Peritoneal Cavity Regulatory B Cells (B10 Cells) Modulate IFN-γ+CD4+ T Cell Numbers during Colitis Development in Mice
Open accessAbstract
The spleen regulatory B cell subset with the functional capacity to express IL-10 (B10 cells) modulates both immune responses and autoimmune disease severity. However, the peritoneal cavity also contains relatively high frequencies of functionally defined IL-10–competent B10 cells. In this study, peritoneal cavity B10 cells shared similar cell surface phenotypes with their spleen counterparts. However, peritoneal cavity B10 cells were 10-fold more frequent among B cells than occurred within the spleen, intestinal tract, or mesenteric lymph nodes and were present at higher proportions among the phenotypically defined peritoneal B1a > B1b > B2 cell subpopulations. The development or localization of B10 cells within the peritoneal cavity was not dependent on the presence of commensal microbiota, T cells, IL-10 or B10 cell IL-10 production, or differences between their fetal liver or adult bone marrow progenitor cell origins. The BCR repertoire of peritoneal cavity B10 cells was diverse, as occurs in the spleen, and predominantly included germline-encoded VH and VL regions commonly found in either the conventional or B1 B cell compartments. Thereby, the capacity to produce IL-10 appears to be an intrinsic functional property acquired by clonally diverse B cells. Importantly, IL-10 production by peritoneal cavity B cells significantly reduced disease severity in spontaneous and induced models of colitis by regulating neutrophil infiltration, colitogenic CD4+ T cell activation, and proinflammatory cytokine production during colitis onset. Thus, the numerically small B10 cell subset within the peritoneal cavity has regulatory function and is important for maintaining homeostasis within gastrointestinal tissues and the immune system.
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The proportion of Bregs ranges from 1 to 3% of total B cells in the spleen and peritoneal cavity of healthy mice, whereas in humans Bregs typically constitute 1-4% of circulating B cells under homeostatic conditions.
“The proportion of Bregs ranges from 1 to 3% of total B cells in the spleen and peritoneal cavity of healthy mice, whereas in humans, Bregs typically constitute 1 -4% of circulating B cells under homeostatic conditions [57,59,60].”
From Is there a role for B cells in Alzheimer's disease? (2026) · cites this paper as [60]
The Introduction reports B10 cells at 1–5% of spleen B cells in naïve mice, rather than the claimed 1–3%. More decisively, the Results section on IL-10-competent B cells reports about 40% in the peritoneal cavity, contrary to the claimed 1–3%. The passages found do not establish the stated 1–4% figure for circulating human B cells; page numbers were not available in our copy. (LLM, conf=0.88)
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BackgroundInfluentialSelf-citationProstaglandin E2 and SOCS1 have a role in intestinal immune tolerance
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BackgroundSelf-citationIdentifying Regulatory B Cells (B10 Cells) that Produce IL-10 in Mice
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“Mizoguchi and colleagues (67) recently demonstrated a regulatory role for peritoneal cavity B1 cells from TCRa mice during chronic colitis, possibly through generating natural Abs in response to microbial flora.”
BackgroundA differentiation pathway for B1 cells in adult bone marrow
Esplin, B. L., Welner, R. S., Zhang, Q., Borghesi, L., & Kincade, P. W. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811632106 · Cited by 105 · cited 1× · see citing works
“Although the fetal liver was once thought to be the exclusive source of B1 cells, adult bone marrow precursor cells can become fully functional CD5 cells in adult mice (64).”
BackgroundB cell-derived IL-10 suppresses inflammatory disease in Lyn-deficient mice
Scapini, P., Lamagna, C., Hu, Y., Lee, K., Tang, Q., DeFranco, A. L., & Lowell, C. A. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107913108 · Cited by 84 · cited 1× · see citing works
“Receptors or pathways that positively or negatively regulate BCR signaling such as CD19, CD22 and CD40 can also significantly modulate B10 cell numbers (28, 54-57).”
BackgroundIL‐10 Production by CD5 B Cells
O'GARRA, A., & HOWARD, M. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb24615.x · Cited by 74 · cited 1× · see citing works
“Spontaneous ex vivo secretion of IL-10 by peritoneal cavity B cells has been well described (36, 60), with B1a, B1b, and B2 cells variably contributing to IL-10 secretion in vitro (Fig.”
BackgroundAmplified B Lymphocyte CD40 Signaling Drives Regulatory B10 Cell Expansion in Mice
Poe, J. C., Smith, S. H., Haas, K. M., Yanaba, K., Tsubata, T., Matsushita, T., & Tedder, T. F. (2011) · PLoS ONE · doi:10.1371/journal.pone.0022464 · Cited by 70 · cited 1× · see citing works
“Receptors or pathways that positively or negatively regulate BCR signaling such as CD19, CD22 and CD40 can also significantly modulate B10 cell numbers (28, 54-57).”
BackgroundSelf-citationFillatreau, S. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2010.00991.x · Cited by 69 · cited 1× · see citing works
“Thus, spontaneous ex vivo IL-10 production by peritoneal cavity B10 cells may reflect their prior in vivo interactions with T cells, although it remains possible that innate- or pathogeninduced signals may also induce B10 cell IL-10 production in vivo (46, 61).”
