Interleukin-7 receptor mutants initiate early t cell precursor leukemia in murine thymocyte progenitors with multipotent potential

Journal of Experimental Medicine

Volumn 211, Issue 4, 2014, Pages 701-713

  Treanor, Louise M ^a   Zhou, Sheng ^a   Janke, Laura ^a   Churchman, Michelle L ^a   Ma, Zhijun ^a   Lu, Taihe ^a   Chen, Shann Ching ^a   Mullighan, Charles G ^a   Sorrentino, Brian P ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 7 RECEPTOR; JANUS KINASE; MEMBRANE PROTEIN; MESSENGER RNA; NOTCH1 RECEPTOR; PROTEIN LMO2; RUXOLITINIB; STAT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCL11B; UNCLASSIFIED DRUG;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; FEMALE; GENE OVEREXPRESSION; HUMAN; LEUKEMIA CELL; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; THYMOCYTE; TUMOR GROWTH;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CARCINOGENESIS; CELL DIFFERENTIATION; CHILD; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; JANUS KINASES; LIM DOMAIN PROTEINS; MICE; MULTIPOTENT STEM CELLS; MUTATION; NEOPLASM TRANSPLANTATION; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHENOTYPE; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PYRAZOLES; RECEPTORS, INTERLEUKIN-7; RECEPTORS, NOTCH; REPRESSOR PROTEINS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS; THYMOCYTES; TUMOR SUPPRESSOR PROTEINS;

EID: 84897951382     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20122727     Document Type: Article

References (39)

