K-RasG12D-induced T-cell lymphoblastic lymphoma/leukemias harbor Notch1 mutations and are sensitive to {gamma}-secretase inhibitors

Blood

Volumn 112, Issue 8, 2008, Pages 3373-3382

  Kindler, Thomas ^a,e   Cornejo, Melanie G ^a   Scholl, Claudia ^a   Liu, Jianing ^a   Leeman, Dena S ^a   Haydu, J Erika ^a   Fröhling, Stefan ^a   Lee, Benjamin H ^a,b   Gilliland, D Gary ^a,c,d  

^a Division of Hematology   (Germany)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c DANA FARBER CANCER INSTITUTE   (United States)

^d HARVARD MEDICAL SCHOOL   (United States)

^e JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; CD4 ANTIGEN; CD8 ANTIGEN; GAMMA SECRETASE INHIBITOR; HERMES ANTIGEN; K RAS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH1 RECEPTOR; RAPAMYCIN; NOTCH1 PROTEIN, HUMAN; RAS PROTEIN; SECRETASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CONTROLLED STUDY; DOWN REGULATION; GENE MUTATION; IMMUNOPHENOTYPING; LYMPHOBLAST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; T CELL LEUKEMIA; T CELL LYMPHOMA; ANIMAL; BIOSYNTHESIS; BONE MARROW CELL; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; GENE EXPRESSION REGULATION; GENETICS; HUMAN; MUTATION; ONCOGENE RAS; PHYSIOLOGY; TRANSGENIC MOUSE;

AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIGENS, CD44; BONE MARROW CELLS; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION; GENES, RAS; HUMANS; LEUKEMIA, T-CELL; LYMPHOMA, T-CELL; MICE; MICE, TRANSGENIC; MUTATION; RAS PROTEINS; RECEPTOR, NOTCH1;

EID: 54049141335     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2008-03-147587     Document Type: Article

References (55)

