IκBNS Protein Mediates Regulatory T Cell Development via Induction of the Foxp3 Transcription Factor

Immunity

Volumn 37, Issue 6, 2012, Pages 998-1008

  Schuster, Marc ^a,b   Glauben, Rainer ^c   Plaza Sirvent, Carlos ^a,b   Schreiber, Lisa ^a   Annemann, Michaela ^a,b   Floess, Stefan ^a   Kühl, Anja A ^c   Clayton, Linda K ^d   Sparwasser, Tim ^e   Schulze Osthoff, Klaus ^f   Pfeffer, Klaus ^g   Huehn, Jochen ^a   Siegmund, Britta ^c   Schmitz, Ingo ^a,b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^d HARVARD MEDICAL SCHOOL   (United States)

^e INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^f UNIVERSITY OF TÜBINGEN   (Germany)

^g HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; GAMMA INTERFERON; I KAPPA B; INTERLEUKIN 2; PROTEIN P50; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR REL; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CD4+ T LYMPHOCYTE; CELL COUNT; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VIABILITY; CHRONIC INFLAMMATION; CONTROLLED STUDY; GENE LOCUS; IN VITRO STUDY; LAMINA PROPRIA; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; STEM CELL;

ADOPTIVE TRANSFER; ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; I-KAPPA B PROTEINS; IMMUNOMODULATION; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, TRANSGENIC; NF-KAPPA B P50 SUBUNIT; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEINS; PROTO-ONCOGENE PROTEINS C-REL; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84870928198     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2012.08.023     Document Type: Article

References (43)

