Functional proteomics identified an upstream trancription complex promoting piRNA biogenesis
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ABSTRACT:
ORGANISM(S): Caenorhabditis elegans
PROVIDER: GSE112682 | GEO | 2019/04/04
REPOSITORIES: GEO
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Project description:Piwi-interacting RNAs (piRNAs) are genomically encoded small RNAs that engage Piwi Argonaute proteins to direct mRNA surveillance and transposon silencing. Despite advances in understanding piRNA pathways and functions, how the production of piRNA is regulated remains elusive. Here, using a genetic screen, we identify casein kinase II (CK2) as a factor required for piRNA pathway function. We show that CK2 is required for the localization of PRG-1 and for the proper localization of several factors that comprise the ‘upstream sequence transcription complex’ (USTC), which is required for piRNA transcription. Loss of CK2 impairs piRNA levels suggesting that CK2 promotes USTC function. We identify the USTC component twenty-one-U fouled-up 4 (TOFU-4) as a direct substrate for CK2. Our findings suggest that phosphorylation of TOFU-4 by CK2 promotes the assembly of USTC and piRNA transcription. Notably, during the aging process, CK2 activity declines, resulting in the disassembly of USTC, decreased piRNA production, and defects in piRNA-mediated gene silencing, including transposons silencing. These findings highlight the significance of posttranslational modification in regulating piRNA biogenesis and its implications for the aging process. Overall, our study provides compelling evidence for the involvement of a posttranslational modification mechanism in the regulation of piRNA biogenesis.
2024-07-01 | GSE239315 | GEO
Project description:Piwi-interacting RNAs (piRNAs) play significant roles in suppressing transposons and nonself nucleic acids, maintaining genome integrity, and defending against viral infections, and are essential for fertility in a variety of organisms. In C. elegans, most piRNA precursors are transcribed by RNA polymerase II in the nucleus and are subjected to a number of processing and maturation steps. However, the biogenesis of piRNAs is still not fully understood. We used functional proteomics to study piRNA biogenesis in C. elegans and identified a piRNA processing and chromosome segregation (PICS) complex. The PICS complex contains two known piRNA biogenesis factors, TOFU-6 and PID-1, and three new proteins PICS-1, TOST-1, and ERH-2, which exhibit dynamic localization among different subcellular compartments. In the germlines of gravid animals, the PICS complex contains TOFU-6/PICS-1/ERH-2/PID-1, is largely concentrated at the perinuclear granule zone and engages in piRNA processing. During early embryogenesis, the TOFU-6/PICS-1/ERH-2/TOST-1 complex accumulates in the nucleus and plays essential roles in chromosome segregation and cell division. Interestingly, the functions of these factors in mediating chromosome segregation are independent of piRNA production. Therefore, we speculate that differential compositions of PICS factors may help cells coordinate distinct cellular processes.
2019-05-19 | GSE130371 | GEO
Project description:Functional proteomics identified an upstream trancription complex promoting piRNA biogenesis
| PRJNA448738 | ENA
Project description:Piwi-interacting RNAs (piRNAs) play essential roles in silencing repetitive elements to promote fertility in metazoans. Nearly one-third of the ~15,000 piRNA loci in the C. elegans hermaphrodite are enriched during spermatogenesis, whereas >2,000 piRNAs are enriched during oogenesis. However, the mechanism underlying this sex-specific regulation is unknown. Here we identify SNPC-1.3, a variant of a conserved subunit of the snRNA activating protein complex, as a male-specific piRNA transcription factor. Binding of SNPC-1.3 at male piRNA loci drives spermatogenic piRNA transcription and requires the core piRNA transcription factor SNPC-4. Loss of snpc-1.3 leads to depletion of spermatogenic piRNAs and defects in male-dependent fertility. Furthermore, TRA-1, a master regulator of sex determination, binds to the snpc-1.3 promoter and represses its expression during oogenesis. Loss of TRA-1 targeting causes ectopic expression of snpc-1.3 and male piRNAs during oogenesis. Thus, sexual dimorphic regulation of snpc-1.3 coordinates male and female piRNA expression during germline development.
2020-12-17 | GSE152831 | GEO
Project description:Remarkably, tens of thousands of piwi-interacting RNAs (piRNAs) arise from a minimal number of discrete clustered regions in many organisms. However, it remains unclear if organization into these domains contributes to the highly coordinated, germline-specific expression of these small RNAs. Here, we show that SNPC-4, the DNA-binding subunit of the small nuclear RNA activating protein complex (SNAPc), binds piRNA clusters in a germline-specific manner and is required for global piRNA expression in C. elegans. Within piRNA domains, SNPC-4 not only binds at discrete sites through its established sequence motif, but also exhibits widely distributed binding across the region. Intriguingly, discrete peaks are not found at every piRNA, but instead occur frequently at Pol III-occupied tRNA genes, which have been previously implicated in chromatin organization. Given its unique binding pattern, we suggest that SNPC-4 promotes robust piRNA expression by establishing a permissive chromatin environment at clusters specifically in the germ line.
