EGFR-mediated chromatin condensation protects kras-mutant cancer cells against ionizing radiation

Cancer Research

Volumn 74, Issue 10, 2014, Pages 2825-2834

  Wang, Meng ^a   Kern, Ashley M ^a   Hülskötter, Marieke ^a   Greninger, Patricia ^b   Singh, Anurag ^b   Pan, Yunfeng ^c   Chowdhury, Dipanjan ^c   Krause, Mechthild ^d,e,f   Baumann, Michael ^d,e,f   Benes, Cyril H ^b   Efstathiou, Jason A ^a   Settleman, Jeff ^b   Willers, Henning ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL CANCER CENTER   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^e INSTITUTE OF ION BEAM PHYSICS AND MATERIALS RESEARCH   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; CETUXIMAB; EPIDERMAL GROWTH FACTOR RECEPTOR; ERLOTINIB; HISTONE H3; K RAS PROTEIN; LYSINE; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN KINASE C ALPHA; SERINE;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER CELL; CELL PROTECTION; CELL SCREENING; CHROMATIN CONDENSATION; CONTROLLED STUDY; DOUBLE STRANDED DNA BREAK; GENE MUTATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INTERPHASE; IONIZING RADIATION; LUNG NON SMALL CELL CANCER; MITOSIS; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN METHYLATION; PROTEIN PHOSPHORYLATION; RADIATION DOSE; RADIATION PROTECTION; RADIOSENSITIZATION; SENESCENCE; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; AURORA KINASE B; BENZIMIDAZOLES; CARCINOMA, NON-SMALL-CELL LUNG; CELL AGING; CELL LINE, TUMOR; CHROMATIN; DNA BREAKS, DOUBLE-STRANDED; HUMANS; LUNG NEOPLASMS; MICE; MUTATION; PROTEIN KINASE C-ALPHA; PROTO-ONCOGENE PROTEINS; QUINAZOLINES; RADIATION TOLERANCE; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84901285595     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-3157     Document Type: Article

References (52)