1. Bourne HR, Sanders DA, McCormick F. The GTPase superfamily: conserved structure and molecular mechanism. Nature. 1991;349:117-127.
2. Herrmann C. Ras-effector interactions: after one decade. Curr Opin Struct Biol. 2003;13:122-129.
3. Boguski MS, McCormick F. Proteins regulating Ras and its relatives. Nature. 1993;366:643-654.
4. Repasky GA, Chenette EJ, Der CJ. Renewing the conspiracy theory debate: does Rat function alone to mediate Ras oncogenesis? Trends Cell Biol. 2004;14:639-647.
5. Rodriguez-Viciana P, Warne PH, Dhand R, et al. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 1994;370:527-532.
6. Wolthuis RM, Bos JL. Ras caught in another affair: the exchange factors for Ral. Curr Opin Genet Dev. 1999;9:112-117.
7. Kelley GG, Reks SE, Ondrako JM, Smrcka AV. Phospholipase C(epsilon): a novel Ras effector. EMBO J. 2001;20:743-754.
8. Hingorani SR, Tuveson DA. Ras redux: rethinking how and where Ras acts. Curr Opin Genet Dev. 2003;13:6-13.
9. Johnson L, Greenbaum D, Cichowski K. et al. K-ras is an essential gene in the mouse with partial functional overlap with N-ras. Genes Dev. 1997;11:2468-2481.
10. Ellis CA, Clark G. The importance of being K-Ras. Cell Signal. 2000;12:425-434.
11. Forbes S, Clements J, Dawson E, et al. Cosmic 2005. Br J Cancer. 2006;94:318-322.
12. Bowen DT, Frew ME, Hills R, et al. RAS mutation in acute myeloid leukemia is associated with distinct cytogenetic subgroups but does not influence outcome in patients younger than 60 years. Blood. 2005;106:2113-2119.
13. Lauchle JO, Braun BS, Loh ML, Shannon K. Inherited predispositions and hyperactive Ras in myeloid leukemogenesis. Pediatr Blood Cancer. 2006;46:579-585.
14. Perentesis JP, Bhatia S, Boyle E, et al. RAS oncogene mutations and outcome of therapy for childhood acute lymphoblastic leukemia. Leukemia. 2004;18:685-692.
15. Schubbert S, Shannon K, Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat Rev Cancer. 2007;7:295-308.
16. Gilliland DG, Griffin JD. Role of FLT3 in leukemia. Curr Opin Hematol. 2002;9:274-281.
17. Beghini A, Peterlongo P, Ripamonti CB, et al. C-kit mutations in core binding factor leukemias. Blood. 2000;95:726-727.
18. Papadopoulos P, Ridge SA, Boucher CA, Stocking C, Wiedemann LM. The novel activation of ABL by fusion to an ets-related gene, TEL. Cancer Res. 1995;55:34-38.
19. Graux C, Cools J, Melotte C, et al. Fusion of NUP214 to ABL1 on amplified episomes in T-cell acute lymphoblastic leukemia. Nat Genet. 2004; 36:1084-1089.
20. von Lintig FC, Huvar I, Law P, Diccianni MB, Yu AL, Boss GR. Ras activation in normal white blood cells and childhood acute lymphoblastic leukemia. Clin Cancer Res. 2000;6:1804-1810.
21. Tuveson DA, Shaw AT, Willis NA, et al. Endogenous oncogenic K-ras(G12D) stimulates proliferation and widespread neoplastic and developmental defects. Cancer Cell. 2004;5:375-387.
22. Chan IT, Kutok JL, Williams IR, et al. Conditional expression of oncogenic K-ras from its endogenous promoter induces a myeloproliferative disease. J Clin Invest. 2004;113:528-538.
23. Braun BS, Tuveson DA, Kong N, et al. Somatic activation of oncogenic Kras in hematopoietic cells initiates a rapidly fatal myeloproliferative disorder. Proc Natl Acad Sci U S A. 2004;101:597-602.
24. Van Meter ME, Diaz-Flores E, Archard JA, et al. K-RasG12D expression induces hyperproliferation and aberrant signaling in primary hematopoietic stem/progenitor cells. Blood. 2007;109:3945-3952.
25. Gartner F, Alt FW, Monroe R, et al. Immature thymocytes employ distinct signaling pathways for allelic exclusion versus differentiation and expansion. Immunity. 1999;10:537-546.
26. Crompton T, Gilmour KC, Owen MJ. The MAP kinase pathway controls differentiation from double-negative to double-positive thymocyte. Cell. 1996;86:243-251.
27. Genot E, Cantrell DA. Ras regulation and function in lymphocytes. Curr Opin Immunol. 2000:12: 289-294.
28. Dunbar CE, Crosier PS, Nienhuis AW. Introduction of an activated RAS oncogene into murine bone marrow lymphoid progenitors via retroviral gene transfer results in thymic lymphomas. Oncogene Res. 1991;6:39-51.
