Candida albicans–epithelial interactions and induction of mucosal innate immunity

Moyes, 2014, Protection against epithelial damage during Candida albicans infection is mediated by PI3K/Akt and mammalian target of rapamycin signaling, J Infect Dis, 209, 1816, 10.1093/infdis/jit824 Moyes, 2010, A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells, Cell Host Microbe, 8, 225, 10.1016/j.chom.2010.08.002 de Koning, 2010, A comprehensive analysis of pattern recognition receptors in normal and inflamed human epidermis: upregulation of dectin-1 in psoriasis, J Investig Dermatol, 130, 2611, 10.1038/jid.2010.196 Naglik, 2011, Candida albicans interactions with epithelial cells and mucosal immunity, Microbes Infect, 13, 963, 10.1016/j.micinf.2011.06.009 Chaffin, 2008, Candida albicans cell wall proteins, Microbiol Mol Biol Rev, 72, 495, 10.1128/MMBR.00032-07 Munro, 2005, Mnt1p and Mnt2p of Candida albicans are partially redundant {alpha}-1, 2-mannosyltransferases that participate in O-linked mannosylation and are required for adhesion and virulence, J Biol Chem, 280, 1051, 10.1074/jbc.M411413200 Murciano, 2011, Candida albicans cell wall glycosylation may be indirectly required for activation of epithelial cell proinflammatory responses, Infect Immun, 79, 4902, 10.1128/IAI.05591-11 Staab, 1999, Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1, Science, 283, 1535, 10.1126/science.283.5407.1535 Hoyer, 1998, Candida albicans ALS3 and insights into the nature of the ALS gene family, Curr Genet, 33, 451, 10.1007/s002940050359 Zhao, 2004, ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p, Microbiology, 150, 2415, 10.1099/mic.0.26943-0 Naglik, 2006, Candida albicans HWP1 gene expression and host antibody responses in colonization and disease, J Med Microbiol, 55, 1323, 10.1099/jmm.0.46737-0 Sundstrom, 2002, Essential role of the Candida albicans transglutaminase substrate, hyphal wall protein 1, in lethal oroesophageal candidiasis in immunodeficient mice, J Infect Dis, 185, 521, 10.1086/338836 Phan, 2007, Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells, PLoS Biol, 5, e64, 10.1371/journal.pbio.0050064 Cota, 2015, The Candida albicans agglutinin-like sequence family of adhesins: functional insights gained from structural analysis, Future Microbiol, 10, 1548, 10.2217/fmb.15.79 Sun, 2010, Host cell invasion and virulence mediated by Candida albicans Ssa1, PLoS Pathog, 6, e1001181, 10.1371/journal.ppat.1001181 Zhu, 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, 10.1073/pnas.1117676109 Wachtler, 2011, From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells, PLoS ONE, 6, e17046, 10.1371/journal.pone.0017046 Liu, 2015, New signaling pathways govern the host response to C. albicans infection in various niches, Genome Res, 25, 679, 10.1101/gr.187427.114 Murciano, 2012, Evaluation of the role of Candida albicans agglutinin-like sequence (Als) proteins in human oral epithelial cell interactions, PLoS ONE, 7, e33362, 10.1371/journal.pone.0033362 Solis, 2017, The aryl hydrocarbon receptor governs epithelial cell invasion during oropharyngeal candidiasis, MBio, 8 Wachtler, 2012, Candida albicans–epithelial interactions: dissecting the roles of active penetration, induced endocytosis and host factors on the infection process, PLoS ONE, 7, e36952, 10.1371/journal.pone.0036952 Moyes, 2016, Candidalysin is a fungal peptide toxin critical for mucosal infection, Nature, 532, 64, 10.1038/nature17625 Moyes, 2011, Candida albicans yeast and hyphae are discriminated by MAPK signaling in vaginal epithelial cells, PLoS ONE, 6, e26580, 10.1371/journal.pone.0026580 Moyes, 2012, Activation of MAPK/c-Fos induced responses in oral epithelial cells is specific to Candida albicans and Candida dubliniensis hyphae, Med Microbiol Immunol, 201, 93, 10.1007/s00430-011-0209-y Naglik, 2014, Candida albicans pathogenicity and epithelial immunity, PLoS Pathog, 10, e1004257, 10.1371/journal.ppat.1004257 Tang, 2016, Epithelial discrimination of commensal and pathogenic Candida albicans, Oral Dis, 22, 114, 10.1111/odi.12395 Wilson, 2016, The missing link between Candida albicans hyphal morphogenesis and host cell damage, PLoS Pathog, 12, e1005867, 10.1371/journal.ppat.1005867 Guma, 2011, Constitutive intestinal NF-{kappa}B does not trigger destructive inflammation unless accompanied by MAPK activation, J Exp Med, 208, 1889, 10.1084/jem.20110242 