Global analysis of fungal morphology exposes mechanisms of host cell escape

Nature Communications

Volumn 6, Issue , 2015, Pages

  Omeara, Teresa R ^a   Veri, Amanda O ^a   Ketela, Troy ^a   Jiang, Bo ^b   Roemer, Terry ^b   Cowen, Leah E ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MERCK RESEARCH LABORATORIES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERGOSTEROL; GLYCOSYLATED PROTEIN;

APOPTOSIS; FUNGUS; GENOME; GERM CELL; GLOBAL PERSPECTIVE; MORPHOGENESIS; PATHOGEN; VIRULENCE;

ARTICLE; CANDIDA ALBICANS; CELL DEATH; CRYPTOCOCCUS NEOFORMANS; CYTOLYSIS; FUNGAL CELL WALL; FUNGAL DEVELOPMENT; FUNGAL GENOME; FUNGAL STRUCTURES; FUNGAL VIRULENCE; FUNGUS IMMUNITY; GENOME ANALYSIS; GLYCOSYLATION; HOST CELL; IMMUNE EVASION; IMMUNOCOMPETENT CELL; MACROPHAGE; MORPHOGENESIS; NONHUMAN; PHAGOSOME; PYROPTOSIS; STEROL SYNTHESIS; ANIMAL; CELL LINE; CELL WALL; FUNGUS HYPHAE; GENETICS; IMMUNOLOGY; INTERFERENCE MICROSCOPY; MOUSE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE; ULTRASTRUCTURE;

CANDIDA ALBICANS; FILOBASIDIELLA NEOFORMANS; FUNGI;

ANIMALS; CANDIDA ALBICANS; CELL DEATH; CELL LINE; CELL WALL; CRYPTOCOCCUS NEOFORMANS; HYPHAE; IMMUNE EVASION; MACROPHAGES; MICE; MICROSCOPY, INTERFERENCE; MORPHOGENESIS; PHAGOSOMES; PYROPTOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SACCHAROMYCES CEREVISIAE;

EID: 84926312414     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms7741     Document Type: Article

References (40)

