Toll-like receptor 6 stimulation promotes T-helper 1 and 17 responses in gastrointestinal-associated lymphoid tissue and modulates murine experimental colitis

Mucosal Immunology

Volumn 7, Issue 5, 2014, Pages 1266-1277

  Morgan, M E ^a   Koelink, P J ^a   Zheng, B ^a   Den Brok, M H M G M ^b   Van De Kant, H Jg ^a   Verspaget, H W ^c   Folkerts, G ^a   Adema, G J ^b   Kraneveld, A D ^a  

^a UTRECHT UNIVERSITY   (Netherlands)

^b RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TOLL LIKE RECEPTOR 6; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; CD3 ANTIBODY; CD69 ANTIGEN; MEMBRANE PROTEIN; PROTEIN FSL 1; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CELL POLARITY; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; ENTERITIS; EXPERIMENTAL COLITIS; FEMALE; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY BOWEL DISEASE; INTESTINE LYMPHATIC TISSUE; LYMPHOCYTE ACTIVATION; MALE; MOUSE; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; RORC GENE; SPLEEN; TH1 CELL; TH17 CELL; TLR6 GENE; DISEASE SEVERITY; GENETIC ASSOCIATION; IMMUNE RESPONSE; IMMUNOMODULATION; PROTEIN ANALYSIS; RADIOIMMUNOPRECIPITATION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; COLITIS; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; LYMPHOID TISSUE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; CELLS, CULTURED; COLITIS; DISEASE MODELS, ANIMAL; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; GASTROINTESTINAL TRACT; GENE EXPRESSION REGULATION; HUMANS; LYMPHOID TISSUE; MICE; MICE, INBRED BALB C; TH1 CELLS; TH17 CELLS; TOLL-LIKE RECEPTOR 6; TRANSCRIPTION FACTORS;

EID: 84906344575     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.16     Document Type: Article

References (34)

