Proteomics and pathway analysis identifies JNK signaling as critical for high linear energy transfer radiation-induced apoptosis in non-small lung cancer cells

Molecular and Cellular Proteomics

Volumn 8, Issue 5, 2009, Pages 1117-1129

  Ståhl, Sara ^a   Fung, Eva ^b   Adams, Christopher ^b   Lengqvist, Johan ^a   Mörk, Birgitta ^a   Stenerlöw, Bo ^c   Lewensohn, Rolf ^a   Lehtiöf, Janne ^a   Zubarev, Roman ^b   Viktorsson, Kristina ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UPPSALA UNIVERSITY   (Sweden)

^c UPPSALA UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

JANUS KINASE;

APOPTOSIS; ARTICLE; CANCER RADIOTHERAPY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IONIZING RADIATION; LINEAR ENERGY TRANSFER; LIQUID CHROMATOGRAPHY; LUNG NON SMALL CELL CANCER; MASS SPECTROMETRY; NANOANALYSIS; PRIORITY JOURNAL; PROTEOMICS; SIGNAL TRANSDUCTION;

APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CASPASE 3; CELL LINE, TUMOR; COMPUTATIONAL BIOLOGY; ENZYME ACTIVATION; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LINEAR ENERGY TRANSFER; LUNG NEOPLASMS; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; PROTEOMICS; REPRODUCIBILITY OF RESULTS; TIME FACTORS;

EID: 67449088495     PISSN: 15359476     EISSN: None     Source Type: Journal    
DOI: 10.1074/mcp.M800274-MCP200     Document Type: Article

References (46)

