GATA-3 dose-dependent checkpoints in early T cell commitment

Journal of Immunology

Volumn 193, Issue 7, 2014, Pages 3470-3491

  Scripture Adams, Deirdre D ^a,b   Damle, Sagar S ^a,c   Li, Long ^a,d   Elihu, Koorosh J ^a,e   Qin, Shuyang ^a   Arias, Alexandra M ^a   Butler, Robert R ^a,f   Champhekar, Ameya ^a,b   Zhang, Jingli A ^a,g   Rothenberg, Ellen V ^a  

^a California Institute of Technology   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c ISIS PHARMACEUTICALS   (United States)

^d TIANJIN MEDICAL UNIVERSITY   (China)

^e HARBOR UCLA MEDICAL CENTER   (United States)

^f ILLINOIS INSTITUTE OF TECHNOLOGY   (United States)

^g GENENTECH INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 9 RECEPTOR; NOTCH RECEPTOR; PROTEIN BCL 2; SHORT HAIRPIN RNA; TAMOXIFEN; TRANSCRIPTION FACTOR ETS 1; TRANSCRIPTION FACTOR GATA 3; ANTINEOPLASTIC HORMONE AGONISTS AND ANTAGONISTS; BCL11B PROTEIN, MOUSE; BCL2 PROTEIN, MOUSE; GATA3 PROTEIN, MOUSE; REPRESSOR PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE DIFFERENTIATION; BCL 2 GENE; BCL11A GENE; BCL11B GENE; BONE MARROW CELL; CELL CYCLE CHECKPOINT; CELL EXPANSION; CELL LINEAGE; CELL MATURATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CPA3 GENE; EMBRYO; ETS1 GENE; FEMALE; FETUS; GATA3 GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; GROWTH INHIBITION; IL17RB GENE; IL9R GENE; IMMUNOPHENOTYPING; IN VITRO STUDY; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RNA INTERFERENCE; RNA SEQUENCE; SPI1 GENE; T CELL COMMITTMENT; T LYMPHOCYTE; ZFPM1 GENE; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECT; GENETICS; IMMUNOLOGY; PRE T LYMPHOCYTE; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS, HORMONAL; CELL LINE; GATA3 TRANSCRIPTION FACTOR; MICE; MYELOID CELLS; PRECURSOR CELLS, T-LYMPHOID; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, NOTCH; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TAMOXIFEN; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84907222575     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301663     Document Type: Article

References (55)

