C-type lectin receptors in tuberculosis: what we know

Medical Microbiology and Immunology

Volumn 205, Issue 6, 2016, Pages 513-535

  Goyal, Surabhi ^a   Klassert, Tilman E ^b   Slevogt, Hortense ^b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

C type lectin receptors; Cell signaling pathways; PRRs; Single nucleotide polymorphisms; Tuberculosis

Indexed keywords

C TYPE LECTIN RECEPTOR; CALCIUM ION; CD209 ANTIGEN; COLLECTIN; COMPLEMENT RECEPTOR; COMPLEMENT RECEPTOR 3; DECTIN 1; DECTIN 2; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; KILLER CELL ACTIVATING RECEPTOR ASSOCIATED PROTEIN; LECTIN RECEPTOR; MACROPHAGE C TYPE LECTIN; MACROPHAGE C TYPE LECTIN PROTEIN; MACROPHAGE INDUCIBLE C TYPE LECTIN; MANNOSE BINDING LECTIN; MANNOSE RECEPTOR; PROTEIN BCL 10; PROTEIN KINASE C DELTA; PROTEIN KINASE SYK; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEIN TYROSINE PHOSPHATASE SHP 2; PROTEOGLYCAN; RAF PROTEIN; SELECTIN; SURFACTANT PROTEIN A; SURFACTANT PROTEIN D; UNCLASSIFIED DRUG; UNINDEXED DRUG; CELL SURFACE RECEPTOR; CYTOKINE; LECTIN; LIGAND; PROTEIN BINDING;

ALLELE; AMINO ACID SEQUENCE; BINDING AFFINITY; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC ASSOCIATION; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; LUNG ALVEOLUS CELL TYPE 2; MOLECULAR RECOGNITION; NONHUMAN; OUTCOME ASSESSMENT; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SINGLE NUCLEOTIDE POLYMORPHISM; TUBERCULOSIS; ANIMAL; BLOOD; CHEMISTRY; GENETICS; IMMUNOLOGY; IMMUNOMODULATION; METABOLISM; MYCOBACTERIUM TUBERCULOSIS;

ANIMALS; COLLECTINS; CYTOKINES; DISEASE SUSCEPTIBILITY; HUMANS; IMMUNOMODULATION; LECTINS, C-TYPE; LIGANDS; MANNOSE-BINDING LECTIN; MYCOBACTERIUM TUBERCULOSIS; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; TUBERCULOSIS;

EID: 84980017904     PISSN: 03008584     EISSN: 14321831     Source Type: Journal    
DOI: 10.1007/s00430-016-0470-1     Document Type: Review

References (262)

1. World Health Organisation (2015) Global tuberculosis report 2015. http://www.who.int/tb/publications/global_report/en/
2. Zumla A, Raviglione M, Hafner R, von Reyn CF (2013) Tuberculosis. New Engl J Med 368(8):745–755. doi:10.1056/NEJMra1200894
3. van Crevel R, Ottenhoff THM, van der Meer JWM (2002) Innate immunity to Mycobacterium tuberculosis. Clin Microbiol Rev 15(2):294–309. doi:10.1128/cmr.15.2.294-309.2002
4. Pieters J (2008) Mycobacterium tuberculosis and the macrophage: maintaining a balance. Cell Host Microbe 3(6):399–407. doi:10.1016/j.chom.2008.05.006
5. Ehrt S, Schnappinger D (2009) Mycobacterial survival strategies in the phagosome: defence against host stresses. Cell Microbiol 11(8):1170–1178. doi:10.1111/j.1462-5822.2009.01335.x
6. Orme IM, Robinson RT, Cooper AM (2015) The balance between protective and pathogenic immune responses in the TB-infected lung. Nat Immunol 16(1):57–63. doi:10.1038/ni.3048
7. Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63. doi:10.1146/annurev.bi.64.070195.000333
8. Fukuda T, Matsumura T, Ato M, Hamasaki M, Nishiuchi Y, Murakami Y, Maeda Y, Yoshimori T, Matsumoto S, Kobayashi K, Kinoshita T, Morita YS (2013) Critical roles for lipomannan and lipoarabinomannan in cell wall integrity of mycobacteria and pathogenesis of tuberculosis. mBio 4(1):e00472-12. doi:10.1128/mBio.00472-12
9. Welsh KJ, Hunter RL, Actor JK (2013) Trehalose 6,6′-dimycolate: a coat to regulate tuberculosis immunopathogenesis. Tuberculosis 93(Suppl):S3–S9. doi:10.1016/S1472-9792(13)70003-9
10. Jo EK (2008) Mycobacterial interaction with innate receptors: TLRs, C-type lectins, and NLRs. Curr Opin Infect Dis 21(3):279–286. doi:10.1097/QCO.0b013e3282f88b5d
11. Takeuchi O, Sato S, Horiuchi T, Hoshino K, Takeda K, Dong Z, Modlin RL, Akira S (2002) Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 169(1):10–14
12. Bafica A, Scanga CA, Feng CG, Leifer C, Cheever A, Sher A (2005) TLR9 regulates Th1 responses and cooperates with TLR2 in mediating optimal resistance to Mycobacterium tuberculosis. J Exp Med 202(12):1715–1724. doi:10.1084/jem.20051782
13. Jo EK, Yang CS, Choi CH, Harding CV (2007) Intracellular signalling cascades regulating innate immune responses to Mycobacteria: branching out from Toll-like receptors. Cell Microbiol 9(5):1087–1098. doi:10.1111/j.1462-5822.2007.00914.x
14. Sanchez D, Rojas M, Hernandez I, Radzioch D, Garcia LF, Barrera LF (2010) Role of TLR2- and TLR4-mediated signaling in Mycobacterium tuberculosis-induced macrophage death. Cell Immunol 260(2):128–136. doi:10.1016/j.cellimm.2009.10.007
15. Uciechowski P, Imhoff H, Lange C, Meyer CG, Browne EN, Kirsten DK, Schroder AK, Schaaf B, Al-Lahham A, Reinert RR, Reiling N, Haase H, Hatzmann A, Fleischer D, Heussen N, Kleines M, Rink L (2011) Susceptibility to tuberculosis is associated with TLR1 polymorphisms resulting in a lack of TLR1 cell surface expression. J Leukoc Biol 90(2):377–388. doi:10.1189/jlb.0409233
16. Liu Q, Li W, Li D, Feng Y, Tao C (2014) TIRAP C539T polymorphism contributes to tuberculosis susceptibility: evidence from a meta-analysis. Infect Genet Evol 27:32–39. doi:10.1016/j.meegid.2014.06.025
17. Dittrich N, Berrocal-Almanza LC, Thada S, Goyal S, Slevogt H, Sumanlatha G, Hussain A, Sur S, Burkert S, Oh DY, Valluri V, Schumann RR, Conrad ML (2015) Toll-like receptor 1 variations influence susceptibility and immune response to Mycobacterium tuberculosis. Tuberculosis. doi:10.1016/j.tube.2015.02.045
18. Qi H, Sun L, Wu X, Jin Y, Xiao J, Wang S, Shen C, Chu P, Qi Z, Xu F, Guo Y, Jiao W, Tian J, Shen A (2015) Toll-like receptor 1(TLR1) Gene SNP rs5743618 is associated with increased risk for tuberculosis in Han Chinese children. Tuberculosis 95(2):197–203. doi:10.1016/j.tube.2014.12.001
19. Schurz H, Daya M, Moller M, Hoal EG, Salie M (2015) TLR1, 2, 4, 6 and 9 variants associated with tuberculosis susceptibility: a systematic review and meta-analysis. PLoS One 10(10):e0139711. doi:10.1371/journal.pone.0139711
20. Azad AK, Sadee W, Schlesinger LS (2012) Innate immune gene polymorphisms in tuberculosis. Infect Immun 80(10):3343–3359. doi:10.1128/IAI.00443-12
21. Ishikawa E, Ishikawa T, Morita YS, Toyonaga K, Yamada H, Takeuchi O, Kinoshita T, Akira S, Yoshikai Y, Yamasaki S (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J Exp Med 206(13):2879–2888. doi:10.1084/jem.20091750
22. Schoenen H, Bodendorfer B, Hitchens K, Manzanero S, Werninghaus K, Nimmerjahn F, Agger EM, Stenger S, Andersen P, Ruland J, Brown GD, Wells C, Lang R (2010) Cutting edge: mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J Immunol 184(6):2756–2760. doi:10.4049/jimmunol.0904013
23. Yonekawa A, Saijo S, Hoshino Y, Miyake Y, Ishikawa E, Suzukawa M, Inoue H, Tanaka M, Yoneyama M, Oh-hora M, Akashi K, Yamasaki S (2014) Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 41(3):402–413. doi:10.1016/j.immuni.2014.08.005
24. Zhao XQ, Zhu LL, Chang Q, Jiang C, You Y, Luo T, Jia XM, Lin X (2014) C-type lectin receptor dectin-3 mediates trehalose 6,6′-dimycolate (TDM)-induced Mincle expression through CARD9/Bcl10/MALT1-dependent nuclear factor (NF)-kappaB activation. J Biol Chem 289(43):30052–30062. doi:10.1074/jbc.M114.588574
25. Wilson GJ, Marakalala MJ, Hoving JC, van Laarhoven A, Drummond RA, Kerscher B, Keeton R, van de Vosse E, Ottenhoff TH, Plantinga TS, Alisjahbana B, Govender D, Besra GS, Netea MG, Reid DM, Willment JA, Jacobs M, Yamasaki S, van Crevel R, Brown GD (2015) The C-type lectin receptor CLECSF8/CLEC4D is a key component of anti-mycobacterial immunity. Cell Host Microbe 17(2):252–259. doi:10.1016/j.chom.2015.01.004
26. Zelensky AN, Gready JE (2005) The C-type lectin-like domain superfamily. FEBS J 272(24):6179–6217. doi:10.1111/j.1742-4658.2005.05031.x
27. Geijtenbeek TB, Gringhuis SI (2009) Signalling through C-type lectin receptors: shaping immune responses. Nat Rev Immunol 9(7):465–479. doi:10.1038/nri2569
28. Drickamer K (1999) C-type lectin-like domains. Curr Opin Struct Biol 9(5):585–590
29. Cambi A, Figdor CG (2003) Dual function of C-type lectin-like receptors in the immune system. Curr Opin Cell Biol 15(5):539–546
30. McGreal EP, Martinez-Pomares L, Gordon S (2004) Divergent roles for C-type lectins expressed by cells of the innate immune system. Mol Immunol 41(11):1109–1121. doi:10.1016/j.molimm.2004.06.013
