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Slam-seq reveals that miR-430 regulates zygotic mRNA during zebrafish embryogenesis [lna_data]

ABSTRACT: Background: Early embryonic developmental programs are guided by the coordinated interplay between maternally inherited and zygotically manufactured RNAs and proteins. Although these processes happen concomitantly and affecting gene function during this period is bound to affect both pools of mRNAs, it has been challenging to study their expression dynamics separately. Results: By employing Slam-seq, a nascent mRNA labeling transcriptomic approach, in a developmental time series we observe that over half of the early zebrafish embryo transcriptome consists of maternal-zygotic genes, emphasizing their pivotal role in early embryogenesis. We provide an hourly resolution of de novo transcriptional waves and follow nascent mRNA trajectories, finding that most de novo transcriptional events are stable throughout this period. Additionally, by blocking microRNA430 function, a key post-transcriptional regulator during zebrafish embryogenesis, we directly show that it destabilizes hundreds of de novo transcribed mRNAs from pure zygotic as well as maternal-zygotic genes. This unveils a novel miR-430 function during embryogenesis, fine-tuning zygotic gene expression, which highlights that Slam-seq can be used to disentangle transcriptional and post-transcriptional regulation of mRNA levels. Conclusion: Such valuable insights into zebrafish early embryo transcriptome dynamics emphasize the significance of post-transcriptional regulators in zygotic genome activation. These findings pave the way for future investigations into the coordinated interplay between transcriptional and post-transcriptional landscapes required for the establishment of animal cell identities and functions.

ORGANISM(S): Danio rerio

PROVIDER: GSE247930 | GEO | 2024/02/10

REPOSITORIES: GEO

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Slam-seq reveals that miR-430 regulates zygotic mRNA during zebrafish embryogenesis [titration_data]

Project description:Background: Early embryonic developmental programs are guided by the coordinated interplay between maternally inherited and zygotically manufactured RNAs and proteins. Although these processes happen concomitantly and affecting gene function during this period is bound to affect both pools of mRNAs, it has been challenging to study their expression dynamics separately. Results: By employing Slam-seq, a nascent mRNA labeling transcriptomic approach, in a developmental time series we observe that over half of the early zebrafish embryo transcriptome consists of maternal-zygotic genes, emphasizing their pivotal role in early embryogenesis. We provide an hourly resolution of de novo transcriptional waves and follow nascent mRNA trajectories, finding that most de novo transcriptional events are stable throughout this period. Additionally, by blocking microRNA430 function, a key post-transcriptional regulator during zebrafish embryogenesis, we directly show that it destabilizes hundreds of de novo transcribed mRNAs from pure zygotic as well as maternal-zygotic genes. This unveils a novel miR-430 function during embryogenesis, fine-tuning zygotic gene expression, which highlights that Slam-seq can be used to disentangle transcriptional and post-transcriptional regulation of mRNA levels. Conclusion: Such valuable insights into zebrafish early embryo transcriptome dynamics emphasize the significance of post-transcriptional regulators in zygotic genome activation. These findings pave the way for future investigations into the coordinated interplay between transcriptional and post-transcriptional landscapes required for the establishment of animal cell identities and functions.

2024-02-10 | GSE247934 | GEO

Slam-seq reveals that miR-430 regulates zygotic mRNA during zebrafish embryogenesis [timecourse_data]

2024-02-10 | GSE247933 | GEO

Topoisomerase 1 activity during mitotic transcription favors the transition from mitosis to G1 [SLAM-seq]

Project description:Using SLAM-seq to capture de novo synthesized polyadenylated RNAs, we quantitated changes in nascent RNA expression, as well as in total RNA expression.

2021-11-11 | GSE171133 | GEO

A single-cell map of maternal and zygotic mRNA dynamics during cell-type specification in zebrafish embryos [scSLAM-seq]

Project description:During early embryogenesis, embryos undergo a massive degradation of maternally inherited mRNAs and produce new zygotic transcripts. This maternal-to-zygotic transition requires a tight interplay of mRNA transcription and degradation, but distinguishing their unique contributions remains a challenge. Here, we dissect gene regulation during the zebrafish maternal-to-zygotic transition by combining single-cell RNA-sequencing with RNA metabolic labeling and nucleotide conversion within zebrafish embryos. We decompose single-cell transcriptomes into their new (zygotic) and old (maternal) mRNA components, and elicit critical information on gene regulation as it unfolds over both time and space. We show that most cell-type restricted expression arises by zygotic transcription, but distinguish a specific role for maternal transcripts in defining germ-cell and enveloping-layer identity, two earliest specified cell identities. We recover the underlying replacement between maternal and zygotic copies of embryonic genes with a relatively constant overall mRNA level, and associate a fast replacement with genes that has a restricted zygotic expression in either cell-type or time. Our study provides a valuable resource to investigate maternal and zygotic transcriptomes and reveals post-transcriptional events that control gene regulation during early embryogenesis.

