References
- Bruno, L., Mazzarella, L., Hoogenkamp, M., Hertweck, A., Cobb, B.S., Sauer, S., Hadjur, S., Leleu, M., Naoe, Y., Telfer, J.C., et al. (2009). Runx proteins regulate Foxp3 expression. J. Exp. Med. 206, 2329-2337. https://doi.org/10.1084/jem.20090226
- Cooper, M.A., Elliott, J.M., Keyel, P.A., Yang, L., Carrero, J.A., and Yokoyama, W.M. (2009). Cytokine-induced memory-like natural killer cells. Proc. Natl. Acad. Sci. U. S. A. 106, 1915-1919. https://doi.org/10.1073/pnas.0813192106
- Cruz-Guilloty, F., Pipkin, M.E., Djuretic, I.M., Levanon, D., Lotem, J., Lichtenheld, M.G., Groner, Y., and Rao, A. (2009). Runx3 and T-box proteins cooperate to establish the transcriptional program of effector CTLs. J. Exp. Med. 206, 51-59. https://doi.org/10.1084/jem.20081242
- Djuretic, I.M., Levanon, D., Negreanu, V., Groner, Y., Rao, A., and Ansel, K.M. (2007). Transcription factors T-bet and Runx3 cooperate to activate Ifng and silence Il4 in T helper type 1 cells. Nat. Immunol. 8, 145-153. https://doi.org/10.1038/ni1424
- Egawa, T., Eberl, G., Taniuchi, I., Benlagha, K., Geissmann, F., Hennighausen, L., Bendelac, A., and Littman, D.R. (2005). Genetic evidence supporting selection of the Valpha14i NKT cell lineage from double-positive thymocyte precursors. Immunity 22, 705-716. https://doi.org/10.1016/j.immuni.2005.03.011
- Egawa, T., Tillman, R.E., Naoe, Y., Taniuchi, I., and Littman, D.R. (2007). The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J. Exp. Med. 204, 1945-1957. https://doi.org/10.1084/jem.20070133
- Growney, J.D., Shigematsu, H., Li, Z., Lee, B.H., Adelsperger, J., Rowan, R., Curley, D.P., Kutok, J.L., Akashi, K., Williams, I.R., et al. (2005). Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood 106, 494-504.
- Guo, H. and Friedman, A.D. (2011). Phosphorylation of RUNX1 by cyclindependent kinase reduces direct interaction with HDAC1 and HDAC3. J. Biol. Chem. 286, 208-215. https://doi.org/10.1074/jbc.M110.149013
- Guo, Y., Maillard, I., Chakraborti, S., Rothenberg, E.V., and Speck, N.A. (2008). Core binding factors are necessary for natural killer cell development and cooperate with Notch signaling during T-cell specification. Blood 112, 480-492.
- Ha-Lee, Y.M., Lee, Y., Kim, Y.K., and Sohn, J. (2000). Cross-linking of CD4 induces cytoskeletal association of CD4 and p56lck. Exp. Mol. Med. 32, 18-22. https://doi.org/10.1038/emm.2000.4
- Hanai, J., Chen, L.F., Kanno, T., Ohtani-Fujita, N., Kim, W.Y., Guo, W.H., Imamura, T., Ishidou, Y., Fukuchi, M., Shi, M.J., et al. (1999). Interaction and functional cooperation of PEBP2/CBF with Smads. Synergistic induction of the immunoglobulin germline Calpha promoter. J. Biol. Chem. 274, 31577-31582. https://doi.org/10.1074/jbc.274.44.31577
- Ichikawa, M., Asai, T., Saito, T., Seo, S., Yamazaki, I., Yamagata, T., Mitani, K., Chiba, S., Ogawa, S., Kurokawa, M., et al. (2004). AML-1 is required for megakaryocytic maturation and lymphocytic differentiation, but not for maintenance of hematopoietic stem cells in adult hematopoiesis. Nat. Med. 10, 299-304. https://doi.org/10.1038/nm997
