Dendritic cell-bound IgE functions to restrain allergic inflammation at mucosal sites

Mucosal Immunology

Volumn 8, Issue 3, 2015, Pages 516-532

  Platzer, B ^a   Baker, K ^b   Vera, M P ^b   Singer, K ^a   Panduro, M ^a   Lexmond, W S ^a   Turner, D ^c   Vargas, S O ^c   Kinet, J P ^c   Maurer, D ^d   Baron, R M ^b   Blumberg, R S ^b   Fiebiger, E ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d Universitatsklinik fur Dermatologie   (Austria)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; FC RECEPTOR; IMMUNOGLOBULIN E; LIPOPOLYSACCHARIDE; PAPAIN; ALLERGEN; CROSS LINKING REAGENT; FCEPSILONRI ALPHA-CHAIN, HUMAN; IMMUNOGLOBULIN E RECEPTOR; OVALBUMIN; PROTEIN BINDING;

ALLERGIC REACTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTHMA; BASOPHIL; CELL MATURATION; CONTROLLED STUDY; CROSS LINKING; CYTOKINE PRODUCTION; DENDRITIC CELL; FEEDBACK SYSTEM; FOOD ALLERGY; HUMAN; HUMAN CELL; IMMUNOREGULATION; IN VIVO STUDY; MAST CELL; MOUSE; NONHUMAN; NORMAL HUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; CELL MIGRATION ASSAY; CELL MOTION; CHEMISTRY; DRUG EFFECTS; EGG ALLERGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; MUCOSAL IMMUNITY; PATHOLOGY; PRIMARY CELL CULTURE; SECRETION (PROCESS); TRANSGENIC MOUSE;

ALLERGENS; ANIMALS; ASTHMA; CELL MIGRATION ASSAYS; CELL MOVEMENT; CROSS-LINKING REAGENTS; CYTOKINES; DENDRITIC CELLS; EGG HYPERSENSITIVITY; FEEDBACK, PHYSIOLOGICAL; GENE EXPRESSION REGULATION; HUMANS; IMMUNITY, MUCOSAL; IMMUNOGLOBULIN E; LIPOPOLYSACCHARIDES; MAST CELLS; MICE; MICE, TRANSGENIC; OVALBUMIN; PAPAIN; PRIMARY CELL CULTURE; PROTEIN BINDING; RECEPTORS, IGE; SIGNAL TRANSDUCTION;

EID: 84928885641     PISSN: 19330219     EISSN: 19353456     Source Type: Journal    
DOI: 10.1038/mi.2014.85     Document Type: Article

References (79)

