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C-Type Lectin Receptors in Antifungal Immunity

  • Christina Nikolakopoulou
  • Janet A. Willment
  • Gordon D. BrownEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1204)

Abstract

Most fungal species are harmless to humans and some exist as commensals on mucocutaneous surfaces. Yet many fungi are opportunistic pathogens, causing life-threatening invasive infections when the immune system becomes compromised. The fungal cell wall contains conserved pathogen-associated molecular patterns (PAMPs), which allow the immune system to distinguish between self (endogenous molecular patterns) and foreign material. Sensing of invasive microbial pathogens is achieved through recognition of PAMPs by pattern recognition receptors (PRRs). One of the predominant fungal-sensing PRRs is the C-type lectin receptor (CLR) family. These receptors bind to structures present on the fungal cell wall, eliciting various innate immune responses as well as shaping adaptive immunity. In this chapter, we specifically focus on the four major human fungal pathogens, Candida albicans, Aspergillus fumigatus, Cryptococcus neoformans and Pneumocystis jirovecii, reviewing our current understanding of the CLRs that are involved in their recognition and protection of the host.

Keywords

Pathogenic fungi Antifungal immunity PRRs CLRs 

Notes

Acknowledgements

We thank the Wellcome Trust (102705) and the Medical Research Council Centre for Medical Mycology and the University of Exeter (MR/N006364/1) for funding.

References

  1. Ballou ER, Avelar GM, Childers DS et al (2016) Lactate signalling regulates fungal β-glucan masking and immune evasion. Nat Microbiol 2:16238.  https://doi.org/10.1038/nmicrobiol.2016.238
  2. Barrett NA, Maekawa A, Rahman OM et al (2009) Dectin-2 recognition of house dust mite triggers cysteinyl leukotriene generation by dendritic cells. J Immunol 182:1119–1128.  https://doi.org/10.4049/jimmunol.182.2.1119CrossRefPubMedPubMedCentralGoogle Scholar
  3. Bashirova AA, Geijtenbeek TB, van Duijnhoven GC et al (2001) A dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin (DC-SIGN)-related protein is highly expressed on human liver sinusoidal endothelial cells and promotes HIV-1 infection. J Exp Med 193:671–678CrossRefGoogle Scholar
  4. Bi L, Gojestani S, Wu W et al (2010) CARD9 mediates Dectin-2-induced IκBα kinase ubiquitination leading to activation of NF-κB in response to stimulation by the hyphal form of Candida albicans. J Biol Chem 285:25969–25977.  https://doi.org/10.1074/jbc.M110.131300CrossRefPubMedPubMedCentralGoogle Scholar
  5. Blanco-Menéndez N, del Fresno C, Fernandes S et al (2015) SHIP-1 Couples to the Dectin-1 hemITAM and selectively modulates reactive oxygen species production in dendritic cells in response to Candida albicans. J Immunol 195:4466–4478.  https://doi.org/10.4049/jimmunol.1402874CrossRefPubMedPubMedCentralGoogle Scholar
  6. Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6:33–43.  https://doi.org/10.1038/nri1745CrossRefPubMedGoogle Scholar
  7. Brown GD (2011) Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 29:1–21.  https://doi.org/10.1146/annurev-immunol-030409-101229CrossRefPubMedPubMedCentralGoogle Scholar
  8. Brown GD, Denning DW, Gow NAR et al (2012) Hidden killers: human fungal infections. Sci Transl Med 4:1–10.  https://doi.org/10.1126/scitranslmed.3004404CrossRefGoogle Scholar
  9. Brown GD, Willment JA, Whitehead L (2018) C-type lectins in immunity and homeostasis. Nat Rev Immunol 1:1.  https://doi.org/10.1038/s41577-018-0004-8CrossRefGoogle Scholar
  10. Buchanan KL, Murphy JW (1998) What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4:71–83.  https://doi.org/10.3201/eid0401.980109CrossRefPubMedPubMedCentralGoogle Scholar
  11. Camacho E, Vij R, Chrissian C et al (2019) The structural unit of melanin in the cell wall of the fungal pathogen Cryptococcus neoformans. 1–29.  https://doi.org/10.1074/jbc.ra119.008684
  12. Cambi A, Netea MG, Mora-Montes HM et al (2008) Dendritic cell interaction with Candida albicans critically depends on N-linked Mannan. J Biol Chem 283:20590–20599.  https://doi.org/10.1074/jbc.M709334200CrossRefPubMedPubMedCentralGoogle Scholar
  13. Campuzano A, Castro-Lopez N, Wozniak KL et al (2017) Dectin-3 is not required for protection against Cryptococcus neoformans infection. PLoS ONE 12:1–14.  https://doi.org/10.1371/journal.pone.0169347CrossRefGoogle Scholar
  14. Cano E, Planas A, Enamorado M et al (2018) DNGR-1 in dendritic cells limits tissue damage by dampening neutrophil recruitment. Science 362:351–356.  https://doi.org/10.1126/science.aan8423CrossRefPubMedGoogle Scholar
