Interleukin-10-producing CD5+ B cells inhibit mast cells during immunoglobulin E-mediated allergic responses

Science Signaling

Volumn 8, Issue 368, 2015, Pages ra28-

  Kim, Hyuk Soon ^a   Kim, A Ram ^a   Kim, Do Kyun ^a   Kim, Hyun Woo ^a   Park, Young Hwan ^a   Jang, Geun Hyo ^a   Kim, Bokyung ^a   Park, Yeong Min ^a   You, Jueng Soo ^a   Kim, Hyung Sik ^b   Beaven, Michael A ^c   Kim, Young Mi ^d   Choi, Wahn Soo ^a  

^a Konkuk University School of Medicine   (South Korea)

^b Sungkyunkwan University   (South Korea)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^d Duksung Women's University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; IMMUNOGLOBULIN E; INTERLEUKIN 10; STAT3 PROTEIN; CD40 ANTIGEN; CD5 ANTIGEN; CD5 PROTEIN, MOUSE; FYN PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN KINASE FYN; PROTEIN TYROSINE KINASE; PROTO-ONCOGENE PROTEINS C-FGR; STAT3 PROTEIN, MOUSE;

ALLERGIC REACTION; ANAPHYLAXIS; ARTICLE; B LYMPHOCYTE; CD5+ B LYMPHOCYTE; CELL ACTIVATION; CELL INTERACTION; CYTOKINE PRODUCTION; FLOW CYTOMETRY; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MAST CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; WILD TYPE; ANIMAL; GENETICS; HYPERSENSITIVITY; IMMUNOLOGY; KNOCKOUT MOUSE; MOUSE; PATHOLOGY; SIGNAL TRANSDUCTION;

MUS;

ANIMALS; ANTIGENS, CD40; ANTIGENS, CD5; B-LYMPHOCYTES; HYPERSENSITIVITY; IMMUNOGLOBULIN E; INTERLEUKIN-10; MAST CELLS; MICE; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-FYN; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR;

EID: 84925018269     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2005861     Document Type: Article

References (45)