29. Hawley RG, Fong AZ, Ngan BY, HawleyTS. Hematopoietic transforming potential of activated ras in chimeric mice. Oncogene. 1995; 11:1113-1123.
30. Kelliher MA, Seldin DC, Leder P. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase llalpha. EMBO J. 1996;15:5160-5166.
31. Larson RC, Lavenir I, Larson TA, 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.
32. Bain G, Engel I, Robanus Maandag EC, et al. 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.
33. Yan W, Young AZ, Soares VC, Kelley R, Benezra R, Zhuang Y. High incidence of T-cell tumors in E2A-null mice and E2A/ld1 double-knockout mice. Mol Cell Biol. 1997;17:7317-7327.
34. Shank-Calvo JA, Draheim K, Bhasin M, Kelliher MA. p161nk4a or p19Arf loss contributes to Tall-induced leukemogenesis in mice. Oncogene. 2006;25:3023-3031.
35. Grabher C, von Boehmer H, Look AT. Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer. 2006:6:347-359.
36. Weng AP, Ferrando AA, Lee W, et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 2004;306:269-271.
37. Reschly EJ, Spaulding C, Vilimas T, et al. Notch1 promotes survival of E2A-deficient T cell lymphomas through pre-T cell receptor-dependent and -independent mechanisms. Blood. 2006;107: 4115-4121.
38. Lin YW, Nichols RA, Letterio JJ, Apian PD. Notchl mutations are important for leukemic transformation in murine models of precursor-T leukernia/lymphoma. Blood. 2006;107:2540-2543.
39. Baker FJ, Lee M, Chien YH, Davis MM. Restricted islet-cell reactive T cell repertoire of early pancreatic islet infiltrates in NOD mice. Proc Natl Acad Sci U S A. 2002;99:9374-9379.
40. O'Neil J, Calvo J, McKenna K, et al. Activating Notchl mutations in mouse models of T-ALL. Blood. 2006;107:781-785.
41. KindlerT, Breitenbuecher F, Kasper S, et al. Identification of a novel activating mutation (Y842C) within the activation loop of FLT3 in patients with acute myeloid leukemia (AML). Blood. 2005;105: 335-340.
42. Rothenberg EV, Taghon T. Molecular genetics of Tcell development. Annu Rev Immunol. 2005;23: 601-649.
43. Gutierrez A, LookAT. NOTCH and PI3K-AKT pathways intertwined. Cancer Cell. 2007; 12:411-413.
44. Chervinsky DS, Zhao XF, Lam DH, Ellsworth M, Gross KW, Apian PD. Disordered T-cell development and T-cell malignancies in SCL LMOI double-transgenic mice: parallels with E2A-deficient mice. Mol Cell Biol. 1999;19:5025-5035.
45. Herblot S, Steff AM, Hugo P, Apian 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.
46. O'Neil J, Shank J, Cusson N, Murre C, Kelliher M. TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Gancer Cell. 2004;5:587-596.
47. Zhang J, Liu Y, Beard C, et al. Expression of oncogenic K-ras from its endogenous promoter leads to a partial block of erythroid differentiation and hyperactivation of cytokine-dependent signaling pathways. Blood. 2007;109:5238-5241.
48. Braun BS, Archard JA, Van Ziffle JA, Tuveson DA, Jacks TE, Shannon K. Somatic activation of a conditional KrasG1 2 D allele causes ineffective erythropoiesis in vivo. Blood. 2006;108:2041-2044.
49. Walkley CR, Olsen GH. Dworkin S, et al. A microenvironment-induced myeloproliferative syndrome caused by retinoic acid receptor gamma deficiency. Cell. 2007;129:1097-1110.
50. Walkley CR, Shea JM, Sims NA, Purton LE, Orkin SH. Rb regulates interactions between hematopoietic stem cells and their bone marrow microenvironment. Cell. 2007;129:1081-1095.
51. O'Neil J, Grim J, Strack P, etal. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J Exp Med. 2007;204:1813-1824.
52. Thompson BJ, Buonamici S, Sulis ML, et al. The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in Tcell leukemia. J Exp Med. 2007; 204:1825-1835.
53. Graux C, Cools J, Michaux L, Vandenberghe P, Hagemeijer A. Cytogenetics and molecular genetics of T-cell acute lymphoblastic leukemia: from thymocyte to lymphoblast. Leukemia. 2006; 20:1496-1510.
54. Chan SM, Weng AP, Tibshirani R, Aster JC, Utz PJ. Notch signals positively regulate activity of the mTOR pathway in T-cell acute lymphoblastic leukemia. Blood. 2007;110:278-286.
55. Weijzen S, Rizzo P, Braid M, et al. Activation of Notch-1 signaling maintains the neoplastic phenotype in human Ras-transformed cells. Nat Med. 2002;8:979-986.