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IL-10-producing regulatory B cells are present and functional in primary Sjögren patients

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Fig. 1
Fig. 2

Data availability

All data generated or analyzed during this study are included in this published article.

Change history

Abbreviations

ANA:

anti-nuclear antibodies

Anti-SSA:

anti-sicca syndrome A

Anti-SSB:

anti-sicca syndrome A

B10+:

IL-10-producing B cells

B10neg:

IL-10 non-producing B cells

BFA:

Brefeldin A

ESSDAI:

Eular Sjögren Syndrome Disease Activity Index

PBMCs:

peripheral blood mononuclear cells

PMA:

Phorbol 12-myristate 13-acetate

pSS:

primary Sjögren syndrome

RA:

rheumatoid arthritis

RF:

rheumatoid factor

Th1:

T helper 1

TNFα T cells:

TNFα-producing T cells

Tregs:

regulatory T cells

References

  1. Mariette X, Criswell LA. Primary Sjögren’s syndrome. N Engl J Med. 2018;378(10):931–9.

    Article  Google Scholar 

  2. Sheldon J. Laboratory testing in autoimmune rheumatic diseases. Best Pract Res Clin Rheumatol. 2004;18(3):249–69.

    Article  CAS  Google Scholar 

  3. Fillatreau S, Sweenie CH, McGeachy MJ, Gray D, Anderton SM. B cells regulate autoimmunity by provision of IL-10. Nat Immunol. 2002;3(10):944–50.

    Article  CAS  Google Scholar 

  4. Mauri C, Gray D, Mushtaq N, Londei M. Prevention of arthritis by interleukin 10-producing B cells. J Exp Med. 2003;197(4):489–501.

    Article  CAS  Google Scholar 

  5. Carter NA, Vasconcellos R, Rosser EC, Tulone C, Muñoz-Suano A, Kamanaka M, et al. Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol. 2011;186(10):5569–79.

    Article  CAS  Google Scholar 

  6. Daien CI, Gailhac S, Mura T, Audo R, Combe B, Hahne M, et al. Regulatory B10 cells are decreased in patients with rheumatoid arthritis and are inversely correlated with disease activity. Arthritis Rheumatol (Hoboken, NJ). 2014;66(8):2037–46.

    Article  CAS  Google Scholar 

  7. Blair PA, Noreña LY, Flores-Borja F, Rawlings DJ, Isenberg DA, Ehrenstein MR, et al. CD19(+)CD24(hi)CD38(hi) B cells exhibit regulatory capacity in healthy individuals but are functionally impaired in systemic lupus erythematosus patients. Immunity. 2010;32(1):129–40.

    Article  CAS  Google Scholar 

  8. Flores-Borja F, Bosma A, Ng D, Reddy V, Ehrenstein MR, Isenberg DA, et al. CD19+CD24hiCD38hi B cells maintain regulatory T cells while limiting TH1 and TH17 differentiation. Sci Transl Med. 2013;5(173):173ra23.

    Article  Google Scholar 

  9. Simon Q, Pers J-O, Cornec D, Le Pottier L, Mageed RA, Hillion S. In-depth characterization of CD24(high)CD38(high) transitional human B cells reveals different regulatory profiles. J Allergy Clin Immunol. 2015.

  10. 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.

    Article  CAS  Google Scholar 

  11. Furuzawa-Carballeda J, Hernández-Molina G, Lima G, Rivera-Vicencio Y, Férez-Blando K, Llorente L. Peripheral regulatory cells immunophenotyping in primary Sjögren’s syndrome: a cross-sectional study. Arthritis Res Ther. 2013;15(3):R68.

    Article  Google Scholar 

  12. Lin W, Cerny D, Chua E, Duan K, Yi JTJ, Shadan NB, et al. Human regulatory B cells combine phenotypic and genetic hallmarks with a distinct differentiation fate. J Immunol. 2014;193(5):2258–66.

    Article  CAS  Google Scholar 

  13. Papp G, Gyimesi E, Szabó K, Zöld É, Zeher M. Increased IL-21 expression induces granzyme B in peripheral CD5(+) B Cells as a potential counter-regulatory effect in primary Sjögren’s syndrome. Mediat Inflamm. 2016;2016:4328372.

    Article  Google Scholar 

  14. Lin X, Wang X, Xiao F, Ma K, Liu L, Wang X, et al. IL-10-producing regulatory B cells restrain the T follicular helper cell response in primary Sjögren’s syndrome. Cell Mol Immunol. 2019;16(12):921–31.

    Article  CAS  Google Scholar 

  15. Iwata Y, Matsushita T, Horikawa M, Dilillo DJ, Yanaba K, Venturi GM, et al. Characterization of a rare IL-10-competent B-cell subset in humans that parallels mouse regulatory B10 cells. Blood. 2011;117(2):530–41.

