Targeting the microRNA-regulating DNA damage/repair pathways in cancer

Expert Opinion on Biological Therapy

Volumn 14, Issue 11, 2014, Pages 1667-1683

  Bottai, Giulia ^a   Pasculli, Barbara ^b,c   Calin, George A ^d   Santarpia, Libero ^a  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d UNIVERSITY OF TEXAS   (United States)

Author keywords

Apoptosis; Cancer therapies; Cell cycle; Chemotherapy; DNA damage response; DNA repair; Drug response; microRNAs

Indexed keywords

ANTINEOPLASTIC AGENT; MICRORNA;

APOPTOSIS; BIOGENESIS; CANCER CELL; CANCER CHEMOTHERAPY; CANCER GROWTH; CANCER RESISTANCE; CARCINOGENESIS; CELL CYCLE; CELL CYCLE CHECKPOINT; DNA DAMAGE; DNA REPAIR; DRUG SENSITIVITY; GENE; GENE EXPRESSION REGULATION; GENE TARGETING; HUMAN; NONHUMAN; PREDICTIVE VALUE; REVIEW; RNA PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG DELIVERY SYSTEM; DRUG EFFECTS; GENETICS; GENOMIC INSTABILITY; NEOPLASMS; PHYSIOLOGY; TRENDS;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; DNA DAMAGE; DNA REPAIR; DRUG DELIVERY SYSTEMS; GENE TARGETING; GENOMIC INSTABILITY; HUMANS; MICRORNAS; NEOPLASMS;

EID: 84911135072     PISSN: 14712598     EISSN: 17447682     Source Type: Journal    
DOI: 10.1517/14712598.2014.950650     Document Type: Review

References (99)

