Phagocytosis in Drosophila: From molecules and cellular machinery to physiology

Insect Biochemistry and Molecular Biology - Tập 109 - Trang 1-12 - 2019
C. Melcarne1, B. Lemaitre1, E. Kurant2
1Global Health Institute, School of Life Science, École Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
2Department of Human Biology, Faculty of Natural Sciences, University of Haifa, Haifa 34988, Israel

Tài liệu tham khảo

Abrams, 1993, Programmed cell death during Drosophila embryogenesis, Development, 117, 29, 10.1242/dev.117.1.29 Agaisse, 2005, Genome-wide RNAi screen for host factors required for intracellular bacterial infection, Science, 1248, 1116008 Akbar Alvarez-Dominguez, 1996, Phagocytosed live Listeria monocytogenes influences rab5-regulated in vitro phagosome-endosome fusion, J. Biol. Chem., 271, 13834, 10.1074/jbc.271.23.13834 Armitage, 2012, The evolution of Dscam genes across the arthropods, BMC Evol. Biol., 12, 1, 10.1186/1471-2148-12-53 Armitage, 2014, Quantitative Profiling of Drosophila melanogaster Dscam1 isoforms reveals no changes in splicing after bacterial exposure, PLoS One, 9, 10.1371/journal.pone.0108660 Avet-Rochex, 2005, Suppression of Drosophila cellular immunity by directed expression of the ExoS toxin GAP domain of Pseudomonas aeruginosa, Cell Microbiol., 7, 799, 10.1111/j.1462-5822.2005.00512.x Awasaki, 2006, Essential role of the apoptotic cell engulfment genes draper and ced-6 in programmed axon pruning during Drosophila metamorphosis, Neuron, 50, 855, 10.1016/j.neuron.2006.04.027 Basset, 2000, The phytopathogenic bacteria Erwinia carotovora infects Drosophila and activates an immune response, Proc. Natl. Acad. Sci. Unit. States Am., 97, 3376, 10.1073/pnas.97.7.3376 Batz, 2014, The transmembrane protein Macroglobulin complement-related is essential for septate junction formation and epithelial barrier function in Drosophila, Development, 141, 899, 10.1242/dev.102160 Blandin, 2004, Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae, Cell, 116, 661, 10.1016/S0092-8674(04)00173-4 Bork, 1996, Structure and distribution of modules in extracellular proteins, Q. Rev. Biophys., 29, 119, 10.1017/S0033583500005783 Bou Aoun, 2011, Analysis of thioester-containing proteins during the innate immune response of Drosophila melanogaster, J. Innate Immun., 3, 52, 10.1159/000321554 Braun, 1998, Analysis of the Drosophila host defense in domino mutant larvae, which are devoid of hemocytes, Proc. Natl. Acad. Sci. Unit. States Am., 95, 14337, 10.1073/pnas.95.24.14337 Brennan, 2007, Psidin is required in Drosophila blood cells for both phagocytic degradation and immune activation of the fat body, Curr. Biol., 17, 67, 10.1016/j.cub.2006.11.026 Bretscher, 2015, The Nimrod transmembrane receptor Eater is required for hemocyte attachment to the sessile compartment in Drosophila melanogaster, Biol. Open, 4, 355, 10.1242/bio.201410595 Brown, 2012, Eaten alive! Cell death by primary phagocytosis: “Phagoptosis, Trends Biochem. Sci., 37, 325, 10.1016/j.tibs.2012.05.002 Brown, 1983, Lipoprotein metabolism in the macrophage: implications for cholesterol deposition in atherosclerosis, Annu. Rev. Biochem., 52, 223, 10.1146/annurev.bi.52.070183.001255 Brown, 2000, Integrins as mediators of morphogenesis in Drosophila, Dev. Biol., 223, 1, 10.1006/dbio.2000.9711 Callebaut, 2003, EMI domains are widespread and reveal the probable orthologs of the Caenorhabditis elegans CED-1 