31. Garcia-Vallejo JJ, van Kooyk Y (2009) Endogenous ligands for C-type lectin receptors: the true regulators of immune homeostasis. Immunol Rev 230(1):22–37. doi:10.1111/j.1600-065X.2009.00786.x
32. Graham LM, Brown GD (2009) The Dectin-2 family of C-type lectins in immunity and homeostasis. Cytokine 48(1–2):148–155. doi:10.1016/j.cyto.2009.07.010
33. Atochina EN, Gow AJ, Beck JM, Haczku A, Inch A, Kadire H, Tomer Y, Davis C, Preston AM, Poulain F, Hawgood S, Beers MF (2004) Delayed clearance of pneumocystis carinii infection, increased inflammation, and altered nitric oxide metabolism in lungs of surfactant protein-D knockout mice. J Infect Dis 189(8):1528–1539. doi:10.1086/383130
34. Madan T, Reid KBM, Singh M, Sarma PU, Kishore U (2005) Susceptibility of mice genetically deficient in the surfactant protein (SP)-A or SP-D gene to pulmonary hypersensitivity induced by antigens and allergens of Aspergillus fumigatus. J Immunol 174(11):6943–6954
35. Wells CA, Salvage-Jones JA, Li X, Hitchens K, Butcher S, Murray RZ, Beckhouse AG, Lo YL, Manzanero S, Cobbold C, Schroder K, Ma B, Orr S, Stewart L, Lebus D, Sobieszczuk P, Hume DA, Stow J, Blanchard H, Ashman RB (2008) The macrophage-inducible C-type lectin, mincle, is an essential component of the innate immune response to Candida albicans. J Immunol 180(11):7404–7413
36. Yamasaki S, Matsumoto M, Takeuchi O, Matsuzawa T, Ishikawa E, Sakuma M, Tateno H, Uno J, Hirabayashi J, Mikami Y, Takeda K, Akira S, Saito T (2009) C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc Natl Acad Sci USA 106(6):1897–1902. doi:10.1073/pnas.0805177106
37. Balderramas HA, Penitenti M, Rodrigues DR, Bachiega TF, Fernandes RK, Ikoma MRV, Dias-Melicio LA, Oliveira SL, Soares AMVC (2014) Human neutrophils produce IL-12, IL-10, PGE2 and LTB4 in response to Paracoccidioides brasiliensis: involvement of TLR2, mannose receptor and dectin-1. Cytokine 67(1):36–43. doi:10.1016/j.cyto.2014.02.004
38. Holmer SM, Evans KS, Asfaw YG, Saini D, Schell WA, Ledford JG, Frothingham R, Wright JR, Sempowski GD, Perfect JR (2014) Impact of surfactant protein D, interleukin-5, and eosinophilia on Cryptococcosis. Infect Immun 82(2):683–693. doi:10.1128/IAI.00855-13
39. Ou XT, Wu JQ, Zhu LP, Guan M, Xu B, Hu XP, Wang X, Weng XH (2011) Genotypes coding for mannose-binding lectin deficiency correlated with cryptococcal meningitis in HIV-uninfected Chinese patients. J Infect Dis 203(11):1686–1691. doi:10.1093/infdis/jir152
40. Rosentul DC, Plantinga TS, Oosting M, Scott WK, Velez Edwards DR, Smith PB, Alexander BD, Yang JC, Laird GM, Joosten LA, van der Meer JW, Perfect JR, Kullberg BJ, Netea MG, Johnson MD (2011) Genetic variation in the dectin-1/CARD9 recognition pathway and susceptibility to candidemia. J Infect Dis 204(7):1138–1145. doi:10.1093/infdis/jir458
41. Sainz J, Lupianez CB, Segura-Catena J, Vazquez L, Rios R, Oyonarte S, Hemminki K, Forsti A, Jurado M (2012) Dectin-1 and DC-SIGN polymorphisms associated with invasive pulmonary Aspergillosis infection. PLoS One 7(2):e32273. doi:10.1371/journal.pone.0032273
42. Yamamoto H, Nakamura Y, Sato K, Takahashi Y, Nomura T, Miyasaka T, Ishii K, Hara H, Yamamoto N, Kanno E, Iwakura Y, Kawakami K (2014) Defect of CARD9 leads to impaired accumulation of gamma interferon-producing memory phenotype T cells in lungs and increased susceptibility to pulmonary infection with Cryptococcus neoformans. Infect Immun 82(4):1606–1615. doi:10.1128/IAI.01089-13
43. Qu X, Che C, Gao A, Lin J, Wang N, Du X, Liu Y, Guo Y, Chen W, Zhao G (2015) Association of Dectin-1 and DC-SIGN gene single nucleotide polymorphisms with fungal keratitis in the northern Han Chinese population. Mol Vis 21:391–402
44. Wang MY, Wang FP, Yang JB, Zhao DF, Wang HP, Shao F, Wang WJ, Sun RL, Ling MZ, Zhai JJ, Song SJ (2013) Mannan-binding lectin inhibits Candida albicans-induced cellular responses in PMA-activated THP-1 cells through Toll-like receptor 2 and Toll-like receptor 4. PLoS One. doi:10.1371/journal.pone.0083517
45. Zhu LL, Zhao XQ, Jiang C, You Y, Chen XP, Jiang YY, Jia XM, Lin X (2013) C-type lectin receptors Dectin-3 and Dectin-2 form a heterodimeric pattern-recognition receptor for host defense against fungal infection. Immunity 39(2):324–334. doi:10.1016/j.immuni.2013.05.017
46. Wevers BA, Kaptein TM, Zijlstra-Willems EM, Theelen B, Boekhout T, Geijtenbeek TB, Gringhuis SI (2014) Fungal engagement of the C-type lectin mincle suppresses dectin-1-induced antifungal immunity. Cell Host Microbe 15(4):494–505. doi:10.1016/j.chom.2014.03.008
47. Loures FV, Araujo EF, Feriotti C, Bazan SB, Calich VLG (2015) TLR-4 cooperates with Dectin-1 and mannose receptor to expand Th17 and Tc17 cells induced by Paracoccidioides brasiliensis stimulated dendritic cells. Front Microbiol. doi:10.3389/Fmicb.2015.00261
48. Watford WT, Wright JR, Hester CG, Jiang H, Frank MM (2001) Surfactant protein A regulates complement activation. J Immunol 167(11):6593–6600
49. Kostina E, Ofek I, Crouch E, Friedman R, Sirota L, Klinger G, Sahly H, Keisari Y (2005) Noncapsulated Klebsiella pneumoniae bearing mannose-containing O antigens is rapidly eradicated from mouse lung and triggers cytokine production by macrophages following opsonization with surfactant protein D. Infect Immun 73(12):8282–8290. doi:10.1128/IAI.73.12.8282-8290.2005
50. Malherbe DC, Erpenbeck VJ, Abraham SN, Crouch EC, Hohlfeld JM, Wright JR (2005) Surfactant protein D decreases pollen-induced IgE-dependent mast cell degranulation. Am J Physiol Lung Cell Mol Physiol 289(5):L856–L866. doi:10.1152/ajplung.00009.2005
51. Palaniyar N, Clark H, Nadesalingam J, Shih MJ, Hawgood S, Reid KB (2005) Innate immune collectin surfactant protein D enhances the clearance of DNA by macrophages and minimizes anti-DNA antibody generation. J Immunol 174(11):7352–7358
52. Holmskov U, Thiel S, Jensenius JC (2003) Collectins and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21:547–578. doi:10.1146/annurev.immumol.21.120601.140954
53. Ferguson JS, Voelker DR, McCormack FX, Schlesinger LS (1999) Surfactant protein D binds to Mycobacterium tuberculosis bacilli and lipoarabinomannan via carbohydrate–lectin interactions resulting in reduced phagocytosis of the bacteria by macrophages. J Immunol 163(1):312–321
54. Beharka AA, Gaynor CD, Kang BK, Voelker DR, McCormack FX, Schlesinger LS (2002) Pulmonary surfactant protein A up-regulates activity of the mannose receptor, a pattern recognition receptor expressed on human macrophages. J Immunol 169(7):3565–3573
55. Sancho D, Reis e Sousa C (2012) Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu Rev Immunol 30:491–529. doi:10.1146/annurev-immunol-031210-101352
56. Kerrigan AM, Brown GD (2010) Syk-coupled C-type lectin receptors that mediate cellular activation via single tyrosine based activation motifs. Immunol Rev 234(1):335–352. doi:10.1111/j.0105-2896.2009.00882.x
57. Marakalala MJ, Graham LM, Brown GD (2010) The role of Syk/CARD9-coupled C-type lectin receptors in immunity to Mycobacterium tuberculosis infections. Clin Dev Immunol 2010:567571. doi:10.1155/2010/567571
58. Strasser D, Neumann K, Bergmann H, Marakalala MJ, Guler R, Rojowska A, Hopfner KP, Brombacher F, Urlaub H, Baier G, Brown GD, Leitges M, Ruland J (2012) Syk kinase-coupled C-type lectin receptors engage protein kinase C-sigma to elicit Card9 adaptor-mediated innate immunity. Immunity 36(1):32–42. doi:10.1016/j.immuni.2011.11.015
59. Billadeau DD, Leibson PJ (2002) ITAMs versus ITIMs: striking a balance during cell regulation. J Clin Investig 109(2):161–168. doi:10.1172/Jci14843
60. Marshall AS, Willment JA, Lin HH, Williams DL, Gordon S, Brown GD (2004) Identification and characterization of a novel human myeloid inhibitory C-type lectin-like receptor (MICL) that is predominantly expressed on granulocytes and monocytes. J Biol Chem 279(15):14792–14802. doi:10.1074/jbc.M313127200
61. Richard M, Thibault N, Veilleux P, Gareau-Page G, Beaulieu AD (2006) Granulocyte macrophage-colony stimulating factor reduces the affinity of SHP-2 for the ITIM of CLECSF6 in neutrophils: a new mechanism of action for SHP-2. Mol Immunol 43(10):1716–1721. doi:10.1016/j.molimm.2005.10.006
62. Barrow AD, Trowsdale J (2006) You say ITAM and I say ITIM, let’s call the whole thing off: the ambiguity of immunoreceptor signalling. Eur J Immunol 36(7):1646–1653. doi:10.1002/eji.200636195
