Structural Hot Spots Determine Functional Diversity of the Candida glabrata Epithelial Adhesin Family

Journal of Biological Chemistry

Volumn 290, Issue 32, 2015, Pages 19597-19613

  Diderrich, Rike ^a   Kock, Michael ^a   Maestre Reyna, Manuel ^a   Keller, Petra ^b   Steuber, Holger ^a   Rupp, Steffen ^b,c   Essen, Lars Oliver ^a   Mösch, Hans Ulrich ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b FRAUNHOFER INSTITUTE FOR INTERFACIAL ENGINEERING AND BIOTECHNOLOGY IGB   (Germany)

^c UNIVERSITY OF STUTTGART   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; LIGANDS; PROTEINS; YEAST;

CELL WALL PROTEINS; EPITHELIAL CELL ADHESION; FUNCTIONAL CLASSIFICATION; FUNCTIONAL DIVERSITY; PHYLOGENETIC RELATIONSHIPS; STRUCTURAL FEATURE; STRUCTURAL STUDIES; STRUCTURE-FUNCTION RELATIONSHIP;

CANDIDA;

ADHESIN; EPITHELIAL ADHESIN; GALACTOSIDE; PROTEIN EPA1A; PROTEIN EPA6A; PROTEIN EPA7A; PROTEIN EPAA; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; FUNGAL PROTEIN; LECTIN; POLYSACCHARIDE; PROTEIN BINDING; RECOMBINANT PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CANDIDA GLABRATA; CONTROLLED STUDY; HOST PATHOGEN INTERACTION; HUMAN; HUMAN CELL; LIGAND BINDING; MICROBIAL ADHESION; MICROBIAL DIVERSITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; STRUCTURE ACTIVITY RELATION; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; EVOLUTION; GENE EXPRESSION; GENETIC VARIABILITY; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT; X RAY CRYSTALLOGRAPHY;

CANDIDA GLABRATA;

AMINO ACID SEQUENCE; BINDING SITES; BIOLOGICAL EVOLUTION; CANDIDA GLABRATA; CELL ADHESION MOLECULES; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; FUNGAL PROTEINS; GENE EXPRESSION; GENETIC VARIATION; LECTINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYSACCHARIDES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 84939159972     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.655654     Document Type: Article

References (54)

