Epigenetic interventions increase the radiation sensitivity of cancer cells

Current Pharmaceutical Design

Volumn 20, Issue 11, 2014, Pages 1857-1865

  Ren, Juan ^a   Chu, Yongli ^b   Ma, Hongbing ^c   Zhang, Yuelang ^a   Zhang, Xiaozhi ^a   Zhao, Dongli ^a   Li, Zongfang ^c   Wang, Jiansheng ^a   Gao, Yan e ^c   Xiao, Lisha ^e   Liu, Rui ^a   Qian, Jiansheng ^a   Liu, Yan ^a   Wei, Hongxia ^a   Jiang, Shiwen ^d  

^a XI'AN JIAOTONG UNIVERSITY   (China)

^b YANTAI YUHUANGDING HOSPITAL   (China)

^c THE SECOND AFFILIATED HOSPITAL OF XI AN JIAOTONG UNIVERSITY   (China)

^d MERCER UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e NONE

Author keywords

Anticancer drugs; Demethylating agents; Epigenetic; Histone deacetylase inhibitors; Radiosensitization; Radiotherapy

Indexed keywords

ABEXINOSTAT; BRCA1 PROTEIN; DEATH ASSOCIATED PROTEIN KINASE; DNA METHYLTRANSFERASE INHIBITOR; ENTINOSTAT; HEAT SHOCK PROTEIN 90; KU ANTIGEN; MICRORNA; MICRORNA 101; MICRORNA 155; MICRORNA 18A; MICRORNA 34; MICRORNA 7; PROTEIN MLH1; PROTEIN P16; PROTEIN P53; RAD50 PROTEIN; RAD51 PROTEIN; TRICHOSTATIN A; UNCLASSIFIED DRUG; VALPROIC ACID; VORINOSTAT; ZEBULARINE;

ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIOGENESIS; CANCER CELL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA END JOINING REPAIR; DNA METHYLATION; DNA REPAIR; EPIGENETICS; G2 PHASE CELL CYCLE CHECKPOINT; GENE EXPRESSION; HISTONE ACETYLATION; HISTONE MODIFICATION; HOMOLOGOUS RECOMBINATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTERVENTION STUDY; IONIZING RADIATION; M PHASE CELL CYCLE CHECKPOINT; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; RADIOSENSITIVITY; RADIOSENSITIZATION; TUMOR CELL; UPREGULATION; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; NEOPLASMS; RADIATION DOSE;

ANIMALS; APOPTOSIS; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICRORNAS; NEOPLASMS; RADIATION TOLERANCE; RADIATION, IONIZING;

EID: 84903691923     PISSN: 13816128     EISSN: 18734286     Source Type: Journal    
DOI: 10.2174/13816128113199990529     Document Type: Article

References (111)