1. Foster SS, De S, Johnson LK, et al. Cell cycle- and DNA repair pathway-specific effects of apoptosis on tumor suppression. Proc Natl Acad Sci USA 2012;109:9953-8
2. Hoeijmakers JH. Genome maintenance mechanisms for preventing cancer. Nature 2001;411:366-74
3. d'Adda di Fagagna F. Living on a break: cellular senescence as a DNA-damage response. Nat Rev Cancer 2008;8:512-22
4. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009;461:1071-8
5. Bouwman P, Jonkers J. The effects of deregulated DNA damage signalling on cancer chemotherapy response and resistance. Nat Rev Cancer 2012;12:587-98
6. d'Adda di Fagagna F. A direct role for small non-coding RNAs in DNA damage response. Trends Cell Biol 2014;24:171-8
7. Wei W, Ba Z, Gao M, et al. A role for small RNAs in DNA double-strand break repair. Cell 2012;149:101-12
8. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004;116:281-97
9. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med 2009;60:167-79
10. Sharma V, Misteli T. Non-coding RNAs in DNA damage and repair. FEBS Lett 2013;587:1832-9
11. Chowdhury D, Choi YE, Brault ME. Charity begins at home: non-coding RNA functions in DNA repair. Nat Rev Mol Cell Biol 2013;14:181-9
12. van Jaarsveld MT, Wouters MD, Boersma AW, et al. DNA damage responsive microRNAs misexpressed in human cancer modulate therapy sensitivity. Mol Oncol 2014;8:458-68
13. Holohan C, Van Schaeybroeck S, Longley DB, Johnston PG. Cancer drug resistance: an evolving paradigm. Nat Rev Cancer 2013;13:714-26
14. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010;40:179-204
15. Lund E, Güttinger S, Calado A, et al. Nuclear export of microRNA precursors. Science 2004;303:95-8
16. Diederichs S, Haber DA. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007;131:1097-108
17. Grosshans H, Chatterjee S. MicroRNAses and the regulated degradation of mature animal miRNAs. Adv Exp Med Biol 2010;700:140-55
18. Han C, Wan G, Langley RR, et al. Crosstalk between the DNA damage response pathway and microRNAs. Cell Mol Life Sci 2012;69:2895-906
19. Wouters MD, van Gent DC, Hoeijmakers JH, Pothof J. MicroRNAs, the DNA damage response and cancer. Mutat Res 2011;717:54-66
20. Hermeking H. MicroRNAs in the p53 network: micromanagement of tumour suppression. Nat Rev Cancer 2012;12:613-26
21. Cannell IG, Kong YW, Johnston SJ, et al. p38 MAPK/MK2-mediated induction of miR-34c following DNA damage prevents Myc-dependent DNA replication. Proc Natl Acad Sci USA 2010;107:5375-80
22. Georges SA, Biery MC, Kim SY, et al. Coordinated regulation of cell cycle transcripts by p53-Inducible microRNAs, miR-192 and miR-215. Cancer Res 2008;68:10105-12
23. Yan HL, Xue G, Mei Q, et al. Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis. EMBO J 2009;28:2719-32
24. Ugalde AP, Ramsay AJ, de la Rosa J, et al. Aging and chronic DNA damage response activate a regulatory pathway involving miR-29 and p53. EMBO J 2011;30:2219-32
25. Su X, Chakravarti D, Cho MS, et al. TAp63 suppresses metastasis through coordinate regulation of Dicer and miRNAs. Nature 2010;467:986-90
26. Aguda BD, Kim Y, Piper-Hunter MG, et al. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc Natl Acad Sci USA 2008;105:19678-83
27. Wan G, Mathur R, Hu X, et al. miRNA response to DNA damage. Trends Biochem Sci 2011;36:478-84
28. Suzuki HI, Yamagata K, Sugimoto K, et al. Modulation of microRNA processing by p53. Nature 2009;460:529-33
29. Wang Y, Taniguchi T. MicroRNAs and DNA damage response: implications for cancer therapy. Cell Cycle 2013;12:32-42
30. Boominathan L. The tumor suppressors p53, p63, and p73 are regulators of microRNA processing complex. PLoS One 2010;5:e10615
31. Wang X, Zhao X, Gao P, Wu M. c-Myc modulates microRNA processing via the transcriptional regulation of Drosha. Sci Rep 2013;3:1942
32. Mao G, Lee S, Ortega J, et al. Modulation of microRNA processing by mismatch repair protein MutLa. Cell Res 2012;22:973-85
33. Kawai S, Amano A. BRCA1 regulates microRNA biogenesis via the DROSHA microprocessor complex. J Cell Biol 2012;197:201-8
34. Zhang X, Wan G, Berger FG, et al. The ATM kinase induces microRNA biogenesis in the DNA damage response. Mol Cell 2011;41:371-83
35. Trabucchi M, Briata P, Garcia-Mayoral M, et al. The RNA-binding protein KSRP promotes the biogenesis of a subset of microRNAs. Nature 2009;459:1010-14
36. Wan G, Zhang X, Langley RR, et al. DNA-damage-induced nuclear export of precursor microRNAs is regulated by the ATM-AKT pathway. Cell Rep 2013;3:2100-12
37. Dent P, Yacoub A, Fisher PB, et al. MAPK pathways in radiation responses. Oncogene 2003;22:5885-96
38. van Attikum H, Gasser SM. Crosstalk between histone modifications during the DNA damage response. Trends Cell Biol 2009;19:207-17
39. Lal A, Pan Y, Navarro F, et al. miR-24-mediated downregulation of H2AX suppresses DNA repair in terminally differentiated blood cells. Nat Struct Mol Biol 2009;16:492-8
