Inhibitory role of the transcription repressor Gfi1 in the generation of thymus-derived regulatory T cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 34, 2013, Pages

  Shi, Lewis Zhichang ^a   Kalupahana, Nishan S ^a   Turnis, Meghan E ^a   Neale, Geoffrey ^a   Hock, Hanno ^b   Vignali, Dario A A ^a   Chi, Hongbo ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; CRE RECOMBINASE; GROWTH FACTOR INDEPENDENT 1; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BYSTANDER EFFECT; CD4+ T LYMPHOCYTE; CELL EXPANSION; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; CHIMERA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DNA SYNTHESIS; GENE DELETION; GERM LINE; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INTRACELLULAR SIGNALING; MELANOMA B16; MICROENVIRONMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STEADY STATE; T LYMPHOCYTE SUBPOPULATION; THYMOCYTE; THYMUS; TRANSCRIPTION REGULATION; TUMOR IMMUNITY; UPREGULATION; WILD TYPE;

ANALYSIS OF VARIANCE; ANIMALS; CELLS, CULTURED; DNA-BINDING PROTEINS; FLOW CYTOMETRY; HOMEOSTASIS; INTERLEUKIN-2; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION; T-LYMPHOCYTES, REGULATORY; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 84882739214     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1300950110     Document Type: Article

References (51)