1. Esteller M. The necessity of a human epigenome project. Carcinogenesis 2006; 27: 1121-5
2. Kim HJ, Kim JH, Chie EK, Young PD, Kim IA, Kim IH. DNMT (DNA methyltransferase) inhibitors radiosensitize human cancer cells by suppressing DNA repair activity. Radiat Oncol 2012; 7: 39.
3. Esteller M. Epigenetics provides a new generation of oncogenes and tumour-suppressor genes. Br J Cancer 2006; 94: 179-183.
4. Manoharan M, Ramachandran K, Soloway MS, Singal R. Epigenetic targets in the diagnosis and treatment of prostate cancer. Int Braz J Urol 2007; 33: 11-8.
5. Lin RK, Hsu HS, Chang JW, Chen CY, Chen JT, Wang YC. Alteration of DNA methyltransferases contributes to 5'CpG methylation and poor prognosis in lung cancer. Lung Cancer 2007; 55: 205-13.
6. Eads CA, Danenberg KD, Kawakami K, Saltz LB, Danenberg PV, Laird PW. CpG island hypermethylation in human colorectal tumors is not associated with DNA methyltransferase overexpression. Cancer Res 1999; 59: 2302-6.
7. Robertson KD. DNA methylation, methyltransferases, and cancer. Oncogene 2001; 20: 3139-55.
8. Gore SD, Baylin S, Sugar E, Carraway H, Miller CB, et al. Combined DNA methyltransferase and histone deacetylase inhibition in the treatment of myeloid neoplasms. Cancer Res 2006; 66: 6361-9.
9. Issa JP, Garcia-Manero G, Giles FJ, et al. Phase 1 study of lowdose prolonged exposure schedules of the hypomethylating agent 5-aza-2'-deoxycytidine (decitabine) in hematopoietic malignancies. Blood 2004; 103; 1635-40.
10. Marquez VE, Kelley JA, Agbaria R., et al. Zebularine: a unique molecule for an epigenetically based strategy in cancer chemotherapy. Ann N Y Acad Sci 2005; 1058: 246-54.
11. Hofstetter B, Niemierko A, Forrer C, et al. Impact of genomic methylation on radiation sensitivity of colorectal carcinoma. Int J Radiat Oncol Biol. Phys 2010; 76: 1512-9.
12. Qiu H, Yashiro M, Shinto O, Matsuzaki T, Hirakawa K. DNA methyltransferase inhibitor 5-aza-CdR enhances the radiosensitivity of gastric cancer cells. Cancer Sci 2009; 100: 181-8.
13. Cho HJ, Kim SY, Kim KH, et al. The combination effect of sodium butyrate and 5-Aza-2'-deoxycytidine on radiosensitivity in RKO colorectal cancer and MCF-7 breast cancer cell lines. World J Surg Oncol 2009; 7: 49.
14. De Schutter H, Kimpe M, Isebaert S, Nuyts S. A systematic assessment of radiation dose enhancement by 5-Aza-2'-deoxycytidine and histone deacetylase inhibitors in head-and-neck squamous cell carcinoma. Int J Radiat Oncol Biol Phys 2009; 73: 904-12.
15. Dote H, Cerna D, Burgan WE, et al. Enhancement of in vitro and in vivo tumor cell radiosensitivity by the DNA methylation inhibitor zebularine. Clin. Cancer Res 2005; 11: 4571-9
16. Ahn MY, Jung JH, Na YJ, Kim HS. A natural histone deacetylase inhibitor, Psammaplin A, induces cell cycle arrest and apoptosis in human endometrial cancer cells. Gynecol Oncol 2008; 108: 27-33.
17. Kim DH, Shin J, Kwon HJ. Psammaplin A is a natural prodrug that inhibits class I histone deacetylase. Exp Mol Med 2007; 39: 47-55.
18. Luzhna L, Kovalchuk O. Modulation of DNA methylation levels sensitizes doxorubicin-resistant breast adenocarcinoma cells to radiation-induced apoptosis. Biochem Biophys Res Commun 2010; 392: 113-7.
19. Yi P, Melnyk S, Pogribna M, Pogribny IP, Hine RJ, James SJ. Increase in plasma homocysteine associated with parallel increases in plasma Sadenosylhomocysteine and lymphocyte DNA hypomethylation. J Biol Chem 2000; 275: 29318-23.
20. Castro R, Rivera I, Martins C, Struys EA, et al. Intracellular Sadenosylhomocysteine increased levels are associated with DNA hypomethylation in HUVEC. J Mol Med 2005; 83: 831-6.
21. Hoffman DR, Cornatzer WE, Duerre JA. Relationship between tissue levels of S-adenosylmethionine, S-adenylhomocysteine, and transmethylation reactions. Can J Biochem 1979; 57: 56-65.
22. Baylin SB. DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2005; 2: 4-11.
