The C. elegans CSR-1 argonaute pathway counteracts epigenetic silencing to promote germline gene expression

Developmental Cell
Meetu SethCraig C Mello

Abstract

Organisms can develop adaptive sequence-specific immunity by reexpressing pathogen-specific small RNAs that guide gene silencing. For example, the C. elegans PIWI-Argonaute/piwi-interacting RNA (piRNA) pathway recruits RNA-dependent RNA polymerase (RdRP) to foreign sequences to amplify a transgenerational small-RNA-induced epigenetic silencing signal (termed RNAe). Here, we provide evidence that, in addition to an adaptive memory of silenced sequences, C. elegans can also develop an opposing adaptive memory of expressed/self-mRNAs. We refer to this mechanism, which can prevent or reverse RNAe, as RNA-induced epigenetic gene activation (RNAa). We show that CSR-1, which engages RdRP-amplified small RNAs complementary to germline-expressed mRNAs, is required for RNAa. We show that a transgene with RNAa activity also exhibits accumulation of cognate CSR-1 small RNAs. Our findings suggest that C. elegans adaptively acquires and maintains a transgenerational CSR-1 memory that recognizes and protects self-mRNAs, allowing piRNAs to recognize foreign sequences innately, without the need for prior exposure

References

Sep 17, 2004·Nature·Zachary Lippman, Rob Martienssen
Dec 13, 2005·Microbiology and Molecular Biology Reviews : MMBR·Franklin M Harold
May 13, 2006·Current Genetics·Heriberto Cerutti, J Armando Casas-Mollano
Nov 4, 2006·Cell·Michael J AxtellDavid P Bartel
Nov 7, 2006·Proceedings of the National Academy of Sciences of the United States of America·Long-Cheng LiRajvir Dahiya
Dec 13, 2006·Science·Titia SijenRonald H A Plasterk
Jan 30, 2007·Nature Chemical Biology·Bethany A JanowskiDavid R Corey
Apr 21, 2007·Science·Susan Strome, Ruth Lehmann
May 25, 2007·Nature·Adrian Bird
May 25, 2007·Nature·Shiv I S Grewal, Sarah C R Elgin
May 25, 2007·Nature·Ian R Henderson, Steven E Jacobsen
Dec 25, 2007·Nature Reviews. Microbiology·Rotem SorekPhilip Hugenholtz
Jan 30, 2008·Proceedings of the National Academy of Sciences of the United States of America·Robert F PlaceRajvir Dahiya
Jul 26, 2008·Science·Shouhong GuangScott Kennedy
Jan 17, 2009·Nature Reviews. Genetics·Megha Ghildiyal, Phillip D Zamore
Jan 24, 2009·Proceedings of the National Academy of Sciences of the United States of America·Kenichi ShibuyaHiroshi Takatsuji
Mar 6, 2009·Genome Biology·Ben LangmeadSteven L Salzberg
Feb 6, 2010·Proceedings of the National Academy of Sciences of the United States of America·Colin C ConineCraig C Mello
Dec 27, 2011·Cell·Jaspreet S KhuranaWilliam E Theurkauf
Feb 1, 2012·Nature Reviews. Genetics·Lucia Daxinger, Emma Whitelaw
Jun 16, 2012·Science·Marloes P BagijnEric A Miska
Aug 2, 2012·The EMBO Journal·Maartje J LuteijnRené F Ketting
Feb 16, 2013·Trends in Genetics : TIG·Jana P Lim, Anne Brunet
Apr 2, 2013·Trends in Biochemical Sciences·Claus-D Kuhn, Leemor Joshua-Tor
May 15, 2013·Annual Review of Genomics and Human Genetics·Derek LessingJeannie T Lee
Dec 24, 2013·Developmental Cell·Christopher J WedelesJulie M Claycomb

