Targeting DNA damage response in the radio(Chemo)therapy of non-small cell lung cancer

International Journal of Molecular Sciences

Volumn 17, Issue 6, 2016, Pages

  Li, Ling ^a,b   Zhu, Tao ^a,b   Gao, Yuan Feng ^a,b   Zheng, Wei ^a,b   Wang, Chen Jing ^a,b   Xiao, Ling ^a,b   Huang, Ma Sha ^a,b   Yin, Ji Ye ^a,b   Zhou, Hong Hao ^a,b   Liu, Zhao Qian ^a,b  

^a CENTRAL SOUTH UNIVERSITY   (China)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

DNA damage and repair; Epigenetics; Genetic polymorphisms; Non small cell lung cancer; Radiotherapy and chemotherapy; Resistance

Indexed keywords

DNA DEPENDENT PROTEIN KINASE; DOUBLE STRANDED DNA; LONG UNTRANSLATED RNA; MICRORNA; XRCC1 PROTEIN;

ATAXIA TELANGIECTASIA; CHEMOTHERAPY; DNA DAMAGE; DNA REPAIR; ERCC GENE; EXCISION REPAIR; GENE; GENE EXPRESSION; GENETIC POLYMORPHISM; GENETIC VARIABILITY; GENOMIC INSTABILITY; HUMAN; MISMATCH REPAIR; NON SMALL CELL LUNG CANCER; OVERALL SURVIVAL; REVIEW; SENSITIVITY ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM; SMOKING; XRCC1 GENE; CARCINOMA, NON-SMALL-CELL LUNG; CHEMORADIOTHERAPY; DRUG RESISTANCE; GENETIC EPIGENESIS; GENETICS; LUNG NEOPLASMS; TREATMENT OUTCOME;

CARCINOMA, NON-SMALL-CELL LUNG; CHEMORADIOTHERAPY; DNA DAMAGE; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; HUMANS; LUNG NEOPLASMS; MICRORNAS; POLYMORPHISM, GENETIC; RNA, LONG NONCODING; TREATMENT OUTCOME;

EID: 84971517382     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17060839     Document Type: Review

References (95)

1. Siegel, R.L, Miller, K.D, Jemal, A. Cancer statistics, 2016. CA Cancer J. Clin. 2016, 66, 7-30. [CrossRef] [PubMed]
2. Kastan, M.B. DNA damage responses: Mechanisms and roles in human disease: 2007 G.H.A. clowes memorial award lecture. Mol. Cancer Res. 2008, 6, 517-524. [CrossRef] [PubMed]
3. Ettinger, D.S, Wood, D.E, Akerley, W, Bazhenova, L.A, Borghaei, H, Camidge, D.R, Cheney, R.T, Chirieac, L.R, D’Amico, T.A, Dilling, T.J, et al. NCCN guidelines insights: Non-small cell lung cancer, version 4.2016. J. Natl. Compr. Cancer Netw. 2016, 14, 255-264.