23. Bolden JE, Peart MJ, Johnstone RW. Anticancer activities of histone deacetylase inhibitors. Nat Rev Drug Discov 2006; 5: 769-84.
24. Karagiannis TC, El-Osta A. Modulation of cellular radiation responses by histone deacetylase inhibitors. Oncogene 2006; 25: 3885-93.
25. Dokmanovic M, Marks PA. Prospects: histone deacetylase inhibitors. J Cell Biochem 2005; 96: 293-304.
26. Carew JS, Giles FJ, Nawrocki ST. Histone deacetylase inhibitors: Mechanisms of cell death and promise in combination cancer therapy. Cancer Lett 2008; 269: 7-17.
27. Chen JS, Faller DV. Histone deacetylase inhibition-mediated posttranslational elevation of p27KIP1 protein levels is required for G1 arrest in fibroblasts. J Cell Physiol 2005; 202: 87-99.
28. Marks PA, Richon VM, Breslow R, Rifkind RA. Histone deacetylase inhibitors as new cancer drugs. Curr Opin Oncol 2001; 13: 477-83.
29. Crazzolara R, Jöhrer K, Johnstone RW, et al. Histone deacetylase inhibitors potently repress CXCR4 chemokine receptor expression and function in acute lymphoblastic leukaemia. Br J Haematol 2002; 119: 965-9.
30. Deroanne CF, Bonjean K, Servotte S, et al. Histone deacetylases inhibitors as anti-angiogenic agents altering vascular endothelial growth factor signaling. Oncogene 2002; 21: 427-36.
31. Goh M, Chen F, Paulsen MT, et al. Phenylbutyrate attenuates the expression of Bcl-X(L), DNA-PK, caveolin-1, and VEGF in prostate cancer cells. Neoplasia 2001; 3: 331-8.
32. Qian DZ, Kato Y, Shabbeer S, et al. Targeting tumor angiogenesis with histone deacetylase inhibitors: the hydroxamic acid derivative LBH589. Clin. Cancer Res 2006; 12: 634-42.
33. Nusinzon I, Horvath CM. Interferon-stimulated transcription and innate antiviral immunity require deacetylase activity and histone deacetylase 1. Proc Natl Acad Sci USA 2003; 100: 14742-7.
34. Yuan ZL, Guan Y J, Chatterjee D, Chin YE. Stat3 dimerization regulated by reversible acetylation of a single lysine residue. Science 2005; 307: 269-73
35. Chen L, Fischle W, Verdin E, Greene WC. Duration of nuclear NFkappaB action regulated by reversible acetylation. Science 2001; 293: 1653-7.
36. Martínez-Balbás MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J 2000; 19: 662-71.
37. Scroggins BT, Robzyk K, Wang D, et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 2007; 25: 151-9.
38. Gu W, Roeder RG. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell 1997 l90: 595-606.
39. Siddiqui H, Solomon DA, Gunawardena RW, et al. Histone deacetylation of RB-responsive promoters: requisite for specific gene repression but dispensable for cell cycle inhibition. Mol Cell Biol 2003; 23: 7719-31.
40. Munshi A, Kurland JF, Nishikawa T, et al. Histone deacetylase inhibitors radiosensitize human melanoma cells by suppressing DNA repair activity. Clin Cancer Res 2005; 11: 4912-22.
41. Camphausen K, Cerna D, Scott T, et al. Enhancement of in vitro and in vivo tumor cell radio-sensitivity by valproic acid. Int J Cancer 2005; 114: 380-6
42. Zhang Y, Jung M, Dritschilo A, Jung M. Enhancement of radiation sensitivity of human squamous carcinoma cells by histone deacetylase inhibitors. Radiat Res 2004; 161: 667-74.
43. Zhang Y, Adachi M, Zhao X, et al. Histone deacetylase inhibitors FK228. N-(2-aminophenyll-4-IN-ipyridm-3-ylmethoxycarbonyqamino-methypbenzamide and mcarboxycinnamic acid bis-hydrmamide augment radiation-induced cell death in gastrcintestinal adenocarcinoma cells Int J Cancer 2004; 110: 301-8.
44. Chinnaiyan P, Vallabhaneni G, Armstrong E, et al. Modulation of radiation response by histone deacetylase inhibition. Int J Radiat Oncol Biol Phys 2005; 62: 223-9.
45. Konsoula Z, Cao H, Velena A, Jung M. Adamantanyl histone deacetylase inhibitor H6 caha exhibits favorable Pharmacokinetics and augments prostate cancer radiation sensitivity. Int J Radiat Oncol Biol Phys 2011; 79: 1541-8.
46. Camphausen K, Scott T, Sproull M, Tofilon PJ. Enhancement of xenograft tumor radiosensitivity by the histone deacetylase inhibitor MS-275 and correlation with histone hyperacetylation. Clin Cancer Res 2004; 10: 6066-71.
