Histone H3 Lysine 27 demethylases Jmjd3 and Utx are required for T-cell differentiation

Nature Communications

Volumn 6, Issue , 2015, Pages

  Manna, Sugata ^a   Kim, Jong Kyong ^a,d   Baugé, Catherine ^a,e   Cam, Margaret ^a   Zhao, Yongmei ^b   Shetty, Jyoti ^b   Vacchio, Melanie S ^a   Castro, Ehydel ^a   Tran, Bao ^b   Tessarollo, Lino ^c   Bosselut, Rémy ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SUN YAT SEN UNIVERSITY   (China)

^e UNIVERSITÉ DE CAEN   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H3; JMJD3 HISTONE; KRUPPEL LIKE FACTOR 2; UNCLASSIFIED DRUG; UTX HISTONE; HISTONE DEMETHYLASE; KDM6B PROTEIN, MOUSE; S1PR1 PROTEIN, MOUSE; SPHINGOSINE 1 PHOSPHATE RECEPTOR; UTX PROTEIN, MOUSE;

AMINO ACID; CELLS AND CELL COMPONENTS; ENZYME; GENE EXPRESSION; MALE; PROTEIN; RODENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; HISTONE DEMETHYLATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MALE; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; TRANSCRIPTION INITIATION SITE; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; FLOW CYTOMETRY; GENETICS; KNOCKOUT MOUSE; METABOLISM; REAL TIME POLYMERASE CHAIN REACTION;

MUS;

ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CHROMATIN IMMUNOPRECIPITATION; FLOW CYTOMETRY; HISTONE DEMETHYLASES; IN VITRO TECHNIQUES; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, LYSOSPHINGOLIPID; THYMOCYTES;

EID: 84940837110     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9152     Document Type: Article

References (63)

