Disruption of αβ but not of γδ T cell development by overexpression of the helix-loop-helix protein Id3 in committed T cell progenitors

EMBO Journal

Volumn 18, Issue 10, 1999, Pages 2793-2802

  Blom, Bianca ^b   Heemskerk, Mirjam H M ^b   Verschuren, Martie C M ^a   Van Dongen, Jacques J M ^a   Stegmann, Alexander P A ^b   Bakker, Arjen Q ^b   Couwenberg, Franka ^b   Res, Pieter C M ^b   Spits, Hergen ^b  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

Basic helix loop helix protein; NK cell; T cells; Thymus; Transcription

Indexed keywords

CD34 ANTIGEN; HELIX LOOP HELIX PROTEIN; MEMBRANE ANTIGEN; MESSENGER RNA; T LYMPHOCYTE RECEPTOR;

ARTICLE; CELL MATURATION; DOWN REGULATION; GENE REARRANGEMENT; GENETIC RECOMBINATION; GENETIC TRANSCRIPTION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LYMPHOCYTE DIFFERENTIATION; NATURAL KILLER CELL; NORMAL HUMAN; ORGAN CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; THYMUS;

ANTIGENS, CD; CELL DIFFERENTIATION; CELLS, CULTURED; GENE EXPRESSION REGULATION; GENE REARRANGEMENT, T-LYMPHOCYTE; HELIX-LOOP-HELIX MOTIFS; HEMATOPOIETIC STEM CELLS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; NEOPLASM PROTEINS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; RETROVIRIDAE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; T-LYMPHOCYTES; THYMUS GLAND; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 0033577695     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.10.2793     Document Type: Article

References (53)

