The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus

Journal of Experimental Medicine

Volumn 197, Issue 7, 2003, Pages 831-844

  Yücel, Raif ^a   Karsunky, Holger ^a,b   Klein Hitpass, Ludger ^a   Möröy, Tarik ^a  

^a UNIVERSITY HOSPITAL ESSEN   (Germany)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Apoptosis; Helix loop helix proteins; Lineage skewing; T cell differentiation; Zinc finger protein

Indexed keywords

CD4 ANTIGEN; CD8 ANTIGEN; DNA BINDING PROTEIN; GENE PRODUCT; HELIX LOOP HELIX PROTEIN; LUNG KRUPPEL LIKE FACTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; STEM CELL FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GFI1; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DEATH; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CELL SUBPOPULATION; CELL SURVIVAL; CONTROLLED STUDY; CORRELATION ANALYSIS; GENE EXPRESSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN FUNCTION; STEM CELL; T LYMPHOCYTE; THYMOCYTE; THYMUS;

ANIMALS; ANTIGENS, CD; ANTIGENS, CD4; ANTIGENS, CD8; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; CELL SURVIVAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HEMATOPOIETIC STEM CELLS; HISTOCOMPATIBILITY ANTIGENS CLASS I; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION FACTORS;

EID: 17644443312     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20021417     Document Type: Article

References (59)

