Lyl1 interacts with CREB1 and alters expression of CREB1 target genes

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1783, Issue 3, 2008, Pages 503-517

  San Marina, Serban ^a   Han, YouQi ^a   Suarez Saiz, Fernando ^a   Trus, Michael R ^b   Minden, Mark D ^a  

^a PRINCESS MARGARET HOSPITAL   (Canada)

^b HENDERSON GENERAL HOSPITAL   (Canada)

Author keywords

Acute myelogenous leukemia; CREB1; Gene expression; Helix loop helix transcription factor; Lyl1; Tal1

Indexed keywords

BRCA1 PROTEIN; CRE RECOMBINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; CYCLIN D3; EARLY GROWTH RESPONSE FACTOR 1; GENE PRODUCT; HISTONE ACETYLTRANSFERASE; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 3; PROTEIN BTG2; PROTEIN CBP; PROTEIN LYL1; PROTEIN P300; TRANSCRIPTION FACTOR TAL1; TUMOR PROTEIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING SITE; CHROMATIN IMMUNOPRECIPITATION; COMPLEX FORMATION; CONTROLLED STUDY; GENE TARGETING; HUMAN; HUMAN CELL; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; TRANSACTIVATION; TRANSCRIPTION INITIATION; UPREGULATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CERCOPITHECUS AETHIOPS; COS CELLS; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA; E1A-ASSOCIATED P300 PROTEIN; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEINS; K562 CELLS; NEOPLASM PROTEINS; PROMOTER REGIONS (GENETICS); PROTEIN BINDING; TRANSFECTION;

EID: 39149126346     PISSN: 01674889     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2007.11.015     Document Type: Article

References (62)

