Advertisement

The Ligands of C-Type Lectins

  • Amy J. Foster
  • Jessie H. Bird
  • Mattie S. M. Timmer
  • Bridget L. StockerEmail author
Chapter

Abstract

In this chapter, a comprehensive overview of the known ligands for the C-type lectins (CTLs) is provided. Emphasis has been placed on the chemical structure of the glycans that bind to the different CTLs and the amount of structural variation (or overlap) that each CTL can tolerate. In this way, both the synthetic carbohydrate chemist and the immunologist can more readily gain insight into the existing structure-activity space for the CTL ligands and, ideally, see areas of synergy that will help identify and refine the ligands for these receptors.

Keywords

C-type lectin Receptor Ligand Pathogen Immunity Carbohydrates Glycolipids 

References

  1. Adams EL, Rice PJ, Graves B et al (2008) Differential high-affinity interaction of Dectin-1 with natural or synthetic glucans is dependent upon primary structure and is influenced by polymer chain length and side-chain branching. J Pharmacol Exp Ther 325:115–123PubMedCrossRefGoogle Scholar
  2. Ahrens S, Zelenay S, Sancho D et al (2012) F-Actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 36:635–645PubMedCrossRefGoogle Scholar
  3. Apostolov EO, Shah SV, Ray D et al (2009) Scavenger receptors of endothelial cells mediate the uptake and cellular proatherogenic effects of carbamylated LDL. Arterioscler Thromb Vasc Biol 29:1622–1630PubMedCrossRefGoogle Scholar
  4. Aragane Y, Maeda A, Schwarz A et al (2003) Involvement of Dectin-2 in ultraviolet radiation-induced tolerance. J Immunol 171:3801–3807PubMedCrossRefGoogle Scholar
  5. Ariizumi K, Shen GL, Shikano S et al (2000) Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J Biol Chem 275:20157–20167PubMedCrossRefGoogle Scholar
  6. Bloem K, Vuist IM, van der Plas AJ et al (2013) Ligand binding and signaling of dendritic cell immunoreceptor (DCIR) is modulated by the glycosylation of the carbohydrate recognition domain. PLoS ONE 8, e66266PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bloem K, Vuist IM, van den Berk M et al (2014) DCIR interacts with ligands from both endogenous and pathogenic origin. Immunol Lett 158:33–41PubMedCrossRefGoogle Scholar
  8. Brown GD, Gordon S (2001) Immune recognition: a new receptor for beta-glucans. Nature 413:36–37PubMedCrossRefGoogle Scholar
  9. Burgarcic A, Hitchens K, Beckhouse AG et al (2008) Human and mouse macrophage-inducible C-type lectin (Mincle) bind Candida albicans. Glycobiology 18:679–685CrossRefGoogle Scholar
  10. Chabrol E, Nurisso A, Daina A et al (2012) Glycosaminoglycans are interactants of Langerin: comparison with gp120 highlights an unexpected calcium-independent binding mode. PLoS ONE 7, e50722PubMedPubMedCentralCrossRefGoogle Scholar
  11. Chen XP, Du GH (2007) Lectin-like oxidized low-density lipoprotein receptor-1: protein, ligands, expression and pathophysiological significance. Chin Med J 120:421–426PubMedGoogle Scholar
  12. Chen ST, Lin YL, Huang MT (2008) CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453:672–676PubMedCrossRefGoogle Scholar
  13. Chen S, Liu R, Wu M et al (2012) CLEC5A regulates Japanese encephalitis virus-induced neuroinflammation and lethality. PLoS Pathog 8, e1002655PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chiba S, Ikushima H, Ueki H et al (2014) Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. eLife 3, e04177PubMedPubMedCentralCrossRefGoogle Scholar
  15. Coombs PJ, Graham SA, Drickamer K et al (2005) Selective binding of the scavenger receptor C-type lectin to Lewis(x) trisaccharide and related glycan ligands. J Biol Chem 280:22993–22999PubMedCrossRefGoogle Scholar
