Importance of PKCδ signaling in fractionatedradiation-induced expansion of glioma-initiating cells and resistance to cancer treatment

Journal of Cell Science

Volumn 124, Issue 18, 2011, Pages 3084-3094

  Kim, Min Jung ^a,b   Kim, Rae Kwon ^a   Yoon, Chang Hwan ^a   An, Sungkwan ^c   Hwang, Sang Gu ^d   Suh, Yongjoon ^a   Park, Myung Jin ^d   Chung, Hee Young ^a   Kim, In Gyu ^b   Lee, Su Jae ^a  

^a Hanyang University   (South Korea)

^b Korea Atomic Energy Research Institute   (South Korea)

^c Konkuk University   (South Korea)

^d Korea Institute of Radiation and Medical Science   (South Korea)

Author keywords

ABL; Fractionated radiation; Glioma stem like cells; PKC ; Resistance to cancer treatments

Indexed keywords

CD133 ANTIGEN; CELL MARKER; PROTEIN KINASE C DELTA; SMALL INTERFERING RNA;

ABELSON MURINE LEUKEMIA ONCOVIRUS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER STEM CELL; CANCER THERAPY; CELL EXPANSION; CELL POPULATION; ENZYME ACTIVITY; FEMALE; GENE SILENCING; GLIOMA CELL; HUMAN; HUMAN CELL; INTRACELLULAR SIGNALING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; VIRUS ONCOGENE;

ANIMALS; ANTIGENS, CD; BRAIN NEOPLASMS; CELL GROWTH PROCESSES; CELL LINE, TUMOR; DOSE FRACTIONATION; DRUG RESISTANCE, NEOPLASM; GLIOMA; GLYCOPROTEINS; HUMANS; MICE; MICE, NUDE; NEOPLASM TRANSPLANTATION; NEOPLASTIC STEM CELLS; ONCOGENE PROTEINS V-ABL; PEPTIDES; PROTEIN KINASE C-DELTA; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TUMOR BURDEN;

MURINAE;

EID: 80054011693     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.080119     Document Type: Article

References (41)

