Untangling the web: The diverse functions of the PIWI/piRNA pathway

Mani, Subha; Juliano, Celina E.

doi:10.1002/mrd.22195

Cited by 96 publications

(101 citation statements)

References 248 publications

(442 reference statements)

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“…Beyond a handful of well-studied bilaterian models, very little is known about the localization of PIWI proteins (reviewed in ref. 34). Interestingly, Drosophila Piwi protein and the zebrafish PIWI protein Zili can be nuclear or cytoplasmic depending on the developmental stage (16,35).…”

Section: Discussionmentioning

confidence: 99%

“…Aside from Drosophila, genomic mapping of putative piRNAs in several other organisms also revealed very little enrichment for repeat sequences over total genomic content (reviewed in ref. 34). Therefore, when considering piRNAs associated with cytoplasmic PIWI proteins, our transcriptomemapping approach may be preferable to genomic mapping for drawing conclusions about the function of the pathway.…”

Section: Discussionmentioning

confidence: 99%

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PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells

Juliano

Reich

Liu

et al. 2013

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

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167

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PIWI proteins and their bound PIWI-interacting RNAs (piRNAs) are found in animal germlines and are essential for fertility, but their functions outside of the gonad are not well understood. The cnidarian Hydra is a simple metazoan with well-characterized stem/progenitor cells that provides a unique model for analysis of PIWI function. Here we report that Hydra has two PIWI proteins, Hydra PIWI (Hywi) and Hydra PIWI-like (Hyli), both of which are expressed in all Hydra stem/progenitor cells, but not in terminally differentiated cells. We identified ∼15 million piRNAs associated with Hywi and/or Hyli and found that they exhibit the ping-pong signature of piRNA biogenesis. Hydra PIWI proteins are strictly cytoplasmic and thus likely act as posttranscriptional regulators. To explore this function, we generated a Hydra transcriptome for piRNA mapping. piRNAs map to transposons with a 25-to 35-fold enrichment compared with the abundance of transposon transcripts. By sequencing the small RNAs specific to the interstitial, ectodermal, and endodermal lineages, we found that the targeting of transposons appears to be largely restricted to the interstitial lineage. We also identified putative nontransposon targets of the pathway unique to each lineage. Finally we demonstrate that hywi function is essential in the somatic epithelial lineages. This comprehensive analysis of the PIWI-piRNA pathway in the somatic stem/progenitor cells of a nonbilaterian animal suggests that this pathway originated with broader stem cell functionality.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells

Juliano

Reich

Liu

et al. 2013

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

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144

167

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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).…”

mentioning

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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Piwi regulates Vasa accumulation during embryogenesis in the sea urchin

Yajima

Gustafson

Song

et al. 2013

Developmental Dynamics

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Background Piwi proteins are essential for germ line development, stem cell maintenance, and more recently found to function in epigenetic and somatic gene regulation. In the sea urchin Strongylocentrotus purpuratus, two Piwi proteins, Seawi and Piwi-like1, have been identified, yet their functional contributions have not been reported. Result Here we found that Seawi protein was localized uniformly in the early embryo and then became enriched in the primordial germ cells (PGCs) (the small micromere lineage) from blastula stage and thereafter. Morpholino knockdown of Sp-seawi diminished PGC-specific localization of Seawi proteins, and altered expression of other germ line markers such as Vasa and Gustavus, but had no effect on Nanos. Further, Seawi knockdown transiently resulted in Vasa positive cell proliferation in the right coelomic pouch that appear to be derived from the small micromere lineage, yet they quickly disappeared with an indication of apoptosis by larval stage. Severe Seawi knockdown resulted in an increased number of apoptotic cells in the entire gut area. Piwi proteins appear to regulate PGC proliferation perhaps through control of Vasa accumulation. In this organism, Piwi is likely regulating mRNAs, not just transposons, and is potentially functioning both inside and outside of the germ line during embryogenesis.

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Untangling the web: The diverse functions of the PIWI/piRNA pathway

Cited by 96 publications

References 248 publications

PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells

PIWI proteins and PIWI-interacting RNAs function in Hydra somatic stem cells

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

Piwi regulates Vasa accumulation during embryogenesis in the sea urchin

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