Embryonated eggs as an alternative infection model to investigate Aspergillus fumigatus virulence

Infection and Immunity

Volumn 78, Issue 7, 2010, Pages 2995-3006

  Jacobsen, Ilse D ^a   Große, Katharina ^a   Slesiona, Silvia ^a   Hube, Bernhard ^a   Berndt, Angela ^b   Brock, Matthias ^a  

^a HANS KNÖLL INSTITUTE   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; BACTERIAL VIRULENCE; CELL CULTURE; CHICKEN; DISEASE MODEL; EMBRYO; EMBRYO DEATH; EMBRYO MEMBRANE; NONHUMAN; PATHOGENESIS; PATHOGENICITY; PRIORITY JOURNAL; UPREGULATION; ZYGOTE;

ANIMALS; ASPERGILLOSIS; ASPERGILLUS FUMIGATUS; CHEMOKINES; CHICK EMBRYO; CHICKENS; CYTOKINES; DISEASE MODELS, ANIMAL; LIVER; MICE; MICROBIOLOGICAL TECHNIQUES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, FUNGAL;

EID: 77953927869     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00268-10     Document Type: Article

References (59)

1. Abdul-Careem, M. F., D. B. Hunter, M. D. Lambourne, J. Barta, and S. Sharif. 2007. Ontogeny of cytokine gene expression in the chicken spleen. Poult. Sci. 86:1351-1355.
2. Adam, R., S. Mussa, D. Lindemann, T. A. Oelschlaeger, M. Deadman, D. J. Ferguson, R. Moxon, and H. Schroten. 2002. The avian chorioallantoic membrane in ovo - a useful model for bacterial invasion assays. Int. J. Med. Microbiol. 292:267-275.
3. Armstrong-James, D. P., S. A. Turnbull, I. Teo, J. Stark, N. J. Rogers, T. R. Rogers, E. Bignell, and K. Haynes. 2009. Impaired interferon-gamma responses, increased interleukin-17 expression, and a tumor necrosis factoralpha transcriptional program in invasive aspergillosis. J. Infect. Dis. 200: 1341-1351.
4. Balloy, V., M. Huerre, J. P. Latge, and M. Chignard. 2005. Differences in patterns of infection and inflammation for corticosteroid treatment and chemotherapy in experimental invasive pulmonary aspergillosis. Infect. Immun. 73:494-503.
5. Berndt, A., A. Wilhelm, C. Jugert, J. Pieper, K. Sachse, and U. Methner. 2007. Chicken cecum immune response to Salmonella enterica serovars of different levels of invasiveness. Infect. Immun. 75:5993-6007.
6. Cacciuttolo, E., G. Rossi, S. Nardoni, R. Legrottaglie, and P. Mani. 2009. Anatomopathological aspects of avian aspergillosis. Vet. Res. Commun. 33:521-527.
7. Carvajal, B. G., U. Methner, J. Pieper, and A. Berndt. 2008. Effects of Salmonella enterica serovar Enteritidis on cellular recruitment and cytokine gene expression in caecum of vaccinated chickens. Vaccine 26:5423-5433.
8. Centeno-Lima, S., H. Silveira, C. Casimiro, P. Aguiar, and V. E. do Rosario. 2002. Kinetics of cytokine expression in mice with invasive aspergillosis: lethal infection and protection. FEMS Immunol. Med. Microbiol. 32:167-173.
9. Chiang, L. Y., D. C. Sheppard, F. N. Gravelat, T. F. Patterson, and S. G. Filler. 2008. Aspergillus fumigatus stimulates leukocyte adhesion molecules and cytokine production by endothelial cells in vitro and during invasive pulmonary disease. Infect. Immun. 76:3429-3438.
10. Chute, H. L. 1975. Characteristics of immunity in fungal infections. Am. J. Vet. Res. 36:601-602.
11. Clemons, K. V., and D. A. Stevens. 2005. The contribution of animal models of aspergillosis to understanding pathogenesis, therapy and virulence. Med. Mycol. 43(Suppl. 1):S101-S110.
