Galleria mellonella - a novel infection model for the Mycobacterium tuberculosis complex

References

• W.H.O. Global tuberculosis report. 2016. Switzerland: W.H.O Press.
   Google Scholar
• Dheda K, Gumbo T, Maartens G, et al. The epidemiology, pathogenesis, transmission, diagnosis, and management of multidrug-resistant, extensively drug-resistant, and incurable tuberculosis. Lancet Respir Med. 2017;5:291–360.
   Web of Science ®Google Scholar
• Bell LCK, Noursadeghi M. Pathogenesis of HIV-1 and Mycobacterium tuberculosis co-infection. Nat Rev Microbiol. 2017;16:80–90.
   PubMed Web of Science ®Google Scholar
• Zhan L, Tang J, Sun M, et al. Animal models for tuberculosis in translational and precision medicine. Front Microbiol. 2017;8:717.
   PubMed Web of Science ®Google Scholar
• Gumbo T, Lenaerts AJ, Hanna D, et al. Non-clinical models for anti-tuberculosis drug development: a landscape analysis. J Infect Dis. 2015;211(Suppl 3):S83–95.
   PubMed Web of Science ®Google Scholar
• Cadena AM, Fortune SM, Flynn JL. Heterogeneity in tuberculosis. Nat Rev Immunol. 2017;17:691–702.
   PubMed Web of Science ®Google Scholar
• Flynn JL. Lessons from experimental Mycobacterium tuberculosis infections. Microbes Infect. 2006;8:1179–1188.
   PubMed Web of Science ®Google Scholar
• Kramnik I, Beamer G. Mouse models of human TB pathology: roles in the analysis of necrosis and the development of host-directed therapies. Semin Immunopathol. 2016;38:221–237.
   PubMed Web of Science ®Google Scholar
• Flynn JL, Gideon HP, Mattila JT, et al. Immunology studies in non-human primate models of tuberculosis. Immunol Rev. 2015;264:60–73.
   PubMed Web of Science ®Google Scholar
• Pena JC, Ho WZ. Monkey models of tuberculosis: lessons learned. Infect Immun. 2015;83:852–862.
   PubMed Web of Science ®Google Scholar
• Cook SM, McArthur JD. Developing Galleria mellonella as a model host for human pathogens. Virulence. 2013;4:350–353.
   PubMed Web of Science ®Google Scholar
• Binder U, Maurer E, Lass-Florl C. Galleria mellonella: an invertebrate model to study pathogenicity in correctly defined fungal species. Fungal Biol. 2016;120:288–295.
   PubMed Web of Science ®Google Scholar
• Borman AM. Of mice and men and larvae: Galleria mellonella to model the early host-pathogen interactions after fungal infection. Virulence. 2017;9:9–12.
   PubMed Web of Science ®Google Scholar
• Jander G, Rahme LG, Ausubel FM. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J Bacteriol. 2000;182:3843–3845.
   PubMed Web of Science ®Google Scholar
• Tsai CJ, Loh JM, Proft T. Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence. 2016;7:214–229.
   PubMed Web of Science ®Google Scholar
• Wojda I. Immunity of the greater wax moth Galleria mellonella. Insect Sci. 2017;24:342–357.
   PubMed Web of Science ®Google Scholar
• Wu G, Liu Y, Ding Y, et al. Ultrastructural and functional characterization of circulating hemocytes from Galleria mellonella larva: cell types and their role in the innate immunity. Tissue Cell. 2016;48:297–304.
   PubMed Web of Science ®Google Scholar
• Mak P, Zdybicka-Barabas A, Cytrynska M. A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev Comp Immunol. 2010;34:1129–1136.
   PubMed Web of Science ®Google Scholar
• Lopez Hernandez Y, Yero D, Pinos-Rodriguez JM, et al. Animals devoid of pulmonary system as infection models in the study of lung bacterial pathogens. Front Microbiol. 2015;6:38.
   PubMed Web of Science ®Google Scholar
• Ramarao N, Nielsen-Leroux C, Lereclus D. The insect Galleria mellonella as a powerful infection model to investigate bacterial pathogenesis. J Vis Exp. 2012;70:e4392.
   Google Scholar
• Snewin V, Gares MP, Gaora PO, et al. Assessment of immunity to mycobacterial infection with luciferase reporter constructs. Infect Immun. 1999;67:4586–4593.
   PubMed Web of Science ®Google Scholar
• Newton S, Martineau A, Kampmann B. A functional whole blood assay to measure viability of mycobacteria, using reporter-gene tagged BCG or M.Tb (BCG lux/M.Tb lux). J Vis Exp. 2011;55:e3332.
   Google Scholar
• Kampmann B, Gaora PO, Snewin VA, et al. Evaluation of human anti-mycobacterial immunity using recombinant reporter mycobacteria. J Infect Dis. 2000;182:895–901.
   PubMed Web of Science ®Google Scholar
• Kampmann B, Tena GN, Mzazi S, et al. Novel human in vitro system for evaluating antimycobacterial vaccines. Infect Immun. 2004;72:6401–6407.