1. Greenbaum S., and Zhuang Y. Regulation of early lymphocyte development by E2A family proteins. Semin. Immunol. 14 (2002) 405-414
2. Quong M.W., Romanow W.J., and Murre C. E protein function in lymphocyte development. Annu. Rev. Immunol. 20 (2002) 301-322
3. Herblot S., Aplan P.D., and Hoang T. Gradient of E2A activity in B-cell development. Mol. Cell Biol. 22 (2002) 886-900
4. Rivera R., and Murre C. The regulation and function of the Id proteins in lymphocyte development. Oncogene 20 (2001) 8308-8316
5. Bernard O., Guglielmi P., Jonveaux P., Cherif D., Gisselbrecht S., Mauchauffe M., Berger R., Larsen C.J., and Mathieu-Mahul D. Two distinct mechanisms for the SCL gene activation in the t(1;14) translocation of T-cell leukemias. Genes, Chromosomes Cancer 1 (1990) 194-208
6. Chen Q., Yang C.Y., Tsan J.T., Xia Y., Ragab A.H., Peiper S.C., Carroll A., and Baer R. Coding sequences of the tal-1 gene are disrupted by chromosome translocation in human T cell leukemia. J. Exp. Med. 172 (1990) 1403-1408
7. Saltman D.L., Mellentin J.D., Smith S.D., and Cleary M.L. Mapping of translocation breakpoints on the short arm of chromosome 19 in acute leukemias by in situ hybridization. Genes, Chromosomes Cancer 2 (1990) 259-265
8. Begley C.G., Aplan P.D., Denning S.M., Haynes B.F., Waldmann T.A., and Kirsch I.R. The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 10128-10132
9. Mellentin J.D., Smith S.D., and Cleary M.L. lyl-1, a novel gene altered by chromosomal translocation in T cell leukemia, codes for a protein with a helix-loop-helix DNA binding motif. Cell 58 (1989) 77-83
10. Begley C.G., Aplan P.D., Davey M.P., Nakahara K., Tchorz K., Kurtzberg J., Hershfield M.S., Haynes B.F., Cohen D.I., and Waldmann T.A. Chromosomal translocation in a human leukemic stem-cell line disrupts the T-cell antigen receptor delta-chain diversity region and results in a previously unreported fusion transcript. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 2031-2035
11. Finger L.R., Kagan J., Christopher G., Kurtzberg J., Hershfield M.S., Nowell P.C., and Croce C.M. Involvement of the TCL5 gene on human chromosome 1 in T-cell leukemia and melanoma. Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 5039-5043
12. Cleary M.L., Mellentin J.D., Spies J., and Smith S.D. Chromosomal translocation involving the beta T cell receptor gene in acute leukemia. J. Exp. Med. 167 (1988) 682-687
13. Porcher C., Swat W., Rockwell K., Fujiwara Y., Alt F.W., and Orkin S.H. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86 (1996) 47-57
14. Hall M.A., Curtis D.J., Metcalf D., Elefanty A.G., Sourris K., Robb L., Gothert J.R., Jane S.M., and Begley C.G. The critical regulator of embryonic hematopoiesis, SCL, is vital in the adult for megakaryopoiesis, erythropoiesis, and lineage choice in CFU-S12. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 992-997
15. Mikkola H.K., Klintman J., Yang H., Hock H., Schlaeger T.M., Fujiwara Y., and Orkin S.H. Haematopoietic stem cells retain long-term repopulating activity and multipotency in the absence of stem-cell leukaemia SCL/tal-1 gene. Nature 421 (2003) 547-551
16. Robb L., Elwood N.J., Elefanty A.G., Kontgen F., Li R., Barnett L.D., and Begley C.G. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15 (1996) 4123-4129
17. Capron C., Lecluse Y., Kaushik A.L., Foudi A., Lacout C., Sekkai D., Godin I., Albagli O., Poullion I., Svinartchouk F., Schanze E., Vainchenker W., Sablitzky F., Bennaceur-Griscelli A., and Dumenil D. The SCL relative LYL-1 is required for fetal and adult hematopoietic stem cell function and B-cell differentiation. Blood 107 (2006) 4678-4686
18. Kaufman D.S., Hanson E.T., Lewis R.L., Auerbach R., and Thomson J.A. Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10716-10721
19. Meng Y.S., Khoury H., Dick J.E., and Minden M.D. Oncogenic potential of the transcription factor LYL1 in acute myeloblastic leukemia. Leukemia 19 (2005) 1941-1947
20. Schlaeger T.M., Schuh A., Flitter S., Fisher A., Mikkola H., Orkin S.H., Vyas P., and Porcher C. Decoding hematopoietic specificity in the helix-loop-helix domain of the transcription factor SCL/Tal-1. Mol. Cell Biol. 24 (2004) 7491-7502
