Invertebrate models of fungal infection

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1832, Issue 9, 2013, Pages 1378-1383

  Arvanitis, Marios ^a   Glavis Bloom, Justin ^a   Mylonakis, Eleftherios ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Antifungal compound; Fungal infection; Fungal virulence; Innate immunity; Invertebrate; Model host

Indexed keywords

ANTIFUNGAL AGENT;

ANTIFUNGAL ACTIVITY; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; DRUG DETERMINATION; FUNGAL VIRULENCE; GALLERIA MELLONELLA; HOST; INVERTEBRATE MODEL; MYCOSIS; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; DISEASE MODEL; DRUG DEVELOPMENT; DRUG EFFECT; FUNGUS; GENETICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; INVERTEBRATE; MICROBIOLOGY; PATHOGENICITY;

ANIMALIA; CAENORHABDITIS ELEGANS; DROSOPHILA MELANOGASTER; GALLERIA MELLONELLA; HEXAPODA; INVERTEBRATA; MAMMALIA;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG DISCOVERY; FUNGI; HUMANS; IMMUNITY, INNATE; INVERTEBRATES; MYCOSES;

MLCS; MLOWN;

EID: 84881249975     PISSN: 09254439     EISSN: 1879260X     Source Type: Journal    
DOI: 10.1016/j.bbadis.2013.03.008     Document Type: Review

References (84)

