Irreversible pan-ERBB inhibitor canertinib elicits anti-leukaemic effects and induces the regression of FLT3-ITD transformed cells in mice

British Journal of Haematology

Volumn 155, Issue 2, 2011, Pages 198-208

  Nordigården, Amanda ^a   Zetterblad, Jenny ^a   Trinks, Cecilia ^a   Gréen, Henrik ^a   Eliasson, Pernilla ^a   Druid, Pia ^a   Lotfi, Kourosh ^a,b   Rönnstrand, Lars ^c   Walz, Thomas M ^a   Jönsson, Jan Ingvar ^a  

^a LINKÖPING UNIVERSITY   (Sweden)

^b LINKÖPING UNIVERSITY HOSPITAL   (Sweden)

^c LUND UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Acute myeloid leukaemia; Apoptosis; Drugs; Leukaemia therapy; Murine model; Signalling

Indexed keywords

BIM PROTEIN; CANERTINIB; CD135 ANTIGEN; EPIDERMAL GROWTH FACTOR RECEPTOR; FLT3 LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR FKHRL1;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; AUTOPHOSPHORYLATION; BLAST CELL; CELL CYCLE ARREST; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; DRUG DOSE COMPARISON; ENZYME ACTIVITY; GENE MUTATION; HUMAN; HUMAN CELL; INTERNAL TANDEM DUPLICATION; LEUKEMIA; LEUKEMIA CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR REGRESSION;

ANIMALS; APOPTOSIS; DRUG SCREENING ASSAYS, ANTITUMOR; FMS-LIKE TYROSINE KINASE 3; HEMATOPOIETIC STEM CELLS; HUMANS; LEUKEMIA, MYELOID, ACUTE; MICE; MICE, INBRED DBA; MORPHOLINES; NEOPLASM PROTEINS; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; ONCOGENE PROTEINS V-ERBB; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; TANDEM REPEAT SEQUENCES; TUMOR CELLS, CULTURED;

EID: 80053576720     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2011.08819.x     Document Type: Article

References (40)