47. Camphausen K, Tofilon PJ. Inhibition of Histone Deacetylation: A Strategy for Tumor Radiosensitization. J Clin Oncol 2007; 25: 4051-6.
48. Karagiannis TC, El-Osta A. Clinical potential of histone deacetylase inhibitors as stand alone therapeutics and in combination with other chemotherapeutics or radiotherapy for cancer. Epigenetics 2006; 1: 121-6.
49. Kouraklis G, Theocharis S. Histone deacetylase inhibitors: a novel target of anticancer therapy (review). Oncol Rep 2006; 15: 489-94.
50. Ree AH, Dueland S, Folkvord S, et al. Vorinostat, a histone deacetylase inhibitor, combined with pelvic palliative radiotherapy for gastrointestinal carcinoma: the Pelvic Radiation and Vorinostat (PRAVO) phase 1 study. Lancet Oncol 2010; 11: 459-64.
51. Saito A, Yamashita T, Mariko Y, et al. A synthetic inhibitor of histone deacetylase, MS-27-275, with marked in vivo antitumor activity against human tumors. Proc Natl Acad Sci USA 1999; 96: 4592-7.
52. Arundel C, Glicksman A, Leith J. Enhancement of radiation injury in human colon tumor cells by the maturational agent sodium butyrate (NaB). Radiat Res 1985; 104: 443-8.
53. Arundel CM, Leith JT. Ettects of nucleoside analogs and sodium butyrate on recovery from potentially lethal X ray damage in human colon tumor cells. Int J Radiat Oncnl Biol Phys 1987; 13: 593-601
54. Hallows KR, Bliven SF, Leith JT. Effects of the differentiating agents sodium butyrate and N-methylformamide on the oxygen enhancement ratio of human colon tumor cells. Radiat Res 1988; 113: 191-8.
55. Leith JT. Effects of sodium butyrate and 3-aminobenzamide on survival of Chinese hamster HA-1 cells after X irradiation. Radiat Res 1988; 114: 186-91.
56. Bar-Sela G, Jacobs KM, Gius D. Histone Deacetylase Inhibitor and Demethylating Agent Chromatin Compaction and the Radiation Response by Cancer Cells. Cancer J 2007; 13: 65-9.
57. Blagosklonny MV, Robey R, Sackett DL, et al. Histone deacetylase inhibitors all induce p21 but differentially cause tubulin acetylation, mitotic arrest, and cytotoxicity. Mol Cancer Ther 2002; 1: 937-41.
58. Yoshida M, Furumai R, Nishiyama M, et al. Histone deacetylase as a new target for cancer chemotherapy. Cancer Chemother Pharmacol 2001; 48: S20-6
59. Biade S, Stobbe CC, Boyd JT, et al. Chemical agents that promote chromatin compaction radiosensitize tumour cells. Int J Radiat Biol 2001; 77: 1033-42.
60. Hubbert C, Guardiola A, Shao R, et al. HDAC6 is a microtubuleassociated deacetylase. Nature 2002; 417: 455-8.
61. Zhang Y, Reinberg D. Transcription regulation by histone methylation: interplay between different covalent modifications of the core histone tails. Genes Dev 2001; 15: 2343-60.
62. Cerna D, Camphausen K, Tofilon PJ. Histone deacetylation as a target for radiosensitization. Curr Top Dev Biol 2006; 73: 173-204
63. Banuelos CA, Banáth JP, MacPhail SH, et al. Radiosensitization by the Histone Deacetylase Inhibitor PCI-24781. Clin Cancer Res 2007; 13: 6816-26.
64. Kao GD, McKenna WG, Guenther MG, et al. Histone deacetylase 4 interacts with 53BP1 to mediate the DNA damage response. J Cell Biol 2003; 160: 1017-27.
65. Kim GD, Choi YH, Dimtchev A, et al. Sensing of ionizing radiation-induced DNA damage by ATM through interaction with histone deacetylase. J Biol Chem 1999; 274: 31127-30.
66. Zhang Y, Carr T, Dimtchev A, et al. Attenuated DNA damage repair by trichostatin A through BRCA1 suppression. Radiat Res 2007; 168: 115-124.
67. Munshi A, Tanaka T, Hobbs ML, et al. Vorinostat, a histone deacetylase inhibitor, enhances the response of human tumor cells to ionizing radiation through prolongation of gamma-H2AX foci. Mol Cancer Ther 2006; 5: 1967-74.
68. Subramanian C, Opipari AW Jr, Bian X, et al. Ku70 acetylation mediates neuroblastoma cell death induced by histone deacetylase inhibitors. Proc Natl Acad Sci USA 2005; 102: 4842-7.