BackgroundThe peritoneal micromilieu commits B cells to home to body cavities and the small intestine
Berberich, S., Förster, R., & Pabst, O. (2007) · Blood · doi:10.1182/blood-2006-12-064345 · Cited by 69 · cited 1× · see citing works
“3A) (69), B10 cells may be functionally important both centrally within the spleen and within the peritoneal cavity and GALTs during colitis.”
BackgroundFrequent occurrence of identical heavy and light chain Ig rearrangements
Seidl, K. (1997) · International Immunology · doi:10.1093/intimm/9.5.689 · Cited by 62 · cited 1× · see citing works
“Thereby, peritoneal cavity B10 cell VH use was similar to that observed for spleen B10 cells (46) and conventional B cells (49), but it also included sequences commonly associated with peritoneal cavity B1 cells (58, 59).”
ResultNakashima, H., Hamaguchi, Y., Watanabe, R., Ishiura, N., Kuwano, Y., Okochi, H., Takahashi, Y., Tamaki, K., Sato, S., Tedder, T. F., et al. (2010) · The Journal of Immunology · doi:10.4049/jimmunol.0901719 · Cited by 55 · cited 10× · see citing works
“The mAbs used in this study are as follows: CD21/35 (7G6), CD23 (B3B4), CD24 (M1/69), CD25 (PC61), CD38 (90/CD38), CD43 (S7), CD44 (IM7), CD138 (281-2), and CD11b (M1/70) (all from BD Pharmingen, San Diego, CA); IgM (11/41), CD4 (GK1.”
BackgroundInfluentialSelf-citationRohatgi, S., Ganju, P., & Sehgal, D. (2008) · Journal of Immunological Methods · doi:10.1016/j.jim.2008.09.017 · Cited by 48 · cited 1× · see citing works
“cDNA was synthesized, and Ig H and L chain transcripts were amplified using nested PCR primers, as described (43).”
MethodAithal, G. P., Craggs, A., Day, C. P., Welfare, M., Daly, A. K., Mansfield, J. C., & Hudson, M. (2001) · Digestive Diseases and Sciences · doi:10.1023/a:1010604307776 · Cited by 42 · cited 1× · see citing works
“Human IBD is also genetically linked with il10 locus polymorphisms or altered serum IL-10 concentrations (11, 12).”
BackgroundNemoto, Y., Kanai∥, T., Kameyama, K., Shinohara, T., Sakamoto, N., Totsuka, T., Okamoto, R., Tsuchiya, K., Nakamura, T., Sudo, T., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803684 · Cited by 36 · cited 1× · see citing works
“Given that T cells also play critical regulatory roles during IBD development in mice, as well as in humans (1, 3), it is likely that B10 and regulatory Foxp3 CD4 T cells share complementary regulatory functions for IBD, as previously shown for experimental autoimmune encephalomyelitis (29).”
BackgroundB Cells Exposed to Enterobacterial Components Suppress Development of Experimental Colitis
Schmidt, E., Larsen, H. L., Kristensen, N., Poulsen, S., Claesson, M., & Pedersen, A. (2012) · Inflammatory Bowel Diseases · doi:10.1002/ibd.21769 · Cited by 25 · cited 2× · see citing works
“Spleen B cells exposed to enterobacterial components can also acquire IL-10-dependent suppressive functions and inhibit experimental colitis (21).”
Background
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- [49]Kantor AB Merrill CE Herzenberg LA Hillson JL An unbiased analysis of VH-D-JH sequences from B1-a, B1-b, and conventional B cells. J. Immunol 1996 158 1175 1186 9013957
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Sorted by citations
B cell regulation in cancer and anti-tumor immunity
Sarvaria, A., Madrigal, J. A., & Saudemont, A. (2017) · Cellular and Molecular Immunology · doi:10.1038/cmi.2017.35 · Cited by 633 · see citing works
Antibody-independent functions of B cells: a focus on cytokines
Shen, P., & Fillatreau, S. (2015) · Nature Reviews Immunology · doi:10.1038/nri3857 · Cited by 508 · see citing works
B cells responses and cytokine production are regulated by their immune microenvironment
Vazquez, M. I., Catalan-Dibene, J., & Zlotnik, A. (2015) · Cytokine · doi:10.1016/j.cyto.2015.02.007 · Cited by 421 · see citing works
“These data are reminiscent of animal studies where Breg cells have been shown to lead to the resolution of colitis in mice [88].”
BackgroundResultImmunosuppressive Mechanisms of Regulatory B Cells
Catalán, D., Mansilla, M. A., Ferrier, A., Soto, L., Oļeiņika, K., Aguillón, J. C., & Aravena, O. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.611795 · Cited by 407 · see citing works
“Besides, murine IL-10 Bregs can prevent the recruitment of neutrophils to the sites of inflammation in a model of colitis (42).”
BackgroundInfluentialB10 Cells: A Functionally Defined Regulatory B Cell Subset
Tedder, T. F. (2015) · The Journal of Immunology · doi:10.4049/jimmunol.1401329 · Cited by 283 · see citing works
“Whether these regulatory activities and mechanisms of action are attributable to a single B cell subset or functionally diverse B cell populations during IBD is unresolved.”
