The basic helix-loop-helix transcription factor TAL1/SCL inhibits the expression of the p16INK4A and pTα genes

Biochemical and Biophysical Research Communications

Volumn 312, Issue 4, 2003, Pages 1073-1081

  Hansson, Anders ^a   Manetopoulos, Christina ^a   Jönsson, Jan Ingvar ^a   Axelson, Håkan ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

Cell cycle; E boxes; p16; Promoter; pT ; TAL1

Indexed keywords

HELIX LOOP HELIX PROTEIN; ONCOPROTEIN; PROTEIN P16; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR SCL; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; E BOX ELEMENT; FEMALE; GENE ACTIVITY; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DNA BINDING; T LYMPHOCYTE; TRANSCRIPTION INITIATION;

EID: 0344926374     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2003.11.030     Document Type: Article

References (46)

1. Chen Q., Cheng J.T., Tasi L.H., Schneider N., Buchanan G., Carroll A., Crist W., Ozanne B., Siciliano M.J., Baer R. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J. 9:1990;415-424.
2. Finger L.R., Kagan J., Christopher G., Kurtzberg J., Hershfield M.S., Nowell P.C., Croce C.M. Involvement of the TCL5 gene on human chromosome 1 in T-cell leukemia and melanoma. Proc. Natl. Acad. Sci. USA. 86:1989;5039-5043.
3. Begley C.G., Aplan P.D., Denning S.M., Haynes B.F., Waldmann T.A., Kirsch I.R. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. USA. 86:1989;10128-10132.
4. Shivdasani R.A., Mayer E.L., Orkin S.H. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature. 373:1995;432-434.
5. Visvader J.E., Fujiwara Y., Orkin S.H. Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development. Genes Dev. 12:1998;473-479.
6. Porcher C., Swat W., Rockwell K., Fujiwara Y., Alt F.W., Orkin S.H. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell. 86:1996;47-57.
7. Hsu H.L., Cheng J.T., Chen Q., Baer R. Enhancer-binding activity of the tal-1 oncoprotein in association with the E47/E12 helix-loop-helix proteins. Mol. Cell. Biol. 11:1991;3037-3042.
8. Hsu H.L., Wadman I., Baer R. Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells. Proc. Natl. Acad. Sci. USA. 91:1994;3181-3185.
9. Vitelli L., Condorelli G., Lulli V., Hoang T., Luchetti L., Croce C.M., Peschle C. A pentamer transcriptional complex including tal-1 and retinoblastoma protein downmodulates c-kit expression in normal erythroblasts. Mol. Cell. Biol. 20:2000;5330-5342.
10. Lecuyer E., Herblot S., Saint-Denis M., Martin R., Begley C.G., Porcher C., Orkin S.H., Hoang T. The SCL complex regulates c-kit expression in hematopoietic cells through functional interaction with Sp1. Blood. 100:2002;2430-2440.
11. Hsu H.L., Wadman I., Tsan J.T., Baer R. Positive and negative transcriptional control by the TAL1 helix-loop-helix protein. Proc. Natl. Acad. Sci. USA. 91:1994;5947-5951.
12. Herblot S., Steff A.M., Hugo P., Aplan P.D., Hoang T. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat. Immunol. 1:2000;138-144.
13. Krosl G., He G., Lefrancois M., Charron F., Romeo P.H., Jolicoeur P., Kirsch I.R., Nemer M., Hoang T. Transcription factor SCL is required for c-kit expression and c-Kit function in hemopoietic cells. J. Exp. Med. 188:1998;439-450.
14. Carroll A.J., Crist W.M., Link M.P., Amylon M.D., Pullen D.J., Ragab A.H., Buchanan G.R., Wimmer R.S., Vietti T.J. The t(1;14)(p34;q11) is nonrandom and restricted to T-cell acute lymphoblastic leukemia: a pediatric oncology group study. Blood. 76:1990;1220-1224.
15. Bash R.O., Hall S., Timmons C.F., Crist W.M., Amylon M., Smith R.G., Baer R. Does activation of the TAL1 gene occur in a majority of patients with T-cell acute lymphoblastic leukemia? A pediatric oncology group study. Blood. 86:1995;666-676.
16. Brown L., Cheng J.T., Chen Q., Siciliano M.J., Crist W., Buchanan G., Baer R. Site-specific recombination of the tal-1 gene is a common occurrence in human T cell leukemia. EMBO J. 9:1990;3343-3351.
17. Kelliher M.A., Seldin D.C., Leder P. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase IIalpha. EMBO J. 15:1996;5160-5166.
18. Condorelli G.L., Facchiano F., Valtieri M., Proietti E., Vitelli L., Lulli V., Huebner K., Peschle C., Croce C.M. T-cell-directed TAL-1 expression induces T-cell malignancies in transgenic mice. Cancer Res. 56:1996;5113-5119.
19. Anderegg B., Horstmann M., Kabisch H. Effects of anti-tal-1 oligodeoxynucleotides in T-ALL cell lines. Cancer Gene Ther. 4:1997;84-90.
20. Valtieri M., Tocci A., Gabbianelli M., Luchetti L., Masella B., Vitelli L., Botta R., Testa U., Condorelli G.L., Peschle C. Enforced TAL-1 expression stimulates primitive, erythroid and megakaryocytic progenitors but blocks the granulopoietic differentiation program. Cancer Res. 58:1998;562-569.
21. Condorelli G.L., Tocci A., Botta R., Facchiano F., Testa U., Vitelli L., Valtieri M., Croce C.M., Peschle C. Ectopic TAL-1/SCL expression in phenotypically normal or leukemic myeloid precursors: proliferative and antiapoptotic effects coupled with a differentiation blockade. Mol. Cell. Biol. 17:1997;2954-2969.
