Inhibition of dectin-1 signaling ameliorates colitis by inducing lactobacillus-mediated regulatory T cell expansion in the intestine

Cell Host and Microbe

Volumn 18, Issue 2, 2015, Pages 183-197

  Tang, Ce ^a,b,c   Kamiya, Tomonori ^b   Liu, Yang ^b,g   Kadoki, Motohiko ^a,b   Kakuta, Shigeru ^b,h   Oshima, Kenshiro ^b   Hattori, Masahira ^b   Takeshita, Kozue ^d   Kanai, Takanori ^d   Saijo, Shinobu ^b,e   Ohno, Naohito ^f   Iwakura, Yoichiro ^a,b,c,e  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^e CHIBA UNIVERSITY   (Japan)

^f TOKYO UNIVERSITY OF PHARMACY AND LIFE SCIENCES   (Japan)

^g SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^h UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

DECTIN 1; DEXTRAN SULFATE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 1BETA; LAMINARAN; RETINOID RELATED ORPHAN RECEPTOR GAMMA; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; LECTIN;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; COLITIS; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; INFLAMMATORY BOWEL DISEASE; INTESTINE; INTESTINE FLORA; LACTOBACILLUS; LACTOBACILLUS MURINUS; MOUSE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; ANIMAL; ANTAGONISTS AND INHIBITORS; COLON; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; COLITIS; COLON; LACTOBACILLUS; LECTINS, C-TYPE; MICE; MICE, KNOCKOUT; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 84954452665     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.07.003     Document Type: Article

References (40)