BackgroundResultInfluentialSelf-citationMishima, Y., Oka, A., Liu, B., Herzog, J. W., Eun, C. S., Fan, T.-J., Bulik-Sullivan, E., Carroll, I. M., Hansen, J. J., Chen, L., et al. (2019) · Journal of Clinical Investigation · doi:10.1172/jci93820 · Cited by 166 · see citing works
“These findings are consistent with the lack of differences in the number or function of IL-10–producing peritoneal regulatory B cells in GF versus SPF mice (28).”
ResultB10 cell regulation of health and disease
Candando, K. M., Lykken, J. M., & Tedder, T. F. (2014) · Immunological Reviews · doi:10.1111/imr.12176 · Cited by 163 · see citing works
“Thus, the shared ability of B10 and CLL cells from TCL1 transgenic mice to secrete IL-10, inhibit innate effector cell activation, and express CD5 indicate that either similar molecular processes, comparably self-reactive BCRs, or shared cellular origins dictate the IL-10-dependent regulatory function observed in both…”
BackgroundInfluentialSelf-citationZou, F., Qiu, Y., Huang, Y., Zou, H., Xiao, C., Niu, Q., Luo, A., & Sun, J. (2021) · Cell Death and Disease · doi:10.1038/s41419-021-03880-9 · Cited by 155 · see citing works
Regulatory B10 cell development and function
Lykken, J. M., Candando, K. M., & Tedder, T. F. (2015) · International Immunology · doi:10.1093/intimm/dxv046 · Cited by 131 · see citing works
Self-citationSpecialized immune responses in the peritoneal cavity and omentum
Liu, M., Silva-Sánchez, A., Randall, T. D., & Meza‐Perez, S. (2020) · Journal of Leukocyte Biology · doi:10.1002/jlb.5mir0720-271rr · Cited by 128 · see citing works
The role of B-1 cells in inflammation
Aziz, M., Holodick, N. E., Rothstein, T. L., & Wang, P. (2015) · Immunologic Research · doi:10.1007/s12026-015-8708-3 · Cited by 118 · see citing works
Srikakulapu, P., Hu, D., Yin, C., Mohanta, S. K., Bontha, S. V., Peng, L., Beer, M., Weber, C., McNamara, C. A., Grassia, G., et al. (2016) · Arteriosclerosis Thrombosis and Vascular Biology · doi:10.1161/atvbaha.115.306983 · Cited by 120 · see citing works
Tao, H., Lü, L., Xia, Y., Dai, F., Wang, Y., Bao, Y., Lundy, S. K., Ito, F., Pan, Q., Zhang, X., et al. (2014) · European Journal of Immunology · doi:10.1002/eji.201444625 · Cited by 113 · see citing works
Regulatory B cells: the cutting edge of immune tolerance in kidney transplantation
Peng, B., Ming, Y., & Yang, C. (2018) · Cell Death and Disease · doi:10.1038/s41419-017-0152-y · Cited by 103 · see citing works
Miyagaki, T., Fujimoto, M., & Sato, S. (2015) · International Immunology · doi:10.1093/intimm/dxv026 · Cited by 99 · see citing works
JMJD family proteins in cancer and inflammation
Wang, M., Jianxin, X., Hong, W., Chen, S., & Huashan, S. (2022) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-022-01145-1 · Cited by 103 · see citing works
Skin-Associated B Cells in Health and Inflammation
Debes, G. F., & McGettigan, S. E. (2019) · The Journal of Immunology · doi:10.4049/jimmunol.1801211 · Cited by 94 · see citing works
“testinal inflammation (82, 85), are recruited into inflamed skin (14).”
BackgroundIL-10 Plays Opposing Roles during Staphylococcus aureus Systemic and Localized Infections
Leech, J. M., Lacey, K. A., Mulcahy, M. E., Medina, E., & McLoughlin, R. M. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1601018 · Cited by 92 · see citing works
“tularensis (47) and Th1 responses during colitis (48).”
BackgroundRegulatory B cells in infection, inflammation, and autoimmunity
Dasgupta, S., Dasgupta, S., & Bandyopadhyay, M. (2020) · Cellular Immunology · doi:10.1016/j.cellimm.2020.104076 · Cited by 91 · see citing works
A regulatory CD9+ B‐cell subset inhibits HDM‐induced allergic airway inflammation
Braza, F., Chesné, J., Durand, M., Dirou, S., Brosseau, C., Mahay, G., Cheminant, M., Magnan, A., & Brouard, S. (2015) · Allergy. European Journal of Allergy and Clinical Immunology · doi:10.1111/all.12697 · Cited by 79 · see citing works
Human Mesenchymal Stem Cell-Treated Regulatory CD23+CD43+ B Cells Alleviate Intestinal Inflammation
Chen, X., Cai, C., Xu, D., Liu, Q., Zheng, S., Liu, L., Li, G., Zhang, X., Li, X., Ma, Y., et al. (2019) · Theranostics · doi:10.7150/thno.32260 · Cited by 76 · see citing works
“IL-10 producing Breg cells were decreased in mice or humans with colitis [51, 52].”
BackgroundRegulatory B Cells in Pregnancy: Lessons from Autoimmunity, Graft Tolerance, and Cancer
Guzman‐Genuino, R. M., & Diener, K. R. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00172 · Cited by 75 · see citing works
“Lower percentages are found in the blood, lymph nodes, intestinal tissues, Peyer’s patches, and the central nervous system (21, 44, 45).”
