MicroRNAs in cancer cell response to ionizing radiation

Antioxidants and Redox Signaling

Volumn 21, Issue 2, 2014, Pages 293-312

  Czochor, Jennifer R ^a   Glazer, Peter M ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DOUBLE STRANDED DNA; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

APOPTOSIS; BIOGENESIS; CANCER CELL; CELL CYCLE CHECKPOINT; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENE CONTROL; GENE EXPRESSION PROFILING; IONIZING RADIATION; PRIORITY JOURNAL; RADIATION RESPONSE; REVIEW; SIGNAL TRANSDUCTION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOPLASMS; PATHOLOGY;

DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; HUMANS; MICRORNAS; NEOPLASMS; RADIATION, IONIZING; SIGNAL TRANSDUCTION;

EID: 84899542792     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5718     Document Type: Review

References (174)

1. Adlakha YK and Saini N. MicroRNA-128 downregulates Bax and induces apoptosis in human embryonic kidney cells. Cell Mol Life Sci 68: 1415-1428, 2011
2. Afanasyeva EA, Mestdagh P, Kumps C, Vandesompele J, Ehemann V, Theissen J, Fischer M, Zapatka M, Brors B, Savelyeva L, Sagulenko V, Speleman F, Schwab M, and Westermann F. MicroRNA miR-885-5p targets CDK2 and MCM5, activates p53 and inhibits proliferation and survival. Cell Death Differ 18: 974-984, 2011
3. Ambs S, Prueitt RL, Yi M, Hudson RS, Howe TM, Petrocca F, Wallace TA, Liu CG, Volinia S, Calin GA, Yfantis HG, Stephens RM, and Croce CM. Genomic profiling of microRNA and messenger RNA reveals deregulated microRNA expression in prostate cancer. Cancer Res 68: 6162-6170, 2008
4. Anastasov N, Hofig I, Vasconcellos IG, Rappl K, Braselmann H, Ludyga N, Auer G, Aubele M, and Atkinson MJ. Radiation resistance due to high expression of miR-21 and G2/M checkpoint arrest in breast cancer cells. Radiat Oncol 7: 206, 2012
5. Babar IA, Czochor J, Steinmetz A, Weidhaas JB, Glazer PM, and Slack FJ. Inhibition of hypoxia-induced miR-155 radiosensitizes hypoxic lung cancer cells. Cancer Biol Ther 12: 908-914, 2011
6. Bertero T, Gastaldi C, Bourget-Ponzio I, Mari B, Meneguzzi G, Barbry P, Ponzio G, and Rezzonico R. CDC25A targeting by miR-483-3p decreases CCND-CDK4/6 assembly and contributes to cell cycle arrest. Cell Death Differ 20: 800-811, 2013
7. Bhattacharya A, Schmitz U, Wolkenhauer O, Schonherr M, Raatz Y, and Kunz M. Regulation of cell cycle checkpoint kinase WEE1 by miR-195 in malignant melanoma. Oncogene 32: 3175-3183, 2012
8. Butz H, Liko I, Czirjak S, Igaz P, Khan MM, Zivkovic V, Balint K, Korbonits M, Racz K, and Patocs A. Downregulation of Wee1 kinase by a specific subset of micro- RNA in human sporadic pituitary adenomas. J Clin Endocrinol Metab 95: E181-E191, 2010
9. Cai N, Wang YD, and Zheng PS. The microRNA-302-367 cluster suppresses the proliferation of cervical carcinoma cells through the novel target AKT1. RNA 19: 85-95, 2013
10. Calin GA, Dumitru CD, Shimizu M, Bichi R, Zupo S, Noch E, Aldler H, Rattan S, Keating M, Rai K, Rassenti L, Kipps T, Negrini M, Bullrich F, and Croce CM. Frequent deletions and down-regulation of micro- RNA genes miR15 and miR16 at 13q14 in chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 99: 15524-15529, 2002 (Pubitemid 35403967)
11. Catucci I, Yang R, Verderio P, Pizzamiglio S, Heesen L, Hemminki K, Sutter C, Wappenschmidt B, Dick M, Arnold N, Bugert P, Niederacher D, Meindl A, Schmutzler RK, Bartram CC, Ficarazzi F, Tizzoni L, Zaffaroni D, Manoukian S, Barile M, Pierotti MA, Radice P, Burwinkel B, and Peterlongo P. Evaluation of SNPs in miR-146a, miR196a2 and miR-499 as low-penetrance alleles in German and Italian familial breast cancer cases. Hum Mutat 31: E1052-E1057, 2010
12. Cazanave SC, Mott JL, Elmi NA, Bronk SF, Masuoka HC, Charlton MR, and Gores GJ. A role for miR-296 in the regulation of lipoapoptosis by targeting PUMA. J Lipid Res 52: 1517-1525, 2011
13. Cha HJ, Shin S, Yoo H, Lee EM, Bae S, Yang KH, Lee SJ, Park IC, Jin YW, and An S. Identification of ionizing radiation-responsive microRNAs in the IM9 human B lymphoblastic cell line. Int J Oncol 34: 1661-1668, 2009
14. Chang TC, Wentzel EA, Kent OA, Ramachandran K, Mullendore M, Lee KH, Feldmann G, Yamakuchi M, Ferlito M, Lowenstein CJ, Arking DE, Beer MA, Maitra A, and Mendell JT. Transactivation of miR-34a by p53 broadly influences gene expression and promotes apoptosis. Mol Cell 26: 745-752, 2007 (Pubitemid 46856245)
15. Chaudhry MA and Omaruddin RA. Differential regulation of microRNA expression in irradiated and bystander cells. Mol Biol (Mosk) 46: 634-643, 2012
