Candida albicans CUG mistranslation is a mechanism to create cell surface variation

mBio

Volumn 4, Issue 4, 2013, Pages

  Miranda, Isabel ^a   Silva Dias, Ana ^a   Rocha, Rita ^a   Teixeira Santos, Rita ^a   Coelho, Carolina ^b   Gonçalves, Teresa ^b   Santos, Manuel A S ^c   Pina Vaz, Cidália ^a,d   Solis, Norma V ^e   Filler, Scott G ^e,f   Rodrigues, Acácio G ^a,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSITY OF AVEIRO   (Portugal)

^d HOSPITAL DE SÃO JOÃO   (Portugal)

^e HARBOR UCLA MEDICAL CENTER   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; BETA GLUCAN; INVASIN; LEUCINE; MEMBRANE PROTEIN; SERINE;

ANIMAL CELL; ARTICLE; CANDIDA ALBICANS; CELL ADHESION; CELL SURFACE; CELL WALL; CODON; CONTROLLED STUDY; FLOCCULATION; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS HOST INTERACTION; HOST; HOST PATHOGEN INTERACTION; HYDROPHOBICITY; IMMUNE SYSTEM; MOLECULAR EVOLUTION; NONHUMAN; PHAGOCYTOSIS; PHENOTYPE; PRIORITY JOURNAL; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; STRAIN DIFFERENCE; SURFACE PROPERTY; WILD TYPE;

CANDIDA ALBICANS; FUNGI; MURINAE; SACCHAROMYCES CEREVISIAE;

EID: 84883429281     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00285-13     Document Type: Article

References (51)

