Dynamic interaction between TAL1 oncoprotein and LSD1 regulates TAL1 function in hematopoiesis and leukemogenesis

Oncogene

Volumn 31, Issue 48, 2012, Pages 5007-5018

  Li, Y ^a,b   Deng, C ^a   Hu, X ^a,b   Patel, B ^a   Fu, X ^b   Qiu, Y ^a,c   Brand, M ^d   Zhao, K ^e   Huang, S ^a,c  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b JILIN UNIVERSITY   (China)

^c UNIVERSITY OF FLORIDA   (United States)

^d OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^e NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

epigenetic regulation; H3K4 demethylation; leukemogenesis; LSD1; serine phosphorylation; TAL1 SCL

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ENZYME; FORSKOLIN; HISTONE H3; LYSINE; LYSINE SPECIFIC DEMETHYLASE 1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; EPIGENETICS; ERYTHROID CELL; GENE ACTIVATION; GENE REPRESSION; HEMATOPOIESIS; HISTONE METHYLATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LEUKEMOGENESIS; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; T LYMPHOCYTE; WILD TYPE;

BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA METHYLATION; HEMATOPOIESIS; HISTONE DEMETHYLASES; HUMANS; PHOSPHORYLATION; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; SERINE;

EID: 84870506589     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.8     Document Type: Article

References (59)

