Galleria mellonella as an alternative model of Coxiella burnetii infection

Microbiology (United Kingdom)

Volumn 160, Issue PART 6, 2014, Pages 1175-1181

  Norville, I H ^a   Hartley, M G ^a   Martinez, E ^b   Cantet, F ^b   Bonazzi, M ^b   Atkins, T P ^a,c  

^a DEFENCE SCIENCE AND TECHNOLOGY LABORATORY   (United Kingdom)

^b CNRS   (France)

^c UNIVERSITY OF EXETER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOXYCYCLINE;

ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BLOOD CELL; CELL INTERACTION; DRUG EFFICACY; GALLERIA MELLONELLA; GENETIC MANIPULATION; INFECTION SENSITIVITY; LARVA; NONHUMAN; PRIORITY JOURNAL; Q FEVER; TYPE IV SECRETION SYSTEM;

EID: 84901697934     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.077230-0     Document Type: Article

References (50)

1. Anderson, A., Bijlmer, H., Fournier, P.-E., Graves, S., Hartzell, J., Kersh, G. J., Limonard, G., Marrie, T. J., Massung, R. F. & other authors (2013). Diagnosis and Management of Q Fever-United States, 2013: Recommendations from CDC and the Q Fever Working Group. Atlanta, GA: Centers for Disease Control and Prevention. http://www.cdc.gov/mmwr/preview/mmwrhtml/rr6203a1.htm
2. Andoh, M., Naganawa, T., Hotta, A., Yamaguchi, T., Fukushi, H., Masegi, T. & Hirai, K. (2003). SCID mouse model for lethal Q fever. Infect Immun 71, 4717-4723.
3. Andoh, M., Zhang, G., Russell-Lodrigue, K. E., Shive, H. R., Weeks, B. R. & Samuel, J. E. (2007). T cells are essential for bacterial clearance, and gamma interferon, tumor necrosis factor alpha, and B cells are crucial for disease development in Coxiella burnetii infection in mice. Infect Immun 75, 3245-3255.
4. Aperis, G., Fuchs, B. B., Anderson, C. A., Warner, J. E., Calderwood, S. B. & Mylonakis, E. (2007). Galleria mellonella as a model host to study infection by the Francisella tularensis live vaccine strain. Microbes Infect 9, 729-734.
5. Bailey, M. S., Trinick, T. R., Dunbar, J. A., Hatch, R., Osborne, J. C., Brooks, T. J. & Green, A. D. (2011). Undifferentiated febrile illnesses amongst British troops in Helmand, Afghanistan. J R Army Med Corps 157, 150-155.
6. Beare, P. A., Howe, D., Cockrell, D. C., Omsland, A., Hansen, B. & Heinzen, R. A. (2009). Characterization of a Coxiella burnetii ftsZ mutant generated by Himar1 transposon mutagenesis. J Bacteriol 191, 1369-1381.
7. Beare, P. A., Sandoz, K. M., Omsland, A., Rockey, D. D. & Heinzen, R. A. (2011a). Advances in genetic manipulation of obligate intracellular bacterial pathogens. Front Microbiol 2, 97.
8. Beare, P. A., Gilk, S. D., Larson, C. L., Hill, J., Stead, C. M., Omsland, A., Cockrell, D. C., Howe, D., Voth, D. E. & Heinzen, R. A. (2011b). Dot/Icm type IVB secretion system requirements for Coxiella burnetii growth in human macrophages. MBio 2, e00175-11.
9. Beare, P. A., Larson, C. L., Gilk, S. D. & Heinzen, R. A. (2012). Two systems for targeted gene deletion in Coxiella burnetii. Appl Environ Microbiol 78, 4580-4589.
10. Bergin, D., Reeves, E. P., Renwick, J., Wientjes, F. B. & Kavanagh, K. (2005). Superoxide production in Galleria mellonella hemocytes: identification of proteins homologous to the NADPH oxidase complex of human neutrophils. Infect Immun 73, 4161-4170.
11. Champion, O. L., Karlyshev, A. V., Senior, N. J., Woodward, M., La Ragione, R., Howard, S. L., Wren, B. W. & Titball, R. W. (2010). Insect infection model for Campylobacter jejuni reveals that O-methyl phosphoramidate has insecticidal activity. J Infect Dis 201, 776-782.
12. Derrick, E. H. (1983). Q fever, a new fever entity: clinical features, diagnosis and laboratory investigation. Rev Infect Dis 5, 790-800.
13. Desbois, A. P. & Coote, P. J. (2011). Wax moth larva (Galleria mellonella): an in vivo model for assessing the efficacy of antistaphylococcal agents. J Antimicrob Chemother 66, 1785-1790.
