The Candida glabrata adhesin Epa1p causes adhesion, phagocytosis, and cytokine secretion by innate immune cells

Kuhn, Duncan M.; Vyas, Valmik K.

doi:10.1111/j.1567-1364.2011.00785.x

Cited by 38Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

The Candida glabrata adhesin Epa1p causes adhesion, phagocytosis, and cytokine secretion by innate immune cells

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Kuhn, Duncan M., Vyas, Valmik K.·2012·FEMS Yeast Research

DOI 10.1111/j.1567-1364.2011.00785.x

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Abstract

While Candida albicans is the most significant fungal pathogen for humans, Candida glabrata accounts for an increasing number of infections. Little is known about how C. glabrata interacts with the innate immune system, the first line of defense against such organisms. The C. glabrata adhesin Epa1p was previously shown to bind mammalian epithelial cells. We hypothesized that Epa1p mediates unique, nonopsonic binding to macrophages, leading to induction of immune responses. We found that Epa1p mediated adhesion by both C. glabrata (Cg) and transformed Saccharomyces cerevisiae (Sc(EPA1) ) to human macrophage-like cells, including Thp1 and U937 lines, and donor PBMCs. Adhesion was distinct from described mechanisms such as Dectin-1. Epa1p expression was necessary and sufficient for S. cerevisiae binding and phagocytosis, the latter of which was actin-mediated. Sc(EPA1) induced inflammatory cytokine production (IL-8 and TNF-α) by human PBMC-derived macrophages. Despite expressing Epa1p and binding to macrophages, Cg avoided phagocytosis and cytokine induction. In contrast to human results, in murine cell models (RAW264.7, J774A.1, and C57BL/6-derived cells), Epa1p-mediated binding was only revealed after blocking the Dectin-1 system. Recognition of Epa1p represents a novel mechanism by which human innate immune cells bind fungi, and for Sc(EPA1) results in phagocytosis and subsequent cytokine production.

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Epa1 is a calcium-dependent lectin that aids adhesion to epithelial cells and macrophages.
“The founding member of the Epa adhesin family, Epa1, is a calcium-dependent lectin, and aids adhesion to epithelial cells [32] and macrophages [33].”
From Candida glabrata: A Lot More Than Meets the Eye (2019) · cites this paper as [33]

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Establishment and characterization of a human histiocytic lymphoma cell line (U‐937)
Sundström, C., & Nilsson, K. (1976) · International Journal of Cancer · doi:10.1002/ijc.2910170504 · Cited by 2,409 · see citing works
Establishment and characterization of a human acute monocytic leukemia cell line (THP‐1)
Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T., & Tada, K. (1980) · International Journal of Cancer · doi:10.1002/ijc.2910260208 · Cited by 2,258 · see citing works
Collaborative Induction of Inflammatory Responses by Dectin-1 and Toll-like Receptor 2
Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S., & Underhill, D. M. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021787 · Cited by 1,644 · see citing works
Dectin-1 Mediates the Biological Effects of β-Glucans
Brown, G. D., Herre, J., Williams, D. L., Willment, J. A., Marshall, A. S. J., & Gordon, S. (2003) · The Journal of Experimental Medicine · doi:10.1084/jem.20021890 · Cited by 1,209 · see citing works
Dectin-1: a signalling non-TLR pattern-recognition receptor
Brown, G. D. (2006) · Nature Reviews Immunology · doi:10.1038/nri1745 · Cited by 1,158 · see citing works
Major trends in the microbial etiology of nosocomial infection
Schaberg, D. R., Culver, D. H., & Gaynes, R. P. (1991) · The American Journal of Medicine · doi:10.1016/0002-9343(91)90346-y · Cited by 1,119 · see citing works
Dectin-1 Is A Major β-Glucan Receptor On Macrophages
Brown, G. D., Taylor, P. R., Reid, D. M., Willment, J. A., Williams, D. L., Martínez‐Pomares, L., Wong, S. Y. C., & Gordon, S. (2002) · The Journal of Experimental Medicine · doi:10.1084/jem.20020470 · Cited by 1,015 · see citing works
Functional macrophage cell lines transformed by abelson leukemia virus
Raschke, W. C., Baird, S. M., Ralph, P., & Nakoinz, I. (1978) · Cell · doi:10.1016/0092-8674(78)90101-0 · Cited by 906 · see citing works
Secular trends in nosocomial primary bloodstream infections in the United States, 1980–1989.