1. J. Ring, U. Krämer, T. Schäfer, H. Behrendt, Why are allergies increasing? Curr. Opin. Immunol. 13, 701-708 (2001).
2. S. N. Georas, J. Guo, U. De Fanis, V. Casolaro, T-helper cell type-2 regulation in allergic disease. Eur. Respir. J. 26, 1119-1137 (2005).
3. M. J. Nadler, S. A. Matthews, H. Turner, J. P. Kinet, Signal transduction by the high-affinity immunoglobulin E receptor Fc epsilon RI: Coupling form to function. Adv. Immunol. 76, 325-355 (2000).
4. T. W. LeBien, T. F. Tedder, B lymphocytes: How they develop and function. Blood 112, 1570-1580 (2008).
5. T. Matsushita, K. Yanaba, J.-D. Bouaziz, M. Fujimoto, T. F. Tedder, Regulatory B cells inhibit EAE initiation in mice while other B cells promote disease progression. J. Clin. Invest. 118, 3420-3430 (2008).
6. J. G. Evans, K. A. Chavez-Rueda, A. Eddaoudi, A. Meyer-Bahlburg, D. J. Rawlings, M. R. Ehrenstein, C. Mauri, Novel suppressive function of transitional 2 B cells in experimental arthritis. J. Immunol. 178, 7868-7878 (2007).
7. + phenotype controls T cell dependent inflammatory responses. Immunity 28, 639-650 (2008).
8. Q. Ding, M. Yeung, G. Camirand, Q. Zeng, H. Akiba, H. Yagita, G. Chalasani, M. H. Sayegh, N. Najafian, D. M. Rothstein, Regulatory B cells are identified by expression of TIM-1 and can be induced through TIM-1 ligation to promote tolerance in mice. J. Clin. Invest. 121, 3645-3656 (2011).
9. A. Mizoguchi, A. K. Bhan, A case for regulatory B cells. J. Immunol. 176, 705-710 (2006).
10. D. J. DiLillo, T. Matsushita, T. F. Tedder, B10 cells and regulatory B cells balance immune responses during inflammation, autoimmunity, and cancer. Ann. N. Y. Acad. Sci. 1183, 38-57 (2010).
11. N. E. Mangan, R. E. Fallon, P. Smith, N. van Rooijen, A. N. McKenzie, P. G. Fallon, Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J. Immunol. 173, 6346-6356 (2004).
12. S. Amu, S. P. Saunders, M. Kronenberg, N. E. Mangan, A. Atzberger, P. G. Fallon, Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J. Allergy Clin. Immunol. 125, 1114-1124 (2010).
13. C. F. Yeatman 2nd, S. M. Jacobs-Helber, P. Mirmonsef, S. R. Gillespie, L. A. Bouton, H. A. Collins, S. T. Sawyer, C. P. Shelburne, J. J. Ryan, Combined stimulation with the T helper cell type 2 cytokines interleukin (IL)-4 and IL-10 induces mouse mast cell apoptosis. J. Exp. Med. 192, 1093-1103 (2000).
14. S. Kennedy Norton, B. Barnstein, J. Brenzovich, D. P. Bailey, M. Kashyap, K. Speiran, J. Ford, D. Conrad, S. Watowich, M. R. Moralle, C. L. Kepley, P. J. Murray, J. J. Ryan, IL-10 suppresses mast cell IgE receptor expression and signaling in vitro and in vivo. J. Immunol. 180, 2848-2854 (2008).
15. S. J. Galli, M. Grimbaldeston, M. Tsai, Immunomodulatory mast cells: Negative, as well as positive, regulators of immunity. Nat. Rev. Immunol. 8, 478-486 (2008).
16. M. A. Beaven, Our perception of the mast cell from Paul Ehrlich to now. Eur. J. Immunol. 39, 11-25 (2009).
17. A. M. Gilfillan, M. A. Beaven, Regulation of mast cell responses in health and disease. Crit. Rev. Immunol. 31, 475-529 (2011).
18. S. J. Galli, M. Tsai, IgE and mast cells in allergic disease. Nat. Med. 18, 693-704 (2012).
19. S. Merluzzi, B. Frossi, G. Gri, S. Parusso, C. Tripodo, C. Pucillo, Mast cells enhance proliferation of B lymphocytes and drive their differentiation toward IgA-secreting plasma cells. Blood 115, 2810-2817 (2010).
20. K. Hitomi, S. Tahara-Hanaoka, S. Someya, A. Fujiki, H. Tada, T. Sugiyama, S. Shibayama, K. Shibuya, A. Shibuya, An immunoglobulin-like receptor, Allergin-1, inhibits immuno-globulin E-mediated immediate hypersensitivity reactions. Nat. Immunol. 11, 601-607 (2010).
21. S. Constant, N. Schweitzer, J. West, P. Ranney, K. Bottomly, B lymphocytes can be competent antigen-presenting cells for priming CD4+ T cells to protein antigens in vivo. J. Immunol. 155, 3734-3741 (1995).
22. + T cell activation in mice. Proc. Natl. Acad. Sci. U.S.A. 104, 20878-20883 (2007).
23. Y. Xiu, C. P. Wong, J. D. Bouaziz, Y. Hamaguchi, Y. Wang, S. M. Pop, R. M. Tisch, T. F. Tedder, B lymphocyte depletion by CD20 monoclonal antibody prevents diabetes in nonobese diabetic mice despite isotype-specific differences in FcgR effector functions. J. Immunol. 180, 2863-2875 (2008).
