E2A Deficiency Leads to Abnormalities in αβ T-Cell Development and to Rapid Development of T-Cell Lymphomas

REFERENCES

• Aronheim, A., R. Shiran, A. Rosen, and M. D. Walker. 1993. The E2A gene product contains two separable and functionally distinct transcription activation domains. Proc. Natl. Acad. Sci. USA 90:8063–8067.
   PubMedGoogle Scholar
• Bain, G., and I. Engel. Unpublished results.
   Google Scholar
• Bain, G., S. Gruenwald, and C. Murre. 1993. E2A and E2-2 are subunits of B-cell-specific E2-box DNA-binding proteins. Mol. Cell. Biol. 13:3522–3529.
   PubMed Web of Science ®Google Scholar
• Bain, G., E. Robanus Maandag, D. Izon, D. Armsen, A. Kruisbeek, B. C. Weintraub, I. Krop, M. S. Schlissel, A. Feeney, M. van Roon, M. van der Valk, H. P. J. te Riele, A. Berns, and C. Murre. 1994. E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79:885–892.
   PubMed Web of Science ®Google Scholar
• Bain, G., E. C. Robanus Maandag, H. P. J. te Riele, A. J. Feeney, A. Sheehy, M. Schlissel, S. A. Shinton, R. R. Hardy, and C. Murre. 1997. Both E12 and E47 allow commitment to the B cell lineage. Immunity 6:145–154.
   PubMedGoogle Scholar
• Bain, G. Unpublished results.
   Google Scholar
• Begley, C. G., P. D. Aplan, S. M. Denning, F. Haynes, T. A. Wadman, and I. R. Kirsch. 1989. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related motif. Proc. Natl. Acad. Sci. USA 86:10128–10132.
   PubMed Web of Science ®Google Scholar
• Bernard, O., P. Guglielmi, P. Jonveaux, D. Cherif, S. Gisselbrecht, M. Mauchauffe, R. Berger, C. J. Larsen, and D. Mathieu-Mahul. 1990. Two distinct mechanisms for the SCL gene activation in the t(1;14) translocation of T-cell leukemias. Genes Chromosomes Cancer 1:194–208.
   PubMed Web of Science ®Google Scholar
• Brady, H., and A. Berns. Unpublished results.
   Google Scholar
• Chakraborty, T., T. J. Brennan, L. Li, D. Edmondson, and E. Olson. 1991. Inefficient homooligomerization contributes to the dependence of myogenin on E2A products for efficient DNA binding. Mol. Cell. Biol. 11:3633–3641.
   PubMed Web of Science ®Google Scholar
• Chen, Q., J. Cheng, L. Tsai, N. Buchanan, G. Schneider, A. Carroll, W. Crist, B. Ozanne, M. Siciliano, and R. Baer. 1990. The tal-gene undergoes chromosomal translocation in T-cell leukemia and potentially encodes a helixloop-helix protein. EMBO J. 9:415–424.
   PubMed Web of Science ®Google Scholar
• Davis, R. L., P. F. Cheng, A. B. Lassar, and H. Weintraub. 1990. The MyoD DNA binding domain contains a recognition code for muscle-specific gene activation. Cell 60:733–746.
   PubMedGoogle Scholar
• Duncan, D. D., M. Adlam, and G. Siu. 1996. Asymmetric redundancy in CD4 silencer function. Immunity 4:301–311.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Grabstein, K. H., T. J. Waldschmidt, F. D. Finkelman, B. W. Hess, A. R. Alpert, N. E. Boiani, A. E. Namen, and P. J. Morrissey. 1993. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J. Exp. Med. 178:257.
   PubMed Web of Science ®Google Scholar
• Hardy, R. R., C. E. Carmack, S. A. Shinton, J. D. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse development. J. Exp. Med. 173:1213–1225.
