The roles of metals in insect–microbe interactions and immunity

Golonka, 2019, The iron tug-of-war between bacterial siderophores and innate immunity, J Innate Immun, 11, 249, 10.1159/000494627 Monteith, 2021, The impact of metal availability on immune function during infection, Trends Endocrinol Metab, 32, 916, 10.1016/j.tem.2021.08.004 Lopez, 2018, The impact of dietary transition metals on host-bacterial interactions, Cell Host Microbe, 23, 737, 10.1016/j.chom.2018.05.008 Hood, 2012, Nutritional immunity: transition metals at the pathogen–host interface, Nat Rev Microbiol, 10, 525, 10.1038/nrmicro2836 Kehl-Fie, 2010, Nutritional immunity beyond iron: a role for manganese and zinc, Curr Opin Chem Biol, 14, 218, 10.1016/j.cbpa.2009.11.008 Sheldon, 2019, Metals as phagocyte antimicrobial effectors, Curr Opin Immunol, 60, 1, 10.1016/j.coi.2019.04.002 Rivera-Pérez, 2017, How micronutrients influence the physiology of mosquitoes, Curr Opin Insect Sci, 23, 112, 10.1016/j.cois.2017.07.002 Dow, 2017, The essential roles of metal ions in insect homeostasis and physiology, Curr Opin Insect Sci, 23, 43, 10.1016/j.cois.2017.07.001 Missirlis, 2021, Regulation and biological function of metal ions in Drosophila, Curr Opin Insect Sci, 47, 18, 10.1016/j.cois.2021.02.002 Tiklová, 2010, Epithelial septate junction assembly relies on melanotransferrin iron binding and endocytosis in Drosophila, Nat Cell Biol, 12, 1071, 10.1038/ncb2111 Mumbauer, 2019, Ferritin heavy chain protects the developing wing from reactive oxygen species and ferroptosis, PLoS Genet, 15, 10.1371/journal.pgen.1008396 Pedersen, 2009, Proteomic characterization of a temperature-sensitive conditional lethal in Drosophila melanogaster, Heredity, 104, 125, 10.1038/hdy.2009.132 Kosmidis, 2011, Ferritin overexpression in Drosophila glia leads to iron deposition in the optic lobes and late-onset behavioral defects, Neurobiol Dis, 43, 213, 10.1016/j.nbd.2011.03.013 Mandilaras, 2012, Genes for iron metabolism influence circadian rhythms in Drosophila melanogaster, Metallomics, 4, 928, 10.1039/c2mt20065a Chamilos, 2008, Drosophila melanogaster as a model host to dissect the immunopathogenesis of zygomycosis, Proc Natl Acad Sci U S A, 105, 9367, 10.1073/pnas.0709578105 Iatsenko, 2020, Iron sequestration by transferrin 1 mediates nutritional immunity in Drosophila melanogaster, Proc Natl Acad Sci U S A, 117, 7317, 10.1073/pnas.1914830117 Duchemin, 2017, Iron availability affects West Nile virus infection in its mosquito vector, Virol J, 14, 1, 10.1186/s12985-017-0770-0 Lambert, 2012, Molecular evolution of the transferrin family and associated receptors, Biochim Biophys Acta Gen Subj, 1820, 244, 10.1016/j.bbagen.2011.06.002 Lambert, 2005, Evolution of the transferrin family: conservation of residues associated with iron and anion binding, Comp Biochem Physiol Part B Biochem Mol Biol, 142, 129, 10.1016/j.cbpb.2005.07.007 Ong, 2006, Iron-withholding strategy in innate immunity, Immunobiology, 211, 295, 10.1016/j.imbio.2006.02.004 Cartwright, 1946, The anemia associated with chronic infection, Science, 103, 72, 10.1126/science.103.2664.72 Bruhn, 2015, Transferrin-mediated iron sequestration as a novel therapy for bacterial and fungal infections, Curr Opin Microbiol, 27, 57, 10.1016/j.mib.2015.07.005 Geiser, 2012, Insect transferrins: multifunctional proteins, Biochim Biophys Acta Gen Subj, 1820, 437, 10.1016/j.bbagen.2011.07.011 Weber, 2020, Secreted insect transferrin-1 with strong and reversible iron-binding has potentially tissue specific roles in immunity and iron transport, FASEB J, 34, 1 Weber, 2020, Iron binding and release properties of transferrin-1 from Drosophila melanogaster and Manduca sexta: implications for insect iron homeostasis, Insect Biochem Mol