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Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation

Nature Immunology volume 12, pages 898–907 (2011)Cite this article

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Abstract

Regulatory T cells (Treg cells) are essential for self-tolerance and immune homeostasis. Lack of effector T cell (Teff cell) function and gain of suppressive activity by Treg cells are dependent on the transcriptional program induced by Foxp3. Here we report that repression of SATB1, a genome organizer that regulates chromatin structure and gene expression, was crucial for the phenotype and function of Treg cells. Foxp3, acting as a transcriptional repressor, directly suppressed the SATB1 locus and indirectly suppressed it through the induction of microRNAs that bound the SATB1 3′ untranslated region. Release of SATB1 from the control of Foxp3 in Treg cells caused loss of suppressive function, establishment of transcriptional Teff cell programs and induction of Teff cell cytokines. Our data support the proposal that inhibition of SATB1-mediated modulation of global chromatin remodeling is pivotal for maintaining Treg cell functionality.

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Figure 1: Foxp3-dependent repression of SATB1 expression in human Treg cells.
Figure 2: Restoration of SATB1 expression after silencing of Foxp3 in Treg cells.
Figure 3: Foxp3-dependent repression of SATB1 expression in mouse Treg cells.
Figure 4: Direct suppression of SATB1 transcription by Foxp3.
Figure 5: SATB1 expression in human Treg cells reprograms them into Teff cells.
Figure 6: Induction of transcriptional Teff cell programs in SATB1-expressing Treg cells.
Figure 7: Repression of SATB1 expression by miRNA in Treg cells.
Figure 8: Ectopic expression of SATB1 in Treg cells results in less suppressive function in vivo.

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Acknowledgements

We thank M. Mai, M. Kraut, S. Keller, N. Kuhn, J. Birke, I. Büchmann, A. Dolf and P. Wurst for technical assistance; M. Hoch, M. Pankratz, S. Burgdorf, A. Popov and A. Staratschek-Jox, as well as all other laboratory members, for discussions; and J. Oldenburg for blood samples from healthy subjects. Supported by the German Research Foundation (Sonderforschungsbereich 832, SFB 704, INST 217/576-1 and INST 217/577-1 to J.L.S. and M.B.), the Wilhelm-Sander-Foundation (J.L.S. and M.B.), the German Cancer Aid (J.L.S.), the German Jose-Carreras-Foundation (J.L.S. and M.B.), the Federal Ministry of Education and Research (Nationale Genomforschungsnetz 2 to J.L.S.), the Humboldt Foundation (J.L.S.), the Leukemia and Lymphoma Society of America (R6029-07 to B.R.B. and K.L.H.), the Juvenile Diabetes Research Foundation (16-2008-643 to X.Z., S.L.B.-B. and J.A.B.), the University of California, San Francisco, Autoimmunity Center of Excellence (X.Z., S.L.B.-B. and J.A.B.), the National Health and Medical Research Council (339123, 565314 to S.C.B.), the German Research Foundation (SCHE 1562 and SFB832 to B.S.), the Juvenile Diabetes Research Foundation Collaborative Centers for Cell Therapy (S.B., T.G. and J.L.R.) and the Juvenile Diabetes Research Foundation Center on Cord Blood Therapies for Type 1 Diabetes (S.B., T.G. and J.L.R.).

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Authors and Affiliations

  1. Life and Medical Sciences Institute, Laboratory for Genomics and Immunoregulation, University of Bonn, Bonn, Germany

    Marc Beyer, Yasser Thabet, Sabine Classen, Wolfgang Krebs, Eva A Schönfeld, Andrea Hofmann, Daniel Sommer, Svenja Debey-Pascher & Joachim L Schultze

  2. Renal Division, Department of Medicine and Centre for Molecular Medicine, University of Cologne, Cologne, Germany

    Roman-Ulrich Müller & Bernhard Schermer

  3. Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases, University of Cologne, Cologne, Germany

    Roman-Ulrich Müller & Bernhard Schermer

  4. Discipline of Paediatrics, Women's and Children's Health Research Institute, University of Adelaide, North Adelaide, Australia