16. Chaudhry MA, Omaruddin RA, Brumbaugh CD, Tariq MA, and Pourmand N. Identification of radiation-induced microRNA transcriptome by next-generation massively parallel sequencing. J Radiat Res 54: 808-822, 2013
17. Chaudhry MA, Omaruddin RA, Kreger B, de Toledo SM, and Azzam EI. Micro RNA responses to chronic or acute exposures to low dose ionizing radiation. Mol Biol Rep 39: 7549-7558, 2012
18. Chaudhry MA, Sachdeva H, and Omaruddin RA. Radiation- induced micro-RNA modulation in glioblastoma cells differing in DNA-repair pathways. DNA Cell Biol 29: 553-561, 2010
19. Chen G, Zhu W, Shi D, Lv L, Zhang C, Liu P, and Hu W. MicroRNA-181a sensitizes human malignant glioma U87MG cells to radiation by targeting Bcl-2. Oncol Rep 23: 997-1003, 2010
20. Chen J, Zhang X, Lentz C, Abi-Daoud M, Pare GC, Yang X, Feilotter HE, and Tron VA. miR-193b Regulates Mcl-1 in Melanoma. Am J Pathol 179: 2162-2168, 2011
21. Chen S, Wang H, Ng WL, Curran WJ, and Wang Y. Radiosensitizing effects of ectopic miR-101 on non-smallcell lung cancer cells depend on the endogenous miR-101 level. Int J Radiat Oncol Biol Phys 81: 1524-1529, 2011
22. Chen X, Guo X, Zhang H, Xiang Y, Chen J, Yin Y, Cai X, Wang K, Wang G, Ba Y, Zhu L, Wang J, Yang R, Zhang Y, Ren Z, Zen K, Zhang J, and Zhang CY. Role of miR- 143 targeting KRAS in colorectal tumorigenesis. Oncogene 28: 1385-1392, 2009
23. Chen Y, Song Y, Wang Z, Yue Z, Xu H, Xing C, and Liu Z. Altered expression of MiR-148a and MiR-152 in gastrointestinal cancers and its clinical significance. J Gastrointest Surg 14: 1170-1179, 2010
24. Chen Z, Chen LY, Dai HY, Wang P, Gao S, and Wang K. miR-301a promotes pancreatic cancer cell proliferation by directly inhibiting Bim expression. J Cell Biochem 113: 3229-3235, 2012
25. Chien WW, Domenech C, Catallo R, Kaddar T, Magaud JP, Salles G, and Ffrench M. Cyclin-dependent kinase 1 expression is inhibited by p16(INK4a) at the posttranscriptional level through the microRNA pathway. Oncogene 30: 1880-1891, 2011
26. Chun-Zhi Z, Lei H, An-Ling Z, Yan-Chao F, Xiao Y, Guang-Xiu W, Zhi-Fan J, Pei-Yu P, Qing-Yu Z, and Chun-Sheng K. MicroRNA-221 and microRNA-222 regulate gastric carcinoma cell proliferation and radioresistance by targeting PTEN. BMC Cancer 10: 367, 2010
27. Ciafre SA, Galardi S, Mangiola A, Ferracin M, Liu CG, Sabatino G, Negrini M, Maira G, Croce CM, and Farace MG. Extensive modulation of a set of microRNAs in primary glioblastoma. Biochem Biophys Res Commun 334: 1351-1358, 2005 (Pubitemid 41074723)
28. Crawford M, Batte K, Yu L, Wu X, Nuovo GJ, Marsh CB, Otterson GA, and Nana-Sinkam SP. MicroRNA 133B targets pro-survival molecules MCL-1 and BCL2L2 in lung cancer. Biochem Biophys Res Commun 388: 483-489, 2009
29. Creevey L, Ryan J, Harvey H, Bray IM, Meehan M, Khan AR, and Stallings RL. MicroRNA-497 increases apoptosis in MYCN amplified neuroblastoma cells by targeting the key cell cycle regulator WEE1. Mol Cancer 12: 23, 2013
30. Crosby M, Kulshreshtha R, Ivan M, and Glazer P. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 69: 1221-1229, 2009
31. Dar AA, Majid S, Rittsteuer C, de Semir D, Bezrookove V, Tong S, Nosrati M, Sagebiel R, Miller JR, 3rd, and Kashani-Sabet M. The role of miR-18b in MDM2-p53 pathway signaling and melanoma progression. J Natl Cancer Inst 105: 433-442, 2013
32. de Oliveira PE, Zhang L, Wang Z, and Lazo JS. Hypoxiamediated regulation of Cdc25A phosphatase by p21 and miR-21. Cell Cycle 8: 3157-3164, 2009
33. Deckbar D, Jeggo PA, and Lobrich M. Understanding the limitations of radiation-induced cell cycle checkpoints. Crit Rev Biochem Mol Biol 46: 271-283, 2011
34. Dent P, Yacoub A, Contessa J, Caron R, Amorino G, Valerie K, Hagan MP, Grant S, and Schmidt-Ullrich R. Stress and radiation-induced activation of multiple intracellular signaling pathways. Radiat Res 159: 283-300, 2003 (Pubitemid 36314943)
35. Ding DP, Chen ZL, Zhao XH, Wang JW, Sun J, Wang Z, Tan FW, Tan XG, Li BZ, Zhou F, Shao K, Li N, Qiu B, and He J. miR-29c induces cell cycle arrest in esophageal squamous cell carcinoma by modulating cyclin E expression. Carcinogenesis 32: 1025-1032, 2011
36. El Ouaamari A, Baroukh N, Martens GA, Lebrun P, Pipeleers D, and van Obberghen E. miR-375 targets 3- phosphoinositide-dependent protein kinase-1 and regulates glucose-induced biological responses in pancreatic betacells. Diabetes 57: 2708-2717, 2008
37. Eulalio A, Huntzinger E, Nishihara T, Rehwinkel J, Fauser M, and Izaurralde E. Deadenylation is a widespread effect of miRNA regulation. RNA 15: 21-32, 2009