Pukkila-Worley, 2011, Candida albicans infection of caenorhabditis elegans induces antifungal immune defenses, PLoS Pathog, 7, e1002074, 10.1371/journal.ppat.1002074 Conti, 2009, Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis, J Exp Med, 206, 299, 10.1084/jem.20081463 Naglik, 2014, Candida immunity, New J Sci, 2014, 10.1155/2014/390241 Duhring, 2015, Host–pathogen interactions between the human innate immune system and Candida albicans-understanding and modeling defense and evasion strategies, Front Microbiol, 6, 625, 10.3389/fmicb.2015.00625 Cheng, 2014, The interplay between central metabolism and innate immune responses, Cytokine Growth Factor Rev, 25, 707, 10.1016/j.cytogfr.2014.06.008 Cheng, 2012, Interplay between Candida albicans and the mammalian innate host defense, Infect Immun, 80, 1304, 10.1128/IAI.06146-11 Weindl, 2007, Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling, J Clin Invest, 117, 3664 Rubin-Bejerano, 2003, Phagocytosis by neutrophils induces an amino acid deprivation response in Saccharomyces cerevisiae and Candida albicans, Proc Natl Acad Sci U S A, 100, 11007, 10.1073/pnas.1834481100 Fradin, 2005, Granulocytes govern the transcriptional response, morphology and proliferation of Candida albicans in human blood, Mol Microbiol, 56, 397, 10.1111/j.1365-2958.2005.04557.x Gabrielli, 2016, In vivo induction of neutrophil chemotaxis by secretory aspartyl proteinases of Candida albicans, Virulence, 10.1080/21505594.2016.1184385 Urban, 2006, Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms, Cell Microbiol, 8, 668, 10.1111/j.1462-5822.2005.00659.x Urban, 2009, Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans, PLoS Pathog, 5, e1000639, 10.1371/journal.ppat.1000639 Kenny, 2017, Diverse stimuli engage different neutrophil extracellular trap pathways, Elife, 6 Kenno, 2016, Autophagy and reactive oxygen species are involved in neutrophil extracellular traps release induced by C. albicans morphotypes, Front Microbiol, 7, 879, 10.3389/fmicb.2016.00879 Ermert, 2009, Mouse neutrophil extracellular traps in microbial infections, J Innate Immun, 1, 181, 10.1159/000205281 Byrd, 2013, An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans, J Immunol, 190, 4136, 10.4049/jimmunol.1202671 Nani, 2014, Src family kinases and syk are required for neutrophil extracellular trap formation in response to beta-glucan particles, J Innate Immun Branzk, 2014, Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens, Nat Immunol, 15, 1017, 10.1038/ni.2987 Filler, 2006, Candida–host cell receptor–ligand interactions, Curr Opin Microbiol, 9, 333, 10.1016/j.mib.2006.06.005 Miramon, 2013, Thriving within the host: Candida spp. interactions with phagocytic cells, Med Microbiol Immunol, 202, 183, 10.1007/s00430-013-0288-z Wellington, 2014, Candida albicans triggers NLRP3-mediated pyroptosis in macrophages, Eukaryot Cell, 13, 329, 10.1128/EC.00336-13 Uwamahoro, 2014, The pathogen Candida albicans hijacks pyroptosis for escape from macrophages, MBio, 5, 10.1128/mBio.00003-14 McKenzie, 2010, Contribution of Candida albicans cell wall components to recognition by and escape from murine macrophages, Infect Immun, 78, 1650, 10.1128/IAI.00001-10 O’Meara, 2015, Global analysis of fungal morphology exposes mechanisms of host cell escape, Nat Commun, 6, 6741, 10.1038/ncomms7741 Wellington, 2012, Candida albicans morphogenesis is not required for macrophage interleukin 1beta production, MBio, 4 Vylkova, 2014, Modulation of phagosomal pH by Candida albicans promotes hyphal morphogenesis and requires Stp2p, a regulator of amino acid transport, PLoS Pathog, 10, e1003995, 10.1371/journal.ppat.1003995 van de Veerdonk, 2011, The inflammasome drives protective Th1 and Th17 cellular responses in disseminated candidiasis, Eur J Immunol, 41, 2260, 10.1002/eji.201041226 Ho, 2010, IL-17RC is required for immune signaling via an extended SEF/IL-17R signaling domain in the cytoplasmic tail, J Immunol, 185, 1063, 10.4049/jimmunol.0903739 Ferreira, 2014, Interleukin-17-induced protein lipocalin 2 is dispensable for immunity to oral candidiasis, Infect Immun, 82, 1030, 10.1128/IAI.01389-13 Puel, 2011, Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity, Science, 332, 65, 10.1126/science.1200439 Boisson, 2013, An ACT1 mutation selectively abolishes interleukin-17 responses in humans with chronic mucocutaneous candidiasis, Immunity, 39, 676, 