Cited by 436T-cell and B-cell ImmunologyImmune Response and InflammationMultiple Sclerosis Research Studies

The DOI matches its Crossref record; 79 of the 81 references it cites were found in a registry or an index.

TLR-Activated B Cells Suppress T Cell-Mediated Autoimmunity

Lampropoulou, Vicky, Hoehlig, Kai, Roch, Toralf, Neves, Patricia, Gómez, Elisabeth Calderón, Sweenie, Claire H, Hao, Yi, Freitas, Antonio A, Steinhoff, Ulrich, Anderton, Stephen M, Fillatreau, Simon·2008·The Journal of Immunology

DOI 10.4049/jimmunol.180.7.4763

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Abstract

TLR sense microbial infections, and control activation of immune responses. Dendritic cells, macrophages, and B lymphocytes express TLR and the TLR-signaling adaptor protein MyD88. The impact of TLR-activated B cells on T cell-mediated inflammation is unknown. In this study, we have used mice carrying B cell-restricted deficiencies in MyD88 or in distinct TLR to examine the impact of TLR-activated B cells on a T cell-mediated autoimmune disease, experimental autoimmune encephalomyelitis (EAE). We demonstrate that TLR-signaling in B cells suppresses inflammatory T cell responses (both Th1 and Th17), and stimulates recovery from EAE. Only certain TLR are required on B cells for resolution of EAE, and these are dispensable for disease initiation, indicating that a category of TLR agonists preferentially triggers a suppressive function in B cells and thereby limits autoimmune disease. The TLR agonists controlling the regulatory function of B cells are provided by components of Mycobacterium tuberculosis present in the adjuvant. Thus, MyD88 signaling in B cells antagonizes MyD88 signaling in other cells, which drives differentiation of Th17 cells and is required for induction of EAE. Altogether, our data indicate that B cells link recognition of microbial products via TLR to suppression of a T cell-mediated autoimmune disease.