4. Spira, A, Ettinger, D.S. Multidisciplinary management of lung cancer. N. Engl. J. Med. 2004, 350, 379-392. [PubMed]
5. Willers, H, Held, K.D. Introduction to clinical radiation biology. Hematol. Oncol. Clin. N. Am. 2006, 20, 1-24. [CrossRef] [PubMed]
6. Cobo, M, Isla, D, Massuti, B, Montes, A, Sanchez, J.M, Provencio, M, Vinolas, N, Paz-Ares, L, Lopez-Vivanco, G, Munoz, M.A, et al. Customizing cisplatin based on quantitative excision repair cross-complementing 1 mRNA expression: A phase III trial in non-small-cell lung cancer. J. Clin. Oncol. 2007, 25, 2747-2754. [CrossRef] [PubMed]
7. Bentzen, S.M, Overgaard, J. Patient-to-patient variability in the expression of radiation-induced normal tissue injury. Semin. Radiat. Oncol. 1994, 4, 68-80. [CrossRef]
8. Burdett, S, Pignon, J.P, Tierney, J, Tribodet, H, Stewart, L, le Pechoux, C, Auperin, A, le Chevalier, T, Stephens, R.J, Arriagada, R, et al. Adjuvant chemotherapy for resected early-stage non-small cell lung cancer. Cochrane Database Syst. Rev. 2015. [CrossRef]
9. Andreassen, C.N, Alsner, J, Overgaard, J. Does variability in normal tissue reactions after radiotherapy have a genetic basis—Where and how to look for it? Radiother. Oncol. 2002, 64, 131-140. [CrossRef]
10. Barnett, G.C, West, C.M, Dunning, A.M, Elliott, R.M, Coles, C.E, Pharoah, P.D, Burnet, N.G. Normal tissue reactions to radiotherapy: Towards tailoring treatment dose by genotype. Nat. Rev. Cancer 2009, 9, 134-142. [CrossRef] [PubMed]
11. Tung, M.C, Lin, P.L, Wang, Y.C, He, T.Y, Lee, M.C, Yeh, S.D, Chen, C.Y, Lee, H. Mutant p53 confers chemoresistance in non-small cell lung cancer by upregulating Nrf2. Oncotarget 2015, 6, 41692-41705. [PubMed]
12. Smela, M.E, Hamm, M.L, Henderson, P.T, Harris, C.M, Harris, T.M, Essigmann, J.M. The aflatoxin B formamidopyrimidine adduct plays a major role in causing the types of mutations observed in human hepatocellular carcinoma. Proc. Natl. Acad. Sci. USA 2002, 99, 6655-6660. [CrossRef] [PubMed]
13. Cadet, J, Ravanat, J.L, TavernaPorro, M, Menoni, H, Angelov, D. Oxidatively generated complex DNA damage: Tandem and clustered lesions. Cancer Lett. 2012, 327, 5-15. [CrossRef] [PubMed]
14. Roos, W.P, Kaina, B. DNA damage-induced cell death: From specific DNA lesions to the DNA damage response and apoptosis. Cancer Lett. 2013, 332, 237-248. [CrossRef] [PubMed]
15. Ciccia, A, Elledge, S.J. The DNA damage response: Making it safe to play with knives. Mol. Cell 2010, 40, 179-204. [CrossRef] [PubMed]
16. Miller, E.C, Miller, J.A. Mechanisms of chemical carcinogenesis. Cancer Am. Cancer Soc. 1981, 47, 1055-1064. [CrossRef]
17. Hoeijmakers, J.H. Genome maintenance mechanisms for preventing cancer. Nature 2001, 411, 366-374. [CrossRef] [PubMed]
18. Lips, J, Kaina, B. DNA double-strand breaks trigger apoptosis in p53-deficient fibroblasts. Carcinogenesis 2001, 22, 579-585. [CrossRef] [PubMed]
19. Fortini, P, Ferretti, C, Dogliotti, E. The response to DNA damage during differentiation: Pathways and consequences. Mutat. Res. 2013, 743-744, 160-168. [CrossRef] [PubMed]
20. Lord, C.J, Ashworth, A. The DNA damage response and cancer therapy. Nature 2012, 481, 287-294. [CrossRef] [PubMed]
21. Roos, W.P, Thomas, A.D, Kaina, B. DNA damage and the balance between survival and death in cancer biology. Nat. Rev. Cancer 2016, 16, 20-33. [CrossRef] [PubMed]
