Role of regulatory B cells in immune tolerance to allergens and beyond

Journal of Allergy and Clinical Immunology

Volumn 138, Issue 3, 2016, Pages 654-665

  van de Veen, Willem ^a,b   Stanic, Barbara ^a,c   Wirz, Oliver F ^a   Jansen, Kirstin ^a   Globinska, Anna ^a,d   Akdis, Mübeccel ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b CHRISTINE KÜHNE CENTER FOR ALLERGY RESEARCH AND EDUCATION CK CARE   (Switzerland)

^c AO RESEARCH INSTITUTE   (Switzerland)

^d MEDICAL UNIVERSITY OF LODZ   (Poland)

Author keywords

allergen; autoimmunity; B10; BR1; IgG4; IL 10; IL 35; Regulatory B cells; suppression; TGF ; tolerance

Indexed keywords

ALLERGEN; ALPHA INTERFERON; CD19 ANTIGEN; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 35; INTERLEUKIN 6; KIDNEY INJURY MOLECULE 1; L SELECTIN; PROGRAMMED DEATH 1 LIGAND 1; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TRANSFORMING GROWTH FACTOR BETA;

ALLERGIC AIRWAY INFLAMMATION; ALLERGY; AUTOIMMUNE DISEASE; B LYMPHOCYTE; CANCER PATIENT; CELL THERAPY; CELLS; ENTERITIS; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFECTION; INFLAMMATION; NEOPLASM; NONHUMAN; ORGAN TRANSPLANTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; IMMUNOLOGY; REGULATORY B LYMPHOCYTE;

ALLERGENS; ANIMALS; B-LYMPHOCYTES, REGULATORY; HUMANS; IMMUNE TOLERANCE; INFECTION; INFLAMMATION;

EID: 84995404062     PISSN: 00916749     EISSN: 10976825     Source Type: Journal    
DOI: 10.1016/j.jaci.2016.07.006     Document Type: Review

References (84)