  16. Curtis BM, Scharnowske S, Watson AJ (1992) Sequence and expression of a membrane-associated C-type lectin that exhibits CD4-independent binding of human immunodeficiency virus envelope glycoprotein gp120. Proc Nat Acad Sci 89:8356–8360PubMedPubMedCentralCrossRefGoogle Scholar
  17. 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 47:1216–1225PubMedPubMedCentralCrossRefGoogle Scholar
  18. De Witte L, Nabatov A, Pion M et al (2007) Langerin is a natural barrier to HIV-1 transmission by Langerhans cells. Nat Med 13:367–371PubMedCrossRefGoogle Scholar
  19. Dominguez-Soto A, Aragoneses-Fenoll L, Martin-Gayo E et al (2007) The DC-SIGN-related lectin LSECtin mediates antigen capture and pathogen binding by human myeloid cells. Blood 109:5337–5345PubMedCrossRefGoogle Scholar
  20. Dong B, Li D, Li R et al (2014) A chitin-like component on sclerotic cells of Fonsecaea pedrosoi inhibits Dectin-1-mediated murine Th17 development by masking β-glucans. PLoS ONE 9, e114113PubMedPubMedCentralCrossRefGoogle Scholar
  21. Driessen NN, Ummels R, Maaskant JJ et al (2009) Role of phosphatidylinositol mannosides in the interaction between mycobacteria and DC-SIGN. Infect Immun 77:4538–4547PubMedPubMedCentralCrossRefGoogle Scholar
  22. Dzionek A, Sohma Y, Nagafune J et al (2001) BDCA-2, a novel plasmacytoid Dendritic Cell-specific Type II C-type Lectin, mediates antigen capture and is a potent inhibitor of interferon α/β Induction. J Exp Med 194:1823–1834PubMedPubMedCentralCrossRefGoogle Scholar
  23. Ehlers S (2010) DC-SIGN and mannosylated surface structures of Mycobacterium tuberculosis: a deceptive liaison. Eur J Cell Biol 89:95–101PubMedCrossRefGoogle Scholar
  24. Eriksson M, Johannssen T, von Smolinski D et al (2013) The C-Type lectin receptor SIGNR3 binds to fungi present in commensal microbiota and influences immune regulation in experimental colitis. Front Immunol 4:196PubMedPubMedCentralCrossRefGoogle Scholar
  25. Eriksson M, Serna S, Maglinao M et al (2014) Biological evaluation of multivalent LewisX-MGL-1 interactions. ChemBioChem 15:844–851PubMedCrossRefGoogle Scholar
  26. Feinberg H, Rowntree TJ, Tan SL et al (2013) Common polymorphisms in human langerin change specificity for glycan ligands. J Biol Chem 288:36762–36771PubMedPubMedCentralCrossRefGoogle Scholar
  27. Ferry A, Malik G, Guinchard X et al (2014) Synthesis and evaluation of di- and trimeric hydroxylamine-based β-(1→3)-glucan mimetics. J Am Chem Soc 136:14852–14857PubMedCrossRefGoogle Scholar
  28. Furukawa A, Kamishikiryo J, Mori D et al (2013) Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL. Proc Natl Acad Sci U S A 110:17438–17443PubMedPubMedCentralCrossRefGoogle Scholar
  29. Galustian C, Park CG, Chai W et al (2004) High and low affinity carbohydrate ligands revealed for murine SIGN-R1 by carbohydrate array and cell binding approaches, and differing specificities for SIGN-R3 and langerin. Int Immunol 16:853–866PubMedCrossRefGoogle Scholar
  30. Geijtenbeek TB, Groot PC, Nolte MA et al (2002) Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo. Blood 100:2908–2916PubMedCrossRefGoogle Scholar
  31. Geurtsen J, Chedammi S, Mesters J et al (2009) Identification of mycobacterial α-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. J Immunol 183:5221–5231PubMedCrossRefGoogle Scholar
  32. Gillotte KL, Hörkkö S, Witztum JL et al (2000) Oxidized phospholipids, linked to apolipoprotein B of oxidized LDL, are ligands for macrophage scavenger receptors. J Lipid Res 41:824–833PubMedGoogle Scholar
  33. Gramberg T, Hofmann H, Möller P et al (2005) LSECtin interacts with filovirus glycoproteins and the spike protein of SARS coronavirus. Virology 340:224–236PubMedCrossRefGoogle Scholar
