Roles of regulatory B cells in the pathogenesis of allergic rhinitis
Main Article Content
Keywords
allergic rhinitis, IL-10, regulatory B cells, TGF-β
Abstract
Allergic rhinitis (AR) is a common otolaryngologic disease with frequent episodes of sneezing, clear nasal discharge flow and nasal congestion. The mechanisms of AR are complex and considered generally caused by the immune tolerance deficiency. Regulatory B cells (Bregs) are immunosuppressive cells that can modulate immune responses by the secretion of IL-10, IL-35, and tumor growth factor-β (TGF-β) and via the interaction of membrane surface molecules. However, Bregs are numerically deficient and/or dysfunctional in airway allergic diseases such as AR and allergic asthma, and the related mechanisms remain unclear. In this review, we summarize the role of Bregs in AR pathogenesis and highlight the importance of Bregs in maintaining immune tolerance. It is believed that further research on Bregs will contribute to developing new treatments and finding specific biomarkers that could help to predict disease progression.
References
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2. Yao Y, Wang ZC, Wang N, Zhou PC, Chen CL, Song J, et al. Allergen immunotherapy improves defective follicular regulatory T cells in patients with allergic rhinitis. J Allergy Clin Immunol. 2019;144:118–28. 10.1016/j.jaci.2019.02.008
3. Palomares O, Akdis M, Martin-Fontecha M, Akdis CA. Mechanisms of immune regulation in allergic diseases: the role of regulatory T and B cells. Immunol Rev. 2017;278: 219–36. 10.1111/imr.12555
4. Xu LZ, Yang LT, Qiu SQ, Yang G, Luo XQ, Miao BP, et al. Combination of specific allergen and probiotics induces specific regulatory B cells and enhances specific immunotherapy effect on allergic rhinitis. Oncotarget. 2016;7:54360–9. 10.18632/oncotarget.10946
5. Yanaba K, Bouaziz JD, Haas KM, Poe JC, Fujimoto M, Tedder TF. A regulatory B cell subset with a unique CD1dhiCD5+ pheno-type controls T cell-dependent inflammatory responses. Immunity. 2008;28:639–50. 10.1016/j.immuni.2008.03.017
6. Cerutti A, Cols M, Puga I. Marginal zone B cells: virtues of innate-like antibody-producing lymphocytes. Nat Rev Immunol. 2013;13:118–32. 10.1038/nri3383
7. Rosser EC, Oleinika K, Tonon S, Doyle R, Bosma A, Carter NA, et al. Regulatory B cells are induced by gut microbiota-driven interleukin-1beta and interleukin-6 production. Nat Med. 2014;20:1334–39. 10.1038/nm.3680
8. Xu C, Zhang M, Li K, Ni M, Bai Y, Zhang J, et al. CD24(hi)CD38(hi) B regulatory cells from patients with end plate inflammation presented reduced functional potency. Int Immunopharmacol. 2019;70:295–301. 10.1016/j.intimp.2019.02.034
9. Kala M, Rhodes SN, Piao WH, Shi FD, Campagnolo DI, Vollmer TL. B cells from glatiramer acetate-treated mice suppress experi-mental autoimmune encephalomyelitis. Exp Neurol. 2010;221: 136–45. 10.1016/j.expneurol.2009.10.015
10. Lampropoulou V, Calderon-Gomez E, Roch T, Neves P, Shen P, Stervbo U, et al. Suppressive functions of activated B cells in autoimmune diseases reveal the dual roles of Toll-like receptors in immunity. Immunol Rev. 2010;233:146–61. 10.1111/j.0105-2896.2009.00855.x
11. van de Veen W, Stanic B, Wirz OF, Jansen K, Globinska A, Akdis M. Role of regulatory B cells in immune tolerance to allergens and beyond. J Allergy Clin Immunol. 2016;138:654–65. 10.1016/j.jaci.2016.07.006
