FLT3 Mutations in Early T-Cell Precursor ALL Characterize a Stem Cell Like Leukemia and Imply the Clinical Use of Tyrosine Kinase Inhibitors

PLoS ONE

Volumn 8, Issue 1, 2013, Pages

  Neumann, Martin ^a   Coskun, Ebru ^a   Fransecky, Lars ^a   Mochmann, Liliana H ^a   Bartram, Isabelle ^a   Farhadi Sartangi, Nasrin ^a   Heesch, Sandra ^a   Gökbuget, Nicola ^b   Schwartz, Stefan ^a   Brandts, Christian ^b   Schlee, Cornelia ^a   Haas, Rainer ^c   Dührsen, Ulrich ^d   Griesshammer, Martin ^e   Döhner, Hartmut ^f   Ehninger, Gerhard ^g   Burmeister, Thomas ^a   Blau, Olga ^a   Thiel, Eckhard ^a   Hoelzer, Dieter ^b   Hofmann, Wolf Karsten ^h   Baldus, Claudia D ^a   more..

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c HEINRICH HEINE UNIVERSITY   (Germany)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e KLINIKUM MINDEN   (Germany)

^f UNIVERSITY OF ULM   (Germany)

^g DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^h UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CD135 ANTIGEN; CD2 ANTIGEN; CD33 ANTIGEN; CD5 ANTIGEN; CYTARABINE; DOVITINIB; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN 7; MICROSOMAL AMINOPEPTIDASE; MIDOSTAURIN; NOTCH1 RECEPTOR; SOMATOMEDIN BINDING PROTEIN; SORAFENIB; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; WT1 PROTEIN;

ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; AGED; ALLOGENEIC STEM CELL TRANSPLANTATION; ARTICLE; CELL PROLIFERATION; CLINICAL EFFECTIVENESS; CLINICAL FEATURE; CONTROLLED STUDY; DISEASE CLASSIFICATION; FEMALE; FLT3 GENE; GENE; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC TRANSFORMATION; HUMAN; HUMAN CELL; IC 50; IMMUNOPHENOTYPING; INSULIN LIKE GROWTH FACTOR BINDING PROTEIN 7 GENE; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; MUTATION RATE; MUTATIONAL ANALYSIS; OUTCOME ASSESSMENT; OVERALL SURVIVAL; SURVIVAL RATE; T LYMPHOCYTE RECEPTOR GENE; TRANSCRIPTION FACTOR GATA 3 GENE; WT1 GENE;

ADULT; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; FMS-LIKE TYROSINE KINASE 3; HUMANS; MUTATION; PRECURSOR T-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PROTEIN KINASE INHIBITORS; PROTEIN-TYROSINE KINASES;

EID: 84872851349     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053190     Document Type: Article

References (52)

