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Review

Innate humoral immune defences in mammals and insects: The same, with differences ?

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Pages 1625-1639 | Received 07 Aug 2018, Accepted 14 Sep 2018, Published online: 13 Oct 2018

References

  • Riera Romo M, Pérez-Martínez D, Castillo Ferrer C. Innate immunity in vertebrates: an overview. Immunology. 2016;148:125–139.
  • Bergin D, Reeves EP, Renwick J, et al. Superoxide production in galleria mellonella hemocytes : identification of proteins homologous to the NADPH oxidase complex of human neutrophils superoxide production in galleria mellonella hemocytes : identification of proteins homologous to the NADPH Ox. Infect Immun. 2005;73:4161–4170.
  • Renwick J, Reeves EP, Wientjes FB, et al. Translocation of proteins homologous to human neutrophil p47phox and p67phox to the cell membrane in activated hemocytes of Galleria mellonella. Dev Comp Immunol. 2007;31:347–359.
  • Browne N, Heelan M, Kavanagh K. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence. 2013;4:597–603.
  • Flajnik MF, Kasahara M. Origin and evolution of the adaptive immune system: genetic events and selective pressures. Nat Rev Genet. 2010;11:47–59.
  • Cooper MD, Alder MN. The evolution of adaptive immune systems. Cell. 2006;124:815–822.
  • Mowlds P, Coates C, Renwick J, et al. Dose-dependent cellular and humoral responses in Galleria mellonella larvae following β-glucan inoculation. Microbes Infect. 2010;12:146–153.
  • Cooper D, Eleftherianos I. Memory and specificity in the insect immune system: current perspectives and future challenges. Front Immunol. 2017;8:539.
  • Cox CR, Gilmore MS. Native microbial colonization of Drosophila melanogaster and its use as a model of Enterococcus faecalis pathogenesis. Infect Immun. 2007;75:1565–1576.
  • Erickson DL, Lines JL, Pesci EC, et al. Pseudomonas aeruginosa relA contributes to virulence in drosophila melanogaster. Infect Immun. 2004;72:5638–5645.
  • Lau GW, Goumnerov BC, Walendziewicz CL, et al. The Drosophila melanogaster toll pathway participates in resistance to infection by the gram-negative human pathogen Pseudomonas aeruginosa. Infect Immun. 2003;71:4059–4066.
  • Brennan M, Thomas DY, Whiteway M, et al. Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol. 2002;34:153–157.
  • Reeves EP, Messina CGM, Doyle S, et al. Correlation between gliotoxin production and virulence of Aspergillus fumigatus in Galleria mellonella. Mycopathologia. 2004;158:73–79.
  • Mylonakis E, Moreno R, El Khoury JB, et al. Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun. 2005;73:3842–3850.
  • Mukherjee K, Hain T, Fischer R, et al. Brain infection and activation of neuronal repair mechanisms by the human pathogen Listeria monocytogenes in the lepidopteran model host Galleria mellonella. Virulence. 2013;4:324–332.
  • Leger RJS, Durrands PK, Charnley AK, et al. Role of extracellular chymoelastase in the virulence of Metarhizium anisopliae for Manduca sexta. J Invertebr Pathol. 1988;52:285–293.
  • Cowles KN, Goodrich-Blair H. Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell Microbiol. 2005;7:209–219.
  • Iiyama K, Chieda Y, Lee JM, et al. Effect of superoxide dismutase gene inactivation on virulence of Pseudomonas aeruginosa PAO1 toward the silkworm, Bombyx mori. Appl Environ Microbiol. 2007;73:1569–1575.
  • Kavanagh K, Reeves EP. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev. 2004;28:101–112.
  • Tannenbaum J, Bennett BT. Russell and Burch’s 3Rs then and now: the need for clarity in definition and purpose. J Am Assoc Lab Anim Sci. 2015;54:120–132.
  • Yang H-F, Pan A-J, Hu L-F, et al. Galleria mellonella as an in vivo model for assessing the efficacy of antimicrobial agents against Enterobacter cloacae infection. J Microbiol Immunol Infect. 2014;50:55–61.
  • Barnoy S, Gancz H, Zhu Y, et al. The Galleria mellonella larvae as an in vivo model for evaluation of Shigella virulence. Gut Microbes. 2017;8:335–350.
