The transcriptomic landscape and directed chemical interrogation of MLL-rearranged acute myeloid leukemias

Nature Genetics

Volumn 47, Issue 9, 2015, Pages 1030-1037

  Lavallée, Vincent Philippe ^a,b   Baccelli, Irène ^a   Krosl, Jana ^a   Wilhelm, Brian ^a,c   Barabé, Frédéric ^a,d,e   Gendron, Patrick ^a   Boucher, Geneviève ^a   Lemieux, Sébastien ^a,c   Marinier, Anne ^a,c   Meloche, Sylvain ^a,c   Hébert, Josée ^a,b,c   Sauvageau, Guy ^a,b,c  

^a INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^b MAISONNEUVE ROSEMONT HOSPITAL   (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

^d LAVAL UNIVERSITY   (Canada)

^e UNIVERSITÉ LAVAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MIXED LINEAGE LEUKEMIA PROTEIN; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; TRANSCRIPTOME; ANTINEOPLASTIC AGENT; HISTONE LYSINE METHYLTRANSFERASE; MLL PROTEIN, HUMAN; ONCOPROTEIN; RAS PROTEIN;

ACUTE MYELOBLASTIC LEUKEMIA; ADULT; AGED; ARTICLE; CONTROLLED STUDY; EXOME; FEMALE; FUSION GENE; GENE DUPLICATION; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; HUMAN; MAJOR CLINICAL STUDY; MALE; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; PROTEIN INTERACTION; TRANSCRIPTOMICS; UPREGULATION; ANIMAL; CANCER TRANSPLANTATION; CASE CONTROL STUDY; DRUG RESISTANCE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE TRANSLOCATION; GENETICS; METABOLISM; MUTATION; NONOBESE DIABETIC MOUSE; SCID MOUSE;

ANIMALS; ANTINEOPLASTIC AGENTS; CASE-CONTROL STUDIES; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, LEUKEMIC; GENE REGULATORY NETWORKS; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE, INBRED NOD; MICE, SCID; MUTATION; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NEOPLASM TRANSPLANTATION; ONCOGENE PROTEINS, FUSION; RAS PROTEINS; TRANSCRIPTOME; TRANSLOCATION, GENETIC;

EID: 84940584908     PISSN: 10614036     EISSN: 15461718     Source Type: Journal    
DOI: 10.1038/ng.3371     Document Type: Article

References (43)