22. Rosell, R, Taron, M, Barnadas, A, Scagliotti, G, Sarries, C, Roig, B. Nucleotide excision repair pathways involved in Cisplatin resistance in non-small-cell lung cancer. Cancer Control 2003, 10, 297-305. [PubMed]
23. Rogakou, E.P, Pilch, D.R, Orr, A.H, Ivanova, V.S, Bonner, W.M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 1998, 273, 5858-5868. [CrossRef] [PubMed]
24. Helleday, T, Petermann, E, Lundin, C, Hodgson, B, Sharma, R.A. DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 2008, 8, 193-204. [CrossRef] [PubMed]
25. Christmann, M, Kaina, B. Transcriptional regulation of human DNA repair genes following genotoxic stress: Trigger mechanisms, inducible responses and genotoxic adaptation. Nucleic Acids Res. 2013, 41, 8403-8420. [CrossRef] [PubMed]
26. Yin, J.Y, Shen, J, Dong, Z.Z, Huang, Q, Zhong, M.Z, Feng, D.Y, Zhou, H.H, Zhang, J.T, Liu, Z.Q. Effect of eIF3a on response of lung cancer patients to platinum-based chemotherapy by regulating DNA repair. Clin. Cancer Res. 2011, 17, 4600-4609. [CrossRef] [PubMed]
27. Chen, J, Wu, L, Wang, Y, Yin, J, Li, X, Wang, Z, Li, H, Zou, T, Qian, C, Li, C, et al. Effect of transporter and DNA repair gene polymorphisms to lung cancer chemotherapy toxicity. Tumor Biol. 2015, 37, 2275-2284. [CrossRef] [PubMed]
28. Jin, J.Y, Wang, W, Ten, H.R, Chen, J, Bi, N, Sadek, R, Zhang, H, Lawrence, T.S, Kong, F.M. Use a survival model to correlate single-nucleotide polymorphisms of DNA repair genes with radiation dose-response in patients with non-small cell lung cancer. Radiother. Oncol. 2015, 117, 77-82. [CrossRef] [PubMed]
29. De Boer, J, Hoeijmakers, J.H. Nucleotide excision repair and human syndromes. Carcinogenesis 2000, 21, 453-460. [CrossRef] [PubMed]
30. Zhou, W, Gurubhagavatula, S, Liu, G, Park, S, Neuberg, D.S, Wain, J.C, Lynch, T.J, Su, L, Christiani, D.C. Excision repair cross-complementation group 1 polymorphism predicts overall survival in advanced non-small cell lung cancer patients treated with platinum-based chemotherapy. Clin. Cancer Res. 2004, 10, 4939-4943. [CrossRef] [PubMed]
31. Chang-Claude, J, Popanda, O, Tan, X.L, Kropp, S, Helmbold, I, von Fournier, D, Haase, W, Sautter-Bihl, M.L, Wenz, F, Schmezer, P, et al. Association between polymorphisms in the DNA repair genes, XRCC1, APE1, and XPD and acute side effects of radiotherapy in breast cancer patients. Clin. Cancer Res. 2005, 11, 4802-4809. [CrossRef] [PubMed]
32. Kang, C.H, Jang, B.G, Kim, D.W, Chung, D.H, Kim, Y.T, Jheon, S, Sung, S.W, Kim, J.H. The prognostic significance of ERCC1, BRCA1, XRCC1, and betaIII-tubulin expression in patients with non-small cell lung cancer treated by platinum- and taxane-based neoadjuvant chemotherapy and surgical resection. Lung Cancer 2010, 68, 478-483. [CrossRef] [PubMed]
33. Weaver, D.A, Crawford, E.L, Warner, K.A, Elkhairi, F, Khuder, S.A, Willey, J.C. ABCC5, ERCC2, XPA and XRCC1 transcript abundance levels correlate with cisplatin chemoresistance in non-small cell lung cancer cell lines. Mol. Cancer 2005, 4, 18. [CrossRef] [PubMed]
34. Bosken, C.H, Wei, Q, Amos, C.I, Spitz, M.R. An analysis of DNA repair as a determinant of survival in patients with non-small-cell lung cancer. J. Natl. Cancer Inst. 2002, 94, 1091-1099. [CrossRef] [PubMed]