69. Masumoto H, Hawke D, Kobayashi R, et al. A role for: cell-cycleregulated histone H3 lysine 56 acetylation-in the DNA damage response. Nature 2005; 436: 294-8.
70. Hassa PO, Hottiger MO.An epigenetic code for DNA damage repair pathways? Biochem Cell Biol 2005; 83: 270-85.
71. Sedelnikova OA, Rogakou EP, Panyutin IG, et al. Quantitative detection of (125)IdU-induced DNA double-strand breaks,with gamma-H2AX antibody.Radiat Fies 2002; 158: 486-92
72. Nazarov I, Smimova A, Krutilina RI, et al. Dephosphoryfation of histone gamma-H2AX during repair of DNA double-strand breaks in mammalian cells and its ihhibition by calyculin A. Radiat Res 2003; 160: 309-17.
73. Rothkamm K. Lobrich. Evidence for a lack of DNA double-strand break repair in human cells ex-posed to very low x-ray doses. Proc Natl Acad Sci USA 2003; 100: 5057-62.
74. Rothkamm K, Kruger I, Thompson L, et al. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003; 23: 5706-15.
75. Camphausen K, Burgan W, Cerra M, et al. Enhanced radiationinduced cell killing and prolongation of gammal H2AX foci expression by the histona deacetylase inhibitor MS-275. Cancer Res 2004; 64: 316-23.
76. MacPhail S, Banath J, Yu T, et al. Expression of-phosphorylated histone -H2AX in cultured cell lines following exposure to-X-rays. Int J Radiat Biol 2003; 79: 351-8.
77. Zhang Y, Adachi M, Zou H, et al. Histone deacetylase inhibitors enhance phosphorylation of histone H2AX-after ionizing radiation. Int J Radiat Onco Biol Phys 2006; 65: 859-66.
78. Camphausen K, Tofilon PJ. Inhibition of Histone Deacetylation: A Strategy for Tumor Radiosensitization. J Clin Oncol 2007; 25: 4051-6.
79. Flatmark K, Nome RV, Folkvord S, et al. Radiosensitization of colorectal carcinoma cell lines by histone deacetylase inhibition. Radiat Oncol 2006; 1: 25.
80. Kim IA, Shin JH, Kim IH, et al. Histone deacetylase inhibitormediated radiosensitization of human cancer cells: class differences and the potential influence of p53. Clin. Cancer Res 2006; 12: 940-9.
81. Miller AC, Whittaker T, Thibault A, Samid D. Modulation of radiation response of human tumour cells by the differentiation in ducers phenylacetate and phenylbutyrate. Int J Radiat Biol 1997; 72: 211-8.
82. Sonnemann J, Kumar KS, Heesch S, et al. Histone deacetylase inhibitors induce cell death and enhance the susceptibility to ionizing radiation, etoposide, and TRAIL in medulloblastoma cells. Int J Oncol 2006; 28: 755-66.
83. Seo SK, Jin HO, Lee HC, et al. Combined effects of sulindac and suberoylanilide hydroxamic Acid on apoptosis induction in human lung cancer cells. Mol Pharmacol 2008; 73: 1005-12.
84. Geng L, Cuneo KC, Fu A, et al. Histone deacetylase (HDAC) inhibitor LBH589 increases duration of gamma-H2AX foci and confines HDAC4 to the cytoplasm in irradiated non-small cell lung cancer. Cancer Res 2006; 66: 11298-304.
85. Cuneo KC, Fu A, Osusky K, et al. Histone deacetylase inhibitor NVP-LAQ824 sensitizes human nonsmall cell lung cancer to the cytotoxic effects of ionizing radiation. Anticancer Drugs 2007; 18: 793-800.
86. Zaskodova D, Rezacova M, Vavrova J, Vokurkova D, Tichy A. Effect of valproic acid, a histone deacetylase inhibitor, on cell death and molecular changes caused by low-dose irradiation. Ann N Y Acad Sci 2006; 1091: 385-98.
87. Entin-Meer M, Rephaeli A, Yang X, et al. Butyric acid prodrugs are histonedeacetylase inhibitors that show antineoplastic activity and radiosensitizing capacity in the treatment of malignant gliomas. Mol Cancer Ther 2005; 4: 1952-61.
88. Entin-Meer M, Rephaeli A, Yang X, et al. AN-113, a novel prodrug of 4-phenylbutyrate with increased anti-neoplastic activity in glioma cell lines. Cancer Lett 2007; 253: 205-14.
89. Sah NK, Munshi A, Hobbs M, Carter BZ, Andreeff M, Meyn RE. Effect of downregulation of survivin expression on radiosensitivity of human epidermoid carcinoma cells. Int J Radiat Oncol Biol Phys 2006; 66: 852-9.