  • Zhang G, Ghosh S. Toll-like receptor-mediated NF-κB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest. 2001;107:13–19.
  • Imler J-L. Biology of Toll receptors: lessons from insects and mammals. J Leukoc Biol. 2003;75:18–26.
  • Lemaitre B, Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007;25:697–743.
  • Akira S, Hemmi H. Recognition of pathogen-associated molecular patterns by TLR family. Immunol Lett. 2003;85:85–95.
  • Silverman N, Maniatis T. NF-κB signaling pathways in mammalian and insect innate immunity. Genes Dev. 2001;15:2321–2342.
  • Govind S. Innate immunity in Drosophila: pathogens and pathways. Insect Sci. 2008;15:29–43.
  • Valanne S, Wang J-H, Ramet M. The Drosophila toll signaling pathway. J Immunol. 2011;186:649–656.
  • Ganesan S, Aggarwal K, Paquette N, et al. Nf-κB/Rel proteins and the humoral immune responses of Drosophila melanogaster. Curr Top Microbiol Immunol. 2011;349:25–60.
  • Kleino A, Silverman N. The Drosophila IMD pathway in the activation of the humoral immune response. Dev Comp Immunol. 2014;42:25–35.
  • Liu ZG. Molecular mechanism of TNF signaling and beyond. Cell Res. 2005;15:24–27.
  • Ertürk-Hasdemir D, Broemer M, Leulier F, et al. Two roles for the Drosophila IKK complex in the activation of Relish and the induction of antimicrobial peptide genes. Proc Natl Acad Sci USA. 2009;106:9779–9784.
  • Myllymäki H, Rämet M. JAK/STAT pathway in Drosophila immunity. Scand J Immunol. 2014;79:377–385.
  • Ting AT, Bertrand MJM. More to life than NF-κB in TNFR1 signaling. Trends Immunol. 2016;37:535–545.
  • Dushay MS. Insect hemolymph clotting. Cell Mol Life Sci. 2009;66:2643–2650.
  • Haine ER, Rolff J, Siva-Jothy MT. Functional consequences of blood clotting in insects. Dev Comp Immunol. 2007;31:456–464.
  • Theopold U, Krautz R, Dushay MS. The Drosophila clotting system and its messages for mammals. Dev Comp Immunol. 2014;42:42–46.
  • Wang Z, Wilhelmsson C, Hyrsl P, et al. Pathogen entrapment by transglutaminase - A conserved early innate immune mechanism. PLoS Pathog. 2010;6:e1000763.
  • Loof TG, Schmidt O, Herwald H, et al. Coagulation systems of invertebrates and vertebrates and their roles in innate immunity: the same side of two coins? J Innate Immun. 2011;3:34–40.
  • Goto A, Kumagai T, Kumagai C, et al. Drosophila haemocyte-specific protein, hemolectin, similar to human von Willebrand factor. Biochem J. 2001;359:99–108.
  • Rowley AF, Ratcliffe NA. The granular cells of Galleria mellonella during clotting and phagocytic reactions in vitro. Tissue Cell. 1976;8:437–446.
  • Cerenius L, Söderhäll K. Coagulation in invertebrates. J Innate Immun. 2011;3:3–8.
  • Eleftherianos I, Revenis C. Role and importance of phenoloxidase in insect hemostasis. J Innate Immun. 2011;3:28–33.
  • Li D, Scherfer C, Korayem AM, et al. Insect hemolymph clotting: evidence for interaction between the coagulation system and the prophenoloxidase activating cascade. Insect Biochem Mol Biol. 2002;32:919–928.
  • Scherfer C, Karlsson C, Loseva O, et al. Isolation and characterization of hemolymph clotting factors in Drosophila melanogaster by a pullout method. Curr Biol. 2004;14:625–629.
  • Lindgren M, Riazi R, Lesch C, et al. Fondue and transglutaminase in the Drosophila larval clot. J Insect Physiol. 2008;54:586–592.
  • Palta S, Saroa R, Palta A. Overview of the coagulation system. Indian J Anaesth. 2014;58:515–523.
  • Smith SA, Travers RJ, Morrissey JH. How it all starts: initiation of the clotting cascade. Crit Rev Biochem Mol Biol. 2015;50:326–336.
