C-Type Lectin Receptor DCAR Recognizes Mycobacterial Phosphatidyl-Inositol Mannosides to Promote a Th1 Response during Infection

Immunity

Volumn 45, Issue 6, 2016, Pages 1245-1257

  Toyonaga, Kenji ^a   Torigoe, Shota ^a   Motomura, Yoshitomo ^b   Kamichi, Takane ^a,b   Hayashi, Jennifer M ^c   Morita, Yasu S ^c   Noguchi, Naoto ^a   Chuma, Yasushi ^d   Kiyohara, Hideyasu ^d   Matsuo, Kazuhiro ^d   Tanaka, Hiroshi ^e   Nakagawa, Yoshiko ^f   Sakuma, Tetsushi ^g   Ohmuraya, Masaki ^f   Yamamoto, Takashi ^g   Umemura, Masayuki ^h   Matsuzaki, Goro ^h   Yoshikai, Yasunobu ^a   Yano, Ikuya ^d   Miyamoto, Tomofumi ^a   Yamasaki, Sho ^a,i   more..

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d Kiyose   (Japan)

^e TOKYO INSTITUTE OF TECHNOLOGY   (Japan)

^f KUMAMOTO UNIVERSITY   (Japan)

^g HIROSHIMA UNIVERSITY   (Japan)

^h UNIVERSITY OF THE RYUKYUS   (Japan)

ⁱ CHIBA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD64 ANTIGEN; DENDRITIC CELL IMMUNOACTIVATING RECEPTOR; FC RECEPTOR; GAMMA INTERFERON; GLYCOLIPID; GLYCOPROTEIN P 15095; INTERLEUKIN 12P40; INTERLEUKIN 6; LECTIN RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 2; MANNOSIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; DENDRITIC CELL IMMUNOACTIVATING RECEPTOR, MOUSE; IMMUNOGLOBULIN RECEPTOR; LECTIN; PHOSPHATIDYLINOSITOL MANNOSIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL LOAD; BACTERIAL VIRULENCE; CONTROLLED STUDY; CYTOKINE PRODUCTION; IMMUNOSTIMULATION; INFLAMMATORY CELL; INNATE IMMUNITY; INTERFERON PRODUCTION; LUNG ALVEOLUS CELL; MOLECULAR RECOGNITION; MONOCYTE; MONOCYTE DERIVED INFLAMMATORY CELL; MOUSE; MYCOBACTERIOSIS; MYCOBACTERIUM BOVIS BCG; MYCOBACTERIUM SMEGMATIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PERITONEUM MACROPHAGE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPLEEN CELL; TH1 CELL; ANIMAL; C57BL MOUSE; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; MYCOBACTERIUM;

ANIMALS; BACTERIAL PROTEINS; LECTINS, C-TYPE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYCOBACTERIUM; MYCOBACTERIUM INFECTIONS; PHOSPHATIDYLINOSITOLS; RECEPTORS, IMMUNOLOGIC; TH1 CELLS;

EID: 85006823504     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.10.012     Document Type: Article

References (75)