  34. Hattori Y, Morita D, Fujiwara N et al (2014) Glycerol monomycolate is a novel ligand for the human, but not mouse macrophage inducible C-type lectin, Mincle. J Biol Chem 289:15405–15412PubMedPubMedCentralCrossRefGoogle Scholar
  35. Holla A, Skerra A (2011) Comparative analysis reveals selective recognition of glycans by the dendritic cell receptors DC-SIGN and langerin. Protein Eng Des Sel 24:659–669PubMedCrossRefGoogle Scholar
  36. Hsu TL, Cheng SC, Yang WB et al (2009) Profiling carbohydrate-receptor interaction with recombinant innate immunity receptor-Fc fusion proteins. J Biol Chem 284:34479–34489PubMedPubMedCentralCrossRefGoogle Scholar
  37. Iida S, Yamamoto K, Irimura T (1999) Interaction of human macrophage C-type lectin with O-linked N-acetylgalactosamine residues on mucin glycopeptides. J Biol Chem 274:10697–10705PubMedCrossRefGoogle Scholar
  38. Ishikawa E, Ishikawa T, Morita YS et al (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206:2879–2888PubMedPubMedCentralCrossRefGoogle Scholar
  39. Ishikawa T, Itoh F, Yoshida S et al (2013) Identification of distinct ligands for the C-type lectin receptors Mincle and Dectin-2 in the pathogenic fungus Malassezia. Cell Host Microbe 13:477–488PubMedCrossRefGoogle Scholar
  40. Jono T, Miyazaki A, Nagai R et al (2002) Lectin-like oxidized low density lipoprotein receptor-1 (LOX-1) serves as an endothelial receptor for advanced glycation end products (AGE). FEBS Lett 511:170–174PubMedCrossRefGoogle Scholar
  41. Joyce-Shaikh B, Bigler ME, Cao CC et al (2010) Myeloid DAP12-associating lectin (MDL)-1 regulates synovial inflammation and bone erosion associated with autoimmune arthritis. J Exp Med 207:579–589PubMedPubMedCentralCrossRefGoogle Scholar
  42. Joyce-Shaikh B, Wilson DC, Cua DJ et al (2014) Mdl-1 Ligand. Patent WO20140227719Google Scholar
  43. Kakutani M, Masaki T, Sawamura T (2000) A platelet-endothelium interaction mediated by lectin-like oxidized low-density lipoprotein receptor-1. Proc Natl Acad Sci U S A 97:360–364PubMedPubMedCentralCrossRefGoogle Scholar
  44. Kaneko MK, Kato Y, Kameyama A et al (2007) Functional glycosylation of human podoplanin: glycan structure of platelet aggregation-inducing factor. FEBS Lett 581:331–336PubMedCrossRefGoogle Scholar
  45. Kang YS, Yamazaki S, Iyoda T et al (2003) SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int Immunol 15:177–186PubMedCrossRefGoogle Scholar
  46. Kang PB, Azad AK, Torrelles JB et al (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202:987–999PubMedPubMedCentralCrossRefGoogle Scholar
  47. Kato Y, Kaneko MK, Kunita A et al (2008) Molecular analysis of the pathophysiological binding of the platelet aggregation-inducing factor podoplanin to the C-type lectin-like receptor CLEC-2. Cancer Sci 99:54–61PubMedGoogle Scholar
  48. Khan AA, Chee SH, McLaughlin RJ et al (2011) Long-chain lipids are required for the innate recognition of trehalose diesters by macrophages. ChemBioChem 12:2572–2576PubMedCrossRefGoogle Scholar
  49. Khan AA, Kamena F, Timmer MS et al (2013) Development of a benzophenone and alkyne functionalised trehalose probe to study trehalose dimycolate binding proteins. Org Biomol Chem 11:881–885PubMedCrossRefGoogle Scholar
  50. Kim HJ, Brennan PJ, Heaslip D et al (2015) Carbohydrate-dependent binding of langerin to SodC, a cell wall glycoprotein of Mycobacterium leprae. J Bacteriol 197:615–625PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kodar K, Eising S, Khan AA et al (2015) The uptake of Trehalose glycolipids by macrophages is independent of Mincle. ChemBioChem 16:683–693PubMedCrossRefGoogle Scholar
