Of mice, flies - and men? Comparing fungal infection models for large-scale screening efforts

DMM Disease Models and Mechanisms

Volumn 8, Issue 5, 2015, Pages 473-486

  Brunke, Sascha ^a,b   Quintin, Jessica ^c,i   Kasper, Lydia ^b   Jacobsen, Ilse D ^b,d   Richter, Martin E ^a   Hiller, Ekkehard ^e   Schwarzmüller, Tobias ^f   D'Enfert, Christophe ^g,h   Kuchler, Karl ^f   Rupp, Steffen ^e   Hube, Bernhard ^a,b,d   Ferrandon, Dominique ^c  

^a JENA UNIVERSITY HOSPITAL   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^e FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

^f MEDICAL UNIVERSITY OF VIENNA   (Austria)

^g INSTITUT PASTEUR   (France)

^h USC 2019   (France)

ⁱ RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Alternative infection models; Candida glabrata; Drosophila melanogaster; Fungal virulence factors; Mutant library; Signature tagged mutagenesis

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANDIDA GLABRATA; CONTROLLED STUDY; DELETION MUTANT; DISEASE MODEL; DROSOPHILA MELANOGASTER; FRUIT FLY MODEL; FUNGAL CELL WALL; FUNGAL VIRULENCE; FUNGUS GROWTH; FUNGUS MUTANT; GENE DELETION; HOST PATHOGEN INTERACTION; IN VITRO STUDY; MICROARRAY ANALYSIS; MOUSE; MUTAGENESIS; MYCOSIS; NONHUMAN; PATHOGEN LOAD; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN GLYCOSYLATION; SCREENING; SIGNAL TRANSDUCTION; SURVIVAL TIME; ANIMAL; ANTIBODY SPECIFICITY; GENE ONTOLOGY; GENETICS; HUMAN; MALE; MICROBIOLOGY; MUTATION; PATHOGENICITY; POLYMERASE CHAIN REACTION; STATISTICAL MODEL; VIRULENCE;

CANDIDA GLABRATA; DROSOPHILA MELANOGASTER; INVERTEBRATA; MAMMALIA; MURINAE; MUS;

ANIMALS; CANDIDA GLABRATA; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; GENE ONTOLOGY; HUMANS; LOGISTIC MODELS; MALE; MICE; MUTATION; MYCOSES; ORGAN SPECIFICITY; POLYMERASE CHAIN REACTION; VIRULENCE;

EID: 84928995109     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.019901     Document Type: Article

References (63)