1. Pfaller M.A. Antifungal drug resistance: mechanisms, epidemiology, and consequences for treatment. Am. J. Med. 2012, 125:S3-S13.
2. Lin S.J., Schranz J., Teutsch S.M. Aspergillosis case-fatality rate: systematic review of the literature. Clin. Infect. Dis. 2001, 32:358-366.
3. Zirkel J., Klinker H., Kuhn A., Abele-Horn M., Tappe D., Turnwald D., Einsele H., Heinz W.J. Epidemiology of Candida blood stream infections in patients with hematological malignancies or solid tumors. Med. Mycol. 2012, 50:50-55.
4. Eggimann P., Garbino J., Pittet D. Epidemiology of Candida species infections in critically ill non-immunosuppressed patients. Lancet Infect. Dis. 2003, 3:685-702.
5. Hoffmann J.A., Kafatos F.C., Janeway C.A., Ezekowitz R.A. Phylogenetic perspectives in innate immunity. Science 1999, 284:1313-1318.
6. Lemaitre B., Nicolas E., Michaut L., Reichhart J.M., Hoffmann J.A. The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 1996, 86:973-983.
7. De Gregorio E., Spellman P.T., Rubin G.M., Lemaitre B. Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:12590-12595.
8. Foley E., O'Farrell P.H. Functional dissection of an innate immune response by a genome-wide RNAi screen. PLoS Biol. 2004, 2:E203.
9. Ferrandon D., Imler J.L., Hetru C., Hoffmann J.A. The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 2007, 7:862-874.
10. Hamilos G., Samonis G., Kontoyiannis D.P. Recent advances in the use of Drosophila melanogaster as a model to study immunopathogenesis of medically important filamentous fungi. Int. J. Microbiol. 2012, 2012:583792.
11. Lionakis M.S. Drosophila and Galleria insect model hosts: new tools for the study of fungal virulence, pharmacology and immunology. Virulence 2011, 2:521-527.
12. Zhang Z.T., Zhu S.Y. Drosomycin, an essential component of antifungal defence in Drosophila. Insect Mol. Biol. 2009, 18:549-556.
13. Levashina E.A., Ohresser S., Bulet P., Reichhart J.M., Hetru C., Hoffmann J.A. Metchnikowin, a novel immune-inducible proline-rich peptide from Drosophila with antibacterial and antifungal properties. Eur. J. Biochem. 1995, 233:694-700.
14. Gottar M., Gobert V., Matskevich A.A., Reichhart J.M., Wang C., Butt T.M., Belvin M., Hoffmann J.A., Ferrandon D. Dual detection of fungal infections in Drosophila via recognition of glucans and sensing of virulence factors. Cell 2006, 127:1425-1437.
15. Akhouayri I., Turc C., Royet J., Charroux B. Toll-8/Tollo negatively regulates antimicrobial response in the Drosophila respiratory epithelium. PLoS Pathog. 2011, 7:e1002319.
16. Tzou P., Ohresser S., Ferrandon D., Capovilla M., Reichhart J.M., Lemaitre B., Hoffmann J.A., Imler J.L. Tissue-specific inducible expression of antimicrobial peptide genes in Drosophila surface epithelia. Immunity 2000, 13:737-748.
17. Charroux B., Royet J. Drosophila immune response: from systemic antimicrobial peptide production in fat body cells to local defense in the intestinal tract. Fly (Austin) 2010, 4:40-47.
18. Cronin S.J., Nehme N.T., Limmer S., Liegeois S., Pospisilik J.A., Schramek D., Leibbrandt A., Simoes Rde M., Gruber S., Puc U., Ebersberger I., Zoranovic T., Neely G.G., von Haeseler A., Ferrandon D., Penninger J.M. Genome-wide RNAi screen identifies genes involved in intestinal pathogenic bacterial infection. Science 2009, 325:340-343.
19. Chen J., Xie C., Tian L., Hong L., Wu X., Han J. Participation of the p38 pathway in Drosophila host defense against pathogenic bacteria and fungi. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20774-20779.
20. Alarco A.M., Marcil A., Chen J., Suter B., Thomas D., Whiteway M. Immune-deficient Drosophila melanogaster: a model for the innate immune response to human fungal pathogens. J. Immunol. 2004, 172:5622-5628.
21. Apidianakis Y., Rahme L.G., Heitman J., Ausubel F.M., Calderwood S.B., Mylonakis E. Challenge of Drosophila melanogaster with Cryptococcus neoformans and role of the innate immune response. Eukaryot. Cell 2004, 3:413-419.
22. Lionakis M.S., Kontoyiannis D.P. Drosophila melanogaster as a model organism for invasive aspergillosis. Methods Mol. Biol. 2012, 845:455-468.
