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Casein kinase II promotes piRNA production through direct phosphorylation of USTC component TOFU-4

ABSTRACT: 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.

ORGANISM(S): Caenorhabditis elegans

PROVIDER: GSE239315 | GEO | 2024/07/01

REPOSITORIES: GEO

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Functional proteomics identified an upstream trancription complex promoting piRNA biogenesis

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2019-04-04 | GSE112682 | GEO

Functional proteomics identified a PICS complex required for piRNA maturation and chromosome segregation

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

A MILI-independent piRNA biogenesis pathway empowers partial germline reprogramming.

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2017-04-25 | E-MTAB-5561 | biostudies-arrayexpress

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2020-06-18 | PXD019087 | Pride

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2011-10-28 | E-MTAB-730 | biostudies-arrayexpress

The Function of Piwi is Independent of Its Slicer Activity

Project description:In diverse organisms, the highly-conserved Piwi proteins bind to a complex class of small non-coding RNAs called piRNAs, and are essential for germline stem cell maintenance, transposon silencing, fertility, and offspring viability1. By homology with other Argonautes, Piwi proteins have been proposed and later reported to possess endonuclease activity in vitro, effected by its conserved aspartate catalytic triad2,3. Indeed, mutation of these residues in one of the three mouse PIWI proteins, MILI, affects the production of Line 1 piRNAs and spermatogenesis4. In Drosophila, the conserved slicer function has been proposed to be crucial for all Piwi proteins in piRNA amplification and transposon silencing5. Here, we report in vivo evidence that, in contrast to common belief, the catalytic triad of Piwi is not required for the function of PIwi in the germline for stem cell maintenance, fertility, transposon silencing, or piRNA biogenesis. In addition, it is not required for piRNA biogenesis in the soma where Piwi is the sole Piwi-subfamily protein involved in the process. These observations, together with the recent findings on MILI and MIWI2 triad mutant, indicate that even though the slicer function may be required for a subset of piRNA-mediated process, it is overall inconsequential for the function of Piwi proteins Assess the role of the endonuclease activity of Piwi in all known biological processes that involve Piwi function in Drosophila ovary

2013-02-04 | E-GEOD-34032 | biostudies-arrayexpress

TEX15 is an essential executor of MIWI2-directed transposon DNA methylation and silencing.

2020-06-17 | E-MTAB-9090 | biostudies-arrayexpress

GLH/VASA helicases promote germ granule formation to ensure the fidelity of piRNA-mediated transcriptome surveillance

Project description:The ability to distinguish non-self from self is the key characteristic for any defense system. piRNAs function as guardians of the genome by silencing non-self nucleic acids and transposable elements in animals. Many piRNA factors are enriched in perinuclear germ granules, but whether their localization is required for piRNA biogenesis or function is not known. Here we show that GLH/VASA helicase mutants exhibit defects in forming perinuclear condensates containing PIWI and other small RNA cofactors. These mutant animals produce largely normal levels of piRNA but are defective in triggering piRNA silencing. Strikingly, while many piRNA targets are activated in GLH mutants, we observed that hundreds of endogenous genes are aberrantly silenced by piRNAs. This defect in self versus non-self recognition was also observed in other mutants where perinuclear P granules are disrupted. Together, our results argue that perinuclear germ granules function critically to promote the fidelity of piRNA-based transcriptome surveillance in C. elegans and preserve self versus non-self distinction.

2022-08-05 | PXD033506 | Pride

The Function of Piwi is Independent of Its Slicer Activity

2013-02-04 | GSE34032 | GEO

A critical role for nucleoporin 358 (Nup358) in transposon silencing and piRNA biogenesis in Drosophila [RNA-Seq]

Project description:Piwi-interacting RNAs (piRNAs) are a class of small non-coding RNAs that bind Piwi proteins to silence transposons and to regulate gene expression. In Drosophila germ cells, the Aubergine (Aub)-Argonaute 3 (Ago3)-dependent ping-pong cycle generates most germline piRNAs. Loading of anti-sense piRNAs amplified by this cycle enables Piwi to enter the nucleus and silence transposons. Nuclear localization is crucial for Piwi function in transposon silencing, but how this process is regulated remains unknown. It is also not known whether any of the components of the nuclear pore complex (NPC) directly function in the piRNA pathway. Here, we show that nucleoporin 358 (Nup358) and Piwi interact with each other and that a germline knockdown (GLKD) of Nup358 with short hairpin RNA prevents Piwi entry into the nucleus. The Nup358 GLKD also activated transposons, increased genomic instability, and derailed piRNA biogenesis because of a combination of decreased piRNA precursor transcription and a collapse of the ping-pong cycle. Our results point to a critical role for Nup358 in the piRNA pathway, laying the foundation for future studies to fully elucidate the mechanisms by which Nup358 contributes to piRNA biogenesis and transposon silencing.

2018-05-14 | GSE103564 | GEO

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