Candida albicans Interactions with Mucosal Surfaces during Health and Disease
Abstract
:1. Introduction
2. Adhesion of C. albicans to the Epithelium
3. Structural and Mechanistic Aspects of Adhesion to the Epithelial Surface
4. The Commensal Relationship with the Host
5. Invasion of the Mucosal Surface
6. Epithelial Recognition of C. albicans
7. Epithelial Responses to C. albicans
8. Secreted Fungal Factors
9. Acquisition of Micronutrients
9.1. Assimilation of Zinc
9.2. Iron Uptake
9.3. Copper
10. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Hallen-Adams, H.E.; Suhr, M.J. Fungi in the healthy human gastrointestinal tract. Virulence 2017, 8, 352–358. [Google Scholar] [CrossRef] [PubMed]
- Huffnagle, G.B.; Noverr, M.C. The emerging world of the fungal microbiome. Trends Microbiol. 2013, 21, 334–341. [Google Scholar] [CrossRef] [PubMed]
- Calderone, R.A.; Fonzi, W.A. Virulence factors of Candida albicans. Trends Microbiol. 2001, 9, 327–335. [Google Scholar] [CrossRef]
- Gulati, M.; Nobile, C.J. Candida albicans biofilms: Development, regulation, and molecular mechanisms. Microbes Infect. 2016, 18, 310–321. [Google Scholar] [CrossRef] [PubMed]
- de Repentigny, L.; Aumont, F.; Bernard, K.; Belhumeur, P. Characterization of binding of Candida albicans to small intestinal mucin and its role in adherence to mucosal epithelial cells. Infect. Immun. 2000, 68, 3172–3179. [Google Scholar] [CrossRef] [PubMed]
- Williams, D.W.; Jordan, R.P.; Wei, X.Q.; Alves, C.T.; Wise, M.P.; Wilson, M.J.; Lewis, M.A. Interactions of Candida albicans with host epithelial surfaces. J. Oral Microbiol. 2013, 5, 22434. [Google Scholar] [CrossRef] [PubMed]
- Hobden, C.; Teevan, C.; Jones, L.; O’Shea, P. Hydrophobic properties of the cell surface of Candida albicans: A role in aggregation. Microbiology 1995, 141 Pt 8, 1875–1881. [Google Scholar] [CrossRef]
- Douglas, L.J. Adhesion of Candida species to epithelial surfaces. Crit. Rev. Microbiol. 1987, 15, 27–43. [Google Scholar] [CrossRef]
- Hazen, K.C. Participation of yeast cell surface hydrophobicity in adherence of Candida albicans to human epithelial cells. Infect. Immun. 1989, 57, 1894–1900. [Google Scholar]
- Hazen, K.C.; Lay, J.G.; Hazen, B.W.; Fu, R.C.; Murthy, S. Partial biochemical characterization of cell surface hydrophobicity and hydrophilicity of Candida albicans. Infect. Immun. 1990, 58, 3469–3476. [Google Scholar]
- Jones, D.S.; Schep, L.J.; Shepherd, M.G. The effect of cetylpyridinium chloride (cpc) on the cell surface hydrophobicity and adherence of Candida albicans to human buccal epithelial cells in vitro. Pharm. Res. 1995, 12, 1896–1900. [Google Scholar] [CrossRef]
- Skerl, K.G.; Calderone, R.A.; Segal, E.; Sreevalsan, T.; Scheld, W.M. In vitro binding of Candida albicans yeast cells to human fibronectin. Can. J. Microbiol. 1984, 30, 221–227. [Google Scholar] [CrossRef] [PubMed]
- Klotz, S.A.; Smith, R.L. A fibronectin receptor on Candida albicans mediates adherence of the fungus to extracellular matrix. J. Infect. Dis. 1991, 163, 604–610. [Google Scholar] [CrossRef]
- O’Sullivan, J.M.; Cannon, R.D.; Sullivan, P.A.; Jenkinson, H.F. Identification of salivary basic proline-rich proteins as receptors for Candida albicans adhesion. Microbiology 1997, 143 Pt 2, 341–348. [Google Scholar] [CrossRef]
- Enache, E.; Eskandari, T.; Borja, L.; Wadsworth, E.; Hoxter, B.; Calderone, R. Candida albicans adherence to a human oesophageal cell line. Microbiology 1996, 142 Pt 10, 2741–2746. [Google Scholar] [CrossRef]
- Samaranayake, L.P.; MacFarlane, T.W. The effect of dietary carbohydrates on the in-vitro adhesion of Candida albicans to epithelial cells. J. Med. Microbiol. 1982, 15, 511–517. [Google Scholar] [CrossRef]
- Hoyer, L.L.; Green, C.B.; Oh, S.H.; Zhao, X. Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—A sticky pursuit. Med. Mycol. 2008, 46, 1–15. [Google Scholar] [CrossRef]
- Gaur, N.K.; Klotz, S.A. Expression, cloning, and characterization of a Candida albicans gene, ALA1, that confers adherence properties upon Saccharomyces cerevisiae for extracellular matrix proteins. Infect. Immun. 1997, 65, 5289–5294. [Google Scholar] [PubMed]
- Gaur, N.K.; Klotz, S.A.; Henderson, R.L. Overexpression of the Candida albicans ALA1 gene in Saccharomyces cerevisiae results in aggregation following attachment of yeast cells to extracellular matrix proteins, adherence properties similar to those of Candida albicans. Infect. Immun. 1999, 67, 6040–6047. [Google Scholar] [PubMed]
- Gaur, N.K.; Smith, R.L.; Klotz, S.A. Candida albicans and Saccharomyces cerevisiae expressing ALA1/ALS5 adhere to accessible threonine, serine, or alanine patches. Cell Commun. Adhes. 2002, 9, 45–57. [Google Scholar] [CrossRef] [PubMed]
- Rauceo, J.M.; Gaur, N.K.; Lee, K.G.; Edwards, J.E.; Klotz, S.A.; Lipke, P.N. Global cell surface conformational shift mediated by a Candida albicans adhesin. Infect. Immun. 2004, 72, 4948–4955. [Google Scholar] [CrossRef] [PubMed]
- Rauceo, J.M.; De Armond, R.; Otoo, H.; Kahn, P.C.; Klotz, S.A.; Gaur, N.K.; Lipke, P.N. Threonine-rich repeats increase fibronectin binding in the Candida albicans adhesin Als5p. Eukaryot. Cell 2006, 5, 1664–1673. [Google Scholar] [CrossRef] [PubMed]
- Bois, M.; Singh, S.; Samlalsingh, A.; Lipke, P.N.; Garcia, M.C. Does Candida albicans Als5p amyloid play a role in commensalism in Caenorhabditis elegans? Eukaryot. Cell 2013, 12, 703–711. [Google Scholar] [CrossRef] [PubMed]
- Alsteens, D.; Garcia, M.C.; Lipke, P.N.; Dufrene, Y.F. Force-induced formation and propagation of adhesion nanodomains in living fungal cells. Proc. Natl. Acad. Sci. USA 2010, 107, 20744–20749. [Google Scholar] [CrossRef]
- Lipke, P.N.; Garcia, M.C.; Alsteens, D.; Ramsook, C.B.; Klotz, S.A.; Dufrene, Y.F. Strengthening relationships: Amyloids create adhesion nanodomains in yeasts. Trends Microbiol. 2012, 20, 59–65. [Google Scholar] [CrossRef] [PubMed]
- Cheng, G.; Wozniak, K.; Wallig, M.A.; Fidel, P.L., Jr.; Trupin, S.R.; Hoyer, L.L. Comparison between Candida albicans agglutinin-like sequence gene expression patterns in human clinical specimens and models of vaginal candidiasis. Infect. Immun. 2005, 73, 1656–1663. [Google Scholar] [CrossRef]