   PubMed Web of Science ®Google Scholar
• Henthorn, P., M. Kiledjian, and T. Kadesch. 1990. Two distinct transcription factors that bind the immunoglobulin enhancer mE5/kE2 motif. Science 247:467–470.
   PubMed Web of Science ®Google Scholar
• Herman, A., J. W. Kappler, P. Marrack, and A. M. Pullen. 1991. Superantigens: mechanism of T cell stimulation and role in immune responses. Annu. Rev. Immunol. 9:745–772.
   PubMed Web of Science ®Google Scholar
• 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 beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948–962.
   PubMedGoogle Scholar
• Hsu, H. L., J. T. Cheng, Q. Chen, and R. Baer. 1991. Enhancer-binding activity of the tal-1 oncoprotein in association with the E47/E12 helix-loop-helix proteins. Mol. Cell. Biol. 14:1256–1265.
   Google Scholar
• Hsu, H., I. Wadman, J. L. Tsan, and R. Baer. 1994. Positive and negative transcriptional control by the TAL1 helix-loop-helix protein. Proc. Natl. Acad. Sci. USA 91:5947–5951.
   PubMedGoogle Scholar
• Kallioniemi, A., O.-P. Kallioniemi, D. Sudar, D. Rutovitz, J. W. Gray, F. Waldman, and D. Pinkel. 1992. Comparative genomic hybridization for molecular cytogenetic analysis of solid tumors. Science 258:818–821.
   PubMed Web of Science ®Google Scholar
• Lassar, A. B., J. N. Buskin, D. Lockshon, R. L. Davis, S. Apone, S. D. Hauschka, and H. Weintraub. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823–831.
   PubMedGoogle Scholar
• Lassar, A. B., R. L. Davis, W. E. Wright, T. Kadesch, C. Murre, A. Voronova, D. Baltimore, and H. Weintraub. 1991. Functional activity of myogenic HLH proteins requires hetero-oligomerization with E12/E47-like proteins in vivo. Cell 66:305–315.
   PubMed Web of Science ®Google Scholar
• Mallick, C., E. C. Dudley, J. L. Viney, M. J. Owen, and A. C. Hayday. 1993. Rearrangement and diversity of T cell receptor beta chain genes in thymocytes: a critical role for the beta chain in development. Cell 73:513–519.
   PubMed Web of Science ®Google Scholar
• Marcu, K. B., L. J. Harris, L. W. Stanton, J. Erikson, R. Watt, and C. M. Croce. 1983. Transcriptionally active c-myc oncogene is contained within NIARD, a DNA sequence associated with chromosome translocations in B-cell neoplasia. Proc. Natl. Acad. Sci. USA 80:519–523.
   PubMed Web of Science ®Google Scholar
• Massari, M. E., P. Jennings, and C. Murre. 1996. The AD1 transactivation domain of E2A contains a highly conserved helix which is required for its activity in both Saccharomyces cerevisiae and mammalian cells. Mol. Cell. Biol. 16:121–129.
   PubMedGoogle Scholar
• Melletin, J. D., S. D. Smith, and M. L. Cleary. 1989. lyl-1, a novel gene altered by chromosomal translocation in T cell lymphomas, codes for a protein with a helix-loop-helix DNA binding motif. Cell 58:77–84.
   PubMedGoogle Scholar
• Meyer, K. B., M. Skogberg, C. Margenfeld, J. Ireland, and S. Pettersson. 1995. Repression of the immunoglobulin heavy chain 3′ enhancer by helixloop-helix protein Id3 via a functionally important E47/E12 binding site: implications for developmental control of enhancer function. Eur. J. Immunol. 25:1770–1777.
   PubMed Web of Science ®Google Scholar
• Miyamoto, A., X. Cui, L. Naumovski, and M. L. Cleary. 1996. Helix-loop-helix proteins LYL-1 and E2A form heterodimeric complexes with distinctive DNA binding properties in hematolymphoid cells. Mol. Cell. Biol. 16:2394–2401.