38. Fang J, Song XW, Tian J, Chen HY, Li DF, Wang JF, Ren AJ, Yuan WJ, and Lin L. Overexpression of microRNA- 378 attenuates ischemia-induced apoptosis by inhibiting caspase-3 expression in cardiac myocytes. Apoptosis 17: 410-423, 2012
39. Fang Y, Xue JL, Shen Q, Chen J, and Tian L. MicroRNA- 7 inhibits tumor growth and metastasis by targeting the phosphoinositide 3-kinase/Akt pathway in hepatocellular carcinoma. Hepatology 55: 1852-1862, 2012
40. Friedman RC, Farh KK, Burge CB, and Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19: 92-105, 2009
41. Garcia AI, Buisson M, Bertrand P, Rimokh R, Rouleau E, Lopez BS, Lidereau R, Mikaelian I, and Mazoyer S. Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers. EMBO Mol Med 3: 279-290, 2011
42. Garcia AI, Cox DG, Barjhoux L, Verny-Pierre C, Barnes D, Antoniou AC, Stoppa-Lyonnet D, Sinilnikova OM, and Mazoyer S. The rs2910164:G C SNP in the MIR146A gene is not associated with breast cancer risk in BRCA1 and BRCA2 mutation carriers. Hum Mutat 32: 1004- 1007, 2011
43. Giovannetti E, Funel N, Peters GJ, Del Chiaro M, Erozenci LA, Vasile E, Leon LG, Pollina LE, Groen A, Falcone A, Danesi R, Campani D, Verheul HM, and Boggi U. MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Res 70: 4528-4538, 2010
44. Gong J, Zhang JP, Li B, Zeng C, You K, Chen MX, Yuan Y, and Zhuang SM. MicroRNA-125b promotes apoptosis by regulating the expression of Mcl-1, Bcl-w and IL-6R. Oncogene 32: 3071-3079, 2012
45. Guttilla IK and White BA. Coordinate regulation of FOXO1 by miR-27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 284: 23204-23216, 2009
46. Gwak HS, Kim TH, Jo GH, Kim YJ, Kwak HJ, Kim JH, Yin J, Yoo H, Lee SH, and Park JB. Silencing of micro- RNA-21 confers radio-sensitivity through inhibition of the PI3K/AKT pathway and enhancing autophagy in malignant glioma cell lines. PLoS One 7: e47449, 2012
47. He L, He X, Lim LP, de Stanchina E, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D, Jackson AL, Linsley PS, Chen C, Lowe SW, Cleary MA, and Hannon GJ. A microRNA component of the p53 tumour suppressor network. Nature 447: 1130-1134, 2007 (Pubitemid 47014436)
48. Hirata H, Hinoda Y, Ueno K, Shahryari V, Tabatabai ZL, and Dahiya R. MicroRNA-1826 targets VEGFC, betacatenin (CTNNB1) and MEK1 (MAP2K1) in human bladder cancer. Carcinogenesis 33: 41-48, 2012
49. Hu H, Du L, Nagabayashi G, Seeger RC, and Gatti RA. ATM is down-regulated by N-Myc-regulated microRNA- 421. Proc Natl Acad Sci U S A 107: 1506-1511, 2010
50. Hu W, Chan CS, Wu R, Zhang C, Sun Y, Song JS, Tang LH, Levine AJ, and Feng Z. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell 38: 689- 699, 2010
51. Huang S, Li XQ, Chen X, Che SM, Chen W, and Zhang XZ. Inhibition of microRNA-21 increases radiosensitivity of esophageal cancer cells through phosphatase and tensin homolog deleted on chromosome 10 activation. Dis Esophagus 26: 823-831, 2012
52. Huang TH, Wu F, Loeb GB, Hsu R, Heidersbach A, Brincat A, Horiuchi D, Lebbink RJ, Mo YY, Goga A, and McManus MT. Up-regulation of miR-21 by HER2/neu signaling promotes cell invasion. J Biol Chem 284: 18515-18524, 2009
53. Huang V, Place RF, Portnoy V, Wang J, Qi Z, Jia Z, Yu A, Shuman M, Yu J, and Li LC. Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucleic Acids Res 40: 1695-1707, 2012
54. Ichimura A, Ruike Y, Terasawa K, Shimizu K, and Tsujimoto G. MicroRNA-34a inhibits cell proliferation by repressing mitogen-activated protein kinase kinase 1 during megakaryocytic differentiation of K562 cells. Mol Pharmacol 77: 1016-1024, 2010
55. Iorio MV and Croce CM. Causes and consequences of microRNA dysregulation. Cancer J 18: 215-222, 2012
56. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, Kobayashi SV, Lim L, Burchard J, Jackson AL, Linsley PS, and Cleary MA. MicroRNAs in the miR- 106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28: 2167-2174, 2008 (Pubitemid 351429964)
57. Ji Q, Hao X, Meng Y, Zhang M, Desano J, Fan D, and Xu L. Restoration of tumor suppressor miR-34 inhibits human p53-mutant gastric cancer tumorspheres. BMC Cancer 8: 266, 2008
58. Ji Q, Hao X, Zhang M, Tang W, Yang M, Li L, Xiang D, Desano JT, Bommer GT, Fan D, Fearon ER, Lawrence TS, and Xu L. MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells. PLoS One 4: e6816, 2009
59. Ji S, Shao G, Lv X, Liu Y, Fan Y, Wu A, and Hu H. Downregulation of miRNA-128 sensitises breast cancer cell to chemodrugs by targeting Bax. Cell Biol Int 37: 653-658, 2013
60. Jiang Q, Feng MG, and Mo YY. Systematic validation of predicted microRNAs for cyclin D1. BMC Cancer 9: 194, 2009
