BRG1 and NRG1 form a novel feedback circuit regulating Candida albicans hypha formation and virulence

Molecular Microbiology

Volumn 85, Issue 3, 2012, Pages 557-573

  Cleary, Ian A ^a   Lazzell, Anna L ^a   Monteagudo, Carlos ^b   Thomas, Derek P ^c   Saville, Stephen P ^a  

^a UNIVERSITY OF TEXAS AT SAN ANTONIO   (United States)

^b UNIVERSITY OF VALENCIA   (Spain)

^c GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; MESSENGER RNA;

ANIMAL TISSUE; ARTICLE; BRG1 GENE; CANDIDA ALBICANS; CONTROLLED STUDY; ENVIRONMENTAL FACTOR; FEEDBACK SYSTEM; FUNGAL GENE; FUNGAL GENETICS; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE INDUCTION; GENE OVEREXPRESSION; GENE REPRESSION; GENETIC TRAIT; MOUSE; NONHUMAN; NRG1 GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; RNA STABILITY; TRANSCRIPTION REGULATION; YEAST;

ANIMALS; BIOFILMS; CANDIDA ALBICANS; FEMALE; FUNGAL PROTEINS; GATA TRANSCRIPTION FACTORS; GENE EXPRESSION; GENE EXPRESSION REGULATION, FUNGAL; HYPHAE; MICE; MICE, INBRED BALB C; OPEN READING FRAMES; REPRESSOR PROTEINS; RNA STABILITY; TRANSCRIPTION, GENETIC; VIRULENCE;

CANDIDA ALBICANS;

EID: 84864086156     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2012.08127.x     Document Type: Article

References (59)