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Oral Combined Therapy with Probiotics and Alloantigen Induces B Cell–Dependent Long-Lasting Specific Tolerance
Mercadante, A. C. T., Perobelli, S. M., Alves, A. P. G., Gonçalves-Silva, T., Mello, W., Gomes-Santos, A. C., Miyoshi, A., Faria, A. C., & Bonomo, A. (2014) · Journal of Immunology · doi:10.4049/jimmunol.1301034 · Cited by 20
Hepatic B cells are readily activated by Toll-like receptor-4 ligation and secrete less interleukin-10 than lymphoid tissue B cells
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A New Paradigm for an Old Story: The Role of Regulatory B Cells in Cancer
Biragyn, A., & Lee-Chang, C. (2012) · Frontiers in Immunology · doi:10.3389/fimmu.2012.00206 · Cited by 21
“Humans also have IL-10 and TGFβ-producing CD25hi CD27hi CD86hi CD1dhi B cells that can suppress proliferation of autologous T cells and induce the generation of Foxp3+ CTLA-4+ Tregs (Kessel et al., 2012).”
BackgroundInfluential
B cells in allergic diseases: Bad or Better?
Smits, H. H. (2012) · Autoimmunity · doi:10.3109/08916934.2012.665525 · Cited by 18
“Since then, a large number of other mouse studies have confirmed the regulatory potential of IL-10 producing B cells in either similar or other models of auto-immunity, including inflammatory bowel disease (IHB) [27,28], EAE [29,30], type 1 diabetes [31] or systemic lupus erythematosus (SLE) [32–34].”
BackgroundInfluential
Pharmacologic P2X purinergic receptor antagonism in the treatment of collagen-induced arthritis.
Ardissone, V., Radaelli, E., Zaratin, P., Ardizzone, M., Ladel, C., Gattorno, M., Martini, A., Grassi, F., & Traggiai, E. (2011) · Arthritis & Rheumatism · doi:10.1002/art.30556 · Cited by 20
Oxidative phosphorylation regulates interleukin‐10 production in regulatory B cells via the extracellular signal‐related kinase pathway
Zhu, Y., Zhang, X., Xie, S., Bao, W., Chen, J., Wu, Q., Lai, X., Liu, L., Xiong, S., & Peng, Y. (2022) · Immunology · doi:10.1111/imm.13554 · Cited by 21
TLR9 and its signaling pathway in multiple sclerosis
Zhou, Y., Fang, L., Peng, L., & Qiu, W. (2016) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2016.12.027 · Cited by 24
Regulatory B Cells: Key Players in Hepatocellular Carcinoma Progression
Hetta, H., Elkady, A., Tohamy, T. A., & Badary, M. (2016) · Gastroenterology & Hepatology Open Access · doi:10.15406/ghoa.2016.05.00136 · Cited by 19
Pathogenic functions of B cells in autoimmune diseases: IFN‐γ production joins the criminal gang
Fillatreau, S. (2015) · European Journal of Immunology · doi:10.1002/eji.201545544 · Cited by 19
Self-citation
Differentially activated B cells develop regulatory phenotype and show varying immunosuppressive features: a comparative study
Zheremyan, E. A., Ustiugova, A. S., Uvarova, A. N., Karamushka, N. M., Stasevich, E. M., Gogoleva, V. S., Васильевна, Б. А., Mitkin, N. A., Kuprash, D. V., & Korneev, K. V. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1178445 · Cited by 19
Regulatory B cells in transplantation: roadmaps to clinic
Beckett, J., Hester, J., Issa, F., & Shankar, S. (2020) · Transplant International · doi:10.1111/tri.13706 · Cited by 17
“in vivo, optimal production of IL-10 occurred after TLR-activated B cells interacted with CD154-expressing CD4 T cells [58,59].”
Background
Reducing the Endotoxin Burden of Desaminotyrosine‐ and Desaminotyrosyl Tyrosine‐Functionalized Gelatin
Roch, T., Pierce, B. F., Zaupa, A., Jung, F., Neffe, A., & Lendlein, A. (2011) · Macromolecular Symposia · doi:10.1002/masy.201100048 · Cited by 18
Self-citation
Regulatory B cells in experimental autoimmune encephalomyelitis (EAE).
Ray, A., & Basu, S. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1161-5_17 · Cited by 18
Pharmacogenomic and epigenomic approaches to untangle the enigma of IL-10 blockade in oncology
Elemam, N. M., Mekky, R. Y., Rashid, G., Braoudaki, M., & Youness, R. A. (2024) · Expert Reviews in Molecular Medicine · doi:10.1017/erm.2023.26 · Cited by 19
The Role of the Oxidative State and Innate Immunity Mediated by TLR7 and TLR9 in Lupus Nephritis
Miranda‐Díaz, A. G., Echavarría, R., Cardona-Muñóz, E. G., Ortiz‐Lazareno, P. C., Sierra, J. A., Gómez-Hermosillo, L. F., Casillas-Moreno, J., Campos-Bayardo, T. I., Román-Rojas, D., & García-Sánchez, A. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms242015234 · Cited by 17
“Genetic association studies implicate TLR signaling in SLE [63].”
Background
Towards regulatory cellular therapies in solid organ transplantation
Bottomley, M. J., Brook, M. O., Shankar, S., Hester, J., & Issa, F. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.11.001 · Cited by 21
Macrophage regulation of B cell proliferation
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Innate Immune Responses in the CNS: Role of Toll-Like Receptors, Mechanisms, and Therapeutic Opportunities in Multiple Sclerosis
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“TLR4 expression has also been observed in B cells, which are thought to affect MS through mechanisms including the production of regulatory cytokines (IL-10 and TGF-β) and the production of antibodies (Mizoguchi and Bhan 2006).”
