T Cell Receptor (TCR) and Transforming Growth Factor β (TGF-β) signaling converge on DNA (cytosine-5)-methyltransferase to control forkhead box protein 3 (foxp3) locus methylation and inducible regulatory T cell differentiation

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 19127-19139

  Li, Chaoran ^a   Ebert, Peter J R ^b   Li, Qi Jing ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DAUGHTER CELLS; LIGAND AFFINITY; METHYLTRANSFERASES; POST-TRANSCRIPTIONAL MECHANISMS; PROTEASOMAL DEGRADATION; REGULATORY T CELLS; T-CELL RECEPTORS; TRANSFORMING GROWTH FACTORS;

ALKYLATION; CELL MEMBRANES; CYTOLOGY; ELECTRIC REACTORS; METHYLATION; NUCLEIC ACIDS; PROTEINS;

CELL SIGNALING;

DNA (CYTOSINE 5) METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 3B; GLYCOGEN SYNTHASE KINASE 3BETA; MICRORNA; MICRORNA 148A; MITOGEN ACTIVATED PROTEIN KINASE P38; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; ENZYME ACTIVATION; FOXP3 GENE; GENE EXPRESSION; GENE LOCUS; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RECEPTOR AFFINITY; SIGNAL TRANSDUCTION; T LYMPHOCYTE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

DNA METHYLTRANSFERASE; EPIGENETICS; FOXP3; MICRORNA; MIR-148A; PROTEIN DEGRADATION; REGULATORY T CELL DIFFERENTIATION; TCR SIGNALING; TRANSFORMING GROWTH FACTOR Β (TGFΒ);

ANIMALS; CELL DIFFERENTIATION; CELL PROLIFERATION; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; EPIGENESIS, GENETIC; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; PROMOTER REGIONS, GENETIC; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84879590240     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.453357     Document Type: Article

References (59)