1. Alonso-Escolano, D., Medina, C., Cieslik, K., Radomski, A., Jurasz, P., Santos-Martinez, M. J., Jiffar, T., Ruvolo, P. and Radomski, M. W. (2006). Protein kinase C delta mediates platelet-induced breast cancer cell invasion. J. Pharmacol. Exp. Ther. 318, 373-380.
2. Bao, S., Wu, Q., McLendon, R. E., Hao, Y., Shi, Q., Hjelmeland, A. B., Dewhirst, M. W., Bigner, D. D. and Rich, J. N. (2006). Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760.
3. Beier, D., Hau, P., Proescholdt, M., Lohmeier, A., Wischhusen, J., Oefner, P. J., Aigner, L., Brawanski, A., Bogdahn, U. and Beier, C. P. (2007). CD133(+) and CD133(-) glioblastoma-derived cancer stem cells show differential growth characteristics and molecular profiles. Cancer Res. 67, 4010-4015.
4. Bredel, M. (2001). Anticancer drug resistance in primary human brain tumors. Brain Res. Brain Res. Rev. 35, 161-204.
5. Bredel, M. and Pollack, I. F. (1997). The role of protein kinase C (PKC) in the evolution and proliferation of malignant gliomas, and the application of PKC inhibition as a novel approach to anti-glioma therapy. Acta Neurochir. 139, 1000-1013.
6. Campos, B., Wan, F., Farhadi, M., Ernst, A., Zeppernick, F., Tagscherer, K. E., Ahmadi, R., Lohr, J., Dictus, C., Gdynia, G. et al. (2010). Differentiation therapy exerts antitumor effects on stem-like glioma cells. Clin. Cancer Res. 16, 2715-2728.
7. Cheng, L., Bao, S. and Rich, J. N. (2010). Potential therapeutic implications of cancer stem cells in glioblastoma. Biochem. Pharmacol. 80, 654-665.
8. 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. et al. (2006). Activation of Bak and Bax through c-abl-protein kinase Cdelta-p38 MAPK signaling in response to ionizing radiation in human non-small cell lung cancer cells. J. Biol. Chem. 281, 7049-7059.
9. da Rocha, A. B., Mans, D. R., Regner, A. and Schwartsmann, G. (2002). Targeting protein kinase C: new therapeutic opportunities against high-grade malignant gliomas? Oncologist 7, 17-33.
10. Dewey, W. C., Ling, C. C. and Meyn, R. E. (1995). Radiation-induced apoptosis: relevance to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 33, 781-796.
11. Dungey, F. A., Caldecott, K. W. and Chalmers, A. J. (2009). Enhanced radiosensitization of human glioma cells by combining inhibition of poly(ADPribose) polymerase with inhibition of heat shock protein 90. Mol. Cancer Ther. 8, 2243-2254.
12. El-Rayes, B. F., Ali, S., Philip, P. A. and Sarkar, F. H. (2008). Protein kinase C: a target for therapy in pancreatic cancer. Pancreas 36, 346-352.
13. Furnari, F. B., Fenton, T., Bachoo, R. M., Mukasa, A., Stommel, J. M., Stegh, A., Hahn, W. C., Ligon, K. L., Louis, D. N., Brennan, C. et al. (2007). Malignant astrocytic glioma: genetics, biology, and paths to treatment. Genes Dev. 21, 2683-2710.
14. Galli, R., Binda, E.,Orfanelli, U., Cipelletti, B., Gritti, A., De Vitis, S., Fiocco, R., Foroni, C., Dimeco, F. and Vescovi, A. (2004). Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 64, 7011-7021.
15. Geoerger, B., Gaspar, N., Opolon, P., Morizet, J., Devanz, P., Lecluse, Y., Valent, A., Lacroix, L., Grill, J. and Vassal, G. (2008). EGFR tyrosine kinase inhibition radiosensitizes and induces apoptosis in malignant glioma and childhood ependymoma xenografts. Int. J. Cancer 123, 209-216.
16. Gokmen-Polar, Y., Murray, N. R., Velasco, M. A., Gatalica, Z. and Fields, A. P. (2001). Elevated protein kinase C betaII is an early promotive event in colon carcinogenesis. Cancer Res. 61, 1375-1381.
17. Graff, J. R., McNulty, A. M., Hanna, K. R., Konicek, B. W., Lynch, R. L., Bailey, S. N., Banks, C., Capen, A., Goode, R., Lewis, J. E. et al. (2005). The protein kinase Cbeta-selective inhibitor, Enzastaurin (LY317615.HCl), suppresses signaling through the AKT pathway, induces apoptosis, and suppresses growth of human colon cancer and glioblastoma xenografts. Cancer Res. 65, 7462-7469.
18. Griner, E. M. and Kazanietz, M. G. (2007). Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 7, 281-294.