- Dranginis, A.M.; Rauceo, J.M.; Coronado, J.E.; Lipke, P.N. A biochemical guide to yeast adhesins: Glycoproteins for social and antisocial occasions. Microbiol. Mol. Biol. Rev. 2007, 71, 282–294. [Google Scholar] [CrossRef] [PubMed]
- Phan, Q.T.; Myers, C.L.; Fu, Y.; Sheppard, D.C.; Yeaman, M.R.; Welch, W.H.; Ibrahim, A.S.; Edwards, J.E., Jr.; Filler, S.G. Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol. 2007, 5, e64. [Google Scholar] [CrossRef]
- Zhu, W.; Phan, Q.T.; Boontheung, P.; Solis, N.V.; Loo, J.A.; Filler, S.G. EGFR and HER2 receptor kinase signaling mediate epithelial cell invasion by Candida albicans during oropharyngeal infection. Proc. Natl. Acad. Sci. USA 2012, 109, 14194–14199. [Google Scholar] [CrossRef]
- Murciano, C.; Moyes, D.L.; Runglall, M.; Tobouti, P.; Islam, A.; Hoyer, L.L.; Naglik, J.R. Evaluation of the role of Candida albicans agglutinin-like sequence (ALS) proteins in human oral epithelial cell interactions. PLoS ONE 2012, 7, e33362. [Google Scholar] [CrossRef]
- Laforce-Nesbitt, S.S.; Sullivan, M.A.; Hoyer, L.L.; Bliss, J.M. Inhibition of Candida albicans adhesion by recombinant human antibody single-chain variable fragment specific for Als3p. FEMS Immunol. Med. Microbiol. 2008, 54, 195–202. [Google Scholar] [CrossRef] [PubMed]
- Kamai, Y.; Kubota, M.; Kamai, Y.; Hosokawa, T.; Fukuoka, T.; Filler, S.G. Contribution of Candida albicans ALS1 to the pathogenesis of experimental oropharyngeal candidiasis. Infect. Immun. 2002, 70, 5256–5258. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Oh, S.H.; Cheng, G.; Green, C.B.; Nuessen, J.A.; Yeater, K.; Leng, R.P.; Brown, A.J.; Hoyer, L.L. ALS3 and ALS8 represent a single locus that encodes a Candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology 2004, 150, 2415–2428. [Google Scholar] [CrossRef] [PubMed]
- Zhao, X.; Oh, S.H.; Yeater, K.M.; Hoyer, L.L. Analysis of the Candida albicans Als2p and Als4p adhesins suggests the potential for compensatory function within the ALS family. Microbiology 2005, 151, 1619–1630. [Google Scholar] [CrossRef] [PubMed]
- Sohn, K.; Urban, C.; Brunner, H.; Rupp, S. EFG1 is a major regulator of cell wall dynamics in Candida albicans as revealed by DNA microarrays. Mol. Microbiol. 2003, 47, 89–102. [Google Scholar] [CrossRef] [PubMed]
- Granger, B.L.; Flenniken, M.L.; Davis, D.A.; Mitchell, A.P.; Cutler, J.E. Yeast wall protein 1 of Candida albicans. Microbiology 2005, 151, 1631–1644. [Google Scholar] [CrossRef]
- Granger, B.L. Insight into the antiadhesive effect of yeast wall protein 1 of Candida albicans. Eukaryot. Cell 2012, 11, 795–805. [Google Scholar] [CrossRef]
- Zhao, X.; Oh, S.H.; Hoyer, L.L. Deletion of ALS5, ALS6 or ALS7 increases adhesion of Candida albicans to human vascular endothelial and buccal epithelial cells. Med. Mycol. 2007, 45, 429–434. [Google Scholar] [CrossRef] [PubMed]
- Sandin, R.L.; Rogers, A.L.; Patterson, R.J.; Beneke, E.S. Evidence for mannose-mediated adherence of Candida albicans to human buccal cells in vitro. Infect. Immun. 1982, 35, 79–85. [Google Scholar] [PubMed]
- Willaert, R.G. Adhesins of yeasts: Protein structure and interactions. J. Fungi 2018, 4, 119. [Google Scholar] [CrossRef] [PubMed]
- Staab, J.F.; Bahn, Y.S.; Tai, C.H.; Cook, P.F.; Sundstrom, P. Expression of transglutaminase substrate activity on Candida albicans germ tubes through a coiled, disulfide-bonded N-terminal domain of Hwp1 requires C-terminal glycosylphosphatidylinositol modification. J. Biol. Chem. 2004, 279, 40737–40747. [Google Scholar] [CrossRef]
- Hoyer, L.L.; Cota, E. Candida albicans agglutinin-like sequence (ALS) family vignettes: A review of ALS protein structure and function. Front. Microbiol. 2016, 7, 280. [Google Scholar] [CrossRef]
- Cota, E.; Hoyer, L.L. The Candida albicans agglutinin-like sequence family of adhesins: Functional insights gained from structural analysis. Future Microbiol. 2015, 10. [Google Scholar] [CrossRef] [PubMed]
- Silva-Dias, A.; Miranda, I.M.; Branco, J.; Monteiro-Soares, M.; Pina-Vaz, C.; Rodrigues, A.G. Adhesion, biofilm formation, cell surface hydrophobicity, and antifungal planktonic susceptibility: Relationship among Candida spp. Front. Microbiol. 2015, 6, 205. [Google Scholar] [CrossRef] [PubMed]
- Gaur, N.K.; Klotz, S.A. Accessibility of the peptide backbone of protein ligands is a key specificity determinant in Candida albicans SRS adherence. Microbiology 2004, 150, 277–284. [Google Scholar] [CrossRef]
- 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.; Edwards, J.E., Jr. Functional and structural diversity in the ALS protein family of Candida albicans. J. Biol. Chem. 2004, 279, 30480–30489. [Google Scholar] [CrossRef] [PubMed]
- Almeida, R.S.; Brunke, S.; Albrecht, A.; Thewes, S.; Laue, M.; Edwards, J.E.; Filler, S.G.; Hube, B. The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog. 2008, 4, e1000217. [Google Scholar] [CrossRef]
- Liu, Y.; Mittal, R.; Solis, N.V.; Prasadarao, N.V.; Filler, S.G. Mechanisms of Candida albicans trafficking to the brain. PLoS Pathog. 2011, 7, e1002305. [Google Scholar] [CrossRef]
- Salgado, P.S.; Yan, R.; Taylor, J.D.; Burchell, L.; Jones, R.; Hoyer, L.L.; Matthews, S.J.; Simpson, P.J.; Cota, E. Structural basis for the broad specificity to host-cell ligands by the pathogenic fungus Candida albicans. Proc. Natl. Acad. Sci. USA 2011, 108, 15775–15779. [Google Scholar] [CrossRef] [PubMed]
- Lin, J.; Oh, S.H.; Jones, R.; Garnett, J.A.; Salgado, P.S.; Rusnakova, S.; Matthews, S.J.; Hoyer, L.L.; Cota, E. The peptide-binding cavity is essential for Als3-mediated adhesion of Candida albicans to human cells. J. Biol. Chem. 2014, 289, 18401–18412. [Google Scholar] [CrossRef]
- Hoyer, L.L.; Oh, S.H.; Jones, R.; Cota, E. A proposed mechanism for the interaction between the Candida albicans Als3 adhesin and streptococcal cell wall proteins. Front. Microbiol. 2014, 5, 564. [Google Scholar] [CrossRef] [PubMed]
- Klotz, S.A.; Gaur, N.K.; Lake, D.F.; Chan, V.; Rauceo, J.; Lipke, P.N. Degenerate peptide recognition by Candida albicans adhesins Als5p and Als1p. Infect. Immun. 2004, 72, 2029–2034. [Google Scholar] [CrossRef] [PubMed]
- Otoo, H.N.; Lee, K.G.; Qiu, W.; Lipke, P.N. Candida albicans Als adhesins have conserved amyloid-forming sequences. Eukaryot. Cell 2008, 7, 776–782. [Google Scholar] [CrossRef] [PubMed]