Biol, 125, 10.1016/j.ibmb.2020.103438 Levy, 2004, Proteomic analysis of the systemic immune response of Drosophila, Mol Cell Proteomics, 3, 156, 10.1074/mcp.M300114-MCP200 Troha, 2018, Comparative transcriptomics reveals CrebA as a novel regulator of infection tolerance in D. melanogaster, PLoS Pathog, 14, 10.1371/journal.ppat.1006847 De Gregorio, 2002, The Toll and Imd pathways are the major regulators of the immune response in Drosophila, EMBO J, 21, 2568, 10.1093/emboj/21.11.2568 Brummett, 2017, The immune properties of Manduca sexta transferrin, Insect Biochem Mol Biol, 81, 1, 10.1016/j.ibmb.2016.12.006 Yoshiga, 1997, Mosquito transferrin, an acute-phase protein that is up-regulated upon infection, Proc Natl Acad Sci U S A, 94, 12337, 10.1073/pnas.94.23.12337 Mandilaras, 2013, Iron absorption in Drosophila melanogaster, Nutrients, 5, 1622, 10.3390/nu5051622 Rani, 2021, Functional disruption of transferrin expression alters reproductive physiology in Anopheles culicifacies, bioRxiv Yun, 2009, Bombyx mori transferrin: genomic structure, expression and antimicrobial activity of recombinant protein, Dev Comp Immunol, 33, 1064, 10.1016/j.dci.2009.05.008 Ciencialová, 2008, Mapping the peptide and protein immune response in the larvae of the fleshfly Sarcophaga bullata, J Pept Sci, 14, 670, 10.1002/psc.967 Kim, 2010, A viral histone H4 suppresses expression of a transferrin that plays a role in the immune response of the diamondback moth, Plutella xylostella, Insect Mol Biol, 19, 567, 10.1111/j.1365-2583.2010.01014.x Xu, 2020, Suppression of transferrin expression enhances the susceptibility of Plutella xylostella to Isaria cicadae, Insects, 11, 281, 10.3390/insects11050281 Lehane, 2008, Differential expression of fat body genes in Glossina morsitans morsitans following infection with Trypanosoma brucei brucei, Int J Parasitol, 38, 93, 10.1016/j.ijpara.2007.06.004 Rodríguez-García, 2021, Transferrin-mediated iron sequestration suggests a novel therapeutic strategy for controlling Nosema disease in the honey bee, Apis mellifera, PLoS Pathog, 17, 10.1371/journal.ppat.1009270 Xiao, 2019, Transferrin 1 functions in iron trafficking and genetically interacts with ferritin in Drosophila melanogaster, Cell Rep, 26, 748, 10.1016/j.celrep.2018.12.053 Najera, 2021, Phylogenetic and sequence analyses of insect transferrins suggest that only transferrin 1 has a role in iron homeostasis, Insect Sci, 28, 495, 10.1111/1744-7917.12783 Cao, 2020, Two ferritin genes (MdFerH and MdFerL) are involved in iron homeostasis, antioxidation and immune defense in housefly Musca domestica, J Insect Physiol, 124, 10.1016/j.jinsphys.2020.104073 Geiser, 2013, The effect of bacterial challenge on ferritin regulation in the yellow fever mosquito, Aedes aegypti, Insect Sci, 20, 601, 10.1111/j.1744-7917.2012.01581.x Douglas, 2015, Multiorganismal insects: diversity and function of resident microorganisms, Annu Rev Entomol, 60, 17, 10.1146/annurev-ento-010814-020822 Chen, 2020, Beyond tug-of-war: iron metabolism in cooperative host–microbe interactions, PLoS Pathog, 16, 10.1371/journal.ppat.1008698 Kremer, 2009, Wolbachia interferes with ferritin expression and iron metabolism in insects, PLoS Pathog, 5, 10.1371/journal.ppat.1000630 Hrusa, 2015, TonB-dependent heme iron acquisition in the tsetse fly symbiont Sodalis glossinidius, Appl Environ Microbiol, 81, 2900, 10.1128/AEM.04166-14 Masson, 2021, Dual proteomics of Drosophila melanogaster hemolymph infected with the heritable endosymbiont Spiroplasma poulsonii, PLoS One, 16, 10.1371/journal.pone.0250524 Marra, 2021, The iron transporter transferrin 1 mediates homeostasis of the endosymbiotic relationship between Drosophila melanogaster and Spiroplasma poulsonii, microLife, 2, 10.1093/femsml/uqab008 