Distinct classes of c-Kit-activating mutations differ in their ability to promote RUNX1-ETO-associated acute myeloid leukemia

Blood

Volumn 119, Issue 6, 2012, Pages 1522-1531

  Nick, Heidi J ^a   Kim, Hyung Gyoon ^a   Chang, Chia Wei ^b   Harris, Kevin W ^c   Reddy, Vishnu ^d   Klug, Christopher A ^a,b,d  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

^d University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETROVIRUS VECTOR; STEM CELL FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR ETO; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B CELL LEUKEMIA; BONE MARROW CELL; CANCER TRANSPLANTATION; CELL LINEAGE; CELL STRUCTURE; CONTROLLED STUDY; CYTOGENETICS; DIMERIZATION; EXON; GENE EXPRESSION; GENE MUTATION; GENOTYPE PHENOTYPE CORRELATION; GRANULOCYTIC SARCOMA; HEMATOPOIETIC STEM CELL; IMMUNOPHENOTYPING; LEUKEMIA CELL; LEUKEMOGENESIS; MOUSE; MYELOPROLIFERATIVE DISORDER; NONHUMAN; PHENOTYPE; PRE B LYMPHOCYTE; PRIORITY JOURNAL; VIRAL GENE DELIVERY SYSTEM;

EID: 84863183137     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-02-338228     Document Type: Article

References (50)

