Skip to main content
SpringerLink
Log in
Book cover

The Fungal Cell Wall pp 297–330Cite as

Impact of the Environment upon the Candida albicans Cell Wall and Resultant Effects upon Immune Surveillance

  • Chapter
  • First Online:

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 425))

Abstract

The fungal cell wall is an essential organelle that maintains cellular morphology and protects the fungus from environmental insults. For fungal pathogens such as Candida albicans, it provides a degree of protection against attack by host immune defences. However, the cell wall also presents key epitopes that trigger host immunity and attractive targets for antifungal drugs. Rather than being a rigid shield, it has become clear that the fungal cell wall is an elastic organelle that permits rapid changes in cell volume and the transit of large liposomal particles such as extracellular vesicles. The fungal cell wall is also flexible in that it adapts to local environmental inputs, thereby enhancing the fitness of the fungus in these microenvironments. Recent evidence indicates that this cell wall adaptation affects host-fungus interactions by altering the exposure of major cell wall epitopes that are recognised by innate immune cells. Therefore, we discuss the impact of environmental adaptation upon fungal cell wall structure, and how this affects immune recognition, focussing on C. albicans and drawing parallels with other fungal pathogens.

Delma S. Childers, Gabriela M. Avelar, Judith M. Bain—These authors contributed equally to this work.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR et al (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460(7259):1117–1121

    Article  CAS  PubMed  Google Scholar 

  • Albrecht A, Felk A, Pichova I, Naglik JR, Schaller M, de Groot P et al (2006) Glycosylphosphatidylinositol-anchored proteases of Candida albicans target proteins necessary for both cellular processes and host-pathogen interactions. J Biol Chem 281(2):688–694

    Article  CAS  PubMed  Google Scholar 

  • Almeida RS, Brunke S, Albrecht A, Thewes S, Laue M, Edwards JE et al (2008) The hyphal-associated adhesin and invasin Als3 of Candida albicans mediates iron acquisition from host ferritin. PLoS Pathog 4(11):e1000217

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bain JM, Louw J, Lewis LE, Okai B, Walls CA, Ballou ER et al (2014) Candida albicans hypha formation and mannan masking of beta-glucan inhibit macrophage phagosome maturation. MBio 5(6):e01874–14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballou ER, Avelar GM, Childers DS, Mackie J, Bain JM, Wagener J et al (2016) Lactate signalling regulates fungal beta-glucan masking and immune evasion. Nat Microbiol 12(2):16238

    Article  CAS  Google Scholar 

  • Barelle CJ, Priest CL, Maccallum DM, Gow NA, Odds FC, Brown AJ (2006) Niche-specific regulation of central metabolic pathways in a fungal pathogen. Cell Microbiol 8(6):961–971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bates S, MacCallum DM, Bertram G, Munro CA, Hughes HB, Buurman ET et al (2005) Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+ -ATPase, is required for glycosylation and virulence. J Biol Chem 280(24):23408–23415

    Article  CAS  PubMed  Google Scholar 

  • Bates S, Hughes HB, Munro CA, Thomas WP, MacCallum DM, Bertram G et al (2006) Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem 281(1):90–98

    Article  CAS  PubMed  Google Scholar 

  • Bensen ES, Martin SJ, Li M, Berman J, Davis DA (2004) Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 54(5):1335–1351

    Article  CAS  PubMed  Google Scholar 

  • Blankenship JR, Fanning S, Hamaker JJ, Mitchell AP (2010) An extensive circuitry for cell wall regulation in Candida albicans. PLoS Pathog 6(2):e1000752

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. BioEssays 28(8):799–808

    Article  PubMed  Google Scholar 

  • Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413(6851):36–37

    Article  CAS  PubMed  Google Scholar 

  • Brown GD, Netea MG (2007) SpringerLink. Immunology of fungal infections

    Google Scholar 

  • Brown GD, Herre J, Williams DL, Willment JA, Marshall AS, Gordon S (2003) Dectin-1 mediates the biological effects of beta-glucans. J Exp Med 197(9):1119–1124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC (2012) Hidden killers: human fungal infections. Sci Transl Med 4(165):165rv13

    Google Scholar 

  • Bruno VM, Kalachikov S, Subaran R, Nobile CJ, Kyratsous C, Mitchell AP (2006) Control of the C. albicans cell wall damage response by transcriptional regulator Cas5. PLoS Pathog 2(3):e21

    Google Scholar 

  • Buurman ET, Westwater C, Hube B, Brown AJ, Odds FC, Gow NA (1998) Molecular analysis of CaMnt1p, a mannosyl transferase important for adhesion and virulence of Candida albicans. Proc Natl Acad Sci USA 95(13):7670–7675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campuzano A, Castro-Lopez N, Wozniak KL, Leopold Wager CM, Wormley FL Jr (2017) Dectin-3 is not required for protection against Cryptococcus neoformans infection. PLoS ONE 12(1):e0169347

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cantero PD, Ernst JF (2011) Damage to the glycoshield activates PMT-directed O-mannosylation via the Msb2-Cek1 pathway in Candida albicans. Mol Microbiol 80(3):715–725

    Article  CAS  PubMed  Google Scholar 

  • Carrion Sde J, Leal SM Jr, Ghannoum MA, Aimanianda V, Latge JP, Pearlman E (2013) The RodA hydrophobin on Aspergillus fumigatus spores masks dectin-1- and dectin-2-dependent responses and enhances fungal survival in vivo. J Immunol 191(5):2581–2588

    Article  PubMed  CAS  Google Scholar 

  • Castillo L, Calvo E, Martinez AI, Ruiz-Herrera J, Valentin E, Lopez JA et al (2008) A study of the Candida albicans cell wall proteome. Proteomics 8(18):3871–3881

    Article  CAS  PubMed  Google Scholar 

  • Chaffin WL (2008) Candida albicans cell wall proteins. Microbiol Mol Biol Rev 72(3):495–544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheetham J, Smith DA, da Silva Dantas A, Doris KS, Patterson MJ, Bruce CR et al (2007) A single MAPKKK regulates the Hog1 MAPK pathway in the pathogenic fungus Candida albicans. Mol Biol Cell 18(11):4603–4614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choteau L, Parny M, Francois N, Bertin B, Fumery M, Dubuquoy L et al (2016) Role of mannose-binding lectin in intestinal homeostasis and fungal elimination. Mucosal Immunol 9(3):767–776

    Article  CAS  PubMed  Google Scholar 

  • Citiulo F, Jacobsen ID, Miramon P, Schild L, Brunke S, Zipfel P et al (2012) Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 8(6):e1002777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crowe JD, Sievwright IK, Auld GC, Moore NR, Gow NA, Booth NA (2003) Candida albicans binds human plasminogen: identification of eight plasminogen-binding proteins. Mol Microbiol 47(6):1637–1651

    Article  CAS  PubMed  Google Scholar 

  • Cuskin F, Lowe EC, Temple MJ, Zhu Y, Cameron E, Pudlo NA et al (2015) Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism. Nature 517(7533):165–169

