Legionella pneumophila pathogenesis in the Galleria mellonella infection model

Infection and Immunity

Volumn 80, Issue 8, 2012, Pages 2780-2790

  Harding, Clare R ^a   Schroeder, Gunnar N ^a   Reynolds, Stuart ^b   Kosta, Artemis ^a   Collins, James W ^a   Mousnier, Aurélie ^a   Frankel, Gad ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b University of Bath   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MONOPHENOL MONOOXYGENASE; POLYPEPTIDE ANTIBIOTIC AGENT; PROTEIN SIDC; THYMIDINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BLOOD CELL; CELL ULTRASTRUCTURE; CELL VACUOLE; CONTROLLED STUDY; EXPERIMENTAL MODEL; GALLERIA MELLONELLA; IMMUNE RESPONSE; IMMUNOFLUORESCENCE MICROSCOPY; INNATE IMMUNITY; LARVA; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; MOTH; NODULATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY; TYPE IV SECRETION SYSTEM; UPREGULATION; WILD TYPE;

ANIMALS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HEMOCYTES; IMMUNITY, INNATE; INSECT PROTEINS; KINETICS; LARVA; LEGIONELLA PNEUMOPHILA; MOTHS; RNA, MESSENGER; VIRULENCE;

EID: 84864811129     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00510-12     Document Type: Article

References (54)