- Ito, Y., Bae, S.C., and Chuang, L.S. (2015). The RUNX family: developmental regulators in cancer. Nat. Rev. Cancer 15, 81-95. https://doi.org/10.1038/nrc3877
- Jin, Y.H., Jeon, E.J., Li, Q.L., Lee, Y.H., Choi, J.K., Kim, W.J., Lee, K.Y., and Bae, S.C. (2004). Transforming growth factor-beta stimulates p300-dependent RUNX3 acetylation, which inhibits ubiquitination-mediated degradation. J. Biol. Chem. 279, 29409-29417. https://doi.org/10.1074/jbc.M313120200
- Kamimura, Y. and Lanier, L.L. (2015). Homeostatic control of memory cell progenitors in the natural killer cell lineage. Cell Rep. 10, 280-291. https://doi.org/10.1016/j.celrep.2014.12.025
- Kim, J.H., Jang, J.W., Lee, Y.S., Lee, J.W., Chi, X.Z., Li, Y.H., Kim, M.K., Kim, D.M., Choi, B.S., Kim, J., et al. (2014). RUNX family members are covalently modified and regulated by PIAS1-mediated sumoylation. Oncogenesis 3, e101. https://doi.org/10.1038/oncsis.2014.15
- Kim, W.Y., Sieweke, M., Ogawa, E., Wee, H.J., Englmeier, U., Graf, T., and Ito, Y. (1999). Mutual activation of Ets-1 and AML1 DNA binding by direct interaction of their autoinhibitory domains. EMBO J. 18, 1609-1620. https://doi.org/10.1093/emboj/18.6.1609
- Kitagawa, Y., Ohkura, N., Kidani, Y., Vandenbon, A., Hirota, K., Kawakami, R., Yasuda, K., Motooka, D., Nakamura, S., Kondo, M., et al. (2017). Guidance of regulatory T cell development by Satb1-dependent super-enhancer establishment. Nat. Immunol. 18, 173-183. https://doi.org/10.1038/ni.3646
- Kitoh, A., Ono, M., Naoe, Y., Ohkura, N., Yamaguchi, T., Yaguchi, H., Kitabayashi, I., Tsukada, T., Nomura, T., Miyachi, Y., et al. (2009). Indispensable role of the Runx1-Cbfbeta transcription complex for in vivosuppressive function of FoxP3+ regulatory T cells. Immunity 31, 609-620. https://doi.org/10.1016/j.immuni.2009.09.003
- Komine, O., Hayashi, K., Natsume, W., Watanabe, T., Seki, Y., Seki, N., Yagi, R., Sukzuki, W., Tamauchi, H., Hozumi, K., et al. (2003). The Runx1 transcription factor inhibits the differentiation of naive CD4+ T cells into the Th2 lineage by repressing GATA3 expression. J. Exp. Med. 198, 51-61. https://doi.org/10.1084/jem.20021200
- Komori, T., Yagi, H., Nomura, S., Yamaguchi, A., Sasaki, K., Deguchi, K., Shimizu, Y., Bronson, R.T., Gao, Y.H., Inada, M., et al. (1997). Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell 89, 755-764. https://doi.org/10.1016/S0092-8674(00)80258-5
- Levanon, D., Bettoun, D., Harris-Cerruti, C., Woolf, E., Negreanu, V., Eilam, R., Bernstein, Y., Goldenberg, D., Xiao, C., Fliegauf, M., et al. (2002). The Runx3 transcription factor regulates development and survival of TrkC dorsal root ganglia neurons. EMBO J. 21, 3454-3463. https://doi.org/10.1093/emboj/cdf370
- Levanon, D., Negreanu, V., Lotem, J., Bone, K.R., Brenner, O., Leshkowitz, D., and Groner, Y. (2014). Transcription factor Runx3 regulates interleukin-15-dependent natural killer cell activation. Mol. Cell. Biol. 34, 1158-1169. https://doi.org/10.1128/MCB.01202-13