  52. Koppel EA, Ludwig IS, Appelmelk BJ et al (2005) Carbohydrate specificities of the murine DC-SIGN homologue mSIGNR1. Immunobiology 210:195–201PubMedCrossRefGoogle Scholar
  53. Kumamoto Y, Linehan M, Weinstein JS et al (2013) CD301b+ dermal dendritic cells drive T helper 2 cell-mediated immunity. Immunity 39:733–743PubMedCrossRefGoogle Scholar
  54. Lahoud MH, Ahmet F, Zhang JG et al (2012) DEC-205 is a cell surface receptor for CpG oligonucleotides. Proc Natl Acad Sci U S A 109:16270–16275PubMedPubMedCentralCrossRefGoogle Scholar
  55. Lambert AA, Gilbert C, Richard M et al (2008) The C-type lectin surface receptor DCIR acts as a new attachment factor for HIV-1 in dendritic cells and contributes to trans- and cis-infection pathways. Blood 112:1299–1307PubMedPubMedCentralCrossRefGoogle Scholar
  56. Laskarin G, Redzovic A, Vlastelic I et al (2011) Tumor-associated glycoprotein (TAG-72) is a natural ligand for the C-type lectin-like domain that induces anti-inflammatory orientation of early pregnancy decidual CD1a+ dendritic cells. Am J Reprod Immunol 88:12–23CrossRefGoogle Scholar
  57. Layzer JM, Mahanty SK, Redick CC et al (2010) Nucleic acid modulators of CLEC-2. Patent WO2012051571Google Scholar
  58. Lee RT, Hsu TL, Huang SK et al (2011) Survey of immune-related, mannose/fucose-binding C-type lectin receptors reveals widely divergent sugar-binding specificities. Glycobiology 21:512–520PubMedPubMedCentralCrossRefGoogle Scholar
  59. Lefèvre L, Lugo-Villarino G, Meunier E et al (2013) The C-type lectin receptors Dectin-1, MR, and SIGNR4 contribute both positively and negatively to the macrophage response to Leishmania infantum. Immunity 38:1038–1049PubMedCrossRefGoogle Scholar
  60. Leteux C, Chai W, Loveless RW et al (2000) The cysteine-rich domain of the macrophage mannose receptor is a multispecific lectin that recognizes chondroitin sulfates A and B and sulfated oligosaccharides of blood group Lewisa and Lewisx types in addition to the sulfated N-glycans of lutropin. J Exp Med 191:1117–1126PubMedPubMedCentralCrossRefGoogle Scholar
  61. Li X, Wang J, Wang W et al (2013) Immunomodulatory activity of a novel, synthetic beta-glucan (β-glu6) in murine macrophages and human peripheral blood mononuclear cells. PLoS ONE 8, e80399PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lightfoot YL, Selle K, Yang T et al (2015) SIGNR3-dependent immune regulation by lactobacillus acidophilus surface layer protein A in colitis. EMBO J 34:881–895PubMedCrossRefGoogle Scholar
  63. Liu W, Tang L, Zhang G et al (2004) Characterization of a novel C-type lectin-like gene, LSECtin: demonstration of carbohydrate binding and expression in sinusoidal endothelial cells of liver and lymph node. J Biol Chem 279:18748–18758PubMedCrossRefGoogle Scholar
  64. Lu J, Yang JH, Burns AR et al (2009) Mediation of electronegative low-density lipoprotein signaling by LOX-1: a possible mechanism of endothelial apoptosis. Circ Res 104:619–627PubMedCrossRefGoogle Scholar
  65. Maeda N, Nigou J, Herrmann JL et al (2003) The cell surface receptor DC-SIGN discriminates between mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J Biol Chem 278:5513–5516PubMedCrossRefGoogle Scholar
  66. Maglinao M, Eriksson M, Schlegel MK et al (2014) A platform to screen for C-type lectin receptor-binding carbohydrates and their potential for cell-specific targeting and immune modulation. J Control Release 175:36–42PubMedCrossRefGoogle Scholar
  67. Manne BK, Getz TM, Hughes CE et al (2013) Fucoidan is a novel platelet agonist for the C-type lectin-like receptor 2 (CLEC-2). J Biol Chem 288:7717–7726PubMedPubMedCentralCrossRefGoogle Scholar
