STAT3 mediates oncogenic addiction to TEL-AML1 in t(12;21) acute lymphoblastic leukemia

Blood

Volumn 122, Issue 4, 2013, Pages 542-549

  Mangolini, Maurizio ^a   De Boer, Jasper ^a   Walf Vorderwülbecke, Vanessa ^a   Pieters, Rob ^b   Den Boer, Monique L ^b   Williams, Owen ^a  

^a GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^b SOPHIA CHILDREN S HOSPITAL   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINO 6 [2 [[4 (DIETHYLAMINO) 1 METHYLBUTYL]AMINO] 6 METHYL 4 PYRIMIDINYL] 2 METHYLQUINOLINE; 4 [[(4 METHYLPHENYL)SULFONYLOXY]ACETAMIDO]SALICYLIC ACID; ERYTHROPOIETIN RECEPTOR; MYC PROTEIN; RAC1 PROTEIN; SHORT HAIRPIN RNA; STAT3 PROTEIN; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR RUNX1; ONCOPROTEIN; STAT3 PROTEIN, HUMAN; TEL AML1 FUSION PROTEIN; TEL-AML1 FUSION PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL PROLIFERATION; CELL SELF-RENEWAL; CONTROLLED STUDY; DRUG MECHANISM; DRUG SENSITIVITY; FETUS; GENE SILENCING; GENE TRANSLOCATION; HUMAN; HUMAN CELL; LEUKEMOGENESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; C57BL MOUSE; CELL CULTURE; CELL TRANSFORMATION; CHROMOSOME 12; CHROMOSOME 21; GENETICS; ONCOGENE; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ANIMALS; APOPTOSIS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; CHROMOSOMES, HUMAN, PAIR 12; CHROMOSOMES, HUMAN, PAIR 21; CORE BINDING FACTOR ALPHA 2 SUBUNIT; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; ONCOGENE PROTEINS, FUSION; ONCOGENES; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; STAT3 TRANSCRIPTION FACTOR; TRANSLOCATION, GENETIC;

EID: 84886895426     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2012-11-465252     Document Type: Article

References (50)

