Top

Published in:

2013 | OriginalPaper | Chapter

Galleria Mellonella as a Model Host to Study Gut Microbe Homeostasis and Brain Infection by the Human Pathogen Listeria Monocytogenes

Authors : Krishnendu Mukherjee, Ramya Raju, Rainer Fischer, Andreas Vilcinskas

Published in: Yellow Biotechnology I

Publisher: Springer Berlin Heidelberg

Activate our intelligent search to find suitable subject content or patents.

search-config

AI-assisted search

Off

Abstract

The gastrointestinal tract in both mammals and insects is associated with microbes (collectively the microbiota), which are controlled by the intestinal immune system. These microbes regulate pathogens that can infect gut epithelial cells, and there is increasing evidence for a reciprocal relationship between beneficial and pathogenic bacteria in the gut and the intestinal immune system. Deciphering these complex interactions between the microbiota and intestinal immune system in mammals requires surrogate model systems, such as larvae of the greater wax moth Galleria mellonella. The exposure of G. mellonella microbiota to antibiotics induces immunity and stress-related genes in the intestine. The model can also provide insight into the virulence mechanisms of pathogens such as Listeria monocytogenes in the human gut and brain. We also discuss the current uses of G. mellonella as a model to develop therapeutic strategies against listeriosis.

Graphical Abstract

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

inform now

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

inform now

previous chapter Utility of Insects for Studying Human Pathogens and Evaluating New Antimicrobial Agents

next chapter Drosophila as a Model to Study Metabolic Disorders

Maynard CL, Elson CO, Hatton RD, Weaver CT (2012) Reciprocal interactions of the intestinal microbiota and immune system. Nature 489(7415):231–241CrossRef

Kelly D, Mulder IE (2012) Microbiome and immunological interactions. Nutr Rev 70(Suppl 1):S18–S30CrossRef

Boissière A, Tchioffo MT, Bachar D, Abate L, Marie A, Nsango SE, Shahbazkia HR, Awono-Ambene PH, Levashina EA, Christen R, Morlais I (2012) Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum infection. PLoS Pathog 8(5):e1002742. doi:10.1371/journal.ppat.1002742 CrossRef

Glavis-Bloom J, Muhammed M, Mylonakis E (2012) Of model hosts and man: using Caenorhabditis elegans, Drosophila melanogaster and Galleria mellonella as model hosts for infectious disease research. Adv Exp Med Biol 710:11–17

Chamilos G, Samonis G, Kontoyiannis DP (2011) Drosophila melanogaster as a model host for the study of microbial pathogenicity and the discovery of novel antimicrobial compounds. Curr Pharm Des 17(13):1246–1253CrossRef

Vilcinskas A (2011) Anti-infective therapeutics from the Lepidopteran model host Galleria mellonella. Curr Pharm Des 17(13):1240–1245CrossRef

Mukherjee K, Fischer R, Vilcinskas A (2012) Histone acetylation mediates epigenetic regulation of transcriptional reprogramming in insects during metamorphosis, wounding and infection. Front Zool 9:25

Ooi ST, Lorber B (2005) Gastroenteritis due to Listeria monocytogenes. Clin Infect Dis 40(9):1327–1332CrossRef

Mukherjee K, Hain T, Fischer R, Chakraborty T, Vilcinskas A (2013) Brain infection and activation of neuronal repair mechanisms by the human pathogen Listeria monocytogenes in the lepidopteran model host Galleria mellonella. Virulence 4(4):324–332. doi:10.4161/viru.23629

10.

Mukherjee K, Abu Mraheil M, Silva S, Müller D, Cemic F, Hemberger J, Hain T, Vilcinskas A, Chakraborty T (2011) Anti-listeria activities of Galleria mellonella hemolymph proteins. Appl Environ Microbiol 77(12):4237–4240CrossRef

11.

Sudakaran S, Salem H, Kost C, Kaltenpoth M (2012) Geographical and ecological stability of the symbiotic mid-gut microbiota in European firebugs, Pyrrhocoris apterus (Hemiptera, Pyrrhocoridae). Mol Ecol 21(24):6134–6151. doi:10.1111/mec.12027 CrossRef

12.

Koch H, Schmid-Hempel P (2012) Gut microbiota instead of host genotype drive the specificity in the interaction of a natural host-parasite system. Ecol Lett 15(10):1095–1103CrossRef

13.

