Cord factor and peptidoglycan recapitulate the Th17-promoting adjuvant activity of mycobacteria through mincle/CARD9 signaling and the inflammasome

Journal of Immunology

Volumn 190, Issue 11, 2013, Pages 5722-5730

  Shenderov, Kevin ^a,b   Barber, Daniel L ^a   Mayer Barber, Katrin D ^a   Gurcha, Sudagar S ^c   Jankovic, Dragana ^a   Feng, Carl G ^a   Oland, Sandy ^a   Hieny, Sara ^a   Caspar, Pat ^a   Yamasaki, Sho ^d   Lin, Xin ^e   Ting, Jenny P Y ^f   Trinchieri, Giorgio ^g   Besra, Gurdyal S ^c   Cerundolo, Vincenzo ^b   Sher, Alan ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d KYUSHU UNIVERSITY   (Japan)

^e UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CASPASE ACTIVATION AND RECRUITMENT DOMAIN 9; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; CORD FACTOR; CRYOPYRIN; INFLAMMASOME; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LECTIN RECEPTOR; MINERAL OIL; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDOGLYCAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; IMMUNIZATION; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MICROBIAL ACTIVITY; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TH17 CELL;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADJUVANTS, IMMUNOLOGIC; ANIMALS; CELL DIFFERENTIATION; CORD FACTORS; INFLAMMASOMES; INTERLEUKIN-1BETA; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MYCOBACTERIUM; MYELOID DIFFERENTIATION FACTOR 88; PEPTIDOGLYCAN; RECEPTORS, INTERLEUKIN-1; RECEPTORS, INTERLEUKIN-18; SIGNAL TRANSDUCTION; TH17 CELLS; TOLL-LIKE RECEPTORS;

EID: 84878022309     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1203343     Document Type: Article

References (49)

