The importance of relative mutant level for evaluating impact on outcome of KIT, FLT3 and CBL mutations in core-binding factor acute myeloid leukemia

Leukemia

Volumn 27, Issue 9, 2013, Pages 1891-1901

  Allen, C ^a   Hills, R K ^b   Lamb, K ^a   Evans, C ^a   Tinsley, S ^a   Sellar, R ^a   O'Brien, M ^c   Yin, J L ^b   Burnett, A K ^a   Linch, D C ^a   Gale, R E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^c MANCHESTER ROYAL INFIRMARY   (United Kingdom)

Author keywords

acute myeloid leukemia; CBL; core binding factor; FLT3; KIT; RAS

Indexed keywords

CBL PROTEIN; CD135 ANTIGEN; CORE BINDING FACTOR; STEM CELL FACTOR RECEPTOR;

ACUTE GRANULOCYTIC LEUKEMIA; ARTICLE; GENE LOCUS; GENE MUTATION; GENOTYPE; HUMAN; LEUKEMIA RELAPSE; MINIMAL RESIDUAL DISEASE; MUTANT; OVERALL SURVIVAL; PRIORITY JOURNAL;

ADOLESCENT; ADULT; AGED; CHROMOSOME ABERRATIONS; COHORT STUDIES; CORE BINDING FACTORS; EXONS; FEMALE; FMS-LIKE TYROSINE KINASE 3; GENOTYPE; HUMANS; LEUKEMIA, MYELOID, ACUTE; MALE; MIDDLE AGED; MUTATION; PROGNOSIS; PROTO-ONCOGENE PROTEINS C-CBL; PROTO-ONCOGENE PROTEINS C-KIT; RECURRENCE; REMISSION INDUCTION; TREATMENT OUTCOME; YOUNG ADULT;

EID: 84883742457     PISSN: 08876924     EISSN: 14765551     Source Type: Journal    
DOI: 10.1038/leu.2013.186     Document Type: Article

References (58)