1. Bendel, C.M., Hess, D.J., Garni, R.M., Henry-Stanley, M., and Wells, C.L. (2003) Comparative virulence of Candida albicans yeast and filamentous forms in orally and intravenously inoculated mice. Crit Care Med 31: 501-507.
2. Bernardo, S.M., Khalique, Z., Kot, J., Jones, J.K., and Lee, S.A. (2008) Candida albicans VPS1 contributes to protease secretion, filamentation, and biofilm formation. Fungal Genet Biol 45: 861-877.
3. Bernstein, D.A., Vyas, V.K., Weinberg, D.E., Drinnenberg, I.A., Bartel, D.P., and Fink, G.R. (2012) Candida albicans Dicer (CaDcr1) is required for efficient ribosomal and spliceosomal RNA maturation. Proc Natl Acad Sci USA 109: 523-528.
4. Biswas, S., Dijck, P.V., and Datta, A. (2007) Environmental sensing and signal transduction pathways regulating morphopathogenic determinants of Candida albicans. Microbiol Mol Biol Rev 71: 348-376.
5. Boland, J.M., Chung, H.H., Robberts, F.J., Wilson, W.R., Steckelberg, J.M., Baddour, L.M., and Miller, D.V. (2011) Fungal prosthetic valve endocarditis: Mayo Clinic experience with a clinicopathological analysis. Mycoses 54: 354-360.
6. Braun, B.R., and Johnson, A.D. (1997) Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277: 105-109.
7. Braun, B.R., Head, W.S., Wang, M.X., and Johnson, A.D. (2000) Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156: 31-44.
8. Braun, B.R., Kadosh, D., and Johnson, A.D. (2001) NRG1, a repressor of filamentous growth in C.albicans, is down-regulated during filament induction. EMBO J 20: 4753-4761.
9. Bruno, V.M., Wang, Z., Marjani, S.L., Euskirchen, G.M., Martin, J., Sherlock, G., and Snyder, M. (2010) Comprehensive annotation of the transcriptome of the human fungal pathogen Candida albicans using RNA-seq. Genome Res 20: 1451-1458.
10. Cai, X., Hagedorn, C.H., and Cullen, B.R. (2004) Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10: 1957-1966.
11. Catalanotto, C., Azzalin, G., Macino, G., and Cogoni, C. (2000) Gene silencing in worms and fungi. Nature 404: 245.
12. Catalanotto, C., Pallotta, M., ReFalo, P., Sachs, M.S., Vayssie, L., Macino, G., and Cogoni, C. (2004) Redundancy of the two dicer genes in transgene-induced posttranscriptional gene silencing in Neurospora crassa. Mol Cell Biol 24: 2536-2545.
13. Cenik, E.S., and Zamore, P.D. (2011) Argonaute proteins. Curr Biol 21: R446-R449.
14. Chen, C.G., Yang, Y.L., Cheng, H.H., Su, C.L., Huang, S.F., Chen, C.T., etal. (2006) Non-lethal Candida albicans cph1/cph1 efg1/efg1 transcription factor mutant establishing restricted zone of infection in a mouse model of systemic infection. Int J Immunopathol Pharmacol 19: 561-565.
15. Chen, H.M., and Neiman, A.M. (2011) A conserved regulatory role for antisense RNA in meiotic gene expression in yeast. Curr Opin Microbiol 14: 655-659.
16. Cleary, I.A., and Saville, S.P. (2010) An analysis of the impact of NRG1 overexpression on the Candida albicans response to specific environmental stimuli. Mycopathologia 170: 1-10.
17. Cleary, I.A., Mulabagal, P., Reinhard, S.M., Yadev, N., Murdoch, C., Thornhill, M.H., etal. (2010) Pseudohyphal regulation by the transcription factor Rfg1p in Candida albicans. Eukaryot Cell 9: 1363-1373.
18. Dang, Y., Yang, Q., Xue, Z., and Liu, Y. (2011) RNA interference in fungi: pathways, functions, and applications. Eukaryot Cell 10: 1148-1155.
19. Ding, S.W., and Voinnet, O. (2007) Antiviral immunity directed by small RNAs. Cell 130: 413-426.
20. Drinnenberg, I.A., Weinberg, D.E., Xie, K.T., Mower, J.P., Wolfe, K.H., Fink, G.R., and Bartel, D.P. (2009) RNAi in budding yeast. Science 326: 544-550.
21. Drinnenberg, I.A., Fink, G.R., and Bartel, D.P. (2011) Compatibility with killer explains the rise of RNAi-deficient fungi. Science 333: 1592.
22. Du, H., Guan, G., Xie, J., Sun, Y., Tong, Y., Zhang, L., and Huang, G. (2012) Roles of Candida albicans Gat2, a GATA-type zinc finger transcription factor, in biofilm formation, filamentous growth and virulence. PLoS ONE 7: e29707.
23. Farazi, T.A., Juranek, S.A., and Tuschl, T. (2008) The growing catalog of small RNAs and their association with distinct Argonaute/Piwi family members. Development 135: 1201-1214.
24. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811.
25. Gelfand, B., Mead, J., Bruning, A., Apostolopoulos, N., Tadigotla, V., Nagaraj, V., etal. (2011) Regulated antisense transcription controls expression of cell-type-specific genes in yeast. Mol Cell Biol 31: 1701-1709.
26. Gillum, A.M., Tsay, E.Y., and Kirsch, D.R. (1984) Isolation of the Candida albicans gene for orotidine-5′-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198: 179-182.
27. Gossen, M., and Bujard, H. (1992) Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc Natl Acad Sci USA 89: 5547-5551.
28. Grocott, R.G. (1955) A stain for fungi in tissue sections and smears using Gomori's methenamine-silver nitrate technic. Am J Clin Pathol 25: 975-979.
29. Grubb, S.E., Murdoch, C., Sudbery, P.E., Saville, S.P., Lopez-Ribot, J.L., and Thornhill, M.H. (2009) Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infect Immun 77: 3872-3878.
