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Multipolar zygotic divisions are characterized by parental genome segregation errors

ABSTRACT: The first mitotic division causes both parental genomes present in the zygote to segregate into two biparental diploid daughter cells. This fundamental tenet was challenged by the observation that blastomeres with different genome ploidy and distinct parental genotypes can coexist within individual embryos. We hypothesized that whole parental genomes can segregate into distinct blastomere lines during the multipolar division of the zygote, a phenomenon referred to as “heterogoneic” cell division. Here, we provide evidence of genome-wide segregation errors in two human blastocysts and further pinpoint its origin in a bovine model by mapping the genomic landscape of 82 blastomeres from 25 embryos that underwent multipolar division at the zygote stage using genome-wide SNP arrays and sequencing. In most embryos, the coexistence of androgenetic and diploid or polyploid blastomeres with or without anuclear blastomeres, androgenetic and anuclear blastomeres, and androgenetic and gynogenetic blastomeres within the same embryo provided proof that multipolar zygotic division coincides with heterogoneic segregation of the parental genome. By mapping the segregational origin of the genomic content, we deduced distinct segregation mechanisms underlying heterogoneic cell division including segregation by a tripolar spindle, the pronuclear extrusion of a paternal genome and, the operation of an ectopic paternal or private parental spindles. Polyspermic embryos expel excessive paternal genomes resulting in an androgenetic or polyploid blastomere. Confirming the results in human blastocysts we found genome-wide segregation errors to persist in bovine blastocysts.

ORGANISM(S): Bos taurus

PROVIDER: GSE182345 | GEO | 2021/08/21

REPOSITORIES: GEO

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Multipolar zygotic divisions are characterized by parental genome segregation errors

Project description:The first mitotic division causes both parental genomes present in the zygote to segregate into two biparental diploid daughter cells. This fundamental tenet was challenged by the observation that blastomeres with different genome ploidy and distinct parental genotypes can coexist within individual embryos. We hypothesized that whole parental genomes can segregate into distinct blastomere lines during the multipolar division of the zygote, a phenomenon referred to as Ã¢Â€ÂœheterogoneicÃ¢Â€Â cell division. Here, we provide evidence of genome-wide segregation errors in two human blastocysts and further pinpoint its origin in a bovine model by mapping the genomic landscape of 82 blastomeres from 25 embryos that underwent multipolar division at the zygote stage using genome-wide SNP arrays and sequencing. In most embryos, the coexistence of androgenetic and diploid or polyploid blastomeres with or without anuclear blastomeres, androgenetic and anuclear blastomeres, and androgenetic and gynogenetic blastomeres within the same embryo provided proof that multipolar zygotic division coincides with heterogoneic segregation of the parental genome. By mapping the segregational origin of the genomic content, we deduced distinct segregation mechanisms underlying heterogoneic cell division including segregation by a tripolar spindle, the pronuclear extrusion of a paternal genome and, the operation of an ectopic paternal or private parental spindles. Polyspermic embryos expel excessive paternal genomes resulting in an androgenetic or polyploid blastomere Confirming the results in human blastocysts we found genome-wide segregation errors to persist in bovine blastocysts.

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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 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 differences between sister blastomeres can be modulated experimentally. To this end, we separate the sister blastomeres, yielding monozygotic twins. We culture these twins in two different media (GM501 vs. Sage 1 step), to see if the mRNA ratios of twin blastocysts lie more far apart from each other when culture took place in different media as compared to culture in the same medium (GSE90674). Transcriptome analysis followed by intra-pair mRNA ratio analysis revealed differences between the blastocysts of the same monozygotic pair. Some of the differences were sensitive to the choice of culture conditions, while other differences were insensitive.

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Multipolar zygotic divisions are characterized by parental genome segregation errors

Project description:Multipolar zygotic divisions are characterized by parental genome segregation errors

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Multipolar zygotic divisions are characterized by parental genome segregation errors

Project description:Multipolar zygotic divisions are characterized by parental genome segregation errors

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Active Demethylation of Both Maternal and Paternal Genomes in Mouse Zygotes

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Zygotes segregate entire parental genomes in distinct blastomere lineages causing cleavage stage chimaerism and mixolpoidy

Project description:Chimaerism and mixoploidy define the presence of cell lineages with different parental genomes or different ploidy states in a single individual. Our knowledge on their mechanistic origin results from indirect observations, often when the cell lineages have been subject to rigorous selective pressure during development. Here, we applied haplarithmisis to infer the haplotypes and the copy number of parental genomes in 116 single blastomeres comprising entire preimplantation stage bovine embryos (n=23) following in vitro fertilization. Not only abnormal fertilizations leading to triploid zygotes, but also normally fertilized zygotes can spontaneously segregate entire parental genomes into different cell lineages during cleavage of the zygote. We coin the term “heterogoneic division” to indicate the events leading to non-canonical zygotic cytokinesis segregating the parental genomes into distinct lineages. Persistence of those cell lines during development is the likely cause of chimaerism and mixoploidy in mammals.

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Active Demethylation of Both Maternal and Paternal Genomes in Mouse Zygotes

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Maternal DNMT3A-dependent de novo methylation of the zygotic paternal genome inhibits gene expression in the early embryo

Project description:De novo DNA methylation (DNAme) during mammalian spermatogenesis yields a densely methylated genome, with the exception of CpG islands (CGIs), which are hypomethylated in sperm. Following fertilization, the paternal genome undergoes widespread DNAme loss before the first S-phase. Paradoxically, recent mass spectrometry analysis revealed that a low level of de novo DNAme occurs exclusively on the zygotic paternal genome. However, the genomic loci involved and impact on genic transcription was not addressed. Here, we employ allele-specific analysis of whole-genome bisulphite sequencing (WGBS) data and show that a number of genomic loci, including several dozen CGI promoters, are de novo methylated on the paternal genome in 2-cell embryos. A subset of these promoters maintain DNAme through development to the blastocyst stage. Consistent with zygotic paternal DNAme acquisition (PDA), many of these loci are hypermethylated in androgenetic blastocysts but hypomethylated in parthenogenetic blastocysts. Strikingly, PDA is lost following maternal deletion of Dnmt3a. Furthermore, a subset of promoters showing PDA which are normally transcribed from the paternal allele in ICM cells show premature transcription at the 4C stage in maternal Dnmt3a knockout embryos. Taken together, these observations uncover an unexpected role for maternal DNMT3A activity in post-fertilization epigenetic reprogramming and transcriptional silencing of the paternal genome.

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