  15. Carvalho A, Giovannini G, De Luca A et al (2012) Dectin-1 isoforms contribute to distinct Th1/Th17 cell activation in mucosal candidiasis. Cell Mol Immunol 9:276–286.  https://doi.org/10.1038/cmi.2012.1CrossRefPubMedPubMedCentralGoogle Scholar
  16. Casadevall A, Rosas AL, Nosanchuk JD (2000) Melanin and virulence in Cryptococcus neoformans. Curr Opin Microbiol 3:354–358.  https://doi.org/10.1016/S1369-5274(00)00103-XCrossRefPubMedGoogle Scholar
  17. Chabé M, Aliouat-Denis CM, Delhaes L et al (2011) Pneumocystis: from a doubtful unique entity to a group of highly diversified fungal species. FEMS Yeast Res 11:2–17.  https://doi.org/10.1111/j.1567-1364.2010.00698.xCrossRefPubMedGoogle Scholar
  18. Chaffin WL, López-Ribot JL, Casanova M et al (1998) Cell wall and secreted proteins of Candida albicans: identification, function, and expression. Microbiol Mol Biol Rev 62:130–180CrossRefGoogle Scholar
  19. Chai LYA, De Boer MGJ, Van Der Velden WJFM et al (2011) The Y238X stop codon polymorphism in the human β-glucan receptor Dectin-1 and susceptibility to invasive aspergillosis. J Infect Dis 203:736–743.  https://doi.org/10.1093/infdis/jiq102CrossRefPubMedPubMedCentralGoogle Scholar
  20. Colonna M, Samaridis J, Angman L (2000) Molecular characterization of two novel C-type lectin-like receptors, one of which is selectively expressed in human dendritic cells. Eur J Immunol 30:697–704.  https://doi.org/10.1002/1521-4141(200002)30:2%3c697:AID-IMMU697%3e3.0.CO;2-MCrossRefPubMedGoogle Scholar
  21. Cunha C, Di Ianni M, Bozza S et al (2010) Dectin-1 Y238X polymorphism associates with susceptibility to invasive aspergillosis in hematopoietic transplantation through impairment of both recipient- and donor-dependent mechanisms of antifungal immunity. Blood 116:5394–5402.  https://doi.org/10.1182/blood-2010-04-279307CrossRefPubMedGoogle Scholar
  22. Daley D, Mani VR, Mohan N et al (2017) Dectin-1 activation on macrophages by galectin 9 promotes pancreatic carcinoma and peritumoral immune tolerance. Nat Med.  https://doi.org/10.1038/nm.4314CrossRefPubMedPubMedCentralGoogle Scholar
  23. Dan JM, Kelly RM, Lee CK, Levitz SM (2008) Role of the mannose receptor in a murine model of Cryptococcus neoformans infection. Infect Immun 76:2362–2367.  https://doi.org/10.1128/IAI.00095-08CrossRefPubMedPubMedCentralGoogle Scholar
  24. Deng Z, Ma S, Zhou H et al (2015) SHP-2 mediates C-type lectin receptors-induced Syk activation and anti-fungal TH17 responses. Nat Immunol 16:642–652.  https://doi.org/10.1038/nature13527.StructureCrossRefPubMedPubMedCentralGoogle Scholar
  25. Denning DW (1998) Invasive aspergillosis. Clin Infect Dis 26:781–803CrossRefGoogle Scholar
  26. Deslée G, Charbonnier AS, Hammad H et al (2002) Involvement of the mannose receptor in the uptake of Derp1, a major mite allergen, by human dendritic cells. J Allergy Clin Immunol 110:763–770.  https://doi.org/10.1067/mai.2002.129121CrossRefPubMedGoogle Scholar
  27. Drummond RA, Brown GD (2011) The role of Dectin-1 in the host defence against fungal infections. Curr Opin Microbiol 14:392–399.  https://doi.org/10.1016/j.mib.2011.07.001CrossRefPubMedGoogle Scholar
  28. Drummond RA, Saijo S, Iwakura Y, Brown GD (2011) The role of Syk/CARD9 coupled C-type lectins in antifungal immunity. Eur J Immunol 41:276–281.  https://doi.org/10.1002/eji.201041252CrossRefPubMedGoogle Scholar
  29. 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 9:492–502.  https://doi.org/10.1038/mi.2015.79CrossRefPubMedGoogle Scholar
  30. Emara M, Royer PJ, Mahdavi J et al (2012) Retagging identifies dendritic cell-specific intercellular adhesion molecule-3 (ICAM3)-grabbing non-integrin (DC-SIGN) protein as a novel receptor for a major allergen from house dust mite. J Biol Chem 287:5756–5763.  https://doi.org/10.1074/jbc.M111.312520CrossRefPubMedGoogle Scholar
  31. Erwig LP, Gow NAR (2016) Interactions of fungal pathogens with phagocytes. Nat Rev Microbiol 14:163–176.  https://doi.org/10.1038/nrmicro.2015.21CrossRefPubMedGoogle Scholar
  32. Escobar N, Ordonez SR, Wösten HAB et al (2016) Hide, keep quiet, and keep low: properties that make Aspergillus fumigatus a successful lung pathogen. Front Microbiol 7:1–13.  https://doi.org/10.3389/fmicb.2016.00438CrossRefGoogle Scholar
  33. Ezekowitz RAB, Williams DJ, Koziel H et al (1991) Uptake of Pneumocystis carinii mediated by the macrophage mannose receptor. Nature 351:155–158.  https://doi.org/10.1038/351155a0CrossRefPubMedGoogle Scholar
  34. Ferwerda B, Ferwerda G, Plantinga TS et al (2009) Human Dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 361:1760–1767.  https://doi.org/10.1056/NEJMoa0901053CrossRefPubMedPubMedCentralGoogle Scholar
  35. Fisher CE, Hohl TM, Fan W et al (2017) Validation of single nucleotide polymorphisms in invasive aspergillosis following hematopoietic cell transplantation. Blood 129:2693–2701.  https://doi.org/10.1182/blood-2016-10-743294CrossRefPubMedPubMedCentralGoogle Scholar
