Core Transcriptional Regulatory Circuit Controlled by the TAL1 Complex in Human T Cell Acute Lymphoblastic Leukemia

Cancer Cell

Volumn 22, Issue 2, 2012, Pages 209-221

  Sanda, Takaomi ^a   Lawton, Lee N ^b   Barrasa, M Inmaculada ^b   Fan, Zi Peng ^b,c   Kohlhammer, Holger ^d   Gutierrez, Alejandro ^a,e   Ma, Wenxue ^f   Tatarek, Jessica ^g   Ahn, Yebin ^a   Kelliher, Michelle A ^f   Jamieson, Catriona H M ^f   Staudt, Louis M ^d   Young, Richard A ^b,c   Look, A Thomas ^a,e  

^a HARVARD MEDICAL SCHOOL   (United States)

^b WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^c MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e BOSTON CHILDREN S HOSPITAL   (United States)

^f UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^g UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN MYB; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR E2A; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR HEB; TRANSCRIPTION FACTOR LMO1; TRANSCRIPTION FACTOR LMO2; TRANSCRIPTION FACTOR RUNX1; TRANSCRIPTION FACTOR TAL1; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ARTICLE; CELL SURVIVAL; GENE; GENE ACTIVATION; HUMAN; HUMAN CELL; LEUKEMOGENESIS; NUCLEOTIDE SEQUENCE; ONCOGENE C MYB; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSCRIPTION REGULATION; TRIB2 GENE;

EID: 84865109759     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2012.06.007     Document Type: Article

References (61)

