Active STAT5 regulates T-bet and eomesodermin expression in CD8 T cells and imprints a T-bet-dependent Tc1 program with repressed IL-6/TGF-β1 signaling

Journal of Immunology

Volumn 191, Issue 7, 2013, Pages 3712-3724

  Grange, Magali ^a,b,c   Verdeil, Gregory ^a,b,c   Arnoux, Fanny ^a,b,c   Griffon, Aurélien ^c   Spicuglia, Salvatore ^c   Maurizio, Julien ^a,b,c   Buferne, Michel ^a,b,c   Schmitt Verhulst, Anne Marie ^a,b,c   Auphan Anezin, Nathalie ^a,b,c  

^a CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^b INSERM   (France)

^c CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EOMESODERMIN; GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; STAT5 PROTEIN; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CD8+ T LYMPHOCYTE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EFFECTOR CELL; FLOW CYTOMETRY; GENE EXPRESSION; GENE IDENTIFICATION; IN VITRO STUDY; MASTOCYTOMA; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; TUMOR CELL LINE;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; GENE EXPRESSION REGULATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; INTERLEUKIN-17; INTERLEUKIN-6; MICE; MICE, TRANSGENIC; RECEPTORS, CYTOKINE; SIGNAL TRANSDUCTION; STAT5 TRANSCRIPTION FACTOR; T-BOX DOMAIN PROTEINS; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, CYTOTOXIC; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA1;

EID: 84885156779     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300319     Document Type: Article

References (54)