12. Cooper, M. D., C. L. Chen, R. P. Bucy, and C. B. Thompson. 1991. Avian T cell ontogeny. Adv. Immunol. 50:87-117.
13. da Silva Ferreira, M. E., M. R. Kress, M. Savoldi, M. H. Goldman, A. Härtl, T. Heinekamp, A. A. Brakhage, and G. H. Goldman. 2006. The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5:207-211.
14. Gallien, S., S. Fournier, R. Porcher, J. Bottero, P. Ribaud, A. Sulahian, G. Socie, and J. M. Molina. 2008. Therapeutic outcome and prognostic factors of invasive aspergillosis in an infectious disease department: a review of 34 cases. Infection 36:533-538.
15. Gottfredsson, M., and H. Steingrimsdottir. 2006. Disseminated invasive aspergillosis in a patient with acute leukaemia. Acta Biomed, 77(Suppl. 2):10-13.
16. Gow, N. A., Y. Knox, C. A. Munro, and W. D. Thompson. 2003. Infection of chick chorioallantoic membrane (CAM) as a model for invasive hyphal growth and pathogenesis of Candida albicans. Med. Mycol. 41:331-338.
17. Härtl, A., H. G. Hillesheim, W. Kunkel, and E. J. Schrinner. 1995. The Candida infected hen's egg. An alternative test system for systemic anticandida activity. Arzneimittelforschung 45:926-928. (In German.)
18. Herren, C. D., A. Mitra, S. K. Palaniyandi, A. Coleman, S. Elankumaran, and S. Mukhopadhyay. 2006. The BarA-UvrY two-component system regulates virulence in avian pathogenic Escherichia coli O78:K80:H9. Infect. Immun. 74:4900-4909.
19. Hohl, T. M., and M. Feldmesser. 2007. Aspergillus fumigatus: principles of pathogenesis and host defense. Eukaryot. Cell 6:1953-1963.
20. Ibrahim-Granet, O., M. Dubourdeau, J. P. Latgé, P. Ave, M. Huerre, A. A. Brakhage, and M. Brock. 2008. Methylcitrate synthase from Aspergillus fumigatus is essential for manifestation of invasive aspergillosis. Cell. Microbiol. 10:134-148.
21. Jackson, J. C., L. A. Higgins, and X. Lin. 2009. Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One 4:e4224.
22. Khosravi, A. R., H. Shokri, T. Ziglari, A. R. Naeini, Z. Mousavi, and H. Hashemi. 2008. Outbreak of severe disseminated aspergillosis in a flock of ostrich (Struthio camelus). Mycoses 51:557-559.
23. King, V., A. Bavetsia, and N. Bumstead. 1993. Effect of host lineage on the virulence of Campylobacter jejuni/coli in the chick embryo model. FEMS Microbiol. Lett. 106:271-274.
24. Krappmann, S., C. Sasse, and G. H. Braus. 2006. Gene targeting in Aspergillus fumigatus by homologous recombination is facilitated in a nonhomologous end-joining-deficient genetic background. Eukaryot. Cell 5:212-215.
25. Kupfahl, C., T. Heinekamp, G. Geginat, T. Ruppert, A. Hartl, H. Hof, and A. A. Brakhage. 2006. Deletion of the gliP gene of Aspergillus fumigatus results in loss of gliotoxin production but has no effect on virulence of the fungus in a low-dose mouse infection model. Mol. Microbiol. 62:292-302.
26. Laurent, F., R. Mancassola, S. Lacroix, R. Menezes, and M. Naciri. 2001. Analysis of chicken mucosal immune response to Eimeria tenella and Eimeria maxima infection by quantitative reverse transcription-PCR. Infect. Immun. 69:2527-2534.
27. Lehmann, P. F. 1985. Immunology of fungal infections in animals. Vet. Immunol. Immunopathol. 10:33-69.
