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Research Paper

Establishing an invertebrate Galleria mellonella greater wax moth larval model of Neisseria gonorrhoeae infection

, , , ORCID Icon & ORCID Icon
Pages 1900-1920 | Received 06 May 2021, Accepted 26 Jun 2021, Published online: 25 Jul 2021

References

  • Rowley J, Vander Hoorn S, Korenromp E, et al. Chlamydia, gonorrhoea, trichomoniasis and syphilis: global prevalence and incidence estimates, 2016. Bull World Health Organ. 2019 Aug 1;97(8):548–562.
  • Mayor MT, Roett MA, Uduhiri KA. Diagnosis and management of gonococcal infections. Am Fam Physician. 2012 Nov 15;86(10):931–938.
  • Humbert MV, Christodoulides M. Atypical, yet not infrequent, infections with Neisseria species. Pathogens. 2019 Dec 20;9(1):10.
  • Hobbs MM, Sparling PF, Cohen MS, et al. Experimental gonococcal infection in male volunteers: cumulative experience with Neisseria gonorrhoeae strains FA1090 and MS11mkC. Front Microbiol. 2011;2:123.
  • Rice PA, Shafer WM, Ram S, et al. Neisseria gonorrhoeae: drug resistance, mouse models, and vaccine development. Annu Rev Microbiol. 2017 Sep 08;71(1):665–686.
  • Islam EA, Anipindi VC, Francis I, et al. Specific binding to differentially expressed human carcinoembryonic antigen-related cell adhesion molecules determines the outcome of Neisseria gonorrhoeae infections along the female reproductive tract. Infect Immun. 2018 Aug;86(8). doi:10.1128/IAI.00092-18.
  • Kaser T, Renois F, Wilson HL, et al. Contribution of the swine model in the study of human sexually transmitted infections. Infect Genet Evol. 2018 Dec;66:346–360.
  • Christodoulides M. Neisseria gonorrhoeae: methods and protocols. Christodoulides M, editor. New York: Springer/Humana Press. 2019. Walker J, editor. Methods in Molecular Biology.
  • Ma M, Powell DA, Weyand NJ, et al. A natural mouse model for Neisseria colonization. Infect Immun. 2018 May;86(5). doi:10.1128/IAI.00839-17.
  • Unemo M, Del Rio C, Shafer WM. Antimicrobial resistance expressed by Neisseria gonorrhoeae: a major global public health problem in the 21st century. Microbiol Spectr. 2016 Jun;4(3):DOI:10.1128/microbiolspec.EI10-0009-2015
  • Chantawannakul P, De Guzman LI, Li JL, et al. Parasites, pathogens, and pests of honeybees in Asia. Apidologie. 2016 May;47(3):301–324.
  • Ellis JD, Graham JR, Mortensen A. Standard methods for wax moth research. J Apicult Res. 2013;52(1):1–17.
  • Tsai CJ, Loh JM, Proft T. Galleria mellonella infection models for the study of bacterial diseases and for antimicrobial drug testing. Virulence. 2016 Apr 2;7(3):214–229.
  • Vilmos P, Kurucz E. Insect immunity: evolutionary roots of the mammalian innate immune system. Immunol Lett. 1998 Jun;62(2):59–66.
  • Ratcliffe NA. Invertebrate immunity--a primer for the non-specialist. Immunol Lett. 1985;10(5):253–270.
  • Soderhall K, Cerenius L. Role of the prophenoloxidase-activating system in invertebrate immunity. Curr Opin Immunol. 1998 Feb;10(1):23–28.
  • Kavanagh K, Reeves EP. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol Rev. 2004 Feb;28(1):101–112.
  • Wilson R, Ratcliffe NA. Effect of lysozyme on the lectin-mediated phagocytosis of Bacillus cereus by haemocytes of the cockroach, Blaberus discoidalis. J Insect Physiol. 2000 May 1;46(5):663–670.
  • Lysenko O. The mechanism of pathogenicity of Pseudomonas aeruginosa (Schroeter) Migula. I. The pathogenicity of the strain N 06 to the wax moth larvae. J Insect Pathol. 1963;5.
  • Li Y, Spiropoulos J, Cooley W, et al. Galleria mellonella - a novel infection model for the Mycobacterium tuberculosis complex. Virulence. 2018;9(1):1126–1137.
  • Schell MA, Lipscomb L, DeShazer D. Comparative genomics and an insect model rapidly identify novel virulence genes of Burkholderia mallei. J Bact. 2008 Apr;190(7):2306–2313.