Banerjee, S. N., Emori, T. G., Culver, D. H., Gaynes, R. P., Jarvis, W. R., Horan, T., Edwards, J. R., Tolson, J., Henderson, T., Martone, W. J., et al. (1991) · The American Journal of Medicine · doi:10.1016/0002-9343(91)90349-3 · Cited by 880 · see citing works
Dectin-2 Recognition of α-Mannans and Induction of Th17 Cell Differentiation Is Essential for Host Defense against Candida albicans
Saijo, S., Ikeda, S., Yamabe, K., Kakuta, S., Ishigame, H., Akitsu, A., Fujikado, N., Kusaka, T., Kubo, S., Chung, S.-H., et al. (2010) · Immunity · doi:10.1016/j.immuni.2010.05.001 · Cited by 735 · see citing works
Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1.
Staab, J., Bradway, S. D., Fidel, P., & Sundstrom, P. (1999) · Science · doi:10.1126/science.283.5407.1535 · Cited by 683 · see citing works
Phagocytosis
Stuart, L. M., & Ezekowitz, R. A. B. (2005) · Immunity · doi:10.1016/j.immuni.2005.05.002 · Cited by 667 · see citing works
Als3 Is a Candida albicans Invasin That Binds to Cadherins and Induces Endocytosis by Host Cells
Phan, Q. T., Myers, C. L., Fu, Y., Sheppard, D. C., Yeaman, M. R., Welch, W. H., Ibrahim, A. S., Edwards, J. E., & Filler, S. G. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050064 · Cited by 641 · see citing works
Molecular characterization of the human macrophage mannose receptor: demonstration of multiple carbohydrate recognition-like domains and phagocytosis of yeasts in Cos-1 cells.
Ezekowitz, R. A. B., Sastry, K., Bailly, P., & Warner, A. (1990) · The Journal of Experimental Medicine · doi:10.1084/jem.172.6.1785 · Cited by 501 · see citing works
The Role of Toll‐like Receptor (TLR) 2 and TLR4 in the Host Defense against Disseminated Candidiasis
Netea, M. G., van der Graaf, C. A. A., Vonk, A. G., Verschueren, I., van der Meer, J. W. M., & Kullberg, B. J. (2002) · The Journal of Infectious Diseases · doi:10.1086/340511 · Cited by 486 · see citing works
Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection
Robinson, M. J., Osorio, F., Rosas, M., Freitas, R. P., Schweighoffer, E., Groß, O., Verbeek, J. S., Ruland, J., Tybulewicz, V. L. J., Brown, G. D., et al. (2009) · The Journal of Experimental Medicine · doi:10.1084/jem.20082818 · Cited by 464 · see citing works
National Surveillance of Nosocomial Blood Stream Infection Due to Species of Candida Other than Candida albicans: Frequency of Occurrence and Antifungal Susceptibility in the SCOPE Program
Pfaller, M. A., Jones, R. N., Messer, S. A., Edmond, M. B., & Wenzel, R. P. (1998) · Diagnostic Microbiology and Infectious Disease · doi:10.1016/s0732-8893(97)00192-2 · Cited by 424 · see citing works
An Adhesin of the Yeast Pathogen Candida glabrata Mediating Adherence to Human Epithelial Cells
Cormack, B. P., Ghori, N., & Falkow, S. (1999) · Science · doi:10.1126/science.285.5427.578 · Cited by 383 · see citing works
A Saccharomyces gene family involved in invasive growth, cell–cell adhesion, and mating
Guo, B., Styles, C. A., Feng, Q., & Fink, G. R. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.220420397 · Cited by 382 · see citing works
Dectin-1 synergizes with TLR2 and TLR4 for cytokine production in human primary monocytes and macrophages
Ferwerda, G., Meyer‐Wentrup, F. A. G., Kullberg, B. J., Netea, M. G., & Adema, G. J. (2008) · Cellular Microbiology · doi:10.1111/j.1462-5822.2008.01188.x · Cited by 363 · see citing works
A Drug-Sensitive Genetic Network Masks Fungi from the Immune System
Wheeler, R. T., & Fink, G. R. (2006) · PLoS Pathogens · doi:10.1371/journal.ppat.0020035 · Cited by 360 · see citing works
Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1.