1. Ainge, G.D., Parlane, N.A., Denis, M., Hayman, C.M., Larsen, D.S., Painter, G.F., Phosphatidylinositol mannosides: synthesis and adjuvant properties of phosphatidylinositol di- and tetramannosides. Bioorg. Med. Chem. 14 (2006), 7615–7624.
2. Apostolou, I., Takahama, Y., Belmant, C., Kawano, T., Huerre, M., Marchal, G., Cui, J., Taniguchi, M., Nakauchi, H., Fournié, J.J., et al. Murine natural killer T(NKT) cells [correction of natural killer cells] contribute to the granulomatous reaction caused by mycobacterial cell walls. Proc. Natl. Acad. Sci. USA 96 (1999), 5141–5146.
3. Bansal, K., Kapoor, N., Narayana, Y., Puzo, G., Gilleron, M., Balaji, K.N., PIM2 Induced COX-2 and MMP-9 expression in macrophages requires PI3K and Notch1 signaling. PLoS ONE, 4, 2009, e4911.
4. Bansal-Mutalik, R., Nikaido, H., Quantitative lipid composition of cell envelopes of Corynebacterium glutamicum elucidated through reverse micelle extraction. Proc. Natl. Acad. Sci. USA 108 (2011), 15360–15365.
5. Behler, F., Steinwede, K., Balboa, L., Ueberberg, B., Maus, R., Kirchhof, G., Yamasaki, S., Welte, T., Maus, U.A., Role of Mincle in alveolar macrophage-dependent innate immunity against mycobacterial infections in mice. J. Immunol. 189 (2012), 3121–3129.
6. Boonyarattanakalin, S., Liu, X., Michieletti, M., Lepenies, B., Seeberger, P.H., Chemical synthesis of all phosphatidylinositol mannoside (PIM) glycans from Mycobacterium tuberculosis. J. Am. Chem. Soc. 130 (2008), 16791–16799.
7. Cain, D.W., O'Koren, E.G., Kan, M.J., Womble, M., Sempowski, G.D., Hopper, K., Gunn, M.D., Kelsoe, G., Identification of a tissue-specific, C/EBPβ-dependent pathway of differentiation for murine peritoneal macrophages. J. Immunol. 191 (2013), 4665–4675.
8. Chow, K.V., Lew, A.M., Sutherland, R.M., Zhan, Y., Monocyte-derived dendritic cells promote Th polarization, whereas conventional dendritic cells promote Th proliferation. J. Immunol. 196 (2016), 624–636.
9. Cooper, A.M., Cell-mediated immune responses in tuberculosis. Annu. Rev. Immunol. 27 (2009), 393–422.
10. Court, N., Rose, S., Bourigault, M.L., Front, S., Martin, O.R., Dowling, J.K., Kenny, E.F., O'Neill, L., Erard, F., Quesniaux, V.F., Mycobacterial PIMs inhibit host inflammatory responses through CD14-dependent and CD14-independent mechanisms. PLoS ONE, 6, 2011, e24631.
11. Dorhoi, A., Desel, C., Yeremeev, V., Pradl, L., Brinkmann, V., Mollenkopf, H.J., Hanke, K., Gross, O., Ruland, J., Kaufmann, S.H., The adaptor molecule CARD9 is essential for tuberculosis control. J. Exp. Med. 207 (2010), 777–792.
12. Doz, E., Rose, S., Court, N., Front, S., Vasseur, V., Charron, S., Gilleron, M., Puzo, G., Fremaux, I., Delneste, Y., et al. Mycobacterial phosphatidylinositol mannosides negatively regulate host Toll-like receptor 4, MyD88-dependent proinflammatory cytokines, and TRIF-dependent co-stimulatory molecule expression. J. Biol. Chem. 284 (2009), 23187–23196.
13. Driessen, N.N., Ummels, R., Maaskant, J.J., Gurcha, S.S., Besra, G.S., Ainge, G.D., Larsen, D.S., Painter, G.F., Vandenbroucke-Grauls, C.M., Geurtsen, J., Appelmelk, B.J., Role of phosphatidylinositol mannosides in the interaction between mycobacteria and DC-SIGN. Infect. Immun. 77 (2009), 4538–4547.
14. Fischer, K., Scotet, E., Niemeyer, M., Koebernick, H., Zerrahn, J., Maillet, S., Hurwitz, R., Kursar, M., Bonneville, M., Kaufmann, S.H., Schaible, U.E., Mycobacterial phosphatidylinositol mannoside is a natural antigen for CD1d-restricted T cells. Proc. Natl. Acad. Sci. USA 101 (2004), 10685–10690.
