C-type lectins in immunity: Recent developments

Current Opinion in Immunology

Volumn 32, Issue , 2015, Pages 21-27

  Dambuza, Ivy M ^a   Brown, Gordon D ^a  

^a UNIVERSITY OF ABERDEEN   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

C TYPE LECTIN RECEPTOR; DECTIN 1; DECTIN 2; LECTIN RECEPTOR; UNCLASSIFIED DRUG; LECTIN;

ALLERGY; ANTIGEN RECOGNITION; AUTOIMMUNITY; CANCER CELL; CELL DEATH; HOMEOSTASIS; HOST RESISTANCE; HUMAN; INTRACELLULAR SIGNALING; MYCOBACTERIOSIS; MYCOSIS; NONHUMAN; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; ANIMAL; CHEMISTRY; FUNGUS; HYPERSENSITIVITY; IMMUNITY; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; MYCOBACTERIUM; NEOPLASM; SIGNAL TRANSDUCTION;

ANIMALS; AUTOIMMUNITY; FUNGI; HOMEOSTASIS; HUMANS; HYPERSENSITIVITY; IMMUNITY; IMMUNOMODULATION; LECTINS, C-TYPE; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; MYCOSES; NEOPLASMS; RECEPTORS, MITOGEN; SIGNAL TRANSDUCTION;

EID: 84920896754     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.12.002     Document Type: Review

References (73)