Gale, C. A., Bendel, C. M., McClellan, M., Hauser, M., Becker, J. M., Berman, J., & Hostetter, M. K. (1998) · Science · doi:10.1126/science.279.5355.1355 · Cited by 356 · see citing works
Involvement of CD14 in lipopolysaccharide-induced tumor necrosis factor-alpha, IL-6 and IL-8 release by human monocytes and alveolar macrophages
Dentener, M. A., Bažil, V., von Asmuth, E. J., Ceska, M., & Buurman, W. A. (1993) · The Journal of Immunology · doi:10.4049/jimmunol.150.7.2885 · Cited by 318 · see citing works
Candida albicansPhospholipomannan Is Sensed through Toll‐Like Receptors
Jouault, T., Ibata‐Ombetta, S., Takeuchi, O., Trinel, P. A., Sacchetti, P., Lefèbvre, P., Akira, S., & Poulain, D. (2003) · The Journal of Infectious Diseases · doi:10.1086/375784 · Cited by 310 · see citing works
Dynamic, Morphotype-Specific Candida albicans β-Glucan Exposure during Infection and Drug Treatment
Wheeler, R. T., Kombe, D., Agarwala, S. D., & Fink, G. R. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000227 · Cited by 309 · see citing works
A family of glycosylphosphatidylinositol-linked aspartyl proteases is required for virulence of Candida glabrata
Kaur, R., Ma, B., & Cormack, B. P. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611195104 · Cited by 284 · see citing works
Protection from Lethal Gram-Positive Infection by Macrophage Scavenger Receptor–Dependent Phagocytosis
Thomas, C. A., Li, Y., Kodama, T., Suzuki, H., Silverstein, S. C., & Khoury, J. B. E. (2000) · The Journal of Experimental Medicine · doi:10.1084/jem.191.1.147 · Cited by 279 · see citing works
Phagocytosis and Intracellular Fate ofAspergillus fumigatusConidia in Alveolar Macrophages
Ibrahim-Granet, O., Philippe, B., Boleti, H., Boisvieux-Ulrich, E., Grenet, D., Stern, M., & Latgé, J. P. (2003) · Infection and Immunity · doi:10.1128/iai.71.2.891-903.2003 · Cited by 277 · see citing works
Nucleotide-Binding Oligomerization Domain-2 Modulates Specific TLR Pathways for the Induction of Cytokine Release
Netea, M. G., Ferwerda, G., de Jong, D. J., Jansen, T., Jacobs, L., Kramer, M., Naber, A. H. J., Drenth, J. P. H., Girardin, S. E., Kullberg, B. J., et al. (2005) · The Journal of Immunology · doi:10.4049/jimmunol.174.10.6518 · Cited by 274 · see citing works
Resilience to Bacterial Infection: Difference between Species Could Be Due to Proteins in Serum
Warren, H. S., Fitting, C., Hoff, E., Adib‐Conquy, M., Beasley‐Topliffe, L., Tesini, B., Liang, X., Valentine, C., Hellman, J., Hayden, D., et al. (2010) · The Journal of Infectious Diseases · doi:10.1086/649557 · Cited by 269 · see citing works
Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1 - and SIR -dependent transcriptional silencing
De Las Peñas, A., Pan, S.-J., Castaño, I., Alder, J., Cregg, R., & Cormack, B. P. (2003) · Genes & Development · doi:10.1101/gad.1121003 · Cited by 268 · see citing works
The human β‐glucan receptor is widely expressed and functionally equivalent to murine Dectin‐1 on primary cells
Willment, J. A., Marshall, A. S. J., Reid, D. M., Williams, D. L., Wong, S. Y. C., Gordon, S., & Brown, G. D. (2005) · European Journal of Immunology · doi:10.1002/eji.200425725 · Cited by 257 · see citing works
