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High-resolution Ribosome Profiling Reveals Translational Selectivity in Bovine Preimplantation Embryo Development

ABSTRACT: High resolution polysome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscape of early embryo development at an unprecedented level. We systematically and comparatively analyzed the transcriptome, polysome- and nonpolysome-bound RNA profiles of bovine oocytes and early embryos at 2-, 8-cell, morula, and blastocyst stage, and defined four modes of translational selectivity in bovine preimplantation embryo development: i. selective translation of non-abundant mRNAs, ii. active translating highly expressed mRNAs, iii. Translationally suppressed abundant mRNAs, and iv. Monosomaly occupied mRNAs. A strong selection towards genes involved in mitochondrial function and metabolic pathways was found throughout bovine preimplantation development. We found translatome largely follows transcriptome at oocytes, followed by a marked translational control at 8-cell embryos, which is gradually synchronized at the morula and blastocyst stage. We identified important novel cellular/embryonic functional regulators that being utilized and prioritized for translation at each developmental stage, that accompanies little-known bovine embryonic developmental programming. Together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

ORGANISM(S): Bos taurus

PROVIDER: GSE196484 | GEO | 2022/10/01

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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High-resolution Ribosome Profiling Reveals Translational Selectivity in Bovine Preimplantation Embryo Development

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