1. 1 Platts-Mills, T.A., The allergy epidemics: 1870-2010. J Allergy Clin Immunol 136 (2015), 3–13.
2. 2 Akdis, M., Akdis, C.A., Mechanisms of allergen-specific immunotherapy: multiple suppressor factors at work in immune tolerance to allergens. J Allergy Clin Immunol 133 (2014), 621–631.
3. 3 Akdis, C.A., Akdis, M., Advances in allergen immunotherapy: aiming for complete tolerance to allergens. Sci Transl Med, 7, 2015, 280ps6.
4. 4 Katz, S.I., Parker, D., Turk, J.L., B-cell suppression of delayed hypersensitivity reactions. Nature 251 (1974), 550–551.
5. 5 Neta, R., Salvin, S.B., Specific suppression of delayed hypersensitivity: the possible presence of a suppressor B cell in the regulation of delayed hypersensitivity. J Immunol 113 (1974), 1716–1725.
6. 6 Goetz, M., Atreya, R., Ghalibafian, M., Galle, P.R., Neurath, M.F., Exacerbation of ulcerative colitis after rituximab salvage therapy. Inflamm Bowel Dis 13 (2007), 1365–1368.
7. 7 Dass, S., Vital, E.M., Emery, P., Development of psoriasis after B cell depletion with rituximab. Arthritis Rheum 56 (2007), 2715–2718.
8. 8 Wolf, S.D., Dittel, B.N., Hardardottir, F., Janeway, C.A. Jr., Experimental autoimmune encephalomyelitis induction in genetically B cell-deficient mice. J Exp Med 184 (1996), 2271–2278.
9. 9 Fillatreau, S., Sweenie, C.H., McGeachy, M.J., Gray, D., Anderton, S.M., B cells regulate autoimmunity by provision of IL-10. Nat Immunol 3 (2002), 944–950.
10. 10 Mizoguchi, A., Mizoguchi, E., Takedatsu, H., Blumberg, R.S., Bhan, A.K., Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16 (2002), 219–230.
11. 11 Mauri, C., Gray, D., Mushtaq, N., Londei, M., Prevention of arthritis by interleukin 10-producing B cells. J Exp Med 197 (2003), 489–501.
12. 12 Shen, P., Roch, T., Lampropoulou, V., O'Connor, R.A., Stervbo, U., Hilgenberg, E., et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature 507 (2014), 366–370.
13. 13 Parekh, V.V., Prasad, D.V., Banerjee, P.P., Joshi, B.N., Kumar, A., Mishra, G.C., B cells activated by lipopolysaccharide, but not by anti-Ig and anti-CD40 antibody, induce anergy in CD8+ T cells: role of TGF-beta 1. J Immunol 170 (2003), 5897–5911.
14. 14 Tian, J., Zekzer, D., Hanssen, L., Lu, Y., Olcott, A., Kaufman, D.L., Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol 167 (2001), 1081–1089.
15. 15 van de Veen, W., Stanic, B., Yaman, G., Wawrzyniak, M., Sollner, S., Akdis, D.G., et al. IgG4 production is confined to human IL-10-producing regulatory B cells that suppress antigen-specific immune responses. J Allergy Clin Immunol 131 (2013), 1204–1212.
16. 16 Khan, A.R., Amu, S., Saunders, S.P., Hams, E., Blackshields, G., Leonard, M.O., et al. Ligation of TLR7 on CD19(+) CD1d(hi) B cells suppresses allergic lung inflammation via regulatory T cells. Eur J Immunol 45 (2015), 1842–1854.
17. 17 Liu, Z.Q., Wu, Y., Song, J.P., Liu, X., Liu, Z., Zheng, P.Y., et al. Tolerogenic CX3CR1+ B cells suppress food allergy-induced intestinal inflammation in mice. Allergy 68 (2013), 1241–1248.
18. 18 van der Vlugt, L.E., Labuda, L.A., Ozir-Fazalalikhan, A., Lievers, E., Gloudemans, A.K., Liu, K.Y., et al. Schistosomes induce regulatory features in human and mouse CD1d(hi) B cells: inhibition of allergic inflammation by IL-10 and regulatory T cells. PLoS One, 7, 2012, e30883.
19. 19 Amu, S., Saunders, S.P., Kronenberg, M., Mangan, N.E., Atzberger, A., Fallon, P.G., Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol 125 (2010), 1114–1124.e8.
20. 20 Singh, A., Carson, W.F., Secor, E.R. Jr., Guernsey, L.A., Flavell, R.A., Clark, R.B., et al. Regulatory role of B cells in a murine model of allergic airway disease. J Immunol 180 (2008), 7318–7326.
21. 21 Smits, H.H., Hammad, H., van Nimwegen, M., Soullie, T., Willart, M.A., Lievers, E., et al. Protective effect of Schistosoma mansoni infection on allergic airway inflammation depends on the intensity and chronicity of infection. J Allergy Clin Immunol 120 (2007), 932–940.
22. 22 Mangan, N.E., Fallon, R.E., Smith, P., van Rooijen, N., McKenzie, A.N., Fallon, P.G., Helminth infection protects mice from anaphylaxis via IL-10-producing B cells. J Immunol 173 (2004), 6346–6356.
