{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,9]],"date-time":"2026-10-09T16:06:51Z","timestamp":1791562011957,"version":"4.3.4"},"reference-count":73,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2020,7,18]],"date-time":"2020-07-18T00:00:00Z","timestamp":1595030400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"National Science Centre of Poland","award":["2016\/23\/B\/NZ6\/00089"],"award-info":[{"award-number":["2016\/23\/B\/NZ6\/00089"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Candida spp. yeast-like fungi are opportunistic pathogens in humans and have been recently found to release extracellular vesicles (EVs) that are involved in many vital biological processes in fungal cells. These include communication between microorganisms and host\u2013pathogen interactions during infection. The production of EVs and their content have been significantly characterized in the most common candidal species Candida albicans, including the identification of numerous virulence factors and cytoplasmic proteins in the EV cargo. We have here conducted the isolation and proteomic characterization of EVs produced by the clinically important non-albicans Candida species C. glabrata, C. tropicalis and C. parapsilosis. With the use of ultracentrifugation of the cell-free culture supernatant, the candidal EVs were collected and found to be a heterogeneous population of particles for each species with sizes ranging from 60\u2013280 nm. The proteinaceous contents of these vesicles were analyzed using LC-MS\/MS, with particular attention paid to surface-expressed proteins that would come into immediate and direct contact with host cells. We thereby identified 42 extracellular and surface-connected proteins from C. glabrata, 33 from C. parapsilosis, and 34 from C. tropicalis, including membrane-associated transporters, glycoproteins and enzymes involved in the organization of the fungal cell wall, as well as several cytoplasmic proteins, including alcohol dehydrogenase, enolase, glyceraldehyde-3-phosphate dehydrogenase, phosphoglycerate kinase and pyruvate kinase, for which the vesicular transport is a possible mechanism underlying their non-classical secretion.<\/jats:p>","DOI":"10.3390\/cells9071722","type":"journal-article","created":{"date-parts":[[2020,7,21]],"date-time":"2020-07-21T06:38:55Z","timestamp":1595313535000},"page":"1722","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":76,"title":["Characteristics of Extracellular Vesicles Released by the Pathogenic Yeast-Like Fungi Candida glabrata, Candida parapsilosis and Candida tropicalis"],"prefix":"10.3390","volume":"9","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6070-6919","authenticated-orcid":false,"given":"Justyna","family":"Karkowska-Kuleta","sequence":"first","affiliation":[{"name":"Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kamila","family":"Kulig","sequence":"additional","affiliation":[{"name":"Department of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387, Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9956-1593","authenticated-orcid":false,"given":"Elzbieta","family":"Karnas","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krak\u00f3w, Poland"},{"name":"Laboratory of Stem Cell Biotechnology, Malopolska Centre of Biotechnology, Jagiellonian University, Gronostajowa 7a, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6814-6127","authenticated-orcid":false,"given":"Ewa","family":"Zuba-Surma","sequence":"additional","affiliation":[{"name":"Department of Cell Biology, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Olga","family":"Woznicka","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1503-9533","authenticated-orcid":false,"given":"Elzbieta","family":"Pyza","sequence":"additional","affiliation":[{"name":"Department of Cell Biology and Imaging, Institute of Zoology and Biomedical Research, Jagiellonian University, Gronostajowa 9, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patryk","family":"Kuleta","sequence":"additional","affiliation":[{"name":"Department of Molecular Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Artur","family":"Osyczka","sequence":"additional","affiliation":[{"name":"Department of Molecular Biophysics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3225-7391","authenticated-orcid":false,"given":"Maria","family":"Rapala-Kozik","sequence":"additional","affiliation":[{"name":"Department of Comparative Biochemistry and Bioanalytics, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387 Krakow, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Andrzej","family":"Kozik","sequence":"additional","affiliation":[{"name":"Department of Analytical Biochemistry, Faculty of Biochemistry, Biophysics and Biotechnology, Jagiellonian University, Gronostajowa 7, 30-387, Krak\u00f3w, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,7,18]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"i4","DOI":"10.1093\/jac\/dkx444","article-title":"Changes in the epidemiological landscape of invasive candidiasis","volume":"73","author":"Lamoth","year":"2018","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1007\/s10123-018-0014-1","article-title":"The continuous changes in the aetiology and epidemiology of invasive candidiasis: From familiar Candida albicans to multiresistant Candida auris","volume":"21","author":"Mateo","year":"2018","journal-title":"Int. Microbiol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1016\/j.ajic.2018.05.015","article-title":"Factors and outcomes associated with candidemia caused by non-albicans Candida spp versus Candida albicans in children","volume":"46","author":"Lee","year":"2018","journal-title":"Am. J. Infect. Control."