Oral tolerance to food-induced systemic anaphylaxis mediated by the C-type lectin SIGNR1

Nature Medicine

Volumn 16, Issue 10, 2010, Pages 1128-1133

  Zhou, Yufeng ^a   Kawasaki, Hirokazu ^a   Hsu, Shih Chang ^a   Lee, Reiko T ^b   Yao, Xu ^a,c   Plunkett, Beverly ^a   Fu, Jinrong ^a   Yang, Kuender ^d   Lee, Yuan C ^b   Huang, Shau Ku ^a,e  

^a JOHNS HOPKINS ASTHMA AND ALLERGY CENTER   (United States)

^b JOHNS HOPKINS UNIVERSITY   (United States)

^c PEKING UNION MEDICAL COLLEGE   (China)

^d CHANG GUNG UNIVERSITY   (Taiwan)

^e KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BOVINE SERUM ALBUMIN; CARBOHYDRATE DERIVATIVE; CD11B ANTIGEN; CD4 ANTIGEN; CELL SURFACE MARKER; CHOLERA TOXIN B SUBUNIT; GAMMA INTERFERON; GLYCOPROTEIN P 15095; GREEN FLUORESCENT PROTEIN; HISTAMINE; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1 ANTIBODY; IMMUNOGLOBULIN G2A ANTIBODY; IMMUNOLOGIC AGENT; IMMUNOLOGICAL ADJUVANT; INTERLEUKIN 10; INTERLEUKIN 10 RECEPTOR; INTERLEUKIN 10 RECEPTOR ANTIBODY; INTERLEUKIN 12P70; INTERLEUKIN 6; LECTIN RECEPTOR; LECTIN RECEPTOR TYPE C; MANNOSIDE; MANNOSIDE 51 BOVINE SERUM ALBUMIN; MYELOID DIFFERENTIATION FACTOR 88; NEOGLYCOPROTEIN; PROTEIN SIGNR 1; RECEPTOR ANTIBODY; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; CELL ADHESION MOLECULE; CELL SURFACE RECEPTOR; DC-SPECIFIC ICAM-3 GRABBING NONINTEGRIN; LECTIN;

ADOPTIVE TRANSFER; ANAPHYLAXIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ARTICLE; BINDING ASSAY; BLOOD VESSEL PERMEABILITY; C3H MOUSE; C57BL 6 MOUSE; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG TARGETING; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; FOOD ALLERGY; GASTROINTESTINAL MUCOSA; HISTAMINE BLOOD LEVEL; IMMUNOCYTOCHEMISTRY; KNOCKOUT MOUSE; LAMINA PROPRIA; MALE; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROVOCATION TEST; RECEPTOR BINDING; REGULATORY T LYMPHOCYTE; SPLEEN CELL; ANIMAL; C57BL MOUSE; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INTESTINE MUCOSA; PHYSIOLOGY; TH1 CELL;

ANAPHYLAXIS; ANIMALS; CELL ADHESION MOLECULES; DENDRITIC CELLS; FEMALE; FOOD HYPERSENSITIVITY; IMMUNE TOLERANCE; INTERLEUKIN-10; INTESTINAL MUCOSA; LECTINS, C-TYPE; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; RECEPTORS, CELL SURFACE; SERUM ALBUMIN, BOVINE; TH1 CELLS;

MUS;

EID: 77957768953     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.2201     Document Type: Article

References (39)