1. Ferrando AA, Neuberg DS, Staunton J, Loh ML, Huard C, et al. (2002) Gene expression signatures define novel oncogenic pathways in T cell acute lymphoblastic leukemia. Cancer Cell 1: 75-87 S1535610802000181 [pii].
2. Soulier J, Clappier E, Cayuela JM, Regnault A, Garcia-Peydro M, et al. (2005) HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (T-ALL). Blood 106: 274-286 2004-10-3900 [pii];10.1182/blood-2004-10-3900 [doi].
3. van Vlierberghe P, van GM, Tchinda J, Lee C, Beverloo HB, et al. (2008) The recurrent SET-NUP214 fusion as a new HOXA activation mechanism in pediatric T-cell acute lymphoblastic leukemia. Blood 111: 4668-4680 blood-2007-09-111872 [pii];10.1182/blood-2007-09-111872 [doi].
4. Coustan-Smith E, Mullighan CG, Onciu M, Behm FG, Raimondi SC, et al. (2009) Early T-cell precursor leukaemia: a subtype of very high-risk acute lymphoblastic leukaemia. Lancet Oncol 10: 147-156.
5. Dadi S, Le NS, Payet-Bornet D, Lhermitte L, Zacarias-Cabeza J, et al. (2012) TLX Homeodomain Oncogenes Mediate T Cell Maturation Arrest in T-ALL via Interaction with ETS1 and Suppression of TCRalpha Gene Expression. Cancer Cell 21: 563-576 S1535-6108(12)00077-3 [pii];10.1016/j.ccr.2012.02.013 [doi].
6. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, et al. (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481: 157-163 nature10725 [pii];10.1038/nature10725 [doi].
7. Paganin M, Ferrando A, (2010) Molecular pathogenesis and targeted therapies for NOTCH1-induced T-cell acute lymphoblastic leukemia. Blood Rev.
8. van Grotel M, Meijerink JP, van Wering ER, Langerak AW, Beverloo HB, et al. (2008) Prognostic significance of molecular-cytogenetic abnormalities in pediatric T-ALL is not explained by immunophenotypic differences. Leukemia 22: 124-131 2404957 [pii];10.1038/sj.leu.2404957 [doi].
9. Weng AP, Ferrando AA, Lee W, Morris JP, Silverman LB, et al. (2004) Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
10. Breit S, Stanulla M, Flohr T, Schrappe M, Ludwig WD, et al. (2006) Activating NOTCH1 mutations predict favorable early treatment response and long-term outcome in childhood precursor T-cell lymphoblastic leukemia. Blood 108: 1151-1157.
11. Asnafi V, Buzyn A, Le Noir S, Baleydier F, Simon A, et al. (2009) NOTCH1/FBXW7 mutation identifies a large subgroup with favorable outcome in adult T-cell acute lymphoblastic leukemia (T-ALL): a Group for Research on Adult Acute Lymphoblastic Leukemia (GRAALL) study. Blood 113: 3918-3924.
12. Zuurbier L, Petricoin EF, Vuerhard MJ, Calvert V, Kooi C, et al. (2012) The significance of PTEN and AKT aberrations in pediatric T-cell acute lymphoblastic leukemia. Haematologica haematol.2011.059030 [pii];10.3324/haematol.2011.059030 [doi].
13. Grabher C, von Boehmer H, Look AT, (2006) Notch 1 activation in the molecular pathogenesis of T-cell acute lymphoblastic leukaemia. Nat Rev Cancer 6: 347-359.
14. Silva A, Jotta PY, Silveira AB, Ribeiro D, Brandalise SR, et al. (2010) Regulation of PTEN by CK2 and Notch1 in primary T-cell acute lymphoblastic leukemia: rationale for combined use of CK2- and gamma-secretase inhibitors. Haematologica 95: 674-678 haematol.2009.011999 [pii];10.3324/haematol.2009.011999 [doi].
15. Paietta E, Ferrando AA, Neuberg D, Bennett JM, Racevskis J, et al. (2004) Activating FLT3 mutations in CD117/KIT(+) T-cell acute lymphoblastic leukemias. Blood 104: 558-560.
16. van Vlierberghe P, Meijerink JP, Stam RW, van der Smissen W, van Wering ER, et al. (2005) Activating FLT3 mutations in CD4+/CD8- pediatric T-cell acute lymphoblastic leukemias. Blood 106: 4414-4415 106/13/4414 [pii];10.1182/blood-2005-06-2267 [doi].
17. Hoehn D, Medeiros LJ, Chen SS, Tian T, Jorgensen JL, et al. (2012) CD117 expression is a sensitive but nonspecific predictor of FLT3 mutation in T acute lymphoblastic leukemia and T/myeloid acute leukemia. Am J Clin Pathol 137: 213-219 137/2/213 [pii];10.1309/AJCPR3N3JMSYLPFG [doi].
