Zbtb16 (PLZF) is stably suppressed and not inducible in non-innate T cells via T cell receptor-mediated signaling

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Zhang, Sai ^a,b   Laouar, Amale ^a,b   Denzin, Lisa K ^a,b   Sant'Angelo, Derek B ^a,b  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b CHILD HEALTH INSTITUTE OF NEW JERSEY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KRUPPEL LIKE FACTOR; LYMPHOCYTE ANTIGEN RECEPTOR; ZBTB16 PROTEIN, MOUSE;

ANIMAL; CYTOLOGY; METABOLISM; MOUSE; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMUS;

ANIMALS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84937604065     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep12113     Document Type: Article

References (51)

1. Beaulieu, A. M. & Sant'Angelo, D. B. The BTB-ZF family of transcription factors: key regulators of lineage commitment and effector function development in the immune system. J. Immunol. 187, 2841-2847 (2011).
2. Jenkinson, S. R. et al. Expression of the transcription factor cKrox in peripheral CD8 T cells reveals substantial postthymic plasticity in CD4-CD8 lineage differentiation. J. Exp. Med. 204, 267-272 (2007).
3. 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).
4. Savage, A. K. et al. The transcription factor PLZF directs the effector program of the NKT cell lineage. Immunity 29, 391-403 (2008).
5. Zhao, J., Weng, X., Bagchi, S. & Wang, C. R. Polyclonal type II natural killer T cells require PLZF and SAP for their development and contribute to CpG-mediated antitumor response. Proc. Natl. Acad. Sci. USA 111, 2674-2679 (2014).
6. Alonzo, E. S. et al. Development of promyelocytic zinc finger and ThPOK-expressing innate gamma delta T cells is controlled by strength of TCR signaling and Id3. J. Immunol. 184, 1268-1279 (2010).
7. Constantinides, M. G., McDonald, B. D., Verhoef, P. A. & Bendelac, A. A committed precursor to innate lymphoid cells. Nature 508, 397-401 (2014).
8. Martin, E. et al. Stepwise development of MAIT cells in mouse and human. PLoS Biol. 7, e54 (2009).
9. Eidson, M. et al. Altered development of NKT cells, gammadelta T cells, CD8 T cells and NK cells in a PLZF deficient patient. PLoS ONE 6, e24441 (2011).
10. Bendelac, A., Savage, P. B. & Teyton, L. The biology of NKT cells. Annu. Rev. Immunol. 25, 297-336 (2007).
11. Godfrey, D. I., Stankovic, S. & Baxter, A. G. Raising the NKT cell family. Nat. Immunol. 11, 197-206 (2010).
12. Subleski, J. J., Jiang, Q., Weiss, J. M. & Wiltrout, R. H. The split personality of NKT cells in malignancy, autoimmune and allergic disorders. Immunother 3, 1167-1184 (2011).
13. Albacker, L. A. et al. Invariant natural killer T cells recognize a fungal glycosphingolipid that can induce airway hyperreactivity. Nat. Med. 19, 1297-1304 (2013).
14. Chang, Y. J., DeKruyff, R. H. & Umetsu, D. T. The role of type 2 innate lymphoid cells in asthma. J. Leukoc. Biol. 94, 933-940 (2013).
15. Kovalovsky, D. et al. PLZF induces the spontaneous acquisition of memory/effector functions in T cells independently of NKT cell-related signals. J. Immunol. 184, 6746-6755 (2010).
16. Raberger, J. et al. The transcriptional regulator PLZF induces the development of CD44 high memory phenotype T cells. Proc. Natl. Acad. Sci. USA 105, 17919-17924 (2008).
17. 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).
18. 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).
19. Verykokakis, M. et al. Essential functions for ID proteins at multiple checkpoints in invariant NKT cell development. J. Immunol. 191, 5973-5983 (2013).
20. Zhang, B., Lin, Y. Y., Dai, M. & Zhuang, Y. Id3 and Id2 act as a dual safety mechanism in regulating the development and population size of innate-like gammadelta T cells. J. Immunol. 192, 1055-1063 (2014).
21. Hu, T. et al. Increased level of E protein activity during invariant NKT development promotes differentiation of invariant NKT2 and invariant NKT17 subsets. J. Immunol. 191, 5065-5073 (2013).
22. D'Cruz, L. M., Stradner, M. H., Yang, C. Y. & Goldrath, A. W. E and id proteins influence invariant NKT cell sublineage differentiation and proliferation. J. Immunol. 192, 2227-2236 (2014).