35. Wang, L.E, Yin, M, Dong, Q, Stewart, D.J, Merriman, K.W, Amos, C.I, Spitz, M.R, Wei, Q. DNA repair capacity in peripheral lymphocytes predicts survival of patients with non-small-cell lung cancer treated with first-line platinum-based chemotherapy. J. Clin. Oncol. 2011, 29, 4121-4128. [CrossRef] [PubMed]
36. Wu, J, Liu, J, Zhou, Y, Ying, J, Zou, H, Guo, S, Wang, L, Zhao, N, Hu, J, Lu, D, et al. Predictive value of XRCC1 gene polymorphisms on platinum-based chemotherapy in advanced non-small cell lung cancer patients: A systematic review and meta-analysis. Clin. Cancer Res. 2012, 18, 3972-3981. [CrossRef] [PubMed]
37. Lunn, R.M, Langlois, R.G, Hsieh, L.L, Thompson, C.L, Bell, D.A. XRCC1 polymorphisms: Effects on aflatoxin B1-DNA adducts and glycophorin A variant frequency. Cancer Res. 1999, 59, 2557-2561. [PubMed]
38. Kelsey, C.R, Jackson, I.L, Langdon, S, Owzar, K, Hubbs, J, Vujaskovic, Z, Das, S, Marks, L.B. Analysis of single nucleotide polymorphisms and radiation sensitivity of the lung assessed with an objective radiologic endpoin. Clin. Lung Cancer 2013, 14, 267-274. [CrossRef] [PubMed]
39. Du, Y, Su, T, Zhao, L, Tan, X, Chang, W, Zhang, H, Cao, G. Associations of polymorphisms in DNA repair genes and MDR1 gene with chemotherapy response and survival of non-small cell lung cancer. PLoS ONE 2014, 9, e99843. [CrossRef] [PubMed]
40. Chen, J, Zhao, Q.W, Shi, G.M, Wang, L.R. XRCC1 Arg399Gln and clinical outcome of platinum-based treatment for advanced non-small cell lung cancer: A meta-analysis in 17 studies. J. Zhejiang Univ. Sci. B 2012, 13, 875-883. [CrossRef] [PubMed]
41. Peng, Y, Li, Z, Zhang, S, Xiong, Y, Cun, Y, Qian, C, Li, M, Ren, T, Xia, L, Cheng, Y, et al. Association of DNA base excision repair genes (OGG1, APE1 and XRCC1) polymorphisms with outcome to platinum-based chemotherapy in advanced nonsmall-cell lung cancer patients. Int. J. Cancer 2014, 135, 2687-2296. [CrossRef] [PubMed]
42. Yuan, Z, Li, J, Hu, R, Jiao, Y, Han, Y, Weng, Q. Predictive assessment in pharmacogenetics of XRCC1 gene on clinical outcomes of advanced lung cancer patients treated with platinum-based chemotherapy. Sci. Rep. 2015, 5, 16482. [CrossRef] [PubMed]
43. Sun, X, Li, F, Sun, N, Shukui, Q, Baoan, C, Jifeng, F, Lu, C, Zuhong, L, Hongyan, C, Yuan Dong, C, et al. Polymorphisms in XRCC1 and XPG and response to platinum-based chemotherapy in advanced non-small cell lung cancer patients. Lung Cancer 2009, 65, 230-236. [CrossRef] [PubMed]
44. Cui, X, Brenneman, M, Meyne, J, Oshimura, M, Goodwin, E.H, Chen, D.J. The XRCC2 and XRCC3 repairgenes are required for chromosome stability in mammalian cells. Mutat. Res. 1999, 434, 75-88. [CrossRef]
45. Yin, M, Liao, Z, Huang, Y.J, Liu, Z, Yuan, X, Gomez, D, Wang, L.E, Wei, Q. Polymorphisms of homologous recombination genes and clinical outcomes of non-small cell lung cancer patients treated with definitive radiotherapy. PLoS ONE 2011, 6, e20055. [CrossRef] [PubMed]
46. Qiu, M, Xu, L, Yang, X, Ding, X, Hu, J, Jiang, F, Xu, L, Yin, R. XRCC3 Thr241Met is associated with response to platinum-based chemotherapy but not survival in advanced non-small cell lung cancer. PLoS ONE 2013, 8, e77005. [CrossRef] [PubMed]
47. Yin, M, Liao, Z, Liu, Z, Wang, L.E, O’Reilly, M, Gomez, D, Li, M, Komaki, R, Wei, Q. Genetic variants of the nonhomologous end joining gene LIG4 and severe radiation pneumonitis in nonsmall cell lung cancer patients treated with definitive radiotherapy. Cancer Am. Cancer Soc. 2012, 118, 528-535.
