Kinome profiling of non-canonical TRAIL signaling reveals RIP1-Src-STAT3-dependent invasion in resistant non-small cell lung cancer cells

Journal of Cell Science

Volumn 125, Issue 19, 2012, Pages 4651-4661

  Azijli, Kaamar ^a,b   Yuvaraj, Saravanan ^a   Peppelenbosch, Maikel P ^c   Würdinger, Thomas ^b,d   Dekker, Henk ^b   Joore, Jos ^c   van Dijk, Evert ^e   Quax, Wim J ^f   Peters, Godefridus J ^b   De Jong, Steven ^a   Kruyt, Frank A E ^a  

^a UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e Pepscan Presto BV   (Netherlands)

^f UNIVERSITY OF GRONINGEN   (Netherlands)

Author keywords

Kinome profiling; Migration; NSCLC; RIP1; Src inhibitors; TRAIL

Indexed keywords

HYBRID PROTEIN; RECEPTOR INTERACTING PROTEIN 140; STAT3 PROTEIN; STEROID RECEPTOR COACTIVATOR 1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

APOPTOSIS; ARTICLE; CANCER CELL; CELL INVASION; CELL MIGRATION; CYTOTOXICITY; ENZYME ACTIVATION; ENZYME INHIBITION; LUNG NON SMALL CELL CANCER; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

APOPTOSIS; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; CELL MOVEMENT; DRUG RESISTANCE, NEOPLASM; ENZYME ACTIVATION; HUMANS; LUNG NEOPLASMS; MODELS, BIOLOGICAL; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEOME; RECEPTOR-INTERACTING PROTEIN SERINE-THREONINE KINASES; RECEPTORS, TNF-RELATED APOPTOSIS-INDUCING LIGAND; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; STAT3 TRANSCRIPTION FACTOR; TNF-RELATED APOPTOSIS-INDUCING LIGAND;

EID: 84872190750     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.109587     Document Type: Article

References (43)

