Ras pathway mutations are prevalent in relapsed childhood acute lymphoblastic leukemia and confer sensitivity to MEK inhibition

Blood

Volumn 124, Issue 23, 2014, Pages 3420-3430

  Irving, Julie ^a   Matheson, Elizabeth ^a   Minto, Lynne ^a   Blair, Helen ^a   Case, Marian ^a   Halsey, Christina ^b   Swidenbank, Isabella ^a   Ponthan, Frida ^a   Kirschner Schwabe, Renate ^c   Groeneveld Krentz, Stefanie ^c   Hof, Jana ^c   Allan, James ^a   Harrison, Christine ^a   Vormoor, Josef ^a   Von Stackelberg, Arend ^c   Eckert, Cornelia ^c  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CBL PROTEIN; CD135 ANTIGEN; K RAS PROTEIN; NRAS PROTEIN; PROTEIN TYROSINE PHOSPHATASE SHP 2; RAS PROTEIN; SELUMETINIB; TRANSCRIPTION FACTOR ETV6; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; BENZIMIDAZOLE DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; PROTEIN KINASE INHIBITOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER SCREENING; CELL VIABILITY; CHILD; CHILDHOOD LEUKEMIA; CONTROLLED STUDY; DENATURING HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; DRUG MECHANISM; DRUG SCREENING; ENZYME INHIBITION; EVENT FREE SURVIVAL; EXON; FEMALE; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LEUKEMIA CELL; LEUKEMIA RELAPSE; MAJOR CLINICAL STUDY; MALE; MOUSE; MULTIPLE CYCLE TREATMENT; NONHUMAN; OVERALL SURVIVAL; PREVALENCE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SOMATIC MUTATION; TREATMENT OUTCOME; TUMOR VOLUME; ANIMAL; ANTAGONISTS AND INHIBITORS; CLINICAL TRIAL (TOPIC); DRUG RESISTANCE; GENE FREQUENCY; GENETICS; MUTATION; NONOBESE DIABETIC MOUSE; ONCOGENE RAS; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; RECURRENT DISEASE; SCID MOUSE; TRANSGENIC MOUSE; TUMOR CELL LINE;

ANIMALS; BENZIMIDAZOLES; CELL LINE, TUMOR; CHILD; CLINICAL TRIALS AS TOPIC; DRUG RESISTANCE, NEOPLASM; GENE FREQUENCY; GENES, RAS; HUMANS; MAP KINASE KINASE KINASES; MICE; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; MUTATION; PRECURSOR CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN KINASE INHIBITORS; RECURRENCE; SIGNAL TRANSDUCTION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84914106704     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-04-531871     Document Type: Article

References (34)