23. Glittenberg M.T., Silas S., MacCallum D.M., Gow N.A., Ligoxygakis P. Wild-type Drosophila melanogaster as an alternative model system for investigating the pathogenicity of Candida albicans. Dis. Model. Mech. 2011, 4:504-514.
24. Quintin J., Asmar J., Matskevich A.A., Lafarge M.C., Ferrandon D. The Drosophila Toll pathway controls but does not clear Candida glabrata infections. J. Immunol. 2013, 190:2818-2827.
25. Lohse M.B., Johnson A.D. Differential phagocytosis of white versus opaque Candida albicans by Drosophila and mouse phagocytes. PLoS One 2008, 3:e1473.
26. Qin Q.M., Luo J., Lin X., Pei J., Li L., Ficht T.A., de Figueiredo P. Functional analysis of host factors that mediate the intracellular lifestyle of Cryptococcus neoformans. PLoS Pathog. 2011, 7:e1002078.
27. Desalermos A., Fuchs B.B., Mylonakis E. Selecting an invertebrate model host for the study of fungal pathogenesis. PLoS Pathog. 2012, 8:e1002451.
28. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998, 391:806-811.
29. Muhammed M., Coleman J.J., Mylonakis E. Caenorhabditis elegans: a nematode infection model for pathogenic fungi. Methods Mol. Biol. 2012, 845:447-454.
30. Kim D.H., Feinbaum R., Alloing G., Emerson F.E., Garsin D.A., Inoue H., Tanaka-Hino M., Hisamoto N., Matsumoto K., Tan M.W., Ausubel F.M. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 2002, 297:623-626.
31. Liberati N.T., Fitzgerald K.A., Kim D.H., Feinbaum R., Golenbock D.T., Ausubel F.M. Requirement for a conserved Toll/interleukin-1 resistance domain protein in the Caenorhabditis elegans immune response. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:6593-6598.
32. Couillault C., Pujol N., Reboul J., Sabatier L., Guichou J.F., Kohara Y., Ewbank J.J. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 2004, 5:488-494.
33. Couillault C., Fourquet P., Pophillat M., Ewbank J.J. A UPR-independent infection-specific role for a BiP/GRP78 protein in the control of antimicrobial peptide expression in C. elegans epidermis. Virulence 2012, 3:299-308.
34. Lamitina T., Chevet E. To UPR and beyond! A new role for a BiP/GRP78 protein in the control of antimicrobial peptide expression in C. elegans epidermis. Virulence 2012, 3:238-240.
35. Simonsen K.T., Moller-Jensen J., Kristensen A.R., Andersen J.S., Riddle D.L., Kallipolitis B.H. Quantitative proteomics identifies ferritin in the innate immune response of C. elegans. Virulence 2011, 2:120-130.
36. Irazoqui J.E. Transparent worms help survey the fortress of innate immunity. Virulence 2011, 2:83-85.
37. Pukkila-Worley R., Peleg A.Y., Tampakakis E., Mylonakis E. Candida albicans hyphal formation and virulence assessed using a Caenorhabditis elegans infection model. Eukaryot. Cell 2009, 8:1750-1758.
38. Pukkila-Worley R., Ausubel F.M., Mylonakis E. Candida albicans infection of Caenorhabditis elegans induces antifungal immune defenses. PLoS Pathog. 2011, 7:e1002074.
39. Peleg A.Y., Tampakakis E., Fuchs B.B., Eliopoulos G.M., Moellering R.C., Mylonakis E. Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:14585-14590.
40. Tampakakis E., Peleg A.Y., Mylonakis E. Interaction of Candida albicans with an intestinal pathogen, Salmonella enterica serovar Typhimurium. Eukaryot. Cell 2009, 8:732-737.
41. Cruz M.R., Graham C.E., Gagliano B.C., Lorenz M.C., Garsin D.A. Enterococcus faecalis inhibits hyphal morphogenesis and virulence of Candida albicans. Infect. Immun. 2013, 81:189-200.
42. Mylonakis E., Ausubel F.M., Perfect J.R., Heitman J., Calderwood S.B. Killing of Caenorhabditis elegans by Cryptococcus neoformans as a model of yeast pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:15675-15680.
43. Johnson C.H., Ayyadevara S., McEwen J.E., Shmookler Reis R.J. Histoplasma capsulatum and Caenorhabditis elegans: a simple nematode model for an innate immune response to fungal infection. Med. Mycol. 2009, 47:808-813.
44. Breger J., Fuchs B.B., Aperis G., Moy T.I., Ausubel F.M., Mylonakis E. Antifungal chemical compounds identified using a C. elegans pathogenicity assay. PLoS Pathog. 2007, 3:e18.
45. Coleman J.J., Okoli I., Tegos G.P., Holson E.B., Wagner F.F., Hamblin M.R., Mylonakis E. Characterization of plant-derived saponin natural products against Candida albicans. ACS Chem. Biol. 2010, 5:321-332.