Toll-like receptor 4-activated B cells out-compete Toll-like receptor 9-activated B cells to establish peripheral immunological tolerance
Matheu, M. P., Su, Y. A., Greenberg, M. L., Blanc, C. A., Parker, I., Scott, D. W., & Cahalan, M. D. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1205150109 · Cited by 16
“Our study builds on previous investigations of tolerance induction in which adoptive transfer of LPS-activated B cells expressing antigen (hereafter, “LPS B cells”) led to tolerance and to suppression of experimental autoimmune encephalomyelitis, whereas transfer of B cells activated by unmethylated CpG oligonucleotid…”
Result
B-Cell Gene Therapy for Tolerance Induction: Host but Not Donor B-Cell Derived IL-10 is Necessary for Tolerance
Su, Y.-X., Zhang, A.-H., Noben-Trauth, N., & Scott, D. (2011) · Front. Microbio. · doi:10.3389/fmicb.2011.00154 · Cited by 17
What are regulatory B cells?
Gray, D., & Gray, M. (2010) · European Journal of Immunology · doi:10.1002/eji.201040961 · Cited by 17
Function and dysfunction of dendritic cells in autoimmune rheumatic diseases
Rutella, S., CRISTOFARO, R. D., & Ferraccioli, G. (2009) · Human Immunology · doi:10.1016/j.humimm.2009.01.023 · Cited by 14
TCL1A, B Cell Regulation and Tolerance in Renal Transplantation
Brinas, F., Danger, R., & Brouard, S. (2021) · Cells · doi:10.3390/cells10061367 · Cited by 20
Regulatory B cells induced by ultraviolet B through toll‐like receptor 4 signalling contribute to the suppression of contact hypersensitivity responses in mice
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Plasmacytoid dendritic cells control B cell-derived IL-10 production
Georg, P., & Bekeredjian-Ding, I. (2012) · Autoimmunity · doi:10.3109/08916934.2012.719955 · Cited by 16
Chapter 1 Immune Regulation by B Cells and Antibodies
Hoehlig, K., Lampropoulou, V., Roch, T., Neves, P., Calderón‐Gómez, E., Anderton, S. M., Steinhoff, U., & Fillatreau, S. (2008) · Advances in immunology · doi:10.1016/s0065-2776(08)00401-x · Cited by 23
Self-citation
Intruders or protectors – the multifaceted role of B cells in CNS disorders
Aspden, J. W., Murphy, M. A., Kashlan, R. D., Xiong, Y., Poznansky, M. C., & Sîrbulescu, R. F. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1329823 · Cited by 16
Characterization of Definitive Regulatory B Cell Subsets by Cell Surface Phenotype, Function and Context
Neu, S. D., & Dittel, B. N. (2021) · Frontiers in Immunology · doi:10.3389/fimmu.2021.787464 · Cited by 23
“Interestingly, CFA used to induce EAE has numerous TLR ligands and B cells stimulated via TLR ligands were shown to suppress EAE (44, 46).”
Background
Leptin: an unappreciated key player in SLE
Yuan, Q., Chen, H., Li, X., & Wei, J. (2019) · Clinical Rheumatology · doi:10.1007/s10067-019-04831-8 · Cited by 18
Recombinant murine calreticulin fragment 39-272 expands CD1d(hi)CD5+ IL-10-secreting B cells that modulate experimental autoimmune encephalomyelitis in C57BL/6 mice.
Hong, C., Zhang, T., & Gao, X.-M. (2013) · Molecular Immunology · doi:10.1016/j.molimm.2013.02.003 · Cited by 15
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
“Using EAE, the experimental mouse model of autoimmune diseases, a significant impact of TLR-signaling on B cells was revealed (85).”
Background
Murine gammaherpesvirus M2 antigen modulates splenic B cell activation and terminal differentiation in vivo
Terrell, S. L., & Speck, S. H. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006543 · Cited by 14
“Activation of TLR, CD40, and/or BCR signaling induces IL10 production in B cells, but the mechanisms underlying the development and function of IL10-competent B cells have yet to be fully elucidated [26, 31, 32].”
Background
Toll-like receptor (TLR)7 and TLR9 agonists enhance interferon (IFN) beta-1a's immunoregulatory effects on B cells in patients with relapsing-remitting multiple sclerosis (RRMS).
Tao, Y.-Z., Zhang, X., & Markovic-Plese, S. (2016) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2016.07.019 · Cited by 14
“However, B cell TLR9-deficient mice did not differ from wild type mice in their susceptibility to EAE (Lampropoulou et al., 2008).”
Depletion of regulatory T cells leads to an exacerbation of delayed-type hypersensitivity arthritis in C57BL/6 mice that can be counteracted by IL-17 blockade
Atkinson, S. M., Hoffmann, U., Hamann, A., Bach, E., Danneskiold‐Samsøe, N. B., Kristiansen, K., Serikawa, K. A., Fox, B. A., Kruse, K., Haase, C., et al. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.022905 · Cited by 17
“In experimental autoimmune encephalitis (EAE), components from Mycobacterium tuberculosis in the complete Freund ’ s adjuvant (CFA) that is used to induce disease provide Toll-like receptor (TLR) agonists that can trigger regulatory functions of B cells that are required for the resolution of EAE (Lampropoulou et al.,…”
Method
Adaptive Immune Responses in CNS Autoimmune Disease: Mechanisms and Therapeutic Opportunities
McPherson, R. C., & Anderton, S. (2013) · Journal of Neuroimmune Pharmacology · doi:10.1007/s11481-013-9453-9 · Cited by 14
Self-citation
Higher CD19+CD25+ Bregs are independently associated with better graft function in renal transplant recipients