- Maier, H., Ostraat, R., Gao, H., Fields, S., Shinton, S.A., Medina, K.L., Ikawa, T., Murre, C., Singh, H., Hardy, R.R., et al. (2004). Early B cell factor cooperates with Runx1 and mediates epigenetic changes associated with mb-1 transcription. Nat. Immunol. 5, 1069-1077. https://doi.org/10.1038/ni1119
- Mandel, E.M. and Grosschedl, R. (2010). Transcription control of early B cell differentiation. Curr. Opin. Immunol. 22, 161-167. https://doi.org/10.1016/j.coi.2010.01.010
- Milner, J.J., Toma, C., Yu, B., Zhang, K., Omilusik, K., Phan, A.T., Wang, D., Getzler, A.J., Nguyen, T., Crotty, S., et al. (2017). Runx3 programs CD8(+) T cell residency in non-lymphoid tissues and tumours. Nature 552, 253-257. https://doi.org/10.1038/nature24993
- Mucida, D., Husain, M.M., Muroi, S., van Wijk, F., Shinnakasu, R., Naoe, Y., Reis, B.S., Huang, Y., Lambolez, F., Docherty, M., et al. (2013). Transcriptional reprogramming of mature CD4(+) helper T cells generates distinct MHC class II-restricted cytotoxic T lymphocytes. Nat. Immunol. 14, 281-289. https://doi.org/10.1038/ni.2523
- Mundlos, S., Otto, F., Mundlos, C., Mulliken, J.B., Aylsworth, A.S., Albright, S., Lindhout, D., Cole, W.G., Henn, W., Knoll, J.H., et al. (1997). Mutations involving the transcription factor CBFA1 cause cleidocranial dysplasia. Cell 89, 773-779. https://doi.org/10.1016/S0092-8674(00)80260-3
- Nieke, S., Yasmin, N., Kakugawa, K., Yokomizo, T., Muroi, S., and Taniuchi, I. (2017). Unique N-terminal sequences in two Runx1 isoforms are dispensable for Runx1 function. BMC Dev. Biol. 17, 14. https://doi.org/10.1186/s12861-017-0156-y
- O’Sullivan, T.E., Sun, J.C., and Lanier, L.L. (2015). Natural killer cell memory. Immunity 43, 634-645. https://doi.org/10.1016/j.immuni.2015.09.013
- Ohno, S., Sato, T., Kohu, K., Takeda, K., Okumura, K., Satake, M., and Habu, S. (2008). Runx proteins are involved in regulation of CD122, Ly49 family and IFN-gamma expression during NK cell differentiation. Int. Immunol. 20, 71-79. https://doi.org/10.1093/intimm/dxm120
- Okuda, T., van Deursen, J., Hiebert, S.W., Grosveld, G., and Downing, J.R. (1996). AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321-330. https://doi.org/10.1016/S0092-8674(00)80986-1
- Ono, M., Yaguchi, H., Ohkura, N., Kitabayashi, I., Nagamura, Y., Nomura, T., Miyachi, Y., Tsukada, T., and Sakaguchi, S. (2007). Foxp3 controls regulatory T-cell function by interacting with AML1/Runx1. Nature 446, 685-689. https://doi.org/10.1038/nature05673
- Otto, F., Thornell, A.P., Crompton, T., Denzel, A., Gilmour, K.C., Rosewell, I.R., Stamp, G.W., Beddington, R.S., Mundlos, S., Olsen, B.R., et al. (1997). Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell 89, 765-771. https://doi.org/10.1016/S0092-8674(00)80259-7
- Pardali, E., Xie, X.Q., Tsapogas, P., Itoh, S., Arvanitidis, K., Heldin, C.H., ten Dijke, P., Grundstrom, T., and Sideras, P. (2000). Smad and AML proteins synergistically confer transforming growth factor beta1 responsiveness to human germ-line IgA genes. J. Biol. Chem. 275, 3552-3560. https://doi.org/10.1074/jbc.275.5.3552