23. 23 Evans, J.G., Chavez-Rueda, K.A., Eddaoudi, A., Meyer-Bahlburg, A., Rawlings, D.J., Ehrenstein, M.R., et al. Novel suppressive function of transitional 2 B cells in experimental arthritis. J Immunol 178 (2007), 7868–7878.
24. 24 Matsumoto, M., Baba, A., Yokota, T., Nishikawa, H., Ohkawa, Y., Kayama, H., et al. Interleukin-10-producing plasmablasts exert regulatory function in autoimmune inflammation. Immunity 41 (2014), 1040–1051.
25. 25 Neves, P., Lampropoulou, V., Calderon-Gomez, E., Roch, T., Stervbo, U., Shen, P., et al. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity 33 (2010), 777–790.
26. 26 Yanaba, K., Bouaziz, J.D., Haas, K.M., Poe, J.C., Fujimoto, M., Tedder, T.F., A regulatory B cell subset with a unique CD1dhiCD5+ phenotype controls T cell-dependent inflammatory responses. Immunity 28 (2008), 639–650.
27. 27 Klinker, M.W., Reed, T.J., Fox, D.A., Lundy, S.K., Interleukin-5 supports the expansion of fas ligand-expressing killer B cells that induce antigen-specific apoptosis of CD4(+) T cells and secrete interleukin-10. PLoS One, 8, 2013, e70131.
28. 28 Lundy, S.K., Boros, D.L., Fas ligand-expressing B-1a lymphocytes mediate CD4(+)-T-cell apoptosis during schistosomal infection: induction by interleukin 4 (IL-4) and IL-10. Infect Immun 70 (2002), 812–819.
29. 29 Shalapour, S., Font-Burgada, J., Di Caro, G., Zhong, Z., Sanchez-Lopez, E., Dhar, D., et al. Immunosuppressive plasma cells impede T-cell-dependent immunogenic chemotherapy. Nature 521 (2015), 94–98.
30. 30 Zhang, X.M., Deriaud, E., Jiao, X.N., Braun, D., Leclerc, C., Lo-Man, R., Type I interferons protect neonates from acute inflammation through interleukin 10-producing B cells. J Exp Med 204 (2007), 1107–1118.
31. 31 Kalampokis, I., Yoshizaki, A., Tedder, T.F., IL-10-producing regulatory B cells (B10 cells) in autoimmune disease. Arthritis Res Ther, 15(suppl 1), 2013, S1.
32. 32 Bankoti, R., Gupta, K., Levchenko, A., Stager, S., Marginal zone B cells regulate antigen-specific T cell responses during infection. J Immunol 188 (2012), 3961–3971.
33. 33 Blair, P.A., Chavez-Rueda, K.A., Evans, J.G., Shlomchik, M.J., Eddaoudi, A., Isenberg, D.A., et al. Selective targeting of B cells with agonistic anti-CD40 is an efficacious strategy for the generation of induced regulatory T2-like B cells and for the suppression of lupus in MRL/lpr mice. J Immunol 182 (2009), 3492–3502.
34. 34 Watanabe, R., Ishiura, N., Nakashima, H., Kuwano, Y., Okochi, H., Tamaki, K., et al. Regulatory B cells (B10 cells) have a suppressive role in murine lupus: CD19 and B10 cell deficiency exacerbates systemic autoimmunity. J Immunol 184 (2010), 4801–4809.
35. 35 Yang, M., Deng, J., Liu, Y., Ko, K.H., Wang, X., Jiao, Z., et al. IL-10-producing regulatory B10 cells ameliorate collagen-induced arthritis via suppressing Th17 cell generation. Am J Pathol 180 (2012), 2375–2385.
36. 36 Sheng, J.R., Quan, S., Soliven, B., CD1d(hi)CD5+ B cells expanded by GM-CSF in vivo suppress experimental autoimmune myasthenia gravis. J Immunol 193 (2014), 2669–2677.
37. 37 Yanaba, K., Yoshizaki, A., Asano, Y., Kadono, T., Tedder, T.F., Sato, S., IL-10-producing regulatory B10 cells inhibit intestinal injury in a mouse model. Am J Pathol 178 (2011), 735–743.
38. 38 Wang, R.X., Yu, C.R., Dambuza, I.M., Mahdi, R.M., Dolinska, M.B., Sergeev, Y.V., et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med 20 (2014), 633–641.
39. 39 Lal, G., Kulkarni, N., Nakayama, Y., Singh, A.K., Sethi, A., Burrell, B.E., et al. IL-10 from marginal zone precursor B cells controls the differentiation of Th17, Tfh and Tfr cells in transplantation tolerance. Immunol Lett 170 (2016), 52–63.
40. 40 Shimomura, Y., Mizoguchi, E., Sugimoto, K., Kibe, R., Benno, Y., Mizoguchi, A., et al. Regulatory role of B-1 B cells in chronic colitis. Int Immunol 20 (2008), 729–737.
41. 41 Moreau, A., Blair, P.A., Chai, J.-G., Ratnasothy, K., Stolarczyk, E., Alhabbab, R., et al. Transitional-2 B cells acquire regulatory function during tolerance induction and contribute to allograft survival. Eur J Immunol 45 (2015), 843–853.
42. 42 Rafei, M., Hsieh, J., Zehntner, S., Li, M., Forner, K., Birman, E., et al. A granulocyte-macrophage colony-stimulating factor and interleukin-15 fusokine induces a regulatory B cell population with immune suppressive properties. Nat Med 15 (2009), 1038–1045.
