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Epigenetics and Transgenerational Inheritance Emilie Brasset, S Epigenetics and transgenerational inheritance Emilie Brasset, S. Chambeyron To cite this version: Emilie Brasset, S. Chambeyron. Epigenetics and transgenerational inheritance. Genome Biology, BioMed Central, 2013, 14 (5), pp.306. 10.1186/gb-2013-14-5-306. hal-00852741 HAL Id: hal-00852741 https://hal.archives-ouvertes.fr/hal-00852741 Submitted on 3 Jun 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Brasset and Chambeyron Genome Biology 2013, 14:306 http://genomebiology.com/2013/14/5/306 MEETING REPORT Epigenetics and transgenerational inheritance Emilie Brasset1* and Séverine Chambeyron2* piRNAs are produced by two mechanisms: the primary Abstract processing pathway and secondary biogenesis, which is A report on the ‘Non-coding RNA, epigenetics and also called the ping-pong amplifi cation loop. Primary transgenerational inheritance’ meeting, Churchill piRNAs are likely processed from single-stranded College, Cambridge, UK, 11-12 April 2013. precursor transcripts that are encoded by heterochro- matic loci called piRNA clusters. Secondary piRNAs result from the processing of transposon mRNAs and Th e discovery of RNA interference in 1998 by Andrew piRNA clusters by an effi cient feed-forward amplifi cation Fire and Craig Mello revealed the complexity of gene loop. Mutation of piRNA pathway components in several regulation. Th e role of non-coding RNAs in post-trans- organisms (Bombyx, Drosophila, mice and zebrafi sh) has criptional gene silencing is well documented from plants provided a better understanding of their functions in the to vertebrates; conversely, their involvement in trans crip- piRNA biogenesis pathways. tional gene silencing by altering chromatin structure is Ramesh Pillai (European Molecular Biology Laboratory, well described in plants and Schizosaccharomyces pombe Grenoble, France) showed in both Bombyx mori and but has just started to be explored in metazoans. Th e goal Drosophila melanogaster that the DEAD box domain of of this meeting was to bring together scientists working an RNA helicase, Vasa, is required for disassembling the on the biogenesis of small non-coding RNAs and on their ribonucleoprotein complex during secondary biogenesis function as carriers of epigenetic information in fungi, of piRNAs. He also reported that a mouse Tudor- plants and animals. Here, we highlight the four major domain-containing protein, TDRD12, is needed for themes discussed at the meeting: the wide variety of secondary biogenesis. Emile Brasset (Auvergne Univer- biological functions undertaken by small non-coding sity, Clermont-Ferrand, France) reported diff erences in RNAs; the role of Piwi-interacting RNAs (piRNAs) in the spatio-temporal requirement of piRNA pathway com- RNA biogenesis and transposable element silencing; the ponents for TE silencing during Drosophila oogenesis roles of small non-coding RNAs in intercellular and using a sensor transgene based on the Idefi x transposon. systemic signaling; and transgenerational epigenetic Moreover, in the dividing cysts of the germarium, a inheritance. component of insect ovaries, she described a time window that she called the ‘piwiless pocket’, when low Piwi-interacting RNA biogenesis and transposable piwi expression correlates with loss of repression of the element silencing Idefi x sensor. It is well established that piRNAs bind Piwi proteins, To go further in understanding the piRNA pathway in which are members of the Argonaute family, and are zebrafi sh, René Ketting (Hubrecht Institute, the Nether- employed in the silencing of transposable elements (TEs). lands) studied Tdrd6, a newly identifi ed component of However, the mode of action and the function of the the piRNA pathway. Th is protein seems to be required piRNA pathway proteins remains elusive, possibly for the correct localization of the Argonaute-family because of their specifi c expression in the gonads, which protein Ziwi to the nuage, a perinuclear cytoplasmic makes piRNAs more diffi cult to study. structure, in embryos, but not for piRNA biogenesis, as only a minor piRNA loss was observed in mutants. Tdrd6 was also reported to be expressed in the ovarian ooplasm’s *Correspondence: [email protected]; [email protected] Balbiani body, a transient cytoplasmic structure com- 1 GReD - Inserm, U1103, CNRS UMR6293, Clermont Université, Université posed of various organelles. He proposed that Tdrd6 d’Auvergne, Faculté de Médecine, 28 place Henri Dunant, 63001 Clermont-Ferrand Cedex, France might be involved in maternal transcript inheritance. 