-776. PMID: 17046852
6. Rountree MR, Bachman KE, Baylin SB. DNMT1 binds HDAC2 and a new co-repressor, DMAP1, to form a complex at replication foci. Nat Genet. 2000; 25: 269-277. PMID: 10888872
7. Kim GD, Ni J, Kelesoglu N, Roberts RJ, Pradhan S. Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J. 2002; 21: 4183-4195. PMID: 12145218
8. Pradhan S, Kim GD. The retinoblastoma gene product interacts with maintenance human DNA (cytosine- 5) methyltransferase and modulates its activity. EMBO J. 2002; 21: 779-788. PMID: 11847125
9. Chuang L, Ian HI, Koh TW, Ng HH, Xu G, Li BF. Human DNA-(Cytosine-5) methyltransferase-PCNA complex as a target for p21WAF1. Science. 1997; 277: 1996-2000. PMID: 9302295
10. Kameshita I, Sekiguchi M, Hamasaki D, Sugiyama Y, Hatano N, Suetake I, et al. Cyclin-dependent kinase-like 5 binds and phosphorylates DNA methyltransferase 1. Biochem Biophys Res Commun. 2008; 377: 1162-1167. doi: 10.1016/j.bbrc.2008.10.113 PMID: 18977197
11. Sugiyama Y, Hatano N, Sueyoshi N, Suetake I, Tajima S, Kinoshita E, et al. The DNA-binding activity of mouse DNA methyltransferase 1 is regulated by phosphorylation with casein kinase 1δ/ε. Biochem J. 2010; 427: 489-497. doi: 10.1042/BJ20091856 PMID: 20192920
12. Takeshita K, Suetake I, Yamashita E, Suga M, Narita H, Nakagawa A, et al. Structural insight into maintenance methylation by mouse DNA methyltransferase 1 (Dnmt1). Proc Natl Acad Sci USA. 2011; 108: 9055-9059. doi: 10.1073/pnas.1019629108 PMID: 21518897
13. Berkyurek AC, Suetake I, Arita K, Takeshita K, Nakagawa A, Shirakawa M, et al. The DNA methyltransferase Dnmt1 directly interacts with the SET and RING finger associated (SRA) domain of the multifunctional protein Uhrf1 to facilitate accession of the catalytic center to hemi-methylated DNA. J Biol Chem. 2014; 289: 379-386. doi: 10.1074/jbc.M113.523209 PMID: 24253042
14. Song J, Rechkoblit O, Bestor TH, Patel DJ. Structure of DNMT1-DNA complex reveals a role for autoinhibition in maintenance DNA methylation. Science. 2011; 331: 1036-1040. doi: 10.1126/science. 1195380 PMID: 21163962
15. Song J, Teplova M, Ishibe-Murakami S, Patel DJ. Structure-based mechanistic insights into DNMT1- mediated maintenance methylation. Science. 2012; 335: 709-712. doi: 10.1126/science.1214453 PMID: 22323818
16. Leonhardt H, Page AW, Weier HU, Bestor TH. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell. 1992; 71: 865-873. PMID: 1423634
17. Klein CJ, Botuyan MV, Wu Y, Ward CJ, Nicholson GA, Hammans S, et al. Mutations in DNMT1 cause hereditary sensory neuropathy with dementia and hearing loss. Nat Genet. 2011; 43: 595-600. doi: 10. 1038/ng.830 PMID: 21532572
18. Winkelmann J, Lin L, Schormair B, Kornum BR, Faraco J, Plazzi G, et al. Mutations in DNMT1 cause autosomal dominant cerebellar ataxia, deafness and narcolepsy. Hum Mol Genet. 2012; 21: 2205-2210. doi: 10.1093/hmg/dds035 PMID: 22328086
19. Bostick M, Kim JK, Estève PO, Clark A, Pradhan S, Jacobsen SE. UHRF1 plays a role in maintaining DNA methylation in mammalian cells. Science. 2007; 317: 1760-1764. PMID: 17673620
20. Sharif J, Muto M, Takebayashi S, Suetake I, Iwamatsu A, Endo TA, et al. The SRA protein Np95 mediates epigenetic inheritance by recruiting Dnmt1 to methylated DNA. Nature. 2007; 450: 908-913. PMID: 17994007
21. Arita K, Ariyoshi M, Tochio H, Nakamura Y, Shirakawa M. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base flipping mechanism. Nature. 2008; 455: 818-822. doi: 10.1038/ nature07249 PMID: 18772891
