MTOR inhibitors radiosensitize PTEN-deficient non-small-cell lung cancer cells harboring an EGFR activating mutation by inducing autophagy

Journal of Cellular Biochemistry

Volumn 114, Issue 6, 2013, Pages 1248-1256

  Kim, Eun Ju ^a   Jeong, Jae Hoon ^a   Bae, Sangwoo ^a   Kang, Seongman ^b   Kim, Cheol Hyeon ^a   Lim, Young Bin ^a  

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

^b Korea University   (South Korea)

Author keywords

NSCLC; PTEN; Radiosensitivity

Indexed keywords

EPIDERMAL GROWTH FACTOR RECEPTOR; EVEROLIMUS; GEFITINIB; LENTIVIRUS VECTOR; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RAPAMYCIN; SHORT HAIRPIN RNA;

ARTICLE; AUTOPHAGY; CANCER CELL; CANCER RADIOTHERAPY; CELL VIABILITY; HUMAN; HUMAN CELL; LUNG NON SMALL CELL CANCER; MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY; RADIOSENSITIZATION;

ANTINEOPLASTIC AGENTS; AUTOPHAGY; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; DRUG RESISTANCE, NEOPLASM; GENE KNOCKDOWN TECHNIQUES; HUMANS; LUNG NEOPLASMS; MUTATION, MISSENSE; PTEN PHOSPHOHYDROLASE; QUINAZOLINES; RADIATION TOLERANCE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RNA, SMALL INTERFERING; SIROLIMUS; TOR SERINE-THREONINE KINASES;

EID: 84876219974     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.24465     Document Type: Article

References (34)

