Advertisement

pp 1-37 | Cite as

PAMPs of the Fungal Cell Wall and Mammalian PRRs

  • Remi Hatinguais
  • Janet A. Willment
  • Gordon D. BrownEmail author
Chapter
Part of the Current Topics in Microbiology and Immunology book series

Abstract

Fungi are opportunistic pathogens that infect immunocompromised patients and are responsible for an estimated 1.5 million deaths every year. The antifungal innate immune response is mediated through the recognition of pathogen-associated molecular patterns (PAMPs) by the host’s pattern recognition receptors (PRRs). PRRs are immune receptors that ensure the internalisation and the killing of fungal pathogens. They also mount the inflammatory response, which contributes to initiate and polarise the adaptive response, controlled by lymphocytes. Both the innate and adaptive immune responses are required to control fungal infections. The immune recognition of fungal pathogen primarily occurs at the interface between the membrane of innate immune cells and the fungal cell wall, which contains a number of PAMPs. This chapter will focus on describing the main mammalian PRRs that have been shown to bind to PAMPs from the fungal cell wall of the four main fungal pathogens: Candida albicans, Aspergillus fumigatus, Cryptococcus neoformans and Pneumocystis jirovecii. We will describe these receptors, their functions and ligands to provide the reader with an overview of how the immune system recognises fungal pathogens and responds to them.

Notes

Acknowledgements

We thank the Wellcome Trust (102705) and the Medical Research Council Centre for Medical Mycology and the University of Exeter (MR/N006364/2) for funding.

Statement

All figures were made using BioRender.com.

References

  1. Aaron PA, Jamklang M, Uhrig JP et al (2018).The blood-brain barrier internalises Cryptococcus neoformans via the EphA2-tyrosine kinase receptor. Cell Microbiol 20(3)Google Scholar
  2. Acharya M, Borland G, Edkins AL et al (2010) CD23/FcepsilonRII: molecular multi-tasking. Clin Exp Immunol 162(1):12–23Google Scholar
  3. Aimanianda V, Bayry J, Bozza S et al (2009) Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460(7259):1117–1121Google Scholar
  4. Annane D, Bellissant E, Cavaillon JM (2005) Septic shock. Lancet 365(9453):63–78Google Scholar
  5. Arthur JS, Ley SC (2013) Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 13(9):679–692Google Scholar
  6. Ballou ER, Avelar GM, Childers DS et al (2016) Lactate signalling regulates fungal beta-glucan masking and immune evasion. Nat Microbiol 2:16238Google Scholar
  7. Balloy V, Si-Tahar M, Takeuchi O et al (2005) Involvement of toll-like receptor 2 in experimental invasive pulmonary aspergillosis. Infect Immun 73(9):5420–5425Google Scholar
  8. Beavil RL, Graber P, Aubonney N et al (1995) CD23/Fc epsilon RII and its soluble fragments can form oligomers on the cell surface and in solution. Immunology 84(2):202–206Google Scholar
  9. Becker KL, Aimanianda V, Wang X et al (2016) Aspergillus cell wall chitin induces anti- and proinflammatory cytokines in human pbmcs via the fc-gamma receptor/Syk/PI3K pathway. mBio 7(3)Google Scholar
  10. Bello-Irizarry SN, Wang J, Olsen K et al (2012) The alveolar epithelial cell chemokine response to pneumocystis requires adaptor molecule MyD88 and interleukin-1 receptor but not toll-like receptor 2 or 4. Infect Immun 80(11):3912–3920Google Scholar
  11. Bellocchio S, Montagnoli C, Bozza S et al (2004) The contribution of the Toll-like/IL-1 receptor superfamily to innate and adaptive immunity to fungal pathogens in vivo. J Immunol 172(5):3059–3069Google Scholar
  12. Bigley V, McGovern N, Milne P et al (2015) Langerin-expressing dendritic cells in human tissues are related to CD1c + dendritic cells and distinct from Langerhans cells and CD141high XCR1 + dendritic cells. J Leukoc Biol 97(4):627–634Google Scholar
  13. Biondo C, Midiri A, Gambuzza M et al (2008) IFN-alpha/beta signaling is required for polarization of cytokine responses toward a protective type 1 pattern during experimental cryptococcosis. J Immunol 181(1):566–573Google Scholar
  14. Biondo C, Signorino G, Costa A et al (2011) Recognition of yeast nucleic acids triggers a host-protective type I interferon response. Eur J Immunol 41(7):1969–1979Google Scholar
  15. Bochud PY, Chien JW, Marr KA et al (2008) Toll-like receptor 4 polymorphisms and aspergillosis in stem-cell transplantation. N Engl J Med 359(17):1766–1777Google Scholar
  16. Bose N, Wurst LR, Chan AS et al (2014) Differential regulation of oxidative burst by distinct beta-glucan-binding receptors and signaling pathways in human peripheral blood mononuclear cells. Glycobiology 24(4):379–391Google Scholar
  17. Branzk N, Lubojemska A, Hardison SE et al (2014) Neutrophils sense microbe size and selectively release neutrophil extracellular traps in response to large pathogens. Nat Immunol 15(11):1017–1025Google Scholar
  18. Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6(1):33–43Google Scholar
  19. Brown GD, Denning DW, Gow NA et al (2012) Hidden killers: human fungal infections. Sci Transl Med 4(165):165rv113Google Scholar
  20. Brown GD, Gordon S (2001) Immune recognition. A new receptor for beta-glucans. Nature 413(6851):36–37Google Scholar
  21. Brown GD, Herre J, Williams DL et al (2003) Dectin-1 mediates the biological effects of beta-glucans. J Exp Med 197(9):1119–1124Google Scholar
  22. Brown GD, Willment JA, Whitehead L (2018) C-type lectins in immunity and homeostasis. Nat Rev Immunol 18(6):374–389Google Scholar
