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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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References

  1. Sakaguchi, S., Yamaguchi, T., Nomura, T. & Ono, M. Regulatory T cells and immune tolerance. Cell 133, 775–787 (2008).

    Article  CAS  PubMed  Google Scholar 

  2. Lin, W. et al. Regulatory T cell development in the absence of functional Foxp3. Nat. Immunol. 8, 359–368 (2007).

    Article  CAS  PubMed  Google Scholar 

  3. Wan, Y.Y. & Flavell, R.A. Regulatory T-cell functions are subverted and converted owing to attenuated Foxp3 expression. Nature 445, 766–770 (2007).

    Article  CAS  PubMed  Google Scholar 

  4. Lahl, K. et al. Nonfunctional regulatory T cells and defective control of Th2 cytokine production in natural scurfy mutant mice. J. Immunol. 183, 5662–5672 (2009).

    Article  CAS  PubMed  Google Scholar 

  5. Williams, L.M. & Rudensky, A.Y. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat. Immunol. 8, 277–284 (2007).

    Article  CAS  PubMed  Google Scholar 

  6. Fontenot, J.D., Gavin, M.A. & Rudensky, A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330–336 (2003).

    Article  CAS  PubMed  Google Scholar 

  7. Hori, S., Nomura, T. & Sakaguchi, S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057–1061 (2003).

    Article  CAS  PubMed  Google Scholar 

  8. O'Shea, J.J. & Paul, W.E. Mechanisms underlying lineage commitment and plasticity of helper CD4v T cells. Science 327, 1098–1102 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Murphy, K.M. & Stockinger, B. Effector T cell plasticity: flexibility in the face of changing circumstances. Nat. Immunol. 11, 674–680 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Feuerer, M., Hill, J.A., Mathis, D. & Benoist, C. Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nat. Immunol. 10, 689–695 (2009).

    Article  CAS  PubMed  Google Scholar 

  11. Lee, Y.K., Mukasa, R., Hatton, R.D. & Weaver, C.T. Developmental plasticity of Th17 and Treg cells. Curr. Opin. Immunol. 21, 274–280 (2009).

    Article  CAS  PubMed  Google Scholar 

  12. Gavin, M.A. et al. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445, 771–775 (2007).

    Article  CAS  PubMed  Google Scholar 

  13. Pan, F. et al. Eos mediates Foxp3-dependent gene silencing in CD4+ regulatory T cells. Science 325, 1142–1146 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ouyang, W. et al. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nat. Immunol. 11, 618–627 (2010).

    Article  CAS  PubMed  Google Scholar 

  15. Harada, Y. et al. Transcription factors Foxo3a and Foxo1 couple the E3 ligase Cbl-b to the induction of Foxp3 expression in induced regulatory T cells. J. Exp. Med. 207, 1381–1391 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Zheng, Y. et al. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control TH2 responses. Nature 458, 351–356 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chaudhry, A. et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 326, 986–991 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Ziegler, S.F. FOXP3: of mice and men. Annu. Rev. Immunol. 24, 209–226 (2006).

    Article  CAS  PubMed  Google Scholar 

  19. Chong, M.M., Rasmussen, J.P., Rudensky, A.Y. & Littman, D.R. The RNAseIII enzyme Drosha is critical in T cells for preventing lethal inflammatory disease. J. Exp. Med. 205, 2005–2017 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Liston, A., Lu, L.F., O'Carroll, D., Tarakhovsky, A. & Rudensky, A.Y. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J. Exp. Med. 205, 1993–2004 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Zhou, X. et al. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205, 1983–1991 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Floess, S. et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5, e38 (2007).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Li, B. et al. FOXP3 interactions with histone acetyltransferase and class II histone deacetylases are required for repression. Proc. Natl. Acad. Sci. USA 104, 4571–4576 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Zhou, X., Bailey-Bucktrout, S., Jeker, L.T. & Bluestone, J.A. Plasticity of CD4+ FoxP3+ T cells. Curr. Opin. Immunol. 21, 281–285 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Alvarez, J.D. et al. The MAR-binding protein SATB1 orchestrates temporal and spatial expression of multiple genes during T-cell development. Genes Dev. 14, 521–535 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  26. Cai, S., Han, H.J. & Kohwi-Shigematsu, T. Tissue-specific nuclear architecture and gene expression regulated by SATB1. Nat. Genet. 34, 42–51 (2003).