  • Peleg AY, Monga D, Pillai S, et al. Reduced susceptibility to vancomycin influences pathogenicity in Staphylococcus aureus Infection. J Infect Dis. 2009 Feb;199(4):532–536.
  • Mukherjee K, Altincicek B, Hain T, et al. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol. 2010 Jan;76(1):310–317.
  • Evans BA, Rozen DE. A Streptococcus pneumoniae infection model in larvae of the wax moth Galleria mellonella. Eur J Clin Micro Infect Dis. 2012 Oct;31(10):2653–2660.
  • Pereira MF, Rossi CC, Vieira de Queiroz M, et al. Galleria mellonella is an effective model to study Actinobacillus pleuropneumoniae infection. Microbiology (Reading). 2015 Feb;161(Pt 2):387–400.
  • 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 Jul 4;8(4):335–350.
  • Yang HF, Pan AJ, Hu LF, et al. Galleria mellonella as an in vivo model for assessing the efficacy of antimicrobial agents against Enterobacter cloacae infection. J Micro Imm Infect. 2017 Feb;50(1):55–61.
  • White AG, Gibson NHE, Wolf J. A method for measuring dose of a pathogen ingested by larvae of greater wax moth Galleria mellonella, in bioassays of Bacillus thuringiensis. J Invert Path. 1970;15(2):196.
  • Cotter G, Doyle S, Kavanagh K. Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol Med Micro. 2000 Feb;27(2):163–169.
  • Torrecilhas AC, Xander P, Ferreira KS, et al. Alternative host models for testing anti-protozoal or antifungal compounds and fungal infection. Current Top Med Chem. 2018;18(4):300–311.
  • Cutuli MA, Petronio Petronio G, Vergalito F, et al. Galleria mellonella as a consolidated in vivo model hosts: new developments in antibacterial strategies and novel drug testing. Virulence. 2019;10(1):527–541. 2019/01/01.
  • Zak K, Diaz JL, Jackson D, et al. Antigenic variation during infection with Neisseria gonorrhoeae: detection of antibodies to surface proteins in sera of patients with gonorrhea. J Infect Dis. 1984;1984(149):166–173.
  • Williams JN, Skipp PJ, Humphries HE, et al. Proteomic analysis of outer membranes and vesicles from wild-type serogroup B Neisseria meningitidis and a lipopolysaccharide-deficient mutant. Infect Immun. 2007 2007;75(3):1364–1372.
  • Loh JM, Adenwalla N, Wiles S, et al. Galleria mellonella larvae as an infection model for group A streptococcus. Virulence. 2013 Jul 1;4(5):419–428.
  • Santos RB, Scorzoni L, Namba AM, et al. Lactobacillus species increase the survival of Galleria mellonella infected with Candida albicans and non-albicans Candida clinical isolates. Med Mycol. 2019 Apr 1;57(3):391–394.
  • Scalfaro C, Iacobino A, Nardis C, et al. Galleria mellonella as an in vivo model for assessing the protective activity of probiotics against gastrointestinal bacterial pathogens. FEMS Micro Lett. 2017 Apr 1;364(7). 10.1093/femsle/fnx064
  • 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 Jul;8(8):2105–2112.
  • Taszlow P, Vertyporokh L, Wojda I. Humoral immune response of Galleria mellonella after repeated infection with Bacillus thuringiensis. J Invertebr Pathol. 2017 Oct;149:87–96.
  • Kameka AM, Haddadi S, Jamaldeen FJ, et al. Clodronate treatment significantly depletes macrophages in chickens. Can J Vet Res. 2014 Oct;78(4):274–282.
  • Kwon H, Smith RC. Chemical depletion of phagocytic immune cells in Anopheles gambiae reveals dual roles of mosquito hemocytes in anti-Plasmodium immunity. Proc Natl Acad Sci U S A. 2019 Jul 9;116(28):14119–14128.
  • Ignasiak K, Maxwell A. Galleria mellonella (greater wax moth) larvae as a model for antibiotic susceptibility testing and acute toxicity trials. BMC Res Notes. 2017 Aug 29;10(1):428.
  • Lucio MI, Kyriazi ME, Hamilton J, et al. Bactericidal effect of 5-Mercapto-2-nitrobenzoic Acid-Coated silver nanoclusters against multidrug-resistant Neisseria gonorrhoeae. ACS Appl Mater Interfaces. 2020 Jun 24;12(25):27994–28003.
  • Churchward CP, Alany RG, Kirk RS, et al. Prevention of Ophthalmia Neonatorum Caused by Neisseria gonorrhoeae Using a fatty acid-based formulation. mBio. 2017 Jul 25;8(4). DOI:10.1128/mBio.00534-17.