BackgroundRegulatory B cells: Development, phenotypes, functions, and role in transplantation
Alhabbab, R. Y., Nova‐Lamperti, E., Aravena, O., Burton, H. M., Lechler, R. I., Dorling, A., & Lombardi, G. (2019) · Immunological Reviews · doi:10.1111/imr.12800 · Cited by 74 · see citing works
Jiao, J., He, S., Wang, Y., Lu, Y., Gu, M., Li, D., Tang, T., Nie, S., Zhang, M., Lv, B., et al. (2021) · Basic Research in Cardiology · doi:10.1007/s00395-021-00886-4 · Cited by 73 · see citing works
Patel, A. J., Willsmore, Z. N., Khan, N., Richter, A. G., Naidu, B. V., Drayson, M. T., Papa, S., Cope, A. P., Karagiannis, S. N., Perucha, E., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-30863-x · Cited by 73 · see citing works
Geherin, S. A., Gómez, D., Glabman, R. A., Ruthel, G. T., Hamann, A., & Debes, G. F. (2016) · The Journal of Immunology · doi:10.4049/jimmunol.1403246 · Cited by 71 · see citing works
Tissue-resident B cells orchestrate macrophage polarisation and function
Suchánek, O., Ferdinand, J. R., Tuong, Z. K., Wijeyesinghe, S., Chandra, A., Clauder, A., de Almeida, L. N., Clare, S., Harcourt, K., Ward, C. J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-42625-4 · Cited by 69 · see citing works
“We hypothesized that this may be of relevance to the pro-in fl ammatory kidney MNPs phenotype that we observed in μ MT - mice, as some B cells subsets have previously been shown to produce IL10, including B-1a cells 60 .”
Unraveling the diversity and functions of tissue-resident plasma cells
Tellier, J., Tarasova, I., Nie, J., Smillie, C. S., Fedele, P. L., Cao, W. H. J., Groom, J. R., Belz, G. T., Bhattacharya, D., Smyth, G. K., et al. (2024) · Nature Immunology · doi:10.1038/s41590-023-01712-w · Cited by 69 · see citing works
Matsushita, T., Huu, D. L., Kobayashi, T., Hamaguchi, Y., Hasegawa, M., Naka, K., Hirao, A., Muramatsu, M., Takehara, K., & Fujimoto, M. (2016) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2015.12.1319 · Cited by 64 · see citing works
Regulatory B Cells and Its Role in Central Nervous System Inflammatory Demyelinating Diseases
Ran, Z., Luo, Y., Qiu-Ming, Z., & Yang, H. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01884 · Cited by 64 · see citing works
“In colitis model, IL-10 production by B1a significantly reduced disease severity by regulating neutrophil infiltration, CD4 T cell activation, and proinflammatory cytokine production during disease onset (64).”
BackgroundBusse, M., Campe, K.-N. J., Nowak, D., Schumacher, A., Plenagl, S., Langwisch, S., Tiegs, G., Reinhold, A., & Zenclussen, A. C. (2019) · Scientific Reports · doi:10.1038/s41598-019-45860-2 · Cited by 64 · see citing works
Lino, A., Dörner, T., Bar-Or, A., & Fillatreau, S. (2016) · Immunological Reviews · doi:10.1111/imr.12374 · Cited by 66 · see citing works
“Although a B-cell deficiency does not result in an aggravation of the disease course in Il-10-deficient mice (154), an adoptive transfer of peritoneal cavity B cells, which are CD1d, can attenuate via an IL-10-dependent mechanism the pathogenic TH1-cell response and the disease progression in Il-10-deficient recipient…”
BackgroundRegulatory functions of B cells and regulatory plasma cells
Fillatreau, S. (2019) · Biomedical Journal · doi:10.1016/j.bj.2019.05.008 · Cited by 50 · see citing works
“[15] Maseda D, Candando KM, Smith SH, Kalampokis I, Weaver CT, Plevy SE, et al.”
BackgroundReyes, J. L., Wang, A., Fernando, M., Graepel, R., Leung, G., van Rooijen, N., Sigvardsson, M., & McKay, D. M. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1400738 · Cited by 54 · see citing works
“Based on these results, we suggest that, analogous to B10 cells (49), the H.”
BackgroundResultMorris, G., Puri, B. K., OLIVE, L. S., Carvalho, A. F., Berk, M., & Maes, M. H. J. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.104408 · Cited by 51 · see citing works
Hu, S., Chen, M., Wang, Y., Wang, Z., Pei, Y.-F., Fan, R., Liu, X., Wang, L., Zhou, J., Zheng, S., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0154564 · Cited by 51 · see citing works
B cells promote tumor progression in a mouse model of HPV‐mediated cervical cancer
Tang, A., Dadaglio, G., Oberkampf, M., Carlo, S. E. D., Peduto, L., Laubreton, D., Desrues, B., Sun, C., Montagutelli, X., & Leclerc, C. (2016) · International Journal of Cancer · doi:10.1002/ijc.30169 · Cited by 49 · see citing works
Rodgers, D. T., Pineda, M. A., McGrath, M., Al‐Riyami, L., Harnett, W., & Harnett, M. M. (2013) · Immunology · doi:10.1111/imm.12208 · Cited by 48 · see citing works
Simeonova, D., Stoyanov, D., Leunis, J., Murdjeva, M., & Maes, M. H. J. (2020) · Nitric Oxide · doi:10.1016/j.niox.2020.11.001 · Cited by 41 · see citing works
Activation of B-1 Cells Promotes Tumor Cell Killing in the Peritoneal Cavity
Haro, M., Dyevoich, A. M., Phipps, J. P., & Haas, K. M. (2018) · Cancer Research · doi:10.1158/0008-5472.can-18-0981 · Cited by 47 · see citing works
“MPL/TDCM treatment induces protection independent ofMHC class II antigen (Ag) presentation and IL10 production B-1a cells produce a large amount of IL10 (14, 15), which in some cases, actually support antitumor immune responses (28).”