protein, Biochem. Biophys. Res. Commun., 300, 619, 10.1016/S0006-291X(02)02904-2 Cantera, 1996, Glial cells phagocytose neuronal debris during the metamorphosis of the central nervous system in Drosophila melanogaster, Dev. Gene. Evol., 277, 10.1007/s004270050052 Charroux, 2009, Elimination of plasmatocytes by targeted apoptosis reveals their role in multiple aspects of the Drosophila immune response, Proc. Natl. Acad. Sci. Unit. States Am., 106, 9797, 10.1073/pnas.0903971106 Cheng, 2005, Use of RNA interference in Drosophila S2 cells to identify host pathways controlling compartmentalization of an intracellular pathogen, Proc. Natl. Acad. Sci. U. S. A, 102, 13646, 10.1073/pnas.0506461102 Chung, 2011, Recognition of pathogenic microbes by the Drosophila phagocytic pattern recognition receptor eater, J. Biol. Chem., 286, 26524, 10.1074/jbc.M110.214007 Cosson, 2008, Eat, kill or die: when amoeba meets bacteria, Curr. Opin. Microbiol., 11, 271, 10.1016/j.mib.2008.05.005 Cuttell, 2008, Undertaker, a Drosophila junctophilin, links draper-mediated phagocytosis and calcium homeostasis, Cell, 135, 524, 10.1016/j.cell.2008.08.033 Defaye, 2009, Genetic ablation of Drosophila phagocytes reveals their contribution to both development and resistance to bacterial infection, J. Innate Immun., 1, 322, 10.1159/000210264 Dionne, 2003, Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum, Infect. Immun., 71, 3540, 10.1128/IAI.71.6.3540-3550.2003 Dong, 2006, AgDscam, a hypervariable immunoglobulin domain-containing receptor of the Anopheles gambiae innate immune system, PLoS Biol., 4, 1137, 10.1371/journal.pbio.0040229 Dostálová, 2017, Thioester-containing proteins regulate the Toll pathway and play a role in Drosophila defence against microbial pathogens and parasitoid wasps, BMC Biol., 15, 1, 10.1186/s12915-017-0408-0 Duclos, 2000, 3531 Elrod-Erickson, 2000, Interactions between the cellular and humoral immune responses in Drosophila, Curr. Biol., 10, 781, 10.1016/S0960-9822(00)00569-8 Estévez-Lao, 2014, Involvement of the Anopheles gambiae Nimrod gene family in mosquito immune responses, Insect Biochem. Mol. Biol., 44, 12, 10.1016/j.ibmb.2013.10.008 Etchegaray, 2016, Defective phagocytic corpse processing results in neurodegeneration and can Be rescued by TORC1 activation, J. Neurosci., 36, 3170, 10.1523/JNEUROSCI.1912-15.2016 Etchegaray, 2012, Draper acts through the JNK pathway to control synchronous engulfment of dying germline cells by follicular epithelial cells, Development, 139, 4029, 10.1242/dev.082776 Flannagan, 2012, The cell biology of phagocytosis, Annu. Rev. Pathol., 7, 61, 10.1146/annurev-pathol-011811-132445 Franc, 1996, Croquemort, a novel drosophila hemocyte/macrophage receptor that recognizes apoptotic cells, Immunity, 4, 431, 10.1016/S1074-7613(00)80410-0 Franc, 1999, Requirement for croquemort in phagocytosis of apoptotic cells in Drosophila, Science, 284, 1991, 10.1126/science.284.5422.1991 Freeman, 2003, Unwrapping glial biology: Gcm target genes regulating glial development, diversification, and function, Neuron, 38, 567, 10.1016/S0896-6273(03)00289-7 Garg, 2014, Drosophila Rab14 mediates phagocytosis in the immune response to staphylococcus aureus, Cell Microbiol., 16, 296, 10.1111/cmi.12220 Garin, 2001, The phagosome proteome, J. Cell Biol., 152, 165, 10.1083/jcb.152.1.165 Garver, 2006, The peptidoglycan recognition protein PGRP-SC1a is essential for Toll signaling and phagocytosis of Staphylococcus