Role of microRNA in response to ionizing radiations: Evidences and potential impact on clinical practice for radiotherapy

Molecules

Volumn 19, Issue 4, 2014, Pages 5379-5401

  Cellini, Francesco ^a   Morganti, Alessio G ^b,c   Genovesi, Domenico ^d   Silvestris, Nicola ^e   Valentini, Vincenzo ^c  

^a Radiation Oncology Campus Bio Medico University   (Italy)

^b CATHOLIC UNIVERSITY   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITY OF CHIETI   (Italy)

^e NATIONAL CANCER INSTITUTE GIOVANNI PAOLO II   (Italy)

Author keywords

DNA damage repair; MicroRNA; MiRNA; MiRNAs; Radiation; Radiosensibilization; Radiotherapy; Resistance; Review; Tumor

Indexed keywords

MICRORNA;

ANIMAL; DNA DAMAGE; DNA REPAIR; GENETICS; HUMAN; NEOPLASMS; PATHOLOGY; PHYSIOLOGY; RADIATION DOSE; RADIATION INJURY; SIGNAL TRANSDUCTION;

ANIMALS; DNA DAMAGE; DNA REPAIR; HUMANS; MICRORNAS; NEOPLASMS; RADIATION INJURIES; RADIATION TOLERANCE; SIGNAL TRANSDUCTION;

EID: 84899549916     PISSN: None     EISSN: 14203049     Source Type: Journal    
DOI: 10.3390/molecules19045379     Document Type: Review

References (104)