1. Castano, I., De Las Penas, A., and Cormack, B. P. (2006) in Molecular Principles of Fungal Pathogenesis (Heitman, J., Filler, S. G., Edwards, J. E., Jr., and Mitchell, A. P., eds) pp. 163-175, American Society for Microbiology, Washington, D. C.
2. Perlroth, J., Choi, B., and Spellberg, B. (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med. Mycol. 45, 321-346
3. Pfaller, M. A., and Diekema, D. J. (2007) Epidemiology of invasive candidiasis: a persistent public health problem. Clin. Microbiol. Rev. 20, 133-163
4. Borg-von Zepelin, M., Kunz, L., Rüchel, R., Reichard, U., Weig, M., and Gross, U. (2007) Epidemiology and antifungal susceptibilities of Candida spp. to six antifungal agents: results from a surveillance study on fungaemia in Germany from July 2004 to August 2005. J. Antimicrob. Chemother. 60, 424-428
5. de Groot, P. W., Bader, O., de Boer, A. D., Weig, M., and Chauhan, N. (2013) Adhesins in human fungal pathogens: glue with plenty of stick. Eukaryot. Cell 12, 470-481
6. Verstrepen, K. J., Reynolds, T. B., and Fink, G. R. (2004) Origins of variation in the fungal cell surface. Nat. Rev. Microbiol. 2, 533-540
7. Frieman, M. B., McCaffery, J. M., and Cormack, B. P. (2002) Modular domain structure in the Candida glabrata adhesin Epa1p, a β1,6-glucan cross-linked cell wall protein. Mol. Microbiol. 46, 479-492
8. Dranginis, A. M., Rauceo, J. M., Coronado, J. E., and Lipke, P. N. (2007) A biochemical guide to yeast adhesins: glycoproteins for social and antisocial occasions. Microbiol. Mol. Biol. Rev. 71, 282-294
9. 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
10. Liu, Y., and Filler, S. G. (2011) Candida albicans Als3, a multifunctional adhesin and invasin. Eukaryot. Cell 10, 168-173
11. Cormack, B. P., Ghori, N., and Falkow, S. (1999) An adhesin of the yeast pathogen Candida glabrata mediating adherence to human epithelial cells. Science 285, 578-582
12. Zupancic, M. L., Frieman, M., Smith, D., Alvarez, R. A., Cummings, R. D., and Cormack, B. P. (2008) Glycan microarray analysis of Candida glabrata adhesin ligand specificity. Mol. Microbiol. 68, 547-559
13. 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
14. Maestre-Reyna, M., Diderrich, R., Veelders, M. S., Eulenburg, G., Kalugin, V., Brückner, S., Keller, P., Rupp, S., Mösch, H.-U., and Essen, L.-O. (2012) Structural basis for promiscuity and specificity during Candida glabrata invasion of host epithelia. Proc. Natl. Acad. Sci. U.S.A. 109, 16864-16869
15. Butler, G., Rasmussen, M. D., Lin, M. F., Santos, M. A., Sakthikumar, S., Munro, C. A., Rheinbay, E., Grabherr, M., Forche, A., Reedy, J. L., Agrafioti, I., Arnaud, M. B., Bates, S., Brown, A. J., Brunke, S., et al. (2009) Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature 459, 657-662
16. Desai, C., Mavrianos, J., and Chauhan, N. (2011) Candida glabrata Pwp7p and Aed1p are required for adherence to human endothelial cells. FEMS Yeast Res. 11, 595-601
17. Kaur, R., Domergue, R., Zupancic, M. L., and Cormack, B. P. (2005) A yeast by any other name: Candida glabrata and its interaction with the host. Curr. Opin. Microbiol. 8, 378-384
18. de Groot, P. W., Kraneveld, E. A., Yin, Q. Y., Dekker, H. L., Gross, U., Crielaard, W., de Koster, C. G., Bader, O., Klis, F. M., and Weig, M. (2008) The cell wall of the human pathogen Candida glabrata: differential incorporation of novel adhesin-like wall proteins. Eukaryot. Cell 7, 1951-1964
19. Gabaldón, T., Martin, T., Marcet-Houben, M., Durrens, P., Bolotin-Fukuhara, M., Lespinet, O., Arnaise, S., Boisnard, S., Aguileta, G., Atanasova, R., Bouchier, C., Couloux, A., Creno, S., Almeida Cruz, J., Devillers, H., et al. (2013) Comparative genomics of emerging pathogens in the Candida glabrata clade. BMC Genomics 14, 623
20. Domergue, R., Castaño, I., De Las Peñas, A., Zupancic, M., Lockatell, V., Hebel, J. R., Johnson, D., and Cormack, B. P. (2005) Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 308, 866-870
21. de Groot, P. W., and Klis, F. M. (2008) The conserved PA14 domain of cell wall-associated fungal adhesins governs their glycan-binding specificity. Mol. Microbiol. 68, 535-537
22. Rigden, D. J., Mello, L. V., and Galperin, M. Y. (2004) The PA14 domain, a conserved all-β domain in bacterial toxins, enzymes, adhesins, and signaling molecules. Trends Biochem. Sci. 29, 335-339
23. Veelders, M., Brückner, S., Ott, D., Unverzagt, C., Mösch, H.-U., and Essen, L.-O. (2010) Structural basis of flocculin-mediated social behavior in yeast. Proc. Natl. Acad. Sci. U.S.A. 107, 22511-22516
24. Ielasi, F. S., Decanniere, K., and Willaert, R. G. (2012) The epithelial adhesin 1 (Epa1p) from the human-pathogenic yeast Candida glabrata: structural and functional study of the carbohydrate-binding domain. Acta Crystallogr. D Biol. Crystallogr. 68, 210-217
25. Guthrie, C., and Fink, G. R. (eds) (1991) Guide to Yeast Genetics and Molecular Biology, Vol. 194, pp. 1-863, Academic Press, San Diego