63. Pinheiro da Silva F, Aloulou M, Benhamou M, Monteiro RC (2008) Inhibitory ITAMs: a matter of life and death. Trends Immunol 29(8):366–373. doi:10.1016/j.it.2008.05.001
64. Geijtenbeek TBH, van Vliet SJ, Koppel EA, Sanchez-Hernandez M, Vandenbroucke-Grauls CMJE, Appelmelk B, van Kooyk Y (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J Exp Med 197(1):7–17. doi:10.1084/jem.20021229
65. Gold JA, Hoshino Y, Tanaka N, Rom WN, Raju B, Condos R, Weiden MD (2004) Surfactant protein A modulates the inflammatory response in macrophages during tuberculosis. Infect Immun 72(2):645–650
66. Lee HM, Yuk JM, Shin DM, Jo EK (2009) Dectin-1 is inducible and plays an essential role for mycobacteria-induced innate immune responses in airway epithelial cells. J Clin Immunol 29(6):795–805. doi:10.1007/s10875-009-9319-3
67. Astarie-Dequeker C, N’Diaye EN, Le Cabec V, Rittig MG, Prandi J, Maridonneau-Parini I (1999) The mannose receptor mediates uptake of pathogenic and nonpathogenic mycobacteria and bypasses bactericidal responses in human macrophages. Infect Immun 67(2):469–477
68. Gupta G, Surolia A (2007) Collectins: sentinels of innate immunity. BioEssays: news and reviews in molecular, cellular and developmental biology 29(5):452–464. doi:10.1002/bies.20573
69. Kishore U, Greenhough TJ, Waters P, Shrive AK, Ghai R, Kamran MF, Bernal AL, Reid KBM, Madan T, Chakraborty T (2006) Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol Immunol 43(9):1293–1315. doi:10.1016/j.molimm.2005.08.004
70. Ferguson JS, Martin JL, Azad AK, McCarthy TR, Kang PB, Voelker DR, Crouch EC, Schlesinger LS (2006) Surfactant protein D increases fusion of Mycobacterium tuberculosis-containing phagosomes with lysosomes in human macrophages. Infect Immun 74(12):7005–7009. doi:10.1128/Iai.01402-06
71. Hoppe HC, deWet BJM, Cywes C, Daffe M, Ehlers MRW (1997) Identification of phosphatidylinositol mannoside as a mycobacterial adhesin mediating both direct and opsonic binding to nonphagocytic mammalian cells. Infect Immun 65(9):3896–3905
72. Sidobre S, Nigou J, Puzo G, Riviere M (2000) Lipoglycans are putative ligands for the human pulmonary surfactant protein A attachment to mycobacteria: critical role of the lipids for lectin-carbohydrate recognition. J Biol Chem 275(4):2415–2422
73. Seaton BA, Crouch EC, McCormack FX, Head JF, Hartshorn KL, Mendelsohn R (2010) Review: structural determinants of pattern recognition by lung collectins. Innate Immun 16(3):143–150. doi:10.1177/1753425910368716
74. Ragas A, Roussel L, Puzo G, Riviere M (2007) The Mycobacterium tuberculosis cell-surface glycoprotein apa as a potential adhesin to colonize target cells via the innate immune system pulmonary C-type lectin surfactant protein A. J Biol Chem 282(8):5133–5142. doi:10.1074/jbc.M610183200
75. Gaynor CD, McCormack FX, Voelker DR, McGowan SE, Schlesinger LS (1995) Pulmonary surfactant protein A mediates enhanced phagocytosis of Mycobacterium tuberculosis by a direct interaction with human macrophages. J Immunol 155(11):5343–5351
76. Hu H, Teng GL, Gai LZ, Yang Y, Zhu CJ (2013) Clinical value of surfactant protein-A in serum and sputum for pulmonary tuberculosis diagnosis. Genet Mol Res: GMR 12(4):4918–4924. doi:10.4238/2013.October.24.2
77. Pasula R, Wright JR, Kachel DL, Martin WJ (1999) Surfactant protein A suppresses reactive nitrogen intermediates by alveolar macrophages in response to Mycobacterium tuberculosis. J Clin Investig 103(4):483–490. doi:10.1172/Jci2991
78. Weikert LF, Lopez JP, Abdolrasulnia R, Chroneos ZC, Shepherd VL (2000) Surfactant protein A enhances mycobacterial killing by rat macrophages through a nitric oxide-dependent pathway. Am J Physiol-Lung C 279(2):L216–L223
79. Ferguson JS, Voelker DR, Ufnar JA, Dawson AJ, Schlesinger LS (2002) Surfactant protein D inhibition of human macrophage uptake of Mycobacterium tuberculosis is independent of bacterial agglutination. J Immunol 168(3):1309–1314
80. Lemos MP, McKinney J, Rhee KY (2011) Dispensability of surfactant proteins A and D in immune control of Mycobacterium tuberculosis infection following aerosol challenge of mice. Infect Immun 79(3):1077–1085. doi:10.1128/Iai.00286-10
81. Floros J, Lin HM, Garcia A, Salazar MA, Guo X, DiAngelo S, Montano M, Luo J, Pardo A, Selman M (2000) Surfactant protein genetic marker alleles identify a subgroup of tuberculosis in a Mexican population. J Infect Dis 182(5):1473–1478. doi:10.1086/315866
82. Malik S, Greenwood CM, Eguale T, Kifle A, Beyene J, Habte A, Tadesse A, Gebrexabher H, Britton S, Schurr E (2006) Variants of the SFTPA1 and SFTPA2 genes and susceptibility to tuberculosis in Ethiopia. Hum Genet 118(6):752–759. doi:10.1007/s00439-005-0092-y
83. Madan T, Saxena S, Murthy KJR, Muralidhar K, Sarma PU (2002) Association of polymorphisms in the collagen region of human SP-A1 and SP-A2 genes with pulmonary tuberculosis in Indian population. Clin Chem Lab Med 40(10):1002–1008. doi:10.1515/Cclm.2002.174
84. Yang HY, Li H, Wang YG, Xu CY, Zhao YL, Ma XG, Li XW, Chen H (2014) Correlation analysis between single nucleotide polymorphisms of pulmonary surfactant protein A gene and pulmonary tuberculosis in the Han population in China. Int J Infect Dis 26:31–36. doi:10.1016/j.ijid.2014.03.1395
85. Vaid M, Kaur S, Madan T, Singh H, Gupta VK, Murthy KJR, Sarma PU (2006) Association of SP-D, MNL and I-NOS genetic variants with pulmonary tuberculosis. Indian J Hum Genet 12(3):105–110
86. Helke KL, Mankowski JL, Manabe YC (2006) Animal models of cavitation in pulmonary tuberculosis. Tuberculosis 86(5):337–348. doi:10.1016/j.tube.2005.09.001
87. Turner MW (1996) Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today 17(11):532–540
88. Ip WK, Takahashi K, Ezekowitz RA, Stuart LM (2009) Mannose-binding lectin and innate immunity. Immunol Rev 230(1):9–21. doi:10.1111/j.1600-065X.2009.00789.x
89. Lugo-Villarino G, Hudrisier D, Tanne A, Neyrolles O (2011) C-type lectins with a sweet spot for Mycobacterium tuberculosis. Eur J Microbiol Immunol 1(1):25–40. doi:10.1556/EuJMI.1.2011.1.6
90. Bartlomiejczyk MA, Swierzko AS, Brzostek A, Dziadek J, Cedzynski M (2014) Interaction of lectin pathway of complement-activating pattern recognition molecules with mycobacteria. Clin Exp Immunol 178(2):310–319. doi:10.1111/cei.12416
91. Takahashi K, Ezekowitz RA (2005) The role of the mannose-binding lectin in innate immunity. Clin Infect Dis 41(Suppl 7):S440–S444. doi:10.1086/431987
92. Shi L, Takahashi K, Dundee J, Shahroor-Karni S, Thiel S, Jensenius JC, Gad F, Hamblin MR, Sastry KN, Ezekowitz RA (2004) Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J Exp Med 199(10):1379–1390. doi:10.1084/jem.20032207
93. Genster N, Takahashi M, Sekine H, Endo Y, Garred P, Fujita T (2014) Lessons learned from mice deficient in lectin complement pathway molecules. Mol Immunol 61(2):59–68. doi:10.1016/j.molimm.2014.07.007
94. Moller-Kristensen M, Ip WK, Shi L, Gowda LD, Hamblin MR, Thiel S, Jensenius JC, Ezekowitz RA, Takahashi K (2006) Deficiency of mannose-binding lectin greatly increases susceptibility to postburn infection with Pseudomonas aeruginosa. J Immunol 176(3):1769–1775
95. Held K, Thiel S, Loos M, Petry F (2008) Increased susceptibility of complement factor B/C2 double knockout mice and mannan-binding lectin knockout mice to systemic infection with Candida albicans. Mol Immunol 45(15):3934–3941. doi:10.1016/j.molimm.2008.06.021
96. Heitzeneder S, Seidel M, Forster-Waldl E, Heitger A (2012) Mannan-binding lectin deficiency: good news, bad news, doesn’t matter? Clin Immunol 143(1):22–38. doi:10.1016/j.clim.2011.11.002
97. Thiel S, Frederiksen PD, Jensenius JC (2006) Clinical manifestations of mannan-binding lectin deficiency. Mol Immunol 43(1–2):86–96. doi:10.1016/j.molimm.2005.06.018
98. El Sahly HM, Reich RA, Dou SJ, Musser JM, Graviss EA (2004) The effect of mannose binding lectin gene polymorphisms on susceptibility to tuberculosis in different ethnic groups. Scand J Infect Dis 36(2):106–108
99. Soborg C, Madsen HO, Andersen AB, Lillebaek T, Kok-Jensen A, Garred P (2003) Mannose-binding lectin polymorphisms in clinical tuberculosis. J Infect Dis 188(5):777–782. doi:10.1086/377183
100. Ozbas-Gerceker F, Tezcan I, Berkel AI, Ozkara S, Ozcan A, Ersoy F, Sanal O, Ozguc M (2003) The effect of mannose-binding protein gene polymorphisms in recurrent respiratory system infections in children and lung tuberculosis. Turk J Pediatr 45(2):95–98