22. Awakumov GV, Walker JR, Xue S, Li Y, Duan S, Bronner C, et al. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature. 2008; 455: 822-826. doi: 10. 1038/nature07273 PMID: 18772889
23. Hashimoto H, Horton JR, Zhang X, Bostick M, Jacobsen SE, Cheng X. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature. 2008; 455: 826-830. doi: 10.1038/nature07280 PMID: 18772888
24. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, et al. The tandem affinity purification (TAP) method: A general procedure of protein complex purification. Methods. 2001; 24: 218-229. PMID: 11403571
25. Sanger F, Nicklen S, Coulson AR. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA. 1977; 74: 5463-5467. PMID: 271968
26. Jackson-Grusby L, Beard C, Possemato R, Tudor M, Fambrough D, Csankovszki G, et al. Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat Genet. 2001; 27: 31-39. PMID: 11137995
27. Tsumura A, Hayakawa T, Kumaki Y, Takebayashi S, Sakaue M, Matsuoka C, et al. Maintenance of self-renewal ability of mouse embryonic stem cells in the absence of DNA methyltransferases Dnmt1, Dnmt3a and Dnmt3b. Genes Cells. 2006; 11: 805-814. PMID: 16824199
28. Matsui T, Leung D, Miyashita H, Maksakova IA, Miyachi H, Kimura H, et al. Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature. 2010; 464: 927-931. doi: 10. 1038/nature08858 PMID: 20164836
29. Sambrook J, Russell DW. Molecular Cloning, A Laboratory Manual. 3rd edition. New York: Cold Spring Harbor Laboratory Press; 2001.
30. Brown T. Dot and slot blotting of DNA. Curr Protoc Mol Biol. 2001 May Chapter2: Unit2. 9B. 10.1002/ 0471142727.mb0209bs21.
31. Harland RM. In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 1991; 36: 685-695. PMID: 1811161
32. Ohki I, Shimotake N, Fujita N, Jee J, Ikegami T, Nakao M, et al. Solution structure of the methyl-CpG binding domain of human MBD1 in complex with methylated DNA. Cell. 2001; 105: 487-497. PMID: 11371345
33. Morita S, Takahashi RU, Yamashita R, Toyoda A, Horii T, Kimura M, et al. Genome-wide analysis of DNA methylation and expression of microRNA in breast cancer cells. Int J Mol Sci. 2012; 13: 8259-8272. doi: 10.3390/ijms13078259 PMID: 22942701
34. Taiwo O, Wilson GA, Morris T, Seisenberger S, Reik W, Pearce D, et al. Methylome analysis using MeDIP-seq with low DNA concentrations. Nat Protoc. 2012; 7: 617-636. doi: 10.1038/nprot.2012.012 PMID: 22402632
35. Tomizawa S, Kobayashi H, Watanabe T, Andrews S, Hata K, Kelsey G, et al. Dynamic stage-specific changes in imprinted differentially methylated regions during early mammalian development and prevalence of non-CpG methylation in oocytes. Development. 2011; 138: 811-820. doi: 10.1242/dev. 061416 PMID: 21247965
36. Kumaki Y, Oda M, Okano M. QUMA. Quantification tool for methylation analysis. Nucl Acids Res. 2008; 36: W170-175. doi: 10.1093/nar/gkn294 PMID: 18487274
37. Takagi H, Tajima S, Asano A. Overexpression of DNA methyltransferase in myoblast cells accelerates myotube formation. Eur J Biochem. 1995; 231: 282-291. PMID: 7635139
38. Bashtrykov P, Jankevicius G, Smarandache A, Jurkowska RZ, Ragozin S, Jeltsch A. Specificity of Dnmt1 for methylation of hemimethylated CpG sites resides in its catalytic domain. Chem Biol. 2012; 19: 572-578. doi: 10.1016/j.chembiol.2012.03.010 PMID: 22633409
39. Mertineit C, Yoder JA, Taketo T, Laird DW, Trasler JM, Bestor TH. Sex-specific exons control DNA methyltransferase in mammalian germ cells. Development. 1998; 125: 889-897. PMID: 9449671