  23. Brubaker SW, Bonham KS, Zanoni I et al (2015) Innate immune pattern recognition: a cell biological perspective. Annu Rev Immunol 33:257–290Google Scholar
  24. Brummer E, Stevens DA (2010) Collectins and fungal pathogens: roles of surfactant proteins and mannose binding lectin in host resistance. Med Mycol 48(1):16–28Google Scholar
  25. Bugarcic A, Hitchens K, Beckhouse AG et al (2008) Human and mouse macrophage-inducible C-type lectin (Mincle) bind Candida albicans. Glycobiology 18(9):679–685Google Scholar
  26. Camilli G, Eren E, Williams DL et al (2018) Impaired phagocytosis directs human monocyte activation in response to fungal derived beta-glucan particles. Eur J Immunol 48(5):757–770Google Scholar
  27. Campos CF, van de Veerdonk FL, Goncalves SM et al (2019) Host genetic signatures of susceptibility to fungal disease. Curr Top Microbiol Immunol 422:237–263Google Scholar
  28. Campuzano A, Castro-Lopez N, Wozniak KL et al (2017) Dectin-3 Is not required for protection against Cryptococcus neoformans infection. PLoS ONE 12(1):e0169347Google Scholar
  29. Carrion Sde J, Leal SM Jr, Ghannoum MA et al (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):2581–2588Google Scholar
  30. Carvalho A, De Luca A, Bozza S et al (2012) TLR3 essentially promotes protective class I-restricted memory CD8(+) T-cell responses to Aspergillus fumigatus in hematopoietic transplanted patients. Blood 119(4):967–977Google Scholar
  31. Carvalho A, Pasqualotto AC, Pitzurra L et al (2008) Polymorphisms in toll-like receptor genes and susceptibility to pulmonary aspergillosis. J Infect Dis 197(4):618–621Google Scholar
  32. Cavalieri D, Di Paola M, Rizzetto L et al (2017) Genomic and phenotypic variation in morphogenetic networks of two Candida albicans isolates subtends their different pathogenic potential. Front Immunol 8:1997Google Scholar
  33. Cheng SC, Quintin J, Cramer RA et al (2014) mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345(6204):1250684Google Scholar
  34. Clark HL, Abbondante S, Minns MS et al (2018) Protein deiminase 4 and CR3 regulate Aspergillus fumigatus and beta-glucan-induced neutrophil extracellular trap formation, but hyphal killing is dependent Only on CR3. Front Immunol 9:1182Google Scholar
  35. Da Silva CA, Chalouni C, Williams A et al (2009) Chitin is a size-dependent regulator of macrophage TNF and IL-10 production. J Immunol 182(6):3573–3582Google Scholar
  36. Dan JM, Kelly RM, Lee CK et al (2008) Role of the mannose receptor in a murine model of Cryptococcus neoformans infection. Infect Immun 76(6):2362–2367Google Scholar
  37. Darling TK, Lamb TJ (2019) Emerging roles for Eph receptors and Ephrin Ligands in immunity. Front Immunol 10:1473Google Scholar
  38. De Jesus M, Ostroff GR, Levitz SM et al (2014) A population of Langerin-positive dendritic cells in murine Peyer’s patches involved in sampling beta-glucan microparticles. PLoS ONE 9(3):e91002Google Scholar
  39. de Jong MA, Vriend LE, Theelen B 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):1216–1225Google Scholar
  40. del Fresno C, Soulat D, Roth S et al (2013) Interferon-beta production via Dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 38(6):1176–1186Google Scholar
  41. den Dunnen J, Gringhuis SI, Geijtenbeek TB (2009) Innate signaling by the C-type lectin DC-SIGN dictates immune responses. Cancer Immunol Immunother 58(7):1149–1157Google Scholar
  42. Deng Z, Ma S, Zhou H et al (2015) Tyrosine phosphatase SHP-2 mediates C-type lectin receptor-induced activation of the kinase Syk and anti-fungal TH17 responses. Nat Immunol 16(6):642–652Google Scholar
  43. Dennehy KM, Ferwerda G, Faro-Trindade I et al (2008) Syk kinase is required for collaborative cytokine production induced through Dectin-1 and Toll-like receptors. Eur J Immunol 38(2):500–506Google Scholar
  44. Ding K, Shibui A, Wang Y et al (2005) Impaired recognition by Toll-like receptor 4 is responsible for exacerbated murine Pneumocystis pneumonia. Microbes Infect 7(2):195–203Google Scholar
  45. Dong ZM, Murphy JW (1997) Cryptococcal polysaccharides bind to CD18 on human neutrophils. Infect Immun 65(2):557–563Google Scholar
  46. Drewniak A, Gazendam RP, Tool AT et al (2013) Invasive fungal infection and impaired neutrophil killing in human CARD9 deficiency. Blood 121(13):2385–2392Google Scholar
  47. Drummond RA, Dambuza IM, Vautier S et al (2016) CD4(+) T-cell survival in the GI tract requires dectin-1 during fungal infection. Mucosal Immunol 9(2):492–502Google Scholar
  48. Drummond RA, Swamydas M, Oikonomou V et al (2019) CARD9(+) microglia promote antifungal immunity via IL-1beta- and CXCL1-mediated neutrophil recruitment. Nat Immunol 20(5):559–570Google Scholar
  49. Dubourdeau M, Athman R, Balloy V et al (2006) Aspergillus fumigatus induces innate immune responses in alveolar macrophages through the MAPK pathway independently of TLR2 and TLR4. J Immunol 177(6):3994–4001Google Scholar
  50. Erdei A, Lukacsi S, Macsik-Valent B et al (2019) Non-identical twins: different faces of CR3 and CR4 in myeloid and lymphoid cells of mice and men. Semin Cell Dev Biol 85:110–121Google Scholar
  51. Erwig LP, Gow NA (2016) Interactions of fungal pathogens with phagocytes. Nat Rev Microbiol 14(3):163–176Google Scholar
  52. Farhat K, Riekenberg S, Heine H et al (2008) Heterodimerization of TLR2 with TLR1 or TLR6 expands the ligand spectrum but does not lead to differential signaling. J Leukoc Biol 83(3):692–701Google Scholar
  53. Faro-Trindade I, Willment JA, Kerrigan AM et al (2012) Characterisation of innate fungal recognition in the lung. PLoS ONE 7(4):e35675Google Scholar
