5-Hydroxymethylcytosine Remodeling Precedes Lineage Specification during Differentiation of Human CD4+ T Cells

Cell Reports

Volumn 16, Issue 2, 2016, Pages 559-570

  Nestor, Colm E ^a   Lentini, Antonio ^a   Hägg Nilsson, Cathrine ^a   Gawel, Danuta R ^a   Gustafsson, Mika ^a   Mattson, Lina ^a   Wang, Hui ^b   Rundquist, Olof ^a   Meehan, Richard R ^c   Klocke, Bernward ^d   Seifert, Martin ^d   Hauck, Stefanie M ^e   Laumen, Helmut ^e,f,g   Zhang, Huan ^a   Benson, Mikael ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d Genomatix GmbH   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE;

ARTICLE; CD4+ T LYMPHOCYTE; CELL DENSITY; CELL INTERACTION; CELL LINEAGE; CONTROLLED STUDY; DIABETES MELLITUS; DNA EXTRACTION; DNA METHYLATION; DNA REPLICATION; EX VIVO STUDY; GENE EXPRESSION PROFILING; GENE INTERACTION; GENE REGULATORY NETWORK; GENETIC VARIABILITY; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MEMORY T LYMPHOCYTE; MULTIPLE SCLEROSIS; NEXT GENERATION SEQUENCING; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; RNA EXTRACTION; TH1 CELL; TH2 CELL; TRANSCRIPTION INITIATION SITE; ANALOGS AND DERIVATIVES; CELL CULTURE; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

5-METHYLCYTOSINE; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DNA METHYLATION; GENE EXPRESSION REGULATION; HUMANS;

EID: 84992504084     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.05.091     Document Type: Article

References (50)