1. Ott, G., and G. Van Nest. 2007. Development of vaccine adjuvants: a historical perspective. In Vaccine Adjuvants and delivery systems. S. Manmohan, ed. Wiley-Interscience, Hoboken, N.J., p. 1-32.
2. Luo, Y., J. Henning, and M. A. O'Donnell. 2011. Th1 cytokine-secreting recombinant Mycobacterium bovis bacillus Calmette-Guérin and prospective use in immunotherapy of bladder cancer. Clin. Dev. Immunol. 2011: 728930.
3. Billiau, A., and P. Matthys. 2001. Modes of action of Freund's adjuvants in experimental models of autoimmune diseases. J. Leukoc. Biol. 70: 849-860. (Pubitemid 33151123)
4. Komiyama, Y., S. Nakae, T. Matsuki, A. Nambu, H. Ishigame, S. Kakuta, K. Sudo, and Y. Iwakura. 2006. IL-17 plays an important role in the development of experimental autoimmune encephalomyelitis. J. Immunol. 177: 566-573. (Pubitemid 43939170)
5. Peck, A., and E. D. Mellins. 2010. Precarious balance: Th17 cells in host defense. Infect. Immun. 78: 32-38.
6. Milner, J. D., J. M. Brenchley, A. Laurence, A. F. Freeman, B. J. Hill, K. M. Elias, Y. Kanno, C. Spalding, H. Z. Elloumi, M. L. Paulson, et al. 2008. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper- IgE syndrome. Nature 452: 773-776. (Pubitemid 351521078)
7. Khader, S. A., G. K. Bell, J. E. Pearl, J. J. Fountain, J. Rangel-Moreno, G. E. Cilley, F. Shen, S. M. Eaton, S. L. Gaffen, S. L. Swain, et al. 2007. IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat. Immunol. 8: 369-377. (Pubitemid 46745412)
8. Lin, Y., S. Ritchea, A. Logar, S. Slight, M. Messmer, J. Rangel-Moreno, L. Guglani, J. F. Alcorn, H. Strawbridge, S. M. Park, et al. 2009. Interleukin-17 is required for T helper 1 cell immunity and host resistance to the intracellular pathogen Francisella tularensis. Immunity 31: 799-810.
9. Ishikawa, E., T. Ishikawa, Y. S. Morita, K. Toyonaga, H. Yamada, O. Takeuchi, T. Kinoshita, S. Akira, Y. Yoshikai, and S. Yamasaki. 2009. Direct recognition of the mycobacterial glycolipid, trehalose dimycolate, by C-type lectin Mincle. J. Exp. Med. 206: 2879-2888.
10. Schoenen, H., B. Bodendorfer, K. Hitchens, S. Manzanero, K. Werninghaus, F. Nimmerjahn, E. M. Agger, S. Stenger, P. Andersen, J. Ruland, et al. 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.
11. McGreal, E. P., M. Rosas, G. D. Brown, S. Zamze, S. Y. Wong, S. Gordon, L. Martinez-Pomares, and P. R. Taylor. 2006. The carbohydrate-recognition domain of Dectin-2 is a C-type lectin with specificity for high mannose. Glycobiology 16: 422-430.
12. Rothfuchs, A. G., A. Bafica, C. G. Feng, J. G. Egen, D. L. Williams, G. D. Brown, and A. Sher. 2007. Dectin-1 interaction with Mycobacterium tuberculosis leads to enhanced IL-12p40 production by splenic dendritic cells. J. Immunol. 179: 3463-3471.
13. Kleinnijenhuis, J., M. Oosting, L. A. Joosten, M. G. Netea, and R. Van Crevel. 2011. Innate immune recognition of Mycobacterium tuberculosis. Clin. Dev. Immunol. 2011: 405310.
14. Fritz, J. H., L. Le Bourhis, G. Sellge, J. G. Magalhaes, H. Fsihi, T. A. Kufer, C. Collins, J. Viala, R. L. Ferrero, S. E. Girardin, and D. J. Philpott. 2007. Nod1- mediated innate immune recognition of peptidoglycan contributes to the onset of adaptive immunity. Immunity 26: 445-459. (Pubitemid 46604867)
15. Magalhaes, J. G., J. H. Fritz, L. Le Bourhis, G. Sellge, L. H. Travassos, T. Selvanantham, S. E. Girardin, J. L. Gommerman, and D. J. Philpott. 2008. Nod2-dependent Th2 polarization of antigen-specific immunity. J. Immunol. 181: 7925-7935.
16. Werninghaus, K., A. Babiak, O. Gross, C. Hölscher, H. Dietrich, E. M. Agger, J. Mages, A. Mocsai, H. Schoenen, K. Finger, et al. 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.
17. Davis, B. K., H.Wen, and J. P. Ting. 2011. The inflammasome NLRs in immunity, inflammation, and associated diseases. Annu. Rev. Immunol. 29: 707-735.