  • Tanaka KA, Key NS, Levy JH. Blood coagulation: hemostasis and thrombin regulation. Anesth Analg. 2009;108:1433–1446.
  • Mackman N, Tilley RE, Key NS. Role of the extrinsic pathway of blood coagulation in hemostasis and thrombosis. Arterioscler Thromb Vasc Biol. 2007;27:1687–1693.
  • Brenner M, Hearing VJ. The protective role of melanin against UV damage in human skin. Photochem Photobiol. 2008;84:539–549.
  • Sugumaran M, Barek H. Critical analysis of the melanogenic pathway in insects and higher animals. Int J Mol Sci. 2016;17. pii: E1753.
  • Waisberg M, Vickers BK, Yager SB, et al. Testing in mice the hypothesis that melanin is protective in malaria infections. PLoS One. 2012;7:e29493.
  • Cerenius L, Lee BL, Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008;29:263–271.
  • Cerenius L, Kawabata SI, Lee BL, et al. Proteolytic cascades and their involvement in invertebrate immunity. Trends Biochem Sci. 2010;35:575–583.
  • Chen YY, Chen JC, Lin YC, et al. Endogenous molecules induced by a Pathogen-Associated Molecular Pattern (PAMP) elicit innate immunity in shrimp. PLoS One. 2014;9:e115232.
  • Park SY, Kim CH, Jeong WH, et al. Effects of two hemolymph proteins on humoral defense reactions in the wax moth, Galleria mellonella. Dev Comp Immunol. 2005;29:43–51.
  • Zhao P, Li J, Wang Y, et al. Broad-spectrum antimicrobial activity of the reactive compounds generated in vitro by Manduca sexta phenoloxidase. Insect Biochem Mol Biol. 2007;37:952–959.
  • Lu A, Zhang Q, Zhang J, et al. Insect prophenoloxidase: the view beyond immunity. Front Physiol. 2014;5:252.
  • Shokal U, Eleftherianos I. Evolution and function of thioester-containing proteins and the complement system in the innate immune response. Front Immunol. 2017;29;8:759.
  • Nappi AJ, Frey F, Carton Y. Drosophila serpin 27A is a likely target for immune suppression of the blood cell-mediated melanotic encapsulation response. J Insect Physiol. 2005;51:197–205.
  • Binggeli O, Neyen C, Poidevin M, et al. Prophenoloxidase activation is required for survival to microbial infections in Drosophila. PLoS Pathog. 2014;10:1–15.
  • Galván I, Alonso-Alvarez C, Negro JJ. Relationships between hair melanization, glutathione levels, and senescence in wild boars. Physiol Biochem Zool. 2012;85:332–347.
  • Slominski A. Melanin pigmentation in mammalian skin and its hormonal regulation. Physiol Rev. 2004;84:1155–1228.
  • Zhang LJ, Gallo RL. Antimicrobial peptides. Curr Biol. 2016;26:R14–9.
  • Wiesner J, Vilcinskas A. Antimicrobial peptides: the ancient arm of the human immune system. Virulence. 2010;1:440–464.
  • Lai Y, Gallo RL. AMPed up immunity: how antimicrobial peptides have multiple roles in immune defense. Trends Immunol. 2009;30:131–141.
  • Van Der Weerden NL, Bleackley MR, Anderson MA. Properties and mechanisms of action of naturally occurring antifungal peptides. Cell Mol Life Sci. 2013;70:3545–3570.
  • Maróti Gergely G, Kereszt A, Kondorosi É, et al. Natural roles of antimicrobial peptides in microbes, plants and animals. Res Microbiol. 2011;162:363–374.
  • De Y, Chen Q, Schmidt AP, et al. Ll-37, the neutrophil granule–and epithelial cell–derived cathelicidin, utilizes formyl peptide receptor–like 1 (Fprl1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J Exp Med. 2000;192:1069–1074.
  • Bals R. Epithelial antimicrobial peptides in host defense against infection. Respir Res. 2000;1:141–150.
  • Boman HG. Antibacterial peptides: basic facts and emerging concepts. J Intern Med. 2003;254:197–215.
  • Zasloff M. Antimicrobial peptides of multicellular organisms. Nature. 2002;415:389–395.