1. Hauptman, N.; Glavac, D. MicroRNAs and long non-coding RNAs: Prospects in diagnostics and therapy of cancer. Radiol. Oncol. 2013, 47, 311-318.
2. Kong, Y.W.; Ferland-McCollough, D.; Jackson, T.J.; Bushell, M. microRNAs in cancer management. Lancet Oncol. 2012, 13, e249-58.
3. Suzuki, H.; Maruyama, R.; Yamamoto, E.; Kai, M. Epigenetic alteration and microRNA dysregulation in cancer. Front. Genet. 2013, 4, 1-8.
4. Ma, R.; Jiang, T.; Kang, X. Circulating microRNAs in cancer: Origin, function and application. J. Exp. Clin. Cancer Res. 2012, 31, 38-47.
5. Friedman, R.C.; Farh, K.K.; Burge, C.B.; Bartel, D.P. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 2009, 19, 92-105.
6. Meng, W.; McElroy, J.P.; Volinia, S.; Palatini, J.; Warner, S.; Ayers, L.W.; Palanichamy, K.; Chakravarti, A.; Lautenschlaeger, T. Comparison of microRNA deep sequencing of matched formalin-fixed paraffin-embedded and fresh frozen cancer tissues. PLoS One 2013, 8, e64393.
7. Jensen, K.P.; Kranzler, H.R.; Stein, M.B.; Gelernter, J. The effects of a MAP2K5 microRNA target site SNP on risk for anxiety and depressive disorders. Am. J. Med. Genet. B Neuropsychiatr. Genet. 2014, 165, 175-183.
8. Iorio, M.V.; Croce, C.M. MicroRNA dysregulation in cancer: Diagnostics, monitoring and therapeutics. A comprehensive review. EMBO Mol. Med. 2012, 4, 143-159.
9. To, K.K. MicroRNA: A prognostic biomarker and a possible druggable target for circumventing multidrug resistance in cancer chemotherapy. J. Biomed. Sci. 2013, 20, 1-19.
10. Bovell, L.C.; Putcha, B.D.; Samuel, T.; Manne, U. Clinical implications of microRNAs in cancer. Biotech. Histochem. 2013, 88, 388-396.
11. Schoof, C.R.; Botelho, E.L.; Izzotti, A.; Vasques Ldos, R. MicroRNAs in cancer treatment and prognosis. Am. J. Cancer Res. 2012, 2, 414-433.
12. Janssen, H.L.; Reesink, H.W.; Lawitz, E.J.; Zeuzem, S.; Rodriguez-Torres, M.; Patel, K.; van der Meer, A.J.; Patick, A.K.; Chen, A.; Zhou, Y.; et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 2013, 368, 1685-1694.
13. Metheetrairut, C.; Slack, F.J. MicroRNAs in the ionizing radiation response and in radiotherapy. Curr. Opin. Genet. Dev. 2013, 23, 12-19.
14. Zhao, L.; Lu, X.; Cao, Y. MicroRNA and signal transduction pathways in tumor radiation response. Cell. Signal. 2013, 25, 1625-1634.
15. Simone, N.L.; Soule, B.P.; Ly, D.; Saleh, A.D.; Savage, J.E.; Degraff, W.; Cook, J.; Harris, C.C.; Gius, D.; Mitchell, J.B. Ionizing radiation-induced oxidative stress alters miRNA expression. PLoS One 2009, 4, e6377.
16. Templin, T.; Paul, S.; Amundson, S.A.; Young, E.F.; Barker, C.A.; Wolden, S.L.; Smilenov, L.B. Radiation-induced micro-RNA expression changes in peripheral blood cells of radiotherapy patients. Int. J. Radiat. Oncol. Biol. Phys. 2011, 80, 549-557.
17. Liu, J.; Zhu, H.; Yang, X.; Ge, Y.; Zhang, C.; Qin, Q.; Lu, J.; Zhan, L.; Cheng, H.; Sun, X. MicroRNA-21 is a novel promising target in cancer radiation therapy. Tumour Biol. 2014, in press.
18. Shi, Y.; Zhang, X.; Tang, X.; Wang, P.; Wang, H.; Wang, Y. MiR-21 is continually elevated long-term in the brain after exposure to ionizing radiation. Radiat. Res. 2012, 177, 124-128.
19. Bussing, I.; Slack, F.J.; Grosshans, H. let-7 microRNAs in development, stem cells and cancer. Trends Mol. Med. 2008, 14, 400-409.
20. Chaudhry, M.A. Radiation-induced microRNA: Discovery, functional analysis, and cancer radiotherapy. J. Cell. Biochem. 2013, 115, 436-449.