1. Drickamer K., Fadden A.J. Genomic analysis of C-type lectins. Biochem Soc Symp 2002, 59-72.
2. Zelensky A.N., Gready J.E. The C-type lectin-like domain superfamily. FEBS J 2005, 272:6179-6217.
3. Kerrigan A.M., Brown G.D. Syk-coupled C-type lectins in immunity. Trends Immunol 2011, 32:151-156.
4. Sancho D., Reis e Sousa C. Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 2012, 30:491-529.
5. Redelinghuys P., Brown G.D. Inhibitory C-type lectin receptors in myeloid cells. Immunol Lett 2011, 136:1-12.
6. Plato A., Willment J.A., Brown G.D. C-type lectin-like receptors of the dectin-1 cluster: ligands and signaling pathways. Int Rev Immunol 2013, 32:134-156.
7. Kerscher B., Willment J.A., Brown G.D. The Dectin-2 family of C-type lectin-like receptors: an update. Int Immunol 2013, 25:271-277.
8. Hardison S.E., Brown G.D. C-type lectin receptors orchestrate antifungal immunity. Nat Immunol 2012, 13:817-822.
9. Wüthrich M., Deepe G.S., Klein B. Adaptive immunity to fungi. Annu Rev Immunol 2012, 30:115.
10. Hernández-Santos N., Gaffen Sarah L. Th17 cells in immunity to Candida albicans. Cell Host Microbe 2012, 11:425-435.
11. Puel A., Cypowyj S., Bustamante J., Wright J.F., Liu L., Lim H.K., Migaud M., Israel L., Chrabieh M., Audry M. Chronic mucocutaneous candidiasis in humans with inborn errors of interleukin-17 immunity. Science 2011, 332:65-68.
12. Ferwerda B., Ferwerda G., Plantinga T.S., Willment J.A., van Spriel A.B., Venselaar H., Elbers C.C., Johnson M.D., Cambi A., Huysamen C., et al. Human dectin-1 deficiency and mucocutaneous fungal infections. N Engl J Med 2009, 361:1760-1767.
13. Glocker E-O., Hennigs A., Nabavi M., Schäffer A.A., Woellner C., Salzer U., Pfeifer D., Veelken H., Warnatz K., Tahami F. A homozygous CARD9 mutation in a family with susceptibility to fungal infections. N Engl J Med 2009, 361:1727-1735.
14. Brown G.D., Gordon S. Immune recognition: a new receptor for [beta]-glucans. Nature 2001, 413:36-37.
15. Goodridge H.S., Reyes C.N., Becker C.A., Katsumoto T.R., Ma J., Wolf A.J., Bose N., Chan A.S., Magee A.S., Danielson M.E. Activation of the innate immune receptor Dectin-1 upon formation of a 'phagocytic synapse'. Nature 2011, 472:471-475.
16. Drummond R.A., Brown G.D. Signalling C-type lectins in antimicrobial immunity. PLoS Pathog 2013, 9:e1003417.
17. Goodridge H.S., Shimada T., Wolf A.J., Hsu Y-M.S., Becker C.A., Lin X., Underhill D.M. Differential use of CARD9 by dectin-1 in macrophages and dendritic cells. J Immunol 2009, 182:1146-1154.
18. Strasser D., Neumann K., Bergmann H., Marakalala Mohlopheni J., Guler R., Rojowska A., Hopfner K-P., Brombacher F., Urlaub H., Baier G., et al. Syk kinase-coupled C-type lectin receptors engage protein kinase C-δ to elicit Card9 adaptor-mediated innate immunity. Immunity 2009, 36:32-42.
19. Wevers Brigitte A., Kaptein Tanja M., Zijlstra-Willems Esther M., Theelen B., Boekhout T., Geijtenbeek Teunis B.H., Gringhuis Sonja I. Fungal engagement of the C-type lectin mincle suppresses dectin-1-induced antifungal immunity. Cell Host Microbe 2014, 15:494-505.
20. Jia X-M., Tang B., Zhu L-L., Liu Y-H., Zhao X-Q., Gorjestani S., Hsu Y-M.S., Yang L., Guan J-H., Xu G-T., et al. CARD9 mediates Dectin-1-induced ERK activation by linking Ras-GRF1 to H-Ras for antifungal immunity. J Exp Med 2014, 211:2307-2321.
21. Ma J., Becker C., Reyes C., Underhill D.M. Cutting edge: FYCO1 recruitment to dectin-1 phagosomes is accelerated by light chain 3 protein and regulates phagosome maturation and reactive oxygen production. J Immunol 2014, 192:1356-1360.
22. Gringhuis S.I., Kaptein T.M., Wevers B.A., Theelen B., van der Vlist M., Boekhout T., Geijtenbeek T.B.H. Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1[beta] via a noncanonical caspase-8 inflammasome. Nat Immunol 2012, 13:246-254.