1. Carpenter, A. C. & Bosselut, R. Decision checkpoints in the thymus. Nat. Immunol. 11, 666-673 (2010).
2. Rothenberg, E. V. Transcriptional drivers of the T-cell lineage program. Curr. Opin. Immunol. 24, 132-138 (2012).
3. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007).
4. Yun, M., Wu, J., Workman, J. L. & Li, B. Readers of histone modifications. Cell. Res. 21, 564-578 (2011).
5. Bannister, A. J. & Kouzarides, T. Regulation of chromatin by histone modifications. Cell. Res. 21, 381-395 (2011).
6. Margueron, R. & Reinberg, D. The Polycomb complex PRC2 and its mark in life. Nature 469, 343-349 (2011).
7. Pengelly, A. R., Copur, O., Jackle, H., Herzig, A. & Muller, J. A histone mutant reproduces the phenotype caused by loss of histone-modifying factor Polycomb. Science 339, 698-699 (2013).
8. Simon, J. A. & Kingston, R. E. Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol. Cell. 49, 808-824 (2013).
9. Agger, K. et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 449, 731-734 (2007).
10. De Santa, F. et al. The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing. Cell 130, 1083-1094 (2007).
11. Hong, S. et al. Identification of JmjC domain-containing UTX and JMJD3 as histone H3 lysine 27 demethylases. Proc. Natl Acad. Sci. USA 104, 18439-18444 (2007).
12. Lan, F. et al. A histone H3 lysine 27 demethylase regulates animal posterior development. Nature 449, 689-694 (2007).
13. Lee, M. G. et al. Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318, 447-450 (2007).
14. Welstead, G. G. et al. X-linked H3K27me3 demethylase Utx is required for embryonic development in a sex-specific manner. Proc. Natl Acad. Sci. USA 109, 13004-13009 (2012).
15. Burgold, T. et al. The H3K27 demethylase JMJD3 is required for maintenance of the embryonic respiratory neuronal network, neonatal breathing, and survival. Cell Rep. 2, 1244-1258 (2012).
16. Shpargel, K. B., Sengoku, T., Yokoyama, S. & Magnuson, T. UTX and UTY demonstrate histone demethylase-independent function in mouse embryonic development. PLoS. Genet. 8, e1002964 (2012).
17. Wang, C. et al. UTX regulates mesoderm differentiation of embryonic stem cells independent of H3K27 demethylase activity. Proc. Natl Acad. Sci. USA 109, 15324-15329 (2012).
18. Morales Torres, C., Laugesen, A. & Helin, K. Utx is required for proper induction of ectoderm and mesoderm during differentiation of embryonic stem cells. PLoS ONE 8, e60020 (2013).
19. Li, Q. et al. Stage-dependent and locus-specific role of histone demethylase Jumonji D3 (JMJD3) in the embryonic stages of lung development. PLoS Genet. 10, e1004524 (2014).
20. Xu, J., Deng, X., Watkins, R. & Disteche, C. M. Sex-specific differences in expression of histone demethylases Utx and Uty in mouse brain and neurons. J. Neurosci. 28, 4521-4527 (2008).
21. Shpargel, K. B., Starmer, J., Yee, D., Pohlers, M. & Magnuson, T. KDM6 demethylase independent loss of histone H3 lysine 27 trimethylation during early embryonic development. PLoS Genet. 10, e1004507 (2014).
22. Barski, A. et al. High-resolution profiling of histone methylations in the human genome. Cell 129, 823-837 (2007).
23. Wei, G. et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30, 155-167 (2009).
24. Zhang, J. et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13, 86-94 (2012).
25. Zhang, J. A., Mortazavi, A., Williams, B. A., Wold, B. J. & Rothenberg, E. V. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 149, 467-482 (2012).
26. Tanaka, H. et al. Epigenetic Thpok silencing limits the time window to choose CD4(+) helper-lineage fate in the thymus. EMBO J. 32, 1183-1194 (2013).
27. Wang, L. & Bosselut, R. CD4-CD8 lineage differentiation: Thpok-ing into the nucleus. J. Immunol. 183, 2903-2910 (2009).
28. Satoh, T. et al. The Jmjd3-Irf4 axis regulates M2 macrophage polarization and host responses against helminth infection. Nat. Immunol. 11, 936-944 (2010).
29. Clissold, P. M. & Ponting, C. P. JmjC: cupin metalloenzyme-like domains in jumonji, hairless and phospholipase A2beta. Trends Biochem. Sci. 26, 7-9 (2001).
30. Barnden, M. J., Allison, J., Heath, W. R. & Carbone, F. R. Defective TCR expression in transgenic mice constructed using cDNA-based alpha-And betachain genes under the control of heterologous regulatory elements. Immunol. Cell. Biol. 76, 34-40 (1998).
31. Matloubian, M. et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature 427, 355-360 (2004).
32. Allende, M. L., Dreier, J. L., Mandala, S. & Proia, R. L. Expression of the sphingosine 1-phosphate receptor, S1P1, on T-cells controls thymic emigration. J. Biol. Chem. 279, 15396-15401 (2004).
33. Carlson, C. M. et al. Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442, 299-302 (2006).
34. Shiow, L. R. et al. CD69 acts downstream of interferon-Alpha/beta to inhibit S1P1 and lymphocyte egress from lymphoid organs. Nature 440, 540-544 (2006).
