Multiple E2F-Induced MicroRNAs Prevent Replicative Stress in Response to Mitogenic Signaling

REFERENCES

• Aguda, B. D., Y. Kim, M. G. Piper-Hunter, A. Friedman, and C. B. Marsh. 2008. MicroRNA regulation of a cancer network: consequences of the feedback loops involving miR-17-92, E2F, and Myc. Proc. Natl. Acad. Sci. U. S. A. 105:19678–19683.
   PubMed Web of Science ®Google Scholar
• Al-Shahrour, F., P. Minguez, J. M. Vaquerizas, L. Conde, and J. Dopazo. 2005. BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Res. 33:W460–W464.
   PubMedGoogle Scholar
• Ambros, V. 2004. The functions of animal microRNAs. Nature 431:350–355.
   PubMed Web of Science ®Google Scholar
• Arata, Y., M. Fujita, K. Ohtani, S. Kijima, and J. Y. Kato. 2000. Cdk2-dependent and -independent pathways in E2F-mediated S phase induction. J. Biol. Chem. 275:6337–6345.
   PubMedGoogle Scholar
• Bartel, D. P. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136:215–233.
   PubMed Web of Science ®Google Scholar
• Bartkova, J., Z. Horejsi, K. Koed, A. Kramer, F. Tort, K. Zieger, P. Guldberg, M. Sehested, J. M. Nesland, C. Lukas, T. Orntoft, J. Lukas, and J. Bartek. 2005. DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434:864–870.
   PubMed Web of Science ®Google Scholar
• Bhat-Nakshatri, P., G. Wang, N. R. Collins, M. J. Thomson, T. R. Geistlinger, J. S. Carroll, M. Brown, S. Hammond, E. F. Srour, Y. Liu, and H. Nakshatri. 2009. Estradiol-regulated microRNAs control estradiol response in breast cancer cells. Nucleic Acids Res. 37:4850–4861.
   PubMed Web of Science ®Google Scholar
• Bonci, D., V. Coppola, M. Musumeci, A. Addario, R. Giuffrida, L. Memeo, L. D'Urso, A. Pagliuca, M. Biffoni, C. Labbaye, M. Bartucci, G. Muto, C. Peschle, and R. De Maria. 2008. The miR-15a-miR-16-1 cluster controls prostate cancer by targeting multiple oncogenic activities. Nat. Med. 14:1271–1277.
   PubMed Web of Science ®Google Scholar
• Brosh, R., R. Shalgi, A. Liran, G. Landan, K. Korotayev, G. H. Nguyen, E. Enerly, H. Johnsen, Y. Buganim, H. Solomon, I. Goldstein, S. Madar, N. Goldfinger, A. L. Borresen-Dale, D. Ginsberg, C. C. Harris, Y. Pilpel, M. Oren, and V. Rotter. 2008. p53-repressed miRNAs are involved with E2F in a feed-forward loop promoting proliferation. Mol. Syst. Biol. 4:229.
   PubMed Web of Science ®Google Scholar
• Bueno, M. J., I. P. de Castro, and M. Malumbres. 2008. Control of cell proliferation pathways by microRNAs. Cell Cycle 7:3143–3148.
   PubMed Web of Science ®Google Scholar
• Bueno, M. J., I. Perez de Castro, M. Gomez de Cedron, J. Santos, G. A. Calin, J. C. Cigudosa, C. M. Croce, J. Fernandez-Piqueras, and M. Malumbres. 2008. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell 13:496–506.
   PubMed Web of Science ®Google Scholar
• Calin, G. A., and C. M. Croce. 2006. MicroRNA signatures in human cancers. Nat. Rev. Cancer 6:857–866.
   PubMed Web of Science ®Google Scholar
• Calin, G. A., C. D. Dumitru, M. Shimizu, R. Bichi, S. Zupo, E. Noch, H. Aldler, S. Rattan, M. Keating, K. Rai, L. Rassenti, T. Kipps, M. Negrini, F. Bullrich, and C. M. Croce. 2002. 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.