  54. Feinberg H, Jegouzo SAF, Rex MJ et al (2017) Mechanism of pathogen recognition by human dectin-2. J Biol Chem 292(32):13402–13414Google Scholar
  55. Fonseca FL, Nohara LL, Cordero RJ et al (2010) Immunomodulatory effects of serotype B glucuronoxylomannan from Cryptococcus gattii correlate with polysaccharide diameter. Infect Immun 78(9):3861–3870Google Scholar
  56. Fraser IP, Takahashi K, Koziel H et al (2000) Pneumocystis carinii enhances soluble mannose receptor production by macrophages. Microbes Infect 2(11):1305–1310Google Scholar
  57. Frison N, Taylor ME, Soilleux E et al (2003) Oligolysine-based oligosaccharide clusters: selective recognition and endocytosis by the mannose receptor and dendritic cell-specific intercellular adhesion molecule 3 (ICAM-3)-grabbing nonintegrin. J Biol Chem 278(26):23922–23929Google Scholar
  58. Fuchs K, Cardona Gloria Y, Wolz OO et al (2018) The fungal ligand chitin directly binds TLR2 and triggers inflammation dependent on oligomer size. EMBO Rep 19(12)Google Scholar
  59. Funk SD, Orr AW (2013) Ephs and ephrins resurface in inflammation, immunity, and atherosclerosis. Pharmacol Res 67(1):42–52Google Scholar
  60. Gantner BN, Simmons RM, Canavera SJ et al (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J Exp Med 197(9):1107–1117Google Scholar
  61. Gantner BN, Simmons RM, Underhill DM (2005) Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J 24(6):1277–1286Google Scholar
  62. Gao X, Zhao G, Li C et al (2016) LOX-1 and TLR4 affect each other and regulate the generation of ROS in A. fumigatus keratitis. Int Immunopharmacol 40:392–399Google Scholar
  63. Gasparoto TH, Tessarolli V, Garlet TP et al (2010) Absence of functional TLR4 impairs response of macrophages after Candida albicans infection. Med Mycol 48(8):1009–1017Google Scholar
  64. Gavino AC, Chung JS, Sato K et al (2005) Identification and expression profiling of a human C-type lectin, structurally homologous to mouse dectin-2. Exp Dermatol 14(4):281–288Google Scholar
  65. Gay NJ, Symmons MF, Gangloff M et al (2014) Assembly and localization of Toll-like receptor signalling complexes. Nat Rev Immunol 14(8):546–558Google Scholar
  66. Gazendam RP, van Hamme JL, Tool AT et al (2016) Human neutrophils use different mechanisms to kill Aspergillus fumigatus conidia and hyphae: evidence from phagocyte defects. J Immunol 196(3):1272–1283Google Scholar
  67. Gazendam RP, van Hamme JL, Tool AT et al (2014) Two independent killing mechanisms of Candida albicans by human neutrophils: evidence from innate immunity defects. Blood 124(4):590–597Google Scholar
  68. Gazi U, Rosas M, Singh S et al (2011) Fungal recognition enhances mannose receptor shedding through dectin-1 engagement. J Biol Chem 286(10):7822–7829Google Scholar
  69. Gersuk GM, Underhill DM, Zhu L et al (2006) Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states. J Immunol 176(6):3717–3724Google Scholar
  70. Glocker EO, Hennigs A, Nabavi M et al (2009) A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 361(18):1727–1735Google Scholar
  71. Goodridge HS, Reyes CN, Becker CA et al (2011) Activation of the innate immune receptor Dectin-1 upon formation of a ‘phagocytic synapse’. Nature 472(7344):471–475Google Scholar
  72. Gow NAR, Latge JP Munro CA (2017) The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr 5(3)Google Scholar
  73. Graham LM, Gupta V, Schafer G et al (2012) The C-type lectin receptor CLECSF8 (CLEC4D) is expressed by myeloid cells and triggers cellular activation through Syk kinase. J Biol Chem 287(31):25964–25974Google Scholar
  74. Gresnigt MS, Becker KL, Smeekens SP et al (2013) Aspergillus fumigatus-induced IL-22 is not restricted to a specific Th cell subset and is dependent on complement receptor 3. J Immunol 190(11):5629–5639Google Scholar
  75. Gringhuis SI, den Dunnen J, Litjens M et al (2009) Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappaB activation through Raf-1 and Syk. Nat Immunol 10(2):203–213Google Scholar
  76. Gringhuis SI, den Dunnen J, Litjens M et al (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26(5):605–616Google Scholar
  77. Gringhuis SI, Wevers BA, Kaptein TM et al (2011) Selective C-Rel activation via Malt1 controls anti-fungal T(H)-17 immunity by dectin-1 and dectin-2. PLoS Pathog 7(1):e1001259Google Scholar
  78. Gross O, Gewies A, Finger K et al (2006) Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442(7103):651–656Google Scholar
  79. Gross O, Poeck H, Bscheider M et al (2009) Syk kinase signalling couples to the Nlrp3 inflammasome for anti-fungal host defence. Nature 459(7245):433–436Google Scholar
  80. Guo Y, Chang Q, Cheng L et al (2018) C-Type lectin receptor CD23 Is required for host defense against Candida albicans and Aspergillus fumigatus infection. J Immunol 201(8):2427–2440Google Scholar
  81. Haider M, Dambuza IM, Asamaphan P et al (2019) The pattern recognition receptors dectin-2, mincle, and FcRgamma impact the dynamics of phagocytosis of Candida, Saccharomyces, Malassezia, and Mucor species. PLoS ONE 14(8):e0220867Google Scholar
  82. Hanna S, Etzioni A (2012) Leukocyte adhesion deficiencies. Ann N Y Acad Sci 1250:50–55Google Scholar
  83. He K, Yue LH, Zhao GQ et al (2016) The role of LOX-1 on innate immunity against Aspergillus keratitis in mice. Int J Ophthalmol 9(9):1245–1250Google Scholar
  84. Heinsbroek SE, Taylor PR, Martinez FO et al (2008) Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 4(11):e1000218Google Scholar
  85. Herbst S, Shah A, Mazon Moya M et al (2015) Phagocytosis-dependent activation of a TLR9-BTK-calcineurin-NFAT pathway co-ordinates innate immunity to Aspergillus fumigatus. EMBO Mol Med 7(3):240–258Google Scholar