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"260","DOI":"10.20411\/pai.v4i2.291","article-title":"Environmental contamination with Candida species in multiple hospitals in a Tertiary Care Hospital with a Candida auris outbreak","volume":"4","author":"Kumar","year":"2019","journal-title":"Pathog. Immun."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"1056","DOI":"10.1111\/myc.12988","article-title":"Characterisation of candidemia in patients with recent surgery: A 7-year experience","volume":"62","author":"Orsetti","year":"2019","journal-title":"Mycoses"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"S79","DOI":"10.1093\/ofid\/ofy358","article-title":"Twenty Years of the SENTRY Antifungal Surveillance Program: Results for Candida Species From 1997\u20132016","volume":"6","author":"Pfaller","year":"2019","journal-title":"Open Forum Infect. Dis."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Mohr, A., Simon, M., Joha, T., Hanses, F., Salzberger, B., and Hitzenbichler, F. (2020). Epidemiology of candidemia and impact of infectious disease consultation on survival and care. Infection.","DOI":"10.1007\/s15010-020-01393-9"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1007\/978-1-4939-6515-1_2","article-title":"The Changing Epidemiology of Invasive Fungal Infections","volume":"1508","author":"Enoch","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Giacobbe, D.R., Maraolo, A.E., Simeon, V., Magn\u00e8, F., Pace, M.C., Gentile, I., Chiodini, P., Viscoli, C., Sanguinetti, M., and Mikulska, M. (2020). Changes in the relative prevalence of candidemia due to non-albicans Candida species in adult in-patients: A systematic review, meta-analysis, and meta-regression. Mycoses.","DOI":"10.1111\/myc.13054"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Mesini, A., Mikulska, M., Giacobbe, D.R., Del Puente, F., Gandolfo, N., Codda, G., Orsi, A., Tassinari, F., Beltramini, S., and Marchese, A. (2020). Changing epidemiology of candidemia: Increase in fluconazole-resistant Candida parapsilosis. Mycoses.","DOI":"10.1111\/myc.13050"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"3860","DOI":"10.1099\/mic.0.032854-0","article-title":"Vesicle-associated melanization in Cryptococcus neoformans","volume":"155","author":"Eisenman","year":"2009","journal-title":"Microbiology"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1676","DOI":"10.1021\/pr200872s","article-title":"Vesicle and vesicle-free extracellular proteome of Paracoccidioides brasiliensis: Comparative analysis with other pathogenic fungi","volume":"11","author":"Vallejo","year":"2012","journal-title":"J. Proteome Res."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1484","DOI":"10.1128\/EC.00111-14","article-title":"Interaction of Cryptococcus neoformans extracellular vesicles with the cell wall","volume":"13","author":"Wolf","year":"2014","journal-title":"Eukaryot Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"7763","DOI":"10.1038\/srep07763","article-title":"Extracellular vesicle-mediated export of fungal RNA","volume":"5","author":"Puccia","year":"2015","journal-title":"Sci. Rep."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1038\/s42003-019-0538-8","article-title":"Extracellular vesicles secreted by Saccharomyces cerevisiae are involved in cell wall remodelling","volume":"2","author":"Zhao","year":"2019","journal-title":"Commun. Biol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1027","DOI":"10.2174\/1389203720666190529124055","article-title":"Extracellular Vesicles as Vehicles for the Delivery of Biologically Active Fungal Molecules","volume":"20","author":"Herkert","year":"2019","journal-title":"Curr. Protein Pept. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/mSphere.00176-19","article-title":"Extracellular Vesicle-Mediated RNA Release in Histoplasma capsulatum","volume":"4","author":"Alves","year":"2019","journal-title":"mSphere"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1016\/j.mib.2013.04.002","article-title":"Vesicular mechanisms of traffic of fungal molecules to the extracellular space","volume":"16","author":"Rodrigues","year":"2013","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_19","first-page":"1","article-title":"Antibody binding alters the characteristics and contents of extracellular vesicles released by Histoplasma capsulatum","volume":"1","author":"Nakayasu","year":"2016","journal-title":"mSphere"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"8065","DOI":"10.1038\/s41598-018-25665-5","article-title":"Concentration-dependent