Cargando…

Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis

Transposable elements in the genome are generally silenced in differentiated somatic cells. However, increasing evidence indicates that some of them are actively transcribed in early embryos and the proper regulation of retrotransposon expression is essential for normal development. Although their d...

Descripción completa

Detalles Bibliográficos
Autores principales: Herberg, Sarah, Simeone, Angela, Oikawa, Mami, Jullien, Jerome, Bradshaw, Charles R, Teperek, Marta, Gurdon, John, Miyamoto, Kei
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4585706/
https://www.ncbi.nlm.nih.gov/pubmed/26387861
http://dx.doi.org/10.1038/srep14236
_version_ 1782392258159443968
author Herberg, Sarah
Simeone, Angela
Oikawa, Mami
Jullien, Jerome
Bradshaw, Charles R
Teperek, Marta
Gurdon, John
Miyamoto, Kei
author_facet Herberg, Sarah
Simeone, Angela
Oikawa, Mami
Jullien, Jerome
Bradshaw, Charles R
Teperek, Marta
Gurdon, John
Miyamoto, Kei
author_sort Herberg, Sarah
collection PubMed
description Transposable elements in the genome are generally silenced in differentiated somatic cells. However, increasing evidence indicates that some of them are actively transcribed in early embryos and the proper regulation of retrotransposon expression is essential for normal development. Although their developmentally regulated expression has been shown, the mechanisms controlling retrotransposon expression in early embryos are still not well understood. Here, we observe a dynamic expression pattern of retrotransposons with three out of ten examined retrotransposons (1a11, λ-olt 2-1 and xretpos(L)) being transcribed solely during early embryonic development. We also identified a transcript that contains the long terminal repeat (LTR) of λ-olt 2-1 and shows a similar expression pattern to λ-olt 2-1 in early Xenopus embryos. All three retrotransposons are transcribed by RNA polymerase II. Although their expression levels decline during development, the LTRs are marked by histone H3 lysine 4 trimethylation. Furthermore, retrotransposons, especially λ-olt 2-1, are enriched with histone H3 lysine 9 trimethylation (H3K9me3) when their expression is repressed. Overexpression of lysine-specific demethylase 4d removes H3K9me3 marks from Xenopus embryos and inhibits the repression of λ-olt 2-1 after gastrulation. Thus, our study shows that H3K9me3 is important for silencing the developmentally regulated retrotransposon in Xenopus laevis.
format Online
Article
Text
id pubmed-4585706
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-45857062015-09-29 Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis Herberg, Sarah Simeone, Angela Oikawa, Mami Jullien, Jerome Bradshaw, Charles R Teperek, Marta Gurdon, John Miyamoto, Kei Sci Rep Article Transposable elements in the genome are generally silenced in differentiated somatic cells. However, increasing evidence indicates that some of them are actively transcribed in early embryos and the proper regulation of retrotransposon expression is essential for normal development. Although their developmentally regulated expression has been shown, the mechanisms controlling retrotransposon expression in early embryos are still not well understood. Here, we observe a dynamic expression pattern of retrotransposons with three out of ten examined retrotransposons (1a11, λ-olt 2-1 and xretpos(L)) being transcribed solely during early embryonic development. We also identified a transcript that contains the long terminal repeat (LTR) of λ-olt 2-1 and shows a similar expression pattern to λ-olt 2-1 in early Xenopus embryos. All three retrotransposons are transcribed by RNA polymerase II. Although their expression levels decline during development, the LTRs are marked by histone H3 lysine 4 trimethylation. Furthermore, retrotransposons, especially λ-olt 2-1, are enriched with histone H3 lysine 9 trimethylation (H3K9me3) when their expression is repressed. Overexpression of lysine-specific demethylase 4d removes H3K9me3 marks from Xenopus embryos and inhibits the repression of λ-olt 2-1 after gastrulation. Thus, our study shows that H3K9me3 is important for silencing the developmentally regulated retrotransposon in Xenopus laevis. Nature Publishing Group 2015-09-21 /pmc/articles/PMC4585706/ /pubmed/26387861 http://dx.doi.org/10.1038/srep14236 Text en Copyright © 2015, Macmillan Publishers Limited http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Herberg, Sarah
Simeone, Angela
Oikawa, Mami
Jullien, Jerome
Bradshaw, Charles R
Teperek, Marta
Gurdon, John
Miyamoto, Kei
Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title_full Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title_fullStr Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title_full_unstemmed Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title_short Histone H3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in Xenopus laevis
title_sort histone h3 lysine 9 trimethylation is required for suppressing the expression of an embryonically activated retrotransposon in xenopus laevis
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4585706/
https://www.ncbi.nlm.nih.gov/pubmed/26387861
http://dx.doi.org/10.1038/srep14236
work_keys_str_mv AT herbergsarah histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT simeoneangela histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT oikawamami histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT jullienjerome histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT bradshawcharlesr histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT teperekmarta histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT gurdonjohn histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis
AT miyamotokei histoneh3lysine9trimethylationisrequiredforsuppressingtheexpressionofanembryonicallyactivatedretrotransposoninxenopuslaevis