The peptide-binding cavity is essential for ALS3-mediated adhesion of Candida albicans to human cells

Journal of Biological Chemistry

Volumn 289, Issue 26, 2014, Pages 18401-18412

  Lin, Jing ^a   Oh, Soon Hwan ^b   Jones, Rhian ^a   Garnett, James A ^a   Salgado, Paula S ^c   Rusnakova, Sophia ^a   Matthews, Steve J ^a   Hoyer, Lois L ^b   Cota, Ernesto ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CANDIDA; CELL MEMBRANES; ENDOTHELIAL CELLS; PEPTIDES; YEAST;

ADHESIVE PROPERTIES; CANDIDA ALBICANS; DELETION MUTANTS; EPITHELIAL CELLS; MOLECULAR MECHANISM; MUTANT PHENOTYPE; N-TERMINAL DOMAINS; UMBILICAL VEIN ENDOTHELIAL CELLS;

ADHESION;

ALS3 PROTEIN; CELL SURFACE PROTEIN; FUNGAL PROTEIN; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ALS3 GENE; AMINO TERMINAL SEQUENCE; ARTICLE; CANDIDA ALBICANS; CELL ADHESION; DELETION MUTANT; EPITHELIUM CELL; FUNGAL GENE; FUNGAL PHENOMENA AND FUNCTIONS; FUNGAL STRAIN; FUNGUS ADHESION; GENE LOCUS; GENETIC REGULATION; HUMAN; HUMAN CELL; LOSS OF FUNCTION MUTATION; MOUTH MUCOSA; NUCLEOTIDE SEQUENCE; PEPTIDE BINDING CAVITY; PHARYNGEAL EPITHELIAL CELL; PHENOTYPE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN STRUCTURE; SURFACE PROPERTY; UMBILICAL VEIN ENDOTHELIAL CELL;

ADHESION; AGGREGATION; ALS ADHESINS; CANDIDA ALBICANS; FUNCTIONAL AMYLOID; NUCLEAR MAGNETIC RESONANCE (NMR); PEPTIDE-BINDING CAVITY; PEPTIDE-BINDING PROTEIN; X-RAY CRYSTALLOGRAPHY;

CANDIDA ALBICANS; CANDIDIASIS; CRYSTALLOGRAPHY, X-RAY; ENDOTHELIAL CELLS; FUNGAL PROTEINS; HUMANS; MODELS, MOLECULAR; PROTEIN STRUCTURE, TERTIARY;

EID: 84903516002     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.547877     Document Type: Article

References (40)

