Epigenetic control of FOXP3 expression: The key to a stable regulatory T-cell lineage?

Nature Reviews Immunology

Volumn 9, Issue 2, 2009, Pages 83-89

  Huehn, Jochen ^a   Polansky, Julia K ^a   Hamann, Alf ^b  

^a HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^b CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYTOKINE; HERMES ANTIGEN; HISTONE H4; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; INTERLEUKIN 21; INTERLEUKIN 23; INTERLEUKIN 6; JANUS KINASE 1; JANUS KINASE 3; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; RETINOIC ACID; RETINOL; SMAD PROTEIN; STAT5 PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR NFAT; TRANSFORMING GROWTH FACTOR BETA;

CELL FUNCTION; CELL LINEAGE; CELL MATURATION; CELL SPECIFICITY; DEMETHYLATION; DNA MODIFICATION; EPIGENETICS; GENE EXPRESSION REGULATION; GENE LOCUS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOSENSOR; IMMUNOSTIMULATION; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

ANIMALS; CELL LINEAGE; EPIGENESIS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LYMPHOPOIESIS; MICE; PROMOTER REGIONS, GENETIC; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND;

EID: 58849118836     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2474     Document Type: Review

References (72)

1. + regulatory T cells. Nature Immunol. 4, 330-336 (2003).
2. + T regulatory cells. Nature Immunol. 4, 337-342 (2003).
3. Hori, S., Nomura, T. & Sakaguchi, S. Control of regulatory T cell development by the transcription factor Foxp3. Science. 299, 1057-1061 (2003).
4. Fontenot, J. D., Dooley, J. L., Farr, A. G. & Rudensky, A. Y. Developmental regulation of Foxp3 expression during ontogeny. J. Exp. Med. 202, 901-906 (2005).
5. + T cells in the thymic cortex. Proc. Natl Acad. Sci. USA 105, 11903-11908 (2008).
6. + medullary thymic epithelial cells. Nature Immunol. 8, 351-358 (2007).
7. + regulatory T cells originate from both naive T cells and naturally occurring naive-like regulatory T cells. J. Immunol. 180, 146-155 (2008).
8. Kretschmer, K. et al. Inducing and expanding regulatory T cell populations by foreign antigen. Nature Immunol. 12, 1219-1227 (2005).
9. Sun, C. M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
10. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007).
11. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
12. Floess, S. et al. Epigenetic control of the foxp3 locus in regulatory T cells. PLOS Biol. 5, e38 (2007).
13. - T cells. J. Clin. Invest. 112, 1437-1443 (2003).
14. Mantel, P. Y. et al. Molecular mechanisms underlying FOXP3 induction in human T cells. J. Immunol. 176, 3593-3602 (2006).
15. Gavin, M. A. et al. Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development. Proc. Natl Acad. Sci. USA 103, 6659-6664 (2006).
16. - T cells by T cell receptor stimulation is TGF-β-dependent but does not confer a regulatory phenotype. Blood 110, 2983-2990 (2007).
17. Allan, S. E. et al. Activation-induced FOXP3 in human T effector cells does not suppress proliferation or cytokine production. Int. Immunol. 19, 345-354 (2007).
18. Pillai, V., Ortega, S. B., Wang, C. K. & Karandikar, N. J. Transient regulatory T-cells: a state attained by all activated human T-cells. Clin. Immunol. 123, 18-29 (2007).
19. Kim, H. P. & Leonard, W. J. CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression: a role for DNA methylation. J. Exp. Med. 204, 1543-1551 (2007).
20. Gupta, S. et al. Differential requirement of PKC-θ in the development and function of natural regulatory T cells. Mol. Immunol. 46, 213-214 (2008).
21. + regulatory T cells in mice. Transplantation 82, 1484-1492 (2006).
22. + T cells. Bone Marrow Transplant. 39, 537-545 (2007).
23. San Segundo, D., Fabrega, E., Lopez-Hoyos, M. & Pons, F. Reduced numbers of blood natural regulatory T cells in stable liver transplant recipients with high levels of calcineurin inhibitors. Transplant. Proc. 39, 2290-2292 (2007).
24. Brandt, C., Pavlovic, V., Worm, M., Radbruch, A. & Baumgrass, R. Low-dose cyclosporine A therapy increases the regulatory T cell population in patients with atopic dermatitis. Allergy (in the press).
25. Kim, J. M. & Rudensky, A. The role of the transcription factor Foxp3 in the development of regulatory T cells. Immunol. Rev. 212, 86-98 (2006).
26. Sauer, S. et al. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl Acad. Sci. USA 105, 7797-7802 (2008).
27. + cells. J. Exp. Med. 205, 565-574 (2008).
28. Tai, X., Cowan, M., Feigenbaum, L. & Singer, A. CD28 costimulation of developing thymocytes induces Foxp3 expression and regulatory T cell differentiation independently of interleukin 2. Nature Immunol. 6, 152-162 (2005).
29. Benson, M. J., Pino-Lagos, K., Rosemblatt, M. & Noelle, R. J. All-trans retinoic acid mediates enhanced T reg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204, 1765-1774 (2007).
30. Fontenot, J. D., Rasmussen, J. P., Gavin, M. A. & Rudensky, A. Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nature Immunol. 6, 1142-1151 (2005).