1. Aifantis, I., Azogui, O., Feinberg, J., Saint Ruf, C., Buer, J. and von Boehmer, H. (1998) On the role of the pre-T cell receptor in αβ versus γδ T lineage commitment. Immunity, 9, 649-655.
2. Bain, G. et al. (1994) E2A proteins are required for proper B cell development and initiation of Ig gene rearrangements. Cell, 79, 885-892.
3. Bain, G. et al. (1997a) E2A deficiency leads to abnormalities in αβ and γδ T cell development, perturbations in V(D)J rearrangement and to the rapid development of T-cell lymphomas. Mol. Cell. Biol., 17, 4782-4791.
4. Bain, G., Robanus Maandag, E., Te Riele, H., Feeney, A.J., Sheehy, A., Schlissel, M., Shinton, S.A., Hardy, R.R. and Murre, C. (1997b) Both E12 and E47 allow commitment to the B cell lineage. Immunity, 6, 145-154.
5. Benezra, R., Davis, R.L., Lockshon, D., Turner, D.L. and Weintraub, H. (1990) The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell, 61, 49-59.
6. + progenitors capable of developing into T cells are not committed to the T cell lineage. J. Immunol., 158, 3571-3577.
7. Blom, B., Res, P.C.M. and Spits, H. (1998) T cell precursors in mice and man. Crit. Rev. Immunol., 18, 371-388.
8. Blom, B., Verschuren, M.C.M., Heemskerk, M.H.M., Bakker, A.Q., van Gastel-Mol, E.J, Wolvers-Tettero, I.L.M. van Dongen, J.J.M. and Spits, H. (1999) TCR gene rearrangements and expression of the pre-T cell receptor complex during T cell differentiation. Blood, in press.
9. Breit, T.M., Wolvers Tettero, I.L., Hahlen, K., Van Wering, E.J. and van Dongen, J.J. (1991) Extensive junctional diversity of γδ T-cell receptors expressed by T-cell acute lymphoblastic leukemias: implications for the detection of minimal residual disease. Leukemia, 5, 1076-1086.
10. Breit, T.M., Wolvers-Tettero, I.L., Beishuizen, A., Verhoeven, M.A., Van Wering, E.R. and van Dongen, J.J. (1993) Southern blot patterns, frequencies, and junctional diversity of T-cell receptor-δ gene rearrangements in acute lymphoblastic leukemia. Blood, 82, 3063-3074.
11. + pro-T thymocytes. Proc. Natl Acad. Sci. USA, 95, 12522-12527.
12. Christy, B.A., Sanders, L.K., Lau, L.F., Copeland, N.G., Jenkins, N.A. and Nathans, D. (1991) An Id-related helix-loop-helix protein encoded by a growth factor-inducible gene. Proc. Natl Acad. Sci. USA, 88, 1815-1819.
13. Church, G.M., Ephrussi, A., Gilbert, W. and Tonegawa, S. (1985) Cell-type-specific contacts to immunoglobulin enhancers in nuclei. Nature, 313, 798-801.
14. Davies, M.V. and Kaufman, R.J. (1992) The sequence context of the initiation codon in the encephalomyocarditis virus leader modulates efficiency of internal translation initiation. J. Virol., 66, 1924-1932.
15. Donskoy, E. and Goldschneider, I. (1992) Thymocytopoiesis is maintained by blood-borne precursors throughout postnatal life. A study in parabiotic mice. J. Immunol., 148, 1604-1612.
16. Ephrussi, A., Church, G.M., Tonegawa, S. and Gilbert, W. (1985) B lineage-specific interactions of an immunoglobulin enhancer with cellular factors in vivo. Science, 227, 134-140.
17. Fehling, H.J., Krotkova, A., Saint Ruf, C. and Von Boehmer, H. (1995) Crucial role of the pre-T-cell receptor a gene in development of αβ but not γδ T cells. Nature, 375, 795-798.
18. + cells in the human thymus are defined by expression of CD34. Delineation of early events in human thymic development. J. Exp. Med., 178, 391-401.
19. Godfrey, D.I. and Zlotnik, A. (1993) Control points in early T-cell development. Immunol. Today, 14, 547-553.
20. Hanenberg, H., Xiao, X.L., Dilloo, D., Hashino, K., Kato, I. and Williams, D.A. (1996) Colocalization of retrovirus and target cells on specific fibronectin fragments increases genetic transduction of mammalian cells. Nature Med., 2, 876-882.
21. + hematopoietic cells. Human Gene Ther., 8, 2193-2206.
22. Heemskerk, M.H.M., Blom, B., Nolan, G., Stegmann, A.P.A., Balcker, A.Q., Weijer, K., Res, P.C.M. and Spits, H. (1997) Inhibition of T cell and promotion of natural killer cell development by the dominant negative helix-loop-helix factor Id3. J. Exp. Med., 186, 1597-1602.
23. + cells into T cells. J. Immunol., 159, 694-702.
24. Kang, J., Baker, J. and Raulet, D.H. (1995) Evidence that productive rearrangements of TCRygenes influence the commitment of progenitor cells to differentiate into αβ or γδ T cells. Eur. J. Immunol., 25, 2706-2709.
25. Kimizuka, F., Taguchi, Y., Ohdate, Y., Kawase, Y., Shimojo, T., Hashino, K., Kato, I., Sekiguchi, K. and Titani, K. (1991) Production and characterization of functional domains of human fibronectin expressed in Escherichia coli. J. Biochem. (Tokyo), 110, 284-291.
26. Kinsella, T.M. and Nolan, G.P. (1996) Episomal vectors rapidly and stably produce high-liter recombinant retrovirus. Human Gene Ther., 7, 1405-1413.
