High-resolution ribosome fractionation and low-input ribosome profiling of bovine oocytes and preimplantation embryos has enabled us to define the translational landscapes of early embryo development at an unprecedented level. We analyzed the transcriptome and the polysome- and non-polysome-bound RNA profiles of bovine oocytes (germinal vesicle and metaphase II stages) and early embryos at the two-cell, eight-cell, morula and blastocyst stages, and revealed four modes of translational selectivity: (1) selective translation of non-abundant mRNAs; (2) active, but modest translation of a selection of highly expressed mRNAs; (3) translationally suppressed abundant to moderately abundant mRNAs; and (4) mRNAs associated specifically with monosomes. A strong translational selection of low-abundance transcripts involved in metabolic pathways and lysosomes was found throughout bovine embryonic development. Notably, genes involved in mitochondrial function were prioritized for translation. We found that translation largely reflected transcription in oocytes and two-cell embryos, but observed a marked shift in the translational control in eight-cell embryos that was associated with the main phase of embryonic genome activation. Subsequently, transcription and translation become more synchronized in morulae and blastocysts. Taken together, these data reveal a unique spatiotemporal translational regulation that accompanies bovine preimplantation development.

• Keywords
• Bovine, Preimplantation embryo development, Ribosome profiling, Transcription, Translation, Translational selectivity,
• MeSH
• Blastocyst * metabolism   MeSH
• Embryonic Development * genetics   MeSH
• Morula metabolism   MeSH
• Oocytes metabolism   MeSH
• Ribosomes genetics   MeSH
• Cattle MeSH
• Pregnancy MeSH
• Gene Expression Regulation, Developmental MeSH
• Animals MeSH
• Check Tag
• Cattle MeSH
• Pregnancy MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH

Successful reproduction requires an oocyte competent to sustain early embryo development. By the end of oogenesis, the oocyte has entered a transcriptionally silenced state, the mechanisms and significance of which remain poorly understood. Histone H3.3, a histone H3 variant, has unique cell cycle-independent functions in chromatin structure and gene expression. Here, we have characterised the H3.3 chaperone Hira/Cabin1/Ubn1 complex, showing that loss of function of any of these subunits causes early embryogenesis failure in mouse. Transcriptome and nascent RNA analyses revealed that transcription is aberrantly silenced in mutant oocytes. Histone marks, including H3K4me3 and H3K9me3, are reduced and chromatin accessibility is impaired in Hira/Cabin1 mutants. Misregulated genes in mutant oocytes include Zscan4d, a two-cell specific gene involved in zygote genome activation. Overexpression of Zscan4 in the oocyte partially recapitulates the phenotypes of Hira mutants and Zscan4 knockdown in Cabin1 mutant oocytes partially restored their developmental potential, illustrating that temporal and spatial expression of Zscan4 is fine-tuned at the oocyte-to-embryo transition. Thus, the H3.3 chaperone Hira complex has a maternal effect function in oocyte developmental competence and embryogenesis, through modulating chromatin condensation and transcriptional quiescence.

• Keywords
• Competent oocyte, Hira complex, Histone H3.3, Oocyte-to-embryo transition, Zygotic genome activation,
• MeSH
• Adaptor Proteins, Signal Transducing metabolism   MeSH
• Chromatin metabolism   MeSH
• Embryonic Development genetics   MeSH
• Gene Knockdown Techniques MeSH
• Histone Chaperones genetics   metabolism   MeSH
• Histones metabolism   MeSH
• Mice, Inbred C57BL MeSH
• Mice, Transgenic MeSH
• Mice MeSH
• Oocytes growth & development   metabolism   MeSH
• Oogenesis genetics   MeSH
• Cell Cycle Proteins genetics   metabolism   MeSH
• Signal Transduction genetics   MeSH
• Transcription Factors genetics   metabolism   MeSH
• Animals MeSH
• Zygote metabolism   MeSH
• Check Tag
• Male MeSH
• Mice MeSH
• Female MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Research Support, Non-U.S. Gov't MeSH
• Research Support, N.I.H., Extramural MeSH
• Research Support, U.S. Gov't, Non-P.H.S. MeSH
• Names of Substances
• Adaptor Proteins, Signal Transducing MeSH
• Cabin1 protein, mouse MeSH Browser
• Chromatin MeSH
• Hira protein, mouse MeSH Browser
• Histone Chaperones MeSH
• Histones MeSH
• Cell Cycle Proteins MeSH
• Transcription Factors MeSH
• Zscan4d protein, mouse MeSH Browser

The onset of an early development is, in mammals, characterized by profound changes of multiple aspects of cellular morphology and behavior. These are including, but not limited to, fertilization and the merging of parental genomes with a subsequent transition from the meiotic into the mitotic cycle, followed by global changes of chromatin epigenetic modifications, a gradual decrease in cell size and the initiation of gene expression from the newly formed embryonic genome. Some of these important, and sometimes also dramatic, changes are executed within the period during which the gene transcription is globally silenced or not progressed, and the regulation of most cellular activities, including those mentioned above, relies on controlled translation. It is known that the blastomeres within an early embryo are prone to chromosome segregation errors, which might, when affecting a significant proportion of a cell within the embryo, compromise its further development. In this review, we discuss how the absence of transcription affects the transition from the oocyte to the embryo and what impact global transcriptional silencing might have on the basic cell cycle and chromosome segregation controlling mechanisms.

• Keywords
• cell cycle, embryo, oocyte, transcriptional repression, translation,
• MeSH
• Cell Cycle genetics   MeSH
• Chromatin genetics   MeSH
• Embryo, Mammalian physiology   MeSH
• Embryonic Development genetics   MeSH
• Transcription, Genetic genetics   MeSH
• Humans MeSH
• Chromosome Segregation genetics   MeSH
• Gene Silencing physiology   MeSH
• Gene Expression Regulation, Developmental genetics   MeSH
• Animals MeSH
• Check Tag
• Humans MeSH
• Animals MeSH
• Publication type
• Journal Article MeSH
• Review MeSH
• Names of Substances
• Chromatin MeSH