The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in <i>Drosophila melanogaster</i>

Szakmary, Akos; Reedy, Mary C.; Qi, Hongying; Lin, Haifan

doi:10.1083/jcb.200903034

Cited by 80 publications

(103 citation statements)

References 53 publications

(73 reference statements)

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“…Yb bodies are also present in niche cells (52), and their key component, the Yb protein, is indispensable for GSC maintenance (26,(52)(53)(54). Defects of GSC self-renewal observed in the Yb mutant ovaries lacking Yb bodies are very similar to those in piwi mutants (26,(52)(53)(54). Piwi protein is uniformly distributed throughout the cytoplasm of Yb-deficient somatic cells (24,26).…”

Section: Discussionmentioning

confidence: 54%

“…Presumably, the Yb body mediates piRNA biogenesis and loading into Piwi complexes, which is a prerequisite for Piwi nuclear import (24,25). Yb bodies are also present in niche cells (52), and their key component, the Yb protein, is indispensable for GSC maintenance (26,(52)(53)(54). Defects of GSC self-renewal observed in the Yb mutant ovaries lacking Yb bodies are very similar to those in piwi mutants (26,(52)(53)(54).…”

Section: Discussionmentioning

confidence: 59%

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Separation of stem cell maintenance and transposon silencing functions of Piwi protein

Klenov

Sokolova

Yakushev

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

169

165

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Piwi-interacting RNAs (piRNAs) and Piwi proteins have the evolutionarily conserved function of silencing of repetitive genetic elements in germ lines. The founder of the Piwi subfamily, Drosophila nuclear Piwi protein, was also shown to be required for the maintenance of germ-line stem cells (GSCs). Hence, null mutant piwi females exhibit two types of abnormalities, overexpression of transposons and severely underdeveloped ovaries. It remained unknown whether the failure of GSC maintenance is related to transposon derepression or if GSC self-renewal and piRNA silencing are two distinct functions of the Piwi protein. We have revealed a mutation, piwi Nt , removing the nuclear localization signal of the Piwi protein. piwi Nt females retain the ability of GSC self-renewal and a near-normal number of egg chambers in the ovarioles but display a drastic transposable element derepression and nuclear accumulation of their transcripts in the germ line. piwi Nt mutants are sterile most likely because of the disturbance of piRNA-mediated transposon silencing. Analysis of chromatin modifications in the piwi Nt ovaries indicated that Piwi causes chromatin silencing only of certain types of transposons, whereas others are repressed in the nuclei without their chromatin modification. Thus, Piwi nuclear localization that is required for its silencing function is not essential for the maintenance of GSCs. We suggest that the Piwi function in GSC selfrenewal is independent of transposon repression and is normally realized in the cytoplasm of GSC niche cells.oogenesis | short RNA

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Section: Discussionmentioning

confidence: 54%

Section: Discussionmentioning

confidence: 59%

Separation of stem cell maintenance and transposon silencing functions of Piwi protein

Klenov

Sokolova

Yakushev

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

169

165

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“…piRNA clusters give rise to long, single-stranded transcripts (Brennecke et al 2007) that are thought to be exported to the cytoplasm and processed into primary piRNAs, most likely in specialized cytoplasmic structures (Saito et al 2010;Handler et al 2011). A number of proteins have been implicated in primary piRNA biogenesis and their loading into PIWI-family proteins, including Armitage, Zucchini, Vreteno, and the Yb family (Klattenhoff et al 2007;Pane et al 2007;Szakmary et al 2009;Haase et al 2010;Olivieri et al 2010;Saito et al 2010;Handler et al 2011;Zamparini et al 2011). Yet, almost nothing is known about how each of these promotes the production of primary piRNAs.…”

