Jarid2 is induced by TCR signalling and controls iNKT cell maturation

Nature Communications

Volumn 5, Issue , 2014, Pages

  Pereira, Renata M ^a   Martinez, Gustavo J ^a,f   Engel, Isaac ^a   Cruz Guilloty, Fernando ^b,g   Barboza, Bianca A ^a,h   Tsagaratou, Ageliki ^a   Lio, Chan Wang J ^a   Berg, Leslie J ^c   Lee, Youngsook ^d   Kronenberg, Mitchell ^a   Bandukwala, Hozefa S ^a,i   Rao, Anjana ^a,e  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f SCRIPPS RESEARCH INSTITUTE   (United States)

^g Immucor Inc   (United States)

^h INSTITUTO NACIONAL DE CÂNCER   (Brazil)

ⁱ PFIZER INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CXCR3; EARLY GROWTH RESPONSE FACTOR 2; HERMES ANTIGEN; HISTONE H3; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 4; JARID2 PROTEIN; MESSENGER RNA; METHYLTRANSFERASE; POLYCOMB REPRESSIVE COMPLEX 2; PROMYELOCYTIC LEUKEMIA ZINC FINGER PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG; CD69 ANTIGEN; HISTONE; JARID2 PROTEIN, MOUSE; KRUPPEL LIKE FACTOR; LECTIN; LEUKOCYTE ANTIGEN; LYMPHOCYTE ANTIGEN RECEPTOR; LYSINE; MICRORNA; T LYMPHOCYTE ANTIGEN; ZBTB16 PROTEIN, MOUSE; ZINC FINGER PROTEIN;

AMINO ACID; ENZYME ACTIVITY; GENE EXPRESSION; IMMUNE RESPONSE; MATURATION; METHYLATION; PATHOLOGY; PROTEIN; RODENT;

ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; HUMAN; HUMAN CELL; INVARIANT NATURAL KILLER CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TH17 CELL; THYMOCYTE; THYMUS; UPREGULATION; ANIMAL; BONE MARROW CELL; C57BL MOUSE; CELL SEPARATION; CHEMISTRY; CYTOLOGY; FEMALE; FLOW CYTOMETRY; MALE; METABOLISM; METHYLATION; PROMOTER REGION; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BONE MARROW CELLS; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL SEPARATION; FEMALE; FLOW CYTOMETRY; HISTONES; INTERLEUKIN-4; KILLER CELLS, NATURAL; KRUPPEL-LIKE TRANSCRIPTION FACTORS; LECTINS, C-TYPE; LYSINE; MALE; METHYLATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MICRORNAS; POLYCOMB REPRESSIVE COMPLEX 2; PROMOTER REGIONS, GENETIC; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; THYMUS GLAND; UP-REGULATION; ZINC FINGERS;

EID: 84907316977     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms5540     Document Type: Article

References (71)

