Glycerol monomycolate is a novel ligand for the human, but not mouse macrophage inducible C-type lectin, Mincle

Journal of Biological Chemistry

Volumn 289, Issue 22, 2014, Pages 15405-15412

  Hattori, Yuki ^a   Morita, Daisuke ^a   Fujiwara, Nagatoshi ^b   Mori, Daiki ^c   Nakamura, Takashi ^d   Harashima, Hideyoshi ^d   Yamasaki, Sho ^c   Sugita, Masahiko ^a  

^a KYOTO UNIVERSITY   (Japan)

^b TEZUKAYAMA UNIVERSITY   (Japan)

^c KYUSHU UNIVERSITY   (Japan)

^d HOKKAIDO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LIGANDS; MAMMALS;

C-TYPE LECTINS; INNATE IMMUNES; MOLECULAR BASIS; NOVEL LIGANDS; TRANSFECTANTS; TRANSGENIC MICE;

GLYCEROL;

AMINO ACID; C TYPE LECTIN; CORD FACTOR; CYTOKINE; GLYCEROL MONOMYCOLATE; LECTIN; LIGAND; LIPID; MINCLE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INNATE IMMUNITY; KNOCKOUT MOUSE; LIPID ANALYSIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; RESIDUE ANALYSIS; SITE DIRECTED MUTAGENESIS; TRANSGENIC MOUSE;

GLYCEROL MONOMYCOLATE; HOST-PATHOGEN INTERACTIONS; INNATE IMMUNITY; LIPIDS; MACROPHAGES; MINCLE; MYCOBACTERIA; TRANSGENIC MICE;

ANIMALS; FEMALE; GLYCOLIPIDS; HEK293 CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNITY, INNATE; LECTINS, C-TYPE; LIGANDS; MACROPHAGES; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MONOGLYCERIDES; MUTAGENESIS, SITE-DIRECTED; MYCOBACTERIUM; RATS; RATS, WISTAR; RECEPTORS, IMMUNOLOGIC; TUBERCULOSIS;

EID: 84901718538     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.566489     Document Type: Article

References (35)