1. Stringer JR, Keely SP. 2001. Genetics of surface antigen expression in Pneumocystis carinii. Infect. Immun. 69:627-639.
2. Deitsch KW. 2005. Malaria virulence genes controlling expression through chromatin modification. Cell 121:1-2.
3. Rando OJ, Verstrepen KJ. 2007. Timescales of genetic and epigenetic inheritance. Cell 128:655-668.
4. Verstrepen KJ, Reynolds TB, Fink GR. 2004. Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2:533-540.
5. Verstrepen KJ, Jansen A, Lewitter F, Fink GR. 2005. Intragenic tandem repeats generate functional variability. Nat. Genet. 37:986-990.
6. 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.
7. Krinos CM, Coyne MJ, Weinacht KG, Tzianabos AO, Kasper DL, Comstock LE. 2001. Extensive surface diversity of a commensal microorganism by multiple DNA inversions. Nature 414:555-558.
8. De Las Peñas A, Pan SJ, Castaño I, Alder J, Cregg R, Cormack BP. 2003. Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1-and SIR-dependent transcriptional silencing. Genes Dev. 17:2245-2258.
9. Boothroyd CE, Dreesen O, Leonova T, Ly KI, Figueiredo LM, Cross GA, Papavasiliou FN. 2009. A yeast-endonuclease-generated DNA break induces antigenic switching in Trypanosoma brucei. Nature 459:278-281.
10. Sundstrom P. 2002. Adhesion in Candida spp. Cell. Microbiol. 4:461-469.
11. Nobile CJ, Andes DR, Nett JE, Smith FJ, Yue F, Phan QT, Edwards JE, Filler SG, Mitchell AP. 2006. Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog. 2:e63. doi: 10.1371/journal.ppat.0020063.
12. Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH, Ibrahim AS, Edwards JE, Jr, Filler SG. 2007. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5:e64. doi: 10.1371/journal.pbio.0050064.
13. Almeida RS, Brunke S, Albrecht A, Thewes S, Laue M, Edwards JE, Filler SG, Hube B. 2008. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4:e1000217. doi: 10.1371/journal.ppat.1000217.
14. Santos MA, Gomes AC, Santos MC, Carreto LC, Moura GR. 2011. The genetic code of the fungal CTG clade. C. R. Biol. 334:607-611.
15. Gomes AC, Miranda I, Silva RM, Moura GR, Thomas B, Akoulitchev A, Santos MA. 2007. A genetic code alteration generates a proteome of high diversity in the human pathogen Candida albicans. Genome Biol. 8:R206. doi: 10.1186/gb-2007-8-10-r206.
16. Santos MA, Keith G, Tuite MF. 1993. Non-standard translational events in Candida albicans mediated by an unusual seryl-tRNA with a 5=-CAG-3 (leucine) anticodon. EMBO J. 12:607-616.
17. Rocha R, Pereira PJ, Santos MA, Macedo-Ribeiro S. 2011. Unveiling the structural basis for translational ambiguity tolerance in a human fungal pathogen. Proc. Natl. Acad. Sci. U. S. A. 108:14091-14096.
18. Miranda I, Rocha R, Santos MC, Mateus DD, Moura GR, Carreto L, Santos MA. 2007. A genetic code alteration is a phenotype diversity generator in the human pathogen Candida albicans. PLoS One 2:e996. doi: 10.1371/journal.pone.0000996.
19. Silva-Dias A, Miranda IM, Rocha R, Monteiro-Soares M, Salvador A, Rodrigues AG, Pina-Vaz C. 2012. A novel flow cytometric protocol for assessment of yeast cell adhesion. Cytometry A 81:265-270.
20. Sheppard DC, Yeaman MR, Welch WH, Phan QT, Fu Y, Ibrahim AS, Filler SG, Zhang M, Waring AJ, Edwards JE, Jr. 2004. Functional and structural diversity in the Als protein family of Candida albicans. J. Biol. Chem. 279:30480-30489.
21. Fu Y, Ibrahim AS, Sheppard DC, Chen YC, French SW, Cutler JE, Filler SG, Edwards JE, Jr. 2002. Candida albicans. Als1p: an adhesin that is a downstream effector of the EFG1 filamentation pathway. Mol. Microbiol. 44:61-72.
22. Rauceo JM, Gaur NK, Lee KG, Edwards JE, Klotz SA, Lipke PN. 2004. Global cell surface conformational shift mediated by a Candida albicans adhesin. Infect. Immun. 72:4948-4955.
23. Rosenberg M, Gutnick D, Rosenberg E. 1980. Adherence of bacteria to hydrocarbons: a simple method for measuring cell-surface hydrophobicity. FEMS Microbiol. Lett. 9:29-33.
24. Ramsook CB, Tan C, Garcia MC, Fung R, Soybelman G, Henry R, Litewka A, O'Meally S, Otoo HN, Khalaf RA, Dranginis AM, Gaur NK, Klotz SA, Rauceo JM, Jue CK, Lipke PN. 2010. Yeast cell adhesion molecules have functional amyloid-forming sequences. Eukaryot. Cell 9:393-404.
25. Salgado PS, Yan R, Taylor JD, Burchell L, Jones R, Hoyer LL, Matthews SJ, Simpson PJ, Cota E. 2011. Structural basis for the broad specificity to host-cell ligands by the pathogenic fungus Candida albicans. Proc. Natl. Acad. Sci. U. S. A. 108:15775-15779.
26. Gow NA, Netea MG, Munro CA, Ferwerda G, Bates S, Mora-Montes HM, Walker L, Jansen T, Jacobs L, Tsoni V, Brown GD, Odds FC, Van der Meer JW, Brown AJ, Kullberg BJ. 2007. Immune recognition of Candida albicans beta-glucan by dectin-1. J. Infect. Dis. 196:1565-1571.