2Institut de Génétique Humaine, Centre National de la Recherche Scientifi que, During spermatogenesis in mice, primordial germ cells 34396 Montpellier Cedex 5, France undergo massive epigenetic reprogramming as they colonize the fetal gonads, notably in the form of a © 2010 BioMed Central Ltd © 2013 BioMed Central Ltd genome-wide loss of DNA methylation, which correlates Brasset and Chambeyron Genome Biology 2013, 14:306 Page 2 of 3 http://genomebiology.com/2013/14/5/306 with TE expression. Fetal male germ cells specifically HRDE-1 as an actor of multigenerational RNAi inheri- express the Argonaute-family proteins Mili and Miwi2, tance that is essential to maintain the germ-cell lineage. which are responsible for the production of piRNAs In their model, the deficiency in the RNAi machinery through the degradation of transposon mRNAs. Donal could be correlated with a slow decrease of the H3K9me3 O’Carroll (EMBL, Monterotondo, Italy) described a repressive chromatin mark during several generations. conditional mili mutant in which slicer activity, which is Consequently, potentially toxic regions or genes may be required for the secondary piRNA processing mecha- transcribed over time, thus destabilizing germline stem nism, was substantially reduced in the pre-leptotene to cells. zygotene stages. He demonstrated that Mili slicer activity is not required for the repression of the L1 retro trans- Small non-coding RNAs in intercellular and poson during this time window. Transposon silencing is systemic signaling maintained by deposition of the H3K9me2 histone mark, Studies in plants, fission yeast and worms suggest that which is lost at the zygotene transition. He showed that RNA silencing requires mobile RNA regulators that L1 silencing requires the orchestration of three distinct move from cell to cell, and long distance silencing has mechanisms during spermatogenesis: DNA methylation, been shown in plants by grafting plants of one genotype histone methylation and post-transcriptional silencing by onto another. In Arabidopsis thaliana, long distance cell piRNAs. to cell mobility has been reported for various types of small non-coding RNAs, notably the 21- and 24-nucleotide Small non-coding RNAs: a wide repertoire of RNA species implicated in post-trans criptional regula- biological function tion and transcriptional silencing, respect ively. Using a In S. pombe, non-coding RNAs are involved in the for ma- potato grafting model, David Baulcombe (University of tion of constitutive heterochromatin at pericentromer ic Cambridge, UK) demonstrated that production of regions by orchestrating the deposition of hetero- 24-nucleotide small RNAs in the shoot can cause trans- chromatin marks. However, to maintain genome homeo- missible transcriptional gene silencing of a target stasis heterochromatin and euchromatin must be expressed in the tuber. This silencing was associated with partitioned; centromeric heterochromatin is demarcated promoter methylation in the grafted potatoes, indicating from euchromatin by transcriptionally active tRNA that the epigenome of a plant can be altered to create genes. Marc Bühler (Friedrich Miescher Institute, Basel, epigenetically modified plants. Grafting might be a new Switzerland) described a new class of small non-coding tool for transferring an epigenetic modifier (specifically, a RNAs that are produced at the edge of heterochromatin. small RNA) and thus to establish transcriptional silencing He suggested that their role was to counteract the by DNA methylation. spreading of heterochromatic regions that do not have The suggestion of a role for mobile small non-coding tRNA sequences. These new classes of 22-nucleotide- RNAs in gene silencing is also strengthened by work in long RNAs are not loaded onto Argonaute proteins, and nematodes. Miska and colleagues have addressed the they accumulate in dicer1 mutants. fundamental question of the possible functions for RNA Eric Miska (Gurdon Institute, University of Cambridge, interference in the life cycle of nematodes in the wild. UK) and Scott Kennedy (Laboratory of Genetics, Madison, Several clades of parasitic nematodes, including Brugia USA) reported the role of piRNAs in the regulation of malayi, live in symbiosis with intracellular bacteria such germinal transcripts in Caenorhabditis elegans. Using a as Wolbachia, whereas others, for instance Globodera transcriptomic approach Miska’s team showed that the pallida or Trichinella spiralis, are parasites of plants and transgenerational
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