aureus in Drosophila, Proc. Natl. Acad. Sci. Unit. States Am., 103, 660, 10.1073/pnas.0506182103 Gonzalez, 2013, A glutamate-dependent redox system in blood cells is integral for phagocytosis in Drosophila melanogaster, Curr. Biol., 23, 2319, 10.1016/j.cub.2013.09.061 Guillou, 2016, The Drosophila CD36 homologue croquemort is required to maintain immune and gut homeostasis during development and aging, PLoS Pathog., 12, 1, 10.1371/journal.ppat.1005961 Halder, 2008, Drosophila melanogaster as a model host to dissect the immunopathogenesis of zygomycosis, Proc. Natl. Acad. Sci. Unit. States Am., 105, 9367, 10.1073/pnas.0709578105 Haller, 2018, Quorum‐sensing regulator RhlR but not its autoinducer RhlI enables Pseudomonas to evade opsonization, EMBO Rep., 10.15252/embr.201744880 Hamon, 2006, Listeria monocytogenes: a multifaceted model, Nat. Rev. Microbiol., 4, 423, 10.1038/nrmicro1413 Han, 2014, Epidermal cells are the primary phagocytes in the fragmentation and clearance of degenerating dendrites in Drosophila, Neuron, 81, 544, 10.1016/j.neuron.2013.11.021 Hao, 2018, Jumu is required for circulating hemocyte differentiation and phagocytosis in Drosophila, 3, 1 Hashimoto, 2009, Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes, J. Immunol., 183, 7451, 10.4049/jimmunol.0901032 Herboso, 2011, Expression of the scavenger receptor class B type I (SR-BI) family in drosophila melanogaster, Int. J. Dev. Biol., 55, 603, 10.1387/ijdb.103254lh Hilu-Dadia, 2018, Draper-mediated JNK signaling is required for glial phagocytosis of apoptotic neurons during Drosophila metamorphosis, Glia, 66, 1520, 10.1002/glia.23322 Horn, 2014, Phagocytic ability declines with age in adult Drosophila hemocytes, Aging Cell, 13, 719, 10.1111/acel.12227 Huynh, 2007, LAMP proteins are required for fusion of lysosomes with phagosomes, EMBO J., 26, 313, 10.1038/sj.emboj.7601511 Irving, 2005, New insights into Drosophila larval haemocyte functions through genome-wide analysis, Cell Microbiol., 7, 335, 10.1111/j.1462-5822.2004.00462.x Jahraus, 1998, In vitro fusion of phagosomes with different endocytic organelles from J774 macrophages, J. Biol. Chem., 273, 30379, 10.1074/jbc.273.46.30379 Ju, 2006, A novel 40-kDa protein containing six repeats of an epidermal growth factor-like domain functions as a pattern recognition protein for lipopolysaccharide, J. Immunol., 177, 1838, 10.4049/jimmunol.177.3.1838 Kato, 2009, Neuronal programmed cell death induces glial cell division in the adult Drosophila brain, Development, 136, 51, 10.1242/dev.023366 Kinchen, 2008, A novel pathway for phagosome maturation during engulfment of apoptotic cells, Nat. Cell Biol., 556, 10.1038/ncb1718 Kinchen, 2010, Identification of two evolutionarily conserved genes regulating processing of engulfed apoptotic cells, Nature, 464, 778, 10.1038/nature08853 Kitano, 2008, Imaging of Rab5 activity identifies essential regulators for phagosome maturation, Nature, 453, 241, 10.1038/nature06857 Kocks, 2005, Eater, a transmembrane protein mediating phagocytosis of bacterial pathogens in Drosophila, Cell, 123, 335, 10.1016/j.cell.2005.08.034 Kocks, 2003, Functional proteomics of the active cysteine protease content in Drosophila S2 cells, Mol. Cell. Proteomics, 2, 1188, 10.1074/mcp.M300067-MCP200 Kuraishi, 2009, Pretaporter, a Drosophila protein serving as a ligand for Draper in the phagocytosis of apoptotic cells, EMBO J., 28, 3868, 10.1038/emboj.2009.343 Kurant, 