Ibrahim, E., Aly, M., Opelz, G., Morath, C., Zeier, M., Süsal, C., Sayed, D., Hassan, E., Ekpoom, N., & Daniel, V. (2021) · BMC Nephrology · doi:10.1186/s12882-021-02374-2 · Cited by 13
A combination of the percentages of IFN-γ+CD4+T cells and granzyme B+CD19+B cells is associated with acute hepatic rejection: a case control study
Zhu, J.-Q., Wang, J., Li, X.-L., Xu, W.-L., Lv, S.-C., Zhao, X., Lang, R., & He, Q. (2021) · Journal of Translational Medicine · doi:10.1186/s12967-021-02855-w · Cited by 13
Phenotypes, roles, and modulation of regulatory lymphocytes in periodontitis and its associated systemic diseases
Zou, H., Zhou, N., Huang, Y., Luo, A., & Sun, J. (2021) · Journal of Leukocyte Biology · doi:10.1002/jlb.3vmr0321-027rrr · Cited by 18
B Cells Loaded with Synthetic Particulate Antigens: A Versatile Platform To Generate Antigen-Specific Helper T Cells for Cell Therapy.
Sicard, A., Koenig, A., Graff‐Dubois, S., Dussurgey, S., Rouers, A., Dubois, V., Blanc, P., Chartoire, D., Errazuriz-Cerda, E., Paidassi, H., et al. (2016) · Nano letters (Print) · doi:10.1021/acs.nanolett.5b03801 · Cited by 13
Cell Therapy to Induce Allograft Tolerance: Time to Switch to Plan B?
Sicard, A., Koenig, A., Morélon, E., Defrance, T., & Thaunat, O. (2015) · Frontiers in Immunology · doi:10.3389/fimmu.2015.00149 · Cited by 16
“In the mouse, a rare population of splenic B cells characterized by a unique phenotype (CD5+ CD1d high) has been reported to play a critical role in the regulation of murine EAE (94).”
BackgroundMethodInfluential
Reprogramming of B cells into regulatory cells with engineered fusokines
Deng, J.-S., & Galipeau, J. (2012) · Infectious Diseases - Drug Targets · doi:10.2174/187152612800564392 · Cited by 13
“As an anti-inflammatory cytokine, IL-10 inhibits T cell polarization and proliferation [42, 56, 58], blocks antigen presentation by antigen presenting cells, and inhibits inflammatory cytokine production by immune effector cells [39].”
Background
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
TLR7 Negatively Regulates B10 Cells Predominantly in an IFNγ Signaling Dependent Manner
Chodisetti, S. B., Fike, A. J., Domeier, P. P., Choi, N. M., Soni, C., & Rahman, Z. S. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01632 · Cited by 15
“Although various inflammatory cytokines (16–18) and tolllike receptor (TLR) signals (19) were previously described to regulate IL-10-producing Breg or B10 cells, the role of RNA sensing through TLR7 in the development of these regulatory B cells is unknown.”
Background
The regulatory roles of B cell subsets in transplantation
Chu, Z., Zou, W., Xu, Y., Sun, Q., & Zhao, Y. X. (2018) · Expert Review of Clinical Immunology · doi:10.1080/1744666x.2018.1426461 · Cited by 13
The atypical IκB protein IκBNS is important for Toll‐like receptor‐induced interleukin‐10 production in B cells
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B cells in MS: Why, where and how?
Pikor, N., & Gommerman, J. (2012) · Multiple Sclerosis and Related Disorders · doi:10.1016/j.msard.2012.03.006 · Cited by 12
“These disparate clinical outcomes revealed a regulatory IL-10 producing B cell subset that is polyclonally activated by toll like receptor antagonists contained in the adjuvant used for EAE induction (Lampropoulou et al., 2008; Yanaba et al., 2009).”
Background
Expanding Human Breg for Cellular Therapy in Transplantation: Time for Translation
McNee, A., Kannan, A., Jull, P., & Shankar, S. (2024) · Transplantation · doi:10.1097/tp.0000000000005243 · Cited by 11
“70,71 Other innate stimuli may induce similar Breg responses; ex vivo stimulation of mouse splenic mononuclear cells with LPS and Astilibin induced both CD19 + CD1d hi and CD19 + TIM-1 + Breg in STAT3-dependent mechanisms.”
TLR9/FCRL3 regulates B cell viability, apoptosis, and antibody and IL-10 production through ERK1/2, p38, and STAT3 signaling pathways
Liu, Q.-B., Zhou, R., & Liu, C. (2022) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-022-00720-8 · Cited by 11
“0.05 vs CpG. 708 1 3 TLR9 REGULATES B CELL BIOLOGICAL FUNCTIONS THROUGH FCRL3 promoting experimental autoimmune encephalomyelitis (EAE) recovery (Lampropoulou et al. 2008).”
BackgroundInfluential
Botanically-Derived Δ9-Tetrahydrocannabinol and Cannabidiol, and Their 1:1 Combination, Modulate Toll-like Receptor 3 and 4 Signalling in Immune Cells from People with Multiple Sclerosis
Fitzpatrick, J., Hackett, B., Costelloe, L., Hind, W. H., & Downer, E. J. (2022) · Molecules · doi:10.3390/molecules27061763 · Cited by 11
“Such TLR signalling cascades are activated via a suite of adaptor proteins, most commonly myeloid differentiation factor 88 (MyD88) [3].”
BackgroundInfluential
A higher frequency of IL‐10‐producing B cells in Hepatitis B virus‐associated membranous nephropathy
Liu, Y., Wang, H., Hu, X.-T., Qu, Z., Zhang, H., Crew, R. M., Ayana, D., Li, M., Qiu, J.-P., & Jiang, Y.-F. (2016) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/1440-1681.12552 · Cited by 11
Fluorescence tagging and inducible depletion of PD-L2–expressing B-1 B cells in vivo
Lee, R., Mao, C., Vo, H., Gao, W.-D., & Zhong, X. (2015) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12865 · Cited by 11

