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      Thioester-containing proteins regulate the Toll pathway and play a role in Drosophila defence against microbial pathogens and parasitoid wasps

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          Abstract

          Background

          Members of the thioester-containing protein (TEP) family contribute to host defence in both insects and mammals. However, their role in the immune response of Drosophila is elusive. In this study, we address the role of TEPs in Drosophila immunity by generating a mutant fly line, referred to as TEPq Δ , lacking the four immune-inducible TEPs, TEP1, 2, 3 and 4.

          Results

          Survival analyses with TEPq Δ flies reveal the importance of these proteins in defence against entomopathogenic fungi, Gram-positive bacteria and parasitoid wasps. Our results confirm that TEPs are required for efficient phagocytosis of bacteria, notably for the two Gram-positive species tested, Staphylococcus aureus and Enterococcus faecalis. Furthermore, we show that TEPq Δ flies have reduced Toll pathway activation upon microbial infection, resulting in lower expression of antimicrobial peptide genes. Epistatic analyses suggest that TEPs function upstream or independently of the serine protease ModSP at an initial stage of Toll pathway activation.

          Conclusions

          Collectively, our study brings new insights into the role of TEPs in insect immunity. It reveals that TEPs participate in both humoral and cellular arms of immune response in Drosophila. In particular, it shows the importance of TEPs in defence against Gram-positive bacteria and entomopathogenic fungi, notably by promoting Toll pathway activation.

          Electronic supplementary material

          The online version of this article (doi:10.1186/s12915-017-0408-0) contains supplementary material, which is available to authorized users.

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          Most cited references52

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          Immunity in Drosophila melanogaster--from microbial recognition to whole-organism physiology.

          Since the discovery of antimicrobial peptide responses 40 years ago, the fruit fly Drosophila melanogaster has proven to be a powerful model for the study of innate immunity. Early work focused on innate immune mechanisms of microbial recognition and subsequent nuclear factor-κB signal transduction. More recently, D. melanogaster has been used to understand how the immune response is regulated and coordinated at the level of the whole organism. For example, researchers have used this model in studies investigating interactions between the microbiota and the immune system at barrier epithelial surfaces that ensure proper nutritional and immune homeostasis both locally and systemically. In addition, studies in D. melanogaster have been pivotal in uncovering how the immune response is regulated by both endocrine and metabolic signalling systems, and how the immune response modifies these systems as part of a homeostatic circuit. In this Review, we briefly summarize microbial recognition and antiviral immunity in D. melanogaster, and we highlight recent studies that have explored the effects of organism-wide regulation of the immune response and, conversely, the effects of the immune response on organism physiology.
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            Drosophila intestinal response to bacterial infection: activation of host defense and stem cell proliferation.

            Although Drosophila systemic immunity is extensively studied, little is known about the fly's intestine-specific responses to bacterial infection. Global gene expression analysis of Drosophila intestinal tissue to oral infection with the Gram-negative bacterium Erwinia carotovora revealed that immune responses in the gut are regulated by the Imd and JAK-STAT pathways, but not the Toll pathway. Ingestion of bacteria had a dramatic impact on the physiology of the gut that included modulation of stress response and increased stem cell proliferation and epithelial renewal. Our data suggest that gut homeostasis is maintained through a balance between cell damage due to the collateral effects of bacteria killing and epithelial repair by stem cell division. The Drosophila gut provides a powerful model to study the integration of stress and immunity with pathways associated with stem cell control, and this study should prove to be a useful resource for such further studies.
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              The Toll and Imd pathways are the major regulators of the immune response in Drosophila.

              Microarray studies have shown recently that microbial infection leads to extensive changes in the Drosophila gene expression programme. However, little is known about the control of most of the fly immune-responsive genes, except for the antimicrobial peptide (AMP)-encoding genes, which are regulated by the Toll and Imd pathways. Here, we used oligonucleotide microarrays to monitor the effect of mutations affecting the Toll and Imd pathways on the expression programme induced by septic injury in Drosophila adults. We found that the Toll and Imd cascades control the majority of the genes regulated by microbial infection in addition to AMP genes and are involved in nearly all known Drosophila innate immune reactions. However, we identified some genes controlled by septic injury that are not affected in double mutant flies where both Toll and Imd pathways are defective, suggesting that other unidentified signalling cascades are activated by infection. Interestingly, we observed that some Drosophila immune-responsive genes are located in gene clusters, which often are transcriptionally co-regulated.
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                Author and article information

                Contributors
                anna.svarovska@gmail.com
                samuel.rommelaere@epfl.ch
                mickael.poidevin@i2bc.paris-saclay.fr
                + 41 (0) 21 693 18 31 , bruno.lemaitre@epfl.ch
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                5 September 2017
                5 September 2017
                2017
                : 15
                : 79
                Affiliations
                [1 ]ISNI 0000000121839049, GRID grid.5333.6, Global Health Institute, School of Life Sciences, École Polytechnique Fédérale Lausanne (EPFL), ; CH-1015 Lausanne, Switzerland
                [2 ]GRID grid.457334.2, Institute for Integrative Biology of the Cell, Université Paris-Saclay, CEA, CNRS, Université Paris Sud, ; 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, France
                Author information
                http://orcid.org/0000-0001-7970-1667
                Article
                408
                10.1186/s12915-017-0408-0
                5584532
                28874153
                06e23894-681e-4ba6-8aa1-5f9169607ab1
                © Lemaitre et al. 2017

                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
                : 17 January 2017
                : 25 July 2017
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2017

                Life sciences
                innate immunity,complement,beauveria,entomopathogenic fungus,phagocytosis,drosophila,insect,parasitoid wasp

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