Nuclear Factor-κB Modulates Regulatory T Cell Development by Directly Regulating Expression of Foxp3 Transcription Factor

Immunity

Volumn 31, Issue 6, 2009, Pages 921-931

  Long, Meixiao ^a,b   Park, Sung Gyoo ^a,b   Strickland, Ian ^a   Hayden, Matthew S ^a   Ghosh, Sankar ^a,b  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b College of Physicians and Surgeons ^*  (United States)

Author keywords

CELLIMMUNO; MOLIMMUNO

Indexed keywords

I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR REL; CARD11 PROTEIN, MOUSE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; I KAPPA B; MAP KINASE KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; RAG 1 PROTEIN; RAG-1 PROTEIN;

ANIMAL CELL; ARTICLE; CELL COUNT; CELL MATURATION; CONTROLLED STUDY; DEMETHYLATION; EMBRYO; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC TRANSCRIPTION; GENOME IMPRINTING; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PLEIOTROPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FAMILY; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; THYMUS; TRANSGENE; ADOPTIVE TRANSFER; ANIMAL; C57BL MOUSE; GENETICS; IMMUNOLOGY; METABOLISM; MOLECULAR GENETICS; MOUSE MUTANT; NUCLEOTIDE SEQUENCE; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; BASE SEQUENCE; CARD SIGNALING ADAPTOR PROTEINS; FORKHEAD TRANSCRIPTION FACTORS; GENOMIC IMPRINTING; HOMEODOMAIN PROTEINS; I-KAPPA B PROTEINS; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MOLECULAR SEQUENCE DATA; NF-KAPPA B; PROTO-ONCOGENE PROTEINS C-REL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 71749088574     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.09.022     Document Type: Article

References (46)