  86. Hernanz-Falcon P, Joffre O, Williams DL et al (2009) Internalization of Dectin-1 terminates induction of inflammatory responses. Eur J Immunol 39(2):507–513Google Scholar
  87. Hole CR, Leopold Wager CM, Mendiola AS et al (2016) Antifungal activity of plasmacytoid dendritic cells against cryptococcus neoformans in vitro requires expression of Dectin-3 (CLEC4D) and reactive oxygen species. Infect Immun 84(9):2493–2504Google Scholar
  88. Hopke A, Brown AJP, Hall RA et al (2018) Dynamic fungal cell wall architecture in stress adaptation and immune evasion. Trends Microbiol 26(4):284–295Google Scholar
  89. Hu XP, Wang RY, Wang X et al (2015) Dectin-2 polymorphism associated with pulmonary cryptococcosis in HIV-uninfected Chinese patients. Med Mycol 53(8):810–816Google Scholar
  90. Huang JH, Lin CY, Wu SY 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):e1004985Google Scholar
  91. Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110(6):673–687Google Scholar
  92. Icenhour CR, Kottom TJ, Limper AH (2003) Evidence for a melanin cell wall component in Pneumocystis carinii. Infect Immun 71(9):5360–5363Google Scholar
  93. Ifrim DC, Joosten LA, Kullberg BJ et al (2013) Candida albicans primes TLR cytokine responses through a Dectin-1/Raf-1-mediated pathway. J Immunol 190(8):4129–4135Google Scholar
  94. Ifrim DC, Quintin J, Courjol F et al (2016) The role of dectin-2 for host defense against disseminated candidiasis. J Interferon Cytokine Res 36(4):267–276Google Scholar
  95. Igyarto BZ, Haley K, Ortner D et al (2011) Skin-resident murine dendritic cell subsets promote distinct and opposing antigen-specific T helper cell responses. Immunity 35(2):260–272Google Scholar
  96. Jaeger M, van der Lee R, Cheng SC et al (2015) The RIG-I-like helicase receptor MDA5 (IFIH1) is involved in the host defense against candida infections. Eur J Clin Microbiol Infect Dis 34(5):963–974Google Scholar
  97. Janeway CA Jr (1989) Approaching the asymptote? Evolution and revolution in immunology. Cold Spring Harb Symp Quant Biol 54(Pt 1):1–13Google Scholar
  98. Jhingran A, Mar KB, Kumasaka DK et al (2012) Tracing conidial fate and measuring host cell antifungal activity using a reporter of microbial viability in the lung. Cell Rep 2(6):1762–1773Google Scholar
  99. Jouault T, Ibata-Ombetta S, Takeuchi O et al (2003) Candida albicans phospholipomannan is sensed through toll-like receptors. J Infect Dis 188(1):165–172Google Scholar
  100. Kasperkovitz PV, Khan NS, Tam JM et al (2011) Toll-like receptor 9 modulates macrophage antifungal effector function during innate recognition of Candida albicans and Saccharomyces cerevisiae. Infect Immun 79(12):4858–4867Google Scholar
  101. Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11(5):373–384Google Scholar
  102. Kerscher B, Wilson GJ, Reid DM et al (2016) Mycobacterial receptor, Clec4d (CLECSF8, MCL), is coregulated with Mincle and upregulated on mouse myeloid cells following microbial challenge. Eur J Immunol 46(2):381–389Google Scholar
  103. Kesh S, Mensah NY, Peterlongo P et al (2005) TLR1 and TLR6 polymorphisms are associated with susceptibility to invasive aspergillosis after allogeneic stem cell transplantation. Ann N Y Acad Sci 1062:95–103Google Scholar
  104. Kilmon MA, Shelburne AE, Chan-Li Y et al (2004) CD23 trimers are preassociated on the cell surface even in the absence of its ligand, IgE. J Immunol 172(2):1065–1073Google Scholar
  105. Koldehoff M, Beelen DW, Elmaagacli AH (2013) Increased susceptibility for aspergillosis and post-transplant immune deficiency in patients with gene variants of TLR4 after stem cell transplantation. Transpl Infect Dis 15(5):533–539Google Scholar
  106. Kosmidis C, Denning DW (2015) The clinical spectrum of pulmonary aspergillosis. Thorax 70(3):270–277Google Scholar
  107. Kottom TJ, Hebrink DM, Jenson PE et al (2018) Dectin-2 is a C-type lectin receptor that recognizes pneumocystis and participates in innate immune responses. Am J Respir Cell Mol Biol 58(2):232–240Google Scholar
  108. Kottom TJ, Hebrink DM, Jenson PE et al (2017) The interaction of pneumocystis with the C-type lectin receptor mincle exerts a significant role in host defense against infection. J Immunol 198(9):3515–3525Google Scholar
  109. Kottom TJ, Hebrink DM, Monteiro JT et al (2019) Myeloid C-type lectin receptors that recognize fungal mannans interact with Pneumocystis organisms and major surface glycoprotein. J Med Microbiol 68(11):1649–1654Google Scholar
  110. Kwon-Chung KJ, Fraser JA, Doering TL et al (2014) Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis. Cold Spring Harb Perspect Med 4(7):a019760Google Scholar
  111. Lam JS, Huang H, Levitz SM (2007) Effect of differential N-linked and O-linked mannosylation on recognition of fungal antigens by dendritic cells. PLoS ONE 2(10):e1009Google Scholar
  112. Lanternier F, Cypowyj S, Picard C et al (2013) Primary immunodeficiencies underlying fungal infections. Curr Opin Pediatr 25(6):736–747Google Scholar
  113. Latge JP, Beauvais A, Chamilos G (2017) The cell wall of the human fungal pathogen Aspergillus fumigatus: biosynthesis, organization, immune response, and virulence. Annu Rev Microbiol 71:99–116Google Scholar
  114. Lee SJ, Zheng NY, Clavijo M et al (2003) Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect Immun 71(1):437–445Google Scholar
  115. Li C, Zhao G, Che C et al (2015) The role of LOX-1 in innate immunity to Aspergillus fumigatus in corneal epithelial cells. Invest Ophthalmol Vis Sci 56(6):3593–3603Google Scholar