18. Park, J. H., Y. G. Kim, C. McDonald, T. D. Kanneganti, M. Hasegawa, M. Body- Malapel, N. Inohara, and G. Núñez. 2007. RICK/RIP2 mediates innate immune responses induced through Nod1 and Nod2 but not TLRs. J. Immunol. 178: 2380-2386. (Pubitemid 46233437)
19. Hsu, Y. M., Y. Zhang, Y. You, D. Wang, H. Li, O. Duramad, X. F. Qin, C. Dong, and X. Lin. 2007. The adaptor protein CARD9 is required for innate immune responses to intracellular pathogens. Nat. Immunol. 8: 198-205. (Pubitemid 46152651)
20. Yamasaki, S., M. Matsumoto, O. Takeuchi, T. Matsuzawa, E. Ishikawa, M. Sakuma, H. Tateno, J. Uno, J. Hirabayashi, Y. Mikami, et al. 2009. C-type lectin Mincle is an activating receptor for pathogenic fungus, Malassezia. Proc. Natl. Acad. Sci. USA 106: 1897-1902.
21. Goldszmid, R. S., J. Idoyaga, A. I. Bravo, R. Steinman, J. Mordoh, and R. Wainstok. 2003. Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma. J. Immunol. 171: 5940-5947. (Pubitemid 37467212)
22. Dobson, G., D. E. Minnikin, S. M. Minnikin, J. H. Parlett, M. Goodfellow, M. Ridell, and M. Magnusson. 1985. Systematic analysis of complex mycobacterial lipids. In Chemical methods in bacterial systematics. M. Goodfellow, and D. E. Minnikin, eds. Academic Press, Orlando, FL, p. 237-265.
23. Mishra, A. K., K. Krumbach, D. Rittmann, B. Appelmelk, V. Pathak, A. K. Pathak, J. Nigou, J. Geurtsen, L. Eggeling, and G. S. Besra. 2011. Lipoarabinomannan biosynthesis in Corynebacterineae: the interplay of two a(1→2)-mannopyranosyltransferases MptC and MptD in mannan branching. Mol. Microbiol. 80: 1241-1259.
24. Besra, G. S., K. H. Khoo, M. R. McNeil, A. Dell, H. R. Morris, and P. J. Brennan. 1995. A new interpretation of the structure of the mycolylarabinogalactan complex of Mycobacterium tuberculosis as revealed through characterization of oligoglycosylalditol fragments by fast-atom bombardment mass spectrometry and 1H nuclear magnetic resonance spectroscopy. Biochemistry 34: 4257-4266.
25. Davidson, L. A., P. Draper, and D. E. Minnikin. 1982. Studies on the mycolic acids from the walls of Mycobacterium microti. J. Gen. Microbiol. 128: 823-828. (Pubitemid 12073749)
26. Schnare, M., G. M. Barton, A. C. Holt, K. Takeda, S. Akira, and R. Medzhitov. 2001. Toll-like receptors control activation of adaptive immune responses. Nat. Immunol. 2: 947-950. (Pubitemid 32976167)
27. Koo, I. C., C. Wang, S. Raghavan, J. H. Morisaki, J. S. Cox, and E. J. Brown. 2008. ESX-1-dependent cytolysis in lysosome secretion and inflammasome activation during mycobacterial infection. Cell. Microbiol. 10: 1866-1878.
28. Martinon, F., L. Agostini, E. Meylan, and J. Tschopp. 2004. Identification of bacterial muramyl dipeptide as activator of the NALP3/cryopyrin inflammasome. Curr. Biol. 14: 1929-1934. (Pubitemid 39464816)
29. Hsu, L. C., S. R. Ali, S. McGillivray, P. H. Tseng, S. Mariathasan, E. W. Humke, L. Eckmann, J. J. Powell, V. Nizet, V. M. Dixit, and M. Karin. 2008. A NOD2- NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc. Natl. Acad. Sci. USA 105: 7803-7808. (Pubitemid 351872719)
30. Pan, Q., J. Mathison, C. Fearns, V. V. Kravchenko, J. Da Silva Correia, H. M. Hoffman, K. S. Kobayashi, J. Bertin, E. P. Grant, A. J. Coyle, et al. 2007. MDP-induced interleukin-1beta processing requires Nod2 and CIAS1/NALP3. J. Leukoc. Biol. 82: 177-183. (Pubitemid 47026429)
31. Girardin, S. E., I. G. Boneca, L. A. Carneiro, A. Antignac, M. Jéhanno, J. Viala, K. Tedin, M. K. Taha, A. Labigne, U. Zähringer, et al. 2003. Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 300: 1584-1587. (Pubitemid 36682892)
32. Inohara, N., Y. Ogura, A. Fontalba, O. Gutierrez, F. Pons, J. Crespo, K. Fukase, S. Inamura, S. Kusumoto, M. Hashimoto, et al. 2003. Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn's disease. J. Biol. Chem. 278: 5509-5512. (Pubitemid 36800790)
33. Osorio, F., and C. Reis e Sousa. 2011. Myeloid C-type lectin receptors in pathogen recognition and host defense. Immunity 34: 651-664.
