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      The raspberry Gene Is Involved in the Regulation of the Cellular Immune Response in Drosophila melanogaster

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          Abstract

          Drosophila is an extremely useful model organism for understanding how innate immune mechanisms defend against microbes and parasitoids. Large foreign objects trigger a potent cellular immune response in Drosophila larva. In the case of endoparasitoid wasp eggs, this response includes hemocyte proliferation, lamellocyte differentiation and eventual encapsulation of the egg. The encapsulation reaction involves the attachment and spreading of hemocytes around the egg, which requires cytoskeletal rearrangements, changes in adhesion properties and cell shape, as well as melanization of the capsule. Guanine nucleotide metabolism has an essential role in the regulation of pathways necessary for this encapsulation response. Here, we show that the Drosophila inosine 5'-monophosphate dehydrogenase (IMPDH), encoded by raspberry ( ras), is centrally important for a proper cellular immune response against eggs from the parasitoid wasp Leptopilina boulardi. Notably, hemocyte attachment to the egg and subsequent melanization of the capsule are deficient in hypomorphic ras mutant larvae, which results in a compromised cellular immune response and increased survival of the parasitoid.

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          Most cited references49

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          Role of the prophenoloxidase-activating system in invertebrate immunity.

          The melanization reaction, which is a common response to parasite entry in invertebrate animals, especially arthropods, is due to the activity of an oxidoreductase, phenoloxidase. This enzyme is part of a complex system of proteinases, pattern recognition proteins and proteinase inhibitors constituting the so-called prophenoloxidase-activating system. It is proposed to be a non-self recognition system because conversion of prophenoloxidase to active enzyme can be brought about by minuscule amounts of molecules such as lipopolysaccharide, peptidoglycan and beta-1, 3-glucans from micro-organisms. Several components of this system recently have been isolated and their structure determined.
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            Phagocytosis: elegant complexity.

            Phagocytosis requires receptor-mediated recognition of particles, usually in the guise of infectious agents and apoptotic cells. Phagosomes fuse with lysosomes to generate phagolysosomes, which play a key role in enzymatic digestion of the internalized contents into component parts. Recent findings indicate that a simple paradigm of a single cognate receptor interaction that guides the phagosome to phagolysosome formation belies the complexity of combinatorial receptor recognition and diversity of phagosome function. In fact, phagosomes are comprised of hundreds of proteins that play a key role in deciphering the contents of the phagosome and in defining host response. In this review we discuss how the challenge of recognizing diverse molecular patterns is met by combinatorial interactions between phagocytic receptors. Furthermore, these combinations are dynamic and both sculpt the balance between a proinflammatory or anti-inflammatory response and direct phagosome diversity. We also indicate an important role for genetically tractable model organisms in defining key components of this evolutionarily conserved process.
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              Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta.

              We describe here a signal transduction pathway controlling the establishment of mammalian cell polarity. Scratching a confluent monolayer of primary rat astrocytes leads to polarization of cells at the leading edge. The microtubule organizing center, the microtubule cytoskeleton, and the Golgi reorganize to face the new free space, and directed cell protrusion and migration specifically occur perpendicularly to the scratch. We show here that the interaction of integrins with extracellular matrix at the newly formed cell front leads to the activation and polarized recruitment of Cdc42, which in turn recruits and activates a cytoplasmic mPar6/PKCzeta complex. Localized PKCzeta activity, acting through the microtubule motor protein dynein, is required for all aspects of induced polarity in these cells.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                4 March 2016
                2016
                : 11
                : 3
                : e0150910
                Affiliations
                [1 ]Immunology Unit, Institute of Genetics, Biological Research Centre of the Hungarian Academy of Sciences, Szeged, Hungary
                [2 ]Functional Pharmacology, Department of Neuroscience, Uppsala University, Uppsala, Sweden
                Institute of Plant Physiology and Ecology, CHINA
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: BK VH IA EK. Performed the experiments: BK G. Csordás VH G. Cinege IA EK. Analyzed the data: BK G. Csordás VH G. Cinege MJW IA EK. Contributed reagents/materials/analysis tools: BK G. Csordás VH IA EK. Wrote the paper: BK MJW IA EK.

                Article
                PONE-D-15-55262
                10.1371/journal.pone.0150910
                4778902
                26942456
                d2eac659-2c65-4045-9a21-db4f7a3f145b
                © 2016 Kari et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 21 December 2015
                : 21 February 2016
                Page count
                Figures: 5, Tables: 0, Pages: 13
                Funding
                This work was funded by the Hungarian Science Foundation: NK-101730, www.otka.hu, and Carl Tryggers Stiftelsen, http://www.carltryggersstiftelse.se/. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Research and Analysis Methods
                Model Organisms
                Animal Models
                Drosophila Melanogaster
                Biology and Life Sciences
                Organisms
                Animals
                Invertebrates
                Arthropoda
                Insects
                Drosophila
                Drosophila Melanogaster
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Larvae
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Blood Cells
                White Blood Cells
                Hemocytes
                Biology and Life Sciences
                Cell Biology
                Cellular Types
                Animal Cells
                Immune Cells
                White Blood Cells
                Hemocytes
                Biology and Life Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Hemocytes
                Medicine and Health Sciences
                Immunology
                Immune Cells
                White Blood Cells
                Hemocytes
                Biology and life sciences
                Genetics
                Epigenetics
                RNA interference
                Biology and life sciences
                Genetics
                Gene expression
                RNA interference
                Biology and life sciences
                Genetics
                Genetic interference
                RNA interference
                Biology and life sciences
                Biochemistry
                Nucleic acids
                RNA
                RNA interference
                Biology and Life Sciences
                Immunology
                Immune Response
                Medicine and Health Sciences
                Immunology
                Immune Response
                Biology and Life Sciences
                Zoology
                Entomology
                Insect Metamorphosis
                Pupae
                Biology and Life Sciences
                Developmental Biology
                Metamorphosis
                Insect Metamorphosis
                Pupae
                Research and Analysis Methods
                Microscopy
                Light Microscopy
                Fluorescence Microscopy
                Biology and Life Sciences
                Genetics
                Gene Expression
                Gene Regulation
                Custom metadata
                All relevant data are within the paper and are available from the www.mtmt.hu.

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