    Timothy Sadlon & Simon C Barry

  5. Institute of Infection Immunology, TWINCORE, Centre for Experimental and Clinical Infection Research, a joint venture between the Medical School Hannover and the Helmholtz Centre for Infection Research, Hannover, Germany

    Katharina Lahl, Christian T Mayer & Tim Sparwasser

  6. Department of Microbiology, Translational Research Program, Abramson Family Cancer Research Institute, University of Pennsylvania, Philadelphia, Philadelphia, USA

    Samik Basu, Tatiana Golovina & James L Riley

  7. Diabetes Center and the Department of Medicine, University of California, San Francisco, California, USA

    Xuyu Zhou, Samantha L Bailey-Bucktrout & Jeffrey A Bluestone

  8. Institutes of Molecular Medicine and Experimental Immunology, University Hospital Bonn, Bonn, Germany

    Jan Böttcher, Elmar Endl, Andreas Limmer & Percy A Knolle

  9. Cancer Center and Department of Pediatrics, Division of Blood and Marrow Transplantation, University of Minnesota, Minneapolis, Minnesota, USA

    Keli L Hippen & Bruce R Blazar

  10. BD Biosciences–Pharmingen, San Diego, California, USA

    Robert Balderas

  11. Life and Medical Sciences Institute, Laboratory for Molecular Immunology, University of Bonn, Bonn, Germany

    Thomas Quast & Waldemar Kolanus

  12. Department of Neuropathology, University Hospital Bonn, Bonn, Germany

    Andreas Waha

  13. Life and Medical Sciences Institute, Laboratory of Chemical Biology, University of Bonn, Bonn, Germany

    Günter Mayer & Michael Famulok

  14. Department for Diagnostic, Institute for Pathology, University Hospital Leipzig, Leipzig, Germany

    Claudia Wickenhauser

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Contributions

M.B. designed, did and supervised experiments, analyzed data and wrote the manuscript; Y.T. did quantitative PCR, cytometric bead assay, immunoblot analysis, overexpression experiments and filter-retention analysis and analyzed data; R.-U.M. designed and did reporter assays; S.C. did experiments and analyzed data; T.S. did ChIP experiments and analyzed data; K.L. and C.T.M. did experiments with DEREG mice; S.B. and T.G. did overexpression experiments; E.A.S. did and analyzed immunofluorescence experiments; W.K. did histone-methylation studies, S.L.B.-B. and X.Z. did experiments with mice with loxP-flanked Dicer1 alleles; A.H. did bioinformatics analysis; D.S. generated lentivirus contructs; S.D.-P. did microarray experiments; E.E. did flow cytometry sorting; J.B. and A.L. did experiments with Rag2−/− mice; P.A.K. was involved in study design; K.L.H. and B.R.B. provided vital analytical tools; R.B. provided vital analytical tools; T.Q. supervised and analyzed immunofluorescence experiments; C.W. did immunohistochemistry; A.W. did, designed and supervised DNA-methylation experiments; G.M. and M.F. designed and supervised filter-retention experiments; W.K. designed and supervised experiments and wrote the manuscript; B.S. designed and analyzed reporter assays; S.C.B. designed and supervised ChIP experiments; T.S. designed and supervised experiments with DEREG mice and provided vital analytical tools; J.A.B. designed and supervised experiments with mice with loxP-flanked Dicer1 alleles; J.L.R. designed and supervised SATB1-overexpression experiments and wrote the manuscript; J.L.S. designed, supervised and analyzed experiments and wrote the manuscript; and all authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Joachim L Schultze.

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Competing interests

Research support to J.L.S. and M.B. has been provided in part by Becton Dickinson; R.B. is employed by Becton Dickinson; S.C. is employed by Miltenyi Biotech; and J.L.S., M.B. and R.B. have applied for several US and international patents on Treg cell biology.

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Beyer, M., Thabet, Y., Müller, RU. et al. Repression of the genome organizer SATB1 in regulatory T cells is required for suppressive function and inhibition of effector differentiation. Nat Immunol 12, 898–907 (2011). https://doi.org/10.1038/ni.2084

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