1. Marcucci G, Haferlach T, Dohner H. Molecular genetics of adult acute myeloid leukemia: prognostic and therapeutic implications. J Clin Oncol 2011; 29: 475-486.
2. Patel JP, Levine RL. How do novel molecular genetic markers influence treatment decisions in acute myeloid leukemia? Hematology Am Soc Hematol Educ Program 2012; 2012: 28-34.
3. Grimwade D, Hills RK, Moorman AV, Walker H, Chatters S, Goldstone AH et al. Refinement of cytogenetic classification in acute myeloid leukemia: determination of prognostic significance of rare recurring chromosomal abnormalities among 5876 younger adult patients treated in the United Kingdom Medical Research Council trials. Blood 2010; 116: 354-365.
4. Burnett AK, Hills RK, Milligan D, Kjeldsen L, Kell J, Russell NH et al. Identification of patients with acute myeloblastic leukemia who benefit from the addition of gemtuzumab ozogamicin: results of the MRC AML15 trial. J Clin Oncol 2011; 29: 369-377.
5. Mrozek K, Marcucci G, Paschka P, Bloomfield CD. Advances in molecular genetics and treatment of core-binding factor acute myeloid leukemia. Curr Opin Oncol 2008; 20: 711-718.
6. Care RS, Valk PJ, Goodeve AC, Abu-Duhier FM, Geertsma-Kleinekoort WM, Wilson GA et al. Incidence and prognosis of c-KIT and FLT3 mutations in core binding factor (CBF) acute myeloid leukaemias. Br J Haematol 2003; 121: 775-777. (Pubitemid 36718195)
7. Nanri T, Matsuno N, Kawakita T, Suzushima H, Kawano F, Mitsuya H 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: 1361-1366. (Pubitemid 41136329)
8. Cairoli R, Beghini A, Grillo G, Nadali G, Elice F, Ripamonti CB et al. Prognostic impact of c-KIT mutations in core binding factor leukemias: an Italian retrospective study. Blood 2006; 107: 3463-3468.
9. Boissel N, Leroy H, Brethon B, Philippe N, de Botton S, Auvrignon A 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: 965-970. (Pubitemid 43797286)
10. Schnittger S, Kohl TM, Haferlach T, Kern W, Hiddemann W, Spiekermann K et al. KIT-D816 mutations in AML1-ETO-positive AML are associated with impaired event-free and overall survival. Blood 2006; 107: 1791-1799. (Pubitemid 43289355)
11. Park SH, Chi HS, Min SK, Park BG, Jang S, Park CJ. Prognostic impact of c-KIT mutations in core binding factor acute myeloid leukemia. Leuk Res 2011; 35: 1376-1383.
12. Paschka P, Marcucci G, Ruppert AS, Mrozek K, Chen H, Kittles RA 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: 3904-3911. (Pubitemid 46630738)
13. Paschka P, Du J, Schlenk RF, Gaidzik VI, Bullinger L, Corbacioglu A et al. Secondary genetic lesions in acute myeloid leukemia with inv(16) or t(16;16): a study of the German-Austrian AML Study Group (AMLSG). Blood 2013; 121: 170-177.
14. Shih LY, Liang DC, Huang CF, Chang YT, Lai CL, Lin TH et al. Cooperating mutations of receptor tyrosine kinases and Ras genes in childhood core-binding factor acute myeloid leukemia and a comparative analysis on paired diagnosis and relapse samples. Leukemia 2008; 22: 303-307.
15. Pollard JA, Alonzo TA, Gerbing RB, Ho PA, Zeng R, Ravindranath Y et al. Prevalence and prognostic significance of KIT mutations in pediatric patients with core binding factor AML enrolled on serial pediatric cooperative trials for de novo AML. Blood 2010; 115: 2372-2379.
16. Thiede C, Steudel C, Mohr B, Schaich M, Schakel U, Platzbecker U et al. Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood 2002; 99: 4326-4335. (Pubitemid 34627197)
17. Meshinchi S, Alonzo TA, Stirewalt DL, Zwaan M, Zimmerman M, Reinhardt D et al. Clinical implications of FLT3 mutations in pediatric AML. Blood 2006; 108: 3654-3661. (Pubitemid 44864541)
18. Mead AJ, Linch DC, Hills RK, Wheatley K, Burnett AK, Gale RE. FLT3 tyrosine kinase domain mutations are biologically distinct from and have a significantly more favorable prognosis than FLT3 internal tandem duplications in patients with acute myeloid leukemia. Blood 2007; 110: 1262-1270. (Pubitemid 47281424)
19. Gale RE, Green C, Allen C, Mead AJ, Burnett AK, Hills RK et al. The impact of FLT3 internal tandem duplication mutant level, number, size, and interaction with NPM1 mutations in a large cohort of young adult patients with acute myeloid leukemia. Blood 2008; 111: 2776-2784.
20. Schnittger S, Bacher U, Kern W, Alpermann T, Haferlach C, Haferlach T. Prognostic impact of FLT3-ITD load in NPM1 mutated acute myeloid leukemia. Leukemia 2011; 25: 1297-1304.