1. Kouzarides, T. Chromatin modifications and their function. Cell 128, 693-705 (2007). (Pubitemid 46273577)
2. Black, J. C., Van Rechem, C. & Whetstine, J. R. Histone lysine methylation dynamics: establishment, regulation, and biological impact. Mol. Cell 48, 491-507 (2012).
3. Schuettengruber, B., Chourrout, D., Vervoort, M., Leblanc, B. & Cavalli, G. Genome regulation by polycomb and trithorax proteins. Cell 128, 735-745 (2007). (Pubitemid 46273581)
4. Raaphorst, F. M. Deregulated expression of Polycomb-group oncogenes in human malignant lymphomas and epithelial tumors. Hum. Mol. Genet. 14 Spec No 1, R93-R100 (2005). (Pubitemid 40542625)
5. Heard, E. Recent advances in X-chromosome inactivation. Curr. Opin. Cell Biol. 16, 247-255 (2004). (Pubitemid 38610404)
6. Shen, X. et al. EZH1 mediates methylation on histone H3 lysine 27 and complements EZH2 in maintaining stem cell identity and executing pluripotency. Mol. Cell 32, 491-502 (2008).
7. Li, G. et al. Jarid2 and PRC2, partners in regulating gene expression. Genes Dev. 24, 368-380 (2010).
8. Landeira, D. et al. Jarid2 is a PRC2 component in embryonic stem cells required for multi-lineage differentiation and recruitment of PRC1 and RNA Polymerase II to developmental regulators. Nat. Cell Biol. 12, 618-624 (2010).
9. Pasini, D. et al. JARID2 regulates binding of the Polycomb repressive complex 2 to target genes in ES cells. Nature 464, 306-310 (2010).
10. Peng, J. C. et al. Jarid2/Jumonji coordinates control of PRC2 enzymatic activity and target gene occupancy in pluripotent cells. Cell 139, 1290-1302 (2009).
11. Shen, X. et al. Jumonji modulates polycomb activity and self-renewal versus differentiation of stem cells. Cell 139, 1303-1314 (2009).
12. Takeuchi, T., Watanabe, Y., Takano-Shimizu, T. & Kondo, S. Roles of jumonji and jumonji family genes in chromatin regulation and development. Dev. Dyn. 235, 2449-2459 (2006). (Pubitemid 44325259)
13. Shirato, H. et al. A jumonji (Jarid2) protein complex represses cyclin D1 expression by methylation of histone H3-K9. J. Biol. Chem. 284, 733-739 (2009).
14. Jung, J., Kim, T. G., Lyons, G. E., Kim, H. R. & Lee, Y. Jumonji regulates cardiomyocyte proliferation via interaction with retinoblastoma protein. J. Biol. Chem. 280, 30916-30923 (2005). (Pubitemid 41291823)
15. Mysliwiec, M. R. et al. Jarid2 (Jumonji, AT rich interactive domain 2) regulates NOTCH1 expression via histone modification in the developing heart. J. Biol. Chem. 287, 1235-1241 (2012).
16. Kitajima, K. et al. Definitive but not primitive hematopoiesis is impaired in jumonji mutant mice. Blood 93, 87-95 (1999). (Pubitemid 29019392)
17. Ansel, K. M., Djuretic, I., Tanasa, B. & Rao, A. Regulation of Th2 differentiation and Il4 locus accessibility. Annu. Rev. Immunol. 24, 607-656 (2006).
18. 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).
19. 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).
20. Stritesky, G. L., Jameson, S. C. & Hogquist, K. A. Selection of self-reactive T cells in the thymus. Annu. Rev. Immunol. 30, 95-114 (2012).
21. Baldwin, T. A., Hogquist, K. A. & Jameson, S. C. The fourth way? Harnessing aggressive tendencies in the thymus. J. Immunol. 173, 6515-6520 (2004). (Pubitemid 39541032)
22. Oh-Hora, M. et al. Agonist-selected T cell development requires strong T cell receptor signaling and store-operated calcium entry. Immunity 38, 881-895 (2013).
23. Engel, I. & Kronenberg, M. Making memory at birth: understanding the differentiation of natural killer T cells. Curr. Opin. Immunol. 24, 184-190 (2012).
24. Gapin, L., Matsuda, J. L., Surh, C. D. & Kronenberg, M. NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2, 971-978 (2001). (Pubitemid 32976171)
25. Coquet, J. M. et al. Diverse cytokine production by NKT cell subsets and identification of an IL-17-producing CD4-NK1.1-NKT cell population. Proc. Natl Acad. Sci. USA 105, 11287-11292 (2008).