1. Downing JR. The core-binding factor leukemias: lessons learned from murine models. Curr Opin Genet Dev. 2003;13(1):48-54. (Pubitemid 36143927)
2. Look AT. Oncogenic transcription factors in the human acute leukemias. Science. 1997; 278(5340):1059-1064. (Pubitemid 27517875)
3. Erickson P, Gao J, Chang KS, et al. Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ ETO, with similarity to Drosophila segmentation gene, runt. Blood. 1992;80(7):1825-1831.
4. Miyoshi H, Shimizu K, Kozu T, Maseki N, Kaneko Y, Ohki M. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc Natl Acad Sci U S A. 1991;88(23): 10431-10434. (Pubitemid 21915849)
5. Wang J, Hoshino T, Redner RL, Kajigaya S, Liu JM. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc Natl Acad Sci U S A. 1998;95(18): 10860-10865. (Pubitemid 28413159)
6. Amann JM, Nip J, Strom DK, et al. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol Cell Biol. 2001;21(19):6470-6483. (Pubitemid 32927415)
7. Lutterbach B, Westendorf JJ, Linggi B, et al. ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol Cell Biol. 1998;18(12):7176-7184. (Pubitemid 28533037)
8. Gelmetti V, Zhang J, Fanelli M, Minucci S, Pelicci PG, Lazar MA. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol Cell Biol. 1998;18(12): 7185-7191. (Pubitemid 28533038)
9. Okuda T, Cai Z, Yang S, et al. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood. 1998;91(9):3134-3143. (Pubitemid 28193861)
10. Wang Q, Stacy T, Binder M, Marin-Padilla M, Sharpe AH, Speck NA. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc Natl Acad Sci U S A. 1996; 93(8):3444-3449. (Pubitemid 26125639)
11. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 1996;84(2):321-330. (Pubitemid 26042836)
12. Yergeau DA, Hetherington CJ, Wang Q, et al. Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat Genet. 1997;15(3):303-306. (Pubitemid 27098728)
13. Wiemels JL, Xiao Z, Buffler PA, et al. In utero origin of t(8;21) AML1-ETO translocations in childhood acute myeloid leukemia. Blood. 2002; 99(10):3801-3805. (Pubitemid 34534554)
14. Higuchi M, O'Brien D, Kumaravelu P, Lenny N, Yeoh EJ, Downing JR. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell. 2002;1(1):63-74. (Pubitemid 41039177)
15. Rhoades KL, Hetherington CJ, Harakawa N, et al. Analysis of the role of AML1-ETO in leukemogenesis, using an inducible transgenic mouse model. Blood. 2000;96(6):2108-2115.
16. de Guzman CG, Warren AJ, Zhang Z, et al. Hematopoietic stem cell expansion and distinct myeloid developmental abnormalities in a murine model of the AML1-ETO translocation. Mol Cell Biol. 2002;22(15):5506-5517.
17. Miyamoto T, Nagafuji K, Akashi K, et al. Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood. 1996;87(11):4789-4796. (Pubitemid 26162380)
18. Muller AM, Duque J, Shizuru JA, Lubbert M. Complementing mutations in core binding factor leukemias: from mouse models to clinical applications. Oncogene. 2008;27(44):5759-5773.
19. Grisolano JL, O'Neal J, Cain J, Tomasson MH. An activated receptor tyrosine kinase, TEL/PDGF-betaR, cooperates with AML1/ETO to induce acute myeloid leukemia in mice. Proc Natl Acad Sci U S A. 2003;100(16):9506-9511. (Pubitemid 37033958)
20. Schessl C, Rawat VP, Cusan M, et al. The AML1- ETO fusion gene and the FLT3 length mutation collaborate in inducing acute leukemia in mice. J Clin Invest. 2005;115(8):2159-2168. (Pubitemid 41134157)
21. Nishida S, Hosen N, Shirakata T, et al. AML1- ETO rapidly induces acute myeloblastic leukemia in cooperation with the Wilms tumor gene, WT1. Blood. 2006;107(8):3303-3312.
22. Schwieger M, Lohler J, Friel J, Scheller M, Horak I, Stocking C. AML1-ETO inhibits maturation of multiple lymphohematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency. J Exp Med. 2002;196(9): 1227-1240. (Pubitemid 35304188)
23. Peterson LF, Yan M, Zhang DE. The p21Waf1 pathway is involved in blocking leukemogenesis by the t(8;21) fusion protein AML1-ETO. Blood. 2007;109(10):4392-4398. (Pubitemid 46743408)
24. Schnittger S, Kohl TM, Haferlach T, et al. KITD816 mutations in AML1-ETO-positive AML are associated with impaired event-free and overall survival. Blood. 2006;107(5):1791-1799. (Pubitemid 43289355)
25. Gari M, Goodeve A, Wilson G, et al. c-kit protooncogene exon 8 in-frame deletion plus insertion mutations in acute myeloid leukaemia. Br J Haematol. 1999;105(4):894-900. (Pubitemid 29309094)
26. Beghini A, Peterlongo P, Ripamonti CB, et al. Ckit mutations in core binding factor leukemias. Blood. 2000;95(2):726-727. (Pubitemid 30041697)
27. Care RS, Valk PJ, Goodeve AC, et al. Incidence and prognosis of c-KIT and FLT3 mutations in core binding factor (CBF) acute myeloid leukaemias. Br J Haematol. 2003;121(5):775-777. (Pubitemid 36718195)
28. Cairoli R, Grillo G, Beghini A, et al. C-Kit point mutations in core binding factor leukemias: correlation with white blood cell count and the white blood cell index. Leukemia. 2003;17(2):471-472. (Pubitemid 36266930)