- Lipke, P.N.; Klotz, S.A.; Dufrene, Y.F.; Jackson, D.N.; Garcia-Sherman, M.C. Amyloid-like beta-aggregates as force-sensitive switches in fungal biofilms and infections. Microbiol. Mol. Biol. Rev. 2018, 82, e00035-17. [Google Scholar] [PubMed]
- Witchley, J.N.; Penumetcha, P.; Abon, N.V.; Woolford, C.A.; Mitchell, A.P.; Noble, S.M. Candida albicans morphogenesis programs control the balance between gut commensalism and invasive infection. Cell Host Microbe 2019, 25, 432.e6–443.e6. [Google Scholar] [CrossRef]
- Prieto, D.; Pla, J. Distinct stages during colonization of the mouse gastrointestinal tract by Candida albicans. Front. Microbiol. 2015, 6, 792. [Google Scholar] [CrossRef]
- Prieto, D.; Roman, E.; Correia, I.; Pla, J. The Hog pathway is critical for the colonization of the mouse gastrointestinal tract by Candida albicans. PLoS ONE 2014, 9, e87128. [Google Scholar] [CrossRef]
- Perez, J.C.; Kumamoto, C.A.; Johnson, A.D. Candida albicans commensalism and pathogenicity are intertwined traits directed by a tightly knit transcriptional regulatory circuit. PLoS Biol. 2013, 11, e1001510. [Google Scholar] [CrossRef] [PubMed]
- Shao, T.Y.; Ang, W.X.G.; Jiang, T.T.; Huang, F.S.; Andersen, H.; Kinder, J.M.; Pham, G.; Burg, A.R.; Ruff, B.; Gonzalez, T.; et al. Commensal Candida albicans positively calibrates systemic Th17 immunological responses. Cell Host Microbe 2019, 25, 404.e6–417.e6. [Google Scholar] [CrossRef]
- Bacher, P.; Hohnstein, T.; Beerbaum, E.; Rocker, M.; Blango, M.G.; Kaufmann, S.; Rohmel, J.; Eschenhagen, P.; Grehn, C.; Seidel, K.; et al. Human anti-fungal Th17 immunity and pathology rely on cross-reactivity against Candida albicans. Cell 2019, 176, 1340.e15–1355.e15. [Google Scholar] [CrossRef] [PubMed]
- Pierce, J.V.; Kumamoto, C.A. Variation in candida albicans EFG1 expression enables host-dependent changes in colonizing fungal populations. MBio 2012, 3, e00117-12. [Google Scholar] [CrossRef] [PubMed]
- Liang, S.H.; Anderson, M.Z.; Hirakawa, M.P.; Wang, J.M.; Frazer, C.; Alaalm, L.M.; Thomson, G.J.; Ene, I.V.; Bennett, R.J. Hemizygosity enables a mutational transition governing fungal virulence and commensalism. Cell Host Microbe 2019, 25, 418.e6–431.e6. [Google Scholar] [CrossRef]
- Pande, K.; Chen, C.; Noble, S.M. Passage through the mammalian gut triggers a phenotypic switch that promotes Candida albicans commensalism. Nat. Genet. 2013, 45, 1088–1091. [Google Scholar] [CrossRef]
- Xie, J.; Tao, L.; Nobile, C.J.; Tong, Y.; Guan, G.; Sun, Y.; Cao, C.; Hernday, A.D.; Johnson, A.D.; Zhang, L.; et al. White-opaque switching in natural MTLa/α isolates of Candida albicans: Evolutionary implications for roles in host adaptation, pathogenesis, and sex. PLoS Biol. 2013, 11, e1001525. [Google Scholar] [CrossRef] [PubMed]
- Tso, G.H.W.; Reales-Calderon, J.A.; Tan, A.S.M.; Sem, X.; Le, G.T.T.; Tan, T.G.; Lai, G.C.; Srinivasan, K.G.; Yurieva, M.; Liao, W.; et al. Experimental evolution of a fungal pathogen into a gut symbiont. Science 2018, 362, 589–595. [Google Scholar] [CrossRef] [PubMed]
- Moreno-Ruiz, E.; Galan-Diez, M.; Zhu, W.; Fernandez-Ruiz, E.; d’Enfert, C.; Filler, S.G.; Cossart, P.; Veiga, E. Candida albicans internalization by host cells is mediated by a clathrin-dependent mechanism. Cell Microbiol. 2009, 11, 1179–1189. [Google Scholar] [CrossRef]
- Atre, A.N.; Surve, S.V.; Shouche, Y.S.; Joseph, J.; Patole, M.S.; Deopurkar, R.L. Association of small Rho GTPases and actin ring formation in epithelial cells during the invasion by Candida albicans. FEMS Immunol. Med. Microbiol. 2009, 55, 74–84. [Google Scholar] [CrossRef]
- Solis, N.V.; Swidergall, M.; Bruno, V.M.; Gaffen, S.L.; Filler, S.G. The aryl hydrocarbon receptor governs epithelial cell invasion during oropharyngeal candidiasis. MBio 2017, 8, e00025-17. [Google Scholar] [CrossRef]
- Liu, Y.; Shetty, A.C.; Schwartz, J.A.; Bradford, L.L.; Xu, W.; Phan, Q.T.; Kumari, P.; Mahurkar, A.; Mitchell, A.P.; Ravel, J.; et al. New signaling pathways govern the host response to C. albicans infection in various niches. Genome Res. 2015, 25, 679–689. [Google Scholar] [CrossRef] [PubMed]
- Nucci, M.; Anaissie, E. Revisiting the source of candidemia: Skin or gut? Clin. Infect. Dis. 2001, 33, 1959–1967. [Google Scholar] [CrossRef]
- Bougnoux, M.E.; Diogo, D.; Francois, N.; Sendid, B.; Veirmeire, S.; Colombel, J.F.; Bouchier, C.; Van Kruiningen, H.; d’Enfert, C.; Poulain, D. Multilocus sequence typing reveals intrafamilial transmission and microevolutions of Candida albicans isolates from the human digestive tract. J. Clin. Microbiol. 2006, 44, 1810–1820. [Google Scholar] [CrossRef] [PubMed]
- Gouba, N.; Drancourt, M. Digestive tract mycobiota: A source of infection. Med. Mal. Infect. 2015, 45, 9–16. [Google Scholar] [CrossRef]
- Allert, S.; Forster, T.M.; Svensson, C.M.; Richardson, J.P.; Pawlik, T.; Hebecker, B.; Rudolphi, S.; Juraschitz, M.; Schaller, M.; Blagojevic, M.; et al. Candida albicans-induced epithelial damage mediates translocation through intestinal barriers. MBio 2018, 9, e00915-18. [Google Scholar] [CrossRef] [PubMed]
- Colina, A.R.; Aumont, F.; Deslauriers, N.; Belhumeur, P.; de Repentigny, L. Evidence for degradation of gastrointestinal mucin by Candida albicans secretory aspartyl proteinase. Infect. Immun. 1996, 64, 4514–4519. [Google Scholar] [PubMed]
- Villar, C.C.; Kashleva, H.; Nobile, C.J.; Mitchell, A.P.; Dongari-Bagtzoglou, A. Mucosal tissue invasion by Candida albicans is associated with E-cadherin degradation, mediated by transcription factor Rim101p and protease Sap5p. Infect. Immun. 2007, 75, 2126–2135. [Google Scholar] [CrossRef] [PubMed]
- Dalle, F.; Wachtler, B.; L’Ollivier, C.; Holland, G.; Bannert, N.; Wilson, D.; Labruere, C.; Bonnin, A.; Hube, B. Cellular interactions of Candida albicans with human oral epithelial cells and enterocytes. Cell Microbiol. 2010, 12, 248–271. [Google Scholar] [CrossRef] [PubMed]
- Albac, S.; Schmitz, A.; Lopez-Alayon, C.; d’Enfert, C.; Sautour, M.; Ducreux, A.; Labruere-Chazal, C.; Laue, M.; Holland, G.; Bonnin, A.; et al. Candida albicans is able to use M cells as a portal of entry across the intestinal barrier in vitro. Cell Microbiol. 2016, 18, 195–210. [Google Scholar] [CrossRef] [PubMed]
