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Genome activity during the emergence of mouse embryonic totipotency (time course)

ABSTRACT: Fertilization transforms sperm and egg into a totipotent embryo but the underlying mechanisms are unknown. We here report that gene expression initiates during the gamete-to-embryo transition in mouse embryos. Meiotic exit induced by sperm entry enhances a transcriptionally-permissive epigenetic landscape. Time-course analysis of single embryos revealed a succession of genome-wide transcription 'ripples' initiating within 2 hours. Disrupting key pluripotency transcription factor levels prior to sperm entry had little immediate effect, indicating that different mechanisms engender pluripotent and totipotent states. These findings suggest that a hierarchical gene expression program characterizes the emergence of totipotency during the gamete-to-embryo transition, with broad mechanistic implications for the reprogramming of cellular potency.

ORGANISM(S): Mus musculus

PROVIDER: GSE64649 | GEO | 2023/03/02

SECONDARY ACCESSION(S): PRJNA271563

REPOSITORIES: GEO

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Genome activity during the emergence of mouse embryonic totipotency (morpholino)

Project description:Fertilization transforms sperm and egg into a totipotent embryo but the underlying mechanisms are unknown. We here report that gene expression initiates during the gamete-to-embryo transition in mouse embryos. Meiotic exit induced by sperm entry enhances a transcriptionally-permissive epigenetic landscape. Time-course analysis of single embryos revealed a succession of genome-wide transcription 'ripples' initiating within 2 hours. Disrupting key pluripotency transcription factor levels prior to sperm entry had little immediate effect, indicating that different mechanisms engender pluripotent and totipotent states. These findings suggest that a hierarchical gene expression program characterizes the emergence of totipotency during the gamete-to-embryo transition, with broad mechanistic implications for the reprogramming of cellular potency.

2023-03-02 | GSE64648 | GEO

Single cell analysis of sister blastomeres of parthenogenetic 2-cell mouse embryos respecting pair associations

Project description:Following fertilization in mammals, it is generally accepted that totipotent cells are exclusive to the zygote and to each of the two blastomeres originating from the first mitotic division. We counter that this classic view needs to be revised, because we have presented compelling evidence that the sister blastomeres are both totipotent in only a subset of 2-cell stage mouse embryos (PMID 28811525). Building on our previous findings, we here ask the question if the interblastomere differences depend - at least in part - on the contribution of sperm, since the area of sperm entry is inherited preferentially by one blastomere. To this end, we created sister 2-cell stage blastomeres without sperm entry point, by parthenogenesis. We compare the transcriptomes of the sister blastomeres, to see if the interblastomere mRNA differences observed after fertilization (GSE94050) are still there when the sperm entry point is missing.

2019-07-10 | GSE111589 | GEO

embryo_proteome

Project description:We collected over 8000 mouse embryos of each developmental stage (zygote, 2-cell, 4-cell, 8-cell, morula, blastocyst) and performed tandem mass tag (TMT)-based quantitative mass spectrometry and identified nearly 5000 proteins for each stage. In-depth analysis indicates that protein expression profiles of zygote, morula and blastocyst show apparent difference from 2- to 8-cell embryos due to the maternal-totipotent-differentiation transition. We further identified novel factors and proved that they play important roles in determining pre-implantation embryo development

2015-12-10 | MSV000079417 | MassIVE

Totipotency of mouse zygotes extends to single blastomeres of 4-cell stage embryos

Project description:In multicellular organisms, heterogametes of oocytes and sperms are fertilized and resulting zygotes give rise to new individuals. The ability of zygotes that produce a fully formed individual from single cell when placed in a supportive environment is defined as totipotency. Given that totipotent cells are the source of all multicellular organisms, better understanding of totipotency has a profound effect on not only biology but also our society. However, the exact distribution of totipotent cells in mammals remains elusive, although zygotes and single blastomeres at 2-cell stage embryos has been thought to be only mouse cells to be totipotent. We now show that a single blastomere isolated from 2- and 4-cell stage embryos gives rise to a fertile adult individual when it placed in a uterus, although isolation of blastomeres at these stage results in the disturbance of transcriptome in single blastomere derived embryos. Single blastomeres from 8-cell and morula stage embryos that were separately cultured in vitro exhibited severe defects in the formation of epiblast and primitive endoderm in the inner cell mass and the development to blastocysts, respectively. Our results thus indicate that totipotency of mouse zygotes extends to single blastomeres of 4-cell stage embryos.

2021-05-27 | GSE163427 | GEO

Gene expression in mature pollen and sperm cells versus young seedling as a vegetative sporophyte reference control

Project description:Sperm cells represent the male partner that fuses with the egg cell during fertilization in all multi-cellular eukaryotic organisms, and, in flowering plants, is a founder of both embryo and nutritive endosperm. We examined the transcriptome of Oryza sativa ssp. japonica using the Affymetrix 57K rice genome GeneChip to provide an overview of genes activated in the paternal gamete. We used microarrays to detail the global program of gene expression in mature pollen and sperm cells at anthesis, which constitutes the stage immediately preceding pollen germination and gamete deposition leading up to fertilization. This documents the condition of the male gametophytic cells prior to fertilization. Keywords: tissue expression profile, male gametophyte, sperm, pollen, seedling Male gametophytic cells consisting of isolated pollen and isolated sperm cells collected at anthesis were compared with seedlings containing leaf, stem, root and apical meristems as a vegetative sporophytic control; three separate biological replicates were used.