1. Pandolfi, P. P., M. E. Roth, A. Karis, M. W. Leonard, E. Dzierzak, F. G. Grosveld, J. D. Engel, and M. H. Lindenbaum. 1995. Targeted disruption of the GATA3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nat. Genet. 11: 40-44.
2. Ting, C. N., M. C. Olson, K. P. Barton, and J. M. Leiden. 1996. Transcription factor GATA-3 is required for development of the T-cell lineage. Nature 384: 474-478.
3. Hendriks, R. W., M. C. Nawijn, J. D. Engel, H. van Doorninck, F. Grosveld, and A. Karis. 1999. Expression of the transcription factor GATA-3 is required for the development of the earliest T cell progenitors and correlates with stages of cellular proliferation in the thymus. Eur. J. Immun ol. 29: 1912-1918.
4. Vosshenrich, C. A., M. E. Garcia-Ojeda, S. I. Samson-Villeger, V. Pasqualetto, L. Enault, O. Richard-Le Goff, E. Corcuff, D. Guy-Grand, B. Rocha, A. Cumano, et al. 2006. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 7: 1217-1224.
5. Samson, S. I., O. Richard, M. Tavian, T. Ranson, C. A. Vosshenrich, F. Colucci, J. Buer, F. Grosveld, I. Godin, and J. P. Di Santo. 2003. GATA-3 promotes maturation, IFN-g production, and liver-specific homing of NK cells. Immunity 19: 701-711.
6. Hattori, N., H. Kawamoto, S. Fujimoto, K. Kuno, and Y. Katsura. 1996. Involvement of transcription factors TCF-1 and GATA-3 in the initiation of the earliest step of T cell development in the thymus. J. Exp. Med. 184: 1137-1147.
7. Hosoya, T., T. Kuroha, T. Moriguchi, D. Cummings, I. Maillard, K. C. Lim, and J. D. Engel. 2009. GATA-3 is required for early T lineage progenitor development. J. Exp. Med. 206: 2987-3000.
8. Ku, C. J., T. Hosoya, I. Maillard, and J. D. Engel. 2012. GATA-3 regulates hematopoietic stem cell maintenance and cell-cycle entry. Blood 119: 2242-2251.
9. Bu za-Vidas, N., S. Duarte, S. Luc, T. Bouriez-Jones, P. S. Woll, and S. E. Jacobsen. 2011. GATA3 is redundant for maintenance and self-renewal of hematopoietic stem cells. Blood 118: 1291-1293.
10. Pai, S. Y., M. L. Truitt, C. N. Ting, J. M. Leiden, L. H. Glimcher, and I. C. Ho. 2003. Critical roles for transcription factor GATA-3 in thymocyte development. Immunity 19: 863-875.
11. Garcí a-Ojeda, M. E., R. G. Klein Wolterink, F. Lemaître, O. Richard-Le Goff, M. Hasan, R. W. Hendriks, A. Cumano, and J. P. Di Santo. 2013. GATA-3 promotes T cell specification by repressing B cell pot ential in pro-T cells in mice. Blood 121: 1749-1759.
12. Wei, G., B. J. Abraham, R. Yagi, R. Jothi, K. Cui, S. Sharma, L. Narlikar, D. L. Northrup, Q. Tang, W. E. Paul, et al. 2011. Genome-wide analyses of transcription factor GATA3-mediated gene regulation in distinct T cell types. Immunity 35: 299-311.
13. Zhang, J. A., A. Mortazavi, B. A. Williams, B. J. Wold, and E. V. Rothenberg. 2012. Dynamic transformations of genome-wide epigenetic marking and transcriptional control establish T cell identity. Cell 149: 467-482.
14. Taghon, T., M. A. Yui, and E. V. Rothenberg. 2007. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat. Immunol. 8: 845-855.
15. Schmitt T.M.,J.C. Zún?iga-Pflücker. 2002. Induction of T cell development from hematopoietic progenitor cells by Delta-like-1 in vitro. Immunity. 17: 749-756.
16. Taghon, T. N., E. S. David, J. C. Zún?iga-Pflücker, and E. V. Rothenberg. 2005. Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev. 19: 965-978.
17. Strasser, A., A. W. Harris, and S. Cory. 1991. bcl-2 transgene inhibits T cell death and perturbs thymic self-censorship. Cell 67: 889-899.
18. Srinivas, S., T. Watanabe, C. S. Lin, C. M. William, Y. Tanabe, T. M. Jessell, and F. Costantini. 2001. Cre reporter strains produced by targeted insertion of EYFP and ECFP into the ROSA26 locus. BMC Dev. Biol. 1: 4.
19. Nutt, S. L., D. Metcalf, A. D'Amico, M. Polli, and L. Wu. 2005. Dynamic regulation of PU.1 expression in multipotent hematopoietic progenitors. J. Exp. Med. 201: 221-231.
