Cited by 144T-cell and B-cell ImmunologyInflammatory Bowel DiseaseRheumatoid Arthritis Research and Therapies

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Peritoneal Cavity Regulatory B Cells (B10 Cells) Modulate IFN-γ+CD4+ T Cell Numbers during Colitis Development in Mice

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Maseda, Damian, Candando, Kathleen M, Smith, Susan H, Kalampokis, Ioannis, Weaver, Casey T, Plevy, Scott E, Poe, Jonathan C, Tedder, Thomas F·2013·The Journal of Immunology

DOI 10.4049/jimmunol.1300649PMC PMC3770313

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Abstract

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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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
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
“In addition, several other B cell subsets manifest activities that overlap with B-1a cells, including B10 cells or Breg cells (81).”
Background
Indoleamine 2, 3-Dioxygenase Promotes Aryl Hydrocarbon Receptor-Dependent Differentiation Of Regulatory B Cells in Lung Cancer
Tousif, S., Wang, Y., Jackson, J. D., Hough, K. P., Strenkowski, J. G., Athar, M., Thannickal, V. J., McCusker, R. H., Ponnazhagan, S., & Deshane, J. S. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.747780 · Cited by 30
“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).”
Background
IL-10-producing B cells attenuate cardiac inflammation by regulating Th1 and Th17 cells in acute viral myocarditis induced by coxsackie virus B3
Wei, B. K., Deng, Y., Huang, Y., Gao, X., & Wu, W.-F. (2019) · Life Sciences · doi:10.1016/j.lfs.2019.116838 · Cited by 29
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 31
S1P Signalling Differentially Affects Migration of Peritoneal B Cell Populations In Vitro and Influences the Production of Intestinal IgA In Vivo
Kleinwort, A., Lührs, F., Heidecke, C.-D., Lipp, M., & Schulze, T. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020391 · Cited by 28
“About 50% of peritoneal B1a and 24% of peritoneal B1b B cells showed the capacity for Interleukin (IL)-10 production [41].”
Background
Role 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
“However, as a proinflammatory cytokine, the level of IL-12 was increased in patients with CD [60, 61].”
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Avoiding Immunological Rejection in Regenerative Medicine
Bolton, E. M., & Bradley, J. A. (2015) · Regenerative Medicine · doi:10.2217/rme.15.11 · Cited by 27
Transient BAFF Blockade Inhibits Type 1 Diabetes Development in Nonobese Diabetic Mice by Enriching Immunoregulatory B Lymphocytes Sensitive to Deletion by Anti-CD20 Cotherapy
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
“Peritoneal cavity B cells have been reported to possess regulatory functions through IL-10 production (42).”
Background
Gut Antibody Deficiency in a Mouse Model of CVID Results in Spontaneous Development of a Gluten-Sensitive Enteropathy
Mohammed, 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
Intraperitoneally Delivered Mesenchymal Stem Cells Alleviate Experimental Colitis Through THBS1-Mediated Induction of IL-10-Competent Regulatory B Cells
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
“Peritoneal cavity resident B cells and macrophages are both associated with IBD (56, 57).”
Background
What do we know about the role of regulatory B cells (Breg) during the course of infection of two major parasitic diseases, malaria and leishmaniasis?
Soares, 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
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
The yin and yang of B cells in a constant state of battle: intestinal inflammation and inflammatory bowel disease
Zogorean, R., & Wirtz, S. J. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1260266 · Cited by 26
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
“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…”
Background
Platelets convert peripheral blood circulating monocytes to regulatory cells via immunoglobulin G and activating-type Fcγ receptors
Inui, M., Tazawa, K., Kishi, Y., & Takai, T. (2015) · BMC Immunology · doi:10.1186/s12865-015-0086-z · Cited by 24
“particularly monocytes/macrophages, as a rich source of IL-10 in the bloodstream and tissues [7-13].”
Background
Transplantation 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 24
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
Expanding Diversity and Common Goal of Regulatory T and B Cells. I: Origin, Phenotype, Mechanisms
Bocian, K., Kiernozek, E., Domagala-Kulawik, J. J., Korczak-Kowalska, G., Stelmaszczyk‐Emmel, A., & Drela, N. (2017) · Archivum Immunologiae et Therapiae Experimentalis · doi:10.1007/s00005-017-0469-3 · Cited by 24
“…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).”
Background
B cell depletion reduces T cell activation in pancreatic islets in a murine autoimmune diabetes model
da 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
B1 cells protect against Schistosoma japonicum–induced liver inflammation and fibrosis by controlling monocyte infiltration
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
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 21
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 18
IL-10 Production Is Critical for Sustaining the Expansion of CD5+ B and NKT Cells and Restraining Autoantibody Production in Congenic Lupus-Prone Mice
Baglaenko, Y., Manion, K., Chang, N., Gracey, E., Loh, C., & Wither, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0150515 · Cited by 20
A TLR4–TRIF-dependent signaling pathway is required for protective natural tumor-reactive IgM production by B1 cells
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
Anti‐TIM‐1 Monoclonal Antibody (RMT1‐10) Attenuates Atherosclerosis By Expanding IgM‐producing B1a Cells
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 19
“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…”
Background
Isolation 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
Schistosome-induced pulmonary B cells inhibit allergic airway inflammation and display a reduced Th2-driving function
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 18
“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).”
Background
Rapid activation and hepatic recruitment of innate-like regulatory B cells after invariant NKT cell stimulation in mice
Almishri, W., Deans, J. P., & Swain, M. G. (2015) · Journal of Hepatology · doi:10.1016/j.jhep.2015.06.007 · Cited by 19
“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.”
Background
Ablation 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
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 16
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
“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].”
Background
The 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
“Peritoneal B1a B cells CD19CD5 CD11b – (50, 62)”
Deconvolution of B cell receptor repertoire in multiple sclerosis patients revealed a delay in tBreg maturation
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
The Generation of Regulatory B Cells by Helminth Parasites
Khan, A. R., Amu, S., Saunders, S. P., & Fallon, P. G. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1161-5_11 · Cited by 15
Rejection of xenogeneic porcine islets in humanized mice is characterized by graft-infiltrating Th17 cells and activated B cells
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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
Dysregulation of peritoneal cavity B1a cells and murine primary biliary cholangitis
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Noncanonical B Cells: Characteristics of Uncharacteristic B Cells
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The identification, development and therapeutic potential of IL-10-producing regulatory B cells in multiple sclerosis
Xiang, W., Xie, C., & Guan, Y. (2021) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2021.577520 · Cited by 12
Heterozygous Mutation in IκBNS Leads to Reduced Levels of Natural IgM Antibodies and Impaired Responses to T-Independent Type 2 Antigens
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“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
ORCID: Smith, Susan H
Kalampokis, Ioannis
Weaver, Casey T
Poe, Jonathan C
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
DOI: 10.4049/jimmunol.1300649
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
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
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
Health Sciences › Medicine › Gastroenterology › 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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Peritoneal Cavity Regulatory B Cells (B10 Cells) Modulate IFN-γ+CD4+ T Cell Numbers during Colitis Development in Mice

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