Post-transcriptional regulation of BRCA1 through its coding sequence by the miR-15/107 group of miRNAs

Frontiers in Genetics

Volumn 6, Issue JUL, 2015, Pages

  Quann, Kevin ^a   Jing, Yi ^a   Rigoutsos, Isidore ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

BRCA1; DNA damage repair; microRNAs; MiRNAs; Non coding RNA; Post transcriptional regulation

Indexed keywords

BRCA1 PROTEIN; LUCIFERASE; MESSENGER RNA; MICRORNA 107;

3' UNTRANSLATED REGION; ARTICLE; COLORECTAL CARCINOMA; CONTROLLED STUDY; DNA REPAIR; ELASTOGRAPHY; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC TRANSCRIPTION; HCT116 CELL LINE; HUMAN; HUMAN CELL; HUMAN TISSUE; LUCIFERASE ASSAY; PANCREAS ADENOCARCINOMA; PLASMID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN DNA INTERACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PROCESSING; TRANSIENT TRANSFECTION; WESTERN BLOTTING;

AGOUTI PACA;

EID: 84940101957     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2015.00242     Document Type: Article

References (56)

1. Aqeilan, R. I., Calin, G. A., and Croce, C. M. (2010). miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ. 17, 215-220. doi: 10.1038/cdd.2009.69.
2. Bhattacharya, R., Nicoloso, M., Arvizo, R., Wang, E., Cortez, A., Rossi, S., et al. (2009). MiR-15a and MiR-16 control Bmi-1 expression in ovarian cancer. Cancer Res. 69, 9090-9095. doi: 10.1158/0008-5472.CAN-09-2552.
3. Bonci, D., Coppola, V., Musumeci, M., Addario, A., Giuffrida, R., Memeo, L., et al. (2008). The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat. Med. 14, 1271-1277. doi: 10.1038/nm.1880.
4. Brodersen, P., and Voinnet, O. (2009). Revisiting the principles of microRNA target recognition and mode of action. Nat. Rev. Mol. Cell Biol. 10, 141-148. doi: 10.1038/nrm2619.
5. Chang, S., and Sharan, S. K. (2012). BRCA1 and microRNAs: emerging networks and potential therapeutic targets. Mol. Cells 34, 425-432. doi: 10.1007/s10059-012-0118-y.
6. Chen, C. Q., Chen, C. S., Chen, J. J., Zhou, L. P., Xu, H. L., Jin, W. W., et al. (2013). Histone deacetylases inhibitor trichostatin A increases the expression of Dleu2/miR-15a/16-1 via HDAC3 in non-small cell lung cancer. Mol. Cell. Biochem. 383, 137-148. doi: 10.1007/s11010-013-1762-z.
7. Chi, S. W., Hannon, G. J., and Darnell, R. B. (2012). An alternative mode of microRNA target recognition. Nat. Struct. Mol. Biol. 19, 321-327. doi: 10.1038/nsmb.2230.
8. Chi, S. W., Zang, J. B., Mele, A., and Darnell, R. B. (2009). Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps. Nature 460, 479-486. doi: 10.1038/nature08170.
9. Clark, P. M., Loher, P., Quann, K., Brody, J., Londin, E. R., and Rigoutsos, I. (2014). Argonaute CLIP-Seq reveals miRNA targetome diversity across tissue types. Sci. Rep. 4, 5947. doi: 10.1038/srep05947.
10. Cunningham, F., Amode, M. R., Barrell, D., Beal, K., Billis, K., Brent, S., et al. (2015). Ensembl 2015. Nucleic Acids Res. 43, D662-D669. doi: 10.1093/nar/gku1010.
11. Duursma, A. M., Kedde, M., Schrier, M., Le Sage, C., and Agami, R. (2008). miR-148 targets human DNMT3b protein coding region. RNA 14, 872-877. doi: 10.1261/rna.972008.