   PubMedGoogle Scholar
• Mombaerts, P., A. R. Clarke, M. A. Rudnicki, J. Iacomini, S. Itohara, J. J. Lafaille, L. Wang, Y. Ichikawa, R. Jaenisch, M. L. Hooper, and S. Tonegawa. 1992. Mutations in T-cell antigen receptor genes a and b block thymocyte development at different developmental stages. Nature 360:225–231.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777–783.
   PubMed Web of Science ®Google Scholar
• Murre, C., P. S. McCaw, H. Vaessin, M. Caudy, L. Y. Jan, Y. N. Jan, C. V. Cabrera, J. N. Buskin, S. D. Hauschka, A. B. Lassar, H. Weintraub, and D. Baltimore. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537–544.
   PubMed Web of Science ®Google Scholar
• Murre, C., A. Voronova, and D. Baltimore. 1991. B-cell- and myocyte-specific E2-box-binding factors contain E12/E47-like subunits. Mol. Cell. Biol. 11:1156–1160.
   PubMedGoogle Scholar
• Peers, B., J. Leonard, S. Sharma, G. Teitelman, and M. R. Montminy. 1994. Insulin expression in pancreatic islet cells relies on cooperative interactions between the helix-loop-helix factor E47 and the homeobox factor STF-1. Mol. Endocrinol. 8:1798–1806.
   PubMedGoogle Scholar
• Penit, C., B. Lucas, and F. Vasseur. 1995. Cell expansion and growth arrest phases during the transition from precursor (CD4-8-) to immature (CD4181) thymocytes in normal and genetically modified mice. J. Immunol. 154:5103–5113.
   PubMed Web of Science ®Google Scholar
• Piper, J., D. Rutovitz, D. Sudar, A. Kallioniemi, O.-P. Kallioniemi, F. M. Waldman, J. W. Gray, and D. Pinkel. 1995. Computer image analysis of comparative genomic hybridization. Cytometry 19:10–26.
   PubMedGoogle Scholar
• Pongubala, J., and M. Atchison. 1991. Functional characterization of the developmentally controlled immunoglobulin kappa 3′ enhancer: regulation by Id, a repressor of helix-loop-helix transcription factors. Mol. Cell. Biol. 11:1040–1047.
   PubMedGoogle Scholar
• Quong, M. W., M. E. Massari, R. Zwart, and C. Murre. 1993. A new transcriptional activation motif restricted to a class of helix-loop-helix proteins is functionally conserved in both yeast and mammalian cells. Mol. Cell. Biol. 13:792–800.
   PubMedGoogle Scholar
• Roberts, V. J., R. Steenbergen, and C. Murre. 1993. Localization of E2A mRNA expression in developing and adult rat tissues. Proc. Natl. Acad. Sci. USA 90:7583–7587.
   PubMedGoogle Scholar
• Rolink, A., E. ten Boekel, F. Melchers, D. T. Fearon, I. Krop, and J. Andersson. 1996. A subpopulation of B2201 cells in murine bone marrow does not express CD19 and contains natural killer cell progenitors. J. Exp. Med. 183:187–194.
   PubMedGoogle Scholar
• Sawada, S., and D. R. Littman. 1993. A heterodimer of HEB and an E12-related protein interacts with the CD4 enhancer and regulates its activity in T-cell lines. Mol. Cell. Biol. 13:5620–5628.
   PubMedGoogle Scholar
• Shen, C. P., and T. Kadesch. 1995. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol. 15:4518–4524.
   PubMedGoogle Scholar
• Shinkai, Y., G. Rathbun, K.-P. Lam, E. M. Oltz, V. Stewart, M. Mendelsohn, J. Charron, M. Datta, F. Young, A. M. Stall, and F. W. Alt. 1992. RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855–867.