    Article  CAS  Google Scholar 

  16. Szabó K, Papp G, Szántó A, Tarr T, Zeher M. A comprehensive investigation on the distribution of circulating follicular T helper cells and B cell subsets in primary Sjögren’s syndrome and systemic lupus erythematosus. Clin Exp Immunol. 2016;183(1):76–89.

    Article  Google Scholar 

  17. Furuzawa-Carballeda J, Sánchez-Guerrero J, Betanzos JL, Enriquez AB, Avila-Casado C, Llorente L, et al. Differential cytokine expression and regulatory cells in patients with primary and secondary Sjögren’s syndrome. Scand J Immunol. 2014;80(6):432–40.

    Article  CAS  Google Scholar 

  18. Vitali C, Bombardieri S, Jonsson R, Moutsopoulos HM, Alexander EL, Carsons SE, et al. Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis. 2002;61(6):554–8.

    Article  CAS  Google Scholar 

  19. Mielle J, Audo R, Hahne M, Macia L, Combe B, Morel J, et al. IL-10 producing B cells ability to induce regulatory T cells is maintained in rheumatoid arthritis. Front Immunol. 2018;9:961.

    Article  Google Scholar 

  20. Davies R, Hammenfors D, Bergum B, Jakobsen K, Solheim M, Vogelsang P, et al. Patients with primary Sjögren’s syndrome have alterations in absolute quantities of specific peripheral leucocyte populations. Scand J Immunol. 2017;86(6):491–502.

    Article  CAS  Google Scholar 

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Acknowledgments

We thank Sumaiya Hoque for English correction of the manuscript and Claire Rempenault for her help in writing the manuscript. We acknowledge the imaging facility MRI, member of the national infrastructure France-BioImaging, supported by the French National Research Agency (ANR-10-INBS-04, “Investments for the future”), and more especially, Myriam Boyer and Sarah Gailhac for the cell sorting.

Funding

We received the financial support of the GCS-MERRI Nimes Montpellier and the AFGS (Association Française des patients atteints de Gougerot Sjögren et syndromes secs).

Author information

Authors and Affiliations

  1. Institute of Molecular Genetics of Montpellier, CNRS, UMR5535, Montpellier, France

    Julie Mielle, Anaïz Nutz, Rachel Audo, Bernard Combe, Jacques Morel & Claire Daien

  2. Department of Rheumatology, Chu of Montpellier, University of Montpellier, Av Doyen G. Giraud, 34295, Montpellier, France

    Julie Mielle, Anaïz Nutz, Rachel Audo, Bernard Combe, Jacques Morel & Claire Daien

  3. Department of Internal Medicine and Multi-Organic Diseases, St Eloi Hospital, Montpellier, France

    Philippe Guillpain

  4. Montpellier University, Medical School, F-34967, Montpellier, France

    Philippe Guillpain & Claire Daien

  5. Department of Rheumatology, CHU Nîmes, EA 2415, University of Montpellier, Nîmes, France

    Cécile Gaujoux-Viala

Authors
  1. Julie Mielle
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  2. Anaïz Nutz
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  3. Philippe Guillpain
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  4. Rachel Audo
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  5. Cécile Gaujoux-Viala
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  6. Bernard Combe
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  7. Jacques Morel
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  8. Claire Daien
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Contributions

J.Mi designed and performed the experiments; collected, analyzed, and interpreted the data; and prepared and wrote the manuscript. A.R designed and performed the experiments; collected, analyzed, and interpreted the data; and wrote the manuscript. A.N. designed, conducted patient enrolment into the study and performed the experiments, interpreted the data, and critically read the manuscript. GV critically read the manuscript and gave scientific advice. P.G, B.C, and J.Mo contributed to patient enrolment into the study and critically read the manuscript. C.D. obtained financial support, designed the experiments, conducted patient enrolment into the study, interpreted the data, and wrote the manuscript. All the authors read and approved the final manuscript.

Corresponding author

Correspondence to Claire Daien.

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Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval and consent to participate

This study has been approved by the Medical Ethics Committee of Nimes hospital, France (CPP_2012-A00592-41).

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Not applicable.

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The original online version of this article was revised: The first name and last name of the authors in the published version of this article have been exchanged.

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Mielle, J., Nutz, A., Guillpain, P. et al. IL-10-producing regulatory B cells are present and functional in primary Sjögren patients. Immunol Res 69, 107–113 (2021). https://doi.org/10.1007/s12026-021-09171-x

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  • DOI: https://doi.org/10.1007/s12026-021-09171-x

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