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dague E, Bitar R, Ranchon H, Durand F, Yken HM, Francois JM (2010) An atomic force microscopy analysis of yeast mutants defective in cell wall architecture. Yeast 27(8):673–684

    Article  CAS  PubMed  Google Scholar 

  • Dambuza IM, Brown GD (2015) C-type lectins in immunity: recent developments. Curr Opin Immunol 32:21–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dan JM, Kelly RM, Lee CK, Levitz SM (2008) Role of the mannose receptor in a murine model of Cryptococcus neoformans infection. Infect Immun 76(6):2362–2367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Day AM, Smith DA, Ikeh MA, Haider M, Herrero-de-Dios CM, Brown AJ et al (2017) Blocking two-component signalling enhances Candida albicans virulence and reveals adaptive mechanisms that counteract sustained SAPK activation. PLoS Pathog 13(1):e1006131

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • De Jesus M, Rodriguez AE, Yagita H, Ostroff GR, Mantis NJ (2015) Sampling of Candida albicans and Candida tropicalis by langerin-positive dendritic cells in mouse Peyer’s patches. Immunol Lett 168(1):64–72

    Article  PubMed  CAS  Google Scholar 

  • de Jong MA, Vriend LE, Theelen B, Taylor ME, Fluitsma D, Boekhout T et al (2010) C-type lectin langerin is a beta-glucan receptor on human Langerhans cells that recognizes opportunistic and pathogenic fungi. Mol Immunol 47(6):1216–1225

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deatherage BL, Cookson BT (2012) Membrane vesicle release in bacteria, eukaryotes, and archaea: a conserved yet underappreciated aspect of microbial life. Infect Immun 80(6):1948–1957

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Delgado-Silva Y, Vaz C, Carvalho-Pereira J, Carneiro C, Nogueira E, Correia A et al (2014) Participation of Candida albicans transcription factor RLM1 in cell wall biogenesis and virulence. PLoS ONE 9(1):e86270

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Denning DW, Kneale M, Sobel JD, Rautemaa-Richardson R (2018) Global burden of recurrent vulvovaginal candidiasis: a systematic review. Lancet Infect Dis

    Google Scholar 

  • Dichtl K, Samantaray S, Wagener J (2016) Cell wall integrity signalling in human pathogenic fungi. Cell Microbiol 18(9):1228–1238

    Article  CAS  PubMed  Google Scholar 

  • Dong R, Zhang M, Hu Q, Zheng S, Soh A, Zheng Y et al (2018) Galectin-3 as a novel biomarker for disease diagnosis and a target for therapy (Review). Int J Mol Med 41(2):599–614

    CAS  PubMed  Google Scholar 

  • Donlin MJ, Upadhya R, Gerik KJ, Lam W, VanArendonk LG, Specht CA et al (2014) Cross talk between the cell wall integrity and cyclic AMP/protein kinase A pathways in Cryptococcus neoformans. MBio 5(4). https://doi.org/10.1128/mbio.01573-14

  • Douglas CM, D’Ippolito JA, Shei GJ, Meinz M, Onishi J, Marrinan JA et al (1997) Identification of the FKS1 gene of Candida albicans as the essential target of 1,3-beta-D-glucan synthase inhibitors. Antimicrob Agents Chemother 41(11):2471–2479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drummond RA, Dambuza IM, Vautier S, Taylor JA, Reid DM, Bain CC et al (2016) CD4(+) T-cell survival in the GI tract requires dectin-1 during fungal infection. Mucosal Immunol 9(2):492–502

    Article  CAS  PubMed  Google Scholar 

  • Ebanks RO, Chisholm K, McKinnon S, Whiteway M, Pinto DM (2006) Proteomic analysis of Candida albicans yeast and hyphal cell wall and associated proteins. Proteomics 6(7):2147–2156

    Article  CAS  PubMed  Google Scholar 

  • Edwards JA, Alore EA, Rappleye CA (2011) The yeast-phase virulence requirement for alpha-glucan synthase differs among Histoplasma capsulatum chemotypes. Eukaryot Cell 10(1):87–97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ene IV, Adya AK, Wehmeier S, Brand AC, MacCallum DM, Gow NA et al (2012a) Host carbon sources modulate cell wall architecture, drug resistance and virulence in a fungal pathogen. Cell Microbiol 14(9):1319–1335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ene IV, Heilmann CJ, Sorgo AG, Walker LA, de Koster CG, Munro CA et al (2012b) Carbon source-induced reprogramming of the cell wall proteome and secretome modulates the adherence and drug resistance of the fungal pathogen Candida albicans. Proteomics 12(21):3164–3179

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ene IV, Walker LA, Schiavone M, Lee KK, Martin-Yken H, Dague E et al (2015) Cell wall remodeling enzymes modulate fungal cell wall elasticity and osmotic stress resistance. MBio 6(4):e00986–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Enjalbert B, Smith DA, Cornell MJ, Alam I, Nicholls S, Brown AJ et al (2006) Role of the Hog1 stress-activated protein kinase in the global transcriptional response to stress in the fungal pathogen Candida albicans. Mol Biol Cell 17(2):1018–1032

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Erwig LP, Gow NA (2016) Interactions of fungal pathogens with phagocytes. Nat Rev Microbiol 14(3):163–176

    Article  CAS  PubMed  Google Scholar 

  • Evans DF, Pye G, Bramley R, Clark AG, Dyson TJ, Hardcastle JD (1988) Measurement of gastrointestinal pH profiles in normal ambulant human subjects. Gut 29(8):1035–1041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fallingborg J (1999) Intraluminal pH of the human gastrointestinal tract. Dan Med Bull 46(3):183–196

    CAS  PubMed  Google Scholar 

  • Fanning S, Xu W, Beaurepaire C, Suhan JP, Nantel A, Mitchell AP (2012) Functional control of the Candida albicans cell wall by catalytic protein kinase A subunit Tpk1. Mol Microbiol 86(2):284–302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferwerda B, Ferwerda G, Plantinga TS, Willment JA, van Spriel AB, Venselaar H et al (2009) Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361(18):1760–1767

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fonzi WA (1999) PHR1 and PHR2 of Candida albicans encode putative glycosidases required for proper cross-linking of beta-1,3- and beta-1,6-glucans. J Bacteriol 181(22):7070–7079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frohner IE, Bourgeois C, Yatsyk K, Majer O, Kuchler K (2009) Candida albicans cell surface superoxide dismutases degrade host-derived reactive oxygen species to escape innate immune surveillance. Mol Microbiol 71(1):240–252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs BB, Mylonakis E (2009) Our paths might cross: the role of the fungal cell wall integrity pathway in stress response and cross talk with other stress response pathways. Eukaryot Cell 8(11):1616–1625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galan-Diez M, Arana DM, Serrano-Gomez D, Kremer L, Casasnovas JM, Ortega M et al (2010) Candida albicans beta-glucan exposure is controlled by the fungal CEK1-mediated mitogen-activated protein kinase pathway that modulates immune responses triggered through dectin-1. Infect Immun 78(4):1426–1436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gantner BN, Simmons RM, Canavera SJ, Akira S, Underhill DM (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197(9):1107–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gantner BN, Simmons RM, Underhill DM (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J 24(6):1277–1286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia R, Bravo E, Diez-Muniz S, Nombela C, Rodriguez-Pena JM, Arroyo J (2017) A novel connection between the cell wall integrity and the PKA pathways regulates cell wall stress response in yeast. Sci Rep 7(1):5703 https://doi.org/10.1038/s41598-017-06001-9