  • Foerster S, Gustafsson TN, Brochado AR, et al. The first wide-scale drug repurposing screen using the prestwick chemical library (1200 bioactive molecules) against Neisseria gonorrhoeae identifies high in vitro activity of auranofin and many additional drugs. APMIS. 2020 Mar;128(3):242–250.
  • Merz AJ, So M. Interactions of pathogenic Neisseriae with epithelial cell membranes. Annu Rev Cell Dev Biol. 2000;2000(16):423–457.
  • Wetzler LM, Barry K, Blake MS, et al. Gonococcal lipooligosaccharide sialylation prevents complement-dependent killing by immune sera. Infect Immun. 1992;60(1):39–43.
  • Francis IP, Lui X, Wetzler LM. Isolation of naturally released gonococcal outer membrane vesicles as vaccine antigens. In: Christodoulides M, editor. Neisseria gonorrhoeae: methods and protocols. Methods in molecular biology 1997. New York: Springer/Humana Press; 2019. 2019/05/24ed: pp 121–142.
  • Uronen H, Williams AJ, Dixon G, et al. Gram-negative bacteria induce proinflammatory cytokine production by monocytes in the absence of lipopolysaccharide (LPS). Clin Exp Immunol. 2000;122(3):312–315.
  • Fowler MI, Yin KYHW, Humphries HE, et al. Comparison of the inflammatory responses of human meningeal cells following challenge with Neisseria lactamica and with Neisseria meningitidis. Infect Immun. 2006;74(11):6467–6478.
  • Vaneechoutte M. The human vaginal microbial community. Res Microbiol. 2017 Nov-Dec;168(9–10):811–825.
  • Betts JW, Hornsey M, Wareham DW, et al. In vitro and In vivo Activity of Theaflavin-Epicatechin combinations versus Multidrug-Resistant Acinetobacter baumannii. Infect Dis Ther. 2017 Sep;6(3):435–442.
  • Betts J, Nagel C, Schatzschneider U, et al. Antimicrobial activity of carbon monoxide-releasing molecule [Mn(CO)3(tpa-kappa3N)]Br versus multidrug-resistant isolates of avian pathogenic Escherichia coli and its synergy with colistin. PLoS One. 2017;12(10):e0186359.
  • Guntzel P, Nagel C, Weigelt J, et al. Biological activity of manganese(i) tricarbonyl complexes on multidrug-resistant Gram-negative bacteria: from functional studies to in vivo activity in Galleria mellonella. Metallomics. 2019 Dec 11;11(12):2033–2042.
  • Dolange V, Churchward CP, Christodoulides M, et al. The Growing Threat of Gonococcal Blindness. Antibiotics (Basel). 2018 Jul 12;7(3):59.
  • Strateva T, Mitov I. Contribution of an arsenal of virulence factors to pathogenesis of Pseudomonas aeruginosa infections. Ann Microbiol. 2011;61(4):717–732. 2011/12/01.
  • Sengupta R, Altermann E, Anderson RC, et al. The role of cell surface architecture of Lactobacilli in host-microbe interactions in the gastrointestinal tract. Mediators Inflamm. 2013; Article ID 237921. 2013/03/13.
  • Spurbeck RR, Arvidson CG. Inhibition of Neisseria gonorrhoeae epithelial cell interactions by vaginal Lactobacillus species. Infect Immun. 2008 Jul;76(7):3124–3130.
  • Spurbeck RR, Arvidson CG. Lactobacillus jensenii surface-associated proteins inhibit Neisseria gonorrhoeae adherence to epithelial cells. Infect Immun. 2010 Jul;78(7):3103–3111.
  • Vielfort K, Sjolinder H, Roos S, et al. Adherence of clinically isolated lactobacilli to human cervical cells in competition with Neisseria gonorrhoeae. Microbes Infect. 2008 Oct;10(12–13):1325–1334.
  • Foschi C, Salvo M, Cevenini R, et al. Vaginal lactobacilli reduce Neisseria gonorrhoeae viability through multiple strategies: an in vitro study. Front Cell Infect Microbiol. 2017;7:502.
  • Zheng HY, Alcorn TM, Cohen MS. Effects of H2O2-producing lactobacilli on Neisseria gonorrhoeae growth and catalase activity. J Infect Dis. 1994 Nov;170(5):1209–1215.
  • Graver MA, Wade JJ. The role of acidification in the inhibition of Neisseria gonorrhoeae by vaginal lactobacilli during anaerobic growth. Ann Clin Microbiol Antimicrob. 2011 Feb;17(10):8.