1. Klein, B. S., Tebbets, B. Dimorphism and virulence in fungi. Curr. Opin. Microbiol. 10, 314-319 (2007).
2. Saville, S. P., Lazzell, A. L., Monteagudo, C., Lopez-Ribot, J. L. 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 (2003).
3. Lo, H. J. et al. Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949 (1997).
4. Noble, S. M., French, S., Kohn, L. A., Chen, V., Johnson, A. D. Systematic screens of a Candida albicans homozygous deletion library decouple morphogenetic switching and pathogenicity. Nat. Genet. 42, 590-598 (2010).
5. Xu, D. et al. Genome-wide fitness test and mechanism-of-action studies of inhibitory compounds in Candida albicans. PLoS Pathogens 3, e92 (2007).
6. Gow, N. A. R., van de Veerdonk, F. L., Brown, A. J. P., Netea, M. G. Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat. Rev. Microbiol. 10, 112-122 (2011).
7. Roemer, T. et al. Large-scale essential gene identification in Candida albicans and applications to antifungal drug discovery. Mol. Microbiol. 50, 167-181 (2003).
8. Sudbery, P. E. Growth of Candida albicans hyphae. Nat. Rev. Microbiol. 9, 737-748 (2011).
9. Shapiro, R. S., Robbins, N., Cowen, L. E. Regulatory circuitry governing fungal development, drug resistance, and disease. Microbiol. Mol. Biol. Rev. 75, 213-267 (2011).
10. Ryan, O. et al. Global gene deletion analysis exploring yeast filamentous growth. Science 337, 1353-1356 (2012).
11. Braun, B. R. et al. A human-curated annotation of the Candida albicans genome. PLoS Genet. 1, e1 (2005).
12. Netea, M. G., Brown, G. D., Kullberg, B. J., Gow, N. A. R. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6, 67-78 (2008).
13. Bensen, E. S., Clemente-Blanco, A., Finley, K. R., Correa-Bordes, J., Berman, J. The mitotic cyclins Clb2p and Clb4p affect morphogenesis in Candida albicans. Mol. Biol. Cell 16, 3387-3400 (2005).
14. Umeyama, T., Kaneko, A., Niimi, M., Uehara, Y. Repression of CDC28 reduces the expression of the morphology-related transcription factors, Efg1p, Nrg1p, Rbf1p, Rim101p, Fkh2p and Tec1p and induces cell elongation in Candida albicans. Yeast 23, 537-552 (2006).
15. Berman, J. Morphogenesis and cell cycle progression in Candida albicans. Curr. Opin. Microbiol. 9, 595-601 (2006).
16. Becker, J. M. et al. Pathway analysis of Candida albicans survival and virulence determinants in a murine infection model. Proc. Natl Acad. Sci USA 107, 22044-22049 (2010).
17. Smith, A. M. et al. Highly-multiplexed barcode sequencing: an efficient method for parallel analysis of pooled samples. Nucleic Acids Res. 38, e142 (2010).
18. Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906 (1999).
19. Uhl, M. A., Biery, M., Craig, N., Johnson, A. D. Haploinsufficiency-based large-scale forward genetic analysis of filamentous growth in the diploid human fungal pathogen C. albicans. EMBO J. 22, 2668-2678 (2003).
20. Onyewu, C., Blankenship, J. R., Del Poeta, M., Heitman, J. Ergosterol biosynthesis inhibitors become fungicidal when combined with calcineurin inhibitors against Candida albicans, Candida glabrata, and Candida krusei. Antimicrob. Agents Chemother. 47, 956-964 (2003).
21. Vincent, B. M., Lancaster, A. K., Scherz-Shouval, R., Whitesell, L., Lindquist, S. Fitness trade-offs restrict the evolution of resistance to Amphotericin B. PLoS Biol. 11, e1001692 (2013).
22. Wachtler, B., Wilson, D., Hube, B. Candida albicans adhesion to and invasion and damage of vaginal epithelial cells: stage-specific inhibition by clotrimazole and bifonazole. Antimicrob. Agents Chemother. 55, 4436-4439 (2011).
23. Martnez-Duncker, I., Daz-Jmenez, D. F., Mora-Montes, H. M. Comparative analysis of protein glycosylation pathways in humans and the fungal pathogen Candida albicans. Int. J. Microbiol. 2014, 267497 (2014).
24. Helenius, J. et al. Translocation of lipid-linked oligosaccharides across the ER membrane requires Rft1 protein. Nature 415, 447-450 (2002).
25. Krysan, D. J., Sutterwala, F. S., Wellington, M. Catching fire: Candida albicans, macrophages, and pyroptosis. PLoS Pathogens 10, e1004139 (2014).
26. Wellington, M., Koselny, K., Krysan, D. J. Candida albicans morphogenesis is not required for macrophage interleukin 1-beta production. MBio 4, e00433-12 (2012).
27. Uwamahoro, N. et al. The pathogen Candida albicans hijacks pyroptosis for escape from macrophages. MBio 5, e00003-e00014 (2014).
28. Hall, R. A., Gow, N. A. R. Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol. Microbiol. 90, 1147-1161 (2013).
29. Guo, C. et al. Acapsular Cryptococcus neoformans activates the NLRP3 inflammasome. Microb. Infect. 16, 845-854 (2014).
30. OMeara, T., Alspaugh, J. A. The Cryptococcus neoformans capsule: a sword and a shield. Clin. Microbiol. Rev. 25, 387-408 (2012).
31. Epp, E. et al. Forward genetics in Candida albicans that reveals the Arp2/3 complex is required for hyphal formation, but not endocytosis. Mol. Microbiol. 75, 1182-1198 (2010).
32. Li, Z. et al. Systematic exploration of essential yeast gene function with temperature-sensitive mutants. Nat. Biotechnol. 29, 361-367 (2011).
33. Vizeacoumar, F. S., Chong, Y., Boone, C., Andrews, B. J. A picture is worth a thousand words: genomics to phenomics in the yeast Saccharomyces cerevisiae. FEBS Lett. 583, 1656-1661 (2009).
34. Li, X., Gianoulis, T. A., Yip, K. Y., Gerstein, M., Snyder, M. Extensive in vivo metabolite-protein interactions revealed by large-scale systematic analyses. Cell 143, 639-650 (2010).
35. Martin, S. W., Konopka, J. B. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3, 675-684 (2004).
36. Hise, A. G. et al. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 5, 487-497 (2009).
37. Kumamoto, C. A., Vinces, M. D. Contributions of hyphae and hypha-coregulated genes to Candida albicans virulence. Cell Micro Biol. 7, 1546-1554 (2005).
38. Bain, J. M. et al. Candida albicans hypha formation and mannan masking of beta-glucan inhibit macrophage phagosome maturation. MBio 5, e01874 (2014).
39. Wright, G. J., Rayner, J. C. Plasmodium falciparum erythrocyte invasion: combining function with immune evasion. PLoS Pathogens 10, e1003943 (2014).
40. Clatworthy, A. E., Pierson, E., Hung, D. T. Targeting virulence: a new paradigm for antimicrobial therapy. Nat. Chem. Biol. 3, 541-548 (2007).