10.1016/j.immuni.2013.09.002 Ling, 2015, Inherited IL-17RC deficiency in patients with chronic mucocutaneous candidiasis, J Exp Med, 212, 619, 10.1084/jem.20141065 Conti, 2015, IL-17-mediated immunity to the opportunistic fungal pathogen Candida albicans, J Immunol, 195, 780, 10.4049/jimmunol.1500909 Conti, 2014, Oral-resident natural Th17 cells and gammadelta T cells control opportunistic Candida albicans infections, J Exp Med, 211, 2075, 10.1084/jem.20130877 Gladiator, 2013, Cutting edge: IL-17-secreting innate lymphoid cells are essential for host defense against fungal infection, J Immunol, 190, 521, 10.4049/jimmunol.1202924 Huppler, 2015, Neutrophils do not express IL-17A in the context of acute oropharyngeal candidiasis, Pathogens, 4, 559, 10.3390/pathogens4030559 LeibundGut-Landmann, 2007, Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17, Nat Immunol, 8, 630, 10.1038/ni1460 Bishu, 2014, The adaptor CARD9 is required for adaptive but not innate immunity to oral mucosal Candida albicans infections, Infect Immun, 82, 1173, 10.1128/IAI.01335-13 Verma, 2017, Oral epithelial cells orchestrate innate type 17 responses to Candida albicans through the virulence factor Candidalysin, Sci Immunol, 2, eaam8834, 10.1126/sciimmunol.aam8834 Hise, 2009, An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans, Cell Host Microbe, 5, 487, 10.1016/j.chom.2009.05.002 Altmeier, 2016, IL-1 coordinates the neutrophil response to C. albicans in the oral mucosa, PLoS Pathog, 12, e1005882, 10.1371/journal.ppat.1005882 Conti, 2016, IL-17 receptor signaling in oral epithelial cells is critical for protection against oropharyngeal candidiasis, Cell Host Microbe, 20, 606, 10.1016/j.chom.2016.10.001 Trautwein-Weidner, 2015, Antigen-specific Th17 cells are primed by distinct and complementary dendritic cell subsets in oropharyngeal candidiasis, PLoS Pathog, 11, e1005164, 10.1371/journal.ppat.1005164 Tomalka, 2015, beta-Defensin 1 plays a role in acute mucosal defense against Candida albicans, J Immunol, 194, 1788, 10.4049/jimmunol.1203239 Conti, 2011, New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome, Mucosal Immunol, 4, 448, 10.1038/mi.2011.5 Tati, 2016, Candida glabrata binding to Candida albicans hyphae enables its development in oropharyngeal candidiasis, PLoS Pathog, 12, e1005522, 10.1371/journal.ppat.1005522 Milner, 2013, The cup runneth over: lessons from the ever-expanding pool of primary immunodeficiency diseases, Nat Rev Immunol, 13, 635, 10.1038/nri3493 Klatt, 2010, Th17 cell dynamics in HIV infection, Curr Opin HIV AIDS, 5, 135, 10.1097/COH.0b013e3283364846 Sanford, 2015, Secukinumab: first global approval, Drugs, 75, 329, 10.1007/s40265-015-0359-0 Langley, 2014, Secukinumab in plaque psoriasis—results of two phase 3 trials, N Engl J Med, 371, 326, 10.1056/NEJMoa1314258 Whibley, 2016, Antibody blockade of IL-17 family cytokines in immunity to acute murine oral mucosal candidiasis, J Leukoc Biol, 99, 1153, 10.1189/jlb.4A0915-428R Zhu, 2010, Interactions of Candida albicans with epithelial cells, Cell Microbiol, 12, 273, 10.1111/j.1462-5822.2009.01412.x Hoyer, 2016, Candida albicans agglutinin-like sequence (Als) family vignettes: a review of Als protein structure and function, Front Microbiol, 7, 10.3389/fmicb.2016.00280 Yan, 2010, Backbone 1H, 15N, 13C and Ile, Leu, Val methyl chemical shift assignments for the 33.5kDa N-terminal domain of Candida albicans ALS1, Biomol NMR Assign, 4, 187, 10.1007/s12104-010-9243-8 Lin, 2014, The peptide-binding cavity is essential for Als3-mediated adhesion of Candida albicans to human cells, J Biol Chem, 289, 18401, 10.1074/jbc.M114.547877 Gale, 1998, Linkage of adhesion, filamentous growth, and virulence in Candida albicans to a single gene, INT1, Science, 279, 1355, 10.1126/science.279.5355.1355 Naglik, 2003, Candida albicans secreted aspartyl proteinases in virulence and pathogenesis, Microbiol Mol Biol Rev, 67, 400, 10.1128/MMBR.67.3.400-428.2003 Villar, 2007, Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p, Infect Immun, 75, 2126, 10.1128/IAI.00054-07 Mukherjee, 2001, Reintroduction of the PLB1 gene into Candida albicans restores virulence in vivo, Microbiology, 147, 2585, 10.1099/00221287-147-9-2585 Schofield, 2005, Differential Candida albicans lipase gene expression during alimentary tract colonization and infection, FEMS Microbiol Lett, 244, 359, 10.1016/j.femsle.2005.02.015