❮ Previous
Next ❯

Citations

Apr 1, 2014·Epigenetics & Chromatin·William G Kelly
Apr 1, 2014·Nature Structural & Molecular Biology·Germano CecereAlla Grishok
Jun 21, 2014·Cell Research·Martine Simonelig
Sep 16, 2014·Cell Reports·Sergio Barberán-SolerJuan Valcárcel
Aug 25, 2015·ELife·Annalise B PaabyMatthew V Rockman
Jun 3, 2014·The Journal of Physiology·Mor SelaOded Rechavi
May 6, 2015·Proceedings of the National Academy of Sciences of the United States of America·Luciana E LeopoldShawn Ahmed
Feb 24, 2016·Cell Research·Victoria PortnoyLong-Cheng Li
Nov 20, 2015·Seminars in Cell & Developmental Biology·Robyn S M Lim, Toshie Kai
Sep 1, 2015·Seminars in Cell & Developmental Biology·Stéphane Ronsseray
Sep 1, 2015·Seminars in Cell & Developmental Biology·Janelle M Gabriel, Jay B Hollick
Jan 2, 2015·Scientific Reports·Daniel SchottCraig P Hunter
Jan 21, 2015·RNA Biology·Dan GuoLong-Cheng Li
May 27, 2014·Biochimica Et Biophysica Acta·Youngeun Choi, Susan E Mango
Aug 12, 2014·Biochemical Society Transactions·Monica J Piatek, Andreas Werner
Jun 23, 2015·Molecular Cell·Tomoko NotoKazufumi Mochizuki
Mar 10, 2015·Annual Review of Biochemistry·Yuka W IwasakiHaruhiko Siomi
Sep 26, 2014·Worm·Christopher J WedelesJulie M Claycomb
Oct 24, 2014·Worm·Suzanne W HoogstrateL Basten Snoek
Aug 6, 2014·Current Biology : CB·Julie M Claycomb
Dec 17, 2014·Frontiers in Genetics·Elaine M Youngman, Julie M Claycomb
Jan 3, 2015·Nature Reviews. Genetics·Daniel Holoch, Danesh Moazed
May 4, 2016·Current Opinion in Genetics & Development·Adam Klosin, Ben Lehner
Mar 27, 2015·PLoS Genetics·Alexandra SapetschnigEric A Miska
Jun 14, 2016·Developmental Dynamics : an Official Publication of the American Association of Anatomists·Ebru KaymakSean P Ryder
Sep 19, 2016·Journal of Experimental & Clinical Cancer Research : CR·Huan-Lei WuZhang-Qun Ye
Nov 1, 2016·Nature Reviews. Genetics·Jay B Hollick
May 28, 2014·Integrative and Comparative Biology·Pamela A PadillaLee S Toni
Feb 22, 2017·Biological Reviews of the Cambridge Philosophical Society·Yan WangZhongsheng Sun
Dec 29, 2013·Developmental Cell·Bruno F M de Albuquerque, René F Ketting
Jul 13, 2017·Antioxidants & Redox Signaling·Nihay Laham-KaramSeppo Ylä-Herttuala
Dec 21, 2018·Genes & Development·Chenchun WengEric A Miska

❮ Previous
Next ❯

Related Concepts

Related Feeds

Anthelmintics (ASM)

Anthelmintics or antihelminthics are a group of antiparasitic drugs that expel parasitic worms (helminths) and other internal parasites from the body by either stunning or killing them and without causing significant damage to the host. Discover the latest research on anthelmintics here.

Advanced Imaging of Cellular Signaling

Cell signaling is a vital mechanism for communication within cells and outside with the environment. Several different signaling pathways have been found and advanced imaging techniques are being developed to visualize the molecules involved in these signaling pathways. Find the latest research in advanced imaging of cellular signaling here.

Anthelmintics

Anthelmintics or antihelminthics are a group of antiparasitic drugs that expel parasitic worms (helminths) and other internal parasites from the body by either stunning or killing them and without causing significant damage to the host. Discover the latest research on anthelmintics here.

Cell Signaling & Cancer Epigenetics (Keystone)

Epigenetic changes are present and dysregulated in many cancers, including DNA methylation, non-coding RNA segments and post-translational protein modifications. This feed covers the latest research on signaling and epigenetics in cell growth and cancer.