The piRNA pathway in planarian flatworms: new model, new insights

Kim, Iana V; Riedelbauch, Sebastian; Kuhn, Claus-D.

doi:10.1515/hsz-2019-0445

Cited by 12 publications

(10 citation statements)

References 171 publications

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“…The expression of piRNAs and the machinery required for their synthesis and action in somatic cells is controversial and the subject of debate (24, 27, 29). piRNAs have been also reported in a small number of somatic cells such as cancer cells (Mei et al, 2013) and regenerative stem-like cells in invertebrates (57). For example, PIWI-like proteins and piRNAs have been identified in somatic cells of the Cnidarian Hydra and the flatworm Macrostomum, although it is thought that their expression is restricted to stem-like progenitor cells that have the capacity to regenerate all cell types of the animal including gonad (58, 59).…”

Section: Discussionmentioning

confidence: 99%

Somatic piRNAs and Transposons are Differentially Regulated During Skeletal Muscle Atrophy and Programmed Cell Death

Tsuji

Thomson

Brown

et al. 2021

Preprint

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PiWi-interacting RNAs (piRNAs) are small single-stranded RNAs that can repress transposon expression via epigenetic silencing and transcript degradation. They have been identified predominantly in the ovary and testis, where they serve essential roles in transposon silencing in order to protect the integrity of the genome in the germline. The potential expression of piRNAs in somatic cells has been controversial. In the present study we demonstrate the expression of piRNAs derived from both genic and transposon RNAs in the intersegmental muscles (ISMs) from the tobacco hawkmoth Manduca sexta. These piRNAs are abundantly expressed, are ~27 nt long, map antisense to transposons, are oxidation resistant, exhibit a uridine bias at their first nucleotide, and amplify via the canonical ping-pong pathway. An RNA-seq analysis demonstrated that 20 piRNA pathway genes are expressed in the ISMs and are developmentally regulated. The abundance of piRNAs does not change when the muscles initiate developmentally-regulated atrophy, but are repressed when cells become committed to undergo programmed cell death at the end of metamorphosis. This change in piRNA expression is associated with the targeted repression of several retrotransposons and the induction of specific DNA transposons. The developmental changes in the expression of piRNAs, piRNA pathway genes, and transposons are all regulated by 20-hydroxyecdysone, the steroid hormone that controls the timing of ISM death. Taken together, these data provide compelling evidence for the existence of piRNA in somatic tissues and suggest that they may play roles in developmental processes such as programmed cell death.Author SummarypiRNAs are a class of small non-coding RNAs that suppress the expression of transposable elements, parasitic DNA that if reintegrated, can harm the integrity of the host genome. The expression of piRNAs and their associated regulatory proteins has been studied predominantly in germ cells and some stem cells. We have found that they are also expressed in skeletal muscles in the moth Manduca sexta that undergo developmentally-regulated atrophy and programmed cell death at the end of metamorphosis. The expression of transposons becomes deregulated when the muscles become committed to die, which may play a functional role in the demise of the cell by inducing genome damage. piRNA-mediated control of transposons may represent a novel mechanism that contributes to the regulated death of highly differentiated somatic cells.

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Section: Discussionmentioning

confidence: 99%

Somatic piRNAs and Transposons are Differentially Regulated During Skeletal Muscle Atrophy and Programmed Cell Death

Tsuji

Thomson

Brown

et al. 2021

Preprint

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“…The highest levels of piwi-1 are found in epidermal progenitors and tetraspanin-1-positive neoblasts. Differentiation of pluripotent neoblasts into fate-determined progenitors and terminally differentiated cells is accompanied by a successive reduction of piwi-1 levels (Kim et al, 2020). In M. lignano, piwi-1 (Mli034222) but not piwi-2 (Mli016226) was found to be involved in the piRNA pathway in both germline and somatic cells, as well as in the maintenance of stem cells (Zhou et al, 2015).…”

Section: The Argonaute Gene Familymentioning

confidence: 99%

“…The FLiwi cluster showed several independent gene duplications that have probably occurred after speciation, although we cannot rule out that gene duplications might be overestimated in those species in those species for which only transcriptomic data is available. We cannot rule out that transcripts from different genes were counted as one if the sequences were too similar due to very recent gene duplication events, as was the case for S. mediterranea's FLiwis (Kim et al, 2020). Interestingly, S. mediterranea displayed the widest expansion of FLiwis (Figure 4 dark green arch).…”

Section: Amplifications In the Argonaute Family Show Differential Distributions Across Flatwormsmentioning

confidence: 99%

“…Here, eight genes clustered in this group, some with identical sequences that can be collapsed to five quite similar genes (SmeT032534, SmeT030029, SmeT030034 and SmeT030033 present >99% identity). Whether these are functional genes or represent transcribed pseudogenes remains unknown (Kim et al, 2020). Interestingly, single Ago (Sle67413) and Piwi (Sle58342) genes can be detected in the catenulid S. leucops, that generally is placed outside of the clades from other flatworms.…”

Section: Amplifications In the Argonaute Family Show Differential Distributions Across Flatwormsmentioning

confidence: 99%

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Lost and Found: Piwi and Argonaute Pathways in Flatworms

Fontenla

Rinaldi

Tort

2021

Front. Cell. Infect. Microbiol.