20. Li, L., M. Leid, and E. V. Rothenberg. 2010. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 329: 89-93.
21. Li, P., S. Burke, J. Wang, X. Chen, M. Ortiz, S. C. Lee, D. Lu, L. Campos, D. Goulding, B. L. Ng, et al. 2010. Reprogramming of T cells to natura l killerlike cells upon Bcl11b deletion. Science 329: 85-89.
22. Carleton, M., N. R. Ruetsch, M. A. Berger, M. Rhodes, S. Kaptik, and D. L. Wiest. 1999. Signals transduced by CD3ε, but no t by surface pre-TCR complexes, are able to induce maturation of an early thymic lymphoma in vitro. J. Immunol. 163: 2576-2585.
23. Dionne, C. J., K. Y. Tse, A. H. Weiss, C. B. Franco, D. L. Wiest, M. K. Anderson, and E. V. Rothenberg. 2005. Subversion of T lineage commitment by PU.1 in a clonal cell line system. Dev. Biol. 280: 448-466.
24. Mohtashami, M., D. K. Shah, H. Nakase, K. Kianizad, H. T. Petrie, and J. C. Zún?iga-Pfl€ ucker. 2010. Direct comparison of Dll1-and Dll4-mediated Notch activation levels shows differential lymphomyeloid lineage commitment outcomes. J. Immunol. 185: 867-876.
25. Franco, C. B., D. D. Scripture-Adams, I. Proekt, T. Taghon, A. H. Weiss, M. A. Yui, S. L. Adams, R. A. Diamond, and E. V. Rothenberg. 2006. Notch/Delta signaling constrains reengineering of pro-T cells by PU.1. Proc. Natl. Acad. Sci. USA 103: 11993-11998.
26. Hernandez-Hoyos, G., M. K. Anderson, C. Wang, E. V. Rothenberg, and J. Alberola-Ila. 2003. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 19: 83-94.
27. Hernandez-Hoyos, G., and J. Alberola-Ila. 200 5. Analysis of T-cell development by using short interfering RNA to knock down protein expression. Methods Enzymol. 392: 199-217.
28. Anderson, M. K., G. Hernandez-Hoyos, C. J. Dionne, A. M. Arias, D. Chen, and E. V. Rothenberg. 2002. Definition of regulatory network elements for T cell development by perturbation analysis with PU.1 and GATA-3. Dev. Biol. 246: 103-121.
29. Kurata, H., H. J. Lee, A. O'Garra, and N. Arai. 1999. Ectopic expression of activated Stat6 induces the expression of Th2-specific cytokines and transcription factors in developing Th1 cells. Immunity 11: 677-688.
30. Zarn egar, M. A., J. Chen, and E. V. Rothenberg. 2010. Cell-type-specific activation and repression of PU.1 by a complex of discrete, functionally specialized cis-regulatory elements. Mol. Cell. Biol. 30: 4922-4939.
31. David-Fung, E. S., R. Butler, G. Buzi, M. A. Yui, R. A. Diamond, M. K. Anderson, L. Rowen, and E. V. Rothenberg. 2009. Transcription factor expression dynamics of early T-lymphocyte specification and commitm ent. Dev. Biol. 325: 444-467.
32. Trapnell, C., D. G. Hendrickson, M. Sauvageau, L. Goff, J. L. Rinn, and L. Pachter. 2013. Differential analysis of gene regulation at transcript resolution with RNA-seq. Na t. Biotechnol. 31: 46-53.
33. Breitling, R., P. Armengaud, A. Amtmann, and P. Herzyk. 2004. Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated mic roarray experiments. FEBS Lett. 573: 83-92.
34. Igarashi, H., S. C. Gregory, T. Yokota, N. Sakaguchi, and P. W. Kincade. 2002. Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17: 117-130.
35. Tydell, C. C., E. S. David-Fung, J. E. Moore, L. Rowen, T. Taghon, and E. V. Rothenberg. 2007. Molecular dissection of prethymic prog enitor entry into the T lymphocyte developmental pathway. J. Immunol. 179: 421-438.
36. Tabrizifard, S., A. Olaru, J. Plotkin, M. Fallahi-Sichani, F. Livak, and H. T. Petrie. 2004. Analysis of transcription factor expression during discrete stages of postnatal thymocyte differentiation. J. Immunol. 173: 1094-1102.
37. Shinnakasu, R., M. Yamashita, M. Kuwahara, H. Hosokawa, A. Hasegawa, S. Motohashi, and T. Nakayama. 2008. Gfi1-mediated stabilization of GATA3 protein is required for Th2 cell differentiation. J. Biol. Chem. 283: 28216-28225.
