The Role of Regulatory B Cells in Health and Diseases: A Systemic Review

References

• Kato A, Hulse KE, Tan BK, Schleimer RP. B-lymphocyte lineage cells and the respiratory system. J Allergy Clin Immunol. 2013;131(4):933–957. doi:10.1016/j.jaci.2013.02.023
   PubMed Web of Science ®Google Scholar
• Moore TC, Gonzaga LM, Mather JM, Messer RJ, Hasenkrug KJ. B cell requirement for robust regulatory T cell responses to Friend retrovirus infection. MBio. 2017;8:4. doi:10.1128/mBio.01122-17
   Web of Science ®Google Scholar
• Han J, Sun L, Fan X, et al. Role of regulatory B cells in neuroimmunologic disorders. J Neurosci Res. 2016;94(8):693–701. doi:10.1002/jnr.23749
   PubMed Web of Science ®Google Scholar
• Mizoguchi A, Mizoguchi E, Smith RN, Preffer FI, Bhan AK. Suppressive role of B cells in chronic colitis of T cell receptor α mutant mice. J Exp Med. 1997;186(10):1749–1756. doi:10.1084/jem.186.10.1749
   PubMed Web of Science ®Google Scholar
• Rosser EC, Mauri C. Regulatory B cells: origin, phenotype, and function. Immunity. 2015;42(4):607–612. doi:10.1016/j.immuni.2015.04.005
   PubMed Web of Science ®Google Scholar
• Harris DP, Haynes L, Sayles PC, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol. 2000;1(6):475–482. doi:10.1038/82717
   PubMed Web of Science ®Google Scholar
• Shlomchik MJ, Craft JE, Mamula MJ. From T to B and back again: positive feedback in systemic autoimmune disease. Nat Rev Immunol. 2001;1(2):147–153. doi:10.1038/35100573
   PubMed Web of Science ®Google Scholar
• Xiao X, Lao X-M, Chen -M-M, et al. PD-1hi identifies a novel regulatory B-cell population in human hepatoma that promotes disease progression. Cancer Discov. 2016;6(5):546–559. doi:10.1158/2159-8290.CD-15-1408
   PubMed Web of Science ®Google Scholar
• Yanaba K, Bouaziz J-D, Matsushita T, Tsubata T, Tedder TF. The development and function of regulatory B cells expressing IL-10 (B10 cells) requires antigen receptor diversity and TLR signals. J Immunol. 2009;182(12):7459–7472. doi:10.4049/jimmunol.0900270
   PubMed Web of Science ®Google Scholar
• Bankó Z, Pozsgay J, Szili D, et al. Induction and differentiation of IL-10–producing regulatory B cells from healthy blood donors and rheumatoid arthritis patients. J Immunol. 2017;198(4):1512–1520. doi:10.4049/jimmunol.1600218
   PubMed Web of Science ®Google Scholar
• Vitale G, Mion F, Pucillo C. Regulatory B cells: evidence, developmental origin and population diversity. Mol Immunol. 2010;48(1–3):1–8. doi:10.1016/j.molimm.2010.09.010
   PubMed Web of Science ®Google Scholar
• Lindner S, Dahlke K, Sontheimer K, et al. Interleukin 21–induced granzyme B–expressing B cells infiltrate tumors and regulate T cells. Cancer Res. 2013;73(8):2468–2479. doi:10.1158/0008-5472.CAN-12-3450
   PubMed Web of Science ®Google Scholar
• Chesneau M, Michel L, Dugast E, et al. Tolerant kidney transplant patients produce B cells with regulatory properties. J Am Society Nephrol. 2015;26(10):2588–2598. doi:10.1681/ASN.2014040404
   PubMed Web of Science ®Google Scholar
• Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944–950. doi:10.1038/ni833
   PubMed Web of Science ®Google Scholar
• Blair PA, Noreña LY, Flores-Borja F, et al. CD19+ CD24hiCD38hi B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32(1):129–140. doi:10.1016/j.immuni.2009.11.009
   PubMed Web of Science ®Google Scholar
• Moritoki Y, Zhang W, Tsuneyama K, et al. B cells suppress the inflammatory response in a mouse model of primary biliary cirrhosis. Gastroenterology. 2009;136(3):1037–1047. doi:10.1053/j.gastro.2008.11.035
   PubMed Web of Science ®Google Scholar
• Baba Y, Matsumoto M, Kurosaki T. Signals controlling the development and activity of regulatory B-lineage cells. Int Immunol. 2015;27(10):487–493. doi:10.1093/intimm/dxv027
   PubMed Web of Science ®Google Scholar
• Yoshizaki A, Miyagaki T, DiLillo DJ, et al. Regulatory B cells control T-cell autoimmunity through IL-21-dependent cognate interactions. Nature. 2012;491(7423):264–268. doi:10.1038/nature11501
   PubMed Web of Science ®Google Scholar
• Neves P, Lampropoulou V, Calderon-Gomez E, et al. Signaling via the MyD88 adaptor protein in B cells suppresses protective immunity during Salmonella typhimurium infection. Immunity. 2010;33(5):777–790. doi:10.1016/j.immuni.2010.10.016
   PubMed Web of Science ®Google Scholar
• Hua C, Audo R, Yeremenko N, et al. A proliferation inducing ligand (APRIL) promotes IL-10 production and regulatory functions of human B cells. J Autoimmun. 2016;73:64–72. doi:10.1016/j.jaut.2016.06.002
   PubMed Web of Science ®Google Scholar
• Nouel A, Pochard P, Simon Q, et al. B-Cells induce regulatory T cells through TGF-β/IDO production in A CTLA-4 dependent manner. J Autoimmun. 2015;59:53–60. doi:10.1016/j.jaut.2015.02.004
   PubMed Web of Science ®Google Scholar
• Ray A, Wang L, Dittel BN. IL-10-independent regulatory B-cell subsets and mechanisms of action. Int Immunol. 2015;27(10):531–536. doi:10.1093/intimm/dxv033
   PubMed Web of Science ®Google Scholar
• 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(3):654–665. doi:10.1016/j.jaci.2016.07.006
   PubMed Web of Science ®Google Scholar
• Miyagaki T, Fujimoto M, Sato S. Regulatory B cells in human inflammatory and autoimmune diseases: from mouse models to clinical research. Int Immunol. 2015;27(10):495–504. doi:10.1093/intimm/dxv026
   PubMed Web of Science ®Google Scholar
• Moudgil KD, Choubey D. Cytokines in autoimmunity: role in induction, regulation, and treatment. J Interferon Cytokine Res. 2011;31(10):695–703. doi:10.1089/jir.2011.0065
   PubMed Web of Science ®Google Scholar
• Knippenberg S, Peelen E, Smolders J, et al. Reduction in IL-10 producing B cells (Breg) in multiple sclerosis is accompanied by a reduced naive/memory Breg ratio during a relapse but not in remission. J Neuroimmunol. 2011;239(1–2):80–86. doi:10.1016/j.jneuroim.2011.08.019
   PubMed Web of Science ®Google Scholar
• Ota S-I, Niiro H, Ueki N, et al. Elucidation of molecular mechanisms of Breg induction in autoimmune diseases.: 1952. Arthritis Rheumatol. 2014;66.
