E2A proteins enforce a proliferation checkpoint in developing thymocytes

EMBO Journal

Volumn 23, Issue 1, 2004, Pages 202-211

  Engel, Isaac ^a   Murre, Cornelis ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

selection; Cell cycle; E proteins; Id; T cell development

Indexed keywords

LAT PROTEIN; PROTEIN; PROTEIN BCL 2; PROTEIN KINASE FYN; PROTEIN KINASE LCK; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR BETA CHAIN; TRANSCRIPTION FACTOR E2A; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARCINOGENESIS; CELL CYCLE; CELL MATURATION; CELL PROLIFERATION; CONTROLLED STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; THYMOCYTE;

ANIMALS; ANTIGENS, CD8; CELL CYCLE; CELL DIFFERENTIATION; CELL DIVISION; DNA-BINDING PROTEINS; DOWN-REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; GENES, HOMEOBOX; HETEROZYGOTE; HOMEODOMAIN PROTEINS; HOMOZYGOTE; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION; PROTO-ONCOGENE PROTEINS C-BCL-2; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTES; TCF TRANSCRIPTION FACTORS; THYMUS GLAND; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 0842285394     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600017     Document Type: Article

References (58)

1. Alani RM, Young AZ, Shifflett CB (2001) Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc Natl Acad Sci USA 98: 7812-7816
2. Appleby MW, Gross JA, Cooke MP, Levin SD, Qian X, Perlmutter RM (1992) Defective T cell receptor signaling in mice lacking the thymic isoform of p59fyn. Cell 70: 751-763
3. Asp J, Thornemo M, Inerot S, Lindahl A (1998) The helix-loop-helix transcription factors Id1 and Id3 have a functional role in control of cell division in human normal and neoplastic chondrocytes. FEBS Lett 438: 85-90
4. Bain G, Cravatt CB, Loomans C, Alberola-Ila J, Hedrick SM, Murre C (2001) Regulation of the helix-loop-helix proteins, E2A and Id3, by the Ras-ERK MAPK cascade. Nat Immunol 2: 165-171
5. Bain G, Engel I, Maandag ECR, Riele HPJt, Voland JR, Sharp LL, Chun J, Huey B, Pinkel D, Murre C (1997a) E2A deficiency leads to abnormalities in αβ T-cell development and to rapid development of T-cell lymphomas. Mol Cell Biol 17: 4782-4791
6. Bain G, Maandag E, Izon D, Amsen D, Kruisbeek A, Weintraub B, Krop I, Schlissel M, Feeney A, van Roon M, van der Valk M, te Riele H, Berns A, Murre C (1994) E2A proteins are required for proper B cell development and initiation of immunoglobulin gene rearrangements. Cell 79: 885-892
7. Bain G, Maandag ECR, Riele H, Feeney AJ, Sheehy A, Schlissel M, Shinton SA, Hardy RR, Murre C (1997b) Both E12 and E47 allow commitment to the B cell lineage. Immunity 6: 145-154
8. Bain G, Quong MW, Soloff RS, Hedrick SM, Murre C (1999) Thymocyte maturation is regulated by the activity of the helix-loop-helix protein, E47. J Exp Med 190: 1605-1616
9. Barndt R, Dai MF, Zhuang Y (1999) A novel role for HEB down-stream or parallel to the pre-TCR signaling pathway during alpha beta thymopoiesis. J Immunol 163: 3331-3343
10. Barndt RJ, Dai M, Zhuang Y (2000) Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Mol Cell Biol 20: 6677-6685
11. Bergqvist I, Eriksson M, Saarikettu J, Eriksson B, Corneliussen B, Grundstrom T, Holmberg D (2000) The basic helix-loop-helix transcription factor E2-2 is involved in T lymphocyte development. Eur J Immunol 30: 2857-2863
12. Cantrell D (1996) T cell antigen receptor signal transduction pathways. Annu Rev Immunol 14: 259-274
13. Carayon P, Bord A (1992) Identification of DNA-replicating lymphocyte subsets using a new method to label the bromodeoxyuridine incorporated into the DNA. J Immunol Methods 147: 225-230