  • Breshears LM, Edwards VL, Ravel J, et al. Lactobacillus crispatus inhibits growth of Gardnerella vaginalis and Neisseria gonorrhoeae on a porcine vaginal mucosa model. BMC Microbiol. 2015 Dec;9(15):276.
  • 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 Sep-Oct;2(5):413–421.
  • Kohler GA, Assefa S, Reid G. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect Dis Obstet Gynecol. 2012;2012:636474.
  • Vilela SF, Barbosa JO, Rossoni RD, et al. Lactobacillus acidophilus ATCC 4356 inhibits biofilm formation by C. albicans and attenuates the experimental candidiasis in Galleria mellonella. Virulence. 2015;6(1):29–39.
  • Rossoni RD, Fuchs BB, De Barros PP, et al. Lactobacillus paracasei modulates the immune system of Galleria mellonella and protects against Candida albicans infection. PLoS One. 2017;12(3):e0173332.
  • Huang XW, Xu MN, Zheng HX, et al. Pre-exposure to Candida glabrata protects Galleria mellonella against subsequent lethal fungal infections. Virulence. 2020;11(1): 1674–1684
  • Krachler AM, Sirisaengtaksin N, Monteith P, et al. Defective phagocyte association during infection of Galleria mellonella with Yersinia pseudotuberculosis is detrimental to both insect host and microbe. Virulence. 2021 Dec;12(1):638–653.
  • Luiz de Freitas L, Pereira da Silva F, Km F, et al. The virulence of Salmonella Enteritidis in Galleria mellonella is improved by N-dodecanoyl-homoserine lactone. Microb Pathog. 2021 Jan;11(152):104730.
  • Kovacs-Simon A, Metters G, Norville I, et al. Coxiella burnetii replicates in Galleria mellonella hemocytes and transcriptome mapping reveals in vivo regulated genes. Virulence. 2020 Dec;11(1):1268–1278.
  • Thomaz L, Gustavo de Almeida L, Fro S, et al. In vivo activity of silver nanoparticles against Pseudomonas aeruginosa Infection in Galleria mellonella. Front Microbiol. 2020;11:582107.
  • Sadarangani M, Pollard AJ, Gray-Owen SD. Opa proteins and CEACAMs: pathways of immune engagement for pathogenic Neisseria. FEMS Microbiol Rev. 2011;35(3):498–514. 5/2011.
  • Chen T, Belland RJ, Wilson J, et al. Adherence of pilus− Opa+ gonococci to epithelial cells in vitro involves heparan sulfate. J Exp Med. 1995;1995(182):511–517.
  • Princivalle M, de Agostini A. Developmental roles of heparan sulfate proteoglycans: a comparative review in Drosophila, mouse and human. Int J Dev Biol. 2002 May;46(3):267–278.
  • Estes Z, Faust R. Studies on the mucopolysaccharides of the greater wax moth, Galleria mellonella (Linnaeus). Comp Biochem Physiol. 1964;13(4):443–452.
  • Melly MA, McGee ZA, Rosenthal RS. Ability of Monomeric Peptidoglycan Fragments from Neisseria gonorrhoeae to Damage Human Fallopian-Tube Mucosa. J Infect Dis. 1984;149(3):378–386.
  • Cloud KA, Dillard JP. A lytic transglycosylase of Neisseria gonorrhoeae is involved in peptidoglycan-derived cytotoxin production. Infect Immun. 2002 Jun;70(6):2752–2757.
  • Almonacid-Mendoza HL, Humbert MV, Dijokaite A, et al. Structure of the recombinant Neisseria gonorrhoeae adhesin complex protein (rNg-ACP) and generation of murine antibodies with bactericidal activity against gonococci. mSphere. 2018 Oct 10;3(5):5.
  • Ward ME, Watt PJ, Glyn AA. Gonococci in urethral exudates possess a virulence factor lost on subculture. Nature. 1970;227(5256):382–384.
  • Lambden PR, Heckels JE. Outer membrane protein composition and colonial morphology of Neisseria gonorrhoeae strain P9. FEMS Micro Lett. 1979;5(4):263–265.
  • McGuinness BT, Clarke IN, Lambden PR, et al. Point mutation in meningococcal porA gene associated with increased endemic disease. Lancet. 1991;337(8740):514–517.
  • Pandey AK, Cleary DW, Laver JR, et al. Neisseria lactamica Y92–1009 complete genome sequence. Stand Genomic Sci. 2017;12(1):41.