Abstract
Engulfment of foreign particles by phagocytes is initiated by the engagement of phagocytic receptors. We have previously reported that NimC1 is involved in the phagocytosis of bacteria in Drosophila melanogaster. We have identified a family of genes, the Nimrod gene superfamily, encoding characteristic NIM domain containing structural homologues of NimC1. In this work we studied the bacterium-binding properties of the Nimrod proteins by using a novel immunofluorescencebased flow cytometric assay. This method proved to be highly reproducible and suitable for investigations of the bacteriumbinding capacities of putative phagocytosis receptors. We found that NimC1, NimA, NimB1 and NimB2 bind bacteria significantly but differently. In this respect they are similar to other NIM domain containing receptors Eater and Draper.
Similar content being viewed by others
References
Stuart L.M., Ezekowitz R.A., Phagocytosis: Elegant complexity, Immunity, 2005, 22, 539–550
Kurucz E., Márkus R., Zsámboki J., Folkl-Medzihradszky K., Darula Z., Vilmos P., et al., Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes, Curr. Biol., 2007, 17, 649–654
Stuart L.M., Ezekowitz R.A., Phagocytosis and comparative innate immunity: learning on the fly, Nat. Rev. Immunol., 2008, 2, 131–141
Ulvila J., Vanha-Aho L.M., Rämet M., Drosophila phagocytosis — still many unknowns under the surface, APMIS., 2011, 119, 651–662
Somogyi K., Sipos B., Pénzes Z., Andó I., A conserved gene cluster as a putative functional unit in insect innate immunity, FEBS Lett., 2010, 584, 4375–4378
Irving P., Ubeda J.M., Doucet D., Troxler L., Lagueux M., Zachary D., et al., New insights into Drosophila larval haemocyte functions through genome-wide analysis, Cell Microbiol., 2005, 7, 335–350
Kocks C., Cho J.H., Nehme N., Ulvila J., Pearson A.M., Meister M., et al., Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila, Cell, 2005, 123, 335–346
Chung Y.A., Kocks C., Recognition of pathogenic microbes by the Drosophila phagocytic pattern recognition receptor, Eater, J. of Biol. Chem., 2011, 286, 26524–26532
Hashimoto Y., Tabuchi Y., Sakurai K., Kutsuna M., Kurokawa K., Awasaki T., et al., Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes, J. Immunol., 2009, 183, 7451–7460
Konrad L., Becker G., Schmidt A., Klockner T., Kaufer-Stillger G., Dreschers S., et al., Cloning, structure, cellular localization, and possible function of the tumor suppressor gene lethal(3)malignant blood neoplasm-1 of Drosophila melanogaster, Dev. Biol., 1994, 163, 98–111
Goto A., Kadowaki T., Kitagawa Y., Drosophila hemolectin gene is expressed in embryonic and larval hemocytes and its knock down causes bleeding defects, Dev. Biol., 2003, 264, 582–591
Baba T., Ara T., Hasegawa M., Takai Y., Okumura Y., Baba M., et al., Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection, Mol. Syst. Biol., 2006, 2, 1–11
Kurucz E., Zettervall C.J., Sinka R., Vilmos P., Pivarcsi A., Ekengren S., et al., Hemese, a hemocyte-specific transmembrane protein, affects the cellular immune response in Drosophila, PNAS, 2003, 100, 2622–2627
Kurucz E., Váczi B., Márkus R., Laurinyecz B., Vilmos P., Zsámboki J., et al., Definition of Drosophila hemocyte subsets by cell-type specific antigens, Acta Biol. Hung., 2007, 58, 95–111
Honti V., Kurucz E., Csordás G., Laurinyecz B., Márkus R., Andó I., In vivo detection of lamellocytes in Drosophila melanogaster, Immunol. Lett., 2009, 126, 83–84
Ren J., Wen L., Gao X., Jin C., Xue Y., Yao X., DOG 1.0: Illustrator of Protein Domain Structures, Cell Res., 2009, 19, 271–273
Chen L., Coleman W.G. Jr., Cloning and characterization of the Escherichia coli K-12 rfa-2 (rfaC) gene, a gene required for lipopolysaccharide inner core synthesis, J. Bact., 1993, 175, 2534–2540
Heinrichs D.E., Yethon J.A., Whitfield C., Molecular basis for structural diversity in the core regions of the lipopolysaccharides of Escherichia coli and Salmonella enterica, Mol. Microbiol., 1998, 30, 221–232
Qimron U., Marintcheva B., Tabor S., Richardson C.C., Genomewide screens for Escherichia coli genes affecting growth of T7 bacteriophage, PNAS, 2006, 103, 19039–19044
Markovic I., Pulyaeva H., Sokoloff A., Chernomordik L.V., Membrane fusion mediated by baculovirus gp64 involves assembly of stable gp64 trimers into multiprotein aggregates, J. Cell Biol., 1998, 143, 1155–1166
Cuttell L., Vaughan A., Silva E., Escaron C.J., Lavine M., Van Goethem E., et al., Undertaker, a Drosophila junctophilin, links Draper-mediated phagocytosis and calcium homeostasis, Cell, 2008, 135, 524–534
Blom N., Gammeltoft S., Brunak S., Sequenceand structure-based prediction of eukaryotic protein phosphorylation sites, J. Mol. Biol., 1999, 294, 1351–1362
Somogyi K., Sipos B., Pénzes Z., Kurucz E., Zsámboki J., Hultmark D., et al., Evolution of genes and repeats in the Nimrod superfamily, Mol. Biol. Evol., 2008, 25, 2337–2347
Author information
Authors and Affiliations
About this article
Cite this article
Zsámboki, J., Csordás, G., Honti, V. et al. Drosophila Nimrod proteins bind bacteria. cent.eur.j.biol. 8, 633–645 (2013). https://doi.org/10.2478/s11535-013-0183-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11535-013-0183-4