14. Engel I, Johns C, Bain G, Rivera RR, Murre C (2001) Early thymocyte development is regulated by modulation of E2A protein activity. J Exp Med 194: 733-745
15. Engel I, Murre C (1999) Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc Natl Acad Sci USA 96: 996-1001
16. Engel I, Murre C (2002) Disruption of pre-TCR expression accelerates lymphomagenesis in E2A-deficient mice. Proc Natl Acad Sci USA 99: 11322-11327
17. Falk I, Nerz G, Haidl I, Krotkova A, Eichmann K (2001) Immature thymocytes that fail to express TCRbeta and/or TCRgamma delta proteins die by apoptotic cell death in the CD44(-)CD25(-) (DN4) subset. Eur J Immunol 31: 3308-3317
18. Ghosh JK, Romanow WJ, Murre C (2001) Induction of a diverse T cell receptor gamma/delta repertoire by the helix-loop-helix proteins E2A and HEB in nonlymphoid cells. J Exp Med 193: 769-776
19. Gounari F, Aifantis I, Khazaie K, Hoeflinger S, Harada N, Taketo MM, von Boehmer H (2001) Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat Immunol 2: 863-869
20. Groves T, Smiley P, Cooke MP, Forbush K, Perlmutter RM, Guidos CJ (1996) Fyn can partially substitute for Lck in T lymphocyte development. Immunity 5: 417-428
21. Heemskerk MHM, Blom B, Nolan G, Stegmann APA, Bakker AQ, Weijer K, Res PCM, 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
22. Herblot S, Steff AM, Hugo P, Aplan PD, Hoang T (2000) SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat Immunol 1: 138-144
23. Hoffman ES, Passoni L, Crompton T, Leu TMJ, Schatz DG, Koff A, Owen MJ, Hayday AC (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
24. Jacobs H, Vandeputte D, Tolkamp L, Vries Ed, Borst J, Berns A (1994) CD3 components at the surface of pro-T cells can mediate pre-T cell development in vivo. Eur J Immunol 24: 934-939
25. Kim D, Peng XC, Sun XH (1999) Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Mol Cell Biol 19: 8240-8253
26. Kim D, Xu M, Nie L, Peng XC, Jimi E, Voll RE, Nguyen T, Ghosh S, Sun XH (2002) Helix-loop-helix proteins regulate pre-TCR and TCR signaling through modulation of Rel/NF-kappaB activities. Immunity 16: 9-21
27. Kruisbeek AM, Haks MC, Carleton M, Michie AM, Zuniga-Pflucker JC, Wiest DL (2000) Branching out to gain control: how the pre-TCR is linked to multiple functions. Immunol Today 21: 637-644
28. Lasorella A, Noseda M, Beyna M, Yokota Y, Iavarone A (2000) Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 407: 592-598
29. Levelt CN, Mombaerts P, Iglesias A, Tonegawa S, Eichmann K (1993) Restoration of early thymocyte differentiation in T-cell receptor beta-chain-deficient mutant mice by transmembrane signaling through CD3 epsilon. Proc Natl Acad Sci USA 90: 11401-11405
30. Lind EF, Wayne J, Wang QZ, Staeva T, Stolzer A, Petrie HT (1999) Bcl-2-induced changes in E2F regulatory complexes reveal the potential for integrated cell cycle and cell death functions. J Immunol 162: 5374-5379
31. Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20: 429-440
32. lck. Nature 357: 161-164
33. Morrow MA, Mayer EW, Perez CA, Adlam M, Siu G (1999) Overexpression of the helix-loop-helix protein Id2 blocks T cell development at multiple stages. Mol Immunol 36: 491-503
34. Nishimori H, Sasaki Y, Yoshida K, Irifune H, Zembutsu H, Tanaka T, Aoyama T, Hosaka T, Kawaguchi S, Wada T, Hata J, Toguchida J, Nakamura Y, Tokino T (2002) The Id2 gene is a novel target of transcriptional activation by EWS-ETS fusion proteins in Ewing family tumors. Oncogene 21: 8302-8309
35. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E (2001) Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409: 1067-1070
36. Pan L, Hanrahan J, Li J, Hale LP, Zhuang Y (2002) An analysis of T cell intrinsic roles of E2A by conditional gene disruption in the thymus. J Immunol 168: 3923-3932