   PubMed Web of Science ®Google Scholar
• Chang, T. C., D. Yu, Y. S. Lee, E. A. Wentzel, D. E. Arking, K. M. West, C. V. Dang, A. Thomas-Tikhonenko, and J. T. Mendell. 2008. Widespread microRNA repression by Myc contributes to tumorigenesis. Nat. Genet. 40:43–50.
   PubMed Web of Science ®Google Scholar
• Chen, D., M. Pacal, P. Wenzel, P. S. Knoepfler, G. Leone, and R. Bremner. 2009. Division and apoptosis of E2f-deficient retinal progenitors. Nature 462:925–929.
   PubMedGoogle Scholar
• Chivukula, R. R., and J. T. Mendell. 2008. Circular reasoning: microRNAs and cell-cycle control. Trends Biochem. Sci. 33:474–481.
   PubMed Web of Science ®Google Scholar
• Chong, J. L., P. L. Wenzel, M. T. Saenz-Robles, V. Nair, A. Ferrey, J. P. Hagan, Y. M. Gomez, N. Sharma, H. Z. Chen, M. Ouseph, S. H. Wang, P. Trikha, B. Culp, L. Mezache, D. J. Winton, O. J. Sansom, D. Chen, R. Bremner, P. G. Cantalupo, M. L. Robinson, J. M. Pipas, and G. Leone. 2009. E2f1-3 switch from activators in progenitor cells to repressors in differentiating cells. Nature 462:930–934.
   PubMed Web of Science ®Google Scholar
• Christensen, J., P. Cloos, U. Toftegaard, D. Klinkenberg, A. P. Bracken, E. Trinh, M. Heeran, L. Di Stefano, and K. Helin. 2005. Characterization of E2F8, a novel E2F-like cell-cycle regulated repressor of E2F-activated transcription. Nucleic Acids Res. 33:5458–5470.
   PubMed Web of Science ®Google Scholar
• Croce, C. M. 2009. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 10:704–714.
   PubMed Web of Science ®Google Scholar
• Deshpande, A., A. Pastore, A. J. Deshpande, Y. Zimmermann, G. Hutter, M. Weinkauf, C. Buske, W. Hiddemann, and M. Dreyling. 2009. 3′UTR mediated regulation of the cyclin D1 proto-oncogene. Cell Cycle 8:3584–3592.
   PubMed Web of Science ®Google Scholar
• Esquela-Kerscher, A., and F. J. Slack. 2006. Oncomirs—microRNAs with a role in cancer. Nat. Rev. Cancer 6:259–269.
   PubMed Web of Science ®Google Scholar
• Eulalio, A., E. Huntzinger, and E. Izaurralde. 2008. Getting to the root of miRNA-mediated gene silencing. Cell 132:9–14.
   PubMed Web of Science ®Google Scholar
• Field, S. J., F. Y. Tsai, F. Kuo, A. M. Zubiaga, W. G. Kaelin, Jr., D. M. Livingston, S. H. Orkin, and M. E. Greenberg. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85:549–561.
   PubMed Web of Science ®Google Scholar
• Filipowicz, W., S. N. Bhattacharyya, and N. Sonenberg. 2008. Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight? Nat. Rev. Genet. 9:102–114.
   PubMed Web of Science ®Google Scholar
• Fontana, L., M. E. Fiori, S. Albini, L. Cifaldi, S. Giovinazzi, M. Forloni, R. Boldrini, A. Donfrancesco, V. Federici, P. Giacomini, C. Peschle, and D. Fruci. 2008. Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 3:e2236.
   PubMed Web of Science ®Google Scholar
• Fornari, F., L. Gramantieri, M. Ferracin, A. Veronese, S. Sabbioni, G. A. Calin, G. L. Grazi, C. Giovannini, C. M. Croce, L. Bolondi, and M. Negrini. 2008. MiR-221 controls CDKN1C/p57 and CDKN1B/p27 expression in human hepatocellular carcinoma. Oncogene 27:5651–5661.