1. Brennan, P. J. (2003) Structure, function, and biogenesis of the cell wall of Mycobacterium tuberculosis. Tuberculosis 83, 91-97
2. Bowdish, D. M., Sakamoto, K., Kim, M. J., Kroos, M., Mukhopadhyay, S., Leifer, C. A., Tryggvason, K., Gordon, S., and Russell, D. G. (2009) MARCO, TLR2, and CD14 are required for macrophage cytokine responses to mycobacterial trehalose dimycolate and Mycobacterium tuberculosis. PLoS Pathog. 5, e1000474
3. Hunter, R. L., Olsen, M., Jagannath, C., and Actor, J. K. (2006) Trehalose 6,6′-dimycolate and lipid in the pathogenesis of caseating granulomas of tuberculosis in mice. Am. J. Pathol. 168, 1249-1261
4. Otsuka, A., Matsunaga, I., Komori, T., Tomita, K., Toda, Y., Manabe, T., Miyachi, Y., and Sugita, M. (2008) Trehalose dimycolate elicits eosinophilic skin hypersensitivity in mycobacteria-infected guinea pigs. J. Immunol. 181, 8528-8533
5. Rao, V., Fujiwara, N., Porcelli, S. A., and Glickman, M. S. (2005) Mycobacterium tuberculosis controls host innate immune activation through cyclopropane modification of a glycolipid effector molecule. J. Exp. Med. 201, 535-543
6. Sakamoto, K., Kim, M. J., Rhoades, E. R., Allavena, R. E., Ehrt, S., Wainwright, H. C., Russell, D. G., and Rohde, K. H. (2013) Mycobacterial trehalose dimycolate reprograms macrophage global gene expression and activates matrix metalloproteinases. Infect. Immun. 81, 764-776
7. Ishikawa, E., Ishikawa, T., Morita, Y. S., Toyonaga, K., Yamada, H., Takeuchi, O., Kinoshita, T., Akira, S., Yoshikai, Y., and Yamasaki, S. (2009) Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by Ctype lectin Mincle. J. Exp. Med. 206, 2879-2888
8. Schoenen, H., Bodendorfer, B., Hitchens, K., Manzanero, S., Werninghaus, K., Nimmerjahn, F., Agger, E. M., Stenger, S., Andersen, P., Ruland, J., Brown, G. D., Wells, C., and 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, 2756-2760
9. Werninghaus, K., Babiak, A., Gross, O., Hölscher, C., Dietrich, H., Agger, E. M., Mages, J., Mocsai, A., Schoenen, H., Finger, K., Nimmerjahn, F., Brown, G. D., Kirschning, C., Heit, A., Andersen, P., Wagner, H., Ruland, J., and Lang, R. (2009) Adjuvanticity of a synthetic cord factor analogue for subunit Mycobacterium tuberculosis vaccination requires FcRgamma- Syk-Card9-dependent innate immune activation. J. Exp. Med. 206, 89-97
10. Miyake, Y., Toyonaga, K., Mori, D., Kakuta, S., Hoshino, Y., Oyamada, A., Yamada, H., Ono, K., Suyama, M., Iwakura, Y., Yoshikai, Y., and Yamasaki, S. (2013) C-type lectin MCL is an FcRgamma-coupled receptor that mediates the adjuvanticity of mycobacterial cord factor. Immunity 38, 1050-1062
11. Geijtenbeek, T. B., Van Vliet, S. J., Koppel, E. A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C. M., Appelmelk, B., and Van Kooyk, Y. (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17
12. Maeda, N., Nigou, J., Herrmann, J. L., Jackson, M., Amara, A., Lagrange, P. H., Puzo, G., Gicquel, B., and Neyrolles, O. (2003) The cell surface receptor DC-SIGN discriminates between Mycobacterium species through selective recognition of the mannose caps on lipoarabinomannan. J. Biol. Chem. 278, 5513-5516
13. Tailleux, L., Schwartz, O., Herrmann, J. L., Pivert, E., Jackson, M., Amara, A., Legres, L., Dreher, D., Nicod, L. P., Gluckman, J. C., Lagrange, P. H., Gicquel, B., and Neyrolles, O. (2003) DC-SIGN is the major Mycobacterium tuberculosis receptor on human dendritic cells. J. Exp. Med. 197, 121-127
14. Sieling, P. A., Chatterjee, D., Porcelli, S. A., Prigozy, T. I., Mazzaccaro, R. J., Soriano, T., Bloom, B. R., Brenner, M. B., Kronenberg, M., and Brennan, P. J. (1995) CD1-restricted T cell recognition of microbial lipoglycan antigens. Science 269, 227-230
15. Layre, E., Collmann, A., Bastian, M., Mariotti, S., Czaplicki, J., Prandi, J., Mori, L., Stenger, S., De Libero, G., Puzo, G., and Gilleron, M. (2009) Mycolic acids constitute a scaffold for mycobacterial lipid antigens stimulating CD1-restricted T cells. Chem. Biol. 16, 82-92
16. Andersen, C. S., Agger, E. M., Rosenkrands, I., Gomes, J. M., Bhowruth, V., Gibson, K. J., Petersen, R. V., Minnikin, D. E., Besra, G. S., and Andersen, P. (2009) A simple mycobacterial monomycolated glycerol lipid has potent immunostimulatory activity. J. Immunol. 182, 424-432