101. Cosar H, Ozkinay F, Onay H, Bayram N, Bakiler AR, Anil M, Can D, Ozkinay C (2008) Low levels of mannose-binding lectin confers protection against tuberculosis in Turkish children. Eur J Clin Microbiol Infect Dis 27(12):1165–1169. doi:10.1007/s10096-008-0573-8
102. Capparelli R, Iannaccone M, Palumbo D, Medaglia C, Moscariello E, Russo A, Iannelli D (2009) Role played by human mannose-binding lectin polymorphisms in pulmonary tuberculosis. J Infect Dis 199(5):666–672. doi:10.1086/596658
103. Selvaraj P, Narayanan PR, Reetha AM (1999) Association of functional mutant homozygotes of the mannose binding protein gene with susceptibility to pulmonary tuberculosis in India. Tuber Lung Dis 79(4):221–227. doi:10.1054/tuld.1999.0204
104. Bellamy R, Ruwende C, McAdam KPWJ, Thursz M, Sumiya M, Summerfield J, Gilbert SC, Corrah T, Kwiatkowski D, Whittle HC, Hill AVS (1998) Mannose binding protein deficiency is not associated with malaria, hepatitis B carriage nor tuberculosis in Africans. Qjm-Mon J Assoc Phys 91(1):13–18. doi:10.1093/qjmed/91.1.13
105. Wu LL, Deng HJ, Zheng YH, Mansjo M, Zheng XB, Hu Y, Xu BA (2015) An association study of NRAMP1, VDR, MBL and their interaction with the susceptibility to tuberculosis in a Chinese population. Int J Infect Dis 38:129–135. doi:10.1016/j.ijid.2015.08.003
106. Liu W, Zhang F, Xin ZT, Zhao QM, Wu XM, Zhang PH, de Vlas S, Richardus JH, Habbema JDF, Yang H, Cao WC (2006) Sequence variations in the MBL gene and their relationship to pulmonary tuberculosis in the Chinese Han population. Int J Tuberc Lung Dis 10(10):1098–1103
107. Denholm JT, McBryde ES, Eisen DP (2010) Mannose-binding lectin and susceptibility to tuberculosis: a meta-analysis. Clin Exp Immunol 162(1):84–90. doi:10.1111/j.1365-2249.2010.04221.x
108. Shi J, Xie M, Wang JM, Xu YJ, Xiong WN, Liu XS (2013) Mannose-binding lectin two gene polymorphisms and tuberculosis susceptibility in Chinese population: a meta-analysis. J Huazhong Univ Sci Technol Med Sci 33(2):166–171. doi:10.1007/s11596-013-1091-1
109. de Wit E, van der Merwe L, van Helden PD, Hoal EG (2011) Gene-gene interaction between tuberculosis candidate genes in a South African population. Mamm Genome 22(1–2):100–110. doi:10.1007/s00335-010-9280-8
110. Chen MS, Deng J, Su CX, Li J, Wang M, Abuaku BK, Hu SM, Tan HZ, Wen SW (2014) Impact of passive smoking, cooking with solid fuel exposure, and MBL/MASP-2 gene polymorphism upon susceptibility to tuberculosis. Int J Infect Dis 29:1–6. doi:10.1016/j.ijid.2014.08.010
111. Chen M, Liang Y, Li W, Wang M, Hu L, Abuaku BK, Huang X, Tan H, Wen SW (2015) Impact of MBL and MASP-2 gene polymorphism and its interaction on susceptibility to tuberculosis. BMC Infect Dis 15:151. doi:10.1186/s12879-015-0879-y
112. Singla N, Gupta D, Joshi A, Batra N, Singh J, Birbian N (2012) Association of mannose-binding lectin gene polymorphism with tuberculosis susceptibility and sputum conversion time. Int J Immunogenet 39(1):10–14. doi:10.1111/j.1744-313X.2011.01047.x
113. Thye T, Niemann S, Walter K, Homolka S, Intemann CD, Chinbuah MA, Enimil A, Gyapong J, Osei I, Owusu-Dabo E, Rusch-Gerdes S, Horstmann RD, Ehlers S, Meyer CG (2011) Variant G57E of mannose binding lectin associated with protection against tuberculosis caused by Mycobacterium africanum but not by M. tuberculosis. PLoS One. doi:10.1371/journal.pone.0020908
114. Chalmers JD, Matsushita M, Kilpatrick DC, Hill AT (2015) No strong relationship between components of the lectin pathway of complement and susceptibility to pulmonary tuberculosis. Inflammation 38(4):1731–1737. doi:10.1007/s10753-015-0150-0
115. Hijikata M, Matsushita I, Hang NT, Maeda S, Thuong PH, do Tam B, Shimbo T, Sakurada S, Cuong VC, Lien LT, Keicho N (2014) Age-dependent association of mannose-binding lectin polymorphisms with the development of pulmonary tuberculosis in Viet Nam. Hum Immunol 75(8):840–846. doi:10.1016/j.humimm.2014.06.006
116. Schlesinger LS (1993) Macrophage phagocytosis of virulent but not attenuated strains of Mycobacterium tuberculosis is mediated by mannose receptors in addition to complement receptors. J Immunol 150(7):2920–2930
117. Tailleux L, Schwartz O, Herrmann JL, Pivert E, Jackson M, Amara A, Legres L, Dreher D, Nicod LP, Gluckman JC, Lagrange PH, Gicquel B, Neyrolles O (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J Exp Med 197(1):121–127. doi:10.1084/jem.20021468
118. Melo MD, Catchpole IR, Haggar G, Stokes RW (2000) Utilization of CD11b knockout mice to characterize the role of complement receptor 3 (CR3, CD11b/CD18) in the growth of Mycobacterium tuberculosis in macrophages. Cell Immunol 205(1):13–23. doi:10.1006/cimm.2000.1710
119. Plato A, Willment JA, Brown GD (2013) C-type Lectin-like receptors of the Dectin-1 cluster: ligands and signaling pathways. Int Rev Immunol 32(2):134–156. doi:10.3109/08830185.2013.777065
120. Taylor ME, Conary JT, Lennartz MR, Stahl PD, Drickamer K (1990) Primary structure of the mannose receptor contains multiple motifs resembling carbohydrate-recognition domains. J Biol Chem 265(21):12156–12162
121. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92(6):1177–1186. doi:10.1189/jlb.0512231
122. Le Cabec V, Emorine LJ, Toesca I, Cougoule C, Maridonneau-Parini I (2005) The human macrophage mannose receptor is not a professional phagocytic receptor. J Leukoc Biol 77(6):934–943. doi:10.1189/jlb.1204705
123. Prigozy TI, Sieling PA, Clemens D, Stewart PL, Behar SM, Porcelli SA, Brenner MB, Modlin RL, Kronenberg M (1997) The mannose receptor delivers lipoglycan antigens to endosomes for presentation to T cells by CD1b molecules. Immunity 6(2):187–197
124. Schlesinger LS, Hull SR, Kaufman TM (1994) Binding of the terminal mannosyl units of lipoarabinomannan from a virulent strain of Mycobacterium tuberculosis to human macrophages. J Immunol 152(8):4070–4079
125. Torrelles JB, Azad AK, Schlesinger LS (2006) Fine discrimination in the recognition of individual species of phosphatidyl-myo-inositol mannosides from Mycobacterium tuberculosis by C-type lectin pattern recognition receptors. J Immunol 177(3):1805–1816
126. Diaz-Silvestre H, Espinosa-Cueto P, Sanchez-Gonzalez A, Esparza-Ceron MA, Pereira-Suarez AL, Bernal-Fernandez G, Espitia C, Mancilla R (2005) The 19-kDa antigen of Mycobacterium tuberculosis is a major adhesin that binds the mannose receptor of THP-1 monocytic cells and promotes phagocytosis of mycobacteria. Microb Pathog 39(3):97–107. doi:10.1016/j.micpath.2005.06.002
127. Astarie-Dequeker C, Carreno S, Cougoule C, Maridonneau-Parini I (2002) The protein tyrosine kinase Hck is located on lysosomal vesicles that are physically and functionally distinct from CD63-positive lysosomes in human macrophages. J Cell Sci 115(1):81–89
128. Kang PB, Azad AK, Torrelles JB, Kaufman TM, Beharka A, Tibesar E, DesJardin LE, Schlesinger LS (2005) The human macrophage mannose receptor directs Mycobacterium tuberculosis lipoarabinomannan-mediated phagosome biogenesis. J Exp Med 202(7):987–999. doi:10.1084/jem.20051239
129. Nigou J, Zelle-Rieser C, Gilleron M, Thurnher M, Puzo G (2001) Mannosylated lipoarabinomannans inhibit IL-12 production by human dendritic cells: evidence for a negative signal delivered through the mannose receptor. J Immunol 166(12):7477–7485
130. Chieppa M, Bianchi G, Doni A, Del Prete A, Sironi M, Laskarin G, Monti P, Piemonti L, Biondi A, Mantovani A, Introna M, Allavena P (2003) Cross-linking of the mannose receptor on monocyte-derived dendritic cells activates an anti-inflammatory immunosuppressive program. J Immunol 171(9):4552–4560
131. Zenaro E, Donini M, Dusi S (2009) Induction of Th1/Th17 immune response by Mycobacterium tuberculosis: role of dectin-1, mannose receptor, and DC-SIGN. J Leukoc Biol 86(6):1393–1401. doi:10.1189/jlb.0409242
132. Balboa L, Romero MM, Yokobori N, Schierloh P, Geffner L, Basile JI, Musella RM, Abbate E, de la Barrera S, Sasiain MC, Aleman M (2010) Mycobacterium tuberculosis impairs dendritic cell response by altering CD1b, DC-SIGN and MR profile. Immunol Cell Biol 88(7):716–726. doi:10.1038/icb.2010.22
133. Rivera-Marrero CA, Schuyler W, Roser S, Ritzenthaler JD, Newburn SA, Roman J (2002) M. tuberculosis induction of matrix metalloproteinase-9: the role of mannose and receptor-mediated mechanisms. Am J Physiol Lung Cell Mol Physiol 282(3):L546–L555. doi:10.1152/ajplung.00175.2001