27. - intermediate. J. Exp. Med., 178, 265-277.
28. Krangel, M.S., Yssel, H., Brocklehurst, C. and Spits, H. (1990) A distinct wave of human T cell receptor γ/δ lymphocytes in the early fetal thymus: evidence for controlled gene rearrangement and cytokine production. J. Exp. Med., 172, 847-859.
29. Livak, F., Petrie, H.T., Crispe, J.N. and Schatz, D.G. (1995) In-frame TCR 8 gene rearrangements play a critical role in the αβ/γδ T cell lineage decision. Immunity, 2, 617-627
30. Loveys, D.A., Streiff, M.B. and Kato, G.J. (1996) E2A basic-helix-loop-helix transcription factors are negatively regulated by serum growth factors and by the Id3 protein. Nucleic Acids Res., 24, 2813-2820.
31. Margolis, D., Yassai, M., Hletko, A., McOlash, L. and Gorski, J. (1997) Concurrent or sequential delta and beta TCR gene rearrangement during thymocyte development: individual thymi follow distinct pathways. J. Immunol., 159, 529-533
32. + human thymic precursors can be traced by the differential expression of CD44. J. Exp. Med., 181, 475-483.
33. Murre, C., McCaw, P.S. and Baltimore, D. (1989) A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell, 56, 777-783.
34. Murre, C. et al. (1994) Structure and function of helix-loop-helix proteins. Biochim. Biaphys. Acta, 1218, 129-135.
35. Pestova, T.V., Hellen, C.U. and Shatsky, I.N. (1996) Canonical eukaryotic initiation factors determine initiation of translation by internal ribosomal entry. Mol. Cell. Biol., 16, 6859-6869.
36. Ramiro, A.R., Trigueros, C., Marquez, C., San, M.J. and Toribio, M.L. (1996) Regulation of pre-T cell receptor (pTα-TCRβ) gene expression during human thymic development. J. Exp. Med., 184, 519-530.
37. dim cells in the human thymus can differentiate into T, natural killer and dendritic cells but are distinct from stem cells. Blood, 87, 5196-5206
38. Res, P., Blom, B., Hori, T., Weijer, K. and Spits, H. (1997) Downregulation of CD1 marks acquisition of functional maturation of human thymocytes and defines a control point in late stages of human T cell development. J. Exp. Med., 185, 141-151.
39. Riechmann, V., Van Cruchten, I. and Sablitzky, F. (1994) The expression pattern of Id4, a novel dominant negative helix-loop-helix protein, is distinct from Id1, Id2 and Id3. Nucleic Acids Res., 22, 749-755.
40. Sachs, A.B., Samow, P. and Hentze, M.W. (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell, 89, 831-838.
41. Sánchez, M.J., Spits, H., Lanier, L.L. and Philips, J.H. (1993) Human natural killer cell committed thymocytes and their relationship to the T cell lineage. J. Exp. Med., 178, 1857-1866.
42. Sanchez, M.-J., Muench, M.O., Roncarolo, M.G., Lanier, L. and Phillips, J.H. (1994) Identification of a common T/NK. cell progenitor in human fetal thymus. J. Exp. Med., 180, 569-576.
43. Scollay, R., Smith, J. and Stauffer, V. (1986) Dynamics of early T cells: prothymocyte migration and proliferation in the adult mouse thymus. Immunol, Rev., 91, 129-157.
44. Shortman, K. and Wu, L. (1996) Early T lymphocyte progenitors. Annu. Rev. Immunol., 14, 29-47.
45. Sigvardsson, M., O'Riordan, M. and Grosschedl, R. (1997) EBF and E47 collaborate to induce expression of the endogenous immunoglobulin surrogate light chain genes. Immunity, 7, 25-36.
46. Spits, H., Lanier, L. and Phillips, J.H. (1995) Development of human T and natural killer cells. Blood, 85, 2654-2670.
47. Spits, H., Blom, B., Jaleco, A.C., Weijer, K., Verschuren, M.C.M, van Dongen, J.J., Heemskerk, M.H.M and Res, P.C.M (1998) Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol. Rev., 165, 75-86.
48. Sun, X.H., Copeland, N.G., Jenkins, N.A. and Baltimore, D. (1991) Id proteins Id1 and Id2 selectively inhibit DNA binding by one class of helix-loop-helix proteins. Mol. Cell. Biol., 11, 5603-5611.
49. Verschuren, M.C.M., Blom, B., Spits, H. and van Dongen, J.J.M. (1998) PjA-Bp expression and T cell receptor δ deletion during human T cell development. Int. Immunol, 10, 1873-1880.
50. Washbura, T., Schweighoffer, E., Gridley, T., Chang, D., Fowlkes, B.J., Cado, D. and Robey, E. (1997) Notch activity influences the αδ versus γδ T cell lineage decision. Cell, 88, 833-843.
51. Yssel, H., De Vries, J.E., Koken, M., Van Blitterswijk, W. and Spits, H. (1984) Serum-free medium for the generation and the propagation of functional human cytotoxic and helper T cell clones. J. Immunol. Methods, 72, 219-227.
52. Zhuang, Y., Soriano, P. and Weintraub, H. (1994) The helix-loop-helix gene E2A is required for B cell formation. Cell, 79, 875-884.
53. Zhuang, Y., Cheng, P. and Weintraub, H. (1996) B lymphocyte development is regulated by the combined dosage of three basic-helix-loop-helix genes, E2A, E2-2 and HEB. Mol. Cell. Biol., 16, 2898-2905.