18. Levis M, Small D, (2003) FLT3: ITDoes matter in leukemia. Leukemia 17: 1738-1752 10.1038/sj.leu.2403099 [doi];2403099 [pii].
19. Marcucci G, Haferlach T, Dohner H, (2011) Molecular genetics of adult acute myeloid leukemia: prognostic and therapeutic implications. J Clin Oncol 29: 475-486 JCO.2010.30.2554 [pii];10.1200/JCO.2010.30.2554 [doi].
20. Sanz M, Burnett A, Lo-Coco F, Lowenberg B, (2009) FLT3 inhibition as a targeted therapy for acute myeloid leukemia. Curr Opin Oncol 21: 594-600.
21. Pemmaraju N, Kantarjian H, Ravandi F, Cortes J, (2011) FLT3 inhibitors in the treatment of acute myeloid leukemia: the start of an era? Cancer 117: 3293-3304 10.1002/cncr.25908 [doi].
22. Neumann M, Heesch S, Gökbuget N, Schwartz S, Schlee C, et al. (2012) Clinical and molecular characterization of early T-cell precursor leukemia: a high-risk subgroup in adult T-ALL with a high frequency of FLT3 mutations. Blood Cancer Journal e55.
23. Bruggemann M, Raff T, Flohr T, Gokbuget N, Nakao M, et al. (2006) Clinical significance of minimal residual disease quantification in adult patients with standard-risk acute lymphoblastic leukemia. Blood 107: 1116-1123.
24. Baldus CD, Martus P, Burmeister T, Schwartz S, Gokbuget N, et al. (2007) Low ERG and BAALC expression identifies a new subgroup of adult acute T-lymphoblastic leukemia with a highly favorable outcome. J Clin Oncol 25: 3739-3745.
25. Heesch S, Goekbuget N, Stroux A, Tanchez JO, Schlee C, et al. (2010) Prognostic implications of mutations and expression of the Wilms tumor 1 (WT1) gene in adult acute T-lymphoblastic leukemia. Haematologica 95: 942-949.
26. Heesch S, Schlee C, Neumann M, Stroux A, Kuhnl A, et al. (2010) BAALC-associated gene expression profiles define IGFBP7 as a novel molecular marker in acute leukemia. Leukemia 24: 1429-1436.
27. Heuser M, Beutel G, Krauter J, Dohner K, von Neuhoff N, et al. (2006) High meningioma 1 (MN1) expression as a predictor for poor outcome in acute myeloid leukemia with normal cytogenetics. Blood 108: 3898-3905.
28. Weng AP, Nam Y, Wolfe MS, Pear WS, Griffin JD, et al. (2003) Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling. Mol Cell Biol 23: 655-664.
29. Baldus CD, Thibaut J, Goekbuget N, Stroux A, Schlee C, et al. (2009) Prognostic implications of NOTCH1 and FBXW7 mutations in adult acute T-lymphoblastic leukemia. Haematologica 94: 1383-1390.
30. Kalender AZ, De KK, Gianfelici V, Geerdens E, Vandepoel R, et al. (2012) High accuracy mutation detection in leukemia on a selected panel of cancer genes. PLoS One 7: e38463 10.1371/journal.pone.0038463 [doi];PONE-D-12-00005 [pii].
31. Brandts CH, Sargin B, Rode M, Biermann C, Lindtner B, et al. (2005) Constitutive activation of Akt by Flt3 internal tandem duplications is necessary for increased survival, proliferation, and myeloid transformation. Cancer Res 65: 9643-9650 65/21/9643 [pii];10.1158/0008-5472.CAN-05-0422 [doi].
32. Homminga I, Pieters R, Langerak AW, de Rooi JJ, Stubbs A, et al. (2011) Integrated transcript and genome analyses reveal NKX2-1 and MEF2C as potential oncogenes in T cell acute lymphoblastic leukemia. Cancer Cell 19: 484-497.
33. Hosoya T, Kuroha T, Moriguchi T, Cummings D, Maillard I, et al. (2009) GATA-3 is required for early T lineage progenitor development. J Exp Med 206: 2987-3000.
34. Rothenberg EV, (2012) Transcriptional drivers of the T-cell lineage program. Curr Opin Immunol 24: 132-138.
35. Anderson MK, Hernandez-Hoyos G, Diamond RA, Rothenberg EV, (1999) Precise developmental regulation of Ets family transcription factors during specification and commitment to the T cell lineage. Development 126: 3131-3148.