28. Lionakis, M. S., and D. P. Kontoyiannis. 2005. Fruit flies as a minihost model for studying drug activity and virulence in Aspergillus. Med. Mycol. 43(Suppl. 1):S111-S114.
29. Lionakis, M. S., R. E. Lewis, G. S. May, N. P. Wiederhold, N. D. Albert, G. Halder, and D. P. Kontoyiannis. 2005. Toll-deficient Drosophila flies as a fast, high-throughput model for the study of antifungal drug efficacy against invasive aspergillosis and Aspergillus virulence. J. Infect. Dis. 191:1188-1195.
30. Maerker, C., M. Rohde, A. A. Brakhage, and M. Brock. 2005. Methylcitrate synthase from Aspergillus fumigatus. Propionyl-CoA affects polyketide synthesis, growth and morphology of conidia. FEBS J. 272:3615-3630.
31. Marr, K. A., T. Patterson, and D. Denning. 2002. Aspergillosis. Pathogenesis, clinical manifestations, and therapy. Infect. Dis. Clin. North Am. 16:875-894, vi.
32. Martin, M. P., K. P. Bouck, J. Helm, M. J. Dykstra, D. P. Wages, and H. J. Barnes. 2007. Disseminated Aspergillus flavus infection in broiler breeder pullets. Avian Dis. 51:626-631.
33. Martinez-Quesada, J., A. Nieto-Cadenazzi, and J. M. Torres-Rodriguez. 1993. Humoral immunoresponse of pigeons to Aspergillus fumigatus antigens. Mycopathologia 124:131-137.
34. Meade, K. G., R. Higgs, A. T. Lloyd, S. Giles, and C. O'Farrelly. 2009. Differential antimicrobial peptide gene expression patterns during early chicken embryological development. Dev. Comp. Immunol. 33:516-524.
35. Mehrad, B., M. Wiekowski, B. E. Morrison, S. C. Chen, E. C. Coronel, D. J. Manfra, and S. A. Lira. 2002. Transient lung-specific expression of the chemokine KC improves outcome in invasive aspergillosis. Am. J. Respir. Crit. Care Med. 166:1263-1268.
36. Mircescu, M. M., L. Lipuma, N. van Rooijen, E. G. Pamer, and T. M. Hohl. 2009. Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection. J. Infect. Dis. 200:647-656.
37. Mylonakis, E. 2008. Galleria mellonella and the study of fungal pathogenesis: making the case for another genetically tractable model host. Mycopathologia 165:1-3.
38. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
39. Philippe, B., O. Ibrahim-Granet, M. C. Prevost, M. A. Gougerot-Pocidalo, M. Sanchez Perez, A. Van der Meeren, and J. P. Latge. 2003. Killing of Aspergillus fumigatus by alveolar macrophages is mediated by reactive oxidant intermediates. Infect. Immun. 71:3034-3042.
40. Pieper, J., U. Methner, and A. Berndt. 2008. Heterogeneity of avian gammadelta T cells. Vet. Immunol. Immunopathol. 124:241-252.
41. Pollock, C. 2003. Fungal diseases of columbiformes and anseriformes. Vet. Clin. North Am. Exot. Anim. Pract. 6:351-361.
42. Reeves, E. P., C. G. Messina, S. Doyle, and K. Kavanagh. 2004. Correlation between gliotoxin production and virulence of Aspergillus fumigatus in Galleria mellonella. Mycopathologia 158:73-79.
43. Renwick, J., P. Daly, E. P. Reeves, and K. Kavanagh. 2006. Susceptibility of larvae of Galleria mellonella to infection by Aspergillus fumigatus is dependent upon stage of conidial germination. Mycopathologia 161:377-384.
44. Ribatti, D., B. Nico, A. Vacca, L. Roncali, P. H. Burri, and V. Djonov. 2001. Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat. Rec. 264:317-324.