- Park, J.H., Adoro, S., Guinter, T., Erman, B., Alag, A.S., Catalfamo, M., Kimura, M.Y., Cui, Y., Lucas, P.J., Gress, R.E., et al. (2010). Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat. Immunol. 11, 257-264. https://doi.org/10.1038/ni.1840
- Pham, D., Vincentz, J.W., Firulli, A.B., and Kaplan, M.H. (2012). Twist1 regulates Ifng expression in Th1 cells by interfering with Runx3 function. J. Immunol. 189, 832-840. https://doi.org/10.4049/jimmunol.1200854
-
Rapp, M., Lau, C.M., Adams, N.M., Weizman, O.E., O'Sullivan, T.E., Geary, C.D., and Sun, J.C. (2017). Core-binding factor
${\beta}$ and Runx transcription factors promote adaptive natural killer cell responses. Sci. Immunol. 2, eaan3796. https://doi.org/10.1126/sciimmunol.aan3796 - Reis, B.S., Rogoz, A., Costa-Pinto, F.A., Taniuchi, I., and Mucida, D. (2013). Mutual expression of the transcription factors Runx3 and ThPOK regulates intestinal CD4(+) T cell immunity. Nat. Immunol. 14, 271-280. https://doi.org/10.1038/ni.2518
- Rudra, D., Egawa, T., Chong, M.M., Treuting, P., Littman, D.R., and Rudensky, A.Y. (2009). Runx-CBFbeta complexes control expression of the transcription factor Foxp3 in regulatory T cells. Nat. Immunol. 10, 1170-1177. https://doi.org/10.1038/ni.1795
- Sakaguchi, S., Hainberger, D., Tizian, C., Tanaka, H., Okuda, T., Taniuchi, I., and Ellmeier, W. (2015). MAZR and Runx factors synergistically repress ThPOK during CD8+ T cell lineage development. J. Immunol. 195, 2879-2887. https://doi.org/10.4049/jimmunol.1500387
- Sakaguchi, S., Hombauer, M., Bilic, I., Naoe, Y., Schebesta, A., Taniuchi, I., and Ellmeier, W. (2010). The zinc-finger protein MAZR is part of the transcription factor network that controls the CD4 versus CD8 lineage fate of double-positive thymocytes. Nat. Immunol. 11, 442-448. https://doi.org/10.1038/ni.1860
- Sellars, M., Huh, J.R., Day, K., Issuree, P.D., Galan, C., Gobeil, S., Absher, D., Green, M.R., and Littman, D.R. (2015). Regulation of DNA methylation dictates Cd4 expression during the development of helper and cytotoxic T cell lineages. Nat. Immunol. 16, 746-754. https://doi.org/10.1038/ni.3198
- Seo, W., Ikawa, T., Kawamoto, H., and Taniuchi, I. (2012). Runx1-Cbfbeta facilitates early B lymphocyte development by regulating expression of Ebf1. J. Exp. Med. 209, 1255-1262. https://doi.org/10.1084/jem.20112745
- Seo, W., Muroi, S., Akiyama, K., and Taniuchi, I. (2017). Distinct requirement of Runx complexes for TCRbeta enhancer activation at distinct developmental stages. Sci. Rep. 7, 41351. https://doi.org/10.1038/srep41351
- Setoguchi, R., Tachibana, M., Naoe, Y., Muroi, S., Akiyama, K., Tezuka, C., Okuda, T., and Taniuchi, I. (2008). Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development. Science 319, 822-825. https://doi.org/10.1126/science.1151844
- Shi, M.J. and Stavnezer, J. (1998). CBF alpha3 (AML2) is induced by TGFbeta1 to bind and activate the mouse germline Ig alpha promoter. J. Immunol. 161, 6751-6760.