1. Abu Kwaik Y. 1996. The phagosome containing Legionella pneumophila within the protozoan Hartmannella vermiformis is surrounded by the rough endoplasmic reticulum. Appl. Environ. Microbiol. 62: 2022-2028.
2. Alli OA, Zink S, von Lackum NK, Abu-Kwaik Y. 2003. Comparative assessment of virulence traits in Legionella spp. Microbiology 149: 631-641.
3. Baskerville A, Fitzgeorge RB, Broster M, Hambleton P, Dennis PJ. 1981. Experimental transmission of Legionnaires' disease by exposure to aerosols of Legionella pneumophila. Lancet ii: 1389-1390.
4. Berger KH, Isberg RR. 1993. Two distinct defects in intracellular growth complemented by a single genetic locus in Legionella pneumophila. Mol. Microbiol. 7: 7-19.
5. Brassinga AK, et al. 2010. Caenorhabditis is a metazoan host for Legionella. Cell. Microbiol. 12: 343-361.
6. Brieland J, et al. 1994. Replicative Legionella pneumophila lung infection in intratracheally inoculated A/J. mice.Amurine model of human Legionnaires' disease. Am. J. Pathol. 145: 1537-1546.
7. Cazalet C, et al. 2004. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat. Genet. 36: 1165-1173.
8. Cerenius L, Soderhall K. 2004. The prophenoloxidase-activating system in invertebrates. Immunol. Rev. 198: 116-126.
9. Champion OL, et al. 2009. Galleria mellonella as an alternative infection model for Yersinia pseudotuberculosis. Microbiology 155: 1516-1522.
10. Champion OL, et al. 2010. Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. J. Infect. Dis. 201: 776-782.
11. Cianciotto NP. 2009. Many substrates and functions of type II secretion: lessons learned from Legionella pneumophila. Future Microbiol. 4: 797-805.
12. De Buck E, et al. 2004. A putative twin-arginine translocation pathway in Legionella pneumophila. Biochem. Biophys. Res. Commun. 317: 654-661.
13. Dolezal P, et al. 2012. Legionella pneumophila secretes a mitochondrial carrier protein during infection. PLoS Pathog. 8: e1002459. doi: 10.1371/ journal.ppat.1002459.
14. Edelstein PH. 1986. Control of Legionella in hospitals. J. Hosp. Infect. 8: 109-115.
15. Eleftherianos I, Millichap PJ, ffrench-Constant RH, Reynolds SE. 2006. RNAi suppression of recognition protein mediated immune responses in the tobacco hornworm Manduca sexta causes increased susceptibility to the insect pathogen Photorhabdus. Dev. Comp. Immunol. 30: 1099-1107.
16. Fraser DW, et al. 1977. Legionnaires' disease: description of an epidemic of pneumonia. N. Engl. J. Med. 297: 1189-1197.
17. Fuchs BB, O'Brien E, Khoury JB, Mylonakis E. 2010. Methods for using Galleria mellonella as a model host to study fungal pathogenesis. Virulence 1: 475-482. 17a
18. Ge J, Shao F. 2011. Manipulation of host vesicular trafficking and innate immune defence by Legionella Dot/Icm effectors. Cell. Microbiol. 13: 1870-1880.
19. Girard F, et al. 2005. Host immune status influences the development of attaching and effacing lesions in weaned pigs. Infect. Immun. 73: 5514-5523.
20. Hammer BK, Swanson MS. 1999. Co-ordination of legionella pneumophila virulence with entry into stationary phase by ppGpp. Mol. Microbiol. 33: 721-731.
21. Hilbi H, Weber SS, Ragaz C, Nyfeler Y, Urwyler S. 2007. Environmental predators as models for bacterial pathogenesis. Environ. Microbiol. 9: 563-575.
22. Horwitz MA. 1983. The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J. Exp. Med. 158: 2108-2126.
23. Jander G, Rahme LG, Ausubel FM. 2000. Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182: 3843-3845.
24. Joyce SA, Gahan CG. 2010. Molecular pathogenesis of Listeria monocytogenes in the alternative model host Galleria mellonella. Microbiology 156: 3456-3468.
25. Kavanagh K, Reeves EP. 2004. Exploiting the potential of insects for in vivo pathogenicity testing of microbial pathogens. FEMS Microbiol. Rev. 28: 101-112.
26. Khoa DB, Trang LT, Takeda M. 2012. Expression analyses of caspase-1 and related activities in the midgut of Galleria mellonella during metamorphosis. Insect Mol. Biol. 21: 247-256.
27. Kosta A, Luciani MF, Geerts WJ, Golstein P. 2008. Marked mitochondrial alterations upon starvation without cell death, caspases or Bcl-2 family members. Biochim. Biophys. Acta 1783: 2013-2019.
28. Kubori T, Shinzawa N, Kanuka H, Nagai H. 2010. Legionella metaeffector exploits host proteasome to temporally regulate cognate effector. PLoS Pathog. 6: e1001216. doi: 10.1371/journal.ppat.1001216.
29. Lavine MD, Strand MR. 2002. Insect hemocytes and their role in immunity. Insect Biochem. Mol. Biol. 32: 1295-1309.
30. Lemaitre B, Hoffmann J. 2007. The host defense of Drosophila melanogaster. Annu. Rev. Immunol. 25: 697-743.
31. Marmaras VJ, Lampropoulou M. 2009. Regulators and signaling in insect haemocyte immunity. Cell Signal. 21: 186-195.
32. Meister M, Lemaitre B, Hoffmann JA. 1997. Antimicrobial peptide defense in Drosophila. Bioessays 19: 1019-1026.
33. Molmeret M, Horn M, Wagner M, Santic M, Abu Kwaik Y. 2005. Amoebae as training grounds for intracellular bacterial pathogens. Appl. Environ. Microbiol. 71: 20-28.
34. Mowlds P, Barron A, Kavanagh K. 2008. Physical stress primes the immune response of Galleria mellonella larvae to infection by Candida albicans. Microbes Infect. 10: 628-634.
35. Mukherjee K, et al. 2010. Galleria mellonella as a model system for studying Listeria pathogenesis. Appl. Environ. Microbiol. 76: 310-317.
36. Nagai H, Kubori T. 2011. Type IVB secretion systems of Legionella and other Gram-negative bacteria. Front. Microbiol. 2: 136.
37. Olsen RJ, Watkins ME, Cantu CC, Beres SB, Musser JM. 2011. Virulence of serotype M3 Group A streptococcus strains in wax worms (Galleria mellonella larvae). Virulence 2: 111-119.
38. Renwick J, Daly P, Reeves EP, Kavanagh K. 2006. Susceptibility of larvae of Galleria mellonella to infection by Aspergillus fumigatus is dependent upon stage of conidial germination. Mycopathologia 161: 377-384.
39. Rowbotham TJ. 1980. Preliminary report on the pathogenicity of Legionella pneumophila for freshwater and soil amoebae. J. Clin. Pathol. 33: 1179-1183.
40. Sadosky AB, Wiater LA, Shuman HA. 1993. Identification of Legionella pneumophila genes required for growth within and killing of human macrophages. Infect. Immun. 61: 5361-5373.
41. Samrakandi MM, Cirillo SL, Ridenour DA, Bermudez LE, Cirillo JD. 2002. Genetic and phenotypic differences between Legionella pneumophila strains. J. Clin. Microbiol. 40: 1352-1362.
42. Sansom FM, et al. 2007. A bacterial ecto-triphosphate diphosphohydrolase similar to human CD39 is essential for intracellular multiplication of Legionella pneumophila. Cell. Microbiol. 9: 1922-1935.
43. Santic M, Asare R, Doric M, Abu Kwaik Y. 2007. Host-dependent trigger of caspases and apoptosis by Legionella pneumophila. Infect. Immun. 75: 2903-2913.
44. Schroeder GN, et al. 2010. The genome of Legionella pneumophila strain 130b contains a unique combination of type IV secretion systems and encodes novel Dot/Icm secretion system effector proteins. J. Bacteriol. 192: 6001-6016.
45. Scully LR, Bidochka MJ. 2006. Developing insect models for the study of current and emerging human pathogens. FEMS Microbiol. Lett. 263: 1-9.
46. Segal G, Purcell M, Shuman HA. 1998. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl. Acad. Sci. U. S. A. 95: 1669-1674.
47. Segal G, Shuman HA. 1998. Intracellular multiplication and human macrophage killing by Legionella pneumophila are inhibited by conjugal components of IncQ plasmid RSF1010. Mol. Microbiol. 30: 197-208.
48. Solomon JM, Rupper A, Cardelli JA, Isberg RR. 2000. Intracellular growth of Legionella pneumophila in Dictyostelium discoideum, a system for genetic analysis of host-pathogen interactions. Infect. Immun. 68: 2939-2947.
49. Swanson MS, Isberg RR. 1995. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63: 3609-3620.
50. Terenius O, et al. 2011. RNA interference in Lepidoptera: an overview of successful and unsuccessful studies and implications for experimental design. J. Insect. Physiol. 57: 231-245.
51. Vogel H, Altincicek B, Glockner G, Vilcinskas A. 2011. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 12: 308.
52. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H. 2006. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog. 2: e46. doi: 10.1371/journal.ppat. 0020046.
53. Wright EK, et al. 2003. Naip5 affects host susceptibility to the intracellular pathogen Legionella pneumophila. Curr. Biol. 13: 27-36.
54. Zhu W, et al. 2011. Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6: e17638. doi: 10.1371/journal.pone.0017638.