   Web of Science ®Google Scholar
• Felton JL, Maseda D, Bonami RH, Hulbert C, Thomas JW. Anti-insulin B cells are poised for antigen presentation in type 1 diabetes. J Immunol. 2018;201(3):861–873. doi:10.4049/jimmunol.1701717
   PubMed Web of Science ®Google Scholar
• Tian J, Zekzer D, Hanssen L, Lu Y, Olcott A, Kaufman DL. Lipopolysaccharide-activated B cells down-regulate Th1 immunity and prevent autoimmune diabetes in nonobese diabetic mice. J Immunol. 2001;167(2):1081–1089. doi:10.4049/jimmunol.167.2.1081
   PubMed Web of Science ®Google Scholar
• Cui D, Zhang L, Chen J, et al. Changes in regulatory B cells and their relationship with rheumatoid arthritis disease activity. Clin Exp Med. 2015;15(3):285–292. doi:10.1007/s10238-014-0310-9
   PubMed Web of Science ®Google Scholar
• Schneider C, Teufel A, Yevsa T, et al. Adaptive immunity suppresses formation and progression of diethylnitrosamine-induced liver cancer. Gut. 2012;61(12):1733–1743. doi:10.1136/gutjnl-2011-301116
   PubMed Web of Science ®Google Scholar
• Horikawa M, Minard-Colin V, Matsushita T, Tedder TF. Regulatory B cell production of IL-10 inhibits lymphoma depletion during CD20 immunotherapy in mice. J Clin Invest. 2011;121:11. doi:10.1172/JCI59266
   Web of Science ®Google Scholar
• Schioppa T, Moore R, Thompson RG, et al. B regulatory cells and the tumor-promoting actions of TNF-α during squamous carcinogenesis. Proc Nat Acad Sci. 2011;108(26):10662–10667. doi:10.1073/pnas.1100994108
   PubMed Web of Science ®Google Scholar
• Wang X, Yuling H, Yanping J, et al. CCL19 and CXCL13 synergistically regulate interaction between B cell acute lymphocytic leukemia CD23+ CD5+ B Cells and CD8+ T cells. J Immunol. 2007;179(5):2880–2888. doi:10.4049/jimmunol.179.5.2880
   PubMed Web of Science ®Google Scholar
• Shao Y, CM L, Ling CC, et al. Regulatory B cells accelerate hepatocellular carcinoma progression via CD40/CD154 signaling pathway. Cancer Lett. 2014;355(2):264–272. doi:10.1016/j.canlet.2014.09.026
   PubMed Web of Science ®Google Scholar
• Olkhanud PB, Damdinsuren B, Bodogai M, et al. Tumor-evoked regulatory B cells promote breast cancer metastasis by converting resting CD4+ T cells to T-regulatory cells. Cancer Res. 2011;71(10):3505–3515. doi:10.1158/0008-5472.CAN-10-4316
   PubMed Web of Science ®Google Scholar
• Wejksza K, Lee-Chang C, Bodogai M, et al. Cancer-produced metabolites of 5-lipoxygenase induce tumor-evoked regulatory B cells via peroxisome proliferator–activated receptor α. J Immunol. 2013;190(6):2575–2584. doi:10.4049/jimmunol.1201920
   PubMed Web of Science ®Google Scholar
• Qiu L, Yu Q, Zhou Y, et al. Functionally impaired follicular helper T cells induce regulatory B cells and CD 14+ human leukocyte antigen‐DR− cell differentiation in non‐small cell lung cancer. Cancer Sci. 2018;109(12):3751–3761. doi:10.1111/cas.13836
   PubMed Web of Science ®Google Scholar
• Pretscher D, Distel LV, Grabenbauer GG, Wittlinger M, Buettner M, Niedobitek G. Distribution of immune cells in head and neck cancer: CD8+ T-cells and CD20+ B-cells in metastatic lymph nodes are associated with favourable outcome in patients with oro-and hypopharyngeal carcinoma. BMC Cancer. 2009;9(1):292. doi:10.1186/1471-2407-9-292
   PubMedGoogle Scholar
• Galdiero M, Pisciotta M, Galdiero E, Carratelli CR. Porins and lipopolysaccharide from Salmonella typhimurium regulate the expression of CD80 and CD86 molecules on B cells and macrophages but not CD28 and CD152 on T cells. Clin Microbiol Infection. 2003;9(11):1104–1111. doi:10.1046/j.1469-0691.2003.00728.x
   PubMed Web of Science ®Google Scholar
• Barr TA, Brown S, Mastroeni P, Gray D. TLR and B cell receptor signals to B cells differentially program primary and memory Th1 responses to Salmonella enterica. J Immunol. 2010;185(5):2783–2789. doi:10.4049/jimmunol.1001431