1. P.P. Ahern, C. Schiering, S. Buonocore, M.J. McGeachy, D.J. Cua, K.J. Maloy, and F. Powrie Interleukin-23 drives intestinal inflammation through direct activity on T cells Immunity 33 2010 279 288
2. T. Arstila, T.P. Arstila, S. Calbo, F. Selz, M. Malassis-Seris, P. Vassalli, P. Kourilsky, and D. Guy-Grand Identical T cell clones are located within the mouse gut epithelium and lamina propia and circulate in the thoracic duct lymph J. Exp. Med. 191 2000 823 834
3. K. Atarashi, T. Tanoue, T. Shima, A. Imaoka, T. Kuwahara, Y. Momose, G. Cheng, S. Yamasaki, T. Saito, Y. Ohba, and et al. Induction of colonic regulatory T cells by indigenous Clostridium species Science 331 2011 337 341
4. M.J. Barnes, and F. Powrie Regulatory T cells reinforce intestinal homeostasis Immunity 31 2009 401 411
5. H.L. Cash, C.V. Whitham, C.L. Behrendt, and L.V. Hooper Symbiotic bacteria direct expression of an intestinal bactericidal lectin Science 313 2006 1126 1130
6. A.M. Castellazzi, C. Valsecchi, L. Montagna, P. Malfa, G. Ciprandi, M.A. Avanzini, and G.L. Marseglia In vitro activation of mononuclear cells by two probiotics: Lactobacillus paracasei I 1688, Lactobacillus salivarius I 1794, and their mixture (PSMIX) Immunol. Invest. 36 2007 413 421
7. A. Chaudhry, R.M. Samstein, P. Treuting, Y. Liang, M.C. Pils, J.M. Heinrich, R.S. Jack, F.T. Wunderlich, J.C. Brüning, W. Müller, and A.Y. Rudensky Interleukin-10 signaling in regulatory T cells is required for suppression of Th17 cell-mediated inflammation Immunity 34 2011 566 578
8. W. Chen, W. Jin, N. Hardegen, K.J. Lei, L. Li, N. Marinos, G. McGrady, and S.M. Wahl Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3 J. Exp. Med. 198 2003 1875 1886
9. J.L. Coombes, N.J. Robinson, K.J. Maloy, H.H. Uhlig, and F. Powrie Regulatory T cells and intestinal homeostasis Immunol. Rev. 204 2005 184 194
10. H.S. Cooper, S.N. Murthy, R.S. Shah, and D.J. Sedergran Clinicopathologic study of dextran sulfate sodium experimental murine colitis Lab. Invest. 69 1993 238 249
11. B.D. Corbin, E.H. Seeley, A. Raab, J. Feldmann, M.R. Miller, V.J. Torres, K.L. Anderson, B.M. Dattilo, P.M. Dunman, R. Gerads, and et al. Metal chelation and inhibition of bacterial growth in tissue abscesses Science 319 2008 962 965
12. H.S. de Vries, T.S. Plantinga, J.H. van Krieken, R. Stienstra, A.A. van Bodegraven, E.A. Festen, R.K. Weersma, J.B. Crusius, R.K. Linskens, L.A. Joosten, and et al. Genetic association analysis of the functional c.714T>G polymorphism and mucosal expression of dectin-1 in inflammatory bowel disease PLoS ONE 4 2009 e7818
13. D. Foell, H. Wittkowski, and J. Roth Monitoring disease activity by stool analyses: from occult blood to molecular markers of intestinal inflammation and damage Gut 58 2009 859 868
14. R.L. Gallo, and L.V. Hooper Epithelial antimicrobial defence of the skin and intestine Nat. Rev. Immunol. 12 2012 503 516
15. S. Hori, T. Nomura, and S. Sakaguchi Control of regulatory T cell development by the transcription factor Foxp3 Science 299 2003 1057 1061
16. H. Huang, G.R. Ostroff, C.K. Lee, S. Agarwal, S. Ram, P.A. Rice, C.A. Specht, and S.M. Levitz Relative contributions of dectin-1 and complement to immune responses to particulate β-glucans J. Immunol. 189 2012 312 317
17. W. Hueber, B.E. Sands, S. Lewitzky, M. Vandemeulebroecke, W. Reinisch, P.D. Higgins, J. Wehkamp, B.G. Feagan, M.D. Yao, M. Karczewski, et al. Secukinumab in Crohn's Disease Study Group Secukinumab, a human anti-IL-17A monoclonal antibody, for moderate to severe Crohn's disease: unexpected results of a randomised, double-blind placebo-controlled trial Gut 61 2012 1693 1700
18. I.D. Iliev, V.A. Funari, K.D. Taylor, Q. Nguyen, C.N. Reyes, S.P. Strom, J. Brown, C.A. Becker, P.R. Fleshner, M. Dubinsky, and et al. Interactions between commensal fungi and the C-type lectin receptor Dectin-1 influence colitis Science 336 2012 1314 1317
19. I.I. Ivanov, B.S. McKenzie, L. Zhou, C.E. Tadokoro, A. Lepelley, J.J. Lafaille, D.J. Cua, and D.R. Littman The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells Cell 126 2006 1121 1133
20. S.O. Jang, H.J. Kim, Y.J. Kim, M.J. Kang, J.W. Kwon, J.H. Seo, H.Y. Kim, B.J. Kim, J. Yu, and S.J. Hong Asthma Prevention by Lactobacillus Rhamnosus in a Mouse Model is Associated With CD4(+)CD25(+)Foxp3(+) T Cells Allergy Asthma Immunol. Res. 4 2012 150 156