  • Garfoot AL, Rappleye CA (2016) Histoplasma capsulatum surmounts obstacles to intracellular pathogenesis. FEBS J 283(4):619–633

    Article  CAS  PubMed  Google Scholar 

  • Garfoot AL, Shen Q, Wuthrich M, Klein BS, Rappleye CA (2016) The Eng1 beta-glucanase enhances histoplasma virulence by reducing beta-glucan exposure. MBio 7(2):e01388–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gatti E, Popolo L, Vai M, Rota N, Alberghina L (1994) O-linked oligosaccharides in yeast glycosyl phosphatidylinositol-anchored protein gp115 are clustered in a serine-rich region not essential for its function. J Biol Chem 269(31):19695–19700

    Article  CAS  PubMed  Google Scholar 

  • Geunes-Boyer S, Oliver TN, Janbon G, Lodge JK, Heitman J, Perfect JR et al (2009) Surfactant protein D increases phagocytosis of hypocapsular Cryptococcus neoformans by murine macrophages and enhances fungal survival. Infect Immun 77(7):2783–2794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gil-Bona A, Parra-Giraldo CM, Hernaez ML, Reales-Calderon JA, Solis NV, Filler SG et al (2015) Candida albicans cell shaving uncovers new proteins involved in cell wall integrity, yeast to hypha transition, stress response and host-pathogen interaction. J Proteomics 127(Pt B):340–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goodridge HS, Reyes CN, Becker CA, Katsumoto TR, Ma J, Wolf AJ et al (2011) Activation of the innate immune receptor Dectin-1 upon formation of a ‘phagocytic synapse’. Nature 472(7344):471–475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouba N, Drancourt M (2015) Digestive tract mycobiota: a source of infection. Med Mal Infect 45(1–2):9–16

    Google Scholar 

  • Gow NA, Hube B (2012) Importance of the Candida albicans cell wall during commensalism and infection. Curr Opin Microbiol 15(4):406–412

    Article  CAS  PubMed  Google Scholar 

  • Gow NA, Robbins PW, Lester JW, Brown AJ, Fonzi WA, Chapman T et al (1994) A hyphal-specific chitin synthase gene (CHS2) is not essential for growth, dimorphism, or virulence of Candida albicans. Proc Natl Acad Sci USA 91(13):6216–6220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gow NAR, Latge JP, Munro CA (2017) The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr 5(3). https://doi.org/10.1128/microbiolspec.funk-0035-2016

  • Grahl N, Shepardson KM, Chung D, Cramer RA (2012) Hypoxia and fungal pathogenesis: to air or not to air? Eukaryot Cell 11(5):560–570

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Graus MS, Wester MJ, Lowman DW, Williams DL, Kruppa MD, Martinez CM et al (2018) Mannan molecular substructures control nanoscale glucan exposure in candida. Cell Rep 24(9):2432–2442.e5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gravelat FN, Beauvais A, Liu H, Lee MJ, Snarr BD, Chen D et al (2013) Aspergillus galactosaminogalactan mediates adherence to host constituents and conceals hyphal beta-glucan from the immune system. PLoS Pathog 9(8):e1003575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Chang Q, Cheng L, Xiong S, Jia X, Lin X et al (2018) C-type lectin receptor CD23 is required for host defense against Candida albicans and Aspergillus fumigatus infection. J Immunol 201(8):2427–2440

    Article  CAS  PubMed  Google Scholar 

  • Hall RA (2015) Dressed to impress: impact of environmental adaptation on the Candida albicans cell wall. Mol Microbiol 97(1):7–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall RA, Gow NA (2013) Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol Microbiol 90(6):1147–1161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall RA, Noverr MC (2017) Fungal interactions with the human host: exploring the spectrum of symbiosis. Curr Opin Microbiol 40:58–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hall RA, Bates S, Lenardon MD, Maccallum DM, Wagener J, Lowman DW et al (2013) The Mnn2 mannosyltransferase family modulates mannoprotein fibril length, immune recognition and virulence of Candida albicans. PLoS Pathog 9(4):e1003276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heilmann CJ, Sorgo AG, Mohammadi S, Sosinska GJ, de Koster CG, Brul S et al (2013) Surface stress induces a conserved cell wall stress response in the pathogenic fungus Candida albicans. Eukaryot Cell 12(2):254–264

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heinekamp T, Schmidt H, Lapp K, Pahtz V, Shopova I, Koster-Eiserfunke N et al (2015) Interference of Aspergillus fumigatus with the immune response. Semin Immunopathol 37(2):141–152

    Article  CAS  PubMed  Google Scholar 

  • Held K, Thiel S, Loos M, Petry F (2008) Increased susceptibility of complement factor B/C2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 45(15):3934–3941

    Article  CAS  PubMed  Google Scholar 

  • Herrero de Dios C, Roman E, Diez C, Alonso-Monge R, Pla J (2013) The transmembrane protein Opy2 mediates activation of the Cek1 MAP kinase in Candida albicans. Fungal Genet Biol 50:21–32

    Google Scholar 

  • Herrero-de-Dios C, Alonso-Monge R, Pla J (2014) The lack of upstream elements of the Cek1 and Hog1 mediated pathways leads to a synthetic lethal phenotype upon osmotic stress in Candida albicans. Fungal Genet Biol 69:31–42

    Article  CAS  PubMed  Google Scholar 

  • Hertel M, Schmidt-Westhausen AM, Strietzel FP (2016) Local, systemic, demographic, and health-related factors influencing pathogenic yeast spectrum and antifungal drug administration frequency in oral candidiasis: a retrospective study. Clin Oral Investig 20(7):1477–1486

    Article  PubMed  Google Scholar 

  • Heung LJ (2017) Innate immune responses to cryptococcus. J Fungi (Basel) 3(3). https://doi.org/10.3390/jof3030035. Epub 2017 Jul 2

  • Hobson RP, Munro CA, Bates S, MacCallum DM, Cutler JE, Heinsbroek SE et al (2004) Loss of cell wall mannosylphosphate in Candida albicans does not influence macrophage recognition. J Biol Chem 279(38):39628–39635

    Article  CAS  PubMed  Google Scholar 

  • Hofs S, Mogavero S, Hube B (2016) Interaction of Candida albicans with host cells: virulence factors, host defense, escape strategies, and the microbiota. J Microbiol 54(3):149–169

    Article  PubMed  CAS  Google Scholar 

  • Hogan LH, Klein BS (1994) Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence. Infect Immun 62(8):3543–3546

