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      Chromatin changes in Anopheles gambiae induced by Plasmodium falciparum infection

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          Abstract

          Background

          Infection by the human malaria parasite leads to important changes in mosquito phenotypic traits related to vector competence. However, we still lack a clear understanding of the underlying mechanisms and, in particular, of the epigenetic basis for these changes. We have examined genome-wide distribution maps of H3K27ac, H3K9ac, H3K9me3 and H3K4me3 by ChIP-seq and the transcriptome by RNA-seq, of midguts from Anopheles gambiae mosquitoes blood-fed uninfected and infected with natural isolates of the human malaria parasite Plasmodium falciparum in Burkina Faso.

          Results

          We report 15,916 regions containing differential histone modification enrichment between infected and uninfected, of which 8339 locate at promoters and/or intersect with genes. The functional annotation of these regions allowed us to identify infection-responsive genes showing differential enrichment in various histone modifications, such as CLIP proteases, antimicrobial peptides-encoding genes, and genes related to melanization responses and the complement system. Further, the motif analysis of regions differentially enriched in various histone modifications predicts binding sites that might be involved in the cis-regulation of these regions, such as Deaf1, Pangolin and Dorsal transcription factors (TFs). Some of these TFs are known to regulate immunity gene expression in Drosophila and are involved in the Notch and JAK/STAT signaling pathways.

          Conclusions

          The analysis of malaria infection-induced chromatin changes in mosquitoes is important not only to identify regulatory elements and genes underlying mosquito responses to P. falciparum infection, but also for possible applications to the genetic manipulation of mosquitoes and to other mosquito-borne systems.

          Electronic supplementary material

          The online version of this article (10.1186/s13072-018-0250-9) contains supplementary material, which is available to authorized users.

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          Most cited references 78

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          The Sequence Alignment/Map format and SAMtools

          Summary: The Sequence Alignment/Map (SAM) format is a generic alignment format for storing read alignments against reference sequences, supporting short and long reads (up to 128 Mbp) produced by different sequencing platforms. It is flexible in style, compact in size, efficient in random access and is the format in which alignments from the 1000 Genomes Project are released. SAMtools implements various utilities for post-processing alignments in the SAM format, such as indexing, variant caller and alignment viewer, and thus provides universal tools for processing read alignments. Availability: http://samtools.sourceforge.net Contact: rd@sanger.ac.uk
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            Fast gapped-read alignment with Bowtie 2.

            As the rate of sequencing increases, greater throughput is demanded from read aligners. The full-text minute index is often used to make alignment very fast and memory-efficient, but the approach is ill-suited to finding longer, gapped alignments. Bowtie 2 combines the strengths of the full-text minute index with the flexibility and speed of hardware-accelerated dynamic programming algorithms to achieve a combination of high speed, sensitivity and accuracy.
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              Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources.

              DAVID bioinformatics resources consists of an integrated biological knowledgebase and analytic tools aimed at systematically extracting biological meaning from large gene/protein lists. This protocol explains how to use DAVID, a high-throughput and integrated data-mining environment, to analyze gene lists derived from high-throughput genomic experiments. The procedure first requires uploading a gene list containing any number of common gene identifiers followed by analysis using one or more text and pathway-mining tools such as gene functional classification, functional annotation chart or clustering and functional annotation table. By following this protocol, investigators are able to gain an in-depth understanding of the biological themes in lists of genes that are enriched in genome-scale studies.
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                Author and article information

                Contributors
                joseluis.ruiz@ebd.csic.es
                yrserge@yahoo.fr
                thierry.lefevre@ird.fr
                jbouedraogo@gmail.com
                vgcorces@gmail.com
                elena.gomez@csic.es
                Journal
                Epigenetics Chromatin
                Epigenetics Chromatin
                Epigenetics & Chromatin
                BioMed Central (London )
                1756-8935
                7 January 2019
                7 January 2019
                2019
                : 12
                Affiliations
                [1 ]ISNI 0000 0001 2183 4846, GRID grid.4711.3, Estación Biológica de Doñana (EBD), , Consejo Superior de Investigaciones Científicas, ; 41092 Seville, Spain
                [2 ]ISNI 0000 0001 2183 4846, GRID grid.4711.3, Instituto de Parasitología y Biomedicina López-Neyra (IPBLN), , Consejo Superior de Investigaciones Científicas, ; 18016 Granada, Spain
                [3 ]ISNI 0000 0004 0564 0509, GRID grid.457337.1, Institut de Recherche en Sciences de la Santé (IRSS), ; 01 BP 171, Bobo Dioulasso, Burkina Faso
                [4 ]ISNI 0000 0001 2097 0141, GRID grid.121334.6, MIVEGEC, IRD, CNRS, , University of Montpellier, ; Montpellier, France
                [5 ]ISNI 0000 0001 0941 6502, GRID grid.189967.8, Department of Biology, , Emory University, ; 1510 Clifton Road NE, Atlanta, GA 30322 USA
                Article
                250
                10.1186/s13072-018-0250-9
                6322293
                30616642
                © The Author(s) 2019

                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.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/100000002, National Institutes of Health;
                Award ID: R01GM035463
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100003329, Ministerio de Economía y Competitividad;
                Award ID: BFU2015-65000-R
                Award ID: BES-2016-076276
                Award ID: Ramon Y Cajal
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: PDOC-006-01
                Award Recipient :
                Funded by: PATH Malaria Vaccine Initiative
                Award ID: -
                Award Recipient :
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                Research
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                © The Author(s) 2019

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