21. Johnson, S.M.; Grosshans, H.; Shingara, J.; Byrom, M.; Jarvis, R.; Cheng, A.; Labourier, E.; Reinert, K.L.; Brown, D.; Slack, F.J. RAS is regulated by the let-7 microRNA family. Cell 2005, 120, 635-647.
22. Chaudhry, M.A.; Omaruddin, R.A.; Kreger, B.; de Toledo, S.M.; Azzam, E.I. Micro RNA responses to chronic or acute exposures to low dose ionizing radiation. Mol. Biol. Rep. 2012, 39, 7549-7558.
23. Dickey, J.S.; Zemp, F.J.; Martin, O.A.; Kovalchuk, O. The role of miRNA in the direct and indirect effects of ionizing radiation. Radiat. Environ. Biophys. 2011, 50, 491-499.
24. Weidhaas, J.B.; Babar, I.; Nallur, S.M.; Trang, P.; Roush, S.; Boehm, M.; Gillespie, E.; Slack, F.J. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res. 2007, 67, 11111-11116.
25. Saleh, A.D.; Savage, J.E.; Cao, L.; Soule, B.P.; Ly, D.; DeGraff, W.; Harris, C.C.; Mitchell, J.B.; Simone, N.L. Cellular stress induced alterations in microRNA let-7a and let-7b expression are dependent on p53. PLoS One 2011, 6, e24429.
26. Chaudhry, M.A.; Sachdeva, H.; Omaruddin, R.A. Radiation-induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways. DNA Cell Biol. 2010, 29, 553-561.
27. Hermeking, H. p53 enters the microRNA world. Cancer Cell. 2007, 12, 414-418.
28. Nikiforova, M.N.; Gandhi, M.; Kelly, L.; Nikiforov, Y.E. MicroRNA dysregulation in human thyroid cells following exposure to ionizing radiation. Thyroid 2011, 21, 261-266.
29. Josson, S.; Sung, S.Y.; Lao, K.; Chung, L.W.; Johnstone, P.A. Radiation modulation of microRNA in prostate cancer cell lines. Prostate 2008, 68, 1599-1606.
30. Mert, U.; Ozgur, E.; Tiryakioglu, D.; Dalay, N.; Gezer, U. Induction of p53-inducible microRNA miR-34 by gamma radiation and bleomycin are different. Front. Genet. 2012, 3, 1-3.
31. Czochor, J.R.; Glazer, P.M. microRNAs in Cancer Cell Response to Ionizing Radiation. Antioxid. Redox Signal. 2014, in press.
32. Willers, H.; Held, K.D. Introduction to clinical radiation biology. Hematol. Oncol. Clin. North. Am. 2006, 20, 1-24.
33. Li, L.; Story, M.; Legerski, R.J. Cellular responses to ionizing radiation damage. Int J. Radiat. Oncol. Biol. Phys. 2001, 49, 1157-1162.
34. Gwak, H.S.; Kim, T.H.; Jo, G.H.; Kim, Y.J.; Kwak, H.J.; Kim, J.H.; Yin, J.; Yoo, H.; Lee, S.H.; Park, J.B. Silencing of microRNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS One 2012, 7, e47449.
35. Dent, P.; Yacoub, A.; Fisher, P.B.; Hagan, M.P.; Grant, S. MAPK pathways in radiation responses. Oncogene 2003, 22, 5885-5896.
36. Oh, J.S.; Kim, J.J.; Byun, J.Y.; Kim, I.A. Lin28-let7 modulates radiosensitivity of human cancer cells with activation of K-Ras. Int. J. Radiat. Oncol. Biol. Phys. 2010, 76, 5-8.
37. Wang, P.; Zou, F.; Zhang, X.; Li, H.; Dulak, A.; Tomko, R.J., Jr.; Lazo, J.S.; Wang, Z.; Zhang, L.; Yu, J. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res. 2009, 69, 8157-8165.
38. Hu, W.; Chan, C.S.; Wu, R.; Zhang, C.; Sun, Y.; Song, J.S.; Tang, L.H.; Levine, A.J.; Feng, Z. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol. Cell. 2010, 38, 689-699.
39. Le, M.T.; Teh, C.; Shyh-Chang, N.; Xie, H.; Zhou, B.; Korzh, V.; Lodish, H.F.; Lim, B. MicroRNA-125b is a novel negative regulator of p53. Gene. Dev. 2009, 23, 862-876.
40. Hu, H.; Du, L.; Nagabayashi, G.; Seeger, R.C.; Gatti, R.A. ATM is down-regulated by N-Myc-regulated microRNA-421. Proc. Natl. Acad. Sci. USA 2010, 107, 1506-1511.
41. Moskwa, P.; Buffa, F.M.; Pan, Y.; Panchakshari, R.; Gottipati, P.; Muschel, R.J.; Beech, J.; Kulshrestha, R.; Abdelmohsen, K.; Weinstock, D.M.; et al. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol. Cell. 2011, 41, 210-220.
