T-cell receptor signaling induces proximal Runx1 transactivation via a calcineurin-NFAT pathway

European Journal of Immunology

Volumn 44, Issue 3, 2014, Pages 894-904

  Wong, Won Fen ^a,b   Looi, Chung Yeng ^a   Kon, Shunsuke ^b   Movahed, Elaheh ^a   Funaki, Tomo ^b   Chang, Li Yen ^a   Satake, Masanobu ^b   Kohu, Kazuyoshi ^c  

^a UNIVERSITY OF MALAYA   (Malaysia)

^b TOHOKU UNIVERSITY   (Japan)

^c NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Cellular activation; Naive cells; T cells; TCR; Transcription factors

Indexed keywords

CALCINEURIN; CYCLOSPORIN A; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RUNX1;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; LUCIFERASE ASSAY; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSACTIVATION; TRANSCRIPTION INITIATION SITE;

CELLULAR ACTIVATION; NAIVE CELLS; T CELLS; TCR; TRANSCRIPTION FACTORS;

ANIMALS; BINDING SITES; CALCINEURIN; CONSERVED SEQUENCE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; CYCLOSPORINE; GENE EXPRESSION REGULATION; MICE; MUTATION; NFATC TRANSCRIPTION FACTORS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RECEPTORS, ANTIGEN, T-CELL; RNA INTERFERENCE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSCRIPTIONAL ACTIVATION;

EID: 84896030432     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201343496     Document Type: Article

References (38)