1. Pfaller, M. A., and Diekema, D. J. (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163
2. Gendreau, L., and Loewy, Z. G. (2011) Epidemiology and etiology of denture stomatitis. J. Prosthodont. 20, 251-260
3. Sobel, J. D. (2007) Vulvovaginal candidosis. Lancet 369, 1961-1971
4. Thompson, G. R., 3rd, Patel, P. K., Kirkpatrick, W. R., Westbrook, S. D., Berg, D., Erlandsen, J., Redding, S. W., and Patterson, T. F. (2010) Oropharyngeal candidiasis in the era of antiretroviral therapy. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 109, 488-495
5. Wisplinghoff, H., Bischoff, T., Tallent, S. M., Seifert, H., Wenzel, R. P., and Edmond, M. B. (2004) Nosocomial bloodstream infections in United States hospitals: analysis of 24, 179 cases from a prospective nationwide surveillance study. Clin. Infect. Dis. 39, 309-317
6. Tortorano, A. M., Peman, J., Bernhardt, H., Klingspor, L., Kibbler, C. C., Faure, O., Biraghi, E., Canton, E., Zimmermann, K., Seaton, S., and Grillot, R. (2004) Epidemiology of candidaemia in Europe: results of 28-month European Confederation of Medical Mycology (ECMM) hospital-based surveillance study. Eur. J. Clin. Microbiol. Infect. Dis. 23, 317-322
7. Chandra, J., Kuhn, D. M., Mukherjee, P. K., Hoyer, L. L., McCormick, T., and Ghannoum, M. A. (2001) Biofilm formation by the fungal pathogen Candida albicans: development, architecture, and drug resistance. J. Bacteriol. 183, 5385-5394
8. Phan, Q. T., Myers, C. L., Fu, Y., Sheppard, D. C., Yeaman, M. R., Welch, W. H., Ibrahim, A. S., Edwards, J. E., Jr., and Filler, S. G. (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 5, e64
9. Silverman, R. J., Nobbs, A. H., Vickerman, M. M., Barbour, M. E., and 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
10. Hoyer, L. L., Green, C. B., Oh, S. H., and Zhao, X. (2008) Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family: a sticky pursuit. Med. Mycol. 46, 1-15
11. Zhao, X., Oh, S. H., Cheng, G., Green, C. B., Nuessen, J. A., Yeater, K., Leng, R. P., Brown, A. J., and 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
12. Loza, L., Fu, Y., Ibrahim, A. S., Sheppard, D. C., Filler, S. G., and Edwards, J. E., Jr. (2004) Functional analysis of the Candida albicans ALS1 gene product. Yeast 21, 473-482
13. Zhao, X., Daniels, K. J., Oh, S. H., Green, C. B., Yeater, K. M., Soll, D. R., and Hoyer, L. L. (2006) Candida albicans Als3p is required for wild-type biofilm formation on silicone elastomer surfaces. Microbiology 152, 2287-2299
14. Salgado, P. S., Yan, R., Taylor, J. D., Burchell, L., Jones, R., Hoyer, L. L., Matthews, S. J., Simpson, P. J., and 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
15. Otoo, H. N., Lee, K. G., Qiu, W., and Lipke, P. N. (2008) Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 7, 776-782
16. Lipke, P. N., Garcia, M. C., Alsteens, D., Ramsook, C. B., Klotz, S. A., and Dufrêne, Y. F. (2012) Strengthening relationships: amyloids create adhesion nanodomains in yeasts. Trends Microbiol. 20, 59-65
17. Yan, R., Simpson, P. J., Matthews, S. J., and Cota, E. (2010) Backbone 1H, 15N, 13C and Ile, Leu, Val methyl chemical shift assignments for the 33.5 kDa N-terminal domain of Candida albicans Als1. Biomol. NMR Assign. 4, 187-190
18. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
19. Evans, P. R. (2011) An introduction to data reduction: space-group determination, scaling and intensity statistics. Acta Crystallogr. D Biol. Crystallogr. 67, 282-292
20. Winter, G., Lobley, C. M., and Prince, S. M. (2013) Decision making in xia2. Acta Crystallogr. D Biol. Crystallogr. 69, 1260-1273
21. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOLREP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
22. Emsley, P., and Cowtan, K. (2004) COOT: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
23. Painter, J., and Merritt, E. A. (2006) TLSMD web server for the generation of multi-group TLS models. J. Appl. Crystallogr. 39, 109-111
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
25. Zwart, P. H., Grosse-Kunstleve, R. W., and Adams, P. D. (2005) Xtriage and Fest: automatic assessment of x-ray data and substructure structure factor estimation. CCP4 Newsl. 43, Contribution 7
26. Coleman, D. A., Oh, S. H., Zhao, X., Zhao, H., Hutchins, J. T., Vernachio, J. H., Patti, J. M., and 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
27. Oh, S. H., Cheng, G., Nuessen, J. A., Jajko, R., Yeater, K. M., Zhao, X., Pujol, C., Soll, D. R., and Hoyer, L. L. (2005) Functional specificity of Candida albicans Als3p proteins and clade specificity of ALS3 alleles discriminated by the number of copies of the tandem repeat sequence in the central domain. Microbiology 151, 673-681
28. Fernandez-Escamilla, A. M., Rousseau, F., Schymkowitz, J., and Serrano, L. (2004) Prediction of sequence-dependent and mutational effects on the aggregation of peptides and proteins. Nat. Biotechnol. 22, 1302-1306
29. Holm, L., Kaariainen, S., Wilton, C., and Plewczynski, D. (2006) Using Dali for structural comparison of proteins. Curr. Protoc. Bioinformatics, Chapter 5, Unit 5.5
30. Garcia, M. C., Lee, J. T., Ramsook, C. B., Alsteens, D., Dufrêne, Y. F., and Lipke, P. N. (2011) A role for amyloid in cell aggregation and biofilm formation. PloS One 6, e17632
31. Porta, A., Ramon, A. M., and Fonzi, W. A. (1999) PRR1, a homolog of Aspergillus nidulans palF, controls pH-dependent gene expression and filamentation in Candida albicans. J. Bacteriol. 181, 7516-7523
32. Sheppard, D. C., Yeaman, M. R., Welch, W. H., Phan, Q. T., Fu, Y., Ibrahim, A. S., Filler, S. G., Zhang, M., Waring, A. J., and Edwards, J. E., Jr. (2004) Functional and structural diversity in the Als protein family of Candida albicans. J. Biol. Chem. 279, 30480-30489
33. Almeida, R. S., Brunke, S., Albrecht, A., Thewes, S., Laue, M., Edwards, J. E., Filler, S. G., and Hube, B. (2008) The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 4, e1000217
34. Gaur, N. K., and Klotz, S. A. (2004) Accessibility of the peptide backbone of protein ligands is a key specificity determinant in Candida albicans SRS adherence. Microbiology 150, 277-284
35. Gaur, N. K., Smith, R. L., and Klotz, S. A. (2002) Candida albicans and Saccharomyces cerevisiae expressing ALA1/ALS5 adhere to accessible threonine, serine, or alanine patches. Cell Commun. Adhes. 9, 45-57
36. Liu, Y., Mittal, R., Solis, N. V., Prasadarao, N. V., and Filler, S. G. (2011) Mechanisms of Candida albicans trafficking to the brain. PLoS Pathog. 7, e1002305
37. Zhu, W., Phan, Q. T., Boontheung, P., Solis, N. V., Loo, J. A., and Filler, S. G. (2012) EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proc. Natl. Acad. Sci. U. S. A. 109, 14194-14199
38. Coleman, D. A., Oh, S. H., Manfra-Maretta, S. L., and Hoyer, L. L. (2012) A monoclonal antibody specific for Candida albicans Als4 demonstrates overlapping localization of Als family proteins on the fungal cell surface and highlights differences between Als localization in vitro and in vivo. FEMS Immunol. Med. Microbiol. 64, 321-333
39. Zhao, X., Oh, S. H., Coleman, D. A., and Hoyer, L. L. (2011) ALS51, a newly discovered gene in the Candida albicans ALS family, created by intergenic recombination: analysis of the gene and protein, and implications for evolution of microbial gene families. FEMS Immunol. Med. Microbiol. 61, 245-257
40. Davis, I. W., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2004) MOLPROBITY: structure validation and all-atom contact analysis for nucleic acids and their complexes. Nucleic Acids Res. 32, W615-W619