14. Dijkstra, F., van der Hoek, W., Wijers, N., Schimmer, B., Rietveld, A., Wijkmans, C. J., Vellema, P. & Schneeberger, P. M. (2012). The 2007-2010 Q fever epidemic in The Netherlands: characteristics of notified acute Q fever patients and the association with dairy goat farming. FEMS Immunol Med Microbiol 64, 3-12.
15. Faix, D. J., Harrison, D. J., Riddle, M. S., Vaughn, A. F., Yingst, S. L., Earhart, K. & Thibault, G. (2008). Outbreak of Q fever among US military in western Iraq, June-July 2005. Clin Infect Dis 46, e65-e68.
16. Gan, Y. H., Chua, K. L., Chua, H. H., Liu, B., Hii, C. S., Chong, H. L. & Tan, P. (2002). Characterization of Burkholderia pseudomallei infection and identification of novel virulence factors using a Caenorhabditis elegans host system. Mol Microbiol 44, 1185-1197.
17. 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.
18. Hackstadt, T., Peacock, M. G., Hitchcock, P. J. & Cole, R. L. (1985). Lipopolysaccharide variation in Coxiella burnetti: intrastrain heterogeneity in structure and antigenicity. Infect Immun 48, 359-365.
19. Harding, C. R., Schroeder, G. N., Reynolds, S., Kosta, A., Collins, J. W., Mousnier, A. & Frankel, G. (2012). Legionella pneumophila pathogenesis in the Galleria mellonella infection model. Infect Immun 80, 2780-2790.
20. Hoover, T. A., Culp, D. W., Vodkin, M. H., Williams, J. C. & Thompson, H. A. (2002). Chromosomal DNA deletions explain phenotypic characteristics of two antigenic variants, phase II and RSA 514 (crazy), of the Coxiella burnetii Nine Mile strain. Infect Immun 70, 6726-6733.
21. Huebner, R. J., Hottle, G. A. & Robinson, E. B. (1948). Action of streptomycin in experimental infection with Q fever. Public Health Rep 63, 357-362.
22. Islam, A., Lockhart, M., Stenos, J. & Graves, S. (2013). The attenuated Nine Mile phase II clone 4/RSA439 strain of Coxiella burnetii is highly virulent for severe combined immunodeficient (SCID) mice. Am J Trop Med Hyg 89, 800-803.
23. Joshua, G. W., Karlyshev, A. V., Smith, M. P., Isherwood, K. E., Titball, R. W. & Wren, B. W. (2003). A Caenorhabditis elegans model of Yersinia infection: biofilm formation on a biotic surface. Microbiology 149, 3221-3229.
24. Komura, T., Yasui, C., Miyamoto, H. & Nishikawa, Y. (2010). Caenorhabditis elegans as an alternative model host for Legionella pneumophila, and protective effects of Bifidobacterium infantis. Appl Environ Microbiol 76, 4105-4108.
25. Laws, T. R., Smith, S. A., Smith, M. P., Harding, S. V., Atkins, T. P. & Titball, R. W. (2005). The nematode Panagrellus redivivus is susceptible to killing by human pathogens at 37 uC. FEMS Microbiol Lett 250, 77-83.
26. Madariaga, M. G., Rezai, K., Trenholme, G. M. & Weinstein, R. A. (2003). Q fever: a biological weapon in your backyard. Lancet Infect Dis 3, 709-721.
27. Marmion, B. (2007). Q fever: the long journey to control by vaccination. Med J Aust 186, 164-166.
28. Martinez, E., Cantet, F., Fava, L., Norville, I. & Bonazzi, M. (2014). Identification of OmpA, a Coxiella burnetii protein involved in host cell invasion, by multi-phenotypic high-content screening. PLoS Pathog 10, e1004013.
29. Maurin, M. & Raoult, D. (1999). Q fever. ClinMicrobiol Rev 12, 518-553.
30. McQuiston, J. H. & Childs, J. E. (2002). Q fever in humans and animals in the United States. Vector Borne Zoonotic Dis 2, 179-191.
31. Moodie, C. E., Thompson, H. A., Meltzer, M. I. & Swerdlow, D. L. (2008). Prophylaxis after exposure to Coxiella burnetii. Emerg Infect Dis 14, 1558-1566.
32. Moos, A. & Hackstadt, T. (1987). Comparative virulence of intra-and interstrain lipopolysaccharide variants of Coxiella burnetii in the guinea pig model. Infect Immun 55, 1144-1150.
33. Newton, H. J., McDonough, J. A. & Roy, C. R. (2013). Effector protein translocation by the Coxiella burnetii Dot/Icm type IV secretion system requires endocytic maturation of the pathogen-occupied vacuole. PLoS ONE 8, e54566.
