RNA helicase Spn-E is required to maintain Aub and AGO3 protein levels for piRNA silencing in the germline of Drosophila

Ryazansky, Sergei; Kotov, A. A.; Kibanov, Mikhail V.; Akulenko, Natalia; Korbut, Alina P.; Lavrov, Sergey; Гвоздев, В. А.; Olenina, Ludmila V.

doi:10.1016/j.ejcb.2016.06.001

Cited by 14 publications

(11 citation statements)

References 53 publications

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“…However, in contrast to previously published observation (12), our results indicate that the ∼76% sequence identity between AT-chX piRNAs and vasa was not sufficient for effective repression of vasa in the testes of D. melanogaster or interspecies hybrids (Supplementary Table S3 and Figure 4C–E). In agreement with this conclusion, the spn-E mutation, which disrupts piRNA biogenesis in the germline (52), did not influence vasa transcription or translation of vasa as would be expected if the AT-chX piRNAs mediated vasa repression. In contrast, strong repression was associated with generation of secondary piRNAs when the level of sequence identity between the target and piRNA is at least 90% as in the case of Su(Ste) piRNAs targeting Stellate (Supplementary Table S5) and in the case of AT-chX piRNAs targeting vasa of D. mauritiana across the melanogaster–mauritiana species barrier (Figure 5 and Supplementary Table S7).…”

Section: Discussionsupporting

confidence: 77%

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

Kotov

Adashev

Godneeva

et al. 2019

Nucleic Acids Research

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The piRNA pathway is an adaptive mechanism that maintains genome stability by repression of selfish genomic elements. In the male germline of Drosophila melanogaster repression of Stellate genes by piRNAs generated from Supressor of Stellate ( Su(Ste) ) locus is required for male fertility, but both Su(Ste) piRNAs and their targets are absent in other Drosophila species. We found that D. melanogaster genome contains multiple X-linked non-coding genomic repeats that have sequence similarity to the protein-coding host gene vasa . In the male germline, these vasa -related AT-chX repeats produce abundant piRNAs that are antisense to vasa ; however, vasa mRNA escapes silencing due to imperfect complementarity to AT-chX piRNAs. Unexpectedly, we discovered AT-chX piRNAs target vasa of Drosophila mauritiana in the testes of interspecies hybrids. In the majority of hybrid flies, the testes were strongly reduced in size and germline content. A minority of hybrids maintained wild-type array of premeiotic germ cells in the testes, but in them harmful Stellate genes were derepressed due to the absence of Su(Ste) piRNAs, and meiotic failures were observed. Thus, the piRNA pathway contributes to reproductive isolation between D. melanogaster and closely related species, causing hybrid male sterility via misregulation of two different host protein factors.

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Section: Discussionsupporting

confidence: 77%

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

Kotov

Adashev

Godneeva

et al. 2019

Nucleic Acids Research

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“…Nuage structures are close to the cytoplasmic face of nuclear pores and are sites where the ping-pong cycle occurs and TE silencing takes place. These reports indicated that SpnE was not required for nuage assembly and that SpnE was required for maintenance of Aub and Ago3 protein levels, but not for transcription of these genes [ 35 , 52 ]. In D. melanogaster mutant for SpnE WNV replication increased compared to control flies which suggested an antiviral activity of SpnE in this model via a RNAi-dependent mechanism; however, this was not directly shown [ 36 ].…”

Section: Discussionmentioning

confidence: 99%

Spindle-E Acts Antivirally Against Alphaviruses in Mosquito Cells

Varjak

Dietrich

Sreenu

et al. 2018

Viruses

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Mosquitoes transmit several human- and animal-pathogenic alphaviruses (Togaviridae family). In alphavirus-infected mosquito cells two different types of virus-specific small RNAs are produced as part of the RNA interference response: short-interfering (si)RNAs and PIWI-interacting (pi)RNAs. The siRNA pathway is generally thought to be the main antiviral pathway. Although an antiviral activity has been suggested for the piRNA pathway its role in host defences is not clear. Knock down of key proteins of the piRNA pathway (Ago3 and Piwi5) in Aedes aegypti-derived cells reduced the production of alphavirus chikungunya virus (CHIKV)-specific piRNAs but had no effect on virus replication. In contrast, knock down of the siRNA pathway key protein Ago2 resulted in an increase in virus replication. Similar results were obtained when expression of Piwi4 was silenced. Knock down of the helicase Spindle-E (SpnE), an essential co-factor of the piRNA pathway in Drosophila melanogaster, resulted in increased virus replication indicating that SpnE acts as an antiviral against alphaviruses such as CHIKV and the related Semliki Forest virus (SFV). Surprisingly, this effect was found to be independent of the siRNA and piRNA pathways in Ae. aegypti cells and specific for alphaviruses. This suggests a small RNA-independent antiviral function for this protein in mosquitoes.

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“…The interface between nuage and the nucleus has been shown to be critical for piRNA biogenesis and transposon target recognition and repression. Although nuage has been characterized as a static and longterm platform for piRNA biogenesis, individual nuage components, such as Aub and Ago3, are dynamically shuttled in and out of nuage [1,6,[19][20][21]. Unlike Aub and Ago3, Piwi shows predominantly nuclear localization [22] and has not been well-characterized within the context of nuage.…”

Section: Introductionmentioning

confidence: 99%

A kinesin Klp10A mediates cell cycle-dependent shuttling of Piwi between nucleus and nuage

et al. 2020

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The piRNA pathway protects germline genomes from selfish genetic elements (e.g. transposons) through their transcript cleavage in the cytoplasm and/or their transcriptional silencing in the nucleus. Here, we describe a mechanism by which the nuclear and cytoplasmic arms of the piRNA pathway are linked. We find that during mitosis of Drosophila spermatogonia, nuclear Piwi interacts with nuage, the compartment that mediates the cytoplasmic arm of the piRNA pathway. At the end of mitosis, Piwi leaves nuage to return to the nucleus. Dissociation of Piwi from nuage occurs at the depolymerizing microtubules of the central spindle, mediated by a microtubule-depolymerizing kinesin, Klp10A. Depletion of klp10A delays the return of Piwi to the nucleus and affects piRNA production, suggesting the role of nuclearcytoplasmic communication in piRNA biogenesis. We propose that cell cycle-dependent communication between the nuclear and cytoplasmic arms of the piRNA pathway may play a previously unappreciated role in piRNA regulation.

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RNA helicase Spn-E is required to maintain Aub and AGO3 protein levels for piRNA silencing in the germline of Drosophila

Cited by 14 publications

References 53 publications

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

piRNA silencing contributes to interspecies hybrid sterility and reproductive isolation in Drosophila melanogaster

Spindle-E Acts Antivirally Against Alphaviruses in Mosquito Cells

A kinesin Klp10A mediates cell cycle-dependent shuttling of Piwi between nucleus and nuage

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