    Article  CAS  PubMed  Google Scholar 

  27. Yasui, D., Miyano, M., Cai, S., Varga-Weisz, P. & Kohwi-Shigematsu, T. SATB1 targets chromatin remodelling to regulate genes over long distances. Nature 419, 641–645 (2002).

    Article  CAS  PubMed  Google Scholar 

  28. Dickinson, L.A., Joh, T., Kohwi, Y. & Kohwi-Shigematsu, T. A tissue-specific MAR/SAR DNA-binding protein with unusual binding site recognition. Cell 70, 631–645 (1992).

    Article  CAS  PubMed  Google Scholar 

  29. Cai, S., Lee, C.C. & Kohwi-Shigematsu, T. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 38, 1278–1288 (2006).

    Article  CAS  PubMed  Google Scholar 

  30. Pfoertner, S. et al. Signatures of human regulatory T cells: an encounter with old friends and new players. Genome Biol. 7, R54 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  31. Zheng, Y. et al. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445, 936–940 (2007).

    Article  CAS  PubMed  Google Scholar 

  32. Sugimoto, N. et al. Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int. Immunol. 18, 1197–1209 (2006).

    Article  CAS  PubMed  Google Scholar 

  33. Lund, R. et al. Identification of genes involved in the initiation of human Th1 or Th2 cell commitment. Eur. J. Immunol. 35, 3307–3319 (2005).

    Article  CAS  PubMed  Google Scholar 

  34. Chen, W. et al. Conversion of peripheral CD4+CD25− naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198, 1875–1886 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Lahl, K. et al. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 204, 57–63 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kuczma, M. et al. Foxp3-deficient regulatory T cells do not revert into conventional effector CD4+ T cells but constitute a unique cell subset. J. Immunol. 183, 3731–3741 (2009).

    Article  CAS  PubMed  Google Scholar 

  37. Ishihara, Y., Ito, F. & Shimamoto, N. Increased expression of c-Fos by extracellular signal-regulated kinase activation under sustained oxidative stress elicits BimEL upregulation and hepatocyte apoptosis. FEBS J. 278, 1873–1881 (2011).

    Article  CAS  PubMed  Google Scholar 

  38. Szymczak, A.L. et al. Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat. Biotechnol. 22, 589–594 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. Wei, G. et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155–167 (2009).

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lu, L.F. et al. Foxp3-dependent microRNA155 confers competitive fitness to regulatory T cells by targeting SOCS1 protein. Immunity 30, 80–91 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Kohlhaas, S. et al. Cutting edge: the Foxp3 target miR-155 contributes to the development of regulatory T cells. J. Immunol. 182, 2578–2582 (2009).

    Article  CAS  PubMed  Google Scholar 

  42. Marson, A. et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445, 931–935 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kitoh, A. et al. Indispensable role of the Runx1-Cbfβ transcription complex for in vivo-suppressive function of FoxP3+ regulatory T cells. Immunity 31, 609–620 (2009).

    Article  CAS  PubMed  Google Scholar 

  44. Rudra, D. et al. Runx-CBFβ complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10, 1170–1177 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Ahlfors, H. et al. SATB1 dictates expression of multiple genes including IL-5 involved in human T helper cell differentiation. Blood 116, 1443–1453 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Koch, M.A. et al. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10, 595–602 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Zhou, X. et al. Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo. Nat. Immunol. 10, 1000–1007 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Oldenhove, G. et al. Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection. Immunity 31, 772–786 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Brunkow, M.E. et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27, 68–73 (2001).

    Article  CAS  PubMed  Google Scholar 

  50. Classen, S. et al. Human resting CD4+ T cells are constitutively inhibited by TGF beta under steady-state conditions. J. Immunol. 178, 6931–6940 (2007).

    Article  CAS  PubMed  Google Scholar 

  51. Sadlon, T.J. et al. Genome-wide identification of human FOXP3 target genes in natural regulatory T cells. J. Immunol. 185, 1071–1081 (2010).

    Article  CAS  PubMed  Google Scholar 

  52. Wiznerowicz, M. & Trono, D. Conditional suppression of cellular genes: lentivirus vector-mediated drug-inducible RNA interference. J. Virol. 77, 8957–8961 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Tang, Q. et al. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J. Exp. Med. 199, 1455–1465 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. ten Hove, T. et al. Dichotomal role of inhibition of p38 MAPK with SB 203580 in experimental colitis. Gut 50, 507–512 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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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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