24. S. I. Katz, D. Parker, J. L. Turk, B-cell suppression of delayed hypersensitivity reactions. Nature 251, 550-551 (1974).
25. J. Tian, D. Zekzer, L. Hanssen, Y. Lu, A. Olcott, D. L. Kaufman, Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J. Immunol. 167, 1081-1089 (2001).
26. S. C. Wong, A. L. Puaux, M. Chittezhath, I. Shalova, T. S. Kajiji, X. Wang, J. P. Abastado, K. P. Lam, S. K. Biswas, Macrophage polarization to a unique phenotype driven by B cells. Eur. J. Immunol. 40, 2296-2307 (2010).
27. D. F. Fiorentino, M. W. Bond, T. R. Mosmann, Two types of mouse T helper cell IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J. Exp. Med. 170, 2081-2095 (1989).
28. C. Zuany-Amorim, S. Hailé, D. Leduc, C. Dumarey, M. Huerre, B. B. Vargaftig, M. Pretolani, Interleukin-10 inhibits antigen-induced cellular recruitment into the airways of sensitized mice. J. Clin. Invest. 95, 2644-2651 (1995).
29. S. Pestka, C. D. Krause, D. Sarkar, M. R. Walter, Y. Shi, P. B. Fisher, Interleukin-10 and related cytokines and receptors. Annu. Rev. Immunol. 22, 929-979 (2004).
30. M. Grimbaldeston, S. Nakae, J. Kalesnikoff, M. Tsai, S. J. Galli, Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat. Immunol. 8, 1095-1104 (2007).
31. G. Gri, S. Piconese, B. Frossi, V. Manfroi, S. Merluzzi, C. Tripodo, A. Viola, S. Odom, J. Rivera, M. P. Colombo, C. E. Pucillo, CD4+CD25+ regulatory T cells suppress mast cell degranulation and allergic responses through OX40-OX40L interaction. Immunity 29, 771-781 (2008).
32. J. H. Lee, J. Noh, G. Noh, H. S. Kim, S. H. Mun, W. S. Choi, S. Cho, S. Lee, Allergen-specific B cell subset responses in cow's milk allergy of late eczematous reactions in atopic dermatitis. Cell. Immunol. 262, 44-51 (2010).
33. L. Thompson-Snipes, V. Dhar, M. W. Bond, T. R. Mosmann, K. W. Moore, D. M. Rennick, Interleukin 10: A novel stimulatory factor for mast cells and their progenitors. J. Exp. Med. 173, 507-510 (1991).
34. C. M. Hawrylowicz, A. O'Garra, Potential role of interleukin-10-secreting regulatory T cells in allergy and asthma. Nat. Rev. Immunol. 5, 271-283 (2005)
35. I. S. Grewal, R. A. Flavell, CD40 and CD154 in cell-mediated immunity. Annu. Rev. Immunol. 16, 111-135 (1998).
36. J. C. Poe, S. H. Smith, K. M. Haas, K. Yanaba, T. Tsubata, T. Matsushita, T. F. Tedder, Amplified B lymphocyte CD40 signaling drives regulatory B10 cell expansion in mice. PLOS One 6, e22464 (2011).
37. E. Mizoguchi, A. Mizoguchi, F. I. Preffer, A. K. Bhan, Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int. Immunol. 12, 597-605 (2000).
38. Y. Iwata, T. Matsushita, M. Horikawa, D. J. Dilillo, K. Yanaba, G. M. Venturi, P. M. Szabolcs, S. H. Bernstein, C. M. Magro, A. D. Williams, R. P. Hall, E. W. St Clair, T. F. Tedder, Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117, 530-541 (2011).
39. D. Y. Kim, D. Jeoung, J. Y. Ro, Signaling pathways in the activation of mast cells cocul-tured with astrocytes and colocalization of both cells in experimental allergic encephalo-myelitis. J. Immunol. 185, 273-283 (2010).
40. G. U. Hong, B. S. Park, J. W. Park, S. Y. Kim, J. Y. Ro, IgE production in CD40/CD40L cross-talk of B and mast cells and mediator release via TGase 2 in mouse allergic asthma. Cell. Signal. 25, 1514-1525 (2013).
41. M. Yu, C. A. Lowell, B. G. Neel, H. Gu, Scaffolding adapter Grb2-associated binder 2 requires Syk to transmit signals from FceRI. J. Immunol. 176, 2421-2429 (2006).
42. J. H. Lee, J. W. Kim, D. K. Kim, H. S. Kim, H. J. Park, D. K. Park, A. R. Kim, B. Kim, M. A. Beaven, K. L. Park, Y. M. Kim, W. S. Choi, The Src family kinase Fgr is critical for activation of mast cells and IgE-mediated anaphylaxis in mice. J. Immunol. 187, 1807-1815 (2011).
43. A. M. Gilfillan, J. Rivera, The tyrosine kinase network regulating mast cell activation. Immunol. Rev. 228, 149-169 (2009).
44. M. Rådinger, B. M. Jensen, H. S. Kuehn, A. Kirshenbaum, A. M. Gilfillan, Generation, isolation, and maintenance of human mast cells and mast cell lines derived from peripheral blood or cord blood. Curr. Protoc. Immunol. Chap. 7, Unit 7.37 (2010).
45. 2+ and purified isozymes in washed permeabilized cells. J. Biol. Chem. 268, 1749-1756 (1993).