2012-04-29 | E-GEOD-17002 | biostudies-arrayexpress

The homeobox transcription factor DUXBL controls exit from totipotency

Project description:In mice, exit from the totipotent 2-cell (2C) embryo stage requires silencing of the 2C-associated transcriptional program. However, the molecular mechanisms involved in this process remain poorly understood. Here, we demonstrate that the 2C-specific transcription factor DUX mediates an essential negative feedback loop by inducing the expression of DUXBL to promote this silencing.We show that DUXBL gains accessibility to DUX-bound regions specifically upon DUX expression.Furthermore, we determine that DUXBL interacts with TRIM24 and TRIM33, members of the tripartite motif superfamily involved in gene silencing and co-localizes with them in nuclear foci upon DUX expression. Importantly, DUXBL overexpression impairs 2C-associated transcription, whereas Duxbl inactivation in ESC increases DUX-dependent induction of the 2C-transcriptional program. Consequently, DUXBL deficiency in embryos results in sustained expression of 2C-associated transcripts, leading to early developmental arrest.Our study identifies DUXBL as an essential regulator of totipotency exit enabling the first divergence of cell fates.

2023-12-07 | GSE234053 | GEO

Discovery and capture of novel dynamic DNA methylation in human sperm with preferential links to altered folate metabolism

Project description:The sperm DNA methylation landscape is unique and critical for offspring health. If gamete-derived DNA methylation escapes reprogramming in early embryos, epigenetic defects in sperm may be transmitted to the next generation. Current techniques to assess sperm DNA methylation show bias towards CpG dense regions and do not target areas of dynamic methylation, those predicted to be environmentally sensitive and tunable regulatory elements. Thus, this study aim to assess variation in human sperm DNA methylation and design a targeted capture panel to interrogate the human sperm methylome.

| EGAS00001003617 | EGA

Distinct transcriptome, translatome, and proteome reprogramming during the oocyte-to-embryo transition

Project description:The oocyte-to-embryo transition converts terminally differentiated gametes into a totipotent embryo. Fertilized embryos undergo the resetting of the transcriptional program as the zygotic genome is activated from a silenced state started from the late-stage oocyte. How transcriptome, translatome, and proteome interplay in this critical developmental window remains poorly understood. Utilizing a highly sensitive mass spectrometry, we obtained high-quality proteome landscapes including nearly 6,000 genes spanning 10 stages, from the mouse full-grown oocyte (FGO) to blastocyst, using 100 oocytes/embryos at each stage. By integrative analysis with corresponding transcriptomes and translatomes, we found transcription and translation levels can not reflect protein abundance in most cases. From FGOs to the 4-cell embryos, the proteomes are predominated by FGO-produced proteins, while the transcriptome and the translatome are much more dynamic. FGO-originated proteins frequently persist in embryos after the corresponding transcripts are already downregulated or decayed. Improved concordance between protein and RNA is observed for genes starting translation only upon meiotic resumption or transcribed only in embryos, although the detected protein dynamics often lag behind transcription and translation. Concordance between protein and transcription/translation is associated with protein half-lives. Finally, a kinetic model well predicts protein dynamics when incorporating both the initial protein abundance in FGO and translation kinetics across developmental stages. In sum, our study reveals multilayer control of gene expression during oocyte maturation and embryogenesis.

2023-06-27 | PXD035696 | Pride

‘Placeholder’ nucleosomes underlie germline-to-embryo DNA methylation reprogramming [RRBS]

Project description:The function and retention/reprogramming of epigenetic marks during the germline-to-embryo transition is a key issue in developmental and cellular biology, with relevance to stem cell programming and trans-generational inheritance. In zebrafish, DNAme patterns are programmed in transcriptionally-quiescent early cleavage embryos; paternally-inherited patterns are maintained, whereas maternal patterns are reprogrammed to match the paternal pattern. Here we show that a ‘placeholder’ nucleosome, containing the histone H2A variant H2A.Z(FV) and H3K4me1, occupies virtually all regions lacking DNAme in both sperm and cleavage embryos – residing at promoters encoding housekeeping and early embryonic transcription factors. Upon genome-wide transcriptional onset, genes with the Placeholder become either active H3K4me3-marked or silent H3K4me3/K27me3-marked (bivalent). Importantly, functional perturbation causing Placeholder loss confers DNAme acquisition, whereas acquisition/expansion of Placeholder confers DNA hypomethylation and improper gene activation. Thus, during transcriptionally quiescent stages (gamete-zygote-cleavage), an H2A.Z(FV)/H3K4me1-containing Placeholder nucleosome deters DNAme, poising parental genes for either gene-specific activation or facultative repression.

2017-12-12 | GSE95032 | GEO

‘Placeholder’ nucleosomes underlie germline-to-embryo DNA methylation reprogramming [RNA-Seq]

2017-12-12 | GSE95031 | GEO

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