1. Abdulghani, J., Gu, L., Dagvadorj, A., Lutz, J., Leiby, B., Bonuccelli, G., Lisanti, M. P., Zellweger, T., Alanen, K., Mirtti, T. et al. (2008). Stat3 promotes metastatic progression of prostate cancer. Am. J. Pathol. 172, 1717-1728.
2. Bijnsdorp, I. V., Capriotti, F., Kruyt, F. A., Losekoot, N., Fukushima, M., Griffioen, A. W., Thijssen, V. L. and Peters, G. J. (2011). Thymidine phosphorylase in cancer cells stimulates human endothelial cell migration and invasion by the secretion of angiogenic factors. Br. J. Cancer 104, 1185-1192.
3. Boyer, B., Bourgeois, Y. and Poupon, M. F. (2002). Src kinase contributes to the metastatic spread of carcinoma cells. Oncogene 21, 2347-2356.
4. Brummelkamp, T. R., Bernards, R. and Agami, R. (2002). Stable suppression of tumorigenicity by virus-mediated RNA interference. Cancer Cell 2, 243-247.
5. Cursi, S., Rufini, A., Stagni, V., Condò, I., Matafora, V., Bachi, A., Bonifazi, A. P., Coppola, L., Superti-Furga, G., Testi, R. et al. (2006). Src kinase phosphorylates Caspase-8 on Tyr380: a novel mechanism of apoptosis suppression. EMBO J. 25, 1895-1905.
6. Declercq, W., Vanden Berghe, T. and Vandenabeele, P. (2009). RIP kinases at the crossroads of cell death and survival. Cell 138, 229-232.
7. Elrod, H. A., Lin, Y. D., Yue, P., Wang, X., Lonial, S., Khuri, F. R. and Sun, S. Y. (2007). The alkylphospholipid perifosine induces apoptosis of human lung cancer cells requiring inhibition of Akt and activation of the extrinsic apoptotic pathway. Mol. Cancer Ther. 6, 2029-2038.
8. Falschlehner, C., Emmerich, C. H., Gerlach, B. and Walczak, H. (2007). TRAIL signalling: decisions between life and death. Int. J. Biochem. Cell Biol. 39, 1462-1475.
9. Field, J. K. and Duffy, S. W. (2008). Lung cancer screening: the way forward. Br. J. Cancer 99, 557-562.
10. Gallick, G. E. (2004). SRC as a potential therapeutic target in solid tumor oncology. Clin. Adv. Hematol. Oncol. 2, 435-437.
11. Gonzalvez, F. and Ashkenazi, A. (2010). New insights into apoptosis signaling by Apo2L/TRAIL. Oncogene 29, 4752-4765.
12. Guarino, M. (2010). Src signaling in cancer invasion. J. Cell. Physiol. 223, 14-26.
13. Herbst, R. S., Heymach, J. V. and Lippman, S. M. (2008). Lung cancer. N. Engl. J. Med. 359, 1367-1380.
14. Hoogwater, F. J., Nijkamp, M. W., Smakman, N., Steller, E. J., Emmink, B. L., Westendorp, B. F., Raats, D. A., Sprick, M. R., Schaefer, U., Van Houdt, W. J. et al. (2010). Oncogenic K-Ras turns death receptors into metastasis-promoting receptors in human and mouse colorectal cancer cells. Gastroenterology 138, 2357-2367.
15. Ishimura, N., Isomoto, H., Bronk, S. F. and Gores, G. J. (2006). Trail induces cell migration and invasion in apoptosis-resistant cholangiocarcinoma cells. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G129-G136.
16. Janmaat, M. L., Kruyt, F. A., Rodriguez, J. A. and Giaccone, G. (2003). Response to epidermal growth factor receptor inhibitors in non-small cell lung cancer cells: limited antiproliferative effects and absence of apoptosis associated with persistent activity of extracellular signal-regulated kinase or Akt kinase pathways. Clin. Cancer Res. 9, 2316-2326.
17. Jemal, A., Siegel, R., Xu, J. and Ward, E. (2010). Cancer statistics, 2010. CA Cancer J. Clin. 60, 277-300.
18. Jin, Z. and El-Deiry, W. S. (2006). Distinct signaling pathways in TRAIL- versus tumor necrosis factor-induced apoptosis. Mol. Cell. Biol. 26, 8136-8148.
19. Johnson, F. M., Saigal, B., Talpaz, M. and Donato, N. J. (2005). Dasatinib (BMS-354825) tyrosine kinase inhibitor suppresses invasion and induces cell cycle arrest and apoptosis of head and neck squamous cell carcinoma and non-small cell lung cancer cells. Clin. Cancer Res. 11, 6924-6932.
20. Kalluri, R. and Weinberg, R. A. (2009). The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119, 1420-1428.
21. Kandasamy, K. and Srivastava, R. K. (2002). Role of the phosphatidylinositol 39-kinase/PTEN/Akt kinase pathway in tumor necrosis factor-related apoptosis-inducing ligand-induced apoptosis in non-small cell lung cancer cells. Cancer Res. 62, 4929-4937.
22. Mazurenko, N. N., Kogan, E. A., Zborovskaya, I. B. and Kisseljov, F. L. (1992). Expression of pp60c-src in human small cell and non-small cell lung carcinomas. Eur. J. Cancer 28, 372-377.
23. Meylan, E. and Tschopp, J. (2005). The RIP kinases: crucial integrators of cellular stress. Trends Biochem. Sci. 30, 151-159.
24. Mukhopadhyay, U. K., Mooney, P., Jia, L., Eves, R., Raptis, L. and Mak, A. S. (2010). Doubles game: Src-Stat3 versus p53-PTEN in cellular migration and invasion. Mol. Cell. Biol. 30, 4980-4995.