1. Pawankar, R., Canonica, G.W., Holgate, S.T. & Lockey, R.F. Allergic diseases and asthma: a major global health concern. Curr. Opin. Allergy Clin. Immunol. 12, 39-41 (2012).
2. Gould, H.J. & Sutton, B.J. IgE in allergy and asthma today. Nat. Rev. Immunol. 8, 205-217 (2008).
3. Galli, S.J. & Tsai, M. IgE and mast cells in allergic disease. Nat. Med. 18, 693-704 (2012).
4. Kinet, J.P. The essential role of mast cells in orchestrating inflammation. Immunol. Rev. 217, 5-7 (2007).
5. Cruse, G. et al. A truncated splice-variant of the FcepsilonRIbeta receptor subunit is critical formicrotubule formation and degranulation inmast cells. Immunity 38, 906-917 (2013).
6. Maurer, D. et al. Peripheral blood dendritic cells express Fc epsilon RI as a complex composed of Fc epsilon RI alpha-and Fc epsilon RI gammachains and can use this receptor for IgE-mediated allergen presentation. J. Immunol. 157, 607-616 (1996).
7. Cheung, D.S. et al. Cutting edge: CD49d+ neutrophils induce FcepsilonRI expression on lung dendritic cells in a mouse model of postviral asthma. J Immunol 185, 4983-4987 (2010).
8. Maurer, D. et al. Expression of functional high affinity immunoglobulin E receptors (Fc epsilon RI) on monocytes of atopic individuals. J. Exp. Med. 179, 745-750 (1994).
9. Aaij, R. et al. Search for the lepton-flavor-violating decays B(s)0-gt;4e(+/-)mu(-/+) and B0->4e(+/-)mu(-/+). Phys. Rev. Lett. 111, 141801 (2013).
10. Porcherie, A. et al. Critical role of the neutrophil-associated high-affinity receptor for IgE in the pathogenesis of experimental cerebral malaria. J. Exp. Med. 208, 2225-2236 (2011).
11. Dehlink, E., Baker, A.H., Yen, E., Nurko, S. & Fiebiger, E. Relationships between levels of serum IgE, cell-bound IgE, and IgE-receptors on peripheral blood cells in a pediatric population. PloS One 5, e12204 (2010).
12. Vasudev, M. et al. Expression of high-affinity IgE receptor on human peripheral blood dendritic cells in children. PloS One 7, e32556 (2012).
13. Holloway, J.A., Holgate, S.T. & Semper, A.E. Expression of the high-affinity IgE receptor on peripheral blood dendritic cells: differential binding of IgE in atopic asthma. J. Allergy Clin. Immunol. 107, 1009-1018 (2001).
14. Pulendran, B., Tang, H. & Manicassamy, S. Programming dendritic cells to induce T(H)2 and tolerogenic responses. Nat Immunol 11, 647-655 (2010).
15. Gill, M.A. The role of dendritic cells in asthma. J. Allergy Clin. Immunol. 129, 889-901 (2012).
16. Ruiter, B. & Shreffler, W.G. The role of dendritic cells in food allergy. J. Allergy Clin. Immunol. 129, 921-928 (2012).
17. van Rijt, L.S. & Lambrecht, B.N. Dendritic cells in asthma: a function beyond sensitization. Clin. Exp. Allergy 35, 1125-1134 (2005).
18. van Rijt, L.S. et al. In vivo depletion of lung CD11c+ dendritic cells during allergen challenge abrogates the characteristic features of asthma. J. Exp. Med. 201, 981-991 (2005).
19. Lambrecht, B.N. Dendritic cells and the regulation of the allergic immune response. Allergy 60, 271-282 (2005).
20. Nakano, H. et al. Pulmonary CD103(+) dendritic cells prime Th2 responses to inhaled allergens. Mucosal Immunol 5, 53-65 (2012).
21. Colonna, M., Pulendran, B. & Iwasaki, A. Dendritic cells at the hostpathogen interface. Nat. Immunol. 7, 117-120 (2006).
22. Hammad, H. et al. Inflammatory dendritic cells-not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J. Exp. Med. 207, 2097-2111 (2010).
23. Gao, Y. et al. Control of T helper 2 responses by transcription factor IRF4-dependent dendritic cells. Immunity 39, 722-732 (2013).
24. Paul, W.E. & Zhu, J. How are T(H)2-type immune responses initiated and amplified?. Nat. Rev. Immunol. 10, 225-235 (2010).
25. Novak, N. et al. Fcepsilon RI engagement of Langerhans cell-like dendritic cells and inflammatory dendritic epidermal cell-like dendritic cells induces chemotactic signals and different T-cell phenotypes in vitro. J. Allergy Clin. Immunol. 113, 949-957 (2004).
26. Kraft, S., Wessendorf, J.H., Hanau, D. & Bieber, T. Regulation of the high affinity receptor for IgE on human epidermal Langerhans cells. J. Immunol. 161, 1000-1006 (1998).
27. Novak, N. et al. Evidence for a differential expression of the FcepsilonRIgamma chain in dendritic cells of atopic and nonatopic donors. J. Clin. Invest. 111, 1047-1056 (2003).
28. Prussin, C. et al. Omalizumab treatment downregulates dendritic cell FcepsilonRI expression. J. Allergy Clin. Immunol. 112, 1147-1154 (2003).