  36. Fraser IP, Takahashi K, Koziel H et al (2000) Pneumocystis carinii enhances soluble mannose receptor production by macrophages. Microbes Infect 2:1305–1310.  https://doi.org/10.1016/S1286-4579(00)01283-1CrossRefPubMedGoogle Scholar
  37. Furmonaviciene R, Ghaemmaghami AM, Boyd SE et al (2007) The protease allergen Derp1 cleaves cell surface DC-SIGN and DC-SIGNR: experimental analysis of in silico substrate identification and implications in allergic responses. Clin Exp Allergy 37:231–242.  https://doi.org/10.1111/j.1365-2222.2007.02651.xCrossRefPubMedGoogle Scholar
  38. Galès A, Conduché A, Bernad J et al (2010) PPARγ controls Dectin-1 expression required for host antifungal defense against Candida albicans. PLoS Pathog 6.  https://doi.org/10.1371/journal.ppat.1000714
  39. Gamaletsou MN, Kontoyiannis DP, Sipsas NV et al (2012) Candida osteomyelitis: analysis of 207 pediatric and adult cases (1970–2011). Clin Infect Dis 55:1338–1351.  https://doi.org/10.1093/cid/cis660
  40. Garcia-Vallejo JJ, van Kooyk Y (2013) The physiological role of DC-SIGN: a tale of mice and men. Trends Immunol 34:482–486.  https://doi.org/10.1016/j.it.2013.03.001CrossRefPubMedGoogle Scholar
  41. Gazi U, Rosas M, Singh S et al (2011) Fungal recognition enhances mannose receptor shedding through Dectin-1 engagement. J Biol Chem 286:7822–7829.  https://doi.org/10.1074/jbc.M110.185025CrossRefPubMedPubMedCentralGoogle Scholar
  42. Geijtenbeek TBH, Gringhuis SI (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9:465–479.  https://doi.org/10.1038/nri2569CrossRefPubMedGoogle Scholar
  43. Gessner MA, Werner JL, Lilly LM et al (2012) Dectin-1-dependent interleukin-22 contributes to early innate lung defense against Aspergillus fumigatus. Infect Immun 80:410–417.  https://doi.org/10.1128/IAI.05939-11CrossRefPubMedPubMedCentralGoogle Scholar
  44. Giles SS, Dagenais TRT, Botts MR et al (2009) Elucidating the pathogenesis of spores from the human fungal pathogen Cryptococcus neoformans. Infect Immun 77:3491–3500.  https://doi.org/10.1128/IAI.00334-09CrossRefPubMedPubMedCentralGoogle Scholar
  45. Goodridge HS, Wolf AJ, Underhill DM (2009) β-glucan recognition by the innate immune system. Immunol Rev 230:38–50Google Scholar
  46. Gour N, Lajoie S, Smole U et al (2018) Dysregulated invertebrate tropomyosin–Dectin-1 interaction confers susceptibility to allergic diseases. Sci Immunol.  https://doi.org/10.1126/sciimmunol.aam9841
  47. Gow NAR, Van De Veerdonk FL, Brown AJP, Netea MG (2012) Candida albicans morphogenesis and host defence: discriminating invasion from colonization. Nat Rev Microbiol 10:112–122.  https://doi.org/10.1038/nrmicro2711CrossRefGoogle Scholar
  48. Griffiths JS, Thompson A, Stott M et al (2018) Differential susceptibility of Dectin-1 isoforms to functional inactivation by neutrophil and fungal proteases. FASEB J 32:3385–3397.  https://doi.org/10.1096/fj.201701145RCrossRefPubMedPubMedCentralGoogle Scholar
  49. 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-κB. Immunity 26:605–616.  https://doi.org/10.1016/j.immuni.2007.03.012CrossRefPubMedGoogle Scholar
  50. Gringhuis SI, den Dunnen J, Litjens M et al (2009) Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-κB activation through Raf-1 and Syk. Nat Immunol 10:203–213.  https://doi.org/10.1038/ni.1692CrossRefPubMedGoogle Scholar
  51. Gugnani HC (2003) Ecology and taxonomy of pathogenic aspergilli. Front Biosci 8:1002.  https://doi.org/10.2741/1002CrossRefGoogle Scholar
  52. Hagen F, Khayhan K, Theelen B et al (2015) Recognition of seven species in the Cryptococcus gattii/Cryptococcus neoformans species complex. Fungal Genet Biol 78:16–48.  https://doi.org/10.1016/j.fgb.2015.02.009CrossRefPubMedGoogle Scholar
  53. Harris N, Super M, Rits M et al (1992) Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription. Blood 80:2363–2373CrossRefGoogle Scholar
  54. Hattori T, Konno S, Hizawa N et al (2009) Genetic variants in the mannose receptor gene (MRC1) are associated with asthma in two independent populations. Immunogenetics.  https://doi.org/10.1007/s00251-009-0403-xCrossRefPubMedGoogle Scholar
  55. Havlickova B, Czaika VA, Fredrich M (2008) Epidemiological trends in skin mycosis worldwide. Mycosis 51:2–15.  https://doi.org/10.1111/j.1439-0507.2008.01606CrossRefGoogle Scholar
  56. Head MG, Fitchett JR, Cooke MK et al (2013) UK investments in global infectious disease research 1997–2010: a case study. Lancet Infect Dis 13:55–64.  https://doi.org/10.1016/S1473-3099(12)70261-XCrossRefPubMedGoogle Scholar
  57. Head MG, Fitchett JR, Atun R, May RC (2014) Systematic analysis of funding awarded for mycology research to institutions in the UK, 1997–2010. BMJ Open 4.  https://doi.org/10.1136/bmjopen-2013-004129