12. Matsushita T, Horikawa M, Iwata Y, Tedder TF. Regulatory B cells (B10 cells) and regulatory T cells have independent roles in controlling experimental autoimmune encephalomyelitis initiation and late-phase immunopathogenesis. J Immunol. 2010;185:2240–52. 10.4049/jimmunol.1001307
13. Wong SC, Puaux AL, Chittezhath M, Shalova I, Kajiji TS, Wang X, et al. Macrophage polarization to a unique phenotype driven by B cells. Eur J Immunol. 2010;40:2296–307. 10.1002/eji.200940288
14. Walter MR. The molecular basis of IL-10 function: from receptor structure to the onset of signaling. Curr Top Microbiol Immunol. 2014;380:191–212. 10.1007/978-3-662-43492-5_9
15. Ouyang W, Rutz S, Crellin NK, Valdez PA, Hymowitz SG. Regulation and functions of the IL-10 family of cytokines in inflammation and disease. Annu Rev Immunol. 2011;29:71–109. 10.1146/annurev-immunol-031210-101312
16. Tamayo E, Alvarez P, Merino R. TGFbeta superfamily members as regulators of B cell development and function-implications for autoimmunity. Int J Mol Sci. 2018;19:3928. 10.3390/ijms19123928
17. Huai G, Markmann JF, Deng S, Rickert CG. TGF-beta-secreting regulatory B cells: unsung players in immune regulation. Clin Transl Immunology. 2021;10:e1270. 10.1002/cti2.1270
18. Collison LW, Delgoffe GM, Guy CS, Vignali KM, Chaturvedi V, Fairweather D, et al. The composition and signaling of the IL-35 receptor are unconventional. Nat Immunol. 2012;13: 290–9. 10.1038/ni.2227
19. Wang RX, Yu CR, Dambuza IM, Mahdi RM, Dolinska MB, Sergeev YV, et al. Interleukin-35 induces regulatory B cells that suppress autoimmune disease. Nat Med. 2014;20:633–41. 10.1038/nm.3554
20. Huang A, Cheng L, He M, Nie J, Wang J, Jiang K. Interleukin-35 on B cell and T cell induction and regulation. J Inflamm. 2017;14:16. 10.1186/s12950-017-0164-5
21. Wirtz S, Billmeier U, McHedlidze T, Blumberg RS, Neurath MF. Interleukin-35 mediates mucosal immune responses that protect against T-cell-dependent colitis. Gastroenterology. 2011;141:1875–86. 10.1053/j.gastro.2011.07.040
22. Lindner S, Dahlke K, Sontheimer K, Hagn M, Kaltenmeier C, Barth TF, et al. Interleukin 21-induced granzyme B-expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013;73:2468–79. 10.1158/0008-5472.CAN-12-3450
23. Amu S, Saunders SP, Kronenberg M, Mangan NE, Atzberger A, Fallon PG. Regulatory B cells prevent and reverse allergic airway inflammation via FoxP3-positive T regulatory cells in a murine model. J Allergy Clin Immunol. 2010;125:1114–24. 10.1016/j.jaci.2010.01.018
24. Mizoguchi E, Mizoguchi A, Preffer FI, Bhan AK. Regulatory role of mature B cells in a murine model of inflammatory bowel disease. Int Immunol. 2000;12:597–605. 10.1093/intimm/12.5.597
25. Fife BT, Bluestone JA. Control of peripheral T-cell tolerance and autoimmunity via the CTLA-4 and PD-1 pathways. Immunol Rev. 2008;224:166–82. 10.1111/j.1600-065X.2008.00662.x
26. Ren X, Akiyoshi K, Vandenbark AA, Hurn PD, Offner H. Programmed death-1 pathway limits central nervous system inflammation and neurologic deficits in murine experimental stroke. Stroke. 2011;42:2578–83. 10.1161/STROKEAHA.111.613182
27. Khan AR, Hams E, Floudas A, Sparwasser T, Weaver CT, Fallon PG. PD-L1hi B cells are critical regulators of humoral immunity. Nat Commun. 2015;6:5997. 10.1038/ncomms6997
