Initiation of X Chromosome Inactivation during Bovine Embryo Development

X-chromosome inactivation (XCI) is a developmental process that aims to equalize the dosage of X-linked gene products between XY males and XX females in eutherian mammals. In female mouse embryos, paternal XCI is initiated at the 4-cell stage; however, the X chromosome is reactivated in the inner ce...

Full description

Bibliographic Details
Main Authors: Bo Yu, Helena T. A. van Tol, Tom A.E. Stout, Bernard A. J. Roelen
Format: Article
Language:English
Published: MDPI AG 2020-04-01
Series:Cells
Subjects:
XCI
Online Access:https://www.mdpi.com/2073-4409/9/4/1016
id doaj-e5de586d0ac846aa9c855dde5c1e32d4
record_format Article
spelling doaj-e5de586d0ac846aa9c855dde5c1e32d42020-11-25T02:54:35ZengMDPI AGCells2073-44092020-04-0191016101610.3390/cells9041016Initiation of X Chromosome Inactivation during Bovine Embryo DevelopmentBo Yu0Helena T. A. van Tol1Tom A.E. Stout2Bernard A. J. Roelen3Farm Animal Health, Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The NetherlandsFarm Animal Health, Department of Population Health Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The NetherlandsEquine Sciences, Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CM Utrecht, The NetherlandsEmbryology, Anatomy and Physiology, Department of Clinical Sciences, Faculty of Veterinary Medicine, Utrecht University, 3584CT Utrecht, The NetherlandsX-chromosome inactivation (XCI) is a developmental process that aims to equalize the dosage of X-linked gene products between XY males and XX females in eutherian mammals. In female mouse embryos, paternal XCI is initiated at the 4-cell stage; however, the X chromosome is reactivated in the inner cell mass cells of blastocysts, and random XCI is subsequently initiated in epiblast cells. However, recent findings show that the patterns of XCI are not conserved among mammals. In this study, we used quantitative RT-PCR and RNA in situ hybridization combined with immunofluorescence to investigate the pattern of XCI during bovine embryo development. Expression of <i>XIST</i> (X-inactive specific transcript) RNA was significantly upregulated at the morula stage. For the first time, we demonstrate that <i>XIST</i> accumulation in bovine embryos starts in nuclei of female morulae, but its colocalization with histone H3 lysine 27 trimethylation was first detected in day 7 blastocysts. Both in the inner cell mass and in putative epiblast precursors, we observed a proportion of cells with <i>XIST</i> RNA and H3K27me3 colocalization. Surprisingly, the onset of XCI did not lead to a global downregulation of X-linked genes, even in day 9 blastocysts. Together, our findings confirm that diverse patterns of XCI initiation exist among developing mammalian embryos.https://www.mdpi.com/2073-4409/9/4/1016XCIbovineembryo<i>XIST</i>H3K27me3inner cell mass
collection DOAJ
language English
format Article
sources DOAJ
author Bo Yu
Helena T. A. van Tol
Tom A.E. Stout
Bernard A. J. Roelen
spellingShingle Bo Yu
Helena T. A. van Tol
Tom A.E. Stout
Bernard A. J. Roelen
Initiation of X Chromosome Inactivation during Bovine Embryo Development
Cells
XCI
bovine
embryo
<i>XIST</i>
H3K27me3
inner cell mass
author_facet Bo Yu
Helena T. A. van Tol
Tom A.E. Stout
Bernard A. J. Roelen
author_sort Bo Yu
title Initiation of X Chromosome Inactivation during Bovine Embryo Development
title_short Initiation of X Chromosome Inactivation during Bovine Embryo Development
title_full Initiation of X Chromosome Inactivation during Bovine Embryo Development
title_fullStr Initiation of X Chromosome Inactivation during Bovine Embryo Development
title_full_unstemmed Initiation of X Chromosome Inactivation during Bovine Embryo Development
title_sort initiation of x chromosome inactivation during bovine embryo development
publisher MDPI AG
series Cells
issn 2073-4409
publishDate 2020-04-01
description X-chromosome inactivation (XCI) is a developmental process that aims to equalize the dosage of X-linked gene products between XY males and XX females in eutherian mammals. In female mouse embryos, paternal XCI is initiated at the 4-cell stage; however, the X chromosome is reactivated in the inner cell mass cells of blastocysts, and random XCI is subsequently initiated in epiblast cells. However, recent findings show that the patterns of XCI are not conserved among mammals. In this study, we used quantitative RT-PCR and RNA in situ hybridization combined with immunofluorescence to investigate the pattern of XCI during bovine embryo development. Expression of <i>XIST</i> (X-inactive specific transcript) RNA was significantly upregulated at the morula stage. For the first time, we demonstrate that <i>XIST</i> accumulation in bovine embryos starts in nuclei of female morulae, but its colocalization with histone H3 lysine 27 trimethylation was first detected in day 7 blastocysts. Both in the inner cell mass and in putative epiblast precursors, we observed a proportion of cells with <i>XIST</i> RNA and H3K27me3 colocalization. Surprisingly, the onset of XCI did not lead to a global downregulation of X-linked genes, even in day 9 blastocysts. Together, our findings confirm that diverse patterns of XCI initiation exist among developing mammalian embryos.
topic XCI
bovine
embryo
<i>XIST</i>
H3K27me3
inner cell mass
url https://www.mdpi.com/2073-4409/9/4/1016
work_keys_str_mv AT boyu initiationofxchromosomeinactivationduringbovineembryodevelopment
AT helenatavantol initiationofxchromosomeinactivationduringbovineembryodevelopment
AT tomaestout initiationofxchromosomeinactivationduringbovineembryodevelopment
AT bernardajroelen initiationofxchromosomeinactivationduringbovineembryodevelopment
_version_ 1724720185869336576