1. Coombes, J.L. & Powrie, F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8, 435-446 (2008).
2. Chehade, M. & Mayer, L. Oral tolerance and its relation to food hypersensitivities. J. Allergy Clin. Immunol. 115, 3-12 (2005).
3. Poulsen, L.K. In search of a new paradigm: mechanisms of sensitization and elicitation of food allergy. Allergy 60, 549-558 (2005).
4. Finkelman, F.D. Anaphylaxis: lessons from mouse models. J. Allergy Clin. Immunol. 120, 506-515 (2007).
5. Izcue, A., Coombes, J.L. & Powrie, F. Regulatory lymphocytes and intestinal infammation. Annu. Rev. Immunol. 27, 313-338 (2009).
6. Mowat, A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 3, 331-341 (2003).
7. Chirdo, F.G., Millington, O.R., Beacock-Sharp, H. & Mowat, A.M. Immunomodulatory dendritic cells in intestinal lamina propria. Eur. J. Immunol. 35, 1831-1840 (2005).
8. Spahn, T.W. et al. Mesenteric lymph nodes are critical for the induction of high-dose oral tolerance in the absence of Peyer's patches. Eur. J. Immunol. 32, 1109-1113 (2002).
9. Worbs, T. et al. Oral tolerance originates in the intestinal immune system and relies on antigen carriage by dendritic cells. J. Exp. Med. 203, 519-527 (2006).
10. Rescigno, M. et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat. Immunol. 2, 361-367 (2001).
11. Fontenot, J.D. & Rudensky, A.Y. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat. Immunol. 6, 331-337 (2005).
12. Taams, L.S. et al. Regulatory T cells in human disease and their potential for therapeutic manipulation. Immunology 118, 1-9 (2006).
13. Taylor, A., Verhagen, J., Blaser, K., Akdis, M. & Akdis, C.A. Mechanisms of immune suppression by interleukin-10 and transforming growth factor-β: the role of T regulatory cells. Immunology 117, 433-442 (2006).
14. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007).
15. reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
16. + DC, with a plasmacytoid phenotype, induce differentiation and support function of T cells with regulatory properties. Immunology 108, 481-492 (2003).
17. Takeda, K., Kaisho, T. & Akira, S. Toll-like receptors. Annu. Rev. Immunol. 21, 335-376 (2003).
18. van Kooyk, Y. & Rabinovich, G.A. Protein-glycan interactions in the control of innate and adaptive immune responses. Nat. Immunol. 9, 593-601 (2008).
19. Cambi, A. & Figdor, C.G. Levels of complexity in pathogen recognition by C-type lectins. Curr. Opin. Immunol. 17, 345-351 (2005).
20. McGreal, E.P., Miller, J.L. & Gordon, S. Ligand recognition by antigen-presenting cell C-type lectin receptors. Curr. Opin. Immunol. 17, 18-24 (2005).
21. Koppel, E.A., van Gisbergen, K.P., Geijtenbeek, T.B. & van Kooyk, Y. Distinct functions of DC-SIGN and its homologues L-SIGN (DC-SIGNR) and mSIGNR1 in pathogen recognition and immune regulation. Cell. Microbiol. 7, 157-165 (2005).
22. Takahara, K. et al. Functional comparison of the mouse DC-SIGN, SIGNR1, SIGNR3 and langerin, C-type lectins. Int. Immunol. 16, 819-829 (2004).
23. Galustian, C. et al. High and low affnity carbohydrate ligands revealed for murine SIGN-R1 by carbohydrate array and cell binding approaches, and differing specifcities for SIGN-R3 and langerin. Int. Immunol. 16, 853-866 (2004).
24. Roy, K., Mao, H.Q., Huang, S.K. & Leong, K.W. Oral gene delivery with chitosan-DNA nanoparticles generates immunologic protection in a murine model of peanut allergy. Nat. Med. 5, 387-391 (1999).
25. Lee, R.T. & Lee, Y.C. Neoglycoproteins. in Glycoproteins II (eds. Montreuil, J., Vliegenthart, J.F.G. & Schachter, H.) 601-620 (Elsevier, Amsterdam, 1997).
26. Stowell, C.P. & Lee, Y.C. Neoglycoproteins: the preparation and application of synthetic glycoproteins. Adv. Carbohydr. Chem. Biochem. 37, 225-281 (1980).
27. Numazaki, M. et al. Cross-linking of SIGNR1 activates JNK and induces TNF-α production in RAW264.7 cells that express SIGNR1. Biochem. Biophys. Res. Commun. 386, 202-206 (2009).
28. Kamanaka, M. et al. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25, 941-952 (2006).
29. Jang, M.H. et al. CCR7 is critically important for migration of dendritic cells in intestinal lamina propria to mesenteric lymph nodes. J. Immunol. 176, 803-810 (2006).
30. Awasthi, A. et al. A dominant function for interleukin 27 in generating interleukin 10-producing anti-infammatory T cells. Nat. Immunol. 8, 1380-1389 (2007).
31. Dillon, S. et al. Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928 (2006).
32. + T cell tolerance. J. Exp. Med. 196, 1627-1638 (2002).
33. Geijtenbeek, T.B. et al. Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17 (2003).
34. Ilarregui, J.M. et al. Tolerogenic signals delivered by dendritic cells to T cells through a galectin-1-driven immunoregulatory circuit involving interleukin 27 and interleukin 10. Nat. Immunol. 10, 981-991 (2009).
35. Fujikado, N. et al. Dcir defciency causes development of autoimmune diseases in mice due to excess expansion of dendritic cells. Nat. Med. 14, 176-180 (2008).
36. Mine, Y. & Yang, M. Recent advances in the understanding of egg allergens: basic, industrial and clinical perspectives. J. Agric. Food Chem. 56, 4874-4900 (2008).
37. Arslanoglu, S. et al. Early dietary intervention with a mixture of prebiotic oligosaccharides reduces the incidence of allergic manifestations and infections during the frst two years of life. J. Nutr. 138, 1091-1095 (2008).
38. Bashir, M.E., Andersen, P., Fuss, I.J., Shi, H.N. & Nagler-Anderson, C. An enteric helminth infection protects against an allergic response to dietary antigen. J. Immunol. 169, 3284-3292 (2002).
39. Hsu, S.C. et al. Functional interaction of common allergens and a C-type lectin receptor, DC-specifc ICAM3-grabbing non-integrin (DC-SIGN), on human dendritic cells. J. Biol. Chem. 285, 7903-7910 (2010).