12. Fackenthal, J. D., and Olopade, O. I. (2007). Breast cancer risk associated with BRCA1 and BRCA2 in diverse populations. Nat. Rev. Cancer 7, 937-948. doi: 10.1038/nrc2054.
13. Filipowicz, W., Bhattacharyya, S. N., and Sonenberg, N. (2008). Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9, 102-114. doi: 10.1038/nrg2290.
14. Finnerty, J. R., Wang, W. X., Hebert, S. S., Wilfred, B. R., Mao, G., and Nelson, P. T. (2010). The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J. Mol. Biol. 402, 491-509. doi: 10.1016/j.jmb.2010.07.051.
15. Forman, J. J., Legesse-Miller, A., and Coller, H. A. (2008). A search for conserved sequences in coding regions reveals that the let-7 microRNA targets Dicer within its coding sequence. Proc. Natl. Acad. Sci. U.S.A. 105, 14879-14884. doi: 10.1073/pnas.0803230105.
16. Furuta, M., Kozaki, K., Tanimoto, K., Tanaka, S., Arii, S., Shimamura, T., et al. (2013). The tumor-suppressive miR-497-195 cluster targets multiple cell-cycle regulators in hepatocellular carcinoma. PLoS ONE 8:e60155. doi: 10.1371/journal.pone.0060155.
17. Garcia, A. I., Buisson, M., Bertrand, P., Rimokh, R., Rouleau, E., Lopez, B. S., et al. (2011). Down-regulation of BRCA1 expression by miR-146a and miR-146b-5p in triple negative sporadic breast cancers. EMBO Mol. Med. 3, 279-290. doi: 10.1002/emmm.201100136.
18. Grey, F., Tirabassi, R., Meyers, H., Wu, G., Mcweeney, S., Hook, L., et al. (2010). A viral microRNA down-regulates multiple cell cycle genes through mRNA 5'UTRs. PLoS Pathog. 6:e1000967. doi: 10.1371/journal.ppat.1000967.
19. Guo, S. T., Jiang, C. C., Wang, G. P., Li, Y. P., Wang, C. Y., Guo, X. Y., et al. (2013). MicroRNA-497 targets insulin-like growth factor 1 receptor and has a tumour suppressive role in human colorectal cancer. Oncogene 32, 1910-1920. doi: 10.1038/onc.2012.214.
20. Ha, I., Wightman, B., and Ruvkun, G. (1996). A bulged lin-4/lin-14 RNA duplex is sufficient for Caenorhabditis elegans lin-14 temporal gradient formation. Genes Dev. 10, 3041-3050. doi: 10.1101/gad.10.23.3041.
21. Hafner, M., Landthaler, M., Burger, L., Khorshid, M., Hausser, J., Berninger, P., et al. (2010). Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141, 129-141. doi: 10.1016/j.cell.2010.03.009.
22. He, L., and Hannon, G. J. (2004). MicroRNAs: small RNAs with a big role in gene regulation. Nat. Rev. Genet. 5, 522-531. doi: 10.1038/nrg1379.
23. Helleday, T. (2011). The underlying mechanism for the PARP and BRCA synthetic lethality: clearing up the misunderstandings. Mol. Oncol. 5, 387-393. doi: 10.1016/j.molonc.2011.07.001.
24. Helleday, T., Petermann, E., Lundin, C., Hodgson, B., and Sharma, R. A. (2008). DNA repair pathways as targets for cancer therapy. Nat. Rev. Cancer 8, 193-204. doi: 10.1038/nrc2342.
25. Helwak, A., Kudla, G., Dudnakova, T., and Tollervey, D. (2013). Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153, 654-665. doi: 10.1016/j.cell.2013.03.043.
26. Huang, J. W., Wang, Y., Dhillon, K. K., Calses, P., Villegas, E., Mitchell, P. S., et al. (2013). Systematic screen identifies miRNAs that target RAD51 and RAD51D to enhance chemosensitivity. Mol. Cancer Res. 11, 1564-1573. doi: 10.1158/1541-7786.MCR-13-0292.