1. Porcher C, Swat W, Rockwell K, Fujiwara Y, Alt FW, Orkin SH. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 1996; 86: 47-57. (Pubitemid 26256577)
2. Sanchez MJ, Bockamp EO, Miller J, Gambardella L, Green AR. Selective rescue of early haematopoietic progenitors in Scl(-/-) mice by expressing Scl under the control of a stem cell enhancer. Development 2001; 128: 4815-4827. (Pubitemid 33138591)
3. Robb L, Elwood NJ, Elefanty AG, Kontgen F, Li R, Barnett LD et al. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J 1996; 15: 4123-4129. (Pubitemid 26278695)
4. Chen Q, Cheng JT, Tasi LH, Schneider N, Buchanan G, Carroll A et al. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J 1990; 9: 415-424.
5. Robb L, Begley CG. The SCL/TAL1 gene: roles in normal and malignant haematopoiesis. Bioessays 1997; 19: 607-613. (Pubitemid 27295531)
6. Orkin SH. Hematopoiesis: how does it happen? Curr Opin Cell Biol 1995; 7: 870-877.
7. Cantor AB, Orkin SH. Transcriptional regulation of erythropoiesis: an affair involving multiple partners. Oncogene 2002; 21: 3368-3376. (Pubitemid 34587709)
8. Kassouf MT, Hughes JR, Taylor S, McGowan SJ, Soneji S, Green AL et al. Genomewide identification of TAL1's functional targets: insights into its mechanisms of action in primary erythroid cells. Genome Res 2010; 20: 1064-1083.
9. Tripic T, Deng W, Cheng Y, Zhang Y, Vakoc CR, Gregory GD et al. SCL and associated proteins distinguish active from repressive GATA transcription factor complexes. Blood 2009; 113: 2191-2201.
10. Huang S, Brandt SJ. mSin3A regulates murine erythroleukemia cell differentiation through association with the TAL1 (or SCL) transcription factor. Mol Cell Biol 2000; 20: 2248-2259. (Pubitemid 30123840)
11. Huang S, Qiu Y, Shi Y, Xu Z, Brandt SJ. P/CAF-mediated acetylation regulates the function of the basic helix-loop-helix transcription factor TAL1/SCL. EMBO J 2000; 19: 6792-6803. (Pubitemid 32011672)
12. Huang S, Qiu Y, Stein RW, Brandt SJ. p300 functions as a transcriptional coactivator for the TAL1/SCL oncoprotein. Oncogene 1999; 18: 4958-4967. (Pubitemid 29425302)
13. Hu X, Li X, Valverde K, Fu X, Noguchi C, Qiu Y et al. LSD1-mediated epigenetic modification is required for TAL1 function and hematopoiesis. Proc Natl Acad Sci USA 2009; 106: 10141-10146.
14. Schuh AH, Tipping AJ, Clark AJ, Hamlett I, Guyot B, Iborra FJ et al. ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol Cell Biol 2005; 25: 10235-10250. (Pubitemid 41681951)
15. Goardon N, Lambert JA, Rodriguez P, Nissaire P, Herblot S, Thibault P et al. ETO2 coordinates cellular proliferation and differentiation during erythropoiesis. EMBO J 2006; 25: 357-366. (Pubitemid 43152856)
16. Cai Y, Xu Z, Xie J, Ham AJ, Koury MJ, Hiebert SW et al. Eto2/MTG16 and MTGR1 are heteromeric corepressors of the TAL1/SCL transcription factor in murine erythroid progenitors. Biochem Biophys Res Commun 2009; 390: 295-301.
17. Palamarchuk A, Efanov A, Maximov V, Aqeilan RI, Croce CM, Pekarsky Y. Akt phosphorylates Tal1 oncoprotein and inhibits its repressor activity. Cancer Res 2005; 65: 4515-4519. (Pubitemid 40740785)
18. Prasad KS, Brandt SJ. Target-dependent effect of phosphorylation on the DNA binding activity of the TAL1/SCL oncoprotein. J Biol Chem 1997; 272: 11457-11462. (Pubitemid 27184154)
19. Prasad KS, Jordan JE, Koury MJ, Bondurant MC, Brandt SJ. Erythropoietin stimulates transcription of the TAL1/SCL gene and phosphorylation of its protein products. J Biol Chem 1995; 270: 11603-11611.
20. Wadman IA, Hsu HL, Cobb MH, Baer R. The MAP kinase phosphorylation site of TAL1 occurs within a transcriptional activation domain. Oncogene 1994; 9: 3713-3716. (Pubitemid 24359412)
21. Hu X, Ybarra R, Qiu Y, Bungert J, Huang S. Transcriptional regulation by TAL1: a link between epigenetic modifications and erythropoiesis. Epigenetics 2009; 4: 357-361.
22. Bash RO, Hall S, Timmons CF, Crist WM, Amylon M, Smith RG et al. Does activation of the TAL1 gene occur in a majority of patients with T-cell acute lymphoblastic leukemia? A pediatric oncology group study. Blood 1995; 86: 666-676.
23. Palomero T, Odom DT, O'Neil J, Ferrando AA, Margolin A, Neuberg DS et al. Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 2006; 108: 986-992. (Pubitemid 44154635)
24. Larson RC, Lavenir I, Larson TA, Baer R, Warren AJ, Wadman I et al. Protein dimerization between Lmo2 (Rbtn2) and Tal1 alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J 1996; 15: 1021-1027. (Pubitemid 26077830)
25. Condorelli GL, Facchiano F, Valtieri M, Proietti E, Vitelli L, Lulli V et al. T-celldirected TAL-1 expression induces T-cell malignancies in transgenic mice. Cancer Res 1996; 56: 5113-5119. (Pubitemid 26383021)
26. Shank-Calvo JA, Draheim K, Bhasin M, Kelliher MA. p16Ink4a or p19Arf loss contributes to Tal1-induced leukemogenesis in mice. Oncogene 2006; 25: 3023-3031. (Pubitemid 43780466)
27. O'Neil J, Shank J, Cusson N, Murre C, Kelliher M. TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 2004; 5: 587-596. (Pubitemid 38748920)
28. Herblot S, Steff AM, Hugo P, Aplan PD, Hoang T. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat Immunol 2000; 1: 138-144.
29. Dey S, Curtis DJ, Jane SM, Brandt SJ. The TAL1/SCL transcription factor regulates cell cycle progression and proliferation in differentiating murine bone marrow monocyte precursors. Mol Cell Biol 2010; 30: 2181-2192.
30. Lacombe J, Herblot S, Rojas-Sutterlin S, Haman A, Barakat S, Iscove NN et al. Scl regulates the quiescence and the long-term competence of hematopoietic stem cells. Blood 2010; 115: 792-803.