1. Kaech, S. M., S. Hemby, E. Kersh, and R. Ahmed. 2002. Molecular and functional profiling of memory CD8 T cell differentiation. Cell 111:837-851.
2. Luckey, C. J., D. Bhattacharya, A. W. Goldrath, I. L. Weissman, C. Benoist, and D. Mathis. 2006. Memory T and memory B cells share a transcriptional program of self-renewal with long-term hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 103:3304-3309.
3. Sarkar, S., V. Kalia, W. N. Haining, B. T. Konieczny, S. Subramaniam, and R. Ahmed. 2008. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205:625-640.
4. Masopust, D., V. Vezys, A. L. Marzo, and L. Lefrançois. 2001. Preferential localization of effector memory cells in nonlymphoid tissue. Science 291:2413-2417.
5. Mora, J. R., and U. H. von Andrian. 2006. T-cell homing specificity and plasticity: new concepts and future challenges. Trends Immunol. 27:235-243.
6. Intlekofer, A. M., N. Takemoto, C. Kao, A. Banerjee, F. Schambach, J. K. Northrop, H. Shen, E. J. Wherry, and S. L. Reiner. 2007. Requirement for T-bet in the aberrant differentiation of unhelped memory CD8+ T cells. J. Exp. Med. 204:2015-2021.
7. + T cell fates via the graded expression of T-bet transcription factor. Immunity 27:281-295.
8. Crotty, S., R. J. Johnston, and S. P. Schoenberger. 2010. Effectors and memories: Bcl-6 and Blimp-1 in T and B lymphocyte differentiation. Nat. Immunol. 11:114-120.
9. Palmer, D. C., and N. P. Restifo. 2009. Suppressors of cytokine signaling (SOCS) in T cell differentiation, maturation, and function. Trends Immunol. 30:592-602.
10. Gattinoni, L., E. Lugli, Y. Ji, Z. Pos, C. M. Paulos, M. F. Quigley, J. R. Almeida, E. Gostick, Z. Yu, C. Carpenito, et al. 2011. A human memory T cell subset with stem cell-like properties. Nat. Med. 17:1290-1297.
11. Walker, S. R., E. A. Nelson, and D. A. Frank. 2007. STAT5 represses BCL6 expression by binding to a regulatory region frequently mutated in lymphomas. Oncogene 26:224-233.
12. Liao, W., J. X. Lin, L. Wang, P. Li, and W. J. Leonard. 2011. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12:551-559.
13. Dudley, M. E., J. R. Wunderlich, J. C. Yang, R. M. Sherry, S. L. Topalian, N. P. Restifo, R. E. Royal, U. Kammula, D. E. White, S. A. Mavroukakis, et al. 2005. Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma. J. Clin. Oncol. 23:2346-2357.
14. Porter, D. L., B. L. Levine, M. Kalos, A. Bagg, and C. H. June. 2011. Chimeric antigen receptor-modified T cells in chronic lymphoid leukemia. N. Engl. J. Med. 365:725-733.
15. Gattinoni, L., C. A. Klebanoff, D. C. Palmer, C. Wrzesinski, K. Kerstann, Z. Yu, S. E. Finkelstein, M. R. Theoret, S. A. Rosenberg, and N. P. Restifo. 2005. Acquisition of full effector function in vitro paradoxically impairs the in vivo antitumor efficacy of adoptively transferred CD8+ T cells. J. Clin. Invest. 115:1616-1626.
16. Dudley, M. E., C. A. Gross, M. M. Langhan, M. R. Garcia, R. M. Sherry, J. C. Yang, G. Q. Phan, U. S. Kammula, M. S. Hughes, D. E. Citrin, et al. 2010. CD8+ enriched "young" tumor infiltrating lymphocytes can mediate regression of metastatic melanoma. Clin. Cancer Res. 16:6122-6131.
17. Boyman, O., and J. Sprent. 2012. The role of interleukin-2 during homeostasis and activation of the immune system. Nat. Rev. Immunol. 12:180-190.
18. Wei, L., A. Laurence, and J. J. O'Shea. 2008. New insights into the roles of Stat5a/b and Stat3 in T cell development and differentiation. Semin. Cell Dev. Biol. 19:394-400.
19. Yu, H., D. Pardoll, and R. Jove. 2009. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 9:798-809.
20. Grange, M., M. Buferne, G. Verdeil, L. Leserman, A. M. Schmitt-Verhulst, and N. Auphan-Anezin. 2012. Activated STAT5 promotes long-lived cytotoxic CD8+ T cells that induce regression of autochthonous melanoma. Cancer Res. 72:76-87.
21. Shanker, A., G. Verdeil, M. Buferne, E. M. Inderberg-Suso, D. Puthier, F. Joly, C. Nguyen, L. Leserman, N. Auphan-Anezin, and A. M. Schmitt-Verhulst. 2007. CD8 T cell help for innate antitumor immunity. J. Immunol. 179:6651-6662.
22. Oliveros, J. 2007. VENNY: an interactive tool for comparing lists with Venn diagrams. Available at: http://bioinfogp. cnb.csic.es/tools/venny/index. html
23. Subramanian, A., P. Tamayo, V. K. Mootha, S. Mukherjee, B. L. Ebert, M. A. Gillette, A. Paulovich, S. L. Pomeroy, T. R. Golub, E. S. Lander, and J. P. Mesirov. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 102:15545-15550.
24. Boyer, L. A., T. I. Lee, M. F. Cole, S. E. Johnstone, S. S. Levine, J. P. Zucker, M. G. Guenther, R. M. Kumar, H. L. Murray, R. G. Jenner, et al. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947-956.
25. McLean, C. Y., D. Bristor, M. Hiller, S. L. Clarke, B. T. Schaar, C. B. Lowe, A. M. Wenger, and G. Bejerano. 2010. GREAT improves functional interpretation of cis-regulatory regions. Nat. Biotechnol. 28:495-501.
26. Laz, E. V., A. Sugathan, and D. J. Waxman. 2009. Dynamic in vivo binding of STAT5 to growth hormone-regulated genes in intact rat liver. Sex-specific binding at low-but not high-affinity STAT5 sites. Mol. Endocrinol. 23:1242-1254.
27. Turatsinze, J. V., M. Thomas-Chollier, M. Defrance, and J. van Helden. 2008. Using RSAT to scan genome sequences for transcription factor binding sites and cis-regulatory modules. Nat. Protoc. 3:1578-1588.
28. Onishi, M., T. Nosaka, K. Misawa, A. L. Mui, D. Gorman, M. McMahon, A. Miyajima, and T. Kitamura. 1998. Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol. 18:3871-3879.