1. Zhu, J., Yamane, H., and Paul, W. E. (2010) Differentiation of effector CD4 T cell populations (&z.ast;) Annu. Rev. Immunol. 28, 445-489
2. + T cells to generate a Th2-inducing cytokine environment. J. Exp. Med. 202, 793-804
3. + T cells by antigenic peptides altered for TCR binding. J. Immunol. 158, 4237-4244
4. + T cells. J. Exp. Med. 182, 1591-1596
5. Purvis, H. A., Stoop, J. N., Mann, J., Woods, S., Kozijn, A. E., Hambleton, S., Robinson, J. H., Isaacs, J. D., Anderson, A. E., and Hilkens, C. M. (2010) Low-strength T-cell activation promotes Th17 responses. Blood 116, 4829-4837
6. Sakaguchi, S., Yamaguchi, T., Nomura, T., and Ono, M. (2008) Regulatory T cells and immune tolerance. Cell 133, 775-787 (Pubitemid 351707693)
7. + regulatory T cells. Nat. Immunol. 4, 330-336
8. Hori, S., Nomura, T., and Sakaguchi, S. (2003) Control of regulatory T cell development by the transcription factor Foxp3. Science 299, 1057-1061 (Pubitemid 36222930)
9. + T regulatory cells. Nat. Immunol. 4, 337-342
10. Williams, L. M., and Rudensky, A. Y. (2007) Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat. Immunol. 8, 277-284 (Pubitemid 46745377)
11. Bennett, C. L., Christie, J., Ramsdell, F., Brunkow, M. E., Ferguson, P. J., Whitesell, L., Kelly, T. E., Saulsbury, F. T., Chance, P. F., and Ochs, H. D. (2001) The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat. Genet. 27, 20-21 (Pubitemid 32044513)
12. 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., and Ramsdell, F. (2001) Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat. Genet. 27, 68-73 (Pubitemid 32044521)
13. + regulatory T cells. More of the same or a division of labor? Immunity 30, 626-635
14. Mantel, P. Y., Ouaked, N., Rückert, B., Karagiannidis, C., Welz, R., Blaser, K., and Schmidt-Weber, C. B. (2006) Molecular mechanisms underlying FOXP3 induction in human T cells. J. Immunol. 176, 3593-3602
15. Kim, H. P., and Leonard, W. J. (2007) CREB/ATF-dependent T cell receptor-induced FoxP3 gene expression. A role for DNA methylation. J. Exp. Med. 204, 1543-1551
16. Long, M., Park, S. G., Strickland, I., Hayden, M. S., and Ghosh, S. (2009) Nuclear factor-kappaB modulates regulatory T cell development by directly regulating expression of Foxp3 transcription factor. Immunity 31, 921-931
17. Tone, Y., Furuuchi, K., Kojima, Y., Tykocinski, M. L., Greene, M. I., and Tone, M. (2008) Smad3 and NFAT cooperate to induce Foxp3 expression through its enhancer. Nat. Immunol. 9, 194-202
18. Martinez, G. J., Zhang, Z., Chung, Y., Reynolds, J. M., Lin, X., Jetten, A. M., Feng, X. H., and Dong, C. (2009) Smad3 differentially regulates the induction of regulatory and inflammatory T cell differentiation. J. Biol. Chem. 284, 35283-35286
19. Huehn, J., Polansky, J. K., and Hamann, A. (2009) Epigenetic control of FOXP3 expression. The key to a stable regulatory T-cell lineage? Nature Rev. Immunol. 9, 83-89
20. Lal, G., and Bromberg, J. S. (2009) Epigenetic mechanisms of regulation of Foxp3 expression. Blood 114, 3727-3735
21. Janson, P. C., Winerdal, M. E., Marits, P., Thörn, M., Ohlsson, R., and Winqvist, O. (2008) FOXP3 promoter demethylation reveals the committed Treg population in humans. PloS ONE 3, e1612
22. Floess, S., Freyer, J., Siewert, C., Baron, U., Olek, S., Polansky, J., Schlawe, K., Chang, H. D., Bopp, T., Schmitt, E., Klein-Hessling, S., Serfling, E., Hamann, A., and Huehn, J. (2007) Epigenetic control of the foxp3 locus in regulatory T cells. PLoS Biol. 5, e38
23. Jiang, S., Li, C., Olive, V., Lykken, E., Feng, F., Sevilla, J., Wan, Y., He, L., and Li, Q. J. (2011) Molecular dissection of the miR-17-92 cluster's critical dual roles in promoting Th1 responses and preventing inducible Treg differentiation. Blood 118, 5487-5497
24. Sauer, S., Bruno, L., Hertweck, A., Finlay, D., Leleu, M., Spivakov, M., Knight, Z. A., Cobb, B. S., Cantrell, D., O'Connor, E., Shokat, K. M., Fisher, A. G., and Merkenschlager, M. (2008) T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. U.S.A. 105, 7797-7802 (Pubitemid 351872718)
25. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M. C., and von Boehmer, H. (2005) Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6, 1219-1227 (Pubitemid 43045633)
26. + T cells from T cell receptor transgenic mice. J. Exp. Med. 176, 1091-1098
27. Davis, M. M., Boniface, J. J., Reich, Z., Lyons, D., Hampl, J., Arden, B., and Chien, Y. (1998) Ligand recognition by αβ T cell receptors. Annu. Rev. Immunol. 16, 523-544
28. Reay, P. A., Kantor, R. M., and Davis, M. M. (1994) Use of global amino acid replacements to define the requirements forMHCbinding and T cell recognition of moth cytochrome c (93-103). J. Immunol. 152, 3946-3957 (Pubitemid 24111066)
29. Huppa, J. B., Gleimer, M., Sumen, C., and Davis, M. M. (2003) Continuous T cell receptor signaling required for synapse maintenance and full effector potential. Nat. Immunol. 4, 749-755 (Pubitemid 36986758)
30. + cells. J. Exp. Med. 205, 565-574
31. Smith-Garvin, J. E., Koretzky, G. A., and Jordan, M. S. (2009) T cell activation. Annu. Rev. Immunol. 27, 591-619
32. Josefowicz, S. Z., and Rudensky, A. (2009) Control of regulatory T cell lineage commitment and maintenance. Immunity 30, 616-625
