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Maternal regulation of chromosomal imprinting in animals

Chromosomal imprinting requires an epigenetic system that “imprints” one of the two parental chromosomes such that it results in a heritable (cell-to-cell) change in behavior of the “imprinted” chromosome. Imprinting takes place when the parental genomes are separate, which occurs during gamete form...

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Autores principales: Singh, Prim B., Shloma, Victor V., Belyakin, Stepan N.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Springer Berlin Heidelberg 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6536480/
https://www.ncbi.nlm.nih.gov/pubmed/30719566
http://dx.doi.org/10.1007/s00412-018-00690-5
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author Singh, Prim B.
Shloma, Victor V.
Belyakin, Stepan N.
author_facet Singh, Prim B.
Shloma, Victor V.
Belyakin, Stepan N.
author_sort Singh, Prim B.
collection PubMed
description Chromosomal imprinting requires an epigenetic system that “imprints” one of the two parental chromosomes such that it results in a heritable (cell-to-cell) change in behavior of the “imprinted” chromosome. Imprinting takes place when the parental genomes are separate, which occurs during gamete formation in the respective germ-lines and post-fertilization during the period when the parental pro-nuclei lie separately within the ooplasm of the zygote. In the mouse, chromosomal imprinting is regulated by germ-line specific DNA methylation. But the methylation machinery in the respective germ-lines does not discriminate between imprinted and non-imprinted regions. As a consequence, the mouse oocyte nucleus contains over a thousand oocyte-specific germ-line differentially methylated regions (gDMRs). Upon fertilization, the sperm provides a few hundred sperm-specific gDMRs of its own. Combined, there are around 1600 imprinted and non-imprinted gDMRs in the pro-nuclei of the newly fertilized zygote. It is a remarkable fact that beginning in the maternal ooplasm, there are mechanisms that manage to preserve DNA methylation at ~ 26 known imprinted gDMRs in the face of the ongoing genome-wide DNA de-methylation that characterizes pre-implantation development. Specificity is achieved through the binding of KRAB-zinc finger proteins to their cognate recognition sequences within the gDMRs of imprinted genes. This in turn nucleates the assembly of localized heterochromatin-like complexes that preserve methylation at imprinted gDMRs through recruitment of the maintenance methyl transferase Dnmt1. These studies have shown that a germ-line imprint may cause parent-of-origin-specific behavior only if “licensed” by mechanisms that operate post-fertilization. Study of the germ-line and post-fertilization contributions to the imprinting of chromosomes in classical insect systems (Coccidae and Sciaridae) show that the ooplasm is the likely site where imprinting takes place. By comparing molecular and genetic studies across these three species, we suggest that mechanisms which operate post-fertilization play a key role in chromosomal imprinting phenomena in animals and conserved components of heterochromatin are shared by these mechanisms.
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spelling pubmed-65364802019-06-12 Maternal regulation of chromosomal imprinting in animals Singh, Prim B. Shloma, Victor V. Belyakin, Stepan N. Chromosoma Review Chromosomal imprinting requires an epigenetic system that “imprints” one of the two parental chromosomes such that it results in a heritable (cell-to-cell) change in behavior of the “imprinted” chromosome. Imprinting takes place when the parental genomes are separate, which occurs during gamete formation in the respective germ-lines and post-fertilization during the period when the parental pro-nuclei lie separately within the ooplasm of the zygote. In the mouse, chromosomal imprinting is regulated by germ-line specific DNA methylation. But the methylation machinery in the respective germ-lines does not discriminate between imprinted and non-imprinted regions. As a consequence, the mouse oocyte nucleus contains over a thousand oocyte-specific germ-line differentially methylated regions (gDMRs). Upon fertilization, the sperm provides a few hundred sperm-specific gDMRs of its own. Combined, there are around 1600 imprinted and non-imprinted gDMRs in the pro-nuclei of the newly fertilized zygote. It is a remarkable fact that beginning in the maternal ooplasm, there are mechanisms that manage to preserve DNA methylation at ~ 26 known imprinted gDMRs in the face of the ongoing genome-wide DNA de-methylation that characterizes pre-implantation development. Specificity is achieved through the binding of KRAB-zinc finger proteins to their cognate recognition sequences within the gDMRs of imprinted genes. This in turn nucleates the assembly of localized heterochromatin-like complexes that preserve methylation at imprinted gDMRs through recruitment of the maintenance methyl transferase Dnmt1. These studies have shown that a germ-line imprint may cause parent-of-origin-specific behavior only if “licensed” by mechanisms that operate post-fertilization. Study of the germ-line and post-fertilization contributions to the imprinting of chromosomes in classical insect systems (Coccidae and Sciaridae) show that the ooplasm is the likely site where imprinting takes place. By comparing molecular and genetic studies across these three species, we suggest that mechanisms which operate post-fertilization play a key role in chromosomal imprinting phenomena in animals and conserved components of heterochromatin are shared by these mechanisms. Springer Berlin Heidelberg 2019-02-05 2019 /pmc/articles/PMC6536480/ /pubmed/30719566 http://dx.doi.org/10.1007/s00412-018-00690-5 Text en © The Author(s) 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.
spellingShingle Review
Singh, Prim B.
Shloma, Victor V.
Belyakin, Stepan N.
Maternal regulation of chromosomal imprinting in animals
title Maternal regulation of chromosomal imprinting in animals
title_full Maternal regulation of chromosomal imprinting in animals
title_fullStr Maternal regulation of chromosomal imprinting in animals
title_full_unstemmed Maternal regulation of chromosomal imprinting in animals
title_short Maternal regulation of chromosomal imprinting in animals
title_sort maternal regulation of chromosomal imprinting in animals
topic Review
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6536480/
https://www.ncbi.nlm.nih.gov/pubmed/30719566
http://dx.doi.org/10.1007/s00412-018-00690-5
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