90. Zhang Y, Adachi M, Kawamura R, et al. Bmf contributes to histone deacetylase inhibitor-mediated enhancing effects on apoptosis after ionizing radiation. Apoptosis 2006; 11: 1349-57.
91. Lopez CA, Feng FY, Herman JM, et al. Phenylbutyrate sensitizes human glioblastoma cells lacking wild-type p53 function to ionizing radiation. Int J Radiat Oncol Biol Phys 2007; 69: 214-20.
92. Chen X, Wong P, Radany E, Wong JY. HDAC Inhibitor, Valproic Acid, Induces p53-Dependent Radiosensitization of Colon Cancer Cells. Cancer Biother Radiopharm 2009; 24: 689-99.
93. Jung MV. Inhibitors of histone deacetylase as new anticancer agents. Curr Med Chem 2001; 8: 1505-11.
94. Chung YL, Wang AJ, Yao LF. Antitumor histone deacetylase inhibitors suppress cutaneous radiation syndrome: Implications for increasing therapeutic gain in cancer radiotherapy. Mol Cancer Ther 2004; 3: 317-25.
95. Stoilov L, Darroudi F, Meschini R, et al. Inhibition of repair of Xray-induced DNA double-strand breaks in human lymphocytes exposed to sodium butyrate. Int J Radiat Biol 2000; 76: 1485-91.
96. Groselj B, Sharma NL, Hamdy FC, Kerr M, Kiltie AE. Histone deacetylase inhibitors as radiosensitisers: effects on DNA damage signalling and repair. Br J Cancer 2013; 108: 748-54.
97. Bishton M, Kenealy M, Johnstone R, Rasheed W, Prince HM. Epigenetic targets in hematological malignancies: combination therapies with HDACis and demethylating agents. Expert Rev Anticancer Ther 2007; 7(10): 1439-49.
98. Weller M, Gorlia T, Cairncross JG, et al. Prolonged survival with valproic acid use in the EORTC/NCIC temozolomide trial for glioblastoma. Neurology 2011; 77(12): 1156-64.
99. Guthrie GD, Eljamel S. Impact of particular antiepileptic drugs on the survival of patients with glioblastoma multiforme. J Neurosurg 2012 Nov 23.[Epub ahead of print].
100. Undevia SD, Janisch L, Schilsky RL, et al. Phase I study of the safety, pharmacokinetics (PK) and pharmacodynamics (PD) of the histone deacetylase inhibitor (HDACi) PCI-24781. Journal of Clinical Oncology, 2008 ASCO Annual Meeting Proceedings (Post-Meeting Edition) 2008; 26: 15S: 14514.
101. Surova O, Akbar NS, Zhivotovsky B. Knock-Down of Core Proteins Regulating MicroRNA Biogenesis Has No Effect on Sensitivity of Lung Cancer Cells to Ionizing Radiation. PLoS One 2012; 7: e33134
102. Kato M, Paranjape T, Müller RU, et al. The mir-34 microRNA is required for the DNA damage response in vivo in C. elegans and in vitro in human breast cancer cells. Oncogene 2009; 28: 2419-24.
103. Babar IA, Czochor J, Steinmetz A, et al. Inhibition of hypoxiainduced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 2011; 12: 908-14.
104. Song L, Lin C, Wu Z, et al. miR-18a Impairs DNA Damage Response through Downregulation of Ataxia Telangiectasia Mutated (ATM) Kinase. PLoS One 2011; 6(9): e25454
105. Lee KM, Choi EJ, Kim IA. microRNA-7 increases radiosensitivity of human cancer cells with activated EGFR-associated signaling. Radiother Oncol 2011; 101: 171-6.
106. Hummel R, Hussey DJ, Haier J. MicroRNAs: Predictors and modifiers of chemo-and radiotherapy in different tumour types. Eur J Cancer 2010; 46: 298-311.
107. Jeong SH, Wu HG, Park WY. LIN28B confersradio-resistance through the posttranscriptional control of KRAS. Exp Mol Med 2009; 41: 912-8.
108. Oh JS, Kim JJ, Byun JY, Kim IA. LIN28-LET7 modulates radiosensitivity of human cancer cells with activation of K-RAS. Int J Radiat Oncol Biol Phys 2010; 76: 5-8.
109. Chen S, Wang H, Ng WL, Curran WJ, Wang Y. Radiosensitizing effect of ectopic MIR-101 on non-small-cell lung cancer cells depend of the endogenous MIR-101 level. Int J Radiat Oncol Biol Phys 2011; 81: 1524-9.
110. Glasspool RM, Teodoridis JM, Brown R. Epigenetics as a mechanism driving polygenic clinical drug resistance. Br J Cancer 2006; 94: 1087-92.
111. De Schutter H, Nuyts S. Radiosensitizing Potential of Epigenetic Anticancer Drugs. Anticancer Agents Med Chem 2009; 9: 99-108.