Heterogeneous expression of the virulence-related adhesin epa1 between individual cells and strains of the pathogen candida Glabrata

Eukaryotic Cell

Volumn 11, Issue 2, 2012, Pages 141-150

  Halliwell, Samantha C ^a   Smith, Matthew C A ^a   Muston, Philippa ^a   Holland, Sara L ^a   Avery, Simon V ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EPITHELIAL ADHESIN 1, CANDIDA GLABRATA; FUNGAL PROTEIN; GLYCOSYLPHOSPHATIDYLINOSITOL; LECTIN;

ARTICLE; CANDIDA GLABRATA; CELL ADHESION; EPITHELIUM CELL; FLUORESCENCE MICROSCOPY; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM; PATHOGENICITY; VIRULENCE;

CANDIDA GLABRATA; CELL ADHESION; EPITHELIAL CELLS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; GLYCOSYLPHOSPHATIDYLINOSITOLS; LECTINS; MICROSCOPY, FLUORESCENCE; VIRULENCE;

CANDIDA GLABRATA;

EID: 84863027436     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.05232-11     Document Type: Article

References (57)

1. Acar M, Mett JT, van Oudenaarden A. 2008. Stochastic switching as a survival strategy in fluctuating environments. Nat. Genet. 40:471-475.
2. Ausubel FM, et al. 2011. Current protocols in molecular biology. John Wiley & Sons, New York, NY.
3. Avery SV. 2006. Microbial cell individuality and the underlying sources of heterogeneity. Nat. Rev. Microbiol. 4:577-587.
4. Bairwa G, Kaur R. 2011. A novel role for a glycosylphosphatidylinositol-anchored aspartyl protease, CgYps1, in the regulation of pH homeostasis in Candida glabrata. Mol. Microbiol. 79:900-913.
5. Bayliss CD. 2009. Determinants of phase variation rate and the fitness implications of differing rates for bacterial pathogens and commensals. FEMS Microbiol. Rev. 33:504-520.
6. Biondo C, et al. 2005. Characterization of two novel cryptococcal man-noproteins recognized by immune sera. Infect. Immun. 73:7348-7355.
7. Blake WJ, et al. 2006. Phenotypic consequences of promoter-mediated transcriptional noise. Mol. Cell 24:853-865.
8. Castano I, et al. 2003. Tn7-based genome-wide random insertional mu-tagenesis of Candida glabrata. Genome Res. 13:905-915.
9. Castano I, et al. 2005. Telomere length control and transcriptional regulation of subtelomeric adhesins in Candida glabrata. Mol. Microbiol. 55:1246-1258.
10. Colman-Lerner A, et al. 2005. Regulated cell-to-cell variation in a cell-fate decision system. Nature 437:699-706.
11. Cormack BP, Ghori N, Falkow S. 1999. An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285:578-582.
12. de Groot PW, et al. 2008. The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell 7:1951-1964.
13. De Las Penas A, et al. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject toRAP1-andSIR-dependent transcriptional silencing. Genes Dev. 17:2245-2258.
14. Domergue R, et al. 2005. Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308:866-870.
15. Fidel PL, Jr, Vazquez JA, Sobel JD. 1999. Candida glabrata: review of epidemiology, pathogenesis, and clinical disease with comparison to C. albicans. Clin. Microbiol. Rev. 12:80-96.
16. Fraser HB, Hirsh AE, Giaever G, Kumm J, Eisen MB. 2004. Noise minimization in eukaryotic gene expression. PLoS Biol. 2:834-838.
17. Frieman MB, McCaffery JM, Cormack BP. 2002. Modular domain structure in the Candida glabrata adhesin Epa1p, a beta1,6 glucan-cross-linked cell wall protein. Mol. Microbiol. 46:479-492.
18. Geisel N, Vilar JM, Rubi JM. 2011. Optimal resting-growth strategies of microbial populations in fluctuating environments. PLoS One 6:e18622.
19. Gregori C, Schueller C, Schwarzmuller T, Ammerer G, Kuchler K. 2007. The high-osmolarity glycerol response pathway in the human fungal pathogen Candida glabrata strain ATCC 2001 lacksasignaling branch that operates in baker's yeast. Eukaryot. Cell 6:1635-1645.
20. Halme A, Bumgarner S, Styles C, Fink GR. 2004. Genetic and epigenetic regulation of the FLO gene family generates cell-surface variation in yeast. Cell 116:405-415.
21. Holland SL, Avery SV. 2009. Actin-mediated endocytosis limits intracel-lularCraccumulation andCrtoxicity during chromate stress. Toxicol. Sci. 111:437-446.
22. Horn DL, et al. 2009. Epidemiology and outcomes of candidemia in 2019 patients: data from the prospective antifungal therapy alliance registry. Clin. Infect. Dis. 48:1695-1703.
23. Kachouri-Lafond R, et al. 2009. Large telomerase RNA, telomere length heterogeneity and escape from senescence in Candida glabrata. FEBS Lett. 583:3605-3610.
24. Kaur R, Domergue R, Zupancic ML, Cormack BP. 2005. A yeast by any other name: Candida glabrata and its interaction with the host. Curr. Opin. Microbiol. 8:378-384.
25. Kaur R, Ma B, Cormack BP. 2007. A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 104:7628-7633.