15. Flornes, L.M., Bryceson, Y.T., Spurkland, A., Lorentzen, J.C., Dissen, E., Fossum, S., Identification of lectin-like receptors expressed by antigen presenting cells and neutrophils and their mapping to a novel gene complex. Immunogenetics 56 (2004), 506–517.
16. Ghosn, E.E., Cassado, A.A., Govoni, G.R., Fukuhara, T., Yang, Y., Monack, D.M., Bortoluci, K.R., Almeida, S.R., Herzenberg, L.A., Herzenberg, L.A., Two physically, functionally, and developmentally distinct peritoneal macrophage subsets. Proc. Natl. Acad. Sci. USA 107 (2010), 2568–2573.
17. Gilleron, M., Nigou, J., Cahuzac, B., Puzo, G., Structural study of the lipomannans from Mycobacterium bovis BCG: characterisation of multiacylated forms of the phosphatidyl-myo-inositol anchor. J. Mol. Biol. 285 (1999), 2147–2160.
18. Gilleron, M., Ronet, C., Mempel, M., Monsarrat, B., Gachelin, G., Puzo, G., Acylation state of the phosphatidylinositol mannosides from Mycobacterium bovis bacillus Calmette Guérin and ability to induce granuloma and recruit natural killer T cells. J. Biol. Chem. 276 (2001), 34896–34904.
19. Gilleron, M., Quesniaux, V.F., Puzo, G., Acylation state of the phosphatidylinositol hexamannosides from Mycobacterium bovis bacillus Calmette Guerin and mycobacterium tuberculosis H37Rv and its implication in Toll-like receptor response. J. Biol. Chem. 278 (2003), 29880–29889.
20. Gonzalez-Juarrero, M., Shim, T.S., Kipnis, A., Junqueira-Kipnis, A.P., Orme, I.M., Dynamics of macrophage cell populations during murine pulmonary tuberculosis. J. Immunol. 171 (2003), 3128–3135.
21. Guerin, M.E., Korduláková, J., Alzari, P.M., Brennan, P.J., Jackson, M., Molecular basis of phosphatidyl-myo-inositol mannoside biosynthesis and regulation in mycobacteria. J. Biol. Chem. 285 (2010), 33577–33583.
22. Guilliams, M., De Kleer, I., Henri, S., Post, S., Vanhoutte, L., De Prijck, S., Deswarte, K., Malissen, B., Hammad, H., Lambrecht, B.N., Alveolar macrophages develop from fetal monocytes that differentiate into long-lived cells in the first week of life via GM-CSF. J. Exp. Med. 210 (2013), 1977–1992.
23. Guo, J.P., Verdrengh, M., Tarkowski, A., Lange, S., Jennische, E., Lorentzen, J.C., Harris, R.A., The rat antigen-presenting lectin-like receptor complex influences innate immunity and development of infectious diseases. Genes Immun. 10 (2009), 227–236.
24. Haites, R.E., Morita, Y.S., McConville, M.J., Billman-Jacobe, H., Function of phosphatidylinositol in mycobacteria. J. Biol. Chem. 280 (2005), 10981–10987.
25. Hanashima, S., Götze, S., Liu, Y., Ikeda, A., Kojima-Aikawa, K., Taniguchi, N., Varón Silva, D., Feizi, T., Seeberger, P.H., Yamaguchi, Y., Defining the interaction of human soluble lectin ZG16p and mycobacterial phosphatidylinositol mannosides. ChemBioChem 16 (2015), 1502–1511.
26. Hattori, Y., Morita, D., Fujiwara, N., Mori, D., Nakamura, T., Harashima, H., Yamasaki, S., Sugita, M., Glycerol monomycolate is a novel ligand for the human, but not mouse macrophage inducible C-type lectin, Mincle. J. Biol. Chem. 289 (2014), 15405–15412.
27. Heitmann, L., Schoenen, H., Ehlers, S., Lang, R., Hölscher, C., Mincle is not essential for controlling Mycobacterium tuberculosis infection. Immunobiology 218 (2013), 506–516.
28. Ishikawa, E., Ishikawa, T., Morita, Y.S., Toyonaga, K., Yamada, H., Takeuchi, O., Kinoshita, T., Akira, S., Yoshikai, Y., Yamasaki, S., Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J. Exp. Med. 206 (2009), 2879–2888.