1. Ward JF. DNA damage produced by ionizing radiation in mammalian cells: identities, mechanisms of formation, and reparability. Prog Nucleic Acid Res Mol Biol 1988;35:95-125.
2. Kegel P, Riballo E, Kuhne M, Jeggo PA, Lobrich M. X-irradiation of cells on glass slides has a dose doubling impact. DNA Repair (Amst) 2007;6:1692-7.
3. Willers H, Held KD. Introduction to clinical radiation biology. Hematol Oncol Clin North Am 2006;20:1-24.
4. Efimova EV, Mauceri HJ, Golden DW, Labay E, Bindokas VP, Darga TE, et al. Poly(ADP-ribose) polymerase inhibitor induces accelerated senescence in irradiated breast cancer cells and tumors. Cancer Res 2010;70:6277-82.
5. Toulany M, Kasten-Pisula U, Brammer I, Wang S, Chen J, Dittmann K, et al. Blockage of epidermal growth factor receptor-phosphatidylinositol 3-kinase-AKT signaling increases radiosensitivity of K-RAS mutated human tumor cells in vitro by affecting DNA repair. Clin Cancer Res 2006;12:4119-26.
6. Wang M,Morsbach F, Sander D, Gheorghiu L, Nanda A, Benes C, et al. EGF receptor inhibition radiosensitizes NSCLC cells by inducing senescence in cells sustaining dna double-strand breaks. Cancer Res 2011;71:6261-9.
7. Roberson RS, Kussick SJ, Vallieres E, Chen SY, Wu DY. Escape from therapy-induced accelerated cellular senescence in p53-null lung cancer cells and in human lung cancers. Cancer Res 2005;65: 2795-803.
8. Saretzki G. Cellular senescence in the development and treatment of cancer. Curr Pharm Des 2010;16:79-100.
9. Willers H, Azzoli CG, Santivasi WL, Xia F. Basic mechanisms of therapeutic resistance to radiation and chemotherapy in lung cancer. Cancer J 2013;19:200-7.
10. Harari PM, Allen GW, Bonner JA. Biology of interactions: antiepidermal growth factor receptor agents. J Clin Oncol 2007;25:4057-65.
11. Nyati MK, Morgan MA, Feng FY, Lawrence TS. Integration of EGFR inhibitors with radiochemotherapy. Nat Rev Cancer 2006;6: 876-85.
12. Rusch V, Baselga J, Cordon-Cardo C, Orazem J, Zaman M, Hoda S, et al. Differential expression of the epidermal growth factor receptor and its ligands in primary non-small cell lung cancers and adjacent benign lung. Cancer Res 1993;53:2379-85.
13. Blumenschein GR Jr., Paulus R, Curran WJ, Robert F, Fossella F, Werner-Wasik M, et al. Phase II study of cetuximab in combination with chemoradiation in patients with stage IIIA/B non-small-cell lung cancer: RTOG 0324. J Clin Oncol 2011;29:2312-8.
14. Govindan R, Bogart J, Stinchcombe T, Wang X, Hodgson L, Kratzke R, et al. Randomized phase II study of pemetrexed, carboplatin, and thoracic radiation with or without cetuximab in patients with locally advanced unresectable non-small-cell lung cancer: Cancer and Leukemia Group B trial 30407. J Clin Oncol 2011;29:3120-5.
15. Ready N, Janne PA, Bogart J, Dipetrillo T, Garst J, Graziano S, et al. Chemoradiotherapy and gefitinib in stage III non-small cell lung cancer with epidermal growth factor receptor and KRAS mutation analysis: cancer and leukemia group B (CALEB) 30106, a CALGB-stratified phase II trial. J Thorac Oncol 2010;5:1382-90.
16. Ausborn NL, Le QT, Bradley JD, Choy H, Dicker AP, Saha D, et al. Molecular profiling to optimize treatment in non-small cell lung cancer: a review of potential molecular targets for radiation therapy by the translational research program of the radiation therapy oncology group. Int J Radiat Oncol Biol Phys 2012;83: e453-64.
17. Gainor JF, Varghese AM, Ou SH, Kabraji S, Awad MM, Katayama R, et al. ALK rearrangements are mutually exclusive with mutations in EGFR or KRAS: an analysis of 1,683 patients with non-small cell lung cancer. Clin Cancer Res 2013;19:4273-81.
18. Eberhard DA, Johnson BE, Amler LC, Goddard AD, Heldens SL, Herbst RS, et al. Mutations in the epidermal growth factor receptor and in KRAS are predictive and prognostic indicators in patients with nonsmall-cell lung cancer treated with chemotherapy alone and in combination with erlotinib. J Clin Oncol 2005;23:5900-9.
19. Han SW, Kim TY, Jeon YK, Hwang PG, Im SA, Lee KH, et al. Optimization of patient selection for gefitinib in non-small cell lung cancer by combined analysis of epidermal growth factor receptor mutation, K-ras mutation, and Akt phosphorylation. Clin Cancer Res 2006;12: 2538-44.
20. Tsao MS, Aviel-Ronen S, Ding K, Lau D, Liu N, Sakurada A, et al. Prognostic and predictive importance of p53 and RAS for adjuvant chemotherapy in non small-cell lung cancer. J Clin Oncol 2007;25: 5240-7.
21. Winton T, Livingston R, Johnson D, Rigas J, Johnston M, Butts C, et al. Vinorelbine plus cisplatin vs. observation in resected non-small-cell lung cancer. N Engl J Med 2005;352:2589-97.
22. Diaz LA Jr., Williams RT, Wu J, Kinde I, Hecht JR, Berlin J, et al. The molecular evolution of acquired resistance to targeted EGFR blockade in colorectal cancers. Nature 2012;486:537-40.
23. Misale S, Yaeger R, Hobor S, Scala E, Janakiraman M, Liska D, et al. Emergence of KRAS mutations and acquired resistance to anti-EGFR therapy in colorectal cancer. Nature 2012;486:532-6.
24. Bernhard EJ, Stanbridge EJ, Gupta S, Gupta AK, Soto D, Bakanauskas VJ, et al. Direct evidence for the contribution of activated N-ras and Kras oncogenes to increased intrinsic radiation resistance in human tumor cell lines. Cancer Res 2000;60:6597-600.