46. Coleman J.J., Ghosh S., Okoli I., Mylonakis E. Antifungal activity of microbial secondary metabolites. PLoS One 2011, 6:e25321.
47. Okoli I., Coleman J.J., Tampakakis E., An W.F., Holson E., Wagner F., Conery A.L., Larkins-Ford J., Wu G., Stern A., Ausubel F.M., Mylonakis E. Identification of antifungal compounds active against Candida albicans using an improved high-throughput Caenorhabditis elegans assay. PLoS One 2009, 4:e7025.
48. Oh S., Go G.W., Mylonakis E., Kim Y. The bacterial signalling molecule indole attenuates the virulence of the fungal pathogen Candida albicans. J. Appl. Microbiol. 2012, 113:622-628.
49. Gotz P., Matha V., Vilcinskas A. Effects of the entomopathogenic fungus Metarhizium anisopliae and its secondary metabolites on morphology and cytoskeleton of plasmatocytes isolated from the greater wax moth, Galleria mellonella. J. Insect Physiol. 1997, 43:1149-1159.
50. Cotter G., Doyle S., Kavanagh K. Development of an insect model for the in vivo pathogenicity testing of yeasts. FEMS Immunol. Med. Microbiol. 2000, 27:163-169.
51. Mowlds P., Kavanagh K. Effect of pre-incubation temperature on susceptibility of Galleria mellonella larvae to infection by Candida albicans. Mycopathologia 2008, 165:5-12.
52. Wojda I., Kowalski P., Jakubowicz T. Humoral immune response of Galleria mellonella larvae after infection by Beauveria bassiana under optimal and heat-shock conditions. J. Insect Physiol. 2009, 55:525-531.
53. Walters J.B., Ratcliffe N.A. Studies on the in vivo cellular reactions of insects: Fate of pathogenic and non-pathogenic bacteria in Galleria mellonella nodules. J. Insect Physiol. 1983, 29:417-424.
54. Vogel H., Altincicek B., Glockner G., Vilcinskas A. A comprehensive transcriptome and immune-gene repertoire of the lepidopteran model host Galleria mellonella. BMC Genomics 2011, 12:308.
55. Renwick J., Reeves E.P., Wientjes F.B., Kavanagh K. Translocation of proteins homologous to human neutrophil p47phox and p67phox to the cell membrane in activated hemocytes of Galleria mellonella. Dev. Comp. Immunol. 2007, 31:347-359.
56. Fallon J.P., Reeves E.P., Kavanagh K. The Aspergillus fumigatus toxin fumagillin suppresses the immune response of Galleria mellonella larvae by inhibiting the action of haemocytes. Microbiology 2011, 157:1481-1488.
57. Dunphy G.B., Oberholzer U., Whiteway M., Zakarian R.J., Boomer I. Virulence of Candida albicans mutants toward larval Galleria mellonella (Insecta, Lepidoptera, Galleridae). Can. J. Microbiol. 2003, 49:514-524.
58. Weers P.M., Ryan R.O. Apolipophorin III: role model apolipoprotein. Insect Biochem. Mol. Biol. 2006, 36:231-240.
59. Mak P., Zdybicka-Barabas A., Cytrynska M. A different repertoire of Galleria mellonella antimicrobial peptides in larvae challenged with bacteria and fungi. Dev. Comp. Immunol. 2010, 34:1129-1136.
60. Schuhmann B., Seitz V., Vilcinskas A., Podsiadlowski L. Cloning and expression of gallerimycin, an antifungal peptide expressed in immune response of greater wax moth larvae, Galleria mellonella. Arch. Insect Biochem. Physiol. 2003, 53:125-133.
61. Bergin D., Murphy L., Keenan J., Clynes M., Kavanagh K. Pre-exposure to yeast protects larvae of Galleria mellonella from a subsequent lethal infection by Candida albicans and is mediated by the increased expression of antimicrobial peptides. Microbes Infect. 2006, 8:2105-2112.
62. Fallon J.P., Troy N., Kavanagh K. Pre-exposure of Galleria mellonella larvae to different doses of Aspergillus fumigatus conidia causes differential activation of cellular and humoral immune responses. Virulence 2011, 2:413-421.
63. Banville N., Browne N., Kavanagh K. Effect of nutrient deprivation on the susceptibility of Galleria mellonella larvae to infection. Virulence 2012, 3.
64. Brennan M., Thomas D.Y., Whiteway M., Kavanagh K. Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol. Med. Microbiol. 2002, 34:153-157.
65. Fuchs B.B., Eby J., Nobile C.J., El Khoury J.B., Mitchell A.P., Mylonakis E. Role of filamentation in Galleria mellonella killing by Candida albicans. Microbes Infect. 2010, 12:488-496.