   PubMed Web of Science ®Google Scholar
• Kampmann B, Tena-Coki GN, Nicol MP, et al. Reconstitution of anti-mycobacterial immune responses in HIV-infected children receiving HAART. AIDS. 2006;20:1011–1018.
   PubMed Web of Science ®Google Scholar
• Tena GN, Young DB, Eley B, et al. Failure to control growth of mycobacteria in blood from children infected with human immunodeficiency virus and its relationship to T cell function. J Infect Dis. 2003;187:1544–1551.
   PubMed Web of Science ®Google Scholar
• Andreu N, Zelmer A, Fletcher T, et al. Optimisation of bioluminescent reporters for use with mycobacteria. PLoS One. 2010;5:e10777.
   PubMed Web of Science ®Google Scholar
• Newton SM, Mackie SL, Martineau AR, et al. Reduction of chemokine secretion in response to mycobacteria in infliximab-treated patients. Clin Vaccine Immunol. 2008;15:506–512.
   PubMed Web of Science ®Google Scholar
• Martineau AR, Newton SM, Wilkinson KA, et al. Neutrophil-mediated innate immune resistance to mycobacteria. J Clin Invest. 2007;117:1988–1994.
   PubMed Web of Science ®Google Scholar
• Martineau AR, Wilkinson KA, Newton SM, et al. IFN-gamma- and TNF-independent vitamin D-inducible human suppression of mycobacteria: the role of cathelicidin LL-37. J Immunol. 2007;178:7190–7198.
   PubMed Web of Science ®Google Scholar
• Martineau AR, Wilkinson RJ, Wilkinson KA, et al. A single dose of vitamin D enhances immunity to mycobacteria. Am J Resp Crit Care. 2007;176:208–213.
   PubMed Web of Science ®Google Scholar
• von Both U, Berk M, Agapow PM, et al. Mycobacterium tuberculosis exploits a molecular off switch of the immune system for intracellular survival. Sci Rep. 2018;8:661.
   PubMed Web of Science ®Google Scholar
• Jarosz J. Gut flora of Galleria mellonella suppressing ingested bacteria. J Invertebr Pathol. 1979;34:192–198.
   PubMed Web of Science ®Google Scholar
• Thomaz L, Garcia-Rodas R, Guimaraes AJ, et al. Galleria mellonella as a model host to study Paracoccidioides lutzii and Histoplasma capsulatum. Virulence. 2013;4:139–146.
   PubMed Web of Science ®Google Scholar
• Entwistle FM, Coote PJ. Evaluation of greater wax moth larvae, Galleria mellonella, as a novel in vivo model for non-tuberculosis Mycobacteria infections and antibiotic treatments. J Med Microbiol. 2018;67:585–597.
   PubMed Web of Science ®Google Scholar
• Browne N, Kavanagh K. Developing the potential of using Galleria mellonella larvae as models for studying brain infection by Listeria monocytogenes. Virulence. 2013;4:271–272.
   PubMed Web of Science ®Google Scholar
• Freires IA, Sardi JC, de Castro RD, et al. Alternative animal and non-animal models for drug discovery and development: bonus or burden? Pharm Res. 2017;34:681–686.
   PubMed Web of Science ®Google Scholar
• Dionne MS, Ghori N, Schneider DS. Drosophila melanogaster is a genetically tractable model host for Mycobacterium marinum. Infect Immun. 2003;71:3540–3550.
   PubMed Web of Science ®Google Scholar
• Dionne MS, Pham LN, Shirasu-Hiza M, et al. Akt and foxo dysregulation contribute to infection-induced wasting in Drosophila. Curr Biol. 2006;16:1977–1985.
   PubMed Web of Science ®Google Scholar
• Oh CT, Moon C, Choi TH, et al. Mycobacterium marinum infection in Drosophila melanogaster for antimycobacterial activity assessment. J Antimicrob Chemother. 2013;68:601–609.
   PubMed Web of Science ®Google Scholar
• Oh CT, Moon C, Jeong MS, et al. Drosophila melanogaster model for Mycobacterium abscessus infection. Microbes Infect. 2013;15:788–795.
   PubMed Web of Science ®Google Scholar
• Buyukguzel E, Tunaz H, Stanley D, et al. Eicosanoids mediate Galleria mellonella cellular immune response to viral infection. J Insect Physiol. 2007;53:99–105.
   PubMed Web of Science ®Google Scholar
• Garzon S, Charpentier G, Kurstak E. Morphogenesis of the nodamura virus in the larvae of the lepidopteran Galleria mellonella (L.). Arch Virol. 1978;56:61–76.
   PubMed Web of Science ®Google Scholar
• Ozkan S, Coutts RH. Aspergillus fumigatus mycovirus causes mild hypervirulent effect on pathogenicity when tested on Galleria mellonella. Fungal Genet Biol. 2015;76:20–26.
   PubMed Web of Science ®Google Scholar
• Dalton JP, Uy B, Swift S, et al. A novel restraint device for injection of Galleria mellonella larvae that minimizes the risk of accidental operator needle stick injury. Front Cell Infect Microbiol. 2017;7:99.