Authors: Lampropoulou, V., Hoehlig, K., Roch, T., Neves, P., Gómez, E. C., Sweenie, C. H., Hao, Y., Freitas, A. A., Steinhoff, U., Anderton, S. M., & Fillatreau, S.
Affiliations: German Rheumatism Research Centre (DE)
Deutsches Rheuma-ForschungsZentrum , Berlin ,
University of Edinburgh (GB)
Centre National de la Recherche Scientifique (FR)
Unité de Recherche Associée Centre National de la Recherche Scientifique 1961, Institut Pasteur , Paris ,
Max Planck Institute for Infection Biology (DE)
ORCID: Lampropoulou, Vicky
Hoehlig, Kai
Roch, Toralf
Hao, Yi
Steinhoff, Ulrich
Fillatreau, Simon
Venue: The Journal of Immunology
Publisher: Oxford University Press (OUP)
Published: 2008-04-01
Volume: 180
Issue: 7
Pages: 4763-4773
ISSN: 0022-1767 (ISSN-L)
1550-6606
DOI: 10.4049/jimmunol.180.7.4763
OpenAlex: W1918941126
Cited by: 436
References: 81
Citations by year: 2026: 11 · 2025: 7 · 2024: 11 · 2023: 13 · 2022: 17 · 2021: 23 · 2020: 13 · 2019: 17 · 2018: 24 · 2017: 24 · 2016: 41 · 2015: 31 · 2014: 34 · 2013: 40 · 2012: 33
FWCI: 13.45
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/pages/standard-publication-reuse-rights (vor)
Locations: The Journal of Immunology (publishedVersion)
PubMed (publishedVersion)
HAL (submittedVersion)
Max Planck Institute for Plasma Physics (submittedVersion)
Topics: Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
Life Sciences › Immunology and Microbiology › Immunology › Immune Response and Inflammation
Health Sciences › Medicine › Clinical Neurology › Multiple Sclerosis Research Studies
Keywords: MyD88, T cell-mediated autoimmunity, experimental autoimmune encephalomyelitis, Th17 cells, Th1 cells, B cell suppression, TLR agonists, dendritic cells, macrophages
MeSH terms: Animals, B-Lymphocytes, Dendritic Cells, Encephalomyelitis, Autoimmune, Experimental, Lymphocyte Activation, Mice, Inbred C57BL, Mycobacterium tuberculosis, T-Lymphocytes, Signal Transduction, Autoimmunity, Interleukin-10, Mice, Knockout, Toll-Like Receptors, Mice, Myeloid Differentiation Factor 88

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TLR-Activated B Cells Suppress T Cell-Mediated Autoimmunity

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