  116. Li LY, Zhang HR, Jiang ZL et al (2018) Overexpression of dendritic cell-specific intercellular adhesion molecule-3-grabbing nonintegrin in dendritic cells protecting against Aspergillosis. Chin Med J (Engl) 131(21):2575–2582Google Scholar
  117. Li X, Cullere X, Nishi H et al (2016) PKC-delta activation in neutrophils promotes fungal clearance. J Leukoc Biol 100(3):581–588Google Scholar
  118. Li X, Utomo A, Cullere X et al (2011) The beta-glucan receptor Dectin-1 activates the integrin Mac-1 in neutrophils via Vav protein signaling to promote Candida albicans clearance. Cell Host Microbe 10(6):603–615Google Scholar
  119. Lim J, Coates CJ, Seoane PI et al (2018) Characterizing the mechanisms of nonopsonic uptake of cryptococci by macrophages. J Immunol 200(10):3539–3546Google Scholar
  120. Loures FV, Rohm M, Lee CK et al (2015) Recognition of Aspergillus fumigatus hyphae by human plasmacytoid dendritic cells is mediated by dectin-2 and results in formation of extracellular traps. PLoS Pathog 11(2):e1004643Google Scholar
  121. Lowell CA (2011). Src-family and Syk kinases in activating and inhibitory pathways in innate immune cells: signaling cross talk. Cold Spring Harb Perspect Biol 3(3)Google Scholar
  122. Lowman DW, Greene RR, Bearden DW 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):3432–3443Google Scholar
  123. Ma J, Becker C, Lowell CA et al (2012) Dectin-1-triggered recruitment of light chain 3 protein to phagosomes facilitates major histocompatibility complex class II presentation of fungal-derived antigens. J Biol Chem 287(41):34149–34156Google Scholar
  124. Mambula SS, Sau K, Henneke P et al (2002) Toll-like receptor (TLR) signaling in response to Aspergillus fumigatus. J Biol Chem 277(42):39320–39326Google Scholar
  125. Mansour MK, Latz E, Levitz SM (2006) Cryptococcus neoformans glycoantigens are captured by multiple lectin receptors and presented by dendritic cells. J Immunol 176(5):3053–3061Google Scholar
  126. Mansour MK, Tam JM, Khan NS et al (2013) Dectin-1 activation controls maturation of beta-1,3-glucan-containing phagosomes. J Biol Chem 288(22):16043–16054Google Scholar
  127. Marakalala MJ, Vautier S, Potrykus J et al (2013) Differential adaptation of Candida albicans in vivo modulates immune recognition by dectin-1. PLoS Pathog 9(4):e1003315Google Scholar
  128. Marcos CM, de Oliveira HC, de Melo WC et al (2016) Anti-immune strategies of pathogenic fungi. Front Cell Infect Microbiol 6:142Google Scholar
  129. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92(6):1177–1186Google Scholar
  130. McCloskey N, Hunt J, Beavil RL et al (2007) Soluble CD23 monomers inhibit and oligomers stimulate IGE synthesis in human B cells. J Biol Chem 282(33):24083–24091Google Scholar
  131. McGreal EP, Rosas M, Brown GD et al (2006) The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16(5):422–430Google Scholar
  132. Means TK, Mylonakis E, Tampakakis E et al (2009) Evolutionarily conserved recognition and innate immunity to fungal pathogens by the scavenger receptors SCARF1 and CD36. J Exp Med 206(3):637–653Google Scholar
  133. Miro MS, Rodriguez E, Vigezzi C et al (2018) Contribution of TLR2 pathway in the pathogenesis of vulvovaginal candidiasis. Pathog Dis 76(5)Google Scholar
  134. Mitchell DA, Fadden AJ, Drickamer K (2001) A novel mechanism of carbohydrate recognition by the C-type lectins DC-SIGN and DC-SIGNR. Subunit organization and binding to multivalent ligands. J Biol Chem 276(31):28939–28945Google Scholar
  135. Mitchell S, Vargas J, Hoffmann A (2016) Signaling via the NFkappaB system. Wiley Interdiscip Rev Syst Biol Med 8(3):227–241Google Scholar
  136. Miyazato A, Nakamura K, Yamamoto N et al (2009) Toll-like receptor 9-dependent activation of myeloid dendritic cells by Deoxynucleic acids from Candida albicans. Infect Immun 77(7):3056–3064Google Scholar
  137. Monari C, Bistoni F, Casadevall A et al (2005) Glucuronoxylomannan, a microbial compound, regulates expression of costimulatory molecules and production of cytokines in macrophages. J Infect Dis 191(1):127–137Google Scholar
  138. Moreira AP, Cavassani KA, Ismailoglu UB et al (2011) The protective role of TLR6 in a mouse model of asthma is mediated by IL-23 and IL-17A. J Clin Invest 121(11):4420–4432Google Scholar
  139. Mukaremera L, Lee KK, Wagener J et al (2018) Titan cell production in Cryptococcus neoformans reshapes the cell wall and capsule composition during infection. Cell Surf 1:15–24Google Scholar
  140. Munoz JF, Delorey T, Ford CB et al (2019) Coordinated host-pathogen transcriptional dynamics revealed using sorted subpopulations and single macrophages infected with Candida albicans. Nat Commun 10(1):1607Google Scholar
  141. Myers RC, Dunaway CW, Nelson MP et al (2013) STAT4-dependent and -independent Th2 responses correlate with protective immunity against lung infection with Pneumocystis murina. J Immunol 190(12):6287–6294Google Scholar
  142. Nakamura K, Kinjo T, Saijo S et al (2007) Dectin-1 is not required for the host defense to Cryptococcus neoformans. Microbiol Immunol 51(11):1115–1119Google Scholar
  143. Nakamura K, Miyagi K, Koguchi Y et al (2006) Limited contribution of Toll-like receptor 2 and 4 to the host response to a fungal infectious pathogen, Cryptococcus neoformans. FEMS Immunol Med Microbiol 47(1):148–154Google Scholar
  144. Nakamura K, Miyazato A, Xiao G et al (2008) Deoxynucleic acids from Cryptococcus neoformans activate myeloid dendritic cells via a TLR9-dependent pathway. J Immunol 180(6):4067–4074Google Scholar