1. Bell, J.J., and A. Bhandoola. 2008. The earliest thymic progenitors for T cells possess myeloid lineage potential. Nature. 452:764-767. http://dx.doi.org/10.1038/nature0684
2. Coustan-Smith, E., C.G. Mullighan, M. Onciu, F.G. Behm, S.C. Raimondi, D. Pei, C. Cheng, X. Su, J.E. Rubnitz, G. Basso, et al. 2009. Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol. 10:147-156. http://dx.doi.org/10.1016/S1470-2045(08)70314-0
3. De Obaldia, M.E., J.J. Bell, and A. Bhandoola. 2013. Early T-cell progenitors are the major granulocyte precursors in the adult mouse thymus. Blood. 121:64-71. http://dx.doi.org/10.1182/blood-2012-08-45177
4. Eppert, K., K. Takenaka, E.R. Lechman, L. Waldron, B. Nilsson, P. van Galen, K.H. Metzeler, A. Poeppl, V. Ling, J. Beyene, et al. 2011. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat. Med. 17:1086-1093. http://dx.doi.org/10.1038/nm.241
5. Felsher, D.W. 2003. Cancer revoked: oncogenes as therapeutic targets. Nat. Rev. Cancer. 3:375-380. http://dx.doi.org/10.1038/nrc107
6. Felsher, D.W., and J.M. Bishop. 1999. Reversible tumorigenesis by MYC in hematopoietic lineages. Mol. Cell. 4:199-207. http://dx.doi.org/1.1016/S1097-2765(00)80367-6
7. Gutierrez, A., A. Kentsis, T. Sanda, L. Holmfeldt, S.C. Chen, J. Zhang, A. Protopopov, L. Chin, S.E. Dahlberg, D.S. Neuberg, et al. 2011. The BCL11B tumor suppressor is mutated across the major molecular subtypes of T-cell acute lymphoblastic leukemia. Blood. 118:4169-4173. http://dx.doi.org/10.1182/blood-2010-11-31887
8. Harrison, C., J.J. Kiladjian, H.K. Al-Ali, H. Gisslinger, R. Waltzman, V. Stalbovskaya, M. McQuitty, D.S. Hunter, R. Levy, L. Knoops, et al. 2012. JAK inhibition with ruxolitinib versus best available therapy for myelofibrosis. N. Engl. J. Med. 366:787-798. http://dx.doi.org/1.1056/NEJMoa1110556
9. Herblot, S., A.M. Steff, P. Hugo, P.D. Aplan, and T. Hoang. 2000. SCL and LMO1 alter thymocyte differentiation: inhibition of E2A-HEB function and pre-T alpha chain expression. Nat. Immunol. 1:138-144. http://dx.doi.org/10.1038/77819
10. Holleman, A., M.H. Cheok, M.L. den Boer, W. Yang, A.J. Veerman, K.M. Kazemier, D. Pei, C. Cheng, C.H. Pui, M.V. Relling, et al. 2004. Geneexpression patterns in drug-resistant acute lymphoblastic leukemia cells and response to treatment. N. Engl. J. Med. 351:533-542. http://dx.doi.org/10.1056/NEJMoa033513
11. Ikawa, T., S. Hirose, K. Masuda, K. Kakugawa, R. Satoh, A. Shibano-Satoh, R. Kominami, Y. Katsura, and H. Kawamoto. 2010. An essential developmental checkpoint for production of the T cell lineage. Science. 329:93-96. http://dx.doi.org/10.1126/science.1188995
12. Kamijo, T., F. Zindy, M.F. Roussel, D.E. Quelle, J.R. Downing, R.A. Ashmun, G. Grosveld, and C.J. Sherr. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell. 91:649-659. http://dx.doi.org/10.1016/S0092-8674(00)80452-3
13. King, A.G., M. Kondo, D.C. Scherer, and I.L. Weissman. 2002. Lineage infidelity in myeloid cells with TCR gene rearrangement: a latent developmental potential of proT cells revealed by ectopic cytokine receptor signaling. Proc. Natl. Acad. Sci. USA. 99:4508-4513. http://dx.doi.org/10.1073/pnas.072087899
14. Larson, R.C., H. Osada, T.A. Larson, I. Lavenir, and T.H. Rabbitts. 1995. The oncogenic LIM protein Rbtn2 causes thymic developmental aberrations that precede malignancy in transgenic mice. Oncogene. 11:853-862.
15. Li, L., M. Leid, and E.V. Rothenberg. 2010. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science. 329:89-93. http://dx.doi.org/10.1126/science.1188989
16. Neale, G.A., J.E. Rehg, and R.M. Goorha. 1995. Ectopic expression of rhombotin-2 causes selective expansion of CD4-CD8-lymphocytes in the thymus and T-cell tumors in transgenic mice. Blood. 86:3060-3071.
17. Neale, G.A., J.E. Rehg, and R.M. Goorha. 1997. Disruption of T-cell differentiation precedes T-cell tumor formation in LMO-2 (rhombotin-2) transgenic mice. Leukemia. 11(Suppl 3):289-290.
18. Nishigaki, H., C. Ito, A. Manabe, M. Kumagai, E. Coustan-Smith, Y. Yanishevski, F.G. Behm, S.C. Raimondi, C.H. Pui, and D. Campana. 1997. Prevalence and growth characteristics of malignant stem cells in B-lineage acute lymphoblastic leukemia. Blood. 89:3735-3744.
19. Richie Ehrlich, L.I., T. Serwold, and I.L. Weissman. 2011. In vitro assays misrepresent in vivo lineage potentials of murine lymphoid progenitors. Blood. 117:2618-2624. http://dx.doi.org/10.1182/blood-2010-05-287102
20. Rothenberg, E.V., J. Zhang, and L. Li. 2010. Multilayered specification of the T-cell lineage fate. Immunol. Rev. 238:150-168. http://dx.doi.org/10.1111/j.1600-065X.2010.00964.x
