Multikinase inhibitor sorafenib exerts cytocidal efficacy against Non-Hodgkin lymphomas associated with inhibition of MAPK14 and AKT phosphorylation

British Journal of Haematology

Volumn 152, Issue 4, 2011, Pages 401-412

  Chapuy, Bjoern ^a   Schuelper, Nikolai ^a   Panse, Melanie ^a   Dohm, Andrea ^a   Hand, Elisabeth ^a   Schroers, Roland ^a   Truemper, Lorenz ^a   Wulf, Gerald G ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

AKT; Lymphoma; MAPK14; Multikinase inhibition; Sorafenib

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 14; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN KINASE B; RAF PROTEIN; SORAFENIB;

ARTICLE; B CELL LYMPHOMA; CELL PROLIFERATION; CELL SURVIVAL; CELL SUSPENSION; CELL VIABILITY; CLONOGENESIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DISEASE ACTIVITY; DRUG CYTOTOXICITY; DRUG TARGETING; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOMA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL LYMPHOMA;

ANTINEOPLASTIC AGENTS; APOPTOSIS; BENZENESULFONATES; CELL CYCLE; CELL DEATH; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; HUMANS; LYMPHOMA, NON-HODGKIN; MITOGEN-ACTIVATED PROTEIN KINASE 14; PHOSPHORYLATION; PROTEIN KINASE INHIBITORS; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; TUMOR STEM CELL ASSAY;

EID: 78851468826     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/j.1365-2141.2010.08526.x     Document Type: Article

References (35)