BackgroundCD1dhiCD5+ B Cells Expanded by GM-CSF In Vivo Suppress Experimental Autoimmune Myasthenia Gravis
Sheng, J. R., Quan, S., & Soliven, B. C. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1303397 · Cited by 46 · see citing works
Floudas, A., Amu, S., & Fallon, P. (2016) · Journal of Clinical Immunology · doi:10.1007/s10875-016-0263-8 · Cited by 48 · see citing works
Ma, S., Satitsuksanoa, P., Jansen, K., Cevhertas, L., van de Veen, W., & Akdiş, M. (2020) · Immunological Reviews · doi:10.1111/imr.12937 · Cited by 45 · see citing works
Characterization of Organ-Specific Regulatory B Cells Using Single-Cell RNA Sequencing
Yang, S.-Y., Long, J., Huang, M.-X., Luo, P., Bian, Z.-H., Xu, Y.-F., Wang, C., Yang, S., Li, L., Selmi, C. F., et al. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.711980 · Cited by 43 · see citing works
Activated Peritoneal Cavity B-1a Cells Possess Regulatory B Cell Properties
Margry, B., Kersemakers, S. C. W., Hoek, A., Arkesteijn, G., Wieland, W., van Eden, W., & Broere, F. (2014) · PLoS ONE · doi:10.1371/journal.pone.0088869 · Cited by 45 · see citing works
Zheng, Y., Ge, W., Ma, Y., Xie, G., Wang, W., Li, H., Bian, B., Li, L., & Shen, L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.00914 · Cited by 43 · see citing works
“Regulatory B cells producing IL-10 have been shown to play an important role in maintaining intestinal homeostasis, and a lack of B10 cell-mediated suppression has been associated with CD development (18).”
BackgroundMast Cells Control the Expansion and Differentiation of IL-10–Competent B Cells
Mion, F., Federica D’Incà, Danelli, L., Toffoletto, B., Guarnotta, C., Frossi, B., Burocchi, A., Rigoni, A., Gerdes, N., Lutgens, E., et al. (2014) · The Journal of Immunology · doi:10.4049/jimmunol.1302593 · Cited by 43 · see citing works
Mishima, Y., Liu, B., Hansen, J. J., & Sartor, R. B. (2015) · Cellular and Molecular Gastroenterology and Hepatology · doi:10.1016/j.jcmgh.2015.01.002 · Cited by 42 · see citing works
The role of IL-10 in microbiome-associated immune modulation and disease tolerance
Levast, B., Li, Z., & Madrenas, J. (2014) · Cytokine · doi:10.1016/j.cyto.2014.11.027 · Cited by 42 · see citing works
B1a cells play a pathogenic role in the development of autoimmune arthritis
Deng, J., Wang, X., Chen, Q., Sun, X., Xiao, F., Ko, K., Zhang, M., & Lu, L. (2016) · Oncotarget · doi:10.18632/oncotarget.8244 · Cited by 37 · see citing works
Contemporary Strategies and Barriers to Transplantation Tolerance
Ezekian, B., Schroder, P. M., Freischlag, K., Yoon, J., Kwun, J., & Knechtle, S. J. (2018) · Transplantation · doi:10.1097/tp.0000000000002242 · Cited by 37 · see citing works
Interleukin-10-producing B cells and the regulation of immunity.
Hilgenberg, E., Shen, P., Dang, V. D., Ries, S., Sakwa, I., & Fillatreau, S. (2014) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-662-43492-5_4 · Cited by 34 · see citing works
Wu, H., Su, Z., & Barnie, P. A. (2019) · International Immunopharmacology · doi:10.1016/j.intimp.2019.106111 · Cited by 36 · see citing works
Immune Tolerance to Apoptotic Self Is Mediated Primarily by Regulatory B1a Cells
Miles, K., Simpson, J. E., Brown, S. L., Cowan, G. J. M., Gray, D., & Gray, M. (2018) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01952 · Cited by 33 · see citing works
“These stable interactions may allow the recognition of AC expressed neoantigens via the B cell receptor (40), which we and others have previously reported to be required for regulatory B cell function (14, 41, 42).”
BackgroundDual Role of B Cells in Multiple Sclerosis
Kumar, G., & Axtell, R. C. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24032336 · Cited by 33 · see citing works
“Mature CD5+ B10 cells are potent producers of IL-10 and inhibit experimental autoimmune diseases in mice [32,33].”