1. Ako, E., Yamashita, Y., Ohira, M., Yamazaki, M., Hori, T., Kubo, N., Sawada, T. & Hirakawa, K. (2007) The pan-erbB tyrosine kinase inhibitor CI-1033 inhibits human esophageal cancer cells in vitro and in vivo. Oncology Reports, 17, 887-893.
2. Bagrintseva, K., Geisenhof, S., Kern, R., Eichenlaub, S., Reindl, C., Ellwart, J.W., Hiddemann, W. & Spiekermann, K. (2005) FLT3-ITD-TKD dual mutants associated with AML confer resistance to FLT3 PTK inhibitors and cytotoxic agents by overexpression of Bcl-x(L). Blood, 105, 3679-3685.
3. Boehrer, S., Ades, L., Braun, T., Galluzzi, L., Grosjean, J., Fabre, C., Le Roux, G., Gardin, C., Martin, A., de Botton, S., Fenaux, P. & Kroemer, G. (2008) Erlotinib exhibits anti-neoplastic off-target effects in AML and MDS: a preclinical study. Blood, 111, 2170-2180.
4. Brandts, C.H., Sargin, B., Rode, M., Biermann, C., Lindtner, B., Schwable, J., Buerger, H., Muller-Tidow, C., Choudhary, C., McMahon, M., Berdel, W.E. & Serve, H. (2005) Constitutive activation of Akt by Flt3 internal tandem duplications is necessary for increased survival, proliferation, and myeloid transformation. Cancer Research, 65, 9643-9650.
5. Campos, S., Hamid, O., Seiden, M.V., Oza, A., Plante, M., Potkul, R.K., Lenehan, P.F., Kaldjian, E.P., Varterasian, M.L., Jordan, C., Charbonneau, C. & Hirte, H. (2005) Multicenter, randomized phase II trial of oral CI-1033 for previously treated advanced ovarian cancer. Journal of Clinical Oncology, 23, 5597-5604.
6. Costa, D.B., Halmos, B., Kumar, A., Schumer, S.T., Huberman, M.S., Boggon, T.J., Tenen, D.G. & Kobayashi, S. (2007) BIM mediates EGFR tyrosine kinase inhibitor-induced apoptosis in lung cancers with oncogenic EGFR mutations. PLoS Medicine, 4, 1669-1679; discussion 1680.
7. Cragg, M.S., Kuroda, J., Puthalakath, H., Huang, D.C. & Strasser, A. (2007) Gefitinib-induced killing of NSCLC cell lines expressing mutant EGFR requires BIM and can be enhanced by BH3 mimetics. PLoS Medicine, 4, 1681-1689; discussion 1690.
8. Dijkers, P.F., Medema, R.H., Lammers, J.W., Koenderman, L. & Coffer, P.J. (2000) Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Current Biology, 10, 1201-1204.
9. Essafi, A., Fernandez de Mattos, S., Hassen, Y.A., Soeiro, I., Mufti, G.J., Thomas, N.S., Medema, R.H. & Lam, E.W. (2005) Direct transcriptional regulation of Bim by FoxO3a mediates STI571-induced apoptosis in Bcr-Abl-expressing cells. Oncogene, 24, 2317-2329.
10. Fabian, M.A., Biggs, W.H. 3rd, Treiber, D.K., Atteridge, C.E., Azimioara, M.D., Benedetti, M.G., Carter, T.A., Ciceri, P., Edeen, P.T., Floyd, M., Ford, J.M., Galvin, M., Gerlach, J.L., Grotzfeld, R.M., Herrgard, S., Insko, D.E., Insko, M.A., Lai, A.G., Lelias, J.M., Mehta, S.A., Milanov, Z.V., Velasco, A.M., Wodicka, L.M., Patel, H.K., Zarrinkar, P.P. & Lockhart, D.J. (2005) A small molecule-kinase interaction map for clinical kinase inhibitors. Nature Biotechnology, 23, 329-336.
11. Gong, Y., Somwar, R., Politi, K., Balak, M., Chmielecki, J., Jiang, X. & Pao, W. (2007) Induction of BIM is essential for apoptosis triggered by EGFR kinase inhibitors in mutant EGFR-dependent lung adenocarcinomas. PLoS Medicine, 4, e294.
12. Green, H., Lotfi, K., Zackrisson, A.L. & Peterson, C. (2003) Spontaneous reversal of p-glycoprotein expression in multidrug resistant cell lines. Pharmacology and Toxicology, 93, 297-304.
13. Janne, P.A., von Pawel, J., Cohen, R.B., Crino, L., Butts, C.A., Olson, S.S., Eiseman, I.A., Chiappori, A.A., Yeap, B.Y., Lenehan, P.F., Dasse, K., Sheeran, M. & Bonomi, P.D. (2007) Multicenter, randomized, phase II trial of CI-1033, an irreversible pan-ERBB inhibitor, for previously treated advanced non small-cell lung cancer. Journal of Clinical Oncology, 25, 3936-3944.
14. Jönsson, M., Engström, M. & Jönsson, J.I. (2004) FLT3 ligand regulates apoptosis through AKT-dependent inactivation of transcription factor FoxO3. Biochemical and Biophysical Research Communications, 318, 899-903.
15. 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.
16. Kindler, T., Lipka, D.B. & Fischer, T. (2010) FLT3 as a therapeutic target in AML: still challenging after all these years. Blood, 116, 5089-5102.
17. Knapper, S., Mills, K.I., Gilkes, A.F., Austin, S.J., Walsh, V. & Burnett, A.K. (2006) The effects of lestaurtinib (CEP701) and PKC412 on primary AML blasts: the induction of cytotoxicity varies with dependence on FLT3 signaling in both FLT3-mutated and wild-type cases. Blood, 108, 3494-3503.
18. Kuribara, R., Honda, H., Matsui, H., Shinjyo, T., Inukai, T., Sugita, K., Nakazawa, S., Hirai, H., Ozawa, K. & Inaba, T. (2004) Roles of Bim in apoptosis of normal and Bcr-Abl-expressing hematopoietic progenitors. Molecular and Cellular Biology, 24, 6172-6183.
19. Lee, B.H., Williams, I.R., Anastasiadou, E., Boulton, C.L., Joseph, S.W., Amaral, S.M., Curley, D.P., Duclos, N., Huntly, B.J., Fabbro, D., Griffin, J.D. & Gilliland, D.G. (2005) FLT3 internal tandem duplication mutations induce myeloproliferative or lymphoid disease in a transgenic mouse model. Oncogene, 24, 7882-7892.