61. Johnson CD, Esquela-Kerscher A, Stefani G, Byrom M, Kelnar K, Ovcharenko D, Wilson M, Wang X, Shelton J, Shingara J, Chin L, Brown D, and Slack FJ. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 67: 7713-7722, 2007 (Pubitemid 47281364)
62. Johnson SM, Grosshans H, Shingara J, Byrom M, Jarvis R, Cheng A, Labourier E, Reinert KL, Brown D, and Slack FJ. RAS is regulated by the let-7 microRNA family. Cell 120: 635-647, 2005 (Pubitemid 40343076)
63. Joly-Tonetti N, Vinuelas J, Gandrillon O, and Lamartine J. Differential miRNA expression profiles in proliferating or differentiated keratinocytes in response to gamma irradiation. BMC Genomics 14: 184, 2013
64. Kan T, Sato F, Ito T, Matsumura N, David S, Cheng Y, Agarwal R, Paun BC, Jin Z, Olaru AV, Selaru FM, Hamilton JP, Yang J, Abraham JM, Mori Y, and Meltzer SJ. The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology 136: 1689-1700, 2009
65. Kawano S and Nakamachi Y. miR-124a as a key regulator of proliferation and MCP-1 secretion in synoviocytes from patients with rheumatoid arthritis. Ann Rheum Dis 70 Suppl 1: i88-i91, 2011
66. Kong W, He L, Coppola M, Guo J, Esposito N, Coppola D, and Cheng J. MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol Chem 285: 17869-17879, 2010
67. Kraemer A, Anastasov N, Angermeier M, Winkler K, Atkinson MJ, and Moertl S. MicroRNA-mediated processes are essential for the cellular radiation response. Radiat Res 176: 575-586, 2011
68. Krishnan K, Steptoe AL, Martin HC, Wani S, Nones K, Waddell N, Mariasegaram M, Simpson PT, Lakhani SR, Gabrielli B, Vlassov A, Cloonan N, and Grimmond SM. MicroRNA-182-5p targets a network of genes involved in DNA repair. RNA 19: 230-242, 2013
69. Kumar M, Lu Z, Takwi AA, Chen W, Callander NS, Ramos KS, Young KH, and Li Y. Negative regulation of the tumor suppressor p53 gene by microRNAs. Oncogene 30: 843-853, 2011
70. Kwon JE, Kim BY, Kwak SY, Bae IH, and Han YH. Ionizing radiation-inducible microRNA miR-193a-3p induces apoptosis by directly targeting Mcl-1. Apoptosis 18: 896-909, 2013
71. Lal A, Navarro F, Maher CA, Maliszewski LE, Yan N, ODay E, Chowdhury D, Dykxhoorn DM, Tsai P, Hofmann O, Becker KG, Gorospe M, Hide W, and Lieberman J. miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to seedless UTR microRNA recognition elements. Mol Cell 35: 610-625, 2009
72. Lal A, Pan Y, Navarro F, Dykxhoorn DM, Moreau L, Meire E, Bentwich Z, Lieberman J, and Chowdhury D. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat Struct Mol Biol 16: 492-498, 2009
73. Le MT, Teh C, Shyh-Chang N, Xie H, Zhou B, Korzh V, Lodish HF, and Lim B. MicroRNA-125b is a novel negative regulator of p53. Genes Dev 23: 862-876, 2009
74. Lee KM, Choi EJ, and Kim IA. microRNA-7 increases radiosensitivity of human cancer cells with activated EGFRassociated signaling. Radiother Oncol 101: 171-176, 2011
75. Lee S and Vasudevan S. Post-transcriptional stimulation of gene expression by microRNAs. Adv Exp Med Biol 768: 97-126, 2013
76. Li D, Zhao Y, Liu C, Chen X, Qi Y, Jiang Y, Zou C, Zhang X, Liu S, Wang X, Zhao D, Sun Q, Zeng Z, Dress A, Lin MC, Kung HF, Rui H, Liu LZ, Mao F, Jiang BH, and Lai L. Analysis of MiR-195 and MiR-497 expression, regulation and role in breast cancer. Clin Cancer Res 17: 1722-1730, 2011
77. Li H and Yang BB. Stress response of glioblastoma cells mediated by miR-17-5p targeting PTEN and the passenger strand miR-17-3p targeting MDM2. Oncotarget 3: 1653- 1668, 2012
78. Li JH, Xiao X, Zhang YN, Wang YM, Feng LM, Wu YM, and Zhang YX. MicroRNA miR-886-5p inhibits apoptosis by down-regulating Bax expression in human cervical carcinoma cells. Gynecol Oncol 120: 145-151, 2011
79. Li X, Lin R, and Li J. Epigenetic silencing of microRNA- 375 regulates PDK1 expression in esophageal cancer. Dig Dis Sci 56: 2849-2856, 2011
80. Li Y, Tan W, Neo TW, Aung MO, Wasser S, Lim SG, and Tan TM. Role of the miR-106b-25 microRNA cluster in hepatocellular carcinoma. Cancer Sci 100: 1234-1242, 2009
81. Li Y, Zhao S, Zhen Y, Li Q, Teng L, Asai A, and Kawamoto K. A miR-21 inhibitor enhances apoptosis and reduces G(2)-M accumulation induced by ionizing radiation in human glioblastoma U251 cells. Brain Tumor Pathol 28: 209-214, 2011
82. Liang Z, Ahn J, Guo D, Votaw JR, and Shim H. Micro- RNA-302 replacement therapy sensitizes breast cancer cells to ionizing radiation. Pharm Res 30: 1008-1016, 2013
83. Linsley PS, Schelter J, Burchard J, Kibukawa M, Martin MM, Bartz SR, Johnson JM, Cummins JM, Raymond CK, Dai H, Chau N, Cleary M, Jackson AL, Carleton M, and Lim L. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol Cell Biol 27: 2240-2252, 2007 (Pubitemid 46418479)
