MicroRNA-182-5p targets a network of genes involved in DNA repair

RNA

Volumn 19, Issue 2, 2013, Pages 230-242

  Krishnan, Keerthana ^a   Steptoe, Anita L ^a   Martin, Hilary C ^a,d   Wani, Shivangi ^a   Nones, Katia ^a   Waddell, Nic ^a   Mariasegaram, Mythily ^b   Simpson, Peter T ^b   Lakhani, Sunil R ^b   Gabrielli, Brian ^a   Vlassov, Alexander ^c   Cloonan, Nicole ^a   Grimmond, Sean M ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Life Technologies   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biotin pull down; MiRNA; PARP inhibition; Target identification

Indexed keywords

MICRORNA; MICRORNA 182 5P; UNCLASSIFIED DRUG;

ARTICLE; BIOTINYLATION; BREAST CANCER; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; FEMALE; GENE OVEREXPRESSION; HOMOLOGOUS RECOMBINATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VALIDATION PROCESS;

BRCA1 PROTEIN; BREAST NEOPLASMS; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CLUSTER ANALYSIS; COHORT STUDIES; DNA DAMAGE; DNA REPAIR; FEMALE; GENE EXPRESSION PROFILING; HELA CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; MICRORNAS; MODELS, GENETIC; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; UP-REGULATION;

EID: 84872576566     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.034926.112     Document Type: Article

References (75)

1. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. 2008. The impact of microRNAs on protein output. Nature 455: 64-71.
2. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
3. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 57: 289-300.
4. Bentwich I. 2005. Prediction and validation of microRNAs and their targets. FEBS Lett 579: 5904-5910.
5. Brennecke J, Stark A, Russell RB, Cohen SM. 2005. Principles of microRNA-target recognition. PLoS Biol 3: e85. doi: 10.1371/ journal.pbio.0030085.
6. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature 434: 913-917.
7. Cho WC, Chow AS, Au JS. 2009. Restoration of tumour suppressor hsa-miR-145 inhibits cancer cell growth in lung adenocarcinoma patients with epidermal growth factor receptor mutation. Eur J Cancer 45: 2197-2206.
8. Cloonan N, Brown MK, Steptoe AL, Wani S, Chan WL, Forrest AR, Kolle G, Gabrielli B, Grimmond SM. 2008. The miR-17-5p microRNA is a key regulator of the G1/S phase cell cycle transition. Genome Biol 9: R127. doi: 10.1186/gb-2008-9-8-r127.
9. Cloonan N, Wani S, Xu Q, Gu J, Lea K, Heater S, Barbacioru C, Steptoe AL, Martin HC, Nourbakhsh E, et al. 2011. MicroRNAs and their isomiRs function cooperatively to target common biological pathways. Genome Biol 12: R126. doi: 10.1186/gb-2011-12-12- r126.
10. Cuadrado M, Gutierrez-Martinez P, Swat A, Nebreda AR, Fernandez- Capetillo O. 2009. p27Kip1 stabilization is essential for the maintenance of cell cycle arrest in response to DNA damage. Cancer Res 69: 8726-8732.
11. Cui Q, Yu Z, Purisima EO, Wang E. 2006. Principles of microRNA regulation of a human cellular signaling network. Mol Syst Biol 2: 46. doi: 10.1038/msb4100089.
12. Deng CX. 2006. BRCA1: Cell cycle checkpoint, genetic instability, DNA damage response and cancer evolution. Nucleic Acids Res 34: 1416-1426.
13. Du P, KibbeWA, Lin SM. 2008. lumi: A pipeline for processing Illumina microarray. Bioinformatics 24: 1547-1548.
14. Frankel LB, Christoffersen NR, Jacobsen A, Lindow M, Krogh A, Lund AH. 2008. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J Biol Chem 283: 1026-1033.
15. Fujieda S, Inuzuka M, Tanaka N, Sunaga H, Fan GK, Ito T, Sugimoto C, Tsuzuki H, Saito H. 1999. Expression of p27 is associated with Bax expression and spontaneous apoptosis in oral and oropharyngeal carcinoma. Int J Cancer 84: 315-320.
16. Gandellini P, Folini M, Longoni N, Pennati M, Binda M, Colecchia M, Salvioni R, Supino R, Moretti R, Limonta P, et al. 2009. miR-205 exerts tumor-suppressive functions in human prostate through downregulation of protein kinase Cε. Cancer Res 69: 2287-2295.
17. Guttilla IK, White BA. 2009. Coordinate regulation of FOXO1 by miR- 27a, miR-96, and miR-182 in breast cancer cells. J Biol Chem 284: 23204-23216.
18. Harper JW, Elledge SJ, Keyomarsi K, Dynlacht B, Tsai LH, Zhang P, Dobrowolski S, Bai C, Connell-Crowley L, Swindell E, et al. 1995. Inhibition of cyclin-dependent kinases by p21. Mol Biol Cell 6: 387-400.
19. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, et al. 2005. A microRNA polycistron as a potential human oncogene. Nature 435: 828-833.
20. Hengst L, Reed SI. 1998. Inhibitors of the Cip/Kip family. Curr Top Microbiol Immunol 227: 25-41.
21. Hossain A, Kuo MT, Saunders GF. 2006. Mir-17-5p regulates breast cancer cell proliferation by inhibiting translation of AIB1 mRNA. Mol Cell Biol 26: 8191-8201.
22. Huse JT, Brennan C, Hambardzumyan D, Wee B, Pena J, Rouhanifard SH, Sohn-Lee C, le Sage C, Agami R, Tuschl T, et al. 2009. The PTEN-regulating microRNA miR-26a is amplified in high-grade glioma and facilitates gliomagenesis in vivo. Genes Dev 23: 1327-1337.
23. Iorio MV, Ferracin M, Liu CG, Veronese A, Spizzo R, Sabbioni S, Magri E, Pedriali M, Fabbri M, Campiglio M, et al. 2005. MicroRNA gene expression deregulation in human breast cancer. Cancer Res 65: 7065-7070.
24. Iorio MV, Visone R, Di Leva G, Donati V, Petrocca F, Casalini P, Taccioli C, Volinia S, Liu CG, Alder H, et al. 2007. MicroRNA signatures in human ovarian cancer. Cancer Res 67: 8699-8707.
25. IorioMV, Casalini P, Piovan C, Di Leva G, Merlo A, Triulzi T, Ménard S, Croce CM, Tagliabue E. 2009. microRNA-205 regulates HER3 in human breast cancer. Cancer Res 69: 2195-2200.
26. Jiang L, Mao P, Song L, Wu J, Huang J, Lin C, Yuan J, Qu L, Cheng SY, Li J. 2010. miR-182 as a prognostic marker for glioma progression and patient survival. Am J Pathol 177: 29-38.