Nicotinic Acid Limitation Regulates Silencing of Candida Adhesins During UTI
Domergue, R., Castaño, I., De Las Peñas, A., Zupancic, M., Lockatell, V., Hebel, J. R., Johnson, D., & Cormack, B. P. (2005) · Science · doi:10.1126/science.1108640 · Cited by 249 · see citing works
Evolutionarily Conserved Recognition and Innate Immunity to Fungal Pathogens by the Scavenger Receptors SCARF1 and CD36
Tampakakis, E., Puckett, L. L., Tai, M., Stewart, C. R., Hickman, S. E., Moore, K. J., El Khoury, J., Means, T. K., Mylonakis, E. E., Colvin, R. A., et al. (2009) · Digital Access to Scholarship at Harvard (DASH) (Harvard University) · Cited by 246 · see citing works
Dectin-1 Expression and Function Are Enhanced on Alternatively Activated and GM-CSF-Treated Macrophages and Are Negatively Regulated by IL-10, Dexamethasone, and Lipopolysaccharide
Willment, J. A., Lin, H.-H., Reid, D. M., Taylor, P. R., Williams, D. L., Wong, S. Y. C., Gordon, S., & Brown, G. D. (2003) · The Journal of Immunology · doi:10.4049/jimmunol.171.9.4569 · Cited by 238 · see citing works
The Cell Wall of the Human Pathogen Candida glabrata : Differential Incorporation of Novel Adhesin-Like Wall Proteins
de Groot, P. W. J., Kraneveld, E. A., Yin, Q. Y., Dekker, H. L., Groß, U., Crielaard, W., de Koster, C. G., Bader, O., Klis, F. M., & Weig, M. (2008) · Eukaryotic Cell · doi:10.1128/ec.00284-08 · Cited by 232 · see citing works
Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans
Rubin-Bejerano, I., Fraser, I., Grisafi, P., & Fink, G. R. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1834481100 · Cited by 223 · see citing works
The Facultative Intracellular Pathogen Candida glabrata Subverts Macrophage Cytokine Production and Phagolysosome Maturation
Seider, K., Brunke, S., Schild, L., Jablonowski, N., Wilson, D., Majer, O., Barz, D., Haas, A., Kuchler, K., Schaller, M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1003730 · Cited by 220 · see citing works
Toll-like receptor-2 is essential in murine defenses against Candida albicans infections
Villamón, E., Gozalbo, D., Roig, P., O’Connor, J., FRADELIZI, D., & Gil, M. L. (2003) · Microbes and Infection · doi:10.1016/j.micinf.2003.09.020 · Cited by 214 · see citing works
A Comparison of Differences in the Gene Expression Profiles of Phorbol 12-myristate 13-acetate Differentiated THP-1 Cells and Human Monocyte-derived Macrophage
Kohro, T., Tanaka, T., Murakami, T., Wada, Y., Aburatani, H., Hamakubo, T., & Kodama, T. (2004) · Journal of Atherosclerosis and Thrombosis · doi:10.5551/jat.11.88 · Cited by 183 · see citing works
Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins
Gaur, N. K., & Klotz, S. A. (1997) · Infection and Immunity · doi:10.1128/iai.65.12.5289-5294.1997 · Cited by 182 · cited 2× · see citing works
“Epa1p is part of the family of functionally conserved fungal adhesins, including Ala1p (Gaur & Klotz, 1997), Als1p (Fu et al., 1998), Int1p (Gale et al., 1998), and Hwp1p (Staab et al., 1999). ª 2011 Federation of European Microbiological Societies FEMS Yeast Res 12 (2012) 398–414 Published by Blackwell Publishing Ltd.”