1. Bernstein, B.E., Stamatoyannopoulos, J.A., Costello, J.F., Ren, B., Milosavljevic, A., Meissner, A., Kellis, M., Marra, M.A., Beaudet, A.L., Ecker, J.R., et al. The NIH Roadmap Epigenomics Mapping Consortium. Nat. Biotechnol. 28 (2010), 1045–1048.
2. Cartron, P.F., Nadaradjane, A., Lepape, F., Lalier, L., Gardie, B., Vallette, F.M., Identification of TET1 Partners That Control Its DNA-Demethylating Function. Genes Cancer 4 (2013), 235–241.
3. Claussnitzer, M., Dankel, S.N., Klocke, B., Grallert, H., Glunk, V., Berulava, T., Lee, H., Oskolkov, N., Fadista, J., Ehlers, K., et al., DIAGRAM+Consortium. Leveraging cross-species transcription factor binding site patterns: from diabetes risk loci to disease mechanisms. Cell 156 (2014), 343–358.
4. Davison, L.J., Wallace, C., Cooper, J.D., Cope, N.F., Wilson, N.K., Smyth, D.J., Howson, J.M., Saleh, N., Al-Jeffery, A., Angus, K.L., et al., Cardiogenics Consortium. Long-range DNA looping and gene expression analyses identify DEXI as an autoimmune disease candidate gene. Hum. Mol. Genet. 21 (2012), 322–333.
5. Delatte, B., Deplus, R., Fuks, F., Playing TETris with DNA modifications. EMBO J. 33 (2014), 1198–1211.
6. Diehl, S., Anguita, J., Hoffmeyer, A., Zapton, T., Ihle, J.N., Fikrig, E., Rincón, M., Inhibition of Th1 differentiation by IL-6 is mediated by SOCS1. Immunity 13 (2000), 805–815.
7. Graves, M., Benton, M., Lea, R., Boyle, M., Tajouri, L., Macartney-Coxson, D., Scott, R., Lechner-Scott, J., Methylation differences at the HLA-DRB1 locus in CD4+ T-Cells are associated with multiple sclerosis. Mult. Scler. 20 (2013), 1033–1041.
8. Guo, J.U., Su, Y., Zhong, C., Ming, G.L., Song, H., Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145 (2011), 423–434.
9. Gustafsson, M., Gawel, D.R., Alfredsson, L., Baranzini, S., Björkander, J., Blomgran, R., Hellberg, S., Eklund, D., Ernerudh, J., Kockum, I., et al. A validated gene regulatory network and GWAS identifies early regulators of T cell-associated diseases. Sci. Transl. Med., 7, 2015, 313ra178.
10. Hawkins, R.D., Larjo, A., Tripathi, S.K., Wagner, U., Luu, Y., Lönnberg, T., Raghav, S.K., Lee, L.K., Lund, R., Ren, B., et al. Global chromatin state analysis reveals lineage-specific enhancers during the initiation of human T helper 1 and T helper 2 cell polarization. Immunity 38 (2013), 1271–1284.
11. Hon, G.C., Song, C.X., Du, T., Jin, F., Selvaraj, S., Lee, A.Y., Yen, C.A., Ye, Z., Mao, S.Q., Wang, B.A., et al. 5mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol. Cell 56 (2014), 286–297.
12. Ichiyama, K., Chen, T., Wang, X., Yan, X., Kim, B.S., Tanaka, S., Ndiaye-Lobry, D., Deng, Y., Zou, Y., Zheng, P., et al. The methylcytosine dioxygenase Tet2 promotes DNA demethylation and activation of cytokine gene expression in T cells. Immunity 42 (2015), 613–626.
13. Janson, P.C., Linton, L.B., Bergman, E.A., Marits, P., Eberhardson, M., Piehl, F., Malmström, V., Winqvist, O., Profiling of CD4+ T cells with epigenetic immune lineage analysis. J. Immunol. 186 (2011), 92–102.
14. Kalender Atak, Z., De Keersmaecker, K., Gianfelici, V., Geerdens, E., Vandepoel, R., Pauwels, D., Porcu, M., Lahortiga, I., Brys, V., Dirks, W.G., et al. High accuracy mutation detection in leukemia on a selected panel of cancer genes. PLoS One, 7, 2012, e38463.
15. Ko, M., Huang, Y., Jankowska, A.M., Pape, U.J., Tahiliani, M., Bandukwala, H.S., An, J., Lamperti, E.D., Koh, K.P., Ganetzky, R., et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 468 (2010), 839–843.
16. Ko, M., Bandukwala, H.S., An, J., Lamperti, E.D., Thompson, E.C., Hastie, R., Tsangaratou, A., Rajewsky, K., Koralov, S.B., Rao, A., Ten-Eleven-Translocation 2 (TET2) negatively regulates homeostasis and differentiation of hematopoietic stem cells in mice. Proc. Natl. Acad. Sci. USA 108 (2011), 14566–14571.
17. Laird, A., Thomson, J.P., Harrison, D.J., Meehan, R.R., 5-hydroxymethylcytosine profiling as an indicator of cellular state. Epigenomics 5 (2013), 655–669.
18. Lee, G.R., Kim, S.T., Spilianakis, C.G., Fields, P.E., Flavell, R.A., T helper cell differentiation: regulation by cis elements and epigenetics. Immunity 24 (2006), 369–379.
19. Leikfoss, I.S., Mero, I.L., Dahle, M.K., Lie, B.A., Harbo, H.F., Spurkland, A., Berge, T., Multiple sclerosis-associated single-nucleotide polymorphisms in CLEC16A correlate with reduced SOCS1 and DEXI expression in the thymus. Genes Immun. 14 (2013), 62–66.
20. Lemonnier, F., Couronné, L., Parrens, M., Jaïs, J.P., Travert, M., Lamant, L., Tournillac, O., Rousset, T., Fabiani, B., Cairns, R.A., et al. Recurrent TET2 mutations in peripheral T-cell lymphomas correlate with TFH-like features and adverse clinical parameters. Blood 120 (2012), 1466–1469.
21. Li, Z., Cai, X., Cai, C.L., Wang, J., Zhang, W., Petersen, B.E., Yang, F.C., Xu, M., Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118 (2011), 4509–4518.
22. Li, M.J., Wang, P., Liu, X., Lim, E.L., Wang, Z., Yeager, M., Wong, M.P., Sham, P.C., Chanock, S.J., Wang, J., GWASdb: a database for human genetic variants identified by genome-wide association studies. Nucleic Acids Res. 40 (2012), D1047–D1054.
23. Licona-Limón, P., Kim, L.K., Palm, N.W., Flavell, R.A., TH2, allergy and group 2 innate lymphoid cells. Nat. Immunol. 14 (2013), 536–542.