21. Miyamoto A., Cui X., Naumovski L., and Cleary M.L. Helix-loop-helix proteins LYL1 and E2a form heterodimeric complexes with distinctive DNA-binding properties in hematolymphoid cells. Mol. Cell Biol. 16 (1996) 2394-2401
22. Ferrando A.A., Neuberg D.S., Staunton J., Loh M.L., Huard C., Raimondi S.C., Behm F.G., Pui C.H., Downing J.R., Gilliland D.G., Lander E.S., Golub T.R., and Look A.T. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1 (2002) 75-87
23. Blobel G.A. CREB-binding protein and p300: molecular integrators of hematopoietic transcription. Blood 95 (2000) 745-755
24. Mayr B., and Montminy M. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev., Mol. Cell Biol. 2 (2001) 599-609
25. Impey S., McCorkle S.R., Cha-Molstad H., Dwyer J.M., Yochum G.S., Boss J.M., McWeeney S., Dunn J.J., Mandel G., and Goodman R.H. Defining the CREB regulon: a genome-wide analysis of transcription factor regulatory regions. Cell 119 (2004) 1041-1054
26. Shaywitz A.J., and Greenberg M.E. CREB: a stimulus-induced transcription factor activated by a diverse array of extracellular signals. Annu. Rev. Biochem. 68 (1999) 821-861
27. Shankar D.B., Cheng J.C., Kinjo K., Federman N., Moore T.B., Gill A., Rao N.P., Landaw E.M., and Sakamoto K.M. The role of CREB as a proto-oncogene in hematopoiesis and in acute myeloid leukemia. Cancer Cell 7 (2005) 351-362
28. Shankar D.B., and Sakamoto K.M. The role of cyclic-AMP binding protein (CREB) in leukemia cell proliferation and acute leukemias. Leuk. Lymphoma 45 (2004) 265-270
29. Ono Y., Fukuhara N., and Yoshie O. TAL1 and LIM-only proteins synergistically induce retinaldehyde dehydrogenase 2 expression in T-cell acute lymphoblastic leukemia by acting as cofactors for GATA3. Mol. Cell Biol. 18 (1998) 6939-6950
30. Ghislain J.J., and Fish E.N. Application of genomic DNA affinity chromatography identifies multiple interferon-alpha-regulated Stat2 complexes. J. Biol. Chem. 271 (1996) 12408-12413
31. Xu Z., Huang S., Chang L.S., Agulnick A.D., and Brandt S.J. Identification of a TAL1 target gene reveals a positive role for the LIM domain-binding protein Ldb1 in erythroid gene expression and differentiation. Mol. Cell Biol. 23 (2003) 7585-7599
32. Holloway A.F., Rao S., Chen X., and Shannon M.F. Changes in chromatin accessibility across the GM-CSF promoter upon T cell activation are dependent on nuclear factor kappaB proteins. J. Exp. Med. 197 (2003) 413-423
33. Yu L., Liu C., Vandeusen J., Becknell B., Dai Z., Wu Y.Z., Raval A., Liu T.H., Ding W., Mao C., Liu S., Smith L.T., Lee S., Rassenti L., Marcucci G., Byrd J., Caligiuri M.A., and Plass C. Global assessment of promoter methylation in a mouse model of cancer identifies ID4 as a putative tumor-suppressor gene in human leukemia. Nat. Genet. 37 (2005) 265-274
34. Pavlidis P., and Noble W.S. Analysis of strain and regional variation in gene expression in mouse brain. Genome Biol. 2 (2001) RESEARCH0042
35. Golub T.R., Slonim D.K., Tamayo P., Huard C., Gaasenbeek M., Mesirov J.P., Coller H., Loh M.L., Downing J.R., Caligiuri M.A., Bloomfield C.D., and Lander E.S. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 286 (1999) 531-537
36. Dal Peraro M., Alber F., and Carloni P. Ser133 phosphate-KIX interactions in the CREB-CBP complex: an ab initio molecular dynamics study. Eur. Biophys. J. 30 (2001) 75-81
37. Radhakrishnan I., Perez-Alvarado G.C., Dyson H.J., and Wright P.E. Conformational preferences in the Ser133-phosphorylated and non-phosphorylated forms of the kinase inducible transactivation domain of CREB. FEBS Lett. 430 (1998) 317-322
38. Heisler L.E., Torti D., Boutros P.C., Watson J., Chan C., Winegarden N., Takahashi M., Yau P., Huang T.H., Farnham P.J., Jurisica I., Woodgett J.R., Bremner R., Penn L.Z., and Der S.D. CpG Island microarray probe sequences derived from a physical library are representative of CpG Islands annotated on the human genome. Nucleic Acids Res. 33 (2005) 2952-2961
39. Zhang X., Odom D.T., Koo S.H., Conkright M.D., Canettieri G., Best J., Chen H., Jenner R., Herbolsheimer E., Jacobsen E., Kadam S., Ecker J.R., Emerson B., Hogenesch J.B., Unterman T., Young R.A., and Montminy M. Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 4459-4464
40. O'Neil J., Shank J., Cusson N., Murre C., and Kelliher M. TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 5 (2004) 587-596
