E2A and HEB are required to block thymocyte proliferation prior to pre-TCR expression

Journal of Immunology

Volumn 178, Issue 9, 2007, Pages 5717-5726

  Wojciechowski, Jason ^a   Lai, Anne ^a   Kondo, Motorari ^a   Zhuang, Yuan ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; INTERLEUKIN 7; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSCRIPTION FACTOR E2A;

ANIMAL CELL; ARTICLE; CELL CYCLE ARREST; CELL CYCLE PROGRESSION; CONTROLLED STUDY; FLOW CYTOMETRY; GENE DELETION; GENE REARRANGEMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; THYMOCYTE;

EID: 34247627897     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.9.5717     Document Type: Article

References (43)

1. - triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150: 4244-4252.
2. Tourigny, M. R., S. Mazel, D. B. Burtrum, and H. T. Petrie. 1997. T cell receptor (TCR)-β gene recombination: dissociation from cell cycle regulation and developmental progression during T cell ontogeny. J. Exp. Med. 185: 1549-1556.
3. 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.
4. 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, et al. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58: 537-544.
5. Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61: 49-59.
6. 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.
7. Shen, C. P., and T. Kadesch. 1995. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol. 15: 4518-4524.
8. Greenbaum, S., and Y. Zhuang. 2002. Identification of E2A target genes in B lymphocyte development by using a gene tagging-based chromatin immunoprecipitation system. Proc. Natl. Acad. Sci. USA 99: 15030-15035.
9. Takeuchi, A., S. Yamasaki, K. Takase, F. Nakatsu, H. Arase, M. Onodera, and T. Saito. 2001. E2A and HEB activate the pre-TCRα promoter during immature T cell development. J. Immunol. 167: 2157-2163.
10. Kee, B. L., G. Bain, and C. Murre. 2002. IL-7Rα and E47: independent pathways required for development of multipotent lymphoid progenitors. EMBO J. 21: 103-113.
11. Bain, G., I. Engel, E. C. Robanus Maandag, H. P. te Riele, J. R. Voland, L. L. Sharp, J. Chun, B. Huey, D. Pinkel, and C. Murre. 1997. E2A deficiency leads to abnormalities in αβ T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17: 4782-4791.
12. Yan, W., A. Z. Young, V. C. Soares, R. Kelley, R. Benezra, and Y. Zhuang. 1997: High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17: 7317-7327.
13. Barndt, R., M. F. Dai, and Y. Zhuang. 1999. A novel role for HEB downstream or parallel to the pre-TCR signaling pathway during αβ thymopoiesis. J. Immunol. 163: 3331-3343.
14. Kim, D., X. C. Peng, and X. H. Sun. 1999. Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Mol. Cell. Biol. 19: 8240-8253.
15. Morrow, M. A., E. W. Mayer, C. A. Perez, M. Adlam, and G. Siu. 1999. Over-expression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Mol. Immunol. 36: 491-503.
16. Zhuang, Y., R. J. Barndt, L. Pan, R. Kelley, and M. Dai. 1998. Functional replacement of the mouse E2A gene with a human HEB cDNA. Mol. Cell. Biol. 18: 3340-3349.
17. Barndt, R. J., M. Dai, and Y. Zhuang. 2000. Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Mol. Cell. Biol. 20: 6677-6685.
18. Pan, L., J. Hanrahan, J. Li, L. P. Hale, and Y. Zhuang. 2002. An analysis of T cell intrinsic roles of E2A by conditional gene disruption in the thymus. J. Immunol. 168: 3923-3932.
19. Jackson, A., H. D. Kondilis, B. Khor, B. P. Sleckman, and M. S. Krangel. 2005. Regulation of T cell receptor β allelic exclusion at a level beyond accessibility. Nat. Immunol. 6: 189-197.