27. Huang, V., Place, R. F., Portnoy, V., Wang, J., Qi, Z., Jia, Z., et al. (2012). Upregulation of Cyclin B1 by miRNA and its implications in cancer. Nucleic Acids Res. 40, 1695-1707. doi: 10.1093/nar/gkr934.
28. Kozomara, A., and Griffiths-Jones, S. (2014). miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Res. 42, D68-D73. doi: 10.1093/nar/gkt1181.
29. Lal, A., Kim, H. H., Abdelmohsen, K., Kuwano, Y., Pullmann, R. Jr., Srikantan, S., et al. (2008). p16(INK4a) translation suppressed by miR-24. PLoS ONE 3:e1864. doi: 10.1371/journal.pone.0001864.
30. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., et al. (2007). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401-1414. doi: 10.1016/j.cell.2007.04.040.
31. Lee, I., Ajay, S. S., Yook, J. I., Kim, H. S., Hong, S. H., Kim, N. H., et al. (2009). New class of microRNA targets containing simultaneous 5'-UTR and 3'-UTR interaction sites. Genome Res. 19, 1175-1183. doi: 10.1101/gr.089367.108.
32. Li, D., Wang, Q., Liu, C., Duan, H., Zeng, X., Zhang, B., et al. (2012). Aberrant expression of miR-638 contributes to benzo(a)pyrene-induced human cell transformation. Toxicol. Sci. 125, 382-391. doi: 10.1093/toxsci/kfr299.
33. Li, D., Zhao, Y., Liu, C., Chen, X., Qi, Y., Jiang, Y., et al. (2011). Analysis of MiR-195 and MiR-497 expression, regulation and role in breast cancer. Clin. Cancer Res. 17, 1722-1730. doi: 10.1158/1078-0432.CCR-10-1800.
34. Li, L. C., Okino, S. T., Zhao, H., Pookot, D., Place, R. F., Urakami, S., et al. (2006). Small dsRNAs induce transcriptional activation in human cells. Proc. Natl. Acad. Sci. U.S.A. 103, 17337-17342. doi: 10.1073/pnas.0607015103.
35. Loeb, G. B., Khan, A. A., Canner, D., Hiatt, J. B., Shendure, J., Darnell, R. B., et al. (2012). Transcriptome-wide miR-155 binding map reveals widespread noncanonical microRNA targeting. Mol. Cell 48, 760-770. doi: 10.1016/j.molcel.2012.10.002.
36. Londin, E. R., Hatzimichael, E., Loher, P., Edelstein, L., Shaw, C., Delgrosso, K., et al. (2014). The human platelet: strong transcriptome correlations among individuals associate weakly with the platelet proteome. Biol. Direct 9, 3. doi: 10.1186/1745-6150-9-3.
37. Miranda, K. C., Huynh, T., Tay, Y., Ang, Y. S., Tam, W. L., Thomson, A. M., et al. (2006). A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203-1217. doi: 10.1016/j.cell.2006.07.031.
38. Moskwa, P., Buffa, F. M., Pan, Y., Panchakshari, R., Gottipati, P., Muschel, R. J., et al. (2011). miR-182-mediated downregulation of BRCA1 impacts DNA repair and sensitivity to PARP inhibitors. Mol. Cell 41, 210-220. doi: 10.1016/j.molcel.2010.12.005.
39. Musumeci, M., Coppola, V., Addario, A., Patrizii, M., Maugeri-Sacca, M., Memeo, L., et al. (2011). Control of tumor and microenvironment cross-talk by miR-15a and miR-16 in prostate cancer. Oncogene 30, 4231-4242. doi: 10.1038/onc.2011.140.
40. Nelson, P. T., Wang, W. X., Mao, G., Wilfred, B. R., Xie, K., Jennings, M. H., et al. (2011). Specific sequence determinants of miR-15/107 microRNA gene group targets. Nucleic Acids Res. 39, 8163-8172. doi: 10.1093/nar/gkr532.