2023-05-11 | GSE224918 | GEO

A single-cell map of maternal and zygotic mRNA dynamics during cell-type specification in zebrafish embryos [SLAM-seq]

2023-05-11 | GSE224113 | GEO

Transposable elements drive the evolution of metazoan zinc finger genes

Project description:Cys2-His2 Zinc finger genes (ZNFs) form the largest family of transcription factors in metazoans. Zebrafish posess a subfamily characterized by the presence of a domain dubbed Fish N-terminal Zinc finger associated (FiNZ). FiNZ-ZNFs are expressed at the onset of zygotic genome activation in zebrafishh, and blocking FiNZ-ZNF translation using morpholinos during early zebrafish embryogenesis results in a broad de-repression of young, transcriptionally active TEs.

2023-04-10 | GSE229157 | GEO

To investigate 4-TU labelling kinetics in a novel zebrafish transgenic line (lf:UPRT). [Adult SLAM-Itseq]

Project description:To understand 4-TU labelling kinetics in a novel zebrafish transgenic line (lf:UPRT), we exposed adult lf:UPRT zebrafish (whereby animals have hepatocyte-specific uracil phosphoribosyltransferase expression) with 4-TU for 1, 3, 6 and 9 hours. We then dissected adult livers for SLAM-ITseq to determine the optimal 4-TU labelling time in our SLAM-ITseq workflow to allow us to study hepatocyte-specific nascent transcriptional changes.

2024-01-13 | GSE230830 | GEO

Transcriptome analysis of wild-type and maternal zygotic double mutant of nup85;nup133 zebrafish embryos during early development

Project description:To study the function of zebrafish nuclear pores during early embryogenesis, we generated maternal zygotic double mutant of nup85;nup133 (MZnup85;nup133) using CRISPR/Cas9 and report the transcriptome-wide changes in comparison to wild-type (WT) embryos. Our analysis reveals a dramatic delay of maternal mRNA degradation and zygotic genome activation in MZnup85;nup133 embryos during maternal-to-zygotic transition.

2023-03-04 | GSE146394 | GEO

Dynamic RNA-protein interactions underlie the zebrafish maternal-to-zygotic transition

Project description:During the maternal-to-zygotic transition (MZT), transcriptionally silent embryos rely on post-transcriptional regulation of maternal mRNAs until zygotic genome activation (ZGA). RNA-binding proteins (RBPs) are important regulators of post-transcriptional RNA processing events, yet their identities and functions during developmental transitions in vertebrates remain largely unexplored. Using mRNA interactome capture, we identified 227 RBPs in zebrafish embryos before and during ZGA, hereby named the zebrafish MZT mRNAbound proteome. This protein constellation consists of many conserved RBPs, with additional embryo- and stage-specific mRNA interactors that likely reflect the dynamics of RNA-protein interactions during MZT. The enrichment of numerous splicing factors like hnRNP proteins before ZGA was surprising, because maternal mRNAs were found to be fully spliced. To address potentially unique roles of RBPs in embryogenesis, we focused on hnRNP A1. iCLIP and subsequent mRNA reporter assays revealed a function for hnRNP A1 in the regulation of poly(A) tail length and translation of maternal mRNAs through sequence-specific association with 3’UTRs before ZGA. Comparison of iCLIP data from two developmental stages revealed that hnRNP A1 dissociates from maternal mRNAs at ZGA and instead regulates the nuclear processing of pri-miR-430 transcripts, which we validated experimentally. The shift from cytoplasmic to nuclear RNA targets was accompanied by a dramatic translocation of hnRNP A1 and other pre-mRNA splicing factors to the nucleus in a transcription-dependent manner. Thus, our study identifies global changes in RNA-protein interactions during vertebrate MZT and shows that hnRNP A1 RNA-binding activities are spatially and temporally coordinated to regulate RNA metabolism during early development.

2017-03-27 | PXD006098 | Pride

N6-methyladenosine dynamics during early vertebrate embryogenesis

Project description:Early vertebrate embryogenesis is characterized by extensive post-transcriptional regulation during the maternal-to-zygotic transition. The N6-methyladenosine (m6A) modifications on mRNA has been shown to affect both translation and stability of transcripts. Here we investigate the m6A topology during early vertebrate embryogenesis and its association with RNA stability, translation efficiency and effect on miR-430 degradation kinetics. Notably, we find a strong association of m6A with cytoplasmic polyadenylation and translational efficiency prior to zygotic genome activation. Genes required for zygotic genome activation such as nanog and pou5f3 display dynamic m6A levels. After zygotic genome activation m6A is associated with improved stability and dampens the effect of miR-430 mediated degradation. Through sequence analyses we identified enrichment of motifs for RNA binding proteins involved in translational regulation and RNA degradation. We propose a role for m6A in multiple mRNA regulatory mechanisms, for the first time in an in vivo system and improve our understanding of the combinatorial code behind the complex post transcriptional regulation of reprogramming during early vertebrate development.

2017-05-01 | GSE89815 | GEO

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