1. Takeuchi, O. et al. TLR6: a novel member of an expanding toll-like receptor family. Gene 231, 59-65 (1999).
2. Hajjar, A.M. et al. Cutting edge: functional interactions between toll-like receptor (TLR) 2 and TLR1 or TLR6 in response to phenol- solublemodulin. J. Immunol. 166, 15-19 (2001).
3. Takeuchi, O. et al. Discrimination of bacterial lipoproteins by Toll-like receptor 6. Int. Immunol. 13, 933-940 (2001).
4. Ozinsky, A. et al. The repertoire for pattern recognition of pathogens by the innate immune system is defined by cooperation between toll-like receptors. Proc. Natl Acad. Sci. USA 97, 13766-13771 (2000).
5. Depaolo, R.W. et al. Toll-like receptor 6 drives differentiation of tolerogenic dendritic cells and contributes to LcrV-mediated plague pathogenesis. Cell Host Microbe 4, 350-361 (2008).
6. DePaolo, R.W., Kamdar, K., Khakpour, S., Sugiura, Y.,Wang,W. & Jabri, B. A specific role for TLR1 in protective T(H)17 immunity during mucosal infection. J. Exp. Med. 209, 1437-1444 (2012).
7. Pot, C., Apetoh, L. & Kuchroo, V.K. Type 1 regulatory T cells (Tr1) in autoimmunity. Semin. Immunol. 23, 202-208 (2011).
8. Moreira, A.P. et al. The protective role of TLR6 in a mouse model of asthma is mediated by IL-23 and IL-17A. J. Clin. Invest. 121, 4420-4432 (2011).
9. Miossec, P. & Kolls, J.K. Targeting IL-17 and TH17 cells in chronic inflammation. Nat. Rev. Drug Discov. 11, 763-776 (2012).
10. Ahern, P.P. et al. Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity 33, 279-288 (2010).
11. Jostins, L. et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491, 119-124 (2012).
12. Kleinschek, M.A. et al. Circulating and gut-resident human Th17 cells express CD161 and promote intestinal inflammation. J. Exp. Med. 206, 525-534 (2009).
13. Eastaff-Leung, N., Mabarrack, N., Barbour, A., Cummins, A. & Barry, S. Foxp3+ regulatory Tcells, Th17 effector cells, and cytokine environment in inflammatory bowel disease. J. Clin. Immunol. 30, 80-89 (2010).
14. Doherty, G.A. et al. CD73 is a phenotypic marker of effector memory Th17 cells in inflammatory bowel disease. Eur. J. Immunol. 42, 3062-3072 (2012).
15. Olsen, T., Rismo, R., Cui, G., Goll, R., Christiansen, I. & Florholmen, J. TH1 and TH17 interactions in untreated inflamed mucosa of inflammatory bowel disease, and their potential to mediate the inflammation. Cytokine 56, 633-640 (2011).
16. Ghoreschi, K., Laurence, A., Yang, X.P., Hirahara, K. & O'Shea, J.J. T helper 17 cell heterogeneity and pathogenicity in autoimmune disease. Trends Immunol. 32, 395-401 (2011).
17. Fong, D.J., Hogaboam, C.M.,Matsuno, Y., Akira, S., Uematsu, S. & Joshi, A.D. Toll-like receptor 6 drives interleukin-17A expression during experimental hypersensitivity pneumonitis. Immunology 130, 125-136 (2010).
18. Pabst, R., Durak, D., Roos, A., Luhrmann, A. & Tschernig, T. TLR2/6 stimulation of the rat lung: effects on lymphocyte subsets, natural killer cells and dendritic cells in different parts of the air-conducting compartments and at different ages. Immunology 126, 132-139 (2009).
19. Oberg, H.H., Ly, T.T., Ussat, S., Meyer, T., Kabelitz, D. & Wesch, D. Differential but direct abolishment of human regulatory T cell suppressive capacity by various TLR2 ligands. J. Immunol. 184, 4733-4740 (2010).
20. Nyirenda, M.H. et al. TLR2 stimulation drives human naive and effector regulatory T cells into a Th17-like phenotype with reduced suppressive function. J. Immunol. 187, 2278-2290 (2011).
21. Zheng, B., Morgan, M.E., van de Kant, H.J., Garssen, J., Folkerts, G. & Kraneveld, A.D. Transcriptional modulation of pattern recognition receptors in acute colitis in mice. Biochim. Biophys. Acta 1832, 2162-2172 (2013).
22. Ivanov, I.I. et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126, 1121-1133 (2006).
23. Ruan, Q. et al. The Th17 immune response is controlled by the Rel-RORgamma-RORgamma T transcriptional axis. J. Exp. Med. 208, 2321-2333 (2011).
24. Kimura, A. & Kishimoto, T. IL-6: regulator of Treg/Th17 balance. Eur. J. Immunol. 40, 1830-1835 (2010).
25. Gao, Z. et al. Synergy between IL-6 and TGF-beta signaling promotes FOXP3 degradation. Int. J. Clin. Exp. Pathol. 5, 626-633 (2012).
26. Kryczek, I. et al. Cutting edge: IFN-gamma enables APC to promote memory Th17 and abate Th1 cell development. J. Immunol. 181, 5842-5846 (2008).
27. Komai-Koma, M., Jones, L., Ogg, G.S., Xu, D. & Liew, F.Y. TLR2 is expressed on activated Tcells as a costimulatory receptor. Proc. Natl Acad. Sci. USA 101, 3029-3034 (2004).
28. Slifka, M.K. & Whitton, J.L. Antigen-specific regulation of T cell-mediated cytokine production. Immunity 12, 451-457 (2000).
29. Walker, J.A., Barlow, J.L. & McKenzie, A.N. Innate lymphoid cells-how did we miss them?. Nat. Rev. Immunol. 13, 75-87 (2013).
30. Li, H., Wojciechowski, W., Dell'Agnola, C., Lopez, N.E. & Espinoza-Delgado, I. IFN-gamma and T-bet expression in human dendritic cells from normal donors and cancer patients is controlled through mechanisms involving ERK-1/2-dependent and IL-12-independent pathways. J. Immunol. 177, 3554-3563 (2006).
31. Gessani, S. & Belardelli, F. IFN-gamma expression in macrophages and its possible biological significance. Cytokine Growth Factor Rev. 9, 117-123 (1998).
32. Bradley, L.M., Dalton, D.K. & Croft, M. A direct role for IFN-gamma in regulation of Th1 cell development. J. Immunol. 157, 1350-1358 (1996).
33. Hall, L.J., Faivre, E., Quinlan, A., Shanahan, F., Nally, K. & Melgar, S. Induction and activation of adaptive immune populations during acute and chronic phases of a murine model of experimental colitis. Dig. Dis. Sci. 56, 79-89 (2011).
34. Gao,Q. et al. Expression of matrix metalloproteinases-2 and -9 in intestinal tissue of patients with inflammatory bowel diseases. Dig. Liver Dis. 37, 584-592 (2005).