Engel P, Moran NA (2012) Functional and evolutionary insights into the simple yet specific gut microbiota of the honey bee from metagenomic analysis. Gut Microbes 4(1):60–65

14.

Koch H, Schmid-Hempel P (2011) Socially transmitted gut microbiota protect bumble bees against an intestinal parasite. Proc Natl Acad Sci USA 108(48):19288–19292CrossRef

15.

Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. Proc Natl Acad Sci USA 109(27):11002–11007CrossRef

16.

Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA (2005) Diversity of the human intestinal microbial flora. Science 308:1635–1638CrossRef

17.

Ley RE, Peterson DA, Gordon JI (2006) Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837–848CrossRef

18.

Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133CrossRef

19.

Whitman WB, Coleman DC, Wiebe WJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578–6583CrossRef

20.

Xu J, Gordon JI (2007) Inaugural article: honor thy symbionts. Proc Natl Acad Sci USA 100:10452–10459CrossRef

21.

Tang X, Freitak D, Vogel H, Ping L, Shao Y, Cordero EA, Andersen G, Westermann M, Heckel DG, Boland W (2012) Complexity and variability of gut commensal microbiota in polyphagous lepidopteran larvae. PLoS ONE 7(7):e36978CrossRef

22.

Sanz Y, Nadal I, Sanchez E (2007) Probiotics as drugs against human gastrointestinal infections. Recent Pat Anti-Infect Drug Disc 2:148–156CrossRef

23.

Medellin-Pena MJ, Griffiths MW (2009) Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl Environ Microbiol 75:1165–1172CrossRef

24.

Corr SC, Gahan CG, Hill C (2007) Impact of selected Lactobacillus and Bifidobacterium species on Listeria monocytogenes infection and the mucosal immune response. FEMS Immunol Med Microbiol 50:380–388CrossRef

25.

Spor A, Koren O, Ley R (2011) Unravelling the effects of the environment and host genotype on the gut microbiome. Nat Rev Microbiol 9(4):279–290CrossRef

26.

Sekirov I, Russell SL, Antunes LC, Finlay BB (2010) Gut microbiota in health and disease. Physiol Rev 90(3):859–904CrossRef

27.

Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI (2004) The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci USA 101:15718–15723CrossRef

28.

Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884CrossRef

29.

Vilcinskas A (2011) Insects emerge as valuable model hosts to explore virulence. Virulence 2(5):376–378CrossRef

30.

Pitsouli C, Apidianakis Y, Perrimon N (2009) Homeostasis in infected epithelia: stem cells take the lead. Cell Host Microbe 6:301–307CrossRef

31.

Rubin DC (2007) Intestinal morphogenesis. Curr Opin Gastroenterol 23:111–114CrossRef

32.

Hooper LV (2009) Do symbiotic bacteria subvert host immunity? Nat Rev Microbiol 7:367–374CrossRef

33.

Othman M, Aguero R, Lin HC (2008) Alterations in intestinal microbial flora and human disease. Curr Opin Gastroenterol 24:11–16CrossRef

34.

Kelly D, Campbell JI, King TP, Grant G, Jansson EA, Coutts AG, Pettersson S, Conway S (2004) Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol 5:104–112CrossRef

35.

Clermont A, Wedde M, Seitz V, Podsiadlowski L, Lenze D, Hummel M, Vilcinskas A (2004) Cloning and expression of an inhibitor of microbial metalloproteinases from insects contributing to innate immunity. Biochem J 382(Pt 1):315–322

36.

Langen G, Imani J, Altincicek B, Kieseritzky G, Kogel KH, Vilcinskas A (2006) Transgenic expression of gallerimycin, a novel antifungal insect defensin from the greater wax moth Galleria mellonella, confers resistance to pathogenic fungi in tobacco. Biol Chem 387(5):549–557CrossRef

37.

Schuhmann B, Seitz V, Vilcinskas A, Podsiadlowski L (2003) Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch Insect Biochem Physiol 53(3):125–133CrossRef

38.

Altincicek B, Vilcinskas A (2008) Identification of a lepidopteran matrix metalloproteinase with dual roles in metamorphosis and innate immunity. Dev Comp Immunol 32(4):400–409CrossRef

39.

Altincicek B, Vilcinskas A (2006) Metamorphosis and collagen-IV-fragments stimulate innate immune response in the greater wax moth Galleria mellonella. Dev Comp Immunol 30(12):1108–1118CrossRef

40.