1. Nel, A. E., T-cell activation through the antigen receptor. Part 1: signaling components, signaling pathways, and signal integration at the T-cell antigen receptor synapse. J. Allergy Clin. Immunol. 2002. 109: 758-770.
2. Chow, C. W., Rincon, M. and Davis, R. J., Requirement for transcription factor NFAT in interleukin-2 expression. Mol. Cell. Biol. 1999. 19: 2300-2307.
3. Satake, M., Nomura, S., Yamaguchi-Iwai, Y., Takahama, Y., Hashimoto, Y., Niki, M., Kitamura, Y. et al., Expression of the Runt domain-encoding PEBP2 alpha genes in T cells during thymic development. Mol. Cell. Biol. 1995. 15: 1662-1670.
4. Wong, W. F., Kohu, K., Chiba, T., Sato, T. and Satake, M., Interplay of transcription factors in T-cell differentiation and function: the role of Runx. Immunology 2011. 132: 157-164.
5. Howcroft, T. K., Weissman, J. D., Gegonne, A. and Singer, D. S., A T lymphocyte-specific transcription complex containing RUNX1 activates MHC class I expression. J. Immunol. 2005. 174: 2106-2115.
6. Giese, K., Kingsley, C., Kirshner, J. R. and Grosschedl, R., Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev. 1995. 9: 995-1108.
7. Egawa, T., Tillman, R. E., Naoe, Y., Taniuchi, I. and Littman, D. R., The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med. 2007. 204: 1945-1957.
8. Wong, W. F., Nakazato, M., Watanabe, T., Kohu, K., Ogata, T., Yoshida, N., Sotomaru, Y. et al., Over-expression of Runx1 transcription factor impairs the development of thymocytes from the double-negative to double-positive stages. Immunology 2010. 130: 243-253.
9. Setoguchi, R., Tachibana, M., Naoe, Y., Muroi, S., Akiyama, K., Tezuka, C., Okuda, T. et al., Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development. Science 2008. 319: 822-825.
10. Hayashi, K., Abe, N., Watanabe, T., Obinata, M., Ito, M., Sato, T., Habu, S. and Satake, M., Overexpression of AML1 transcription factor drives thmocytes into the CD8 single-positive lineage. J. Immunol. 2001. 167: 4957-4965.
11. Wong, W. F., Kohu, K., Nakamura, A., Ebina, M., Kikuchi, T., Tazawa, R., Tanaka, K. et al., Runx1 deficiency in CD4+ T cells causes fatal autoimmune inflammatory lung disease due to spontaneous hyperactivation of cells. J. Immunol. 2012. 188: 5408-5420.
12. Komine, O., Hayashi, K., Natsume, W., Watanabe, T., Seki, Y., Seki, N., Yagi, R. et al., The Runx1 transcription factor inhibits the differentiation of naive CD4+ T cells into the Th2 lineage by repressing GATA3 expression. J. Exp. Med. 2003. 198: 51-61.
13. Zhang, F., Meng, G. and Strober, W., Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 2008. 9: 1297-1306.
14. Ono, M., Yaguchi, H., Ohkura, N., Kitabayashi, I., Nagamura, Y., Nomura, T., Miyachi, Y. et al., Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 2007. 446: 685-689.
15. Ghozi, M. C., Bernstein, Y., Negreanu, V., Levanon, D. and Groner, Y., Expression of the human acute myeloid leukemia gene AML1 is regulated by two promoter regions. Proc. Natl. Acad. Sci. 1996. 93: 1935-1940.
16. Pozner, A., Goldenberg, D., Negreanu, V., Le, S. Y., Elroy-Stein, O., Levanon, D. and Groner, Y., Transcription-coupled translation control of AML1/RUNX1 is mediated by cap- and internal ribosome entry site-dependent mechanisms. Mol. Cell Biol. 2000. 20: 2297-2307.
17. Levanon, D., Glusman, G., Bangsow, T., Ben-Asher, E., Male, D. A., Avidan, N., Bangsow, C. et al., Architecture and anatomu of the genomic locus encoding the human leukemia-associated transcription factor RUNX1/AML1. Gene 2001. 262: 23-33.
18. Li, Q. L., Ito, K., Sakakura, C., Fukamachi, H., Inoue, K., Chi, X. Z., Lee, K. Y. et al., Causal relationship between the loss of RUNX3 expression and gastric cancer. Cell 2002. 109: 113-124.
19. Telfer, J. and Rothenberg, E., Expression and function of a stem cell promoter for the murine CBFalpha2 gene: distinct roles and regulation in natural killer and T cell development. Dev. Biol. 2001. 229: 363-382.
20. Pozner, A., Lotem, J., Xiao, C., Goldenberg, D., Brenner, O., Negreanu, V., Levanon, D. et al., Developmentally regulated promoter-switch transcriptionally controls Runx1 function during embryonic hematopoiesis. BMC Dev. Biol. 2007. 7: 84.
21. Nottingham, W. T., Jarratt, A., Burgess, M., Speck, C. L., Cheng, J. F., Prabhakar, S., Rubin, E. M. et al., Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. Blood 2007. 110: 4188-4197.
22. Ng, C. E., Yokomizo, T., Yamashita, N., Cirovic, B., Jin, H., Wen, Z., Ito, Y. et al., A Runx1 intronic enhancer marks hemogenic endothelial cells and hematopoietic stem cells. Stem Cells 2010. 28: 1869-1881.
23. Wong, W. F., Kurokawa, M., Satake, M. and Kohu, K., Down-regulation of Runx1 expression by TCR signal involves an autoregulatory mechanism and contributes to IL-2 production. J. Biol. Chem. 2011. 286: 11110-11118.
24. Mercurio, F., Zhu, H., Murray, B. W., Shevchenko, A., Bennett, B. L., Li, J. W., Young, D. B. et al., IKK-1 and IKK-2: cytokine-activated IkappaB kinase essential for NF-kappaB activation. Science 1997. 278: 860-866.
25. Macian, F., NFAT proteins: key regulators of T-cell development and function. Nat. Rev. Immunol. 2005. 5: 472-484.
26. Rengarajan, J., Tang, B. and Glimcher, L. H., NFATc2 and NFATc3 regulate T(H)2 differentiation and modulate TCR-responsiveness of naive T(H)cells. Nat. Immunol. 2002. 3: 48-54.
27. Sato, T., Chiba, T., Ohno, S., Sato, C., Sugoh, T., Miyashita, K., Akatsuka, H. et al., Reciprocal control of G1-phase progression is required for Th-POK/Runx3-mediated CD4/8 thymocyte cell fate decision. J. Immunol. 2012. 189: 4426-4436.
28. Hirai, H., Samokhvalov, I. M., Fujimoto, T., Nishikawa, S. and Imanishi, J., Involvement of Runx1 in the down-regulation of fetal liver kinase-1 expression during transition of endothelial cells to hematopoietic cells. Blood 2005. 106: 1948-1955.
29. Bee, T., Swiers, G., Muroi, S., Pozner, A., Nottingham, W., Santos, A. C., Li, P. S. et al., Nonredundant roles for Runx1 alternative promoters reflect their activity at discrete stages of developmental hematopoiesis. Blood 2010. 115: 3042-3050.
30. Spender, L. C., Whiteman, H. J., Karstegl, C. E. and Farrell, P. J., Transcriptional cross-regulation of RUNX1 by RUNX3 in human B cells. Oncogene 2005. 24: 1873-1881.
31. Brady, G., Elgueta Karstegl, C. and Farrell, P. J., Novel function of the unique N-terminal region of RUNX1c in B cell growth regulation. Nucleic Acids Res. 2012. 41: 1555-1568.
32. Drissi, H., Luc, Q. Y., Shakoori, R., De Sousa Lopes, S. C., Choi, J. Y., Terry, A., Hu, M. et al., Transcriptional autoregulation of the bone related CBF1/RUNX2 Gene. J. Cell. Physiol. 2000. 184: 341-350.
33. Maunakea, A. K., Nagarajan, R. P., Bilenky, M., Ballinger, T. J., D'Souza, C., Fouse, S. D., Johnson, B. E. et al., Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010. 466: 253-257.
34. Song, F., Smith, J. F., Kimura, M. T., Morrow, A. D., Matsuyama, T., Nagase, H. and Held, W. A., Association of tissue-specific differentially methylated regions (TDMs) with differential gene expression. Proc. Natl. Acad. Sci. U. S. A. 2005. 102: 3336-3341.
35. Webber, B. R., Iacovino, M., Choi, S. H., Tolar, J., Kyba, M. and Blazar, B. R., DNA methylation of Runx1 regulatory regions correlates with transition from primitive to definitive hematopoietic potential in vitro and in vivo. Blood 2013. 122: 2978-2986.
36. Naoe, Y., Setoguchi, R., Akiyama, K., Muroi, S., Kuroda, M., Hatam, F., Littman, D. R. et al., Repression of interleukin-4 in T helper type 1 cells by Runx/Cbf beta binding to the Il4 silencer. J. Exp. Med. 2007. 204: 1749-1755.
37. Morita, S., Kojima, T. and Kitamura, T., Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther. 2000. 7: 1063-1066.
38. Kanto, S., Chiba, N., Tanaka, Y., Fujita, S., Endo, M., Kamada, N., Yoshikawa, K. et al., The PEBP2beta/CBF beta-SMMHC chimeric protein is localized both in the cell membrane and nuclear subfractions of leukemic cells carrying chromosomal inversion 16. Leukemia 2000. 14: 1253-1259.