   PubMed Web of Science ®Google Scholar
• Galardi, S., N. Mercatelli, E. Giorda, S. Massalini, G. V. Frajese, S. A. Ciafre, and M. G. Farace. 2007. miR-221 and miR-222 expression affects the proliferation potential of human prostate carcinoma cell lines by targeting p27Kip1. J. Biol. Chem. 282:23716–23724.
   PubMed Web of Science ®Google Scholar
• Garcia-Higuera, I., E. Manchado, P. Dubus, M. Canamero, J. Mendez, S. Moreno, and M. Malumbres. 2008. Genomic stability and tumour suppression by the APC/C cofactor Cdh1. Nat. Cell Biol. 10:802–811.
   PubMed Web of Science ®Google Scholar
• Giangrande, P. H., T. C. Hallstrom, C. Tunyaplin, K. Calame, and J. R. Nevins. 2003. Identification of E-box factor TFE3 as a functional partner for the E2F3 transcription factor. Mol. Cell. Biol. 23:3707–3720.
   PubMedGoogle Scholar
• Giannakakis, A., R. Sandaltzopoulos, J. Greshock, S. Liang, J. Huang, K. Hasegawa, C. Li, A. O'Brien-Jenkins, D. Katsaros, B. L. Weber, C. Simon, G. Coukos, and L. Zhang. 2008. miR-210 links hypoxia with cell cycle regulation and is deleted in human epithelial ovarian cancer. Cancer Biol. Ther. 7:255–264.
   PubMed Web of Science ®Google Scholar
• Halazonetis, T. D., V. G. Gorgoulis, and J. Bartek. 2008. An oncogene-induced DNA damage model for cancer development. Science 319:1352–1355.
   PubMed Web of Science ®Google Scholar
• He, L., X. He, S. W. Lowe, and G. J. Hannon. 2007. microRNAs join the p53 network—another piece in the tumour-suppression puzzle. Nat. Rev. Cancer 7:819–822.
   PubMed Web of Science ®Google Scholar
• Hobert, O. 2008. Gene regulation by transcription factors and microRNAs. Science 319:1785–1786.
   PubMed Web of Science ®Google Scholar
• Infante, A., U. Laresgoiti, J. Fernandez-Rueda, A. Fullaondo, J. Galan, R. Diaz-Uriarte, M. Malumbres, S. J. Field, and A. M. Zubiaga. 2008. E2F2 represses cell cycle regulators to maintain quiescence. Cell Cycle 7:3915–3927.
   PubMed Web of Science ®Google Scholar
• Inomata, M., H. Tagawa, Y. M. Guo, Y. Kameoka, N. Takahashi, and K. Sawada. 2009. MicroRNA-17-92 down-regulates expression of distinct targets in different B-cell lymphoma subtypes. Blood 113:396–402.
   PubMed Web of Science ®Google Scholar
• Ivanovska, I., A. S. Ball, R. L. Diaz, J. F. Magnus, M. Kibukawa, J. M. Schelter, S. V. Kobayashi, L. Lim, J. Burchard, A. L. Jackson, P. S. Linsley, and M. A. Cleary. 2008. MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol. Cell. Biol. 28:2167–2174.
   PubMed Web of Science ®Google Scholar
• Ivanovska, I., and M. A. Cleary. 2008. Combinatorial microRNAs: working together to make a difference. Cell Cycle 7:3137–3142.
   PubMed Web of Science ®Google Scholar
• Iyer, V. R., M. B. Eisen, D. T. Ross, G. Schuler, T. Moore, J. C. Lee, J. M. Trent, L. M. Staudt, J. Hudson, Jr., M. S. Boguski, D. Lashkari, D. Shalon, D. Botstein, and P. O. Brown. 1999. The transcriptional program in the response of human fibroblasts to serum. Science 283:83–87.