1. Bellavia D., Campese A.F., Alesse E., Vacca A., Felli M.P., Balestri A., Stoppacciaro A., Tiveron C., Tatangelo L., Giovarelli M., et al. Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J. 19 (2000) 3337-3348
2. Bruniquel D., and Schwartz R.H. Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat. Immunol. 4 (2003) 235-240
3. Burchill M.A., Yang J., Vang K.B., Moon J.J., Chu H.H., Lio C.-W.J., Vegoe A.L., Hsieh C.-S., Jenkins M.K., and Farrar M.A. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 28 (2008) 112-121
4. Clark S.J., Statham A., Stirzaker C., Molloy P.L., and Frommer M. DNA methylation: bisulphite modification and analysis. Nat. Protoc. 1 (2006) 2353-2364
5. Egawa T., Albrecht B., Favier B., Sunshine M.-J., Mirchandani K., O'Brien W., Thome M., and Littman D.R. Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation. Curr. Biol. 13 (2003) 1252-1258
6. Fischer A.M., Katayama C.D., Pagès G., Pouysségur J., and Hedrick S.M. The role of erk1 and erk2 in multiple stages of T cell development. Immunity 23 (2005) 431-443
7. 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. 5 (2007) e38
8. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4 (2003) 330-336
9. Fontenot J.D., Rasmussen J.P., Gavin M.A., and Rudensky A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6 (2005) 1142-1151
10. Gong Q., Cheng A.M., Akk A.M., Alberola-Ila J., Gong G., Pawson T., and Chan A.C. Disruption of T cell signaling networks and development by Grb2 haploid insufficiency. Nat. Immunol. 2 (2001) 29-36
11. Gupta S., Manicassamy S., Vasu C., Kumar A., Shang W., and Sun Z. Differential requirement of PKC-theta in the development and function of natural regulatory T cells. Mol. Immunol. 46 (2008) 213-224
12. Hori S., Nomura T., and Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 299 (2003) 1057-1061
13. Huehn J., Polansky J.K., and Hamann A. Epigenetic control of FOXP3 expression: The key to a stable regulatory T-cell lineage?. Nat. Rev. Immunol. 9 (2009) 83-89
14. Jimi E., Strickland I., Voll R.E., Long M., and Ghosh S. Differential role of the transcription factor NF-kappaB in selection and survival of CD4+ and CD8+ thymocytes. Immunity 29 (2008) 523-537
15. Kim H.P., and Leonard W.J. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: A role for DNA methylation. J. Exp. Med. 204 (2007) 1543-1551
16. Koonpaew S., Shen S., Flowers L., and Zhang W. LAT-mediated signaling in CD4+CD25+ regulatory T cell development. J. Exp. Med. 203 (2006) 119-129
17. Lai J.H., Horvath G., Subleski J., Bruder J., Ghosh P., and Tan T.H. RelA is a potent transcriptional activator of the CD28 response element within the interleukin 2 promoter. Mol. Cell. Biol. 15 (1995) 4260-4271
18. Liston A., and Rudensky A.Y. Thymic development and peripheral homeostasis of regulatory T cells. Curr. Opin. Immunol. 19 (2007) 176-185
19. Long M., and Adler A.J. Cutting edge: Paracrine, but not autocrine, IL-2 signaling is sustained during early antiviral CD4 T cell response. J. Immunol. 177 (2006) 4257-4261
20. Long M., Slaiby A.M., Hagymasi A.T., Mihalyo M.A., Lichtler A.C., Reiner S.L., and Adler A.J. T-bet down-modulation in tolerized Th1 effector CD4 cells confers a TCR-distal signaling defect that selectively impairs IFN-gamma expression. J. Immunol. 176 (2006) 1036-1045
21. McKarns S.C., and Schwartz R.H. Biphasic regulation of Il2 transcription in CD4+ T cells: roles for TNF-alpha receptor signaling and chromatin structure. J. Immunol. 181 (2008) 1272-1281
22. Medoff B.D., Sandall B.P., Landry A., Nagahama K., Mizoguchi A., Luster A.D., and Xavier R.J. Differential requirement for CARMA1 in agonist-selected T-cell development. Eur. J. Immunol. 39 (2009) 78-84
23. Moore N.C., Girdlestone J., Anderson G., Owen J.J., and Jenkinson E.J. Stimulation of thymocytes before and after positive selection results in the induction of different NF-kappa B/Rel protein complexes. J. Immunol. 155 (1995) 4653-4660
24. Neilson J.R., Winslow M.M., Hur E.M., and Crabtree G.R. Calcineurin B1 is essential for positive but not negative selection during thymocyte development. Immunity 20 (2004) 255-266
25. Rao S., Gerondakis S., Woltring D., and Shannon M.F. c-Rel is required for chromatin remodeling across the IL-2 gene promoter. J. Immunol. 170 (2003) 3724-3731
26. Rawlings D.J., Sommer K., and Moreno-García M.E. The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes. Nat. Rev. Immunol. 6 (2006) 799-812
27. Sakaguchi S. Naturally arising CD4+ regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu. Rev. Immunol. 22 (2004) 531-562
28. Sakaguchi S., Sakaguchi N., Asano M., Itoh M., and 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. 155 (1995) 1151-1164
29. Sakaguchi S., Wing K., and Miyara M. Regulatory T cells-A brief history and perspective. Eur. J. Immunol. 37 (2007) S116-S123
30. Schmidt-Supprian M., Courtois G., Tian J., Coyle A.J., Israël A., Rajewsky K., and Pasparakis M. Mature T cells depend on signaling through the IKK complex. Immunity 19 (2003) 377-389
31. Schmidt-Supprian M., Tian J., Grant E.P., Pasparakis M., Maehr R., Ovaa H., Ploegh H.L., Coyle A.J., and Rajewsky K. Differential dependence of CD4+CD25+ regulatory and natural killer-like T cells on signals leading to NF-kappaB activation. Proc. Natl. Acad. Sci. USA 101 (2004) 4566-4571
32. Schulze-Luehrmann J., and Ghosh S. Antigen-receptor signaling to nuclear factor kappa B. Immunity 25 (2006) 701-715
33. Takahashi T., Kuniyasu Y., Toda M., Sakaguchi N., Itoh M., Iwata M., Shimizu J., and Sakaguchi S. Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: induction of autoimmune disease by breaking their anergic/suppressive state. Int. Immunol. 10 (1998) 1969-1980
34. Thomas R.M., Gao L., and Wells A.D. Signals from CD28 induce stable epigenetic modification of the IL-2 promoter. J. Immunol. 174 (2005) 4639-4646
35. Thorstenson K.M., and Khoruts A. Generation of anergic and potentially immunoregulatory CD25+CD4 T cells in vivo after induction of peripheral tolerance with intravenous or oral antigen. J. Immunol. 167 (2001) 188-195
36. Tone Y., Furuuchi K., Kojima Y., Tykocinski M.L., Greene M.I., and Tone M. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9 (2007) 194-202
37. Vallabhapurapu S., Powolny-Budnicka I., Riemann M., Schmid R.M., Paxian S., Pfeffer K., Körner H., and Weih F. Rel/NF-kappaB family member RelA regulates NK1.1- to NK1.1+ transition as well as IL-15-induced expansion of NKT cells. Eur. J. Immunol. 38 (2008) 3508-3519
38. Voll R.E., Jimi E., Phillips R.J., Barber D.F., Rincon M., Hayday A.C., Flavell R.A., and Ghosh S. NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity 13 (2000) 677-689
39. Wan Y.Y., and Flavell R.A. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc. Natl. Acad. Sci. USA 102 (2005) 5126-5131
40. Wan Y.Y., Chi H., Xie M., Schneider M.D., and Flavell R.A. The kinase TAK1 integrates antigen and cytokine receptor signaling for T cell development, survival and function. Nat. Immunol. 7 (2006) 851-858
41. Watts T.H. TNF/TNFR family members in costimulation of T cell responses. Annu. Rev. Immunol. 23 (2005) 23-68
42. Welte T., Leitenberg D., Dittel B.N., al-Ramadi B.K., Xie B., Chin Y.E., Janeway Jr. C.A., Bothwell A.L., Bottomly K., and Fu X.Y. STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science 283 (1999) 222-225
43. Xie M., Zhang D., Dyck J.R.B., Li Y., Zhang H., Morishima M., Mann D.L., Taffet G.E., Baldini A., Khoury D.S., and Schneider M.D. A pivotal role for endogenous TGF-beta-activated kinase-1 in the LKB1/AMP-activated protein kinase energy-sensor pathway. Proc. Natl. Acad. Sci. USA 103 (2006) 17378-17383
44. Yagi H., Nomura T., Nakamura K., Yamazaki S., Kitawaki T., Hori S., Maeda M., Onodera M., Uchiyama T., Fujii S., and Sakaguchi S. Crucial role of FOXP3 in the development and function of human CD25+CD4+ regulatory T cells. Int. Immunol. 16 (2004) 1643-1656
45. Yu A., Zhu L., Altman N.H., and Malek T.R. A low interleukin-2 receptor signaling threshold supports the development and homeostasis of T regulatory cells. Immunity 30 (2009) 204-217
46. Zheng Y., and Rudensky A.Y. Foxp3 in control of the regulatory T cell lineage. Nat. Immunol. 8 (2007) 457-462