NRASG12V oncogene facilitates self-renewal in a murine model of acute myelogenous leukemia

Blood

Volumn 124, Issue 22, 2014, Pages 3274-3283

  Sachs, Zohar ^a   LaRue, Rebecca S ^a,b   Nguyen, Hanh T ^a   Sachs, Karen ^c   Noble, Klara E ^a   Hassan, Nurul Azyan Mohd ^b   Diaz Flores, Ernesto ^d   Rathe, Susan K ^b   Sarver, Aaron L ^b   Bendall, Sean C ^c   Ha, Ngoc A ^b   Diers, Miechaleen D ^a,b   Nolan, Garry P ^c   Shannon, Kevin M ^d   Largaespada, David A ^a,b,e  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; NRAS G12V ONCOPROTEIN; ONCOPROTEIN; RAS PROTEIN; UNCLASSIFIED DRUG; GLYCINE; GUANOSINE TRIPHOSPHATASE; MEMBRANE PROTEIN; NRAS PROTEIN, HUMAN; TRANSCRIPTOME; VALINE;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER STEM CELL; CELL SUBPOPULATION; ENZYME ACTIVATION; GENE EXPRESSION; LEUKEMIA CELL; MOUSE; NONHUMAN; PROTEIN DEPLETION; SIGNAL TRANSDUCTION; TUMOR VOLUME; ACUTE MYELOBLASTIC LEUKEMIA; AMINO ACID SUBSTITUTION; ANIMAL; CELL PROLIFERATION; CELL TRANSFORMATION; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; ONCOGENE; PATHOLOGY; PHYSIOLOGY; SCID MOUSE; TUMOR CELL CULTURE;

AMINO ACID SUBSTITUTION; ANIMALS; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION, LEUKEMIC; GLYCINE; GTP PHOSPHOHYDROLASES; HUMANS; LEUKEMIA, MYELOID, ACUTE; MEMBRANE PROTEINS; MICE; MICE, SCID; ONCOGENES; TRANSCRIPTOME; TUMOR CELLS, CULTURED; VALINE;

EID: 84911498856     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-08-521708     Document Type: Article

References (44)

1. Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med. 2013;368(22):2059-2074.
2. Ward AF, Braun BS, Shannon KM. Targeting oncogenic Ras signaling in hematologic malignancies. Blood. 2012;120(17):3397-3406.
3. Ahearn IM, Haigis K, Bar-Sagi D, Philips MR. Regulating the regulator: post-translational modification of RAS. Nat Rev Mol Cell Biol. 2012;13(1):39-51.
4. Li Q, Haigis KM, McDaniel A, et al. Hematopoiesis and leukemogenesis in mice expressing oncogenic NrasG12D from the endogenous locus. Blood. 2011;117(6):2022-2032.
5. Wang J, Liu Y, Li Z, et al. Endogenous oncogenic Nras mutation initiates hematopoietic malignancies in a dose- and cell type-dependent manner. Blood. 2011;118(2):368-379.
6. Wang J, Kong G, Liu Y, et al. Nras(G12D/+) promotes leukemogenesis by aberrantly regulating hematopoietic stem cell functions. Blood. 2013;121(26):5203-5207.
7. Wiesner SM, Jones JM, Hasz DE, Largaespada DA. Repressible transgenic model of NRAS oncogene-driven mast cell disease in the mouse. Blood. 2005;106(3):1054-1062.
8. Wang J, Kong G, Liu Y, et al. NrasG12D/+ promotes leukemogenesis by aberrantly regulating hematopoietic stem cell functions. Blood. 2013;121(26):5203-5207.
9. Li Q, Bohin N, Wen T, et al. Oncogenic Nras has bimodal effects on stem cells that sustainably increase competitiveness. Nature. 2013;504(7478):143-147.
10. Kim WI, Matise I, Diers MD, Largaespada DA. RAS oncogene suppression induces apoptosis followed by more differentiated and less myelosuppressive disease upon relapse of acute myeloid leukemia. Blood. 2009;113(5):1086-1096.
11. Fung TK, Gandillet A, So CW. Selective treatment of mixed-lineage leukemia leukemic stem cells through targeting glycogen synthase kinase 3 and the canonical Wnt/β-catenin pathway. Curr Opin Hematol. 2012;19(4):280-286.
12. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev. 2003;17(18):2298-2307.
13. Cozzio A, Passegué E, Ayton PM, Karsunky H, Cleary ML, Weissman IL. Similar MLL-associated leukemias arising from self-renewing stem cells and short-lived myeloid progenitors. Genes Dev. 2003;17(24):3029-3035.
14. Krivtsov AV, Twomey D, Feng Z, et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature. 2006;442(7104):818-822.
15. Tamai H, Inokuchi K. 11q23/MLL acute leukemia: update of clinical aspects. J Clin Exp Hematop. 2010;50(2):91-98.
16. Zuber J, Rappaport AR, Luo W, et al. An integrated approach to dissecting oncogene addiction implicates a Myb-coordinated self-renewal program as essential for leukemia maintenance. Genes Dev. 2011;25(15):1628-1640.
17. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-1111.
18. Trapnell C, Williams BA, Pertea G, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-515.
19. Mootha VK, Lindgren CM, Eriksson KF, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34(3):267-273.
20. Subramanian A, Tamayo P, Mootha VK, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 2005;102(43):15545-15550.
21. Somervaille TC, Matheny CJ, Spencer GJ, et al. Hierarchical maintenance of MLL myeloid leukemia stem cells employs a transcriptional program shared with embryonic rather than adult stem cells. Cell Stem Cell. 2009;4(2):129-140.
22. Gentles AJ, Plevritis SK, Majeti R, Alizadeh AA. Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA. 2010;304(24):2706-2715.
23. Mullighan CG, Kennedy A, Zhou X, et al. Pediatric acute myeloid leukemia with NPM1 mutations is characterized by a gene expression profile with dysregulated HOX gene expression distinct from MLL-rearranged leukemias. Leukemia. 2007;21(9):2000-2009.
24. Ross ME, Mahfouz R, Onciu M, et al. Gene expression profiling of pediatric acute myelogenous leukemia. Blood. 2004;104(12):3679-3687.
25. Schaefer CF, Anthony K, Krupa S, et al. PID: the Pathway Interaction Database. Nucleic Acids Res. 2009;37(Database issue):D674-D679.
26. Somervaille TC, Cleary ML. Grist for the MLL: how do MLL oncogenic fusion proteins generate leukemia stem cells? Int J Hematol. 2010;91(5):735-741.
27. Heidel FH, Bullinger L, Feng Z, et al. Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell. 2012;10(4):412-424.
28. Zhang B, Li M, McDonald T, et al. Microenvironmental protection of CML stem and progenitor cells from tyrosine kinase inhibitors through N-cadherin and Wnt-β-catenin signaling. Blood. 2013;121(10):1824-1838.
29. Wang Y, Krivtsov AV, Sinha AU, et al. The Wnt/beta-catenin pathway is required for the development of leukemia stem cells in AML. Science. 2010;327(5973):1650-1653.
30. Yeung J, Esposito MT, Gandillet A, et al. β-Catenin mediates the establishment and drug resistance of MLL leukemic stem cells. Cancer Cell. 2010;18(6):606-618.
31. Chao MP, Seita J, Weissman IL. Establishment of a normal hematopoietic and leukemia stem cell hierarchy. Cold Spring Harb Symp Quant Biol. 2008;73:439-449.
32. Bendall SC, Simonds EF, Qiu P, et al. Single-cell mass cytometry of differential immune and drug responses across a human hematopoietic continuum. Science. 2011;332(6030):687-696.
33. Qiu P, Simonds EF, Bendall SC, et al. Extracting a cellular hierarchy from high-dimensional cytometry data with SPADE. Nat Biotechnol. 2011;29(10):886-891.
34. Tamburini J, Chapuis N, Bardet V, et al. Mammalian target of rapamycin (mTOR) inhibition activates phosphatidylinositol 3-kinase/Akt by up-regulating insulin-like growth factor-1 receptor signaling in acute myeloid leukemia: rationale for therapeutic inhibition of both pathways. Blood. 2008;111(1):379-382.
35. Hu Y, Chen Y, Douglas L, Li S. beta-Catenin is essential for survival of leukemic stem cells insensitive to kinase inhibition in mice with BCR-ABL-induced chronic myeloid leukemia. Leukemia. 2009;23(1):109-116.
36. Zhao C, Blum J, Chen A, et al. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell. 2007;12(6):528-541.
37. Braun BS, Shannon K. Targeting Ras in myeloid leukemias. Clin Cancer Res. 2008;14(8):2249-2252.
38. Pattabiraman DR, Gonda TJ. Role and potential for therapeutic targeting of MYB in leukemia. Leukemia. 2013;27(2):269-277.
39. Braun T, Itzykson R, Renneville A, et al; Groupe Francophone des Myélodysplasies. Molecular predictors of response to decitabine in advanced chronic myelomonocytic leukemia: a phase 2 trial. Blood. 2011;118(14):3824-3831.
40. Park S, Chapuis N, Saint Marcoux F, et al; GOELAMS (Groupe Ouest Est d'Etude des Leucémies aiguës et Autres Maladies du Sang). A phase Ib GOELAMS study of the mTOR inhibitor RAD001 in association with chemotherapy for AML patients in first relapse. Leukemia. 2013;27(7):1479-1486.
41. Radtke I, Mullighan CG, Ishii M, et al. Genomic analysis reveals few genetic alterations in pediatric acute myeloid leukemia. Proc Natl Acad Sci USA. 2009;106(31):12944-12949.
42. Kotecha N, Flores NJ, Irish JM, et al. Single-cell profiling identifies aberrant STAT5 activation in myeloid malignancies with specific clinical and biologic correlates. Cancer Cell. 2008;14(4):335-343.
43. Zhang J, Ding L, Holmfeldt L, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012;481(7380):157-163.
44. Ying H, Kimmelman AC, Lyssiotis CA, et al. Oncogenic Kras maintains pancreatic tumors through regulation of anabolic glucose metabolism. Cell. 2012;149(3):656-670.