42. Yan, D.; Ng, W.L.; Zhang, X.; Wang, P.; Zhang, Z.; Mo, Y.Y.; Mao, H.; Hao, C.; Olson, J.J.; Curran, W.J.; et al. Targeting DNA-PKcs and ATM with miR-101 sensitizes tumors to radiation. PLoS One 2010, 5, e11397.
43. Zheng, Z.; Wang, P.; Wang, H.; Zhang, X.; Wang, M.; Cucinotta, F.A.; Wang, Y. Combining heavy ion radiation and artificial microRNAs to target the homologous recombination repair gene efficiently kills human tumor cells. Int. J. Radiat. Oncol. Biol. Phys. 2013, 85, 466-471.
44. Mueller, A.C.; Sun, D.; Dutta, A. The miR-99 family regulates the DNA damage response through its target SNF2H. Oncogene 2013, 32, 1164-1172.
45. Wang, Y.; Huang, J.W.; Li, M.; Cavenee, W.K.; Mitchell, P.S.; Zhou, X.; Tewari, M.; Furnari, F.B.; Taniguchi, T. MicroRNA-138 modulates DNA damage response by repressing histone H2AX expression. Mol. Cancer Res. 2011, 9, 1100-1111.
46. Zhao, L.; Bode, A.M.; Cao, Y.; Dong, Z. Regulatory mechanisms and clinical perspectives of miRNA in tumor radiosensitivity. Carcinogenesis 2012, 33, 2220-2227.
47. Kraemer, A.; Anastasov, N.; Angermeier, M.; Winkler, K.; Atkinson, M.J.; Moertl, S. MicroRNA-mediated processes are essential for the cellular radiation response. Radiat. Res. 2011, 176, 575-586.
48. Surova, O.; Akbar, N.S.; 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.
49. Francia, S.; Michelini, F.; Saxena, A.; Tang, D.; de Hoon, M.; Anelli, V.; Mione, M.; Carninci, P.; d'Adda di Fagagna, F. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 2012, 488, 231-235.
50. Wagner-Ecker, M.; Schwager, C.; Wirkner, U.; Abdollahi, A.; Huber, P.E. MicroRNA expression after ionizing radiation in human endothelial cells. Radiat. Oncol. 2010, 5, 1-10.
51. Sozzi, G.; Boeri, M.; Rossi, M.; Verri, C.; Suatoni, P.; Bravi, F.; Roz, L.; Conte, D.; Grassi, M.; Sverzellati, N.; et al. Clinical utility of a plasma-based miRNA signature classifier within computed tomography lung cancer screening: A correlative MILD trial study. J. Clin. Oncol. 2014, 32, 768-773.
52. Wang, J.; Zhang, K.Y.; Liu, S.M.; Sen, S. Tumor-Associated Circulating MicroRNAs as Biomarkers of Cancer. Molecules 2014, 19, 1912-1938.
53. Vicentini, C.; Fassan, M.; D'Angelo, E.; Corbo, V.; Silvestris, N.; Nuovo, G.J.; Scarpa, A. Clinical application of microrna testing in neuroendocrine tumors of the gastrointestinal tract. Molecules 2014, 19, 2458-2468.
54. O'Kelly, F.; Marignol, L.; Meunier, A.; Lynch, T.H.; Perry, A.S.; Hollywood, D. MicroRNAs as putative mediators of treatment response in prostate cancer. Nat. Rev. Urol. 2012, 9, 397-407.
55. Walter, B.A.; Valera, V.A.; Pinto, P.A.; Merino, M.J. Comprehensive microRNA Profiling of Prostate Cancer. J. Cancer. 2013, 4, 350-357.
56. Kelly, B.D.; Miller, N.; Healy, N.A.; Walsh, K.; Kerin, M.J. A review of expression profiling of circulating microRNAs in men with prostate cancer. BJU Int. 2013, 111, 17-21.
57. Leung, C.M.; Li, S.C.; Chen, T.W.; Ho, M.R.; Hu, L.Y.; Liu, W.S.; Wu, T.T.; Hsu, P.C.; Chang, H.T.; Tsai, K.W. Comprehensive microRNA profiling of prostate cancer cells after ionizing radiation treatment. Oncol. Rep. 2014, 31, 1067-1078.
58. Li, B.; Shi, X.B.; Nori, D.; Chao, C.K.; Chen, A.M.; Valicenti, R.; White Rde, V. Down-regulation of microRNA 106b is involved in p21-mediated cell cycle arrest in response to radiation in prostate cancer cells. Prostate 2011, 71, 567-574.
