Regulation of DNA methylation dictates Cd4 expression during the development of helper and cytotoxic T cell lineages

Nature Immunology

Volumn 16, Issue 7, 2015, Pages 746-754

  Sellars, Maclean ^a   Huh, Jun R ^a,b   Day, Kenneth ^c   Issuree, Priya D ^a   Galan, Carolina ^a   Gobeil, Stephane ^b,d   Absher, Devin ^c   Green, Michael R ^b   Littman, Dan R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c HUDSONALPHA INSTITUTE FOR BIOTECHNOLOGY   (United States)

^d LAVAL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CHROMATIN; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; TH-POK PROTEIN, MOUSE; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL DIVISION; CELL LINEAGE; CHROMATIN STRUCTURE; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DEMETHYLATION; DNA METHYLATION; ENHANCER REGION; GENE SILENCING; HELPER CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; STABLE EXPRESSION; ANIMAL; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CULTURE; CELL DIFFERENTIATION; CHROMATIN; FLOW CYTOMETRY; GENE EXPRESSION; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; RNA INTERFERENCE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD4; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHROMATIN; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; FLOW CYTOMETRY; GENE EXPRESSION; HEK293 CELLS; HUMANS; MICE, KNOCKOUT; MICE, TRANSGENIC; RNA INTERFERENCE; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, HELPER-INDUCER; TRANSCRIPTION FACTORS;

EID: 84931327865     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.3198     Document Type: Article

References (42)