27. Rubin-Bejerano I, Abeijon C, Magnelli P, Grisafi P, Fink GR. 2007. Phagocytosis by human neutrophils is stimulated by a unique fungal cell wall component. Cell Host Microbe 2:55-67.
28. Galán-Díez M, Arana DM, Serrano-Gómez D, Kremer L, Casasnovas JM, Ortega M, Cuesta-Domínguez A, Corbí AL, Pla J, Fernández-Ruiz E. 2010. Candida albicans beta-glucan exposure is controlled by the fungal CEK1-mediated mitogen-activated protein kinase pathway that modulates immune responses triggered through dectin-1. Infect. Immun. 78: 1426-1436.
29. Gantner BN, Simmons RM, Underhill DM. 2005. Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24:1277-1286.
30. Martínez-Esparza M, Sarazin A, Poulain D, Jouault T. 2009. A method for examining glycans surface expression of yeasts by flow cytometry. Methods Mol. Biol. 470:85-94.
31. Berman J, Sudbery PE. 2002. Candida albicans: a molecular revolution built on lessons from budding yeast. Nat. Rev. Genet. 3:918-930.
32. Glee PM, Cutler JE, Benson EE, Bargatze RF, Hazen KC. 2001. Inhibition of hydrophobic protein-mediated Candida albicans attachment to endothelial cells during physiologic shear flow. Infect. Immun. 69: 2815-2820.
33. Li F, Palecek SP. 2008. Distinct domains of the Candida albicans adhesin Eap1p mediate cell-cell and cell-substrate interactions. Microbiology 154: 1193-1203.
34. Otoo HN, Lee KG, Qiu W, Lipke PN. 2008. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 7:776-782.
35. Alsteens D, Garcia MC, Lipke PN, Dufrêne YF. 2010. Force-induced formation and propagation of adhesion nanodomains in living fungal cells. Proc. Natl. Acad. Sci. U. S. A. 107:20744-20749.
36. Netea MG, Brown GD, Kullberg BJ, Gow NAR. 2008. An integrated model of the recognition of Candida albicans by the innate immune system. Nat. Rev. Microbiol. 6:67-78.
37. Lewis LE, Bain JM, Lowes C, Gillespie C, Rudkin FM, Gow NA, Erwig LP. 2012. Stage specific assessment of Candida albicans phagocytosis by macrophages identifies cell wall composition and morphogenesis as key determinants. PLoS Pathog. 8:e1002578. doi: 10.1371/ journal.ppat.1002578.
38. McKenzie CG, Koser U, Lewis LE, Bain JM, Mora-Montes HM, Barker RN, Gow NA, Erwig LP. 2010. Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect. Immun. 78:1650-1658.
39. Wheeler RT, Kombe D, Agarwala SD, Fink GR. 2008. Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog. 4:e1000227. doi: 10.1371/ journal.ppat.1000227.
40. Netzer N, Goodenbour JM, David A, Dittmar KA, Jones RB, Schneider JR, Boone D, Eves EM, Rosner MR, Gibbs JS, Embry A, Dolan B, Das S, Hickman HD, Berglund P, Bennink JR, Yewdell JW, Pan T. 2009. Innate immune and chemically triggered oxidative stress modifies translational fidelity. Nature 462:522-526.
41. Morley SJ, Willett M. 2009. Kinky binding and SECsy insertions. Mol. Cell 35:396-398.
42. Carlson BA, Yoo MH, Sano Y, Sengupta A, Kim JY, Irons R, Gladyshev VN, Hatfield DL, Park JM. 2009. Selenoproteins regulate macrophage invasiveness and extracellular matrix-related gene expression. BMC Immunol. 10:57. doi: 10.1186/1471-2172-10-57.
43. Ambrogelly A, Palioura S, Söll D. 2007. Natural expansion of the genetic code. Nat. Chem. Biol. 3:29-35.
44. Ribas de Pouplana L, Schimmel P. 2000. A view into the origin of life: aminoacyl-tRNA synthetases. Cell. Mol. Life Sci. 57:865-870.
45. Pezo V, Metzgar D, Hendrickson TL, Waas WF, Hazebrouck S, Döring V, Marlière P, Schimmel P, De Crécy-Lagard V. 2004. Artificially ambiguous genetic code confers growth yield advantage. Proc. Natl. Acad. Sci. U. S. A. 101:8593-8597.
46. Santos MA, Cheesman C, Costa V, Moradas-Ferreira P, Tuite MF. 1999. Selective advantages created by codon ambiguity allowed for the evolution of an alternative genetic code in Candida spp. Mol. Microbiol. 31: 937-947.
47. Bacher JM, Waas WF, Metzgar D, de Crécy-Lagard V, Schimmel P. 2007. Genetic code ambiguity confers a selective advantage on Acinetobacter baylyi. J. Bacteriol. 189:6494-6496.
48. Stothard P. 2000. The sequence manipulation suite: JavaScript programs for analyzing and formatting protein and DNA sequences. Biotechniques 28:-1102-1104.
49. Thompson JD, Higgins DG, Gibson TJ. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
50. Gouet P, Robert X, Courcelle E. 2003. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res. 31:3320-3323.
51. Fernández-Arenas E, Cabezón V, Bermejo C, Arroyo J, Nombela C, Diez-Orejas R, Gil C. 2007. Integrated proteomics and genomics strategies bring new insight into Candida albicans response upon macrophage interaction. Mol. Cell. Proteomics 6:460-478.