29. Ito, T., Hasegawa, A., Hosokawa, H., Yamashita, M., Motohashi, S., Naka, T., Okamoto, Y., Fujita, Y., Ishii, Y., Taniguchi, M., et al. Human Th1 differentiation induced by lipoarabinomannan/lipomannan from Mycobacterium bovis BCG Tokyo-172. Int. Immunol. 20 (2008), 849–860.
30. Jones, B.W., Heldwein, K.A., Means, T.K., Saukkonen, J.J., Fenton, M.J., Differential roles of Toll-like receptors in the elicitation of proinflammatory responses by macrophages. Ann. Rheum. Dis. 60:Suppl 3 (2001), iii6–iii12.
31. Kanazawa, N., Dendritic cell immunoreceptors: C-type lectin receptors for pattern-recognition and signaling on antigen-presenting cells. J. Dermatol. Sci. 45 (2007), 77–86.
32. Kanazawa, N., Tashiro, K., Inaba, K., Miyachi, Y., Dendritic cell immunoactivating receptor, a novel C-type lectin immunoreceptor, acts as an activating receptor through association with Fc receptor gamma chain. J. Biol. Chem. 278 (2003), 32645–32652.
33. Layre, E., Collmann, A., Bastian, M., Mariotti, S., Czaplicki, J., Prandi, J., Mori, L., Stenger, S., De Libero, G., Puzo, G., Gilleron, M., Mycolic acids constitute a scaffold for mycobacterial lipid antigens stimulating CD1-restricted T cells. Chem. Biol. 16 (2009), 82–92.
34. Layre, E., Sweet, L., Hong, S., Madigan, C.A., Desjardins, D., Young, D.C., Cheng, T.Y., Annand, J.W., Kim, K., Shamputa, I.C., et al. A comparative lipidomics platform for chemotaxonomic analysis of Mycobacterium tuberculosis. Chem. Biol. 18 (2011), 1537–1549.
35. Lee, W.B., Kang, J.S., Yan, J.J., Lee, M.S., Jeon, B.Y., Cho, S.N., Kim, Y.J., Neutrophils promote mycobacterial trehalose dimycolate-induced lung inflammation via the mincle pathway. PLoS Pathog., 8, 2012, e1002614.
36. León, B., López-Bravo, M., Ardavín, C., Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26 (2007), 519–531.
37. McCarthy, T.R., Torrelles, J.B., MacFarlane, A.S., Katawczik, M., Kutzbach, B., Desjardin, L.E., Clegg, S., Goldberg, J.B., Schlesinger, L.S., Overexpression of Mycobacterium tuberculosis manB, a phosphomannomutase that increases phosphatidylinositol mannoside biosynthesis in Mycobacterium smegmatis and mycobacterial association with human macrophages. Mol. Microbiol. 58 (2005), 774–790.
38. Miyake, Y., Toyonaga, K., Mori, D., Kakuta, S., Hoshino, Y., Oyamada, A., Yamada, H., Ono, K., Suyama, M., Iwakura, Y., et al. C-type lectin MCL is an FcRγ-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38 (2013), 1050–1062.
39. Miyake, Y., Masatsugu, O.H., Yamasaki, S., C-type lectin receptor MCL facilitates Mincle expression and signaling through complex formation. J. Immunol. 194 (2015), 5366–5374.
40. Morita, Y.S., Sena, C.B., Waller, R.F., Kurokawa, K., Sernee, M.F., Nakatani, F., Haites, R.E., Billman-Jacobe, H., McConville, M.J., Maeda, Y., Kinoshita, T., PimE is a polyprenol-phosphate-mannose-dependent mannosyltransferase that transfers the fifth mannose of phosphatidylinositol mannoside in mycobacteria. J. Biol. Chem. 281 (2006), 25143–25155.
41. Movahedzadeh, F., Smith, D.A., Norman, R.A., Dinadayala, P., Murray-Rust, J., Russell, D.G., Kendall, S.L., Rison, S.C., McAlister, M.S., Bancroft, G.J., et al. The Mycobacterium tuberculosis ino1 gene is essential for growth and virulence. Mol. Microbiol. 51 (2004), 1003–1014.
42. Murray, P.J., Wynn, T.A., Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 11 (2011), 723–737.
43. Nakagawa, Y., Sakuma, T., Nakagata, N., Yamasaki, S., Takeda, N., Ohmuraya, M., Yamamoto, T., Application of oocyte cryopreservation technology in TALEN-mediated mouse genome editing. Exp. Anim. 63 (2014), 349–355.
44. Nigou, J., Gilleron, M., Puzo, G., Lipoarabinomannans: from structure to biosynthesis. Biochimie 85 (2003), 153–166.