  58. Hefter M, Lother J, Weiß E et al (2017) Human primary myeloid dendritic cells interact with the opportunistic fungal pathogen Aspergillus fumigatus via the C-type lectin receptor Dectin-1. Med Mycol 55:573–578.  https://doi.org/10.1093/mmy/myw105CrossRefPubMedGoogle Scholar
  59. Heilmann CJ, Sorgo AG, Siliakus AR et al (2011) Hyphal induction in the human fungal pathogen Candida albicans reveals a characteristic wall protein profile. Microbiology 157:2297–2307.  https://doi.org/10.1099/mic.0.049395-0CrossRefPubMedGoogle Scholar
  60. Heinsbroek SEM, Taylor PR, Martinez FO et al (2008) Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog 4.  https://doi.org/10.1371/journal.ppat.1000218
  61. Heinsbroek SE, Taylor PR, Rosas M et al (2006) Expression of functionally different Dectin-1 isoforms by murine macrophages. J Immunol 176:5513–5518.  https://doi.org/10.4049/jimmunol.176.9.5513CrossRefPubMedGoogle Scholar
  62. Hernanz-Falcón P, Joffre O, Williams DL, Reis e Sousa C (2009) Internalization of Dectin-1 terminates induction of inflammatory responses. Eur J Immunol 39:507–513.  https://doi.org/10.1002/eji.200838687
  63. Huang HR, Li F, Han H et al (2018) Dectin-3 recognizes glucuronoxylomannan of Cryptococcus neoformans serotype AD and Cryptococcus gattii serotype B to initiate host defense against cryptococcosis. Front Immunol 9.  https://doi.org/10.3389/fimmu.2018.01781
  64. Idnurm A, Bahn YS, Nielsen K et al (2005) Deciphering the model pathogenic fungus Cryptococcus neoformans. Nat Rev Microbiol 3:753–764.  https://doi.org/10.1038/nrmicro1245CrossRefPubMedGoogle Scholar
  65. Ifrim DC, Bain JM, Reid DM et al (2014) Role of Dectin-2 for host defense against systemic infection with Candida glabrata. Infect Immun 82:1064–1073.  https://doi.org/10.1128/IAI.01189-13CrossRefPubMedPubMedCentralGoogle Scholar
  66. Iliev ID, Leonardi I (2017) Fungal dysbiosis: immunity and interactions at mucosal barriers. Nat Rev Immunol 17:635–646.  https://doi.org/10.1038/nri.2017.55CrossRefPubMedPubMedCentralGoogle Scholar
  67. Iliev ID, Funari VA, Taylor KD et al (2012) Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 336:1314–1317.  https://doi.org/10.1126/science.1221789CrossRefPubMedPubMedCentralGoogle Scholar
  68. Janeway CA (1992) The immune system evolved to discriminate infectious nonself from noninfectious self. Immunol Today 13:11–16.  https://doi.org/10.1016/0167-5699(92)90198-GCrossRefPubMedGoogle Scholar
  69. Kashem SW, Igyártó BZ, Gerami-Nejad M et al (2015) Candida albicans morphology and dendritic cell subsets determine T helper cell differentiation. Immunity 42:356–366.  https://doi.org/10.1016/j.immuni.2015.01.008CrossRefPubMedPubMedCentralGoogle Scholar
  70. Kerrigan AM, Brown GD (2009) C-type lectins and phagocytosis. Immunobiology 214:562–575.  https://doi.org/10.1016/j.imbio.2008.11.003CrossRefPubMedPubMedCentralGoogle Scholar
  71. Kerrigan AM, Brown GD (2011) Syk-coupled C-type lectins in immunity. Trends Immunol 32:151–156.  https://doi.org/10.1016/j.it.2011.01.002CrossRefPubMedPubMedCentralGoogle Scholar
  72. Koppel EA, van Gisbergen KPJM, Geijtenbeek TBH, van Kooyk Y (2005) Distinct functions of DC-SIGN and its homologues L-SIGN (DC-SIGNR) and mSIGNR1 in pathogen recognition and immune regulation. Cell Microbiol 7:157–165CrossRefGoogle Scholar
  73. 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.  https://doi.org/10.4049/jimmunol.1600744CrossRefPubMedPubMedCentralGoogle Scholar
  74. 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 58:232–240.  https://doi.org/10.1165/rcmb.2016-0186OCCrossRefPubMedPubMedCentralGoogle Scholar
  75. Kousha M, Tadi R, Soubani AO (2011) Pulmonary aspergillosis: a clinical review. Eur Respir Rev 20:156–174CrossRefGoogle Scholar
  76. Koziel H, Eichbaum Q, Kruskal BA et al (1998) Reduced binding and phagocytosis of Pneumocystis carinii by alveolar macrophages from persons infected with HIV-1 correlates with mannose receptor downregulation. J Clin Invest 102:1332–1344.  https://doi.org/10.1172/JCI560CrossRefPubMedPubMedCentralGoogle Scholar
  77. Krutzik SR, Tan B, Li H et al (2005) TLR activation triggers the rapid differentiation of monocytes into macrophages and dendritic cells. Nat Med 11:653–660.  https://doi.org/10.1038/nm1246CrossRefPubMedPubMedCentralGoogle Scholar
  78. Lasbury ME, Lin P, Tschang D et al (2004) Effect of bronchoalveolar lavage fluid from Pneumocystis carinii-infected hosts on phagocytic activity of alveolar macrophages. Infect Immun 72:2140–2147.  https://doi.org/10.1128/IAI.72.4.2140-2147.2004CrossRefPubMedPubMedCentralGoogle Scholar