  68. Marsche G, Levak-Frank S, Quehenberger O et al (2001) Identification of the human analog of SR-BI and LOX-1 as receptors for hypochlorite-modified high-density lipoprotein on human umbilical venous endothelial cells. FASEB J 15:1095–1097PubMedGoogle Scholar
  69. Martinelli E, Cicala C, Van Ryk D et al (2007) HIV-1 gp120 inhibits TLR9-mediated activation and IFN-γ secretion in plasmacytoid dendritic cells. Proc Natl Acad Sci U S A 104:3396–3401PubMedPubMedCentralCrossRefGoogle Scholar
  70. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92:1177–1186PubMedCrossRefGoogle Scholar
  71. 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 16:422–430PubMedCrossRefGoogle Scholar
  72. Meyer S, Van Liempt E, Imberty A et al (2005) DC-SIGN mediates binding of dendritic cells to authentic pseudo-LewisY glycolipids of Schistosoma mansoni cercariae, the first parasite-specific ligand of DC-SIGN. J Biol Chem 280:37349–37359PubMedCrossRefGoogle Scholar
  73. Miszczyk E, Rudnicka K, Moran AP et al (2012) Interaction of Helicobacter pylori with C-type lectin dendritic cellspecific ICAM grabbing nonintegrin. J Biomed Biotechnol 2012, Article ID 206463, 10 ppGoogle Scholar
  74. 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 276:28939–28945PubMedCrossRefGoogle Scholar
  75. Miyake Y, Toyonaga K, Mori D et al (2013) C-type lectin MCL is an FcRγ-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38:1050–1062PubMedCrossRefGoogle Scholar
  76. Moriwaki H, Kume N, Sawamura T et al (1998) Ligand specificity of LOX-1, a novel endothelial receptor for oxidized low density lipoprotein. Arterioscler Thromb Vasc Biol 18:1541–1547PubMedCrossRefGoogle Scholar
  77. Mortezai N, Behnken HN, Kurze AK et al (2013) Tumor-associated Neu5Ac-Tn and Neu5Gc-Tn antigens bind to C-type lectin CLEC10A (CD301, MGL). Glycobiology 23:844–852PubMedCrossRefGoogle Scholar
  78. Mullin NP, Hall KT, Taylor ME (1994) Characterization of ligand binding to a carbohydrate-recognition domain of the macrophage mannose receptor. J Biol Chem 269:28405–28413PubMedGoogle Scholar
  79. Muñoz-García JC, Chabrol E, Vivès RR et al (2015) Langerin-heparin interaction: two binding sites for small and large ligands as revealed by a combination of NMR spectroscopy and cross-linking mapping experiments. J Am Chem Soc 137:4100–4110PubMedCrossRefGoogle Scholar
  80. Murshid A, Theriault J, Gong J et al (2011) Investigating receptors for extracellular heat shock proteins. Methods Mol Biol 787:289–302PubMedPubMedCentralCrossRefGoogle Scholar
  81. Nagae M, Yamanaka K, Hanashima S et al (2013) Recognition of bisecting N-acetylglucosamine: structural basis for asymmetric interaction with the mouse lectin dendritic cell inhibitory receptor 2. J Biol Chem 288:33598–33610PubMedPubMedCentralCrossRefGoogle Scholar
  82. Neumann K, Castiñeiras-Vilariño M, Höckendorf U et al (2014) CLEC12a is an inhibitory receptor for uric acid crystals that regulates inflammation in response to cell death. Immunology 40:389–399Google Scholar
  83. Ng WC, Liong S, Tate MD et al (2014) The macrophage galactose-type lectin can function as an attachment and entry receptor for influenza virus. J Virol 88:1659–1672PubMedPubMedCentralCrossRefGoogle Scholar
  84. Oka K, Sawamura T, Kikuta KI et al (1998) Lectin-like oxidized low-density lipoprotein receptor 1 mediates phagocytosis of aged/apoptotic cells in endothelial cells. Proc Natl Acad Sci U S A 95:9535–9540PubMedPubMedCentralCrossRefGoogle Scholar
  85. Okamura T, Sekikawa A, Sawamura T et al (2013) LOX-1 ligands containing apolipoprotein B and carotid intima-media thickness in middle-aged community-dwelling US Caucasian and Japanese men. Atherosclerosis 229:240–245PubMedPubMedCentralCrossRefGoogle Scholar