BackgroundCarey, A., Nguyen, K., Kandikonda, P., Kruglov, V., Bradley, C., Dahlquist, K. J. V., Cholensky, S. H., Swanson, W. L., Badovinac, V. P., Griffith, T. S., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.113967 · Cited by 32 · see citing works
“14,40,49,50 We transferred B cells isolated from the peritoneal cavity for several reasons: the comparable composition of B1:B2 B cells 51 ; ability of peritoneal B cells to migrate to vWAT 35 ; and insufficient numbers of cells from vWAT for adoptive transfer.”
BackgroundB- and Plasma Cell Subsets in Autoimmune Diseases: Translational Perspectives
Dang, V. D., Stefanski, A., Lino, A. C., & Dörner, T. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.05.038 · Cited by 32 · see citing works
Lu, Y., Liu, F., Li, C., Chen, Y., Weng, D., & Chen, J. (2017) · Mediators of Inflammation · doi:10.1155/2017/8415094 · Cited by 32 · see citing works
“They were also found in low numbers within blood, lymph nodes, Peyer’s patches, intestinal tissues, and the CNS [20, 32, 45, 46].”
BackgroundRegulation of neuroinflammation by B cells and plasma cells
Wang, A. A., Rojas, O. L., Lee, D. S. W., & Gommerman, J. L. (2020) · Immunological Reviews · doi:10.1111/imr.12929 · Cited by 31 · see citing works
Li, J., Shen, C., Liu, Y., Li, Y., Sun, L., Jiao, L., Jiao, W., Xiao, J., Shen, C., Qi, H., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0132173 · Cited by 31 · see citing works
Therapeutic Potential of B-1a Cells in COVID-19
Aziz, M., Brenner, M., & Wang, P. (2020) · Shock · doi:10.1097/shk.0000000000001610 · Cited by 30 · see citing works
“In addition, several other B cell subsets manifest activities that overlap with B-1a cells, including B10 cells or Breg cells (81).”
BackgroundTousif, S., Wang, Y., Jackson, J., Hough, K., Strenkowski, J. G., Athar, M., Thannickal, V., McCusker, R. H., Ponnazhagan, S., & Deshane, J. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.747780 · Cited by 26 · see citing works
“Previous studies have shown that chemoattractant may attract naïve B cells into TME and promote their differentiation into Breg through a series of soluble mediators (IL-1b, IL-6, IL-21 and IL-35) and cell interaction dependent mechanism (CD40-CD40-L) (54, 70, 71).”
BackgroundWei, B., Deng, Y., Huang, Y.-L., Gao, X.-C., & Wu, W.-F. (2019) · Life Science · doi:10.1016/j.lfs.2019.116838 · Cited by 25 · see citing works
Immunoregulation by antibody secreting cells in inflammation, infection, and cancer
McGettigan, S. E., & Debes, G. F. (2021) · Immunological Reviews · doi:10.1111/imr.12991 · Cited by 28 · see citing works
Kleinwort, A., Lührs, F., Heidecke, C.-D., Lipp, M., & Schulze, T. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020391 · Cited by 27 · see citing works
“About 50% of peritoneal B1a and 24% of peritoneal B1b B cells showed the capacity for Interleukin (IL)-10 production [41].”
BackgroundRole of environmental factors in the pathogenesis of Crohn’s disease: a critical review
Chen, Y., Wang, Y., & Shen, J. (2019) · International Journal of Colorectal Disease · doi:10.1007/s00384-019-03441-9 · Cited by 26 · see citing works
“However, as a proinflammatory cytokine, the level of IL-12 was increased in patients with CD [60, 61].”
BackgroundAvoiding Immunological Rejection in Regenerative Medicine
Bolton, E. M., & Bradley, J. A. (2015) · Regenerative Medicine · doi:10.2217/rme.15.11 · Cited by 27 · see citing works
Wang, Q., Racine, J. J., Ratiu, J. J., Wang, S., Ettinger, R., Wasserfall, C. H., Atkinson, M. A., & SERREZE, D. V. (2017) · The Journal of Immunology · doi:10.4049/jimmunol.1700822 · Cited by 27 · see citing works
“Peritoneal cavity B cells have been reported to possess regulatory functions through IL-10 production (42).”
BackgroundMohammed, A. D., Khan, M. A. W., Chatzistamou, I., Chamseddine, D., Kang, K. N., Perry, M., Enos, R. T., Murphy, A. E., Gomez, G., Al-Adhami, A., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02484 · Cited by 26 · see citing works
Liu, J.-L., Lai, X., Bao, Y., Xie, W., Li, Z., Chen, J., Li, G., Wang, T., Huang, W., Ma, Y., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.853894 · Cited by 26 · see citing works
“Peritoneal cavity resident B cells and macrophages are both associated with IBD (56, 57).”