134. Court N, Vasseur V, Vacher R, Fremond C, Shebzukhov Y, Yeremeev VV, Maillet I, Nedospasov SA, Gordon S, Fallon PG, Suzuki H, Ryffel B, Quesniaux VFJ (2010) Partial redundancy of the pattern recognition receptors, scavenger receptors, and C-type lectins for the long-term control of Mycobacterium tuberculosis infection. J Immunol 184(12):7057–7070. doi:10.4049/jimmunol.1000164
135. Zhang X, Jiang F, Wei L, Li F, Liu J, Wang C, Zhao M, Jiang T, Xu D, Fan D, Sun X, Li JC (2012) Polymorphic allele of human MRC1 confer protection against tuberculosis in a Chinese population. Int J Biol Sci 8(3):375–382. doi:10.7150/ijbs.4047
136. Zhang X, Li X, Zhang W, Wei L, Jiang T, Chen Z, Meng C, Liu J, Wu F, Wang C, Li F, Sun X, Li Z, Li JC (2013) The novel human MRC1 gene polymorphisms are associated with susceptibility to pulmonary tuberculosis in Chinese Uygur and Kazak populations. Mol Biol Rep 40(8):5073–5083. doi:10.1007/s11033-013-2610-7
137. Rappocciolo G, Piazza P, Fuller CL, Reinhart TA, Watkins SC, Rowe DT, Jais M, Gupta P, Rinaldo CR (2006) DC-SIGN on B lymphocytes is required for transmission of HIV-1 to T lymphocytes (vol 2, pg 3, 2004). PLoS Pathog 2(8):808. doi:10.1371/journal.ppat.0020088
138. Garcia-Vallejo JJ, van Kooyk Y (2013) The physiological role of DC-SIGN: a tale of mice and men. Trends Immunol 34(10):482–486. doi:10.1016/j.it.2013.03.001
139. Geijtenbeek TB, Krooshoop DJ, Bleijs DA, van Vliet SJ, van Duijnhoven GC, Grabovsky V, Alon R, Figdor CG, van Kooyk Y (2000) DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat Immunol 1(4):353–357. doi:10.1038/79815
140. van Gisbergen KPJM, Ludwig IS, Geijtenbeek TBH, van Kooyk Y (2005) Interactions of DC-SIGN with Mac-1 and CEACAM1 regulate contact between dendritic cells and neutrophils. FEBS Lett 579(27):6159–6168. doi:10.1016/j.febslet.2005.09.089
141. Gringhuis SI, den Dunnen J, Litjens M, van der Vlist M, Geijtenbeek TBH (2009) Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat Immunol 10(10):1081–1088. doi:10.1038/ni.1778
142. Hodges A, Sharrocks K, Edelmann M, Baban D, Moris A, Schwartz O, Drakesmith H, Davies K, Kessler B, McMichael A, Simmons A (2007) Activation of the lectin DC-SIGN induces an immature dendritic cell phenotype triggering Rho-GTPase activity required for HIV-1 replication. Nat Immunol 8(6):569–577. doi:10.1038/ni1470
143. Gringhuis SI, den Dunnen J, Litjens M, van Het Hof B, van Kooyk Y, Geijtenbeek TB (2007) C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 26(5):605–616. doi:10.1016/j.immuni.2007.03.012
144. Tailleux L, Pham-Thi N, Bergeron-Lafaurie A, Herrmann JL, Charles P, Schwartz O, Scheinmann P, Lagrange PH, de Blic J, Tazi A, Gicquel B, Neyrolles O (2005) DC-SIGN induction in alveolar macrophages defines privileged target host cells for mycobacteria in patients with tuberculosis. PLoS Med 2(12):e381. doi:10.1371/journal.pmed.0020381
145. Pitarque S, Herrmann JL, Duteyrat JL, Jackson M, Stewart GR, Lecointe F, Payre B, Schwartz O, Young DB, Marchal G, Lagrange PH, Puzo G, Gicquel B, Nigou J, Neyrolles O (2005) Deciphering the molecular bases of Mycobacterium tuberculosis binding to the lectin DC-SIGN reveals an underestimated complexity. Biochem J 392(Pt 3):615–624. doi:10.1042/BJ20050709
146. Appelmelk BJ, den Dunnen J, Driessen NN, Ummels R, Pak M, Nigou J, Larrouy-Maumus G, Gurcha SS, Movahedzadeh F, Geurtsen J, Brown EJ, Eysink Smeets MM, Besra GS, Willemsen PT, Lowary TL, van Kooyk Y, Maaskant JJ, Stoker NG, van der Ley P, Puzo G, Vandenbroucke-Grauls CM, Wieland CW, van der Poll T, Geijtenbeek TB, van der Sar AM, Bitter W (2008) The mannose cap of mycobacterial lipoarabinomannan does not dominate the Mycobacterium–host interaction. Cell Microbiol 10(4):930–944. doi:10.1111/j.1462-5822.2007.01097.x
147. Driessen NN, Ummels R, Maaskant JJ, Gurcha SS, Besra GS, Ainge GD, Larsen DS, Painter GF, Vandenbroucke-Grauls CM, Geurtsen J, Appelmelk BJ (2009) Role of phosphatidylinositol mannosides in the interaction between mycobacteria and DC-SIGN. Infect Immun 77(10):4538–4547. doi:10.1128/IAI.01256-08
148. Geurtsen J, Chedammi S, Mesters J, Cot M, Driessen NN, Sambou T, Kakutani R, Ummels R, Maaskant J, Takata H, Baba O, Terashima T, Bovin N, Vandenbroucke-Grauls CM, Nigou J, Puzo G, Lemassu A, Daffe M, Appelmelk BJ (2009) Identification of mycobacterial alpha-glucan as a novel ligand for DC-SIGN: involvement of mycobacterial capsular polysaccharides in host immune modulation. J Immunol 183(8):5221–5231. doi:10.4049/jimmunol.0900768
149. Gagliardi MC, Teloni R, Giannoni F, Pardini M, Sargentini V, Brunori L, Fattorini L, Nisini R (2005) Mycobacterium bovis Bacillus Calmette-Guerin infects DC-SIGN- dendritic cell and causes the inhibition of IL-12 and the enhancement of IL-10 production. J Leukoc Biol 78(1):106–113. doi:10.1189/jlb.0105037
150. Driessen NN, Boshoff HI, Maaskant JJ, Gilissen SA, Vink S, van der Sar AM, Vandenbroucke-Grauls CM, Bewley CA, Appelmelk BJ, Geurtsen J (2012) Cyanovirin-N inhibits mannose-dependent Mycobacterium-C-type lectin interactions but does not protect against murine tuberculosis. J Immunol 189(7):3585–3592. doi:10.4049/jimmunol.1102408
151. Schaefer M, Reiling N, Fessler C, Stephani J, Taniuchi I, Hatam F, Yildirim AO, Fehrenbach H, Walter K, Ruland J, Wagner H, Ehlers S, Sparwasser T (2008) Decreased pathology and prolonged survival of human DC-SIGN transgenic mice during mycobacterial infection. J Immunol 180(10):6836–6845
152. Tanne A, Ma B, Boudou F, Tailleux L, Botella H, Badell E, Levillain F, Taylor ME, Drickamer K, Nigou J, Dobos KM, Puzo G, Vestweber D, Wild MK, Marcinko M, Sobieszczuk P, Stewart L, Lebus D, Gicquel B, Neyrolles O (2009) A murine DC-SIGN homologue contributes to early host defense against Mycobacterium tuberculosis. J Exp Med 206(10):2205–2220. doi:10.1084/jem.20090188
153. Tanne A, Neyrolles O (2010) C-type lectins in immune defense against pathogens: the murine DC-SIGN homologue SIGNR3 confers early protection against Mycobacterium tuberculosis infection. Virulence 1(4):285–290. doi:10.4161/viru.1.4.11967
154. Soilleux EJ, Barten R, Trowsdale J (2000) DC-SIGN; a related gene, DC-SIGNR; and CD23 form a cluster on 19p13. J Immunol 165(6):2937–2942
155. Khoo US, Chan KY, Chan VS, Lin CL (2008) DC-SIGN and L-SIGN: the SIGNs for infection. J Mol Med 86(8):861–874. doi:10.1007/s00109-008-0350-2
156. Koppel EA, Ludwig IS, Hernandez MS, Lowary TL, Gadikota RR, Tuzikov AB, Vandenbroucke-Grauls CMJE, van Kooyk Y, Appelmelk BJ, Geijtenbeek TBH (2004) Identification of the mycobacterial carbohydrate structure that binds the C-type lectins DC-SIGN, L-SIGN and SIGNR1. Immunobiology 209(1–2):117–127. doi:10.1016/j.imbio.2004.03.003
157. Feinberg H, Guo Y, Mitchell DA, Drickamer K, Weis WI (2005) Extended neck regions stabilize tetramers of the receptors DC-SIGN and DC-SIGNR. J Biol Chem 280(2):1327–1335. doi:10.1074/jbc.M409925200
158. Soilleux EJ (2003) DC-SIGN (dendritic cell-specific ICAM-grabbing non-integrin) and DC-SIGN-related (DC-SIGNR): friend or foe? Clin Sci 104(4):437–446. doi:10.1042/cs20020092
159. Sakuntabhai A, Turbpaiboon C, Casademont I, Chuansumrit A, Lowhnoo T, Kajaste-Rudnitski A, Kalayanarooj SM, Tangnararatchakit K, Tangthawornchaikul N, Vasanawathana S, Chaiyaratana W, Yenchitsomanus PT, Suriyaphol P, Avirutnan P, Chokephaibulkit K, Matsuda F, Yoksan S, Jacob Y, Lathrop GM, Malasit P, Despres P, Julier C (2005) A variant in the CD209 promoter is associated with severity of dengue disease. Nat Genet 37(5):507–513. doi:10.1038/ng1550
160. Chang K, Deng SL, Lu WP, Wang F, Jia SR, Li FK, Yu LL, Chen M (2012) Association between CD209-336A/G and-871A/G polymorphisms and susceptibility of tuberculosis: a meta-analysis. PLoS One. doi:10.1371/journal.pone.0041519
161. Barreiro LB, Neyrolles O, Babb CL, Tailleux L, Quach H, McElreavey K, Helden PD, Hoal EG, Gicquel B, Quintana-Murci L (2006) Promoter variation in the DC-SIGN-encoding gene CD209 is associated with tuberculosis. PLoS Med 3(2):e20. doi:10.1371/journal.pmed.0030020
162. Ogarkov O, Mokrousov I, Sinkov V, Zhdanova S, Antipina S, Savilov E (2012) ‘Lethal’ combination of Mycobacterium tuberculosis Beijing genotype and human CD209 -336G allele in Russian male population. Infect Genet Evol 12(4):732–736. doi:10.1016/j.meegid.2011.10.005
