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PMID: 19921333 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

CG dinucleotide periodicities recognized by the Dnmt3a-Dnmt3L complex are distinctive at retroelements and imprinted domains.

Glass JL, Fazzari MJ, Ferguson-Smith AC, Greally JM

Abstract

The Dnmt3a and Dnmt3L genes are critical mediators of cytosine methylation during gametogenesis, with major actions noted at transposable elements and imprinted loci. The Dnmt3a-Dnmt3L complex was recently described to have preferential activity at CG dinucleotides located 8-10 bp apart. Because cytosine methylation is heterogeneously distributed in the genome, we tested whether this relative sequence preference explains the effects of mutation of the Dnmt3a and Dnmt3L genes using bioinformatic analysis. We found that the human and mouse genomes are significantly enriched in a CG dinucleotide periodicity of 2 bp, leading to an increased frequency of CGs spaced 8 bp apart that represent widespread targets for this protein complex. When we broke down the human and mouse genomes by annotation, we found that this significant 2-bp periodicity and increased 8-bp periodicity are maintained in Alu SINEs in both species. The 8-bp periodicity was mapped genome-wide, identifying enrichment at the promoters of both paternally and maternally methylated imprinted genes and at CG dinucleotide-enriched sequences. We conclude that CG dinucleotide periodicity helps to explain some but not all of the relative sequence specificity of mutations of Dnmt3a or Dnmt3L in the establishment of germline cytosine methylation patterns.

