FLT3 inhibition in t(4;11)+ adult acute lymphoid leukaemia

British Journal of Haematology

Volumn 130, Issue 1, 2005, Pages 43-50

  Torelli, Giovanni F ^a   Guarini, Anna ^a   Porzia, Alessandra ^a   Chiaretti, Sabina ^a   Tatarelli, Caterina ^a   Diverio, Daniela ^a   Maggio, Roberta ^a   Vitale, Antonella ^a   Ritz, Jerome ^b   Foa, Robin ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Acute lymphoid leukaemia; FLT3; Kinase inhibition; Signal transduction; Targeted therapy

Indexed keywords

FLT3 LIGAND; MESSENGER RNA; MIDOSTAURIN;

ACUTE LYMPHOCYTIC LEUKEMIA; ADULT; ARTICLE; BLAST CELL; CLINICAL ARTICLE; GENE DUPLICATION; GENE MUTATION; HUMAN; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADULT; BLOTTING, WESTERN; CASE-CONTROL STUDIES; CHROMOSOMES, HUMAN, PAIR 11; CHROMOSOMES, HUMAN, PAIR 4; DNA, COMPLEMENTARY; FMS-LIKE TYROSINE KINASE 3; HUMANS; LEUKEMIA, LYMPHOCYTIC, ACUTE; MEMBRANE PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; RNA, MESSENGER; SIGNAL TRANSDUCTION; STAUROSPORINE; TRANSLOCATION, GENETIC;

EID: 22144451152     PISSN: 00071048     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2005.05556.x     Document Type: Article

References (45)