  145. Nakamura Y, Sato K, Yamamoto H 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):671–681Google Scholar
  146. Netea MG, Gow NA, Joosten LA et al (2010) Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 48(7):897–903Google Scholar
  147. Netea MG, Gow NA, Munro CA 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):1642–1650Google Scholar
  148. Netea MG, Sutmuller R, Hermann C et al (2004) Toll-like receptor 2 suppresses immunity against Candida albicans through induction of IL-10 and regulatory T cells. J Immunol 172(6):3712–3718Google Scholar
  149. Netea MG, Warris A, Van der Meer JW et al (2003) Aspergillus fumigatus evades immune recognition during germination through loss of toll-like receptor-4-mediated signal transduction. J Infect Dis 188(2):320–326Google Scholar
  150. Oliveira-Nascimento L, Massari P, Wetzler LM (2012) The role of TLR2 in infection and immunity. Front Immunol 3:79Google Scholar
  151. Overton NL, Simpson A, Bowyer P et al (2017) Genetic susceptibility to severe asthma with fungal sensitization. Int J Immunogenet 44(3):93–106Google Scholar
  152. Palaniyandi S, Tomei E, Li Z et al (2011) CD23-dependent transcytosis of IgE and immune complex across the polarized human respiratory epithelial cells. J Immunol 186(6):3484–3496Google Scholar
  153. Papayannopoulos V (2018) Neutrophil extracellular traps in immunity and disease. Nat Rev Immunol 18(2):134–147Google Scholar
  154. Park CG, Takahara K, Umemoto E et al (2001) Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN. Int Immunol 13(10):1283–1290Google Scholar
  155. Patel VI, Booth JL, Duggan ES et al (2017) Transcriptional classification and functional characterization of human airway macrophage and dendritic cell subsets. J Immunol 198(3):1183–1201Google Scholar
  156. Picard C, Puel A, Bonnet M et al (2003) Pyogenic bacterial infections in humans with IRAK-4 deficiency. Science 299(5615):2076–2079Google Scholar
  157. Pietrella D, Bistoni G, Corbucci C et al (2006) Candida albicans mannoprotein influences the biological function of dendritic cells. Cell Microbiol 8(4):602–612Google Scholar
  158. Powlesland AS, Ward EM, Sadhu SK et al (2006) Widely divergent biochemical properties of the complete set of mouse DC-SIGN-related proteins. J Biol Chem 281(29):20440–20449Google Scholar
  159. Prieto D, Carpena N, Maneu V et al (2016) TLR2 modulates gut colonization and dissemination of Candida albicans in a murine model. Microbes Infect 18(10):656–660Google Scholar
  160. Qiu Y, Zeltzer S, Zhang Y et al (2012) Early induction of CCL7 downstream of TLR9 signaling promotes the development of robust immunity to cryptococcal infection. J Immunol 188(8):3940–3948Google Scholar
  161. Quintin J, Saeed S, Martens JHA et al (2012) Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12(2):223–232Google Scholar
  162. Rajaram MVS, Arnett E, Azad AK et al (2017) M. tuberculosis-initiated human mannose receptor signaling regulates macrophage recognition and vesicle trafficking by FcRgamma-Chain, Grb2, and SHP-1. Cell Rep 21(1):126–140Google Scholar
  163. Ramaprakash H, Ito T, Standiford TJ et al (2009) Toll-like receptor 9 modulates immune responses to Aspergillus fumigatus conidia in immunodeficient and allergic mice. Infect Immun 77(1):108–119Google Scholar
  164. Robinson MJ, Osorio F, Rosas M et al (2009) Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J Exp Med 206(9):2037–2051Google Scholar
  165. Rogers NC, Slack EC, Edwards AD et al (2005) Syk-dependent cytokine induction by Dectin-1 reveals a novel pattern recognition pathway for C type lectins. Immunity 22(4):507–517Google Scholar
  166. Romani L (2011) Immunity to fungal infections. Nat Rev Immunol 11(4):275–288Google Scholar
  167. Rosentul DC, Delsing CE, Jaeger M et al (2014) Gene polymorphisms in pattern recognition receptors and susceptibility to idiopathic recurrent vulvovaginal candidiasis. Front Microbiol 5:483Google Scholar
  168. Ross GD, Cain JA, Myones BL et al (1987) Specificity of membrane complement receptor type three (CR3) for beta-glucans. Complement 4(2):61–74Google Scholar
  169. Roth S, Bergmann H, Jaeger M et al (2016) Vav proteins are key regulators of card9 signaling for innate antifungal immunity. Cell Rep 17(10):2572–2583Google Scholar
  170. Saeed S, Quintin J, Kerstens HH et al (2014) Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 345(6204):1251086Google Scholar
  171. Saijo S, Fujikado N, Furuta T et al (2007) Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans. Nat Immunol 8(1):39–46Google Scholar
  172. Saijo S, Ikeda S, Yamabe K 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):681–691Google Scholar
  173. Sainz J, Lupianez CB, Segura-Catena J et al (2012) Dectin-1 and DC-SIGN polymorphisms associated with invasive pulmonary Aspergillosis infection. PLoS ONE 7(2):e32273Google Scholar
  174. Sancho D, Reis e Sousa C (2012) Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 30:491–529Google Scholar
  175. Sato K, Yang XL, Yudate T et al (2006) Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem 281(50):38854–38866Google Scholar
  176. Sattler S, Reiche D, Sturtzel C et al (2012) The human C-type lectin-like receptor CLEC-1 is upregulated by TGF-beta and primarily localized in the endoplasmic membrane compartment. Scand J Immunol 75(3):282–292Google Scholar
  177. Serrano-Gomez D, Leal JA, Corbi AL (2005) DC-SIGN mediates the binding of Aspergillus fumigatus and keratinophylic fungi by human dendritic cells. Immunobiology 210(2–4):175–183Google Scholar
  178. Shah VB, Ozment-Skelton TR, Williams DL et al (2009) Vav1 and PI3K are required for phagocytosis of beta-glucan and subsequent superoxide generation by microglia. Mol Immunol 46(8–9):1845–1853Google Scholar