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hohl TM, Van Epps HL, Rivera A, Morgan LA, Chen PL, Feldmesser M et al (2005) Aspergillus fumigatus triggers inflammatory responses by stage-specific beta-glucan display. PLoS Pathog 1(3):e30

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hood MI, Skaar EP (2012) Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol 10(8):525–537

    Article  CAS  PubMed  Google Scholar 

  • Hopke A, Nicke N, Hidu EE, Degani G, Popolo L, Wheeler RT (2016) Neutrophil attack triggers extracellular trap-dependent Candida cell wall remodeling and altered immune recognition. PLoS Pathog 12(5):e1005644

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hopke A, Brown AJP, Hall RA, Wheeler RT (2018) Dynamic fungal cell wall architecture in stress adaptation and immune evasion. Trends Microbiol 26(4):284–295

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoyer LL, Payne TL, Bell M, Myers AM, Scherer S (1998) Candida albicans ALS3 and insights into the nature of the ALS gene family. Curr Genet 33(6):451–459

    Article  CAS  PubMed  Google Scholar 

  • Hoyer LL, Green CB, Oh SH, Zhao X (2008) Discovering the secrets of the Candida albicans agglutinin-like sequence (ALS) gene family—a sticky pursuit. Med Mycol 46(1):1–15

    Article  CAS  PubMed  Google Scholar 

  • Huang JH, Lin CY, Wu SY, Chen WY, Chu CL, Brown GD et al (2015) CR3 and dectin-1 collaborate in macrophage cytokine response through association on lipid rafts and activation of Syk-JNK-AP-1 pathway. PLoS Pathog 11(7):e1004985

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jimenez-Lucho V, Ginsburg V, Krivan HC (1990) Cryptococcus neoformans, Candida albicans, and other fungi bind specifically to the glycosphingolipid lactosylceramide (Gal beta 1-4Glc beta 1-1Cer), a possible adhesion receptor for yeasts. Infect Immun 58(7):2085–2090

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Joffe LS, Nimrichter L, Rodrigues ML, Del Poeta M (2016) Potential roles of fungal extracellular vesicles during infection. mSphere 1(4). https://doi.org/10.1128/msphere.00099-16.eCollection

  • Jouault T, Ibata-Ombetta S, Takeuchi O, Trinel PA, Sacchetti P, Lefebvre P et al (2003) Candida albicans phospholipomannan is sensed through toll-like receptors. J Infect Dis 188(1):165–172

    Article  CAS  PubMed  Google Scholar 

  • Kapteyn JC, Hoyer LL, Hecht JE, Muller WH, Andel A, Verkleij AJ et al (2000) The cell wall architecture of Candida albicans wild-type cells and cell wall-defective mutants. Mol Microbiol 35(3):601–611

    Article  CAS  PubMed  Google Scholar 

  • Karababa M, Valentino E, Pardini G, Coste AT, Bille J, Sanglard D (2006) CRZ1, a target of the calcineurin pathway in Candida albicans. Mol Microbiol 59(5):1429–1451

    Article  CAS  PubMed  Google Scholar 

  • Kjellerup L, Winther AL, Wilson D, Fuglsang AT (2018) Cyclic AMP pathway activation and extracellular zinc induce rapid intracellular zinc mobilization in Candida albicans. Front Microbiol 21(9):502

    Article  Google Scholar 

  • Klis FM, de Groot P, Hellingwerf K (2001) Molecular organization of the cell wall of Candida albicans. Med Mycol 39(Suppl 1):1–8

    Article  CAS  PubMed  Google Scholar 

  • Kohatsu L, Hsu DK, Jegalian AG, Liu FT, Baum LG (2006) Galectin-3 induces death of Candida species expressing specific beta-1,2-linked mannans. J Immunol 177(7):4718–4726

    Article  CAS  PubMed  Google Scholar 

  • Kondoh O, Tachibana Y, Ohya Y, Arisawa M, Watanabe T (1997) Cloning of the RHO1 gene from Candida albicans and its regulation of beta-1,3-glucan synthesis. J Bacteriol 179(24):7734–7741

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koyama T, Makita M, Shibata N, Okawa Y (2009) Influence of oxidative and osmotic stresses on the structure of the cell wall mannan of Candida albicans serotype A. Carbohydr Res 344(16):2195–2200

    Article  CAS  PubMed  Google Scholar 

  • Koziolek M, Schneider F, Grimm M, Modebeta C, Seekamp A, Roustom T et al (2015) Intragastric pH and pressure profiles after intake of the high-caloric, high-fat meal as used for food effect studies. J Control Release 220(Pt A):71–78

    Article  CAS  PubMed  Google Scholar 

  • Kullberg BJ, Arendrup MC (2015) Invasive candidiasis. N Engl J Med 373(15):1445–1456

    Article  CAS  PubMed  Google Scholar 

  • Lan CY, Rodarte G, Murillo LA, Jones T, Davis RW, Dungan J et al (2004) Regulatory networks affected by iron availability in Candida albicans. Mol Microbiol 53(5):1451–1469

    Article  CAS  PubMed  Google Scholar 

  • Langfelder K, Jahn B, Gehringer H, Schmidt A, Wanner G, Brakhage AA (1998) Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence. Med Microbiol Immunol 187(2):79–89

    Article  CAS  PubMed  Google Scholar 

  • Leach MD, Stead DA, Argo E, MacCallum DM, Brown AJ (2011) Molecular and proteomic analyses highlight the importance of ubiquitination for the stress resistance, metabolic adaptation, morphogenetic regulation and virulence of Candida albicans. Mol Microbiol 79(6):1574–1593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leach MD, Budge S, Walker L, Munro C, Cowen LE, Brown AJ (2012) Hsp90 orchestrates transcriptional regulation by Hsf1 and cell wall remodelling by MAPK signalling during thermal adaptation in a pathogenic yeast. PLoS Pathog 8(12):e1003069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leberer E, Harcus D, Broadbent ID, Clark KL, Dignard D, Ziegelbauer K et al (1996) Signal transduction through homologs of the Ste20p and Ste7p protein kinases can trigger hyphal formation in the pathogenic fungus Candida albicans. Proc Natl Acad Sci USA 93(23):13217–13222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee KK, Maccallum DM, Jacobsen MD, Walker LA, Odds FC, Gow NA et al (2012) Elevated cell wall chitin in Candida albicans confers echinocandin resistance in vivo. Antimicrob Agents Chemother 56(1):208–217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemaitre B, Nicolas E, Michaut L, Reichhart JM, Hoffmann JA (1996) The dorsoventral regulatory gene cassette spatzle/Toll/cactus controls the potent antifungal response in Drosophila adults. Cell 86(6):973–983

    Article  CAS  PubMed  Google Scholar 

  • Lenardon MD, Whitton RK, Munro CA, Marshall D, Gow NA (2007) Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol Microbiol 66(5):1164–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lenardon MD, Munro CA, Gow NA (2010) Chitin synthesis and fungal pathogenesis. Curr Opin Microbiol 13(4):416–423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levin DE (2011) Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189(4):1145–1175