20. Levis, M., Tse, K.F., Smith, B.D., Garrett, E. & Small, D. (2001) A FLT3 tyrosine kinase inhibitor is selectively cytotoxic to acute myeloid leukemia blasts harboring FLT3 internal tandem duplication mutations. Blood, 98, 885-887.
21. Li, L., Piloto, O., Nguyen, H.B., Greenberg, K., Takamiya, K., Racke, F., Huso, D. & Small, D. (2008) Knock-in of an internal tandem duplication mutation into murine FLT3 confers myeloproliferative disease in a mouse model. Blood, 111, 3849-3858.
22. Mahboobi, S., Uecker, A., Sellmer, A., Cenac, C., Hocher, H., Pongratz, H., Eichhorn, E., Hufsky, H., Trumpler, A., Sicker, M., Heidel, F., Fischer, T., Stocking, C., Elz, S., Bohmer, F.D. & Dove, S. (2006) Novel bis(1H-indol-2-yl)methanones as potent inhibitors of FLT3 and platelet-derived growth factor receptor tyrosine kinase. Journal of Medicinal Chemistry, 49, 3101-3115.
23. Nordigården, A., Kraft, M., Eliasson, P., Labi, V., Lam, E.W., Villunger, A. & Jönsson, J.I. (2009) BH3-only protein Bim more critical than Puma in tyrosine kinase inhibitor-induced apoptosis of human leukemic cells and transduced hematopoietic progenitors carrying oncogenic FLT3. Blood, 113, 2302-2311.
24. Ocana, A. & Amir, E. (2009) Irreversible pan-ErbB tyrosine kinase inhibitors and breast cancer: current status and future directions. Cancer Treatment Reviews, 35, 685-691.
25. Quentmeier, H., Reinhardt, J., Zaborski, M. & Drexler, H.G. (2003) FLT3 mutations in acute myeloid leukemia cell lines. Leukemia, 17, 120-124.
26. Razumovskaya, E., Masson, K., Khan, R., Bengtsson, S. & Rönnstrand, L. (2009) Oncogenic Flt3 receptors display different specificity and kinetics of autophosphorylation. Experimental Hematology, 37, 979-989.
27. Rocha-Lima, C.M., Soares, H.P., Raez, L.E. & Singal, R. (2007) EGFR targeting of solid tumors. Cancer Control, 14, 295-304.
28. Scheijen, B., Ngo, H.T., Kang, H. & Griffin, J.D. (2004) FLT3 receptors with internal tandem duplications promote cell viability and proliferation by signaling through Foxo proteins. Oncogene, 23, 3338-3349.
29. Slichenmyer, W.J., Elliott, W.L. & Fry, D.W. (2001) CI-1033, a pan-erbB tyrosine kinase inhibitor. Seminars in Oncology, 28, 80-85.
30. Smaill, J.B., Rewcastle, G.W., Loo, J.A., Greis, K.D., Chan, O.H., Reyner, E.L., Lipka, E., Showalter, H.D., Vincent, P.W., Elliott, W.L. & Denny, W.A. (2000) Tyrosine kinase inhibitors. 17. Irreversible inhibitors of the epidermal growth factor receptor: 4-(phenylamino)quinazoline- and 4-(phenylamino)pyrido[3, 2-d]pyrimidine-6-acrylamides bearing additional solubilizing functions. Journal of Medicinal Chemistry, 43, 1380-1397.
31. Spiekermann, K., Dirschinger, R.J., Schwab, R., Bagrintseva, K., Faber, F., Buske, C., Schnittger, S., Kelly, L.M., Gilliland, D.G. & Hiddemann, W. (2003) The protein tyrosine kinase inhibitor SU5614 inhibits FLT3 and induces growth arrest and apoptosis in AML-derived cell lines expressing a constitutively activated FLT3. Blood, 101, 1494-1504.
32. Steeghs, N., Nortier, J.W. & Gelderblom, H. (2007) Small molecule tyrosine kinase inhibitors in the treatment of solid tumors: an update of recent developments. Annals of Surgical Oncology, 14, 942-953.
33. Stegmaier, K., Corsello, S.M., Ross, K.N., Wong, J.S., Deangelo, D.J. & Golub, T.R. (2005) Gefitinib induces myeloid differentiation of acute myeloid leukemia. Blood, 106, 2841-2848.
34. Taussig, D.C., Pearce, D.J., Simpson, C., Rohatiner, A.Z., Lister, T.A., Kelly, G., Luongo, J.L., Danet-Desnoyers, G.A. & Bonnet, D. (2005) Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood, 106, 4086-4092.
35. Trinks, C., Djerf, E.A., Hallbeck, A.L., Jönsson, J.I. & Walz, T.M. (2010) The pan-ErbB receptor tyrosine kinase inhibitor canertinib induces ErbB-independent apoptosis in human leukemia (HL-60 and U-937) cells. Biochemical and Biophysical Research Communications, 393, 6-10.
36. Trinks, C., Severinson, E.A., Holmlund, B., Green, A., Green, H., Jönsson, J.I., Hallbeck, A.L. & Walz, T.M. (2011) The pan-ErbB tyrosine kinase inhibitor canertinib induces caspase-mediated cell death in human T-cell leukemia (Jurkat) cells. Biochemical and Biophysical Research Communications, 410, 422-427.
37. Vardiman, J.W., Thiele, J., Arber, D.A., Brunning, R.D., Borowitz, M.J., Porwit, A., Harris, N.L., Le Beau, M.M., Hellström-Lindberg, E., Tefferi, A. & Bloomfield, C.D. (2009) The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood, 114, 937-951.
38. Wang, S.E., Narasanna, A., Perez-Torres, M., Xiang, B., Wu, F.Y., Yang, S., Carpenter, G., Gazdar, A.F., Muthuswamy, S.K. & Arteaga, C.L. (2006) HER2 kinase domain mutation results in constitutive phosphorylation and activation of HER2 and EGFR and resistance to EGFR tyrosine kinase inhibitors. Cancer Cell, 10, 25-38.
39. 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.
40. Zinner, R.G., Nemunaitis, J., Eiseman, I., Shin, H.J., Olson, S.C., Christensen, J., Huang, X., Lenehan, P.F., Donato, N.J. & Shin, D.M. (2007) Phase I clinical and pharmacodynamic evaluation of oral CI-1033 in patients with refractory cancer. Clinical Cancer Research, 13, 3006-3014.