2008, Six-microns-under acts upstream of draper in the glial phagocytosis of apoptotic neurons, Cell, 133, 498, 10.1016/j.cell.2008.02.052 Kurucz, 2007, Nimrod, a putative phagocytosis receptor with EGF repeats in Drosophila plasmatocytes, Curr. Biol., 17, 649, 10.1016/j.cub.2007.02.041 Lagueux, 2000, Constitutive expression of a complement-like protein in Toll and JAK gain-of-function mutants of Drosophila, Proc. Natl. Acad. Sci. Unit. States Am., 97, 11427, 10.1073/pnas.97.21.11427 Lazzaro, 2005, Elevated polymorphism and divergence in the class C scavenger receptors of Drosophila melanogaster and D. simulans, Genetics, 169, 2023, 10.1534/genetics.104.034249 Lemaitre, 2007, The host defense of Drosophila melanogaster, Annu. Rev. Immunol., 25, 697, 10.1146/annurev.immunol.25.022106.141615 Levitin, 2007, Drosophila melanogaster Thor and response to Candida albicans infection, Eukaryot. Cell, 6, 658, 10.1128/EC.00346-06 Li, 2009, 2445 Logan, 2012, Negative regulation of glial engulfment activity by Draper terminates glial responses to axon injury, Nat. Neurosci., 15, 722, 10.1038/nn.3066 Manaka, 2004, Draper-mediated and phosphatidylserine-independent phagocytosis of apoptotic cells by Drosophila hemocytes/macrophages, J. Biol. Chem., 279, 48466, 10.1074/jbc.M408597200 Mangahas, 2005, Clearance of apoptotic cells in Caenorhabditis elegans, Semin. Cell Dev. Biol., 16, 295, 10.1016/j.semcdb.2004.12.005 Mansfield, 2003, Exploration of host-pathogen interactions using Listeria monocytogenes and Drosophila melanogaster, Cell Microbiol., 5, 901, 10.1046/j.1462-5822.2003.00329.x Martinek, 2008, Haemocyte-derived SPARC is required for collagen-IV-dependent stability of basal laminae in Drosophila embryos, J. Cell Sci., 124 Matsunaga, 2002, Identification and characterization of genes abnormally expressed in wing-deficient mutant (flugellos) of the silkworm, Bombyx mori, Insect Biochem., 32, 691, 10.1016/S0965-1748(01)00148-5 McLaughlin, 2019, Dying neurons utilize innate immune signaling to prime glia for phagocytosis during development, Dev. Cell, 0, 506, 10.1016/j.devcel.2018.12.019 Meehan, 2016, Components of the engulfment machinery have distinct roles in corpse processing, PLoS One, 11, 1, 10.1371/journal.pone.0158217 Melcarne, 2018 Mellroth, 2003, A scavenger function for a Drosophila peptidoglycan recognition protein, J. Biol. Chem., 278, 7059, 10.1074/jbc.M208900200 Midega, 2013, Discovery and characterization of two Nimrod superfamily members in Anopheles gambiae, Pathog. Glob. Health, 107, 463, 10.1179/204777213X13867543472674 Möller, 2013, Macrophages lift off surface-bound bacteria using a filopodium- lamellipodium hook-and-shovel mechanism, Sci. Rep., 3, 1, 10.1038/srep02884 Myers, 2018, Inflammatory production of reactive oxygen species by Drosophila hemocytes activates cellular immune defenses, Biochem. Biophys. Res. Commun., 505, 726, 10.1016/j.bbrc.2018.09.126 Nagaosa, 2011, Integrin βν-mediated phagocytosis of apoptotic cells in Drosophila embryos, J. Biol. Chem., 286, 25770, 10.1074/jbc.M110.204503 Nehme, 2007, A model of bacterial intestinal infections in Drosophila melanogaster, PLoS Pathog., 3, 1694, 10.1371/journal.ppat.0030173 Nehme, 2011, Relative roles of the cellular and humoral responses in the Drosophila host defense against three gram-positive bacterial infections, PLoS One, 6, 10.1371/journal.pone.0014743 Nickerson, 2009, Vps-C complexes: gatekeepers of endolysosomal traffic, Curr. Opin. Cell Biol., 21, 543, 10.1016/j.ceb.2009.05.007 Nieto, 2010 Nonaka, 2013, Integrin ??pS3/??