48. Arriagada, R, Bergman, B, Dunant, A, le Chevalier, T, Pignon, J.P, Vansteenkiste, J. Cisplatin-based adjuvant chemotherapy in patients with completely resected non-small-cell lung cancer. N. Engl. J. Med. 2004, 350, 351-360. [PubMed]
49. Olaussen, K.A, Dunant, A, Fouret, P, Brambilla, E, Andre, F, Haddad, V, Taranchon, E, Filipits, M, Pirker, R, Popper, H.H, et al. DNA repair by ERCC1 in non-small-cell lung cancer and cisplatin-based adjuvant chemotherapy. N. Engl. J. Med. 2006, 355, 983-991. [CrossRef] [PubMed]
50. Sun, S, Shi, W, Wu, Z, Zhang, G, Yang, B.O, Jiao, S. Prognostic significance of the mRNA expression of ERCC1, RRM1, TUBB3 and TYMS genes in patients with non-small cell lung cancer. Exp. Ther. Med. 2015, 10, 937-941. [CrossRef] [PubMed]
51. Dong, J, Hu, Z, Shu, Y, Pan, S, Chen, W, Wang, Y, Hu, L, Jiang, Y, Dai, J, Ma, H, et al. Potentially functional polymorphisms in DNA repair genes and non-small-cell lung cancer survival: A pathway-based analysis. Mol. Carcinog. 2012, 51, 546-552. [CrossRef] [PubMed]
52. Wei, S.Z, Zhan, P, Shi, M.Q, Shi, Y, Qian, Q, Yu, L.K, Song, Y. Predictive value of ERCC1 and XPD polymorphism in patients with advanced non-small cell lung cancer receiving platinum-based chemotherapy: A systematic review and meta-analysis. Med. Oncol. 2011, 28, 315-321. [CrossRef] [PubMed]
53. Qin, Q, Zhang, C, Yang, X, Zhu, H, Yang, B, Cai, J, Cheng, H, Ma, J, Lu, J, Zhan, L, et al. Polymorphisms in XPD gene could predict clinical outcome of platinum-based chemotherapy for non-small cell lung cancer patients: A meta-analysis of 24 studies. PLoS ONE 2013, 8, e79864. [CrossRef] [PubMed]
54. Sullivan, I, Salazar, J, Majem, M, Pallares, C, Del, R.E, Paez, D, Baiget, M, Barnadas, A. Pharmacogenetics of the DNA repair pathways in advanced non-small cell lung cancer patients treated with platinum-based chemotherapy. Cancer Lett. 2014, 353, 160-166. [CrossRef] [PubMed]
55. Yang, M, Zhang, L, Bi, N, Ji, W, Tan, W, Zhao, L, Yu, D, Wu, C, Wang, L, Lin, D. Association of P53 and ATM polymorphisms with risk of radiation-induced pneumonitis in lung cancer patients treated with radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 2011, 79, 1402-1407. [CrossRef] [PubMed]
56. Zhang, L, Yang, M, Bi, N, Fang, M, Sun, T, Ji, W, Tan, W, Zhao, L, Yu, D, Lin, D, et al. ATM polymorphisms are associated with risk of radiation-induced pneumonitis. Int. J. Radiat. Oncol. Biol. Phys. 2010, 77, 1360-1368. [CrossRef] [PubMed]
57. Xiong, H, Liao, Z, Liu, Z, Xu, T, Wang, Q, Liu, H, Komaki, R, Gomez, D, Wang, L.E, Wei, Q. ATM polymorphisms predict severe radiation pneumonitis in patients with non-small cell lung cancer treated with definitive radiation therapy. Int. J. Radiat. Oncol. Biol. Phys. 2013, 85, 1066-1073. [CrossRef] [PubMed]
58. Liu, J, Wang, X, Ren, Y, Li, X, Zhang, X, Zhou, B. Effect of single nucleotide polymorphism Rs189037 in ATM gene on risk of lung cancer in Chinese: A case-control study. PLoS ONE 2014, 9, e115845. [CrossRef] [PubMed]