20. Lazorchak, A. S., J. Wojciechowski, M. F. Dai, and Y. Zhuang. 2006. E2A promotes the survival of precursor and mature B lymphocytes. J. Immunol. 177: 2495-2504.
21. 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.
22. Barndt, R. J., and Y. Zhuang. 1999. Controlling lymphopoiesis with a combinatorial E-protein code. Cold Spring Harbor Symp. Quant. Biol. 64: 45-50.
23. Petersson, K., F. Ivars, and M. Sigvardsson. 2002. The pTα promoter and enhancer are direct targets for transactivation by E box-binding proteins. Eur. J. Immunol. 32: 911-920.
24. Tremblay, M., S. Herblot, E. Lecuyer, and T. Hoang. 2003. Regulation of pTα gene expression by a dosage of E2A, HEB, and SCL. J. Biol. Chem. 278: 12680-12687.
25. Wilson, A., C. Marechal, and H. R. MacDonald. 2001. Biased Vβ usage in immature thymocytes is independent of DJβ proximity and pTα pairing. J. Immunol. 166: 51-57.
26. Taghon, T., M. A. Yui, R. Pant, R. A. Diamond, and E. V. Rothenberg. 2006. Developmental and molecular characterization of emerging β- and γδ-selected pre-T cells in the adult mouse thymus. Immunity 24: 53-64.
27. Fehling, H. J., A. Krotkova, C. Saint-Ruf, and H. von Boehmer. 1995. Crucial role of the pre-T-cell receptorα gene in development of αβ but not γδ T cells. Nature 375: 795-798.
28. 1-phase progression. Genes Dev. 13: 1501-1512.
29. Kozar, K., M. A. Ciemerych, V. I. Rebel, H. Shigematsu, A. Zagozdzon, E. Sicinska, Y. Geng, Q. Yu, S. Bhattacharya, R. T. Branson, et al. 2004. Mouse development and cell proliferation in the absence of D-cyclins. Cell 118: 477-491.
30. Prabhu, S., A. Ignatova, S. T. Park, and X. H. Sun. 1997. Regulation of the expression of cyclin-dependent kinase inhibitor p21 by E2A and Id proteins. Mol. Cell. Biol. 17: 5888-5896.
31. Herblot, S., P. D. Aplan, and T. Hoang. 2002. Gradient of E2A activity in B-cell development. Mol. Cell. Biol. 22: 886-900.
32. Pagliuca, A., P. Gallo, P. De Luca, and L. Lania. 2000. Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res. 60: 1376-1382.
33. Schwartz, R., I. Engel, M. Fallahi-Sichani, H. T. Petrie, and C. Murre. 2006. Gene expression patterns define novel roles for E47 in cell cycle progression, cytokine-mediated signaling, and T lineage development. Proc. Natl. Acad. Sci. USA 103: 9976-9981.
34. Kip1 mediate two separate pathways to collaboratively suppress pituitary tumorigenesis. Genes Dev. 12: 2899-2911.
35. Kip1 display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85: 707-720.
36. 1 checkpoint control. Cell 82: 675-684.
37. Jiang, Q., W. Q. Li, F. B. Aiello, R. Mazzucchelli, B. Asefa, A. R. Khaled, and S. K. Durum. 2005. Cell biology of IL-7, a key lymphotrophin. Cytokine Growth Factor Rev. 16: 513-533.
38. Zhuang, Y., P. Cheng, and H. Weintraub. 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.
39. Li, L., and E. N. Olson. 1992. Regulation of muscle cell growth and differentiation by the MyoD family of helix-loop-helix proteins. Adv. Cancer Res. 58: 95-119.
40. Engel, I., and C. Murre. 2001. The function of E- and Id proteins in lymphocyte development. Nat. Rev. Immunol. 1: 193-199.
41. Engel, I., and C. Murre. 2004. E2A proteins enforce a proliferation checkpoint in developing thymocytes. EMBO J. 23: 202-211.
42. Pagano, M., S. W. Tam, A. M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P. R. Yew, G. F. Draetta, and M. Rolfe. 1995. Role of the ubiquitin-proteasome pathway in regulating abundance of the cyclin-dependent kinase inhibitor p27. Science 269: 682-685.
43. Robey, E. A., and J. A. Bluestone. 2004. Notch signaling in lymphocyte development and function. Curr. Opin. Immunol. 16: 360-366.