Nappi, 2005, Melanogenesis and associated cytotoxic reactions: applications to insect innate immunity, Insect Biochem Mol Biol, 35, 443, 10.1016/j.ibmb.2005.01.014 Dudzic, 2019, More than black or white: melanization and Toll share regulatory serine proteases in Drosophila, Cell Rep, 27, 1050, 10.1016/j.celrep.2019.03.101 Smith, 2021, Glyphosate inhibits melanization and increases susceptibility to infection in insects, PLoS Biol, 19, 10.1371/journal.pbio.3001182 Vásquez-Procopio, 2020, Cuticle darkening correlates with increased body copper content in Drosophila melanogaster, BioMetals, 33, 293, 10.1007/s10534-020-00245-1 Riedel, 2011, Megalin-dependent yellow endocytosis restricts melanization in the Drosophila cuticle, Development, 138, 149, 10.1242/dev.056309 Maya-Maldonado, 2021, Mosquito metallomics reveal copper and iron as critical factors for Plasmodium infection, PLoS Negl Trop Dis, 15, 10.1371/journal.pntd.0009509 Derke, 2020, The Cu(II) reductase RclA protects Escherichia coli against the combination of hypochlorous acid and intracellular copper, mBio, 11, 10.1128/mBio.01905-20 Harford, 1997, Amino terminal Cu(II)- and Ni(II)-binding (ATCUN) motif of proteins and peptides: metal binding, DNA cleavage, and other properties, Acc Chem Res, 30, 123, 10.1021/ar9501535 Bouraguba, 2020, Copper-binding motifs Xxx-His or Xxx-Zzz-His (ATCUN) linked to an antimicrobial peptide: Cu-binding, antimicrobial activity and ROS production, J Inorg Biochem, 213, 10.1016/j.jinorgbio.2020.111255 Portelinha, 2021, Antimicrobial peptides and copper(II) ions: novel therapeutic opportunities, Chem Rev, 121, 2648, 10.1021/acs.chemrev.0c00921 Libardo, 2016, Central role of the copper-binding motif in the complex mechanism of action of ixosin: enhancing oxidative damage and promoting synergy with ixosin B, ACS Infect Dis, 2, 71, 10.1021/acsinfecdis.5b00140 Lemaitre, 1997, Drosophila host defense: differential induction of antimicrobial peptide genes after infection by various classes of microorganisms, Proc Natl Acad Sci U S A, 94, 14614, 10.1073/pnas.94.26.14614 Takehana, 2004, Peptidoglycan recognition protein (PGRP)-LE and PGRP-LC act synergistically in Drosophila immunity, EMBO J, 23, 4690, 10.1038/sj.emboj.7600466 Royet, 2011, Peptidoglycan recognition proteins: modulators of the microbiome and inflammation, Nat Rev Immunol, 11, 837, 10.1038/nri3089 Zaidman-Rémy, 2006, The Drosophila amidase PGRP-LB modulates the immune response to bacterial infection, Immunity, 24, 463, 10.1016/j.immuni.2006.02.012 Iatsenko, 2016, PGRP-SD, an extracellular pattern-recognition receptor, enhances peptidoglycan-mediated activation of the Drosophila Imd pathway, Immunity, 45, 1013, 10.1016/j.immuni.2016.10.029 Mellroth, 2006, PGRP-SB1: an N-acetylmuramoyl l-alanine amidase with antibacterial activity, Biochem Biophys Res Commun, 350, 994, 10.1016/j.bbrc.2006.09.139 Maire, 2019, Weevil pgrp-lb prevents endosymbiont TCT dissemination and chronic host systemic immune activation, Proc Natl Acad Sci U S A, 116, 5623, 10.1073/pnas.1821806116 Price, 2021, Yersiniabactin contributes to overcoming zinc restriction during Yersinia pestis infection of mammalian and insect hosts, Proc Natl Acad Sci U S A, 118, 10.1073/pnas.2104073118 Consuegra, 2020, Drosophila-associated bacteria differentially shape the nutritional requirements of their host during juvenile growth, PLoS Biol, 18, 10.1371/journal.pbio.3000681 Husnik, 2020, Insect—symbiont gene expression in the midgut bacteriocytes of a blood-sucking parasite, Genome Biol Evol, 12, 429, 10.1093/gbe/evaa032 Duneau, 2017, The Toll pathway underlies host sexual dimorphism in resistance to both Gram-negative and Gram-positive bacteria in mated Drosophila, BMC Biol, 15, 124, 10.1186/s12915-017-0466-3