31. Hansson A, Manetopoulos C, Jonsson JI, Axelson H. The basic helix-loop-helix transcription factor TAL1/SCL inhibits the expression of the p16INK4A and pTalpha genes. Biochem Biophys Res Commun 2003; 312: 1073-1081. (Pubitemid 37490924)
32. Cui K, Zang C, Roh TY, Schones DE, Childs RW, Peng W et al. Chromatin signatures in multipotent human hematopoietic stem cells indicate the fate of bivalent genes during differentiation. Cell Stem Cell 2009; 4: 80-93.
33. Mikkelsen TS, Ku M, Jaffe DB, Issac B, Lieberman E, Giannoukos G et al. Genome-wide maps of chromatin state in pluripotent and lineage-committed cells. Nature 2007; 448: 553-560. (Pubitemid 47206934)
34. Bernstein BE, Mikkelsen TS, Xie X, Kamal M, Huebert DJ, Cuff J et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 2006; 125: 315-326.
35. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA et al. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1.Cell 2004; 119: 941-953.
36. Lee MG, Wynder C, Cooch N, Shiekhattar R. An essential role for CoREST in nucleosomal histone 3 lysine 4 demethylation. Nature 2005; 437: 432-435. (Pubitemid 41613507)
37. Wang Y, Zhang H, Chen Y, Sun Y, Yang F, Yu W et al. LSD1 is a subunit of the NuRD complex and targets the metastasis programs in breast cancer. Cell 2009; 138: 660-672.
38. Lan F, Nottke AC, Shi Y. Mechanisms involved in the regulation of histone lysine demethylases. Curr Opin Cell Biol 2008; 20: 316-325.
39. Lee MG, Wynder C, Bochar DA, Hakimi MA, Cooch N, Shiekhattar R. Functional interplay between histone demethylase and deacetylase enzymes. Mol Cell Biol 2006; 26: 6395-6402. (Pubitemid 44277880)
40. Scoumanne A, Chen X. The lysine-specific demethylase 1 is required for cell proliferation in both p53-dependent and -independent manners. J Biol Chem 2007; 282: 15471-15475. (Pubitemid 47093261)
41. Wang J, Hevi S, Kurash JK, Lei H, Gay F, Bajko J et al. The lysine demethylase LSD1 (KDM1) is required for maintenance of global DNA methylation. Nat Genet 2009; 41: 125-129.
42. Saleque S, Kim J, Rooke HM, Orkin SH. Epigenetic regulation of hematopoietic differentiation by Gfi-1 and Gfi-1b is mediated by the cofactors CoREST and LSD1. Mol Cell 2007; 27: 562-572. (Pubitemid 47238633)
43. Aplan PD, Lombardi DP, Ginsberg AM, Cossman J, Bertness VL, Kirsch IR. Disruption of the human SCL locus by 00illegitimate00 V-(D)-J recombinase activity. Science 1990; 250: 1426-1429. (Pubitemid 120031866)
44. Begley CG, Green AR. The SCL gene: from case report to critical hematopoietic regulator. Blood 1999; 93: 2760-2770. (Pubitemid 29200765)
45. Chen Q, Yang CY, Tsan JT, Xia Y, Ragab AH, Peiper SC et al. Coding sequences of the tal-1 gene are disrupted by chromosome translocation in human T cell leukemia. J Exp Med 1990; 172: 1403-1408. (Pubitemid 20366215)
46. 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 2003; 278: 12680-12687. (Pubitemid 36800028)
47. Izraeli S. Leukaemia-a developmental perspective. Br J Haematol 2004; 126: 3-10.
48. Palii CG, Perez-Iratxeta C, Yao Z, Cao Y, Dai F, Davison J et al. Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J 2011; 30: 494-509.
49. Linggi BE, Brandt SJ, Sun ZW, Hiebert SW. Translating the histone code into leukemia. J Cell Biochem 2005; 96: 938-950. (Pubitemid 41688720)
50. Martinez MC, Larbret F, Zobairi F, Coulombe J, Debili N, Vainchenker W et al. Transfer of differentiation signal by membrane microvesicles harboring hedgehog morphogens. Blood 2006; 108: 3012-3020.
51. Demers C, Chaturvedi CP, Ranish JA, Juban G, Lai P, Morle F et al. Activatormediated recruitment of the MLL2 methyltransferase complex to the beta-globin locus. Mol Cell 2007; 27: 573-584 [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't]. (Pubitemid 47238629)
52. Grass JA, Boyer ME, Pal S, Wu J, Weiss MJ, Bresnick EH. GATA-1-dependent transcriptional repression of GATA-2 via disruption of positive autoregulation and domain-wide chromatin remodeling. Proc Natl Acad Sci USA 2003; 100: 8811-8816 [Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.]. (Pubitemid 36899180)
53. de Laat W, Grosveld F. Spatial organization of gene expression: the active chromatin hub. Chromosome Res 2003; 11: 447-459 [Research Support, Non-U.S. Gov't Review]. (Pubitemid 37041205)
54. Hsu PY, Hsu HK, Singer GA, Yan PS, Rodriguez BA, Liu JC et al. Estrogen-mediated epigenetic repression of large chromosomal regions through DNA looping. Genome Res 2010; 20: 733-744 [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't].
55. Hu Q, Kwon YS, Nunez E, Cardamone MD, Hutt KR, Ohgi KA et al. Enhancing nuclear receptor-induced transcription requires nuclear motor and LSD1- dependent gene networking in interchromatin granules. Proc Natl Acad Sci USA 2008; 105: 19199-19204 [Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.].
56. Kusy S, Gerby B, Goardon N, Gault N, Ferri F, Gerard D et al. NKX3.1 is a direct TAL1 target gene that mediates proliferation of TAL1-expressing human T cell acute lymphoblastic leukemia. J Exp Med 2010; 207: 2141-2156.
57. Li X, Hu X, Patel B, Zhou Z, Liang S, Ybarra R et al. H4R3 methylation facilitates beta-globin transcription by regulating histone acetyltransferase binding and H3 acetylation. Blood 2010; 115: 2028-2037.
58. Song SH, Hou C, Dean A. A positive role for NLI/Ldb1 in long-range beta-globin locus control region function. Mol Cell 2007; 28: 810-822 [Research Support, N.I.H., Intramural]. (Pubitemid 350217055)
59. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z et al. High-resolution profiling of histone methylations in the human genome. Cell 2007; 129: 823-837. (Pubitemid 46802390)