84. Liu J, Luo XJ, Xiong AW, Zhang ZD, Yue S, Zhu MS, and Cheng SY. MicroRNA-214 promotes myogenic differentiation by facilitating exit from mitosis via downregulation of proto-oncogene N-ras. J Biol Chem 285: 26599-26607, 2010
85. Liu L, Chen L, Xu Y, Li R, and Du X. microRNA-195 promotes apoptosis and suppresses tumorigenicity of human colorectal cancer cells. Biochem Biophys Res Commun 400: 236-240, 2010
86. Liu Q, Fu H, Sun F, Zhang H, Tie Y, Zhu J, Xing R, Sun Z, and Zheng X. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res 36: 5391-5404, 2008
87. Liu Z, Liu J, Segura MF, Shao C, Lee P, Gong Y, Hernando E, and Wei JJ. MiR-182 overexpression in tumourigenesis of high-grade serous ovarian carcinoma. J Pathol 228: 204-215, 2012
88. Liu ZL, Wang H, Liu J, and Wang ZX. 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 372: 35-45, 2013
89. Lok BH and Powell SN. Molecular pathways: understanding the role of Rad52 in homologous recombination for therapeutic advancement. Clin Cancer Res 18: 6400- 6406, 2012
90. Lwin T, Lin J, Choi YS, Zhang X, Moscinski LC, Wright KL, Sotomayor EM, Dalton WS, and Tao J. Follicular dendritic cell-dependent drug resistance of non-Hodgkin lymphoma involves cell adhesion-mediated Bim downregulation through induction of microRNA-181a. Blood 116: 5228-5236, 2010
91. Marquez RT, Bryan W Tsao, Nicolas F Faust, and Liang Xu. Drug resistance and molecular cancer therapy: apoptosis versus autophagy. In: Apoptosis, edited by Rudner J. ISBN: 978-953-51-1133-7, InTech, DOI: 10.5772/55415. Available from: www.intechopen.com/books/apoptosis/ drug-resistance-and-molecular-cancer- therapy-apoptosisversus- autophagy InTech; 2013
92. Meng F, Henson R, Lang M, Wehbe H, Maheshwari S, Mendell JT, Jiang J, Schmittgen TD, and Patel T. Involvement of human micro-RNA in growth and response to chemotherapy in human cholangiocarcinoma cell lines. Gastroenterology 130: 2113-2129, 2006 (Pubitemid 43816961)
93. Meng F, Henson R, Wehbe-Janek H, Ghoshal K, Jacob ST, and Patel T. MicroRNA-21 regulates expression of the PTEN tumor suppressor gene in human hepatocellular cancer. Gastroenterology 133: 647-658, 2007 (Pubitemid 47187346)
94. Mladenov E, Magin S, Soni A, and Iliakis G. DNA double- strand break repair as determinant of cellular radiosensitivity to killing and target in radiation therapy. Front Oncol 3: 113, 2013
95. Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P, Muschel RJ, Beech J, Kulshrestha R, Abdelmohsen K, Weinstock DM, Gorospe M, Harris AL, Helleday T, and Chowdhury D. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 41: 210-220, 2011
96. Mott JL, Kobayashi S, Bronk SF, and Gores GJ. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26: 6133-6140, 2007 (Pubitemid 47414372)
97. Mraz M, Dolezalova D, Plevova K, Stano Kozubik K, Mayerova V, Cerna K, Musilova K, Tichy B, Pavlova S, Borsky M, Verner J, Doubek M, Brychtova Y, Trbusek M, Hampl A, Mayer J, and Pospisilova S. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood 119: 2110-2113, 2012
98. Mueller AC, Sun D, and Dutta A. The miR-99 family regulates the DNA damage response through its target SNF2H. Oncogene 32: 1164-1172, 2013
99. Neijenhuis S, Bajrami I, Miller R, Lord CJ, and Ashworth A. Identification of miRNA modulators to PARP inhibitor response. DNA Repair (Amst) 12: 394-402, 2013
100. Ng WL, Yan D, Zhang X, Mo YY, and Wang Y. Overexpression of miR-100 is responsible for the lowexpression of ATM in the human glioma cell line: M059J. DNA Repair (Amst) 9: 1170-1175, 2010
101. Nie J, Liu L, Zheng W, Chen L, Wu X, Xu Y, Du X, and Han W. microRNA-365, down-regulated in colon cancer, inhibits cell cycle progression and promotes apoptosis of colon cancer cells by probably targeting Cyclin D1 and Bcl-2. Carcinogenesis 33: 220-225, 2012
102. Niemoeller OM, Niyazi M, Corradini S, Zehentmayr F, Li M, Lauber K, and Belka C. MicroRNA expression profiles in human cancer cells after ionizing radiation. Radiat Oncol 6: 29, 2011
103. Ouyang YB, Lu Y, Yue S, and Giffard RG. miR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion 12: 213-219, 2012
104. Palii SS, Cui Y, Innes CL, and Paules RS. Dissecting cellular responses to irradiation via targeted disruptions of the ATM-CHK1-PP2A circuit. Cell Cycle 12: 1105-1118, 2013
105. Pastrello C, Polesel J, Della Puppa L, Viel A, and Maestro R. Association between hsa-mir-146a genotype and tumor age-of-onset in BRCA1/BRCA2-negative familial breast and ovarian cancer patients. Carcinogenesis 31: 2124- 2126, 2010