21. Schneider F, Hoster E, Unterhalt M, Schneider S, Dufour A, Benthaus T et al. The FLT3ITD mRNA level has a high prognostic impact in NPM1 mutated, but not in NPM1 unmutated, AML with a normal karyotype. Blood 2012; 119: 4383-4386.
22. Pratcorona M, Brunet S, Nomdedeu J, Ribera JM, Tormo M, Duarte R et al. Favorable outcome of patients with acute myeloid leukemia harboring a lowallelic burden FLT3-ITD mutation and concomitant NPM1 mutation: relevance to post-remission therapy. Blood 2013; 121(14): 2734-2738.
23. Valk PJ, Bowen DT, Frew ME, Goodeve AC, Lowenberg B, Reilly JT. Second hit mutations in the RTK/RAS signaling pathway in acute myeloid leukemia with inv(16). Haematologica 2004; 89: 106. (Pubitemid 38165863)
24. Reindl C, Quentmeier H, Petropoulos K, Greif PA, Benthaus T, Argiropoulos B et al. CBL exon 8/9 mutants activate the FLT3 pathway and cluster in core binding factor/11q deletion acute myeloid leukemia/myelodysplastic syndrome subtypes. Clin Cancer Res 2009; 15: 2238-2247.
25. Opatz S, Polzer H, Herold T, Konstandin NP, Ksienzyk B, Graf A et al. Exome sequencing identifies recurring FLT3 N676K mutations in core binding factor Leukemia. Blood (ASH Annual Meeting Abstracts) 2012; 120: 404.
26. Haferlach C, Dicker F, Kohlmann A, Schindela S, Weiss T, Kern W et al. AML with CBFB-MYH11 rearrangement demonstrate RAS pathway alterations in 92% of all cases including a high frequency of NF1 deletions. Leukemia 2010; 24: 1065-1069.
27. Abbas S, Rotmans G, Lowenberg B, Valk PJ. Exon 8 splice site mutations in the gene encoding the E3-ligase CBL are associated with core binding factor acute myeloid leukemias. Haematologica 2008; 93: 1595-1597.
28. Hann IM, Stevens RF, Goldstone AH, Rees JK, Wheatley K, Gray RG et al. Randomized comparison of DAT versus ADE as induction chemotherapy in children and younger adults with acute myeloid leukemia. Results of the Medical Research Council's 10th AML trial (MRC AML10). Adult and Childhood Leukaemia Working Parties of the Medical Research Council. Blood 1997; 89: 2311-2318. (Pubitemid 27143277)
29. Burnett AK, Hills RK, Milligan DW, Goldstone AH, Prentice AG, McMullin MF et al. Attempts to optimize induction and consolidation treatment in acute myeloid leukemia: results of the MRC AML12 trial. J Clin Oncol 2010; 28: 586-595.
30. Liu Yin JA, O'Brien MA, Hills RK, Daly SB, Wheatley K, Burnett AK. Minimal residual disease monitoring by RT-qPCR in core-binding factor AML allows risk-stratification and predicts relapse: results of the UK MRC AML-15 trial. Blood 2012; 120: 2826-2835.
31. Schessl C, Rawat VP, Cusan M, Deshpande A, Kohl TM, Rosten PM et al. The AML1-ETO fusion gene and the FLT3 length mutation collaborate in inducing acute leukemia in mice. J Clin Invest 2005; 115: 2159-2168. (Pubitemid 41134157)
32. Wang YY, Zhao LJ, Wu CF, Liu P, Shi L, Liang Y et al. C-KIT mutation cooperates with full-length AML1-ETO to induce acute myeloid leukemia in mice. Proc Natl Acad Sci USA 2011; 108: 2450-2455.
33. Zhao L, Melenhorst JJ, Alemu L, Kirby M, Anderson S, Kench M et al. KIT with D816 mutations cooperates with CBFB-MYH11 for leukemogenesis in mice. Blood 2012; 119: 1511-1521.
34. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood 2009; 114: 937-951.
35. O'Donnell MR, Abboud CN, Altman J, Appelbaum FR, Arber DA, Attar E et al. Acute myeloid leukemia. J Natl Compr Canc Netw 2012; 10: 984-1021.
36. Schlenk RF, Pasquini MC, Perez WS, Zhang MJ, Krauter J, Antin JH et al. HLA-identical sibling allogeneic transplants versus chemotherapy in acute myelogenous leukemia with t(8;21) in first complete remission: collaborative study between the German AML Intergroup and CIBMTR. Biol Blood Marrow Transplant 2008; 14: 187-196.
37. Park JH, Hedvat CV, Tallman MS. Blood consult: acute myeloid leukemia and the t(8;21)(q22;22). Blood 2011; 117: 2775-2777.
38. Whitman SP, Ruppert AS, Radmacher MD, Mró zek K, Paschka P, Langer C et al. FLT3 D835/I836 mutations are associated with poor disease-free survival and a distinct gene-expression signature among younger adults with de novo cytogenetically normal acute myeloid leukemia lacking FLT3 internal tandem duplications. Blood 2008; 111: 1552-1559. (Pubitemid 351213445)
39. Mead AJ, Gale RE, Hills RK, Gupta M, Young BD, Burnett AK et al. Conflicting data on the prognostic significance of FLT3/TKD mutations in acute myeloid leukemia might be related to the incidence of biallelic disease. Blood 2008; 112: 444-445.
