Dataset Information

Temporal patterns of gene regulation and upstream regulators contributing to major developmental transitions during Rhesus macaque preimplantation development.

ABSTRACT: The preimplantation period of life in mammals encompasses a tremendous amount of restructuring and remodeling of the embryonic genome and reprogramming of gene expression. These vast changes support metabolic activation and cellular processes that drive early cleavage divisions and enable the creation of the earliest primitive cell lineages. A major question in mammalian embryology is how such vast, sweeping changes in gene expression are orchestrated, so that changes in gene expression are exactly appropriate to meet the developmental needs of the embryo over time. Using the rhesus macaque as an experimentally tractable model species closely related to the human, we combined high quality RNA-seq libraries, in-depth sequencing and advanced systems analysis to discover the underlying mechanisms that drive major changes in gene regulation during preimplantation development. We identified the major changes in mRNA population and the biological pathways and processes impacted by those changes. Most importantly, we identified 24 key upstream regulators that are themselves modulated during development and that are associated with the regulation of over 1000 downstream genes. Through their roles in extensive gene networks, these 24 upstream regulators are situated to either drive major changes in target gene expression or modify the cellular environment in which other genes function, thereby directing major developmental transitions in the preimplantation embryo. The data presented here highlight some of the specific molecular features that likely drive preimplantation development in a nonhuman primate species and provides an extensive database for novel hypothesis-driven studies.

SUBMITTER: Schall PZ

PROVIDER: S-EPMC6417155 | biostudies-literature | 2019 Mar

REPOSITORIES: biostudies-literature

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Temporal patterns of gene regulation and upstream regulators contributing to major developmental transitions during Rhesus macaque preimplantation development.

Schall Peter Z PZ Ruebel Meghan L ML Midic Uros U VandeVoort Catherine A CA Latham Keith E KE

Molecular human reproduction 20190301 3

The preimplantation period of life in mammals encompasses a tremendous amount of restructuring and remodeling of the embryonic genome and reprogramming of gene expression. These vast changes support metabolic activation and cellular processes that drive early cleavage divisions and enable the creation of the earliest primitive cell lineages. A major question in mammalian embryology is how such vast, sweeping changes in gene expression are orchestrated, so that changes in gene expression are exac ...[more]

PMID: 30698740

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Project description:There are two major developmental transitions that take place during the first four days of mouse embryogenesis. The first one is the maternal-to-zygotic transition in the zygote and 2-cell embryo, the second one is the first cell lineage commitment at the 32-cell stage. A number of transcription factors govern zygotic expression and the specification of pluripotent versus trophectoderm cells, while at the same time there are dynamic changes in DNA methylation and chromatin organization. It is not fully understood which chromatin modifying complexes take part in these processes and whether there is a particular spatiotemporal distribution of certain chromatin players in preimplantation development. To address this question, we performed gene expression profiling of single cells from the oocyte to the blastocyst stage. We describe the patterns of expression of over 100 genes involved in histone methylation, DNA methylation and chromatin remodelling. For a number of these genes we observed differential maternal versus zygotic expression. This is particularly the case for homologous genes like Tet1 and Tet3 (zygotic and maternal respectively), or Suv39h1 and Suv39h2 (zygotic and maternal respectively). In contrast to the maternal-to-zygotic switch, most chromatin modifying genes are ubiquitously expressed in the subsequent lineage specification at the 32-cell stage. The few exceptions that showed a differential expression pattern are Kdm1b, Tet1 and Prdm14. Our data suggests that genes coding for histone modifying complexes are ubiquitously expressed in early embryos and that there are maternal and zygotic variants of most of these complexes. Furthermore, the method that we applied, allows the distinction of female versus male embryos based on the expression of Xist (X-linked, expressed in female embryos) and Kdm5d (Y-linked, expressed strongly in male embryo). With the exception of the X- and Y-linked genes, we did not observe sex-specific gene expression patterns of chromatin modifiers or transcription factors.

Dataset Information

Temporal patterns of gene regulation and upstream regulators contributing to major developmental transitions during Rhesus macaque preimplantation development.

Publications

Temporal patterns of gene regulation and upstream regulators contributing to major developmental transitions during Rhesus macaque preimplantation development.

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