  79. Leal SM, Cowden S, Hsia YC et al (2010) Distinct roles for Dectin-1 and TLR4 in the pathogenesis of Aspergillus fumigatus keratitis. PLoS Pathog 6:1–16.  https://doi.org/10.1371/journal.ppat.1000976CrossRefGoogle Scholar
  80. Lee SJ, Zheng NY, Clavijo M, Nussenzweig MC (2003) Normal host defense during systemic candidiasis in mannose receptor-deficient mice. Infect Immun 71:437–445.  https://doi.org/10.1128/IAI.71.1.437-445.2003CrossRefPubMedPubMedCentralGoogle Scholar
  81. Li X, Fleis RI, Shubitowski DM et al (2007) Fine mapping of murine asthma quantitative trait loci and analyses of Ptgs1 and Mrc1 as positional candidate genes. DNA Seq 18:190–195.  https://doi.org/10.1080/10425170701207166CrossRefPubMedGoogle Scholar
  82. 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) 131:2575–2582.  https://doi.org/10.4103/0366-6999.244103CrossRefGoogle Scholar
  83. Lilly LM, Gessner MA, Dunaway CW et al (2012) The β-glucan receptor Dectin-1 promotes lung immunopathology during fungal allergy via IL-22. J Immunol 189:3653–3660.  https://doi.org/10.4049/jimmunol.1201797CrossRefPubMedPubMedCentralGoogle Scholar
  84. Lim J, Coates CJ, Seoane PI et al (2018) Characterizing the mechanisms of nonopsonic uptake of cryptococci by macrophages. J Immunol.  https://doi.org/10.4049/jimmunol.1700790
  85. Lima-Junior DS, Mineo TWP, Calich VLG, Zamboni DS (2017) Dectin-1 activation during Leishmania amazonensis phagocytosis prompts Syk-dependent reactive oxygen species production to trigger inflammasome assembly and restriction of parasite replication. J Immunol 199:2055–2068.  https://doi.org/10.4049/jimmunol.1700258CrossRefPubMedGoogle Scholar
  86. Lobato-Pascual A, Saether PC, Fossum S et al (2013) Mincle, the receptor for mycobacterial cord factor, forms a functional receptor complex with MCL and FcεRI-γ. Eur J Immunol 43:3167–3174.  https://doi.org/10.1002/eji.201343752CrossRefPubMedGoogle Scholar
  87. Loures FV, Röhm 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 11:1–23.  https://doi.org/10.1371/journal.ppat.1004643CrossRefGoogle Scholar
  88. 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 289:3432–3443.  https://doi.org/10.1074/jbc.M113.529131CrossRefPubMedGoogle Scholar
  89. Ma L, Chen Z, Huang DW et al (2016) Genome analysis of three Pneumocystis species reveals adaptation mechanisms to life exclusively in mammalian hosts. Nat Commun 7.  https://doi.org/10.1038/ncomms10740
  90. Maldonado S, Dai J, Singh S et al (2015) Human pDCs express the C-type lectin receptor Dectin-1 and uptake and kill Aspergillus fumigatus spores in vitro (MPF4P.734). J Immunol 194Google Scholar
  91. Marakalala MJ, Vautier S, Potrykus J et al (2013) Differential adaptation of Candida albicans in vivo modulates immune recognition by Dectin-1. PLoS Pathog 9:1–12.  https://doi.org/10.1371/journal.ppat.1003315CrossRefGoogle Scholar
  92. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92:1177–1186.  https://doi.org/10.1189/jlb.0512231CrossRefPubMedGoogle Scholar
  93. Maruyama K, Takayama Y, Kondo T et al (2017) Nociceptors boost the resolution of fungal osteoinflammation via the TRP channel-CGRP-Jdp2 Axis. Cell Rep 19:2730–2742.  https://doi.org/10.1016/j.celrep.2017.06.002CrossRefPubMedGoogle Scholar
  94. 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 16:422–430.  https://doi.org/10.1093/glycob/cwj077CrossRefPubMedGoogle Scholar
  95. Medrano FJ, Montes-Cano M, Conde M et al (2005) Pneumocystis jirovecii in general population. Emerg Infect Dis 11:245–250.  https://doi.org/10.3201/eid1102.040487CrossRefPubMedPubMedCentralGoogle Scholar
  96. Mezger M, Kneitz S, Wozniok I et al (2008) Proinflammatory response of immature human dendritic cells is mediated by Dectin-1 after exposure to Aspergillus fumigatus germ tubes. J Infect Dis 197:924–931.  https://doi.org/10.1086/528694CrossRefPubMedGoogle Scholar
  97. Mora C, Tittensor DP, Adl S, et al (2011) How many species are there on earth and in the ocean? PLoS Biol 9:.  https://doi.org/10.1371/journal.pbio.1001127
  98. 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 1:15–24.  https://doi.org/10.1016/j.tcsw.2017.12.001CrossRefPubMedPubMedCentralGoogle Scholar
  99. Nakamura K, Kinjo T, Saijo S et al (2007) Dectin-1 is not required for the host defense to Cryptococcus neoformans. Microbiol Immunol 51:1115–1119.  https://doi.org/10.1111/j.1348-0421.2007.tb04007.xCrossRefPubMedGoogle Scholar
  100. 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 83:671–681.  https://doi.org/10.1128/IAI.02835-14CrossRefPubMedPubMedCentralGoogle Scholar
  101. Netea MG, Gow NAR, 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.  https://doi.org/10.1172/JCI27114CrossRefPubMedPubMedCentralGoogle Scholar
  102. Netea MG, Gow NAR, Joosten LAB et al (2010) Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 48:897–903.  https://doi.org/10.3109/13693781003621575CrossRefPubMedGoogle Scholar
