Candida albicans adhesin Als3p is dispensable for virulence in the mouse model of disseminated candidiasis

Microbiology

Volumn 157, Issue 6, 2011, Pages 1806-1815

  Cleary, Ian A ^a   Reinhard, Sara M ^a   Lindsay Miller, C ^a   Murdoch, Craig ^b   Thornhill, Martin H ^b   Lazzell, Anna L ^a   Monteagudo, Carlos ^c   Thomas, Derek P ^a,d   Saville, Stephen P ^a  

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

^b UNIVERSITY OF SHEFFIELD   (United Kingdom)

^c UNIVERSITY OF VALENCIA   (Spain)

^d GRAND VALLEY STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESIN; ALS3P PROTEIN; FUNGAL PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOFILM; CANDIDA ALBICANS; CELL WALL; CONTROLLED STUDY; FEMALE; FUNGAL CELL; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS HYPHAE; GENE DOSAGE; HUMAN; HUMAN CELL; IN VITRO STUDY; INVASIVE CANDIDIASIS; MICROVASCULAR ENDOTHELIAL CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; WILD TYPE; YEAST CELL;

ANIMALS; CANDIDA ALBICANS; CANDIDIASIS; CELL ADHESION; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FEMALE; FUNGAL PROTEINS; GENE DELETION; HUMANS; HYPHAE; MICE; MICE, INBRED BALB C; VIRULENCE;

CANDIDA ALBICANS; MURINAE;

EID: 79958179535     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.046326-0     Document Type: Article

References (51)