34. Saito, R., A. Tanaka, K. Sugiyama, I. Azuma, and Y. Yamamura. 1976. Adjuvant effect of cord factor, a mycobacterial lipid. Infect. Immun. 13: 776-781.
35. Davidsen, J., I. Rosenkrands, D. Christensen, A. Vangala, D. Kirby, Y. Perrie, E. M. Agger, and P. Andersen. 2005. Characterization of cationic liposomes based on dimethyldioctadecylammonium and synthetic cord factor from M. tuberculosis (trehalose 6,6′-dibehenate)-a novel adjuvant inducing both strong CMI and antibody responses. Biochim. Biophys. Acta 1718: 22-31. (Pubitemid 41698893)
36. Chung, Y., S. H. Chang, G. J. Martinez, X. O. Yang, R. Nurieva, H. S. Kang, L. Ma, S. S. Watowich, A. M. Jetten, Q. Tian, and C. Dong. 2009. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 30: 576-587.
37. Sutton, C., C. Brereton, B. Keogh, K. H. Mills, and E. C. Lavelle. 2006. A crucial role for interleukin (IL)-1 in the induction of IL-17-producing T cells that mediate autoimmune encephalomyelitis. J. Exp. Med. 203: 1685-1691. (Pubitemid 44036274)
38. Su, S. B., P. B. Silver, R. S. Grajewski, R. K. Agarwal, J. Tang, C. C. Chan, and R. R. Caspi. 2005. Essential role of the MyD88 pathway, but nonessential roles of TLRs 2, 4, and 9, in the adjuvant effect promoting Th1-mediated autoimmunity. J. Immunol. 175: 6303-6310. (Pubitemid 41598869)
39. Fang, J., D. Fang, P. B. Silver, F. Wen, B. Li, X. Ren, Q. Lin, R. R. Caspi, and S. B. Su. 2010. The role of TLR2, TRL3, TRL4, and TRL9 signaling in the pathogenesis of autoimmune disease in a retinal autoimmunity model. Invest. Ophthalmol. Vis. Sci. 51: 3092-3099.
40. Fukata, M., K. Breglio, A. Chen, A. S. Vamadevan, T. Goo, D. Hsu, D. Conduah, R. Xu, and M. T. Abreu. 2008. The myeloid differentiation factor 88 (MyD88) is required for CD4+ T cell effector function in a murine model of inflammatory bowel disease. J. Immunol. 180: 1886-1894.
41. Lalor, S. J., L. S. Dungan, C. E. Sutton, S. A. Basdeo, J. M. Fletcher, and K. H. Mills. 2011. Caspase-1-processed cytokines IL-1beta and IL-18 promote IL-17 production by gammadelta and CD4 T cells that mediate autoimmunity. J. Immunol. 186: 5738-5748.
42. Stehlik, C. 2009. Multiple interleukin-1beta-converting enzymes contribute to inflammatory arthritis. Arthritis Rheum. 60: 3524-3530.
43. Maelfait, J., E. Vercammen, S. Janssens, P. Schotte, M. Haegman, S. Magez, and R. Beyaert. 2008. Stimulation of Toll-like receptor 3 and 4 induces interleukin- 1beta maturation by caspase-8. J. Exp. Med. 205: 1967-1973.
44. Ellouz, F., A. Adam, R. Ciorbaru, and E. Lederer. 1974. Minimal structural requirements for adjuvant activity of bacterial peptidoglycan derivatives. Biochem. Biophys. Res. Commun. 59: 1317-1325.
45. Shimada, T., B. G. Park, A. J. Wolf, C. Brikos, H. S. Goodridge, C. A. Becker, C. N. Reyes, E. A. Miao, A. Aderem, F. Götz, et al. 2010. Staphylococcus aureus evades lysozyme-based peptidoglycan digestion that links phagocytosis, inflammasome activation, and IL-1beta secretion. Cell Host Microbe 7: 38-49.
46. Mariathasan, S., and D. M. Monack. 2007. Inflammasome adaptors and sensors: intracellular regulators of infection and inflammation. Nat. Rev. Immunol. 7: 31-40. (Pubitemid 46020825)
47. LeibundGut-Landmann, S., O. Gross, M. J. Robinson, F. Osorio, E. C. Slack, S. V. Tsoni, E. Schweighoffer, V. Tybulewicz, G. D. Brown, J. Ruland, and C. Reis e Sousa. 2007. Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17. Nat. Immunol. 8: 630-638.
48. Wüthrich, M., B. Gern, C. Y. Hung, K. Ersland, N. Rocco, J. Pick-Jacobs, K. Galles, H. Filutowicz, T. Warner, M. Evans, et al. 2011. Vaccine-induced protection against 3 systemic mycoses endemic to North America requires Th17 cells in mice. J. Clin. Invest. 121: 554-568.
49. Desel, C., K. Werninghaus, M. Ritter, K. Jozefowski, J. Wenzel, N. Russkamp, U. Schleicher, D. Christensen, S. Wirtz, C. Kirschning, et al. 2013. The Mincleactivating adjuvant TDB induces MyD88-dependent Th1 and Th17 responses through IL-1R signaling. PLoS One. 8: e53531.