MeSH Terms
Animals CpG Islands DNA (Cytosine-5-)-Methyltransferases/genetics,metabolism DNA Methylation DNA Methyltransferase 3A Dinucleotide Repeats Genomic Imprinting Humans Mice Protein Binding Retroelements
Chemicals
DNMT3A protein, human Dnmt3a protein, mouse Retroelements DNMT3L protein, human Dnmt3l protein, mouse DNA (Cytosine-5-)-Methyltransferases DNA Methyltransferase 3A
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Glass Jacob L
Department of Genetics (Computational Genetics), Albert Einstein College of Medicine, 1301 Morris Park Avenue, Bronx, NY 10461, USA.
Fazzari Melissa J
Ferguson-Smith Anne C
Greally John M
References (42)
42 references, click to expand
  1. CG dinucleotide clustering is a species-specific property of the genome.
    Nucleic Acids Res. 2007;35(20):6798-807 PMID: 17932072
  2. Maintenance DNA methylation of nucleosome core particles.
    J Biol Chem. 2004 Jan 23;279(4):2904-12 PMID: 14578347
  3. Evolutionary history of 7SL RNA-derived SINEs in Supraprimates.
    Trends Genet. 2007 Apr;23(4):158-61 PMID: 17307271
  4. Essential role for de novo DNA methyltransferase Dnmt3a in paternal and maternal imprinting.
    Nature. 2004 Jun 24;429(6994):900-3 PMID: 15215868
  5. B1 and related SINEs in mammalian genomes.
    Gene. 2003 Nov 13;319:149-60 PMID: 14597180
  6. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L.
    Nature. 2004 Sep 2;431(7004):96-9 PMID: 15318244
  7. CpNpG methylation in mammalian cells.
    Nat Genet. 1995 May;10(1):20-7 PMID: 7647784
  8. Coordinate regulation of DNA methyltransferase expression during oogenesis.
    BMC Dev Biol. 2007 Apr 19;7:36 PMID: 17445268
  9. Meiotic and epigenetic defects in Dnmt3L-knockout mouse spermatogenesis.
    Proc Natl Acad Sci U S A. 2005 Mar 15;102(11):4068-73 PMID: 15753313
  10. The distinguishing sequence characteristics of mouse imprinted genes.
    Mamm Genome. 2002 Nov;13(11):639-45 PMID: 12461650
  11. Dynamic regulation of nucleosome positioning in the human genome.
    Cell. 2008 Mar 7;132(5):887-98 PMID: 18329373
  12. CpG island methylation in human lymphocytes is highly correlated with DNA sequence, repeats, and predicted DNA structure.
    PLoS Genet. 2006 Mar;2(3):e26 PMID: 16520826
  13. CpGcluster: a distance-based algorithm for CpG-island detection.
    BMC Bioinformatics. 2006 Oct 12;7:446 PMID: 17038168
  14. Epigenetics: perceptive enzymes.
    Nature. 2007 Sep 13;449(7159):148-9 PMID: 17851501
  15. Origin and diversification of minisatellites derived from human Alu sequences.
    Gene. 2006 Jan 3;365:21-6 PMID: 16343813
  16. Cytosine methylation and the ecology of intragenomic parasites.
    Trends Genet. 1997 Aug;13(8):335-40 PMID: 9260521
  17. Short interspersed transposable elements (SINEs) are excluded from imprinted regions in the human genome.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):327-32 PMID: 11756672
  18. Large-scale analysis of the Alu Ya5 and Yb8 subfamilies and their contribution to human genomic diversity.
    J Mol Biol. 2001 Aug 3;311(1):17-40 PMID: 11469855
  19. DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA.
    Nature. 2007 Aug 9;448(7154):714-7 PMID: 17687327
  20. Epigenomics: beyond CpG islands.
    Nat Rev Genet. 2004 Jun;5(6):446-55 PMID: 15153997
  21. Alu repeated DNAs are differentially methylated in primate germ cells.
    Nucleic Acids Res. 1994 Nov 25;22(23):5121-7 PMID: 7800508
  22. Comprehensive analysis of CpG islands in human chromosomes 21 and 22.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3740-5 PMID: 11891299
  23. Mechanisms regulating imprinted genes in clusters.
    Curr Opin Cell Biol. 2007 Jun;19(3):281-9 PMID: 17467259
  24. Structure of Dnmt3a bound to Dnmt3L suggests a model for de novo DNA methylation.
    Nature. 2007 Sep 13;449(7159):248-51 PMID: 17713477
  25. CpG mutation rates in the human genome are highly dependent on local GC content.
    Mol Biol Evol. 2005 Mar;22(3):650-8 PMID: 15537806
  26. DNA binding selectivity of MeCP2 due to a requirement for A/T sequences adjacent to methyl-CpG.
    Mol Cell. 2005 Sep 2;19(5):667-78 PMID: 16137622
  27. CpG island mapping by epigenome prediction.
    PLoS Comput Biol. 2007 Jun;3(6):e110 PMID: 17559301
  28. A genome-wide analysis of CpG dinucleotides in the human genome distinguishes two distinct classes of promoters.
    Proc Natl Acad Sci U S A. 2006 Jan 31;103(5):1412-7 PMID: 16432200
  29. Mutagenic deamination of cytosine residues in DNA.
    Nature. 1980 Oct 9;287(5782):560-1 PMID: 6999365
  30. Genomewide demarcation of RNA polymerase II transcription units revealed by physical fractionation of chromatin.
    Proc Natl Acad Sci U S A. 2003 May 27;100(11):6364-9 PMID: 12750471
  31. Role of the Dnmt3 family in de novo methylation of imprinted and repetitive sequences during male germ cell development in the mouse.
    Hum Mol Genet. 2007 Oct 1;16(19):2272-80 PMID: 17616512
  32. Cell type-specific methylation profiles occurring disproportionately in CpG-less regions that delineate developmental similarity.
    Genes Cells. 2007 Oct;12(10):1123-32 PMID: 17903172
  33. CpG methylation is targeted to transcription units in an invertebrate genome.
    Genome Res. 2007 May;17(5):625-31 PMID: 17420183
  34. CpG islands in vertebrate genomes.
    J Mol Biol. 1987 Jul 20;196(2):261-82 PMID: 3656447
  35. Distribution, silencing potential and evolutionary impact of promoter DNA methylation in the human genome.
    Nat Genet. 2007 Apr;39(4):457-66 PMID: 17334365
  36. Initial sequencing and analysis of the human genome.
    Nature. 2001 Feb 15;409(6822):860-921 PMID: 11237011
  37. Genome-scale mapping of DNase I sensitivity in vivo using tiling DNA microarrays.
    Nat Methods. 2006 Jul;3(7):511-8 PMID: 16791208
  38. KDM1B is a histone H3K4 demethylase required to establish maternal genomic imprints.
    Nature. 2009 Sep 17;461(7262):415-8 PMID: 19727073
  39. Dnmt3L and the establishment of maternal genomic imprints.
    Science. 2001 Dec 21;294(5551):2536-9 PMID: 11719692
  40. Comparative isoschizomer profiling of cytosine methylation: the HELP assay.
    Genome Res. 2006 Aug;16(8):1046-55 PMID: 16809668
  41. A novel approach for identifying candidate imprinted genes through sequence analysis of imprinted and control genes.
    Hum Genet. 2002 Dec;111(6):511-20 PMID: 12436242
  42. Genome-wide prediction of imprinted murine genes.
    Genome Res. 2005 Jun;15(6):875-84 PMID: 15930497
Article Info
Journal
Mammalian genome : official journal of the International Mammalian Genome Society
Abbr.
Mamm Genome
ISSN
1432-1777
Published
2009-00-00
Epub
2009-00-17
Pages
633-43
Language
English
Region
United States
NLM ID
9100916
Subset
IM
Grants
NHGRI NIH HHS · R01 HG004401 · United States
Wellcome Trust · United Kingdom
NIGMS NIH HHS · GM007288 · United States
Medical Research Council · G9723500 · United Kingdom
NICHD NIH HHS · R01 HD044078 · United States
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