Section: Introductionmentioning

confidence: 99%

shutdown is a component of the Drosophila piRNA biogenesis machinery

Preall¹,

Czech²,

Guzzardo³

et al. 2012

RNA

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In animals, the piRNA pathway preserves the integrity of gametic genomes, guarding them against the activity of mobile genetic elements. This innate immune mechanism relies on distinct genomic loci, termed piRNA clusters, to provide a molecular definition of transposons, enabling their discrimination from genes. piRNA clusters give rise to long, single-stranded precursors, which are processed into primary piRNAs through an unknown mechanism. These can engage in an adaptive amplification loop, the ping-pong cycle, to optimize the content of small RNA populations via the generation of secondary piRNAs. Many proteins have been ascribed functions in either primary biogenesis or the ping-pong cycle, though for the most part the molecular functions of proteins implicated in these pathways remain obscure. Here, we link shutdown (shu), a gene previously shown to be required for fertility in Drosophila, to the piRNA pathway. Analysis of knockdown phenotypes in both the germline and somatic compartments of the ovary demonstrate important roles for shutdown in both primary biogenesis and the ping-pong cycle. shutdown is a member of the FKBP family of immunophilins. Shu contains domains implicated in peptidyl-prolyl cis-trans isomerase activity and in the binding of HSP90-family chaperones, though the relevance of these domains to piRNA biogenesis is unknown.Keywords: piRNAs; transposon silencing; RNAi; FKBP; germ cells INTRODUCTIONEukaryotic genomes are prone to the accumulation of repetitive sequences, including transposable elements, over evolutionary time (McClintock 1953;Kim et al. 1994;Brennecke et al. 2007;Chambeyron et al. 2008;Feschotte 2008). The genomic instability brought about by transposon activity is a double-edged sword. Low levels of transposition can drive evolution in the long term, but loss of control over mobile elements in any individual can threaten reproductive success. Mechanisms for suppressing transposon activation in the germline are therefore both potent and widely conserved (Grimson et al. 2008). In animals, the PIWI-interacting RNA (piRNA) pathway is key to transposon silencing in reproductive tissues (Aravin et al. 2006;Girard et al. 2006;Lau et al. 2006;Vagin et al. 2006;Khurana and Theurkauf 2010;Senti and Brennecke 2010). In Drosophila, piRNAs are active both in the germ cell lineage and in a particular somatic lineage that encysts the germ cells and provides growth and maturation signals piRNA clusters sit at the apex of the pathway and, based upon their sequence content, define transposon targets for repression (Brennecke et al. 2007). piRNA clusters give rise to long, single-stranded transcripts (Brennecke et al. 2007) that are thought to be exported to the cytoplasm and processed into primary piRNAs, most likely in specialized cytoplasmic structures (Saito et al. 2010;Handler et al. 2011). A number of proteins have been implicated in primary piRNA biogenesis and their loading into PIWI-family proteins, including Armitage, Zucchini, Vreteno, and the Yb family (Klattenhoff et al...

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“…As Toshie Kai (Temasek Life Sciences Laboratory, Singapore) reminded us, this French term for 'cloud' describes electron-dense perinuclear structures that are a key cellular location for piRNA function. Another relevant cellular structure is the 'Yb body', which was recently inferred to be a location in which Piwi proteins are loaded (Siomi et al, 2011;Szakmary et al, 2009). Many proteins containing Tudor domains localize to nuage or Yb bodies and, importantly, are required for piRNA pathway function (Siomi et al, 2011).…”

Section: Tudor Domain Proteins and Pirnasmentioning

confidence: 99%

RNA silencing in Monterey

Rissland

Lai

2011

Development

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The tenth annual Keystone Symposium on the Mechanism and Biology of Silencing convened in Monterey, California, in March 2011. Those seeking some West Coast sunshine were, unfortunately, met with incessant precipitation throughout the meeting. Nevertheless, attendees were brightened by enlightening and vigorous scientific discussions. Here, we summarize the results presented at the meeting, which inspire and push this expanding field into new territories.

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The Yb protein defines a novel organelle and regulates male germline stem cell self-renewal in Drosophila melanogaster

Cited by 80 publications

References 53 publications

Separation of stem cell maintenance and transposon silencing functions of Piwi protein

Separation of stem cell maintenance and transposon silencing functions of Piwi protein

shutdown is a component of the Drosophila piRNA biogenesis machinery

RNA silencing in Monterey

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