1. Ades, E. W., Candal, F. J., Swerlick, R. A., George, V. G., Summers, S., Bosse, D. C. & Lawley, T. J. (1992). HMEC-1: establishment of an immortalized human microvascular endothelial cell line. J Invest Dermatol 99, 683-690.
2. Almeida, R. S., Brunke, S., Albrecht, A., Thewes, S., Laue, M., Edwards, J. E., Filler, S. G. & Hube, B. (2008). The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 4, e1000217.
3. Argimón, S., Wishart, J. A., Leng, R., Macaskill, S., Mavor, A., Alexandris, T., Nicholls, S., Knight, A. W., Enjalbert, B. & other authors (2007). Developmental regulation of an adhesin gene during cellular morphogenesis in the fungal pathogen Candida albicans. Eukaryot Cell 6, 682-692.
4. Bassilana, M., Hopkins, J. & Arkowitz, R. A. (2005). Regulation of the Cdc42/Cdc24 GTPase module during Candida albicans hyphal growth. Eukaryot Cell 4, 588-603.
5. Bendel, C. M., Hess, D. J., Garni, R. M., Henry-Stanley, M. & 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.
6. Brand, A., MacCallum, D. M., Brown, A. J., Gow, N. A. & Odds, F. C. (2004). Ectopic expression of URA3 can influence the virulence phenotypes and proteome of Candida albicans but can be overcome by targeted reintegration of URA3 at the RPS10 locus. Eukaryot Cell 3, 900-909.
7. Braun, B. R. & Johnson, A. D. (1997). Control of filament formation in Candida albicans by the transcriptional repressor TUP1. Science 277, 105-109.
8. Braun, B. R., Head, W. S., Wang, M. X. & Johnson, A. D. (2000). Identification and characterization of TUP1-regulated genes in Candida albicans. Genetics 156, 31-44.
9. Chen, C.G., Yang, Y. L., Cheng, H. H., Su, C. L., Huang, S. F., Chen, C. T., Liu, Y. T., Su, I. J. & Lo, H. J. (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.
10. Church, G. M. & Gilbert, W. (1984). Genomic sequencing. Proc Natl Acad Sci U S A 81, 1991-1995.
11. Cleary, I. A., Mulabagal, P., Reinhard, S. M., Yadev, N. P., Murdoch, C., Thornhill, M. H., Lazzell, A. L., Monteagudo, C., Thomas, D. P. & Saville, S. P. (2010). Pseudohyphal regulation by the transcription factor Rfg1p in Candida albicans. Eukaryot Cell 9, 1363-1373.
12. Coleman, D. A., Oh, S. H., Zhao, X., Zhao, H., Hutchins, J. T., Vernachio, J. H., Patti, J. M. & Hoyer, L. L. (2009). Monoclonal antibodies specific for Candida albicans Als3 that immunolabel fungal cells in vitro and in vivo and block adhesion to host surfaces. J Microbiol Methods 78, 71-78.
13. Correia, A., Lermann, U., Teixeira, L., Cerca, F., Botelho, S., da Costa, R. M., Sampaio, P., Gärtner, F., Morschhäuser, J. & other authors (2010). Limited role of secreted aspartyl proteinases Sap1 to Sap6 in Candida albicans virulence and host immune response in murine hematogenously disseminated candidiasis. Infect Immun 78, 4839-4849.
14. Daniels, K. J., Srikantha, T., Lockhart, S. R., Pujol, C. & Soll, D. R. (2006). Opaque cells signal white cells to form biofilms in Candida albicans. EMBO J 25, 2240-2252.
15. Dwivedi, P., Thompson, A., Xie, Z., Kashleva, H., Ganguly, S., Mitchell, A. P. & Dongari-Bagtzoglou, A. (2011). Role of Bcr1-activated genes Hwp1 and Hyr1 in Candida albicans oral mucosal biofilms and neutrophil evasion. PLoS ONE 6, e16218.
16. Fiebig, E., Ley, K. & Arfors, K. E. (1991). Rapid leukocyte accumulation by "spontaneous" rolling and adhesion in the exteriorized rabbit mesentery. Int J Microcirc Clin Exp 10, 127-144.
17. Gillum, A. M., Tsay, E. Y. & Kirsch, D. R. (1984). Isolation of the Candida albicans gene for orotidine-59-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol Gen Genet 198, 179-182.
18. Green, C. B., Zhao, X., Yeater, K. M. & Hoyer, L. L. (2005). Construction and real-time RT-PCR validation of Candida albicans PALS-GFP reporter strains and their use in flow cytometry analysis of ALS gene expression in budding and filamenting cells. Microbiology 151, 1051-1060.
19. 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.
20. Grubb, S. E., Murdoch, C., Sudbery, P. E., Saville, S. P., Lopez-Ribot, J. L. & Thornhill, M. H. (2009). Adhesion of Candida albicans to endothelial cells under physiological conditions of flow. Infect Immun 77, 3872-3878.
21. Hoyer, L. L., Green, C. B., Oh, S. H. & Zhao, X. (2008). Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family-a sticky pursuit. Med Mycol 46, 1-15.
22. Köhler, G. A., White, T. C. & Agabian, N. (1997). Overexpression of a cloned IMP dehydrogenase gene of Candida albicans confers resistance to the specific inhibitor mycophenolic acid. J Bacteriol 179, 2331-2338.
23. Lo, H. J., Köhler, J. R., DiDomenico, B., Loebenberg, D., Cacciapuoti, A. & Fink, G. R. (1997). Nonfilamentous C. albicans mutants are avirulent. Cell 90, 939-949.
24. MacCallum, D. M. & Odds, F. C. (2005). Temporal events in the intravenous challenge model for experimental Candida albicans infections in female mice. Mycoses 48, 151-161.