59. John-Aryankalayil, M.; Palayoor, S.T.; Makinde, A.Y.; Cerna, D.; Simone, C.B.; Falduto, M.T.; Magnuson, S.R.; Coleman, C.N. Fractionated radiation alters oncomir and tumor suppressor miRNAs in human prostate cancer cells. Radiat. Res. 2012, 178, 105-117.
60. Schultz, N.A.; Dehlendorff, C.; Jensen, B.V.; Bjerregaard, J.K.; Nielsen, K.R.; Bojesen, S.E.; Calatayud, D.; Nielsen, S.E.; Yilmaz, M.; Hollander, N.H.; et al. MicroRNA biomarkers in whole blood for detection of pancreatic cancer. JAMA 2014, 311, 392-404.
61. Lou, E.; Subramanian, S.; Steer, C.J. Pancreatic cancer: Modulation of KRAS, MicroRNAs, and intercellular communication in the setting of tumor heterogeneity. Pancreas 2013, 42, 1218-1226.
62. Greither, T.; Grochola, L.F.; Udelnow, A.; Lautenschlager, C.; Wurl, P.; Taubert, H. Elevated expression of microRNAs 155, 203, 210 and 222 in pancreatic tumors is associated with poorer survival. Int. J. Cancer. 2010, 126, 73-80.
63. Ji, Q.; Hao, X.; Zhang, M.; Tang, W.; Yang, M.; Li, L.; Xiang, D.; Desano, J.T.; Bommer, G.T.; Fan, D.; et al. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 2009, 4, e6816.
64. Wang, P.; Zhang, J.; Zhang, L.; Zhu, Z.; Fan, J.; Chen, L.; Zhuang, L.; Luo, J.; Chen, H.; Liu, L.; et al. MicroRNA 23b regulates autophagy associated with radioresistance of pancreatic cancer cells. Gastroenterology 2013, 145, 1133-1143.
65. Paglin, S.; Hollister, T.; Delohery, T.; Hackett, N.; McMahill, M.; Sphicas, E.; Domingo, D.; Yahalom, J. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001, 61, 439-444.
66. Zhang, C.; Kang, C.; Wang, P.; Cao, Y.; Lv, Z.; Yu, S.; Wang, G.; Zhang, A.; Jia, Z.; Han, L.; et al. MicroRNA-221 and -222 regulate radiation sensitivity by targeting the PTEN pathway. Int. J. Radiat. Oncol. Biol. Phys. 2011, 80, 240-248.
67. Wei, F.; Liu, Y.; Guo, Y.; Xiang, A.; Wang, G.; Xue, X.; Lu, Z. miR-99b-targeted mTOR induction contributes to irradiation resistance in pancreatic cancer. Mol. Cancer 2013, 12, doi:10.1186/1476-4598-12-81.
68. Caron, E.; Ghosh, S.; Matsuoka, Y.; Ashton-Beaucage, D.; Therrien, M.; Lemieux, S.; Perreault, C.; Roux, P.P.; Kitano, H. A comprehensive map of the mTOR signaling network. Mol. Syst. Biol. 2010, 6, 1-14.
69. Guertin, D.A.; Sabatini, D.M. Defining the role of mTOR in cancer. Cancer Cell. 2007, 12, 9-22.
70. Drakaki, A.; Iliopoulos, D. MicroRNA-gene signaling pathways in pancreatic cancer. Biomed. J. 2013, 36, 200-208.
71. Wu, C.; Li, M.; Hu, C.; Duan, H. Clinical significance of serum miR-223, miR-25 and miR-375 in patients with esophageal squamous cell carcinoma. Mol. Biol. Rep. 2014, 41, 1257-1266.
72. Xu, X.L.; Jiang, Y.H.; Feng, J.G.; Su, D.; Chen, P.C.; Mao, W.M. MicroRNA-17, microRNA- 18a, and microRNA-19a are prognostic indicators in esophageal squamous cell carcinoma. Ann. Thorac. Surg. 2013, 97,1037-1045.
73. Yu, H.; Duan, B.; Jiang, L.; Lin, M.; Sheng, H.; Huang, J.; Gao, H. Serum miR-200c and clinical outcome of patients with advanced esophageal squamous cancer receiving platinum-based chemotherapy. Am. J. Transl Res. 2013, 6, 71-77.
74. Wu, C.; Li, M.; Hu, C.; Duan, H. Prognostic role of microRNA polymorphisms in patients with advanced esophageal squamous cell carcinoma receiving platinum-based chemotherapy. Cancer Chemother. Pharmacol. 2014, 73, 335-341.
75. Zheng, Z.F.; Su, H.F.; Zou, Y.; Peng, Z.; Wu, S.X. Expression profiles of microRNAs in radioresistant esophageal cell line. Zhonghua Yi Xue Za Zhi 2011, 91, 639-642.