29. Foster, B., Metcalfe, D.D. & Prussin, C. Human dendritic cell 1 and dendritic cell 2 subsets express FcepsilonRI: correlation with serum IgE and allergic asthma. J. Allergy Clin. Immunol. 112, 1132-1138 (2003).
30. Greer, A.M. et al. Serum IgE clearance is facilitated by human FcepsilonRI internalization. J. Clin. Invest. 124, 1187-1198 (2014).
31. Sallmann, E. et al. High-affinity IgE receptors on dendritic cells exacerbate Th2-dependent inflammation. J. Immunol. 187, 164-171 (2011).
32. Amoah, A.S. et al. Peanut-specific IgE antibodies in asymptomatic Ghanaian children possibly caused by carbohydrate determinant cross-reactivity. J. Allergy Clin. Immunol. 132, 639-647 (2013).
33. Robbins, S.H. et al. Novel insights into the relationships between dendritic cell subsets in human and mouse revealed by genome-wide expression profiling. Genome Biol. 9, R17 (2008).
34. Crozat, K. et al. Comparative genomics as a tool to reveal functional equivalences between human andmouse dendritic cell subsets. Immunol. Rev. 234, 177-198 (2010).
35. Gilfillan, A.M. & Rivera, J. The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228, 149-169 (2009).
36. Dombrowicz, D. et al. Anaphylaxis mediated through a humanized high affinity IgE receptor. J. Immunol. 157, 1645-1651 (1996).
37. Nakajima, T. et al. Gene expression screening of human mast cells and eosinophils using high-density oligonucleotide probe arrays: abundant expression of major basic protein in mast cells. Blood 98, 1127-1134 (2001).
38. Geiss, G.K. et al. Direct multiplexed measurement of gene expression with color-coded probe pairs. Nat. Biotechnol. 26, 317-325 (2008).
39. Ahrens, R. et al. Intestinal mast cell levels control severity of oral antigeninduced anaphylaxis in mice. Am. J. Pathol. 180, 1535-1546 (2012).
40. Grayson, M.H. et al. Induction of high-affinity IgE receptor on lung dendritic cells during viral infection leads to mucous cell metaplasia. J. Exp. Med. 204, 2759-2769 (2007).
41. Khodoun, M.V., Strait, R., Armstrong, L., Yanase, N. & Finkelman, F.D. Identification of markers that distinguish IgE-from IgG-mediated anaphylaxis. Proc. Natl. Acad. Sci. U S A 108, 12413-12418 (2011).
42. Williams, C.M. & Galli, S.J. Mast cells can amplify airway reactivity and features of chronic inflammation in an asthma model in mice. J. Exp. Med. 192, 455-462 (2000).
43. Yu, M. et al. Mast cells can promote the development of multiple features of chronic asthma in mice. J. Clin. Invest. 116, 1633-1641 (2006).
44. Willart, M.A. et al. Interleukin-1alpha controls allergic sensitization to inhaled house dust mite via the epithelial release of GM-CSF and IL-33. J. Exp. Med. 209, 1505-1517 (2012).
45. Dombrowicz, D. et al. Absence of Fc epsilonRI alpha chain results in upregulation of Fc gammaRIII-dependent mast cell degranulation and anaphylaxis. Evidence of competition between Fc epsilonRI and Fc gammaRIII for limiting amounts of FcR beta and gamma chains. J. Clin. Invest. 99, 915-925 (1997).
46. Novak, N., Kraft, S. & Bieber, T. Unraveling the mission of FcepsilonRI on antigen-presenting cells. J. Allergy Clin. Immunol. 111, 38-44 (2003).
47. Maurer, D. et al. The high affinity IgE receptor (Fc epsilon RI) mediates IgE-dependent allergen presentation. J Immunol 154, 6285-6290 (1995).
48. Tang, H. et al. The T helper type 2 response to cysteine proteases requires dendritic cell-basophil cooperation via ROS-mediated signaling. Nat. Immunol. 11, 608-617 (2010).
49. Eisenbarth, S.C. et al. Lipopolysaccharide-enhanced, toll-like receptor 4-dependent T helper cell type 2 responses to inhaled antigen. J. Exp. Med. 196, 1645-1651 (2002).
50. Aloulou, M. et al. IgG1 and IVIg induce inhibitory ITAM signaling through FcgammaRIII controlling inflammatory responses. Blood 119, 3084-3096 (2012).
51. Chensue, S.W. et al. Role of monocyte chemoattractant protein-1 (MCP-1) in Th1 (mycobacterial) and Th2 (schistosomal) antigen-induced granuloma formation: relationship to local inflammation, Th cell expression, and IL-12 production. J. Immunol. 157, 4602-4608 (1996).
52. Collington, S.J. et al. The role of the CCL2/CCR2 axis in mouse mast cell migration in vitro and in vivo. J. Immunol. 184, 6114-6123 (2010).
53. Taub, D. et al. Bone marrow-derived murine mast cells migrate, but do not degranulate, in response to chemokines. J. Immunol. 154, 2393-2402 (1995).