1. Alon U. Network motifs: theory and experimental approaches. Nat. Rev. Genet. 2007, 8:450-461.
2. Armstrong S.A., Look A.T. Molecular genetics of acute lymphoblastic leukemia. J. Clin. Oncol. 2005, 23:6306-6315.
3. 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. 1997, 17:4782-4791.
4. Bernard M., Delabesse E., Smit L., Millien C., Kirsch I.R., Strominger J.L., Macintyre E.A. Helix-loop-helix (E2-5, HEB, TAL1 and Id1) protein interaction with the TCRalphadelta enhancers. Int. Immunol. 1998, 10:1539-1549.
5. 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. 1990, 9:3343-3351.
6. Clappier E., Cuccuini W., Kalota A., Crinquette A., Cayuela J.M., Dik W.A., Langerak A.W., Montpellier B., Nadel B., Walrafen P., et al. The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood 2007, 110:1251-1261.
7. Collins A., Littman D.R., Taniuchi I. RUNX proteins in transcription factor networks that regulate T-cell lineage choice. Nat. Rev. Immunol. 2009, 9:106-115.
8. Coustan-Smith E., Mullighan C.G., Onciu M., Behm F.G., Raimondi S.C., Pei D., Cheng C., Su X., Rubnitz J.E., Basso G., et al. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol. 2009, 10:147-156.
9. Della Gatta G., Palomero T., Perez-Garcia A., Ambesi-Impiombato A., Bansal M., Carpenter Z.W., De Keersmaecker K., Sole X., Xu L., Paietta E., et al. Reverse engineering of TLX oncogenic transcriptional networks identifies RUNX1 as tumor suppressor in T-ALL. Nat. Med. 2012, 18:436-440.
10. Ferrando A.A., Look A.T. Clinical implications of recurring chromosomal and associated molecular abnormalities in acute lymphoblastic leukemia. Semin. Hematol. 2000, 37:381-395.
11. 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., et al. Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 2002, 1:75-87.
12. Gerby B., Armstrong F., de la Grange P.B., Medyouf H., Calvo J., Verhoeyen E., Cosset F.L., Bernstein I., Amselem S., Boissel N., et al. Optimized gene transfer into human primary leukemic T cell with NOD-SCID/leukemia-initiating cell activity. Leukemia 2010, 24:646-649.
13. Göttgens B., Ferreira R., Sanchez M.J., Ishibashi S., Li J., Spensberger D., Lefevre P., Ottersbach K., Chapman M., Kinston S., et al. cis-Regulatory remodeling of the SCL locus during vertebrate evolution. Mol. Cell. Biol. 2010, 30:5741-5751.
14. Grossmann V., Kern W., Harbich S., Alpermann T., Jeromin S., Schnittger S., Haferlach C., Haferlach T., Kohlmann A. Prognostic relevance of RUNX1 mutations in T-cell acute lymphoblastic leukemia. Haematologica 2011, 96:1874-1877.
15. Gutierrez A., Dahlberg S.E., Neuberg D.S., Zhang J., Grebliunaite R., Sanda T., Protopopov A., Tosello V., Kutok J., Larson R.S., et al. Absence of biallelic TCRgamma deletion predicts early treatment failure in pediatric T-cell acute lymphoblastic leukemia. J. Clin. Oncol. 2010, 28:3816-3823.
16. 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. 2000, 1:138-144.
17. Ho I.C., Tai T.S., Pai S.Y. GATA3 and the T-cell lineage: essential functions before and after T-helper-2-cell differentiation. Nat. Rev. Immunol. 2009, 9:125-135.
18. Hollenhorst P.C., Shah A.A., Hopkins C., Graves B.J. Genome-wide analyses reveal properties of redundant and specific promoter occupancy within the ETS gene family. Genes Dev. 2007, 21:1882-1894.
19. Hollenhorst P.C., Chandler K.J., Poulsen R.L., Johnson W.E., Speck N.A., Graves B.J. DNA specificity determinants associate with distinct transcription factor functions. PLoS Genet. 2009, 5:e1000778.
20. Homminga I., Pieters R., Langerak A.W., de Rooi J.J., Stubbs A., Verstegen M., Vuerhard M., Buijs-Gladdines J., Kooi C., Klous P., et al. Integrated transcript and genome analyses reveal NKX2-1 and MEF2C as potential oncogenes in T cell acute lymphoblastic leukemia. Cancer Cell 2011, 19:484-497.
21. Hosoya-Ohmura S., Lin Y.H., Herrmann M., Kuroha T., Rao A., Moriguchi T., Lim K.C., Hosoya T., Engel J.D. An NK and T cell enhancer lies 280 kilobase pairs 3' to the gata3 structural gene. Mol. Cell. Biol. 2011, 31:1894-1904.