26. Kovalovsky, D. et al. The BTB-zinc finger transcriptional regulator PLZF controls the development of invariant natural killer T cell effector functions. Nat. Immunol. 9, 1055-1064 (2008).
27. Savage, A. K. et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29, 391-403 (2008).
28. Savage, A. K., Constantinides, M. G. & Bendelac, A. Promyelocytic leukemia zinc finger turns on the effector T cell program without requirement for agonist TCR signaling. J. Immunol. 186, 5801-5806 (2011).
29. Seiler, M. P. et al. Elevated and sustained expression of the transcription factors Egr1 and Egr2 controls NKT lineage differentiation in response to TCR signaling. Nat. Immunol. 13, 264-271 (2012).
30. Macian, F. et al. Transcriptional mechanisms underlying lymphocyte tolerance. Cell 109, 719-731 (2002).
31. Hogan, P. G., Lewis, R. S. & Rao, A. Molecular basis of calcium signaling in lymphocytes: STIM and ORAI. Annu. Rev. Immunol. 28, 491-533 (2010).
32. Schaeffer, E. M. et al. Requirement for Tec kinases Rlk and Itk in T cell receptor signaling and immunity. Science 284, 638-641 (1999). (Pubitemid 29289587)
33. Lucas, J. A., Miller, A. T., Atherly, L. O. & Berg, L. J. The role of Tec family kinases in T cell development and function. Immunol. Rev. 191, 119-138 (2003). (Pubitemid 36398853)
34. Horai, R. et al. Requirements for selection of conventional and innate T lymphocyte lineages. Immunity 27, 775-785 (2007). (Pubitemid 350102265)
35. Broussard, C. et al. Altered development of CD8\+ T cell lineages in mice deficient for the Tec kinases Itk and Rlk. Immunity 25, 93-104 (2006). (Pubitemid 44066833)
36. Mysliwiec, M. R. et al. Generation of a conditional null allele of jumonji. Genesis 44, 407-411 (2006). (Pubitemid 44454045)
37. Intlekofer, A. M. et al. Effector and memory CD8\+ T cell fate coupled by T-bet and eomesodermin. Nat. Immunol. 6, 1236-1244 (2005). (Pubitemid 43045635)
38. Jordan, M. S. et al. Complementation in trans of altered thymocyte development in mice expressing mutant forms of the adaptor molecule SLP76. Immunity 28, 359-369 (2008). (Pubitemid 351343858)
39. Weinreich, M. A., Odumade, O. A., Jameson, S. C. & Hogquist, K. A. T cells expressing the transcription factor PLZF regulate the development of memorylike CD8\+ T cells. Nat. Immunol. 11, 709-716 (2010).
40. Weinreich, M. A. et al. KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31, 122-130 (2009).
41. Fukuyama, T. et al. Histone acetyltransferase CBP is vital to demarcate conventional and innate CD8\+ T-cell development. Mol. Cell Biol. 29, 3894-3904 (2009).
42. Verykokakis, M., Boos, M. D., Bendelac, A. & Kee, B. L. SAP protein-dependent natural killer T-like cells regulate the development of CD8(\+) T cells with innate lymphocyte characteristics. Immunity 33, 203-215 (2010).
43. Lee, Y. J., Jameson, S. C. & Hogquist, K. A. Alternative memory in the CD8 T cell lineage. Trends Immunol. 32, 50-56 (2011).
44. Bendelac, A., Savage, P. B. & Teyton, L. The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007). (Pubitemid 46697911)
45. Lee, Y. J., Holzapfel, K. L., Zhu, J., Jameson, S. C. & Hogquist, K. A. Steady-state production of IL-4 modulates immunity in mouse strains and is determined by lineage diversity of iNKT cells. Nat. Immunol. 14, 1146-1154 (2013).
46. Gadue, P. & Stein, P. L. NK T cell precursors exhibit differential cytokine regulation and require Itk for efficient maturation. J. Immunol. 169, 2397-2406 (2002). (Pubitemid 34920982)
47. Dickgreber, N. et al. Immature murine NKT cells pass through a stage of developmentally programmed innate IL-4 secretion. J. Leukoc. Biol. 92, 999-1009 (2012).
48. Constantinides, M. G. & Bendelac, A. Transcriptional regulation of the NKT cell lineage. Curr. Opin. Immunol. 25, 161-167 (2013).