- Goyer, M.; Loiselet, A.; Bon, F.; L’Ollivier, C.; Laue, M.; Holland, G.; Bonnin, A.; Dalle, F. Intestinal cell tight junctions limit invasion of Candida albicans through active penetration and endocytosis in the early stages of the interaction of the fungus with the intestinal barrier. PLoS ONE 2016, 11, e0149159. [Google Scholar] [CrossRef]
- Pappas, P.G.; Lionakis, M.S.; Arendrup, M.C.; Ostrosky-Zeichner, L.; Kullberg, B.J. Invasive candidiasis. Nat. Rev. Dis. Primers 2018, 4, 18026. [Google Scholar] [CrossRef]
- Gow, N.A.; van de Veerdonk, F.L.; Brown, A.J.; Netea, M.G. Candida albicans morphogenesis and host defence: Discriminating invasion from colonization. Nat. Rev. Microbiol. 2011, 10, 112–122. [Google Scholar] [CrossRef]
- Underhill, D.M.; Pearlman, E. Immune interactions with pathogenic and commensal fungi: A two-way street. Immunity 2015, 43, 845–858. [Google Scholar] [CrossRef] [PubMed]
- Naglik, J.R.; Konig, A.; Hube, B.; Gaffen, S.L. Candida albicans-epithelial interactions and induction of mucosal innate immunity. Curr. Opin. Microbiol. 2017, 40, 104–112. [Google Scholar] [CrossRef] [PubMed]
- Ozinsky, A.; Underhill, D.M.; Fontenot, J.D.; Hajjar, A.M.; Smith, K.D.; Wilson, C.B.; Schroeder, L.; Aderem, A. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc. Natl. Acad. Sci. USA 2000, 97, 13766–13771. [Google Scholar] [CrossRef] [PubMed]
- Bellocchio, S.; Montagnoli, C.; Bozza, S.; Gaziano, R.; Rossi, G.; Mambula, S.S.; Vecchi, A.; Mantovani, A.; Levitz, S.M.; Romani, L. The contribution of the toll-like/Il-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J. Immunol. 2004, 172, 3059–3069. [Google Scholar] [CrossRef]
- Netea, M.G.; Gow, N.A.; Munro, C.A.; Bates, S.; Collins, C.; Ferwerda, G.; Hobson, R.P.; Bertram, G.; Hughes, H.B.; Jansen, T.; et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and toll-like receptors. J. Clin. Investig. 2006, 116, 1642–1650. [Google Scholar] [CrossRef]
- Weindl, G.; Naglik, J.R.; Kaesler, S.; Biedermann, T.; Hube, B.; Korting, H.C.; Schaller, M. Human epithelial cells establish direct antifungal defense through TLR4-mediated signaling. J. Clin. Investig. 2007, 117, 3664–3672. [Google Scholar] [CrossRef]
- Weindl, G.; Wagener, J.; Schaller, M. Epithelial cells and innate antifungal defense. J. Dent. Res. 2010, 89, 666–675. [Google Scholar] [CrossRef]
- Pinheiro, C.R.; Coelho, A.L.; de Oliveira, C.E.; Gasparoto, T.H.; Garlet, G.P.; Silva, J.S.; Santos, C.F.; Cavassani, K.A.; Hogaboam, C.M.; Campanelli, A.P. Recognition of Candida albicans by gingival fibroblasts: The role of TLR2, TLR4/CD14, and MyD88. Cytokine 2018, 106, 67–75. [Google Scholar] [CrossRef]
- Rosentul, D.C.; Delsing, C.E.; Jaeger, M.; Plantinga, T.S.; Oosting, M.; Costantini, I.; Venselaar, H.; Joosten, L.A.; van der Meer, J.W.; Dupont, B.; et al. Gene polymorphisms in pattern recognition receptors and susceptibility to idiopathic recurrent vulvovaginal candidiasis. Front. Microbiol. 2014, 5, 483. [Google Scholar] [CrossRef]
- Brown, G.D.; Gordon, S. Immune recognition. A new receptor for beta-glucans. Nature 2001, 413, 36–37. [Google Scholar] [CrossRef]
- Taylor, P.R.; Tsoni, S.V.; Willment, J.A.; Dennehy, K.M.; Rosas, M.; Findon, H.; Haynes, K.; Steele, C.; Botto, M.; Gordon, S.; et al. Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat. Immunol. 2007, 8, 31–38. [Google Scholar] [CrossRef] [PubMed]
- Reid, D.M.; Gow, N.A.; Brown, G.D. Pattern recognition: Recent insights from dectin-1. Curr. Opin. Immunol. 2009, 21, 30–37. [Google Scholar] [CrossRef] [PubMed]
- Swidergall, M.; Solis, N.V.; Lionakis, M.S.; Filler, S.G. Epha2 is an epithelial cell pattern recognition receptor for fungal beta-glucans. Nat. Microbiol. 2018, 3, 53–61. [Google Scholar] [CrossRef] [PubMed]
- Moyes, D.L.; Shen, C.; Murciano, C.; Runglall, M.; Richardson, J.P.; Arno, M.; Aldecoa-Otalora, E.; Naglik, J.R. Protection against epithelial damage during Candida albicans infection is mediated by PI3K/AKT and mammalian target of rapamycin signaling. J. Infect. Dis. 2014, 209, 1816–1826. [Google Scholar] [CrossRef] [PubMed]
- Ferwerda, B.; Ferwerda, G.; Plantinga, T.S.; Willment, J.A.; van Spriel, A.B.; Venselaar, H.; Elbers, C.C.; Johnson, M.D.; Cambi, A.; Huysamen, C.; et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N. Engl. J. Med. 2009, 361, 1760–1767. [Google Scholar] [CrossRef] [PubMed]
- Moyes, D.L.; Runglall, M.; Murciano, C.; Shen, C.; Nayar, D.; Thavaraj, S.; Kohli, A.; Islam, A.; Mora-Montes, H.; Challacombe, S.J.; et al. A biphasic innate immune MAPK response discriminates between the yeast and hyphal forms of Candida albicans in epithelial cells. Cell Host Microbe 2010, 8, 225–235. [Google Scholar] [CrossRef] [PubMed]
- Moyes, D.L.; Murciano, C.; Runglall, M.; Islam, A.; Thavaraj, S.; Naglik, J.R. Candida albicans yeast and hyphae are discriminated by MAPK signaling in vaginal epithelial cells. PLoS ONE 2011, 6, e26580. [Google Scholar] [CrossRef]
- Moyes, D.L.; Richardson, J.P.; Naglik, J.R. Candida albicans-epithelial interactions and pathogenicity mechanisms: Scratching the surface. Virulence 2015, 6, 338–346. [Google Scholar] [CrossRef] [PubMed]
- Gladiator, A.; Wangler, N.; Trautwein-Weidner, K.; LeibundGut-Landmann, S. Cutting edge: Il-17-secreting innate lymphoid cells are essential for host defense against fungal infection. J. Immunol. 2013, 190, 521–525. [Google Scholar] [CrossRef] [PubMed]
- Verma, A.H.; Richardson, J.P.; Zhou, C.; Coleman, B.M.; Moyes, D.L.; Ho, J.; Huppler, A.R.; Ramani, K.; McGeachy, M.J.; Mufazalov, I.A.; et al. Oral epithelial cells orchestrate innate type 17 responses to Candida albicans through the virulence factor candidalysin. Sci. Immunol. 2017, 2. [Google Scholar] [CrossRef]
- Verma, A.H.; Zafar, H.; Ponde, N.O.; Hepworth, O.W.; Sihra, D.; Aggor, F.E.Y.; Ainscough, J.S.; Ho, J.; Richardson, J.P.; Coleman, B.M.; et al. Il-36 and Il-1/Il-17 drive immunity to oral candidiasis via parallel mechanisms. J. Immunol. 2018, 201, 627–634. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.; Shepherd, E.G.; Nelin, L.D. Mapk phosphatases--regulating the immune response. Nat. Rev. Immunol. 2007, 7, 202–212. [Google Scholar] [CrossRef] [PubMed]
