A heterochromatin-specific RNA export pathway facilitates piRNA production
Ontology highlight
ABSTRACT:
PROVIDER: PRJNA522430 | ENA |
REPOSITORIES: ENA
Dataset's files
| Action | DRS | |||
|---|---|---|---|---|
| SRR8578620.fastq.gz | Fastqsanger.gz | |||
| SRR8578630.fastq.gz | Fastqsanger.gz | |||
| SRR8578640.fastq.gz | Fastqsanger.gz | |||
| SRR8578650.fastq.gz | Fastqsanger.gz | |||
| SRR8578660.fastq.gz | Fastqsanger.gz |
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Project description:PIWI-interacting RNAs (piRNAs), a class of small RNAs that guide transposon silencing in animals, are processed in the cytoplasm from RNA Polymerase II transcripts. How piRNA precursors, which often lack RNA maturation signatures and thereby violate quality control checkpoints, achieve nuclear export is unknown. Here, we uncover a germline-specific RNA export pathway in Drosophila, that escorts piRNA precursors from their heterochromatic origins to nuage, the cytoplasmic piRNA processing centres. This pathway connects canonical nuclear export factors—the RNA helicase UAP56, the NXF cofactor Nxt1/p15, and the exportin Crm1/Xpo1—with Nxf3, a variant of the mRNA exporter Nxf1/Tap. Nxf3 recruitment to nascent piRNA precursors occurs via the heterochromatin protein 1-variant Rhino and CG13741/Bootlegger, a new piRNA pathway factor, thereby making piRNA precursor export independent of RNA processing events. Thus, similar to retroviral hijacking of cellular export factors, piRNA precursor export evolved to bend canonical gene expression rules through bypassing nuclear RNA surveillance mechanisms.
2019-03-29 | PXD012717 | Pride
Project description:PIWI-interacting RNAs (piRNAs) guide transposon silencing in animals. The 22-30nt piRNAs are processed in the cytoplasm from long non-coding RNAs. How piRNA precursors, which often lack RNA processing hallmarks of export-competent transcripts, achieve nuclear export is unknown. Here, we uncover the RNA export pathway specific for piRNA precursors in the Drosophila germline. This pathway requires Nxf3-Nxt1, a variant of the hetero-dimeric mRNA export receptor Nxf1-Nxt1. Nxf3 interacts with UAP56, a nuclear RNA helicase essential for mRNA export, and CG13741/Bootlegger, which recruits Nxf3-Nxt1 and UAP56 to heterochromatic piRNA source loci. Upon RNA cargo binding, Nxf3 achieves nuclear export via the exportin Crm1, and accumulates together with Bootlegger in peri-nuclear nuage, suggesting that after export, Nxf3-Bootlegger delivers precursor transcripts to the piRNA processing sites. Our findings indicate that the piRNA pathway bypasses nuclear RNA surveillance systems to achieve export of heterochromatic, unprocessed transcripts to the cytoplasm, a strategy also exploited by retroviruses.
2019-03-28 | GSE126578 | GEO
Project description:Small RNA silencing pathways protect genome integrity in part through establishing heterochromatin at transposon loci. In animals, this process requires piRNA-guided targeting of nuclear PIWI proteins to nascent transcripts. The molecular events contributing to heterochromatin formation upon PIWI binding to nascent RNA, a transient molecule at chromatin, are unknown. Here, we identify SFINX, a protein complex that is required for Piwi-mediated co-transcriptional silencing in Drosophila. It consists of Nxf2—a variant of the nuclear RNA export factor Nxf1/Tap, the mRNA export co-factor Nxt1/p15, and the Piwi-associated protein Panoramix. In the absence of Nxf2, Panoramix is targeted for degradation and piRNA-loaded Piwi is unable to establish heterochromatin. Consequently, nxf2 mutants exhibit severe transposon de-repression and are sterile. We show that within SFINX, Panoramix connects to the heterochromatin machinery while Nxf2 enables target silencing via nascent RNA. Thus, the Nxf2-Nxt1 heterodimer—despite having originated from core mRNA export machinery—has been repurposed for heterochromatin formation. Our data establish an unexpected link between nuclear small RNA biology and NXF-variants, which are widespread in animal lineages, but mostly lack ascribed functions.
2019-06-12 | PXD011201 | Pride
Project description:The piRNA pathway is a conserved small RNA-based immune system that protects animal germ cell genomes from the harmful effects of transposon mobilisation. In Drosophila ovaries, most piRNAs originate from dual-strand clusters, which generate piRNAs from both genomic strands. Dual-strand clusters use non-canonical transcription mechanisms. Although transcribed by RNA polymerase II, cluster transcripts lack splicing signatures and polyA tails. mRNA processing is important for general mRNA export mediated by Nuclear export factor 1. Although UAP56, a component of the transcription and export complex, has been implicated in piRNA precursor export, it remains unknown how dual-strand cluster transcripts are specifically targeted for piRNA biogenesis by export from the nucleus to cytoplasmic processing centers. Here we report that dual-strand cluster transcript export requires CG13741/Bootlegger and the Drosophila Nuclear export factor family protein, Nxf3. Bootlegger is specifically recruited to piRNA clusters and in turn brings Nxf3. We find that Nxf3 specifically binds to piRNA precursors and is essential for their export to piRNA biogenesis sites, a process that is critical for germline transposon silencing. Our data shed light on how dual-strand clusters bypass canonical mRNA features to be specifically exported via Nxf3, ensuring proper piRNA production.