21. T. Kawai, and S. Akira Toll-like receptors and their crosstalk with other innate receptors in infection and immunity Immunity 34 2011 637 650
22. Y.K. Lee, J.S. Menezes, Y. Umesaki, and S.K. Mazmanian Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis Proc. Natl. Acad. Sci. USA 108 Suppl 1 2011 4615 4622
23. R.E. Lehotzky, C.L. Partch, S. Mukherjee, H.L. Cash, W.E. Goldman, K.H. Gardner, and L.V. Hooper Molecular basis for peptidoglycan recognition by a bactericidal lectin Proc. Natl. Acad. Sci. USA 107 2010 7722 7727
24. A.J. Macpherson, and T. Uhr Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria Science 303 2004 1662 1665
25. V. Maneu, A. Yáñez, C. Murciano, A. Molina, M.L. Gil, and D. Gozalbo Dectin-1 mediates in vitro phagocytosis of Candida albicans yeast cells by retinal microglia FEMS Immunol. Med. Microbiol. 63 2011 148 150
26. M. Monteiro, C.F. Almeida, M. Caridade, J.C. Ribot, J. Duarte, A. Agua-Doce, I. Wollenberg, B. Silva-Santos, and L. Graca Identification of regulatory Foxp3+ invariant NKT cells induced by TGF-beta J. Immunol. 185 2010 2157 2163
27. M. Murai, O. Turovskaya, G. Kim, R. Madan, C.L. Karp, H. Cheroutre, and M. Kronenberg Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis Nat. Immunol. 10 2009 1178 1184
28. W. O'Connor Jr., M. Kamanaka, C.J. Booth, T. Town, S. Nakae, Y. Iwakura, J.K. Kolls, and R.A. Flavell A protective function for interleukin 17A in T cell-mediated intestinal inflammation Nat. Immunol. 10 2009 603 609
29. L. O'Mahony, L. O'Callaghan, J. McCarthy, D. Shilling, P. Scully, S. Sibartie, E. Kavanagh, W.O. Kirwan, H.P. Redmond, J.K. Collins, and F. Shanahan Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G839 G845
30. T. Obata, Y. Goto, J. Kunisawa, S. Sato, M. Sakamoto, H. Setoyama, T. Matsuki, K. Nonaka, N. Shibata, M. Gohda, and et al. Indigenous opportunistic bacteria inhabit mammalian gut-associated lymphoid tissues and share a mucosal antibody-mediated symbiosis Proc. Natl. Acad. Sci. USA 107 2010 7419 7424
31. S.J. Ott, T. Kühbacher, M. Musfeldt, P. Rosenstiel, S. Hellmig, A. Rehman, O. Drews, W. Weichert, K.N. Timmis, and S. Schreiber Fungi and inflammatory bowel diseases: Alterations of composition and diversity Scand. J. Gastroenterol. 43 2008 831 841
32. S. Saijo, N. Fujikado, T. Furuta, S.H. Chung, H. Kotaki, K. Seki, K. Sudo, S. Akira, Y. Adachi, N. Ohno, and et al. Dectin-1 is required for host defense against Pneumocystis carinii but not against Candida albicans Nat. Immunol. 8 2007 39 46
33. A.J. Scupham, L.L. Presley, B. Wei, E. Bent, N. Griffith, M. McPherson, F. Zhu, O. Oluwadara, N. Rao, J. Braun, and J. Borneman Abundant and diverse fungal microbiota in the murine intestine Appl. Environ. Microbiol. 72 2006 793 801
34. M.M. Shah, M. Saio, H. Yamashita, H. Tanaka, T. Takami, T. Ezaki, and N. Inagaki Lactobacillus acidophilus strain L-92 induces CD4(+)CD25(+)Foxp3(+) regulatory T cells and suppresses allergic contact dermatitis Biol. Pharm. Bull. 35 2012 612 616
35. P.R. Taylor, G.D. Brown, D.M. Reid, J.A. Willment, L. Martinez-Pomares, S. Gordon, and S.Y. Wong The beta-glucan receptor, dectin-1, is predominantly expressed on the surface of cells of the monocyte/macrophage and neutrophil lineages J. Immunol. 169 2002 3876 3882
36. P.R. Taylor, S.V. Tsoni, J.A. Willment, K.M. Dennehy, M. Rosas, H. Findon, K. Haynes, C. Steele, M. Botto, S. Gordon, and G.D. Brown Dectin-1 is required for beta-glucan recognition and control of fungal infection Nat. Immunol. 8 2007 31 38
37. P.S. Thiagarajan, V.P. Yakubenko, D.H. Elsori, S.P. Yadav, B. Willard, C.D. Tan, E.R. Rodriguez, M. Febbraio, and M.K. Cathcart Vimentin is an endogenous ligand for the pattern recognition receptor Dectin-1 Cardiovasc. Res. 99 2013 494 504
38. H. Tlaskalová-Hogenová, L. Tucková, R. Stepánková, T. Hudcovic, L. Palová-Jelínková, H. Kozáková, P. Rossmann, D. Sanchez, J. Cinová, T. Hrncír, and et al. Involvement of innate immunity in the development of inflammatory and autoimmune diseases Ann. N Y Acad. Sci. 1051 2005 787 798
39. H.J. Wu, I.I. Ivanov, J. Darce, K. Hattori, T. Shima, Y. Umesaki, D.R. Littman, C. Benoist, and D. Mathis Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells Immunity 32 2010 815 827
40. M. Yang, K. Rui, S. Wang, and L. Lu Regulatory B cells in autoimmune diseases Cell. Mol. Immunol. 10 2013 122 132