41. Pascal, L. E., True, L. D., Campbell, D. S., Deutsch, E. W., Risk, M., Coleman, I. M., et al. (2008). Correlation of mRNA and protein levels: cell type-specific gene expression of cluster designation antigens in the prostate. BMC Genomics 9:246. doi: 10.1186/1471-2164-9-246.
42. Place, R. F., Li, L. C., Pookot, D., Noonan, E. J., and Dahiya, R. (2008). MicroRNA-373 induces expression of genes with complementary promoter sequences. Proc. Natl. Acad. Sci. U.S.A. 105, 1608-1613. doi: 10.1073/pnas.0707594105.
43. Polytarchou, C., Iliopoulos, D., and Struhl, K. (2012). An integrated transcriptional regulatory circuit that reinforces the breast cancer stem cell state. Proc. Natl. Acad. Sci. U.S.A. 109, 14470-14475. doi: 10.1073/pnas.1212811109.
44. Rigoutsos, I. (2009). New tricks for animal microRNAS: targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res. 69, 3245-3248. doi: 10.1158/0008-5472.CAN-09-0352.
45. Rosen, E. M. (2013). BRCA1 in the DNA damage response and at telomeres. Front. Genet. 4:85. doi: 10.3389/fgene.2013.00085.
46. Roy, R., Chun, J., and Powell, S. N. (2012). BRCA1 and BRCA2: different roles in a common pathway of genome protection. Nat. Rev. Cancer 12, 68-78. doi: 10.1038/nrc3181.
47. Saunus, J. M., French, J. D., Edwards, S. L., Beveridge, D. J., Hatchell, E. C., Wagner, S. A., et al. (2008). Posttranscriptional regulation of the breast cancer susceptibility gene BRCA1 by the RNA binding protein HuR. Cancer Res. 68, 9469-9478. doi: 10.1158/0008-5472.CAN-08-1159.
48. Schwanhausser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., et al. (2011). Global quantification of mammalian gene expression control. Nature 473, 337-342. doi: 10.1038/nature10098.
49. Shen, J., Ambrosone, C. B., Dicioccio, R. A., Odunsi, K., Lele, S. B., and Zhao, H. (2008a). A functional polymorphism in the miR-146a gene and age of familial breast/ovarian cancer diagnosis. Carcinogenesis 29, 1963-1966. doi: 10.1093/carcin/bgn172.
50. Shen, W. F., Hu, Y. L., Uttarwar, L., Passegue, E., and Largman, C. (2008b). MicroRNA-126 regulates HOXA9 by binding to the homeobox. Mol. Cell. Biol. 28, 4609-4619. doi: 10.1128/MCB.01652-07.
51. Shen, J., Ambrosone, C. B., and Zhao, H. (2009). Novel genetic variants in microRNA genes and familial breast cancer. Int. J. Cancer 124, 1178-1182. doi: 10.1002/ijc.24008.
52. Tay, Y., Zhang, J., Thomson, A. M., Lim, B., and Rigoutsos, I. (2008). MicroRNAs to Nanog, Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature 455, 1124-1128. doi: 10.1038/nature07299.
53. Vogel, C., and Marcotte, E. M. (2012). Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 13, 227-232. doi: 10.1038/nrg3185.
54. Wang, L., Li, B., Li, L., and Wang, T. (2013). MicroRNA-497 suppresses proliferation and induces apoptosis in prostate cancer cells. Asian Pac. J. Cancer Prev. 14, 3499-3502. doi: 10.7314/APJCP.2013.14.6.3499.
55. Zhou, H., and Rigoutsos, I. (2014). MiR-103a-3p targets the 5' UTR of GPRC5A in pancreatic cells. RNA 20, 1431-1439. doi: 10.1261/rna.045757.114.
56. Zhu, J. Y., Pfuhl, T., Motsch, N., Barth, S., Nicholls, J., Grasser, F., et al. (2009). Identification of novel Epstein-Barr virus microRNA genes from nasopharyngeal carcinomas. J. Virol. 83, 3333-3341. doi: 10.1128/JVI.01689-08.