45. Nigou, J., Vasselon, T., Ray, A., Constant, P., Gilleron, M., Besra, G.S., Sutcliffe, I., Tiraby, G., Puzo, G., Mannan chain length controls lipoglycans signaling via and binding to TLR2. J. Immunol. 180 (2008), 6696–6702.
46. Ohira, S., Yamaguchi, Y., Takahashi, T., Tanaka, H., Synthesis of a phosphatidylinositol dimannoside using 2-(azidomethyl)benzoate mannosyl donors. Heterocycles 89 (2014), 763–774.
47. Okabe, Y., Medzhitov, R., Tissue-specific signals control reversible program of localization and functional polarization of macrophages. Cell 157 (2014), 832–844.
48. Park, S.Y., Ueda, S., Ohno, H., Hamano, Y., Tanaka, M., Shiratori, T., Yamazaki, T., Arase, H., Arase, N., Karasawa, A., et al. Resistance of Fc receptor- deficient mice to fatal glomerulonephritis. J. Clin. Invest. 102 (1998), 1229–1238.
49. Parlane, N.A., Compton, B.J., Hayman, C.M., Painter, G.F., Basaraba, R.J., Heiser, A., Buddle, B.M., Phosphatidylinositol di-mannoside and derivates modulate the immune response to and efficacy of a tuberculosis protein vaccine against Mycobacterium bovis infection. Vaccine 30 (2012), 580–588.
50. Patil, P.S., Cheng, T.J., Zulueta, M.M., Yang, S.T., Lico, L.S., Hung, S.C., Total synthesis of tetraacylated phosphatidylinositol hexamannoside and evaluation of its immunomodulatory activity. Nat. Commun., 6, 2015, 7239.
51. Peters, W., Scott, H.M., Chambers, H.F., Flynn, J.L., Charo, I.F., Ernst, J.D., Chemokine receptor 2 serves an early and essential role in resistance to Mycobacterium tuberculosis. Proc. Natl. Acad. Sci. USA 98 (2001), 7958–7963.
52. Rocha-Ramírez, L.M., Estrada-García, I., López-Marín, L.M., Segura-Salinas, E., Méndez-Aragón, P., Van Soolingen, D., Torres-González, R., Chacón-Salinas, R., Estrada-Parra, S., Maldonado-Bernal, C., et al. Mycobacterium tuberculosis lipids regulate cytokines, TLR-2/4 and MHC class II expression in human macrophages. Tuberculosis (Edinb.) 88 (2008), 212–220.
53. Rosas, M., Davies, L.C., Giles, P.J., Liao, C.T., Kharfan, B., Stone, T.C., O'Donnell, V.B., Fraser, D.J., Jones, S.A., Taylor, P.R., The transcription factor Gata6 links tissue macrophage phenotype and proliferative renewal. Science 344 (2014), 645–648.
54. Rose, S., Misharin, A., Perlman, H., A novel Ly6C/Ly6G-based strategy to analyze the mouse splenic myeloid compartment. Cytometry A 81 (2012), 343–350.
55. Saito, K., Yajima, T., Kumabe, S., Doi, T., Yamada, H., Sad, S., Shen, H., Yoshikai, Y., Impaired protection against Mycobacterium bovis bacillus Calmette-Guerin infection in IL-15-deficient mice. J. Immunol. 176 (2006), 2496–2504.
56. Sakuma, T., Ochiai, H., Kaneko, T., Mashimo, T., Tokumasu, D., Sakane, Y., Suzuki, K., Miyamoto, T., Sakamoto, N., Matsuura, S., Yamamoto, T., Repeating pattern of non-RVD variations in DNA-binding modules enhances TALEN activity. Sci. Rep., 3, 2013, 3379.
57. Sancho, D., Reis e Sousa, C., Signaling by myeloid C-type lectin receptors in immunity and homeostasis. Annu. Rev. Immunol. 30 (2012), 491–529.
58. Schlame, M., Brody, S., Hostetler, K.Y., Mitochondrial cardiolipin in diverse eukaryotes. Comparison of biosynthetic reactions and molecular acyl species. Eur. J. Biochem. 212 (1993), 727–735.
59. Schoenen, H., Bodendorfer, B., Hitchens, K., Manzanero, S., Werninghaus, K., Nimmerjahn, F., Agger, E.M., Stenger, S., Andersen, P., Ruland, J., et al. Cutting edge: Mincle is essential for recognition and adjuvanticity of the mycobacterial cord factor and its synthetic analog trehalose-dibehenate. J. Immunol. 184 (2010), 2756–2760.