Background
Normal Host Defense during Systemic Candidiasis in Mannose Receptor-Deficient Mice
Lee, S. J., Zheng, N., Clavijo, M., & Nussenzweig, M. C. (2002) · Infection and Immunity · doi:10.1128/iai.71.1.437-445.2003 · Cited by 178 · see citing works
Molecular Cloning of a Dendritic Cell-associated Transmembrane Protein, DC-HIL, That Promotes RGD-dependent Adhesion of Endothelial Cells through Recognition of Heparan Sulfate Proteoglycans
Shikano, S., Bonkobara, M., Zukas, P. K., & Ariizumi, K. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m008539200 · Cited by 166 · see citing works
Modular domain structure in the Candida glabrata adhesin Epa1p, a β1,6 glucan‐cross‐linked cell wall protein
Frieman, M., McCaffery, J. M., & Cormack, B. (2002) · Molecular Microbiology · doi:10.1046/j.1365-2958.2002.03166.x · Cited by 159 · see citing works
Expression of the Candida albicans Gene ALS1 in Saccharomyces cerevisiae Induces Adherence to Endothelial and Epithelial Cells
Fu, Y., Rieg, G., Fonzi, W. A., Belanger, P. H., Edwards, J. E., & Filler, S. G. (1998) · Infection and Immunity · doi:10.1128/iai.66.4.1783-1786.1998 · Cited by 159 · see citing works
Complementation between mutants of CHO cells resistant to a variety of plant lectins
Stanley, P., & Siminovitch, L. (1977) · Somatic Cell and Molecular Genetics · doi:10.1007/bf01542968 · Cited by 152 · see citing works
Phenotypic diversity of Flo protein family-mediated adhesion inSaccharomyces cerevisiae
Mulders, S. E. V., Christianen, E., Saerens, S., et al. (2008) · FEMS Yeast Research · doi:10.1111/j.1567-1364.2008.00462.x · Cited by 150 · see citing works
Biologic and Biochemical Activities of Continuous Macrophage Cell Lines P388D1 and J774.1
Snyderman, R., Pike, M. C., Fischer, D. G., et al. (1977) · The Journal of Immunology · doi:10.4049/jimmunol.119.6.2060 · Cited by 145 · see citing works
Glycan microarray analysis of Candida glabrata adhesin ligand specificity
Zupancic, M. L., Frieman, M., Smith, D., Alvarez, R. A., Cummings, R. D., & Cormack, B. P. (2008) · Molecular Microbiology · doi:10.1111/j.1365-2958.2008.06184.x · Cited by 143 · see citing works
Autophagy supportsCandida glabratasurvival during phagocytosis
Roetzer, A., Gratz, N., Kovarik, P., & SchÃ¼ller, C. (2010) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01391.x · Cited by 142 · see citing works
Lipopolysaccharide Induces Scavenger Receptor A Expression in Mouse Macrophages: A Divergent Response Relative to Human THP-1 Monocyte/Macrophages
Fitzgerald, M. L., Moore, K. J., Freeman, M. W., & Reed, G. L. (2000) · The Journal of Immunology · doi:10.4049/jimmunol.164.5.2692 · Cited by 139 · see citing works
Candida albicansinternalization by host cells is mediated by a clathrin-dependent mechanism
Moreno-Ruiz, E., Galán-Díez, M., Zhu, W., Fernández-Ruiz, E., d'Enfert, C., Filler, S. G., Cossart, P., & Veiga, E. (2009) · Cellular Microbiology · doi:10.1111/j.1462-5822.2009.01319.x · Cited by 133 · see citing works
Synthetic lipopeptide adjuvants and Toll-like receptor 2—structure–activity relationships
Spohn, R., Buwitt‐Beckmann, U., Brock, R. E., et al. (2004) · Vaccine · doi:10.1016/j.vaccine.2003.11.074 · Cited by 133 · see citing works
Invasive Candida species infections: a 5 year population-based assessment
Laupland, K. B., Gregson, D. B., Church, D. L., Ross, T., & Elsayed, S. (2005) · Journal of Antimicrobial Chemotherapy · doi:10.1093/jac/dki258 · Cited by 129 · see citing works
Conventional Dendritic Cells Mount a Type I IFN Response against Candida spp. Requiring Novel Phagosomal TLR7-Mediated IFN-β Signaling
Bourgeois, C., Majer, O., Frohner, I. E., Lesiak-Markowicz, I., Hildering, K.-S., Glaser, W., Stockinger, S., Decker, T., Akira, S., Müller, M., et al. (2011) · The Journal of Immunology · doi:10.4049/jimmunol.1002599 · Cited by 116 · see citing works
Effects of anti-CD44 monoclonal antibodies on differentiation and apoptosis of human myeloid leukemia cell lines
Charrad, R.-S., Gadhoum, Z., Qi, J., Glachant, A., Allouche, M., Jasmin, C., Chomienne, C., & Smadja‐Joffe, F. (2002) · Blood · doi:10.1182/blood.v99.1.290 · Cited by 113 · see citing works
Mannoproteins from Cryptococcus neoformans Promote Dendritic Cell Maturation and Activation
Pietrella, D., Corbucci, C., Perito, S., Bistoni, G., & Vecchiarelli, A. (2005) · Infection and Immunity · doi:10.1128/iai.73.2.820-827.2005 · Cited by 102 · see citing works
The ω‐site sequence of glycosylphosphatidylinositol‐anchored proteins in Saccharomyces cerevisiae can determine distribution between the membrane and the cell wall
Frieman, M., & Cormack, B. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03722.x · Cited by 98 · see citing works
Genetic and epigenetic mechanisms underlying cell-surface variability in protozoa and fungi.
