Of mice and men and larvae: Galleria mellonella to model the early host-pathogen interactions after fungal infection

References

• Marr KA. Invasive Candida infections: the changing epidemiology. Oncology. 2004;14:9–14
   Google Scholar
• Nucci M, Marr KA. Emerging fungal diseases. Clin Infect Dis. 2005;41:521–526. doi:10.1086/432060. PMID:16028162
   PubMed Web of Science ®Google Scholar
• Ruhnke M. Epidemiology of Candida albicans infections and role of non-Candida albicans yeasts. Curr Drug Targets. 2006;7:495–504. doi:10.2174/138945006776359421. PMID:16611037
   PubMed Web of Science ®Google Scholar
• Borman AM, Szekely A, Johnson EM. Comparative pathogenicity of United Kingdom isolates of the emerging pathogen Candida auris and other key pathogenic Candida species. mSphere. 2016;1(4):e00189–16. doi:10.1128/mSphere.00189-16. PMID:27547827
   PubMed Web of Science ®Google Scholar
• Mayer FL, Wilson D, Hube B. Candida albicans pathogenicity mechanisms. Virulence. 2013;4(2):119–28. doi:10.4161/viru.22913. PMID:23302789
   PubMed Web of Science ®Google Scholar
• Casadevall A, Pirofski LA. What is a host? Incorporating the microbiota into the damage-response framework. Infect Immun. 2015;83(1):2–7 doi:10.1128/IAI.02627-14. PMID:25385796
   PubMed Web of Science ®Google Scholar
• Conti HR, Huppler AR, Whibley N, Gaffen SL. Animal models for candidiasis. Curr Protoc Immunol. 2014;105:19.6.1–17.
   PubMedGoogle Scholar
• Sparber F, LeibundGut-Landmann S. Interleukin 17-mediated host defence against Candida albicans. Pathogens. 2015;4(3):606–19. doi:10.3390/pathogens4030606. PMID:26274976
   PubMed Web of Science ®Google Scholar
• Lionakis MS. Drosophila and Galleria insect model hosts: new tools for the study of fungal virulence, pharmacology and immunology. Virulence. 2011;2(6):521–7. doi:10.4161/viru.2.6.18520. PMID:22186764
   PubMed Web of Science ®Google Scholar
• Kavanagh K, Reeves EP. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev. 2004;28(1):101–12. doi:10.1016/j.femsre.2003.09.002. PMID:14975532
   PubMed Web of Science ®Google Scholar
• Brennan M, Thomas DY, Whiteway M, Kavanagh K. Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol Med Microbiol. 2002;34(2):153–7. doi:10.1111/j.1574-695X.2002.tb00617.x. PMID:12381467
   PubMedGoogle Scholar
• Stokes BA, Yadav S, Shokal U, Smith LC, Eleftherianos I. Bacterial and fungal pattern recognition receptors in homologous innate signaling pathways of insects and mammals. Front Microbiol. 2015;6:19. doi:10.3389/fmicb.2015.00019. PMID:25674081
   PubMed Web of Science ®Google Scholar
• Kim CH, Shin YP, Noh MY, Jo YH, Han YS, Seong YS, Lee IH. An insect multiligand recognition protein functions as an opsonin for the phagocytosis of microorganisms. J Biol Chem. 2010;285(33):25243–50. doi:10.1074/jbc.M110.134940. PMID:20519517
   PubMed Web of Science ®Google Scholar
• Browne N, Heelan M, Kavanagh K. An analysis of the structural and functional similarities of insect hemocytes and mammalian phagocytes. Virulence. 2013;4(7):597–603. doi:10.4161/viru.25906. PMID:23921374
   PubMed Web of Science ®Google Scholar
• Bergin D, Reeves EP, Renwick J, Wientjes FB, Kavanagh K. Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun. 2005;73(7):4161–70
   PubMed Web of Science ®Google Scholar
• Bergman P, Seyedoleslami Esfahani S, Engström Y. Drosophila as a model for human diseases- focus on innate immunity in barrier epithelia. Curr Top Dev Biol. 2017;121:29–81. doi:10.1016/bs.ctdb.2016.07.002. PMID:28057304
   PubMed Web of Science ®Google Scholar
• Yi HY, Chowdhury M, Huang YD, Yu XQ. Insect antimicrobial peptides and their applications. Appl Microbiol Biotechnol. 2014;98(13):5807–22. doi:10.1007/s00253-014-5792-6. PMID:24811407
   PubMed Web of Science ®Google Scholar
• Panayidou S, Ioannidou E, Apidianakis Y. Human pathogenic bacteria, fungi, and viruses in Drosophila: disease modeling, lessons, and shortcomings. Virulence. 2014;5(2):253–69. doi:10.4161/viru.27524. PMID:24398387
   PubMed Web of Science ®Google Scholar
• Lin SC, Chang YY, Chan CC. Strategies for gene disruption in Drosophila. Cell Biosci. 2014;4(1):63. doi:10.1186/2045-3701-4-63. PMID:25364499