106. Pichiorri F, Suh SS, Ladetto M, Kuehl M, Palumbo T, Drandi D, Taccioli C, Zanesi N, Alder H, Hagan JP, Munker R, Volinia S, Boccadoro M, Garzon R, Palumbo A, Aqeilan RI, and Croce CM. MicroRNAs regulate critical genes associated with multiple myeloma pathogenesis. Proc Natl Acad Sci U S A 105: 12885-12890, 2008
107. Portnoy V, Huang V, Place RF, and Li LC. Small RNA and transcriptional upregulation. Wiley Interdiscip Rev RNA 2: 748-760, 2011
108. PosthumaDeBoer J, Wurdinger T, Graat HC, van Beusechem VW, Helder MN, van Royen BJ, and Kaspers GJ. WEE1 inhibition sensitizes osteosarcoma to radiotherapy. BMC Cancer 11: 156, 2011
109. Pothof J, Verkaik NS, van IW, Wiemer EA, Ta VT, van der Horst GT, Jaspers NG, van Gent DC, Hoeijmakers JH, and Persengiev SP. MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response. EMBO J 28: 2090-2099, 2009
110. Pouliot LM, Chen YC, Bai J, Guha R, Martin SE, Gottesman MM, and Hall MD. Cisplatin sensitivity mediated by WEE1 and CHK1 is mediated by miR-155 and the miR-15 family. Cancer Res 72: 5945-5955, 2012
111. Qian L, Van Laake LW, Huang Y, Liu S, Wendland MF, and Srivastava D. miR-24 inhibits apoptosis and represses Bim in mouse cardiomyocytes. J Exp Med 208: 549-560, 2011
112. Qu C, Liang Z, Huang J, Zhao R, Su C, Wang S, Wang X, Zhang R, Lee MH, and Yang H. MiR-205 determines the radioresistance of human nasopharyngeal carcinoma by directly targeting PTEN. Cell Cycle 11: 785-96, 2012
113. Raver-Shapira N, Marciano E, Meiri E, Spector Y, Rosenfeld N, Moskovits N, Bentwich Z, and Oren M. Transcriptional activation of miR-34a contributes to p53- mediated apoptosis. Mol Cell 26: 731-743, 2007 (Pubitemid 46856247)
114. Romano G, Acunzo M, Garofalo M, Di Leva G, Cascione L, Zanca C, Bolon B, Condorelli G, and Croce CM. MiR- 494 is regulated by ERK1/2 and modulates TRAILinduced apoptosis in non-small-cell lung cancer through BIM down-regulation. Proc Natl Acad Sci U S A 109: 16570-16575, 2012
115. Roy R, Chun J, and Powell SN. BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat Rev Cancer 12: 68-78, 2012
116. Saleh AD, Savage JE, Cao L, Soule BP, Ly D, DeGraff W, Harris CC, Mitchell JB, and Simone NL. Cellular stress induced alterations in microRNA let-7a and let-7b expression are dependent on p53. PLoS One 6: e24429, 2011
117. Schultz J, Lorenz P, Gross G, Ibrahim S, and Kunz M. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage- independent growth. Cell Res 18: 549-557, 2008 (Pubitemid 351630945)
118. Shen J, Ambrosone CB, DiCioccio RA, Odunsi K, Lele SB, and Zhao H. A functional polymorphism in the miR- 146a gene and age of familial breast/ovarian cancer diagnosis. Carcinogenesis 29: 1963-1966, 2008
119. Shi L, Cheng Z, Zhang J, Li R, Zhao P, Fu Z, and You Y. hsa-mir-181a and hsa-mir-181b function as tumor suppressors in human glioma cells. Brain Res 1236: 185-193, 2008
120. Shi XB, Xue L, Yang J, Ma AH, Zhao J, Xu M, Tepper CG, Evans CP, Kung HJ, and deVere White RW. An androgen- regulated miRNA suppresses Bak1 expression and induces androgen-independent growth of prostate cancer cells. Proc Natl Acad Sci U S A 104: 19983-19988, 2007
121. Shi Y, Zhang X, Tang X, Wang P, Wang H, and Wang Y. MiR-21 is continually elevated long-term in the brain after exposure to ionizing radiation. Radiat Res 177: 124-128, 2012
122. Shibuya H, Iinuma H, Shimada R, Horiuchi A, and Watanabe T. Clinicopathological and prognostic value of microRNA-21 and microRNA-155 in colorectal cancer. Oncology 79: 313-320, 2010
123. Shin KH, Bae SD, Hong HS, Kim RH, Kang MK, and Park NH. miR-181a shows tumor suppressive effect against oral squamous cell carcinoma cells by downregulating K-ras. Biochem Biophys Res Commun 404: 896-902, 2011
124. Shin S, Cha HJ, Lee EM, Lee SJ, Seo SK, Jin HO, Park IC, Jin YW, and An S. Alteration of miRNA profiles by ionizing radiation in A549 human non-small cell lung cancer cells. Int J Oncol 35: 81-86, 2009
125. Sokolov MV, Panyutin IV, and Neumann RD. Unraveling the global microRNAome responses to ionizing radiation in human embryonic stem cells. PLoS One 7: e31028, 2012
126. Song L, Lin C, Wu Z, Gong H, Zeng Y, Wu J, Li M, and Li J. miR-18a impairs DNA damage response through downregulation of ataxia telangiectasia mutated (ATM) kinase. PLoS One 6: e25454, 2011
127. Su H, Yang JR, Xu T, Huang J, Xu L, Yuan Y, and Zhuang SM. MicroRNA-101, down-regulated in hepatocellular carcinoma, promotes apoptosis and suppresses tumorigenicity. Cancer Res 69: 1135-1142, 2009