  86. Palma AS, Feizi T, Zhang Y et al (2006) Ligands for the β-glucan receptor, Dectin-1, assigned using “designer” microarrays of oligosaccharide probes (neoglycolipids) generated from glucan polysaccharides. J Biol Chem 281:5771–5779PubMedCrossRefGoogle Scholar
  87. Picco G, Beatson R, Taylor-Papadimitriou J et al (2014) Targeting DNGR-1 (CLEC9A) with antibody/MUC1 peptide conjugates as a vaccine for carcinomas. Eur J Immunol 44:1947–1955PubMedPubMedCentralCrossRefGoogle Scholar
  88. Plato A, Willment JA, Brown GD (2013) C-Type lectin-like receptors of the Dectin-1 cluster: ligands and signalling pathways. Int Rev Immunol 32:134–156PubMedPubMedCentralCrossRefGoogle Scholar
  89. 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 281:20440–20449PubMedCrossRefGoogle Scholar
  90. Pyż E, Huysamen C, Marshall ASJ et al (2008) Characterisation of murine MICL (CLEC12A) and evidence for an endogenous ligand. Eur J Immunol 38:1157–1163PubMedPubMedCentralCrossRefGoogle Scholar
  91. Rappleye CA, Groppe Eissenberg L, Goldman WE (2007) Histoplasma capsulatum α-(1,3)-glucan blocks innate immune recognition by the β-glucan receptor. Proc Natl Acad Sci 104:1366–1370PubMedPubMedCentralCrossRefGoogle Scholar
  92. Riboldi E, Daniele R, Parola C et al (2011) Human C-type lectin domain family 4, member C (CLEC4C/BDCA-2/CD303) is a receptor for asialo-galactosyl-oligosaccharides. J Biol Chem 286:35329–35333PubMedPubMedCentralCrossRefGoogle Scholar
  93. 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 U S A 107:20459–20464PubMedPubMedCentralCrossRefGoogle Scholar
  94. Rothfuchs AG, Bafica A, Feng CG et al (2007) Dectin-1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J Immunol 179:3463–3471PubMedCrossRefGoogle Scholar
  95. Saba K, Denda-Nagai K, Irimura T (2009) A C-type lectin MGL1/CD301a plays an anti-inflammatory role in murine experimental colitis. Am J Pathol 174:144–152PubMedPubMedCentralCrossRefGoogle Scholar
  96. Sabatte J, Faigle W, Ceballos A et al (2011) Semen clusterin is a novel DC-SIGN ligand. J Immunol 187:5299–5309PubMedCrossRefGoogle Scholar
  97. Saijo S, Ikeda S, Yamebe K et al (2010) Dectin-2 recognition of α-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32:681–691PubMedCrossRefGoogle Scholar
  98. Sancho D, Reis e Sousa C (2012) Signalling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 30:491–529PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sato K, Yang XI, 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 281:38854–38866PubMedCrossRefGoogle Scholar
  100. Sawamura T, Kume N, Aoyama T et al (1997) An endothelial receptor for oxidized low-density lipoprotein. Nature 386:73–77PubMedCrossRefGoogle Scholar
  101. Scarpellino L, Oeschger F, Guillaume P (2007) Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J Immunol 178:1277–1284PubMedCrossRefGoogle Scholar
  102. Schoenen H, Bodendorfer B, Hitchens K et al (2010) Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 184:2756–2760PubMedPubMedCentralCrossRefGoogle Scholar
  103. Shepherd VL, Lee YC, Schlesinger PH et al (1981) L-Fucose-terminated glycoconjugates are recognized by pinocytosis receptors on macrophages. Proc Nat Acad Sci 78:1019–1022PubMedPubMedCentralCrossRefGoogle Scholar
  104. Shi X, Niimi S, Ohtani T et al (2001) Characterization of residues and sequences of the carbohydrate recognition domain required for cell surface localization and ligand binding of human lectin-like oxidized LDL receptor. J Cell Sci 114:1273–1282PubMedGoogle Scholar