59. Zou, H.Z, Zhao, Y.Q. XPG polymorphisms are associated with prognosis of advanced non-small cell lung cancer treated with platinum-based doublet chemotherapy. Genet. Mol. Res. 2015, 14, 500-506. [CrossRef] [PubMed]
60. Lavin, M.F, Birrell, G, Chen, P, Kozlov, S, Scott, S, Gueven, N. ATM signaling and genomic stability in response to DNA damage. Mutat. Res. 2005, 569, 123-132. [CrossRef] [PubMed]
61. Canman, C.E, Lim, D.S, Cimprich, K.A, Taya, Y, Tamai, K, Sakaguchi, K, Appella, E, Kastan, M.B, Siliciano, J.D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998, 281, 1677-1679. [CrossRef] [PubMed]
62. Velimezi, G, Liontos, M, Vougas, K, Roumeliotis, T, Bartkova, J, Sideridou, M, Dereli-Oz, A, Kocylowski, M, Pateras, I.S, Evangelou, K, et al. Functional interplay between the DNA-damage-response kinase ATM and ARF tumour suppressor protein in human cancer. Nat. Cell Biol. 2013, 15, 967-977. [CrossRef] [PubMed]
63. Evangelou, K, Bartkova, J, Kotsinas, A, Pateras, I.S, Liontos, M, Velimezi, G, Kosar, M, Liloglou, T, Trougakos, I.P, Dyrskjot, L, et al. The DNA damage checkpoint precedes activation of ARF in response to escalating oncogenic stress during tumorigenesis. Cell Death Differ. 2013, 20, 1485-1497. [CrossRef] [PubMed]
64. Stankovic, T, Stewart, G.S, Byrd, P, Fegan, C, Moss, P.A, Taylor, A.M. ATM mutations in sporadic lymphoid tumours. Leuk. Lymphoma 2002, 43, 1563-1571. [CrossRef] [PubMed]
65. Wood, L.D, Parsons, D.W, Jones, S, Lin, J, Sjoblom, T, Leary, R.J, Shen, D, Boca, S.M, Barber, T, Ptak, J, et al. The genomic landscapes of human breast and colorectal cancers. Science 2007, 318, 1108-1113. [CrossRef] [PubMed]
66. Ambros, V. The functions of animal microRNAs. Nature 2004, 431, 350-355. [CrossRef] [PubMed]
67. Hu, H, Gatti, R.A. MicroRNAs: New players in the DNA damage response. J. Mol. Cell. Biol. 2011, 3, 151-158. [CrossRef] [PubMed]
68. Zhao, L, Lu, X, Cao, Y. MicroRNA and signal transduction pathways in tumor radiation response. Cell Signal. 2013, 25, 1625-1634. [CrossRef] [PubMed]
69. Shin, S, Cha, H.J, Lee, E.M, Lee, S.J, Seo, S.K, Jin, H.O, Park, I.C, Jin, Y.W, An, S. Alteration of miRNA profiles by ionizing radiation in A549 human non-small cell lung cancer cells. Int. J. Oncol. 2009, 35, 81-86. [PubMed]
70. El-Awady, R.A, Hersi, F, Al-Tunaiji, H, Saleh, E.M, Abdel-Wahab, A.H, Al, H.A, Suhail, M, El-Serafi, A, Al-Tel, T. Epigenetics and miRNA as predictive markers and targets for lung cancer chemotherapy. Cancer Biol. Ther. 2015, 16, 1056-1070. [CrossRef] [PubMed]
71. Okada, N, Lin, C.P, Ribeiro, M.C, Biton, A, Lai, G, He, X, Bu, P, Vogel, H, Jablons, D.M, Keller, A.C, et al. A positive feedback between p53 and miR-34 miRNAs mediates tumor suppression. Genes Dev. 2014, 28, 438-450. [CrossRef] [PubMed]