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindsay AK, Deveau A, Piispanen AE, Hogan DA (2012) Farnesol and cyclic AMP signaling effects on the hypha-to-yeast transition in Candida albicans. Eukaryot Cell 11(10):1219–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lionakis MS, Levitz SM (2018) Host control of fungal infections: Lessons from basic studies and human cohorts. Annu Rev Immunol 26(36):157–191

    Article  CAS  Google Scholar 

  • Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A, Fink GR (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90(5):939–949

    Google Scholar 

  • Lopes JP, Stylianou M, Backman E, Holmberg S, Jass J, Claesson R et al (2018) Evasion of immune surveillance in low oxygen environments enhances Candida albicans virulence. MBio 9(6). https://doi.org/10.1128/mbio.02120-18

  • Louis P, Scott KP, Duncan SH, Flint HJ (2007) Understanding the effects of diet on bacterial metabolism in the large intestine. J Appl Microbiol 102(5):1197–1208

    Article  CAS  PubMed  Google Scholar 

  • Lowman DW, Greene RR, Bearden DW, Kruppa MD, Pottier M, Monteiro MA et al (2014) Novel structural features in Candida albicans hyphal glucan provide a basis for differential innate immune recognition of hyphae versus yeast. J Biol Chem 289(6):3432–3443

    Article  CAS  PubMed  Google Scholar 

  • Lu Y, Su C, Unoje O, Liu H (2014a) Quorum sensing controls hyphal initiation in Candida albicans through Ubr1-mediated protein degradation. Proc Natl Acad Sci USA 111(5):1975–1980

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lu Y, Su C, Liu H (2014b) Candida albicans hyphal initiation and elongation. Trends Microbiol 22(12):707–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luther K, Torosantucci A, Brakhage AA, Heesemann J, Ebel F (2007) Phagocytosis of Aspergillus fumigatus conidia by murine macrophages involves recognition by the dectin-1 beta-glucan receptor and Toll-like receptor 2. Cell Microbiol 9(2):368–381

    Article  CAS  PubMed  Google Scholar 

  • Malavia D, Lehtovirta-Morley LE, Alamir O, Weiss E, Gow NAR, Hube B et al (2017) Zinc limitation induces a hyper-adherent goliath phenotype in Candida albicans. Front Microbiol 14(8):2238

    Article  Google Scholar 

  • Mansour MK, Schlesinger LS, Levitz SM (2002) Optimal T cell responses to Cryptococcus neoformans mannoprotein are dependent on recognition of conjugated carbohydrates by mannose receptors. J Immunol 168(6):2872–2879

    Article  CAS  PubMed  Google Scholar 

  • Mansour MK, Tam JM, Khan NS, Seward M, Davids PJ, Puranam S et al (2013) Dectin-1 activation controls maturation of beta-1,3-glucan-containing phagosomes. J Biol Chem 288(22):16043–16054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martinez-Lopez R, Park H, Myers CL, Gil C, Filler SG (2006) Candida albicans Ecm33p is important for normal cell wall architecture and interactions with host cells. Eukaryot Cell 5(1):140–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maxson ME, Naj X, O’Meara TR, Plumb JD, Cowen LE, Grinstein S (2018) Integrin-based diffusion barrier separates membrane domains enabling the formation of microbiostatic frustrated phagosomes. Elife 7. https://doi.org/10.7554/elife.34798

  • McGreal EP, Rosas M, Brown GD, Zamze S, Wong SY, Gordon S et al (2006) The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16(5):422–430

    Article  CAS  PubMed  Google Scholar 

  • Means TK, Mylonakis E, Tampakakis E, Colvin RA, Seung E, Puckett L et al (2009) Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J Exp Med 206(3):637–653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mio T, Adachi-Shimizu M, Tachibana Y, Tabuchi H, Inoue SB, Yabe T et al (1997) Cloning of the Candida albicans homolog of Saccharomyces cerevisiae GSC1/FKS1 and its involvement in beta-1,3-glucan synthesis. J Bacteriol 179(13):4096–4105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monge RA, Roman E, Nombela C, Pla J (2006) The MAP kinase signal transduction network in Candida albicans. Microbiology 152(Pt 4):905–912

    Article  CAS  PubMed  Google Scholar 

  • Mora-Montes HM, Bates S, Netea MG, Castillo L, Brand A, Buurman ET et al (2010) A multifunctional mannosyltransferase family in Candida albicans determines cell wall mannan structure and host-fungus interactions. J Biol Chem 285(16):12087–12095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moreno-Ruiz E, Ortu G, de Groot PW, Cottier F, Loussert C, Prevost MC et al (2009) The GPI-modified proteins Pga59 and Pga62 of Candida albicans are required for cell wall integrity. Microbiology 155(Pt 6):2004–2020

    Article  CAS  PubMed  Google Scholar 

  • Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J et al (2016) Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature 532(7597):64–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mukaremera L, Lee KK, Mora-Montes HM, Gow NAR (2017) Candida albicans yeast, pseudohyphal, and hyphal morphogenesis differentially affects immune recognition. Front Immunol 7(8):629

    Article  CAS  Google Scholar 

  • Munro CA, Gow NA (2001) Chitin synthesis in human pathogenic fungi. Med Mycol 39(Suppl 1):41–53

    Article  CAS  PubMed  Google Scholar 

  • Munro CA, Winter K, Buchan A, Henry K, Becker JM, Brown AJ et al (2001) Chs1 of Candida albicans is an essential chitin synthase required for synthesis of the septum and for cell integrity. Mol Microbiol 39(5):1414–1426

    Article  CAS  PubMed  Google Scholar 

  • Munro CA, Bates S, Buurman ET, Hughes HB, Maccallum DM, Bertram G et al (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(2):1051–1060

    Article  CAS  PubMed  Google Scholar 

  • Munro CA, Selvaggini S, de Bruijn I, Walker L, Lenardon MD, Gerssen B et al (2007) The PKC, HOG and Ca2+ signalling pathways co-ordinately regulate chitin synthesis in Candida albicans. Mol Microbiol 63(5):1399–1413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murad AM, Leng P, Straffon M, Wishart J, Macaskill S, MacCallum D et al (2001) NRG1 represses yeast-hypha morphogenesis and hypha-specific gene expression in Candida albicans. EMBO J 20(17):4742–4752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Murciano C, Moyes DL, Runglall M, Islam A, Mille C, Fradin C et al (2011) Candida albicans cell wall glycosylation may be indirectly required for activation of epithelial cell proinflammatory responses. Infect Immun 79(12):4902–4911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura K, Kinjo T, Saijo S, Miyazato A, Adachi Y, Ohno N et al (2007) Dectin-1 is not required for the host defense to Cryptococcus neoformans. Microbiol Immunol 51(11):1115–1119

    Article  CAS  PubMed  Google Scholar 

  • Nakamura Y, Sato K, Yamamoto H, Matsumura K, Matsumoto I, Nomura T et al (2015) Dectin-2 deficiency promotes Th2 response and mucin production in the lungs after pulmonary infection with Cryptococcus neoformans. Infect Immun 83(2):671–681