1. Josefowicz SZ, Lu LF, Rudensky AY (2012) Regulatory T cells: Mechanisms of differentiation and function. Annu Rev Immunol 30:531-564.
2. Hsieh CS, Lee HM, Lio CW (2012) Selection of regulatory T cells in the thymus. Nat Rev Immunol 12(3):157-167.
3. Klein L, Jovanovic K (2011) Regulatory T cell lineage commitment in the thymus. Semin Immunol 23(6):401-409.
4. Lio CW, Hsieh CS (2008) A two-step process for thymic regulatory T cell development. Immunity 28(1):100-111.
5. Burchill MA, et al. (2008) Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 28(1):112-121.
6. Stritesky GL, Jameson SC, Hogquist KA (2012) Selection of self-reactive T cells in the thymus. Annu Rev Immunol 30:95-114.
7. Hock H, Orkin SH (2006) Zinc-finger transcription factor Gfi-1: Versatile regulator of lymphocytes, neutrophils and hematopoietic stem cells. Curr Opin Hematol 13(1):1-6.
8. Möröy T, Khandanpour C (2011) Growth factor independence 1 (Gfi1) as a regulator of lymphocyte development and activation. Semin Immunol 23(5):368-378.
9. Karsunky H, et al. (2002) Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat Genet 30(3):295-300.
10. Hock H, et al. (2003) Intrinsic requirement for zinc finger transcription factor Gfi-1 in neutrophil differentiation. Immunity 18(1):109-120.
11. Spooner CJ, Cheng JX, Pujadas E, Laslo P, Singh H (2009) A recurrent network involving the transcription factors PU.1 and Gfi1 orchestrates innate and adaptive immune cell fates. Immunity 31(4):576-586.
12. Yücel R, Kosan C, Heyd F, Möröy T (2004) Gfi1:green fluorescent protein knock-in mutant reveals differential expression and autoregulation of the growth factor independence 1 (Gfi1) gene during lymphocyte development. J Biol Chem 279(39):40906-40917.
13. Yücel R, Karsunky H, Klein-Hitpass L, Möröy T (2003) The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J Exp Med 197(7):831-844.
14. Zhu J, et al. (2002) Growth factor independent-1 induced by IL-4 regulates Th2 cell proliferation. Immunity 16(5):733-744.
15. Zhu J, Jankovic D, Grinberg A, Guo L, Paul WE (2006) Gfi-1 plays an important role in IL-2-mediated Th2 cell expansion. Proc Natl Acad Sci USA 103(48):18214-18219.
16. Pargmann D, et al. (2007) Differential impact of the transcriptional repressor Gfi1 on mature CD4+ and CD8+ T lymphocyte function. Eur J Immunol 37(12):3551-3563.
17. Zhu J, et al. (2009) Down-regulation of Gfi-1 expression by TGF-beta is important for differentiation of Th17 and CD103+ inducible regulatory T cells. J Exp Med 206(2): 329-341.
18. Ichiyama K, et al. (2009) Gfi1 negatively regulates T(h)17 differentiation by inhibiting RORgammat activity. Int Immunol 21(7):881-889.
19. Liu G, et al. (2009) The receptor S1P1 overrides regulatory T cell-mediated immune suppression through Akt-mTOR. Nat Immunol 10(7):769-777.
20. Carlson CM, et al. (2006) Kruppel-like factor 2 regulates thymocyte and T-cell migration. Nature 442(7100):299-302.
21. van der Meer LT, Jansen JH, van der Reijden BA (2010) Gfi1 and Gfi1b: Key regulators of hematopoiesis. Leukemia 24(11):1834-1843.
22. de Boer J, et al. (2003) Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur J Immunol 33(2):314-325.
23. Lee PP, et al. (2001) A critical role for Dnmt1 and DNA methylation in T cell development, function, and survival. Immunity 15(5):763-774.
24. Lehmann J, et al. (2002) Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25- regulatory T cells. Proc Natl Acad Sci USA 99(20): 13031-13036.
25. Deaglio S, et al. (2007) Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression. J Exp Med 204(6):1257-1265.
26. Chalmin F, et al. (2012) Stat3 and Gfi-1 transcription factors control Th17 cell immunosuppressive activity via the regulation of ectonucleotidase expression. Immunity 36(3):362-373.
27. Shimizu J, Yamazaki S, Sakaguchi S (1999) Induction of tumor immunity by removing CD25+CD4+ T cells: A common basis between tumor immunity and autoimmunity. J Immunol 163(10):5211-5218.
28. Sutmuller RP, et al. (2001) Synergism of cytotoxic T lymphocyte- associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 194(6):823-832.
29. Turk MJ, et al. (2004) Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T cells. J Exp Med 200(6):771-782.
30. Weinreich MA, et al. (2009) KLF2 transcription-factor deficiency in T cells results in unrestrained cytokine production and upregulation of bystander chemokine receptors. Immunity 31(1):122-130.
31. Rubtsov YP, et al. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28(4):546-558.
32. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY (2005) A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 6(11):1142-1151.
33. Bayer AL, Yu A, Adeegbe D, Malek TR (2005) Essential role for interleukin-2 for CD4(+) CD25(+) T regulatory cell development during the neonatal period. J Exp Med 201(5): 769-777.
34. Malek TR, Castro I (2010) Interleukin-2 receptor signaling: At the interface between tolerance and immunity. Immunity 33(2):153-165.
35. Granucci F, et al. (2001) Inducible IL-2 production by dendritic cells revealed by global gene expression analysis. Nat Immunol 2(9):882-888.
36. Setoguchi R, Hori S, Takahashi T, Sakaguchi S (2005) Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201(5):723-735.
37. ChenW, et al. (2003) Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198(12):1875-1886.
38. Liu Y, et al. (2008) A critical function for TGF-beta signaling in the development of natural CD4+CD25+Foxp3+ regulatory T cells. Nat Immunol 9(6):632-640.
39. Murai M, et al. (2009) Interleukin 10 acts on regulatory T cells to maintain expression of the transcription factor Foxp3 and suppressive function in mice with colitis. Nat Immunol 10(11):1178-1184.
40. Denning TL, Wang YC, Patel SR, Williams IR, Pulendran B (2007) Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 8(10):1086-1094.
41. Albu DI, et al. (2007) BCL11B is required for positive selection and survival of doublepositive thymocytes. J Exp Med 204(12):3003-3015.
42. Bouillet P, et al. (2002) BH3-only Bcl-2 family member Bim is required for apoptosis of autoreactive thymocytes. Nature 415(6874):922-926.
43. Wirnsberger G, Mair F, Klein L (2009) Regulatory T cell differentiation of thymocytes does not require a dedicated antigen-presenting cell but is under T cell-intrinsic developmental control. Proc Natl Acad Sci USA 106(25):10278-10283.
44. Weinreich MA, Odumade OA, Jameson SC, Hogquist KA (2010) T cells expressing the transcription factor PLZF regulate the development of memory-like CD8+ T cells. Nat Immunol 11(8):709-716.
45. Verykokakis M, Boos MD, Bendelac A, Kee BL (2010) SAP protein-dependent natural killer T-like cells regulate the development of CD8(+) T cells with innate lymphocyte characteristics. Immunity 33(2):203-215.
46. Lee YJ, Jameson SC, Hogquist KA (2011) Alternative memory in the CD8 T cell lineage. Trends Immunol 32(2):50-56.
47. Khandanpour C, et al. (2011) Growth factor independence 1 protects hematopoietic stem cells against apoptosis but also prevents the development of a myeloproliferativelike disease. Stem Cells 29(2):376-385.
48. Hock H, et al. (2004) Gfi-1 restricts proliferation and preserves functional integrity of haematopoietic stem cells. Nature 431(7011):1002-1007.
49. Yang K, Neale G, Green DR, He W, Chi H (2011) The tumor suppressor Tsc1 enforces quiescence of naive T cells to promote immune homeostasis and function. Nat Immunol 12(9):888-897.
50. Shi LZ, et al. (2011) HIF1alpha-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med 208(7):1367-1376.
51. Woo SR, et al. (2012) Immune inhibitory molecules LAG-3 and PD-1 synergistically regulate T-cell function to promote tumoral immune escape. Cancer Res 72(4): 917-927.