1. Amann J, Kalyankrishna S, Massion PP, Ohm JE, Girard L, Shigematsu H, Peyton M, Juroske D, Huang Y, Stuart Salmon J, Kim YH, Pollack JR, Yanagisawa K, Gazdar A, Minna JD, Kurie JM, Carbone DP,. 2005. Aberrant epidermal growth factor receptor signaling and enhanced sensitivity to EGFR inhibitors in lung cancer. Cancer Res 65: 226-235.
2. Bianco R, Garofalo S, Rosa R, Damiano V, Gelardi T, Daniele G, Marciano R, Ciardiello F, Tortora G,. 2008. Inhibition of mTOR pathway by everolimus cooperates with EGFR inhibitors in human tumours sensitive and resistant to anti-EGFR drugs. Br J Cancer 98: 923-930.
3. Bjornsti M-A, Houghton PJ,. 2004. The tor pathway: A target for cancer therapy. Nat Rev Cancer 4: 335-348.
4. Carew JS, Kelly KR, Nawrocki ST,. 2011. Mechanisms of mTOR inhibitor resistance in cancer therapy. Targeted Oncol 6: 17-27.
5. Chen H, Ma Z, Vanderwaal RP, Feng Z, Gonzalez-Suarez I, Wang S, Zhang J, Roti Roti JL, Gonzalo S, Zhang J,. 2011. The mTOR inhibitor rapamycin suppresses DNA double-strand break repair. Radiat Res 175: 214-224.
6. Das AK, Sato M, Story MD, Peyton M, Graves R, Redpath S, Girard L, Gazdar AF, Shay JW, Minna JD, Nirodi CS,. 2006. Non-small-cell lung cancers with kinase domain mutations in the epidermal growth factor receptor are sensitive to ionizing radiation. Cancer Res 66: 9601-9608.
7. Gao W, Shen Z, Shang L, Wang X,. 2011. Upregulation of human autophagy-initiation kinase ULK1 by tumor suppressor p53 contributes to DNA-damage-induced cell death. Cell Death Differ 18: 1598-1607.
8. Gewirtz DA, Hilliker ML, Wilson EN,. 2009. Promotion of autophagy as a mechanism for radiation sensitization of breast tumor cells. Radiother Oncol 92: 323-328.
9. Girard L, Zöchbauer-Müller S, Virmani AK, Gazdar AF, Minna JD,. 2000. Genome-wide allelotyping of lung cancer identifies new regions of allelic loss, differences between small cell lung cancer and non-small cell lung cancer, and loci clustering. Cancer Res 60: 4894-4906.
10. Gridelli C, Maione P, Rossi A,. 2008. The potential role of mTOR inhibitors in non-small cell lung cancer. Oncologist 13: 139-147.
11. He C, Levine B,. 2010. The beclin 1 interactome. Curr Opin Cell Biol 22: 140-149.
12. Helfrich BA, Raben D, Varella-Garcia M, Gustafson D, Chan DC, Bemis L, Coldren C, Barõn A, Zeng C, Franklin WA, Hirsch FR, Gazdar A, Minna J, Bunn PA,. 2006. Antitumor activity of the epidermal growth factor receptor (EGFR) tyrosine kinase inhibitor gefitinib (ZD1839, Iressa) in non-small cell lung cancer cell lines correlates with gene copy number and EGFR mutations but not EGFR protein levels. Clin Cancer Res 12: 7117-7125.
13. Janmaat ML, Rodriguez JA, Gallegos-Ruiz M, Kruyt FAE, Giaccone G,. 2006. Enhanced cytotoxicity induced by gefitinib and specific inhibitors of the Ras or phosphatidyl inositol-3 kinase pathways in non-small cell lung cancer cells. Int J Cancer 118: 209-214.
14. Jung CH, Jun CB, Ro SH, Kim YM, Otto NM, Cao J, Kundu M, Kim DH,. 2009. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20: 1992-2003.
15. Kokubo Y, Gemma A, Noro R, Seike M, Kataoka K, Matsuda K, Okano T, Minegishi Y, Yoshimura A, Shibuya M, Kudoh S,. 2005. Reduction of PTEN protein and loss of epidermal growth factor receptor gene mutation in lung cancer with natural resistance to gefitinib (IRESSA). Br J Cancer 92: 1711-1719.
16. Kroemer G, Mariño G, Levine B,. 2010. Autophagy and the integrated stress response. Mol Cell 40: 280-293.
17. Linardou H, Dahabreh IJ, Bafaloukos D, Kosmidis P, Murray S,. 2009. Somatic EGFR mutations and efficacy of tyrosine kinase inhibitors in NSCLC. Nat Rev Clin Oncol 6: 352-366.
18. Lynch TJ, Bell DW, Sordella R, Gurubhagavatula S, Okimoto RA, Brannigan BW, Harris PL, Haserlat SM, Supko JG, Haluska FG, Louis DN, Christiani DC, Settleman J, Haber DA,. 2004. Activating mutations in the epidermal growth factor receptor underlying responsiveness of non-small-cell lung cancer to gefitinib. N Engl J Med 350: 2129-2139.
19. Manegold PC, Paringer C, Kulka U, Krimmel K, Eichhorn ME, Wilkowski R, Jauch K-W, Guba M, Bruns CJ,. 2008. Antiangiogenic therapy with mammalian target of rapamycin inhibitor RAD001 (Everolimus) increases radiosensitivity in solid cancer. Clin Cancer Res 14: 892-900.
20. Mizushima N,. 2004. Methods for monitoring autophagy. Int J Biochem Cell Biol 36: 2491-2502.
21. Mizushima N,. 2010. The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22: 132-139.
22. Mizushima N, Yoshimori T,. 2007. How to interpret LC3 immunoblotting. Autophagy 3: 542-545.
23. Mizushima N, Yoshimori T, Levine B,. 2010. Methods in mammalian autophagy research. Cell 140: 313-326.
24. Moreau K, Luo S, Rubinsztein DC,. 2010. Cytoprotective roles for autophagy. Curr Opin Cell Biol 22: 206-211.
25. Moreira-Leite FF, Harrison LR, Mironov A, Roberts RA, Dive C,. 2010. Inducible EGFR T790M-mediated gefitinib resistance in non-small cell lung cancer cells does not modulate sensitivity to PI103 provoked autophagy. J Thorac Oncol 5: 765-777.
26. Naidu SR, Lakhter AJ, Androphy EJ,. 2012. PIASy-mediated Tip60 sumoylation regulates p53-induced autophagy. Cell Cycle 11: 2717-2728.
27. Paez JG, Jänne PA, Lee JC, Tracy S, Greulich H, Gabriel S, Herman P, Kaye FJ, Lindeman N, Boggon TJ, Naoki K, Sasaki H, Fujii Y, Eck MJ, Sellers WR, Johnson BE, Meyerson M,. 2004. EGFR mutations in lung cancer: Correlation with clinical response to gefitinib therapy. Science 304: 1497-1500.
28. Sos ML, Koker M, Weir BA, Heynck S, Rabinovsky R, Zander T, Seeger JM, Weiss J, Fischer F, Frommolt P, Michel K, Peifer M, Mermel C, Girard L, Peyton M, Gazdar AF, Minna JD, Garraway LA, Kashkar H, Pao W, Meyerson M, Thomas RK,. 2009a. PTEN loss contributes to erlotinib resistance in EGFR-mutant lung cancer by activation of Akt and EGFR. Cancer Res 69: 3256-3261.
29. Sos ML, Michel K, Zander T, Weiss J, Frommolt P, Peifer M, Li D, Ullrich R, Koker M, Fischer F, Shimamura T, Rauh D, Mermel C, Fischer S, Stückrath I, Heynck S, Beroukhim R, Lin W, Winckler W, Shah K, LaFramboise T, Moriarty WF, Hanna M, Tolosi L, Rahnenführer J, Verhaak R, Chiang D, Getz G, Hellmich M, Wolf J, Girard L, Peyton M, Weir BA, Chen T-H, Greulich H, Barretina J, Shapiro GI, Garraway LA, Gazdar AF, Minna JD, Meyerson M, Wong K-K, Thomas RK,. 2009b. Predicting drug susceptibility of non-small cell lung cancers based on genetic lesions. J Clin Invest 119: 1727-1740.
30. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M, Criollo A, Morselli E, Zhu C, Harper F, Nannmark U, Samara C, Pinton P, Vicencio JM, Carnuccio R, Moll UM, Madeo F, Paterlini-Brechot P, Rizzuto R, Szabadkai G, Pierron G, Blomgren K, Tavernarakis N, Codogno P, Cecconi F, Kroemer G,. 2008. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol 10: 676-687.
31. Wang X, Sun S-Y,. 2009. Enhancing mTOR-targeted cancer therapy. Expert Opin Ther Targets 13: 1193-1203.
32. Wheeler DL, Dunn EF, Harari PM,. 2010. Understanding resistance to EGFR inhibitors-Impact on future treatment strategies. Nat Rev Clin Oncol 7: 493-507.
33. Zhuang W, Qin Z, Liang Z,. 2009. The role of autophagy in sensitizing malignant glioma cells to radiation therapy. Acta Biochim Biophys Sin 41: 341-351.
34. Zois CE, Koukourakis MI,. 2009. Radiation-induced autophagy in normal and cancer cells: Towards novel cytoprotection and radio-sensitization policies ? Autophagy 5: 442-450.