41. Murre C. Intertwining proteins in thymocyte development and cancer. Nat. Immunol. 1 (2000) 97-98
42. Spits H., Couwenberg F., Bakker A.Q., Weijer K., and Uittenbogaart C.H. Id2 and Id3 inhibit development of CD34(+) stem cells into predendritic cell (pre-DC)2 but not into pre-DC1. Evidence for a lymphoid origin of pre-DC2. J. Exp. Med. 192 (2000) 1775-1784
43. Morrow M.A., Mayer E.W., Perez C.A., Adlam M., and Siu G. Overexpression of the Helix-Loop-Helix protein Id2 blocks T cell development at multiple stages. Mol. Immunol. 36 (1999) 491-503
44. Heemskerk M.H., Blom B., Nolan G., Stegmann A.P., Bakker A.Q., Weijer K., Res P.C., and Spits H. Inhibition of T cell and promotion of natural killer cell development by the dominant negative helix loop helix factor Id3. J. Exp. Med. 186 (1997) 1597-1602
45. Lister J., Forrester W.C., and Baron M.H. Inhibition of an erythroid differentiation switch by the helix-loop-helix protein Id1. J. Biol. Chem. 270 (1995) 17939-17946
46. Sun X.H. Constitutive expression of the Id1 gene impairs mouse B cell development. Cell 79 (1994) 893-900
47. Ferrando A.A., Herblot S., Palomero T., Hansen M., Hoang T., Fox E.A., and Look A.T. Biallelic transcriptional activation of oncogenic transcription factors in T-cell acute lymphoblastic leukemia. Blood 103 (2004) 1909-1911
48. Park S.T., Nolan G.P., and 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
49. Park S.T., and Sun X.H. The Tal1 oncoprotein inhibits E47-mediated transcription. Mechanism of inhibition. J. Biol. Chem. 273 (1998) 7030-7037
50. Voronova A.F., and Lee F. 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. U. S. A. 91 (1994) 5952-5956
51. Chan W.Y., Follows G.A., Lacaud G., Pimanda J.E., Landry J.R., Kinston S., Knezevic K., Piltz S., Donaldson I.J., Gambardella L., Sablitzky F., Green A.R., Kouskoff V., and Gottgens B. The paralogous hematopoietic regulators Lyl1 and Scl are coregulated by Ets and GATA factors, but Lyl1 cannot rescue the early Scl-/- phenotype. Blood 109 (2007) 1908-1916
52. Porcher C., Liao E.C., Fujiwara Y., Zon L.I., and Orkin S.H. Specification of hematopoietic and vascular development by the bHLH transcription factor SCL without direct DNA binding. Development 126 (1999) 4603-4615
53. Engel I., and Murre C. The function of E- and Id proteins in lymphocyte development. Nat. Rev., Immunol. 1 (2001) 193-199
54. Euskirchen G., Royce T.E., Bertone P., Martone R., Rinn J.L., Nelson F.K., Sayward F., Luscombe N.M., Miller P., Gerstein M., Weissman S., and Snyder M. CREB binds to multiple loci on human chromosome 22. Mol. Cell Biol. 24 (2004) 3804-3814
55. Beima K.M., Miazgowicz M.M., Lewis M.D., Yan P.S., Huang T.H., and Weinmann A.S. T-bet binding to newly identified target gene promoters is cell type-independent but results in variable context-dependent functional effects. J. Biol. Chem. 281 (2006) 11992-12000
56. Gering M., Yamada Y., Rabbitts T.H., and Patient R.K. Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development 130 (2003) 6187-6199
57. Osada H., Grutz G.G., Axelson H., Forster A., and Rabbitts T.H. LIM-only protein Lmo2 forms a protein complex with erythroid transcription factor GATA-1. Leukemia 11 Suppl 3 (1997) 307-312
58. Wadman I.A., Osada H., Grutz G.G., Agulnick A.D., Westphal H., Forster A., and Rabbitts T.H. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J. 16 (1997) 3145-3157
59. Tournay O., and Benezra R. Transcription of the dominant-negative helix-loop-helix protein Id1 is regulated by a protein complex containing the immediate-early response gene Egr-1. Mol. Cell Biol. 16 (1996) 2418-2430
60. Lecuyer E., Herblot S., Saint-Denis M., Martin R., Begley C.G., Porcher C., Orkin S.H., and Hoang T. The SCL complex regulates c-kit expression in hematopoietic cells through functional interaction with Sp1. Blood 100 (2002) 2430-2440
61. Cohen-Kaminsky S., Maouche-Chretien L., Vitelli L., Vinit M.A., Blanchard I., Yamamoto M., Peschle C., and Romeo P.H. Chromatin immunoselection defines a TAL-1 target gene. EMBO J. 17 (1998) 5151-5160
62. Palomero T., Odom D.T., O'Neil J., Ferrando A.A., Margolin A., Neuberg D.S., Winter S.S., Larson R.S., Li W., Liu X.S., Young R.A., and Look A.T. Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 108 (2006) 986-992