BackgroundSoares, R. R., Antinarelli, L. M. R., Abramo, C., Macedo, G. C., Coimbra, E. S., & Scopel, K. K. G. (2017) · Pathogens and Global Health · doi:10.1080/20477724.2017.1308902 · Cited by 26 · see citing works
Plasma Cells: From Cytokine Production to Regulation in Experimental Autoimmune Encephalomyelitis
Wang, A. A., Gommerman, J. L., & Rojas, O. L. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2020.09.014 · Cited by 25 · see citing works
Zogorean, R., & Wirtz, S. J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1260266 · Cited by 24 · see citing works
Amyloid fibrils activate B-1a lymphocytes to ameliorate inflammatory brain disease
Kurnellas, M. P., Ghosn, E., Schartner, J., Baker, J., Rothbard, J. J., Negrin, R. S., Herzenberg, L., Fathman, C., Steinman, L., & Rothbard, J. (2015) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.1521206112 · Cited by 23 · see citing works
“IL-10–producing B cells, B10 cells, were shown initially by Janeway and colleagues to be necessary for the recovery from the signs of EAE (11) and were demonstrated subsequently to be immune-suppressive in animal models of multiple sclerosis (12, 13), inflammatory bowel disease (14), collagen-induced arthritis (15), l…”
BackgroundInui, M., Tazawa, K., Kishi, Y., & Takai, T. (2015) · BMC Immunology · doi:10.1186/s12865-015-0086-z · Cited by 24 · see citing works
“particularly monocytes/macrophages, as a rich source of IL-10 in the bloodstream and tissues [7-13].”
BackgroundTransplantation tolerance: don't forget about the B cells
Chong, A. S., & Khiew, S. H. W. (2017) · Clinical & Experimental Immunology · doi:10.1111/cei.12927 · Cited by 22 · see citing works
IL-10 derived from CD1dhiCD5+ B cells regulates experimental autoimmune myasthenia gravis
Sheng, J. R., Quan, S., & Soliven, B. C. (2015) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2015.10.023 · Cited by 22 · see citing works
Expanding Diversity and Common Goal of Regulatory T and B Cells. I: Origin, Phenotype, Mechanisms
Bocian, K., Kiernozek, E., Domagała-Kulawik, J., Korczak-Kowalska, G., Stelmaszczyk-Emmel, A., & Drela, N. (2017) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-017-0469-3 · Cited by 21 · see citing works
“…activity constitute 1–5% of spleen or lymph node B cells and up to 10% of peritoneal cavity B cells; however, their numbers increase following B cell receptor (BCR), CD40, or TLR stimulation in vitro (Fillatreau et al. 2002; Lampropoulou et al. 2008; Maseda et al. 2013; Mauri et al. 2003).”
Backgroundda Rosa, L. C., Boldison, J., Leenheer, E. D., Davies, J. E., Li, W., & Wong, F. S. (2018) · Diabetologia · doi:10.1007/s00125-018-4597-z · Cited by 22 · see citing works
Liang, Y., Tang, Y., Ren, C., Liu, M., Shen, J., & Hou, X. (2019) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0007474 · Cited by 21 · see citing works
Regulatory B cells mediate tolerance to apoptotic self in health: implications for disease
Gray, M., & Gray, D. (2015) · International Immunology · doi:10.1093/intimm/dxv045 · Cited by 20 · see citing works
Breg-Mediated Immunoregulation in the Skin
Zheremyan, E. A., Ustiugova, A. S., Karamushka, N. M., Uvarova, A. N., Stasevich, E. M., Васильевна, Б. А., Kuprash, D. V., & Korneev, K. V. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25010583 · Cited by 20 · see citing works
Baglaenko, Y., Manion, K., Chang, N., Gracey, E., Loh, C., & Wither, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150515 · Cited by 20 · see citing works
Dyevoich, A. M., Disher, N. S., Haro, M., & Haas, K. M. (2020) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-020-02607-7 · Cited by 20 · see citing works
Hosseini, H., Li, Y., Kanellakis, P., Cao, A. H., Tay, C., Peter, K., Bobik, A., Toh, B., & Kyaw, T. S. (2018) · Journal of the American Heart Association · doi:10.1161/jaha.117.008447 · Cited by 20 · see citing works
“Our data showed that TIM-1+ IgM+ IL-10+ B1a cells in the peritoneal cavity and spleen were also found to express CD1d and are most likely similar, to the recently described peritoneal and spleen B10 cells.(5,44) Chronic RMT1-10 treatment expands B1a cells in the spleen and peritoneal cavity, greatly increases plasma I…”
BackgroundIsolation of functional mature peritoneal macrophages from healthy humans
Ruiz‐Alcaraz, A. J., Martínez‐Banaclocha, H., Marín‐Sánchez, P., Carmona‐Martínez, V., Iniesta‐Albadalejo, M. A., Tristán‐Manzano, M., Tapia‐Abellán, A., García–Peñarrubia, P., Machado‐Linde, F., Pelegrı́n, P., et al. (2019) · Immunology and Cell Biology · doi:10.1111/imcb.12305 · Cited by 20 · see citing works
van der Vlugt, L. E. P. M., Obieglo, K., Ozir‐Fazalalikhan, A., Sparwasser, T. D., Haeberlein, S., & Smits, H. H. (2017) · International Journal for Parasitology · doi:10.1016/j.ijpara.2017.02.002 · Cited by 19 · see citing works
“Breg cells have also been found within the mesenteric lymph node (LN), highly expressing the low-affinity IgE Fc receptor CD23 during Heligmosomoides polygyrus infection (Wilson et al., 2010), and within the B-1a B cell compartment of the peritoneal cavity (Maseda et al., 2013).”