17. Hattori, Y., Matsunaga, I., Komori, T., Urakawa, T., Nakamura, T., Fujiwara, N., Hiromatsu, K., Harashima, H., and Sugita, M. (2011) Glycerol monomycolate, a latent tuberculosis-associated mycobacterial lipid, induces eosinophilic hypersensitivity responses in guinea pigs. Biochem. Biophys. Res. Commun. 409, 304-307
18. Matsunaga, I., Naka, T., Talekar, R. S., McConnell, M. J., Katoh, K., Nakao, H., Otsuka, A., Behar, S. M., Yano, I., Moody, D. B., and Sugita, M. (2008) Mycolyltransferase-mediated glycolipid exchange in Mycobacteria. J. Biol. Chem. 283, 28835-28841
19. Matsumoto, M., Tanaka, T., Kaisho, T., Sanjo, H., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., and Akira, S. (1999) A novel LPS-inducible C-type lectin is a transcriptional target of NF-IL6 in macrophages. J. Immunol. 163, 5039-5048
20. Yamasaki, S., Ishikawa, E., Sakuma, M., Hara, H., Ogata, K., and Saito, T. (2008) Mincle is an ITAM-coupled activating receptor that senses damaged cells. Nat. Immunol. 9, 1179-1188
21. Kishiro, Y., Kagawa, M., Naito, I., and Sado, Y. (1995) A novel method of preparing rat-monoclonal antibody-producing hybridomas by using rat medial iliac lymph node cells. Cell Struct. Funct. 20, 151-156
22. Spada, F. M., Borriello, F., Sugita, M., Watts, G. F., Koezuka, Y., and Porcelli, S. A. (2000) Low expression level but potent antigen presenting function of CD1d on monocyte lineage cells. Eur. J. Immunol. 30, 3468-3477
23. Pirson, C., Jones, G. J., Steinbach, S., Besra, G. S., and Vordermeier, H. M. (2012) Differential effects of Mycobacterium bovis-derived polar and apolar lipid fractions on bovine innate immune cells. Vet. Res. 43, 54
24. Furukawa, A., Kamishikiryo, J., Mori, D., Toyonaga, K., Okabe, Y., Toji, A., Kanda, R., Miyake, Y., Ose, T., Yamasaki, S., and Maenaka, K. (2013) Structural analysis for glycolipid recognition by the C-type lectins Mincle and MCL. Proc. Natl. Acad. Sci. U.S.A. 110, 17438-17443
25. Miyake, Y., Ishikawa, E., Ishikawa, T., and Yamasaki, S. (2010) Self and nonself recognition through C-type lectin receptor, Mincle. Self Nonself 1, 310-313
26. Yamasaki, S., Matsumoto, M., Takeuchi, O., Matsuzawa, T., Ishikawa, E., Sakuma, M., Tateno, H., Uno, J., Hirabayashi, J., Mikami, Y., Takeda, K., Akira, S., and Saito, T. (2009) C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc. Natl. Acad. Sci. U.S.A. 106, 1897-1902
27. Cambier, C. J., Takaki, K. K., Larson, R. P., Hernandez, R. E., Tobin, D. M., Urdahl, K. B., Cosma, C. L., and Ramakrishnan, L. (2014) Mycobacteria manipulate macrophage recruitment through coordinated use of membrane lipids. Nature 505, 218-222
28. Yang, Y., Kulka, K., Montelaro, R. C., Reinhart, T. A., Sissons, J., Aderem, A., and Ojha, A. K. (2014) A Hydrolase of Trehalose Dimycolate Induces Nutrient Influx and Stress Sensitivity
29. Roca, F. J., and Ramakrishnan, L. (2013) TNF dually mediates resistance and susceptibility to mycobacteria via mitochondrial reactive oxygen species. Cell 153, 521-534
30. Winthrop, K. L. (2006) Risk and prevention of tuberculosis and other serious opportunistic infections associated with the inhibition of tumor necrosis factor. Nat. Clin. Pract. Rheumatol. 2, 602-610
31. Dascher, C. C., Hiromatsu, K., Xiong, X., Morehouse, C., Watts, G., Liu, G., McMurray, D. N., LeClair, K. P., Porcelli, S. A., and Brenner, M. B. (2003) Immunization with a mycobacterial lipid vaccine improves pulmonary pathology in the guinea pig model of tuberculosis. Int. Immunol. 15, 915-925
32. Meraviglia, S., El Daker, S., Dieli, F., Martini, F., and Martino, A. (2011) γδ T cells cross-link innate and adaptive immunity in Mycobacterium tuberculosis infection. Clin. Dev. Immunol. 2011, 587315
33. Stenger, S., Mazzaccaro, R. J., Uyemura, K., Cho, S., Barnes, P. F., Rosat, J. P., Sette, A., Brenner, M. B., Porcelli, S. A., Bloom, B. R., and Modlin, R. L. (1997) Differential effects of cytolytic T cell subsets on intracellular infection. Science 276, 1684-1687
34. Kondratieva, E., Logunova, N., Majorov, K., Averbakh, M., and Apt, A. (2010) Host genetics in granuloma formation: human-like lung pathology in mice with reciprocal genetic susceptibility to M. tuberculosis and M. avium. PLoS One 5, e10515
35. Via, L. E., Lin, P. L., Ray, S. M., Carrillo, J., Allen, S. S., Eum, S. Y., Taylor, K., Klein, E., Manjunatha, U., Gonzales, J., Lee, E. G., Park, S. K., Raleigh, J. A., Cho, S. N., McMurray, D. N., Flynn, J. L., and Barry, C. E., 3rd. (2008) Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect. Immun. 76, 2333-2340