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Molecular and Cellular Biology, August 2001, p. 5426-5436, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5426-5436.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

DNA Methylation Is Linked to Deacetylation of Histone H3, but Not H4, on the Imprinted Genes Snrpn and U2af1-rs1

Richard I. Gregory,1 Tamzin E. Randall,2 Colin A. Johnson,2 Sanjeev Khosla,1,dagger Izuho Hatada,3 Laura P. O'Neill,2 Bryan M. Turner,2,* and Robert Feil1,4,*

Programme in Developmental Genetics, The Babraham Institute, Cambridge CB2 4AT,1 and Chromatin and Gene Expression Group, University of Birmingham Medical School, Birmingham B15 2TT,2 United Kingdom; Gene Research Center, Gunma University, Maebashi 371-8511, Japan3; and Institute of Molecular Genetics, CNRS UMR-5535, IRF-24, 34293 Montpellier Cedex 5, France4

Received 19 March 2001/Returned for modification 30 April 2001/Accepted 15 May 2001

The relationship between DNA methylation and histone acetylation at the imprinted mouse genes U2af1-rs1 and Snrpn is explored by chromatin immunoprecipitation (ChIP) and resolution of parental alleles using single-strand conformational polymorphisms. The U2af1-rs1 gene lies within a differentially methylated region (DMR), while Snrpn has a 5' DMR (DMR1) with sequences homologous to the imprinting control center of the Prader-Willi/Angelman region. For both DMR1 of Snrpn and the 5' untranslated region (5'-UTR) and 3'-UTR of U2af1-rs1, the methylated and nonexpressed maternal allele was underacetylated, relative to the paternal allele, at all H3 lysines tested (K14, K9, and K18). For H4, underacetylation of the maternal allele was exclusively (U2af1-rs1) or predominantly (Snrpn) at lysine 5. Essentially the same patterns of differential acetylation were found in embryonic stem (ES) cells, embryo fibroblasts, and adult liver from F1 mice and in ES cells from mice that were dipaternal or dimaternal for U2af1-rs1. In contrast, in a region within Snrpn that has biallelic methylation in the cells and tissues analyzed, the paternal (expressed) allele showed relatively increased acetylation of H4 but not of H3. The methyl-CpG-binding-domain (MBD) protein MeCP2 was found, by ChIP, to be associated exclusively with the maternal U2af1-rs1 allele. To ask whether DNA methylation is associated with histone deacetylation, we produced mice with transgene-induced methylation at the paternal allele of U2af1-rs1. In these mice, H3 was underacetylated across both the parental U2af1-rs1 alleles whereas H4 acetylation was unaltered. Collectively, these data are consistent with the hypothesis that CpG methylation leads to deacetylation of histone H3, but not H4, through a process that involves selective binding of MBD proteins.

* Corresponding authors. Mailing address for R. Feil: Institute of Molecular Genetics, CNRS UMR-5535, IRF-24, 1919 Route de Mende, 34293 Montpellier Cedex 5, France. Phone: 33 4 67 61 36 63. Fax: 33 4 67 04 02 03 31. E-mail: feil{at}igm.cnrs-mop.fr. Mailing address for B. M. Turner: Chromatin and Gene Expression Group, University of Birmingham Medical School, Birmingham B15 2TT, United Kingdom. Phone: 44 121 414 6824. Fax: 44 121 414 6815. E-mail: b.m.turner{at}bham.ac.uk.

dagger Present address: Wellcome/CRC Institute of Developmental Biology and Cancer Research, University of Cambridge, Cambridge, United Kingdom.

Molecular and Cellular Biology, August 2001, p. 5426-5436, Vol. 21, No. 16
0270-7306/01/$04.00+0   DOI: 10.1128/MCB.21.16.5426-5436.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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