33. Zheng, Y., Josefowicz, S., Chaudhry, A., Peng, X. P., Forbush, K., and Rudensky, A. Y. (2010) Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463, 808-812
34. Josefowicz, S. Z., Wilson, C. B., and Rudensky, A. Y. (2009) Cutting edge. TCR stimulation is sufficient for induction of Foxp3 expression in the absence of DNA methyltransferase 1. J. Immunol. 182, 6648-6652
35. Kim, G. D., Ni, J., Kelesoglu, N., Roberts, R. J., and Pradhan, S. (2002) Co-operation and communication between the human maintenance and de novo DNA (cytosine-5) methyltransferases. EMBO J. 21, 4183-4195 (Pubitemid 34857450)
36. Rhee, I., Bachman, K. E., Park, B. H., Jair, K. W., Yen, R. W., Schuebel, K. E., Cui, H., Feinberg, A. P., Lengauer, C., Kinzler, K. W., Baylin, S. B., and Vogelstein, B. (2002)DNMT1and DNMT3b cooperate to silence genes in human cancer cells. Nature 416, 552-556 (Pubitemid 34288859)
37. Zhou, X., Jeker, L. T., Fife, B. T., Zhu, S., Anderson, M. S., McManus, M. T., and Bluestone, J. A. (2008) Selective miRNA disruption in T reg cells leads to uncontrolled autoimmunity. J. Exp. Med. 205, 1983-1991
38. Schoenborn, J. R., Dorschner, M. O., Sekimata, M., Santer, D. M., Shnyreva, M., Fitzpatrick, D. R., Stamatoyannopoulos, J. A., Stamatoyonnapoulos, J. A., and Wilson, C. B. (2007) Comprehensive epigenetic profiling identifies multiple distal regulatory elements directing transcription of the gene encoding interferon-γ. Nat. Immunol. 8, 732-742 (Pubitemid 46965349)
39. Cohen, P., and Frame, S. (2001) The renaissance of GSK3. Nat. Rev. Mol. Cell Biol. 2, 769-776 (Pubitemid 33679839)
40. Cross, D. A., Alessi, D. R., Cohen, P., Andjelkovich, M., and Hemmings, B. A. (1995) Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789 (Pubitemid 26004411)
41. Goode, N., Hughes, K., Woodgett, J. R., and Parker, P. J. (1992) Differential regulation of glycogen synthase kinase-3β by protein kinase C isotypes. J. Biol. Chem. 267, 16878-16882
42. Sun, L., Zhao, H., Xu, Z., Liu, Q., Liang, Y., Wang, L., Cai, X., Zhang, L., Hu, L., Wang, G., and Zha, X. (2007) Phosphatidylinositol 3-kinase/protein kinase B pathway stabilizes DNA methyltransferase I protein and maintains DNA methylation. Cell. Signal. 19, 2255-2263 (Pubitemid 47361683)
43. Fabian, M. R., Sonenberg, N., and Filipowicz, W. (2010) Regulation of mRNA translation and stability by microRNAs. Annu. Rev. Biochem. 79, 351-379
44. + T cells by directly and indirectly targeting DNA methyltransferase 1. J. Immunol. 184, 6773-6781
45. Huang, J., Wang, Y., Guo, Y., and Sun, S. (2010) Down-regulated microRNA-152 induces aberrant DNA methylation in hepatitis B virus-related hepatocellular carcinoma by targeting DNA methyltransferase 1. Hepatology 52, 60-70
46. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K., and Flavell, R. A. (2006) Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24, 99-146
47. Luo, X., Zhang, Q., Liu, V., Xia, Z., Pothoven, K. L., and Lee, C. (2008) Cutting edge. TGF-β-induced expression of Foxp3 in T cells is mediated through inactivation of ERK. J. Immunol. 180, 2757-2761
48. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886
49. Li, E., Bestor, T. H., and Jaenisch, R. (1992) Targeted mutation of theDNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926
50. Jackson-Grusby, L., Beard, C., Possemato, R., Tudor, M., Fambrough, D., Csankovszki, G., Dausman, J., Lee, P., Wilson, C., Lander, E., and Jaenisch, R. (2001) Loss of genomic methylation causes p53-dependent apoptosis and epigenetic deregulation. Nat. Genet. 27, 31-39 (Pubitemid 32044515)
51. Szyf, M., Bozovic, V., and Tanigawa, G. (1991) Growth regulation of mouse DNA methyltransferase gene expression. J. Biol. Chem. 266, 10027-10030 (Pubitemid 21906759)
52. Pillai, V., Ortega, S. B., Wang, C. K., and Karandikar, N. J. (2007) Transient regulatory T-cells. A state attained by all activated human T-cells. Clin. Immunol. 123, 18-29 (Pubitemid 46401504)
53. Wang, J., Ioan-Facsinay, A., van der Voort, E. I., Huizinga, T. W., and Toes, R. E. (2007) Transient expression of FOXP3 in human activated nonregulatory CD4+T cells. Eur. J. Immunol. 37, 129-138 (Pubitemid 46128793)
54. + T cells. Immunity 30, 155-167
55. Mukasa, R., Balasubramani, A., Lee, Y. K., Whitley, S. K., Weaver, B. T., Shibata, Y., Crawford, G. E., Hatton, R. D., and Weaver, C. T. (2010) Epigenetic instability of cytokine and transcription factor gene loci underlies plasticity of the T helper 17 cell lineage. Immunity 32, 616-627
56. + T cells. Immunity 35, 400-412
57. Vijayanand, P., Seumois, G., Simpson, L. J., Abdul-Wajid, S., Baumjohann, D., Panduro, M., Huang, X., Interlandi, J., Djuretic, I. M., Brown, D. R., Sharpe, A. H., Rao, A., and Ansel, K. M. (2012) Interleukin-4 production by follicular helper T cells requires the conserved Il4 enhancer hypersensitivity site V. Immunity 36, 175-187
58. Ebert, P. J., Ehrlich, L. I., and Davis, M. M. (2008) Low ligand requirement for deletion and lack of synapses in positive selection enforce the gauntlet of thymic T cell maturation. Immunity 29, 734-745
59. Mempel, T. R., Henrickson, S. E., and Von Andrian, U. H. (2004) T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature 427, 154-159 (Pubitemid 38094955) Diseases, National Institutes of Health Diseases, National Institutes of Health