Galleria mellonella as a model system for studying Listeria pathogenesis.

Krishnendu Mukherjee, Boran Altincicek, Torsten Hain, Eugen Domann, Andreas Vilcinskas, Trinad Chakraborty
Author Information
  1. Krishnendu Mukherjee: Institute for Phytopathology and Applied Zoology, Justus Liebig University, Frankfurter Strasse 107, 35392 Giessen, Germany.

Abstract

Essential aspects of the innate immune response to microbial infection are conserved between insects and mammals. This has generated interest in using insects as model organisms to study host-microbe interactions. We used the greater wax moth Galleria mellonella, which can be reared at 37 degrees C, as a model host for examining the virulence potential of Listeria spp. Here we report that Galleria is an excellent surrogate model of listerial septic infection, capable of clearly distinguishing between pathogenic and nonpathogenic Listeria strains and even between virulent and attenuated Listeria monocytogenes strains. Virulence required listerial genes hitherto implicated in the mouse infection model and was linked to strong antimicrobial activities in both hemolymph and hemocytes of infected larvae. Following Listeria infection, the expression of immune defense genes such as those for lysozyme, galiomycin, gallerimycin, and insect metalloproteinase inhibitor (IMPI) was sequentially induced. Preinduction of antimicrobial activity by treatment of larvae with lipopolysaccharide (LPS) significantly improved survival against subsequent L. monocytogenes challenge and strong antilisterial activity was detected in the hemolymph of LPS pretreated larvae. We conclude that the severity of septic infection with L. monocytogenes is modulated primarily by innate immune responses, and we suggest the use of Galleria as a relatively simple, nonmammalian model system that can be used to assess the virulence of strains of Listeria spp. isolated from a wide variety of settings from both the clinic and the environment.

