Insulators and imprinting from flies to mammals

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Abstract

The nuclear factor CTCF has been shown to be necessary for the maintenance of genetic imprinting at the mammalian H19/Igf2 locus. MacDonald and colleagues now report in BMC Biology that the mechanisms responsible for maintaining the imprinted state in Drosophila may be evolutionarily conserved and that CTCF may also play a critical role in this process.

See research article http://www.biomedcentral.com/1741-7007/8/105

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CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2.

Gholamreza Tavoosidana, Elena Pugacheva, V Tiwari … (2006)

It is thought that the H19 imprinting control region (ICR) directs the silencing of the maternally inherited Igf2 allele through a CTCF-dependent chromatin insulator. The ICR has been shown to interact physically with a silencer region in Igf2, differentially methylated region (DMR)1, but the role of CTCF in this chromatin loop and whether it restricts the physical access of distal enhancers to Igf2 is not known. We performed systematic chromosome conformation capture analyses in the Igf2/H19 region over >160 kb, identifying sequences that interact physically with the distal enhancers and the ICR. We found that, on the paternal chromosome, enhancers interact with the Igf2 promoters but that, on the maternal allele, this is prevented by CTCF binding within the H19 ICR. CTCF binding in the maternal ICR regulates its interaction with matrix attachment region (MAR)3 and DMR1 at Igf2, thus forming a tight loop around the maternal Igf2 locus, which may contribute to its silencing. Mutation of CTCF binding sites in the H19 ICR leads to loss of CTCF binding and de novo methylation of a CTCF target site within Igf2 DMR1, showing that CTCF can coordinate regional epigenetic marks. This systematic chromosome conformation capture analysis of an imprinting cluster reveals that CTCF has a critical role in the epigenetic regulation of higher-order chromatin structure and gene silencing over considerable distances in the genome.

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Completion of mouse embryogenesis requires both the maternal and paternal genomes.

Patrick J McGrath, D Solter (1984)

Transplantation of pronuclei between one-cell-stage embryos was used to construct diploid mouse embryos with two female pronuclei ( biparental gynogenones ) or two male pronuclei ( biparental androgenones ). The ability of these embryos to develop to term was compared with control nuclear-transplant embryos in which the male or the female pronucleus was replaced with an isoparental pronucleus from another embryo. The results show that diploid biparental gynogenetic and androgenetic embryos do not complete normal embryogenesis, whereas control nuclear transplant embryos do. We conclude that the maternal and paternal contributions to the embryonic genome in mammals are not equivalent and that a diploid genome derived from only one of the two parental sexes is incapable of supporting complete embryogenesis.

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Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis.

M Surani, S C Barton, M Norris (2015)

It has been suggested that the failure of parthenogenetic mouse embryos to develop to term is primarily due to their aberrant cytoplasm and homozygosity leading to the expression of recessive lethal genes. The reported birth of homozygous gynogenetic (male pronucleus removed from egg after fertilization) mice and of animals following transplantation of nuclei from parthenogenetic embryos to enucleated fertilized eggs, is indicative of abnormal cytoplasm and not an abnormal genotype of the activated eggs. However, we and others have been unable to obtain such homozygous mice. We investigated this problem further by using reconstituted heterozygous eggs, with haploid parthenogenetic eggs as recipients for a male or female pronucleus. We report here that the eggs which receive a male pronucleus develop to term but those with two female pronuclei develop only poorly after implantation. Therefore, the cytoplasm of activated eggs is fully competent to support development to term but not if the genome is entirely of maternal origin. We propose that specific imprinting of the genome occurs during gametogenesis so that the presence of both a male and a female pronucleus is essential in an egg for full-term development. The paternal imprinting of the genome appears necessary for the normal development of the extraembryonic membranes and the trophoblast.

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Journal

Journal ID (nlm-ta): BMC Biol

Title: BMC Biology

Publisher: BioMed Central

ISSN (Electronic): 1741-7007

Publication date Collection: 2010

Publication date (Electronic): 30 July 2010

Volume: 8

Page: 104

Affiliations

[1 ]Department of Biology, Emory University, 1510 Clifton Road NE, Atlanta, GA 30322, USA

Article

Publisher ID: 1741-7007-8-104

DOI: 10.1186/1741-7007-8-104

PMC ID: 2912829

PubMed ID: 20687908

SO-VID: 7305295b-5399-42b6-ace4-999689012b7f

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Insulators and imprinting from flies to mammals

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Most cited references 7

CTCF binding at the H19 imprinting control region mediates maternally inherited higher-order chromatin conformation to restrict enhancer access to Igf2.

Completion of mouse embryogenesis requires both the maternal and paternal genomes.

Development of reconstituted mouse eggs suggests imprinting of the genome during gametogenesis.

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