1. Abramson, J.S., Chen, W., Juszczynski, P., Takahashi, H., Neuberg, D., Kutok, J.L., Takeyama, K. & Shipp, M.A. (2009) The heat shock protein 90 inhibitor IPI-504 induces apoptosis of AKT-dependent diffuse large B-cell lymphomas. British Journal of Haematology, 144, 358-366.
2. Baohua, Y., Xiaoyan, Z., Tiecheng, Z., Tao, Q. & Daren, S. (2008) Mutations of the PIK3CA gene in diffuse large B cell lymphoma. Diagnostic Molecular Pathology, 17, 159-165.
3. Chen, L., Monti, S., Juszczynski, P., Daley, J., Chen, W., Witzig, T.E., Habermann, T.M., Kutok, J.L. & Shipp, M.A. (2008) SYK-dependent tonic B-cell receptor signaling is a rational treatment target in diffuse large B-cell lymphoma. Blood, 111, 2230-2237.
4. Coiffier, B., Lepage, E., Briere, J., Herbrecht, R., Tilly, H., Bouabdallah, R., Morel, P., Van Den Neste, E., Salles, G., Gaulard, P., Reyes, F., Lederlin, P. & Gisselbrecht, C. (2002) CHOP chemotherapy plus rituximab compared with CHOP alone in elderly patients with diffuse large-B-cell lymphoma. New England Journal of Medicine, 346, 235-242.
5. Datta, S.R., Brunet, A. & Greenberg, M.E. (1999) Cellular survival: a play in three Akts. Genes and Development, 13, 2905-2927.
6. Denizot, F. & Lang, R. (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. Journal of Immunological Methods, 89, 271-277.
7. Druker, B.J., Guilhot, F., O'Brien, S.G., Gathmann, I., Kantarjian, H., Gattermann, N., Deininger, M.W., Silver, R.T., Goldman, J.M., Stone, R.M., Cervantes, F., Hochhaus, A., Powell, B.L., Gabrilove, J.L., Rousselot, P., Reiffers, J., Cornelissen, J.J., Hughes, T., Agis, H., Fischer, T., Verhoef, G., Shepherd, J., Saglio, G., Gratwohl, A., Nielsen, J.L., Radich, J.P., Simonsson, B., Taylor, K., Baccarani, M., So, C., Letvak, L. & Larson, R.A. (2006) Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. New England Journal of Medicine, 355, 2408-2417.
8. Egberts, F., Kahler, K.C., Livingstone, E. & Hauschild, A. (2008) Metastatic melanoma: scientific rationale for sorafenib treatment and clinical results. Onkologie, 31, 398-403.
9. Elenitoba-Johnson, K.S., Jenson, S.D., Abbott, R.T., Palais, R.A., Bohling, S.D., Lin, Z., Tripp, S., Shami, P.J., Wang, L.Y., Coupland, R.W., Buckstein, R., Perez-Ordonez, B., Perkins, S.L., Dube, I.D. & Lim, M.S. (2003) Involvement of multiple signaling pathways in follicular lymphoma transformation: p38-mitogen-activated protein kinase as a target for therapy. Proceedings of the National Academy of Sciences of the United States of America, 100, 7259-7264.
10. Fillmore, G.C., Wang, Q., Carey, M.J., Kim, C.H., Elenitoba-Johnson, K.S. & Lim, M.S. (2005) Expression of Akt (protein kinase B) and its isoforms in malignant lymphomas. Leukaemia & Lymphoma, 46, 1765-1773.
11. Friedberg, J.W., Sharman, J., Sweetenham, J., Johnston, P.B., Vose, J.M., Lacasce, A., Schaefer-Cutillo, J., De Vos, S., Sinha, R., Leonard, J.P., Cripe, L.D., Gregory, S.A., Sterba, M.P., Lowe, A.M., Levy, R. & Shipp, M.A. (2010): Inhibition of Syk with fostamatinib disodium has significant clinical activity in non-Hodgkin lymphoma and chronic lymphocytic leukemia. Blood, 115(13), 2578-85.
12. Gisselbrecht, C. (2008) Use of rituximab in diffuse large B-cell lymphoma in the salvage setting. British Journal of Haematology, 143, 607-621.
13. Hui, L., Bakiri, L., Stepniak, E. & Wagner, E.F. (2007) p38alpha: a suppressor of cell proliferation and tumorigenesis. Cell Cycle, 6, 2429-2433.
14. Kloos, R.T., Ringel, M.D., Knopp, M.V., Hall, N.C., King, M., Stevens, R., Liang, J., Wakely, Jr, P.E., Vasko, V.V., Saji, M., Rittenberry, J., Wei, L., Arbogast, D., Collamore, M., Wright, J.J., Grever, M. & Shah, M.H. (2009) Phase II trial of sorafenib in metastatic thyroid cancer. Journal of Clinical Oncology, 27, 1675-1684.
15. Kurosu, T., Takahashi, Y., Fukuda, T., Koyama, T., Miki, T. & Miura, O. (2005) p38 MAP kinase plays a role in G2 checkpoint activation and inhibits apoptosis of human B cell lymphoma cells treated with etoposide. Apoptosis, 10, 1111-1120.
16. Lin, Z., Crockett, D.K., Jenson, S.D., Lim, M.S. & Elenitoba-Johnson, K.S. (2004) Quantitative proteomic and transcriptional analysis of the response to the p38 mitogen-activated protein kinase inhibitor SB203580 in transformed follicular lymphoma cells. Molecular & Cellular Proteomics, 3, 820-833.
17. Matusali, G., Arena, G., De, L.A., Di, R.L. & Mattia, E. (2009) Inhibition of p38 MAP kinase pathway induces apoptosis and prevents Epstein Barr virus reactivation in Raji cells exposed to lytic cycle inducing compounds. Molecular cancer, 8, 18.
18. Molina, A.M. & Motzer, R.J. (2008) Current algorithms and prognostic factors in the treatment of metastatic renal cell carcinoma. Clinical Genitourinary Cancer, 6, s7-s13.
