PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression

Ku, Hsueh-Yen; Lin, Haifan

doi:10.1093/nsr/nwu014

Cited by 165 publications

(137 citation statements)

References 163 publications

(302 reference statements)

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“…At this time, our suggestion that Piwi-bound RNA is required for PHeMAAH is based solely on extrapolation of published evidence detailing Piwi-piRNA interactions (Le Thomas et al 2013;Mani and Juliano 2013;Ku and Lin 2014). We can only speculate on the identity of Piwi-associated RNAs that might be involved in PHeMAAH and whether these might be mature piRNAs or unprocessed nuclear transcripts.…”

Section: A Model For Hp1a-piwi Interaction In Phemaahmentioning

confidence: 95%

“…A member of the Argonaute protein family, Piwi is able to bind piRNAs and repress the mobilization of retrotransposons within the germline (Mani and Juliano 2013;Ku and Lin 2014). However, Piwi is also a recognized binding partner of HP1a (Brower-Toland et al 2007), plays a role in the establishment of heterochromatin during early embryogenesis (Gu and Elgin 2013), and is required for pairing-sensitive silencing (Grimaud et al 2006), a phenomenon that involves crosstalk between homologous chromosomes (Kassis 1994;Americo et al 2002).…”

Section: Piwi Protein Stably Associates With Oocyte Chromosomesmentioning

confidence: 99%

“…Piwi, a member of the Argonaute superfamily of proteins, is best known for its ability to bind Piwi-interacting RNAs (piRNAs) and prevent transposon mobilization in the germline (Mani and Juliano 2013;Ku and Lin 2014). Most piRNA sequences in the Drosophila genome map to heterochromatic regions (Saito et al 2006), and several lines of investigation have demonstrated that Piwi and HP1a can physically interact (Brower-Toland et al 2007;Mendez et al 2011).…”

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confidence: 99%

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Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Giauque¹,

Bickel

2016

Genetics

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Accurate segregation of homologous chromosomes during meiosis depends on their ability to remain physically connected throughout prophase I. For homologs that achieve a crossover, sister chromatid cohesion distal to the chiasma keeps them attached until anaphase I. However, in Drosophila melanogaster wild-type oocytes, chromosome 4 never recombines, and the X chromosome fails to cross over in 6-10% of oocytes. Proper segregation of these achiasmate homologs relies on their pericentric heterochromatin-mediated association, but the mechanism(s) underlying this attachment remains poorly understood. Using an inducible RNA interference (RNAi) strategy combined with fluorescence in situ hybridization (FISH) to monitor centromere proximal association of the achiasmate FM7a/X homolog pair, we asked whether specific heterochromatin-associated proteins are required for the association and proper segregation of achiasmate homologs in Drosophila oocytes. When we knock down HP1a, H3K9 methytransferases, or the HP1a binding partner Piwi during mid-prophase, we observe significant disruption of pericentric heterochromatin-mediated association of FM7a/X homologs. Furthermore, for both HP1a and Piwi knockdown oocytes, transgenic coexpression of the corresponding wild-type protein is able to rescue RNAi-induced defects, but expression of a mutant protein with a single amino acid change that disrupts the HP1a-Piwi interaction is unable to do so. We show that Piwi is stably bound to numerous sites along the meiotic chromosomes, including centromere proximal regions. In addition, reduction of HP1a or Piwi during meiotic prophase induces a significant increase in FM7a/X segregation errors. We present a speculative model outlining how HP1a and Piwi could collaborate to keep achiasmate chromosomes associated in a homology-dependent manner.

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Section: A Model For Hp1a-piwi Interaction In Phemaahmentioning

confidence: 95%

Section: Piwi Protein Stably Associates With Oocyte Chromosomesmentioning

confidence: 99%

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confidence: 99%

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Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Giauque¹,

Bickel

2016

Genetics

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“…1). Despite the relatively far phylogenetic distance, evidence for the majority of well-known fly and mammalian piRNA components (Ku and Lin 2014) could be found in the M. lignano genome and transcriptome (Supplemental Table 1). This suggests that a canonical piRNA pathway is likely to be operating in M. lignano.…”

Section: Macrostomum Lignano Has Conserved Small Rna Pathway Componentsmentioning

confidence: 99%

Dual functions of Macpiwi1 in transposon silencing and stem cell maintenance in the flatworm Macrostomum lignano

