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A dual function for the chromatin organizer Special A-T rich Binding Protein 1 in B-lineage cells

Cellular & Molecular Immunology volume 20, pages 1114–1126 (2023)Cite this article

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Abstract

SATB1 (Special A-T rich Binding protein 1) is a cell type-specific factor that regulates the genetic network in developing T cells and neurons. In T cells, SATB1 is required for lineage commitment, VDJ recombination, development and maturation. Considering that its expression varies during B-cell differentiation, the involvement of SATB1 needs to be clarified in this lineage. Using a KO mouse model in which SATB1 was deleted from the pro-B-cell stage, we examined the consequences of SATB1 deletion in naive and activated B-cell subsets. Our model indicates first, unlike its essential function in T cells, that SATB1 is dispensable for B-cell development and the establishment of a broad IgH repertoire. Second, we show that SATB1 exhibits an ambivalent function in mature B cells, acting sequentially as a positive and negative regulator of Ig gene transcription in naive and activated cells, respectively. Third, our study indicates that the negative regulatory function of SATB1 in B cells extends to the germinal center response, in which this factor limits somatic hypermutation of Ig genes.

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Data availability

Raw data from RNA-seq, SHM, Rep-Seq, and 3C-HTGTS have been deposited in the European Nucleotide Archive database under accession number PRJEB52320.

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Acknowledgements

The authors are grateful to the BISCEm unit (Univ. Limoges, UAR 2015 CNRS, US 42 Inserm, CHU Limoges) for technical support regarding DNA‒RNA sequencing, cytometry experiments and the animal core facility. We are grateful to Emeline Lhuillier and the Genotoul Plateau GeT-Santé facility (https://get.genotoul.fr) for technical assistance with RNA sequencing, to Mehdi Alizadeh from Etablissement Français du Sang (Rennes; France) for assistance with Repertoire sequencing and to Christelle Oblet for technical help with Western blotting. This work benefitted from data assembled by the ImmGen consortium [50]. MT, CB and OM were supported by PhD fellowships from the French Ministère de l’Enseignement Supérieur, de la Recherche et de l’Innovation and the Fonds Européen de Développement Régional (FEDER). This work was supported by La Ligue Contre le Cancer (comités 87, 23 to EP and SLN); the Fondation ARC pour la recherche sur le cancer (PJA 20181207918 to EP and PhD continuation fellowship to MT and CB), Institut CARNOT CALYM, INCa-Cancéropôle GSO Emergence (to EP). We are grateful to Drs. Charalampos Spilianakis, Jeanne Moreau and Amélie Bonaud for critical reading of the manuscript, helpful comments and edits.

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  1. Morgane Thomas

    Present address: Laboratoire Suivi des Thérapies Innovantes, Institut de Génétique Humaine, UMR 9002 CNRS-UM, Montpellier, France

Authors and Affiliations

  1. Laboratoire Contrôle de la Réponse Immune B et des Lymphoproliférations (CRIBL), Université de Limoges, CNRS Unité Mixte de Recherche 7276, Inserm Unité 1262, Limoges, France

    Morgane Thomas, Charlotte Bruzeau, Ophélie Alyssa Martin, Justine Pollet, Sébastien Bender, Claire Carrion, Sandrine Le Noir & Eric Pinaud

  2. Centre Hospitalier Universitaire Dupuytren, Service d’Immunopathologie, Limoges, France

    Sébastien Bender

  3. Centre Hospitalier Universitaire de Limoges, Centre National de l’Amylose AL et Autres Maladies par Dépôt d’Immunoglobulines Monoclonales, Limoges, France

    Sébastien Bender

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Contributions

MT, CB, OM, SB, and CC performed the experiments. MT analyzed the data. EP and SLN conceived and supervised the study. MT and OM developed the experimental model. JP performed the bioinformatic analysis. MT, CB, EP, and SLN wrote the manuscript.

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Thomas, M., Bruzeau, C., Martin, O.A. et al. A dual function for the chromatin organizer Special A-T rich Binding Protein 1 in B-lineage cells. Cell Mol Immunol 20, 1114–1126 (2023). https://doi.org/10.1038/s41423-023-01069-y

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