36. Paietta E, (2010) Surrogate marker profiles for genetic lesions in acute leukemias. Best Pract Res Clin Haematol 23: 359-368 S1521-6926(10)00058-7 [pii];10.1016/j.beha.2010.08.001 [doi].
37. Carow CE, Levenstein M, Kaufmann SH, Chen J, Amin S, et al. (1996) Expression of the hematopoietic growth factor receptor FLT3 (STK-1/Flk2) in human leukemias. Blood 87: 1089-1096.
38. Chillon MC, Gomez-Casares MT, Lopez-Jorge CE, Rodriguez-Medina C, Molines A, et al. (2012) Prognostic significance of FLT3 mutational status and expression levels in MLL-AF4+ and MLL-germline acute lymphoblastic leukemia. Leukemia leu2012161 [pii];10.1038/leu.2012.161 [doi].
39. Inukai T, Kiyokawa N, Campana D, Coustan-Smith E, Kikuchi A, et al. (2012) Clinical significance of early T-cell precursor acute lymphoblastic leukaemia: results of the Tokyo Children's Cancer Study Group Study L99-15. Br J Haematol 156: 358-365 10.1111/j.1365-2141.2011.08955.x [doi].
40. Baldus CD, Tanner SM, Ruppert AS, Whitman SP, Archer KJ, et al. (2003) BAALC expression predicts clinical outcome of de novo acute myeloid leukemia patients with normal cytogenetics: a Cancer and Leukemia Group B Study. Blood 102: 1613-1618.
41. Paschka P, Marcucci G, Ruppert AS, Whitman SP, Mrozek K, et al. (2008) Wilms' tumor 1 gene mutations independently predict poor outcome in adults with cytogenetically normal acute myeloid leukemia: a cancer and leukemia group B study. J Clin Oncol 26: 4595-4602.
42. Yamamoto Y, Kiyoi H, Nakano Y, Suzuki R, Kodera Y, et al. (2001) Activating mutation of D835 within the activation loop of FLT3 in human hematologic malignancies. Blood 97: 2434-2439.
43. Blom B, Verschuren MC, Heemskerk MH, Bakker AQ, van Gastel-Mol EJ, et al. (1999) TCR gene rearrangements and expression of the pre-T cell receptor complex during human T-cell differentiation. Blood 93: 3033-3043.
44. Dik WA, Pike-Overzet K, Weerkamp F, de RD, de Haas EF, et al. (2005) New insights on human T cell development by quantitative T cell receptor gene rearrangement studies and gene expression profiling. J Exp Med 201: 1715-1723 jem.20042524 [pii];10.1084/jem.20042524 [doi].
45. Gunji Y, Nakamura M, Osawa H, Nagayoshi K, Nakauchi H, et al. (1993) Human primitive hematopoietic progenitor cells are more enriched in KITlow cells than in KIThigh cells. Blood 82: 3283-3289.
46. Cascavilla N, Musto P, D'Arena G, Melillo L, Carella AM, et al. (1998) CD117 (c-kit) is a restricted antigen of acute myeloid leukemia and characterizes early differentiative levels of M5 FAB subtype. Haematologica 83: 392-397.
47. Ikeda H, Kanakura Y, Tamaki T, Kuriu A, Kitayama H, et al. (1991) Expression and functional role of the proto-oncogene c-kit in acute myeloblastic leukemia cells. Blood 78: 2962-2968.
48. Reuss-Borst MA, Buhring HJ, Schmidt H, Muller CA, (1994) AML: immunophenotypic heterogeneity and prognostic significance of c-kit expression. Leukemia 8: 258-263.
49. Gutierrez A, Dahlberg SE, Neuberg DS, Zhang J, Grebliunaite R, et al. (2010) Absence of biallelic TCRgamma deletion predicts early treatment failure in pediatric T-cell acute lymphoblastic leukemia. J Clin Oncol 28: 3816-3823 JCO.2010.28.3390 [pii];10.1200/JCO.2010.28.3390 [doi].
50. Gokbuget N, Hoelzer D, (2006) Treatment of adult acute lymphoblastic leukemia. Hematology Am Soc Hematol Educ Program pp. 133-141.
51. Ravandi F, Cortes JE, Jones D, Faderl S, Garcia-Manero G, et al. (2010) Phase I/II study of combination therapy with sorafenib, idarubicin, and cytarabine in younger patients with acute myeloid leukemia. J Clin Oncol 28: 1856-1862 JCO.2009.25.4888 [pii];10.1200/JCO.2009.25.4888 [doi].
52. Pratz KW, Sato T, Murphy KM, Stine A, Rajkhowa T, et al. (2010) FLT3-mutant allelic burden and clinical status are predictive of response to FLT3 inhibitors in AML. Blood 115: 1425-1432 blood-2009-09-242859 [pii];10.1182/blood-2009-09-242859 [doi].