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Navarro-Garcia F, Alonso-Monge R, Rico H, Pla J, Sentandreu R, Nombela C (1998) A role for the MAP kinase gene MKC1 in cell wall construction and morphological transitions in Candida albicans. Microbiology 144 (Pt 2)(Pt 2):411–424

    Google Scholar 

  • Netea MG, Van Der Graaf CA, Vonk AG, Verschueren I, Van Der Meer JW, Kullberg BJ (2002) The role of toll-like receptor (TLR) 2 and TLR4 in the host defense against disseminated candidiasis. J Infect Dis 185(10):1483–1489

    Article  CAS  PubMed  Google Scholar 

  • Netea MG, Gow NA, Munro CA, Bates S, Collins C, Ferwerda G et al (2006) Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest 116(6):1642–1650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Netea MG, Brown GD, Kullberg BJ, Gow NA (2008) An integrated model of the recognition of Candida albicans by the innate immune system. Nat Rev Microbiol 6(1):67–78

    Article  CAS  PubMed  Google Scholar 

  • Netea MG, Joosten LA, van der Meer JW, Kullberg BJ, van de Veerdonk FL (2015) Immune defence against Candida fungal infections. Nat Rev Immunol 15(10):630–642

    Article  CAS  PubMed  Google Scholar 

  • Nguyen TH, Fleet GH, Rogers PL (1998) Composition of the cell walls of several yeast species. Appl Microbiol Biotechnol 50(2):206–212

    Article  CAS  PubMed  Google Scholar 

  • Noble SM, Gianetti BA, Witchley JN (2017) Candida albicans cell-type switching and functional plasticity in the mammalian host. Nat Rev Microbiol 15(2):96–108

    Article  CAS  PubMed  Google Scholar 

  • O’Brien XM, Reichner JS (2016) Neutrophil integrins and matrix ligands and NET release. Front Immunol 19(7):363

    Google Scholar 

  • Odds FC, Brown AJ, Gow NA (2003) Antifungal agents: mechanisms of action. Trends Microbiol 11(6):272–279

    Article  CAS  PubMed  Google Scholar 

  • O’Hanlon DE, Moench TR, Cone RA (2013) Vaginal pH and microbicidal lactic acid when lactobacilli dominate the microbiota. PLoS ONE 8(11):e80074

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Okawa Y, Goto K (2006) Antigenicity of cell wall mannans of Candida albicans and Candida stellatoidea cultured at high temperatures in BACTEC medium. Biol Pharm Bull 29(8):1723–1727

    Article  CAS  PubMed  Google Scholar 

  • Owen DH, Katz DF (1999) A vaginal fluid simulant. Contraception 59(2):91–95

    Article  CAS  PubMed  Google Scholar 

  • Paravicini G, Mendoza A, Antonsson B, Cooper M, Losberger C, Payton MA (1996) The Candida albicans PKC1 gene encodes a protein kinase C homolog necessary for cellular integrity but not dimorphism. Yeast 12(8):741–756

    Article  CAS  PubMed  Google Scholar 

  • Pardini G, De Groot PW, Coste AT, Karababa M, Klis FM, de Koster CG et al (2006) The CRH family coding for cell wall glycosylphosphatidylinositol proteins with a predicted transglycosidase domain affects cell wall organization and virulence of Candida albicans. J Biol Chem 281(52):40399–40411

    Article  CAS  PubMed  Google Scholar 

  • Pericolini E, Perito S, Castagnoli A, Gabrielli E, Mencacci A, Blasi E et al (2018) Epitope unmasking in vulvovaginal candidiasis is associated with hyphal growth and neutrophilic infiltration. PLoS ONE 13(7):e0201436

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Perlroth J, Choi B, Spellberg B (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45(4):321–346

    Article  PubMed  Google Scholar 

  • Phan QT, Myers CL, Fu Y, Sheppard DC, Yeaman MR, Welch WH et al (2007) Als3 is a Candida albicans invasin that binds to cadherins and induces endocytosis by host cells. PLoS Biol 5(3):e64

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NA et al (2008) Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 45(10):1404–1414

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popolo L, Degani G, Camilloni C, Fonzi WA (2017) The PHR family: the role of extracellular transglycosylases in shaping Candida albicans cells. J Fungi (Basel) 3(4). https://doi.org/10.3390/jof3040059

  • Potrykus J, Stead D, Maccallum DM, Urgast DS, Raab A, van Rooijen N et al (2013) Fungal iron availability during deep seated candidiasis is defined by a complex interplay involving systemic and local events. PLoS Pathog 9(10):e1003676

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pradhan A, Avelar GM, Bain JM, Childers DS, Larcombe DE, Netea MG et al (2018) Hypoxia promotes immune evasion by triggering beta-glucan masking on the Candida albicans cell surface via mitochondrial and cAMP-protein kinase a signaling. MBio 9(6). https://doi.org/10.1128/mbio.01318-18

  • Pradhan A, Avelar GM, Bain JM, Childers D, Pelletier C, Larcombe DE, Shekhova E, Netea MG, Brown GD, Erwig LP, Gow NAR, Brown AJP (2019) Non-canonical signalling mediates changes in fungal cell wall PAMPs that drive immune evasion. Nat Commun (in press)

    Google Scholar 

  • Preechasuth K, Anderson JC, Peck SC, Brown AJ, Gow NA, Lenardon MD (2015) Cell wall protection by the Candida albicans class I chitin synthases. Fungal Genet Biol 82:264–276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramanan N, Wang Y (2000) A high-affinity iron permease essential for Candida albicans virulence. Science 288(5468):1062–1064

    Article  CAS  PubMed  Google Scholar 

  • Rappleye CA, Engle JT, Goldman WE (2004) RNA interference in Histoplasma capsulatum demonstrates a role for alpha-(1,3)-glucan in virulence. Mol Microbiol 53(1):153–165

    Article  CAS  PubMed  Google Scholar 

  • Rappleye CA, Eissenberg LG, Goldman WE (2007) Histoplasma capsulatum alpha-(1,3)-glucan blocks innate immune recognition by the beta-glucan receptor. Proc Natl Acad Sci USA 104(4):1366–1370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Richard M, Ibata-Ombetta S, Dromer F, Bordon-Pallier F, Jouault T, Gaillardin C (2002) Complete glycosylphosphatidylinositol anchors are required in Candida albicans for full morphogenesis, virulence and resistance to macrophages. Mol Microbiol 44(3):841–853

    Article  CAS  PubMed  Google Scholar 

  • Roman E, Cottier F, Ernst JF, Pla J (2009) Msb2 signaling mucin controls activation of Cek1 mitogen-activated protein kinase in Candida albicans. Eukaryot Cell 8(8):1235–1249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roman E, Correia I, Salazin A, Fradin C, Jouault T, Poulain D et al (2016) The Cek1mediated MAP kinase pathway regulates exposure of alpha1,2 and beta1,2mannosides in the cell wall of Candida albicans modulating immune recognition. Virulence 7(5):558–577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saeed S, Quintin J, Kerstens HH, Rao NA, Aghajanirefah A, Matarese F et al (2014) Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345(6204):1251086