protein loading of extracellular vesicles released by Histoplasma capsulatum after antibody treatment and its modulatory action upon macrophages","volume":"8","author":"Baltazar","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_21","first-page":"45","article-title":"Extracellular Vesicles in Fungi: Composition and Functions","volume":"422","author":"Szwarc","year":"2019","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1695","DOI":"10.1111\/j.1462-5822.2008.01160.x","article-title":"Vesicular transport in Histoplasma capsulatum: An effective mechanism for trans-cell wall transfer of proteins and lipids in ascomycetes","volume":"10","author":"Albuquerque","year":"2008","journal-title":"Cell Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1128\/EC.00370-07","article-title":"Extracellular vesicles produced by Cryptococcus neoformans contain protein components associated with virulence","volume":"7","author":"Rodrigues","year":"2008","journal-title":"Eukaryot Cell"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1128\/EC.00227-10","article-title":"The pathogenic fungus Paracoccidioides brasiliensis exports extracellular vesicles containing highly immunogenic \u03b1-Galactosyl epitopes","volume":"10","author":"Vallejo","year":"2011","journal-title":"Eukaryot Cell"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"202","DOI":"10.1093\/mmy\/myt003","article-title":"Characterization of Alternaria infectoria extracellular vesicles","volume":"52","author":"Silva","year":"2014","journal-title":"Med. Mycol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1021\/pr5007944","article-title":"Proteomics unravels extracellular vesicles as carriers of classical cytoplasmic proteins in Candida albicans","volume":"14","author":"Parra","year":"2015","journal-title":"J. Proteome Res."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1111\/cmi.12374","article-title":"Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans","volume":"17","author":"Vargas","year":"2015","journal-title":"Cell Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"9182","DOI":"10.1038\/s41598-018-27451-9","article-title":"Extracellular nanovesicles released from the commensal yeast Malassezia sympodialis are enriched in allergens and interact with cells in human skin","volume":"8","author":"Johansson","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1016\/j.micinf.2018.01.011","article-title":"Fungal extracellular vesicles: Modulating host-pathogen interactions by both the fungus and the host","volume":"20","author":"Nimrichter","year":"2018","journal-title":"Microbes Infect."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"103666","DOI":"10.1016\/j.micpath.2019.103666","article-title":"A comparative analysis of protein virulence factors released via extracellular vesicles in two Candida albicans strains cultivated in a nutrient-limited medium","volume":"136","author":"Benada","year":"2019","journal-title":"Microb. Pathog."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1128\/IAI.01171-09","article-title":"Extracellular vesicles from Cryptococcus neoformans modulate macrophage functions","volume":"78","author":"Oliveira","year":"2010","journal-title":"Infect. Immun."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Gehrmann, U., Qazi, K.R., Johansson, C., Hultenby, K., Karlsson, M., Lundeberg, L., Gabrielsson, S., and Scheynius, A. (2011). Nanovesicles from Malassezia sympodialis and host exosomes induce cytokine responses \u2013 novel mechanisms for host-microbe interactions in atopic eczema. PLoS ONE, 6.","DOI":"10.1371\/journal.pone.0021480"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"35867","DOI":"10.1038\/srep35867","article-title":"Extracellular vesicles from Paracoccidioides brasiliensis induced M1 polarization in vitro","volume":"6","author":"Casadevall","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"745","DOI":"10.1128\/EC.00054-15","article-title":"Lipid biosynthetic genes affect Candida albicans extracellular vesicle morphology, cargo, and immunostimulatory properties","volume":"14","author":"Wolf","year":"2015","journal-title":"Eukaryot Cell"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1073\/pnas.72.2.619","article-title":"O-phthalaldehyde: Fluorogenic detection of primary amines in the picomole range. Comparison with fluorescamine and ninhydrin","volume":"72","author":"Benson","year":"1975","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.3168\/jds.S0022-0302(83)81926-2","article-title":"Spectrophotometric assay using o-phthaldialdehyde for determination of proteolysis in milk and isolated milk proteins","volume":"66","author":"Church","year":"1983","journal-title":"J. Dair. