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Transcriptome profiling of individual rhesus macaque oocytes and preimplantation embryos

ABSTRACT: Early mammalian embryonic transcriptomes are dynamic throughout the process of preimplantation development. Cataloging of primate transcriptomics during early development has been accomplished in humans, but global characterization of transcripts is lacking in the rhesus macaque: a key model for human reproductive processes. We report here the systematic classification of individual macaque transcriptomes using RNA-Seq technology from the germinal vesicle stage oocyte through the blastocyst stage embryo. Major differences in gene expression were found between sequential stages, with the 4- to 8-cell stages showing the highest level of differential gene expression. Analysis of putative transcription factor binding sites also revealed a striking increase in key regulatory factors in 8-cell embryos, indicating a strong likelihood of embryonic genome activation occurring at this stage. Furthermore, clustering analyses of gene co-expression throughout this period resulted in distinct groups of transcripts significantly associated to the different embryo stages assayed. The sequence data provided here along with characterizations of major regulatory transcript groups presents a comprehensive atlas of polyadenylated transcripts that serves as a useful resource for comparative studies of preimplantation development in humans and other species.

ORGANISM(S): Macaca mulatta

PROVIDER: GSE103313 | GEO | 2017/09/01

SECONDARY ACCESSION(S): PRJNA401876

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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Transcriptome profiling of individual rhesus macaque oocytes and preimplantation embryos

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