1. Alonso-Monge, R., Navarro-Garcia, F., Molero, G., Diez-Orejas, R., Gustin, M., Pla, J., Sanchez, M. and Nombela, C. (1999). Role of the mitogen-activated protein kinase Hog1p in morphogenesis and virulence of Candida albicans. J. Bacteriol. 181, 3058-3068.
2. Arendrup, M. C. (2010). Epidemiology of invasive candidiasis. Curr. Opin. Crit. Care 16, 445-452.
3. Atanasova, R., Angoulvant, A., Tefit, M., Gay, F., Guitard, J., Mazier, D., Fairhead, C. and Hennequin, C. (2013). A mouse model for Candida glabrata hematogenous disseminated infection starting from the gut: evaluation of strains with different adhesion properties. PLoS ONE 8, e69664.
4. Bairwa, G., Rasheed, M., Taigwal, R., Sahoo, R. and Kaur, R. (2014). GPI (glycosylphosphatidylinositol)-linked aspartyl proteases regulate vacuole homoeostasis in Candida glabrata. Biochem. J. 458, 323-334.
5. Bates, S., Hughes, H. B., Munro, C. A., Thomas, W. P. H., MacCallum, D. M., Bertram, G., Atrih, A., Ferguson, M. A. J., Brown, A. J. P., Odds, F. C. et al. (2006). Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J. Biol. Chem. 281, 90-98.
6. Ben-Ami, R., Garcia-Effron, G., Lewis, R. E., Gamarra, S., Leventakos, K., Perlin, D. S. and Kontoyiannis, D. P. (2011). Fitness and virulence costs of Candida albicans FKS1 hot spot mutations associated with echinocandin resistance. J. Infect. Dis. 204, 626-635.
7. Borghi, E., Andreoni, S., Cirasola, D., Ricucci, V., Sciota, R. and Morace, G. (2014). Antifungal resistance does not necessarily affect Candida glabrata fitness. J. Chemother. 26, 32-36.
8. Boyle, E. I., Weng, S., Gollub, J., Jin, H., Botstein, D., Cherry, J. M. and Sherlock, G. (2004). GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics 20, 3710-3715.
9. Breger, J., Fuchs, B. B., Aperis, G., Moy, T. I., Ausubel, F. M. and Mylonakis, E. (2007). Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog. 3, e18.
10. Brieland, J., Essig, D., Jackson, C., Frank, D., Loebenberg, D., Menzel, F., Arnold, B., DiDomenico, B. and Hare, R. (2001). Comparison of pathogenesis and host immune responses to Candida glabrata and Candida albicans in systemically infected immunocompetent mice. Infect. Immun. 69, 5046-5055.
11. Briones-Martin-Del-Campo, M., Orta-Zavalza, E., Juarez-Cepeda, J., Gutierrez-Escobedo, G., Cañas-Villamar, I., Castaño, I. and De Las Peñas, A. (2014). The oxidative stress response of the opportunistic fungal pathogen Candida glabrata. Rev. Iberoam. Micol. 31, 67-71.
12. Brothers, K. M., Newman, Z. R. and Wheeler, R. T. (2011). Live imaging of disseminated candidiasis in zebrafish reveals role of phagocyte oxidase in limiting filamentous growth. Eukaryot. Cell 10, 932-944.
13. Brown, J. S., Aufauvre-Brown, A., Brown, J., Jennings, J. M., Arst, H., Jr and Holden, D.W. (2000). Signature-tagged and directed mutagenesis identify PABA synthetase as essential for Aspergillus fumigatus pathogenicity. Mol. Microbiol. 36, 1371-1380.
14. Casadevall, A. (2005). Fungal virulence, vertebrate endothermy, and dinosaur extinction: is there a connection? Fungal Genet. Biol. 42, 98-106.
15. Chamilos, G., Nobile, C. J., Bruno, V. M., Lewis, R. E., Mitchell, A. P. and Kontoyiannis, D. P. (2009). Candida albicans Cas5, a regulator of cell wall integrity, is required for virulence in murine and toll mutant fly models. J. Infect. Dis. 200, 152-157.
16. Chamilos, G., Bignell, E. M., Schrettl, M., Lewis, R. E., Leventakos, K., May, G. S., Haas, H. and Kontoyiannis, D. P. (2010). Exploring the concordance of Aspergillus fumigatus pathogenicity in mice and Toll-deficient flies. Med. Mycol. 48, 506-510.
17. Chao, C. C., Hsu, P. C., Jen, C. F., Chen, I. H., Wang, C. H., Chan, H. C., Tsai, P.W., Tung, K. C., Wang, C. H., Lan, C. Y. et al. (2010). Zebrafish as a model host for Candida albicans infection. Infect. Immun. 78, 2512-2521.
18. Chen, Y.-L., Konieczka, J. H., Springer, D. J., Bowen, S. E., Zhang, J., Silao, F. G. S., Bungay, A. A. C., Bigol, U. G., Nicolas, M. G., Abraham, S. N. et al. (2012). Convergent evolution of calcineurin pathway roles in thermotolerance and virulence in Candida glabrata. G3 (Bethesda) 2, 675-691.
19. Cotter, G., Doyle, S. and Kavanagh, K. (2000). Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol. Med. Microbiol. 27, 163-169.