26. McCoy, A. J. (2007) Solving structures of protein complexes by molecular replacement with Phaser. Acta Crystallogr. D Biol. Crystallogr. 63, 32-41
27. Kabsch, W. (2010) Integration, scaling, space-group assignment and post-refinement. Acta Crystallogr. D Biol. Crystallogr. 66, 133-144
28. Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C., et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
29. Collaborative Computational Project No. 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50, 760-763
30. Murshudov, G. N., Skubák, P., Lebedev, A. A., Pannu, N. S., Steiner, R. A., Nicholls, R. A., Winn, M. D., Long, F., and Vagin, A. A. (2011) REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367
31. Emsley, P., and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132
32. Heinig, M., and Frishman, D. (2004) STRIDE: a web server for secondary structure assignment from known atomic coordinates of proteins. Nucleic Acids Res. 32, W500-W502
33. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675
34. Dieterich, C., Schandar, M., Noll, M., Johannes, F. J., Brunner, H., Graeve, T., and Rupp, S. (2002) In vitro reconstructed human epithelia reveal contributions of Candida albicans EFG1 and CPH1 to adhesion and invasion. Microbiology 148, 497-506
35. Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. (1998) Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. U.S.A. 95, 14863-14868
36. de Hoon, M. J., Imoto, S., Nolan, J., and Miyano, S. (2004) Open source clustering software. Bioinformatics 20, 1453-1454
37. Saldanha, A. J. (2004) Java Treeview-extensible visualization of microarray data. Bioinformatics 20, 3246-3248
38. DeLano, W. L. (2002) The PyMOL Molecular Graphics System, Version 1.4.1, DeLano Scientific LLC, San Carlos, CA
39. Eswar, N., Webb, B., Marti-Renom, M. A., Madhusudhan, M. S., Eramian, D., Shen, M. Y., Pieper, U., and Sali, A. (2006) Comparative protein structure modeling using Modeller. Curr. Protoc. Bioinformatics Chap. 5, Unit 5.6, 10.1002/0471250953.bi0506s15
40. Inglis, D. O., Arnaud, M. B., Binkley, J., Shah, P., Skrzypek, M. S., Wymore, F., Binkley, G., Miyasato, S. R., Simison, M., and Sherlock, G. (2012) The Candida genome database incorporates multiple Candida species: multispecies search and analysis tools with curated gene and protein information for Candida albicans and Candida glabrata. Nucleic Acids Res. 40, D667-D674
41. Landau, M., Mayrose, I., Rosenberg, Y., Glaser, F., Martz, E., Pupko, T., and Ben-Tal, N. (2005) ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33, W299-W302
42. Celniker, G., Nimrod, G., Ashkenazy, H., Glaser, F., Martz, E., Mayrose, I., Pupko, T., and Ben-Tal, N. (2013) ConSurf: using evolutionary data to raise testable hypotheses about protein function. Isr. J. Chem. 53, 199-206
43. Notredame, C., Higgins, D. G., and Heringa, J. (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 302, 205-217
44. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis, version 6.0. Mol. Biol. Evol. 30, 2725-2729
45. Sim, L., Groes, M., Olesen, K., and Henriksen, A. (2013) Structural and biochemical characterization of the N-terminal domain of flocculin Lg-Flo1p from Saccharomyces pastorianus reveals a unique specificity for phosphorylated mannose. FEBS J. 280, 1073-1083
46. Bolotin-Fukuhara, M., and Fairhead, C. (2014) Candida glabrata: a deadly companion? Yeast 31, 279-288
47. Geissner, A., Anish, C., and Seeberger, P. H. (2014) Glycan arrays as tools for infectious disease research. Curr. Opin. Chem. Biol. 18, 38-45
48. Gallegos-García, V., Pan, S. J., Juárez-Cepeda, J., Ramírez-Zavaleta, C. Y., Martin-del-Campo, M. B., Martínez-Jiménez, V., Castaño, I., Cormack, B., and De Las Peñas, A. (2012) A novel downstream regulatory element cooperates with the silencing machinery to repress EPA1 expression in Candida glabrata. Genetics 190, 1285-1297
49. Halliwell, S. C., Smith, M. C., Muston, P., Holland, S. L., and Avery, S. V. (2012) Heterogeneous expression of the virulence-related adhesin Epa1 between individual cells and strains of the pathogen Candida glabrata. Eukaryot. Cell 11, 141-150
50. Brown, G. D., Denning, D. W., and Levitz, S. M. (2012) Tackling human fungal infections. Science 336, 647
51. Wittmann, V., and Pieters, R. J. (2013) Bridging lectin binding sites by multivalent carbohydrates. Chem. Soc. Rev. 42, 4492-4503
52. O'Sullivan, O., Suhre, K., Abergel, C., Higgins, D. G., and Notredame, C. (2004) 3DCoffee: combining protein sequences and structures within multiple sequence alignments. J. Mol. Biol. 340, 385-395
53. Glaser, F., Pupko, T., Paz, I., Bell, R. E., Bechor-Shental, D., Martz, E., and Ben-Tal, N. (2003) ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinformatics 19, 163-164
54. Gietz, R. D., and Sugino, A. (1988) New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534