  103. Nollstadt KH, Powles MA, Fujioka H et al (1994) Use of β-1,3-glucan-specific antibody to study the cyst wall of Pneumocystis carinii and effects of pneumocandin B0 analog L-733,560. Antimicrob Agents Chemother 38:2258–2265.  https://doi.org/10.1128/AAC.38.10.2258CrossRefPubMedPubMedCentralGoogle Scholar
  104. Norimoto A, Hirose K, Iwata A et al (2014) Dectin-2 promotes house dust mite-induced T helper type 2 and type 17 cell differentiation and allergic airway inflammation in mice. Am J Respir Cell Mol Biol 51:201–209.  https://doi.org/10.1165/rcmb.2013-0522OCCrossRefPubMedGoogle Scholar
  105. O’Riordan DM, Standing JE, Limper AH (1995) Pneumocystis carinii glycoprotein A binds macrophage mannose receptors. Infect Immun 63:779–784CrossRefGoogle Scholar
  106. Park CG, Takahara K, Umemoto E et al (2001) Five mouse homologues of the human dendritic cell C-type lectin, DC-SIGN. Int Immunol.  https://doi.org/10.1093/intimm/13.10.1283
  107. Parsons MW, Li L, Wallace AM et al (2014) Dectin-2 regulates the effector phase of house dust mite-elicited pulmonary inflammation independently from its role in sensitization. J Immunol 192:1361–1371.  https://doi.org/10.4049/jimmunol.1301809CrossRefPubMedPubMedCentralGoogle Scholar
  108. Patin EC, Orr SJ, Schaible UE (2017) Macrophage inducible C-type lectin as a multifunctional player in immunity. Front Immunol 8:1–10.  https://doi.org/10.3389/fimmu.2017.00861CrossRefGoogle Scholar
  109. Perfect JR (2005) Cryptococcus neoformans: a sugar-coated killer with designer genes. FEMS Immunol Med Microbiol 45:395–404.  https://doi.org/10.1016/j.femsim.2005.06.005CrossRefPubMedGoogle Scholar
  110. Perlroth J, Choi B, Spellberg B (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45:321–346.  https://doi.org/10.1080/13693780701218689CrossRefPubMedGoogle Scholar
  111. Phair J, Muñoz A, Detels R et al (1990) The risk of Pneumocystis carinii pneumonia among men infected with human immunodeficiency virus type 1. Multicenter AIDS Cohort Study Group. N Engl J Med.  https://doi.org/10.1056/nejm199001183220304
  112. Pinke KH, de Lima HG, Cunha FQ, Lara VS (2016) Mast cells phagocyte Candida albicans and produce nitric oxide by mechanisms involving TLR2 and Dectin-1. Immunobiology 221:220–227.  https://doi.org/10.1016/j.imbio.2015.09.004CrossRefPubMedGoogle Scholar
  113. Plantinga TS, van der Velden WJFM, Ferwerda B et al (2009) Early stop polymorphism in human Dectin-1 is associated with increased Candida colonization in hematopoietic stem cell transplant recipients. Clin Infect Dis 49:724–732.  https://doi.org/10.1086/604714CrossRefPubMedGoogle Scholar
  114. Plantinga M, Guilliams M, Vanheerswynghels M et al (2013) Conventional and monocyte-derived CD11b + dendritic cells initiate and maintain T Helper 2 cell-mediated immunity to house dust mite allergen. Immunity 38:322–335.  https://doi.org/10.1016/j.immuni.2012.10.016CrossRefPubMedGoogle Scholar
  115. Porcaro I, Vidal M, Jouvert S et al (2003) Mannose receptor contribution to Candida albicans phagocytosis by murine E-clone J774 macrophages. J Leukoc Biol 74:206–215.  https://doi.org/10.1189/jlb.1202608CrossRefPubMedGoogle Scholar
  116. 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 281:20440–20449.  https://doi.org/10.1074/jbc.M601925200CrossRefPubMedGoogle Scholar
  117. Rajaram MVS, Arnett E, Azad AK et al (2017) M. tuberculosis-initiated human mannose receptor signaling regulates macrophage recognition and vesicle trafficking by FcRγ-chain, Grb2, and SHP-1. Cell Rep.  https://doi.org/10.1016/j.celrep.2017.09.034
  118. Ritter M, Gross O, Kays S et al (2010) Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci 107:20459–20464.  https://doi.org/10.1073/pnas.1010337107CrossRefPubMedGoogle Scholar
  119. Rizzetto L, Weil T, Cavalieri D (2015) Systems level dissection of Candida recognition by dectins: a matter of fungal morphology and site of infection. Pathogens 4:639–661.  https://doi.org/10.3390/pathogens4030639CrossRefPubMedPubMedCentralGoogle Scholar
  120. Romani L (2011) Immunity to fungal infections. Nat Rev Immunol 11:275–288.  https://doi.org/10.1038/nri2939CrossRefPubMedGoogle Scholar
  121. Royer PJ, Emara M, Yang C et al (2010) The mannose receptor mediates the uptake of diverse native allergens by dendritic cells and determines allergen-induced T cell polarization through modulation of IDO activity. J Immunol 185:1522–1531.  https://doi.org/10.4049/jimmunol.1000774CrossRefPubMedGoogle Scholar
  122. 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 8:39–46.  https://doi.org/10.1038/ni1425CrossRefPubMedGoogle Scholar
  123. 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 32:681–691.  https://doi.org/10.1016/j.immuni.2010.05.001CrossRefPubMedGoogle Scholar