37. Park ST, Nolan GP, Sun X-H (1999) Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. J Exp Med 189: 501-508
38. Penit C, Lucas B, Vasseur F (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
39. Peverali F, Ramqvist T, Saffrich R, Pepperkok R, Barone M, Philipson L (1994) Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO J 13: 4291-4301
40. Reizis B, Leder P (2001) The upstream enhancer is necessary and sufficient for the expression of the pre-T cell receptor {alpha} gene in immature T lymphocytes. J Exp Med 194: 979-990
41. Rivera RR, Johns CP, Quan J, Johnson RS, Murre C (2000) Thymocyte selection is regulated by the helix-loop-helix inhibitor protein, Id3. Immunity 12: 17-26
42. Rockman SP, Currie SA, Ciavarella M, Vincan E, Dow C, Thomas RJ, Phillips WA (2001) Id2 is a target of the beta-catenin/T cell factor pathway in colon carcinoma. J Biol Chem 276: 45113-45119
43. Romanow WJ, Langerak AW, Goebel P, Wolvers-Tettero IL, van Dongen JJ, Feeney AJ, Murre C (2000) E2A and EBF act in synergy with the V(D)J recombinase to generate a diverse immunoglobulin repertoire in nonlymphoid cells. Mol Gell 5: 343-353
44. Schlissel M, Voronova A, Baltimore D (1991) Helix-loop-helix transcription factor-E47 activates germ-line immunoglobulin heavy-chain gene transcription and rearrangement in a pre-T-cell line. Genes Dev 5: 1367-1376
45. Schmid I, Uittenbogaart CH, Giorgi JV (1991) A gentle fixation and permeabilization method for combined cell surface and intracellular staining with improved precision in DNA quantification. Cytometry 12: 279-285
46. -/- mice in the absence of TCRβ chain expression. Int Immunol 6: 995-1001
47. Takeuchi A, Yamasaki S, Takase K, Nakatsu F, Arase H, Onodera M, Saito T (2001) E2A and HEB activate the pre-TCRalpha promoter during immature T cell development. J Immunol 167: 2157-2163
48. van Oers NS, Lowin-Kropf B, Finlay D, Connolly K, Weiss A (1996) Alpha beta T cell development is abolished in mice lacking both Lck and Fyn protein tyrosine kinases. Immunity 5: 429-436
49. Veis DJ, Sentman CL, Bach EA, Korsmeyer SJ (1993) Expression of the Bcl-2 protein in murine and human thymocytes and in peripheral T-lymphocytes. J Immunol 151: 2546-2554
50. Voll RE, Jimi E, Phillips RJ, Barber DF, Rincon M, Hayday AC, Flavell RA, Ghosh S (2000) NF-kappa B activation by the pre-T cell receptor serves as a selective survival signal in T lymphocyte development. Immunity 13: 677-689
51. Wang X, Xu K, Ling MT, Wong YC, Feng HC, Nicholls J, Tsao SW (2002) Evidence of increased Id-1 expression and its role in cell proliferation in nasopharyngeal carcinoma cells. Mol Carcinogen 35: 42-49
52. Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y (1997) High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol Cell Biol 17: 7317-7327
53. Zhang W, Sloan-Lancaster J, Kitchen J, Trible RP, Samelson LE (1998) LAT: the ZAP-70 tyrosine kinase substrate that links T cell receptor to cellular activation. Cell 92: 83-92
54. Zhang W, Sommers CL, Burshtyn DN, Stebbins CC, DeJarnette JB, Trible RP, Grinberg A, Tsay HC, Jacobs HM, Kessler CM, Long EO, Love PE, Samelson LE (1999) Essential role of LAT in T cell development. Immunity 10: 323-332
55. Zhao F, Vilardi A, Neely RJ, Choi JK (2001) Promotion of cell cycle progression by basic helix-loop-helix E2A. Mol Cell Biol 21: 6346-6357
56. Zhuang Y, Barndt RJ, Pan L, Kelley R, Dai M (1998) Functional replacement of the mouse E2A gene with a human HEB cDNA. Mol Cell Biol 18: 3340-3349
57. Zhuang Y, Soriano P, Weintraub H (1994) The helix-loop-helix gene E2A is required for B cell formation. Cell 79: 875-884
58. Zuniga-Pflucker JC, Lenardo MJ (1996) Regulation of thymocyte development from immature progenitors. Curr Opin Immunol 8: 215-224