1. Turesson, I., Carlsson, J., Brahme, A., Glimelius, B., Zackrisson, B., and Stenerlow, B. (2003) Biological response to radiation therapy. Acta Oncol. 42, 92-106 (Pubitemid 36570774)
2. Schulz-Ertner, D., Jakel, O., and Schlegel, W. (2006) Radiation therapy with charged particles. Semin. Radiat. Oncol. 16, 249-259 (Pubitemid 44436966)
3. Joseph, B., Ekedahl, J., Lewensohn, R., Marchetti, P., Formstecher, P., and Zhivotovsky, B. (2001) Defective caspase-3 relocalization in non-small cell lung carcinoma. Oncogene 20, 2877-2888 (Pubitemid 33027755)
4. Joseph, B., Marchetti, P., Formstecher, P., Kroemer, G., Lewensohn, R., and Zhivotovsky, B. (2002) Mitochondrial dysfunction is an essential step for killing of non-small cell lung carcinomas resistant to conventional treatment. Oncogene 21, 65-77 (Pubitemid 34076379)
5. Sirzen, F., Zhivotovsky, B., Nilsson, A., Bergh, J., and Lewensohn, R. (1998) Spontaneous and radiation-induced apoptosis in lung carcinoma cells with different intrinsic radiosensitivities. Anticancer Res. 18, 695-699 (Pubitemid 28239582)
6. Viktorsson, K., Ekedahl, J., Lindebro, M. C., Lewensohn, R., Zhivotovsky, B., Linder, S., and Shoshan, M. C. (2003) Defective stress kinase and Bak activation in response to ionizing radiation but not cisplatin in a non- small cell lung carcinoma cell line. Exp. Cell Res. 289, 256-264 (Pubitemid 37117411)
7. Viktorsson, K., Lewensohn, R., and Zhivotovsky, B. (2005) Apoptotic pathways and therapy resistance in human malignancies. Adv. Cancer Res. 94, 143-196 (Pubitemid 41213078)
8. Austin-Seymour, M., Griffin, T., Laramore, G., Maor, M., and Parker, R. (1989) High-LET radiation therapy of non-small cell lung cancer. Chest 96, 72S-73S (Pubitemid 19173103)
9. Nakano, T., Suzuki, Y., Ohno, T., Kato, S., Suzuki, M., Morita, S., Sato, S., Oka, K., and Tsujii, H. (2006) Carbon beam therapy overcomes the radiation resistance of uterine cervical cancer originating from hypoxia. Clin. Cancer Res. 12, 2185-2190
10. Tsujii, H., Mizoe, J. E., Kamada, T., Baba, M., Kato, S., Kato, H., Tsuji, H., Yamada, S., Yasuda, S., Ohno, T., Yanagi, T., Hasegawa, A., Sugawara, T., Ezawa, H., Kandatsu, S., Yoshikawa, K., Kishimoto, R., and Miyamoto, T. (2004) Overview of clinical experiences on carbon ion radiotherapy at NIRS. Radiother. Oncol. 73, Suppl. 2, S41-S49
11. Stenerlow, B., Carlsson, J., Blomquist, E., and Erixon, K. (1994) Clonogenic cell survival and rejoining of DNA double-strand breaks: comparisons between three cell lines after photon or He ion irradiation. Int. J. Radiat. Biol. 65, 631-639 (Pubitemid 24218774)
12. Goodhead, D. T. (1994) Initial events in the cellular effects of ionizing radiations: clustered damage in DNA. Int. J. Radiat. Biol. 65, 7-17 (Pubitemid 24063524)
13. Radulescu, I., Elmroth, K., and Stenerlow, B. (2004) Chromatin organization contributes to non-randomly distributed double-strand breaks after exposure to high-LET radiation. Radiat. Res. 161, 1-8 (Pubitemid 38018718)
14. Davis, R. J. (2000) Signal transduction by the JNK group of MAP kinases. Cell 103, 239-252
15. Dent, P., Yacoub, A., Fisher, P. B., Hagan, M. P., and Grant, S. (2003) MAPK pathways in radiation responses. Oncogene 22, 5885-5896 (Pubitemid 37176709)
16. Sanchez-Perez, I., Murguia, J. R., and Perona, R. (1998) Cisplatin induces a persistent activation of JNK that is related to cell death. Oncogene 16, 533-540 (Pubitemid 28062081)
17. Tournier, C., Hess, P., Yang, D. D., Xu, J., Turner, T. K., Nimnual, A., Bar-Sagi, D., Jones, S. N., Flavell, R. A., and Davis, R. J. (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288, 870-874 (Pubitemid 30257738)