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A et al (2010) Dectin-2 recognition of alpha-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32(5):681–691

    Article  CAS  PubMed  Google Scholar 

  • San Jose C, Monge RA, Perez-Diaz R, Pla J, Nombela C (1996) The mitogen-activated protein kinase homolog HOG1 gene controls glycerol accumulation in the pathogenic fungus Candida albicans. J Bacteriol 178(19):5850–5852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • San-Blas G, San-Blas F, Serrano LE (1977) Host-parasite relationships in the yeastlike form of Paracoccidioides brasiliensis strain IVIC Pb9. Infect Immun 15(2):343–346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sanglard D, Ischer F, Marchetti O, Entenza J, Bille J (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48(4):959–976

    Article  CAS  PubMed  Google Scholar 

  • Santos M, de Larrinoa IF (2005) Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor. Curr Genet 48(2):88–100

    Article  CAS  PubMed  Google Scholar 

  • Saporito-Irwin SM, Birse CE, Sypherd PS, Fonzi WA (1995) PHR1, a pH-regulated gene of Candida albicans, is required for morphogenesis. Mol Cell Biol 15(2):601–613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato T, Ueno Y, Watanabe T, Mikami T, Matsumoto T (2004) Role of Ca2+/calmodulin signaling pathway on morphological development of Candida albicans. Biol Pharm Bull 27(8):1281–1284

    Article  CAS  PubMed  Google Scholar 

  • Savage DC (1977) Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107–133

    Article  CAS  PubMed  Google Scholar 

  • Saville SP, Lazzell AL, Monteagudo C, Lopez-Ribot JL (2003) Engineered control of cell morphology in vivo reveals distinct roles for yeast and filamentous forms of Candida albicans during infection. Eukaryot Cell 2(5):1053–1060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sem X, Le GT, Tan AS, Tso G, Yurieva M, Liao WW et al (2016) β-glucan exposure on the fungal cell wall tightly correlates with competitive fitness of Candida species in the mouse gastrointestinal tract. Front Cell Infect Microbiol 22(6):186

    Google Scholar 

  • Setiadi ER, Doedt T, Cottier F, Noffz C, Ernst JF (2006) Transcriptional response of Candida albicans to hypoxia: linkage of oxygen sensing and Efg1p-regulatory networks. J Mol Biol 361(3):399–411

    Article  CAS  PubMed  Google Scholar 

  • Shepherd MG (1987) Cell envelope of Candida albicans. Crit Rev Microbiol 15(1):7–25

    Article  CAS  PubMed  Google Scholar 

  • Sherrington SL, Sorsby E, Mahtey N, Kumwenda P, Lenardon MD, Brown I et al (2017) Adaptation of Candida albicans to environmental pH induces cell wall remodelling and enhances innate immune recognition. PLoS Pathog 13(5):e1006403

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shoham S, Huang C, Chen JM, Golenbock DT, Levitz SM (2001) Toll-like receptor 4 mediates intracellular signaling without TNF-alpha release in response to Cryptococcus neoformans polysaccharide capsule. J Immunol 166(7):4620–4626

    Article  CAS  PubMed  Google Scholar 

  • Smith DA, Nicholls S, Morgan BA, Brown AJ, Quinn J (2004) A conserved stress-activated protein kinase regulates a core stress response in the human pathogen Candida albicans. Mol Biol Cell 15(9):4179–4190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sobel JD (2007) Vulvovaginal candidosis. Lancet 369(9577):1961–1971

    Article  PubMed  Google Scholar 

  • Sorgo AG, Heilmann CJ, Dekker HL, Bekker M, Brul S, de Koster CG et al (2011) Effects of fluconazole on the secretome, the wall proteome, and wall integrity of the clinical fungus Candida albicans. Eukaryot Cell 10(8):1071–1081

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sosinska GJ, de Groot PWJ, Teixeira de Mattos MJ, Dekker HL, de Koster CG, Hellingwerf KJ et al (2008) Hypoxic conditions and iron restriction affect the cell-wall proteome of Candida albicans grown under vagina-simulative conditions. Microbiology 154(Pt 2):510–520

    Google Scholar 

  • Staab JF, Bradway SD, Fidel PL, Sundstrom P (1999) Adhesive and mammalian transglutaminase substrate properties of Candida albicans Hwp1. Science 283(5407):1535–1538

    Article  CAS  PubMed  Google Scholar 

  • Staniszewska M, Bondaryk M, Rabczenko D, Smolenska-Sym G, Kurzatkowski W (2013) Cell wall carbohydrates content of pathogenic Candida albicans strain morphological forms. Med Dosw Mikrobiol 65(2):119–128

    CAS  PubMed  Google Scholar 

  • Stappers MHT, Clark AE, Aimanianda V, Bidula S, Reid DM, Asamaphan P et al (2018) Recognition of DHN-melanin by a C-type lectin receptor is required for immunity to Aspergillus. Nature 555(7696):382–386

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su C, Lu Y, Liu H (2013) Reduced TOR signaling sustains hyphal development in Candida albicans by lowering Hog1 basal activity. Mol Biol Cell 24(3):385–397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sudbery PE (2011) Growth of Candida albicans hyphae. Nat Rev Microbiol 9(10):737–748

    Article  CAS  PubMed  Google Scholar 

  • Tada H, Nemoto E, Shimauchi H, Watanabe T, Mikami T, Matsumoto T et al (2002) Saccharomyces cerevisiae- and Candida albicans-derived mannan induced production of tumor necrosis factor alpha by human monocytes in a CD14- and Toll-like receptor 4-dependent manner. Microbiol Immunol 46(7):503–512

    Article  CAS  PubMed  Google Scholar 

  • Taylor PR, Brown GD, Herre J, Williams DL, Willment JA, Gordon S (2004) The role of SIGNR1 and the beta-glucan receptor (dectin-1) in the nonopsonic recognition of yeast by specific macrophages. J Immunol 172(2):1157–1162

    Article  CAS  PubMed  Google Scholar 

  • Taylor PR, Tsoni SV, Willment JA, Dennehy KM, Rosas M, Findon H et al (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8(1):31–38

    Article  CAS  PubMed  Google Scholar 

  • Te Riet J, Joosten B, Reinieren-Beeren I, Figdor CG, Cambi A (2017) N-glycan mediated adhesion strengthening during pathogen-receptor binding revealed by cell-cell force spectroscopy. Sci Rep 7(1):6713. https://doi.org/10.1038/s41598-017-07220-w

  • Thornton BP, Vetvicka V, Pitman M, Goldman RC, Ross GD (1996) Analysis of the sugar specificity and molecular location of the beta-glucan-binding lectin site of complement receptor type 3 (CD11b/CD18). J Immunol 156(3):1235–1246

    CAS  PubMed  Google Scholar 

  • Thywissen A, Heinekamp T, Dahse HM, Schmaler-Ripcke J, Nietzsche S, Zipfel PF et al (2011) Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway. Front Microbiol 3(2):96