- Stavnezer, J. and Kang, J. (2009). The surprising discovery that TGF beta specifically induces the IgA class switch. J. Immunol. 182, 5-7. https://doi.org/10.4049/jimmunol.182.1.5
- Sun, G., Liu, X., Mercado, P., Jenkinson, S.R., Kypriotou, M., Feigenbaum, L., Galera, P., and Bosselut, R. (2005). The zinc finger protein cKrox directs CD4 lineage differentiation during intrathymic T cell positive selection. Nat. Immunol. 6, 373-381. https://doi.org/10.1038/ni1183
- Sun, J.C., Madera, S., Bezman, N.A., Beilke, J.N., Kaplan, M.H., and Lanier, L.L. (2012). Proinflammatory cytokine signaling required for the generation of natural killer cell memory. J. Exp. Med. 209, 947-954. https://doi.org/10.1084/jem.20111760
- Taniuchi, I., Osato, M., Egawa, T., Sunshine, M.J., Bae, S.C., Komori, T., Ito, Y., and Littman, D.R. (2002). Differential requirements for Runx proteins in CD4 repression and epigenetic silencing during T lymphocyte development. Cell 111, 621-633. https://doi.org/10.1016/S0092-8674(02)01111-X
- Tenno, M., Kojo, S., Lawir, D.F., Hess, I., Shiroguchi, K., Ebihara, T., Endo, T.A., Muroi, S., Satoh, R., Kawamoto, H., et al. (2018). Cbfbeta2 controls differentiation of and confers homing capacity to prethymic progenitors. J. Exp. Med. 215, 595-610. https://doi.org/10.1084/jem.20171221
- Tenno, M., Shiroguchi, K., Muroi, S., Kawakami, E., Koseki, K., Kryukov, K., Imanishi, T., Ginhoux, F., and Taniuchi, I. (2017). Cbfbeta2 deficiency preserves Langerhans cell precursors by lack of selective TGFbeta receptor signaling. J. Exp. Med. 214, 2933-2946. https://doi.org/10.1084/jem.20170729
- Thapa, P., Manso, B., Chung, J.Y., Romera Arocha, S., Xue, H.H., Angelo, D.B.S., and Shapiro, V.S. (2017). The differentiation of ROR-gammat expressing iNKT17 cells is orchestrated by Runx1. Sci. Rep. 7, 7018. https://doi.org/10.1038/s41598-017-07365-8
- Tsagaratou, A., Aijo, T., Lio, C.W., Yue, X., Huang, Y., Jacobsen, S.E., Lahdesmaki, H., and Rao, A. (2014). Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc. Natl. Acad. Sci. U. S. A. 111, E3306-E3315. https://doi.org/10.1073/pnas.1412327111
- Vivier, E., Raulet, D.H., Moretta, A., Caligiuri, M.A., Zitvogel, L., Lanier, L.L., Yokoyama, W.M., and Ugolini, S. (2011). Innate or adaptive immunity? The example of natural killer cells. Science 331, 44-49. https://doi.org/10.1126/science.1198687
- Wang, D., Diao, H., Getzler, A.J., Rogal, W., Frederick, M.A., Milner, J., Yu, B., Crotty, S., Goldrath, A.W., and Pipkin, M.E. (2018). The transcription factor Runx3 establishes chromatin accessibility of cis-regulatory landscapes that drive memory cytotoxic t lymphocyte formation. Immunity 48, 659-674.e6. https://doi.org/10.1016/j.immuni.2018.03.028
- Wang, Q., Stacy, T., Binder, M., Marin-Padilla, M., Sharpe, A.H., and Speck, N.A. (1996a). Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. U. S. A. 93, 3444-3449. https://doi.org/10.1073/pnas.93.8.3444
- Wang, Q., Stacy, T., Miller, J.D., Lewis, A.F., Gu, T.L., Huang, X., Bushweller, J.H., Bories, J.C., Alt, F.W., Ryan, G., et al. (1996b). The CBFbeta subunit is essential for CBFalpha2 (AML1) function in vivo. Cell 87, 697-708. https://doi.org/10.1016/S0092-8674(00)81389-6