   PubMed Web of Science ®Google Scholar
• Johnson, C. D., A. Esquela-Kerscher, G. Stefani, M. Byrom, K. Kelnar, D. Ovcharenko, M. Wilson, X. Wang, J. Shelton, J. Shingara, L. Chin, D. Brown, and F. J. Slack. 2007. The let-7 microRNA represses cell proliferation pathways in human cells. Cancer Res. 67:7713–7722.
   PubMed Web of Science ®Google Scholar
• Kim, V. N., J. Han, and M. C. Siomi. 2009. Biogenesis of small RNAs in animals. Nat. Rev. Mol. Cell Biol. 10:126–139.
   PubMed Web of Science ®Google Scholar
• Klein, U., M. Lia, M. Crespo, R. Siegel, Q. Shen, T. Mo, A. Ambesi-Impiombato, A. Califano, A. Migliazza, G. Bhagat, and R. Dalla-Favera. 2010. The DLEU2/miR-15a/16-1 cluster controls B cell proliferation and its deletion leads to chronic lymphocytic leukemia. Cancer Cell 17:28–40.
   PubMed Web of Science ®Google Scholar
• Lee, S. O., T. Masyuk, P. Splinter, J. M. Banales, A. Masyuk, A. Stroope, and N. Larusso. 2008. MicroRNA15a modulates expression of the cell-cycle regulator Cdc25A and affects hepatic cystogenesis in a rat model of polycystic kidney disease. J. Clin. Invest. 118:3714–3724.
   PubMed Web of Science ®Google Scholar
• Legesse-Miller, A., O. Elemento, S. J. Pfau, J. J. Forman, S. Tavazoie, and H. A. Coller. 2009. let-7 overexpression leads to an increased fraction of cells in G2/M, direct down-regulation of Cdc34, and stabilization of Wee1 kinase in primary fibroblasts. J. Biol. Chem. 284:6605–6609.
   PubMedGoogle Scholar
• le Sage, C., R. Nagel, D. A. Egan, M. Schrier, E. Mesman, A. Mangiola, C. Anile, G. Maira, N. Mercatelli, S. A. Ciafre, M. G. Farace, and R. Agami. 2007. Regulation of the p27(Kip1) tumor suppressor by miR-221 and miR-222 promotes cancer cell proliferation. EMBO J. 26:3699–3708.
   PubMed Web of Science ®Google Scholar
• Li, G., C. Luna, J. Qiu, D. L. Epstein, and P. Gonzalez. 2009. Alterations in microRNA expression in stress-induced cellular senescence. Mech. Ageing Dev. 130:731–741.
   PubMed Web of Science ®Google Scholar
• Linsley, P. S., J. Schelter, J. Burchard, M. Kibukawa, M. M. Martin, S. R. Bartz, J. M. Johnson, J. M. Cummins, C. K. Raymond, H. Dai, N. Chau, M. Cleary, A. L. Jackson, M. Carleton, and L. Lim. 2007. Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol. 27:2240–2252.
   PubMed Web of Science ®Google Scholar
• Liu, Q., H. Fu, F. Sun, H. Zhang, Y. Tie, J. Zhu, R. Xing, Z. Sun, and X. Zheng. 2008. miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res. 36:5391–5404.
   PubMed Web of Science ®Google Scholar
• Malumbres, M., and M. Barbacid. 2009. Cell cycle, CDKs and cancer: a changing paradigm. Nat. Rev. Cancer 9:153–166.
   PubMed Web of Science ®Google Scholar
• Malumbres, M., and M. Barbacid. 2001. To cycle or not to cycle: a critical decision in cancer. Nat. Rev. Cancer 1:222–231.
   PubMed Web of Science ®Google Scholar
• Malumbres, M., R. Sotillo, D. Santamaria, J. Galan, A. Cerezo, S. Ortega, P. Dubus, and M. Barbacid. 2004. Mammalian cells cycle without the D-type cyclin-dependent kinases Cdk4 and Cdk6. Cell 118:493–504.