1. Tong, B., H.L. Grimes, T.Y. Yang, S.E. Bear, Z. Qin, K. Du, W.S. El-Deiry, and P.N. Tsichlis. 1998. The Gfi-1B proto-oncoprotein represses p21WAF1 and inhibits myeloid cell differentiation. Mol. Cell. Biol. 18:2462-2473.
2. Rödel, B., T. Wagner, M. Zörnig, J. Niessing, and T. Möröy. 1998. The human homologue (GFI1B) of the chicken GFI gene maps to chromosome 9q34.13-A locus frequently altered in hematopoietic diseases. Genomics. 54:580-582.
3. Grimes, H.L., T.O. Chan, P.A. Zweidler-McKay, B. Tong, and P.N. Tsichlis. 1996. The Gfi-1 proto-oncoprotein contains a novel transcriptional repressor domain, SNAG, and inhibits G1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16:6263-6272.
4. Zweidler-Mckay, P.A., H.L. Grimes, M.M. Flubacher, and P.N. Tsichlis. 1996. Gfi-1 encodes a nuclear zinc finger protein that binds DNA and functions as a transcriptional repressor. Mol. Cell. Biol. 16:4024-4034.
5. Rödel, B., K. Tavassoli, H. Karsunky, T. Schmidt, M. Bachmann, F. Schaper, P. Heinrich, K. Shuai, H.P. Elsasser, and T. Möröy. 2000. The zinc finger protein Gfi-1 can enhance STAT3 signaling by interacting with the STAT3 inhibitor PIAS3. EMBO J. 19:5845-5855.
6. Chung, C.D., J. Liao, B. Liu, X. Rao, P. Jay, P. Berta, and K. Shuai. 1997. Specific inhibition of Stat3 signal transduction by PIAS3. Science. 278:1803-1805.
7. Gilks, C.B., S.E. Bear, H.L. Grimes, and P.N. Tsichlis. 1993. Progession of interleukin-2 (IL-2)-dependent rat T cell lymphoma lines to IL-2-independent growth following activation of a gene (Gfi-1) encoding a novel zinc finger protein. Mol. Cell. Biol. 13:1759-1768.
8. Zörnig, M., T. Schmidt, H. Karsunky, A. Grzeschiczek, and T. Möröy. 1996. Zinc finger protein GFI-1 cooperates with myc and pim-1 in T-cell lymphomagenesis by reducing the requirements for IL-2. Oncogene. 12:1789-1801.
9. Scheijen, B., J. Jonkers, D. Acton, and A. Berns. 1997. Characterization of pal-1, a common proviral insertion site in murine leukemia virus-induced lymphomas of c-myc and Pim-1 transgenic mice. J. Virol. 71:9-16.
10. Schmidt, T., M. Zörnig, R. Beneke, and T. Möröy. 1996. MoMuLV proviral integrations identified by Sup-F selection in tumors from infected myc/pim bitransgenic mice correlate with activation of the gfi-1 gene. Nucleic Acids Res. 24:2528-2534.
11. Schmidt, T., H. Karsunky, E. Gau, B. Zevnik, H.P. Elsasser, and T. Möröy. 1998. Zinc finger protein GFI-1 has low oncogenic potential but cooperates strongly with pim and myc genes in T-cell lymphomagenesis. Oncogene. 17:2661-2667.
12. Schmidt, T., H. Karsunky, B. Rödel, B. Zevnik, H.P. Elsasser, and T. Möröy. 1998b. Evidence implicating Gfi-1 and Pim-1 in pre-T-cell differentiation steps associated with beta-selection. EMBO J. 17:5349-5359.
13. Godfrey, D.I., J. Kennedy, T. Suda, and A. Zlotnik. 1993. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3-CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150:4244-4252.
14. Murray, R., T. Suda, N. Wrighton, F. Lee, and A. Zlotnik. 1989. IL-7 is a growth and maintenance factor for mature and immature thymocyte subsets. Int. Immunol. 1:526-531.
15. Baird, A.M., R.M. Gerstein, and L.J. Berg. 1999. The role of cytokine receptor signaling in lymphocyte development. Curr. Opin. Immunol. 11:157-166.
16. Fehling, H.J., and H. von Boehmer. 1997. Early αβ T cell development in the thymus of normal and genetically altered mice. Curr. Opin. Immunol. 9:263-275.
17. Rodewald, H.R., K. Kretzschmar, W. Swat, and S. Takeda. 1995. Intrathymically expressed c-kit ligand (stem cell factor) is a major factor driving expansion of very immature thymocytes in vivo. Immunity. 3:313-319.
18. Rodewald, H.R., M. Ogawa, C. Haller, C. Waskow, and J.P. DiSanto. 1997. Pro-thymocyte expansion by c-kit and the common cytokine receptor gamma chain is essential for repertoire formation. Immunity. 6:265-272.
19. Fehling, H.J., S. Gilfillan, and R. Ceredig. 1999. αβ/γδ lineage commitment in the thymus of normal and genetically manipulated mice. Adv. Immunol. 71:1-76.
20. Peschon, J.J., P.J. Morrissey, K.H. Grabstein, F.J. Ramsdell, E. Maraskovsky, B.C. Gliniak, L.S. Park, S.F. Ziegler, D.E. Williams, C.B. Ware, et al. 1994. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. J. Exp. Med. 180:1955-1960.
21. von Freeden-Jeffry, U., P. Vieira, L.A. Lucian, T. McNeil, S.E. Burdach, and R. Murray. 1995. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. J. Exp. Med. 181:1519-1526.
22. Petrie, H.T., F. Livak, D. Burtrum, and S. Mazel. 1995. T cell receptor gene recombination patterns and mechanisms: cell death, rescue, and T cell production. J. Exp. Med. 182:121-127.
23. Dudley, E.C., H.T. Petrie, L.M. Shah, M.J. Owen, and A.C. Hayday. 1994. T cell receptor beta chain gene rearrangement and selection during thymocyte development in adult mice. Immunity. 1:83-93.
24. Godfrey, D.I., and A. Zlotnik. 1993b. Control points in early T-cell development. Immunol. Today. 14:547-553.
25. Godfrey, D.I., J. Kennedy, P. Mombaerts, S. Tonegawa, and A. Zlotnik. 1994. Onset of TCR-beta gene rearrangement and role of TCR-beta expression during CD3-CD4-CD8-thymocyte differentiation. J. Immunol. 152:4783-4792.
26. Hoffman, E.S., L. Passoni, T. Crompton, T.M. Leu, D.G. Schatz, A. Koff, M.J. Owen, and A.C. Hayday. 1996. Productive T-cell receptor β-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948-962.
27. Anderson, S.J., and R.M. Perlmutter. 1995. A signaling pathway governing early thymocyte maturation. Immunol. Today. 16:99-105.
28. Penit, C., B. Lucas, and F. Vasseur. 1995. Cell expansion and growth arrest phases during the transition from precursor (CD4-8-) to immature (CD4+8+) thymocytes in normal and genetically modified mice. J. Immunol. 154:5103-5113.