1. Armstrong, S.A., Staunton, J.E., Silverman, L.B., Pieters, R., den Boer, M.L., Minden, M.D., Sallan, S.E., Lander, E.S., Golub, T.R. & Korsmeyer, S.J. (2002) MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nature Genetics, 30, 41-47.
2. Armstrong, S.A., Kung, A.L., Mabon, M.E., Silverman, L.B., Stam, R.W., Den Boer, M.L., Pieters, R., Kersey, J.H., Sallan, S.E., Fletcher, J.A., Golub, T.R., Griffin, J.D. & Korsmeyer, S.J. (2003) Inhibition of FLT3 in MLL. Validation of a therapeutic target identified by gene expression based classification. Cancer Cell, 3, 173-183.
3. Armstrong, S.A., Mabon, M.E., Silverman, L.B., Li, A., Gribben, J.G., Fox, E.A., Sallan, S.E. & Korsmeyer, S.J. (2004) FLT3 mutations in childhood acute lymphoblastic leukemia. Blood, 103, 3544-3546.
4. Beniamini, Y. & Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal Royal Statistical Society B, 57, 289-300.
5. Brasel, K., Escobar, S., Anderberg, R., de Vries, P., Gruss, H.J. & Lyman, S.D. (1995) Expression of the flt3 receptor and its ligand on hematopoietic cells. Leukemia, 9, 1212-1218.
6. Brown, P., Levis, M., Shurtleff, S., Campana, D., Downing, J. & Small, D. (2005) FLT3 inhibition selectively kills childhood acute lymphoblastic leukemia cells with high levels of FLT3 expression. Blood, 105, 812-820.
7. Chiaretti, S., Gentleman, R., Wang, K., Vitale, A., Ritz, J. & Foa, R. (2001) Gene expression profiles of adult acute lymphocytic leukemia (ALL) reveal distintc genetic patterns that correlate with cell surface phenotype, chromosomal abnormalities and clinical outcome [abstract]. Blood, 98, 304a.
8. Chiaretti, S., Li, X., Gentleman, R., Vitale, A., Vignetti, M., Mandelli, F., Ritz, J. & Foa, R. (2004) Gene expression profile of adult T-cell acute lymphocytic leukemia identifies distinct subsets of patients with different response to therapy and survival. Blood, 103, 2771-2778.
9. Chomczynski, P. & Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry, 162, 156-159.
10. Cimino, G., Elia, L., Rapanotti, M.C., Sprovieri, T., Mancini, M., Cuneo, A., Mecucci, C., Fioritoni, G., Carotenuto, M., Morra, E., Liso, V., Annino, L., Saglio, G., De Rossi, G., Foa, R. & Mandelli, F. (2000) A prospective study of residual-disease monitoring of the ALL1/AF4 transcript in patients with t(4;11) acute lymphoblastic leukemia. Blood, 95, 96-101.
11. Cimino, G., Elia, L., Mancini, M., Annino, L., Anaclerico, B., Fazi, P., Vitale, A., Specchia, G., Di Raimondo, F., Recchia, A., Cuneo, A., Mecucci, C., Pane, F., Saglio, G., Foa, R. & Mandelli, F. (2003) Clinico-biologic features and treatment outcome of adult pro-B-ALL patients enrolled in the GIMEMA 0496 study: absence of the ALL1/AF4 and of the BCR/ABL fusion genes correlates with a significantly better clinical outcome. Blood, 102, 2014-2020.
12. Cools, I., Mentens, N., Furet, P., Fabbro, D., Clark, J.J., Griffin, J.D., Marynen, P. & Gilliland, D.G. (2004) Prediction of resistance to small molecule FLT3 inhibitors: implications for molecularly targeted therapy of acute leukemia. Cancer Research, 64, 6385-6389.
13. van Dongen, J.J., Macintyre, E.A., Gabert, J.A., Delabesse, E., Rossi, V., Saglio, G., Gottardi, E., Rambaldi, A., Dotti, G., Griesinger, F., Parreira, A., Gameiro, P., Diaz, M.G., Malec, M., Langerak, A.W., San Miguel, J.F. & Biondi, A. (1999) Standardized RT-PCR analysis of fusion gene transcripts from chromosome aberrations in acute leukemia for detection of minimal residual disease. Report of the BIOMED-1 Concerted Action: investigation of minimal residual disease in acute leukemia. Leukemia, 13, 1901-1928.
14. Elia, L., Gottardi, E., Floriddia, G., Grillo, R., Ciambelli, F., Luciana, M., Chiusolo, P., Invernizzi, R., Meloni, G., Foa, R., Saglio, G. & Cimino, G. (2004) Retrospective comparison of qualitative and quantitative reverse-transcriptase polymerase chain reaction in diagnosing and monitoring the ALL1-AF4 fusion transcript in patients with acute lymphoblastic leukemia Leukemia, 18, 1824-1830.
15. Ferrando, A.A. & Look, A.T. (2000) Clinical implications of recurring chromosomal and associated molecular abnormalities in acute lymphoblastic leukemia. Seminars in Hematology, 37, 381-395.