19. Grossoni, V. C., Falbo, K. B., Kazanietz, M. G., de Kier Joffe, E. D. and Urtreger, A. J. (2007). Protein kinase C delta enhances proliferation and survival of murine mammary cells. Mol. Carcinog. 46, 381-390.
20. Martin, P. M. and Hussaini, I. M. (2005). PKC eta as a therapeutic target in glioblastoma multiforme. Expert Opin. Ther. Targets 9, 299-313.
21. Mercer, R. W., Tyler, M. A., Ulasov, I. V. and Lesniak, M. S. (2009). Targeted therapies for malignant glioma: progress and potential. BioDrugs 23, 25-35.
22. Moffat, J., Grueneberg, D. A., Yang, X., Kim, S. Y., Kloepfer, A. M., Hinkle, G., Piqani, B., Eisenhaure, T. M., Luo, B., Grenier, J. K. et al. (2006). A lentiviral RNAi library for human and mouse genes applied to an arrayed viral high-content screen. Cell 124, 1283-1298.
23. Naldini, L., Blömer, U., Gallay, P., Ory, D., Mulligan, R., Gage, F. H., Verma, I. M. and Trono, D. (1996). In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 272, 263-267.
24. Nelsona, T. J. and Alkona, D. L. (2009). Neuroprotective versus tumorigenic protein kinase C activators. Trends Biochem. Sci. 34, 136-145.
25. Panchision, D. M. and McKay, R. D. (2002). The control of neural stem cells by morphogenic signals. Curr. Opin. Genet. Dev. 12, 478-487.
26. Parekh, D. B., Ziegler, W. and Parker, P. J. (2000). Multiple pathways control protein kinase C phosphorylation. EMBO J. 19, 496-503.
27. Puchner, M. J. and Giese, A. (2000). Tamoxifen-resistant glioma-cell sub-populations are characterized by increased migration and proliferation. Int. J. Cancer 86, 468-473.
28. Rich, J. N. (2007). Cancer stem cells in radiation resistance. Cancer Res. 67, 8980-8984.
29. Rodriguez, E. M., Dunham, E. E. and Martin, G. S. (2009). Atypical protein kinase C activity is required for extracellular matrix degradation and invasion by Srctransformed cells. J. Cell. Physiol. 221, 171-182.
30. Rosen, J. M. and Jordan, C. T. (2009). The increasing complexity of the cancer stem cell paradigm. Science 324, 1670-1673.
31. Ross, G. M. (1999). Induction of cell death by radiotherapy. Endocr. Relat. Cancer 6, 41-44.
32. Singh, A., Greninger, P., Rhodes, D., Koopman, L., Violette, S., Bardeesy, N. and Settleman, J. (2009). A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 15, 489-500.
33. Singh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E., Hawkins, C., Squire, J. and Dirks, P. B. (2003). Identification of a cancer stem cell in human brain tumors. Cancer Res. 63, 5821-5828.
34. Singh, S. K., Hawkins, C., Clarke, I. D., Squire, J. A., Bayani, J., Hide, T., Henkelman, R. M., Cusimano, M. D. and Dirks, P. B. (2004). Identification of human brain tumour initiating cells. Nature 432, 396-401.
35. Steinberg, S. F. (2004). Distinctive activation mechanisms and functions for protein kinase Cdelta. Biochem. J. 384, 449-459.
36. Steinhart, R., Kazimirsky, G., Okhrimenk, H., Ben-Hur, T. and Brodie, C. (2007). PKCepsilon induces astrocytic differentiation of multipotential neural precursor cells. Glia 55, 224-232.
37. Vescovi, A. L., Galli, R. and Reynolds, B. A. (2006). Brain tumour stem cells. Nat. Rev. Cancer 6, 425-436.
38. Wang, J., Wakeman, T. P., Lathia, J. D., Hjelmeland, A. B., Wang, X. F., White, R. R., Rich, J. N. and Sullenger, B. A. (2010). Notch promotes radioresistance of glioma stem cells. Stem Cells 28, 17-28.
39. Wang, S., Garcia, A. J., Wu, M., Lawson, D. A., Witte, O. N. and Wu, H. (2006). Pten deletion leads to the expansion of a prostatic stem/progenitor cell subpopulation and tumor initiation. Proc. Natl. Acad. Sci. USA 103, 1480-1485.
40. Welsh, J. W., Mahadevan, D., Ellsworth, R., Cooke, L., Bearss, D. and Stea, B. (2009). The c-Met receptor tyrosine kinase inhibitor MP470 radiosensitizes glioblastoma cells. Radiat. Oncol. 4, 69.
41. Zhang, M., Atkinson, R. L. and Rosen, J. M. (2010). Selective targeting of radiationresistant tumor-initiating cells. Proc. Natl. Acad. Sci. USA 107, 3522-3527.