49. Gordon, S. M. et al. Requirements for eomesodermin and promyelocytic leukemia zinc finger in the development of innate-like CD8\+ T cells. J. Immunol. 186, 4573-4578 (2011).
50. Hammond, K. J. & Kronenberg, M. Natural killer T cells: natural or unnatural regulators of autoimmunity? Curr. Opin. Immunol. 15, 683-689 (2003). (Pubitemid 37434076)
51. Singh, A. K. et al. Natural killer T cell activation protects mice against experimental autoimmune encephalomyelitis. J. Exp. Med. 194, 1801-1811 (2001). (Pubitemid 34028659)
52. Bandukwala, H. S. et al. Selective inhibition of CD4\+ T-cell cytokine production and autoimmunity by BET protein and c-Myc inhibitors. Proc. Natl Acad. Sci. USA 109, 14532-14537 (2012).
53. Escobar, T. M. et al. miR-155 activates cytokine gene expression in Th17 cells by regulating the DNA-binding protein Jarid2 to relieve polycomb-mediated repression. Immunity 19, 865-879 (2014).
54. Zhang, J. et al. Harnessing of the nucleosome-remodeling-deacetylase complex controls lymphocyte development and prevents leukemogenesis. Nat. Immunol. 13, 86-94 (2012).
55. Beuchle, D., Struhl, G. & Muller, J. Polycomb group proteins and heritable silencing of Drosophila Hox genes. Development 128, 993-1004 (2001). (Pubitemid 32288208)
56. Landeira, D. & Fisher, A. G. Inactive yet indispensable: the tale of Jarid2. Trends Cell. Biol. 21, 74-80 (2011).
57. Godfrey, D. I., Stankovic, S. & Baxter, A. G. Raising the NKT cell family. Nat. Immunol. 11, 197-206 (2010).
58. Dutta, M. et al. A role for Ly108 in the induction of promyelocytic zinc finger transcription factor in developing thymocytes. J. Immunol. 190, 2121-2128 (2013).
59. Seiler, M. P. et al. Elevated and sustained expression of the transcription factors Egr1 and Egr2 controls NKT lineage differentiation in response to TCR signaling. Nat. Immunol. 14, 413 (2013).
60. Mozzetta, C. et al. The histone H3 lysine 9 methyltransferases G9a and GLP regulate polycomb repressive complex 2-mediated gene silencing. Mol. Cell 53, 277-289 (2014).
61. Kaneko, S. et al. Interactions between JARID2 and noncoding RNAs regulate PRC2 recruitment to chromatin. Mol. Cell 53, 290-300 (2014).
62. 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).
63. Son, J., Shen, S. S., Margueron, R. & Reinberg, D. Nucleosome-binding activities within JARID2 and EZH1 regulate the function of PRC2 on chromatin. Genes Dev. 28, 921 (2014).
64. Toyoda, M. et al. jumonji downregulates cardiac cell proliferation by repressing cyclin D1 expression. Dev. Cell 5, 85-97 (2003). (Pubitemid 36827344)
65. Mysliwiec, M. R., Bresnick, E. H. & Lee, Y. Endothelial Jarid2/Jumonji is required for normal cardiac development and proper Notch1 expression. J. Biol. Chem. 286, 17193-17204 (2011).
66. Berg, L. J. Signalling through TEC kinases regulates conventional versus innate CD8(\+) T-cell development. Nat. Rev. Immunol. 7, 479-485 (2007). (Pubitemid 46834846)
67. Atherly, L. O. et al. The Tec family tyrosine kinases Itk and Rlk regulate the development of conventional CD8\+ T cells. Immunity 25, 79-91 (2006). (Pubitemid 44066834)
68. Verykokakis, M. et al. Inhibitor of DNA binding 3 limits development of murine slam-associated adaptor protein-dependent 'innate' gammadelta T cells. PLoS ONE 5, e9303 (2010).
69. Xanthoudakis, S. et al. An enhanced immune response in mice lacking the transcription factor NFAT1. Science 272, 892-895 (1996).
70. Vaeth, M. et al. Dependence on nuclear factor of activated T-cells (NFAT) levels discriminates conventional T cells from Foxp3\+ regulatory T cells. Proc. Natl Acad. Sci. USA 109, 16258-16263 (2012).
71. Bettelli, E. et al. Myelin oligodendrocyte glycoprotein-specific T cell receptor transgenic mice develop spontaneous autoimmune optic neuritis. J. Exp. Med. 197, 1073-1081 (2003). (Pubitemid 36570063)