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Stable Polycomb-dependent transgenerational inheritance of chromatin states in Drosophila

Ciabrelli, Filippo and Comoglio, Federico and Fellous, Simon and Bonev, Boyan and Ninova, Maria and Szabo, Quentin and Xuéreb, Anne and Klopp, Christophe and Aravin, Alexei and Paro, Renato and Bantignies, Frédéric and Cavalli, Giacomo (2017) Stable Polycomb-dependent transgenerational inheritance of chromatin states in Drosophila. Nature Genetics, 49 (6). pp. 876-886. ISSN 1061-4036.

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Transgenerational epigenetic inheritance (TEI) describes the transmission of alternative functional states through multiple generations in the presence of the same genomic DNA sequence. Very little is known about the principles and the molecular mechanisms governing this type of inheritance. Here, by transiently enhancing 3D chromatin interactions, we established stable and isogenic Drosophila epilines that carry alternative epialleles, as defined by differential levels of Polycomb-dependent trimethylation of histone H3 Lys27 (forming H3K27me3). After being established, epialleles can be dominantly transmitted to naive flies and can induce paramutation. Importantly, epilines can be reset to a naive state by disruption of chromatin interactions. Finally, we found that environmental changes modulate the expressivity of the epialleles, and we extended our paradigm to naturally occurring phenotypes. Our work sheds light on how nuclear organization and Polycomb group (PcG) proteins contribute to epigenetically inheritable phenotypic variability.

Item Type:Article
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URLURL TypeDescription ReadCube access
Comoglio, Federico0000-0002-8970-6610
Ninova, Maria0000-0001-5051-5502
Klopp, Christophe0000-0001-7126-5477
Paro, Renato0000-0003-3308-2965
Cavalli, Giacomo0000-0003-3709-3469
Additional Information:© 2017 Macmillan Publishers Limited, part of Springer Nature. Received 09 August 2016; Accepted 27 March 2017; Published online 24 April 2017. This study benefited from the CNRS human and technical resources allocated to the ECOTRONS Research Infrastructure as well as from the state allocation 'Investissement d'Avenir' AnaEE-France ANR-11-INBS-0001. We thank J. Roy, S. Devidal, A. Milcu, D. Landais, O. Ravel and A. Faez for assistance at the Ecotron-CNRS Facility in Montpellier; J. Foucaud, B. Serrate and A. Rombaut for assistance with conducting experiments on environmental effects in CBGP; J.-M. Chang and V. Loubiere for technical support; M. Siomi (Keio University) for providing the anti-Aubergine 4D10 antibody; and the Montpellier Ressources Imagerie facility MRI-IGH for microscopy support. F. Ciabrelli was supported by the Fondation pour la Recherche Médicale (FRM). F.B. was supported by CNRS. F. Comoglio was supported by ETH Zurich. B.B. was supported by the Sir Henry Wellcome Postdoctoral Fellowship (WT100136MA). The research of R.P. was supported by the FP7 European Network of Excellence EpiGeneSys, the Swiss National Science Foundation and ETH Zurich. M.N. and A.A. were supported by NIH R01 grant GM097363. Research in the laboratory of G.C. was supported by grants from the European Research Council (ERC-2008-AdG no. 232947), the CNRS, the FP7 European Network of Excellence EpiGeneSys, the European Union's Horizon 2020 Research and Innovation Programme under grant agreement 676556 (MuG), the Agence Nationale de la Recherche, the Fondation pour la Recherche Médicale, the INSERM, the French National Cancer Institute (INCa) and the Laboratory of Excellence EpiGenMed. Author Contributions: F. Ciabrelli and G.C. initiated and led the project. F. Ciabrelli designed and performed the experiments. F. Ciabrelli and G.C. interpreted the data. F. Ciabrelli and F.B. performed the FISH-I experiments. F. Ciabrelli, F.B. and Q.S. analyzed and interpreted the FISH-I data. F. Ciabrelli and F.B. performed the Antp[Ns] genetic crosses, scored the phenotypes and interpreted the data. F. Ciabrelli, S.F. and G.C. designed the experiments on environmental effects and interpreted the data. F. Ciabrelli, S.F. and A.X. performed the experiments on environmental effects. F. Comoglio analyzed genomic DNA sequencing data and performed bioinformatic analyses. C.K. analyzed sequencing data on the transgenic region. B.B. analyzed RNA-sequencing data and performed bioinformatic analyses. M.N. analyzed small-RNA-sequencing data and performed bioinformatic analyses. F. Ciabrelli, F.B., F. Comoglio, A.A., R.P. and G.C. wrote the manuscript. All the authors reviewed and commented on the manuscript. The authors declare no competing financial interests.
Funding AgencyGrant Number
Agence Nationale pour la Recherche (ANR)ANR-11-INBS-0001
Fondation pour la Recherche MédicaleUNSPECIFIED
Centre National de la Recherche Scientifique (CNRS)UNSPECIFIED
Wellcome TrustWT100136MA
European UnionEpiGeneSys
Swiss National Science Foundation (SNSF)UNSPECIFIED
NIHR01 GM097363
European Research Council (ERC)232947
European Research Council (ERC)676556
Institut national de la santé et de la recherche médicale (INSERM)UNSPECIFIED
Institut National du CancerUNSPECIFIED
Laboratory of ExcellenceEpiGenMed
Issue or Number:6
Record Number:CaltechAUTHORS:20170504-075656920
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Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:77184
Deposited By: Tony Diaz
Deposited On:04 May 2017 16:06
Last Modified:03 Oct 2019 17:54

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