   PubMed Web of Science ®Google Scholar
• Stewart, M., E. Cameron, M. Campbell, R. McFarlane, S. Toth, K. Lang, D. Onions, and J. C. Neil. 1993. Conditional expression and oncogenicity of c-myc linked to a CD2 gene dominant control region. Int. J. Cancer 53:1023–1030.
   PubMed Web of Science ®Google Scholar
• Sun, X. H., and D. Baltimore. 1991. An inhibitory domain of E12 transcription factor prevents DNA binding in E12 homodimers but not in E12 heterodimers. Cell 64:459–470.
   PubMed Web of Science ®Google Scholar
• Sun, X. H. 1994. Constitutive expression of the Id1 gene impairs mouse B cell development. Cell 79:893–901.
   PubMed Web of Science ®Google Scholar
• Takeda, J., A. Cheng, F. Mauxion, C. A. Nelson, R. D. Newberry, W. C. Sha, R. Sen, and D. Y. Loh. 1990. Functional analysis of the murine T-cell receptor b enhancer and characteristics of its DNA-binding proteins. Mol. Cell. Biol. 10:5027–5035.
   PubMedGoogle Scholar
• von Boehmer, H. 1990. Developmental biology of T cells in T cell-receptor transgenic mice. Annu. Rev. Immunol. 8:531–556.
   PubMedGoogle Scholar
• Voronova, A. F., and D. Baltimore. 1990. Mutations that disrupt DNA binding and dimer formation in the E47 helix-loop-helix protein map to distinct domains. Proc. Natl. Acad. Sci. USA 87:4722–4726.
   PubMed Web of Science ®Google Scholar
• Voronova, A. F., and F. Lee. 1994. The E2A and tal-1 helix-loop-helix proteins associate in vivo and are modulated by Id proteins during interleukin-6 induced myeloid differentiation. Proc. Natl. Acad. Sci. USA 91:5952–5956.
   PubMedGoogle Scholar
• Whelan, J., S. R. Cordle, E. Henderson, P. A. Weil, and R. Stein. 1990. Identification of a pancreatic b-cell insulin gene transcription factor that binds to and appears to activate cell-type-specific gene expression: its possible relationship to other cellular factors that bind to a common insulin gene sequence. Mol. Cell. Biol. 10:1564–1572.
   PubMedGoogle Scholar
• Wilson, A., A. D’Amico, T. Ewing, R. Scollay, and K. Shortman. 1988. Subpopulations of early thymocytes. A cross-correlation flow cytometric analysis of adult mouse Ly-2-L3T4- (CD8-CD4-) thymocytes using eight different surface markers. J. Immunol. 140:1461–1470.
   PubMedGoogle Scholar
• Xia, Y., L. Brown, C. Y. C. Yang, J. T. Tsan, M. J. Siciliano, I. Espinosas, M. M. LeBeau, and R. Baer. 1991. TAL-2, a helix-loop-helix gene activated by the (7;9)(q34;32) translocation in human T-cell lymphoma. Proc. Natl. Acad. Sci. USA 88:11416–11420.
   PubMed Web of Science ®Google Scholar
• Xia, Y., L. Y. Hwang, M. H. Cobb, and R. Baer. 1994. Products of the tal2 oncogene in leukemic T cells: bHLH phosphoproteins with DNA-binding activity. Oncogene 9:1437–1446.
   PubMedGoogle Scholar
• Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B cell formation. Cell 79:875–885.
   PubMedGoogle Scholar
• Zuniga-Pflucker, J. C., D. Jiang, and M. J. Lenardo. 1995. Requirement for TNF-a and IL-1a in fetal thymocyte commitment and differentiation. Science 268:1906–1909.
   PubMedGoogle Scholar
• Zuniga-Pflucker, J. C., and M. Lenardo. 1996. Regulation of thymocyte development from immature progenitors. Curr. Opin. Immunol. 8:215–224.
   PubMed Web of Science ®Google Scholar