Cargando…

Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting

Thousands of regions in gametes have opposing methylation profiles that are largely resolved during the post-fertilization epigenetic reprogramming. However some specific sequences associated with imprinted loci survive this demethylation process. Here we present the data describing the fate of germ...

Descripción completa

Detalles Bibliográficos
Autores principales: Sanchez-Delgado, Marta, Court, Franck, Vidal, Enrique, Medrano, Jose, Monteagudo-Sánchez, Ana, Martin-Trujillo, Alex, Tayama, Chiharu, Iglesias-Platas, Isabel, Kondova, Ivanela, Bontrop, Ronald, Poo-Llanillo, Maria Eugenia, Marques-Bonet, Tomas, Nakabayashi, Kazuhiko, Simón, Carlos, Monk, David
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5106035/
https://www.ncbi.nlm.nih.gov/pubmed/27835649
http://dx.doi.org/10.1371/journal.pgen.1006427
_version_ 1782466981378654208
author Sanchez-Delgado, Marta
Court, Franck
Vidal, Enrique
Medrano, Jose
Monteagudo-Sánchez, Ana
Martin-Trujillo, Alex
Tayama, Chiharu
Iglesias-Platas, Isabel
Kondova, Ivanela
Bontrop, Ronald
Poo-Llanillo, Maria Eugenia
Marques-Bonet, Tomas
Nakabayashi, Kazuhiko
Simón, Carlos
Monk, David
author_facet Sanchez-Delgado, Marta
Court, Franck
Vidal, Enrique
Medrano, Jose
Monteagudo-Sánchez, Ana
Martin-Trujillo, Alex
Tayama, Chiharu
Iglesias-Platas, Isabel
Kondova, Ivanela
Bontrop, Ronald
Poo-Llanillo, Maria Eugenia
Marques-Bonet, Tomas
Nakabayashi, Kazuhiko
Simón, Carlos
Monk, David
author_sort Sanchez-Delgado, Marta
collection PubMed
description Thousands of regions in gametes have opposing methylation profiles that are largely resolved during the post-fertilization epigenetic reprogramming. However some specific sequences associated with imprinted loci survive this demethylation process. Here we present the data describing the fate of germline-derived methylation in humans. With the exception of a few known paternally methylated germline differentially methylated regions (DMRs) associated with known imprinted domains, we demonstrate that sperm-derived methylation is reprogrammed by the blastocyst stage of development. In contrast a large number of oocyte-derived methylation differences survive to the blastocyst stage and uniquely persist as transiently methylated DMRs only in the placenta. Furthermore, we demonstrate that this phenomenon is exclusive to primates, since no placenta-specific maternal methylation was observed in mouse. Utilizing single cell RNA-seq datasets from human preimplantation embryos we show that following embryonic genome activation the maternally methylated transient DMRs can orchestrate imprinted expression. However despite showing widespread imprinted expression of genes in placenta, allele-specific transcriptional profiling revealed that not all placenta-specific DMRs coordinate imprinted expression and that this maternal methylation may be absent in a minority of samples, suggestive of polymorphic imprinted methylation.
format Online
Article
Text
id pubmed-5106035
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-51060352016-12-08 Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting Sanchez-Delgado, Marta Court, Franck Vidal, Enrique Medrano, Jose Monteagudo-Sánchez, Ana Martin-Trujillo, Alex Tayama, Chiharu Iglesias-Platas, Isabel Kondova, Ivanela Bontrop, Ronald Poo-Llanillo, Maria Eugenia Marques-Bonet, Tomas Nakabayashi, Kazuhiko Simón, Carlos Monk, David PLoS Genet Research Article Thousands of regions in gametes have opposing methylation profiles that are largely resolved during the post-fertilization epigenetic reprogramming. However some specific sequences associated with imprinted loci survive this demethylation process. Here we present the data describing the fate of germline-derived methylation in humans. With the exception of a few known paternally methylated germline differentially methylated regions (DMRs) associated with known imprinted domains, we demonstrate that sperm-derived methylation is reprogrammed by the blastocyst stage of development. In contrast a large number of oocyte-derived methylation differences survive to the blastocyst stage and uniquely persist as transiently methylated DMRs only in the placenta. Furthermore, we demonstrate that this phenomenon is exclusive to primates, since no placenta-specific maternal methylation was observed in mouse. Utilizing single cell RNA-seq datasets from human preimplantation embryos we show that following embryonic genome activation the maternally methylated transient DMRs can orchestrate imprinted expression. However despite showing widespread imprinted expression of genes in placenta, allele-specific transcriptional profiling revealed that not all placenta-specific DMRs coordinate imprinted expression and that this maternal methylation may be absent in a minority of samples, suggestive of polymorphic imprinted methylation. Public Library of Science 2016-11-11 /pmc/articles/PMC5106035/ /pubmed/27835649 http://dx.doi.org/10.1371/journal.pgen.1006427 Text en © 2016 Sanchez-Delgado et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Sanchez-Delgado, Marta
Court, Franck
Vidal, Enrique
Medrano, Jose
Monteagudo-Sánchez, Ana
Martin-Trujillo, Alex
Tayama, Chiharu
Iglesias-Platas, Isabel
Kondova, Ivanela
Bontrop, Ronald
Poo-Llanillo, Maria Eugenia
Marques-Bonet, Tomas
Nakabayashi, Kazuhiko
Simón, Carlos
Monk, David
Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title_full Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title_fullStr Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title_full_unstemmed Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title_short Human Oocyte-Derived Methylation Differences Persist in the Placenta Revealing Widespread Transient Imprinting
title_sort human oocyte-derived methylation differences persist in the placenta revealing widespread transient imprinting
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5106035/
https://www.ncbi.nlm.nih.gov/pubmed/27835649
http://dx.doi.org/10.1371/journal.pgen.1006427
work_keys_str_mv AT sanchezdelgadomarta humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT courtfranck humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT vidalenrique humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT medranojose humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT monteagudosanchezana humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT martintrujilloalex humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT tayamachiharu humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT iglesiasplatasisabel humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT kondovaivanela humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT bontropronald humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT poollanillomariaeugenia humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT marquesbonettomas humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT nakabayashikazuhiko humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT simoncarlos humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting
AT monkdavid humanoocytederivedmethylationdifferencespersistintheplacentarevealingwidespreadtransientimprinting