21. Ryu, B.Y., M.V. Evans-Galea, J.T. Gray, D.M. Bodine, D.A. Persons, and A.W. Nienhuis. 2008. An experimental system for the evaluation of retroviral vector design to diminish the risk for proto-oncogene activation. Blood. 111:1866-1875. http://dx.doi.org/10.1182/blood-2007-04-085506
22. Schlenner, S.M., and H.R. Rodewald. 2010. Early T cell development and the pitfalls of potential. Trends Immunol. 31:303-310. http://dx.doi.org/10.1016/j.it.2010.06.002
23. Schlenner, S.M., V. Madan, K. Busch, A. Tietz, C. Läufle, C. Costa, C. Blum, H.J. Fehling, and H.R. Rodewald. 2010. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity. 32:426-436. http://dx.doi.org/10.1016/j.immuni.2010.03.005
24. Shah, N.P., C. Kasap, C. Weier, M. Balbas, J.M. Nicoll, E. Bleickardt, C. Nicaise, and C.L. Sawyers. 2008. Transient potent BCR-ABL inhibition is sufficient to commit chronic myeloid leukemia cells irreversibly to apoptosis. Cancer Cell. 14:485-493. http://dx.doi.org/10.1016/j.ccr.2008.11.001
25. Sherr, C.J. 2004. An Arf(GFP/GFP) reporter mouse reveals that the Arf tumor suppressor monitors latent oncogenic signals in vivo. Cell Cycle. 3:239-240. http://dx.doi.org/10.4161/cc.3.3.744
26. Shochat, C., N. Tal, O.R. Bandapalli, C. Palmi, I. Ganmore, G. te Kronnie, G. Cario, G. Cazzaniga, A.E. Kulozik, M. Stanulla, et al. 2011. Gainof-function mutations in interleukin-7 receptor-α (IL7R) in childhood acute lymphoblastic leukemias. J. Exp. Med. 208:901-908. http://dx.doi.org/10.1084/jem.20110580
27. Shou, Y., Z. Ma, T. Lu, and B.P. Sorrentino. 2006. Unique risk factors for insertional mutagenesis in a mouse model of XSCID gene therapy. Proc. Natl. Acad. Sci. USA. 103:11730-11735. http://dx.doi.org/10.1073/pnas.0603635103
28. Singh, A., P. Greninger, D. Rhodes, L. Koopman, S. Violette, N. Bardeesy, and J. Settleman. 2009. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell. 15:489-500. http://dx.doi.org/10.1016/j.ccr.2009.03.022
29. Tanigaki, K., and T. Honjo. 2007. Regulation of lymphocyte development by Notch signaling. Nat. Immunol. 8:451-456. http://dx.doi.org/10.1038/ni1453
30. Torchia, E.C., K. Boyd, J.E. Rehg, C. Qu, and S.J. Baker. 2007. EWS/FLI-1 induces rapid onset of myeloid/erythroid leukemia in mice. Mol. Cell. Biol. 27:7918-7934. http://dx.doi.org/10.1128/MCB.00099-07
31. Treanor, L.M., E.J. Volanakis, S. Zhou, T. Lu, C.J. Sherr, and B.P. Sorrentino. 2011. Functional interactions between Lmo2, the Arf tumor suppressor, and Notch1 in murine T-cell malignancies. Blood. 117:5453-5462. http://dx.doi.org/10.1182/blood-2010-09-309831
32. Volanakis, E.J., R.T. Williams, and C.J. Sherr. 2009. Stage-specific Arf tumor suppression in Notch1-induced T-cell acute lymphoblastic leukemia. Blood. 114:4451-4459. http://dx.doi.org/10.1182/blood-2009-07-233346
33. Wada, H., K. Masuda, R. Satoh, K. Kakugawa, T. Ikawa, Y. Katsura, and H. Kawamoto. 2008. Adult T-cell progenitors retain myeloid potential. Nature. 452:768-772. http://dx.doi.org/10.1038/nature06839
34. Wakabayashi, Y., H. Watanabe, J. Inoue, N. Takeda, J. Sakata, Y. Mishima, J. Hitomi, T. Yamamoto, M. Utsuyama, O. Niwa, et al. 2003. Bcl11b is required for differentiation and survival of alphabeta T lymphocytes. Nat. Immunol. 4:533-539. http://dx.doi.org/10.1038/ni927
35. Weng, A.P., A.A. Ferrando, W. Lee, J.P. Morris IV, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 306:269-271. http://dx.doi.org/10.1126/science.1102160
36. Yui, M.A., N. Feng, and E.V. Rothenberg. 2010. Fine-scale staging of T cell lineage commitment in adult mouse thymus. J. Immunol. 185:284-293. http://dx.doi.org/10.4049/jimmunol.1000679
37. Zenatti, P.P., D. Ribeiro, W. Li, L. Zuurbier, M.C. Silva, M. Paganin, J. Tritapoe, J.A. Hixon, A.B. Silveira, B.A. Cardoso, et al. 2011. Oncogenic IL7R gain-of-function mutations in childhood T-cell acute lymphoblastic leukemia. Nat. Genet. 43:932-939. http://dx.doi.org/10.1038/ng.924
38. Zhang, J., L. Ding, L. Holmfeldt, G. Wu, S.L. Heatley, D. Payne-Turner, J. Easton, X. Chen, J. Wang, M. Rusch, et al. 2012. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 481:157-163. http://dx.doi.org/10.1038/nature10725
39. Zuber, J., A.R. Rappaport, W. Luo, E. Wang, C. Chen, A.V. Vaseva, J. Shi, S. Weissmueller, C. Fellmann, M.J. Taylor, et al. 2011. An integrated approach to dissecting oncogene addiction implicates a Myb-coordinated self-renewal program as essential for leukemia maintenance. Genes Dev. 25:1628-1640. http://dx.doi.org/10.1101/gad.17269211