Verstrepen, K., & Fink, G. (2009) · Annual Review of Genetics · doi:10.1146/annurev-genet-102108-134156 · Cited by 97 · see citing works
TLR-2, TLR-4 and dectin-1 expression in human monocytes and neutrophils stimulated byParacoccidioides brasiliensis
Bonfim, C. V., Mamoni, R. L., & Blotta, M. H. S. L. (2009) · Medical Mycology · doi:10.3109/13693780802641425 · Cited by 94 · see citing works
A single‐step, sensitive flow cytofluorometric assay for the simultaneous assessment of membrane‐bound and ingested Candida albicans in phagocytosing neutrophils
Busetto, S., Trevisan, E., Patriarca, P., et al. (2004) · Cytometry Part A · doi:10.1002/cyto.a.20014 · Cited by 93 · see citing works
IL-13 down-regulates CD14 expression and TNF-α secretion in normal human monocytes
Cosentino, G., Soprana, E., Thienes, C. P., et al. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.155.6.3145 · Cited by 88 · see citing works
A C‐terminal EGF‐like domain governs BAD1 localization to the yeast surface and fungal adherence to phagocytes, but is dispensable in immune modulation and pathogenicity of Blastomyces dermatitidis
Brandhorst, T. T., Wüthrich, M., Finkel‐Jimenez, B., & Klein, B. S. (2003) · Molecular Microbiology · doi:10.1046/j.1365-2958.2003.03415.x · Cited by 86 · see citing works
Differential Flo8p‐dependent regulation of FLO1 and FLO11 for cell–cell and cell–substrate adherence of S. cerevisiae S288c
Fichtner, L., Schulze, F., & Braus, G. H. (2007) · Molecular Microbiology · doi:10.1111/j.1365-2958.2007.06014.x · Cited by 85 · see citing works
The Anti-Candida Vaccine Based on the Recombinant N-Terminal Domain of Als1p Is Broadly Active against Disseminated Candidiasis
Ibrahim, A., Spellberg, B., Avanesian, V., Fu, Y., & Edwards, J. (2006) · Infection and Immunity · doi:10.1128/iai.74.5.3039-3041.2006 · Cited by 83 · see citing works
Recognition of Yeast by Murine Macrophages Requires Mannan but Not Glucan
Keppler‐Ross, S., Douglas, L. M., Konopka, J. B., & Dean, N. (2010) · Eukaryotic Cell · doi:10.1128/ec.00156-10 · Cited by 83 · see citing works
Regulation of Innate Immune Response toCandida albicansInfections by αMβ2-Pra1p Interaction
Soloviev, D. A., Jawhara, S., & Fonzi, W. A. (2011) · Infection and Immunity · doi:10.1128/iai.00650-10 · Cited by 82 · see citing works
Contribution of Candida albicans ALS1 to the Pathogenesis of Experimental Oropharyngeal Candidiasis
Kamai, Y., Kubota, M., Kamai, Y., Hosokawa, T., Fukuoka, T., & Filler, S. (2002) · Infection and Immunity · doi:10.1128/iai.70.9.5256-5258.2002 · Cited by 80 · see citing works
Localised PtdIns(3,4,5)P3 or PtdIns(3,4)P2 at the phagocytic cup is required for both phagosome closure and Ca2+ signalling in HL60 neutrophils
Dewitt, S., Tian, W., & Hallett, M. B. (2006) · Journal of Cell Science · doi:10.1242/jcs.02756 · Cited by 76 · see citing works
Coronin Function Is Required for Chemotaxis and Phagocytosis in Human Neutrophils
Yan, M., Ciano‐Oliveira, C. D., Grinstein, S., & Trimble, W. S. (2007) · The Journal of Immunology · doi:10.4049/jimmunol.178.9.5769 · Cited by 68 · see citing works
Distinct roles of complement receptor 3, Dectin-1, and sialic acids in murine macrophage interaction with Histoplasma yeast
Lin, J., Huang, J.-H., Hung, L., et al. (2010) · Journal of Leukocyte Biology · doi:10.1189/jlb.1109717 · Cited by 64 · see citing works