24. Liu, Y., Aryee, M.J., Padyukov, L., Fallin, M.D., Hesselberg, E., Runarsson, A., Reinius, L., Acevedo, N., Taub, M., Ronninger, M., et al. Epigenome-wide association data implicate DNA methylation as an intermediary of genetic risk in rheumatoid arthritis. Nat. Biotechnol. 31 (2013), 142–147.
25. Lu, F., Liu, Y., Jiang, L., Yamaguchi, S., Zhang, Y., Role of Tet proteins in enhancer activity and telomere elongation. Genes Dev. 28 (2014), 2103–2119.
26. Martin, P., McGovern, A., Orozco, G., Duffus, K., Yarwood, A., Schoenfelder, S., Cooper, N.J., Barton, A., Wallace, C., Fraser, P., et al. Capture Hi-C reveals novel candidate genes and complex long-range interactions with related autoimmune risk loci. Nat. Commun., 6, 2015, 10069.
27. Mönnich, M., Hess, I., Wiest, W., Bachrati, C., Hickson, I.D., Schorpp, M., Boehm, T., Developing T lymphocytes are uniquely sensitive to a lack of topoisomerase III alpha. Eur. J. Immunol. 40 (2010), 2379–2384.
28. Nestor, C.E., Ottaviano, R., Reddington, J., Sproul, D., Reinhardt, D., Dunican, D., Katz, E., Dixon, J.M., Harrison, D.J., Meehan, R.R., Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 22 (2012), 467–477.
29. Nestor, C.E., Barrenäs, F., Wang, H., Lentini, A., Zhang, H., Bruhn, S., Jörnsten, R., Langston, M.A., Rogers, G., Gustafsson, M., Benson, M., DNA methylation changes separate allergic patients from healthy controls and may reflect altered CD4+ T-cell population structure. PLoS Genet., 10, 2014, e1004059.
30. Nestor, C.E., Reddington, J.P., Benson, M., Meehan, R.R., Investigating 5-hydroxymethylcytosine (5hmC): the state of the art. Methods Mol. Biol. 1094 (2014), 243–258.
31. Nestor, C.E., Ottaviano, R., Reinhardt, D., Cruickshanks, H.A., Mjoseng, H.K., McPherson, R.C., Lentini, A., Thomson, J.P., Dunican, D.S., Pennings, S., et al. Rapid reprogramming of epigenetic and transcriptional profiles in mammalian culture systems. Genome Biol., 16, 2015, 11.
32. Quinlan, A.R., Hall, I.M., BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26 (2010), 841–842.
33. Sallusto, F., Lenig, D., Förster, R., Lipp, M., Lanzavecchia, A., Two subsets of memory T lymphocytes with distinct homing potentials and effector functions. Nature 401 (1999), 708–712.
34. Sallusto, F., Geginat, J., Lanzavecchia, A., Central memory and effector memory T cell subsets: function, generation, and maintenance. Annu. Rev. Immunol. 22 (2004), 745–763.
35. Schuster, C., Gerold, K.D., Schober, K., Probst, L., Boerner, K., Kim, M.J., Ruckdeschel, A., Serwold, T., Kissler, S., The Autoimmunity-Associated Gene CLEC16A Modulates Thymic Epithelial Cell Autophagy and Alters T Cell Selection. Immunity 42 (2015), 942–952.
36. Shen, L., Shao, N., Liu, X., Nestler, E., ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics, 15, 2014, 284.
37. Song, J., Chen, K.C., Spectacle: fast chromatin state annotation using spectral learning. Genome Biol., 16, 2015, 33.
38. Song, C.X., Szulwach, K.E., Fu, Y., Dai, Q., Yi, C., Li, X., Li, Y., Chen, C.H., Zhang, W., Jian, X., et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat. Biotechnol. 29 (2011), 68–72.
39. Tahiliani, M., Koh, K.P., Shen, Y., Pastor, W.A., Bandukwala, H., Brudno, Y., Agarwal, S., Iyer, L.M., Liu, D.R., Aravind, L., Rao, A., Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324 (2009), 930–935.
40. Taiwo, O., Wilson, G.A., Morris, T., Seisenberger, S., Reik, W., Pearce, D., Beck, S., Butcher, L.M., Methylome analysis using MeDIP-seq with low DNA concentrations. Nat. Protoc. 7 (2012), 617–636.
41. Tsagaratou, A., Äijö, T., Lio, C.W., Yue, X., Huang, Y., Jacobsen, S.E., Lähdesmäki, H., Rao, A., Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc. Natl. Acad. Sci. USA 111 (2014), E3306–E3315.
42. Wahren-Herlenius, M., Dörner, T., Immunopathogenic mechanisms of systemic autoimmune disease. Lancet 382 (2013), 819–831.
43. Wellcome Trust Case Control, C., Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447 (2007), 661–678.
44. Williams, K., Christensen, J., Pedersen, M.T., Johansen, J.V., Cloos, P.A., Rappsilber, J., Helin, K., TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473 (2011), 343–348.
45. Wu, H., Zhang, Y., Reversing DNA methylation: mechanisms, genomics, and biological functions. Cell 156 (2014), 45–68.
46. Wu, H., D'Alessio, A.C., Ito, S., Xia, K., Wang, Z., Cui, K., Zhao, K., Sun, Y.E., Zhang, Y., Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473 (2011), 389–393.
47. Yamane, H., Paul, W.E., Early signaling events that underlie fate decisions of naive CD4(+) T cells toward distinct T-helper cell subsets. Immunol. Rev. 252 (2013), 12–23.
48. Yang, R., Qu, C., Zhou, Y., Konkel, J.E., Shi, S., Liu, Y., Chen, C., Liu, S., Liu, D., Chen, Y., et al. Hydrogen sulfide promotes Tet1- and Tet2-mediated Foxp3 demethylation to drive regulatory T cell differentiation and maintain immune homeostasis. Immunity 43 (2015), 251–263.
49. Yu, M., Hon, G.C., Szulwach, K.E., Song, C.X., Zhang, L., Kim, A., Li, X., Dai, Q., Shen, Y., Park, B., et al. Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149 (2012), 1368–1380.
50. Zhang, Y., Liu, T., Meyer, C.A., Eeckhoute, J., Johnson, D.S., Bernstein, B.E., Nusbaum, C., Myers, R.M., Brown, M., Li, W., Liu, X.S., Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, 2008, R137.