23. Hise A.G., Tomalka J., Ganesan S., Patel K., Hall B.A., Brown G.D., Fitzgerald K.A. An essential role for the NLRP3 inflammasome in host defense against the human fungal pathogen Candida albicans. Cell Host Microbe 2009, 5:487-497.
24. del Fresno C., Soulat D., Roth S., Blazek K., Udalova I., Sancho D., Ruland J., Ardavín C. Interferon-β production via dectin-1-Syk-IRF5 signaling in dendritic cells is crucial for immunity to C. albicans. Immunity 2013, 38:1176-1186.
25. Bourgeois C., Majer O., Frohner I.E., Lesiak-Markowicz I., Hildering K-S., Glaser W., Stockinger S., Decker T., Akira S., Müller M. Conventional dendritic cells mount a type I IFN response against Candida spp. requiring novel phagosomal TLR7-mediated IFN-β signaling. J Immunol 2011, 186:3104-3112.
26. Smeekens S.P., Ng A., Kumar V., Johnson M.D., Plantinga T.S., van Diemen C., Arts P., Verwiel E.T.P., Gresnigt M.S., Fransen K., et al. Functional genomics identifies type I interferon pathway as central for host defense against Candida albicans. Nat Commun 2013, 4:1342.
27. Quintin J., Saeed S., Martens J.H., Giamarellos-Bourboulis E.J., Ifrim D.C., Logie C., Jacobs L., Jansen T., Kullberg B.J., Wijmenga C., et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 2012, 12:223-232.
28. Saeed S., Quintin J., Kerstens H.H., Rao N.A., Aghajanirefah A., Matarese F., Cheng S-C., Ratter J., Berentsen K., van der Ent M.A. Epigenetic programming of monocyte-to-macrophage differentiation and trained innate immunity. Science 2014, 345. 1251086.
29. Ifrim D.C., Bain J.M., Reid D.M., Oosting M., Verschueren I., Gow N.A., van Krieken J.H., Brown G.D., Kullberg B-J., Joosten L.A. Role of dectin-2 for host defense against systemic infection with Candida glabrata. Infect Immun 2014, 82:1064-1073.
30. Ishikawa T., Itoh F., Yoshida S., Saijo S., Matsuzawa T., Gonoi T., Saito T., Okawa Y., Shibata N., Miyamoto T., et al. Identification of distinct ligands for the C-type lectin receptors Mincle and Dectin-2 in the pathogenic fungus Malassezia. Cell Host Microbe 2013, 13:477-488.
31. Zhu L-L., Zhao X-Q., Jiang C., You Y., Chen X-P., Jiang Y-Y., Jia X-M., Lin X. C-type lectin receptors dectin-3 and dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity 2013, 39:324-334.
32. Taylor P.R., Roy S., Leal S.M., Sun Y., Howell S.J., Cobb B.A., Li X., Pearlman E. 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 2014, 15:143-151.
33. Marakalala M.J., Graham L.M., Brown G.D. The role of Syk/CARD9-coupled C-type lectin receptors in immunity to Mycobacterium tuberculosis infections. Clin Dev Immunol 2011, 2010:567571.
34. Miyake Y., Toyonaga K., Mori D., Kakuta S., Hoshino Y., Oyamada A., Yamada H., Ono K-i., Suyama M., Iwakura Y., et al. C-type lectin MCL is an FcRγ-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 2013, 38:1050-1062.
35. Yonekawa A., Saijo S., Hoshino Y., Miyake Y., Ishikawa E., Suzukawa M., Inoue H., Tanaka M., Yoneyama M., Oh-hora M. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 2014, 41:402-413.
36. Shenderov K., Barber D.L., Mayer-Barber K.D., Gurcha S.S., Jankovic D., Feng C.G., Oland S., Hieny S., Caspar P., Yamasaki S. Cord factor and peptidoglycan recapitulate the Th17-promoting adjuvant activity of mycobacteria through mincle/CARD9 signaling and the inflammasome. J Immunol 2013, 190:5722-5730.
37. Lobato-Pascual A., Saether P.C., Fossum S., Dissen E., Daws M.R. Mincle, the receptor for mycobacterial cord factor, forms a functional receptor complex with MCL and FcεRI-γ. Eur J Immunol 2013, 43:3167-3174.
38. Heitmann L., Schoenen H., Ehlers S., Lang R., Hölscher C. Mincle is not essential for controlling Mycobacterium tuberculosis infection. Immunobiology 2013, 218:506-516.
39. Behler F., Steinwede K., Balboa L., Ueberberg B., Maus R., Kirchhof G., Yamasaki S., Welte T., Maus U.A. Role of Mincle in alveolar macrophage-dependent innate immunity against mycobacterial infections in mice. J Immunol 2012, 189:3121-3129.
