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Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in Drosophila

Hur, Junho K. and Luo, Yicheng and Moon, Sungjin and Ninova, Maria and Marinov, Georgi K. and Chung, Yun D. and Aravin, Alexei A. (2016) Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in Drosophila. Genes and Development, 30 (7). pp. 840-855. ISSN 0890-9369. PMCID PMC4826399. https://resolver.caltech.edu/CaltechAUTHORS:20160425-132521525

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Abstract

The conserved THO/TREX (transcription/export) complex is critical for pre-mRNA processing and mRNA nuclear export. In metazoa, TREX is loaded on nascent RNA transcribed by RNA polymerase II in a splicing-dependent fashion; however, how TREX functions is poorly understood. Here we show that Thoc5 and other TREX components are essential for the biogenesis of piRNA, a distinct class of small noncoding RNAs that control expression of transposable elements (TEs) in the Drosophila germline. Mutations in TREX lead to defects in piRNA biogenesis, resulting in derepression of multiple TE families, gametogenesis defects, and sterility. TREX components are enriched on piRNA precursors transcribed from dual-strand piRNA clusters and colocalize in distinct nuclear foci that overlap with sites of piRNA transcription. The localization of TREX in nuclear foci and its loading on piRNA precursor transcripts depend on Cutoff, a protein associated with chromatin of piRNA clusters. Finally, we show that TREX is required for accumulation of nascent piRNA precursors. Our study reveals a novel splicing-independent mechanism for TREX loading on nascent RNA and its importance in piRNA biogenesis.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1101/gad.276030.115 DOIArticle
http://genesdev.cshlp.org/content/30/7/840.shortPublisherArticle
http://genesdev.cshlp.org/content/30/7/840/suppl/DC1PublisherSupplemental Material
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4826399/PubMed CentralArticle
ORCID:
AuthorORCID
Ninova, Maria0000-0001-5051-5502
Marinov, Georgi K.0000-0003-1822-7273
Additional Information:© 2016 Hur et al. This article is distributed exclusively by Cold Spring Harbor Laboratory Press for the first six months after the full-issue publication date (see http://genesdev.cshlp.org/site/misc/terms.xhtml). After six months, it is available under a Creative Commons License (Attribution-NonCommercial 4.0 International, as described at http://creativecommons.org/licenses/by-nc/4.0/. Received December 6, 2015; revised version accepted March 7, 2016. We greatly thank Katalin Fejes Toth for discussion and help with manuscript preparation.We thank members of the Aravin laboratory for discussion and comments on the manuscript. We thank Sergei Manakov for processing the RNA-seq data, and Jang-Hyun Oh for help in coimmunoprecipitation experiments. We thank Masakazu Hamada for establishing and optimizing the protocol for isolation of chromatin-associated RNA. We thank Long Cai and Kelly Burke for help with FISH. This work was supported by grants from the National Institutes of Health (R01 GM097363 and DP2 OD007371A) as well as by the Searle Scholar and the Packard Fellowship Awards to A.A.A., and the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT, and Future Planning (no. 2015R1A2A2A01003598) to Y.D.C.
Funders:
Funding AgencyGrant Number
NIHR01 GM097363
NIHDP2 OD007371A
Searle Scholars ProgramUNSPECIFIED
David and Lucile Packard FoundationUNSPECIFIED
National Research Foundation of KoreaUNSPECIFIED
Ministry of Science, ICT and Future Planning (Korea)2015R1A2A2A01003598
Subject Keywords:TREX; Thoc5; mRNA loading; piRNA biogenesis; transcriptional regulation
Issue or Number:7
PubMed Central ID:PMC4826399
Record Number:CaltechAUTHORS:20160425-132521525
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160425-132521525
Official Citation:Splicing-independent loading of TREX on nascent RNA is required for efficient expression of dual-strand piRNA clusters in Drosophila Junho K. Hur, Yicheng Luo, Sungjin Moon, Maria Ninova, Georgi K. Marinov, Yun D. Chung, and Alexei A. Aravin Genes Dev. April 1, 2016 30: 840-855; doi:10.1101/gad.276030.115
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:66455
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:02 May 2016 23:30
Last Modified:03 Oct 2019 09:56

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