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Karkowska-Kuleta, J., Satala, D., Bochenska, O., Rapala-Kozik, M., and Kozik, A. (2019). Moonlighting proteins are variably exposed at the cell surfaces of Candida glabrata, Candida parapsilosis and Candida tropicalis under certain growth conditions. BMC Microbiol., 19.","DOI":"10.1186\/s12866-019-1524-5"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"807","DOI":"10.18388\/abp.2015_1140","article-title":"Surfaceome of pathogenic yeasts, Candida parapsilosis and Candida tropicalis, revealed with the use of cell surface shaving method and shotgun proteomic approach","volume":"62","author":"Zajac","year":"2015","journal-title":"Acta Biochim. Pol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"391","DOI":"10.18388\/abp.2017_1609","article-title":"Binding of human plasminogen and high-molecular-mass kininogen by cell surface-exposed proteins of Candida parapsilosis","volume":"64","author":"Zajac","year":"2017","journal-title":"Acta Biochim. Pol."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1535750","DOI":"10.1080\/20013078.2018.1535750","article-title":"Minimal information for studies of extracellular vesicles 2018 (MISEV2018): A position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines","volume":"7","author":"Witwer","year":"2018","journal-title":"J. Extracell. Vesicles"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"36331","DOI":"10.1038\/srep36331","article-title":"Isolation and mass spectrometry analysis of urinary extraexosomal proteins","volume":"6","author":"Hildonen","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"727","DOI":"10.1016\/j.jconrel.2015.09.031","article-title":"Microvesicle- and exosome-mediated drug delivery enhances the cytotoxicity of Paclitaxel in autologous prostate cancer cells","volume":"220","author":"Saari","year":"2015","journal-title":"J. Control. Release"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"D358","DOI":"10.1093\/nar\/gki003","article-title":"The Candida genome database (CGD), a community resource for Candida albicans gene and protein information","volume":"33","author":"Arnaud","year":"2005","journal-title":"Nucleic Acids Res."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"D700","DOI":"10.1093\/nar\/gkr1029","article-title":"Saccharomyces genome database: The genomics resource of budding yeast","volume":"40","author":"Cherry","year":"2012","journal-title":"Nucleic Acids Res."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"(2019). The UniProt Consortium. UniProt: A worldwide hub of protein knowledge. Nucleic Acids Res., 47, D506\u2013D515.","DOI":"10.1093\/nar\/gky1049"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Woith, E., Fuhrmann, G., and Melzig, M.F. (2019). Extracellular Vesicles-Connecting Kingdoms. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20225695"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1016\/j.mib.2019.05.007","article-title":"Extracellular vesicles of human pathogenic fungi","volume":"52","author":"Bielska","year":"2019","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e2006872","DOI":"10.1371\/journal.pbio.2006872","article-title":"Candida albicans biofilm\u2013induced vesicles confer drug resistance through matrix biogenesis","volume":"16","author":"Zarnowski","year":"2018","journal-title":"PLoS Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1034","DOI":"10.3389\/fmicb.2016.01034","article-title":"Extracellular Vesicle-Associated Transitory Cell Wall Components and Their Impact on the Interaction of Fungi with Host Cells","volume":"7","author":"Nimrichter","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1111\/mmi.12426","article-title":"Mannosylation in Candida albicans: Role in cell wall function and immune recognition","volume":"90","author":"Hall","year":"2013","journal-title":"Mol. Microbiol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1631","DOI":"10.1099\/mic.0.27663-0","article-title":"Yeast wall protein 1 of Candida albicans","volume":"151","author":"Granger","year":"2005","journal-title":"Microbiology"},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Granger, B.L. (2018). Accessibility and contribution to glucan masking of natural and genetically tagged versions of yeast wall protein 1 of Candida albicans. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0191194"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"602","DOI":"10.1111\/j.1462-5822.2005.00651.x","article-title":"Candida albicans mannoprotein influences the biological function of dendritic cells","volume":"8","author":"Pietrella","year":"2006","journal-title":"Cell Microbiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1223","DOI":"10.1111\/j.1462-5822.2006.00862.x","article-title":"The 65 kDa mannoprotein gene of Candida albicans encodes a putative beta-glucanase adhesin required for hyphal morphogenesis and experimental pathogenicity","volume":"9","author":"Sandini","year":"2007","journal-title":"Cell Microbiol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1128\/EC.00387-08","article-title":"Property differences among the four major Candida albicans strain clades","volume":"8","author":"MacCallum","year":"2009","journal-title":"Eukaryot. Cell"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1128\/IAI.69.1.405-412.2001","article-title":"Secreted aspartic proteinase family of Candida tropicalis","volume":"69","author":"Zaugg","year":"2001","journal-title":"Infect. Immun."