Candida albicans hyphal formation and virulence assessed using a caenorhabditis elegans infection model

Eukaryotic Cell

Volumn 8, Issue 11, 2009, Pages 1750-1758

  Pukkila Worley, Read ^a,c   Peleg, Anton Y ^a,b,c   Tampakakis, Emmanouil ^a   Mylonakis, Eleftherios ^a,c  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b BETH ISRAEL DEACONESS MEDICAL CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN;

ANIMAL; ANIMAL MODEL; ARTICLE; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CANDIDIASIS; FUNGUS HYPHAE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METABOLISM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; VIRULENCE;

ANIMALS; CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CANDIDIASIS; FUNGAL PROTEINS; HUMANS; HYPHAE; MODELS, ANIMAL; VIRULENCE;

CAENORHABDITIS ELEGANS; CANDIDA ALBICANS; CLAVISPORA LUSITANIAE; DEBARYOMYCES HANSENII;

EID: 72449144198     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00163-09     Document Type: Article

References (52)

1. Aballay, A., and F. M. Ausubel. 2002. Caenorhabditis elegans as a host for the study of host-pattiogen interactions. Curr. Opin. Microbiol. 5:97-101.
2. Arendrup, M., T. Horn, and N. Frimodt-Moller. 2002. In vivo pathogenicity of eight medically relevant Candida species in an animal model. Infection 30:286-291.
3. Berman, J., and P. E. Sudbery. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3:918-930.
4. Braun, B. R., W. S. Head, M. X. Wang, and A. D. Johnson. 2000. Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156:31-44.
5. Braun, B. R., D. Kadosh, and A. D. Johnson. 2001. NRG1, a repressor of filamentous growth in Candida albicans, is downregulated during filament induction. EMBO J. 20:4753-4761.
6. Breger, J., B. B. Fuchs, G. Aperis, T. I. Moy, F. M. Ausubel, and E. Mylonakis. 2007. Antifungal chemical compounds identified using a Caenorhabditis elegans pathogenicity assay. PLoS Pattiog. 3:e18.
7. Brennan, M., D. Y. Thomas, M. Whiteway, and K. Kavanagh. 2002. Correlation between virulence of Candida albicans mutants in mice and Galleria mellonella larvae. FEMS Immunol. Med. Microbiol. 34:153-157.
8. Brenner, S. 1974. The genetics of Caenorhabditis elegans. Genetics 77:71-94.
9. Bruno, V. M., S. Kalachikov, R. Subaran, C. J. Nobile, C. Kyratsous, and A. P. Mitchell. 2006. Control of the C. albicans cell wall damage response by transcriptional regulator Cas5. PLoS Pathog. 2:e21.
10. 10. Cao, F., S. Lane, P. P. Raniga, Y. Lu, Z. Zhou, K. Ramon, J. Chen, and H. Liu. 2006. The Flo8 transcription factor is essential for hyphal development and virulence in Candida albicans. Mol. Biol. Cell 17:295-307. (Pubitemid 43049482)
11. Chamilos, G., M. S. Lionakis, R. E. Lewis, J. L. Lopez-Ribot, S. P. Saville, N. D. Albert, G. Haider, and D. P. Kontoyiannis. 2006. Drosophila melanogaster as a facile model for large-scale studies of virulence mechanisms and antifungal drug efficacy in Candida species. J. Infect. Dis. 193:1014-1022.
12. Chamilos, G., C. J. Nobile, V. M. Bruno, R. E. Lewis, A. P. Mitchell, and D. P. Kontoyiannis. 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.
13. Couillault, C., N. Pujol, J. Reboul, L. Sabatier, J. F. Guichou, Y. Kohara, and J. J. Ewbank, 2004. TLR-independent control of innate immunity in Caenorhabditis elegans by the TIR domain adaptor protein TIR-1, an ortholog of human SARM. Nat. Immunol. 5:488-494.
14. Davis, D., J. E. Edwards, Jr., A. P. Mitchell, and A. S. Ibrahim. 2000. Candida albicans RIM101 pH response pattiway is required for host-pathogen interactions. Infect. Immun. 68:5953-5959.
15. Davis, D., R. B. Wilson, and A. P. Mitchell. 2000. RIM101-dependent and-independent pathways govern pH responses in Candida albicans. Mol. Cell. Biol. 20:971-978.
16. Davis, D. A., V. M. Bruno, L. Loza, S. G. Filler, and A. P. Mitchell. 2002. Candida albicans Mds3p, a conserved regulator of pH responses and virulence identified through insertional mutagenesis. Genetics 162:1573-1581.
