Nxf3: a middleman with the right connections for unspliced piRNA precursor export

Mendel, Mateusz; Pillai, Ramesh S.

doi:10.1101/gad.330530.119

Cited by 9 publications

(6 citation statements)

References 11 publications

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“…Discrete piRNA clusters on genomic locus are active in gonads, producing dual-strand piRNA precursors in germline cells or uni-strand piRNAs precursors in somatic gonadal cells (Gleason et al 2018; Ozata et al 2019). In germline cells, nascent piRNA precursors are transported from the nucleus to the perinuclear region in Nxf3-Nxt1 transport pathway (Kneuss et al 2019; ElMaghraby et al 2019; Mendel and Pillai 2019). There, those precursors and transposon RNAs are thought to be processed and/or cleaved in a unique membrane-less structure called nuage, composed of those RNAs, two PIWI family proteins, Aub and Ago3, and other relevant components; DExH-box ATP-binding RNA helicase Vasa (Vas), Spindle-E (Spn-E), and a group of Tudor domain-containing proteins (Tdrds), Krimper (Krimp), Tejas (Tej), Tudor, Tapas, Qin/Kumo, and Vreteno (Gillespie and Berg 1995; Liang, Diehl-Jones, and Lasko 1994; Brennecke et al 2007; Gunawardane et al 2007; Golumbeski et al 1991; Lim and Kai 2007; Patil and Kai 2010; Zamparini et al 2011; Anand and Kai 2012; Patil et al 2014).…”

Section: Introductionmentioning

confidence: 99%

Tejas functions as a core component of nuage assembly and precursor processing inDrosophilapiRNA biogenesis

Lin

Suyama

Kawaguchi

et al. 2022

Preprint

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Piwi-interacting RNAs (piRNAs), a class of 23- to 29-nt gonad-specific small RNAs, function to combat transposons in gonads. piRNAs are thought to be processed and amplified in membrane-less granules called nuage in germline cells. In Drosophila, two PIWI family proteins, several Tudor-domain containing (Tdrd) proteins and RNA helicases are assembled at perinuclear region of germline cells, forming nuage to process into piRNAs. Among those, Tejas (Tej), a fly homolog of mouse Tdrd5, has been known as a robust nuage component required for piRNA biogenesis in germline cells, yet its molecular functions remained elusive. To understand its molecular basis on nuage assembly and functions for piRNA biogenesis, we investigated subcellular localization of fluorescent-tagged nuage proteins including Tej and monitored the behavior of piRNA precursors. Tej functions as a core component for assembly of Vasa and Spindle-E to nuage granules through distinct motifs, respectively. The loss of Tej function resulted in malformation of nuage and accumulation of piRNA precursors en route in processing, perturbing further piRNA biogenesis in germline cells. Our study also revealed that the low complexity region of Tej regulates the mobility of nuage by phase separation. Collectively, we propose that Tej plays a pivotal role in processing of piRNA precursors by assembling RNA helicases, Vasa and Spindle-E, to nuage, by controlling the dynamics of nuage components.

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Section: Introductionmentioning

confidence: 99%

Tejas functions as a core component of nuage assembly and precursor processing inDrosophilapiRNA biogenesis

Lin

Suyama

Kawaguchi

et al. 2022

Preprint

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“…Vasa binds to cluster transcripts and localizes to nuage granules that are biased toward regions of the nuclear envelope opposite clusters (Zhang et al 2012), Localization of Vasa to the nucleus on heat shock thus raised the intriguing possibility that Vasa cycles between the nucleus and nuage, perhaps facilitating precursor delivery to nuage. Cluster transcripts are exported from the nucleus through a CRM1-dependent process (ElMaghraby et al 2019;Kneuss et al 2019;Mendel and Pillai 2019). We therefore treated live egg chambers expressing GFP-Vasa with the CRM-1 inhibitor Leptomycin B and assayed localization (Prasad et al 2007;Findley et al 2003).…”

Section: Heat Shock Control Of Cytoplasmic Pirna Machinerymentioning

confidence: 99%

“…The RDC complex, consisting of Rhino, Deadlock, and Cuff, drives transcription from both genomic strands, producing long un-spliced transcripts that are bound by the conserved THO complex and UAP56, which are components of the Transcription and Export (TREX) complex (Chen et al 2016;Mohn et al 2014;Zhang et al 2018;Zhang, Wang, et al 2014). piRNA cluster transcripts are transferred from TREX to a specialized noncanonical export system that includes the Drosophila specific Nxf3 protein and CRM1 (D. melanogaster gene embargoed) (ElMaghraby et al 2019;Kneuss et al 2019;Mendel and Pillai 2019). Following export, these transcripts undergo ping-pong and phased processing.…”