- Moyes, D.L.; Wilson, D.; Richardson, J.P.; Mogavero, S.; Tang, S.X.; Wernecke, J.; Hofs, S.; Gratacap, R.L.; Robbins, J.; Runglall, M.; et al. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 2016, 532, 64–68. [Google Scholar] [CrossRef] [PubMed]
- Richardson, J.P.; Willems, H.M.E.; Moyes, D.L.; Shoaie, S.; Barker, K.S.; Tan, S.L.; Palmer, G.E.; Hube, B.; Naglik, J.R.; Peters, B.M. Candidalysin drives epithelial signaling, neutrophil recruitment, and immunopathology at the vaginal mucosa. Infect. Immun. 2018, 86, e00645-17. [Google Scholar] [CrossRef] [PubMed]
- Richardson, J.P.; Mogavero, S.; Moyes, D.L.; Blagojevic, M.; Kruger, T.; Verma, A.H.; Coleman, B.M.; De La Cruz Diaz, J.; Schulz, D.; Ponde, N.O.; et al. Processing of Candida albicans Ece1p is critical for candidalysin maturation and fungal virulence. MBio 2018, 9, e02178-17. [Google Scholar] [CrossRef] [PubMed]
- Bischofberger, M.; Iacovache, I.; van der Goot, F.G. Pathogenic pore-forming proteins: Function and host response. Cell Host Microbe 2012, 12, 266–275. [Google Scholar] [CrossRef]
- Peters, B.M.; Yano, J.; Noverr, M.C.; Fidel, P.L., Jr. Candida vaginitis: When opportunism knocks, the host responds. PLoS Pathog. 2014, 10, e1003965. [Google Scholar] [CrossRef] [PubMed]
- Foxman, B.; Muraglia, R.; Dietz, J.P.; Sobel, J.D.; Wagner, J. Prevalence of recurrent vulvovaginal candidiasis in 5 european countries and the united states: Results from an internet panel survey. J. Lower Genit. Tract Dis. 2013, 17, 340–345. [Google Scholar] [CrossRef]
- Fidel, P.L., Jr.; Barousse, M.; Espinosa, T.; Ficarra, M.; Sturtevant, J.; Martin, D.H.; Quayle, A.J.; Dunlap, K. An intravaginal live Candida challenge in humans leads to new hypotheses for the immunopathogenesis of vulvovaginal candidiasis. Infect. Immun. 2004, 72, 2939–2946. [Google Scholar] [CrossRef] [PubMed]
- Yano, J.; Noverr, M.C.; Fidel, P.L., Jr. Vaginal heparan sulfate linked to neutrophil dysfunction in the acute inflammatory response associated with experimental vulvovaginal candidiasis. MBio 2017, 8, e00211-17. [Google Scholar] [CrossRef] [PubMed]
- Yano, J.; Peters, B.M.; Noverr, M.C.; Fidel, P.L., Jr. Novel mechanism behind the immunopathogenesis of vulvovaginal candidiasis: “Neutrophil anergy”. Infect. Immun. 2018, 86, e00684-17. [Google Scholar] [CrossRef]
- Conti, H.R.; Shen, F.; Nayyar, N.; Stocum, E.; Sun, J.N.; Lindemann, M.J.; Ho, A.W.; Hai, J.H.; Yu, J.J.; Jung, J.W.; et al. Th17 cells and Il-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J. Exp. Med. 2009, 206, 299–311. [Google Scholar] [CrossRef] [PubMed]
- Swidergall, M.; Filler, S.G. Oropharyngeal candidiasis: Fungal invasion and epithelial cell responses. PLoS Pathog. 2017, 13, e1006056. [Google Scholar] [CrossRef] [PubMed]
- Richardson, J.P.; Moyes, D.L.; Ho, J.; Naglik, J.R. Candida innate immunity at the mucosa. Semin. Cell Dev. Biol. 2018. [Google Scholar] [CrossRef] [PubMed]
- Diamond, G.; Ryan, L. Beta-defensins: What are they really doing in the oral cavity? Oral Dis. 2011, 17, 628–635. [Google Scholar] [CrossRef] [PubMed]
- Chairatana, P.; Chiang, I.L.; Nolan, E.M. Human alpha-defensin 6 self-assembly prevents adhesion and suppresses virulence traits of Candida albicans. Biochemistry 2017, 56, 1033–1041. [Google Scholar] [CrossRef] [PubMed]
- Hua, X.; Yuan, X.; Tang, X.; Li, Z.; Pflugfelder, S.C.; Li, D.Q. Human corneal epithelial cells produce antimicrobial peptides LL-37 and beta-defensins in response to heat-killed Candida albicans. Ophthalmic Res. 2014, 51, 179–186. [Google Scholar] [CrossRef] [PubMed]
- Sawaki, K.; Mizukawa, N.; Yamaai, T.; Fukunaga, J.; Sugahara, T. Immunohistochemical study on expression of alpha-defensin and beta-defensin-2 in human buccal epithelia with candidiasis. Oral Dis. 2002, 8, 37–41. [Google Scholar] [CrossRef]
- Feng, Z.; Jiang, B.; Chandra, J.; Ghannoum, M.; Nelson, S.; Weinberg, A. Human beta-defensins: Differential activity against candidal species and regulation by Candida albicans. J. Dent. Res. 2005, 84, 445–450. [Google Scholar] [CrossRef] [PubMed]
- Vylkova, S.; Li, X.S.; Berner, J.C.; Edgerton, M. Distinct antifungal mechanisms: Beta-defensins require Candida albicans Ssa1 protein, while Trk1p mediates activity of cysteine-free cationic peptides. Antimicrob. Agents Chemother. 2006, 50, 324–331. [Google Scholar] [CrossRef] [PubMed]
- Conti, H.R.; Bruno, V.M.; Childs, E.E.; Daugherty, S.; Hunter, J.P.; Mengesha, B.G.; Saevig, D.L.; Hendricks, M.R.; Coleman, B.M.; Brane, L.; et al. Il-17 receptor signaling in oral epithelial cells is critical for protection against oropharyngeal candidiasis. Cell Host Microbe 2016, 20, 606–617. [Google Scholar] [CrossRef] [PubMed]
- Tsai, P.W.; Yang, C.Y.; Chang, H.T.; Lan, C.Y. Human antimicrobial peptide LL-37 inhibits adhesion of Candida albicans by interacting with yeast cell-wall carbohydrates. PLoS ONE 2011, 6, e17755. [Google Scholar] [CrossRef]
- Yano, J.; Lilly, E.; Barousse, M.; Fidel, P.L., Jr. Epithelial cell-derived S100 calcium-binding proteins as key mediators in the hallmark acute neutrophil response during Candida vaginitis. Infect. Immun. 2010, 78, 5126–5137. [Google Scholar] [CrossRef]
- Yano, J.; Palmer, G.E.; Eberle, K.E.; Peters, B.M.; Vogl, T.; McKenzie, A.N.; Fidel, P.L., Jr. Vaginal epithelial cell-derived S100 alarmins induced by Candida albicans via pattern recognition receptor interactions are sufficient but not necessary for the acute neutrophil response during experimental vaginal candidiasis. Infect. Immun. 2014, 82, 783–792. [Google Scholar] [CrossRef] [PubMed]
- Sohnle, P.G.; Hahn, B.L.; Santhanagopalan, V. Inhibition of Candida albicans growth by calprotectin in the absence of direct contact with the organisms. J. Infect. Dis. 1996, 174, 1369–1372. [Google Scholar] [CrossRef]
- Kuhbacher, A.; Burger-Kentischer, A.; Rupp, S. Interaction of Candida species with the skin. Microorganisms 2017, 5, 32. [Google Scholar] [CrossRef] [PubMed]
- Nikawa, H.; Samaranayake, L.P.; Tenovuo, J.; Pang, K.M.; Hamada, T. The fungicidal effect of human lactoferrin on Candida albicans and Candida krusei. Arch. Oral. Biol. 1993, 38, 1057–1063. [Google Scholar] [CrossRef]