17. Desnos-Ollivier, M., M. Ragon, V. Robert, D. Raoux, J. C. Gantier, and F. Dromer. 2008. Debaryomyces hansenii (Candida famata), a rare human fungal pathogen often misidentified as Pichia guilliermondii (Candida guilliermondii). J. Clin. Microbiol. 46:3237-3242.
18. Diekema, D. J., S. A. Messer, A. B. Brueggemann, S. L. Coffman, G. V. Doern, L. A. Herwaldt, and M. A. Pfaller. 2002. Epidemiology of candidemia: 3-year results from the emerging infections and the epidemiology of Iowa organisms study. J. Clin. Microbiol. 40:1298-1302.
19. Dujon, B., D. Sherman, G. Fischer, P. Durrens, S. Casaregola, I. Lafontaine, J. De Montigny, C. Marek, C. Neuveglise, E. Talla, N. Goffard, L. Frangeul, M. Aigle, V. Anthouard, A. Babour, V. Barbe, S. Barnay, S. Blanchin, J. M. Beckerich, E. Beyne, C. Bleykasten, A. Boisrame, J. Boyer, L. Cattolico, F. Confanioleri, A. De Daruvar, L. Despons, E. Fabre, C. Fairhead, H. Ferry-Dumazet, A. Groppi, F. Hantraye, C. Hennequin, N. Jauniaux, P. Joyet, R. Kachouri, A. Kerrest, R. Koszul, M. Lemaire, I. Lesur, L. Ma, H. Muller, J. M. Nicaud, M. Nikolski, S. Oztas, O. Ozier-Kalogeropoulos, S. Pellenz, S. Potier, G. F. Richard, M. L. Straub, A. Suleau, D. Swennen, F. Tekaia, M. Wesolowski-Louvel, E. Westhof, B. Wirth, M. Zeniou-Meyer, I. Zivanovic, M. Bolotin-Fukuhara, A. Thierry, C. Bouchier, B. Caudron, C. Scarpelli, C. Gaillardin, J. Weissenbach, P. Wincker, and J. L. Souciet. 2004. Genome evolution in yeasts. Nature 430:35-44.
20. 20. El Barkani, A., O. Kurzai, W. A. Fonzi, A. Ramon, A. Porta, M. Frosch, and F. A. Mühlschlegel. 2000. Dominant active alleles of RIM101 (PRR2) bypass the pH restriction on filamentation of Candida albicans. Mol. Cell. Biol. 20:4635-4647. (Pubitemid 30396111)
21. Fuchs, B. B., and E. Mylonakis. 2006. Using non-mammalian hosts to study fungal virulence and host defense. Curr. Opin. Microbiol. 9:346-351.
22. Gillum, A. M., E. Y. Tsay, and D. R. Kirsch. 1984. Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of Saccharomyces cerevisiae ura3 and Escherichia coli pyrF mutations. Mol. Gen. Genet. 198:179-182.
23. Gow, N. A., A. J. Brown, and F. C. Odds. 2002. Fungal morphogenesis and host invasion. Curr. Opin. Microbiol. 5:366-371.
24. Gudlaugsson, O., S. Gillespie, K. Lee, J. Vande Berg, J. Hu, S. Messer, L. Herwaldt, M. Pfaller, and D. Diekema. 2003. Attributable mortality of nosocomial candidemia, revisited. Clin. Infect. Dis. 37:1172-1177.
25. Holzschu, D. L., H. L. Presley, M. Miranda, and H. J. Phaff. 1979. Identification of Candida lusitaniae as an opportunistic yeast in humans. J. Clin. Microbiol. 10:202-205.
26. Huisinga, K. L., and B. F. Pugh. 2004. A genome-wide housekeeping role for TFIID and a highly regulated stress-related role for SAGA in Saccharomyces cerevisiae. Mol. Cell 13:573-585.
27. Kato, Y., T. Aizawa, H. Hoshino, K. Kawano, K. Nitta, and H. Zhang. 2002. abf-1 and abf-2, ASABF-type antimicrobial peptide genes in Caenorhabditis elegans. Biochem. J. 361:221-230.
28. Kim, D. H., R. Feinbaum, G. Alloing, F. E. Emerson, D. A. Garsin, H. Inoue, M. Tanaka-Hino, N. Hisamoto, K. Matsumoto, M. W. Tan, and F. M. Ausubel. 2002. A conserved p38 MAP kinase pathway in Caenorhabditis elegans innate immunity. Science 297:623-626.
29. Koh, A. Y., J. R. Kohler, K. T. Coggshall, N. Van Rooijen, and G. B. Pier. 2008. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 4:e35.
30. Kohler, J. R., and G. R. Fink. 1996. Candida albicans strains heterozygous and homozygous for mutations in mitogen-activated protein kinase signaling components have defects in hyphal development. Proc. Natl. Acad. Sci. USA 93:13223-13228.
31. 31. Kontoyiannis, D. P., and R. E. Lewis. 2002. Antifungal drug resistance of pathogenic fungi. Lancet 359:1135-1144. (Pubitemid 34270742)
32. Lamagni, T. L., B. G. Evans, M. Shigematsu, and E. M. Johnson. 2001. Emerging trends in the epidemiology of invasive mycoses in England and Wales (1990-9). Epidemiol. Infect. 126:397-414.