163. Fayssel N, Bensghir R, Ouladlahsen A, Abdelghaffar H, Sodqi M, Lahlou K, Benjelloun S, Marhoum El Filali K, Ezzikouri S, Wakrim L (2015) Association of CD209L tandem repeats polymorphism with susceptibility to human immunodeficiency virus-1 infection, disease progression, and treatment outcomes: a Moroccan cohort study. Clin Microbiol Infect 21(5):513.e1-5. doi:10.1016/j.cmi.2014.12.012
164. Chan VS, Chan KY, Chen Y, Poon LL, Cheung AN, Zheng B, Chan KH, Mak W, Ngan HY, Xu X, Screaton G, Tam PK, Austyn JM, Chan LC, Yip SP, Peiris M, Khoo US, Lin CL (2006) Homozygous L-SIGN (CLEC4M) plays a protective role in SARS coronavirus infection. Nat Genet 38(1):38–46. doi:10.1038/ng1698
165. Ezzikouri S, Rebbani K, Fakhir FZ, Alaoui R, Nadir S, Diepolder H, Thursz M, Khakoo SI, Benjelloun S (2014) The allele 4 of neck region liver-lymph node-specific ICAM-3-grabbing integrin variant is associated with spontaneous clearance of hepatitis C virus and decrease of viral loads. Clin Microbiol Infect 20(5):O325–O332. doi:10.1111/1469-0691.12403
166. Barreiro LB, Neyrolles O, Babb CL, van Helden PD, Gicquel B, Hoal EG, Quintana-Murci L (2007) Length variation of DC-SIGN and L-SIGN neck-region has no impact on tuberculosis susceptibility. Hum Immunol 68(2):106–112. doi:10.1016/j.humimm.2006.10.020
167. da Silva RC, Segat L, da Cruz HL, Schindler HC, Montenegro LM, Crovella S, Guimaraes RL (2014) Association of CD209 and CD209L polymorphisms with tuberculosis infection in a Northeastern Brazilian population. Mol Biol Rep 41(8):5449–5457. doi:10.1007/s11033-014-3416-y
168. Ariizumi K, Shen GL, Shikano S, Xu S, Ritter R 3rd, Kumamoto T, Edelbaum D, Morita A, Bergstresser PR, Takashima A (2000) Identification of a novel, dendritic cell-associated molecule, dectin-1, by subtractive cDNA cloning. J Biol Chem 275(26):20157–20167. doi:10.1074/jbc.M909512199
169. Brown GD, Taylor PR, Reid DM, Willment JA, Williams DL, Martinez-Pomares L, Wong SYC, Gordon S (2002) Dectin-1 is a major beta-glucan receptor on macrophages. J Exp Med 196(3):407–412. doi:10.1084/Jem.20020470
170. Taylor PR, Brown GD, Reid DM, Willment JA, Martinez-Pomares L, Gordon S, Wong SYC (2002) The beta-glucan receptor, dectin-1, is predominantly expressed on the, surface of cells of the monocyte/macrophage and neutrophil lineages. J Immunol 169(7):3876–3882
171. Heyl KA, Klassert TE, Heinrich A, Muller MM, Klaile E, Dienemann H, Grunewald C, Bals R, Singer BB, Slevogt H (2014) Dectin-1 is expressed in human lung and mediates the proinflammatory immune response to nontypeable haemophilus influenzae. mBio. doi:10.1128/mBio.01492-14
172. Kerrigan AM, Brown GD (2010) Syk-coupled C-type lectin receptors that mediate cellular activation via single tyrosine based activation motifs. Immunol Rev 234:335–352
173. Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6(1):33–43. doi:10.1038/nri1745
174. Kerrigan AM, Brown GD (2011) Syk-coupled C-type lectins in immunity. Trends Immunol 32(4):151–156. doi:10.1016/j.it.2011.01.002
175. Dambuza IM, Brown GD (2015) C-type lectins in immunity: recent developments. Curr Opin Immunol 32:21–27. doi:10.1016/j.coi.2014.12.002
176. Gross O, Gewies A, Finger K, Schafer M, Sparwasser T, Peschel C, Forster I, Ruland J (2006) Card9 controls a non-TLR signalling pathway for innate anti-fungal immunity. Nature 442(7103):651–656. doi:10.1038/nature04926
177. Gringhuis SI, den Dunnen J, Litjens M, van der Vlist M, Wevers B, Bruijns SCM, Geijtenbeek TBH (2009) Dectin-1 directs T helper cell differentiation by controlling noncanonical NF-kappa B activation through Raf-1 and Syk. Nat Immunol 10(2):203–213. doi:10.1038/ni.1692
178. Gringhuis SI, Wevers BA, Kaptein TM, van Capel TM, Theelen B, Boekhout T, de Jong EC, Geijtenbeek TB (2011) Selective C-Rel activation via Malt1 controls anti-fungal T(H)-17 immunity by dectin-1 and dectin-2. PLoS Pathog 7(1):e1001259. doi:10.1371/journal.ppat.1001259
179. Gringhuis SI, Kaptein TM, Wevers BA, Theelen B, van der Vlist M, Boekhout T, Geijtenbeek TB (2012) Dectin-1 is an extracellular pathogen sensor for the induction and processing of IL-1beta via a noncanonical caspase-8 inflammasome. Nat Immunol 13(3):246–254. doi:10.1038/ni.2222
180. Underhill DM, Rossnagle E, Lowell CA, Simmons RM (2005) Dectin-1 activates Syk tyrosine kinase in a dynamic subset of macrophages for reactive oxygen production. Blood 106(7):2543–2550. doi:10.1182/blood-2005-03-1239
181. Yadav M, Schorey JS (2006) The beta-glucan receptor dectin-1 functions together with TLR2 to mediate macrophage activation by mycobacteria. Blood 108(9):3168–3175. doi:10.1182/blood-2006-05-024406
182. Shin DM, Yang CS, Yuk JM, Lee JY, Kim KH, Shin SJ, Takahara K, Lee SJ, Jo EK (2008) Mycobacterium abscessus activates the macrophage innate immune response via a physical and functional interaction between TLR2 and dectin-1. Cell Microbiol 10(8):1608–1621. doi:10.1111/j.1462-5822.2008.01151.x
183. Romero MM, Basile JI, Corra Feo L, Lopez B, Ritacco V, Aleman M (2015) Reactive oxygen species production by human dendritic cells involves TLR2 and dectin-1 and is essential for efficient immune response against Mycobacteria. Cell Microbiol. doi:10.1111/cmi.12562
184. Rothfuchs AG, Bafica A, Feng CG, Egen JG, Williams DL, Brown GD, Sher A (2007) Dectin-1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J Immunol 179(6):3463–3471
185. Romero MM, Basile JI, Feo LC, Lopez B, Ritacco V, Aleman M (2016) Reactive oxygen species production by human dendritic cells involves TLR2 and dectin-1 and is essential for efficient immune response against Mycobacteria. Cell Microbiol 18(6):875–886. doi:10.1111/cmi.12562
186. van de Veerdonk FL, Teirlinck AC, Kleinnijenhuis J, Kullberg BJ, van Crevel R, van der Meer JW, Joosten LA, Netea MG (2010) Mycobacterium tuberculosis induces IL-17A responses through TLR4 and dectin-1 and is critically dependent on endogenous IL-1. J Leukoc Biol 88(2):227–232. doi:10.1189/jlb.0809550
187. Marakalala MJ, Guler R, Matika L, Murray G, Jacobs M, Brombacher F, Rothfuchs AG, Sher A, Brown GD (2011) The Syk/CARD9-coupled receptor Dectin-1 is not required for host resistance to Mycobacterium tuberculosis in mice. Microbes Infect 13(2):198–201. doi:10.1016/j.micinf.2010.10.013
188. Rosentul DC, Plantinga TS, Papadopoulos A, Joosten LA, Antoniadou A, Venselaar H, Kullberg BJ, van der Meer JW, Giamarellos-Bourboulis EJ, Netea MG (2011) Variation in genes of beta-glucan recognition pathway and susceptibility to opportunistic infections in HIV-positive patients. Immunol Invest 40(7–8):735–750. doi:10.3109/08820139.2011.599088
189. Usluogullari B, Gumus I, Gunduz E, Kaygusuz I, Simavli S, Acar M, Oznur M, Gunduz M, Kafali H (2014) The role of Human Dectin-1 Y238X Gene Polymorphism in recurrent vulvovaginal candidiasis infections. Mol Biol Rep 41(10):6763–6768. doi:10.1007/s11033-014-3562-2
190. Ariizumi K, Shen GL, Shikano S, Ritter R 3rd, Zukas P, Edelbaum D, Morita A, Takashima A (2000) Cloning of a second dendritic cell-associated C-type lectin (dectin-2) and its alternatively spliced isoforms. J Biol Chem 275(16):11957–11963
191. Sato K, Yang XL, Yudate T, Chung JS, Wu JM, Luby-Phelps K, Kimberly RP, Underhill D, Cruz PD, Ariizumi K (2006) Dectin-2 is a pattern recognition receptor for fungi that couples with the Fc receptor gamma chain to induce innate immune responses. J Biol Chem 281(50):38854–38866. doi:10.1074/jbc.M606542200
192. Kanazawa N, Tashiro K, Inaba K, Lutz MB, Miyachi Y (2004) Molecular cloning of human dectin-2. J Invest Dermatol 122(6):1522–1524. doi:10.1111/j.0022-202X.2004.22602.x
193. Gavino AC, Chung JS, Sato K, Ariizumi K, Cruz PD Jr (2005) Identification and expression profiling of a human C-type lectin, structurally homologous to mouse dectin-2. Exp Dermatol 14(4):281–288. doi:10.1111/j.0906-6705.2005.00312.x
194. Taylor PR, Reid DM, Heinsbroek SEM, Brown GD, Gordon S, Wong SYC (2005) Dectin-2 is predominantly myeloid restricted and exhibits unique activation-dependent expression on maturing inflammatory monocytes elicited in vivo. Eur J Immunol 35(7):2163–2174. doi:10.1002/eji.200425785
195. McGreal EP, Rosas M, Brown GD, Zamze S, Wong SYC, Gordon S, Martinez-Pomares L, Taylor PR (2006) The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16(5):422–430. doi:10.1093/glycob/cwj077