16. Ferrando, A.A., Armstrong, S.A., Neuberg, D.S., Sallan, S.E., Silverman, L.B., Korsmeyer, S.J. & Look, A.T. (2003) Gene expression sig-natures in MLL-rearranged T-lineage and B-precursor acute leukemias: dominance of HOX dysregulation. Blood, 102, 262-268.
17. Foa, R. & Vitale, A. (2002) Towards an integrated classification of adult acute lymphoblastic leukemia. Reviews in Clinical and Experimental Hematology, 6, 181-199; discussion 200-182.
18. Gilliland, D.G. & Griffin, J.D. (2002) The roles of FLT3 in hematopoiesis and leukemia. Blood, 100, 1532-1542.
19. Hannum, C., Culpepper, J., Campbell, D., McClanahan, T., Zurawski, S., Bazan, J.F., Kastelein, R., Hudak, S., Wagner, J., Mattson, J., Luh, Duda, G., Martina, N., Peterson, D., Menon, S., Shanafelt, A., Muench, M., Keiner, G., Namikawa, R., Rennick, D., Roncarolo, M.G., Zlotnik, A., Rosnet, O., Dubreuil, P., Birnbaum, D. & Lee, F. (1994) Ligand for FLT3/FLK2 receptor tyrosine kinase regulates growth of haematopoietic stem cells and is encoded by variant RNAs. Nature, 368, 643-648.
20. Hayakawa, F., Towatari, M., Kiyoi, H., Tanimoto, M., Kitamura, T., Saito, H. & Naoe, T. (2000) Tandem-duplicated Flt3 constitutively activates STAT5 and MAP kinase and introduces autonomous cell growth in IL-3-dependent cell lines. Oncogene, 19, 624-631.
21. Hoelzer, D., Gokbuget, N. & Ottmann, O.G. (2002) Targeted therapies in the treatment of Philadelphia chromosome-positive acute lymphoblastic leukemia. Seminars in Hematology, 39, 32-37.
22. Kelly, L.M., Liu, Q., Kutok, J.L., Williams, I.R., Boulton, C.L. & Gilliland, D.G. (2002) FLT3 internal tandem duplication mutations associated with human acute myeloid leukemias induce myeloproliferative disease in a murine bone marrow transplant model. Blood, 99, 310-318.
23. Krampera, M., Vitale, A., Vincenzi, C., Perbellini, O., Guarini, A., Annino, L., Todeschini, G., Camera, A., Fabbiano, F., Fioritoni, G., Mobile, F., Szydlo, R., Mandelli, F., Foa, R. & Pizzolo, G. (2003) Outcome prediction by immunophenotypic minimal residual disease detection in adult T-cell acute lymphoblastic leukaemia. British Journal of Haematology, 120, 74-79.
24. Levis, M., Allebach, J., Tse, K.F., Zheng, R., Baldwin, B.R., Smith, B.D., Jones-Bolin, S., Ruggeri, B., Dionne, C. & Small, D. (2002) A FLT3-targeted tyrosine kinase inhibitor is cytotoxic to leukemia cells in vitro and in vivo. Blood, 99, 3885-3891.
25. Li, C. & Wong, W.H. (2001) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proceedings of the National Academy of Sciences of the United States of America, 98, 31-36.
26. Lyman, S.D. (1995) Biology of flt3 ligand and receptor. International Journal of Hematology, 62, 63-73.
27. Monnerat, C., Henriksson, R., Le Chevalier, T., Novello, S., Berthaud, P., Faivre, S. & Raymond, E. (2004) Phase I study of PKC412 (N-benzoyl-staurosporine), a novel oral protein kinase C inhibitor, combined with gemcitabine and cisplatin in patients with non-small-cell lung cancer. Annals of Oncology, 15, 316-323.
28. Noguera, N.I., Breccia, M., Divona, M., Diverio, D., Costa, V., De Santis, S., Awisati, G., Pinazzi, M.B., Petti, M.C., Mandelli, F. & Lo Coco, F. (2002) Alterations of the FLT3 gene in acute promyelocytic leukemia: association with diagnostic characteristics and analysis of clinical outcome in patients treated with the Italian AIDA protocol. Leukemia, 16, 2185-2189.
29. Ottmann, O.G. & Wassmann, B. (2002) Imatinib in the treatment of Philadelphia chromosome-positive acute lymphoblastic leukaemia: current status and evolving concepts. Best Practice and Research Clinical Haematology, 15, 757-769.
30. Paietta, E., Ferrando, A.A., Neuberg, D., Bennett, J.M., Racevskis, J., Lazarus, H., Dewald, G., Rowe, J.M., Wiernik, P.H., Tallman, M.S. & Look, A.T. (2004) Activating FLT3 mutations in CD117/KIT positive T-cell acute lymphoblastic leukemias. Blood, 104, 558-560.
31. Propper, D.J., McDonald, A.C., Man, A., Thavasu, P., Balkwill, F., Braybrooke, J.P., Caponigro, F., Graf, P., Dutreix, C., Blackie, R., Kaye, S.B., Ganesan, T.S., Talbot, D.C., Harris, A.L. & Twelves, C. (2001) Phase I and pharmacokinetic study of PKC412, an inhibitor of protein kinase C. Journal of Clinical Oncology, 19, 1485-1492.