23. 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).
24. Kreslavsky, T. et al. TCR-inducible PLZF transcription factor required for innate phenotype of a subset of gammadelta T cells with restricted TCR diversity. Proc. Natl. Acad. Sci. USA 106, 12453-12458 (2009).
25. 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).
26. Zhu, L. et al. A transgenic TCR directs the development of IL-4+ and PLZF+ innate CD4 T cells. J. Immunol. 191, 737-744 (2013).
27. Thapa, P. et al. The transcriptional repressor NKAP is required for the development of iNKT cells. Nat. Commun. 4, 1582 (2013).
28. Nichols, K. E. et al. Regulation of NKT cell development by SAP, the protein defective in XLP. Nat. Med. 11, 340-345 (2005).
29. Griewank, K. et al. Homotypic interactions mediated by Slamf1 and Slamf6 receptors control NKT cell lineage development. Immunity 27, 751-762 (2007).
30. Domen, J., Gandy, K. L. & Weissman, I. L. Systemic overexpression of BCL-2 in the hematopoietic system protects transgenic mice from the consequences of lethal irradiation. Blood 91, 2272-2282 (1998).
31. Vaux, D. L., Cory, S. & Adams, J. M. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335, 440-442 (1988).
32. 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).
33. Bendelac, A., Rivera, M. N., Park, S. H. & Roark, J. H. Mouse CD1-specific NK1 T cells: development, specificity, and function. Annu. Rev. Immunol. 15, 535-562 (1997).
34. MacDonald, H. R. & Mycko, M. P. Development and selection of Valpha l4i NKT cells. Curr. Top. Microbiol. Immunol. 314, 195-212 (2007).
35. 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).
36. Murphy, K. M., Heimberger, A. B. & Loh, D. Y. Induction by antigen of intrathymic apoptosis of CD4+ CD8+ TCRlo thymocytes in vivo. Science 250, 1720-1723 (1990).
37. Liu, C. P., Kappler, J. W. & Marrack, P. Thymocytes can become mature T cells without passing through the CD4+ CD8+ , double-positive stage. J. Exp. Med. 184, 1619-1630 (1996).
38. Zhou, L., Chong, M. M. & Littman, D. R. Plasticity of CD4+ T cell lineage differentiation. Immunity 30, 646-655 (2009).
39. Mucida, D. et al. Transcriptional reprogramming of mature CD4(+ ) helper T cells generates distinct MHC class II-restricted cytotoxic T lymphocytes. Nat. Immunol. 14, 281-289 (2013).
40. 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).
41. Felices, M., Yin, C. C., Kosaka, Y., Kang, J. & Berg, L. J. Tec kinase Itk in gammadeltaT cells is pivotal for controlling IgE production in vivo. Proc. Natl. Acad. Sci. USA 106, 8308-8313 (2009).
42. Bedel, R. et al. Effective functional maturation of invariant natural killer T cells is constrained by negative selection and T-cell antigen receptor affinity. Proc. Natl. Acad. Sci. USA 111, E119-128 (2014).
43. Zietara, N. et al. Critical role for miR-181a/b-1 in agonist selection of invariant natural killer T cells. Proc. Natl. Acad. Sci. USA 110, 7407-7412 (2013).
44. Li, J., Wu, D., Jiang, N. & Zhuang, Y. Combined deletion of Id2 and Id3 genes reveals multiple roles for E proteins in invariant NKT cell development and expansion. J. Immunol. 191, 5052-5064 (2013).
45. 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).
46. Bernstein, B. E. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
47. McKittrick, E., Gafken, P. R., Ahmad, K. & Henikoff, S. Histone H3.3 is enriched in covalent modifications associated with active chromatin. Proc. Natl. Acad. Sci. USA 101, 1525-1530 (2004).
48. Li, W. et al. An alternate pathway for CD4 T cell development: thymocyte-expressed MHC class II selects a distinct T cell population. Immunity 23, 375-386 (2005).
49. Vahl, J. C. et al. NKT cell-TCR expression activates conventional T cells in vivo, but is largely dispensable for mature NKT cell biology. PLoS Biol. 11, e1001589 (2013).
50. Haks, M. C. et al. Attenuation of gammadeltaTCR signaling efficiently diverts thymocytes to the alphabeta lineage. Immunity 22, 595-606 (2005).
51. Alonzo, E. S. & Sant'Angelo, D. B. Development of PLZF-expressing innate T cells. Curr. Opin. Immunol. 23, 220-227 (2011).