22. 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. 1991, 11:3037-3042.
23. 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 1994, 91:3181-3185.
24. Kassouf M.T., Hughes J.R., Taylor S., McGowan S.J., Soneji S., Green A.L., Vyas P., Porcher C. Genome-wide identification of TAL1's functional targets: insights into its mechanisms of action in primary erythroid cells. Genome Res. 2010, 20:1064-1083.
25. Kee B.L. E and ID proteins branch out. Nat. Rev. Immunol. 2009, 9:175-184.
26. Keeshan K., He Y., Wouters B.J., Shestova O., Xu L., Sai H., Rodriguez C.G., Maillard I., Tobias J.W., Valk P., et al. Tribbles homolog 2 inactivates C/EBPalpha and causes acute myelogenous leukemia. Cancer Cell 2006, 10:401-411.
27. Kusy S., Gerby B., Goardon N., Gault N., Ferri F., Gérard D., Armstrong F., Ballerini P., Cayuela J.M., Baruchel A., 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.
28. Lahortiga I., De Keersmaecker K., Van Vlierberghe P., Graux C., Cauwelier B., Lambert F., Mentens N., Beverloo H.B., Pieters R., Speleman F., et al. Duplication of the MYB oncogene in T cell acute lymphoblastic leukemia. Nat. Genet. 2007, 39:593-595.
29. Landry J.R., Bonadies N., Kinston S., Knezevic K., Wilson N.K., Oram S.H., Janes M., Piltz S., Hammett M., Carter J., et al. Expression of the leukemia oncogene Lmo2 is controlled by an array of tissue-specific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 2009, 113:5783-5792.
30. Larson R.C., Lavenir I., Larson T.A., Baer R., Warren A.J., Wadman I., Nottage K., Rabbitts T.H. Protein dimerization between Lmo2 (Rbtn2) and Tal1 alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J. 1996, 15:1021-1027.
31. Lécuyer 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 2002, 100:2430-2440.
32. Lee T.I., Johnstone S.E., Young R.A. Chromatin immunoprecipitation and microarray-based analysis of protein location. Nat. Protoc. 2006, 1:729-748.
33. Lin Y.C., Jhunjhunwala S., Benner C., Heinz S., Welinder E., Mansson R., Sigvardsson M., Hagman J., Espinoza C.A., Dutkowski J., et al. A global network of transcription factors, involving E2A, EBF1 and Foxo1, that orchestrates B cell fate. Nat. Immunol. 2010, 11:635-643.
34. Look A.T. Oncogenic transcription factors in the human acute leukemias. Science 1997, 278:1059-1064.
35. Marson A., Levine S.S., Cole M.F., Frampton G.M., Brambrink T., Johnstone S., Guenther M.G., Johnston W.K., Wernig M., Newman J., et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 2008, 134:521-533.
36. Miyazaki M., Rivera R.R., Miyazaki K., Lin Y.C., Agata Y., Murre C. The opposing roles of the transcription factor E2A and its antagonist Id3 that orchestrate and enforce the naive fate of T cells. Nat. Immunol. 2011, 12:992-1001.
37. Ngo V.N., Davis R.E., Lamy L., Yu X., Zhao H., Lenz G., Lam L.T., Dave S., Yang L., Powell J., Staudt L.M. A loss-of-function RNA interference screen for molecular targets in cancer. Nature 2006, 441:106-110.
38. Nottingham W.T., Jarratt A., Burgess M., Speck C.L., Cheng J.F., Prabhakar S., Rubin E.M., Li P.S., Sloane-Stanley J., Kong-A-San J., de Bruijn M.F. Runx1-mediated hematopoietic stem-cell emergence is controlled by a Gata/Ets/SCL-regulated enhancer. Blood 2007, 110:4188-4197.
39. Novershtern N., Subramanian A., Lawton L.N., Mak R.H., Haining W.N., McConkey M.E., Habib N., Yosef N., Chang C.Y., Shay T., et al. Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 2011, 144:296-309.
40. 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.
41. O'Neil J., Tchinda J., Gutierrez A., Moreau L., Maser R.S., Wong K.K., Li W., McKenna K., Liu X.S., Feng B., et al. Alu elements mediate MYB gene tandem duplication in human T-ALL. J. Exp. Med. 2007, 204:3059-3066.
42. Ono Y., Fukuhara N., 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. 1998, 18:6939-6950.
43. Palii, C.G., Pasha, R., and Brand, M. (2011a). Lentiviral-mediated knockdown during ex vivo erythropoiesis of human hematopoietic stem cells. J. Vis. Exp. (53). , doi:10.3791/2813.