  179. Shoham S, Huang C, Chen JM et al (2001) Toll-like receptor 4 mediates intracellular signaling without TNF-alpha release in response to Cryptococcus neoformans polysaccharide capsule. J Immunol 166(7):4620–4626Google Scholar
  180. Skalski JH, Kottom TJ Limper AH (2015) Pathobiology of Pneumocystis pneumonia: life cycle, cell wall and cell signal transduction. FEMS Yeast Res 15(6)Google Scholar
  181. Smeekens SP, van de Veerdonk FL, Joosten LAB, Jacobs L, Jansen T, Williams DL, van der Meer JVM, Kullberg BJ, Netea MG (2011) The classical CD14++CD16 monocytes, but not the patrolling CD14+CD16+ monocytes, promote Th17 responses to Candida albicans. Eur J Immunol 41(10):2915–2924Google Scholar
  182. Smith DFQ, Casadevall A (2019) The role of melanin in fungal pathogenesis for animal hosts. Curr Top Microbiol Immunol 422:1–30Google Scholar
  183. Sparber F, Dolowschiak T, Mertens S et al (2018) Langerin + DCs regulate innate IL-17 production in the oral mucosa during Candida albicans-mediated infection. PLoS Pathog 14(5):e1007069Google Scholar
  184. Speakman EA, Dambuza IM, Salazar F et al (2020) T Cell antifungal immunity and the role of C-Type lectin receptors. Trends Immunol 41(1):61–76Google Scholar
  185. Speth C, Rambach G, Wurzner R et al (2008) Complement and fungal pathogens: an update. Mycoses 51(6):477–496Google Scholar
  186. Stappers MHT, Clark AE, Aimanianda V et al (2018) Recognition of DHN-melanin by a C-type lectin receptor is required for immunity to Aspergillus. Nature 555(7696):382–386Google Scholar
  187. Steele C, Marrero L, Swain S et al (2003) Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the Dectin-1 beta-glucan receptor. J Exp Med 198(11):1677–1688Google Scholar
  188. Steele C, Rapaka RR, Metz A et al (2005) The beta-glucan receptor dectin-1 recognizes specific morphologies of Aspergillus fumigatus. PLoS Pathog 1(4):e42Google Scholar
  189. Stephen-Victor E, Karnam A, Fontaine T et al (2017) Aspergillus fumigatus cell wall alpha-(1,3)-glucan stimulates regulatory T-cell polarization by inducing PD-L1 expression on human dendritic cells. J Infect Dis 216(10):1281–1294Google Scholar
  190. Strasser D, Neumann K, Bergmann H et al (2012) Syk kinase-coupled C-type lectin receptors engage protein kinase C-sigma to elicit Card9 adaptor-mediated innate immunity. Immunity 36(1):32–42Google Scholar
  191. Sun H, Xu XY, Tian XL et al (2014) Activation of NF-kappaB and respiratory burst following Aspergillus fumigatus stimulation of macrophages. Immunobiology 219(1):25–36Google Scholar
  192. Swidergall M, Solis NV, Lionakis MS et al (2018) EphA2 is an epithelial cell pattern recognition receptor for fungal beta-glucans. Nat Microbiol 3(1):53–61Google Scholar
  193. Swidergall M, Solis NV, Wang Z et al (2019) EphA2 Is a neutrophil receptor for Candida albicans that stimulates antifungal activity during oropharyngeal infection. Cell Rep 28(2):423–433.e425Google Scholar
  194. Tada H, Nemoto E, Shimauchi H 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):503–512Google Scholar
  195. Takahara K, Omatsu Y, Yashima Y et al (2002) Identification and expression of mouse Langerin (CD207) in dendritic cells. Int Immunol 14(5):433–444Google Scholar
  196. Takahara K, Arita T, Tokieda S et al (2012a) Difference in fine specificity to polysaccharides of Candida albicans mannoprotein between mouse SIGNR1 and human DC-SIGN. Infect Immun 80(5):1699–1706Google Scholar
  197. Takahara K, Tokieda S, Nagaoka K et al (2012b) Efficient capture of Candida albicans and zymosan by SIGNR1 augments TLR2-dependent TNF-alpha production. Int Immunol 24(2):89–96Google Scholar
  198. Tassi I, Cella M, Castro I et al (2009) Requirement of phospholipase C-gamma2 (PLCgamma2) for Dectin-1-induced antigen presentation and induction of TH1/TH17 polarization. Eur J Immunol 39(5):1369–1378Google Scholar
  199. Tateno H, Ohnishi K, Yabe R et al (2010) Dual specificity of Langerin to sulfated and mannosylated glycans via a single C-type carbohydrate recognition domain. J Biol Chem 285(9):6390–6400Google Scholar
  200. Taylor PR, Brown GD, Herre J et al (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):1157–1162Google Scholar
  201. Taylor PR, Roy S, Leal SM Jr et al (2014) Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORgammat and dectin-2. Nat Immunol 15(2):143–151Google Scholar
  202. Taylor PR, Tsoni SV, Willment JA et al (2007) Dectin-1 is required for beta-glucan recognition and control of fungal infection. Nat Immunol 8(1):31–38Google Scholar
  203. Thebault P, Lhermite N, Tilly G et al (2009) The C-type lectin-like receptor CLEC-1, expressed by myeloid cells and endothelial cells, is up-regulated by immunoregulatory mediators and moderates T cell activation. J Immunol 183(5):3099–3108Google Scholar
  204. Thompson A, Davies LC, Liao CT et al (2019) The protective effect of inflammatory monocytes during systemic C. albicans infection is dependent on collaboration between C-type lectin-like receptors. PLoS Pathog 15(6):e1007850Google Scholar
  205. Urban CF, Reichard U, Brinkmann V et al (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 8(4):668–676Google Scholar
  206. van Bruggen R, Drewniak A, Jansen M et al (2009) Complement receptor 3, not Dectin-1, is the major receptor on human neutrophils for beta-glucan-bearing particles. Mol Immunol 47(2–3):575–581Google Scholar
  207. van de Veerdonk FL, Marijnissen RJ, Kullberg BJ et al (2009) The macrophage mannose receptor induces IL-17 in response to Candida albicans. Cell Host Microbe 5(4):329–340Google Scholar