40. Jourdan E, Boissel N, Chevret S, Delabesse E, Renneville A, Cornillet P et al. Prospective evaluation of gene mutations and minimal residual disease in patients with core binding factor acute myeloid leukemia. Blood 2013; 121: 2213-2223.
41. 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: 3319-3321.
42. Cammenga J, Horn S, Bergholz U, Sommer G, Besmer P, Fiedler W et al. Extracellular KIT receptor mutants, commonly found in core binding factor AML, are constitutively active and respond to imatinib mesylate. Blood 2005; 106: 3958-3961. (Pubitemid 41739038)
43. Yang Y, Letard S, Borge L, Chaix A, Hanssens K, Lopez S et al. Pediatric mastocytosis-associated KIT extracellular domain mutations exhibit different functional and signaling properties compared with KIT-phosphotransferase domain mutations. Blood 2010; 116: 1114-1123.
44. Kim SY, Kang JJ, Lee HH, Kim B, Kim CG, Park TK et al. Mechanism of activation of human c-KIT kinase by internal tandem duplications of the juxtamembrane domain and point mutations at aspartic acid 816. Biochem Biophys Res Commun 2011; 410: 224-228.
45. Nick HJ, Kim HG, Chang CW, Harris KW, Reddy V, Klug CA. Distinct classes of c-Kitactivating mutations differ in their ability to promote RUNX1-ETO-associated acute myeloid leukemia. Blood 2012; 119: 1522-1531.
46. Schittenhelm MM, Shiraga S, Schroeder A, Corbin AS, Griffith D, Lee FY et al. Dasatinib (BMS-354825), a dual SRC/ABL kinase inhibitor, inhibits the kinase activity of wild-type, juxtamembrane, and activation loop mutant KIT isoforms associated with human malignancies. Cancer Res 2006; 66: 473-481. (Pubitemid 43166056)
47. Kottaridis PD, Gale RE, Langabeer SE, Frew ME, Bowen DT, Linch DC. Studies of FLT3 mutations in paired presentation and relapse samples from patients with acute myeloid leukemia: implications for the role of FLT3 mutations in leukemogenesis, minimal residual disease detection, and possible therapy with FLT3 inhibitors. Blood 2002; 100: 2393-2398.
48. Shih LY, Huang CF, Wu JH, Lin TL, Dunn P, Wang PN et al. Internal tandem duplication of FLT3 in relapsed acute myeloid leukemia: a comparative analysis of bone marrow samples from 108 adult patients at diagnosis and relapse. Blood 2002; 100: 2387-2392.
49. Ding L, Ley TJ, Larson DE, Miller CA, Koboldt DC, Welch JS et al. Clonal evolution in relapsed acute myeloid leukaemia revealed by whole-genome sequencing. Nature 2012; 481: 506-510.
50. Parikh C, Subrahmanyam R, Ren R. Oncogenic NRAS, KRAS, and HRAS exhibit different leukemogenic potentials in mice. Cancer Res 2007; 67: 7139-7146. (Pubitemid 47206541)
51. Chou FS, Wunderlich M, Griesinger A, Mulloy JC. N-Ras(G12D) induces features of stepwise transformation in preleukemic human umbilical cord blood cultures expressing the AML1-ETO fusion gene. Blood 2011; 117: 2237-2240.
52. Bowen DT, Frew ME, Hills R, Gale RE, Wheatley K, Groves MJ et al. RAS mutation in acute myeloid leukemia is associated with distinct cytogenetic subgroups but does not influence outcome in patients younger than 60 years. Blood 2005; 106: 2113-2119. (Pubitemid 41291728)
53. Bacher U, Haferlach T, Schoch C, Kern W, Schnittger S. Implications of NRAS mutations in AML: a study of 2502 patients. Blood 2006; 107: 3847-3853. (Pubitemid 43726786)
54. Sargin B, Choudhary C, Crosetto N, Schmidt MH, Grundler R, Rensinghoff M et al. Flt3-dependent transformation by inactivating c-Cbl mutations in AML. Blood 2007; 110: 1004-1012. (Pubitemid 47267440)
55. Rathinam C, Thien CB, Flavell RA, Langdon WY. Myeloid leukemia development in c-Cbl RING finger mutant mice is dependent on FLT3 signaling. Cancer Cell 2010; 18: 341-352.
56. Schlenk RF, Benner A, Krauter J, Buchner T, Sauerland C, Ehninger G et al. Individual patient data-based meta-analysis of patients aged 16 to 60 years with core binding factor acute myeloid leukemia: a survey of the German Acute Myeloid Leukemia Intergroup. J Clin Oncol 2004; 22: 3741-3750. (Pubitemid 41102131)
57. Marcucci G, Mrozek K, Ruppert AS, Maharry K, Kolitz JE, Moore JO et al. Prognostic factors and outcome of core binding factor acute myeloid leukemia patients with t(8;21) differ from those of patients with inv(16): a Cancer and Leukemia Group B study. J Clin Oncol 2005; 23: 5705-5717.
58. Appelbaum FR, Kopecky KJ, Tallman MS, Slovak ML, Gundacker HM, Kim HT et al. The clinical spectrum of adult acute myeloid leukaemia associated with core binding factor translocations. Br J Haematol 2006; 135: 165-173. (Pubitemid 44401613)