60. Sena, C.B., Fukuda, T., Miyanagi, K., Matsumoto, S., Kobayashi, K., Murakami, Y., Maeda, Y., Kinoshita, T., Morita, Y.S., Controlled expression of branch-forming mannosyltransferase is critical for mycobacterial lipoarabinomannan biosynthesis. J. Biol. Chem. 285 (2010), 13326–13336.
61. Serbina, N.V., Jia, T., Hohl, T.M., Pamer, E.G., Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26 (2008), 421–452.
62. Shi, C., Pamer, E.G., Monocyte recruitment during infection and inflammation. Nat. Rev. Immunol. 11 (2011), 762–774.
63. Sieling, P.A., Chatterjee, D., Porcelli, S.A., Prigozy, T.I., Mazzaccaro, R.J., Soriano, T., Bloom, B.R., Brenner, M.B., Kronenberg, M., Brennan, P.J., et al. CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 269 (1995), 227–230.
64. Sprott, G.D., Dicaire, C.J., Gurnani, K., Sad, S., Krishnan, L., Activation of dendritic cells by liposomes prepared from phosphatidylinositol mannosides from Mycobacterium bovis bacillus Calmette-Guerin and adjuvant activity in vivo. Infect. Immun. 72 (2004), 5235–5246.
65. Takimoto, H., Maruyama, H., Shimada, K.I., Yakabe, R., Yano, I., Kumazawa, Y., Interferon-gamma independent formation of pulmonary granuloma in mice by injections with trehalose dimycolate (cord factor), lipoarabinomannan and phosphatidylinositol mannosides isolated from Mycobacterium tuberculosis. Clin. Exp. Immunol. 144 (2006), 134–141.
66. Torrelles, J.B., Azad, A.K., Schlesinger, L.S., 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 (2006), 1805–1816.
67. Trowsdale, J., Genetic and functional relationships between MHC and NK receptor genes. Immunity 15 (2001), 363–374.
68. Tsou, C.L., Peters, W., Si, Y., Slaymaker, S., Aslanian, A.M., Weisberg, S.P., Mack, M., Charo, I.F., Critical roles for CCR2 and MCP-3 in monocyte mobilization from bone marrow and recruitment to inflammatory sites. J. Clin. Invest. 117 (2007), 902–909.
69. Villeneuve, C., Gilleron, M., Maridonneau-Parini, I., Daffé, M., Astarie-Dequeker, C., Etienne, G., Mycobacteria use their surface-exposed glycolipids to infect human macrophages through a receptor-dependent process. J. Lipid Res. 46 (2005), 475–483.
70. Vir, P., Gupta, D., Agarwal, R., Verma, I., Immunomodulation of alveolar epithelial cells by Mycobacterium tuberculosis phosphatidylinositol mannosides results in apoptosis. APMIS 122 (2014), 268–282.
71. Wilson, G.J., Marakalala, M.J., Hoving, J.C., van Laarhoven, A., Drummond, R.A., Kerscher, B., Keeton, R., van de Vosse, E., Ottenhoff, T.H., Plantinga, T.S., et al. The C-type lectin receptor CLECSF8/CLEC4D is a key component of anti-mycobacterial immunity. Cell Host Microbe 17 (2015), 252–259.
72. Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K., Saito, T., Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9 (2008), 1179–1188.
73. Yonekawa, A., Saijo, S., Hoshino, Y., Miyake, Y., Ishikawa, E., Suzukawa, M., Inoue, H., Tanaka, M., Yoneyama, M., Oh-Hora, M., et al. Dectin-2 is a direct receptor for mannose-capped lipoarabinomannan of mycobacteria. Immunity 41 (2014), 402–413.
74. Zhang, Y., Broser, M., Cohen, H., Bodkin, M., Law, K., Reibman, J., Rom, W.N., Enhanced interleukin-8 release and gene expression in macrophages after exposure to Mycobacterium tuberculosis and its components. J. Clin. Invest. 95 (1995), 586–592.
75. Zheng, T., Luo, D., Compton, B., Painter, G., Alley, M., Adjuvanticity of a synthetic phosphatidylinositol dimannoside to a subvirion influenza vaccine in an influenza mouse model. J. Vaccines Vaccin., 6, 2015, 277.