De La Cochetiere MF, Durand T, Lalande V, Petit JC, Potel G, Beaugerie L (2008) Effect of antibiotic therapy on human fecal microbiota and the relation to the development of Clostridium difficile. Microb Ecol 56:395–402CrossRef

41.

Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280CrossRef

42.

Jernberg C, Lofmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1:56–66CrossRef

43.

Lofmark S, Jernberg C, Jansson JK, Edlund C (2006) Clindamycin-induced enrichment and long-term persistence of resistant Bacteroides spp. and resistance genes. J Antimicrob Chemother 58:1160–1167CrossRef

44.

Danese S, Sans M, Fiocchi C (2004) Inflammatory bowel disease: the role of environmental factors. Autoimmun Rev 3:394–400CrossRef

45.

Beaugerie L, Petit JC (2004) Microbial-gut interactions in health and disease. Antibiotic-associated diarrhoea. Best Pract Res Clin Gastroenterol 18:337–352CrossRef

46.

Sommer MO, Dantas G, Church GM (2009) Functional characterization of the antibiotic resistance reservoir in the human microflora. Science 325:1128–1131CrossRef

47.

Lee HR, Pimentel M (2006) Bacteria and irritable bowel syndrome: the evidence for small intestinal bacterial overgrowth. Curr Gastroenterol Rep 8:305–311CrossRef

48.

Croswell A, Amir E, Teggatz P, Barman M, Salzman NH (2009) Prolonged impact of antibiotics on intestinal microbial ecology and susceptibility to enteric Salmonella infection. Infect Immun 77:2741–2753CrossRef

49.

Dethlefsen L, Huse S, Sogin ML, Relman DA (2008) The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol 6:e280CrossRef

50.

Jernberg C, Lofmark S, Edlund C, Jansson JK (2007) Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J 1:56–66CrossRef

51.

Lindgren M, Lofmark S, Edlund C, Huovinen P, Jalava J (2009) Prolonged impact of a one-week course of clindamycin on Enterococcus spp. in human normal microbiota. Scand J Infect Dis 41:215–219CrossRef

52.

53.

Garrett WS, Gordon JI, Glimcher LH (2010) Homeostasis and inflammation in the intestine. Cell 140:859–870CrossRef

54.

O’Shea EF, O’Connor PM, Raftis EJ, O’Toole PW, Stanton C, Cotter PD, Ross RP, Hill C (2011) Production of multiple bacteriocins from a single locus by gastrointestinal strains of Lactobacillus salivarius. J Bacteriol 193(24):6973–6982CrossRef

55.

Mukherjee K, Altincicek B, Hain T, Domann E, Vilcinskas A, Chakraborty T (2010) Galleria mellonella as a model system for studying Listeria pathogenesis. Appl Environ Microbiol 76(1):310–317CrossRef

56.

Joyce SA, Gahan CG (2010) Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella. Microbiology 156(Pt 11):3456–3468CrossRef

57.

Vogel H, Altincicek B, Glöckner G, Vilcinskas A (2011) A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 12:308CrossRef

58.

van Sorge NM, Doran KS (2012) Defense at the border: the blood-brain barrier versus bacterial foreigners. Future Microbiol 7(3):383–394CrossRef

59.

Schuchat A, Robinson K, Wenger JD, Harrison LH, Farley M, Reingold AL, Lefkowitz L, Perkins BA (1997) Bacterial meningitis in the United States in 1995. N Engl J Med 337:970–976CrossRef

60.

van de Beek D, de Gans J, Spanjaard L, Weisfelt M, Reitsma JB, Vermeulen M (2004) Clinical features and prognostic factors in adults with bacterial meningitis. N Engl J Med 351:1849–1859CrossRef

61.

Clauss HE, Lorber B (2008) Central nervous system infection with Listeria monocytogenes. Curr Infect Dis Rep 10:300–306CrossRef

62.

Disson O, Lecuit M (2012) Targeting of the central nervous system by Listeria monocytogenes. Virulence 3:213–221CrossRef

Title: Galleria Mellonella as a Model Host to Study Gut Microbe Homeostasis and Brain Infection by the Human Pathogen Listeria Monocytogenes
Authors: Krishnendu Mukherjee
Ramya Raju
Rainer Fischer
Andreas Vilcinskas
Publisher: Springer Berlin Heidelberg
Book: Yellow Biotechnology I
Print ISBN: 978-3-642-39862-9

Electronic ISBN: 978-3-642-39863-6

Copyright Year: 2013
DOI: https://doi.org/10.1007/10_2013_203