20. Cuellar-Cruz, M., Briones-Martin-del-Campo, M., Canas-Villamar, I., Montalvo-Arredondo, J., Riego-Ruiz, L., Castano, I. and De Las Penas, A. (2008). High resistance to oxidative stress in the fungal pathogen Candida glabrata is mediated by a single catalase, Cta1p, and is controlled by the transcription factors Yap1p, Skn7p, Msn2p, and Msn4p. Eukaryot. Cell 7, 814-825.
21. Desalermos, A., Fuchs, B. B. and Mylonakis, E. (2012). Selecting an invertebrate model host for the study of fungal pathogenesis. PLoS Pathog. 8, e1002451.
22. Desalermos, A., Tan, X., Rajamuthiah, R., Arvanitis, M., Wang, Y., Li, D., Kourkoumpetis, T. K., Fuchs, B. B. and Mylonakis, E. (2015). A multi-host approach for the systematic analysis of virulence factors in Cryptococcus neoformans. J. Infect. Dis. 211, 298-305.
23. Ferrandon, D., Imler, J.-L., Hetru, C. and Hoffmann, J. A. (2007). The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7, 862-874.
24. Glittenberg, M. T., Silas, S., MacCallum, D. M., Gow, N. A. R. and Ligoxygakis, P. (2011). Wild-type Drosophila melanogaster as an alternative model system for investigating the pathogenicity of Candida albicans. Dis. Model. Mech. 4, 504-514.
25. Gratacap, R. L. and Wheeler, R. T. (2014). Utilization of zebrafish for intravital study of eukaryotic pathogen-host interactions. Dev. Comp. Immunol. 46, 108-115.
26. Gregori, C., Schüller, C., Roetzer, A., Schwarzmüller, T., Ammerer, G. and Kuchler, K. (2007). The high-osmolarity glycerol response pathway in the human fungal pathogen Candida glabrata strain ATCC 2001 lacks a signaling branch that operates in baker's yeast. Eukaryot. Cell 6, 1635-1645.
27. Gullo, A. (2009). Invasive fungal infections: the challenge continues. Drugs 69 Suppl. 1, 65-73.
28. Jacobsen, I. D. (2014). Galleria mellonella as a model host to study virulence of Candida. Virulence 5, 237-239.
29. Jacobsen, I. D., Brunke, S., Seider, K., Schwarzmüller, T., Firon, A., d'Enfert, C., Kuchler, K. and Hube, B. (2010a). Candida glabrata persistence in mice does not depend on host immunosuppression and is unaffected by fungal amino acid auxotrophy. Infect. Immun. 78, 1066-1077.
30. Jacobsen, I. D., Grosse, K., Slesiona, S., Hube, B., Berndt, A. and Brock, M. (2010b). Embryonated eggs as an alternative infection model to investigate Aspergillus fumigatus virulence. Infect. Immun. 78, 2995-3006.
31. Jacobsen, I. D., Grosse, K., Berndt, A. and Hube, B. (2011). Pathogenesis of Candida albicans infections in the alternative chorio-allantoic membrane chicken embryo model resembles systemic murine infections. PLoS ONE 6, e19741.
32. Jacobsen, I. D., Wilson, D., Wächtler, B., Brunke, S., Naglik, J. R. and Hube, B. (2012). Candida albicans dimorphism as a therapeutic target. Expert Rev. Anti Infect. Ther. 10, 85-93.
33. Jander, G., Rahme, L. G. and Ausubel, F. M. (2000). Positive correlation between virulence of Pseudomonas aeruginosa mutants in mice and insects. J. Bacteriol. 182, 3843-3845.
34. phox-/- knockout mice. Antimicrob. Agents Chemother. 46, 1240-1245.
35. Jungmann, J., Rayner, J. C. and Munro, S. (1999). The Saccharomyces cerevisiae protein Mnn10p/Bed1p is a subunit of a Golgi mannosyltransferase complex. J. Biol. Chem. 274, 6579-6585.
36. Kampfenkel, K., Kushnir, S., Babiychuk, E., Inzé, D. and Van Montagu, M. (1995). Molecular characterization of a putative Arabidopsis thaliana copper transporter and its yeast homologue. J. Biol. Chem. 270, 28479-28486.
37. Kasper, L., Seider, K., Gerwien, F., Allert, S., Brunke, S., Schwarzmüller, T., Ames, L., Zubiria Barrera, C., Mansour, M. K., Becken, U. et al. (2014). Identification of Candida glabrata genes involved in pH modulation and modification of the phagosomal environment in macrophages. PLoS ONE 9, e96015.
38. Katiyar, S. K., Alastruey-Izquierdo, A., Healey, K. R., Johnson, M. E., Perlin, D. S. and Edlind, T. D. (2012). Fks1 and Fks2 are functionally redundant but differentially regulated in Candida glabrata: implications for echinocandin resistance. Antimicrob. Agents Chemother. 56, 6304-6309.
39. Kaur, R., Ma, B. and Cormack, B. P. (2007). A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. USA 104, 7628-7633.
40. Ligoxygakis, P., Pelte, N., Ji, C., Leclerc, V., Duvic, B., Belvin, M., Jiang, H., Hoffmann, J. A. and Reichhart, J.-M. (2002). A serpin mutant links Toll activation to melanization in the host defence of Drosophila. EMBO J. 21, 6330-6337.