  105. Shih HH, Zhang S, Cao W et al (2009) CRP is a novel ligand for the oxidized LDL receptor LOX-1. Am J Physiol Heart Circ Physiol 296:H1643–H1650PubMedCrossRefGoogle Scholar
  106. Shimaoka T, Kume N, Minami M et al (2001) LOX-1 supports adhesion of Gram-positive and Gram-negative bacteria. J Immunol 166:5108–5114PubMedCrossRefGoogle Scholar
  107. Shrimpton RE, Butler M, Morel AS et al (2009) CD205 (DEC-205): a recognition receptor for apoptotic and necrotic self. Mol Immunol 46:1229–1239PubMedPubMedCentralCrossRefGoogle Scholar
  108. Singh SK, Streng-Ouwehand I, Litjens M et al (2009) Characterization of murine MGL1 and MGL2 C-type lectins: distinct glycan specificities and tumor binding properties. Mol Immunol 46:1240–1249PubMedCrossRefGoogle Scholar
  109. Singh SK, Streng-Ouwehand I, Litjens M et al (2011) Tumour-associated glycan modifications of antigen enhance MGL2 dependent uptake and MHC class I restricted CD8 T cell responses. Int J Cancer 128:1371–1383PubMedCrossRefGoogle Scholar
  110. Srivastava L, Tundup S, Choi BS et al (2014) Immunomodulatory glycan lacto-N-fucopentaose III requires clathrin-mediated endocytosis to induce alternative activation of antigen-presenting cells. Infect Immun 82:1891–1903PubMedPubMedCentralCrossRefGoogle Scholar
  111. Stahl P, Schlesinger PH, Rodman JS et al (1976) Recognition of lysosomal glycosidases in vivo inhibited by modified glycoproteins. Nature 264:86–88PubMedCrossRefGoogle Scholar
  112. Stambach NS, Taylor ME (2003) Characterization of carbohydrate recognition by langerin, a C-type lectin of Langerhans cells. Glycobiology 13:401–410PubMedCrossRefGoogle Scholar
  113. Stocker BL, Khan AA, Chee SH et al (2014) On one leg: trehalose monoesters activate macrophages in a Mincle-dependent manner. ChemBioChem 15:382–388PubMedCrossRefGoogle Scholar
  114. Suzuki N, Yamamoto K, Toyoshima S et al (1996) Molecular cloning and expression of cDNA encoding human macrophage C-type lectin. Its unique carbohydrate binding specificity for Tn antigen. J Immunol 156:128–135PubMedGoogle Scholar
  115. Suzuki-Inoue K, Kato Y, Inoue O et al (2007) Involvement of the snake toxin receptor CLEC-2, in podoplanin-mediated platelet activation, by cancer cells. J Biol Chem 282:25993–26001PubMedCrossRefGoogle Scholar
  116. Suzuki-Inoue K, Inoue O, Ozaki Y (2011) Novel platelet activation receptor CLEC-2: from discovery to prospects. J Thromb Haemost 9(Suppl 1):44–55PubMedCrossRefGoogle Scholar
  117. Tai LH, Goulet ML, Belanger S et al (2007) Recognition of H-2Kb by Ly49Q suggests a role for class Ia MHC regulation of plasmacytoid dendritic cell function. Mol Immunol 44:2638–2646PubMedCrossRefGoogle Scholar
  118. Takahara K, Yashima Y, Omatsu Y et al (2004) Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and Langerin, C-type lectins. Int Immunol 16:819–829PubMedCrossRefGoogle Scholar
  119. Tanne A, Ma B, Boudou F et al (2009) A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. J Exp Med 206:2205–2220PubMedPubMedCentralCrossRefGoogle Scholar
  120. 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 285:6390–6400PubMedPubMedCentralCrossRefGoogle Scholar
  121. Taylor ME, Bezouska K, Drickamer K (1992) Contribution to ligand binding by multiple carbohydrate-recognition domains in the macrophage mannose receptor. J Biol Chem 267:1719–1726PubMedGoogle Scholar
  122. Terrazas CA, Alcántara-Hernández M, Bonifaz L et al (2013) Helminth-excreted/secreted products are recognized by multiple receptors on DCs to block the TLR response and bias Th2 polarization in a cRAF dependent pathway. FASEB J 27:4547–4560PubMedPubMedCentralCrossRefGoogle Scholar