76. Su, H.; Jin, X.; Zhang, X.; Xue, S.; Deng, X.; Shen, L.; Fang, Y.; Xie, C. Identification of microRNAs involved in the radioresistance of esophageal cancer cells. Cell Biol. Int. 2013, 38, 318-325.
77. Huang, S.; Li, X.Q.; Chen, X.; Che, S.M.; Chen, W.; Zhang, X.Z. Inhibition of microRNA-21 increases radiosensitivity of esophageal cancer cells through phosphatase and tensin homolog deleted on chromosome 10 activation. Dis. Esophagus 2013, 26, 823-831.
78. Lynam-Lennon, N.; Reynolds, J.V.; Marignol, L.; Sheils, O.M.; Pidgeon, G.P.; Maher, S.G. MicroRNA-31 modulates tumour sensitivity to radiation in oesophageal adenocarcinoma. J. Mol. Med. 2012, 90, 1449-1458.
79. Wang, X.C.; Zhang, Z.B.; Wang, Y.Y.; Wu, H.Y.; Li, D.G.; Meng, A.M.; Fan, F.Y. Increased miRNA-22 expression sensitizes esophageal squamous cell carcinoma to irradiation. J. Radiat. Res. 2013, 54, 401-408.
80. Yongchun, Z.; Linwei, T.; Xicai, W.; Lianhua, Y.; Guangqiang, Z.; Ming, Y.; Guangjian, L.; Yujie, L.; Yunchao, H. MicroRNA-195 inhibits non-small cell lung cancer cell proliferation, migration and invasion by targeting MYB. Cancer Lett. 2014, 347, 65-74.
81. Meng, W.; Ye, Z.; Cui, R.; Perry, J.; Dedousi-Huebner, V.; Huebner, A.; Wang, Y.; Li, B.; Volinia, S.; Nakanishi, H.; et al. MicroRNA-31 predicts the presence of lymph node metastases and survival in patients with lung adenocarcinoma. Clin. Cancer Res. 2013, 19, 5423-5433.
82. 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.
83. Wang, X.C.; Du, L.Q.; Tian, L.L.; Wu, H.L.; Jiang, X.Y.; Zhang, H.; Li, D.G.; Wang, Y.Y.; Wu, H.Y.; She, Y.; et al. Expression and function of miRNA in postoperative radiotherapy sensitive and resistant patients of non-small cell lung cancer. Lung Cancer 2011, 72, 92-99.
84. Arora, H.; Qureshi, R.; Jin, S.; Park, A.K.; Park, W.Y. miR-9 and let-7g enhance the sensitivity to ionizing radiation by suppression of NFkappaB1. Exp. Mol. Med. 2011, 43, 298-304.
85. Liu, Y.J.; Lin, Y.F.; Chen, Y.F.; Luo, E.C.; Sher, Y.P.; Tsai, M.H.; Chuang, E.Y.; Lai, L.C. MicroRNA-449a enhances radiosensitivity in CL1-0 lung adenocarcinoma cells. PLoS One 2013, 8, e62383.
86. Di Francesco, A.; de Pitta, C.; Moret, F.; Barbieri, V.; Celotti, L.; Mognato, M. The DNA-damage response to gamma-radiation is affected by miR-27a in A549 cells. Int. J. Mol. Sci. 2013, 14, 17881-17896.
87. Chen, S.; Wang, H.; Ng, W.L.; Curran, W.J.; Wang, Y. Radiosensitizing effects of ectopic miR-101 on non-small-cell lung cancer cells depend on the endogenous miR-101 level. Int J. Radiat. Oncol. Biol. Phys. 2011, 81, 1524-1529.
88. Babar, I.A.; Czochor, J.; Steinmetz, A.; Weidhaas, J.B.; Glazer, P.M.; Slack, F.J. Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol. Ther. 2011, 12, 908-914.
89. Grosso, S.; Doyen, J.; Parks, S.K.; Bertero, T.; Paye, A.; Cardinaud, B.; Gounon, P.; Lacas-Gervais, S.; Noel, A.; Pouyssegur, J.; et al. MiR-210 promotes a hypoxic phenotype and increases radioresistance in human lung cancer cell lines. Cell Death Dis. 2013, 4, e544.
90. Duan, W.; Xu, Y.; Dong, Y.; Cao, L.; Tong, J.; Zhou, X. Ectopic expression of miR-34a enhances radiosensitivity of non-small cell lung cancer cells, partly by suppressing the LyGDI signaling pathway. J. Radiat. Res. 2013, 54, 611-619.
91. Balca-Silva, J.; Sousa Neves, S.; Goncalves, A.C.; Abrantes, A.M.; Casalta-Lopes, J.; Botelho, M.F.; Sarmento-Ribeiro, A.B.; Silva, H.C. Effect of miR-34b overexpression on the radiosensitivity of non-small cell lung cancer cell lines. Anticancer Res. 2012, 32, 1603-1609.