   PubMed Web of Science ®Google Scholar
• Rwegasila E, Mubofu EB, Nyandoro SS, et al. Preparation, characterization and in vivo antimycobacterial studies of panchovillin-chitosan nanocomposites. Int J Mol Sci. 2016;17:E1559.
   PubMed Web of Science ®Google Scholar
• Erasto P, Omolo J, Sunguruma R, et al. Evaluation of antimycobacterial activity of higenamine using Galleria mellonella as an in vivo infection model. Nat Prod Bioprospect. 2018;8:63–69.
   PubMed Web of Science ®Google Scholar
• Meir M, Grosfeld T, Barkan D. Establishment and validation of Galleria mellonella as a novel model organism to study Mycobacterium abscessus infection, pathogenesis and treatment. Antimicrob Agents Chemother. 2018;62:e02539-17.
   PubMed Web of Science ®Google Scholar
• Harding CR, Schroeder GN, Reynolds S, et al. Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun. 2012;80:2780–2790.
   PubMed Web of Science ®Google Scholar
• Vogel H, Altincicek B, Glockner G, et al. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics. 2011;12:308.
   PubMed Web of Science ®Google Scholar
• Khara JS, Wang Y, Ke XY, et al. Anti-mycobacterial activities of synthetic cationic alpha-helical peptides and their synergism with rifampicin. Biomaterials. 2014;35:2032–2038.
   PubMed Web of Science ®Google Scholar
• Tomiotto-Pellissier F, Cataneo AHD, Orsini TM, et al. Galleria mellonella hemocytes: A novel phagocytic assay for Leishmania (Viannia) braziliensis. J Microbiol Methods. 2016;131:45–50.
   PubMed Web of Science ®Google Scholar
• Harding CR, Schroeder GN, Collins JW, et al. Use of Galleria mellonella as a model organism to study Legionella pneumophila infection. J Vis Exp. 2013;81:e50964.
   Google Scholar
• Card R, Vaughan K, Bagnall M, et al. Virulence characterisation of Salmonella enterica isolates of differing antimicrobial resistance recovered from UK livestock and imported meat samples. Front Microbiol. 2016;7:640.
   PubMed Web of Science ®Google Scholar
• La Rosa SL, Casey PG, Hill C, et al. In vivo assessment of growth and virulence gene expression during commensal and pathogenic lifestyles of luxABCDE-tagged Enterococcus faecalis strains in murine gastrointestinal and intravenous infection models. Appl Environ Microbiol. 2013;79:3986–3997.
   PubMed Web of Science ®Google Scholar
• Barry CE 3rd, Boshoff HI, Dartois V, et al. The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol. 2009;7:845–855.
   PubMed Web of Science ®Google Scholar
• Meijer AH. Protection and pathology in TB: learning from the zebrafish model. Semin Immunopathol. 2016;38:261–273.
   PubMed Web of Science ®Google Scholar
• Nuermberger EL. Preclinical efficacy testing of new drug candidates. Microbiol Spectr. 2017;5:TBTB2-0034–2017.
   PubMed Web of Science ®Google Scholar
• Meijer AH, Spaink HP. Host-pathogen interactions made transparent with the zebrafish model. Curr Drug Targets. 2011;12:1000–1017.
   PubMed Web of Science ®Google Scholar
• Myllymaki H, Bauerlein CA, Ramet M. The zebrafish breathes new life into the study of tuberculosis. Front Immunol. 2016;7:196.
   PubMed Web of Science ®Google Scholar
• van der Vaart M, van Soest JJ, Spaink HP, et al. Functional analysis of a zebrafish myd88 mutant identifies key transcriptional components of the innate immune system. Dis Model Mech. 2013;6:841–854.
   PubMed Web of Science ®Google Scholar
• Hammaren MM, Oksanen KE, Nisula HM, et al. Adequate Th2-type response associates with restricted bacterial growth in latent mycobacterial infection of zebrafish. PLoS Pathog. 2014;10:e1004190.
   PubMed Web of Science ®Google Scholar
• Santucci P, Bouzid F, Smichi N, et al. Experimental models of foamy macrophages and approaches for dissecting the mechanisms of lipid accumulation and consumption during dormancy and reactivation of tuberculosis. Front Cell Infect Microbiol. 2016;6:122.
   PubMed Web of Science ®Google Scholar
• Russell DG, Cardona PJ, Kim MJ, et al. Foamy macrophages and the progression of the human tuberculosis granuloma. Nat Immunol. 2009;10:943–948.
   PubMed Web of Science ®Google Scholar
• Prosser G, Brandenburg J, Reiling N, et al. The bacillary and macrophage response to hypoxia in tuberculosis and the consequences for T cell antigen recognition. Microbes Infect. 2017;19:177–192.
   PubMed Web of Science ®Google Scholar
• Desbois AP, Coote PJ. Utility of greater wax moth larva (Galleria mellonella) for evaluating the toxicity and efficacy of new antimicrobial agents. Adv Appl Microbiol. 2012;78:25–53.
   PubMed Web of Science ®Google Scholar