  124. Sainz J, Lupiáñez CB, Segura-Catena J et al (2012) Dectin-1 and DC-SIGN polymorphisms associated with invasive pulmonary aspergillosis infection. PLoS ONE 7:1–10.  https://doi.org/10.1371/journal.pone.0032273CrossRefGoogle Scholar
  125. Salazar F, Sewell HF, Shakib F, Ghaemmaghami AM (2013) The role of lectins in allergic sensitization and allergic disease. J Allergy Clin Immunol 132:27–36.  https://doi.org/10.1016/j.jaci.2013.02.001CrossRefPubMedGoogle Scholar
  126. Sato K, Yang XL, Yudate T et al (2006) Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor γ chain to induce innate immune responses. J Biol Chem 281:38854–38866.  https://doi.org/10.1074/jbc.M606542200CrossRefPubMedGoogle Scholar
  127. Sattler S, Reiche D, Sturtzel C et al (2012) The human C-Type lectin-like receptor CLEC-1 is upregulated by TGF-β and primarily localized in the endoplasmic membrane compartment. Scand J Immunol 75:282–292.  https://doi.org/10.1111/j.1365-3083.2011.02665.xCrossRefPubMedGoogle Scholar
  128. 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 2:1053–1060.  https://doi.org/10.1128/EC.2.5.1053-1060.2003
  129. Schlamm HT, Tarallo M, Baddley JW et al (2013) Aspergillosis in intensive care unit (ICU) patients: epidemiology and economic outcomes. BMC Infect Dis 13.  https://doi.org/10.1186/1471-2334-13-29
  130. Schop J (2007) Protective immunity against Cryptococcus neoformans infection. McGill J Med 10:35–43PubMedPubMedCentralGoogle Scholar
  131. Serrano-Gomez D, Dominguez-Soto A, Ancochea J et al (2004) Dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin mediates binding and internalization of Aspergillus fumigatus conidia by dendritic cells and macrophages. J Immunol 173:5635–5643.  https://doi.org/10.4049/jimmunol.173.9.5635CrossRefPubMedGoogle Scholar
  132. Serrano-Gómez D, Leal JA, Corbí AL (2005) DC-SIGN mediates the binding of Aspergillus fumigatus and keratinophylic fungi by human dendritic cells. Immunobiology 210:175–183.  https://doi.org/10.1016/j.imbio.2005.05.011CrossRefPubMedGoogle Scholar
  133. Shiokawa M, Yamasaki S, Saijo S (2017) C-type lectin receptors in anti-fungal immunity. Curr Opin Microbiol 40:123–130.  https://doi.org/10.1016/j.mib.2017.11.004CrossRefPubMedGoogle Scholar
  134. Skalski JH, Kottom TJ, Limper AH (2015) Pathobiology of Pneumocystis pneumonia: life cycle, cell wall and cell signal transduction. FEMS Yeast Res 15:1–12.  https://doi.org/10.1093/femsyr/fov046CrossRefGoogle Scholar
  135. Sobanov Y, Bernreiter A, Derdak S et al (2001) A novel cluster of lectin-like receptor genes expressed in monocytic, dendritic and endothelial cells maps close to the NK receptor genes in the human NK gene complex. Eur J Immunol 31:3493–3503.  https://doi.org/10.1002/1521-4141(200112)31:12%3c3493:AID-IMMU3493%3e3.0.CO;2-9CrossRefPubMedGoogle Scholar
  136. Soilleux EJ, Barten R, Trowsdale J (2000) DC-SIGN; a related gene, DC-SIGNR and CD23 form a cluster on 19p13. J Immunol 165:2937–2942.  https://doi.org/10.4049/jimmunol.165.6.2937CrossRefPubMedGoogle Scholar
  137. 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 555:382–386.  https://doi.org/10.1038/nature25974CrossRefPubMedPubMedCentralGoogle Scholar
  138. 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 198:1677–1688.  https://doi.org/10.1084/jem.20030932CrossRefPubMedPubMedCentralGoogle Scholar
  139. Stehle SE, Rogers RA, Harmsen AG, Ezekowitz RA (2000) A soluble mannose receptor immunoadhesin enhances phagocytosis of Pneumocystis carinii by human polymorphonuclear leukocytes in vitro. Scand J Immunol 52:131–137.  https://doi.org/10.1046/j.1365-3083.2000.00755.x
  140. Strasser D, Neumann K, Bergmann H et al (2012) Syk kinase-coupled C-type lectin receptors engage protein kinase C-δ to elicit Card9 adaptor-mediated innate immunity. Immunity 36:32–42.  https://doi.org/10.1016/j.immuni.2011.11.015CrossRefPubMedPubMedCentralGoogle Scholar
  141. Sun H, Xu XY, Shao HT et al (2013) Dectin-2 is predominately macrophage restricted and exhibits conspicuous expression during Aspergillus fumigatus invasion in human lung. Cell Immunol 284:60–67.  https://doi.org/10.1016/j.cellimm.2013.06.013CrossRefPubMedGoogle Scholar
  142. Swain SD, Lee SJ, Nussenzweig MC, Harmsen AG (2003) Absence of the macrophage mannose receptor in mice does not increase susceptibility to Pneumocystis carinii infection in vivo. Infect Immun 71:6213–6221.  https://doi.org/10.1128/IAI.71.11.6213-6221.2003CrossRefPubMedPubMedCentralGoogle Scholar
  143. Swidergall M, Filler SG (2017) Oropharyngeal candidiasis: fungal invasion and epithelial cell responses. PLoS Pathog 13:1–7.  https://doi.org/10.1371/journal.ppat.1006056CrossRefGoogle Scholar