  208. van der Graaf CA, Netea MG, Verschueren I et al (2005) Differential cytokine production and Toll-like receptor signaling pathways by Candida albicans blastoconidia and hyphae. Infect Immun 73(11):7458–7464Google Scholar
  209. Vautier S, Drummond RA, Redelinghuys P et al (2012) Dectin-1 is not required for controlling Candida albicans colonization of the gastrointestinal tract. Infect Immun 80(12):4216–4222Google Scholar
  210. Vera J, Fenutria R, Canadas O et al (2009) The CD5 ectodomain interacts with conserved fungal cell wall components and protects from zymosan-induced septic shock-like syndrome. Proc Natl Acad Sci U S A 106(5):1506–1511Google Scholar
  211. Vijayan D, Radford KJ, Beckhouse AG et al (2012) Mincle polarizes human monocyte and neutrophil responses to Candida albicans. Immunol Cell Biol 90(9):889–895Google Scholar
  212. von Bernuth H, Picard C, Jin Z et al (2008) Pyogenic bacterial infections in humans with MyD88 deficiency. Science 321(5889):691–696Google Scholar
  213. Wagener J, Malireddi RK, Lenardon MD et al (2014) Fungal chitin dampens inflammation through IL-10 induction mediated by NOD2 and TLR9 activation. PLoS Pathog 10(4):e1004050Google Scholar
  214. Walker AN, Garner RE, Horst MN (1990) Immunocytochemical detection of chitin in Pneumocystis carinii. Infect Immun 58(2):412–415Google Scholar
  215. Walsh NM, Wuthrich M, Wang H et al (2017) Characterization of C-type lectins reveals an unexpectedly limited interaction between Cryptococcus neoformans spores and Dectin-1. PLoS ONE 12(3):e0173866Google Scholar
  216. Wang JE, Warris A, Ellingsen EA et al (2001) Involvement of CD14 and toll-like receptors in activation of human monocytes by Aspergillus fumigatus hyphae. Infect Immun 69(4):2402–2406Google Scholar
  217. Wang JP, Lee CK, Akalin A et al (2011) Contributions of the MyD88-dependent receptors IL-18R, IL-1R, and TLR9 to host defenses following pulmonary challenge with Cryptococcus neoformans. PLoS ONE 6(10):e26232Google Scholar
  218. Wang Q, Zhao G, Lin J et al (2016) Role of the mannose receptor during Aspergillus fumigatus Infection and Interaction With Dectin-1 in corneal epithelial cells. Cornea 35(2):267–273Google Scholar
  219. Wang SH, Zhang C, Lasbury ME et al (2008) Decreased inflammatory response in Toll-like receptor 2 knockout mice is associated with exacerbated Pneumocystis pneumonia. Microbes Infect 10(4):334–341Google Scholar
  220. Warr GA (1980) A macrophage receptor for (mannose/glucosamine)-glycoproteins of potential importance in phagocytic activity. Biochem Biophys Res Commun 93(3):737–745Google Scholar
  221. Wells CA, Salvage-Jones JA, Li X 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):7404–7413Google Scholar
  222. Werner JL, Metz AE, Horn D et al (2009) Requisite role for the dectin-1 beta-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182(8):4938–4946Google Scholar
  223. Wevers BA, Kaptein TM, Zijlstra-Willems EM et al (2014) Fungal engagement of the C-type lectin mincle suppresses dectin-1-induced antifungal immunity. Cell Host Microbe 15(4):494–505Google Scholar
  224. Wheeler RT, Kombe D, Agarwala SD et al (2008) Dynamic, morphotype-specific Candida albicans beta-glucan exposure during infection and drug treatment. PLoS Pathog 4(12):e1000227Google Scholar
  225. Wiesner DL, Specht CA, Lee CK et al (2015) Chitin recognition via chitotriosidase promotes pathologic type-2 helper T cell responses to cryptococcal infection. PLoS Pathog 11(3):e1004701Google Scholar
  226. Wirnsberger G, Zwolanek F, Asaoka T et al (2016) Inhibition of CBLB protects from lethal Candida albicans sepsis. Nat Med 22(8):915–923Google Scholar
  227. Wong SSW, Aimanianda V (2017) Host Soluble Mediators: Defying the Immunological Inertness of Aspergillus fumigatus Conidia. J Fungi (Basel) 4(1)Google Scholar
  228. Wu Z, Zhang Z, Lei Z et al (2019) CD14: Biology and role in the pathogenesis of disease. Cytokine Growth Factor Rev 48:24–31Google Scholar
  229. Xiao Y, Tang J, Guo H et al (2016) Targeting CBLB as a potential therapeutic approach for disseminated candidiasis. Nat Med 22(8):906–914Google Scholar
  230. Xu Q, Zhao G, Lin J et al (2015) Role of Dectin-1 in the innate immune response of rat corneal epithelial cells to Aspergillus fumigatus. BMC Ophthalmol 15:126Google Scholar
  231. Xu S, Huo J, Lee KG et al (2009) Phospholipase Cgamma2 is critical for Dectin-1-mediated Ca2 + flux and cytokine production in dendritic cells. J Biol Chem 284(11):7038–7046Google Scholar
  232. Yauch LE, Mansour MK, Shoham S et al (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):5373–5382Google Scholar
  233. Yu GR, Lin J, Zhang J et al (2018) Mincle in the innate immune response of mice fungal keratitis. Int J Ophthalmol 11(4):539–547Google Scholar
  234. Zani IA, Stephen SL, Mughal NA et al (2015) Scavenger receptor structure and function in health and disease. Cells 4(2):178–201Google Scholar
  235. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272(24):6179–6217Google Scholar
  236. Zhang C, Wang SH, Lasbury ME et al (2006) Toll-like receptor 2 mediates alveolar macrophage response to Pneumocystis murina. Infect Immun 74(3):1857–1864Google Scholar
  237. Zhu LL, Zhao XQ, Jiang C 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):324–334Google Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Remi Hatinguais
    • 1
  • Janet A. Willment
    • 1
  • Gordon D. Brown
    • 1
    Email author
  1. 1.MRC Centre for Medical Mycology at University of ExeterExeterUK

Personalised recommendations