30. Ho, E.C., Donaldson, M.E., and Saville, B.J. (2010) Detection of antisense RNA transcripts by strand-specific RT-PCR. Methods Mol Biol 630: 125-138.
31. Homann, O.R., Dea, J., Noble, S.M., and Johnson, A.D. (2009) A phenotypic profile of the Candida albicans regulatory network. PLoS Genet 5: e1000783.
32. Hubbard, M.J., Sullivan, P.A., and Shepherd, M.G. (1985) Morphological studies of N-acetylglucosamine induced germ tube formation by Candida albicans. Can J Microbiol 31: 696-701.
33. Ketting, R.F. (2011) The many faces of RNAi. Dev Cell 20: 148-161.
34. Lee, H.C., Li, L., Gu, W., Xue, Z., Crosthwaite, S.K., Pertsemlidis, A., etal. (2010) Diverse pathways generate microRNA-like RNAs and Dicer-independent small interfering RNAs in fungi. Mol Cell 38: 803-814.
35. Lee, K.L., Buckley, H.R., and Campbell, C.C. (1975) An amino acid liquid synthetic medium for the development of mycelial and yeast forms of Candida albicans. Sabouraudia 13: 148-153.
36. Liu, H., Kohler, J., and Fink, G.R. (1994) Suppression of hyphal formation in Candida albicans by mutation of a STE12 homolog. Science 266: 1723-1726.
37. Liu, J., Carmell, M.A., Rivas, F.V., Marsden, C.G., Thomson, J.M., Song, J.J., etal. (2004) Argonaute2 is the catalytic engine of mammalian RNAi. Science 305: 1437-1441.
38. Lo, H.J., Kohler, J.R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A., and Fink, G.R. (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
39. Lu, Y., Su, C., Wang, A., and Liu, H. (2011) Hyphal development in Candida albicans requires two temporally linked changes in promoter chromatin for initiation and maintenance. PLoS Biol 9: e1001105.
40. Murad, A.M., Leng, P., Straffon, M., Wishart, J., Macaskill, S., MacCallum, D., etal. (2001) NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J 20: 4742-4752.
41. Nakayama, H., Mio, T., Nagahashi, S., Kokado, M., Arisawa, M., and Aoki, Y. (2000) Tetracycline-regulatable system to tightly control gene expression in the pathogenic fungus Candida albicans. Infect Immun 68: 6712-6719.
42. Nobile, C.J., Fox, E.P., Nett, J.E., Sorrells, T.R., Mitrovich, Q.M., Hernday, A.D., etal. (2012) A recently evolved transcriptional network controls biofilm development in Candida albicans. Cell 148: 126-138.
43. 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.
44. Pierce, C.G., Uppuluri, P., Tristan, A.R., Wormley, F.L., Jr, Mowat, E., Ramage, G., and Lopez-Ribot, J.L. (2008) A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 3: 1494-1500.
45. Ramage, G., Saville, S.P., Thomas, D.P., and Lopez-Ribot, J.L. (2005) Candida biofilms: an update. Eukaryot Cell 4: 633-638.
46. Romano, N., and Macino, G. (1992) Quelling: transient inactivation of gene expression in Neurospora crassa by transformation with homologous sequences. Mol Microbiol 6: 3343-3353.
47. Saville, S.P., Lazzell, A.L., Monteagudo, C., and Lopez-Ribot, J.L. (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., Hogues, H., Askew, C., Tebbji, F., van Het Hoog, M., Lavoie, H., etal. (2010) Experimental annotation of the human pathogen Candida albicans coding and noncoding transcribed regions using high-resolution tiling arrays. Genome Biol 11: R71.
49. Skrzypek, M.S., Arnaud, M.B., Costanzo, M.C., Inglis, D.O., Shah, P., Binkley, G., etal. (2010) New tools at the Candida Genome Database: biochemical pathways and full-text literature search. Nucleic Acids Res 38: D428-D432.
50. Staab, J.F., White, T.C., and Marr, K.A. (2011) Hairpin dsRNA does not trigger RNA interference in Candida albicans cells. Yeast 28: 1-8.
51. Stoldt, V.R., Sonneborn, A., Leuker, C.E., and Ernst, J.F. (1997) Efg1p, an essential regulator of morphogenesis of the human pathogen Candida albicans, is a member of a conserved class of bHLH proteins regulating morphogenetic processes in fungi. EMBO J 16: 1982-1991.
52. Sudbery, P.E. (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9: 737-748.
53. Tisseur, M., Kwapisz, M., and Morillon, A. (2011) Pervasive transcription - lessons from yeast. Biochimie 93: 1889-1896.
54. Tomari, Y., and Zamore, P.D. (2005) Perspective: machines for RNAi. Genes Dev 19: 517-529.
55. Tuch, B.B., Mitrovich, Q.M., Homann, O.R., Hernday, A.D., Monighetti, C.K., De La Vega, F.M., and Johnson, A.D. (2010) The transcriptomes of two heritable cell types illuminate the circuit governing their differentiation. PLoS Genet 6: e1001070.
56. Uhl, M.A., and Johnson, A.D. (2001) Development of Streptococcus thermophilus lacZ as a reporter gene for Candida albicans. Microbiology 147: 1189-1195.
57. Viudes, A., Peman, J., Canton, E., Ubeda, P., Lopez-Ribot, J.L., and Gobernado, M. (2002) Candidemia at a tertiary-care hospital: epidemiology, treatment, clinical outcome and risk factors for death. Eur J Clin Microbiol Infect Dis 21: 767-774.
58. Wey, S.B., Mori, M., Pfaller, M.A., Woolson, R.F., and Wenzel, R.P. (1988) Hospital-acquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med 148: 2642-2645.
59. Wilusz, C.J., and Wilusz, J. (2004) Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet 20: 491-497.