28. Yoshizaki A, Miyagaki T, DiLillo DJ, Matsushita T, Horikawa M, Kountikov EI, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 2012;491:264–8. 10.1038/nature11501
29. Lee KM, Kim JI, Stott R, Soohoo J, O’Connor MR, Yeh H, et al. Anti-CD45RB/anti-TIM-1-induced tolerance requires regulatory B cells. Am J Transplant. 2012;12:2072–8. 10.1111/j.1600-6143.2012.04055.x
30. Lundberg K, Rydnert F, Broos S, Andersson M, Greiff L, Lindstedt M. C-type lectin receptor expression on human basophils and effects of allergen-specific immunotherapy. Scand J Immunol. 2016;84:150–7. 10.1111/sji.12457
31. van der Vlugt LE, Mlejnek E, Ozir-Fazalalikhan A, Janssen Bonas M, Dijksman TR, Labuda LA, et al. CD24(hi)CD27(+) B cells from patients with allergic asthma have impaired regulatory activity in response to lipopolysaccharide. Clin Exp Allergy. 2014;44:517–28. 10.1111/cea.12238
32. 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. 2015;70:1421–31. 10.1111/all.12697
33. Natarajan P, Singh A, McNamara JT, Secor ER Jr., Guernsey LA, Thrall RS, et al. Regulatory B cells from hilar lymph nodes of tolerant mice in a murine model of allergic airway disease are CD5+, express TGF-beta, and co-localize with CD4+Foxp3+ T cells. Mucosal Immunol. 2012;5:691–701. 10.1038/mi.2012.42
34. Lundy SK, Berlin AA, Martens TF, Lukacs NW. Deficiency of regulatory B cells increases allergic airway inflammation. Inflamm Res. 2005;54:514–21. 10.1007/s00011-005-1387-0
35. Kim AS, Doherty TA, Karta MR, Das S, Baum R, Rosenthal P, et al. Regulatory B cells and T follicular helper cells are reduced in allergic rhinitis. J Allergy Clin Immunol. 2016;138:1192–5. 10.1016/j.jaci.2016.03.017
36. Shamji MH, Kappen J, Abubakar-Waziri H, Zhang J, Steveling E, Watchman S, et al. Nasal allergen-neutralizing IgG4 anti-bodies block IgE-mediated responses: novel biomarker of subcutaneous grass pollen immunotherapy. J Allergy Clin Immunol. 2019;143:1067–76. 10.1016/j.jaci.2018.09.039
37. Wang M, Gu Z, Yang J, Zhao H, Cao Z. Changes among TGF-beta1(+) Breg cells and helper T cell subsets in a murine model of allergic rhinitis with prolonged OVA challenge. Int Immunopharmacol. 2019;69:347–57. 10.1016/j.intimp.2019.01.009
38. Xue JM, Yang LT, Yang G, Geng XR, Liu ZQ, Wang S, et al. Protease-activated receptor-2 suppresses interleukin (IL)-10 expression in B cells via upregulating Bcl2L12 in patients with allergic rhinitis. Allergy. 2017;72:1704–12. 10.1111/all.13186
39. Wan J, Luo Y, Yang C, Liu J, Du Y, Wang K. Expression of IL-35, Epstein-Barr virus-induced gene 3 mRNA and IL-12A mRNA in peripheral blood of patients with allergic rhinitis. Lin Chung Er Bi Yan Hou Tou Jing Wai Ke Za Zhi. 2014;28:952–4.
40. Stanic B, van de Veen W, Wirz OF, Ruckert B, Morita H, Sollner S, et al. IL-10-overexpressing B cells regulate innate and adaptive immune responses. J Allergy Clin Immunol. 2015;135:771–80. 10.1016/j.jaci.2014.07.041
41. Liang R, Xie J, Li J, Wang K, Liu L, Gao Y, et al. Liposomes-coated gold nanocages with antigens and adjuvants targeted delivery to dendritic cells for enhancing antitumor immune response. Biomaterials. 2017;149:41–50. 10.1016/j.biomaterials.2017.09.029
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