   PubMed Web of Science ®Google Scholar
• Martin, A., J. Odajima, S. L. Hunt, P. Dubus, S. Ortega, M. Malumbres, and M. Barbacid. 2005. Cdk2 is dispensable for cell cycle inhibition and tumor suppression mediated by p27(Kip1) and p21(Cip1). Cancer Cell 7:591–598.
   PubMed Web of Science ®Google Scholar
• Muller, H., A. P. Bracken, R. Vernell, M. C. Moroni, F. Christians, E. Grassilli, E. Prosperini, E. Vigo, J. D. Oliner, and K. Helin. 2001. E2Fs regulate the expression of genes involved in differentiation, development, proliferation, and apoptosis. Genes Dev. 15:267–285.
   PubMed Web of Science ®Google Scholar
• Murga, M., O. Fernandez-Capetillo, S. J. Field, B. Moreno, L. R. Borlado, Y. Fujiwara, D. Balomenos, A. Vicario, A. C. Carrera, S. H. Orkin, M. E. Greenberg, and A. M. Zubiaga. 2001. Mutation of E2F2 in mice causes enhanced T lymphocyte proliferation, leading to the development of autoimmunity. Immunity 15:959–970.
   PubMedGoogle Scholar
• Murga, M., I. Jaco, Y. Fan, R. Soria, B. Martinez-Pastor, M. Cuadrado, S. M. Yang, M. A. Blasco, A. I. Skoultchi, and O. Fernandez-Capetillo. 2007. Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol. 178:1101–1108.
   PubMed Web of Science ®Google Scholar
• O'Donnell, K. A., E. A. Wentzel, K. I. Zeller, C. V. Dang, and J. T. Mendell. 2005. c-Myc-regulated microRNAs modulate E2F1 expression. Nature 435:839–843.
   PubMed Web of Science ®Google Scholar
• Pantoja, C., and M. Serrano. 1999. Murine fibroblasts lacking p21 undergo senescence and are resistant to transformation by oncogenic Ras. Oncogene 18:4974–4982.
   PubMed Web of Science ®Google Scholar
• Petrocca, F., R. Visone, M. R. Onelli, M. H. Shah, M. S. Nicoloso, I. de Martino, D. Iliopoulos, E. Pilozzi, C. G. Liu, M. Negrini, L. Cavazzini, S. Volinia, H. Alder, L. P. Ruco, G. Baldassarre, C. M. Croce, and A. Vecchione. 2008. E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13:272–286.
   PubMed Web of Science ®Google Scholar
• Pickering, M. T., B. M. Stadler, and T. F. Kowalik. 2009. miR-17 and miR-20a temper an E2F1-induced G1 checkpoint to regulate cell cycle progression. Oncogene 28:140–145.
   PubMedGoogle Scholar
• Ritchie, W., S. Flamant, and J. E. Rasko. 2009. Predicting microRNA targets and functions: traps for the unwary. Nat. Methods 6:397–398.
   PubMed Web of Science ®Google Scholar
• Roush, S., and F. J. Slack. 2008. The let-7 family of microRNAs. Trends Cell Biol. 18:505–516.
   PubMed Web of Science ®Google Scholar
• Saeed, A. I., V. Sharov, J. White, J. Li, W. Liang, N. Bhagabati, J. Braisted, M. Klapa, T. Currier, M. Thiagarajan, A. Sturn, M. Snuffin, A. Rezantsev, D. Popov, A. Ryltsov, E. Kostukovich, I. Borisovsky, Z. Liu, A. Vinsavich, V. Trush, and J. Quackenbush. 2003. TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34:374–378.
   PubMed Web of Science ®Google Scholar
• Saini, H. K., S. Griffiths-Jones, and A. J. Enright. 2007. Genomic analysis of human microRNA transcripts. Proc. Natl. Acad. Sci. U. S. A. 104:17719–17724.
