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.
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References
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
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.182.2.1119
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 193:671–678
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.M110.131300
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.1402874
Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6:33–43. https://doi.org/10.1038/nri1745
Brown GD (2011) Innate antifungal immunity: the key role of phagocytes. Annu Rev Immunol 29:1–21. https://doi.org/10.1146/annurev-immunol-030409-101229
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.3004404
Brown GD, Willment JA, Whitehead L (2018) C-type lectins in immunity and homeostasis. Nat Rev Immunol 1:1. https://doi.org/10.1038/s41577-018-0004-8
Buchanan KL, Murphy JW (1998) What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4:71–83. https://doi.org/10.3201/eid0401.980109
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
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.M709334200
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.0169347
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.aan8423
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.2012.1
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-X
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.x
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 62:130–180
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/jiq102
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-M
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-2010-04-279307
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.4314
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.00095-08
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.Structure
Denning DW (1998) Invasive aspergillosis. Clin Infect Dis 26:781–803
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.2002.129121
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.2011.07.001
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.201041252
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.2015.79
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.M111.312520
Erwig LP, Gow NAR (2016) Interactions of fungal pathogens with phagocytes. Nat Rev Microbiol 14:163–176. https://doi.org/10.1038/nrmicro.2015.21
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.2016.00438
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/10.1038/351155a0
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/NEJMoa0901053
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-2016-10-743294
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)01283-1
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.x
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
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
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.2013.03.001
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.M110.185025
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/nri2569
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.05939-11
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.00334-09
Goodridge HS, Wolf AJ, Underhill DM (2009) β-glucan recognition by the innate immune system. Immunol Rev 230:38–50
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
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/nrmicro2711
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.201701145R
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.2007.03.012
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.1692
Gugnani HC (2003) Ecology and taxonomy of pathogenic aspergilli. Front Biosci 8:1002. https://doi.org/10.2741/1002
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.2015.02.009
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 80:2363–2373
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-x
Havlickova B, Czaika VA, Fredrich M (2008) Epidemiological trends in skin mycosis worldwide. Mycosis 51:2–15. https://doi.org/10.1111/j.1439-0507.2008.01606
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-X
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
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/myw105
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.0.049395-0
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
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.176.9.5513
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
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
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/nrmicro1245
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.01189-13
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.2017.55
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.1221789
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-G
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.2015.01.008
Kerrigan AM, Brown GD (2009) C-type lectins and phagocytosis. Immunobiology 214:562–575. https://doi.org/10.1016/j.imbio.2008.11.003
Kerrigan AM, Brown GD (2011) Syk-coupled C-type lectins in immunity. Trends Immunol 32:151–156. https://doi.org/10.1016/j.it.2011.01.002
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 7:157–165
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.1600744
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.2016-0186OC
Kousha M, Tadi R, Soubani AO (2011) Pulmonary aspergillosis: a clinical review. Eur Respir Rev 20:156–174
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/JCI560
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/nm1246
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.72.4.2140-2147.2004
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.1000976
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.71.1.437-445.2003
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/10.1080/10425170701207166
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/10.4103/0366-6999.244103
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.1201797
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
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.1700258
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.201343752
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.1004643
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.M113.529131
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
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 194
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.1003315
Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92:1177–1186. https://doi.org/10.1189/jlb.0512231
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.2017.06.002
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/cwj077
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/eid1102.040487
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/10.1086/528694
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
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.2017.12.001
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.x
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.02835-14
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/JCI27114
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/10.3109/13693781003621575
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.38.10.2258
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.2013-0522OC
O’Riordan DM, Standing JE, Limper AH (1995) Pneumocystis carinii glycoprotein A binds macrophage mannose receptors. Infect Immun 63:779–784
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
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.1301809
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.2017.00861
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.2005.06.005
Perlroth J, Choi B, Spellberg B (2007) Nosocomial fungal infections: epidemiology, diagnosis, and treatment. Med Mycol 45:321–346. https://doi.org/10.1080/13693780701218689
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
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.2015.09.004
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/10.1086/604714
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.2012.10.016
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.1202608
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.M601925200
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
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.1010337107
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/pathogens4030639
Romani L (2011) Immunity to fungal infections. Nat Rev Immunol 11:275–288. https://doi.org/10.1038/nri2939
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.1000774
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/ni1425
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.2010.05.001
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.0032273
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.2013.02.001
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.M606542200
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.x
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
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
Schop J (2007) Protective immunity against Cryptococcus neoformans infection. McGill J Med 10:35–43
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.173.9.5635
Serrano-Gómez D, Leal JA, Corbà 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.2005.05.011
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.2017.11.004
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/fov046
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;2-9
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.165.6.2937
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/nature25974
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.20030932
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
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.2011.11.015
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.2013.06.013
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.71.11.6213-6221.2003
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.1006056
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.70.11.5972
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/ni1408
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.2797
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/cvt117
Thomas CF, Limper AH (2004) Pneumocystis pneumonia. N Engl J Med 107:830–842. https://doi.org/10.1016/S0929-6646(08)60199-0
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.2009.02.006
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.2017.90
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.00559-12
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
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.2018.00225
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.0173866
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.0000000000000710
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.1006568
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.x
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.0804250
Williams SJ (2017) Sensing lipids with mincle: structure and function. Front Immunol 8. https://doi.org/10.3389/fimmu.2017.01662
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/s12886-015-0112-1
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/JCI90562
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.2017.09.008
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)01204-0
Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272:6179–6217
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.2013.05.017
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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.
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Nikolakopoulou, C., Willment, J.A., Brown, G.D. (2020). C-Type Lectin Receptors in Antifungal Immunity. In: Hsieh, SL. (eds) Lectin in Host Defense Against Microbial Infections. Advances in Experimental Medicine and Biology, vol 1204. Springer, Singapore. https://doi.org/10.1007/978-981-15-1580-4_1
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