27. Katayose Y, Kim M, Rakkar AN, Li Z, Cowan KH, Seth P. 1997. Promoting apoptosis: A novel activity associated with the cyclin-dependent kinase inhibitor p27. Cancer Res 57: 5441-5445.
28. Khanna KK, Jackson SP. 2001. DNA double-strand breaks: Signaling, repair and the cancer connection. Nat Genet 27: 247-254.
29. Kim H, Huang W, Jiang X, Pennicooke B, Park PJ, Johnson MD. 2010. Integrative genome analysis reveals an oncomir/oncogene cluster regulating glioblastoma survivorship. Proc Natl Acad Sci 107: 2183-2188.
30. Kloosterman WP, Plasterk RH. 2006. The diverse functions of micro- RNAs in animal development and disease. Dev Cell 11: 441-450.
31. Kong WQ, Bai R, Liu T, Cai CL, Liu M, Li X, Tang H. 2012. MicroRNA- 182 targets cyclic adenosine monophosphate responsive element binding protein 1 (CREB1) and suppresses cell growth in human gastric adenocarcinoma. FEBS J 279: 1252-1260.
32. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, Chang TC, Vivekanandan P, Torbenson M, Clark KR, et al. 2009. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 137: 1005-1017.
33. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. 2005. Combinatorial microRNA target predictions. Nat Genet 37: 495-500.
34. Lagos-Quintana M, Rauhut R, Meyer J, Borkhardt A, Tuschl T. 2003. New microRNAs from mouse and human. RNA 9: 175-179.
35. Lassot I, Ségéral E, Berlioz-Torrent C, Durand H, Groussin L, Hai T, Benarous R, Margottin-Goguet F. 2001. ATF4 degradation relies on a phosphorylation-dependent interaction with the SCFβTrCP ubiquitin ligase. Mol Cell Biol 21: 2192-2202.
36. Lewis BP, Burge CB, Bartel DP. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
37. Li H, Bian C, Liao L, Li J, Zhao RC. 2011. miR-17-5p promotes human breast cancer cell migration and invasion through suppression of HBP1. Breast Cancer Res Treat 126: 565-575.
38. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, Bartel DP, Linsley PS, Johnson JM. 2005. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433: 769-773.
39. Lin SM, Du P, HuberW, KibbeWA. 2008. Model-based variance-stabilizing transformation for Illumina microarray data. Nucleic Acids Res 36: e11. doi: 10.1093/nar/gkm1075.
40. Liu Z, Liu J, Segura MF, Shao C, Lee P, Gong Y, Hernando E, Wei JJ. 2012. MiR182 overexpression in tumorigenesis of high-grade ovarian papillary serous carcinoma. J Pathol 228: 204-215.
41. Lord CJ, Ashworth A. 2012. The DNA damage response and cancer therapy. Nature 481: 287-294.
42. Ma L, Teruya-Feldstein J, Weinberg RA. 2007. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449: 682-688.
43. McCabe N, Turner NC, Lord CJ, Kluzek K, Bialkowska A, Swift S, Giavara S, O'Connor MJ, Tutt AN, Zdzienicka MZ, et al. 2006. Deficiency in the repair of DNA damage by homologous recombination and sensitivity to poly(ADP-ribose) polymerase inhibition. Cancer Res 66: 8109-8115.
44. Meyerson M, Harlow E. 1994. Identification of G1 kinase activity for cdk6, a novel cyclin D partner. Mol Cell Biol 14: 2077-2086.
45. Moskwa P, Buffa FM, Pan Y, Panchakshari R, Gottipati P, Muschel RJ, Beech J, Kulshrestha R, Abdelmohsen K, Weinstock DM, et al. 2011. miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol Cell 41: 210-220.
46. Moynahan ME, Jasin M. 2010. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11: 196-207.
47. Moynahan ME, Chiu JW, Koller BH, Jasin M. 1999. Brca1 controls homology- directed DNA repair. Mol Cell 4: 511-518.
48. Mraz M, Malinova K, Kotaskova J, Pavlova S, Tichy B, Malcikova J, Stano Kozubik K, Smardova J, Brychtova Y, Doubek M, et al. 2009. miR-34a, miR-29c and miR-17-5p are downregulated in CLL patients with TP53 abnormalities. Leukemia 23: 1159-1163.
49. Myatt SS, Wang J, Monteiro LJ, Christian M, Ho KK, Fusi L, Dina RE, Brosens JJ, Ghaem-Maghami S, Lam EW. 2010. Definition of microRNAs that repress expression of the tumor suppressor gene FOXO1 in endometrial cancer. Cancer Res 70: 367-377.
50. Rajewsky N. 2006. microRNA target predictions in animals. Nat Genet 38: S8-S13.
51. Saito T, Saetrom P. 2010. MicroRNAs - targeting and target prediction. N Biotechnol 27: 243-249.
52. Sander S, Bullinger L, Klapproth K, Fiedler K, Kestler HA, Barth TF, Möller P, Stilgenbauer S, Pollack JR, Wirth T. 2008. MYC stimulates EZH2 expression by repression of its negative regulator miR-26a. Blood 112: 4202-4212.