  144. Syme RM, Spurrell JCL, Amankwah EK et al (2002) Primary dendritic cells phagocytose Cryptococcus neoformans via mannose receptors and Fcγ receptor II for presentation to T lymphocytes. Infect Immun 70:5972–5981.  https://doi.org/10.1128/IAI.70.11.5972CrossRefPubMedPubMedCentralGoogle Scholar
  145. Taylor PR, Tsoni SV, Willment JA et al (2007) Dectin-1 is required for β-glucan recognition and control of fungal infection. Nat Immunol 8:31–38.  https://doi.org/10.1038/ni1408CrossRefPubMedGoogle Scholar
  146. Taylor PR, Roy S, Leal SM et al (2014) Activation of neutrophils by autocrine IL-17A-IL-17RC interactions during fungal infection is regulated by IL-6, IL-23, RORγt and Dectin-2. Nat Immunol 15:143–151.  https://doi.org/10.1038/ni.2797CrossRefPubMedGoogle Scholar
  147. Thiagarajan PS, Yakubenko VP, Elsori DH et al (2013) Vimentin is an endogenous ligand for the pattern recognition receptor Dectin-1. Cardiovasc Res 99:494–504.  https://doi.org/10.1093/cvr/cvt117CrossRefPubMedPubMedCentralGoogle Scholar
  148. Thomas CF, Limper AH (2004) Pneumocystis pneumonia. N Engl J Med 107:830–842.  https://doi.org/10.1016/S0929-6646(08)60199-0CrossRefGoogle Scholar
  149. 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 5:329–340.  https://doi.org/10.1016/j.chom.2009.02.006CrossRefPubMedGoogle Scholar
  150. Van De Veerdonk FL, Gresnigt MS, Romani L et al (2017) Aspergillus fumigatus morphology and dynamic host interactions. Nat Rev Microbiol 15:661–674.  https://doi.org/10.1038/nrmicro.2017.90CrossRefPubMedGoogle Scholar
  151. 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 80:4216–4222.  https://doi.org/10.1128/IAI.00559-12CrossRefPubMedPubMedCentralGoogle Scholar
  152. Wächtler B, Wilson D, Haedicke K et al (2011) From attachment to damage: defined genes of Candida albicans mediate adhesion, invasion and damage during interaction with oral epithelial cells. PLoS ONE 6.  https://doi.org/10.1371/journal.pone.0017046
  153. Wagener M, Hoving JC, Ndlovu H, Marakalala MJ (2018) Dectin-1-Syk-CARD9 signaling pathway in TB immunity. Front Immunol 9:1–7.  https://doi.org/10.3389/fimmu.2018.00225CrossRefGoogle Scholar
  154. 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 12:1–21.  https://doi.org/10.1371/journal.pone.0173866CrossRefGoogle Scholar
  155. 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.  https://doi.org/10.1097/ICO.0000000000000710CrossRefPubMedGoogle Scholar
  156. Wang H, Lee TJ, Fites SJ et al (2017) Ligation of Dectin-2 with a novel microbial ligand promotes adjuvant activity for vaccination. PLoS Pathog 13:1–20.  https://doi.org/10.1371/journal.ppat.1006568CrossRefGoogle Scholar
  157. Weis WI, Taylor ME, Drickamer K (1998) The C-type lectin superfamily in the immune system. Immunol Rev 163:19–34.  https://doi.org/10.1111/j.1600-065X.1998.tb01185.xCrossRefPubMedGoogle Scholar
  158. Werner JL, Metz AE, Horn D et al (2009) Requisite role for the dectin-1 β-glucan receptor in pulmonary defense against Aspergillus fumigatus. J Immunol 182:4938–4946.  https://doi.org/10.4049/jimmunol.0804250CrossRefPubMedPubMedCentralGoogle Scholar
  159. Williams SJ (2017) Sensing lipids with mincle: structure and function. Front Immunol 8.  https://doi.org/10.3389/fimmu.2017.01662
  160. 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 cornea and external eye diseases. BMC Ophthalmol 15:1–7.  https://doi.org/10.1186/s12886-015-0112-1CrossRefGoogle Scholar
  161. Yang AM, Inamine T, Hochrath K et al (2017) Intestinal fungi contribute to development of alcoholic liver disease. J Clin Invest 127:2829–2841.  https://doi.org/10.1172/JCI90562CrossRefPubMedPubMedCentralGoogle Scholar
  162. Yuan K, Zhao G, Che C et al (2017) Dectin-1 is essential for IL-1β production through JNK activation and apoptosis in Aspergillus fumigatus keratitis. Int Immunopharmacol 52:168–175.  https://doi.org/10.1016/j.intimp.2017.09.008CrossRefPubMedGoogle Scholar
  163. Zaragoza O, Rodrigues ML, De Jesus M et al (2010) The capsule of the fungal pathogen Cryptococcus neoformans. Adv Appl Microbiol 2164:1–64.  https://doi.org/10.1016/S0065-2164(09)01204-0CrossRefGoogle Scholar
  164. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272:6179–6217CrossRefGoogle Scholar
  165. 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 39:324–334.  https://doi.org/10.1016/j.immuni.2013.05.017CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2020

Authors and Affiliations

  • Christina Nikolakopoulou
    • 1
    • 2
  • Janet A. Willment
    • 1
    • 2
  • Gordon D. Brown
    • 1
    • 2
    Email author
  1. 1.Medical Research Council Centre for Medical MycologyUniversity of ExeterExeterUK
  2. 2.Previous address: MRC Centre for Medical MycologyUniversity of AberdeenAberdeenUK

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