26. Kumamoto CA, Pierce JV. 2011. Immunosensing during colonization by Candida albicans: does it take a village to colonize the intestine? Trends Microbiol. 19:263-267.
27. Lewis K. 2010. Persister cells. Annu. Rev. Microbiol. 64:357-372.
28. Luo G, Samaranayake LP. 2002. Candida glabrata, an emerging fungal pathogen, exhibits superior relative cell surface hydrophobicity and adhesion to denture acrylic surfaces compared with Candida albicans. APMIS 110:601-610.
29. Martin SW, Konopka JB. 2004. Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryot. Cell 3:675-684.
30. Mateus C, Avery SV. 2000. Destabilized green fluorescent protein for monitoring dynamic changes in yeast gene expression with flow cytometry. Yeast 16:1313-1323.
31. Mishra S, Joshi PG. 2007. Lipid raft heterogeneity: an enigma. J. Neuro-chem 103(Suppl 1):135-142.
32. Muller H, et al. 2009. Genomic polymorphism in the population of Candida glabrata: gene copy-number variation and chromosomal translocations. Fungal Genet. Biol. 46:264-276.
33. Mundy RD, Cormack B. 2009. Expression of Candida glabrata adhesins after exposure to chemical preservatives. J. Infect. Dis. 199:1891-1898.
34. Newman JR, et al. 2006. Single-cell proteomic analysis of S. cerevisiae reveals the architecture of biological noise. Nature 441:840-846.
35. Payne T. 2007. Protein secretion in Saccharomyces cerevisiae. Ph.D. thesis. University of Nottingham, Nottingham, United Kingdom.
36. Pike LJ. 2004. Lipid rafts: heterogeneity on the high seas. Biochem. J. 378:281-292.
37. Polakova S, et al. 2009. Formation of new chromosomes as a virulence mechanism in yeast Candida glabrata. Proc. Natl. Acad. Sci. U. S. A. 106: 2688-2693.
38. Raisner RM, Madhani HD. 2008. Genomewide screen for negative regulators of sirtuin activity in Saccharomyces cerevisiae reveals 40 loci and links to metabolism. Genetics 179:1933-1944.
39. Ramirez-Zavaleta CY, Salas-Delgado GE, De Las Penas A, Castano I. 2010. Subtelomeric silencing of the MTL3 locus of Candida glabrata requires yKu70, yKu80, and Rif1 proteins. Eukaryot. Cell 9:1602-1611.
40. Raser JM, O'Shea EK. 2004. Control of stochasticity in eukaryotic gene expression. Science 304:1811-1814.
41. Renauld H, et al. 1993. Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev. 7:1133-1145.
42. Rosas-Hernandez LL, et al. 2008. Yku70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot. Cell 7:2168-2178.
43. Rusche LN, Kirchmaier AL, Rine J. 2003. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu. Rev. Biochem. 72:481-516.
44. Scherf A, Lopez-Rubio JJ, Riviere L. 2008. Antigenic variation in Plasmodium falciparum. Annu. Rev. Microbiol. 62:445-470.
45. Serio TR, Lindquist SL. 1999. PSI+: an epigenetic modulator of translation termination efficiency. Annu. Rev. Cell Dev. Biol. 15:661-703.
46. Sherman D, et al. 2006. Genolevures complete genomes provide data and tools for comparative genomics of hemiascomycetous yeasts. Nucleic Acids Res. 34:D432-D435.
47. Smith MC, Sumner ER, Avery SV. 2007. Glutathione and Gts1p drive beneficial variability in the cadmium resistances of individual yeast cells. Mol. Microbiol. 66:699-712.
48. Snijder B, Pelkmans L. 2011. Origins of regulated cell-to-cell variability. Nat. Rev. Mol. Cell Biol. 12:119-125.
49. Steels H, James SA, Roberts IN, Stratford M. 2000. Sorbic acid resistance: the inoculum effect. Yeast 16:1173-1183.
50. Sumner ER, Avery AM, Houghton JE, Robins RA, Avery SV. 2003. Cell cycle- and age-dependent activation of Sod1p drives the formation of stress resistant cell subpopulations within clonal yeast cultures. Mol. Mi-crobiol. 50:857-870.
51. Talbert PB, Henikoff S. 2006. Spreading of silent chromatin: inaction at a distance. Nat. Rev. Genet. 7:793-803.
52. Thierry A, Bouchier C, Dujon B, Richard GF. 2008. Megasatellites: a peculiar class of giant minisatellites in genes involved in cell adhesion and pathogenicity in Candida glabrata. Nucleic Acids Res. 36:5970-5982.
53. Thierry A, Dujon B, Richard GF. 2010. Megasatellites: a new class of large tandem repeats discovered in the pathogenic yeast Candida glabrata. Cell. Mol. Life Sci. 67:671-676.
54. True HL, Berlin I, Lindquist SL. 2004. Epigenetic regulation of translation reveals hidden genetic variation to produce complex traits. Nature 431:184-187.
55. van Dyk D, Pretorius IS, Bauer FF. 2005. Mss11p is a central element of the regulatory network that controls FLO11 expression and invasive growth in Saccharomyces cerevisiae. Genetics 169:91-106.
56. Zheng W, Zhao HY, Mancera E, Steinmetz LM, Snyder M. 2010. Genetic analysis of variation in transcription factor binding in yeast. Nature 464:1187-1191.
57. Zupancic ML, et al. 2008. Glycan microarray analysis of Candida glabrata adhesin ligand specificity. Mol. Microbiol. 68:547-559.