1. Pui CH, Carroll WL, Meshinchi S, Arceci RJ. Biology, risk stratification, and therapy of pediatric acute leukemias: an update. J Clin Oncol. 2011; 29(5):551-565.
2. Malempati S, Gaynon PS, Sather H, La MK, Stork LC; Children's Oncology Group. Outcome after relapse among children with standard-risk acute lymphoblastic leukemia: Children's Oncology Group study CCG-1952. J Clin Oncol. 2007;25(36):5800-5807.
3. Einsiedel HG, von Stackelberg A, Hartmann R, et al. Long-term outcome in children with relapsed ALL by risk-stratified salvage therapy: results of trial acute lymphoblastic leukemia-relapse study of the Berlin-Frankfurt-Münster Group 87. J Clin Oncol. 2005;23(31):7942-7950.
4. Parker C, Waters R, Leighton C, et al. Effect of mitoxantrone on outcome of children with first relapse of acute lymphoblastic leukaemia (ALL R3): an open-label randomised trial. Lancet. 2010;376(9757):2009-2017.
5. Harrison CJ. Cytogenetics of paediatric and adolescent acute lymphoblastic leukaemia. Br J Haematol. 2009;144(2):147-156.
6. Mullighan CG, Goorha S, Radtke I, et al. Genomewide analysis of genetic alterations in acute lymphoblastic leukaemia. Nature. 2007; 446(7137):758-764.
7. Case M, Matheson E, Minto L, et al. Mutation of genes affecting the RAS pathway is common in childhood acute lymphoblastic leukemia. Cancer Res. 2008;68(16):6803-6809.
8. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer. 2011;11(11):761-774.
9. Nicholson L, Knight T, Matheson E, et al. Casitas B lymphoma mutations in childhood acute lymphoblastic leukemia. Genes Chromosomes Cancer. 2012;51(3):250-256.
10. Paulsson K, Horvat A, Str ömbeck B, et al. Mutations of FLT3, NRAS, KRAS, and PTPN11 are frequent and possibly mutually exclusive in high hyperdiploid childhood acute lymphoblastic leukemia. Genes Chromosomes Cancer. 2008; 47(1):26-33.
11. Wiemels JL, Zhang Y, Chang J, et al. RAS mutation is associated with hyperdiploidy and parental characteristics in pediatric acute lymphoblastic leukemia. Leukemia. 2005;19(3): 415-419.
12. Zhang J, Mullighan CG, Harvey RC, et al. Key pathways are frequently mutated in high-risk childhood acute lymphoblastic leukemia: a report from the Children's Oncology Group. Blood. 2011; 118(11):3080-3087.
13. Wiemels JL, Kang M, Chang JS, et al. Backtracking RAS mutations in high hyperdiploid childhood acute lymphoblastic leukemia. Blood Cells Mol Dis. 2010;45(3):186-191.
14. Holmfeldt L, Wei L, Diaz-Flores E, et al. The genomic landscape of hypodiploid acute lymphoblastic leukemia. Nat Genet. 2013;45(3): 242-252.
15. Perentesis JP, Bhatia S, Boyle E, et al. RAS oncogene mutations and outcome of therapy for childhood acute lymphoblastic leukemia. Leukemia. 2004;18(4):685-692.
16. Davidsson J, Paulsson K, Lindgren D, et al. Relapsed childhood high hyperdiploid acute lymphoblastic leukemia: presence of preleukemic ancestral clones and the secondary nature of microdeletions and RTK-RAS mutations. Leukemia. 2010;24(5):924-931.
17. Harrison CJ, Haas O, Harbott J, et al; Biology and Diagnosis Committee of International Berlin-Frankfüurt-Müunster study group. Detection of prognostically relevant genetic abnormalities in childhood B-cell precursor acute lymphoblastic leukaemia: recommendations from the Biology and Diagnosis Committee of the International Berlin-Frankfüurt-Müunster study group. Br J Haematol. 2010;151(2):132-142.
18. Brüggemann M, Schrauder A, Raff T, et al; European Working Group for Adult Acute Lymphoblastic Leukemia (EWALL); International Berlin-Frankfurt-Münster Study Group (I-BFM-SG). Standardized MRD quantification in European ALL trials: proceedings of the Second International Symposium on MRD assessment in Kiel, Germany, 18-20 September 2008. Leukemia. 2010;24(3):521-535.
19. Archambeault S, Flores NJ, Yoshimi A, et al. Development of an allele-specific minimal residual disease assay for patients with juvenile myelomonocytic leukemia. Blood. 2008;111(3): 1124-1127.
20. Wellcome Trust Sanger Institute, Genome Research Limited. COSMIC: catalogue of somatic mutations in cancer. http://www.sanger.ac.uk/genetics/CGP/cosmic/. Accessed June 1, 2013.
21. Balgobind BV, Van Vlierberghe P, van den Ouweland AM, et al. Leukemia-associated NF1 inactivation in patients with pediatric T-ALL and AML lacking evidence for neurofibromatosis. Blood. 2008;111(8):4322-4328.
22. Ng MH, Ng RK, Kong CT, Jin DY, Chan LC. Activation of Ras-dependent Elk-1 activity by MLL-AF4 family fusion oncoproteins. Exp Hematol. 2010;38(6):481-488.
23. Garza AS, Miller AL, Johnson BH, Thompson EB. Converting cell lines representing hematological malignancies from glucocorticoid-resistant to glucocorticoid-sensitive: signaling pathway interactions. Leuk Res. 2009;33(5):717-727.
24. McCubrey JA, Steelman LS, Chappell WH, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta. 2007;1773(8): 1263-1284.
25. Braoudaki M, Karpusas M, Katsibardi K, Papathanassiou C, Karamolegou K, Tzortzatou- Stathopoulou F. Frequency of FLT3 mutations in childhood acute lymphoblastic leukemia. Med Oncol. 2009;26(4):460-462.
26. Driessen EM, van Roon EH, Spijkers-Hagelstein JA, et al. Frequencies and prognostic impact of RAS mutations in MLL-rearranged acute lymphoblastic leukemia in infants. Haematologica. 2013;98(6):937-944.
27. Mullighan CG, Phillips LA, Su X, et al. Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science. 2008; 322(5906):1377-1380.
28. Mullighan CG, Zhang J, Kasper LH, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature. 2011;471(7337): 235-239.
29. Molteni CG, Te Kronnie G, Bicciato S, et al. PTPN11 mutations in childhood acute lymphoblastic leukemia occur as a secondary event associated with high hyperdiploidy. Leukemia. 2010;24(1):232-235.
30. Xiao J, Lee ST, Xiao Y, et al. PTPRG inhibition by DNA methylation and cooperation with RAS gene activation in childhood acute lymphoblastic leukemia. Int J Cancer. 2014; 135(5):1101-1109.
31. Ward AF, Braun BS, Shannon KM. Targeting oncogenic Ras signaling in hematologic malignancies. Blood. 2012;120(17): 3397-3406.
32. Hof J, Krentz S, van Schewick C, et al. Mutations and deletions of the TP53 gene predict nonresponse to treatment and poor outcome in first relapse of childhood acute lymphoblastic leukemia. J Clin Oncol. 2011; 29(23):3185-3193.
33. Bennouna J, Lang I, Valladares-Ayerbes M, et al. A Phase II, open-label, randomised study to assess the efficacy and safety of the MEK1/2 inhibitor AZD6244 (ARRY-142886) versus capecitabine monotherapy in patients with colorectal cancer who have failed one or two prior chemotherapeutic regimens. Invest New Drugs. 2011;29(5):1021-1028.
34. Davies BR, Logie A, McKay JS, et al. AZD6244 (ARRY-142886), a potent inhibitor of mitogen-activated protein kinase/extracellular signal-regulated kinase kinase 1/2 kinases: mechanism of action in vivo, pharmacokinetic/pharmacodynamic relationship, and potential for combination in preclinical models. Mol Cancer Ther. 2007;6(8):2209-2219.