  123. Thiagarajan PS, Yakubenko VP, Elsori DH et al (2013) Vimentin is an endogenous ligand for the pattern recognition receptor Dectin-1. Cardiovasc Res 99:494–504PubMedPubMedCentralCrossRefGoogle Scholar
  124. Tsuiji M, Fujimori M, Ohashi Y et al (2002) Molecular cloning and characterization of a novel mouse macrophage C-type lectin, mMGL2, which has a distinct carbohydrate specificity from mMGL1. J Biol Chem 277:28892–28901PubMedCrossRefGoogle Scholar
  125. Upham JP, Pickett D, Irimura T et al (2010) Macrophage receptors for influenza A virus: role of the macrophage galactose-type lectin and mannose receptor in viral entry. J Virol 84:3730–3737PubMedPubMedCentralCrossRefGoogle Scholar
  126. Van der Peet PL, Gunawan C, Torigoe S et al (2015) Corynomycolic acid-containing glycolipids signal through the pattern recognition receptor Mincle. Chem Commun 51:5100–5103CrossRefGoogle Scholar
  127. Van Die I, Van Vliet SJ, Nyame AK et al (2003) The dendritic cell-specific C-type lectin DC-SIGN is a receptor for Schistosoma mansoni egg antigens and recognizes the glycan antigen Lewis x. Glycobiology 13:471–478PubMedCrossRefGoogle Scholar
  128. Van Kooyk Y, Ilarregui JM, Van Vliet SJ (2015) Novel insights into the immunomodulatory role of the dendritic cell and macrophage-expressed C-type lectin MGL. Immunobiology 220:185–192PubMedCrossRefGoogle Scholar
  129. Van Vliet SJ, Van Liempt E, Saeland E et al (2005) Carbohydrate profiling reveals a distinctive role for the C-type lectin MGL in the recognition of helminth parasites and tumor antigens by dendritic cells. Int Immunol 17:661–669PubMedCrossRefGoogle Scholar
  130. Vázquez A, Ruiz-Rosado Jde D, Terrazas LI et al (2014) Mouse macrophage galactose-type lectin (mMGL) is critical for host resistance against Trypanosoma cruzi infection. Int J Biol Sci 10:909–920PubMedPubMedCentralCrossRefGoogle Scholar
  131. 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 180:7404–7413PubMedCrossRefGoogle Scholar
  132. Yadav M, Schorey JS (2006) The β-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108:3168–3175PubMedPubMedCentralCrossRefGoogle Scholar
  133. Yamasaki S, Ishikawa E, Sakuma M et al (2008) Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 9:1179–1188PubMedCrossRefGoogle Scholar
  134. Yamasaki S, Matsumoto M, Takeuchi O et al (2009) C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci U S A 106:1897–1902PubMedPubMedCentralCrossRefGoogle Scholar
  135. Yang K, Park CG, Cheong C et al (2015) Host Langerin (CD207) is a receptor for Yersinia pestis phagocytosis and promotes dissemination. Immunol Cell Biol 93:815–24PubMedPubMedCentralCrossRefGoogle Scholar
  136. Yonekawa A, Saijo S, Hoshino Y et al (2014) Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of Mycobacteria. Immunity 41:402–413PubMedCrossRefGoogle Scholar
  137. Yoshimoto R, Fujita Y, Kakino A et al (2011) The discovery of LOX-1, its ligands and clinical significance. Cardiovasc Drugs Ther 25:379–391PubMedPubMedCentralCrossRefGoogle Scholar
  138. Zhang SS, Park C, Zhang P et al (2008) Plasminogen activator Pla of Yersinia pestis utilizes murine DEC-205 (CD205) as a receptor to promote dissemination. J Biol Chem 283:31511–31521PubMedPubMedCentralCrossRefGoogle Scholar
  139. Zhang JG, Czabotar PE, Policheni AN et al (2012) The dendritic cell receptor CLEC9A binds damaged cells via exposed actin filaments. Immunity 36:646–657PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Amy J. Foster
    • 1
  • Jessie H. Bird
    • 1
  • Mattie S. M. Timmer
    • 1
  • Bridget L. Stocker
    • 1
    Email author
  1. 1.School of Chemical and Physical SciencesVictoria University of WellingtonWellingtonNew Zealand

Personalised recommendations