128. Sun F, Fu H, Liu Q, Tie Y, Zhu J, Xing R, Sun Z, and Zheng X. Downregulation of CCND1 and CDK6 by miR- 34a induces cell cycle arrest. FEBS Lett 582: 1564-1568, 2008
129. Tan G, Shi Y, and Wu ZH. MicroRNA-22 promotes cell survival upon UV radiation by repressing PTEN. Biochem Biophys Res Commun 417: 546-551, 2012
130. Tang T, Wong HK, Gu W, Yu MY, To KF, Wang CC, Wong YF, Cheung TH, Chung TK, and Choy KW. MicroRNA- 182 plays an onco-miRNA role in cervical cancer. Gynecol Oncol 129: 199-208, 2013
131. Tang Y, Zheng J, Sun Y, Wu Z, Liu Z, and Huang G. MicroRNA-1 regulates cardiomyocyte apoptosis by targeting Bcl-2. Int Heart J 50: 377-387, 2009
132. Tili E, Michaille JJ, Wernicke D, Alder H, Costinean S, Volinia S, and Croce CM. Mutator activity induced by microRNA-155 (miR-155) links inflammation and cancer. Proc Natl Acad Sci U S A 108: 4908-4913, 2011
133. Trabucchi M, Briata P, Garcia-Mayoral M, Haase AD, Filipowicz W, Ramos A, Gherzi R, and Rosenfeld MG. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 459: 1010-1014, 2009
134. Tsang WP and Kwok TT. Let-7a microRNA suppresses therapeutics-induced cancer cell death by targeting caspase-3. Apoptosis 13: 1215-1222, 2008
135. Tsukamoto Y, Nakada C, Noguchi T, Tanigawa M, Nguyen LT, Uchida T, Hijiya N, Matsuura K, Fujioka T, Seto M, and Moriyama M. MicroRNA-375 is downregulated in gastric carcinomas and regulates cell survival by targeting PDK1 and 14-3-3zeta. Cancer Res 70: 2339- 2349, 2010
136. Valerie K, Yacoub A, Hagan MP, Curiel DT, Fisher PB, Grant S, and Dent P. Radiation-induced cell signaling: inside-out and outside-in. Mol Cancer Ther 6: 789-801, 2007 (Pubitemid 46554549)
137. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, and Jacks T. Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132: 875-886, 2008 (Pubitemid 351312807)
138. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, and Croce CM. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci U S A 103: 2257-2261, 2006 (Pubitemid 43271657)
139. Wagner-Ecker M, Schwager C, Wirkner U, Abdollahi A, and Huber PE. MicroRNA expression after ionizing radiation in human endothelial cells. Radiat Oncol 5: 25, 2010
140. Wang C and Lees-Miller SP. Detection and repair of ionizing radiation-induced DNA double strand breaks: new developments in nonhomologous end joining. Int J Radiat Oncol Biol Phys 86: 440-449, 2013
141. Wang HQ, Yu XD, Liu ZH, Cheng X, Samartzis D, Jia LT, Wu SX, Huang J, Chen J, and Luo ZJ. Deregulated miR-155 promotes Fas-mediated apoptosis in human intervertebral disc degeneration by targeting FADD and caspase-3. J Pathol 225: 232-242, 2011
142. Wang L, Shi M, Hou S, Ding B, Liu L, Ji X, Zhang J, and Deng Y. MiR-483-5p suppresses the proliferation of glioma cells via directly targeting ERK1. FEBS Lett 586: 1312-1317, 2012
143. Wang P, Zou F, Zhang X, Li H, Dulak A, Tomko RJ, Jr., Lazo JS, Wang Z, Zhang L, and Yu J. microRNA-21 negatively regulates Cdc25A and cell cycle progression in colon cancer cells. Cancer Res 69: 8157-8165, 2009
144. Wang Y, Huang JW, Calses P, Kemp CJ, and Taniguchi T. MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Res 72: 4037-4046, 2012
145. Wang Y, Huang JW, Li M, Cavenee WK, Mitchell PS, Zhou X, Tewari M, Furnari FB, and Taniguchi T. MicroRNA- 138 modulates DNA damage response by repressing histone H2AX expression. Mol Cancer Res 9: 1100-1111, 2011
146. Webster RJ, Giles KM, Price KJ, Zhang PM, Mattick JS, and Leedman PJ. Regulation of epidermal growth factor receptor signaling in human cancer cells by microRNA-7. J Biol Chem 284: 5731-5741, 2009
147. Weidhaas JB, Babar I, Nallur SM, Trang P, Roush S, Boehm M, Gillespie E, and Slack FJ. MicroRNAs as potential agents to alter resistance to cytotoxic anticancer therapy. Cancer Res 67: 11111-11116, 2007 (Pubitemid 350248533)
148. Willimott S and Wagner SD. miR-125b and miR-155 contribute to BCL2 repression and proliferation in response to CD40 ligand (CD154) in human leukemic Bcells. J Biol Chem 287: 2608-2617, 2012
149. Wu CW, Dong YJ, Liang QY, He XQ, Ng SS, Chan FK, Sung JJ, and Yu J. MicroRNA-18a attenuates DNA damage repair through suppressing the expression of ataxia telangiectasia mutated in colorectal cancer. PLoS One 8: e57036, 2013
150. Wu J, Qian J, Li C, Kwok L, Cheng F, Liu P, Perdomo C, Kotton D, Vaziri C, Anderlind C, Spira A, Cardoso WV, and Lu J. miR-129 regulates cell proliferation by downregulating Cdk6 expression. Cell Cycle 9: 1809-1818, 2010
151. Wu L, Fan J, and Belasco JG. MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci U S A 103: 4034-4039, 2006