   PubMed Web of Science ®Google Scholar
• Schultz, J., P. Lorenz, G. Gross, S. Ibrahim, and M. Kunz. 2008. MicroRNA let-7b targets important cell cycle molecules in malignant melanoma cells and interferes with anchorage-independent growth. Cell Res. 18:549–557.
   PubMed Web of Science ®Google Scholar
• Sherr, C. J., and J. M. Roberts. 1999. CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev. 13:1501–1512.
   PubMed Web of Science ®Google Scholar
• Stefani, G., and F. J. Slack. 2008. Small non-coding RNAs in animal development. Nat. Rev. Mol. Cell Biol. 9:219–230.
   PubMed Web of Science ®Google Scholar
• Tazawa, H., N. Tsuchiya, M. Izumiya, and H. Nakagama. 2007. Tumor-suppressive miR-34a induces senescence-like growth arrest through modulation of the E2F pathway in human colon cancer cells. Proc. Natl. Acad. Sci. U. S. A. 104:15472–15477.
   PubMed Web of Science ®Google Scholar
• Trimarchi, J. M., and J. A. Lees. 2002. Sibling rivalry in the E2F family. Nat. Rev. Mol. Cell Biol. 3:11–20.
   PubMed Web of Science ®Google Scholar
• van den Heuvel, S., and N. J. Dyson. 2008. Conserved functions of the pRB and E2F families. Nat. Rev. Mol. Cell Biol. 9:713–724.
   PubMed Web of Science ®Google Scholar
• Visone, R., L. Russo, P. Pallante, I. De Martino, A. Ferraro, V. Leone, E. Borbone, F. Petrocca, H. Alder, C. M. Croce, and A. Fusco. 2007. MicroRNAs (miR)-221 and miR-222, both overexpressed in human thyroid papillary carcinomas, regulate p27Kip1 protein levels and cell cycle. Endocr. Relat. Cancer 14:791–798.
   PubMed Web of Science ®Google Scholar
• Voorhoeve, P. M., C. le Sage, M. Schrier, A. J. Gillis, H. Stoop, R. Nagel, Y. P. Liu, J. van Duijse, J. Drost, A. Griekspoor, E. Zlotorynski, N. Yabuta, G. De Vita, H. Nojima, L. H. Looijenga, and R. Agami. 2006. A genetic screen implicates miRNA-372 and miRNA-373 as oncogenes in testicular germ cell tumors. Cell 124:1169–1181.
   PubMed Web of Science ®Google Scholar
• Woods, K., J. M. Thomson, and S. M. Hammond. 2007. Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J. Biol. Chem. 282:2130–2134.
   PubMed Web of Science ®Google Scholar
• Yang, N., S. Kaur, S. Volinia, J. Greshock, H. Lassus, K. Hasegawa, S. Liang, A. Leminen, S. Deng, L. Smith, C. N. Johnstone, X. M. Chen, C. G. Liu, Q. Huang, D. Katsaros, G. A. Calin, B. L. Weber, R. Butzow, C. M. Croce, G. Coukos, and L. Zhang. 2008. MicroRNA microarray identifies Let-7i as a novel biomarker and therapeutic target in human epithelial ovarian cancer. Cancer Res. 68:10307–10314.
   PubMed Web of Science ®Google Scholar
• Yu, Z., C. Wang, M. Wang, Z. Li, M. C. Casimiro, M. Liu, K. Wu, J. Whittle, X. Ju, T. Hyslop, P. McCue, and R. G. Pestell. 2008. A cyclin D1/microRNA 17/20 regulatory feedback loop in control of breast cancer cell proliferation. J. Cell Biol. 182:509–517.
   PubMed Web of Science ®Google Scholar
• Zhang, Y., T. Chao, R. Li, W. Liu, Y. Chen, X. Yan, Y. Gong, B. Yin, W. Liu, B. Qiang, J. Zhao, J. Yuan, and X. Peng. 2009. MicroRNA-128 inhibits glioma cells proliferation by targeting transcription factor E2F3a. J. Mol. Med. 87:43–51.
   PubMed Web of Science ®Google Scholar