29. Nanri T, Matsuno N, Kawakita T, et al. Mutations in the receptor tyrosine kinase pathway are associated with clinical outcome in patients with acute myeloblastic leukemia harboring t(8;21)(q22; q22). Leukemia. 2005;19(8):1361-1366. (Pubitemid 41136329)
30. Wang YY, Zhou GB, Yin T, et al. AML1-ETO and C-KIT mutation/ overexpression in t(8;21) leukemia: implication in stepwise leukemogenesis and response to Gleevec. Proc Natl Acad Sci U S A. 2005;102(4):1104-1109. (Pubitemid 40170733)
31. Kuchenbauer F, Schnittger S, Look T, et al. Identification of additional cytogenetic and molecular genetic abnormalities in acute myeloid leukaemia with t(8;21)/AML1-ETO. Br J Haematol. 2006; 134(6):616-619. (Pubitemid 44253604)
32. Paschka P, Marcucci G, Ruppert AS, et al. Adverse prognostic significance of KIT mutations in adult acute myeloid leukemia with inv(16) and t(8;21): a Cancer and Leukemia Group B Study. J Clin Oncol. 2006;24(24):3904-3911. (Pubitemid 46630738)
33. Boissel N, Leroy H, Brethon B, et al. Incidence and prognostic impact of c-Kit, FLT3, and Ras gene mutations in core binding factor acute myeloid leukemia (CBF-AML). Leukemia. 2006; 20(6):965-970. (Pubitemid 43797286)
34. Roskoski R Jr. Structure and regulation of Kit protein- tyrosine kinase: the stem cell factor receptor. Biochem Biophys Res Commun. 2005;338(3): 1307-1315.
35. Lennartsson J, Jelacic T, Linnekin D, Shivakrupa R. Normal and oncogenic forms of the receptor tyrosine kinase kit. Stem Cells. 2005; 23(1):16-43. (Pubitemid 40105289)
36. Cairoli R, Beghini A, Grillo G, et al. Prognostic impact of c-KIT mutations in core binding factor leukemias: an Italian retrospective study. Blood. 2006;107(9):3463-3468.
37. Wang YY, Zhao LJ, Wu CF, et al. C-KIT mutation cooperates with full-length AML1-ETO to induce acute myeloid leukemia in mice. Proc Natl Acad Sci U S A. 2011;108(6):2450-2455.
38. Kohl TM, Schnittger S, Ellwart JW, Hiddemann W, Spiekermann K. KIT exon 8 mutations associated with core-binding factor (CBF)-acute myeloid leukemia (AML) cause hyperactivation of the receptor in response to stem cell factor. Blood. 2005; 105(8):3319-3321.
39. Kitayama H, Tsujimura T, Matsumura I, et al. Neoplastic transformation of normal hematopoietic cells by constitutively activating mutations of c-kit receptor tyrosine kinase. Blood. 1996;88(3):995-1004. (Pubitemid 26333324)
40. Xiang Z, Kreisel F, Cain J, Colson A, Tomasson MH. Neoplasia driven by mutant c-KIT is mediated by intracellular, not plasma membrane, receptor signaling. Mol Cell Biol. 2007;27(1):267-282. (Pubitemid 46013250)
41. Anderson MT, Tjioe IM, Lorincz MC, Parks DR, Herzenberg LA, Nolan GP. Simultaneous fluorescence- activated cell sorter analysis of two distinct transcriptional elements within a single cell using engineered green fluorescent proteins. Proc Natl Acad Sci U S A. 1996;93(16):8508-8511. (Pubitemid 26269589)
42. Cotta CV, Zhang Z, Kim HG, Klug CA. Pax5 determines B- versus T-cell fate and does not block early myeloid-lineage development. Blood. 2003; 101(11):4342-4346. (Pubitemid 36857798)
43. Kitayama H, Kanakura Y, Furitsu T, et al. Constitutively activating mutations of c-kit receptor tyrosine kinase confer factor-independent growth and tumorigenicity of factor-dependent hematopoietic cell lines. Blood. 1995;85(3):790-798.
44. Yuan Y, Zhou L, Miyamoto T, et al. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc Natl Acad Sci U S A. 2001;98(18):10398-10403. (Pubitemid 32803031)
45. Cammenga J, Horn S, Bergholz U, et al. Extracellular KIT receptor mutants, commonly found in core binding factor AML, are constitutively active and respond to imatinib mesylate. Blood. 2005; 106(12):3958-3961. (Pubitemid 41739038)
46. Yang Y, Letard S, Borge L, et al. Pediatric mastocytosis-associated KIT extracellular domain mutations exhibit different functional and signaling properties compared with KIT-phosphotransferase domain mutations. Blood. 2010;116(7): 1114-1123.
47. Luck SC, Russ AC, Du J, et al. KIT mutations confer a distinct gene expression signature in core binding factor leukaemia. Br J Haematol. 2010;148(6):925-937.
48. Bougherara H, Subra F, Crepin R, Tauc P, Auclair C, Poul MA. The aberrant localization of oncogenic kit tyrosine kinase receptor mutants is reversed on specific inhibitory treatment. Mol Cancer Res. 2009;7(9):1525-1533.
49. Moriyama Y, Tsujimura T, Hashimoto K, et al. Role of aspartic acid 814 in the function and expression of c-kit receptor tyrosine kinase. J Biol Chem. 1996;271(7):3347-3350. (Pubitemid 26065636)
50. Miyamoto T, Weissman IL, Akashi K. AML1/ETO-expressing nonleukemic stem cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc Natl Acad Sci U S A. 2000; 97(13):7521-7526. (Pubitemid 30431496)