40. Wang Y, Huang JW, Li M, et al. MicroRNA-138 modulates DNA damage response by repressing histone H2AX expression. Mol Cancer Res 2011;9:1100-11
41. Francia S, Michelini F, Saxena A, et al. Site-specific DICER and DROSHA RNA products control the DNA-damage response. Nature 2012;488:231-5
42. Valeri N, Gasparini P, Fabbri M, et al. Modulation of mismatch repair and genomic stability by miR-155. Proc Natl Acad Sci USA 2010;107:6982-7
43. Tessitore A, Cicciarelli G, Del Vecchio F, et al. MicroRNAs in the DNA damage/repair network and cancer. Int J Genomics 2014;2014:820248
44. Di Francesco A, De Pittà C, Moret F, et al. The DNA-damage response to gamma-radiation is affected by miR-27a in A549 cells. Int J Mol Sci 2013;14:17881-96
45. Bisso A, Faleschini M, Zampa F, et al. Oncogenic miR-181a/b affect the DNA damage response in aggressive breast cancer. Cell Cycle 2013;12:1679-87
46. Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 2012;47:497-510
47. Jung EJ, Santarpia L, Kim J, et al. Plasma microRNA 210 levels correlate with sensitivity to trastuzumab and tumor presence in breast cancer patients. Cancer 2012;118:2603-14
48. Crosby ME, Kulshreshtha R, Ivan M, Glazer PM. MicroRNA regulation of DNA repair gene expression in hypoxic stress. Cancer Res 2009;69:1221-9
49. Martin NT, Nakamura K, Davies R, et al. ATM-dependent MiR-335 targets CtIP and modulates the DNA damage response. PLoS Genet 2013;9:e1003505
50. Johnson CD, Esquela-Kerscher A, Stefani G, et al. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res 2007;67:7713-22
51. Jhanwar-Uniyal M. BRCA1 in cancer, cell cycle and genomic stability. Front Biosci 2003;8:s1107-17
52. Nicoloso MS, Sun H, Spizzo R, et al. Single-nucleotide polymorphisms inside microRNA target sites influence tumor susceptibility. Cancer Res 2010;70:2789-98
53. Pouliot LM, Chen YC, Bai J, et al. Cisplatin sensitivity mediated by WEE1 and CHK1 is mediated by miR-155 and the miR-15 family. Cancer Res 2012;72:5945-55
54. Shi W, Alajez NM, Bastianutto C, et al. Significance of Plk1 regulation by miR-100 in human nasopharyngeal cancer. Int J Cancer 2010;126:2036-48
55. Hu W, Chan CS, Wu R, et al. Negative regulation of tumor suppressor p53 by microRNA miR-504. Mol Cell 2010;38:689-99
56. Liu Y, Xing R, Zhang X, et al. miR-375 targets the p53 gene to regulate cellular response to ionizing radiation and etoposide in gastric cancer cells. DNA Repair (Amst) 2013;12:741-50
57. Xiao J, Lin H, Luo X, Wang Z. miR-605 joins p53 network to form a p53:miR-605:mdm2 positive feedback loop in response to stress. EMBO J 2011;30:524-32
58. Santarpia L, Iwamoto T, Di Leo A, et al. DNA repair gene patterns as prognostic and predictive factors in molecular breast cancer subtypes. Oncologist 2013;18:1063-73
59. Lord CJ, Ashworth A. The DNA damage response and cancer therapy. Nature 2012;481:287-94
60. Valeri N, Gasparini P, Braconi C, et al. MicroRNA-21 induces resistance to 5-fluorouracil by down-regulating human DNA MutS homolog 2 (hMSH2). Proc Natl Acad Sci USA 2010;107:21098-103
61. Broustas CG, Lieberman HB. DNA damage response genes and the development of cancer metastasis. Radiat Res 2014;181:111-30
62. Woditschka S, Evans L, Duchnowska R, et al. DNA double-strand break repair genes and oxidative damage in brain metastasis of breast cancer. J Natl Cancer Inst 2014; published online 19 June 2014, doi:10.1093/jnci/dju145
63. Skvortsov S, Debbage P, Lukas P, Skvortsova I. Crosstalk between DNA repair and cancer stem cell (CSC) associated intracellular pathways. Semin Cancer Biol 2014. [Epub ahead of print]
64. Ceppi P, Peter ME. MicroRNAs regulate both epithelial-to-mesenchymal transition and cancer stem cells. Oncogene 2014;33:269-78
65. Bouyssou JM, Manier S, Huynh D, et al. Regulation of microRNAs in cancer metastasis. Biochim Biophys Acta 2014;255-65
66. Johansson J, Berg T, Kurzejamska E, et al. MiR-155-mediated loss of C/EBPbeta shifts the TGF-beta response from growth inhibition to epithelial-mesenchymal transition, invasion and metastasis in breast cancer. Oncogene 2013;32:5614-24
67. Wang Q, Zhong M, Liu W, et al. Alterations of microRNAs in cisplatin-resistant human non-small cell lung cancer cells (A549/DDP). Exp Lung Res 2011;37:427-34
68. Wang Y, Huang JW, Calses P, et al. MiR-96 downregulates REV1 and RAD51 to promote cellular sensitivity to cisplatin and PARP inhibition. Cancer Res 2012;72:4037-46
69. Neijenhuis S, Bajrami I, Miller R, et al. Identification of miRNA modulators to PARP inhibitor response. DNA Repair (Amst) 2013;12:394-402
70. Zhang S, Chen H, Zhao X, et al. REV3L 3'UTR 460 T>C polymorphism in microRNA target sites contributes to lung cancer susceptibility. Oncogene 2013;32:242-50
71. Doles J, Oliver TG, Cameron ER, et al. Suppression of Rev3, the catalytic subunit of Pol{zeta}, sensitizes drug-resistant lung tumors to chemotherapy. Proc Natl Acad Sci USA 2010;107:20786-91
