IDH2 and NPM1 mutations cooperate to activate Hoxa9/Meis1 and Hypoxia pathways in acute myeloid Leukemia

Cancer Research

Volumn 75, Issue 10, 2015, Pages 2005-2016

  Ogawara, Yoko ^a   Katsumoto, Takuo ^a   Aikawa, Yukiko ^a   Shima, Yutaka ^a   Kagiyama, Yuki ^a   Soga, Tomoyoshi ^b   Matsunaga, Hironori ^c   Seki, Takahiko ^c   Araki, Kazushi ^c   Kitabayashi, Issay ^a  

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b KEIO UNIVERSITY   (Japan)

^c DAIICHI SANKYO CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ISOCITRATE DEHYDROGENASE 2; MEMBRANE PROTEIN; NUCLEOPHOSMIN; PROTEIN MEIS1; TAMOXIFEN; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 2, MOUSE; MYELOID ECOTROPIC VIRAL INTEGRATION SITE 1 PROTEIN; NUCLEAR PROTEIN; TUMOR PROTEIN;

ACUTE MYELOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CARCINOGENESIS; CELL SURVIVAL; CONTROLLED STUDY; DNMT3A GENE; EBF1 GENE; ENZYME MODIFICATION; FLT3 GENE; GENE; GENE DELETION; GENE EXPRESSION; GENE MUTATION; GENETIC VARIABILITY; GENOTYPE; HUMAN; IDH2 GENE; ITD GENE; MICROARRAY ANALYSIS; MOLECULARLY TARGETED THERAPY; NONHUMAN; NPM1 GENE; NPMC GENE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; R140Q GENE; R882H GENE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPIB GENE; UPREGULATION; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CELL HYPOXIA; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MISSENSE MUTATION;

ANIMALS; CELL HYPOXIA; GENE EXPRESSION REGULATION, LEUKEMIC; HOMEODOMAIN PROTEINS; HUMANS; ISOCITRATE DEHYDROGENASE; LEUKEMIA, MYELOID, ACUTE; MICE, INBRED C57BL; MUTATION, MISSENSE; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NUCLEAR PROTEINS; UP-REGULATION;

EID: 84937965926     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-2200     Document Type: Article

References (43)

1. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008;321:1807-12.
2. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, Chen K, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med 2009;361:1058-66.
3. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med 2009;360:765-73.
4. Amary MF, Bacsi K, Maggiani F, Damato S, Halai D, Berisha F, et al. IDH1 and IDH2 mutations are frequent events in central chondrosarcoma and centralandperiostealchondromas but notinother mesenchymal tumours. J Pathol 2011;224:334-43.
5. Shibata T, Kokubu A, Miyamoto M, Sasajima Y, Yamazaki N. Mutant IDH1 confers aninvivo growthinamelanoma cell line with BRAF mutation. Am J Pathol 2011;178:1395-402.
6. Borger DR, Tanabe KK, Fan KC, Lopez HU, Fantin VR, Straley KS, et al. Frequent mutation of isocitrate dehydrogenase (IDH)1 and IDH2 in cholangiocarcinoma identified through broad-based tumor genotyping. Oncologist 2012;17:72-9.
7. Cairns RA, Iqbal J, Lemonnier F, Kucuk C, de Leval L, Jais JP, et al. IDH2 mutations are frequent in angioimmunoblastic T-cell lymphoma. Blood 2012;119:1901-3.
8. Ward PS, Patel J, Wise DR, Abdel-Wahab O, Bennett BD, Coller HA, et al. The common feature of leukemia-associated IDH1 and IDH2 mutations is a neomorphic enzyme activity converting alpha-ketoglutarate to 2-hydroxyglutarate. Cancer cell 2010;17:225-34.
9. Figueroa ME, Abdel-Wahab O, Lu C, Ward PS, Patel J, Shih A, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer cell 2010;18:553-67.
10. Chowdhury R, Yeoh KK, Tian YM, Hillringhaus L, Bagg EA, Rose NR, et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep 2011;12:463-9.
11. Xu W, Yang H, Liu Y, Yang Y, Wang P, Kim SH, et al. Oncometabolite 2-hydroxyglutarate is a competitive inhibitor of alpha-ketoglutarate-dependent dioxygenases. Cancer cell 2011;19:17-30.
12. Koivunen P, Lee S, Duncan CG, Lopez G, Lu G, Ramkissoon S, et al. Transformation by the (R)-enantiomer of 2-hydroxyglutarate linked to EGLN activation. Nature 2012;483:484-8.
13. Lu C, Ward PS, Kapoor GS, Rohle D, Turcan S, Abdel-Wahab O, et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 2012;483:474-8.
14. Sasaki M, Knobbe CB, Itsumi M, Elia AJ, Harris IS, Chio II, et al. D-2-hydroxyglutarate produced bymutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev 2012;26:2038-49.
15. Losman JA, Looper RE, Koivunen P, Lee S, Schneider RK, McMahon C, et al. (R)-2-hydroxyglutarate is sufficient to promote leukemogenesis and its effects are reversible. Science 2013;339:1621-5.
16. Wang F, Travins J, DeLaBarre B, Penard-Lacronique V, Schalm S, Hansen E, et al. Targeted inhibition of mutant IDH2 in leukemia cells induces cellular differentiation. Science 2013;340:622-6.
17. Rohle D, Popovici-Muller J, Palaskas N, Turcan S, Grommes C, Campos C, et al. An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 2013;340:626-30.
18. Chaturvedi A, Araujo Cruz MM, Jyotsana N, Sharma A, Yun H, Gorlich K, et al. Mutant IDH1 promotes leukemogenesisinvivo and canbespecifically targeted in human AML. Blood 2013;122:2877-87.
19. Chen C, Liu Y, Lu C, Cross JR, Morris JPt, Shroff AS, et al. Cancer-associated IDH2 mutants drive an acute myeloid leukemia that is susceptible to Brd4 inhibition. Genes Dev 2013;27:1974-85.
20. Lu C, Venneti S, Akalin A, Fang F, Ward PS, Dematteo RG, et al. Induction of sarcomas by mutant IDH2. Genes Dev 2013;27:1986-98.
21. Kats LM, Reschke M, Taulli R, Pozdnyakova O, Burgess K, Bhargava P, et al. Proto-oncogenic role of mutant IDH2 in leukemia initiation and maintenance. Cell stem cell 2014;14:329-41.
22. Shih AH, Abdel-Wahab O, Patel JP, Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer 2012; 12:599-612.
23. Sasaki M, Knobbe CB, Munger JC, Lind EF, Brenner D, Brustle A, et al. IDH1 (R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature 2012;488:656-9.
24. Morita S, Kojima T, Kitamura T. Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 2000;7:1063-6.
25. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 2005;102:15545-50.
26. Falini B, Mecucci C, Tiacci E, Alcalay M, Rosati R, Pasqualucci L, et al. Cytoplasmic nucleophosmin in acute myelogenous leukemia with a normal karyotype. N Engl J Med 2005;352:254-66.
27. Schnabel CA, Jacobs Y, Cleary ML. HoxA9-mediated immortalization of myeloid progenitors requires functional interactions with TALE cofactors Pbx and Meis. Oncogene 2000;19:608-16.
28. Falini B, Bolli N, Shan J, Martelli MP, Liso A, Pucciarini A, et al. Both carboxy-terminus NES motif and mutated tryptophan(s) are crucial for aberrant nuclear export of nucleophosmin leukemic mutants in NPMc+ AML. Blood 2006;107:4514-23.
29. Somervaille TC, Cleary ML. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer cell 2006;10:257-68.
30. Aikawa Y, Katsumoto T, Zhang P, Shima H, Shino M, Terui K, et al. PU.1-mediated upregulation of CSF1R is crucial for leukemia stem cell potential induced by MOZ-TIF2. Nat Med 2010;16:580-5.
31. Krivtsov AV, Twomey D, Feng Z, Stubbs MC, Wang Y, Faber J, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 2006;442:818-22.
32. Elvidge GP, Glenny L, Appelhoff RJ, Ratcliffe PJ, Ragoussis J, Gleadle JM. Concordant regulation of gene expression by hypoxia and 2-oxoglutarate-dependent dioxygenase inhibition: the role of HIF-1alpha, HIF-2alpha, and other pathways. J Biol Chem 2006;281:15215-26.
33. Brown AL, Wilkinson CR, Waterman SR, Kok CH, Salerno DG, Diakiw SM, et al. Genetic regulators of myelopoiesis and leukemic signaling identified by gene profiling and linear modeling. J Leukoc Biol 2006; 80:433-47.
34. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA, Lemischka IR. A stem cell molecular signature. Science 2002;298:601-4.
35. Jaatinen T, Hemmoranta H, Hautaniemi S, Niemi J, Nicorici D, Laine J, et al. Global gene expression profile of human cord blood-derived CD133+ cells. Stem Cells 2006;24:631-41.
36. Lara-Astiaso D, Weiner A, Lorenzo-Vivas E, Zaretsky I, Jaitin DA, David E, et al Immunogenetics. Chromatinstate dynamicsduring blood formation. Science 2014;345:943-9.
37. Shlush LI, Zandi S, Mitchell A, Chen WC, Brandwein JM, Gupta V, et al. Identification of pre-leukaemic haematopoietic stem cells in acute leukaemia. Nature 2014;506:328-33.
38. Corces-Zimmerman MR, Hong WJ, Weissman IL, Medeiros BC, Majeti R. Preleukemic mutationsinhuman acute myeloid leukemia affect epigenetic regulators and persist in remission. Proc Natl Acad Sci U S A 2014;111: 2548-53.
39. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med 2013;368:2059-74.
40. Li L, Piloto O, Kim KT, Ye Z, Nguyen HB, Yu X, et al. FLT3/ITD expression increases expansion, survival and entry into cell cycle of human haematopoietic stem/progenitor cells. Br J Haematol 2007;137:64-75.
41. Tsagaratou A, Aijo T, Lio CW, Yue X, Huang Y, Jacobsen SE, et al. Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc Natl Acad Sci U S A 2014;111:E3306-15.
42. Chu SH, Heiser D, Li L, Kaplan I, Collector M, Huso D, et al. FLT3-ITD knockin impairs hematopoietic stem cell quiescence/homeostasis, leading to myeloproliferative neoplasm. Cell stem Cell 2012;11:346-58.
43. Lee BH, Tothova Z, Levine RL, Anderson K, Buza-Vidas N, Cullen DE, et al. FLT3 mutations confer enhanced proliferation and survival properties to multipotent progenitors in a murine model of chronic myelomonocytic leukemia. Cancer Cell 2007;12:367-80.