2014-11-17 | GSE53412 | GEO
Project description:Remarkably, tens of thousands of piwi-interacting RNAs (piRNAs) arise from a minimal number of discrete clustered regions in many organisms. However, it remains unclear if organization into these domains contributes to the highly coordinated, germline-specific expression of these small RNAs. Here, we show that SNPC-4, the DNA-binding subunit of the small nuclear RNA activating protein complex (SNAPc), binds piRNA clusters in a germline-specific manner and is required for global piRNA expression in C. elegans. Within piRNA domains, SNPC-4 not only binds at discrete sites through its established sequence motif, but also exhibits widely distributed binding across the region. Intriguingly, discrete peaks are not found at every piRNA, but instead occur frequently at Pol III-occupied tRNA genes, which have been previously implicated in chromatin organization. Given its unique binding pattern, we suggest that SNPC-4 promotes robust piRNA expression by establishing a permissive chromatin environment at clusters specifically in the germ line. This data submission includes a total of 11 ChIP-seq samples and 2 RNA-seq samples. The ChIP-seq samples include six timecourse samples (Emb-YA) and three tissue-specific samples (WA, GL, SO) for one factor called SNPC-4 (previously called GEI-11). The remaining two ChIP-seq samples are for pol II (AMA-1) and pol III (RPC-1) at one developmental stage. All of these samples were done in replicate, with inputs, yielding at least four sequencing files per sample. Some of the ChIP-seq samples already have fastq files submitted to GEO: (SNPC-4 EMB _GSE48744: GSM1183805, GSM1183806, GSM1183807, GSM1183808), (SNPC-4 L1_GSE48702: GSM1183629, GSM1183630, GSM1183631, GSM1183632), (SNPC-4 L2_GSE37809: GSM928364, GSM928365, GSM928366, GSM928367), (SNPC-4 L3_GSE35276: GSM864851, GSM864852, GSM864853, GSM864854), and (AMA-1_GSE15535: GSM389309, GSM389310, GSM389312, GSM389313). We are submitting fastq files for the remaining ChIP-seq datasets: SNPC-4 L4 - 4 files, SNPC-4 YA - 5 files, SNPC-4 WA - 4 files, SNPC-4 GL - 4 files, SNPC-4 SO - 4 files, and RPC-1 WA - 5 files. Thus we are submitting an additional 26 fastq files. Additionally, we are submitting processed files for all 11 datasets, consisting of one normalized file for the combined duplicate IP and one normalized file for the input sequence. In the case of the three tissue-specific samples for SNPC-4, we are submitting an additional processed (but not normalized) file that represents the IP data with input-subtracted. Thus, we are submitting a total of 25 processed files. NOTE: The processed files for the ChIP-seq samples that already have fastq files submitted to GEO (SNPC-4 EMB _GSE48744, etc.) are linked below as supplementary files at the foot of the Series record. The RNA-seq samples represent one control (control_RNAseq) and one treatment (SNPC-4(RNAi)_RNA-seq)and were not duplicated. We are submitting one fastq file for each, as well as one processed data file for each, for a total of 2 fastq and 2 processed data files.
2014-11-17 | E-GEOD-53412 | biostudies-arrayexpress
Project description:The piRNA pathway is a conserved germline-specific small RNA pathway that ensures genomic integrity and continued fertility. In C. elegans and other nematodes, Type-I piRNA precursor transcripts are expressed from >10,000 small, independently regulated genes clustered within two discrete domains of 1.5 and 3.5 MB on Chromosome IV. These large domains likely play a significant role in promoting germline-specific expression of piRNAs, but the underlying mechanisms are unclear. By examining the chromatin environment specifically in isolated germ nuclei, we demonstrate that piRNA clusters are located in closed chromatin, and confirm the enrichment for the inactive histone modification H3K27me3. The piRNA biogenesis factor USTC (Upstream Sequence Transcription Complex) plays two roles – it promotes a strong association of nucleosomes throughout the domain, and it organizes the local nucleosome environment to direct the exposure of individual piRNA genes. Overall, this work reveals new insight into how chromatin state coordinates transcriptional regulation over large genomic domains, which has implications for understanding global genome organization in the germ line.
2023-05-14 | GSE232141 | GEO
Project description:The piRNA pathway is a conserved germline-specific small RNA pathway that ensures genomic integrity and continued fertility. In C. elegans and other nematodes, Type-I piRNA precursor transcripts are expressed from >10,000 small, independently regulated genes clustered within two discrete domains of 1.5 and 3.5 MB on Chromosome IV. These large domains likely play a significant role in promoting germline-specific expression of piRNAs, but the underlying mechanisms are unclear. By examining the chromatin environment specifically in isolated germ nuclei, we demonstrate that piRNA clusters are located in closed chromatin, and confirm the enrichment for the inactive histone modification H3K27me3. The piRNA biogenesis factor USTC (Upstream Sequence Transcription Complex) plays two roles – it promotes a strong association of nucleosomes throughout the domain, and it organizes the local nucleosome environment to direct the exposure of individual piRNA genes. Overall, this work reveals new insight into how chromatin state coordinates transcriptional regulation over large genomic domains, which has implications for understanding global genome organization in the germ line.
2023-05-14 | GSE232139 | GEO
Project description:The piRNA pathway is a conserved germline-specific small RNA pathway that ensures genomic integrity and continued fertility. In C. elegans and other nematodes, Type-I piRNA precursor transcripts are expressed from >10,000 small, independently regulated genes clustered within two discrete domains of 1.5 and 3.5 MB on Chromosome IV. These large domains likely play a significant role in promoting germline-specific expression of piRNAs, but the underlying mechanisms are unclear. By examining the chromatin environment specifically in isolated germ nuclei, we demonstrate that piRNA clusters are located in closed chromatin, and confirm the enrichment for the inactive histone modification H3K27me3. The piRNA biogenesis factor USTC (Upstream Sequence Transcription Complex) plays two roles – it promotes a strong association of nucleosomes throughout the domain, and it organizes the local nucleosome environment to direct the exposure of individual piRNA genes. Overall, this work reveals new insight into how chromatin state coordinates transcriptional regulation over large genomic domains, which has implications for understanding global genome organization in the germ line.
2024-07-05 | GSE271339 | GEO
Project description:Casein kinase II promotes piRNA production through direct phosphorylation of USTC component TOFU-4
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