References

  1. Gene. 1990 Sep 28;94(1):129-32 [PMID: 2121618]
  2. Proc Natl Acad Sci U S A. 2009 Feb 24;106(8):2818-23 [PMID: 19196973]
  3. Science. 2001 Oct 26;294(5543):849-52 [PMID: 11679669]
  4. Clin Microbiol Rev. 2001 Jul;14(3):584-640 [PMID: 11432815]
  5. Mycopathologia. 2008 Jan;165(1):1-3 [PMID: 18060516]
  6. Infect Immun. 2007 Jan;75(1):175-83 [PMID: 17074843]
  7. Eur J Immunol. 2000 Dec;30(12):3447-56 [PMID: 11093163]
  8. J Appl Microbiol. 2006 Aug;101(2):300-8 [PMID: 16882137]
  9. Genetics. 2008 Mar;178(3):1807-15 [PMID: 18245331]
  10. J Bacteriol. 2008 Apr;190(7):2306-13 [PMID: 18223084]
  11. Dev Comp Immunol. 2008;32(4):400-9 [PMID: 17850869]
  12. Dev Comp Immunol. 2003 Mar;27(3):207-15 [PMID: 12590972]
  13. PLoS Pathog. 2008 Jul 25;4(7):e1000111 [PMID: 18654628]
  14. Infect Immun. 1995 Sep;63(9):3665-73 [PMID: 7642305]
  15. Infect Immun. 1995 Oct;63(10):3896-903 [PMID: 7558297]
  16. Biotechniques. 1995 Nov;19(5):720-2, 724-5 [PMID: 8588903]
  17. J Bacteriol. 2000 Jul;182(13):3843-5 [PMID: 10851003]
  18. Infect Immun. 2006 Feb;74(2):1323-38 [PMID: 16428782]
  19. Appl Environ Microbiol. 2006 Feb;72(2):1700-1 [PMID: 16461732]
  20. Trends Microbiol. 2006 Mar;14(3):101-4 [PMID: 16473012]
  21. Infect Immun. 1998 Jan;66(1):232-8 [PMID: 9423863]
  22. Microbes Infect. 2007 Aug;9(10):1216-25 [PMID: 17720601]
  23. N Engl J Med. 1988 Sep 29;319(13):823-8 [PMID: 3137471]
  24. Antimicrob Agents Chemother. 2009 May;53(5):2205-8 [PMID: 19223640]
  25. Int J Med Microbiol. 2006 Aug;296(4-5):277-86 [PMID: 16527541]
  26. Microbes Infect. 2007 May;9(6):729-34 [PMID: 17400503]
  27. Mol Microbiol. 2006 Oct;62(2):339-55 [PMID: 16978259]
  28. EMBO J. 1995 Apr 3;14(7):1314-21 [PMID: 7729410]
  29. Nature. 2008 Oct 23;455(7216):1114-8 [PMID: 18806773]
  30. Lett Appl Microbiol. 2007 Feb;44(2):218-23 [PMID: 17257264]
  31. Infect Immun. 2008 Mar;76(3):1267-75 [PMID: 18195031]
  32. Int J Med Microbiol. 2007 Nov;297(7-8):541-57 [PMID: 17482873]
  33. PLoS One. 2009;4(1):e4224 [PMID: 19156203]
  34. Cell Microbiol. 2003 Dec;5(12):901-11 [PMID: 14641175]
  35. Nat Rev Microbiol. 2006 Jun;4(6):423-34 [PMID: 16710323]
  36. N Engl J Med. 1985 Feb 14;312(7):404-7 [PMID: 3918263]
  37. J Mol Biol. 1983 Jun 5;166(4):557-80 [PMID: 6345791]
  38. J Immunol. 2008 Aug 15;181(4):2705-12 [PMID: 18684961]
  39. Appl Environ Microbiol. 2008 Jun;74(12):3823-30 [PMID: 18424542]
  40. Infect Immun. 2007 Apr;75(4):1861-9 [PMID: 17261598]
  41. PLoS Biol. 2008 Dec 9;6(12):2764-73 [PMID: 19071960]
  42. Dev Comp Immunol. 2008;32(5):585-95 [PMID: 17981328]
  43. PLoS Pathog. 2007 Oct 26;3(10):1446-58 [PMID: 17967059]
  44. Cell Microbiol. 2003 Dec;5(12):875-85 [PMID: 14641173]
  45. Dev Comp Immunol. 1987 Winter;11(1):47-55 [PMID: 3109970]
  46. J Infect Dis. 2009 Feb 15;199(4):532-6 [PMID: 19125671]
  47. Microbes Infect. 2006 Jul;8(8):2105-12 [PMID: 16782387]
  48. Appl Environ Microbiol. 2008 Mar;74(6):1892-901 [PMID: 18223114]
  49. FEMS Immunol Med Microbiol. 2002 Oct 11;34(2):153-7 [PMID: 12381467]
  50. Science. 2005 Aug 19;309(5738):1248-51 [PMID: 16020693]
  51. Infect Immun. 2003 May;71(5):2404-13 [PMID: 12704110]
  52. Infect Immun. 2005 Jul;73(7):3842-50 [PMID: 15972469]
  53. Dev Comp Immunol. 2006;30(12):1108-18 [PMID: 16682078]
  54. Can J Microbiol. 2005 Feb;51(2):185-9 [PMID: 16091778]

MeSH Term

Animals
Disease Models, Animal
Gene Expression Profiling
Hemolymph
Host-Pathogen Interactions
Immunity, Innate
Larva
Lepidoptera
Listeria monocytogenes
Sepsis
Survival Analysis
Virulence

Word Cloud

Created with Highcharts 10.0.0modelListeriainfectionGalleriaimmunestrainsmonocytogeneslarvaeinnateinsectsusedmellonellacanvirulencespplisterialsepticgenesstrongantimicrobialhemolymphactivityLPSLsystemEssentialaspectsresponsemicrobialconservedmammalsgeneratedinterestusingorganismsstudyhost-microbeinteractionsgreaterwaxmothreared37degreesChostexaminingpotentialreportexcellentsurrogatecapableclearlydistinguishingpathogenicnonpathogenicevenvirulentattenuatedVirulencerequiredhithertoimplicatedmouselinkedactivitieshemocytesinfectedFollowingexpressiondefenselysozymegaliomycingallerimycininsectmetalloproteinaseinhibitorIMPIsequentiallyinducedPreinductiontreatmentlipopolysaccharidesignificantlyimprovedsurvivalsubsequentchallengeantilisterialdetectedpretreatedconcludeseveritymodulatedprimarilyresponsessuggestuserelativelysimplenonmammalianassessisolatedwidevarietysettingsclinicenvironmentstudyingpathogenesis

Similar Articles

Cited By