- Wang, Y., Godec, J., Ben-Aissa, K., Cui, K., Zhao, K., Pucsek, A.B., Lee, Y.K., Weaver, C.T., Yagi, R., and Lazarevic, V. (2014). The transcription factors T-bet and Runx are required for the ontogeny of pathogenic interferongamma-producing T helper 17 cells. Immunity 40, 355-366. https://doi.org/10.1016/j.immuni.2014.01.002
- Watanabe, K., Sugai, M., Nambu, Y., Osato, M., Hayashi, T., Kawaguchi, M., Komori, T., Ito, Y., and Shimizu, A. (2010). Requirement for Runx proteins in IgA class switching acting downstream of TGF-beta 1 and retinoic acid signaling. J. Immunol. 184, 2785-2792. https://doi.org/10.4049/jimmunol.0901823
- Woolf, E., Brenner, O., Goldenberg, D., Levanon, D., and Groner, Y. (2007). Runx3 regulates dendritic epidermal T cell development. Dev. Biol. 303, 703-714. https://doi.org/10.1016/j.ydbio.2006.12.005
- Xing, S., Shao, P., Li, F., Zhao, X., Seo, W., Wheat, J.C., Ramasamy, S., Wang, J., Li, X., Peng, W., et al. (2018). Tle corepressors are differentially partitioned to instruct CD8(+) T cell lineage choice and identity. J. Exp. Med. 215, 2211-2226. https://doi.org/10.1084/jem.20171514
- Zeidan, N., Damen, H., Roy, D.C., and Dave, V.P. (2019). Critical role for TCR signal strength and MHC specificity in ThPOK-Induced CD4 helper lineage choice. J. Immunol. 202, 3211-3225. https://doi.org/10.4049/jimmunol.1801464
- Zhang, F., Meng, G., and Strober, W. (2008). Interactions among the transcription factors Runx1, RORgammat and Foxp3 regulate the differentiation of interleukin 17-producing T cells. Nat. Immunol. 9, 1297-1306. https://doi.org/10.1038/ni.1663
- Zhang, Y. and Derynck, R. (2000). Transcriptional regulation of the transforming growth factor-beta-inducible mouse germ line Ig alpha constant region gene by functional cooperation of Smad, CREB, and AML family members. J. Biol. Chem. 275, 16979-16985. https://doi.org/10.1074/jbc.M001526200
- Zhao, X., Jankovic, V., Gural, A., Huang, G., Pardanani, A., Menendez, S., Zhang, J., Dunne, R., Xiao, A., Erdjument-Bromage, H., et al. (2008). Methylation of RUNX1 by PRMT1 abrogates SIN3A binding and potentiates its transcriptional activity. Genes Dev. 22, 640-653. https://doi.org/10.1101/gad.1632608
- Zheng, Y., Josefowicz, S., Chaudhry, A., Peng, X.P., Forbush, K., and Rudensky, A.Y. (2010). Role of conserved non-coding DNA elements in the Foxp3 gene in regulatory T-cell fate. Nature 463, 808-812. https://doi.org/10.1038/nature08750
Cited by
- Runx Transcription Factors in T Cells-What Is Beyond Thymic Development? vol.12, 2020, https://doi.org/10.3389/fimmu.2021.701924
- IPEX Syndrome: Genetics and Treatment Options vol.12, pp.3, 2020, https://doi.org/10.3390/genes12030323
- Runx1 shapes the chromatin landscape via a cascade of direct and indirect targets vol.17, pp.6, 2020, https://doi.org/10.1371/journal.pgen.1009574
- The Multiple Interactions of RUNX with the Hippo-YAP Pathway vol.10, pp.11, 2020, https://doi.org/10.3390/cells10112925
- Expression patterns and prognostic value of RUNX genes in kidney cancer vol.11, pp.1, 2020, https://doi.org/10.1038/s41598-021-94294-2
- RUNX1 Regulates a Transcription Program That Affects the Dynamics of Cell Cycle Entry of Naive Resting B Cells vol.207, pp.12, 2021, https://doi.org/10.4049/jimmunol.2001367