43. 43 Iwata, Y., Matsushita, T., Horikawa, M., DiLillo, D.J., Yanaba, K., Venturi, G.M., et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood 117 (2011), 530–541.
44. 44 Blair, P.A., Norena, L.Y., Flores-Borja, F., Rawlings, D.J., Isenberg, D.A., Ehrenstein, M.R., et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity 32 (2010), 129–140.
45. 45 Das, A., Ellis, G., Pallant, C., Lopes, A.R., Khanna, P., Peppa, D., et al. IL-10-producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J Immunol 189 (2012), 3925–3935.
46. 46 Rosser, E.C., Mauri, C., Regulatory B cells: origin, phenotype, and function. Immunity 42 (2015), 607–612.
47. 47 Akdis, M., Burgler, S., Crameri, R., Eiwegger, T., Fujita, H., Gomez, E., et al. Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. J Allergy Clin Immunol 127 (2011), 701–721 e1-70.
48. 48 Palomares, O., Martin-Fontecha, M., Lauener, R., Traidl-Hoffmann, C., Cavkaytar, O., Akdis, M., et al. Regulatory T cells and immune regulation of allergic diseases: roles of IL-10 and TGF-beta. Genes Immun 15 (2014), 511–520.
49. 49 Yoshizaki, A., Miyagaki, T., DiLillo, D.J., Matsushita, T., Horikawa, M., Kountikov, E.I., et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature 491 (2012), 264–268.
50. 50 Ding, Q., Yeung, M., Camirand, G., Zeng, Q., Akiba, H., Yagita, H., et al. 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 (2011), 3645–3656.
51. 51 Lee, K.M., Kim, J.I., Stott, R., Soohoo, J., O'Connor, M.R., Yeh, H., et al. Anti-CD45RB/anti-TIM-1-induced tolerance requires regulatory B cells. Am J Transplant 12 (2012), 2072–2078.
52. 52 Khan, A.R., Hams, E., Floudas, A., Sparwasser, T., Weaver, C.T., Fallon, P.G., PD-L1hi B cells are critical regulators of humoral immunity. Nat Commun, 6, 2015, 5997.
53. 53 Lampropoulou, V., Hoehlig, K., Roch, T., Neves, P., Calderon Gomez, E., Sweenie, C.H., et al. TLR-activated B cells suppress T cell-mediated autoimmunity. J Immunol 180 (2008), 4763–4773.
54. 54 O'Garra, A., Chang, R., Go, N., Hastings, R., Haughton, G., Howard, M., Ly-1 B (B-1) cells are the main source of B cell-derived interleukin 10. Eur J Immunol 22 (1992), 711–717.
55. 55 Cerutti, A., Cols, M., Puga, I., Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol 13 (2013), 118–132.
56. 56 Gray, M., Miles, K., Salter, D., Gray, D., Savill, J., Apoptotic cells protect mice from autoimmune inflammation by the induction of regulatory B cells. Proc Natl Acad Sci U S A 104 (2007), 14080–14085.
57. 57 Yanaba, K., Bouaziz, J.D., Matsushita, T., Tsubata, T., Tedder, T.F., The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol 182 (2009), 7459–7472.
58. 58 Xiao, S., Brooks, C.R., Sobel, R.A., Kuchroo, V.K., Tim-1 is essential for induction and maintenance of IL-10 in regulatory B cells and their regulation of tissue inflammation. J Immunol 194 (2015), 1602–1608.
59. 59 Matsushita, T., Le Huu, D., Kobayashi, T., Hamaguchi, Y., Hasegawa, M., Naka, K., et al. A novel splenic B1 regulatory cell subset suppresses allergic disease through phosphatidylinositol 3-kinase-Akt pathway activation. J Allergy Clin Immunol, Feb 29, 2016 [E-pub ahead of print].
60. 60 Stanic, B., van de Veen, W., Wirz, O.F., Ruckert, B., Morita, H., Sollner, S., et al. IL-10-overexpressing B cells regulate innate and adaptive immune responses. J Allergy Clin Immunol 135 (2015), 771–780.e8.
61. 61 Rosser, E.C., Oleinika, K., Tonon, S., Doyle, R., Bosma, A., Carter, N.A., et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1beta and interleukin-6 production. Nat Med 20 (2014), 1334–1339.
62. 62 Menon, M., Blair, P.A., Isenberg, D.A., Mauri, C., A regulatory feedback between plasmacytoid dendritic cells and regulatory B cells is aberrant in systemic lupus erythematosus. Immunity 44 (2016), 683–697.
63. 63 Fox, E.M., Torrero, M.N., Evans, H., Mitre, E., Immunologic characterization of 3 murine regimens of allergen-specific immunotherapy. J Allergy Clin Immunol 135 (2015), 1341–1351 e1-7.
64. 64 Meiler, F., Zumkehr, J., Klunker, S., Ruckert, B., Akdis, C.A., Akdis, M., In vivo switch to IL-10-secreting T regulatory cells in high dose allergen exposure. J Exp Med 205 (2008), 2887–2898.