92. Kang, J.; Kim, E.; Kim, W.; Seong, K.M.; Youn, H.; Kim, J.W.; Kim, J.; Youn, B. Rhamnetin and cirsiliol induce radiosensitization and inhibition of epithelial-mesenchymal transition (EMT) by miR-34a-mediated suppression of Notch-1 expression in non-small cell lung cancer cell lines. J. Biol. Chem. 2013, 288, 27343-27357.
93. Liu, Z.L.; Wang, H.; Liu, J.; Wang, Z.X. MicroRNA-21 (miR-21) expression promotes growth, metastasis, and chemo- or radioresistance in non-small cell lung cancer cells by targeting PTEN. Mol. Cell. Biochem. 2013, 372, 35-45.
94. Wang, X.C.; Wang, W.; Zhang, Z.B.; Zhao, J.; Tan, X.G.; Luo, J.C. Overexpression of miRNA-21 promotes radiation-resistance of non-small cell lung cancer. Radiat. Oncol. 2013, 8, 1-9.
95. Drebber, U.; Lay, M.; Wedemeyer, I.; Vallbohmer, D.; Bollschweiler, E.; Brabender, J.; Monig, S.P.; Holscher, A.H.; Dienes, H.P.; Odenthal, M. Altered levels of the onco-microRNA 21 and the tumor-supressor microRNAs 143 and 145 in advanced rectal cancer indicate successful neoadjuvant chemoradiotherapy. Int. J. Oncol. 2011, 39, 409-415.
96. Della Vittoria Scarpati, G.; Falcetta, F.; Carlomagno, C.; Ubezio, P.; Marchini, S.; de Stefano, A.; Singh, V.K.; D'Incalci, M.; de Placido, S.; Pepe, S. A specific miRNA signature correlates with complete pathological response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer. Int. J. Radiat. Oncol. Biol. Phys. 2012, 83, 1113-1119.
97. Svoboda, M.; Sana, J.; Fabian, P.; Kocakova, I.; Gombosova, J.; Nekvindova, J.; Radova, L.; Vyzula, R.; Slaby, O. MicroRNA expression profile associated with response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer patients. Radiat. Oncol. 2012, 7, 1-7.
98. Ahmed, F.E.; Vos, P.W.; Jeffries, C.; Wiley, J.E.; Weidner, D.A.; Mota, H.; Bonnerup, C.; Sibata, C.; Allison, R.R. Differences in mRNA and microRNA microarray expression profiles in human colon adenocarcinoma HT-29 cells treated with either Intensity-modulated Radiation Therapy (IMRT), or Conventional Radiation Therapy (RT). Cancer Genomics Proteomics 2009, 6, 109-127.
99. Lutgens, L.C.; Deutz, N.E.; Gueulette, J.; Cleutjens, J.P.; Berger, M.P.; Wouters, B.G.; von Meyenfeldt, M.F.; Lambin, P. Citrulline: A physiologic marker enabling quantitation and monitoring of epithelial radiation-induced small bowel damage. Int. J. Radiat. Oncol. Biol. Phys. 2003, 57, 1067-1074.
100. Lutgens, L.; Lambin, P. Biomarkers for radiation-induced small bowel epithelial damage: An emerging role for plasma Citrulline. World J. Gastroenterol. 2007, 13, 3033-3042.
101. Talwar, S.; House, R.; Sundaramurthy, S.; Balasubramanian, S.; Yu, H.; Palanisamy, V. Inhibition of caspases protects mice from radiation induced oral mucositis and abolishes the cleavage of RNA binding protein HuR. J. Biol. Chem. 2014, 289, 3487-3500.
102. Hamama, S.; Noman, M.Z.; Gervaz, P.; Delanian, S.; Vozenin, M.C. MiR-210: A potential therapeutic target against radiation-induced enteropathy. Radiother. Oncol. 2013, in press.
103. Sullivan, J.M.; Prasanna, P.G.; Grace, M.B.; Wathen, L.K.; Wallace, R.L.; Koerner, J.F.; Coleman, C.N. Assessment of biodosimetry methods for a mass-casualty radiological incident: Medical response and management considerations. Health Phys. 2013, 105, 540-554.
104. Sert, F. MicroRNA changes in advanced radiotherapy techniques and its effect to secondary cancers. Med. Hypotheses 2012, 79, 421-422.