152. Wu Y, Liu GL, Liu SH, Wang CX, Xu YL, Ying Y, and Mao P. MicroRNA-148b enhances the radiosensitivity of non-Hodgkin's Lymphoma cells by promoting radiationinduced apoptosis. J Radiat Res 53: 516-525, 2012
153. Xia L, Zhang D, Du R, Pan Y, Zhao L, Sun S, Hong L, Liu J, and Fan D. miR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int J Cancer 123: 372-379, 2008 (Pubitemid 351842022)
154. Xiong S, Zheng Y, Jiang P, Liu R, Liu X, and Chu Y. MicroRNA-7 inhibits the growth of human non-small cell lung cancer A549 cells through targeting BCL-2. Int J Biol Sci 7: 805-814, 2011
155. Xu J, Li Y, Wang F, Wang X, Cheng B, Ye F, Xie X, Zhou C, and Lu W. Suppressed miR-424 expression via upregulation of target gene Chk1 contributes to the progression of cervical cancer. Oncogene 32: 976-987, 2013
156. Yadav S, Pandey A, Shukla A, Talwelkar SS, Kumar A, Pant AB, and Parmar D. miR-497 and miR-302b regulate ethanol-induced neuronal cell death through BCL2 protein and cyclin D2. J Biol Chem 286: 37347-37357, 2011
157. Yamane K, Jinnin M, Etoh T, Kobayashi Y, Shimozono N, Fukushima S, Masuguchi S, Maruo K, Inoue Y, Ishihara T, Aoi J, Oike Y, and Ihn H. Down-regulation of miR-124/-214 in cutaneous squamous cell carcinoma mediates abnormal cell proliferation via the induction of ERK. J Mol Med (Berl) 91: 69-81, 2013
158. Yan D, Ng WL, Zhang X, Wang P, Zhang Z, Mo YY, Mao H, Hao C, Olson JJ, Curran WJ, and Wang Y. Targeting DNA-PKcs and ATM with miR-101 sensitizes tumors to radiation. PLoS One 5: e11397, 2010
159. Yang X, Feng M, Jiang X, Wu Z, Li Z, Aau M, and Yu Q. miR-449a and miR-449b are direct transcriptional targets of E2F1 and negatively regulate pRb-E2F1 activity through a feedback loop by targeting CDK6 and CDC25A. Genes Dev 23: 2388-2393, 2009
160. Yang Y, Wu J, Guan H, Cai J, Fang L, Li J, and Li M. MiR-136 promotes apoptosis of glioma cells by targeting AEG-1 and Bcl-2. FEBS Lett 586: 3608-3612, 2012
161. Yu Z, Wang C, Wang M, Li Z, Casimiro MC, Liu M, Wu K, Whittle J, Ju X, Hyslop T, McCue P, and Pestell RG. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J Cell Biol 182: 509-517, 2008
162. Zang YS, Zhong YF, Fang Z, Li B, and An J. MiR-155 inhibits the sensitivity of lung cancer cells to cisplatin via negative regulation of Apaf-1 expression. Cancer Gene Ther 19: 773-778, 2012
163. Zhang C, Kang C, Wang P, Cao Y, Lv Z, Yu S, Wang G, Zhang A, Jia Z, Han L, Yang C, Ishiyama H, Teh BS, Xu B, and Pu P. MicroRNA-221 and -222 regulate radiation sensitivity by targeting the PTEN pathway. Int J Radiat Oncol Biol Phys 80: 240-248, 2011
164. Zhang C, Zhang J, Zhang A,Wang Y, Han L, You Y, Pu P, and Kang C. PUMA is a novel target of miR-221/222 in human epithelial cancers. Int J Oncol 37: 1621-1626, 2010
165. Zhang CZ, Zhang JX, Zhang AL, Shi ZD, Han L, Jia ZF, Yang WD, Wang GX, Jiang T, You YP, Pu PY, Cheng JQ, and Kang CS. MiR-221 and miR-222 target PUMA to induce cell survival in glioblastoma. Mol Cancer 9: 229, 2010
166. Zhang H, Cai X, Wang Y, Tang H, Tong D, and Ji F. microRNA-143, down-regulated in osteosarcoma, promotes apoptosis and suppresses tumorigenicity by targeting Bcl-2. Oncol Rep 24: 1363-1369, 2010
167. Zhang H, Li Y, Huang Q, Ren X, Hu H, Sheng H, and Lai M. MiR-148a promotes apoptosis by targeting Bcl-2 in colorectal cancer. Cell Death Differ 18: 1702-1710, 2011
168. Zhang H, Zuo Z, Lu X, Wang L, Wang H, and Zhu Z. MiR-25 regulates apoptosis by targeting Bim in human ovarian cancer. Oncol Rep 27: 594-598, 2012
169. Zhang X, Wan G, Berger FG, He X, and Lu X. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol Cell 41: 371-383, 2011
170. Zhao WG, Yu SN, Lu ZH, Ma YH, Gu YM, and Chen J. The miR-217 microRNA functions as a potential tumor suppressor in pancreatic ductal adenocarcinoma by targeting KRAS. Carcinogenesis 31: 1726-1733, 2010
171. Zheng D, Radziszewska A, and Woo P. MicroRNA 497 modulates interleukin 1 signalling via the MAPK/ERK pathway. FEBS Lett 586: 4165-4172, 2012
172. Zhu W, Zhu D, Lu S, Wang T, Wang J, Jiang B, Shu Y, and Liu P. miR-497 modulates multidrug resistance of human cancer cell lines by targeting BCL2. Med Oncol 29: 384-391, 2012
173. Zhu Y, Yu F, Jiao Y, Feng J, Tang W, Yao HR, Gong C, Chen JN, Su FX, Zhang Y, and Song E. Reduced miR-128 in breast tumor-initiating cells induces chemotherapeutic resistance via Bmi-1 and ABCC5. Clin Cancer Res 17: 7105-7115, 2011
174. Zou C, Xu Q, Mao F, Li D, Bian C, Liu LZ, Jiang Y, Chen X, Qi Y, Zhang X, Wang X, Sun Q, Kung HF, Lin MC, Dress A, Wardle F, Jiang BH, and Lai L. MiR-145 inhibits tumor angiogenesis and growth by N-RAS and VEGF. Cell Cycle 11: 2137-2145, 2012.