Skip to main content

Advertisement

Log in

C-type lectin receptors in tuberculosis: what we know

Medical Microbiology and Immunology Aims and scope Submit manuscript

Abstract

Mycobacterium tuberculosis (Mtb), the etiologic agent of tuberculosis (TB), is recognized by a number of pathogen recognition receptors (PRRs), either soluble or predominantly expressed on the surface of various cells of innate and adaptive immunity. C-type lectin receptors (CTLRs) are a class of PRRs which can recognize a variety of endogenous and exogenous ligands, thereby playing a crucial role in immunity, as well as in maintaining homeostasis. Mtb surface ligands, including mannose-capped lipoarabinomannan and cord factor, are important immune modulators which recently have been found to be directly recognized by several CTLRs. Receptor ligation is followed by cellular activation, mainly via nuclear factor κB mediated by a series of adaptors with subsequent expression of pro-inflammatory cytokines. Mtb recognition by CTLRs and their cross talk with other PRRs on immune cells is of key importance for the better understanding of the Mtb-induced complexity of the host immune responses. Epidemiological studies have shown that single nucleotide polymorphisms (SNPs) in several PRRs, as well as the adaptors in their signaling cascades, are directly involved in the susceptibility for developing disease and the disease outcome. In addition, an increasing number of CTLRs have been studied for their functional effects in the pathogenesis of TB. This review summarizes current knowledge regarding the various roles played by different CTLRs in TB, as well as the role of their SNPs associated with disease susceptibility and outcome in different human populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  7. Brennan PJ, Nikaido H (1995) The envelope of mycobacteria. Annu Rev Biochem 64:29–63. doi:10.1146/annurev.bi.64.070195.000333

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  28. Drickamer K (1999) C-type lectin-like domains. Curr Opin Struct Biol 9(5):585–590

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Google Scholar 

  48. Watford WT, Wright JR, Hester CG, Jiang H, Frank MM (2001) Surfactant protein A regulates complement activation. J Immunol 167(11):6593–6600

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  87. Turner MW (1996) Mannose-binding lectin: the pluripotent molecule of the innate immune system. Immunol Today 17(11):532–540

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  121. Martinez-Pomares L (2012) The mannose receptor. J Leukoc Biol 92(6):1177–1186. doi:10.1189/jlb.0512231

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  173. Brown GD (2006) Dectin-1: a signalling non-TLR pattern-recognition receptor. Nat Rev Immunol 6(1):33–43. doi:10.1038/nri1745

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  CAS  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    Article  CAS  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    PubMed  PubMed Central  Google Scholar 

  237. Arnaout MA (1990) Structure and function of the leukocyte adhesion molecules CD11/CD18. Blood 75(5):1037–1050

    CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  245. Watford WT, Ghio AJ, Wright JR (2000) Complement-mediated host defense in the lung. Am J Physiol-Lung C 279(5):L790–L798

    CAS  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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

    CAS  PubMed  PubMed Central  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This study was supported by the Deutsche Forschungsgemeinschaft (DFG) International Graduate School (IRTG) GRK1673 and by the Federal Ministry for Education and Science (Grant BMBF 03Z2JN22) to HS.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hortense Slevogt.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Goyal, S., Klassert, T.E. & Slevogt, H. C-type lectin receptors in tuberculosis: what we know. Med Microbiol Immunol 205, 513–535 (2016). https://doi.org/10.1007/s00430-016-0470-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00430-016-0470-1

Keywords

Navigation