1. Apostolou I., Sarukhan A., Klein L., von Boehmer H. Origin of regulatory T cells with known specificity for antigen. Nat. Immunol. 2002, 3:756-763.
2. Baldwin A.S. The NF-kappa B and I kappa B proteins: new discoveries and insights. Annu. Rev. Immunol. 1996, 14:649-683.
3. Barnes M.J., Krebs P., Harris N., Eidenschenk C., Gonzalez-Quintial R., Arnold C.N., Crozat K., Sovath S., Moresco E.M., Theofilopoulos A.N., et al. Commitment to the regulatory T cell lineage requires CARMA1 in the thymus but not in the periphery. PLoS Biol. 2009, 7:e51.
4. Bennett C.L., Christie J., Ramsdell F., Brunkow M.E., Ferguson P.J., Whitesell L., Kelly T.E., Saulsbury F.T., Chance P.F., Ochs H.D. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 2001, 27:20-21.
5. Bonizzi G., Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004, 25:280-288.
6. Brunkow M.E., Jeffery E.W., Hjerrild K.A., Paeper B., Clark L.B., Yasayko S.A., Wilkinson J.E., Galas D., Ziegler S.F., Ramsdell F. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 2001, 27:68-73.
7. Burchill M.A., Yang J., Vogtenhuber C., Blazar B.R., Farrar M.A. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. J. Immunol. 2007, 178:280-290.
8. Burchill M.A., Yang J., Vang K.B., Moon J.J., Chu H.H., Lio C.W., Vegoe A.L., Hsieh C.S., Jenkins M.K., Farrar M.A. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 2008, 28:112-121.
9. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., McGrady G., Wahl S.M. 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. 2003, 198:1875-1886.
10. Dechend R., Hirano F., Lehmann K., Heissmeyer V., Ansieau S., Wulczyn F.G., Scheidereit C., Leutz A. The Bcl-3 oncoprotein acts as a bridging factor between NF-kappaB/Rel and nuclear co-regulators. Oncogene 1999, 18:3316-3323.
11. Fiorini E., Schmitz I., Marissen W.E., Osborn S.L., Touma M., Sasada T., Reche P.A., Tibaldi E.V., Hussey R.E., Kruisbeek A.M., et al. Peptide-induced negative selection of thymocytes activates transcription of an NF-kappa B inhibitor. Mol. Cell 2002, 9:637-648.
12. Floess S., Freyer J., Siewert C., Baron U., Olek S., Polansky J., Schlawe K., Chang H.D., Bopp T., Schmitt E., et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 2007, 5:e38.
13. Ghosh S., Hayden M.S. New regulators of NF-kappaB in inflammation. Nat. Rev. Immunol. 2008, 8:837-848.
14. Grigoriadis G., Vasanthakumar A., Banerjee A., Grumont R., Overall S., Gleeson P., Shannon F., Gerondakis S. c-Rel controls multiple discrete steps in the thymic development of Foxp3+ CD4 regulatory T cells. PLoS ONE 2011, 6:e26851.
15. Hayden M.S., Ghosh S. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev. 2012, 26:203-234.
16. Hori S. c-Rel: a pioneer in directing regulatory T-cell lineage commitment?. Eur. J. Immunol. 2010, 40:664-667.
17. Hori S., Nomura T., Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003, 299:1057-1061.
18. Hsieh C.S. Kickstarting Foxp3 with c-Rel. Immunity 2009, 31:852-853.
19. Hsieh C.S., Liang Y., Tyznik A.J., Self S.G., Liggitt D., Rudensky A.Y. Recognition of the peripheral self by naturally arising CD25+ CD4+ T cell receptors. Immunity 2004, 21:267-277.
20. Isomura I., Palmer S., Grumont R.J., Bunting K., Hoyne G., Wilkinson N., Banerjee A., Proietto A., Gugasyan R., Wu L., et al. c-Rel is required for the development of thymic Foxp3+ CD4 regulatory T cells. J. Exp. Med. 2009, 206:3001-3014.
21. Jordan M.S., Boesteanu A., Reed A.J., Petrone A.L., Holenbeck A.E., Lerman M.A., Naji A., Caton A.J. Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat. Immunol. 2001, 2:301-306.
22. Kuwata H., Matsumoto M., Atarashi K., Morishita H., Hirotani T., Koga R., Takeda K. IkappaBNS inhibits induction of a subset of Toll-like receptor-dependent genes and limits inflammation. Immunity 2006, 24:41-51.
23. Lahl K., Loddenkemper C., Drouin C., Freyer J., Arnason J., Eberl G., Hamann A., Wagner H., Huehn J., Sparwasser T. Selective depletion of Foxp3+ regulatory T cells induces a scurfy-like disease. J. Exp. Med. 2007, 204:57-63.
24. Lio C.W., Hsieh C.S. A two-step process for thymic regulatory T cell development. Immunity 2008, 28:100-111.
25. Liston A., Rudensky A.Y. Thymic development and peripheral homeostasis of regulatory T cells. Curr. Opin. Immunol. 2007, 19:176-185.
26. Long M., Park S.G., Strickland I., Hayden M.S., Ghosh S. Nuclear factor-kappaB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity 2009, 31:921-931.
27. Lu L.F., Rudensky A. Molecular orchestration of differentiation and function of regulatory T cells. Genes Dev. 2009, 23:1270-1282.
28. Mankan A.K., Lawless M.W., Gray S.G., Kelleher D., McManus R. NF-kappaB regulation: the nuclear response. J. Cell. Mol. Med. 2009, 13:631-643.
29. Marie J.C., Letterio J.J., Gavin M., Rudensky A.Y. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 2005, 201:1061-1067.
30. Marson A., Kretschmer K., Frampton G.M., Jacobsen E.S., Polansky J.K., MacIsaac K.D., Levine S.S., Fraenkel E., von Boehmer H., Young R.A. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007, 445:931-935.
31. Molinero L.L., Yang J., Gajewski T., Abraham C., Farrar M.A., Alegre M.L. CARMA1 controls an early checkpoint in the thymic development of FoxP3+ regulatory T cells. J. Immunol. 2009, 182:6736-6743.
32. Okamoto K., Iwai Y., Oh-Hora M., Yamamoto M., Morio T., Aoki K., Ohya K., Jetten A.M., Akira S., Muta T., Takayanagi H. IkappaBzeta regulates T(H)17 development by cooperating with ROR nuclear receptors. Nature 2010, 464:1381-1385.
33. Perkins N.D., Gilmore T.D. Good cop, bad cop: the different faces of NF-kappaB. Cell Death Differ. 2006, 13:759-772.
34. Polansky J.K., Kretschmer K., Freyer J., Floess S., Garbe A., Baron U., Olek S., Hamann A., von Boehmer H., Huehn J. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 2008, 38:1654-1663.
35. Polansky J.K., Schreiber L., Thelemann C., Ludwig L., Krüger M., Baumgrass R., Cording S., Floess S., Hamann A., Huehn J. Methylation matters: binding of Ets-1 to the demethylated Foxp3 gene contributes to the stabilization of Foxp3 expression in regulatory T cells. J. Mol. Med. 2010, 88:1029-1040.
36. Ruan Q., Kameswaran V., Tone Y., Li L., Liou H.C., Greene M.I., Tone M., Chen Y.H. Development of Foxp3(+) regulatory t cells is driven by the c-Rel enhanceosome. Immunity 2009, 31:932-940.
37. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 1995, 155:1151-1164.
38. Sakaguchi S., Wing K., Miyara M. Regulatory T cells - a brief history and perspective. Eur. J. Immunol. 2007, 37(Suppl 1):S116-S123.
39. Thome M. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat. Rev. Immunol. 2004, 4:348-359.
40. Touma M., Antonini V., Kumar M., Osborn S.L., Bobenchik A.M., Keskin D.B., Connolly J.E., Grusby M.J., Reinherz E.L., Clayton L.K. Functional role for I kappa BNS in T cell cytokine regulation as revealed by targeted gene disruption. J. Immunol. 2007, 179:1681-1692.
41. Vang K.B., Yang J., Mahmud S.A., Burchill M.A., Vegoe A.L., Farrar M.A. IL-2, -7, and -15, but not thymic stromal lymphopoeitin, redundantly govern CD4+Foxp3+ regulatory T cell development. J. Immunol. 2008, 181:3285-3290.
42. Weil R., Israël A. Deciphering the pathway from the TCR to NF-kappaB. Cell Death Differ. 2006, 13:826-833.
43. Zheng Y., Josefowicz S., Chaudhry A., Peng X.P., Forbush K., Rudensky A.Y. Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 2010, 463:808-812.