45. Richard, J. L., R. C. Cutlip, J. R. Thurston, and J. Songer. 1981. Response of turkey poults to aerosolized spores of Aspergillus fumigatus and aflatoxigenic and nonaflatoxigenic strains of Aspergillus flavus. Avian Dis. 25:53-67.
46. Richard, J. L., J. R. Thurston, R. C. Cutlip, and A. C. Pier. 1982. Vaccination studies of aspergillosis in turkeys: subcutaneous inoculation with several vaccine preparations followed by aerosol challenge exposure. Am. J. Vet. Res. 43:488-492.
47. Schmidt, A. 2002. Animal models of aspergillosis-also useful for vaccination strategies? Mycoses 45:38-40.
48. Schöbel, F., O. Ibrahim-Granet, P. Ave, J. P. Latge, A. A. Brakhage, and M. Brock. 2007. Aspergillus fumigatus does not require fatty acid metabolism via isocitrate lyase for development of invasive aspergillosis. Infect. Immun. 75:1237-1244.
49. Schöbel, F., I. D. Jacobsen, and M. Brock. 2 April 2010, posting date. Evaluation of lysine biosynthesis as antifungal drug target: biochemical characterization of Aspergillus fumigatus homocitrate synthase and virulence studies. Eukaryot. Cell. doi:10.1128/EC.00020-10.
50. Shirkhoda, A., G. Lopez-Berestein, J. M. Holbert, and M. A. Luna. 1986. Hepatosplenic fungal infection: CT and pathologic evaluation after treatment with liposomal amphotericin B. Radiology 159:349-353.
51. Spikes, S., R. Xu, C. K. Nguyen, G. Chamilos, D. P. Kontoyiannis, R. H. Jacobson, D. E. Ejzykowicz, L. Y. Chiang, S. G. Filler, and G. S. May. 2008. Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence. J. Infect. Dis. 197:479-486.
52. Stedham, M. A., T. J. Bucci, and R. R. Maronpot. 1968. Sexual and asexual phases of Aspergillus nidulans in an egret. Mycopathol Mycol. Appl. 36:289-292.
53. Stephens-Romero, S. D., A. J. Mednick, and M. Feldmesser. 2005. The pathogenesis of fatal outcome in murine pulmonary aspergillosis depends on the neutrophil depletion strategy. Infect. Immun. 73:114-125.
54. Tell, L. A. 2005. Aspergillosis in mammals and birds: impact on veterinary medicine. Med. Mycol. 43(Suppl. 1):S71-S73.
55. Townsend, M. K., N. J. Carr, J. G. Iyer, S. M. Horne, P. S. Gibbs, and B. M. Pruss. 2008. Pleiotropic phenotypes of a Yersinia enterocolitica flhD mutant include reduced lethality in a chicken embryo model. BMC Microbiol. 8:12.
56. Vargas, A., M. Zeisser-Labouebe, N. Lange, R. Gurny, and F. Delie. 2007. The chick embryo and its chorioallantoic membrane (CAM) for the in vivo evaluation of drug delivery systems. Adv. Drug Deliv. Rev. 59:1162-1176.
57. Vonberg, R. P., and P. Gastmeier. 2006. Nosocomial aspergillosis in outbreak settings. J. Hosp. Infect. 63:246-254.
58. Withanage, G. S., P. Kaiser, P. Wigley, C. Powers, P. Mastroeni, H. Brooks, P. Barrow, A. Smith, D. Maskell, and I. McConnell. 2004. Rapid expression of chemokines and proinflammatory cytokines in newly hatched chickens infected with Salmonella enterica serovar Typhimurium. Infect. Immun. 72: 2152-2159.
59. Yeom, S. K., H. J. Kim, J. H. Byun, A. Y. Kim, M. G. Lee, and H. K. Ha. 21 September 2009, posting date. Abdominal aspergillosis: CT findings. Eur. J. Radiol. 32 doi:10.1016/j.ejrad.2009.08.016.