18. Brozovic, A., Fritz, G., Christmann, M., Zisowsky, J., Jaehde, U., Osmak, M., and Kaina, B. (2004) Long-term activation of SAPK/JNK, p38 kinase and fas-L expression by cisplatin is attenuated in human carcinoma cells that acquired drug resistance. Int. J. Cancer 112, 974-985 (Pubitemid 39507003)
19. Chen, Y. R., Wang, X., Templeton, D., Davis, R. J., and Tan, T. H. (1996) The role of c-Jun N-terminal kinase (JNK) in apoptosis induced by ultraviolet C and γ radiation. Duration of JNK activation may determine cell death and proliferation. J. Biol. Chem. 271, 31929-31936 (Pubitemid 26422216)
20. Choi, S. Y., Kim, M. J., Kang, C. M., Bae, S., Cho, C. K., Soh, J. W., Kim, J. H., Kang, S., Chung, H. Y., Lee, Y. S., and Lee, S. J. (2006) Activation of Bak and Bax through c-abl-protein kinase CS-p38 MAPK signaling in response to ionizing radiation in human non-small cell lung cancer cells. J. Biol. Chem. 281, 7049-7059 (Pubitemid 43847468)
21. + lymphocytes activated with staphylococcal enterotoxin B, and those malignantly transformed by Marek's disease virus. J. Proteome Res. 7, 2380-2387
22. Ralhan, R., Desouza, L. V., Matta, A., Chandra Tripathi, S., Ghanny, S., Datta Gupta, S., Bahadur, S., and Siu, K. W. (2008) Discovery and verification of head-and-neck cancer biomarkers by differential protein expression analysis using iTRAQ labeling and multidimensional liquid chromatography and tandem mass spectrometry. Mol. Cell. Proteomics 7, 1162-1173 (Pubitemid 351943962)
23. Zubarev, R. A., Nielsen, M. L., Fung, E. M., Savitski, M. M., Kel-Margoulis, O., Wingender, E., and Kel, A. (2008) Identification of dominant signaling pathways from proteomics expression data. J. Proteomics 1, 89-96 (Pubitemid 351711646)
24. Kel, A., Voss, N., Jauregui, R., Kel-Margoulis, O., and Wingender, E. (2006) Beyond microarrays: Finding key transcription factors controlling signal transduction pathways. BMC Bioinformatics 7, Suppl. 2, S13 (Pubitemid 46442966)
25. Krull, M., Pistor, S., Voss, N., Kel, A., Reuter, I., Kronenberg, D., Michael, H., Schwarzer, K., Potapov, A., Choi, C., Kel-Margoulis, O., and Wingender, E. (2006) TRANSPATH: an information resource for storing and visualizing signaling pathways and their pathological aberrations. Nucleic Acids Res. 34, D546-D551
26. Wingender, E. (2008) The TRANSFAC project as an example of framework technology that supports the analysis of genomic regulation. Brief. Bioinform. 9, 326-332 (Pubitemid 351894493)
27. Qi, W., Liu, X., Qiao, D., and Martinez, J. D. (2005) Isoform-specific expression of 14-3-3 proteins in human lung cancer tissues. Int. J. Cancer 113, 359-363 (Pubitemid 40038701)
28. Kharbanda, S., Pandey, P., Ren, R., Mayer, B., Zon, L., and Kufe, D. (1995) c-Abl activation regulates induction of the SEK1/stress-activated protein kinase pathway in the cellular response to 1-β-D-arabinofuranosylcy tosine. J. Biol. Chem. 270, 30278-30281 (Pubitemid 3022820)
29. Kharbanda, S., Pandey, P., Yamauchi, T., Kumar, S., Kaneki, M., Kumar, V., Bharti, A., Yuan, Z. M., Ghanem, L., Rana, A., Weichselbaum, R., Johnson, G., and Kufe, D. (2000) Activation of MEK kinase 1 by the c-Abl protein tyrosine kinase in response to DNA damage. Mol. Cell. Biol. 20, 4979-4989
30. Kharbanda, S., Ren, R., Pandey, P., Shafman, T. D., Feller, S. M., Weichselbaum, R. R., and Kufe, D. W. (1995) Activation of the c-Abl tyrosine kinase in the stress response to DNA-damaging agents. Nature 376, 785-788
31. Kharbanda, S., Yuan, Z. M., Weichselbaum, R., and Kufe, D. (1998) Determination of cell fate by c-Abl activation in the response to DNA damage. Oncogene 17, 3309-3318 (Pubitemid 29043983)