25. Cengel KA, Voong KR, Chandrasekaran S, Maggiorella L, Brunner TB, Stanbridge E, et al. Oncogenic K-Ras signals through epidermal growth factor receptor and wild-type H-Ras to promote radiation survival in pancreatic and colorectal carcinoma cells. Neoplasia 2007;9:341-8.
26. Kim IA, Bae SS, Fernandes A, Wu J, Muschel RJ, McKenna WG, et al. Selective inhibition of Ras, phosphoinositide 3 kinase, and Akt isoforms increases the radiosensitivity of human carcinoma cell lines. Cancer Res 2005;65:7902-10.
27. Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483: 603-7.
28. Garnett MJ, Edelman EJ, Heidorn SJ, Greenman CD, Dastur A, Lau KW, et al. Systematic identification of genomic markers of drug sensitivity in cancer cells. Nature 2012;483:570-5.
29. Gazdar AF, Girard L, Lockwood WW, Lam WL, Minna JD. Lung cancer cell lines as tools for biomedical discovery and research. J Natl Cancer Inst 2010;102:1310-21.
30. McDermott U, Sharma SV, Dowell L, Greninger P,Montagut C, Lamb J, et al. Identification of genotype-correlated sensitivity to selective kinase inhibitors by using high-throughput tumor cell line profiling. Proc Natl Acad Sci U S A 2007;104:19936-41.
31. Chinnaiyan P, Huang S, Vallabhaneni G, Armstrong E, Varambally S, Tomlins SA, et al.Mechanisms of enhanced radiation response following epidermal growth factor receptor signaling inhibition by erlotinib (Tarceva). Cancer Res 2005;65:3328-35.
32. Park JS, Jun HJ, Cho MJ, Cho KH, Lee JS, Zo JI, et al. Radiosensitivity enhancement by combined treatment of celecoxib and gefitinib on human lung cancer cells. Clin Cancer Res 2006;12:4989-99.
33. Schmidt-Ullrich RK, Contessa JN, Lammering G, Amorino G, Lin PS. ERBB receptor tyrosine kinases and cellular radiation responses. Oncogene 2003;22:5855-65.
34. Torrance CJ, Agrawal V, Vogelstein B, Kinzler KW. Use of isogenic human cancer cells for high-throughput screening and drug discovery. Nat Biotechnol 2001;19:940-5.
35. Singh A, Greninger P, Rhodes D, Koopman L, Violette S, Bardeesy N, et al. A gene expression signature associated with "K-Ras addiction" reveals regulators of EMT and tumor cell survival. Cancer Cell 2009; 15:489-500.
36. Dahm-Daphi J, Hubbe P, Horvath F, El-Awady RA, Bouffard KE, Powell SN, et al. Nonhomologous end-joining of site-specific but not of radiation-induced DNA double-strand breaks is reduced in the presence of wild-type p53. Oncogene 2005;24:1663-72.
37. Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P, Muschel RJ, et al. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 2011;41:210-20.
38. Willers H, Kachnic LA, Luo CM, Li L, Purschke M, Borgmann K, et al. Biomarkers and mechanisms of FANCD2 function. J Biomed Biotechnol 2008;2008:821529.
39. Bianco C, Tortora G, Bianco R, Caputo R, Veneziani BM, Caputo R, et al. Enhancement of antitumor activity of ionizing radiation by combined treatment with the selective epidermal growth factor receptor-tyrosine kinase inhibitor ZD1839 (Iressa). Clin Cancer Res 2002; 8:3250-8.
40. Dittmann K, Mayer C, Fehrenbacher B, Schaller M, Raju U, Milas L, et al. Radiation-induced epidermal growth factor receptor nuclear import is linked to activation of DNA-dependent protein kinase. J Biol Chem 2005;280:31182-9.
41. Chen DJ, Nirodi CS. The epidermal growth factor receptor: a role in repair of radiation-induced DNA damage. Clin Cancer Res 2007;13: 6555-60.
42. Falk M, Lukasova E, Kozubek S. Chromatin structure influences the sensitivity of DNA to gamma-radiation. Biochim Biophys Acta 2008; 1783:2398-414.
43. Fischle W, Tseng BS, Dormann HL, Ueberheide BM, Garcia BA, Shabanowitz J, et al. Regulation of HP1-chromatin binding by histone H3 methylation and phosphorylation. Nature 2005;438:1116-22.
44. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, Brinkley BR, et al. Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 1997;106:348-60.
45. Guo JY, Chen HY, Mathew R, Fan J, Strohecker AM, Karsli-Uzunbas G, et al. Activated Ras requires autophagy to maintain oxidative metabolism and tumorigenesis. Genes Dev 2011;25:460-70.
46. Amaravadi RK, Yu D, Lum JJ, Bui T, Christophorou MA, Evan GI, et al. Autophagy inhibition enhances therapy-induced apoptosis in a Mycinduced model of lymphoma. J Clin Invest 2007;117:326-36.
47. Lindon C, Pines J. Ordered proteolysis in anaphase inactivates Plk1 to contribute to proper mitotic exit in human cells. J Cell Biol 2004; 164:233-41.
48. Gorgoulis VG, Halazonetis TD. Oncogene-induced senescence: the bright and dark side of the response. Curr Opin Cell Biol 2010:22: 816-27.
49. Vilenchik MM, Knudson AG. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc Natl Acad Sci U S A 2003;100:12871-6.
50. Singh K, Matsuyama S, Drazba JA, Almasan A. Autophagy-dependent senescence in response to DNA damage and chronic apoptotic stress. Autophagy 2012;8:236-51.
51. Young AR, Narita M, Ferreira M, Kirschner K, Sadaie M, Darot JF, et al. Autophagy mediates the mitotic senescence transition. Genes Dev 2009;23:798-803.
52. Goldberg SB, Supko JG, Neal JW, Muzikansky A, Digumarthy S, Fidias P, et al. A phase I study of erlotinib and hydroxychloroquine in advanced non-small-cell lung cancer. J Thorac Oncol 2012;7: 1602-8.