29. Intlekofer, A. M., A. Banerjee, N. Takemoto, S. M. Gordon, C. S. Dejong, H. Shin, C. A. Hunter, E. J. Wherry, T. Lindsten, and S. L. Reiner. 2008. Anomalous type 17 response to viral infection by CD8+ T cells lacking T-bet and eomesodermin. Science 321:408-411.
30. Matsuda, J. L., T. C. George, J. Hagman, and L. Gapin. 2007. Temporal dissection of T-bet functions. J. Immunol. 178:3457-3465.
31. Bezman, N. A., C. C. Kim, J. C. Sun, G. Min-Oo, D. W. Hendricks, Y. Kamimura, J. A. Best, A. W. Goldrath, and L. L. Lanier; Immunological Genome Project Consortium. 2012. Molecular definition of the identity and activation of natural killer cells. Nat. Immunol. 13:1000-1009.
32. Cush, S. S., and E. Flaño. 2011. KLRG1+NKG2A+ CD8 T cells mediate protection and participate in memory responses during g-herpesvirus infection. J. Immunol. 186:4051-4058.
33. Verdeil, G., J. Chaix, A. M. Schmitt-Verhulst, and N. Auphan-Anezin. 2006. Temporal cross-talk between TCR and STAT signals for CD8 T cell effector differentiation. Eur. J. Immunol. 36:3090-3100.
34. Verdeil, G., D. Puthier, C. Nguyen, A. M. Schmitt-Verhulst, and N. Auphan-Anezin. 2006. STAT5-mediated signals sustain a TCR-initiated gene expression program toward differentiation of CD8 T cell effectors. J. Immunol. 176:4834-4842.
35. Townsend, M. J., A. S. Weinmann, J. L. Matsuda, R. Salomon, P. J. Farnham, C. A. Biron, L. Gapin, and L. H. Glimcher. 2004. T-bet regulates the terminal maturation and homeostasis of NK and Va14i NKT cells. Immunity 20:477-494.
36. Shi, M., T. H. Lin, K. C. Appell, and L. J. Berg. 2008. Janus-kinase-3-dependent signals induce chromatin remodeling at the Ifng locus during T helper 1 cell differentiation. Immunity 28:763-773.
37. Sullivan, B. M., A. Juedes, S. J. Szabo, M. von Herrath, and L. H. Glimcher. 2003. Antigen-driven effector CD8 T cell function regulated by T-bet. Proc. Natl. Acad. Sci. USA 100:15818-15823.
38. + T cell differentiation: toward a molecular understanding of fate determination. Curr. Opin. Immunol. 22:279-285.
39. Yoshida, K., A. Sakamoto, K. Yamashita, E. Arguni, S. Horigome, M. Arima, M. Hatano, N. Seki, T. Ichikawa, and T. Tokuhisa. 2006. Bcl6 controls granzyme B expression in effector CD8+ T cells. Eur. J. Immunol. 36:3146-3156.
40. Lin, J. X., P. Li, D. Liu, H. T. Jin, J. He, M. Ata Ur Rasheed, Y. Rochman, L. Wang, K. Cui, C. Liu, et al. 2012. Critical Role of STAT5 transcription factor tetramerization for cytokine responses and normal immune function. Immunity 36:586-599.
41. Yang, Y., J. Xu, Y. Niu, J. S. Bromberg, and Y. Ding. 2008. T-bet and eomesodermin play critical roles in directing T cell differentiation to Th1 versus Th17. J. Immunol. 181:8700-8710.
42. Moriggl, R., V. Sexl, L. Kenner, C. Duntsch, K. Stangl, S. Gingras, A. Hoffmeyer, A. Bauer, R. Piekorz, D. Wang, et al. 2005. Stat5 tetramer formation is associated with leukemogenesis. Cancer Cell 7:87-99.
43. Xu, M., L. Nie, S. H. Kim, and X. H. Sun. 2003. STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPb. EMBO J. 22:893-904.
44. Pfitzner, E., R. Jähne, M. Wissler, E. Stoecklin, and B. Groner. 1998. p300/CREB-binding protein enhances the prolactin-mediated transcriptional induction through direct interaction with the transactivation domain of Stat5, but does not participate in the Stat5-mediated suppression of the glucocorticoid response. Mol. Endocrinol. 12:1582-1593.
45. Cote-Sierra, J., G. Foucras, L. Guo, L. Chiodetti, H. A. Young, J. Hu-Li, J. Zhu, and W. E. Paul. 2004. Interleukin 2 plays a central role in Th2 differentiation. Proc. Natl. Acad. Sci. USA 101:3880-3885.
46. Xu, R., C. M. Nelson, J. L. Muschler, M. Veiseh, B. K. Vonderhaar, and M. J. Bissell. 2009. Sustained activation of STAT5 is essential for chromatin remodeling and maintenance of mammary-specific function. J. Cell Biol. 184:57-66.
47. Pipkin, M. E., J. A. Sacks, F. Cruz-Guilloty, M. G. Lichtenheld, M. J. Bevan, and A. Rao. 2010. Interleukin-2 and inflammation induce distinct transcriptional programs that promote the differentiation of effector cytolytic T cells. Immunity 32:79-90.
48. + T cells to compete for the memory cell niche. J. Immunol. 185:4988-4992.
49. Hwang, E. S., J. H. Hong, and L. H. Glimcher. 2005. IL-2 production in developing Th1 cells is regulated by heterodimerization of RelA and T-bet and requires T-bet serine residue 508. J. Exp. Med. 202:1289-1300.
50. Sumimoto, H., F. Imabayashi, T. Iwata, and Y. Kawakami. 2006. The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells. J. Exp. Med. 203:1651-1656.
51. Huijbers, I. J., P. Krimpenfort, P. Chomez, M. A. van der Valk, J. Y. Song, E. M. Inderberg-Suso, A. M. Schmitt-Verhulst, A. Berns, and B. J. Van den Eynde. 2006. An inducible mouse model of melanoma expressing a defined tumor antigen. Cancer Res. 66:3278-3286.
52. Soudja, S. M., M. Wehbe, A. Mas, L. Chasson, C. P. de Tenbossche, I. Huijbers, B. Van den Eynde, and A. M. Schmitt-Verhulst. 2010. Tumor-initiated inflammation overrides protective adaptive immunity in an induced melanoma model in mice. Cancer Res. 70:3515-3525.
53. Auphan-Anezin, N., G. Verdeil, M. Grange, S. M. Soudja, M. Wehbe, M. Buferne, A. Mas, and A. M. Schmitt-Verhulst. 2013. Immunosuppression in inflammatory melanoma: can it be resisted by adoptively transferred T cells? Pigment Cell Melanoma Res 26:167-175.
54. Yang, X. P., K. Ghoreschi, S. M. Steward-Tharp, J. Rodriguez-Canales, J. Zhu, J. R. Grainger, K. Hirahara, H. W. Sun, L. Wei, G. Vahedi, et al. 2011. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12:247-254.