40. Lee W-B., Kang J-S., Yan J-J., Lee M.S., Jeon B-Y., Cho S-N., Kim Y-J. Neutrophils promote mycobacterial trehalose dimycolate-induced lung inflammation via the Mincle pathway. PLoS Pathog 2012, 8:e1002614.
41. Dorhoi A., Desel C., Yeremeev V., Pradl L., Brinkmann V., Mollenkopf H-J., Hanke K., Gross O., Ruland J., Kaufmann S.H. The adaptor molecule CARD9 is essential for tuberculosis control. J Exp Med 2010, 207:777-792.
42. Karumuthil-Melethil S., Gudi R., Johnson B.M., Perez N., Vasu C. Fungal β-glucan, a dectin-1 ligand, promotes protection from type 1 diabetes by inducing regulatory innate immune response. J Immunol 2014, 193:3308-3321.
43. Yoshitomi H., Sakaguchi N., Kobayashi K., Brown G.D., Tagami T., Sakihama T., Hirota K., Tanaka S., Nomura T., Miki I. A role for fungal β-glucans and their receptor Dectin-1 in the induction of autoimmune arthritis in genetically susceptible mice. J Exp Med 2005, 201:949-960.
44. Karsten C.M., Pandey M.K., Figge J., Kilchenstein R., Taylor P.R., Rosas M., McDonald J.U., Orr S.J., Berger M., Petzold D., et al. Anti-inflammatory activity of IgG1 mediated by Fc galactosylation and association of Fc[gamma]RIIB and dectin-1. Nat Med 2012, 18:1401-1406.
45. Acton S.E., Astarita J.L., Malhotra D., Lukacs-Kornek V., Franz B., Hess P.R., Jakus Z., Kuligowski M., Fletcher A.L., Elpek K.G. Podoplanin-rich stromal networks induce dendritic cell motility via activation of the C-type lectin receptor CLEC-2. Immunity 2012, 37:276-289.
46. Bénézech C., Nayar S., Finney B.A., Withers D.R., Lowe K., Desanti G.E., Marriott C.L., Watson S.P., Caamaño J.H., Buckley C.D. CLEC-2 is required for development and maintenance of lymph nodes. Blood 2014, 123:3200-3207.
47. Bertozzi C.C., Schmaier A.A., Mericko P., Hess P.R., Zou Z., Chen M., Chen C.Y., Xu B., Lu M.M., Zhou D. Platelets regulate lymphatic vascular development through CLEC-2-SLP-76 signaling. Blood 2010, 116:661-670.
48. Herzog B.H., Fu J., Wilson S.J., Hess P.R., Sen A., McDaniel J.M., Pan Y., Sheng M., Yago T., Silasi-Mansat R. Podoplanin maintains high endothelial venule integrity by interacting with platelet CLEC-2. Nature 2013, 502:105-109.
49. Rochereau N., Drocourt D., Perouzel E., Pavot V., Redelinghuys P., Brown G.D., Tiraby G., Roblin X., Verrier B., Genin C. Dectin-1 is essential for reverse transcytosis of glycosylated SIgA-antigen complexes by intestinal M cells. PLoS Biol 2013, 11:e1001658.
50. Shan M., Gentile M., Yeiser J.R., Walland A.C., Bornstein V.U., Chen K., He B., Cassis L., Bigas A., Cols M. Mucus enhances gut homeostasis and oral tolerance by delivering immunoregulatory signals. Science 2013, 342:447-453.
51. Iliev I.D., Funari V.A., Taylor K.D., Nguyen Q., Reyes C.N., Strom S.P., Brown J., Becker C.A., Fleshner P.R., Dubinsky M. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis. Science 2012, 336:1314-1317.
52. Lilly L.M., Gessner M.A., Dunaway C.W., Metz A.E., Schwiebert L., Weaver C.T., Brown G.D., Steele C. The β-glucan receptor dectin-1 promotes lung immunopathology during fungal allergy via IL-22. J Immunol 2012, 189:3653-3660.
53. Barrett N.A., Maekawa A., Rahman O.M., Austen K.F., Kanaoka Y. Dectin-2 recognition of house dust mite triggers cysteinyl leukotriene generation by dendritic cells. J Immunol 2009, 182:1119-1128.
54. Barrett N.A., Rahman O.M., Fernandez J.M., Parsons M.W., Xing W., Austen K.F., Kanaoka Y. Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes. J Exp Med 2011, 208:593-604.
55. Clarke D.L., Davis N.H.E., Campion C.L., Foster M.L., Heasman S.C., Lewis A.R., Anderson I.K., Corkill D.J., Sleeman M.A., May R.D., et al. Dectin-2 sensing of house dust mite is critical for the initiation of airway inflammation. Mucosal Immunol 2014, 7:558-567.
56. Tjota M.Y., Hrusch C.L., Blaine K.M., Williams J.W., Barrett N.A., Sperling A.I. Signaling through FcRγ-associated receptors on dendritic cells drives IL-33-dependent TH2-type responses. J Allergy Clin Immunol 2014, 134. 706-713.e708.