- Kirkpatrick, C.H.; Green, I.; Rich, R.R.; Schade, A.L. Inhibition of growth of Candida albicans by iron-unsaturated lactoferrin: Relation to host-defense mechanisms in chronic mucocutaneous candidiasis. J. Infect. Dis. 1971, 124, 539–544. [Google Scholar] [CrossRef]
- Li, X.S.; Reddy, M.S.; Baev, D.; Edgerton, M. Candida albicans Ssa1/2p is the cell envelope binding protein for human salivary histatin 5. J. Biol. Chem. 2003, 278, 28553–28561. [Google Scholar] [CrossRef]
- Jang, W.S.; Bajwa, J.S.; Sun, J.N.; Edgerton, M. Salivary histatin 5 internalization by translocation, but not endocytosis, is required for fungicidal activity in Candida albicans. Mol. Microbiol. 2010, 77, 354–370. [Google Scholar] [CrossRef] [PubMed]
- Conti, H.R.; Peterson, A.C.; Brane, L.; Huppler, A.R.; Hernandez-Santos, N.; Whibley, N.; Garg, A.V.; Simpson-Abelson, M.R.; Gibson, G.A.; Mamo, A.J.; et al. Oral-resident natural Th17 cells and γδ T cells control opportunistic Candida albicans infections. J. Exp. Med. 2014, 211, 2075–2084. [Google Scholar] [CrossRef] [PubMed]
- Huppler, A.R.; Verma, A.H.; Conti, H.R.; Gaffen, S.L. Neutrophils do not express Il-17A in the context of acute oropharyngeal candidiasis. Pathogens 2015, 4, 559–572. [Google Scholar] [CrossRef] [PubMed]
- Tomalka, J.; Azodi, E.; Narra, H.P.; Patel, K.; O’Neill, S.; Cardwell, C.; Hall, B.A.; Wilson, J.M.; Hise, A.G. Beta-defensin 1 plays a role in acute mucosal defense against Candida albicans. J. Immunol. 2015, 194, 1788–1795. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Okada, S.; Kong, X.F.; Kreins, A.Y.; Cypowyj, S.; Abhyankar, A.; Toubiana, J.; Itan, Y.; Audry, M.; Nitschke, P.; et al. Gain-of-function human STAT1 mutations impair Il-17 immunity and underlie chronic mucocutaneous candidiasis. J. Exp. Med. 2011, 208, 1635–1648. [Google Scholar] [CrossRef]
- Puel, A.; Cypowyj, S.; Bustamante, J.; Wright, J.F.; Liu, L.; Lim, H.K.; Migaud, M.; Israel, L.; Chrabieh, M.; Audry, M.; et al. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332, 65–68. [Google Scholar] [CrossRef] [PubMed]
- Netea, M.G.; Joosten, L.A.; van der Meer, J.W.; Kullberg, B.J.; van de Veerdonk, F.L. Immune defence against Candida fungal infections. Nat. Rev. Immunol. 2015, 15, 630–642. [Google Scholar] [CrossRef] [PubMed]
- Sorgo, A.G.; Heilmann, C.J.; Brul, S.; de Koster, C.G.; Klis, F.M. Beyond the wall: Candida albicans secret(e)s to survive. FEMS Microbiol. Lett. 2013, 338, 10–17. [Google Scholar] [CrossRef] [PubMed]
- Cauchie, M.; Desmet, S.; Lagrou, K. Candida and its dual lifestyle as a commensal and a pathogen. Res. Microbiol. 2017, 168, 802–810. [Google Scholar] [CrossRef]
- da Silva Dantas, A.; Lee, K.K.; Raziunaite, I.; Schaefer, K.; Wagener, J.; Yadav, B.; Gow, N.A. Cell biology of Candida albicans -host interactions. Curr. Opin. Microbiol. 2016, 34, 111–118. [Google Scholar] [CrossRef] [PubMed]
- Naglik, J.R.; Challacombe, S.J.; Hube, B. Candida albicans secreted aspartyl proteinases in virulence and pathogenesis. Microbiol. Mol. Biol. Rev. 2003, 67, 400–428. [Google Scholar] [CrossRef] [PubMed]
- Albrecht, A.; Felk, A.; Pichova, I.; Naglik, J.R.; Schaller, M.; de Groot, P.; Maccallum, D.; Odds, F.C.; Schafer, W.; Klis, F.; et al. Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J. Biol. Chem. 2006, 281, 688–694. [Google Scholar] [CrossRef]
- Gabrielli, E.; Sabbatini, S.; Roselletti, E.; Kasper, L.; Perito, S.; Hube, B.; Cassone, A.; Vecchiarelli, A.; Pericolini, E. In vivo induction of neutrophil chemotaxis by secretory aspartyl proteinases of Candida albicans. Virulence 2016, 7, 819–825. [Google Scholar] [CrossRef]
- Cassone, A. Vulvovaginal Candida albicans infections: Pathogenesis, immunity and vaccine prospects. BJOG 2015, 122, 785–794. [Google Scholar] [CrossRef]
- Kumar, R.; Breindel, C.; Saraswat, D.; Cullen, P.J.; Edgerton, M. Candida albicans Sap6 amyloid regions function in cellular aggregation and zinc binding, and contribute to zinc acquisition. Sci. Rep. 2017, 7, 2908. [Google Scholar] [CrossRef] [PubMed]
- Naglik, J.R.; Moyes, D.; Makwana, J.; Kanzaria, P.; Tsichlaki, E.; Weindl, G.; Tappuni, A.R.; Rodgers, C.A.; Woodman, A.J.; Challacombe, S.J.; et al. Quantitative expression of the Candida albicans secreted aspartyl proteinase gene family in human oral and vaginal candidiasis. Microbiology 2008, 154, 3266–3280. [Google Scholar] [CrossRef]
- Lermann, U.; Morschhauser, J. Secreted aspartic proteases are not required for invasion of reconstituted human epithelia by Candida albicans. Microbiology 2008, 154, 3281–3295. [Google Scholar] [CrossRef] [PubMed]
- Barrett-Bee, K.; Hayes, Y.; Wilson, R.G.; Ryley, J.F. A comparison of phospholipase activity, cellular adherence and pathogenicity of yeasts. J. Gen. Microbiol. 1985, 131, 1217–1221. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, A.S.; Mirbod, F.; Filler, S.G.; Banno, Y.; Cole, G.T.; Kitajima, Y.; Edwards, J.E., Jr.; Nozawa, Y.; Ghannoum, M.A. Evidence implicating phospholipase as a virulence factor of Candida albicans. Infect. Immun. 1995, 63, 1993–1998. [Google Scholar] [PubMed]
- Leidich, S.D.; Ibrahim, A.S.; Fu, Y.; Koul, A.; Jessup, C.; Vitullo, J.; Fonzi, W.; Mirbod, F.; Nakashima, S.; Nozawa, Y.; et al. Cloning and disruption of caPLB1, a phospholipase b gene involved in the pathogenicity of Candida albicans. J. Biol. Chem. 1998, 273, 26078–26086. [Google Scholar] [CrossRef]
- Mukherjee, P.K.; Seshan, K.R.; Leidich, S.D.; Chandra, J.; Cole, G.T.; Ghannoum, M.A. Reintroduction of the PLB1 gene into Candida albicans restores virulence in vivo. Microbiology 2001, 147, 2585–2597. [Google Scholar] [CrossRef] [PubMed]
- Dolan, J.W.; Bell, A.C.; Hube, B.; Schaller, M.; Warner, T.F.; Balish, E. Candida albicans PLD I activity is required for full virulence. Med. Mycol. 2004, 42, 439–447. [Google Scholar] [CrossRef]
- Fu, Y.; Ibrahim, A.S.; Fonzi, W.; Zhou, X.; Ramos, C.F.; Ghannoum, M.A. Cloning and characterization of a gene (LIP1) which encodes a lipase from the pathogenic yeast Candida albicans. Microbiology 1997, 143 Pt 2, 331–340. [Google Scholar] [CrossRef]
- Hube, B.; Stehr, F.; Bossenz, M.; Mazur, A.; Kretschmar, M.; Schafer, W. Secreted lipases of Candida albicans: Cloning, characterisation and expression analysis of a new gene family with at least ten members. Arch. Microbiol. 2000, 174, 362–374. [Google Scholar] [CrossRef] [PubMed]
