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      DamID profiling of dynamic Polycomb-binding sites in Drosophila imaginal disc development and tumorigenesis

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          Abstract

          Background

          Tracking dynamic protein–chromatin interactions in vivo is key to unravel transcriptional and epigenetic transitions in development and disease. However, limited availability and heterogeneous tissue composition of in vivo source material impose challenges on many experimental approaches.

          Results

          Here we adapt cell-type-specific DamID-seq profiling for use in Drosophila imaginal discs and make FLP/FRT-based induction accessible to GAL driver-mediated targeting of specific cell lineages. In a proof-of-principle approach, we utilize ubiquitous DamID expression to describe dynamic transitions of Polycomb-binding sites during wing imaginal disc development and in a scrib tumorigenesis model. We identify Atf3 and Ets21C as novel Polycomb target genes involved in scrib tumorigenesis and suggest that target gene regulation by Atf3 and AP-1 transcription factors, as well as modulation of insulator function, plays crucial roles in dynamic Polycomb-binding at target sites. We establish these findings by DamID-seq analysis of wing imaginal disc samples derived from 10 larvae.

          Conclusions

          Our study opens avenues for robust profiling of small cell population in imaginal discs in vivo and provides insights into epigenetic changes underlying transcriptional responses to tumorigenic transformation.

          Electronic supplementary material

          The online version of this article (10.1186/s13072-018-0196-y) contains supplementary material, which is available to authorized users.

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          Most cited references55

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          Identification of functional elements and regulatory circuits by Drosophila modENCODE.

          To gain insight into how genomic information is translated into cellular and developmental programs, the Drosophila model organism Encyclopedia of DNA Elements (modENCODE) project is comprehensively mapping transcripts, histone modifications, chromosomal proteins, transcription factors, replication proteins and intermediates, and nucleosome properties across a developmental time course and in multiple cell lines. We have generated more than 700 data sets and discovered protein-coding, noncoding, RNA regulatory, replication, and chromatin elements, more than tripling the annotated portion of the Drosophila genome. Correlated activity patterns of these elements reveal a functional regulatory network, which predicts putative new functions for genes, reveals stage- and tissue-specific regulators, and enables gene-expression prediction. Our results provide a foundation for directed experimental and computational studies in Drosophila and related species and also a model for systematic data integration toward comprehensive genomic and functional annotation.
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            Comprehensive analysis of the chromatin landscape in Drosophila

            Summary Chromatin is composed of DNA and a variety of modified histones and non-histone proteins, which impact cell differentiation, gene regulation and other key cellular processes. We present a genome-wide chromatin landscape for Drosophila melanogaster based on 18 histone modifications, summarized by 9 prevalent combinatorial patterns. Integrative analysis with other data (non-histone chromatin proteins, DNaseI hypersensitivity, GRO-seq reads produced by engaged polymerase, short/long RNA products) reveals discrete characteristics of chromosomes, genes, regulatory elements, and other functional domains. We find that active genes display distinct chromatin signatures that are correlated with disparate gene lengths, exon patterns, regulatory functions, and genomic contexts. We also demonstrate a diversity of signatures among Polycomb targets that include a subset with paused polymerase. This systematic profiling and integrative analysis of chromatin signatures provides insights into how genomic elements are regulated, and will serve as a resource for future experimental investigations of genome structure and function.
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              Polycomb silencers control cell fate, development and cancer.

              Polycomb group (PcG) proteins are epigenetic gene silencers that are implicated in neoplastic development. Their oncogenic function might be associated with their well-established role in the maintenance of embryonic and adult stem cells. In this review, we discuss new insights into the possible mechanisms by which PcGs regulate cellular identity, and speculate how these functions might be relevant during tumorigenesis.
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                Author and article information

                Contributors
                (+49) 761 203 97190 , anne.classen@zbsa.uni-freiburg.de
                Journal
                Epigenetics Chromatin
                Epigenetics Chromatin
                Epigenetics & Chromatin
                BioMed Central (London )
                1756-8935
                5 June 2018
                5 June 2018
                2018
                : 11
                : 27
                Affiliations
                [1 ]ISNI 0000 0004 1936 973X, GRID grid.5252.0, Faculty of Biology, , Ludwig-Maximilians-University Munich, ; Grosshaderner Strasse 2-4, 82152 Planegg, Martinsried, Germany
                [2 ]ISNI 0000 0001 2156 2780, GRID grid.5801.c, Department of Environmental Systems Science, , ETH Zurich, ; Universitätstrasse 16, 8092 Zurich, Switzerland
                [3 ]ISNI 0000 0001 2156 2780, GRID grid.5801.c, Department of Health Sciences and Technology, , ETH Zurich, ; Schorenstrasse 16, 8603 Schwerzenbach, Switzerland
                [4 ]GRID grid.5963.9, Center for Biological Systems Analysis, , Albert-Ludwigs-University Freiburg, ; Habsburgerstrasse 49, 79104 Freiburg, Germany
                [5 ]ISNI 0000 0001 2254 1834, GRID grid.415877.8, Institute of Molecular and Cellular Biology, , Siberian Branch of Russian Academy of Sciences, ; Acad. Lavrentiev Ave. 8/2, Novosibirsk, 630090 Russia
                [6 ]ISNI 0000 0001 1014 0849, GRID grid.419491.0, Max-Delbrück-Center for Molecular Medicine (MDC), ; Robert-Rössle-Str. 10, 13092 Berlin, Germany
                [7 ]ISNI 0000 0004 1936 973X, GRID grid.5252.0, Laboratory for Functional Genome Analysis, Gene Center Munich, , Ludwig-Maximilians-University Munich, ; Feodor-Lynen-Str. 25, 81377 Munich, Germany
                [8 ]GRID grid.430814.a, Division Gene Regulation, , The Netherlands Cancer Institute, ; Plesmanlaan 121, 1066 CX Amsterdam, The Netherlands
                Author information
                http://orcid.org/0000-0001-5157-0749
                Article
                196
                10.1186/s13072-018-0196-y
                5987561
                29871666
                c01b4a4b-5ac1-4fc2-b397-83b58af253be
                © The Author(s) 2018

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                : 20 January 2018
                : 21 May 2018
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: CL490/1
                Award Recipient :
                Funded by: Russian Fundamental Scientific Research Program
                Award ID: 0310-2018-0009
                Award Recipient :
                Categories
                Research
                Custom metadata
                © The Author(s) 2018

                Genetics
                damid,wing imaginal disc,polycomb,scrib
                Genetics
                damid, wing imaginal disc, polycomb, scrib

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