33. 33. Laprade, L., V. L. Boyartchuk, W. F. Dietrich, and F. Winston. 2002. Spt3 plays opposite roles in filamentous growth in Saccharomyces cerevisiae and Candida albicans and is required for C. albicans virulence. Genetics 161:509-519. (Pubitemid 34705394)
34. Leleu, G., P. Aegerter, and B. Guidet. 2002. Systemic candidiasis in intensive care units: a multicenter, matched-cohort study. J. Crit. Care 17:168-175.
35. Leroy, O., J. P. Gangneux, P. Montravers, J. P. Mira, F. Gouin, J. P. Sollet, J. Carlet, J. Reynes, M. Rosenheim, B. Regnier, nd O. Lortholary. 2009. Epidemiology, management, and risk factors for death of invasive Candida infections in critical care: a multicenter, prospective, observational study in France (2005-2006). Crit. Care Med. 37:1612-1618.
36. Liu, H., J. Köhler, and G. R. Fink. 1994. Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266:1713-1726.
37. Lo, H. J., J. R. Köhler, B. DiDomenico, D. Loebenberg, A. Cacciapuoti, and G. R. Fink, 1997. Nonfilamentous Candida albicans mutants are avirulent. Cell 90:939-949.
38. Loeffler, J., and D. A. Stevens. 2003. Antifungal drug resistance. Clin. Infect. Dis. 36:S31-S41.
39. Miyata, S., J. Begun, E. R. Troemel, and F. M. Ausubel. 2008. DAF-16-dependent suppression of immunity during reproduction in Caenorhabditis elegans. Genetics 178:903-918.
40. Moy, T. I., A. R. Ball, Z. Anklesaria, G. Casadei, K. Lewis, and F. M. Ausubel. 2006. Identification of novei antimicrobials using a live-animal infection model. Proc. Natl. Acad. Sci. USA 103:10414-10419.
41. Murad, A. M., P. Leng, M. Straffon, J. Wishart, S. Macaskill, D. MacCallum, N. Schnell, D. Talibi, D. Marechal, F. Tekaia, C. d'Enfert, C. Gaillardin, F. C. Odds, and A. J. Brown. 2001. NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J. 20:4742-4752.
42. Mylonakis, E., and A. Aballay. 2005. Worms and flies as genetically tractable animal models to study host-pathogen interactions. Infect. Immun. 73:3833-3841.
43. Mylonakis, E., A. Casadevall, and F. M. Ausubel. 2007. Exploiting amoeboid and non-vertebrate animal model systems to study the virulence of human pathogenic fungi. FLoS Fathog. 3:e101.
44. Nobile, C. J., and A. P. Mitchell. 2005. Regulation of cell-surface genes and biofilm formation by the Candida albicans transcription factor Bcr1p. Curr. Biol. 15:1150-1155.
45. Peleg, A. Y., E. Tampakakis, B. B. Fuchs, G. M. Eliopoulos, R. C. Moellering, and E. Mylonakis. 2008. Prokaryote-eukaryote interactions identified by using Caenorhabditis elegans. Proc. Nad. Acad. Sci. USA 105:14585-14590.
46. Pukkila-Worley, R., E. Holson, F. Wagner, and E. Mylonakis. 2009. Antifungal drug discovery through the study of invertebrate model hosts. Curr. Med. Chem. 16:1588-1595.
47. Saville, S. P., A. L. Lazzell, C. Monteagudo, and J. L. Lopez-Ribot 2003. Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot. Cell 2:1053-1060.
48. Sellam, A., C. Askew, E. Epp, H. Lavoie, M. Whiteway, and A. Nantel. 2009. Genome-wide mapping of the coactivator Ada2p yields insight into the functional roles of SAGA/ADA complex in Candida albicans. Mol. Biol. Cell 20:2389-2400.
49. Shapiro, R. S., P. Uppuluri, A. K. Zaas, C. Collins, H. Senn, J. R. Perfect, J. Heitman, and L. E. Cowen. 2009. Hsp90 orchestrates temperature-dependent Candida albicans morphogenesis via Ras1-PKA signaling. Curr. Biol. 19:621-629.
50. Sifri, C. D., J. Begun, and F. M. Ausubel. 2005. The worm has turned: microbial virulence modeled in Caenorhabditis elegans. Trends Microbiol. 13:119-127.
51. Wagner, D., A. Sander, H. Bertz, J. Finke, and W. V. Kern. 2005. Break-through invasive infection due to Debaryomyces hansenii (teleomorph Candida famata) and Scopulariopsis brevicaulis in a stem cell transplant patient receiving liposomal amphotericin B and caspofungin for suspected aspergillosis. Infection 33:397-400.
52. Young, L. Y., C. M. Hull, and J. Heitman. 2003. Disruption of ergosterol biosynthesis confers resistance to amphotericin B in Candida lusitaniae. Antimicrob. Agents Chemother. 47:2717-2724.