- Schofield, D.A.; Westwater, C.; Warner, T.; Balish, E. Differential Candida albicans lipase gene expression during alimentary tract colonization and infection. FEMS Microbiol. Lett. 2005, 244, 359–365. [Google Scholar] [CrossRef] [PubMed]
- Stehr, F.; Felk, A.; Gacser, A.; Kretschmar, M.; Mahnss, B.; Neuber, K.; Hube, B.; Schafer, W. Expression analysis of the Candida albicans lipase gene family during experimental infections and in patient samples. FEMS Yeast Res. 2004, 4, 401–408. [Google Scholar] [CrossRef]
- Swidergall, M.; Ernst, A.M.; Ernst, J.F. Candida albicans mucin Msb2 is a broad-range protectant against antimicrobial peptides. Antimicrob. Agents Chemother. 2013, 57, 3917–3922. [Google Scholar] [CrossRef] [PubMed]
- Meiller, T.F.; Hube, B.; Schild, L.; Shirtliff, M.E.; Scheper, M.A.; Winkler, R.; Ton, A.; Jabra-Rizk, M.A. A novel immune evasion strategy of Candida albicans: Proteolytic cleavage of a salivary antimicrobial peptide. PLoS ONE 2009, 4, e5039. [Google Scholar] [CrossRef]
- Li, R.; Kumar, R.; Tati, S.; Puri, S.; Edgerton, M. Candida albicans Flu1-mediated efflux of salivary histatin 5 reduces its cytosolic concentration and fungicidal activity. Antimicrob. Agents Chemother. 2013, 57, 1832–1839. [Google Scholar] [CrossRef] [PubMed]
- Kode, M.A.; Karjodkar, F.R. Estimation of the serum and the salivary trace elements in OSMF patients. J. Clin. Diagn. Res. 2013, 7, 1215–1218. [Google Scholar] [CrossRef]
- Kim, Y.J.; Kim, Y.K.; Kho, H.S. Effects of smoking on trace metal levels in saliva. Oral Dis. 2010, 16, 823–830. [Google Scholar] [CrossRef]
- Chicharro, J.L.; Serrano, V.; Urena, R.; Gutierrez, A.M.; Carvajal, A.; Fernandez-Hernando, P.; Lucia, A. Trace elements and electrolytes in human resting mixed saliva after exercise. Br. J. Sports Med. 1999, 33, 204–207. [Google Scholar] [CrossRef]
- Olmez, I.; Gulovali, M.C.; Gordon, G.E.; Henkin, R.I. Trace elements in human parotid saliva. Biol. Trace Element Res. 1988, 17, 259–270. [Google Scholar] [CrossRef]
- Liu, J.Z.; Jellbauer, S.; Poe, A.J.; Ton, V.; Pesciaroli, M.; Kehl-Fie, T.E.; Restrepo, N.A.; Hosking, M.P.; Edwards, R.A.; Battistoni, A.; et al. Zinc sequestration by the neutrophil protein calprotectin enhances Salmonella growth in the inflamed gut. Cell Host Microbe 2012, 11, 227–239. [Google Scholar] [CrossRef]
- Citiulo, F.; Jacobsen, I.D.; Miramon, P.; Schild, L.; Brunke, S.; Zipfel, P.; Brock, M.; Hube, B.; Wilson, D. Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog. 2012, 8, e1002777. [Google Scholar] [CrossRef]
- Kim, M.J.; Kil, M.; Jung, J.H.; Kim, J. Roles of zinc-responsive transcription factor Csr1 in filamentous growth of the pathogenic yeast Candida albicans. J. Microbiol. Biotechnol. 2008, 18, 242–247. [Google Scholar] [PubMed]
- Nobile, C.J.; Nett, J.E.; Hernday, A.D.; Homann, O.R.; Deneault, J.S.; Nantel, A.; Andes, D.R.; Johnson, A.D.; Mitchell, A.P. Biofilm matrix regulation by Candida albicans Zap1. PLoS Biol. 2009, 7, e1000133. [Google Scholar] [CrossRef]
- Malavia, D.; Lehtovirta-Morley, L.E.; Alamir, O.; Weiss, E.; Gow, N.A.R.; Hube, B.; Wilson, D. Zinc limitation induces a hyper-adherent goliath phenotype in Candida albicans. Front. Microbiol. 2017, 8, 2238. [Google Scholar] [CrossRef] [PubMed]
- Crawford, A.C.; Lehtovirta-Morley, L.E.; Alamir, O.; Niemiec, M.J.; Alawfi, B.; Alsarraf, M.; Skrahina, V.; Costa, A.; Anderson, A.; Yellagunda, S.; et al. Biphasic zinc compartmentalisation in a human fungal pathogen. PLoS Pathog. 2018, 14, e1007013. [Google Scholar] [CrossRef]
- Moors, M.A.; Stull, T.L.; Blank, K.J.; Buckley, H.R.; Mosser, D.M. A role for complement receptor-like molecules in iron acquisition by Candida albicans. J. Exp. Med. 1992, 175, 1643–1651. [Google Scholar] [CrossRef]
- Ramanan, N.; Wang, Y. A high-affinity iron permease essential for Candida albicans virulence. Science 2000, 288, 1062–1064. [Google Scholar] [CrossRef]
- Lesuisse, E.; Knight, S.A.; Camadro, J.M.; Dancis, A. Siderophore uptake by Candida albicans: Effect of serum treatment and comparison with Saccharomyces cerevisiae. Yeast 2002, 19, 329–340. [Google Scholar] [CrossRef] [PubMed]
- Heymann, P.; Gerads, M.; Schaller, M.; Dromer, F.; Winkelmann, G.; Ernst, J.F. The siderophore iron transporter of Candida albicans (Sit1p/Arn1p) mediates uptake of ferrichrome-type siderophores and is required for epithelial invasion. Infect. Immun. 2002, 70, 5246–5255. [Google Scholar] [CrossRef] [PubMed]
- Manns, J.M.; Mosser, D.M.; Buckley, H.R. Production of a hemolytic factor by Candida albicans. Infect. Immun. 1994, 62, 5154–5156. [Google Scholar] [PubMed]
- Watanabe, T.; Takano, M.; Murakami, M.; Tanaka, H.; Matsuhisa, A.; Nakao, N.; Mikami, T.; Suzuki, M.; Matsumoto, T. Characterization of a haemolytic factor from Candida albicans. Microbiology 1999, 145 Pt 3, 689–694. [Google Scholar] [CrossRef]
- Luo, G.; Samaranayake, L.P.; Yau, J.Y. Candida species exhibit differential in vitro hemolytic activities. J. Clin. Microbiol. 2001, 39, 2971–2974. [Google Scholar] [CrossRef]
- Weissman, Z.; Kornitzer, D. A family of Candida cell surface haem-binding proteins involved in haemin and haemoglobin-iron utilization. Mol. Microbiol. 2004, 53, 1209–1220. [Google Scholar] [CrossRef] [PubMed]
- Nasser, L.; Weissman, Z.; Pinsky, M.; Amartely, H.; Dvir, H.; Kornitzer, D. Structural basis of haem-iron acquisition by fungal pathogens. Nat. Microbiol. 2016, 1, 16156. [Google Scholar] [CrossRef] [PubMed]
- Sorgo, A.G.; Heilmann, C.J.; Dekker, H.L.; Brul, S.; de Koster, C.G.; Klis, F.M. Mass spectrometric analysis of the secretome of Candida albicans. Yeast 2010, 27, 661–672. [Google Scholar] [CrossRef]
- Kuznets, G.; Vigonsky, E.; Weissman, Z.; Lalli, D.; Gildor, T.; Kauffman, S.J.; Turano, P.; Becker, J.; Lewinson, O.; Kornitzer, D. A relay network of extracellular heme-binding proteins drives C. albicans iron acquisition from hemoglobin. PLoS Pathog. 2014, 10, e1004407. [Google Scholar] [CrossRef]
- Weissman, Z.; Shemer, R.; Conibear, E.; Kornitzer, D. An endocytic mechanism for haemoglobin-iron acquisition in Candida albicans. Mol. Microbiol. 2008, 69, 201–217. [Google Scholar] [CrossRef]