1. Pui CH, Robison LL, Look AT. Acute lymphoblastic leukaemia. Lancet. 2008; 371(9617):1030-1043.
2. Romana SP, Mauchauffé M, Le Coniat M, Chumakov I, Le Paslier D, Berger R, Bernard OA. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood. 1995; 85(12):3662-3670.
3. Golub TR, Barker GF, Bohlander SK, et al. Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc Natl Acad Sci USA. 1995;92(11):4917-4921.
4. Loh ML, Goldwasser MA, Silverman LB, et al. Prospective analysis of TEL/AML1-positive patients treated on Dana-Farber Cancer Institute Consortium Protocol 95-01. Blood. 2006;107(11): 4508-4513.
5. Stams WA, Beverloo HB, den Boer ML, et al. Incidence of additional genetic changes in the TEL and AML1 genes in DCOG and COALL-treated t(12;21)-positive pediatric ALL, and their relation with drug sensitivity and clinical outcome. Leukemia. 2006;20(3):410-416.
6. Robison LL. Late effects of acute lymphoblastic leukemia therapy in patients diagnosed at 0-20 years of age. Hematology Am Soc Hematol Educ Program. 2011;2011:238-242.
7. Morrow M, Horton S, Kioussis D, Brady HJ, Williams O. TEL-AML1 promotes development of specific hematopoietic lineages consistent with preleukemic activity. Blood. 2004;103(10): 3890-3896.
8. Tsuzuki S, Seto M, Greaves M, Enver T. Modeling first-hit functions of the t(12;21) TEL-AML1 translocation in mice. Proc Natl Acad Sci USA. 2004;101(22):8443-8448.
9. Fischer M, Schwieger M, Horn S, et al. Defining the oncogenic function of the TEL/AML1 (ETV6/RUNX1) fusion protein in a mouse model. Oncogene. 2005;24(51):7579-7591.
10. Schindler JW, Van Buren D, Foudi A, Krejci O, Qin J, Orkin SH, Hock H. TEL-AML1 corrupts hematopoietic stem cells to persist in the bone marrow and initiate leukemia. Cell Stem Cell. 2009;5(1):43-53.
11. Hong D, Gupta R, Ancliff P, et al. Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science. 2008; 319(5861):336-339.
12. Bernardin F, Yang Y, Cleaves R, Zahurak M, Cheng L, Civin CI, Friedman AD. TEL-AML1, expressed from t(12;21) in human acute lymphocytic leukemia, induces acute leukemia in mice. Cancer Res. 2002;62(14):3904-3908.
13. van der Weyden L, Giotopoulos G, Rust AG, et al. Modeling the evolution of ETV6-RUNX1-induced B-cell precursor acute lymphoblastic leukemia in mice. Blood. 2011;118(4):1041-1051.
14. Mullighan CG. Molecular genetics of B-precursor acute lymphoblastic leukemia. J Clin Invest. 2012; 122(10):3407-3415.
15. Wiemels JL, Ford AM, Van Wering ER, Postma A, Greaves M. Protracted and variable latency of acute lymphoblastic leukemia after TEL-AML1 gene fusion in utero. Blood. 1999;94(3): 1057-1062.
16. Mori H, Colman SM, Xiao Z, et al. Chromosome translocations and covert leukemic clones are generated during normal fetal development. Proc Natl Acad Sci USA. 2002;99(12):8242-8247.
17. Lausten-Thomsen U, Madsen HO, Vestergaard TR, Hjalgrim H, Nersting J, Schmiegelow K. Prevalence of t(12;21)[ETV6-RUNX1]-positive cells in healthy neonates. Blood. 2011;117(1): 186-189.
18. Anderson K, Lutz C, van Delft FW, et al. Genetic variegation of clonal architecture and propagating cells in leukaemia. Nature. 2011;469(7330): 356-361.
19. Notta F, Mullighan CG, Wang JC, et al. Evolution of human BCR-ABL1 lymphoblastic leukaemiainitiating cells. Nature. 2011;469(7330):362-367.
20. Diakos C, Krapf G, Gerner C, et al. RNAi-mediated silencing of TEL/AML1 reveals a heat-shock protein-and survivin-dependent mechanism for survival. Blood. 2007;109(6): 2607-2610.
21. Diakos C, Zhong S, Xiao Y, et al. TEL-AML1 regulation of survivin and apoptosis via miRNA-494 and miRNA-320a. Blood. 2010;116(23): 4885-4893.
22. Fuka G, Kantner HP, Grausenburger R, et al. Silencing of ETV6/RUNX1 abrogates PI3K/AKT/mTOR signaling and impairs reconstitution of leukemia in xenografts. Leukemia. 2012;26(5): 927-933.
23. Inthal A, Krapf G, Beck D, et al. Role of the erythropoietin receptor in ETV6/RUNX1-positive acute lymphoblastic leukemia. Clin Cancer Res. 2008;14(22):7196-7204.
24. Krapf G, Kaindl U, Kilbey A, et al. ETV6/RUNX1 abrogates mitotic checkpoint function and targets its key player MAD2L1. Oncogene. 2010;29(22): 3307-3312.