1. Krivtsov, A.V. & Armstrong, S.A. MLL translocations, histone modifcations and leukaemia stem-cell development. Nat. Rev. Cancer 7, 823-833 (2007).
2. Meyer, C. et al. The MLL recombinome of acute leukemias in 2013. Leukemia 27, 2165-2176 (2013).
3. Armstrong, S.A. et al. MLL translocations specify a distinct gene expression profle that distinguishes a unique leukemia. Nat. Genet. 30, 41-47 (2002).
4. Valk, P.J. et al. Prognostically useful gene-expression profles in acute myeloid leukemia. N. Engl. J. Med. 350, 1617-1628 (2004).
5. Mullighan, C.G. et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profle with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia 21, 2000-2009 (2007).
6. Ross, M.E. et al. Gene expression profling of pediatric acute myelogenous leukemia. Blood 104, 3679-3687 (2004).
7. Grossmann, V. et al. High incidence of RAS signalling pathway mutations in MLL-rearranged acute myeloid leukemia. Leukemia 27, 1933-1936 (2013).
8. Gröschel, S. et al. Deregulated expression of EVI1 defnes a poor prognostic subset of MLL-rearranged acute myeloid leukemias: a study of the German-Austrian Acute Myeloid Leukemia Study Group and the Dutch-Belgian-Swiss HOVON/SAKK Cooperative Group. J. Clin. Oncol. 31, 95-103 (2012).
9. The Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N. Engl. J. Med. 368, 2059-2074 (2013).
10. Sandhöfer, N. et al. Dual PI3K/mTOR inhibition shows antileukemic activity in MLL-rearranged acute myeloid leukemia. Leukemia 29, 828-838 (2015).
11. Kampen, K.R. et al. Insights in dynamic kinome reprogramming as a consequence of MEK inhibition in MLL-rearranged AML. Leukemia 28, 589-599 (2014).
12. Steudel, C. et al. Comparative analysis of MLL partial tandem duplication and FLT3 internal tandem duplication mutations in 956 adult patients with acute myeloid leukemia. Genes Chromosom. Cancer 37, 237-251 (2003).
13. Basecke, J., Whelan, J.T., Griesinger, F. & Bertrand, F.E. The MLL partial tandem duplication in acute myeloid leukaemia. Br. J. Haematol. 135, 438-449 (2006).
14. Grossmann, V. et al. A novel hierarchical prognostic model of AML solely based on molecular mutations. Blood 120, 2963-2972 (2012).
15. Daigle, S.R. et al. Selective killing of mixed lineage leukemia cells by a potent small-molecule DOT1L inhibitor. Cancer Cell 20, 53-65 (2011).
16. Kühn, M. et al. MLL partial tandem duplication leukemia cells are sensitive to small molecule DOT1L inhibition. Haematologica 100, e190-e193 (2015).
17. Kwiatkowski, A., Gertler, F. & Loureiro, J. Function and regulation of Ena/VASP proteins. Trends Cell Biol. 13, 386-392 (2003).
18. Zhou, J. et al. PU.1 is essential for MLL leukemia partially via crosstalk with the MEIS/HOX pathway. Leukemia 28, 1436-1448 (2014).
19. Zhang, D.E., Hetherington, C.J., Chen, H.M. & Tenen, D.G. The macrophage transcription factor PU.1 directs tissue-specifc expression of the macrophage colony-stimulating factor receptor. Mol. Cell. Biol. 14, 373-381 (1994).
20. Iwama, A. et al. Use of RDA analysis of knockout mice to identify myeloid genes regulated in vivo by PU.1 and C/EBPalpha. Nucleic Acids Res. 26, 3034-3043 (1998).
21. Pabst, C. et al. Identifcation of small molecules that support human leukemia stem cell activity ex vivo. Nat. Methods 11, 436-442 (2014).
22. Kodandapani, R. et al. A new pattern for helix-turn-helix recognition revealed by the PU.1 ETS-domain-DNA complex. Nature 380, 456-460 (1996).
23. Cook, W. et al. PU.1 is a suppressor of myeloid leukemia, inactivated in mice by gene deletion and mutation of its DNA binding domain. Blood 104, 3437-3444 (2004).
24. Mueller, B.U. et al. Heterozygous PU.1 mutations are associated with acute myeloid leukemia. Blood 100, 998-1007 (2002).
25. Vegesna, V. et al. C/EBP-beta, C/EBP-delta, PU.1, AML1 genes: mutational analysis in 381 samples of hematopoietic and solid malignancies. Leuk. Res. 26, 451-457 (2002).
26. Lamandin, C. et al. Are PU.1 mutations frequent genetic events in acute myeloid leukemia (AML)? Blood 100, 4680-4681 (2002).
27. Döhner, K. et al. Mutation analysis of the transcription factor PU.1 in younger adults (16 to 60 years) with acute myeloid leukemia: a study of the AML Study Group Ulm (AMLSG ULM). Blood 102, 3850 (2003).
28. Ley, T. et al. A pilot study of high-throughput, sequence-based mutational profling of primary human acute myeloid leukemia cell genomes. Proc. Natl. Acad. Sci. USA 100, 14275-14280 (2003).
29. Burgess, M.R. et al. Preclinical effcacy of MEK inhibition in Nras-mutant AML. Blood 124, 3947-3955 (2014).
30. Irving, J. et al. Ras pathway mutations are prevalent in relapsed childhood acute lymphoblastic leukemia and confer sensitivity to MEK inhibition. Blood 124, 3420-3430 (2014).
31. Jain, N. et al. Phase II study of the oral MEK inhibitor selumetinib in advanced acute myelogenous leukemia: a University of Chicago phase II consortium trial. Clin. Cancer Res. 20, 490-498 (2013).
32. Borthakur, G. et al. Phase I/II trial of the MEK1/2 inhibitor trametinib (GSK1120212) in relapsed/refractory myeloid malignancies: evidence of activity in patients with RAS mutation-positive disease. Blood (ASH Annual Meeting Abstracts) 120, Abstract 677 (2012).
33. Diaz, L.A. Jr. et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 486, 537-540 (2012).
34. Prahallad, A. et al. Unresponsiveness of colon cancer to BRAF(V600E) inhibition through feedback activation of EGFR. Nature 483, 100-103 (2012).
35. Misale, S. et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 486, 532-536 (2012).
36. Andersson, A.K. et al. The landscape of somatic mutations in infant MLL-rearranged acute lymphoblastic leukemias. Nat. Genet. 47, 330-337 (2015).
37. Lavallée, V.-P. et al. EVI1-rearranged acute myeloid leukemias are characterized by distinct molecular alterations. Blood 125, 140-143 (2015).
38. Fares, I. et al. Pyrimidoindole derivatives are agonists of human hematopoietic stem cell self-renewal. Science 345, 1509-1512 (2014).
39. Barabé, F. , Kennedy, J.A., Hope, K.J. & Dick, J.E. Modeling the initiation and progression of human acute leukemia in mice. Science 316, 600-604 (2007).
40. Gabert, J. et al. Standardization and quality control studies of 'real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia - A Europe Against Cancer Program. Leukemia 17, 2318-2357 (2003).
41. Beillard, E. et al. Evaluation of candidate control genes for diagnosis and residual disease detection in leukemic patients using 'real-time' quantitative reverse-transcriptase polymerase chain reaction (RQ-PCR) - a Europe against cancer program. Leukemia 17, 2474-2486 (2003).
42. Kern, D.H., Morgan, C.R. & Hildebrand-Zanki, S.U. In vitro pharmacodynamics of 1-beta-D-arabinofuranosylcytosine: synergy of antitumor activity with cis-diammine dichloroplatinum(II). Cancer Res. 48, 117-121 (1988).
43. Rodenak Kladniew, B. et al. Synergistic antiproliferative and anticholesterogenic effects of linalool, 1,8-cineole, and simvastatin on human cell lines. Chem. Biol. Interact. 214, 57-68 (2014).