41. Limmer, S., Quintin, J., Hetru, C. and Ferrandon, D. (2011). Virulence on the fly: Drosophila melanogaster as a model genetic organism to decipher host-pathogen interactions. Curr. Drug Targets 12, 978-999.
42. Lionakis, M. S., Swamydas, M., Fischer, B. G., Plantinga, T. S., Johnson, M. D., Jaeger, M., Green, N. M., Masedunskas, A., Weigert, R., Mikelis, C. et al. (2013). CX3CR1-dependent renal macrophage survival promotes Candida control and host survival. J. Clin. Invest. 123, 5035-5051.
43. Liu, O. W., Chun, C. D., Chow, E. D., Chen, C., Madhani, H. D. and Noble, S. M. (2008). Systematic genetic analysis of virulence in the human fungal pathogen Cryptococcus neoformans. Cell 135, 174-188.
44. Liu, C.-Y., Liao, C.-H., Chen, Y.-C. and Chang, S.-C. (2010). Changing epidemiology of nosocomial bloodstream infections in 11 teaching hospitals in Taiwan between 1993 and 2006. J. Microbiol. Immunol. Infect. 43, 416-429.
45. MacCallum, D. M. (2012). Hosting infection: experimental models to assay Candida virulence. Int. J. Microbiol. 2012, 363764.
46. Morey, J. S., Ryan, J. C. and Van Dolah, F. M. (2006). Microarray validation: factors influencing correlation between oligonucleotide microarrays and real-time PCR. Biol. Proced. Online 8, 175-193.
47. Mylonakis, E., Casadevall, A. and Ausubel, F. M. (2007). Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. PLoS Pathog. 3, e101.
48. Noble, S. M., French, S., Kohn, L. A., Chen, V. and Johnson, A. D. (2010). Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42, 590-598.
49. Odom, A., Muir, S., Lim, E., Toffaletti, D. L., Perfect, J. and Heitman, J. (1997). Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J. 16, 2576-2589.
50. Paisley, D., Robson, G. D. and Denning, D.W. (2005). Correlation between in vitro growth rate and in vivo virulence in Aspergillus fumigatus. Med. Mycol. 43, 397-401.
51. Perlroth, J., Choi, B. and Spellberg, B. (2007). Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45, 321-346.
52. Pukkila-Worley, R., Peleg, A. Y., Tampakakis, E. and Mylonakis, E. (2009). Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot. Cell 8, 1750-1758.
53. Quintin, J., Asmar, J., Matskevich, A. A., Lafarge, M.-C. and Ferrandon, D. (2013). The Drosophila toll pathway controls but does not clear Candida glabrata infections. J. Immunol. 190, 2818-2827.
54. Roetzer, A., Gregori, C., Jennings, A. M., Quintin, J., Ferrandon, D., Butler, G., Kuchler, K., Ammerer, G. and Schüller, C. (2008). Candida glabrata environmental stress response involves Saccharomyces cerevisiae Msn2/4 orthologous transcription factors. Mol. Microbiol. 69, 603-620.
55. Roman, E., Nombela, C. and Pla, J. (2005). The Sho1 adaptor protein links oxidative stress to morphogenesis and cell wall biosynthesis in the fungal pathogen Candida albicans. Mol. Cell. Biol. 25, 10611-10627.
56. Sambrook, J. and Russell, D. (2001). Molecular Cloning - A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
57. Saputo, S., Chabrier-Rosello, Y., Luca, F. C., Kumar, A. and Krysan, D. J. (2012). The RAM network in pathogenic fungi. Eukaryot. Cell 11, 708-717.
58. Schwarzmüller, T., Ma, B., Hiller, E., Istel, F., Tscherner, M., Brunke, S., Ames, L., Firon, A., Green, B., Cabral, V. et al. (2014). Systematic phenotyping of a large-scale Candida glabrata deletion collection reveals novel antifungal tolerance genes. PLoS Pathog. 10, e1004211.
59. Seider, K., Gerwien, F., Kasper, L., Allert, S., Brunke, S., Jablonowski, N., Schwarzmüller, T., Barz, D., Rupp, S., Kuchler, K. et al. (2014). Immune evasion, stress resistance, and efficient nutrient acquisition are crucial for intracellular survival of Candida glabrata within macrophages. Eukaryot. Cell 13, 170-183.
60. Steenbergen, J. N., Shuman, H. A. and Casadevall, A. (2001). Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc. Natl. Acad. Sci. USA 98, 15245-15250.
61. Tauszig-Delamasure, S., Bilak, H., Capovilla, M., Hoffmann, J. A. and Imler, J.- L. (2002). Drosophila MyD88 is required for the response to fungal and Grampositive bacterial infections. Nat. Immunol. 3, 91-97.
62. Tobin, D. M., May, R. C. and Wheeler, R. T. (2012). Zebrafish: a see-through host and a fluorescent toolbox to probe host-pathogen interaction. PLoS Pathog. 8, e1002349.
63. Vandeputte, P., Ischer, F., Sanglard, D. and Coste, A. T. (2011). In vivo systematic analysis of Candida albicans Zn2-Cys6 transcription factors mutants for mice organ colonization. PLoS ONE 6, e26962.