72. Zhou M, Liu Z, Zhao Y, et al. MicroRNA-125b confers the resistance of breast cancer cells to paclitaxel through suppression of pro-apoptotic Bcl-2 antagonist killer 1 (Bak1) expression. J Biol Chem 2010;285:21496-507
73. Kojima K, Fujita Y, Nozawa Y, et al. MiR-34a attenuates paclitaxel-resistance of hormone-refractory prostate cancer PC3 cells through direct and indirect mechanisms. Prostate 2010;70:1501-12
74. Kastl L, Brown I, Schofield AC. miRNA-34a is associated with docetaxel resistance in human breast cancer cells. Breast Cancer Res Treat 2012;131:445-54
75. Ren Y, Zhou X, Mei M, et al. MicroRNA-21 inhibitor sensitizes human glioblastoma cells U251 (PTEN-mutant) and LN229 (PTEN-wild type) to taxol. BMC Cancer 2010;10:27
76. Mei M, Ren Y, Zhou X, et al. Downregulation of miR-21 enhances chemotherapeutic effect of taxol in breast carcinoma cells. Technol Cancer Res Treat 2010;9:77-86
77. Yu Y, Wang Y, Ren X, et al. Context-dependent bidirectional regulation of the MutS homolog 2 by transforming growth factor beta contributes to chemoresistance in breast cancer cells. Mol Cancer Res 2010;8:1633-42
78. Zhang YX, Yue Z, Wang PY, et al. Cisplatin upregulates MSH2 expression by reducing miR-21 to inhibit A549 cell growth. Biomed Pharmacother 2013;67:97-102
79. Kovalchuk O, Filkowski J, Meservy J, et al. Involvement of microRNA-451 in resistance of the MCF-7 breast cancer cells to chemotherapeutic drug doxorubicin. Mol Cancer Ther 2008;7:2152-9
80. Garcia AI, Buisson M, Bertrand P, et al. Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers. EMBO Mol Med 2011;3:279-90
81. Pogribny IP, Filkowski JN, Tryndyak VP, et al. Alterations of microRNAs and their targets are associated with acquired resistance of MCF-7 breast cancer cells to cisplatin. Int J Cancer 2010;127:1785-94
82. Zhou Y, Wan G, Spizzo R, et al. miR-203 induces oxaliplatin resistance in colorectal cancer cells by negatively regulating ATM kinase. Mol Oncol 2014;8:83-92
83. Giovannetti E, Funel N, Peters GJ, et al. MicroRNA-21 in pancreatic cancer: correlation with clinical outcome and pharmacologic aspects underlying its role in the modulation of gemcitabine activity. Cancer Res 2010;70:4528-38
84. Schwarzenbach H, Nishida N, Calin GA, Pantel K. Clinical relevance of circulating cell-free microRNAs in cancer. Nat Rev Clin Oncol 2014;11:145-56
85. Ferracin M, Zagatti B, Rizzotto L. MicroRNAs involvement in fludarabine refractory chronic lymphocytic leukemia. Mol Cancer 2010;9:123
86. Wang H, Tan G, Dong L, et al. Circulating miR-125b as a marker predicting chemoresistance in breast cancer. PLoS One 2012;7:e34210
87. Cui EH, Li HJ, Hua F, et al. Serum microRNA 125b as a diagnostic or prognostic biomarker for advanced NSCLC patients receiving cisplatin-based chemotherapy. Acta Pharmacol Sin 2013;34:309-13
88. Gasparini P, Cascione L, Fassan M, et al. microRNA expression profiling identifies a four microRNA signature as a novel diagnostic and prognostic biomarker in triple negative breast cancers. Oncotarget 2014;5:1174-84
89. Gasparini P, Lovat F, Fassan M, et al. Protective role of miR-155 in breast cancer through RAD51 targeting impairs homologous recombination after irradiation. Proc Natl Acad Sci USA 2014;111:4536-41
90. Cascione L, Gasparini P, Lovat F, et al. Integrated microRNA and mRNA signatures associated with survival in triple negative breast cancer. PLoS One 2013;8:e55910
91. Kong W, He L, Richards EJ, et al. Upregulation of miRNA-155 promotes tumour angiogenesis by targeting VHL and is associated with poor prognosis and triple-negative breast cancer. Oncogene 2014;33:679-89
92. Kong W, He L, Coppola M, et al. MicroRNA-155 regulates cell survival, growth, and chemosensitivity by targeting FOXO3a in breast cancer. J Biol Chem 2010;285:17869-79
93. Ferrajoli A, Shanafelt TD, Ivan C, et al. Prognostic value of miR-155 in individuals with monoclonal B-cell lymphocytosis and patients with B chronic lymphocytic leukemia. Blood 2013;122:1891-9
94. Zhu DX, Zhu W, Fang C, et al. miR-181a/b significantly enhances drug sensitivity in chronic lymphocytic leukemia cells via targeting multiple antiapoptosis genes. Carcinogenesis 2012;33:1294-301
95. Ohyashiki K, Umezu T, Yoshizawa S. Clinical impact of down-regulated plasma miR-92a levels in Non-Hodgkin's Lymphoma. PLoS One 2011;6:e16408
96. Calin GA, Croce CM. MicroRNA signatures in human cancers. Nat Rev Cancer 2006;6:857-66
97. Lu J, Getz G, Miska EA, et al. MicroRNA expression profiles classify human cancers. Nature 2005;435:834-8
98. Chen T, Brownawell AM, Macara IG. Nucleocytoplasmic shuttling of JAZ, a new cargo protein for exportin-5. Mol Cell Biol 2004;24:6608-19
99. Melo SA, Moutinho C, Ropero S, et al. A genetic defect in exportin-5 traps precursor microRNAs in the nucleus of cancer cells. Cancer Cell 2010;18:303-15