   PubMed Web of Science ®Google Scholar
• Gupta V, Oliver B. Drosophila microarray platforms. Brief Funct Genomic Proteomic. 2003;2(2):97–105. doi:10.1093/bfgp/2.2.97. PMID:15239930
   PubMedGoogle Scholar
• Tzou P, De Gregorio E, Lemaitre B. How Drosophila combats microbial infection: a model to study innate immunity and host-pathogen interactions. Curr Opin Microbiol. 2002; 5(1):102–10. doi:10.1016/S1369-5274(02)00294-1. PMID:11834378
   PubMed Web of Science ®Google Scholar
• Imler JL. Overview of Drosophila immunity: a historical perspective. Dev Comp Immunol. 2014;42(1):3–15. doi:10.1016/j.dci.2013.08.018. PMID:24012863
   PubMed Web of Science ®Google Scholar
• Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA. The dorsoventral regulatory gene cassette spätzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell. 1996;86(6):973–83. doi:10.1016/S0092-8674(00)80172-5. PMID:8808632
   PubMed Web of Science ®Google Scholar
• Fallon J, Kelly J, Kavanagh K. Methods. Galleria mellonella as a model for fungal pathogenicity testing. Mol Biol. 2012;845:469–85
   Google Scholar
• Bergin D, Brennan M, Kavanagh K. Fluctuations in haemocyte density and microbial load may be used as indicators of fungal pathogenicity in larvae of Galleria mellonella. Microbes Infect. 2003; 5(15):1389–95. doi:10.1016/j.micinf.2003.09.019. PMID:14670452
   PubMed Web of Science ®Google Scholar
• Mowlds P, Kavanagh K. Effect of pre-incubation temperature on susceptibility of Galleria mellonella larvae to infection by Candida albicans. Mycopathologia. 2008; 165(1):5–12. doi:10.1007/s11046-007-9069-9. PMID:17922218
   PubMed Web of Science ®Google Scholar
• Borman AM, Szekely A, Linton CJ, Palmer MD, Brown P, Johnson EM. Epidemiology, antifungal susceptibility, and pathogenicity of Candida africana isolates from the United Kingdom. J Clin Microbiol. 2013; 51(3):967–72. doi:10.1128/JCM.02816-12. PMID:23303503
   PubMed Web of Science ®Google Scholar
• Bergin D, Murphy L, Keenan J, Clynes M, Kavanagh K. 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(8):2105–12
   PubMed Web of Science ®Google Scholar
• Fallon JP, Troy N, Kavanagh K. Pre-exposure of Galleria mellonella larvae to different doses of Aspergillus fumigatus conidia causes differential activation of cellular and humoral immune responses. Virulence. 2011;2(5):413–21. doi:10.1016/j.micinf.2006.03.005. doi:10.4161/viru.2.5.17811. PMID: 21921688. PMID:16782387
   PubMed Web of Science ®Google Scholar
• Binder U, Maurer E, Lass-Flörl C. Galleria mellonella: An invertebrate model to study pathogenicity in correctly defined fungal species. Fungal Biol. 2016;120(2):288–95. doi:10.1016/j.funbio.2015.06.002. PMID:26781383
   PubMed Web of Science ®Google Scholar
• Cotter G, Doyle S, Kavanagh K. Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Microbiol. 2000;27(2):163–9. doi:10.1111/j.1574-695X.2000.tb01427.x. PMID:10640612
   PubMedGoogle Scholar
• Trieu TA, Navarro-Mendoza MI, Pérez-Arques C, Sanchis M, Capilla J, Navarro-Rodriguez P, Lopez-Fernandez L, Torres-Martínez S, Garre V, Ruiz-Vázquez RM, et al. RNAi-based functional genomics identifies new virulence determinants in Mucormycosis. PLoS Pathog. 2017;13(1):e1006150. doi:10.1371/journal.ppat.1006150. PMID:28107502
   PubMed Web of Science ®Google Scholar
• 33 Renshaw H, Vargas-Muñiz JM, Richards AD, Asfaw YG, Juvvadi PR, Steinbach WJ. Distinct roles of myosins in Aspergillus fumigatus hyphal growth and pathogenesis. Infect Immun. 2016; 84(5):1556–64. doi:10.1128/IAI.01190-15. PMID:26953327
   PubMed Web of Science ®Google Scholar
• 34 Moralez AT, Perini HF, Furlaneto-Maia L, Almeida RS, Panagio LA, Furlaneto MC. Phenotypic switching of Candida tropicalis is associated with cell damage in epithelial cells and virulence in Galleria mellonella model. Virulence. 2016;7(4):379–86. doi:10.1080/21505594.2016.1140297. PMID:26760314
   PubMed Web of Science ®Google Scholar
• 35 Fuchs BB, Li Y, Li D, Johnston T, Hendricks G, Li G, Rajamuthiah R, Mylonakis E. Micafungin elicits an immunomodulatory effect in Galleria mellonella and mice. Mycopathologia. 2016;181(1–2):17–25. doi:10.1007/s11046-015-9940-z. PMID:26384671