1. Gialitakis, M., Sellars, M. & Littman, D.R. The epigenetic landscape of lineage choice: lessons from the heritability of CD4 and CD8 expression. Curr. Top. Microbiol. Immunol. 356, 165-188 (2012).
2. Taniuchi, I., Ellmeier, W. & Littman, D.R. The CD4/CD8 lineage choice: new insights into epigenetic regulation during T cell development. Adv. Immunol. 83, 55-89 (2004).
3. Taniuchi, I. et al. Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111, 621-633 (2002).
4. Taniuchi, I., Sunshine, M.J., Festenstein, R. & Littman, D.R. Evidence for distinct CD4 silencer functions at different stages of thymocyte differentiation. Mol. Cell 10, 1083-1096 (2002).
5. Zou, Y.R. et al. Epigenetic silencing of CD4 in T cells committed to the cytotoxic lineage. Nat. Genet. 29, 332-336 (2001).
6. Sawada, S., Scarborough, J.D., Killeen, N. & Littman, D.R. A lineage-specific transcriptional silencer regulates CD4 gene expression during T lymphocyte development. Cell 77, 917-929 (1994).
7. Chong, M.M. et al. Epigenetic propagation of CD4 expression is established by the Cd4 proximal enhancer in helper T cells. Genes Dev. 24, 659-669 (2010).
8. Lee, P.P. et al. A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15, 763-774 (2001).
9. Tucker, K.L. et al. Germ-line passage is required for establishment of methylation and expression patterns of imprinted but not of nonimprinted genes. Genes Dev. 10, 1008-1020 (1996).
10. Feng, J. et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat. Neurosci. 13, 423-430 (2010).
11. Jeong, M. et al. Large conserved domains of low DNA methylation maintained by Dnmt3a. Nat. Genet. 46, 17-23 (2014).
12. Day, K., Song, J. & Absher, D. Targeted sequencing of large genomic regions with CATCH-Seq. PLoS ONE 9, e111756 (2014).
13. Henson, D.M., Chou, C., Sakurai, N. & Egawa, T. A silencer-proximal intronic region is required for sustained CD4 expression in postselection thymocytes. J. Immunol. 192, 4620-4627 (2014).
14. Collings, C.K., Waddell, P.J. & Anderson, J.N. Effects of DNA methylation on nucleosome stability. Nucleic Acids Res. 41, 2918-2931 (2013).
15. Jimenez-Useche, I. et al. DNA methylation regulated nucleosome dynamics. Sci. Rep. 3, 2121 (2013).
16. Egawa, T. & Littman, D.R. ThPOK acts late in specification of the helper T cell lineage and suppresses Runx-mediated commitment to the cytotoxic T cell lineage. Nat. Immunol. 9, 1131-1139 (2008).
17. Sun, G. et al. The zinc finger protein cKrox directs CD4 lineage differentiation during intrathymic T cell positive selection. Nat. Immunol. 6, 373-381 (2005).
18. He, X. et al. The zinc finger transcription factor Th-POK regulates CD4 versus CD8 T-cell lineage commitment. Nature 433, 826-833 (2005).
19. Egerton, M., Scollay, R. & Shortman, K. Kinetics of mature T-cell development in the thymus. Proc. Natl. Acad. Sci. USA 87, 2579-2582 (1990).
20. Pénit, C. & Vasseur, F. Expansion of mature thymocyte subsets before emigration to the periphery. J. Immunol. 159, 4848-4856 (1997).
21. Ernst, B., Surh, C.D. & Sprent, J. Thymic selection and cell division. J. Exp. Med. 182, 961-971 (1995).
22. Schübeler, D. Function and information content of DNA methylation. Nature 517, 321-326 (2015).
23. Booth, M.J. et al. Quantitative sequencing of 5-methylcytosine and 5-hydroxymethylcytosine at single-base resolution. Science 336, 934-937 (2012).
24. Sato, T. et al. Dual functions of Runx proteins for reactivating CD8 and silencing CD4 at the commitment process into CD8 thymocytes. Immunity 22, 317-328 (2005).
25. He, Y.F. et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333, 1303-1307 (2011).
26. Ito, S. et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333, 1300-1303 (2011).
27. Pfaffeneder, T. et al. The discovery of 5-formylcytosine in embryonic stem cell DNA. Angew. Chem. 50, 7008-7012 (2011).
28. Egawa, T., Tillman, R.E., Naoe, Y., Taniuchi, I. & Littman, D.R. The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med. 204, 1945-1957 (2007).
29. Liu, S. et al. Interplay of RUNX1/MTG8 and DNA methyltransferase 1 in acute myeloid leukemia. Cancer Res. 65, 1277-1284 (2005).
30. Cheng, C.K. et al. Secreted-frizzled related protein 1 is a transcriptional repression target of the t(8;21) fusion protein in acute myeloid leukemia. Blood 118, 6638-6648 (2011).
31. Li, E., Bestor, T.H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
32. Nguyen, S., Meletis, K., Fu, D., Jhaveri, S. & Jaenisch, R. Ablation of de novo DNA methyltransferase Dnmt3a in the nervous system leads to neuromuscular defects and shortened lifespan. Dev. Dyn. 236, 1663-1676 (2007).
33. Okano, M., Bell, D.W., Haber, D.A. & Li, E. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257 (1999).
34. Ruzankina, Y. et al. Deletion of the developmentally essential gene ATR in adult mice leads to age-related phenotypes and stem cell loss. Cell Stem Cell 1, 113-126 (2007).
35. Grusby, M.J., Johnson, R.S., Papaioannou, V.E. & Glimcher, L.H. Depletion of CD4+ T cells in major histocompatibility complex class II-deficient mice. Science 253, 1417-1420 (1991).
36. Zijlstra, M. et al. Beta 2-microglobulin deficient mice lack CD4-8+ cytolytic T cells. Nature 344, 742-746 (1990).
37. Silva, J.M. et al. Second-generation shRNA libraries covering the mouse and human genomes. Nat. Genet. 37, 1281-1288 (2005).
38. Gobeil, S., Zhu, X., Doillon, C.J. & Green, M.R. A genome-wide shRNA screen identifies GAS1 as a novel melanoma metastasis suppressor gene. Genes Dev. 22, 2932-2940 (2008).
39. Morita, S., Kojima, T. & Kitamura, T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 7, 1063-1066 (2000).
40. Kumaki, Y., Oda, M. & Okano, M. QUMA: quantification tool for methylation analysis. Nucleic Acids Res. 36, W170-W175 (2008).
41. Booth, M.J. et al. Oxidative bisulfite sequencing of 5-methylcytosine and 5-hydroxymethylcytosine. Nat. Protoc. 8, 1841-1851 (2013).
42. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).