  • Mylonakis E, Podsiadlowski L, Muhammed M, et al. Diversity, evolution and medical applications of insect antimicrobial peptides. Philos Trans R Soc B Biol Sci. 2016;371(1695). pii:20150290.
  • Ragland SA, Criss AK. From bacterial killing to immune modulation: recent insights into the functions of lysozyme. PLoS Pathog. 2017;21;13(9):e1006512.
  • Callewaert L, Michiels CW. Lysozymes in the animal kingdom. J Biosci. 2010;35:127–160.
  • Hultmark D. Insect lysozymes. EXS. 1996;75:87–102.
  • Gandhe AS, Janardhan G, Nagaraju J. Immune upregulation of novel antibacterial proteins from silkmoths (Lepidoptera) that resemble lysozymes but lack muramidase activity. Insect Biochem Mol Biol. 2007;37:655–666.
  • Vilmos P, Kurucz É. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol Lett. 1998;62:59–66.
  • Yang B, Wang J, Tang B, et al. Characterization of bioactive recombinant human lysozyme expressed in milk of cloned transgenic cattle. PLoS One. 2011;6:e17593.
  • Zdybicka-Barabas A, Mak P, Jakubowicz T, et al. Lysozyme and defense peptides as suppressors of phenoloxidase activity in galleria mellonella. Arch Insect Biochem Physiol. 2014;87:1–12.
  • Mak P, Zdybicka-Barabas A, Cytryńska M. A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev Comp Immunol. 2010;34:1129–1136.
  • Vogel H, Altincicek B, Glöckner G, et al. A comprehensive transcriptome and immune- gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12:308.
  • Sowa-Jasiłek A, Zdybicka-Barabas A, Stączek S, et al. Galleria mellonella lysozyme induces apoptotic changes in Candida albicans cells. Microbiol Res. 2016;193:121–131.
  • Zdybicka-Barabas A, Sta̧Czek S, Mak P, et al. Synergistic action of Galleria mellonella apolipophorin III and lysozyme against Gram-negative bacteria. Biochim Biophys Acta - Biomembr. 2013;1828:1449–1456.
  • Ito Y, Nakamura M, Hotani T, et al. Insect lysozyme from house fly (Musca domestica) larvae: possible digestive function based on sequence and enzymatic properties. J Biochem. 1995;118:546–551.
  • Ibrahim HR, Inazaki D, Abdou A, et al. Processing of lysozyme at distinct loops by pepsin: a novel action for generating multiple antimicrobial peptide motifs in the newborn stomach. Biochim Biophys Acta - Gen Subj. 2005;1726:102–114.
  • Evans EW, Harmon BG. A review of antimicrobial peptides: defensins and related cationic peptides. Vet Clin Pathol. 1995;24:109–116.
  • Gallo RL, Murakami M, Ohtake T, et al. Biology and clinical relevance of naturally occurring antimicrobial peptides. J Allergy Clin Immunol. 2002;110:823–831.
  • Ganz T. Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol. 2003;3:710–720.
  • Pazgier M, Hoover DM, Yang D, et al. Human beta-defensins. Cell Mol Life Sci. 2006;63:1294–1313.
  • Yang D, Biragyn A, Kwak LW, et al. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol. 2002;23:291–296.
  • Faruck MO, Yusof F, Chowdhury S. An overview of antifungal peptides derived from insect. Peptides. 2016;80:80–88.
  • Hoffmann JA, Hetru C. Insect defensins: inducible antibacterial peptides. Immunol. Today 1992;13: 411–415.
  • Koehbach J. Structure-activity relationships of insect defensins. Front Chem. 2017;12;5:45.
  • Yi H-Y, Chowdhury M, Huang Y-D, et al. Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol. 2014;98:5807–5822.
  • Li Y, Xiang Q, Zhang Q, et al. Overview on the recent study of antimicrobial peptides: origins, functions, relative mechanisms and application. Peptides. 2012;37:207–215.
  • Li W, Tailhades J, O’Brien-Simpson NM, et al. Proline-rich antimicrobial peptides: potential therapeutics against antibiotic-resistant bacteria. Amino Acids. 2014;46:2287–2294.
  • Li WF, Ma GX, Zhou XX. Apidaecin-type peptides: biodiversity, structure-function relationships and mode of action. Peptides. 2006;27:2350–2359.