196. Robinson MJ, Osorio F, Rosas M, Freitas RP, Schweighoffer E, Gross O, SjefVerbeek J, Ruland J, Tybulewicz V, Brown GD, Moita LF, Taylor PR, Sousa CRE (2009) Dectin-2 is a Syk-coupled pattern recognition receptor crucial for Th17 responses to fungal infection. J Exp Med 206(9):2037–2051. doi:10.1084/jem.20082818
197. Bi L, Gojestani S, Wu W, Hsu YM, Zhu J, Ariizumi K, Lin X (2010) CARD9 mediates dectin-2-induced IkappaBalpha kinase ubiquitination leading to activation of NF-kappaB in response to stimulation by the hyphal form of Candida albicans. J Biol Chem 285(34):25969–25977. doi:10.1074/jbc.M110.131300
198. Saijo S, Ikeda S, Yamabe K, Kakuta S, Ishigame H, Akitsu A, Fujikado N, Kusaka T, Kubo S, Chung SH, Komatsu R, Miura N, Adachi Y, Ohno N, Shibuya K, Yamamoto N, Kawakami K, Yamasaki S, Saito T, Akira S, Iwakura Y (2010) Dectin-2 recognition of alpha-mannans and induction of th17 cell differentiation is essential for host defense against Candida albicans. Immunity 32(5):681–691. doi:10.1016/j.immuni.2010.05.001
199. Gringhuis SI, Wevers BA, Kaptein TM, van Capel TMM, Theelen B, Boekhout T, de Jong EC, Geijtenbeek TBH (2011) Selective C-Rel activation via Malt1 controls anti-fungal T-H-17 immunity by Dectin-1 and Dectin-2. PLoS Pathog. doi:10.1371/journal.ppat.1001259
200. Ishikawa T, Itoh F, Yoshida S, Saijo S, Matsuzawa T, Gonoi T, Saito T, Okawa Y, Shibata N, Miyamoto T, Yamasaki S (2013) Identification of distinct ligands for the C-type lectin receptors Mincle and Dectin-2 in the pathogenic fungus Malassezia. Cell Host Microbe 13(4):477–488. doi:10.1016/j.chom.2013.03.008
201. Gorjestani S, Yu M, Tang B, Zhang D, Wang D, Lin X (2011) Phospholipase Cgamma2 (PLCgamma2) is key component in Dectin-2 signaling pathway, mediating anti-fungal innate immune responses. J Biol Chem 286(51):43651–43659. doi:10.1074/jbc.M111.307389
202. Ritter M, Gross O, Kays S, Ruland J, Nimmerjahn F, Saijo S, Tschopp J, Layland LE, da Costa CP (2010) Schistosoma mansoni triggers Dectin-2, which activates the Nlrp3 inflammasome and alters adaptive immune responses. Proc Natl Acad Sci USA 107(47):20459–20464. doi:10.1073/pnas.1010337107
203. Barrett NA, Rahman OM, Fernandez JM, Parsons MW, Xing W, Austen KF, Kanaoka Y (2011) Dectin-2 mediates Th2 immunity through the generation of cysteinyl leukotrienes. J Exp Med 208(3):593–604. doi:10.1084/jem.20100793
204. Masumoto M, Tanaka T, Kaisho T, Sanjo H, Copeland NG, Gilbert DJ, Jenkins NA, Akira S (1999) A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J Immunol 163(9):5039–5048
205. Kerscher B, Willment JA, Brown GD (2013) The Dectin-2 family of C-type lectin-like receptors: an update. Int Immunol 25(5):271–277. doi:10.1093/intimm/dxt006
206. Lee RT, Hsu TL, Huang SK, Hsieh SL, Wong CH, Lee YC (2011) Survey of immune-related, mannose/fucose-binding C-type lectin receptors reveals widely divergent sugar-binding specificities. Glycobiology 21(4):512–520. doi:10.1093/glycob/cwq193
207. Yamasaki S, Ishikawa E, Sakuma M, Hara H, Ogata K, Saito T (2008) Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat Immunol 9(10):1179–1188. doi:10.1038/Ni.1651
208. Spargo BJ, Crowe LM, Ioneda T, Beaman BL, Crowe JH (1991) Cord factor (Alpha, Alpha-Trehalose 6,6′-Dimycolate) inhibits fusion between phospholipid-vesicles. Proc Natl Acad Sci USA 88(3):737–740. doi:10.1073/pnas.88.3.737
209. Indrigo J, Hunter RL, Actor JK (2002) Influence of trehalose 6,6 ‘-dimycolate (TDM) during mycobacterial infection of bone marrow macrophages. Microbiol-SGM 148:1991–1998
210. Indrigo J, Hunter RL, Actor JK (2003) Cord factor trehalose 6,6 ‘-dimycolate (TDM) mediates trafficking events during mycobacterial infection of murine macrophages. Microbiol-SGM 149:2049–2059. doi:10.1099/mic.0.26226-0
211. Hunter RL, Olsen M, Jagannath C, Actor JK (2006) Trehalose 6,6 ‘-dimycolate and lipid in the pathogenesis of caseating granulomas of tuberculosis in mice. Am J Pathol 168(4):1249–1261. doi:10.2353/ajpath.2006.050848
212. Axelrod S, Oschkinat H, Enders J, Schlegel B, Brinkmann V, Kaufmann SHE, Haas A, Schaible UE (2008) Delay of phagosome maturation by a mycobacterial lipid is reversed by nitric oxide. Cell Microbiol 10(7):1530–1545. doi:10.1111/j.1462-5822.2008.01147.x
213. Lee WB, Kang JS, Yan JJ, Lee MS, Jeon BY, Cho SN, Kim YJ (2012) Neutrophils promote mycobacterial trehalose dimycolate-induced lung inflammation via the mincle pathway. PLoS Pathog. doi:10.1371/journal.ppat.1002614
214. Heitmann L, Schoenen H, Ehlers S, Lang R, Holscher C (2013) Mincle is not essential for controlling Mycobacterium tuberculosis infection. Immunobiology 218(4):506–516. doi:10.1016/j.imbio.2012.06.005
215. Behler F, Steinwede K, Balboa L, Ueberberg B, Maus R, Kirchhof G, Yamasaki S, Welte T, Maus UA (2012) Role of Mincle in alveolar macrophage-dependent innate immunity against mycobacterial infections in mice. J Immunol 189(6):3121–3129. doi:10.4049/jimmunol.1201399
216. Behler F, Maus R, Bohling J, Knippenberg S, Kirchhof G, Nagata M, Jonigk D, Izykowski N, Magel L, Welte T, Yamasaki S, Maus UA (2015) Macrophage-inducible C-type lectin Mincle-expressing dendritic cells contribute to control of splenic Mycobacterium bovis BCG infection in mice. Infect Immun 83(1):184–196. doi:10.1128/IAI.02500-14
217. Desel C, Werninghaus K, Ritter M, Jozefowski K, Wenzel J, Russkamp N, Schleicher U, Christensen D, Wirtz S, Kirschning C, Agger EM, da Costa CP, Lang R (2013) The Mincle-activating adjuvant TDB induces MyD88-dependent Th1 and Th17 responses through IL-1R signaling. PLoS One. doi:10.1371/journal.pone.0053531
218. Schweneker K, Gorka O, Schweneker M, Poeck H, Tschopp J, Peschel C, Ruland J, Gross O (2013) The mycobacterial cord factor adjuvant analogue trehalose-6,6 ‘-dibehenate (TDB) activates the Nlrp3 inflammasome. Immunobiology 218(4):664–673. doi:10.1016/j.imbio.2012.07.029
219. Shenderov K, Barber DL, Mayer-Barber KD, Gurcha SS, Jankovic D, Feng CG, Oland S, Hieny S, Caspar P, Yamasaki S, Lin X, Ting JPY, Trinchieri G, Besra GS, Cerundolo V, Sher A (2013) Cord factor and peptidoglycan recapitulate the Th17-promoting adjuvant activity of mycobacteria through mincle/CARD9 signaling and the inflammasome. J Immunol 190(11):5722–5730. doi:10.4049/jimmunol.1203343
220. Lee WB, Kang JS, Choi WY, Zhang Q, Kim CH, Choi UY, Kim-Ha J, Kim YJ (2016) Mincle-mediated translational regulation is required for strong nitric oxide production and inflammation resolution. Nat Commun. doi:10.1038/ncomms11322
221. Schoenen H, Huber A, Sonda N, Zimmermann S, Jantsch J, Lepenies B, Bronte V, Lang R (2014) Differential control of mincle-dependent cord factor recognition and macrophage responses by the transcription factors C/EBPbeta and HIF1alpha. J Immunol 193(7):3664–3675. doi:10.4049/jimmunol.1301593
222. Kerscher B, Dambuza IM, Christofi M, Reid DM, Yamasaki S, Willment JA, Brown GD (2016) Signalling through MyD88 drives surface expression of the mycobacterial receptors MCL (Clecsf8, Clec4d) and Mincle (Clec4e) following microbial stimulation. Microbes Infect 18(7–8):505–509. doi:10.1016/j.micinf.2016.03.007
223. Ostrop J, Jozefowski K, Zimmermann S, Hofmann K, Strasser E, Lepenies B, Lang R (2015) Contribution of MINCLE-SYK signaling to activation of primary human APCs by mycobacterial cord factor and the novel adjuvant TDB. J Immunol 195(5):2417–2428. doi:10.4049/jimmunol.1500102
224. Rambaruth NDS, Jegouzo SAF, Marlor H, Taylor ME, Drickamer K (2015) Mouse mincle: characterization as a model for human mincle and evolutionary implications. Molecules 20(4):6670–6682. doi:10.3390/molecules20046670
225. Richardson MB, Torigoe S, Yamasaki S, Williams SJ (2015) Mycobacterium tuberculosis beta-gentiobiosyl diacylglycerides signal through the pattern recognition receptor Mincle: total synthesis and structure activity relationships. Chem Commun 51(81):15027–15030. doi:10.1039/c5cc04773k
226. van der Peet PL, Gunawan C, Torigoe S, Yamasaki S, Williams SJ (2015) Corynomycolic acid-containing glycolipids signal through the pattern recognition receptor Mincle. Chem Commun 51(24):5100–5103. doi:10.1039/c5cc00085h
227. Patin EC, Willcocks S, Orr S, Ward TH, Lang R, Schaible UE (2016) Mincle-mediated anti-inflammatory IL-10 response counter-regulates IL-12 in vitro. Innate Immun. doi:10.1177/1753425916636671
228. Kiyotake R, Oh-hora M, Ishikawa E, Miyamoto T, Ishibashi T, Yamasaki S (2015) Human mincle binds to cholesterol crystals and triggers innate immune responses. J Biol Chem 290(42):25322–25332. doi:10.1074/jbc.M115.645234