    Google Scholar 

  • Timpel C, Strahl-Bolsinger S, Ziegelbauer K, Ernst JF (1998) Multiple functions of Pmt1p-mediated protein O-mannosylation in the fungal pathogen Candida albicans. J Biol Chem 273(33):20837–20846

    Article  CAS  PubMed  Google Scholar 

  • Toh-e A, Yasunaga S, Nisogi H, Tanaka K, Oguchi T, Matsui Y (1993) Three yeast genes, PIR1, PIR2 and PIR3, containing internal tandem repeats, are related to each other, and PIR1 and PIR2 are required for tolerance to heat shock. Yeast 9(5):481–494

    Article  CAS  PubMed  Google Scholar 

  • Umeyama T, Kaneko A, Watanabe H, Hirai A, Uehara Y, Niimi M et al (2006) Deletion of the CaBIG1 gene reduces beta-1,6-glucan synthesis, filamentation, adhesion, and virulence in Candida albicans. Infect Immun 74(4):2373–2381

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urban C, Xiong X, Sohn K, Schroppel K, Brunner H, Rupp S (2005) The moonlighting protein Tsa1p is implicated in oxidative stress response and in cell wall biogenesis in Candida albicans. Mol Microbiol 57(5):1318–1341

    Article  CAS  PubMed  Google Scholar 

  • Valiante V, Macheleidt J, Foge M, Brakhage AA (2015) The Aspergillus fumigatus cell wall integrity signaling pathway: drug target, compensatory pathways, and virulence. Front Microbiol 16(6):325

    Google Scholar 

  • van de Veerdonk FL, Marijnissen RJ, Kullberg BJ, Koenen HJ, Cheng SC, Joosten I et al (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5(4):329–340

    Article  PubMed  CAS  Google Scholar 

  • Vargas G, Rocha JD, Oliveira DL, Albuquerque PC, Frases S, Santos SS et al (2015) Compositional and immunobiological analyses of extracellular vesicles released by Candida albicans. Cell Microbiol 17(3):389–407

    Article  CAS  PubMed  Google Scholar 

  • Vijayan D, Radford KJ, Beckhouse AG, Ashman RB, Wells CA (2012) Mincle polarizes human monocyte and neutrophil responses to Candida albicans. Immunol Cell Biol 90(9):889–895

    Article  CAS  PubMed  Google Scholar 

  • Voelz K, May RC (2010) Cryptococcal interactions with the host immune system. Eukaryot Cell 9(6):835–846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wagener J, Malireddi RK, Lenardon MD, Koberle M, Vautier S, MacCallum DM et al (2014) Fungal chitin dampens inflammation through IL-10 induction mediated by NOD2 and TLR9 activation. PLoS Pathog 10(4):e1004050

    Article  PubMed  PubMed Central  Google Scholar 

  • Wagener J, MacCallum DM, Brown GD, Gow NA (2017) Candida albicans chitin increases arginase-1 activity in human macrophages, with an impact on macrophage antimicrobial functions. MBio 8(1). https://doi.org/10.1128/mbio.01820-16

  • Walker LA, Munro CA, de Bruijn I, Lenardon MD, McKinnon A, Gow NA (2008) Stimulation of chitin synthesis rescues Candida albicans from echinocandins. PLoS Pathog 4(4):e1000040

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Walker L, Sood P, Lenardon MD, Milne G, Olson J, Jensen G, et al (2018) The viscoelastic properties of the fungal cell wall allow traffic of AmBisome as intact liposome vesicles. MBio 9(1). https://doi.org/10.1128/mbio.02383-17

  • Weinberg ED. Nutritional immunity. Host’s attempt to withold iron from microbial invaders. JAMA 1975 Jan 6;231(1):39-41

    Google Scholar 

  • Wells CA, Salvage-Jones JA, Li X, Hitchens K, Butcher S, Murray RZ et al (2008) The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 180(11):7404–7413

    Article  CAS  PubMed  Google Scholar 

  • Wheeler RT, Fink GR (2006) A drug-sensitive genetic network masks fungi from the immune system. PLoS Pathog 2(4):e35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wheeler RT, Kombe D, Agarwala SD, Fink GR (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4(12):e1000227

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Xia Y, Vetvicka V, Yan J, Hanikyrova M, Mayadas T, Ross GD (1999) The beta-glucan-binding lectin site of mouse CR3 (CD11b/CD18) and its function in generating a primed state of the receptor that mediates cytotoxic activation in response to iC3b-opsonized target cells. J Immunol 162(4):2281–2290

    CAS  PubMed  Google Scholar 

  • Yauch LE, Mansour MK, Shoham S, Rottman JB, Levitz SM (2004) Involvement of CD14, toll-like receptors 2 and 4, and MyD88 in the host response to the fungal pathogen Cryptococcus neoformans in vivo. Infect Immun 72(9):5373–5382

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu LL, Zhao XQ, Jiang C, You Y, Chen XP, Jiang YY et al (2013) C-type lectin receptors Dectin-3 and Dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity 39(2):324–334

    Article  CAS  PubMed  Google Scholar 

  • Znaidi S, van Wijlick L, Hernandez-Cervantes A, Sertour N, Desseyn JL, Vincent F et al (2018) Systematic gene overexpression in Candida albicans identifies a regulator of early adaptation to the mammalian gut. Cell Microbiol 20(11):e12890

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Acknowledgements

This work was funded by a programme grant from the UK Medical Research Council [www.mrc.ac.uk: MR/M026663/1], and by PhD studentships from the University of Aberdeen to AP, DL. The work was also supported by the Medical Research Council Centre for Medical Mycology (MR/N006364/1) and by the Wellcome Trust [www.wellcome.ac.uk: 097377]. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.

Author information

Authors and Affiliations

  1. Aberdeen Fungal Group, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen, AB25 2ZD, UK

    Delma S. Childers, Gabriela M. Avelar, Judith M. Bain, Daniel E. Larcombe, Arnab Pradhan, Susan Budge, Helen Heaney & Alistair J. P. Brown

  2. Medical Research Council Centre for Medical Mycology, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, EX4 4QD, UK

    Daniel E. Larcombe, Arnab Pradhan & Alistair J. P. Brown

Authors
  1. Delma S. Childers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Gabriela M. Avelar
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Judith M. Bain
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel E. Larcombe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Arnab Pradhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Susan Budge
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Helen Heaney
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Alistair J. P. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Alistair J. P. Brown .

Editor information

Editors and Affiliations

  1. Foundation for Research and Technology-Hellas (FORTH), Institute of Molecular Biology and Technology, Heraklion, Crete, Greece

    Jean-Paul Latgé

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Childers, D.S. et al. (2019). Impact of the Environment upon the Candida albicans Cell Wall and Resultant Effects upon Immune Surveillance. In: Latgé, JP. (eds) The Fungal Cell Wall . Current Topics in Microbiology and Immunology, vol 425. Springer, Cham. https://doi.org/10.1007/82_2019_182

Download citation

Publish with us

Policies and ethics

Search

Navigation