31. + T cell differentiation is induced following activation in the absence of γ-chain-dependent cytokine signals. J. Immunol. 176, 2059-2063 (2006).
32. Yao, Z. et al. Nonredundant roles for Stat5a/b in directly regulating Foxp3. Blood 109, 4368-4375 (2007).
33. + regulatory T cells through a STAT dependent mechanism and induces the expansion of these cells in vivo. Blood 108, 1571-1579 (2006).
34. + regulatory T cells. J. Immunol. 178, 280-290 (2007).
35. + regulatory T cells in the absence of interleukin 2 signaling. Nature Immunol. 6, 1152-1159 (2005).
36. + regulatory T cells. J. Exp. Med. 201, 1061-1067 (2005).
37. + regulatory T cells. Nature Immunol. 9, 632-640 (2008).
38. Venuprasad, K. et al. The E3 ubiquitin ligase Itch regulates expression of transcription factor Foxp3 and airway inflammation by enhancing the function of transcription factor TIEG1. Nature Immunol. 9, 245-253 (2008).
39. Tone, Y. et al. Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nature Immunol. 9, 194-202 (2008).
40. + regulatory T cells and inhibits development of Th17 cells by enhancing TGF-β-driven Smad3 signaling and inhibiting IL-6 and IL-23 receptor expression. J. Immunol. 181, 2277-2284 (2008).
41. hi cells. Immunity 29, 758-770 (2008).
42. Samon, J. B. et al. Notch1 and TGFβ1 cooperatively regulate Foxp3 expression and the maintenance of peripheral regulatory T cells. Blood 112, 1813-1821 (2008).
43. Ou-Yang, H. F. et al. Notch signaling regulates the FOXP3 promoter through RBP-J- and Hes1-dependent mechanisms. Mol. Cell. Biochem. 8 Sep 2008 (doi: 10.1007/s11010-008-9912-9914).
44. + regulatory T cells. Proc. Natl Acad. Sci. USA 104, 18169-18174 (2007).
45. Mantel, P. Y. et al. GATA3-driven Th2 responses inhibit TGF-β1-induced FOXP3 expression and the formation of regulatory T cells. PLoS Biol. 5, e329 (2007).
46. + Foxp3- effector T cells. Nature Immunol. 9, 1347-1355 (2008).
47. Takaki, H. et al. STAT6 inhibits TGF-β-mediated Foxp3 induction through direct binding to the Foxp3 promoter, which is reverted by retinoic acid receptor. J. Biol. Chem. 283, 14955-14962 (2008).
48. + regulatory T cell differentiation by repressing Foxp3 expression. J. Immunol. 181, 1673-1682 (2008).
49. Fazi, F. & Nervi, C. MicroRNA: basic mechanisms and transcriptional regulatory networks for cell fate determination. Cardiovasc. Res. 79, 553-561 (2008).
50. Hoefig, K. P. & Heissmeyer, V. MicroRNAs grow up in the immune system. Curr. Opin. Immunol. 20, 281-287 (2008).
51. Cobb, B. S. et al. A role for Dicer in immune regulation. J. Exp. Med. 203, 2519-2527 (2006).
52. Zhou, X. et al. Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205, 1983-1991 (2008).
53. Chong, M. M., Rasmussen, J. P., Rundensky, 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).
54. 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).
55. Marson, A. et al. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 445, 931-935 (2007).
56. Wilson, B., Rowell, E. & Sekimata, M. Epigenetic control of T-helper-cell differentiation. Nature Rev. Immunol. 9, 91-105 (2009).
57. Janson, P. C. et al. FOXP3 promoter demethylation reveals the committed Treg population in humans. PLoS ONE 3, e1612 (2008).
58. + conventional T cells. Eur. J. Immunol. 37, 2378-2389 (2007).
59. + T cells. Int. Immunol. 20, 1041-1055 (2008).
60. Polansky, J. et al. DNA methylation controls Foxp3 gene expression. Eur. J. Immunol. 38, 1654-1663 (2008).
61. Ansel, K. M., Lee, D. U. & Rao, A. An epigenetic view of helper T cell differentiation. Nature Immunol. 4, 616-623 (2003).
62. Wieczorek, G. et al. Quantitative DNA methylation analysis of FOXP3 as a new method for counting regulatory T cells in solid tissue and peripheral blood. Cancer Res. 69, 599-608 (2009).
63. Metivier, R. et al. Cyclical DNA methylation of a transcriptionally active promoter. Nature 452, 45-50 (2008).
64. - T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-β. J. Immunol. 178, 6725-6729 (2007).
65. pos regulatory T cells differentiate into IL-17-producing cells. Blood 112, 2340-2352 (2008).
66. + antigen-specific autoimmune effectors in vitro and in vivo. J. Immunol. 181, 3137-3147 (2008).
67. Tao, R. et al. Deacetylase inhibition promotes the generation and function of regulatory T cells. Nature Med. 13, 1299-1307 (2007).
68. Reilly, C. M. et al. The histone deacetylase inhibitor trichostatin A upregulates regulatory T cells and modulates autoimmunity in NZB/W F1 mice. J. Autoimmun. 31, 123-130 (2008).
69. Chen, C., Rowell, E. A., Thomas, R. M., Hancock, W. W. & Wells, A. D. Transcriptional regulation by Foxp3 is associated with direct promoter occupancy and modulation of histone acetylation. J. Biol. Chem. 281, 36828-36834 (2006).
70. Li, B. et al. FOXP3 ensembles in T-cell regulation. Immunol. Rev. 212, 99-113 (2006).
71. Kwon, H. K. et al. Foxp3 induces IL-4 gene silencing by affecting nuclear translocation of NFκB and chromatin structure. Mol. Immunol. 45, 3205-3212 (2008).
72. Samanta, A. et al. TGF-β and IL-6 signals modulate chromatin binding and promoter occupancy by acetylated FOXP3. Proc. Natl Acad. Sci. USA 105, 14023-14027 (2008).