229. Bowker N, Salie M, Schurz H, van Helden PD, Kinnear CJ, Hoal EG, Moller M (2016) Polymorphisms in the pattern recognition receptor Mincle gene (CLEC4E) and association with tuberculosis. Lung. doi:10.1007/s00408-016-9915-y
230. Balch SG, McKnight AJ, Seldin MF, Gordon S (1998) Cloning of a novel C-type lectin expressed by murine macrophages. J Biol Chem 273(29):18656–18664
231. Arce I, Martinez-Munoz L, Roda-Navarro P, Fernandez-Ruiz E (2004) The human C-type lectin CLECSF8 is a novel monocyte/macrophage endocytic receptor. Eur J Immunol 34(1):210–220. doi:10.1002/eji.200324230
232. Miyake Y, Toyonaga K, Mori D, Kakuta S, Hoshino Y, Oyamada A, Yamada H, Ono KI, Suyama M, Iwakura Y, Yoshikai Y, Yamasaki S (2013) C-type lectin MCL is an FcR gamma-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38(5):1050–1062. doi:10.1016/j.immuni.2013.03.010
233. Graham LM, Gupta V, Schafer G, Reid DM, Kimberg M, Dennehy KM, Hornsell WG, Guler R, Campanero-Rhodes MA, Palma AS, Feizi T, Kim SK, Sobieszczuk P, Willment JA, Brown GD (2012) The C-type lectin receptor CLECSF8 (CLEC4D) is expressed by myeloid cells and triggers cellular activation through syk kinase. J Biol Chem 287(31):25964–25974. doi:10.1074/jbc.M112.384164
234. Lobato-Pascual A, Saether PC, Fossum S, Dissen E, Daws MR (2013) Mincle, the receptor for mycobacterial cord factor, forms a functional receptor complex with MCL and Fc epsilon RI-gamma. Eur J Immunol 43(12):3167–3174. doi:10.1002/eji.201343752
235. Miyake Y, Masatsugu OH, Yamasaki S (2015) C-type lectin receptor MCL facilitates mincle expression and signaling through complex formation. J Immunol 194(11):5366–5374. doi:10.4049/jimmunol.1402429
236. Kerscher B, Wilson GJ, Reid DM, Mori D, Taylor JA, Besra GS, Yamasaki S, Willment JA, Brown GD (2015) The mycobacterial receptor, Clec4d (CLECSF8, MCL) is co-regulated with Mincle and upregulated on mouse myeloid cells following microbial challenge. Eur J Immunol. doi:10.1002/eji.201545858
237. Arnaout MA (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75(5):1037–1050
238. Velasco-Velazquez MA, Barrera D, Gonzalez-Arenas A, Rosales C, Agramonte-Hevia J (2003) Macrophage–Mycobacterium tuberculosis interactions: role of complement receptor 3. Microb Pathog 35(3):125–131
239. Ehlers MRW, Daffe M (1998) Interactions between Mycobacterium tuberculosis and host cells: are mycobacterial sugars the key? Trends Microbiol 6(8):328–335. doi:10.1016/S0966-842x(98)01301-8
240. Villeneuve C, Gilleron M, Maridonneau-Parini I, Daffe M, Astarie-Dequeker C, Etienne G (2005) Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process. J Lipid Res 46(3):475–483. doi:10.1194/jlr.M400308-JLR200
241. Le Cabec V, Carreno S, Moisand A, Bordier C, Maridonneau-Parini I (2002) Complement receptor 3 (CD11b/CD18) mediates type I and type II phagocytosis during nonopsonic and opsonic phagocytosis, respectively. J Immunol 169(4):2003–2009
242. Yassin RJ, Hamblin AS (1994) Altered expression of CD11/CD18 on the peripheral blood phagocytes of patients with tuberculosis. Clin Exp Immunol 97(1):120–125
243. Juffermans NP, Dekkers PE, Verbon A, Speelman P, van Deventer SJ, van der Poll T (2001) Concurrent upregulation of urokinase plasminogen activator receptor and CD11b during tuberculosis and experimental endotoxemia. Infect Immun 69(8):5182–5185. doi:10.1128/IAI.69.8.5182-5185.2001
244. Kuo HP, Ho TC, Wang CH, Yu CT, Lin HC (1996) Increased production of hydrogen peroxide and expression of CD11b/CD18 on alveolar macrophages in patients with active pulmonary tuberculosis. Tuber Lung Dis 77(5):468–475
245. Watford WT, Ghio AJ, Wright JR (2000) Complement-mediated host defense in the lung. Am J Physiol-Lung C 279(5):L790–L798
246. Ferguson JS, Weis JJ, Martin JL, Schlesinger LS (2004) Complement protein c3 binding to Mycobacterium tuberculosis is initiated by the classical pathway in human bronchoalveolar lavage fluid. Infect Immun 72(5):2564–2573. doi:10.1128/Iai.72.5.2564-2573.2004
247. Hu C, Mayadas-Norton T, Tanaka K, Chan J, Salgame P (2000) Mycobacterium tuberculosis infection in complement receptor 3-deficient mice. J Immunol 165(5):2596–2602
248. Rooyakkers AWJ, Stokes RW (2005) Absence of complement receptor 3 results in reduced binding and ingestion of Mycobacterium tuberculosis but has no significant effect on the induction of reactive oxygen and nitrogen intermediates or on the survival of the bacteria in resident and interferon-gamma activated macrophages. Microb Pathog 39(3):57–67. doi:10.1016/j.micpath.2005.05.001
249. Carlson TK, Torrelles JB, Smith K, Horlacher T, Castelli R, Seeberger PH, Crouch EC, Schlesinger LS (2009) Critical role of amino acid position 343 of surfactant protein-D in the selective binding of glycolipids from Mycobacterium tuberculosis. Glycobiology 19(12):1473–1484. doi:10.1093/glycob/cwp122
250. Matsunaga I, Moody DB (2009) Mincle is a long sought receptor for mycobacterial cord factor. J Exp Med 206(13):2865–2868. doi:10.1084/jem.20092533
251. Hattori Y, Morita D, Fujiwara N, Mori D, Nakamura T, Harashima H, Yamasaki S, Sugita M (2014) Glycerol monomycolate is a novel ligand for the human, but not mouse macrophage inducible C-type lectin, Mincle. J Biol Chem 289(22):15405–15412. doi:10.1074/jbc.M114.566489
252. Hetland G, Wiker HG (1994) Antigen 85C on Mycobacterium bovis, BCG and M. tuberculosis promotes monocyte-CR3-mediated uptake of microbeads coated with mycobacterial products. Immunology 82(3):445–449
253. Selvaraj P, Jawahar MS, Rajeswari DN, Alagarasu K, Vidyarani M, Narayanan PR (2006) Role of mannose binding lectin gene variants on its protein levels and macrophage phagocytosis with live Mycobacterium tuberculosis in pulmonary tuberculosis. FEMS Immunol Med Microbiol 46(3):433–437. doi:10.1111/j.1574-695X.2006.00053.x
254. Naderi M, Hashemi M, Taheri M, Pesarakli H, Eskandari-Nasab E, Bahari G (2014) CD209 promoter-336 A/G (rs4804803) polymorphism is associated with susceptibility to pulmonary tuberculosis in Zahedan, southeast Iran. J Microbiol Immunol 47(3):171–175. doi:10.1016/j.jmii.2013.03.013
255. Vannberg FO, Chapman SJ, Khor CC, Tosh K, Floyd S, Jackson-Sillah D, Crampin A, Sichali L, Bah B, Gustafson P, Aaby P, McAdam KP, Bah-Sow O, Lienhardt C, Sirugo G, Fine P, Hill AV (2008) CD209 genetic polymorphism and tuberculosis disease. PLoS One 3(1):e1388. doi:10.1371/journal.pone.0001388
256. Gomez LM, Anaya JM, Sierra-Filardi E, Cadena J, Corbi A, Martin J (2006) Analysis of DC-SIGN (CD209) functional variants in patients with tuberculosis. Hum Immunol 67(10):808–811. doi:10.1016/j.humimm.2006.07.003
257. Ben-Ali M, Barreiro LB, Chabbou A, Haltiti R, Braham E, Neyrolles O, Dellagi K, Gicquel B, Quintana-Murci L, Barbouche MR (2007) Promoter and neck region length variation of DC-SIGN is not associated with susceptibility to tuberculosis in Tunisian patients. Hum Immunol 68(11):908–912. doi:10.1016/j.humimm.2007.09.003
258. Selvaraj P, Alagarasu K, Swaminathan S, Harishankar M, Narendran G (2009) CD209 gene polymorphisms in South Indian HIV and HIV-TB patients. Infect Genet Evol 9(2):256–262. doi:10.1016/j.meegid.2008.12.003
259. Zheng RJ, Zhou Y, Qin LH, Jin RL, Wang J, Lu JM, Wang WB, Tang SJ, Hu ZY (2011) Relationship between polymorphism of DC-SIGN (CD209) gene and the susceptibility to pulmonary tuberculosis in an eastern Chinese population. Hum Immunol 72(2):183–186. doi:10.1016/j.humimm.2010.11.004
260. Olesen R, Wejse C, Velez DR, Bisseye C, Sodemann M, Aaby P, Rabna P, Worwui A, Chapman H, Diatta M, Adegbola RA, Hill PC, Ostergaard L, Williams SM, Sirugo G (2007) DC-SIGN (CD209), pentraxin 3 and vitamin D receptor gene variants associate with pulmonary tuberculosis risk in West Africans. Genes Immun 8(6):456–467. doi:10.1038/sj.gene.6364410
261. Sadki K, Lamsyah H, Rueda B, Lahlou O, El Aouad R, Martin J (2009) CD209 promoter single nucleotide polymorphism-336A/G and the risk of susceptibility to tuberculosis disease in the moroccan population. Int J Hum Genet 9(3–4):239–243
262. Kobayashi K, Yuliwulandari R, Yanai H, Lien LT, Hang NT, Hijikata M, Keicho N, Tokunaga K (2011) Association of CD209 polymorphisms with tuberculosis in an Indonesian population. Hum Immunol 72(9):741–745. doi:10.1016/j.humimm.2011.04.004