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Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state

Le Thomas, Adrien and Rogers, Alicia K. and Webster, Alexandre and Marinov, Georgi K. and Liao, Susan E. and Perkins, Edward M. and Hur, Junho K. and Aravin, Alexei A. and Fejes Tóth, Katalin (2013) Piwi induces piRNA-guided transcriptional silencing and establishment of a repressive chromatin state. Genes and Development, 27 (4). pp. 390-399. ISSN 0890-9369. PMCID PMC3589556. https://resolver.caltech.edu/CaltechAUTHORS:20130408-133337079

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Abstract

In the metazoan germline, piwi proteins and associated piwi-interacting RNAs (piRNAs) provide a defense system against the expression of transposable elements. In the cytoplasm, piRNA sequences guide piwi complexes to destroy complementary transposon transcripts by endonucleolytic cleavage. However, some piwi family members are nuclear, raising the possibility of alternative pathways for piRNA-mediated regulation of gene expression. We found that Drosophila Piwi is recruited to chromatin, colocalizing with RNA polymerase II (Pol II) on polytene chromosomes. Knockdown of Piwi in the germline increases expression of transposable elements that are targeted by piRNAs, whereas protein-coding genes remain largely unaffected. Derepression of transposons upon Piwi depletion correlates with increased occupancy of Pol II on their promoters. Expression of piRNAs that target a reporter construct results in a decrease in Pol II occupancy and an increase in repressive H3K9me3 marks and heterochromatin protein 1 (HP1) on the reporter locus. Our results indicate that Piwi identifies targets complementary to the associated piRNA and induces transcriptional repression by establishing a repressive chromatin state when correct targets are found.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1101/gad.209841.112 DOIArticle
http://genesdev.cshlp.org/content/27/4/390PublisherArticle
Additional Information:© 2013 Cold Spring Harbor Laboratory Press. Received November 8, 2012; revised version accepted January 14, 2013. We are grateful to Evelyn Stuwe from the Aravin laboratory for purifying the GFP antibody; I. Antoshechkin of the Millard and Muriel Jacobs Genetics and Genomics Laboratory for sequencing; D. Trout, H. Amrhein, and S. Upchurch for computational assistance; the Bloomington Stock Center for fly stocks; and S. Hess, B. Graham, and M Sweredoski from the Proteome Exploration Laboratory at the Beckmann Institute, California Institute of Technology, for assistance with the mass spectrometry experiments. We thank members of the Aravin laboratory for critical comments on the manuscript. We thank Barbara Wold and members of the Wold laboratory for helpful discussions on ChIP protocols and analysis. A.K.R. and E.M.P. are supported by the Institutional Training Grant NIH/NRSA 5T32 GM07616, and E.M.P. is additionally supported by the Gordon Ross Medical Foundation. G.K.M. is supported by The Beckman Foundation, the Donald Bren Endowment, and NIH grant U54 HG004576. This work was supported by grants from the National Institutes of Health (R01 GM097363, R00 HD057233, and DP2 OD007371A to A.A.A.), the Searle Scholar Award (to A.A.A.), and the Ellison Medical Foundation New Scholar in Aging Award (to K.F.T.). Freely available online through the Genes & Development Open Access option.
Funders:
Funding AgencyGrant Number
NIH/NRSA Institutional Training Grant5T32 GM07616
Gordon Ross Medical FoundationUNSPECIFIED
Arnold and Mabel Beckman FoundationUNSPECIFIED
Donald Bren EndowmentUNSPECIFIED
NIHU54 HG004576
NIHR01 GM097363
NIHR00 HD057233
NIHDP2 OD007371A
Searle Scholar AwardUNSPECIFIED
Ellison Medical Foundation New Scholar in Aging AwardUNSPECIFIED
Subject Keywords:piRNA; Piwi; chromatin; RNA polymerase II; transcription; transposon
Issue or Number:4
PubMed Central ID:PMC3589556
Record Number:CaltechAUTHORS:20130408-133337079
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20130408-133337079
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:37810
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:08 Apr 2013 23:22
Last Modified:03 Oct 2019 04:51

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