- Knight, S.A.; Vilaire, G.; Lesuisse, E.; Dancis, A. Iron acquisition from transferrin by Candida albicans depends on the reductive pathway. Infect. Immun. 2005, 73, 5482–5492. [Google Scholar] [CrossRef]
- Hammacott, J.E.; Williams, P.H.; Cashmore, A.M. Candida albicans Cfl1 encodes a functional ferric reductase activity that can rescue a Saccharomyces cerevisiae fre1 mutant. Microbiology 2000, 146 Pt 4, 869–876. [Google Scholar] [CrossRef]
- Mamouei, Z.; Zeng, G.; Wang, Y.M.; Wang, Y. Candida albicans possess a highly versatile and dynamic high-affinity iron transport system important for its commensal-pathogenic lifestyle. Mol. Microbiol. 2017, 106, 986–998. [Google Scholar] [CrossRef] [PubMed]
- Knight, S.A.; Lesuisse, E.; Stearman, R.; Klausner, R.D.; Dancis, A. Reductive iron uptake by Candida albicans: Role of copper, iron and the Tup1 regulator. Microbiology 2002, 148, 29–40. [Google Scholar] [CrossRef]
- Eck, R.; Hundt, S.; Hartl, A.; Roemer, E.; Kunkel, W. A multicopper oxidase gene from Candida albicans: Cloning, characterization and disruption. Microbiology 1999, 145 Pt 9, 2415–2422. [Google Scholar] [CrossRef]
- Ziegler, L.; Terzulli, A.; Gaur, R.; McCarthy, R.; Kosman, D.J. Functional characterization of the ferroxidase, permease high-affinity iron transport complex from Candida albicans. Mol. Microbiol. 2011, 81, 473–485. [Google Scholar] [CrossRef] [PubMed]
- Weissman, Z.; Shemer, R.; Kornitzer, D. Deletion of the copper transporter caCCC2 reveals two distinct pathways for iron acquisition in Candida albicans. Mol. Microbiol. 2002, 44, 1551–1560. [Google Scholar] [CrossRef] [PubMed]
- Hu, C.J.; Bai, C.; Zheng, X.D.; Wang, Y.M.; Wang, Y. Characterization and functional analysis of the siderophore-iron transporter caArn1p in Candida albicans. J. Biol. Chem. 2002, 277, 30598–30605. [Google Scholar] [CrossRef] [PubMed]
- Wandersman, C.; Delepelaire, P. Bacterial iron sources: From siderophores to hemophores. Annu. Rev. Microbiol. 2004, 58, 611–647. [Google Scholar] [CrossRef] [PubMed]
- Chen, C.; Pande, K.; French, S.D.; Tuch, B.B.; Noble, S.M. An iron homeostasis regulatory circuit with reciprocal roles in Candida albicans commensalism and pathogenesis. Cell Host Microbe 2011, 10, 118–135. [Google Scholar] [CrossRef] [PubMed]
- Marvin, M.E.; Williams, P.H.; Cashmore, A.M. The Candida albicans CTR1 gene encodes a functional copper transporter. Microbiology 2003, 149, 1461–1474. [Google Scholar] [CrossRef]
- Marvin, M.E.; Mason, R.P.; Cashmore, A.M. The caCTR1 gene is required for high-affinity iron uptake and is transcriptionally controlled by a copper-sensing transactivator encoded by caMAC1. Microbiology 2004, 150, 2197–2208. [Google Scholar] [CrossRef] [PubMed]
- Riggle, P.J.; Kumamoto, C.A. Role of a Candida albicans P1-type ATPase in resistance to copper and silver ion toxicity. J. Bacteriol. 2000, 182, 4899–4905. [Google Scholar] [CrossRef]
- Weissman, Z.; Berdicevsky, I.; Cavari, B.Z.; Kornitzer, D. The high copper tolerance of Candida albicans is mediated by a P-type ATPase. Proc. Natl. Acad. Sci. USA 2000, 97, 3520–3525. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, F.J.; Douglas, L.M.; Konopka, J.B. The Sur7 protein resides in punctate membrane subdomains and mediates spatial regulation of cell wall synthesis in Candida albicans. Commun. Integr. Biol. 2009, 2, 76–77. [Google Scholar] [CrossRef] [PubMed]
- Alvarez, F.J.; Douglas, L.M.; Rosebrock, A.; Konopka, J.B. The Sur7 protein regulates plasma membrane organization and prevents intracellular cell wall growth in Candida albicans. Mol. Biol. Cell 2008, 19, 5214–5225. [Google Scholar] [CrossRef]
- Bernardo, S.M.; Lee, S.A. Candida albicans Sur7 contributes to secretion, biofilm formation, and macrophage killing. BMC Microbiol. 2010, 10, 133. [Google Scholar] [CrossRef] [PubMed]
- Wang, H.X.; Douglas, L.M.; Aimanianda, V.; Latge, J.P.; Konopka, J.B. The Candida albicans Sur7 protein is needed for proper synthesis of the fibrillar component of the cell wall that confers strength. Eukaryot. Cell 2011, 10, 72–80. [Google Scholar] [CrossRef] [PubMed]
- Douglas, L.M.; Wang, H.X.; Keppler-Ross, S.; Dean, N.; Konopka, J.B. Sur7 promotes plasma membrane organization and is needed for resistance to stressful conditions and to the invasive growth and virulence of Candida albicans. MBio 2012, 3, e00254-11. [Google Scholar] [CrossRef] [PubMed]
- Douglas, L.M.; Konopka, J.B. Plasma membrane architecture protects Candida albicans from killing by copper. PLoS Genet. 2019, 15, e1007911. [Google Scholar] [CrossRef]
Receptor | Ligand | Reference |
---|---|---|
Aryl hydrocarbon receptor | IFN-γ and L-kynurenine | [68] |
Dectin-1 | β-glucan | [90] |
EGFR/Her2 | Als3p/Ssa1p | [28,29] |
EphA2 | β-glucan | [93] |
Factor | Target | Cell/Tissue | Reference |
---|---|---|---|
α-defensin 6 | Invasion/biofilm formation | Intestinal ECs | [116] |
Murine β-defensin 1 | Reduces mucosal infection | Oral cavity | [133] |
β-defensin 2 | Ssa1p | Buccal epithelium | [118,120] |
β-defensin 3 | Ssa1p | Buccal epithelium | [118,120] |
Cathelicidin | Fungal adherence | Oral cavity | [122] |
S100 alarmins | Immune cell recruitment | Vaginal ECs | [123,124] |
Calprotectin | Fungal cell growth | In vitro | [125] |
Lactoferrin | Plasma membrane | In vitro | [127] |
Histatin-5 | Ssa1/2p | Salivary gland | [129,130] |
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Nikou, S.-A.; Kichik, N.; Brown, R.; Ponde, N.O.; Ho, J.; Naglik, J.R.; Richardson, J.P. Candida albicans Interactions with Mucosal Surfaces during Health and Disease. Pathogens 2019, 8, 53. https://doi.org/10.3390/pathogens8020053
Nikou S-A, Kichik N, Brown R, Ponde NO, Ho J, Naglik JR, Richardson JP. Candida albicans Interactions with Mucosal Surfaces during Health and Disease. Pathogens. 2019; 8(2):53. https://doi.org/10.3390/pathogens8020053
Chicago/Turabian StyleNikou, Spyridoula-Angeliki, Nessim Kichik, Rhys Brown, Nicole O. Ponde, Jemima Ho, Julian R. Naglik, and Jonathan P. Richardson. 2019. "Candida albicans Interactions with Mucosal Surfaces during Health and Disease" Pathogens 8, no. 2: 53. https://doi.org/10.3390/pathogens8020053