72. He, L, He, X, Lim, L.P, de Stanchina, E, Xuan, Z, Liang, Y, Xue, W, Zender, L, Magnus, J, Ridzon, D, et al. A microRNA component of the p53 tumour suppressor network. Nature 2007, 447, 1130-1134. [CrossRef] [PubMed]
73. Mert, U, Ozgur, E, Tiryakioglu, D, Dalay, N, Gezer, U. Induction of p53-inducible microRNA miR-34 by radiation and bleomycin are different. Front. Genet. 2012, 3, 220. [CrossRef] [PubMed]
74. Chakraborty, S, Mazumdar, M, Mukherjee, S, Bhattacharjee, P, Adhikary, A, Manna, A, Chakraborty, S, Khan, P, Sen, A, Das, T. Restoration of p53/miR-34a regulatory axis decreases survival advantage and ensures Bax-dependent apoptosis of non-small cell lung carcinoma cells. FEBS Lett. 2014, 588, 549-559. [CrossRef] [PubMed]
75. Cortez, M.A, Valdecanas, D, Niknam, S, Peltier, H.J, Diao, L, Giri, U, Komaki, R, Calin, G.A, Gomez, D.R, Chang, J.Y, et al. In vivo delivery of miR-34a sensitizes lung tumors to radiation through RAD51 regulation. Mol. Ther. Nucleic Acids 2015, 4, e270. [CrossRef] [PubMed]
76. Rahman, M, Lovat, F, Romano, G, Calore, F, Acunzo, M, Bell, E.H, Nana-Sinkam, P. miR-15b/16-2 regulates factors that promote p53 phosphorylation and augments the DNA damage response following radiation in the lung. J. Biol. Chem. 2014, 289, 26406-26416. [CrossRef] [PubMed]
77. Sarkar, F.H, Li, Y, Wang, Z, Kong, D, Ali, S. Implication of microRNAs in drug resistance for designing novel cancer therapy. Drug Resist. Updat. 2010, 13, 57-66. [CrossRef] [PubMed]
78. Yang, H, Luo, J, Liu, Z, Zhou, R, Luo, H. MicroRNA-138 regulates DNA damage response in small cell lung cancer cells by directly targeting H2AX. Cancer Investig. 2015, 33, 126-136. [CrossRef] [PubMed]
79. Sideridou, M, Zakopoulou, R, Evangelou, K, Liontos, M, Kotsinas, A, Rampakakis, E, Gagos, S, Kahata, K, Grabusic, K, Gkouskou, K, et al. Cdc6 expression represses E-cadherin transcription and activates adjacent replication origins. J. Cell Biol. 2011, 195, 1123-1140. [CrossRef] [PubMed]
80. Petrakis, T.G, Komseli, E.S, Papaioannou, M, Vougas, K, Polyzos, A, Myrianthopoulos, V, Mikros, E, Trougakos, I.P, Thanos, D, Branzei, D, et al. Exploring and exploiting the systemic effects of deregulated replication licensing. Semin. Cancer Biol. 2015. [CrossRef] [PubMed]
81. Galluzzi, L, Morselli, E, Vitale, I, Kepp, O, Senovilla, L, Criollo, A, Servant, N, Paccard, C, Hupe, P, Robert, T, et al. miR-181a and miR-630 regulate cisplatin-induced cancer cell death. Cancer Res. 2010, 70, 1793-1803. [CrossRef] [PubMed]
82. Wang, Q, Zhong, M, Liu, W, Li, J, Huang, J, Zheng, L. Alterations of microRNAs in cisplatin-resistant human non-small cell lung cancer cells (A549/DDP). Exp. Lung Res. 2011, 37, 427-434. [CrossRef] [PubMed]
83. Zhang, X, Zhu, J, Xing, R, Tie, Y, Fu, H, Zheng, X, Yu, B. miR-513a-3p sensitizes human lung adenocarcinoma cells to chemotherapy by targeting GSTP1. Lung Cancer 2012, 77, 488-494. [CrossRef] [PubMed]