  • Mishra AK, Choi J, Moon E, et al. Tryptophan-rich and proline-rich antimicrobial peptides. Molecules. 2018;23:815.
  • Veldhuizen EJA, Schneider VAF, Agustiandari H, et al. Antimicrobial and immunomodulatory activities of PR-39 derived peptides. PLoS One. 2014;9:e95939.
  • Cabiaux V, Agerberth B, Johansson J, et al. Secondary structure and membrane interaction of PR-39, a Pro+Arg-rich antibacterial peptide. Eur J Biochem. 1994;224:1019–1027.
  • Otvos L. The short proline-rich antibacterial peptide family. Cell Mol Life Sci. 2002;59:1138–1150.
  • Runti G, Benincasa M, Giuffrida G, et al. The mechanism of killing by the proline-rich peptide Bac7 (1-35)against clinical strains of Pseudomonas aeruginosa differs from that against other gram-negative bacteria. Antimicrob Agents Chemother. 2017;61. pii:e01660-16.
  • Krizsan A, Prahl C, Goldbach T, et al. Short proline-rich antimicrobial peptides inhibit either the bacterial 70S Ribosome or the assembly of its large 50S subunit. ChemBioChem. 2015;16:2304–2308.
  • Roy RN, Lomakin IB, Gagnon MG, et al. The mechanism of inhibition of protein synthesis by the proline-rich peptide oncocin. Nat Struct Mol Biol. 2015;22:466–469.
  • Mardirossian M, Grzela R, Giglione C, et al. The host antimicrobial peptide Bac71-35 binds to bacterial ribosomal proteins and inhibits protein synthesis. Chem Biol. 2014;21:1639–1647.
  • Wang G, Li X, Wang Z. APD3: the antimicrobial peptide database as a tool for research and education. Nucleic Acids Res. 2016;44:D1087–93.
  • Imler J-L, Bulet P. Antimicrobial peptides in Drosophila: structures, activities and gene regulation. Chem Immunol Allergy. 2005;86:1–21.
  • Andrä J, Berninghausen O, Leippe M. Cecropins, antibacterial peptides from insects and mammals, are potently fungicidal against Candida albicans. Med Microbiol Immunol. 2000;189:169–173.
  • Qu X‐, Steiner H, Engström Å, et al. Insect immunity: isolation and structure of cecropins B and D from Pupae of the Chinese oak silk moth, antheraea pernyi. Eur J Biochem. 1982;127:219–224.
  • Mukherjee K, Mraheil MA, Silva S, et al. Anti-Listeria activities of Galleria mellonella hemolymph proteins. Appl Environ Microbiol. 2011;77:4237–4240.
  • Kim CH, Lee JH, Kim I, et al. Purfication and cDNA cloning of a cecropin-like peptide from the great wax moth, Galleria mellonella. Mol Cells. 2004;17:262–266.
  • Mak P, Chmiel D, Gacek GJ. Antibacterial peptides of the moth Galleria mellonella. Acta Biochim Pol. 2001;48:1191–1195.
  • Bulet P, Hetru C, Dimarcq JL, et al. Antimicrobial peptides in insects; structure and function. Dev Comp Immunol. 1999;23:329–344.
  • Lee J, Lee DG. Antimicrobial peptides (AMPs) with dual mechanisms: membrane disruption and apoptosis. J Microbiol Biotechnol. 2014;25:759–764.
  • Yun JE, Lee DG. Cecropin A-induced apoptosis is regulated by ion balance and glutathione antioxidant system in Candida albicans. IUBMB Life. 2016;68:652–662.
  • Lee E, Shin A, Kim Y. Anti-inflammatory activities of cecropin A and its mechanism of action. Arch Insect Biochem Physiol. 2015;88:31–44.
  • Levashina EA, Ohresser S, Bulet P, et al. Metchnikowin, a novel immune‐inducible proline‐rich peptide from drosophila with antibacterial and antifungal properties. Eur J Biochem. 1995;233:694–700.
  • Moghaddam MRB, Gross T, Becker A, et al. The selective antifungal activity of Drosophila melanogaster metchnikowin reflects the species-dependent inhibition of succinate-coenzyme Q reductase. Sci Rep. 2017;15;7:8192.
  • Wang J, Hu C, Wu Y, et al. Characterization of the antimicrobial peptide attacin loci from Glossina morsitans. Insect Mol Biol. 2008;17:293–302.