29. Saito, T., and N. Watanabe. 1998. Positive and negative thymocyte selection. Crit. Rev. Immunol. 18:359-370.
30. Nossal, G.J. 1994. Negative selection of lymphocytes. Cell. 76:229-239.
31. Kisielow, P., and H. von Boehmer. 1995. Development and selection of T cells: facts and puzzles. Adv. Immunol. 58:87-209.
32. Guidos, C.J. 1996. Positive selection of CD4+ and CD8+ T cells. Curr. Opin. Immunol. 8:225-232.
33. Engel, I., and C. Murre. 2001. The function of E- and Id proteins in lymphocyte development. Nat. Rev. Immunol. 1:193-199.
34. Karsunky, H., H. Zeng, T. Schmidt, B. Zevnik, R. Kluge, K.W. Schmid, U. Duhrsen, and T. Möröy. 2002. Inflammatory reactions and severe neutropenia in mice lacking the transcriptional repressor Gfi1. Nat. Genet. 30:295-300.
35. Möröy, T., A. Grzeschiczek, S. Petzold, and K.U. Hartmann. 1993. Expression of a Pim-1 transgene accelerates lymphoproliferation and inhibits apoptosis in lpr/lpr mice. Proc. Natl. Acad. Sci. USA. 90:10734-10738.
36. Wolfer, A., T. Bakker, A. Wilson, M. Nicolas, V. Ioannidis, D.R. Littman, P.P. Lee, C.B. Wilson, W. Held, H.R. MacDonald, et al. 2001. Inactivation of Notch 1 in immature thymocytes does not perturb CD4 or CD8T cell development. Nat. Immunol. 2:235-241.
37. Lipshutz, R.J., S.P. Fodor, T.R. Gingeras, and D.J. Lockhart. 1999. High density synthetic oligonucleotide arrays. Nat. Genet. 21:20-24.
38. Ikawa, T., S. Fujimoto, H. Kawamoto, Y. Katsura, and Y. Yokota. 2001. Commitment to natural killer cells requires the helix-loop-helix inhibitor Id2. Proc. Natl. Acad. Sci. USA. 98:5164-5169.
39. Lucas, B., and R.N. Germain. 1996. Unexpectedly complex regulation of CD4/CD8 coreceptor expression supports a revised model for CD4+CD8+ thymocyte differentiation. Immunity. 5:461-477.
40. Barthlott, T., H. Kohler, and K. Eichmann. 1997. Asynchronous coreceptor downregulation after positive thymic selection: prolonged maintenance of the double positive state in CD8 lineage differentiation due to sustained biosynthesis of the CD4 coreceptor. J. Exp. Med. 185:357-362.
41. Kisielow, P., H. Bluthmann, U.D. Staerz, M. Steinmetz, and H. von Boehmer. 1988. Tolerance in T-cell-receptor transgenic mice involves deletion of nonmature CD4+8+ thymocytes. Nature. 333:742-746.
42. Germain, R.N. 2002. T-cell development and the CD4-CD8 lineage decision. Nat Rev Immunol. 2:309-322.
43. 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.
44. Mombaerts, P., J. Iacomini, R.S. Johnson, K. Herrup, S. Tonegawa, and V.E. Papaioannou. 1992. RAG-1-deficient mice have no mature B and T lymphocytes. Cell. 68:869-877.
45. Karsunky, H., I. Mende, T. Schmidt, and T. Möröy. 2002. High levels of the onco-protein Gfi-1 accelerate T-cell proliferation and inhibit activation induced T-cell death in Jurkat T-cells. Oncogene. 21:1571-1579.
46. von Freeden-Jeffry, U., N. Solvason, M. Howard, and R. Murray. 1997. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity. 7:147-154.
47. Arch, R.H., and C.B. Thompson. 1998. 4-1BB and Ox40 are members of a tumor necrosis factor (TNF)-nerve growth factor receptor subfamily that bind TNF receptor-associated factors and activate nuclear factor kappaB. Mol. Cell. Biol. 18:558-565.
48. Nakano, H., H. Oshima, W. Chung, L. Williams-Abbott, C.F. Ware, H. Yagita, and K. Okumura. 1996. TRAF5, an activator of NF-kappaB and putative signal transducer for the lymphotoxin-beta receptor. J. Biol. Chem. 271:14661-14664.
49. Akiba, H., H. Nakano, S. Nishinaka, M. Shindo, T. Kobata, M. Atsuta, C. Morimoto, C.F. Ware, N.L. Malinin, D. Wallach, et al. 1998. CD27, a member of the tumor necrosis factor receptor superfamily, activates NF-kappaB and stress-activated protein kinase/c-Jun N-terminal kinase via TRAF2, TRAF5, and NF-kappaB-inducing kinase. J. Biol. Chem. 273:13353-13358.
50. Baseta, J.G., and O. Stutman. 2000. TNF regulates thymocyte production by apoptosis and proliferation of the triple negative (CD3-CD4-CD8-) subset. J. Immunol. 165:5621-5630.
51. Li, R., and D.M. Page. 2001. Requirement for a complex array of costimulators in the negative selection of autoreactive thymocytes in vivo. J. Immunol. 166:6050-6056.
52. Newton, K., A.W. Harris, and A. Strasser. 2000. FADD/MORT1 regulates the pre-TCR checkpoint and can function as a tumour suppressor. EMBO J. 19:931-941.
53. Hogquist, K.A. 2001. Signal strength in thymic selection and lineage commitment. Curr. Opin. Immunol. 13:225-231.
54. Matechak, E.O., N. Killeen, S.M. Hedrick, and B.J. Fowlkes. 1996. MHC class II-specific T cells can develop in the CD8 lineage when CD4 is absent. Immunity. 4:337-347.
55. Itano, A., P. Salmon, D. Kioussis, M. Tolaini, P. Corbella, and E. Robey. 1996. The cytoplasmic domain of CD4 promotes the development of CD4 lineage T cells. J. Exp. Med. 183:731-741.
56. Bosselut, R., L. Feigenbaum, S.O. Sharrow, and A. Singer. 2001. Strength of signaling by CD4 and CD8 coreceptor tails determines the number but not the lineage direction of positively selected thymocytes. Immunity. 14:483-494.
57. Kuo, C.T., M.L. Veselits, and J.M. Leiden. 1997. LKLF: a transcriptional regulator of single-positive T cell quiescence and survival. Science. 277:1986-1990.
58. Quong, M.W., W.J. Romanow, and C. Murre. 2002. E protein function in lymphocyte development. Annu. Rev. Immunol. 20:301-322.
59. Bain, G., M.W. Quong, R.S. Soloff, S.M. Hedrick, and C. Murre. 1999. Thymocyte maturation is regulated by the activity of the helix-loop-helix protein, E47. J. Exp. Med. 190:1605-1616.