54. Taub, D.D. et al. Monocyte chemotactic protein-1 (MCP-1), -2, and -3 are chemotactic for human T lymphocytes. J. Clin. Invest. 95, 1370-1376 (1995).
55. Legrand, N. et al. Humanized mice for modeling human infectious disease: challenges, progress, and outlook. Cell Host Microbe 6, 5-9 (2009).
56. Greer, A.M. et al. Serum IgE clearance is facilitated by human FcepsilonRI internalization. J. Clin. Invest. 124, 1187-1198 (2014).
57. Campbell, E.M. et al. Monocyte chemoattractant protein-1 mediates cockroach allergen-induced bronchial hyperreactivity in normal but not CCR2-/- mice: the role of mast cells. J. Immunol. 163, 2160-2167 (1999).
58. Conti, P. et al. Impact of Rantes and MCP-1 chemokines on in vivo basophilic cell recruitment in rat skin injection model and their role in modifying the protein and mRNA levels for histidine decarboxylase. Blood 89, 4120-4127 (1997).
59. Hallgren, J. & Gurish, M.F. Mast cell progenitor trafficking and maturation. Adv. Exp. Med. Biol. 716, 14-28 (2011).
60. Rose, C.E. Jr, Sung, S.S. & Fu, S.M. Significant involvement of CCL2 (MCP- 1) in inflammatory disordersof the lung. Microcirculation 10, 273-288 (2003).
61. Blank, U., Launay, P., Benhamou, M. & Monteiro, R.C. Inhibitory ITAMs as novel regulators of immunity. Immunol. Rev. 232, 59-71 (2009).
62. Blasius, A.L., Cella, M., Maldonado, J., Takai, T. & Colonna, M. Siglec-H is an IPC-specific receptor that modulates type I IFN secretion through DAP12. Blood 107, 2474-2476 (2006).
63. Fuchs, A., Cella, M., Kondo, T. & Colonna, M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 106, 2076-2082 (2005).
64. Cao, W. et al. Plasmacytoid dendritic cell-specific receptor ILT7-Fc epsilonRI gamma inhibits Toll-like receptor-induced interferon production. J. Exp. Med. 203, 1399-1405 (2006).
65. Rock, J. et al. CD303 (BDCA-2) signals in plasmacytoid dendritic cells via a BCR-like signalosome involving Syk, Slp65 and PLCgamma2. Eur. J. Immunol. 37, 3564-3575 (2007).
66. Pfirsch-Maisonnas, S. et al. Inhibitory ITAM signaling traps activating receptors with the phosphatase SHP-1 to form polarized "inhibisome" clusters. Sci. Signal. 4, ra24 (2011).
67. Wang, L. et al. Indirect inhibition of Toll-like receptor and type I interferon responses by ITAM-coupled receptors and integrins. Immunity 32, 518-530 (2010).
68. Han, C. et al. Integrin CD11b negatively regulates TLR-triggered inflammatory responses by activating Syk and promoting degradation of MyD88 and TRIF via Cbl-b. Nat. Immunol. 11, 734-742 (2010).
69. Lin, Y.C., Huang, D.Y., Chu, C.L., Lin, Y.L. & Lin, W.W. The tyrosine kinase Syk differentially regulates Toll-like receptor signaling downstream of the adaptor molecules TRAF6 and TRAF3. Sci. Signal. 6, ra71 (2013).
70. Hamerman, J.A. & Lanier, L.L. Inhibition of immune responses by ITAMbearing receptors. Sci. STKE 2006, re1 (2006).
71. Pasquier, B. et al. Identification of FcalphaRI as an inhibitory receptor that controls inflammation: dual role of FcRgamma ITAM. Immunity 22, 31-42 (2005).
72. Baravalle, G., Greer, A.M., Laflam, T.N. & Shin, J.S. Antigen-conjugated human IgE induces antigen-specific Tcell tolerance in a humanized mouse model. J. Immunol. 192, 3280-3288 (2014).
73. Maizels, R.M., Hewitson, J.P. & Smith, K.A. Susceptibility and immunity to helminth parasites. Curr. Opin. Immunol. 24, 459-466 (2012).
74. Gause, W.C., Wynn, T.A. & Allen, J.E. Type 2 immunity and wound healing: evolutionary refinement of adaptive immunity by helminths. Nat. Rev. Immunol. 13, 607-614 (2013).
75. Brasel, K., De Smedt, T., Smith, J.L. & Maliszewski, C.R. Generation of murine dendritic cells from flt3-ligand-supplemented bone marrow cultures. Blood 96, 3029-3039 (2000).
76. Naik, S.H. et al. Development of plasmacytoid and conventional dendritic cell subtypes from single precursor cells derived in vitro and in vivo. Nat. Immunol. 8, 1217-1226 (2007).
77. Brandt, E.B. et al. Mast cells are required for experimental oral allergeninduced diarrhea. J. Clin. Invest. 112, 1666-1677 (2003).
78. Lai, P.S. et al. Chronic endotoxin exposure produces airflow obstruction and lung dendritic cell expansion. Am. J. Respir. Cell. Mol. Biol. 47, 209-217 (2012).
79. Bannert, C. et al. Fc-Epsilon-RI, the high affinity IgE-receptor, is robustly expressed in the upper gastrointestinal tract and modulated by mucosal inflammation. PloS One 7, e42066 (2012).