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"7628","DOI":"10.1073\/pnas.0611195104","article-title":"A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata","volume":"104","author":"Kaur","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1175","DOI":"10.3389\/fmicb.2016.01175","article-title":"Distinct Expression Levels of ALS, LIP, and SAP Genes in Candida tropicalis with Diverse Virulent Activities","volume":"7","author":"Yu","year":"2016","journal-title":"Front. Microbiol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1099\/00221287-143-2-367","article-title":"Phenotype in Candida albicans of a disruption of the BGL2 gene encoding a 1,3-beta-glucosyltransferase","volume":"143 Pt 2","author":"Sarthy","year":"1997","journal-title":"Microbiology"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"3317","DOI":"10.1128\/IAI.66.7.3317-3325.1998","article-title":"The pH of the host niche controls gene expression in and virulence of Candida albicans","volume":"66","author":"Cassone","year":"1998","journal-title":"Infect. Immun"},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Miura, N., and Ueda, M. (2018). Evaluation of Unconventional Protein Secretion by Saccharomyces cerevisiae and other Fungi. Cells, 7.","DOI":"10.3390\/cells7090128"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.jprot.2017.12.002","article-title":"The external face of Candida albicans: A proteomic view of the cell surface and the extracellular environment","volume":"180","author":"Gil","year":"2018","journal-title":"J. Proteom."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/S0968-0004(98)01335-8","article-title":"Moonlighting proteins","volume":"24","author":"Jeffery","year":"1999","journal-title":"Trends Biochem. Sci."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"270","DOI":"10.1111\/omi.12078","article-title":"Moonlighting proteins as virulence factors of pathogenic fungi, parasitic protozoa and multicellular parasites","volume":"29","author":"Kozik","year":"2014","journal-title":"Mol. Oral Microbiol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"765","DOI":"10.1128\/MMBR.00012-16","article-title":"The Expanding Landscape of Moonlighting Proteins in Yeasts","volume":"80","author":"Gancedo","year":"2016","journal-title":"Microbiol Mol Biol Rev."},{"key":"ref_66","doi-asserted-by":"crossref","unstructured":"Kozik, A., Karkowska-Kuleta, J., Zajac, D., Bochenska, O., Kedracka-Krok, S., Jankowska, U., and Rapala-Kozik, M. (2015). Fibronectin-, vitronectin- and laminin-binding proteins at the cell walls of Candida parapsilosis and Candida tropicalis pathogenic yeasts. BMC Microbiol., 15.","DOI":"10.1186\/s12866-015-0531-4"},{"key":"ref_67","first-page":"427","article-title":"Characterization of the interactions between human high-molecular-mass kininogen and cell wall proteins of pathogenic yeasts Candida tropicalis","volume":"63","author":"Zajac","year":"2016","journal-title":"Acta Biochim. Pol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"4263","DOI":"10.1128\/iai.61.10.4263-4271.1993","article-title":"Glycolytic enzymes of Candida albicans are nonubiquitous immunogens during candidiasis","volume":"61","author":"Swoboda","year":"1993","journal-title":"Infect. Immun."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"3159","DOI":"10.1099\/00221287-147-11-3159","article-title":"Antibodies to alpha5beta1 and alpha(v)beta3 integrins react with Candida albicans alcohol dehydrogenase","volume":"147","author":"Klotz","year":"2001","journal-title":"Microbiology"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1016\/j.jare.2019.02.005","article-title":"Alcohol dehydrogenase of Candida albicans triggers differentiation of THP-1 cells into macrophages","volume":"18","author":"Liu","year":"2019","journal-title":"J. Adv. Res."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"999","DOI":"10.1111\/jam.12408","article-title":"Identification of immunogenic proteins of Candida parapsilosis by serological proteome analysis","volume":"116","author":"Lee","year":"2014","journal-title":"J. Appl. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"854","DOI":"10.1111\/jam.12562","article-title":"Immunoproteomic analysis of antibody response to cell wall-associated proteins of Candida tropicalis","volume":"117","author":"Lee","year":"2014","journal-title":"J. Appl. Microbiol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"e11113","DOI":"10.1371\/journal.pone.0011113","article-title":"Characterization of yeast extracellular vesicles, evidence for the participation of different pathways of cellular traffic in vesicle biogenesis","volume":"5","author":"Oliveira","year":"2010","journal-title":"PLoS ONE"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/7\/1722\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T09:49:37Z","timestamp":1760176177000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/9\/7\/1722"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,7,18]]},"references-count":73,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2020,7]]}},"alternative-id":["cells9071722"],"URL":"https:\/\/doi.org\/10.3390\/cells9071722","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,7,18]]}}}