2019-07-27 | GSE133528 | GEO
Project description:Here, we analyzed H3K9me3 derived from wild type ovarian tissue. Here we show that deposition of histone 3 lysine 9 by the methyltransferase dSETDB1 (egg) is required for piRNA cluster transcription. In the absence of dSETDB1, cluster precursor transcription collapses in germline and somatic gonadal cells and TEs are activated, resulting in germline loss and a block in germline stem cell differentiation. We propose that heterochromatin protects the germline by activating the piRNA pathway. Examination of H3K9me3 marks in the wild type gonad
2011-09-08 | E-GEOD-30157 | biostudies-arrayexpress
Project description:The piRNA pathway is a conserved small RNA-based immune system that protects animal germ cell genomes from the harmful effects of transposon mobilisation. In Drosophila ovaries, most piRNAs originate from dual-strand clusters, which generate piRNAs from both genomic strands. Dual-strand clusters use non-canonical transcription mechanisms. Although transcribed by RNA polymerase II, cluster transcripts lack splicing signatures and polyA tails. mRNA processing is important for general mRNA export mediated by Nuclear export factor 1. Although UAP56, a component of the transcription and export complex, has been implicated in piRNA precursor export, it remains unknown how dual-strand cluster transcripts are specifically targeted for piRNA biogenesis by export from the nucleus to cytoplasmic processing centers. Here we report that dual-strand cluster transcript export requires CG13741/Bootlegger and the Drosophila Nuclear export factor family protein, Nxf3. Bootlegger is specifically recruited to piRNA clusters and in turn brings Nxf3. We find that Nxf3 specifically binds to piRNA precursors and is essential for their export to piRNA biogenesis sites, a process that is critical for germline transposon silencing. Our data shed light on how dual-strand clusters bypass canonical mRNA features to be specifically exported via Nxf3, ensuring proper piRNA production
2019-07-29 | PXD014472 | Pride
Project description:Here, we analyzed two small RNA libraries derived from ovarian tissue mutant for either the Drosophila SETDB1 gene, or the Bam gene. Here we show that deposition of histone 3 lysine 9 by the methyltransferase dSETDB1 (egg) is required for piRNA cluster transcription. In the absence of dSETDB1, cluster precursor transcription collapses in germline and somatic gonadal cells and TEs are activated, resulting in germline loss and a block in germline stem cell differentiation. We propose that heterochromatin protects the germline by activating the piRNA pathway. Keyword : Epigenetics 2 libraries were analyzed, with 1 being a developmental control (Bam Mutant).
2011-08-15 | E-GEOD-30086 | biostudies-arrayexpress
Project description:The PIWI-interacting RNA (piRNA) pathway protects animal genome integrity in part through establishing repressive heterochromatin at transposon loci. Silencing requires piRNA- guided targeting of nuclear PIWI proteins to nascent transposon transcripts, yet the subsequent molecular events are not understood. Here, we identify SFiNX (Silencing Factor interacting Nuclear eXport variant), an interdependent protein complex required for Piwi-mediated co-transcriptional silencing in Drosophila. SFiNX consists of Nxf2-Nxt1, a gonad- specific variant of the heterodimeric mRNA export receptor Nxf1-Nxt1, and the Piwi-associated protein Panoramix. SFiNX mutant flies are sterile and exhibit transposon de-repression because piRNA-loaded Piwi is unable to establish heterochromatin. Within SFiNX, Panoramix recruits the cellular heterochromatin machinery, while Nxf2 binds the nascent target RNA and licenses co-transcriptional silencing. Our results reveal an unexpected, RNA-export independent role for Nxf2 in nuclear small RNA biology and suggest that NXF-variants, which have largely unknown function in animals, are functionally linked to the genome-transposon conflict.
2019-04-17 | GSE120617 | GEO
Project description:Here, we analyzed H3K9me3 derived from wild type ovarian tissue. Here we show that deposition of histone 3 lysine 9 by the methyltransferase dSETDB1 (egg) is required for piRNA cluster transcription. In the absence of dSETDB1, cluster precursor transcription collapses in germline and somatic gonadal cells and TEs are activated, resulting in germline loss and a block in germline stem cell differentiation. We propose that heterochromatin protects the germline by activating the piRNA pathway.
2011-09-08 | GSE30157 | GEO
Project description:Here, we analyzed two small RNA libraries derived from ovarian tissue mutant for either the Drosophila SETDB1 gene, or the Bam gene. Here we show that deposition of histone 3 lysine 9 by the methyltransferase dSETDB1 (egg) is required for piRNA cluster transcription. In the absence of dSETDB1, cluster precursor transcription collapses in germline and somatic gonadal cells and TEs are activated, resulting in germline loss and a block in germline stem cell differentiation. We propose that heterochromatin protects the germline by activating the piRNA pathway. Keyword : Epigenetics
2011-08-15 | GSE30086 | GEO