   PubMed Web of Science ®Google Scholar
• Souza AC, Fuchs BB, Pinhati HM, Siqueira RA, Hagen F, Meis JF, Mylonakis E, Colombo AL. Candida parapsilosis resistance to fluconazole: molecular mechanisms and in vivo impact in infected Galleria mellonella larvae. Antimicrob Agents Chemother. 2015;59(10):6581–7. doi:10.1128/AAC.01177-15. PMID:26259795
   PubMed Web of Science ®Google Scholar
• Scorzoni L, de Lucas MP, Mesa-Arango AC, Fusco-Almeida AM, Lozano E, Cuenca-Estrella M, Mendes-Giannini MJ, Zaragoza O. Antifungal efficacy during Candida krusei infection in non-conventional models correlates with the yeast in vitro susceptibility profile. PLoS One. 2013;8(3):e60047. doi:10.1371/journal.pone.0060047. PMID:23555877
   PubMed Web of Science ®Google Scholar
• Mylonakis E, Moreno R, El Khoury JB, Idnurm A, Heitman J, Calderwood SB, Ausubel FM, Diener A. Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect Immun. 2005;73(7):3842–50. doi:10.1128/IAI.73.7.3842-3850.2005. PMID:15972469
   PubMed Web of Science ®Google Scholar
• Astvad KMT, Meletiadis J, Whalley S, Arendrup MC. Fluconazole pharmacokinetics in the Galleria mellonella larvae and performance evaluation of a bioassay compared to LC-MS/MS for haemolymph specimens. Antimicrob Agents Chemother. 2017;61(10). pii: e00895–17. doi:10.1128/AAC.00895-17. PMID:28760893
   PubMed Web of Science ®Google Scholar
• de Oliveira HC, Michaloski JS, da Silva JF, Scorzoni L, de Paula E, Silva AC, Marcos CM, Assato PA, Yamazaki DS, Fusco-Almeida AM, et al. Peptides derived from a phage display library inhibit adhesion and protect the host against Infection by Paracoccidioides brasiliensis and Paracoccidioides lutzii. Front Pharmacol. 2016;7:509. doi:10.3389/fphar.2016.00509. PMID:28066254
   PubMed Web of Science ®Google Scholar
• Sangalli-Leite F, Scorzoni L, Alves de Paula E, Silva AC, da Silva JF, de Oliveira HC, de Lacorte Singulani J, Gullo FP, Moraes da Silva R, Regasini LO, et al. Synergistic effect of pedalitin and amphotericin B against Cryptococcus neoformans by in vitro and in vivo evaluation. Int J Antimicrob Agents. 2016;48(5):504–511. doi:10.1016/j.ijantimicag.2016.07.025. PMID:27742203
   PubMed Web of Science ®Google Scholar
• Rossoni RD, Fuchs BB, de Barros PP, Velloso MD, Jorge AO, Junqueira JC, Mylonakis E. Lactobacillus paracasei modulates the immune system of Galleria mellonella and protects against Candida albicans infection. PLoS One. 2017; 12(3):e0173332. doi:10.1371/journal.pone.0173332. PMID:28267809
   PubMed Web of Science ®Google Scholar
• Ribeiro FC, de Barros PP, Rossoni RD, Junqueira JC, Jorge AO. Lactobacillus rhamnosus inhibits Candida albicans virulence factors in vitro and modulates immune system in Galleria mellonella. J Appl Microbiol. 2017;122(1):201–211. doi:10.1111/jam.13324. PMID:27727499
   PubMed Web of Science ®Google Scholar
• Kloezen W, van Helvert-van Poppel M, Fahal AH, van de Sande WW. A Madurella mycetomatis grain model in Galleria mellonella larvae. PLoS Negl Trop Dis. 2015; 9(7):e0003926. doi:10.1371/journal.pntd.0003926. PMID:26173126
   PubMed Web of Science ®Google Scholar
• Mukherjee K, Hain T, Fischer R, Chakraborty T, Vilcinskas A. Brain infection and activation of neuronal repair mechanisms by the human pathogen Listeria monocytogenes in the lepidopteran model host Galleria mellonella. Virulence. 2013; 4(4):324–32 doi:10.4161/viru.23629. PMID:23348912
   PubMed Web of Science ®Google Scholar
• Sheehan G, Kavanagh K. Analysis of the early cellular and humoral responses of Galleria mellonella larvae to infection by Candida albicans. Virulence. 2017 doi:10.1080/21505594.2017.1370174. PMID:28872999
   PubMed Web of Science ®Google Scholar
• Vogel H, Altincicek B, Glöckner G, Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12:308. PMID:21663692
   PubMed Web of Science ®Google Scholar
• MacCallum DM. Massive induction of innate immune response to Candida albicans in the kidney in a murine intravenous challenge model. FEMS Yeast Res. 2009;9:1111–22.
   PubMed Web of Science ®Google Scholar