25. McKenzie, C. G., Koser, U., Lewis, L. E., Bain, J. M., Mora-Montes, H. M., Barker, R. N., Gow, N. A. & Erwig, L. P. (2010). Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages. Infect Immun 78, 1650-1658.
26. Murad, A. M., Leng, P., Straffon, M., Wishart, J., Macaskill, S., MacCallum, D., Schnell, N., Talibi, D., Marechal, D. & other authors (2001). NRG1 represses yeast-hypha morphogenesis and hyphaspecific gene expression in Candida albicans. EMBO J 20, 4742-4752.
27. Nailis, H., Coenye, T., Van Nieuwerburgh, F., Deforce, D. & Nelis, H. J. (2006). Development and evaluation of different normalization strategies for gene expression studies in Candida albicans biofilms by real-time PCR. BMC Mol Biol 7, 25.
28. Nobile, C. J. & Mitchell, A. P. (2005). Regulation of cell-surface genes and biofilm formation by the C. albicans transcription factor Bcr1p. Curr Biol 15, 1150-1155.
29. Nobile, C. J., Andes, D. R., Nett, J. E., Smith, F. J., Yue, F., Phan, Q. T., Edwards, J. E., Filler, S. G. & Mitchell, A. P. (2006). Critical role of Bcr1-dependent adhesins in C. albicans biofilm formation in vitro and in vivo. PLoS Pathog 2, e63.
30. Nobile, C. J., Schneider, H. A., Nett, J. E., Sheppard, D. C., Filler, S. G., Andes, D. R. & Mitchell, A. P. (2008). Complementary adhesin function in C. albicans biofilm formation. Curr Biol 18, 1017-1024.
31. Otoo, H. N., Lee, K. G., Qiu, W. & Lipke, P. N. (2008). Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot Cell 7, 776-782.
32. Paget, M. S., Hintermann, G. & Smith, C. P. (1994). Construction and application of streptomycete promoter probe vectors which employ the Streptomyces glaucescens tyrosinase-encoding gene as reporter. Gene 146, 105-110.
33. Phan, Q. T., Myers, C. L., Fu, Y., Sheppard, D. C., Yeaman, M. R., Welch, W. H., Ibrahim, A. S., Edwards, J. E., Jr & Filler, S. G. (2007). Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5, e64.
34. Ramage, G., Saville, S. P., Thomas, D. P. & López-Ribot, J. L. (2005). Candida biofilms: an update. Eukaryot Cell 4, 633-638.
35. Reuss, O., Vik, A., Kolter, R. & Morschhäuser, J. (2004). The SAT1 flipper, an optimized tool for gene disruption in Candida albicans. Gene 341, 119-127.
36. Sahni, N., Yi, S., Daniels, K. J., Srikantha, T., Pujol, C. & Soll, D. R. (2009). Genes selectively up-regulated by pheromone in white cells are involved in biofilm formation in Candida albicans. PLoS Pathog 5, e1000601.
37. Sahni, N., Yi, S., Daniels, K. J., Huang, G., Srikantha, T. & Soll, D. R. (2010). Tec1 mediates the pheromone response of the white phenotype of Candida albicans: insights into the evolution of new signal transduction pathways. PLoS Biol 8, e1000363.
38. Saville, S. P., Lazzell, A. L., Monteagudo, C. & 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.
39. Silverman, R. J., Nobbs, A. H., Vickerman, M. M., Barbour, M. E. & Jenkinson, H. F. (2010). Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect Immun 78, 4644-4652.
40. Soll, D. R. (2008). Candida biofilms: is adhesion sexy? Curr Biol 18, R717-R720.
41. Spellberg, B., Johnston, D., Phan, Q. T., Edwards, J. E., Jr, French, S. W., Ibrahim, A. S. & Filler, S. G. (2003). Parenchymal organ, and not splenic, immunity correlates with host survival during disseminated candidiasis. Infect Immun 71, 5756-5764.
42. Stichternoth, C. & Ernst, J. F. (2009). Hypoxic adaptation by Efg1 regulates biofilm formation by Candida albicans. Appl Environ Microbiol 75, 3663-3672.
43. Stoldt, V. R., Sonneborn, A., Leuker, C. E. & 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.
44. Toyoda, M., Cho, T., Kaminishi, H., Sudoh, M. & Chibana, H. (2004). Transcriptional profiling of the early stages of germination in Candida albicans by real-time RT-PCR. FEMS Yeast Res 5, 287-296.
45. Tsai, N. Y., Laforce-Nesbitt, S. S., Tucker, R. & Bliss, J. M. (2011). A murine model for disseminated candidiasis in neonates. Pediatr Res 69, 189-193.
46. Uppuluri, P., Pierce, C. G., Thomas, D. P., Bubeck, S. S., Saville, S. P. & Lopez-Ribot, J. L. (2010). The transcriptional regulator Nrg1p controls Candida albicans biofilm formation and dispersion. Eukaryot Cell 9, 1531-1537.
47. Viudes, A., Pemán, J., Cantón, E., Ubeda, P., López-Ribot, J. L. & 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.
48. Wey, S. B., Mori, M., Pfaller, M. A., Woolson, R. F. & Wenzel, R. P. (1988). Hospital-acquired candidemia. The attributable mortality and excess length of stay. Arch Intern Med 148, 2642-2645.
49. Wu, W., Lockhart, S. R., Pujol, C., Srikantha, T. & Soll, D. R. (2007). Heterozygosity of genes on the sex chromosome regulates Candida albicans virulence. Mol Microbiol 64, 1587-1604.
50. Zhao, X., Oh, S. H., Cheng, G., Green, C. B., Nuessen, J. A., Yeater, K., Leng, R. P., Brown, A. J. & Hoyer, L. L. (2004). ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 150, 2415-2428.
51. Zhao, X., Daniels, K. J., Oh, S. H., Green, C. B., Yeater, K. M., Soll, D. R. & Hoyer, L. L. (2006). Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152, 2287-2299.