57. Parsons M.W., Li L., Wallace A.M., Lee M.J., Katz H.R., Fernandez J.M., Saijo S., Iwakura Y., Austen K.F., Kanaoka Y., et al. Dectin-2 regulates the effector phase of house dust mite-elicited pulmonary inflammation independently from its role in sensitization. J Immunol 2014, 192:1361-1371.
58. Norimoto A., Hirose K., Iwata A., Tamachi T., Yokota M., Takahashi K., Saijo S., Iwakura Y., Nakajima H. 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 2014, 51:201-209.
59. Sancho D., Reis e Sousa C. Sensing of cell death by myeloid C-type lectin receptors. Curr Opin Immunol 2013, 25:46-52.
60. Yamasaki S., Ishikawa E., Sakuma M., Hara H., Ogata K., Saito T. Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 2008, 9:1179-1188.
61. Suzuki Y., Nakano Y., Mishiro K., Takagi T., Tsuruma K., Nakamura M., Yoshimura S., Shimazawa M., Hara H. Involvement of Mincle and Syk in the changes to innate immunity after ischemic stroke. Sci Rep 2013, 3:3177.
62. de Rivero Vaccari J.C., Frank Brand I., Berti A.F., Alonso O.F., Bullock R., De Rivero Vaccari J.P. Mincle signaling in the innate immune response after traumatic brain injury. J Neurotrauma 2014, 10.1089/nue.2014.3436.
63. Schraml B.U., van Blijswijk J., Zelenay S., Whitney P.G., Filby A., Acton S.E., Rogers N.C., Moncaut N., Carvajal J.J., Reis e Sousa C. Genetic tracing via DNGR-1 expression history defines dendritic cells as a hematopoietic lineage. Cell 2013, 154:843-858.
64. Ahrens S., Zelenay S., Sancho D., Hanč P., Kjaer S., Feest C., Fletcher G., Durkin C., Postigo A., Skehel M., et al. F-actin is an evolutionarily conserved damage-associated molecular pattern recognized by DNGR-1, a receptor for dead cells. Immunity 2012, 36:635-645.
65. Zhang J-G., Czabotar Peter E., Policheni Antonia N., Caminschi I., San Wan S., Kitsoulis S., Tullett Kirsteen M., Robin Adeline Y., Brammananth R., van Delft Mark F., et al. The dendritic cell receptor Clec9A binds damaged cells via exposed actin filaments. Immunity 2012, 36:646-657.
66. Sancho D., Joffre O.P., Keller A.M., Rogers N.C., Martinez D., Hernanz-Falcon P., Rosewell I., Reis e Sousa C. Identification of a dendritic cell receptor that couples sensing of necrosis to immunity. Nature 2009, 458:899-903.
67. Iborra S., Izquierdo H.M., Martínez-López M., Blanco-Menéndez N., Reis e Sousa C., Sancho D. The DC receptor DNGR-1 mediates cross-priming of CTLs during vaccinia virus infection in mice. J Clin Invest 2012, 122:1628-1643.
68. Zelenay S., Keller A.M., Whitney P.G., Schraml B.U., Deddouche S., Rogers N.C., Schulz O., Sancho D., Reis e Sousa C. The dendritic cell receptor DNGR-1 controls endocytic handling of necrotic cell antigens to favor cross-priming of CTLs in virus-infected mice. J Clin Invest 2012, 122:1615-1627.
69. Neumann K., Castiñeiras-Vilariño M., Höckendorf U., Hannesschläger N., Lemeer S., Kupka D., Meyermann S., Lech M., Anders H-J., Kuster B., et al. Clec12a is an inhibitory receptor for uric acid crystals that regulates inflammation in response to cell death. Immunity 2014, 40:389-399.
70. Roug A.S., Larsen H.Ø., Nederby L., Just T., Brown G., Nyvold C.G., Ommen H.B., Hokland P. hMICL and CD123 in combination with a CD45/CD34/CD117 backbone-a universal marker combination for the detection of minimal residual disease in acute myeloid leukaemia. Br J Haematol 2014, 164:212-222.
71. Chiba S., Ikushima H., Ueki H., Yanai H., Kimura Y., Hangai S., Nishio J., Negishi H., Tamura T., Saijo S. Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses. eLife 2014, 10.755/eLife.04177.
72. Brown G.D., Gordon S. Fungal β-glucans and mammalian immunity. Immunity 2003, 19:311-315.
73. Sattler S., Ghadially H., Hofer E. Evolution of the C-type lectin-like receptor genes of the DECTIN-1 cluster in the NK gene complex. Sci World J 2012, 2012:931386.