-mediated phagocytosis of apoptotic cells and bacteria in Drosophila, J. Biol. Chem., 288, 10374, 10.1074/jbc.M113.451427 O'Leary, 1993, Development of projection neuron types, axon pathways, and patterned connections of the mammalian cortex, Neuron, 10, 991, 10.1016/0896-6273(93)90049-W Paredes, 2011, Negative regulation by amidase PGRPs shapes the Drosophila antibacterial response and protects the fly from innocuous infection, Immunity, 35, 770, 10.1016/j.immuni.2011.09.018 Pearson, 1995, Expression cloning of dSR-CI, a class C macrophage-specific scavenger receptor from Drosophila melanogaster, Proc. Natl. Acad. Sci. U. S. A, 92, 4056, 10.1073/pnas.92.9.4056 Pearson, 2003, Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila, Microb. Infect., 5, 815, 10.1016/S1286-4579(03)00157-6 Peltan, 2012, Identification of Drosophila gene products required for phagocytosis of leishmania donovani, PLoS One, 7, 10.1371/journal.pone.0051831 Peterson, 2002, Reaper is required for neuroblast apoptosis during Drosophila development, Development, 129, 1467, 10.1242/dev.129.6.1467 Philips, 2005, vol 309, 2003 Poteryaev, 2010, Identification of the switch in early-to-late endosome transition, Cell, 141, 497, 10.1016/j.cell.2010.03.011 Poteryaev, 2007, Caenorhabditis elegans SAND-1 is essential for RAB-7 function in endosomal traffic, EMBO J., 26, 301, 10.1038/sj.emboj.7601498 Rämet, 2002, Functional genomic analysis of phagocytosis and identification of a Drosophila receptor for E. Coli, Nature, 416, 644, 10.1038/nature735 Rämet, 2001, Drosophila scavenger receptor CI is a pattern recognition receptor for bacteria, Immunity, 15, 1027, 10.1016/S1074-7613(01)00249-7 Rogulja-Ortmann, 2007, Programmed cell death in the embryonic central nervous system of Drosophila melanogaster, Development, 134, 105, 10.1242/dev.02707 Royet, 2011, Peptidoglycan recognition proteins: modulators of the microbiome and inflammation, Nat. Rev. Immunol., 11, 837, 10.1038/nri3089 Samakovlis, 1990, The immune response in Drosophila: pattern of cecropin expression and biological activity, EMBO J., 9, 2969, 10.1002/j.1460-2075.1990.tb07489.x Savill, 1992, Thrombospondin cooperates with CD36 and the vitronectin receptor in macrophage recognition of neutrophils undergoing apoptosis, J. Clin. Investig., 90, 1513, 10.1172/JCI116019 Schmucker, 2000, Drosophila Dscam is an axon guidance receptor exhibiting extraordinary molecular diversity, Cell, 101, 671, 10.1016/S0092-8674(00)80878-8 Segawa, 2015, An apoptotic “eat me” signal: phosphatidylserine exposure, Trends Cell Biol., 25, 639, 10.1016/j.tcb.2015.08.003 Seong, 2006, DNase II deficiency impairs innate immune function in Drosophila, Cell. Immunol., 240, 5, 10.1016/j.cellimm.2006.05.007 Serizier, 2017, Scrambled eggs: apoptotic cell clearance by non-professional phagocytes in the Drosophila ovary, Front. Immunol., 8, 10.3389/fimmu.2017.01642 Shandala, 2013, A Drosophila model to image phagosome maturation, Cells, 2, 188, 10.3390/cells2020188 Shinzawa, 2009, p38 MAPK-dependent phagocytic encapsulation confers infection tolerance in Drosophila, Cell Host Microbe, 6, 244, 10.1016/j.chom.2009.07.010 Shiratsuchi, 2012, Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila, J. Biol. Chem., 287, 21663, 10.1074/jbc.M111.333807 Shklover, 2015 Shklover, 2015 Shklyar, 2013, Caspase activity