19. Monti, S., Savage, K.J., Kutok, J.L., Feuerhake, F., Kurtin, P., Mihm, M., Wu, B., Pasqualucci, L., Neuberg, D., Aguiar, R.C., Dal, C.P., Ladd, C., Pinkus, G.S., Salles, G., Harris, N.L., Dalla-Favera, R., Habermann, T.M., Aster, J.C., Golub, T.R. & Shipp, M.A. (2005) Molecular profiling of diffuse large B-cell lymphoma identifies robust subtypes including one characterized by host inflammatory response. Blood, 105, 1851-1861.
20. Nicoletti, I., Migliorati, G., Pagliacci, M.C., Grignani, F. & Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. Journal of Immunological Methods, 139, 271-279.
21. Petrelli, A. & Valabrega, G. (2009) Multitarget drugs: the present and the future of cancer therapy. Expert Opinion on Pharmacotherapy, 10, 589-600.
22. Pfreundschuh, M., Trumper, L., Osterborg, A., Pettengell, R., Trneny, M., Imrie, K., Ma, D., Gill, D., Walewski, J., Zinzani, P.L., Stahel, R., Kvaloy, S., Shpilberg, O., Jaeger, U., Hansen, M., Lehtinen, T., Lopez-Guillermo, A., Corrado, C., Scheliga, A., Milpied, N., Mendila, M., Rashford, M., Kuhnt, E. & Loeffler, M. (2006) CHOP-like chemotherapy plus rituximab versus CHOP-like chemotherapy alone in young patients with good-prognosis diffuse large-B-cell lymphoma: a randomised controlled trial by the MabThera International Trial (MInT) Group. The Lancet Oncology, 7, 379-391.
23. Reinhardt, H.C., Aslanian, A.S., Lees, J.A. & Yaffe, M.B. (2007) p53-deficient cells rely on ATM- and ATR-mediated checkpoint signaling through the p38MAPK/MK2 pathway for survival after DNA damage. Cancer Cell, 11, 175-189.
24. 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.
25. Uddin, S., Hussain, A.R., Al-Hussein, K.A., Manogaran, P.S., Wickrema, A., Gutierrez, M.I. & Bhatia, K.G. (2005) Inhibition of phosphatidylinositol 3'-kinase/AKT signaling promotes apoptosis of primary effusion lymphoma cells. Clinical Cancer Research, 11, 3102-3108.
26. Uddin, S., Hussain, A.R., Siraj, A.K., Manogaran, P.S., Al-Jomah, N.A., Moorji, A., Atizado, V., Al-Dayel, F., Belgaumi, A., El-Solh, H., Ezzat, A., Bavi, P. & Al-Kuraya, K.S. (2006) Role of phosphatidylinositol 3'-kinase/AKT pathway in diffuse large B-cell lymphoma survival. Blood, 108, 4178-4186.
27. Wagner, E.F. & Nebreda, A.R. (2009) Signal integration by JNK and p38 MAPK pathways in cancer development. Nature Reviews Cancer, 9, 537-549.
28. Wendel, H.G., De, S.E., Fridman, J.S., Malina, A., Ray, S., Kogan, S., Cordon-Cardo, C., Pelletier, J. & Lowe, S.W. (2004) Survival signalling by Akt and eIF4E in oncogenesis and cancer therapy. Nature, 428, 332-337.
29. Wilhelm, S. & Chien, D.S. (2002) BAY 43-9006: preclinical data. Current Pharmaceutical Design, 8, 2255-2257.
30. Wilhelm, S.M., Carter, C., Tang, L., Wilkie, D., McNabola, A., Rong, H., Chen, C., Zhang, X., Vincent, P., McHugh, M., Cao, Y., Shujath, J., Gawlak, S., Eveleigh, D., Rowley, B., Liu, L., Adnane, L., Lynch, M., Auclair, D., Taylor, I., Gedrich, R., Voznesensky, A., Riedl, B., Post, L.E., Bollag, G. & Trail, P.A. (2004) BAY 43-9006 exhibits broad spectrum oral antitumor activity and targets the RAF/MEK/ERK pathway and receptor tyrosine kinases involved in tumor progression and angiogenesis. Cancer Research, 64, 7099-7109.
31. Wilhelm, S.M., Adnane, L., Newell, P., Villanueva, A., Llovet, J.M. & Lynch, M. (2008) Preclinical overview of sorafenib, a multikinase inhibitor that targets both Raf and VEGF and PDGF receptor tyrosine kinase signaling. Molecular Cancer Therapeutics, 7, 3129-3140.
32. Yang, F., Van Meter, T.E., Buettner, R., Hedvat, M., Liang, W., Kowolik, C.M., Mepani, N., Mirosevich, J., Nam, S., Chen, M.Y., Tye, G., Kirschbaum, M. & Jove, R. (2008) Sorafenib inhibits signal transducer and activator of transcription 3 signaling associated with growth arrest and apoptosis of medulloblastomas. Molecular Cancer Therapeutics, 7, 3519-3526.
33. Yu, C., Friday, B.B., Lai, J.P., Yang, L., Sarkaria, J., Kay, N.E., Carter, C.A., Roberts, L.R., Kaufmann, S.H. & Adjei, A.A. (2006) Cytotoxic synergy between the multikinase inhibitor sorafenib and the proteasome inhibitor bortezomib in vitro: induction of apoptosis through Akt and c-Jun NH2-terminal kinase pathways. Molecular Cancer Therapeutics, 5, 2378-2387.
34. Zhang, W., Konopleva, M., Shi, Y.X., McQueen, T., Harris, D., Ling, X., Estrov, Z., Quintas-Cardama, A., Small, D., Cortes, J. & Andreeff, M. (2008a) Mutant FLT3: a direct target of sorafenib in acute myelogenous leukemia. Journal of the National Cancer Institute, 100, 184-198.
35. Zhang, W., Konopleva, M., Ruvolo, V.R., McQueen, T., Evans, R.L., Bornmann, W.G., McCubrey, J., Cortes, J. & Andreeff, M. (2008b) Sorafenib induces apoptosis of AML cells via Bim-mediated activation of the intrinsic apoptotic pathway. Leukemia, 22, 808-818.