22. Elwood N.J., Zogos H., Pereira D.S., Dick J.E., Begley C.G. Enhanced megakaryocyte and erythroid development from normal human CD34(+) cells: consequence of enforced expression of SCL. Blood. 91:1998;3756-3765.
23. Pagliuca A., Gallo P., De Luca P., Lania L. Class A helix-loop-helix proteins are positive regulators of several cyclin-dependent kinase inhibitors' promoter activity and negatively affect cell growth. Cancer Res. 60:2000;1376-1382.
24. Alani R.M., Young A.Z., Shifflett C.B. Id1 regulation of cellular senescence through transcriptional repression of p16/Ink4a. Proc. Natl. Acad. Sci. USA. 98:2001;7812-7816.
25. Sherr C.J. Cancer cell cycles. Science. 274:1996;1672-1677.
26. Kamb A., Gruis N.A., Weaver-Feldhaus J., Liu Q., Harshman K., Tavtigian S.V., Stockert E., Day 3rd R.S., Johnson B.E., Skolnick M.H. A cell cycle regulator potentially involved in genesis of many tumor types. Science. 264:1994;436-440.
27. Nobori T., Miura K., Wu D.J., Lois A., Takabayashi K., Carson D.A. Deletions of the cyclin-dependent kinase-4 inhibitor gene in multiple human cancers. Nature. 368:1994;753-756.
28. Okamoto A., Demetrick D.J., Spillare E.A., Hagiwara K., Hussain S.P., Bennett W.P., Forrester K., Gerwin B., Serrano M., Beach D.H.et al. Mutations and altered expression of p16INK4 in human cancer. Proc. Natl. Acad. Sci. USA. 91:1994;11045-11049.
29. Omura-Minamisawa M., Diccianni M.B., Batova A., Chang R.C., Bridgeman L.J., Yu J., Pullen J., Bowman W.P., Yu A.L. Universal inactivation of both p16 and p15 but not downstream components is an essential event in the pathogenesis of T-cell acute lymphoblastic leukemia. Clin. Cancer Res. 6:2000;1219-1228.
30. Petersson K., Ivars F., Sigvardsson M. The pT alpha promoter and enhancer are direct targets for transactivation by E box-binding proteins. Eur. J. Immunol. 32:2002;911-920.
31. Hara E., Smith R., Parry D., Tahara H., Stone S., Peters G. Regulation of p16CDKN2 expression and its implications for cell immortalization and senescence. Mol. Cell. Biol. 16:1996;859-867.
32. Manetopoulos C., Hansson A., Karlsson J., Jonsson J.I., Axelson H. The LIM-only protein LMO4 modulates the transcriptional activity of HEN1. Biochem. Biophys. Res. Commun. 307:2003;891-899.
33. Tremblay M., Herblot S., Lecuyer E., Hoang T. Regulation of pT alpha gene expression by a dosage of E2A, HEB, and SCL. J. Biol. Chem. 278:2003;12680-12687.
34. Hsu H.L., Huang L., Tsan J.T., Funk W., Wright W.E., Hu J.S., Kingston R.E., Baer R. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol. Cell. Biol. 14:1994;1256-1265.
35. Bain G., Engel I., Robanus Maandag E.C., te Riele H.P., Voland J.R., Sharp L.L., Chun J., Huey B., Pinkel D., Murre C. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17:1997;4782-4791.
36. Yan W., Young A.Z., Soares V.C., Kelley R., Benezra R., Zhuang Y. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17:1997;7317-7327.
37. Chervinsky D.S., Zhao X.F., Lam D.H., Ellsworth M., Gross K.W., Aplan P.D. Disordered T-cell development and T-cell malignancies in SCL LMO1 double-transgenic mice: parallels with E2A-deficient mice. Mol. Cell. Biol. 19:1999;5025-5035.
38. Park S.T., Nolan G.P., Sun X.H. Growth inhibition and apoptosis due to restoration of E2A activity in T cell acute lymphoblastic leukemia cells. J. Exp. Med. 189:1999;501-508.
39. Engel I., Murre C. Ectopic expression of E47 or E12 promotes the death of E2A-deficient lymphomas. Proc. Natl. Acad. Sci. USA. 96:1999;996-1001.
40. Park S.T., Sun X.H. The Tal1 oncoprotein inhibits E47-mediated transcription. Mechanism of inhibition. J. Biol. Chem. 273:1998;7030-7037.
41. Doyle K., Zhang Y., Baer R., Bina M. Distinguishable patterns of protein-DNA interactions involving complexes of basic helix-loop-helix proteins. J. Biol. Chem. 269:1994;12099-12105.
42. Huang S., Brandt S.J. mSin3A regulates murine erythroleukemia cell differentiation through association with the TAL1 (or SCL) transcription factor. Mol. Cell. Biol. 20:2000;2248-2259.
43. O'Neil J., Billa M., Oikemus S., Kelliher M. The DNA binding activity of TAL-1 is not required to induce leukemia/lymphoma in mice. Oncogene. 20:2001;3897-3905.
44. Aplan P.D., Jones C.A., Chervinsky D.S., Zhao X., Ellsworth M., Wu C., McGuire E.A., Gross K.W. An scl gene product lacking the transactivation domain induces bony abnormalities and cooperates with LMO1 to generate T-cell malignancies in transgenic mice. EMBO J. 16:1997;2408-2419.
45. Ohtani N., Zebedee Z., Huot T.J., Stinson J.A., Sugimoto M., Ohashi Y., Sharrocks A.D., Peters G., Hara E. Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature. 409:2001;1067-1070.
46. Peverali F.A., Ramqvist T., Saffrich R., Pepperkok R., Barone M.V., Philipson L. Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO J. 13:1994;4291-4301.