35. Moran, A. E. et al. T cell receptor signal strength in Treg and iNKT cell development demonstrated by a novel fluorescent reporter mouse. J. Exp. Med. 208, 1279-1289 (2011).
36. Thieme, S. et al. The histone demethylase UTX regulates stem cell migration and hematopoiesis. Blood 121, 2462-2473 (2013).
37. Miller, S. A., Mohn, S. E. & Weinmann, A. S. Jmjd3 and UTX play a demethylase-independent role in chromatin remodeling to regulate T-box family member-dependent gene expression. Mol. Cell. 40, 594-605 (2010).
38. Bai, A., Hu, H., Yeung, M. & Chen, J. Kruppel-like factor 2 controls T cell trafficking by activating L-selectin (CD62L) and sphingosine-1-phosphate receptor 1 transcription. J. Immunol. 178, 7632-7639 (2007).
39. Li, Q. et al. Critical role of histone demethylase Jmjd3 in the regulation of CD4(+) T-cell differentiation. Nat. Commun. 5, 5780 (2014).
40. Dobenecker, M. W. et al. Coupling of T cell receptor specificity to natural killer T cell development by bivalent histone H3 methylation. J. Exp. Med. 212, 297-306 (2015).
41. Bendelac, A., Savage, P. B. & Teyton, L. The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007).
42. Van der Meulen, J., Speleman, F. & Van Vlierberghe, P. The H3K27me3 demethylase UTX in normal development and disease. Epigenetics 9, 658-668 (2014).
43. Ntziachristos, P. et al. Contrasting roles of histone 3 lysine 27 demethylases in acute lymphoblastic leukaemia. Nature 514, 513-517 (2014).
44. Van der Meulen, J. et al. The H3K27me3 demethylase UTX is a gender-specific tumor suppressor in T-cell acute lymphoblastic leukemia. Blood 125, 13-21 (2015).
45. Mingueneau, M. et al. The transcriptional landscape of alphabeta T cell differentiation. Nat. Immunol. 14, 619-632 (2013).
46. Chen, S. et al. The histone H3 Lys 27 demethylase JMJD3 regulates gene expression by impacting transcriptional elongation. Genes Dev. 26, 1364-1375 (2012).
47. Szabo, S. J. et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 100, 655-669 (2000).
48. Cho, Y. W. et al. PTIP associates with MLL3-And MLL4-containing histone H3 lysine 4 methyltransferase complex. J. Biol. Chem. 282, 20395-20406 (2007).
49. Shi, X. et al. An epigenetic switch induced by Shh signalling regulates gene activation during development and medulloblastoma growth. Nat. Commun. 5, 5425 (2014).
50. Vincenz, C. & Kerppola, T. K. Different polycomb group CBX family proteins associate with distinct regions of chromatin using nonhomologous protein sequences. Proc. Natl Acad. Sci. USA 105, 16572-16577 (2008).
51. Klauke, K. et al. Polycomb Cbx family members mediate the balance between haematopoietic stem cell self-renewal and differentiation. Nat. Cell Biol. 15, 353-362 (2013).
52. Smith, E. R. et al. Drosophila UTX is a histone H3 Lys27 demethylase that colocalizes with the elongating form of RNA polymerase II. Mol. Cell. Biol. 28, 1041-1046 (2008).
53. Williams, S. T. et al. Studies on the catalytic domains of multiple JmjC oxygenases using peptide substrates. Epigenetics 9, 1596-1603 (2014).
54. Elsaesser, S. J., Goldberg, A. D. & Allis, C. D. New functions for an old variant: no substitute for histone H3.3. Curr. Opin. Genet. Dev. 20, 110-117 (2010).
55. Carey, B. W., Finley, L. W., Cross, J. R., Allis, C. D. & Thompson, C. B. Intracellular alpha-ketoglutarate maintains the pluripotency of embryonic stem cells. Nature 518, 413-416 (2014).
56. Pircher, H., Burki, K., Lang, R., Hengartner, H. & Zinkernagel, R. M. Tolerance induction in double specific T-cell receptor transgenic mice varies with antigen. Nature 342, 559-561 (1989).
57. Chi, H. & Flavell, R. A. Cutting edge: regulation of T cell trafficking and primary immune responses by sphingosine 1-phosphate receptor 1. J. Immunol. 174, 2485-2488 (2005).
58. Liu, X. et al. Restricting Zap70 expression to CD4+CD8+ thymocytes reveals a T cell receptor-dependent proofreading mechanism controlling the completion of positive selection. J. Exp. Med. 197, 363-373 (2003).
59. Liao, Y., Smyth, G. K. & Shi, W. The Subread aligner: fast, accurate and scalable read mapping by seed-And-vote. Nucleic Acids Res. 41, e108 (2013).
60. Lun, A. T. & Smyth, G. K. De novo detection of differentially bound regions for ChIP-seq data using peaks and windows: controlling error rates correctly. Nucleic Acids Res. 42, e95 (2014).
61. Zang, C. et al. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics. 25, 1952-1958 (2009).
62. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
63. Lund, S. P., Nettleton, D., McCarthy, D. J. & Smyth, G. K. Detecting differential expression in RNA-sequence data using quasi-likelihood with shrunken dispersion estimates. Stat. Appl. Genet. Mol. Biol. 11, doi:10.1515/1544-6115.1826 (2012).