Section: Introductionmentioning

confidence: 99%

Rapid disassembly and Piwi-independent reassembly ofDrosophilapiRNA cluster heterochromatin following acute heat shock

Rice

Weng

et al. 2023

Preprint

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SummaryEnvironmental stress activates transposons and is proposed to generate genetic diversity that facilitates adaptive evolution. piRNAs guide germline transposon silencing, but the impact of stress on the piRNA pathway is not well understood. InDrosophila,the Rhino-Deadlock-Cuff complex (RDC) drives transcription of clusters composed of nested transposon fragments, generating precursors that are processed into mature piRNAs in the cytoplasm. We show that acute heat shock triggers rapid, reversable, loss of RDC localization and cluster transcript expression with coordinate changes in the cytoplasmic processing machinery. Maternal piRNAs bound to Piwi are proposed to guide Rhino localization to clusters during early embryogenesis. However, RDC re-localization after heat shock is accelerated inpiwimutants and delayed inthoc7mutants, which disrupt piRNA precursor binding to THO complex, and we show that maternally deposited piRNAs are dispensable for RDC localization to the major 42AB cluster. Cluster specification is reconsidered in light of these findings.

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“…Discrete piRNA clusters are active in gonads, where they produce dual-strand piRNA precursors in germline cells or unistrand piRNA precursors in somatic gonadal cells ( Gleason et al, 2018 ; Ozata et al, 2019 ). In germline cells, nascent piRNA precursors are transported to a unique, germline-specific membraneless structure called nuage in the perinuclear region via the Nxf3–Nxt1 pathway ( ElMaghraby et al, 2019 ; Kneuss et al, 2019 ; Mendel and Pillai, 2019 ). Nuage consists of precursors and transposon RNAs being processed, two PIWI family proteins—Aub and Ago3—and other relevant components, DEAD-box RNA helicase Vasa (Vas), DEAH box helicase RNA helicase Spindle-E (Spn-E), and a group of Tudor domain-containing proteins (Tdrds), Krimper (Krimp), Tejas (Tej), Tudor, Tapas (Tap), Qin/Kumo, and Vreteno ( Anand and Kai, 2012 ; Brennecke et al, 2007 ; Gillespie and Berg, 1995 ; Golumbeski et al, 1991 ; Gunawardane et al, 2007 ; Liang et al, 1994 ; Lim and Kai, 2007 ; Patil et al, 2014 ; Patil and Kai, 2010 ; Zamparini et al, 2011 ).…”

Section: Introductionmentioning

confidence: 99%

Tejas functions as a core component in nuage assembly and precursor processing in Drosophila piRNA biogenesis

Lin

Suyama

Kawaguchi

et al. 2023

Journal of Cell Biology

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PIWI-interacting RNAs (piRNAs), which protect genome from the attack by transposons, are produced and amplified in membraneless granules called nuage. In Drosophila, PIWI family proteins, Tudor-domain-containing (Tdrd) proteins, and RNA helicases are assembled and form nuage to ensure piRNA production. However, the molecular functions of the Tdrd protein Tejas (Tej) in piRNA biogenesis remain unknown. Here, we conduct a detailed analysis of the subcellular localization of fluorescently tagged nuage proteins and behavior of piRNA precursors. Our results demonstrate that Tej functions as a core component that recruits Vasa (Vas) and Spindle-E (Spn-E) into nuage granules through distinct motifs, thereby assembling nuage and engaging precursors for further processing. Our study also reveals that the low-complexity region of Tej regulates the mobility of Vas. Based on these results, we propose that Tej plays a pivotal role in piRNA precursor processing by assembling Vas and Spn-E into nuage and modulating the mobility of nuage components.

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Nxf3: a middleman with the right connections for unspliced piRNA precursor export

Cited by 9 publications

References 11 publications

Tejas functions as a core component of nuage assembly and precursor processing inDrosophilapiRNA biogenesis

Tejas functions as a core component of nuage assembly and precursor processing inDrosophilapiRNA biogenesis

Rapid disassembly and Piwi-independent reassembly ofDrosophilapiRNA cluster heterochromatin following acute heat shock

Tejas functions as a core component in nuage assembly and precursor processing in Drosophila piRNA biogenesis

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