25. Torrano V, Procter J, Cardus P, Greaves M, Ford AM. ETV6-RUNX1 promotes survival of early B lineage progenitor cells via a dysregulated erythropoietin receptor. Blood. 2011;118(18): 4910-4918.
26. Frank DA. STAT3 as a central mediator of neoplastic cellular transformation. Cancer Lett. 2007;251(2):199-210.
27. Benekli M, Baumann H, Wetzler M. Targeting signal transducer and activator of transcription signaling pathway in leukemias. J Clin Oncol. 2009;27(26):4422-4432.
28. Müller J, Sperl B, Reindl W, Kiessling A, Berg T. Discovery of chromone-based inhibitors of the transcription factor STAT5. ChemBioChem. 2008; 9(5):723-727.
29. Gao Y, Dickerson JB, Guo F, Zheng J, Zheng Y. Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc Natl Acad Sci USA. 2004;101(20):7618-7623.
30. Den Boer ML, Harms DO, Pieters R, et al. Patient stratification based on prednisolone-vincristineasparaginase resistance profiles in children with acute lymphoblastic leukemia. J Clin Oncol. 2003; 21(17):3262-3268.
31. Morrow M, Samanta A, Kioussis D, Brady HJ, Williams O. TEL-AML1 preleukemic activity requires the DNA binding domain of AML1 and the dimerization and corepressor binding domains of TEL. Oncogene. 2007;26(30):4404-4414.
32. Coppo P, Dusanter-Fourt I, Millot G, et al. Constitutive and specific activation of STAT3 by BCR-ABL in embryonic stem cells. Oncogene. 2003;22(26):4102-4110.
33. Siddiquee K, Zhang S, Guida WC, et al. Selective chemical probe inhibitor of Stat3, identified through structure-based virtual screening, induces antitumor activity. Proc Natl Acad Sci USA. 2007;104(18):7391-7396.
34. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature. 2002;420(6916):629-635.
35. Cancelas JA, Williams DA. Rho GTPases in hematopoietic stem cell functions. Curr Opin Hematol. 2009;16(4):249-254.
36. Raptis L, Arulanandam R, Geletu M, Turkson J. The R(h)oads to Stat3: Stat3 activation by the Rho GTPases. Exp Cell Res. 2011;317(13): 1787-1795.
37. Delgado MD, Léon J. Myc roles in hematopoiesis and leukemia. Genes Cancer. 2010;1(6):605-616.
38. Fukuda S, Pelus LM. Survivin, a cancer target with an emerging role in normal adult tissues. Mol Cancer Ther. 2006;5(5):1087-1098.
39. Chou WC, Levy DE, Lee CK. STAT3 positively regulates an early step in B-cell development. Blood. 2006;108(9):3005-3011.
40. Malin S, McManus S, Busslinger M. STAT5 in B cell development and leukemia. Curr Opin Immunol. 2010;22(2):168-176.
41. Peeters P, Raynaud SD, Cools J, et al. Fusion of TEL, the ETS-variant gene 6 (ETV6), to the receptor-associated kinase JAK2 as a result of t(9;12) in a lymphoid and t(9;15;12) in a myeloid leukemia. Blood. 1997;90(7):2535-2540.
42. Mullighan CG, Zhang J, Harvey RC, et al. JAK mutations in high-risk childhood acute lymphoblastic leukemia. Proc Natl Acad Sci USA. 2009;106(23):9414-9418.
43. Deininger MW, Goldman JM, Lydon N, Melo JV. The tyrosine kinase inhibitor CGP57148B selectively inhibits the growth of BCR-ABLpositive cells. Blood. 1997;90(9):3691-3698.
44. Koskela HL, Eldfors S, Ellonen P, et al. Somatic STAT3 mutations in large granular lymphocytic leukemia. N Engl J Med. 2012;366(20): 1905-1913.
45. Fuka G, Kauer M, Kofler R, Haas OA, Panzer-Grümayer R. The leukemia-specific fusion gene ETV6/RUNX1 perturbs distinct key biological functions primarily by gene repression. PLoS ONE. 2011;6(10):e26348.
46. Lyons R, Williams O, Morrow M, Sebire N, Hubank M, Anderson J. The RAC specific guanine nucleotide exchange factor Asef functions downstream from TEL-AML1 to promote leukaemic transformation. Leuk Res. 2010;34(1): 109-115.
47. Kiuchi N, Nakajima K, Ichiba M, et al. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med. 1999;189(1):63-73.
48. Nesbit CE, Tersak JM, Prochownik EV. MYC oncogenes and human neoplastic disease. Oncogene. 1999;18(19):3004-3016.
49. Kato Y, Iwama A, Tadokoro Y, et al. Selective activation of STAT5 unveils its role in stem cell selfrenewal in normal and leukemic hematopoiesis. J Exp Med. 2005;202(1):169-179.
50. Kortylewski M, Kujawski M, Wang T, et al. Inhibiting Stat3 signaling in the hematopoietic system elicits multicomponent antitumor immunity. Nat Med. 2005;11(12):1314-1321.