32. Yoshida, K. (2007) Regulation for nuclear targeting of the Abl tyrosine kinase in response to DNA damage. Adv. Exp. Med. Biol. 604, 155-165
33. Yoshida, K., and Miki, Y. (2005) Enabling death by the Abl tyrosine kinase: mechanisms for nuclear shuttling of c-Abl in response to DNA damage. Cell Cycle 4, 777-779 (Pubitemid 41353828)
34. Yoshida, K., Yamaguchi, T., Natsume, T., Kufe, D., and Miki, Y. (2005) JNK phosphorylation of 14-3-3 proteins regulates nuclear targeting of c-Abl in the apoptotic response to DNA damage. Nat. Cell 7, 278-285 (Pubitemid 40331129)
35. Belka, C., Heinrich, V., Marini, P., Faltin, H., Schulze-Osthoff, K., Bamberg, M., and Budach, W. (1999) Ionizing radiation and the activation of caspase-8 in highly apoptosis-sensitive lymphoma cells. Int. J. Radiat. Biol. 75, 1257-1264 (Pubitemid 29500008)
36. Belka, C., Marini, P., Lepple-Wienhues, A., Budach, W., Jekle, A., Los, M., Lang, F., Schulze-Osthoff, K., Gulbins, E., and Bamberg, M. (1999) The tyrosine kinase lck is required for CD95-independent caspase-8 activation and apoptosis in response to ionizing radiation. Oncogene 18, 4983-4992 (Pubitemid 29425305)
37. Kuwabara, M., Takahashi, K., and Inanami, O. (2003) Induction of apoptosis through the activation of SAPK/JNK followed by the expression of death receptor Fas in X-irradiated cells. J Radiat. Res. (Tokyo) 44, 203-209 (Pubitemid 38738723)
38. Li, X. R., Chong, A. S., Wu, J., Roebuck, K. A., Kumar, A., Parrillo, J. E., Rapp, U. R., Kimberly, R. P., Williams, J. W., and Xu, X. (1999) Transcriptional regulation of Fas gene expression by GA-binding protein and AP-1 in T cell antigen receptor-CD3 complex-stimulated T cells. J. Biol. Chem. 274, 35203-35210 (Pubitemid 129509578)
39. Jia, L., Yu, W., Wang, P., Li, J., Sanders, B. G., and Kline, K. (2008) Critical roles for JNK, c-Jun, and Fas/FasL signaling in vitamin E analog-induced apoptosis in human prostate cancer cells. Prostate 68, 427-441 (Pubitemid 351342648)
40. Cosaceanu, D., Budiu, R. A., Carapancea, M., Castro, J., Lewensohn, R., and Drieu, A. (2007) Ionizing radiation activates IGF-1R triggering a cytoprotective signaling by interfering with Ku-DNA binding and by modulating Ku86 expression via a p38 kinase-dependent mechanism. Oncogene 26, 2423-2434 (Pubitemid 46597267)
41. Hemstrom, T. H., Joseph, B., Schulte, G., Lewensohn, R., and Zhivotovsky, B. (2005) PKC 412 sensitizes U1810 non-small cell lung cancer cells to DNA damage. Exp. Cell Res. 305, 200-213 (Pubitemid 40380666)
42. Hemstrom, T. H., Sandstrom, M., and Zhivotovsky, B. (2006) Inhibitors of the PI3-kinase/Akt pathway induce mitotic catastrophe in non-small cell lung cancer cells. Int. J. Cancer 119, 1028-1038 (Pubitemid 44116909)
43. Benhar, M., Dalyot, I., Engelberg, D., and Levitzki, A. (2001) Enhanced ROS production in oncogenically transformed cells potentiates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase activation and sensitization to genotoxic stress. Mol. Cell. Biol. 21, 6913-6926 (Pubitemid 32911252)
44. Chattopadhyay, S., Machado-Pinilla, R., Manguan-Garcia, C., Belda-Iniesta, C., Moratilla, C., Cejas, P., Fresno-Vara, J. A., de Castro-Carpeno, J., Casado, E., Nistal, M., Gonzalez-Baron, M., and Perona, R. (2006) MKP1/CL100 controls tumor growth and sensitivity to cisplatin in non- small-cell lung cancer. Oncogene 25, 3335-3345
45. Marinov, M., Fischer, B., and Arcaro, A. (2007) Targeting mTOR signaling in lung cancer. Crit. Rev. Oncol. Hematol. 63, 172-182 (Pubitemid 46990916)
46. Gollob, J. A., Wilhelm, S., Carter, C., and Kelley, S. L. (2006) Role of Raf kinase in cancer therapeutic potential of targeting the Raf/MEK/ERK signal transduction pathway. Semin. Oncol. 33, 392-406 (Pubitemid 44142735)