32. Rozovskaia, T., Feinstein, E., Mor, E., Foa, R., Blechman, J., Nakamura, T., Croce, C.M., Cimino, G. & Canaani, E. (2001) Upregulation of Meis1 and HoxA9 in acute lymphocytic leukemias with the t(4:11) abnormality. Oncogene, 20, 874-878.
33. Rozovskaia, T., Ravid-Amir, O., Tillib, S., Getz, G., Feinstein, E., Agrawal, H., Nagler, A., Rappaport, E.F., Issaeva, I., Matsuo, Y., Kees, U.R., Lapidot, T., Lo Coco, F., Foa, R., Mazo, A., Nakamura, T., Croce, C.M., Cimino, G., Domany, E. & Canaani, E. (2003) Expression profiles of acute lymphoblastic and myeloblastic leukemias with ALL-1 rearrangements. Proceedings of the National Academy of Sciences of the United States of America, 100, 7853-7858.
34. Sawyers, C.L. (2002) Finding the next Gleevec: FLT3 targeted kinase inhibitor therapy for acute myeloid leukemia. Cancer Cell, 1, 413-415.
35. Scheuring, U.J., Pfeifer, H., Wassmann, B., Bruck, P., Gehrke, B., Petershofen, E.K., Gschaidmeier, H., Hoelzer, D. & Ottmann, O.G. (2003) Serial minimal residual disease (MRD) analysis as a predictor of response duration in Philadelphia-positive acute lymphoblastic leukemia (Ph+ALL) during imatinib treatment. Leukemia, 17, 1700-1706.
36. Schnittger, S., Schoch, C., Dugas, M., Kern, W., Staib, P., Wuchter, C., Loffler, H., Sauerland, C.M., Serve, H., Buchner, T., Haferlach, T. & Hiddemann, W. (2002) Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: correlation to cytogenetics, FAB subtype and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood, 100, 59-66.
37. Stone, R.M., De Angelo, J., Galinsky, I., Estey, E., Klimek, V., Grandin, W., Lebwohl, D., Yap, A., Cohen, P., Fox, E., Neuberg, D., Clark, J., Gilliland, D.G. & Griffin, J.D. (2004) PKC 412 FLT3 inhibitor therapy in AML: results of a phase II trial. Annals of Hematology, 83(Suppl.1), S89-S90.
38. Stone, R.M., DeAngelo, D.J., Klimek, V., Galinsky, I., Estey, E., Nimer, S.D., Grandin, W., Lebwohl, D., Wang, Y., Cohen, P., Fox, E.A., Neuberg, D., Clark, J., Gilliland, D.G. & Griffin, J.D. (2005) Patients with acute myeloid leukemia and an activating mutation in FLT3 respond to a small-molecule FLT3 tyrosine kinase inhibitor, PKC412. Blood, 105, 54-60.
39. Thiede, C., Steudel, C., Mohr, B., Schaich, M., Schakel, U., Platzbecker, U., Wermke, M., Bornhauser, M., Ritter, M., Neubauer, A., Ehninger, G. & Illmer, T. (2002) Analysis of FLT3-activating mutations in 979 patients with acute myelogenous leukemia: association with FAB subtypes and identification of subgroups with poor prognosis. Blood, 99, 4326-4335.
40. Tse, K.F., Novelli, E., Civin, C.I., Bohmer, F.D. & Small, D. (2001) Inhibition of FLT3-mediated transformation by use of a tyrosine kinase inhibitor. Leukemia, 15, 1001-1010.
41. Tse, K.F., Allebach, J., Levis, M., Smith, B.D., Bohmer, F.D. & Small, D. (2002) Inhibition of the transforming activity of FLT3 internal tandem duplication mutants from AML patients by a tyrosine kinase inhibitor. Leukemia, 16, 2027-2036.
42. Weisberg, E., Boulton, C., Kelly, L.M., Manley, P., Fabbro, D., Meyer, T., Gilliland, D.G. & Griffin, J.D. (2002) Inhibition of mutant FLT3 receptors in leukemia cells by the small molecule tyrosine kinase inhibitor PKC412. Cancer Cell, 1, 433-443.
43. Yee, K.W., O'Farrell, A.M., Smolich, B.D., Cherrington, J.M., McMahon, G., Wait, C.L., McGreevey, L.S., Griffith, D.J. & Heinrich, M.C. (2002) SU5416 and SU5614 inhibit kinase activity of wild-type and mutant FLT3 receptor tyrosine kinase. Blood, 100, 2941-2949.
44. Zhang, S. & Broxmeyer, H.E. (2000) Flt3 ligand induces tyrosine phosphorylation of gab1 and gab2 and their association with shp-2, grb2 and PI3 kinase. Biochemical and Biophysical Research Communications, 277, 195-199.
45. Zhang, S., Fukuda, S., Lee, Y., Hangoc, G., Cooper, S., Spolski, R., Leonard, W.J. & Broxmeyer, H.E. (2000) Essential role of signal transducer and activator of transcription (Stat)5a but not Stat5b for Flt3-dependent signaling. Journal of Experimental Medicine, 192, 719-728.