40. Tucker KL, Beard C, Dausmann J, Jackson-Grusby L, Laird PW, Lei H, et al. Germ-line passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev. 1996; 10: 1008-1020. PMID: 8608936
41. Borowczyk E, Mohan KN, D'Aiuto L, Cirio MC, Chaillet JR. Identification of a region of the DNMT1 methyltransferase that regulates the maintenance of genomic imprints. Proc Natl Acad Sci USA. 2009; 106: 20806-20811. doi: 10.1073/pnas.0905668106 PMID: 19923434
42. Plass C, Shibata H, Kalcheva I, Mullins L, Kotelevtseva N, Mullins J, et al. Identification of Grf1 on mouse chromosome 9 as an imprinted gene by RLGS-M. Nat Genet. 1996; 14: 106-109. PMID: 8782830
43. Kuroiwa Y, Kaneko-Ishino T, Kagitani F, Kohda T, Li LL, Tada M, et al. Peg3 imprinted gene on proximal chromosome 7 encodes for a zinc finger protein. Nat Genet. 1996; 12: 186-190. PMID: 8563758
44. Engemann S, Strödicke M, Paulsen M, Franck O, Reinhardt R, Lane N, et al. Sequence and functional comparison in the Beckwith-Wiedemann region: implications for a novel imprinting centre and extended imprinting. Hum Mol Genet. 2000; 9: 2691-2706. PMID: 11063728
45. Takebayashi S, Tamura T, Matsuoka C, Okano M. Major and essential role for the DNA methylation mark in mouse embryogenesis and stable association of DNMT1 with newly replicated regions. Mol Cell Biol. 2007; 27: 8243-8258. PMID: 17893328
46. Iida T, Suetake I, Tajima S, Morioka H, Ohta S, Obuse C, et al. PCNA clamp facilitates action of DNA cytosine methyltransferase 1 on hemimethylated DNA. Genes Cells. 2002; 7: 997-1007. PMID: 12354094
47. Bashtrykov P, Jankevicius G, Jurkowska RZ, Ragozin S, Jeltsch A. The Uhrf1 protein stimulates the activity and specificity of the maintenance DNA methyltransferase Dnmt1 by an allosteric mechanism. J Biol Chem. 2014; 289: 4106-4115. doi: 10.1074/jbc.M113.528893 PMID: 24368767
48. Moldovan GL, Pfander B, Jentsch S. PCNA, the maestro of the replication fork. Cell. 2007; 129: 665-679. PMID: 17512402
49. Egger G, Jeong S, Escobar SG, Cortez CC, Li TW, Saito Y, et al. Identification of DNMT1 (DNA methyltransferase 1) hypomorphs in somatic knockouts suggests an essential role for DNMT1 in cell survival. Proc Natl Acad Sci USA. 2006; 103: 14080-14085. PMID: 16963560
50. Schneider K, Fuchs C, Dobay A, Rottach A, Qin W, Wolf P, et al. Dissection of cell cycle-dependent dynamics of Dnmt1 by FRAP and diffusion-modeling. Nucl Acids Res. 2013; 41: 4860-4876. doi: 10. 1093/nar/gkt191 PMID: 23535145
51. Bashtrykov P, Rajavelu A, Hackner B, Ragozin S, Carell T, Jeltsch A. Targeted mutagenesis results in an activation of DNA methyltransferase 1 and confirms an autoinhibitory role of its RFTS domain. Chembiochem. 2014; 15: 743-748. doi: 10.1002/cbic.201300740 PMID: 24532244
52. Wu BK, Mei SC, Brenner C. RFTS-deleted DNMT1 enhances tumorigenicity with focal hypermethylation and global hypomethylation. Cell Cycle. 2014; 13: 3222-3231. doi: 10.4161/15384101.2014. 950886 PMID: 25485502
53. Chen T, Ueda Y, Xie S, Li E. A novel Dnmt3a isoform produced from an alternative promoter localizes to euchromatin and its expression correlates with active de novo methylation. J Biol Chem. 2002; 277: 38746-38754. PMID: 12138111
54. Watanabe D, Suetake I, Tada T, Tajima S. Stage- and cell-specific expression of Dnmt3a and Dnmt3b during embryogenesis. Mech Dev. 2002; 118: 187-190. PMID: 12351185
55. Otani J, Kimura H, Sharif J, Endo TA, Mishima Y, Kawakami T, et al. Cell cycle-dependent turnover of 5-hydroxymethyl cytosine in mouse embryonic stem cells. PLoS One. 2013; 8: e82961. doi: 10.1371/ journal.pone.0082961 PMID: 24340069