34. Ochoa-Repáraz, J., Sentissi, J., Trunkle, T., Riccardi, C. & Pascual, D. W. (2007). Attenuated Coxiella burnetii phase II causes a febrile response in gamma interferon knockout and Toll-like receptor 2 knockout mice and protects against reinfection. Infect Immun 75, 5845-5858.
35. Omsland, A., Cockrell, D. C., Howe, D., Fischer, E. R., Virtaneva, K., Sturdevant, D. E., Porcella, S. F. & Heinzen, R. A. (2009). Host cellfree growth of the Q fever bacterium Coxiella burnetii. Proc Natl Acad Sci U S A 106, 4430-4434.
36. Omsland, A., Beare, P. A., Hill, J., Cockrell, D. C., Howe, D., Hansen, B., Samuel, J. E. & Heinzen, R. A. (2011). Isolation from animal tissue and genetic transformation of Coxiella burnetii are facilitated by an improved axenic growth medium. Appl Environ Microbiol 77, 3720-3725.
37. Russell-Lodrigue, K. E., Zhang, G. Q., McMurray, D. N. & Samuel, J. E. (2006). Clinical and pathologic changes in a guinea pig aerosol challenge model of acute Q fever. Infect Immun 74, 6085-6091.
38. Schell, M. A., Lipscomb, L. & DeShazer, D. (2008). Comparative genomics and an insect model rapidly identify novel virulence genes of Burkholderia mallei. J Bacteriol 190, 2306-2313.
39. Scott, G. H., Williams, J. C. & Stephenson, E. H. (1987). Animal models in Q fever: pathological responses of inbred mice to phase I Coxiella burnetii. J Gen Microbiol 133, 691-700.
40. Seitz, V., Clermont, A., Wedde, M., Hummel, M., Vilcinskas, A., Schlatterer, K. & Podsiadlowski, L. (2003). Identification of immunorelevant genes from greater wax moth (Galleria mellonella) by a subtractive hybridization approach. Dev Comp Immunol 27, 207-215.
41. Shannon, J. G., Howe, D. & Heinzen, R. A. (2005). Virulent Coxiella burnetii does not activate human dendritic cells: role of lipopolysaccharide as a shielding molecule. Proc Natl Acad Sci U S A 102, 8722-8727.
42. Thomas, R. J., Hamblin, K. A., Armstrong, S. J., Müller, C. M., Bokori-Brown, M., Goldman, S., Atkins, H. S. & Titball, R. W. (2013). Galleria mellonella as a model system to test the pharmacokinetics and efficacy of antibiotics against Burkholderia pseudomallei. Int J Antimicrob Agents 41, 330-336.
43. Vishwanath, S. & Hackstadt, T. (1988). Lipopolysaccharide phase variation determines the complement-mediated serum susceptibility of Coxiella burnetii. Infect Immun 56, 40-44.
44. 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, 308.
45. Voth, D. E. & Heinzen, R. A. (2007). Lounging in a lysosome: the intracellular lifestyle of Coxiella burnetii. Cell Microbiol 9, 829-840.
46. Waag, D. M., Byrne, W. R., Estep, J., Gibbs, P., Pitt, M. L. M. & Banfield, C. M. (1999). Evaluation of cynomolgus (Macaca fascicularis) and rhesus (Macaca mulatta) monkeys as experimental models of acute Q fever after aerosol exposure to phase-I Coxiella burnetii. Lab Anim Sci 49, 634-638.
47. Wand, M. E., Müller, C. M., Titball, R. W. & Michell, S. L. (2011). Macrophage and Galleria mellonella infection models reflect the virulence of naturally occurring isolates of B. pseudomallei, B. thailandensis and B. oklahomensis. BMC Microbiol 11, 11.
48. Weber, M. M., Chen, C., Rowin, K., Mertens, K., Galvan, G., Zhi, H., Dealing, C. M., Roman, V. A., Banga, S. & other authors (2013). Identification of Coxiella burnetii type IV secretion substrates required for intracellular replication and Coxiella-containing vacuole formation. J Bacteriol 195, 3914-3924.
49. Whelan, J., Schimmer, B., Schneeberger, P., Meekelenkamp, J., Ijff, A., van der Hoek, W. & Robert-Du Ry van Beest Holle, M. (2011). Q fever among culling workers, the Netherlands, 2009-2010. Emerg Infect Dis 17, 1719-1723.
50. Williams, J. C., Peacock, M. G. & McCaul, T. F. (1981). Immunological and biological characterization of Coxiella burnetii, phases I and II, separated from host components. Infect Immun 32, 840-851.