44. Palii C.G., Perez-Iratxeta C., Yao Z., Cao Y., Dai F., Davison J., Atkins H., Allan D., Dilworth F.J., Gentleman R., et al. Differential genomic targeting of the transcription factor TAL1 in alternate haematopoietic lineages. EMBO J. 2011, 30:494-509.
45. 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., et al. Transcriptional regulatory networks downstream of TAL1/SCL in T-cell acute lymphoblastic leukemia. Blood 2006, 108:986-992.
46. Ramsay R.G., Gonda T.J. MYB function in normal and cancer cells. Nat. Rev. Cancer 2008, 8:523-534.
47. Soler E., Andrieu-Soler C., de Boer E., Bryne J.C., Thongjuea S., Stadhouders R., Palstra R.J., Stevens M., Kockx C., van Ijcken W., et al. The genome-wide dynamics of the binding of Ldb1 complexes during erythroid differentiation. Genes Dev. 2010, 24:277-289.
48. Thoms J.A., Birger Y., Foster S., Knezevic K., Kirschenbaum Y., Chandrakanthan V., Jonquieres G., Spensberger D., Wong J.W., Oram S.H., et al. ERG promotes T-acute lymphoblastic leukemia and is transcriptionally regulated in leukemic cells by a stem cell enhancer. Blood 2011, 117:7079-7089.
49. Tijssen M.R., Cvejic A., Joshi A., Hannah R.L., Ferreira R., Forrai A., Bellissimo D.C., Oram S.H., Smethurst P.A., Wilson N.K., et al. Genome-wide analysis of simultaneous GATA1/2, RUNX1, FLI1, and SCL binding in megakaryocytes identifies hematopoietic regulators. Dev. Cell 2011, 20:597-609.
50. Tremblay M., Tremblay C.S., Herblot S., Aplan P.D., Hébert J., Perreault C., Hoang T. Modeling T-cell acute lymphoblastic leukemia induced by the SCL and LMO1 oncogenes. Genes Dev. 2010, 24:1093-1105.
51. Valouev A., Johnson D.S., Sundquist A., Medina C., Anton E., Batzoglou S., Myers R.M., Sidow A. Genome-wide analysis of transcription factor binding sites based on ChIP-Seq data. Nat. Methods 2008, 5:829-834.
52. Verhoeyen E., Dardalhon V., Ducrey-Rundquist O., Trono D., Taylor N., Cosset F.L. IL-7 surface-engineered lentiviral vectors promote survival and efficient gene transfer in resting primary T lymphocytes. Blood 2003, 101:2167-2174.
53. Wadman I.A., Osada H., Grütz G.G., Agulnick A.D., Westphal H., Forster A., 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. 1997, 16:3145-3157.
54. Wilson N.K., Miranda-Saavedra D., Kinston S., Bonadies N., Foster S.D., Calero-Nieto F., Dawson M.A., Donaldson I.J., Dumon S., Frampton J., et al. The transcriptional program controlled by the stem cell leukemia gene Scl/Tal1 during early embryonic hematopoietic development. Blood 2009, 113:5456-5465.
55. Wilson N.K., Foster S.D., Wang X., Knezevic K., Schütte J., Kaimakis P., Chilarska P.M., Kinston S., Ouwehand W.H., Dzierzak E., et al. Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 2010, 7:532-544.
56. Wouters B.J., Jordà M.A., Keeshan K., Louwers I., Erpelinck-Verschueren C.A., Tielemans D., Langerak A.W., He Y., Yashiro-Ohtani Y., Zhang P., et al. Distinct gene expression profiles of acute myeloid/T-lymphoid leukemia with silenced CEBPA and mutations in NOTCH1. Blood 2007, 110:3706-3714.
57. Xu Z., Huang S., Chang L.S., Agulnick A.D., 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. 2003, 23:7585-7599.
58. Yokoyama T., Nakamura T. Tribbles in disease: Signaling pathways important for cellular function and neoplastic transformation. Cancer Sci. 2011, 102:1115-1122.
59. Young R.A. Control of the embryonic stem cell state. Cell 2011, 144:940-954.
60. Zhang J., Ding L., Holmfeldt L., Wu G., Heatley S.L., Payne-Turner D., Easton J., Chen X., Wang J., Rusch M., et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 2012, 481:157-163.
61. Zuber J., Rappaport A.R., Luo W., Wang E., Chen C., Vaseva A.V., Shi J., Weissmueller S., Fellmann C., Taylor M.J., et al. An integrated approach to dissecting oncogene addiction implicates a Myb-coordinated self-renewal program as essential for leukemia maintenance. Genes Dev. 2011, 25:1628-1640.