66. Mylonakis E., Moreno R., El Khoury J.B., Idnurm A., Heitman J., Calderwood S.B., Ausubel F.M., Diener A. Galleria mellonella as a model system to study Cryptococcus neoformans pathogenesis. Infect. Immun. 2005, 73:3842-3850.
67. Garcia-Rodas R., Casadevall A., Rodriguez-Tudela J.L., Cuenca-Estrella M., Zaragoza O. Cryptococcus neoformans capsular enlargement and cellular gigantism during Galleria mellonella infection. PLoS One 2011, 6:e24485.
68. Coleman J.J., Muhammed M., Kasperkovitz P.V., Vyas J.M., Mylonakis E. Fusarium pathogenesis investigated using Galleria mellonella as a heterologous host. Fungal Biol. 2011, 115:1279-1289.
69. Slater J.L., Gregson L., Denning D.W., Warn P.A. Pathogenicity of Aspergillus fumigatus mutants assessed in Galleria mellonella matches that in mice. Med. Mycol. 2011, 49(Suppl. 1):S107-S113.
70. Jackson J.C., Higgins L.A., Lin X. Conidiation color mutants of Aspergillus fumigatus are highly pathogenic to the heterologous insect host Galleria mellonella. PLoS One 2009, 4:e4224.
71. Thomaz L., Garcia-Rodas R., Guimaraes A.J., Taborda C.P., Zaragoza O., Nosanchuk J.D. Galleria mellonella as a model host to study Paracoccidioides lutzii and Histoplasma capsulatum. Virulence 2013, 4:139-146.
72. Mesa-Arango A.C., Forastiero A., Bernal-Martinez L., Cuenca-Estrella M., Mellado E., Zaragoza O. The non-mammalian host Galleria mellonella can be used to study the virulence of the fungal pathogen Candida tropicalis and the efficacy of antifungal drugs during infection by this pathogenic yeast. Med. Mycol. 2012, 10.3109/13693786.2012.737031.
73. Vu K., Gelli A. Astemizole and an analogue promote fungicidal activity of fluconazole against Cryptococcus neoformans var. grubii and Cryptococcus gattii. Med. Mycol. 2010, 48:255-262.
74. Bastidas R.J., Shertz C.A., Lee S.C., Heitman J., Cardenas M.E. Rapamycin exerts antifungal activity in vitro and in vivo against Mucor circinelloides via FKBP12-dependent inhibition of Tor. Eukaryot. Cell 2012, 11:270-281.
75. Kelly J., Kavanagh K. Caspofungin primes the immune response of the larvae of Galleria mellonella and induces a non-specific antimicrobial response. J. Med. Microbiol. 2011, 60:189-196.
76. Steenbergen J.N., Shuman H.A., Casadevall A. Cryptococcus neoformans interactions with amoebae suggest an explanation for its virulence and intracellular pathogenic strategy in macrophages. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:15245-15250.
77. Chrisman C.J., Alvarez M., Casadevall A. Phagocytosis of Cryptococcus neoformans by, and nonlytic exocytosis from, Acanthamoeba castellanii. Appl. Environ. Microbiol. 2010, 76:6056-6062.
78. Chrisman C.J., Albuquerque P., Guimaraes A.J., Nieves E., Casadevall A. Phospholipids trigger Cryptococcus neoformans capsular enlargement during interactions with amoebae and macrophages. PLoS Pathog. 2011, 7:e1002047.
79. Steenbergen J.N., Nosanchuk J.D., Malliaris S.D., Casadevall A. Interaction of Blastomyces dermatitidis, Sporothrix schenckii, and Histoplasma capsulatum with Acanthamoeba castellanii. Infect. Immun. 2004, 72:3478-3488.
80. Steenbergen J.N., Nosanchuk J.D., Malliaris S.D., Casadevall A. Cryptococcus neoformans virulence is enhanced after growth in the genetically malleable host Dictyostelium discoideum. Infect. Immun. 2003, 71:4862-4872.
81. Hanaoka N., Takano Y., Shibuya K., Fugo H., Uehara Y., Niimi M. Identification of the putative protein phosphatase gene PTC1 as a virulence-related gene using a silkworm model of Candida albicans infection. Eukaryot. Cell 2008, 7:1640-1648.
82. Ueno K., Matsumoto Y., Uno J., Sasamoto K., Sekimizu K., Kinjo Y., Chibana H. Intestinal resident yeast Candida glabrata requires Cyb2p-mediated lactate assimilation to adapt in mouse intestine. PLoS One 2011, 6:e24759.
83. Da Silva J.B., De Albuquerque C.M., De Araujo E.C., Peixoto C.A., Hurd H. Immune defense mechanisms of Culex quinquefasciatus (Diptera: Culicidae) against Candida albicans infection. J. Invertebr. Pathol. 2000, 76:257-262.
84. Lionakis M.S., Kontoyiannis D.P. The growing promise of Toll-deficient Drosophila melanogaster as a model for studying Aspergillus pathogenesis and treatment. Virulence 2010, 1:488-499.