BackgroundAlmishri, W., Deans, J. P., & Swain, M. G. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.06.007 · Cited by 18 · see citing works
“B1 cells are found mainly within the peritoneum [25, 26], and both B1a and B1b B cells were readily identified within the peritoneal cavity (Fig.”
BackgroundAblation of STAT3 in the B Cell Compartment Restricts Gammaherpesvirus Latency In Vivo
Reddy, S., Foreman, H., Sioux, T. O., Park, G. H., Poli, V., Reich, N., & Krug, L. (2016) · mBio · doi:10.1128/mbio.00723-16 · Cited by 17 · see citing works
New insights into heterogeneity of peritoneal B‐1a cells
Wang, H., Lin, J.-X., Li, P., Skinner, J., Leonard, W. J., & Morse, H. C. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12791 · Cited by 17 · see citing works
Role of Immune Cells and Immunotherapy in Multiple Myeloma
Radhakrishnan, V., Golla, U., & Kudva, A. K. (2024) · Life · doi:10.3390/life14040461 · Cited by 18 · see citing works
“B1a (natural antibody-producing cells) have been demonstrated to contribute to autoimmune disease by autoantibody generation [54,55], antigen presentation and activation of CD4 T cells [56], and cytokine production [57].”
BackgroundThe Role of Regulatory B cells in Kidney Diseases
Wang, L., Zhang, H., Yuan, W., Lan, G., Lin, Z., Peng, L., & Dai, H. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.683926 · Cited by 16 · see citing works
“Peritoneal B1a B cells CD19CD5 CD11b – (50, 62)”
Lomakin, Y., Zvyagin, I., Ovchinnikova, L. A., Kabilov, M. R., Staroverov, D., Mikelov, A., Tupikin, A., Zakharova, M., Bykova, N., Mukhina, V., et al. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.803229 · Cited by 14 · see citing works
The Generation of Regulatory B Cells by Helminth Parasites
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Suppression of autoimmunity by CD5+ IL-10-producing B cells in lupus-prone mice
Baglaenko, Y., Manion, K., Chang, N.-H., Loh, C., Lajoie, G., & Wither, J. (2015) · Genes and Immunity · doi:10.1038/gene.2015.17 · Cited by 13 · see citing works
Dysregulation of peritoneal cavity B1a cells and murine primary biliary cholangitis
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Noncanonical B Cells: Characteristics of Uncharacteristic B Cells
Haas, K. M. (2023) · The Journal of Immunology · doi:10.4049/jimmunol.2200944 · Cited by 12 · see citing works
Xiang, W.-W., Xie, C., & Guan, Y. (2021) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2021.577520 · Cited by 12 · see citing works
Pedersen, G. K., Ádori, M., Stark, J. M., Khoenkhoen, S., Arnold, C., Beutler, B., & Hedestam, G. B. K. (2016) · Frontiers in Immunology · doi:10.3389/fimmu.2016.00065 · Cited by 11 · see citing works
“The main IL-10 producing innate-like B cells, collectively named B10, are found within the MZB (5) and B-1a cell subsets (4, 6).”
Background
- Authors
- Maseda, D., Candando, K. M., Smith, S. H., Kalampokis, I., Weaver, C. T., Plevy, S. E., Poe, J. C., & Tedder, T. F.
- Affiliations
- Department of Immunology, Duke University Medical Center , Durham, NC 27710
- Duke Medical Center (US)
- University of Alabama at Birmingham (US)
- University of North Carolina at Chapel Hill (US)
- Corresponding author
- Tedder, Thomas F
- Venue
- The Journal of Immunology
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-09-01
- Volume
- 191
- Issue
- 5
- Pages
- 2780-2795
- ISSN
- 0022-1767 (ISSN-L)
- 1550-6606
- PMC
- PMC3770313
- OpenAlex
- W2170857080
- Cited by
- 144
- References
- 73
- Citations by year
- 2026: 7 · 2025: 3 · 2024: 7 · 2023: 4 · 2022: 5 · 2021: 10 · 2020: 13 · 2019: 18 · 2018: 11 · 2017: 14 · 2016: 17 · 2015: 21 · 2014: 12 · 2013: 1
- FWCI
- 9.41
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- The Journal of Immunology (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (P30CA016086)
- National Institute of Allergy and Infectious Diseases (AI 057157, U54AI057157, U19AI056363, AI-56363)
- National Institute of Diabetes and Digestive and Kidney Diseases (DK054452, R01DK054452)
- Topics
- Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Inflammatory Bowel Disease
- Health Sciences › Medicine › Rheumatology › Rheumatoid Arthritis Research and Therapies
- Keywords
- regulatory B cells, B10 cells, peritoneal cavity, IL-10, colitis, B cell subsets, B cell receptor repertoire, commensal microbiota, neutrophil infiltration, inflammatory cytokines, gut immune homeostasis
- MeSH terms
- Animals, Colitis, Disease Models, Animal, Enzyme-Linked Immunosorbent Assay, Fluorescent Antibody Technique, Interferon-gamma, Male, Mice, Inbred C57BL, Peritoneal Cavity, CD4-Positive T-Lymphocytes, Lymphocyte Subsets, Interleukin-10, Mice, Knockout, Adoptive Transfer, Mice, B-Lymphocytes, Regulatory
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