Breakthrough Candidemia in Patients with Cancer Differs from De Novo Candidemia in Host Factors andCandidaSpecies But Not Intensity
Kontoyiannis, D. P., Reddy, B. T., Hanna, H. A., Bodey, G. P., Tarrand, J. T., & RAAD, I. I. (2002) · Infection Control and Hospital Epidemiology · doi:10.1086/502104 · Cited by 55 · see citing works
A new method for studying the binding and ingestion of zymosan particles by macrophages
Lombard, Y., Giaimis, J., Makaya-Kumba, M., et al. (1994) · Journal of Immunological Methods · doi:10.1016/0022-1759(94)90018-3 · Cited by 51 · see citing works
Cytotoxic and cytokine-inducing properties of Candida glabrata in single and mixed oral infection models
Li, L., Kashleva, H., & Dongari‐Bagtzoglou, A. I. (2007) · Microbial Pathogenesis · doi:10.1016/j.micpath.2006.12.003 · Cited by 40 · see citing works
Heterogeneous distribution of Candida albicans cell-surface antigens demonstrated with an Als1-specific monoclonal antibody
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THIS ARTICLE HAS BEEN RETRACTED ï¿½Antifungal antibiotic hamycin increases susceptibility of Candida albicans to phagocytosis by murine macrophages
Dhuley, J. N. (1998) · FEMS Immunology & Medical Microbiology · doi:10.1111/j.1574-695x.1998.tb01122.x · Cited by 4 · see citing works
Retracted
Phagocytosis and intracellular killing of pathogenic yeasts by human monocytes and neutrophils
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Concanavalin A enhances phagocytosis and killing of Candida albicans by mice peritoneal neutrophils and macrophages
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Authors: Kuhn, D. M., & Vyas, V. K.
Affiliations: Whitehead Institute for Biomedical Research (US)
Corresponding author: Kuhn, Duncan M.
ORCID: Kuhn, Duncan M.
Vyas, Valmik K.
Venue: FEMS Yeast Research
Publisher: Oxford University Press (OUP)
Published: 2012-01-23
Volume: 12
Issue: 4
Pages: 398-414
ISSN: 1567-1356 (ISSN-L)
DOI: 10.1111/j.1567-1364.2011.00785.x
OpenAlex: W1986702564
Cited by: 38
References: 82
Citations by year: 2026: 2 · 2025: 1 · 2024: 4 · 2023: 3 · 2021: 1 · 2020: 3 · 2019: 2 · 2018: 4 · 2016: 7 · 2015: 4 · 2014: 2 · 2013: 4 · 2012: 1
FWCI: 2.43
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: FEMS Yeast Research (publishedVersion)
PubMed (publishedVersion)
Funders: National Institutes of Health (5t32hl007874-15, 5k08ai071023-03)
Whitehead Institute for Biomedical Research, Massachusetts Institute of Technology
National Heart, Lung, and Blood Institute (HL-07874)
National Institute of Allergy and Infectious Diseases (AI729353, AI071023-01A1)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords: Candida glabrata, fungal adhesins, macrophage adhesion, phagocytosis, innate immune response, cytokine production, interleukin-8, TNF-α, Dectin-1, host-pathogen interaction, fungal virulence
MeSH terms: Animals, Cell Adhesion, Cells, Cultured, Fungal Proteins, Humans, Macrophages, Phagocytosis, Saccharomyces cerevisiae, Transformation, Genetic, Gene Expression, Cytokines, Lectins, Candida glabrata, Mice

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The Candida glabrata adhesin Epa1p causes adhesion, phagocytosis, and cytokine secretion by innate immune cells

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