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Platyhelminthes comprise one of the major phyla of invertebrate animals, inhabiting a wide range of ecosystems, and one of the most successful in adapting to parasitic life. Small non-coding RNAs have been implicated in regulating complex developmental transitions in model parasitic species. Notably, parasitic flatworms have lost Piwi RNA pathways but gained a novel Argonaute gene. Herein, we analyzed, contrasted and compared the conservation of small RNA pathways among several free-living species (a paraphyletic group traditionally known as ‘turbellarians’) and parasitic species (organized in the monophyletic clade Neodermata) to disentangle possible adaptations during the transition to parasitism. Our findings showed that complete miRNA and RNAi pathways are present in all analyzed free-living flatworms. Remarkably, whilst all ‘turbellarians’ have Piwi proteins, these were lost in parasitic Neodermantans. Moreover, two clusters of Piwi class Argonaute genes are present in all ‘turbellarians’. Interestingly, we identified a divergent Piwi class Argonaute in free living flatworms exclusively, which we named ‘Fliwi’. In addition, other key proteins of the Piwi pathways were conserved in ‘turbellarians’, while none of them were detected in Neodermatans. Besides Piwi and the canonical Argonaute proteins, a flatworm-specific class of Argonautes (FL-Ago) was identified in the analyzed species confirming its ancestrallity to all Platyhelminthes. Remarkably, this clade was expanded in parasitic Neodermatans, but not in free-living species. These phyla-specific Argonautes showed lower sequence conservation compared to other Argonaute proteins, suggesting that they might have been subjected to high evolutionary rates. However, key residues involved in the interaction with the small RNA and mRNA cleavage in the canonical Argonautes were more conserved in the FL-Agos than in the Piwi Argonautes. Whether this is related to specialized functions and adaptations to parasitism in Neodermatans remains unclear. In conclusion, differences detected in gene conservation, sequence and structure of the Argonaute family suggest tentative biological and evolutionary diversifications that are unique to Platyhelminthes. The remarkable divergencies in the small RNA pathways between free-living and parasitic flatworms indicate that they may have been involved in the adaptation to parasitism of Neodermatans.

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“…Some AGO members are present in the germline, bind repeat‐derived small RNAs, and are required for fertility (Borges & Martienssen, 2015 ; Araki et al , 2020 ). In rare animals, such as mosquitoes, planarians, and Aplysia, some PIWI members are present outside of the germlines and are loaded with small RNAs that can map to transposons (Rajasethupathy et al , 2012 ; Shibata et al , 2016 ; Halbach et al , 2020 ; Kim et al , 2020 ). Tetrahymena expresses PIWI proteins, which bind to small RNAs that are produced in a Dicer‐dependent manner (Mochizuki et al , 2002 ; Mochizuki, 2005 ).…”

Section: Introductionmentioning

confidence: 99%

piRNA‐ and siRNA‐mediated transcriptional repression in Drosophila , mice, and yeast: new insights and biodiversity

2021

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The PIWI-interacting RNA (piRNA) pathway acts as a self-defense mechanism against transposons to maintain germline genome integrity. Failures in the piRNA pathway cause DNA damage in the germline genome, disturbing inheritance of "correct" genetic information by the next generations and leading to infertility. piRNAs execute transposon repression in two ways: degrading their RNA transcripts and compacting the genomic loci via heterochromatinization. The former event is mechanistically similar to siRNAmediated RNA cleavage that occurs in the cytoplasm and has been investigated in many species including nematodes, fruit flies, and mammals. The latter event seems to be mechanistically parallel to siRNA-centered kinetochore assembly and subsequent chromosome segregation, which has so far been studied particularly in fission yeast. Despite the interspecies conservations, the overall schemes of the nuclear events show clear biodiversity across species. In this review, we summarize the recent progress regarding piRNAmediated transcriptional silencing in Drosophila and discuss the biodiversity by comparing it with the equivalent piRNA-mediated system in mice and the siRNA-mediated system in fission yeast.

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The piRNA pathway in planarian flatworms: new model, new insights

Cited by 12 publications

References 171 publications

Somatic piRNAs and Transposons are Differentially Regulated During Skeletal Muscle Atrophy and Programmed Cell Death

Somatic piRNAs and Transposons are Differentially Regulated During Skeletal Muscle Atrophy and Programmed Cell Death

Lost and Found: Piwi and Argonaute Pathways in Flatworms

piRNA‐ and siRNA‐mediated transcriptional repression in Drosophila , mice, and yeast: new insights and biodiversity

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