38. Maneechotesuwan, K., Y. Xin, K. Ito, E. Jazrawi, K. Y. Lee, O. S. Usmani, P. J. Barnes, and I. M. Adcock. 2007. Regulation of Th2 cytokine genes by p38 MAPK-mediated phosphorylation of GATA-3. J. Immunol. 178: 2491-2498.
39. Cook, K. D., and J. Miller. 2010. TCR-dependent translational control of GATA-3 enhances Th2 differentiation. J. Immunol. 185: 3209-3216.
40. Gimferrer, I., T. Hu, A. Simmons, C. Wang, A. Souabni, M. Busslinger, T. P. Bender, G. Hernandez-Hoyos, and J. Alberola-Ila. 2011. Regulation of GATA-3 expression during CD4 lineage differentiation. J. Immunol. 186: 3892-3898.
41. Fre lin, C., R. Herrington, S. Janmohamed, M. Barbara, G. Tran, C. J. Paige, P. Benveniste, J. C. Zún?iga-Pflücker, A. Souabni, M. Busslinger, and N. N. Iscove. 2013. GATA-3 regulates the self-renewal of long-term hematopoietic stem cells. Nat. Immunol. 14: 1037-1044.
42. Yui, M. A., N. Feng, and E. V. Rothenberg. 2010. Fine-scale staging of T cell lineage commitment in adult mouse thymus. J. Immunol. 185: 284-293.
43. Del Real, M. M., and E. V. Rothenberg. 2013. Architecture of a lymphomyeloid developmental switch controlled by PU.1, Notch, and GATA-3. Development 140: 1207-1219.
44. Xu, W., T. Carr, K. Ramirez, S. McGregor, M. Sigvardsson, and B. L. Kee. 2013. E2A transcription factors limit expression of Gata3 to facilitate T lymphocyte lineage commitment. Blood 121: 1534-1542.
45. Kim, D. H., and J. J. Rossi. 2009. Overview of gene silencing by RNA interference. Curr. Protoc. Nucleic Acid Chem. Chapter 16: Unit 16.1. doi:10.1002/0471142700.nc1601s36
46. Wang, D., C. L. Claus, G. Vaccarelli, M. Braunstein, T. M. Schmitt, J. C. Zún?iga-Pflücker, E. V. Rothenberg, and M. K. Anderson. 2006. The basic helix-loophelix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J. Immunol. 177: 109-119.
47. Yagi, R., C. Zhong, D. L. Northrup, F. Yu, N. Bouladoux, S. Spencer, G. Hu, L. Barron, S. Sharma, T. Nakayama, et al. 2014. The transcription factor GATA3 is critical for the development of all IL-7Ra-expressing innate lymphoid cells. Immunity 40: 378-388.
48. Sasaki, T., A. Onodera, H. Hosokawa, Y. Watanabe, S. Horiuchi, J. Yamashita, H. Tanaka, Y. Ogawa, Y. Suzuki, and T. Nakayama. 2013. Genome-wide gene expression profiling revealed a critical role for GATA3 in the maintenance of the Th2 cell identity. PLoS ONE 8: e66468.
49. Mahata, B., X. Zhang, A. A. Kolodziejczyk, V. Proserpio, L. Haim-Vilmovsky, A. E. Taylor, D. Hebenstreit, F. A. Dingler, V. Moignard, B. Göttgens, et al. 2014. Single-cell RNA sequencing reveals T helper cells synthesizing steroids de novo to contribute to immune homeostasis. Cell Reports 7: 1130-1142.
50. Ikawa, T., S. Hirose, K. Masuda, K. Kakugawa, R. Satoh, A. Shibano-Satoh, R. Kominami, Y. Katsura, and H. Kawamoto. 2010. An essential developmental checkpoint for production of the T cell lineage. Science 329: 93-96.
51. Heinzel, K., C. Benz, V. C. Martins, I. D. Haidl, and C. C. Bleul. 2007. Bone marrow-derived hemopoietic precursors commit to the T cell lineage only after arrival in the thymic microenvironment. J. Immunol. 178: 858-868.
52. Rothenberg, E. V. 2011 . T cell lineage commitment: identity and renunciation. J. Immunol. 186: 6649-6655.
53. Klein Wolterink, R. G., M. E. Garcia-Ojeda, C. A. Vosshenrich, R. W. Hendriks, and J. P. Di Santo. 2010. The intrathymic crossroads of T and NK cell differentiation. Immunol. Rev. 238: 126-137.
54. Yang, Q., J. Jeremiah Bell, and A. Bhandoola. 2010. T-cell lineage determination. Immunol. Rev. 238: 12-22.
55. Dontje, W., R. Schotte, T. Cupedo, M. Nagasawa, F. Scheeren, R. Gimeno, H. Spits, and B. Blom. 2006. Delta-like1-induced Notch1 signalling regulates t he human plasmacytoid dendritic cell versus T cell lineage decision through control of GATA-3 and Spi-B. Blood 107: 2446-2452.