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Analysis of Chinese sheep preimplantation embryo development and block by single-cell DNA methylome sequencing

ABSTRACT: The early stages of mammalian embryonic development involve the participation and cooperation of numerous complex processes, including nutritional, genetic, and epigenetic mechanisms. However, in embryos cultured in vitro, a developmental block occurs that affects embryo development and the efficiency of culture. Although the block period is reported to involve the transcriptional repression of maternal genes and transcriptional activation of zygotic genes, how epigenetic factors regulate developmental block is still unclear. In this study, we systematically analyzed whole-genome methylation levels during five stages of sheep oocyte and preimplantation embryo development using SC-WGBS technology. Then, we examined several million CpG sites in individual cells at each evaluated developmental stage to identify the methylation changes that take place during the development of sheep preimplantation embryos. Our results showed that two strong waves of methylation changes occurred, namely, demethylation at the 8- to 16-cell stage and methylation at the 16- to 32-cell stage. Analysis of DNA methylation patterns in different functional regions revealed a stable hypermethylation status in 3'UTRs and gene bodies; however, significant differences were observed in intergenic and promoter regions at different developmental stages. Changes in methylation at different stages of preimplantation embryo development were also compared to investigate the molecular mechanisms involved in sheep embryo development at the methylation level. In conclusion, we report a detailed analysis of the DNA methylation dynamics during the development of sheep preimplantation embryos. Our results provide an explanation for the complex regulatory mechanisms underlying the embryo developmental block based on changes in DNA methylation levels.

ORGANISM(S): Ovis aries

PROVIDER: GSE190746 | GEO | 2021/12/15

REPOSITORIES: GEO

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Project description:The transformation of a fertilized oocyte into a multicellular embryo comprised of differentiated cells depends on the processing of genetic orders, first in the form of transcripts and then of proteins. Our current understanding of mouse development has greatly benefited from the analysis of transcripts as proxy for the proteins. However, the hexagonal-shaped free ribosomes that translate mRNAs into proteins are scarce during cleavage and do not become abundant until the morula-blastocyst stage. How accurate, then, is an understanding of mouse and more in general mammalian development that uses the analysis of transcripts as proxy for the proteins? This led us in this study to measure the proteome of seven preimplantation mouse stages (B6C3F1 x CD1), from oocyte to blastocyst, using 'spike-in' SILAC technology combined with high accuracy mass spectrometry (LTQ Orbitrap and Q-Exactive). The relative abundances of embryonic proteins were compared and contrasted with those of transcripts measured by RNA sequencing. A total of 6976 proteins were detected in at least the spike (precondition for determining the heavy/light peptide ratios in oocytes or embryos). Among these 6976 proteins, 4991 proteins were present in all developmental stages, and 1893 proteins were present in all replicates. Our tandem approach uncovered: 1) the different abundance profiles of proteome and transcriptome during the time of preimplantation development; 2) the different reciprocal associations of developmental stages (dendrograms) on the protein level as compared to the mRNA level; and 3) the different gene ontology terms overrepresented among the proteins that increase or decrease across adjacent stages, compared to mRNAs. In essence, the elaborate phasing of embryonic gene expression that has been known for mRNAs leaves an unsuspected footprint on the protein products of those mRNAs. This information facilitates the analysis of mammalian development in two important ways. First, it provides new insight into the regulation of the transition from the differentiated oocyte into the embryo, by identifying the subsets of proteins that accompany the passage from one embryonic stage to the next, which are likely composed of important regulators of the morphogenetic transitions. Second, our analysis provides a reference to determine the degree of ‘embryoness’ of entities produced via assisted reproductive technologies, cloning by somatic cell nuclear transfer, and even artificial gametes.

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Analysis of Chinese sheep preimplantation embryo development and block by single-cell DNA methylome sequencing

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