  • Bang K, Park S, Yoo JY, et al. Characterization and expression of attacin, an antibacterial protein-encoding gene, from the beet armyworm, Spodoptera exigua (Hübner) (Insecta: Lepidoptera: Noctuidae). Mol Biol Rep. 2012;39:5151–5159.
  • Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol. 2000;182:3843–3845.
  • Slater JL, Gregson L, Denning DW, et al. Pathogenicity of Aspergillus fumigatus mutants assessed in Galleria mellonella matches that in mice. Med Mycol. 2011;49(Suppl 1):S107–13.
  • Senior NJ, Bagnall MC, Champion OL, et al. Galleria mellonella as an infection model for campylobacter jejuni virulence. J Med Microbiol. 2011;60:661–669.
  • Mukherjee K, Altincicek B, Hain T, et al. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol. 2010;76:310–317.
  • Sheehan G, Kavanagh K. Analysis of the early cellular and humoral responses of Galleria mellonella larvae to infection by Candida albicans. Virulence. 2018;9:163–172.
  • Maurer E, Browne N, Surlis C, et al. Galleria mellonella as a host model to study Aspergillus terreus virulence and amphotericin B resistance. Virulence. 2015;6(6):1–8.
  • Wojda I. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 2017;24:342–357.
  • Ramarao N, Nielsen-Leroux C, Lereclus D. The insect Galleria mellonella as a powerful infection model to investigate bacterial pathogenesis. J Vis Exp. 2012211;70:e4392.
  • Brown SE, Howard A, Kasprzak AB, et al. A peptidomics study reveals the impressive antimicrobial peptide arsenal of the wax moth Galleria mellonella. Insect Biochem Mol Biol. 2009;39:792–800.
  • Browne N, Surlis C, Maher A, et al. Prolonged pre-incubation increases the susceptibility of Galleria mellonella larvae to bacterial and fungal infection. Virulence. 2015;6:37–41.
  • Schuhmann B, Seitz V, Vilcinskas A, et al. Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch Insect Biochem Physiol. 2003;53:125–133.
  • Lee YS, Yun EK, Jang WS, et al. Purification, cDNA cloning and expression of an insect defensin from the great wax moth, Galleria mellonella. Insect Mol Biol. 2004;13:65–72.
  • Seitz V, Clermont A, Wedde M, et al. Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev Comp Immunol. 2003;27:207–215.
  • Bolouri Moghaddam MR, Tonk M, Schreiber C, et al. The potential of the Galleria mellonella innate immune system is maximized by the co-presentation of diverse antimicrobial peptides. Biol Chem. 2016;397:939–945.
  • Bergin D, Murphy L, Keenan J, et al. Pre-exposure to yeast protects larvae of Galleria mellonella from a subsequent lethal infection by Candida albicans and is mediated by the increased expression of antimicrobial peptides. Microbes Infect. 2006;8:2105–2112.
  • Mowlds P, Barron A, Kavanagh K. Physical stress primes the immune response of Galleria mellonella larvae to infection by Candida albicans. Microbes Infect. 2008;10:628–634.
  • Mowlds P, Kavanagh K. Effect of pre-incubation temperature on susceptibility of Galleria mellonella larvae to infection by Candida albicans. Mycopathologia. 2008;165:5–12.
  • Brown SE, Howard A, Kasprzak AB, et al. The discovery and analysis of a diverged family of novel antifungal moricin-like peptides in the wax moth Galleria mellonella. Insect Biochem Mol Biol. 2008;38:201–212.
  • Yi H-Y, Deng X-J, Yang W-Y, et al. Gloverins of the silkworm Bombyx mori: structural and binding properties and activities. Insect Biochem Mol Biol. 2013;43:612–625.
  • Sheehan G, Clarke G, Kavanagh K. Characterisation of the cellular and proteomic response of Galleria mellonella larvae to the development of invasive aspergillosis. BMC Microbiol. 2018;18.
  • Lange A, Beier S, Huson DH, et al. Genome sequence of Galleria mellonella (Greater Wax Moth). Genome Announc. 2018;6:e01220–17.
  • Harding CR, Schroeder GN, Reynolds S, et al. Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun. 2012;80:2780–2790.