84. Perkel, J.M. Visiting “noncodarnia”. Biotechniques 2013, 54, 303-304.
85. Smith, J.E, Alvarez-Dominguez, J.R, Kline, N, Huynh, N.J, Geisler, S, Hu, W, Coller, J, Baker, K.E. Translation of small open reading frames within unannotated RNA transcripts in Saccharomyces cerevisiae. Cell Rep. 2014, 7, 1858-1866. [CrossRef] [PubMed]
86. Ulitsky, I, Bartel, D.P. lincRNAs: Genomics, evolution, and mechanisms. Cell 2013, 154, 26-46. [CrossRef] [PubMed]
87. He, Y, Meng, X.M, Huang, C, Wu, B.M, Zhang, L, Lv, X.W, Li, J. Long noncoding RNAs: Novel insights into hepatocelluar carcinoma. Cancer Lett. 2014, 344, 20-27. [CrossRef] [PubMed]
88. Huarte, M, Guttman, M, Feldser, D, Garber, M, Koziol, M.J, Kenzelmann-Broz, D, Khalil, A.M, Zuk, O, Amit, I, Rabani, M, et al. A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 2010, 142, 409-419. [CrossRef] [PubMed]
89. Hall, J.R, Messenger, Z.J, Tam, H.W, Phillips, S.L, Recio, L, Smart, R.C. Long noncoding RNA lincRNA-p21 is the major mediator of UVB-induced and p53-dependent apoptosis in keratinocytes. Cell Death Dis. 2015, 6, e1700. [CrossRef] [PubMed]
90. Dimitrova, N, Zamudio, J.R, Jong, R.M, Soukup, D, Resnick, R, Sarma, K, Ward, A.J, Raj, A, Lee, J.T, Sharp, P.A, et al. LincRNA-p21 activates p21 in cis to promote Polycomb target gene expression and to enforce the G1/S checkpoint. Mol. Cell 2014, 54, 777-790. [CrossRef] [PubMed]
91. Sharma, V, Khurana, S, Kubben, N, Abdelmohsen, K, Oberdoerffer, P, Gorospe, M, Misteli, T. A BRCA1-interacting lncRNA regulates homologous recombination. EMBO Rep. 2015, 16, 1520-1534. [CrossRef] [PubMed]
92. Luo, H, Sun, Y, Wei, G, Luo, J, Yang, X, Liu, W, Guo, M, Chen, R. Functional characterization of long noncoding RNA Lnc_bc060912 in human lung carcinoma cells. Biochemistry 2015, 54, 2895-2902. [CrossRef] [PubMed]
93. Liu, J, Wan, L, Lu, K, Sun, M, Pan, X, Zhang, P, Lu, B, Liu, G, Wang, Z. The long noncoding RNA MEG3 contributes to Cisplatin resistance of human lung adenocarcinoma. PLoS ONE 2015, 10, e0114586. [CrossRef] [PubMed]
94. Liu, Z, Sun, M, Lu, K, Liu, J, Zhang, M, Wu, W, De, W, Wang, Z, Wang, R. The long noncoding RNA HOTAIR contributes to cisplatin resistance of human lung adenocarcinoma cells via downregualtion of p21(WAF1/CIP1) expression. PLoS ONE 2013, 8, e77293.
95. Yang, Y, Li, H, Hou, S, Hu, B, Liu, J, Wang, J. The noncoding RNA expression profile and the effect of lncRNA AK126698 on cisplatin resistance in non-small-cell lung cancer cell. PLoS ONE 2013, 8, e65309. [CrossRef] [PubMed]