   PubMed Web of Science ®Google Scholar
• Shen P, Roch T, Lampropoulou V, et al. IL-35-producing B cells are critical regulators of immunity during autoimmune and infectious diseases. Nature. 2014;507(7492):366–370. doi:10.1038/nature12979
   PubMed Web of Science ®Google Scholar
• Gong Y, Zhao C, Zhao P, et al. Role of IL-10-producing regulatory B cells in chronic hepatitis B virus infection. Dig Dis Sci. 2015;60(5):1308–1314. doi:10.1007/s10620-014-3358-1
   PubMed Web of Science ®Google Scholar
• Das A, Ellis G, Pallant C, et al. IL-10–producing regulatory B cells in the pathogenesis of chronic hepatitis B virus infection. J Immunol. 2012;189(8):3925–3935. doi:10.4049/jimmunol.1103139
   PubMed Web of Science ®Google Scholar
• Liu Y, Cheng L-S, Wu S-D, et al. IL-10-producing regulatory B-cells suppressed effector T-cells but enhanced regulatory T-cells in chronic HBV infection. Clin Sci. 2016;130(11):907–919. doi:10.1042/CS20160069
   Web of Science ®Google Scholar
• Han X, Yang J, Zhang Y, et al. Potential role for regulatory B cells as a major source of interleukin-10 in spleen from Plasmodium chabaudi-infected mice. Infect Immun. 2018;86:5. doi:10.1128/IAI.00016-18
   Web of Science ®Google Scholar
• Liu Y, Chen Y, Li Z, et al. Role of IL‐10‐producing regulatory B cells in control of cerebral malaria in P lasmodium berghei infected mice. Eur J Immunol. 2013;43(11):2907–2918. doi:10.1002/eji.201343512
   PubMed Web of Science ®Google Scholar
• Silva HM, Takenaka MC, Moraes-Vieira PM, et al. Preserving the B-cell compartment favors operational tolerance in human renal transplantation. Mol Med. 2012;18(5):733–743. doi:10.2119/molmed.2011.00281
   PubMed Web of Science ®Google Scholar
• Nouël A, Ségalen I, Jamin C, et al. B cells display an abnormal distribution and an impaired suppressive function in patients with chronic antibody–mediated rejection. Kidney Int. 2014;85(3):590–599. doi:10.1038/ki.2013.457
   PubMed Web of Science ®Google Scholar
• Deng S, Moore DJ, Huang X, et al. Cutting edge: transplant tolerance induced by anti-CD45RB requires B lymphocytes. J Immunol. 2007;178(10):6028–6032. doi:10.4049/jimmunol.178.10.6028
   PubMed Web of Science ®Google Scholar
• Singh A, Carson WF, Secor ER, et al. Regulatory role of B cells in a murine model of allergic airway disease. J Immunol. 2008;180(11):7318–7326. doi:10.4049/jimmunol.180.11.7318
   PubMed Web of Science ®Google Scholar
• Geissler EK, Hutchinson JA. Cell therapy as a strategy to minimize maintenance immunosuppression in solid organ transplant recipients. Curr Opin Organ Transplant. 2013;18(4):408–415. doi:10.1097/MOT.0b013e328363319d
   PubMed Web of Science ®Google Scholar
• Jensen F, Muzzio D, Soldati R, Fest S, Zenclussen AC. Regulatory B10 cells restore pregnancy tolerance in a mouse model. Biol Reprod. 2013;89(4):90,1–7. doi:10.1095/biolreprod.113.110791
   Web of Science ®Google Scholar
• Chakravarty EF, Murray ER, Kelman A, Farmer P. Pregnancy outcomes after maternal exposure to rituximab. Blood, J Am Soc Hematol. 2011;117(5):1499–1506.
   Google Scholar
• Muzzio DO, Soldati R, Ehrhardt J, et al. B cell development undergoes profound modifications and adaptations during pregnancy in mice. Biol Reprod. 2014;91(5):115,1–11. doi:10.1095/biolreprod.114.122366
   Web of Science ®Google Scholar
• Li S, Ma F, Hao H, et al. Marked elevation of circulating CD19+ CD38hiCD24hi transitional B cells give protection against neonatal sepsis. Pediatr Neonatol. 2018;59(3):296–304. doi:10.1016/j.pedneo.2017.10.005
   PubMed Web of Science ®Google Scholar
• Sarvaria A, Basar R, Mehta RS, et al. IL-10+ regulatory B cells are enriched in cord blood and may protect against cGVHD after cord blood transplantation. Blood, J Am Soc Hematol. 2016;128(10):1346–1361.
   Google Scholar