25. Newsom-Davis, T., Prieske, S. and Walczak, H. (2009). Is TRAIL the holy grail of cancer therapy? Apoptosis 14, 607-623.
26. Parikh, K., Peppelenbosch, M. P. and Ritsema, T. (2009). Kinome profiling using peptide arrays in eukaryotic cells. Methods Mol. Biol. 527, 269-280.
27. Purnell, P. R., Mack, P. C., Tepper, C. G., Evans, C. P., Green, T. P., Gumerlock, P. H., Lara, P. N., Gandara, D. R., Kung, H. J. and Gautschi, O. (2009). The Src inhibitor AZD0530 blocks invasion and may act as a radiosensitizer in lung cancer cells. J. Thorac. Oncol. 4, 448-454.
28. Reis, C. R., van der Sloot, A. M., Natoni, A., Szegezdi, E., Setroikromo, R., Meijer, M., Sjollema, K., Stricher, F., Cool, R. H., Samali, A. et al. (2010). Rapid and efficient cancer cell killing mediated by high-affinity death receptor homotrimerizing TRAIL variants. Cell Death Dis. 1, e83.
29. Snyder, M., Huang, X. Y. and Zhang, J. J. (2011). Signal transducers and activators of transcription 3 (STAT3) directly regulates cytokine-induced fascin expression and is required for breast cancer cell migration. J. Biol. Chem. 286, 38886-38893.
30. Song, J. H., Tse, M. C., Bellail, A., Phuphanich, S., Khuri, F., Kneteman, N. M. and Hao, C. (2007). Lipid rafts and nonrafts mediate tumor necrosis factor related apoptosis-inducing ligand induced apoptotic and nonapoptotic signals in non small cell lung carcinoma cells. Cancer Res. 67, 6946-6955.
31. Song, J. J., Kim, J. H., Sun, B. K., Alcala, M. A., Jr, Bartlett, D. L. and Lee, Y. J. (2010). c-Cbl acts as a mediator of Src-induced activation of the PI3K-Akt signal transduction pathway during TRAIL treatment. Cell. Signal. 22, 377-385.
32. Spierings, D. C., de Vries, E. G., Timens, W., Groen, H. J., Boezen, H. M. and de Jong, S. (2003). Expression of TRAIL and TRAIL death receptors in stage III nonsmall cell lung cancer tumors. Clin. Cancer Res. 9, 3397-3405.
33. Stegehuis, J. H., de Wilt, L. H., de Vries, E. G., Groen, H. J., de Jong, S. and Kruyt, F. A. (2010). TRAIL receptor targeting therapies for non-small cell lung cancer: current status and perspectives. Drug Resist. Updat. 13, 2-15.
34. Teng, T. S., Lin, B., Manser, E., Ng, D. C. and Cao, X. (2009). Stat3 promotes directional cell migration by regulating Rac1 activity via its activator betaPIX. J. Cell Sci. 122, 4150-4159.
35. Trauzold, A., Siegmund, D., Schniewind, B., Sipos, B., Egberts, J., Zorenkov, D., Emme, D., Röder, C., Kalthoff, H. and Wajant, H. (2006). TRAIL promotes metastasis of human pancreatic ductal adenocarcinoma. Oncogene 25, 7434-7439.
36. van Baal, J. W., Diks, S. H., Wanders, R. J., Rygiel, A. M., Milano, F., Joore, J., Bergman, J. J., Peppelenbosch, M. P. and Krishnadath, K. K. (2006). Comparison of kinome profiles of Barrett's esophagus with normal squamous esophagus and normal gastric cardia. Cancer Res. 66, 11605-11612.
37. van der Sloot, A. M., Tur, V., Szegezdi, E., Mullally, M. M., Cool, R. H., Samali, A., Serrano, L. and Quax, W. J. (2006). Designed tumor necrosis factor-related apoptosis-inducing ligand variants initiating apoptosis exclusively via the DR5 receptor. Proc. Natl. Acad. Sci. USA 103, 8634-8639.
38. van Leuken, R., Clijsters, L., van Zon, W., Lim, D., Yao, X., Wolthuis, R. M., Yaffe, M. B., Medema, R. H. and van Vugt, M. A. (2009). Polo-like kinase-1 controls Aurora A destruction by activating APC/C-Cdh1. PLoS ONE 4, e5282.
39. van Nimwegen, M. J. and van de Water, B. (2007). Focal adhesion kinase: a potential target in cancer therapy. Biochem. Pharmacol. 73, 597-609.
40. Van Schaeybroeck, S., Kelly, D. M., Kyula, J., Stokesberry, S., Fennell, D. A., Johnston, P. G. and Longley, D. B. (2008). Src and ADAM-17-mediated shedding of transforming growth factor-alpha is a mechanism of acute resistance to TRAIL. Cancer Res. 68, 8312-8321.
41. Varfolomeev, E., Maecker, H., Sharp, D., Lawrence, D., Renz, M., Vucic, D. and Ashkenazi, A. (2005). Molecular determinants of kinase pathway activation by Apo2 ligand/tumor necrosis factor-related apoptosis-inducing ligand. J. Biol. Chem. 280, 40599-40608.
42. Voortman, J., Resende, T. P., Abou El Hassan, M. A., Giaccone, G. and Kruyt, F. A. (2007). TRAIL therapy in non-small cell lung cancer cells: sensitization to death receptor-mediated apoptosis by proteasome inhibitor bortezomib. Mol. Cancer Ther. 6, 2103-2112.
43. Yarrow, J. C., Perlman, Z. E., Westwood, N. J. and Mitchison, T. J. (2004). A highthroughput cell migration assay using scratch wound healing, a comparison of imagebased readout methods. BMC Biotechnol. 4, 21.