Zhou

Battistoni

Demerdash

et al. 2015

RNA

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PIWI proteins and piRNA pathways are essential for transposon silencing and some aspects of gene regulation during animal germline development. In contrast to most animal species, some flatworms also express PIWIs and piRNAs in somatic stem cells, where they are required for tissue renewal and regeneration. Here, we have identified and characterized piRNAs and PIWI proteins in the emerging model flatworm Macrostomum lignano. We found that M. lignano encodes at least three PIWI proteins. One of these, Macpiwi1, acts as a key component of the canonical piRNA pathway in the germline and in somatic stem cells. Knockdown of Macpiwi1 dramatically reduces piRNA levels, derepresses transposons, and severely impacts stem cell maintenance. Knockdown of the piRNA biogenesis factor Macvasa caused an even greater reduction in piRNA levels with a corresponding increase in transposons. Yet, in Macvasa knockdown animals, we detected no major impact on stem cell selfrenewal. These results may suggest stem cell maintenance functions of PIWI proteins in flatworms that are distinguishable from their impact on transposons and that might function independently of what are considered canonical piRNA populations.

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“…The primary function of piRNAs in bilaterians appears to be to silence of transposons within the germline (O'Donnell and Boeke 2007), however somatic piRNAs (Ross et al 2014) and piRNAs that function in mRNA translational control have also been identified , Saito et al 2009, Ku and Lin 2014.…”

Section: Rhoadesmentioning

confidence: 99%

RNA interference in early branching metazoans

Calcino¹

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The RNA interference (RNAi) repertoire of metazoans is principally composed of three independent but related systems -endogenous small interfering RNAs (endosiRNAs), micro RNAs (miRNAs) and Piwi-interacting RNAs (piRNAs). Although the endosiRNA pathway has been demonstrated in all five eukaryotic supergroups, the miRNA and piRNA pathways of metazoans likely evolved subsequent to metazoan divergence from other eukaryotes. These innovations evolved in a 100-200 million year period between the emergence of animal multicellularity and the divergence of the sponges. It is not yet known if the organisation and function of these systems, as characterised in bilaterian model species (vertebrates, Drosophila and C. elegans), is shared between early branching phyla (Porifera, Ctenophora, Cnidaria and Placozoa) and bilaterians. Preliminary evidence is mixed with commonalities like the existence of 'ping-pong' piRNA biogenesis in sponges and cnidarians contrasted with the lack of sequence and secondary structure homology of miRNAs between sponges and bilaterians.This thesis focuses on the RNAi systems of three early branching metazoan phyla that represent critical branches in early animal evolution (ie. Porifera, Ctenophora and Cnidaria). As no such tool was available, I developed a bioinformatic pipeline to annotate the RNAi components of mapped small RNA libraries from the demosponge Amphimedon queenslandica, the ctenophore Mnemiopsis leidyi and the cnidarian Nematostella vectensis. Detailed in Chapter 2, this pipeline, named RNAiTool, clusters mapped small RNAs from high-throughput sequencing data and then annotates those clusters based on a simple set of criteria, primarily focused on the read-length of the constituent small RNAs.RNAiTool was also used in the annotation of small RNA datasets from the well-studied bilaterian Drosophila melanogaster, providing a point of comparison for the less wellunderstood non-bilaterian species. As well as interrogating individual datasets, RNAiTool can be used to compare the expression dynamics of endo-siRNA and piRNA cluster between datasets. Although it was used here to investigate the expression dynamics of endo-siRNA and piRNA cluster through development, RNAiTool can be used to assess the expression dynamics of clusters between any test and control datasets.The second major innovation presented in this thesis is the introduction of the uniformity index. This property of small RNA clusters describes the uniformity of small RNA coverage across the length of that cluster. This simple index provides a rapid method 3 for the identification of potential miRNAs and other highly expressed small RNA producing loci from large pools of small RNA clusters. This thesis takes the first steps towards an understanding of the evolution and function of RNAi systems in early branching metazoans, in particular the demosponge A.queenslandica. It is hoped that the framework for RNAi annotation developed here will prove useful for other studies of emerging model RNAi systems. 4

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PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression

Cited by 165 publications

References 163 publications

Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Dual functions of Macpiwi1 in transposon silencing and stem cell maintenance in the flatworm Macrostomum lignano

RNA interference in early branching metazoans

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PIWI proteins and their interactors in piRNA biogenesis, germline development and gene expression

Cited by 165 publications

References 163 publications

Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Heterochromatin-Associated Proteins HP1a and Piwi Collaborate to Maintain the Association of Achiasmate Homologs in Drosophila Oocytes

Dual functions of Macpiwi1 in transposon silencing and stem cell maintenance in the flatworm Macrostomum lignano

﻿RNA interference in early branching metazoans

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RNA interference in early branching metazoans