65. 65 Platts-Mills, T., Vaughan, J., Squillace, S., Woodfolk, J., Sporik, R., Sensitisation, asthma, and a modified Th2 response in children exposed to cat allergen: a population-based cross-sectional study. Lancet 357 (2001), 752–756.
66. 66 Reefer, A.J., Carneiro, R.M., Custis, N.J., Platts-Mills, T.A., Sung, S.S., Hammer, J., et al. A role for IL-10-mediated HLA-DR7-restricted T cell-dependent events in development of the modified Th2 response to cat allergen. J Immunol 172 (2004), 2763–2772.
67. 67 Jutel, M., Agache, I., Bonini, S., Burks, A.W., Calderon, M., Canonica, W., et al. International Consensus on Allergen Immunotherapy II: Mechanisms, standardization, and pharmacoeconomics. J Allergy Clin Immunol 137 (2016), 358–368.
68. 68 Jutel, M., Agache, I., Bonini, S., Burks, A.W., Calderon, M., Canonica, W., et al. International consensus on allergy immunotherapy. J Allergy Clin Immunol 136 (2015), 556–568.
69. 69 Akdis, C.A., Blesken, T., Akdis, M., Wuthrich, B., Blaser, K., Role of interleukin 10 in specific immunotherapy. J Clin Invest 102 (1998), 98–106.
70. 70 Brisslert, M., Bokarewa, M., Larsson, P., Wing, K., Collins, L.V., Tarkowski, A., Phenotypic and functional characterization of human CD25+ B cells. Immunology 117 (2006), 548–557.
71. 71 Sattler, S., Ling, G.S., Xu, D., Hussaarts, L., Romaine, A., Zhao, H., et al. IL-10-producing regulatory B cells induced by IL-33 (Breg(IL-33)) effectively attenuate mucosal inflammatory responses in the gut. J Autoimmun 50 (2014), 107–122.
72. 72 Boonpiyathad, T., Meyer, N., Moniuszko, M., Sokolowska, M., Eljaszewicz, A., Wirz, O.F., et al. High-dose bee venom exposure induces similar tolerogenic B cell responses in patients and healthy beekeepers. Allergy, 2016 [Epub ahead of print].
73. 73 Wysocki, C.A., Jiang, Q., Panoskaltsis-Mortari, A., Taylor, P.A., McKinnon, K.P., Su, L., et al. Critical role for CCR5 in the function of donor CD4+CD25+ regulatory T cells during acute graft-versus-host disease. Blood 106 (2005), 3300–3307.
74. 74 van der Neut Kolfschoten, M., Schuurman, J., Losen, M., Bleeker, W.K., Martinez-Martinez, P., Vermeulen, E., et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science 317 (2007), 1554–1557.
75. 75 Braza, F., Chesne, J., Durand, M., Dirou, S., Brosseau, C., Mahay, G., et al. A regulatory CD9(+) B-cell subset inhibits HDM-induced allergic airway inflammation. Allergy 70 (2015), 1421–1431.
76. 76 Natarajan, P., Singh, A., McNamara, J.T., Secor, E.R., Guernsey, L.A., Thrall, R.S., et al. Regulatory B cells from hilar lymph nodes of tolerant mice in a murine model of allergic airway disease are CD5+, express TGF-β, and co-localize with CD4+Foxp3+ T cells. Mucosal Immunol 5 (2012), 691–701.
77. 77 Zhang, H.P., Wu, Y., Liu, J., Jiang, J., Geng, X.R., Yang, G., et al. TSP1-producing B cells show immune regulatory property and suppress allergy-related mucosal inflammation. Sci Rep, 3, 2013, 3345.
78. 78 Shi, Y., Xu, L.Z., Peng, K., Wu, W., Wu, R., Liu, Z.Q., et al. Specific immunotherapy in combination with Clostridium butyricum inhibits allergic inflammation in the mouse intestine. Sci Rep, 5, 2015, 17651.
79. 79 Fallon, P.G., Mangan, N.E., Suppression of TH2-type allergic reactions by helminth infection. Nat Rev Immunol 7 (2007), 220–230.
80. 80 Mangan, N.E., van Rooijen, N., McKenzie, A.N., Fallon, P.G., Helminth-modified pulmonary immune response protects mice from allergen-induced airway hyperresponsiveness. J Immunol 176 (2006), 138–147.
81. 81 Wilson, M.S., Taylor, M.D., O'Gorman, M.T., Balic, A., Barr, T.A., Filbey, K., et al. Helminth-induced CD19+CD23hi B cells modulate experimental allergic and autoimmune inflammation. Eur J Immunol 40 (2010), 1682–1696.
82. 82 Simon, Q., Pers, J.O., Cornec, D., Le Pottier, L., Mageed, R.A., Hillion, S., In-depth characterization of CD24CD38 transitional human B cells reveals different regulatory profiles. J Allergy Clin Immunol 137 (2016), 1577–1584.e10.
83. 83 Flores-Borja, F., Bosma, A., Ng, D., Reddy, V., Ehrenstein, M.R., Isenberg, D.A., et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med, 5, 2013, 173ra23.
84. 84 Zhang, Y., Gallastegui, N., Rosenblatt, J.D., Regulatory B cells in anti-tumor immunity. Int Immunol 27 (2015), 521–530.