is required for engulfment of apoptotic cells, Mol. Cell Biol., 33, 3191, 10.1128/MCB.00233-13 Shklyar, 2014, Developmental regulation of glial cell phagocytic function during Drosophila embryogenesis, Dev. Biol., 393, 255, 10.1016/j.ydbio.2014.07.005 Stenbak, 2004, Peptidoglycan molecular requirements allowing detection by the Drosophila immune deficiency pathway, J. Immunol., 173, 7339, 10.4049/jimmunol.173.12.7339 Stroschein-Stevenson, 2006, Identification of Drosophila gene products required for phagocytosis of Candida albicans, PLoS Biol., 4, 0087 Stuart, 2007, A systems biology analysis of the Drosophila phagosome, Nature, 445, 95, 10.1038/nature05380 Stuart, 2005, Response to Staphylococcus aureus requires CD36-mediated phagocytosis triggered by the COOH-terminal cytoplasmic domain, J. Cell Biol., 170, 477, 10.1083/jcb.200501113 Tasdemir-Yilmaz, 2014, Astrocytes engage unique molecular programs to engulf pruned neuronal debris from distinct subsets of neurons, Genes Dev., 28, 20, 10.1101/gad.229518.113 Theopold, 2014, The Drosophila clotting system and its messages for mammals, Dev. Comp. Immunol., 42, 42, 10.1016/j.dci.2013.03.014 Timmons, 2016, Phagocytosis genes nonautonomously promote developmental cell death in the Drosophila ovary, Proc. Natl. Acad. Sci. Unit. States Am., 113, E1246, 10.1073/pnas.1522830113 Tissot, 2000, Metamorphosis in Drosophila and other insects: the fate of neurons throughout the stages, Prog. Neurobiol., 62, 89, 10.1016/S0301-0082(99)00069-6 Togane, 2012, Spatio-temporal pattern of programmed cell death in the developing Drosophila optic lobe, Dev. Growth Differ., 54, 503, 10.1111/j.1440-169X.2012.01340.x Tung, 2013, Phosphatidylserine recognition and induction of apoptotic cell clearance by Drosophila engulfment receptor Draper, J. Biochem., 153, 483, 10.1093/jb/mvt014 Vanha-aho, 2016, Cytokines in Drosophila immunity, Immunol. Lett., 170, 42, 10.1016/j.imlet.2015.12.005 Vieira, 2001 Vieira, 2003, vol 23, 2501 Wang, 2002, The Ccz1-Mon1 protein complex is required for the late step of multiple vacuole delivery pathways, J. Biol. Chem., 277, 47917, 10.1074/jbc.M208191200 Watson, 2005, Extensive diversity of Ig-superfamily proteins in the immune system of insects, Science, 309, 1874, 10.1126/science.1116887 Weavers, 2016, Corpse engulfment generates a molecular memory that primes the macrophage inflammatory response, Cell, 165, 1658, 10.1016/j.cell.2016.04.049 Wojtowicz, 2004, Alternative splicing of Drosophila Dscam generates axon guidance teceptors that exhibit isoform-specific homophilic binding, Cell, 118, 619, 10.1016/j.cell.2004.08.021 Woodcock, 2015, Macrophage-derived upd3 cytokine causes impaired glucose homeostasis and reduced lifespan in Drosophila fed a lipid-rich diet, Immunity, 42, 133, 10.1016/j.immuni.2014.12.023 Yeung, 2006, Lipid metabolism and dynamics during phagocytosis, Curr. Opin. Cell Biol., 18, 429, 10.1016/j.ceb.2006.06.006 Yousefian, 2013, Dmon1 controls recruitment of Rab7 to maturing endosomes in Drosophila, J. Cell Sci., 126, 1583, 10.1242/jcs.114934 Zhan, 2004, Analysis of Dscam diversity in regulating axon guidance in Drosophila mushroom bodies, Neuron, 43, 673, 10.1016/j.neuron.2004.07.020 Ziegenfuss, 2008, Draper-dependent glial phagocytic activity is mediated by Src and Syk family kinase signalling, Nature, 453, 935, 10.1038/nature06901 Zsámboki, 2013, Drosophila Nimrod proteins bind bacteria, Cent. Eur. J. Biol., 8, 633