53. Sarver AL, French AJ, Borralho PM, Thayanithy V, Oberg AL, Silverstein KA, Morlan BW, Riska SM, Boardman LA, Cunningham JM, et al. 2009. Human colon cancer profiles show differential microRNA expression depending on mismatch repair status and are characteristic of undifferentiated proliferative states. BMC Cancer 9: 401. doi: 10.1186/1471-2407-9-401.
54. Schaefer A, Jung M, Mollenkopf HJ, Wagner I, Stephan C, Jentzmik F, Miller K, Lein M, Kristiansen G, Jung K. 2010. Diagnostic and prognostic implications of microRNA profiling in prostate carcinoma. Int J Cancer 126: 1166-1176.
55. Segura MF, Hanniford D, Menendez S, Reavie L, Zou X, Alvarez-Diaz S, Zakrzewski J, Blochin E, Rose A, Bogunovic D, et al. 2009. Aberrant miR-182 expression promotes melanoma metastasis by repressing FOXO3 and microphthalmia-associated transcription factor. Proc Natl Acad Sci 106: 1814-1819.
56. Sherr CJ, Roberts JM. 1999. CDK inhibitors: Positive and negative regulators of G1-phase progression. Genes Dev 13: 1501-1512.
57. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. 2007. miR-21-mediated tumor growth. Oncogene 26: 2799-2803.
58. Smyth GK. 2004. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: Article3. doi: 10.2202/1544-6115.1027.
59. Su WL, Kleinhanz RR, Schadt EE. 2011. Characterizing the role of miRNAs within gene regulatory networks using integrative genomics techniques. Mol Syst Biol 7: 490. doi: 10.1038/msb.2011.23.
60. Sun Y, Fang R, Li C, Li L, Li F, Ye X, Chen H. 2010. Hsa-mir-182 suppresses lung tumorigenesis through down regulation of RGS17 expression in vitro. Biochem Biophys Res Commun 396: 501-507.
61. Tenjo T, Toyoda M, Okuda J, Watanabe I, Yamamoto T, Tanaka K, Ohtani M, Nohara T, Kawasaki H, Tanigawa N. 2000. Prognostic significance of p27kip1 protein expression and spontaneous apoptosis in patients with colorectal adenocarcinomas. Oncology 58: 45-51.
62. Thomas M, Lieberman J, Lal A. 2010. Desperately seeking microRNA targets. Nat Struct Mol Biol 17: 1169-1174.
63. Tsang JS, Ebert MS, van Oudenaarden A. 2010. Genome-wide dissection of microRNA functions and cotargeting networks using gene set signatures. Mol Cell 38: 140-153.
64. Turner N, Tutt A, Ashworth A. 2004. Hallmarks of 'BRCAness' in sporadic cancers. Nat Rev Cancer 4: 814-819.
65. Ulitsky I, Laurent LC, Shamir R. 2010. Towards computational prediction of microRNA function and activity. Nucleic Acids Res 38: e160. doi: 10.1093/nar/gkq570.
66. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, et al. 2006. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci 103: 2257-2261.
67. Weeraratne SD, Amani V, Teider N, Pierre-Francois J, Winter D, Kye MJ, Sengupta S, Archer T, Remke M, Bai AH, et al. 2012. Pleiotropic effects of miR-183-96-182 converge to regulate cell survival, proliferation and migration in medulloblastoma. Acta Neuropathol 123: 539-552.
68. Workman C, Jensen LJ, Jarmer H, Berka R, Gautier L, Nielser HB, Saxild HH, Nielsen C, Brunak S, Knudsen S. 2002. A new non-linear normalization method for reducing variability in DNA microarray experiments. Genome Biol 3: presearch0048-research0048.16.
69. Wu J, Shen ZZ, Lu JS, Jiang M, Han QX, Fontana JA, Barsky SH, Shao ZM. 1999. Prognostic role of p27Kip1 and apoptosis in human breast cancer. Br J Cancer 79: 1572-1578.
70. Wu H, Zhu S, Mo YY. 2009. Suppression of cell growth and invasion by miR-205 in breast cancer. Cell Res 19: 439-448.
71. Yu J, Ohuchida K, Mizumoto K, Fujita H, Nakata K, Tanaka M. 2010. MicroRNA miR-17-5p is overexpressed in pancreatic cancer, associated with a poor prognosis, and involved in cancer cell proliferation and invasion. Cancer Biol Ther 10: 748-757.
72. Zhang L, Huang J, Yang N, Greshock J, Megraw MS, Giannakakis A, Liang S, Naylor TL, Barchetti A, Ward MR, et al. 2006. microRNAs exhibit high frequency genomic alterations in human cancer. Proc Natl Acad Sci 103: 9136-9141.
73. Zhang L, Liu T, Huang Y, Liu J. 2011. microRNA-182 inhibits the proliferation and invasion of human lung adenocarcinoma cells through its effect on human cortical actin-associated protein. Int J Mol Med 28: 381-388.
74. Zhu S, Si ML, Wu H, Mo YY. 2007. MicroRNA-21 targets the tumor suppressor gene tropomyosin 1 (TPM1). J Biol Chem 282: 14328-14336.
75. Zhu S, Wu H, Wu F, Nie D, Sheng S, Mo YY. 2008. MicroRNA-21 targets tumor suppressor genes in invasion and metastasis. Cell Res 18: 350-359.