MicroRNA-155 Is Regulated by the Transforming Growth Factor β/Smad Pathway and Contributes to Epithelial Cell Plasticity by Targeting RhoA

REFERENCES

• Ambros, V. 2004. The functions of animal microRNAs. Nature 431:350–355.
   PubMed Web of Science ®Google Scholar
• Burk, U., J. Schubert, U. Wellner, O. Schmalhofer, E. Vincan, S. Spaderna, and T. Brabletz. 2008. A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep. 9:582–589.
   PubMed Web of Science ®Google Scholar
• Cai, X., C. H. Hagedorn, and B. R. Cullen. 2004. Human microRNAs are processed from capped, polyadenylated transcripts that can also function as mRNAs. RNA 10:1957–1966.
   PubMed Web of Science ®Google Scholar
• Costinean, S., N. Zanesi, Y. Pekarsky, E. Tili, S. Volinia, N. Heerema, and C. M. Croce. 2006. Pre-B cell proliferation and lymphoblastic leukemia/high-grade lymphoma in Eμ-miR155 transgenic mice. Proc. Natl. Acad. Sci. USA 103:7024–7029.
   PubMed Web of Science ®Google Scholar
• Deckers, M., M. van Dinther, J. Buijs, I. Que, C. Lowik, G. van der Pluijm, and P. ten Dijke. 2006. The tumor suppressor Smad4 is required for transforming growth factor beta-induced epithelial to mesenchymal transition and bone metastasis of breast cancer cells. Cancer Res. 66:2202–2209.
   PubMed Web of Science ®Google Scholar
• Didiano, D., and O. Hobert. 2006. Perfect seed pairing is not a generally reliable predictor for miRNA-target interactions. Nat. Struct. Mol. Biol. 13:849–851.
   PubMed Web of Science ®Google Scholar
• Doench, J. G., and P. A. Sharp. 2004. Specificity of microRNA target selection in translational repression. Genes Dev. 18:504–511.
   PubMed Web of Science ®Google Scholar
• Eis, P. S., W. Tam, L. Sun, A. Chadburn, Z. Li, M. F. Gomez, E. Lund, and J. E. Dahlberg. 2005. Accumulation of miR-155 and BIC RNA in human B cell lymphomas. Proc. Natl. Acad. Sci. USA 102:3627–3632.
   PubMed Web of Science ®Google Scholar
• Farh, K. K., A. Grimson, C. Jan, B. P. Lewis, W. K. Johnston, L. P. Lim, C. B. Burge, and D. P. Bartel. 2005. The widespread impact of mammalian microRNAs on mRNA repression and evolution. Science 310:1817–1821.
   PubMed Web of Science ®Google Scholar
• Gironella, M., M. Seux, M. J. Xie, C. Cano, R. Tomasini, J. Gommeaux, S. Garcia, J. Nowak, M. L. Yeung, K. T. Jeang, A. Chaix, L. Fazli, Y. Motoo, Q. Wang, P. Rocchi, A. Russo, M. Gleave, J. C. Dagorn, J. L. Iovanna, A. Carrier, M. J. Pebusque, and N. J. Dusetti. 2007. Tumor protein 53-induced nuclear protein 1 expression is repressed by miR-155, and its restoration inhibits pancreatic tumor development. Proc. Natl. Acad. Sci. USA 104:16170–16175.
   PubMed Web of Science ®Google Scholar
• Gottwein, E., N. Mukherjee, C. Sachse, C. Frenzel, W. H. Majoros, J. T. Chi, R. Braich, M. Manoharan, J. Soutschek, U. Ohler, and B. R. Cullen. 2007. A viral microRNA functions as an orthologue of cellular miR-155. Nature 450:1096–1099.
   PubMed Web of Science ®Google Scholar
• Gregory, P. A., A. G. Bert, E. L. Paterson, S. C. Barry, A. Tsykin, G. Farshid, M. A. Vadas, Y. Khew-Goodall, and G. J. Goodall. 2008. The miR-200 family and miR-205 regulate epithelial to mesenchymal transition by targeting ZEB1 and SIP1. Nat. Cell Biol. 10:593–601.
   PubMed Web of Science ®Google Scholar
• Griffiths-Jones, S., R. J. Grocock, S. van Dongen, A. Bateman, and A. J. Enright. 2006. miRBase: microRNA sequences, targets and gene nomenclature. Nucleic Acids Res. 34:D140–144.
   PubMed Web of Science ®Google Scholar
• Grun, D., Y. L. Wang, D. Langenberger, K. C. Gunsalus, and N. Rajewsky. 2005. microRNA target predictions across seven Drosophila species and comparison to mammalian targets. PLoS Comput. Biol. 1:e13.
   PubMed Web of Science ®Google Scholar
• Han, J., Y. Lee, K. H. Yeom, Y. K. Kim, H. Jin, and V. N. Kim. 2004. The Drosha-DGCR8 complex in primary microRNA processing. Genes Dev. 18:3016–3027.
   PubMed Web of Science ®Google Scholar
• Houbaviy, H. B., M. F. Murray, and P. A. Sharp. 2003. Embryonic stem cell-specific microRNAs. Dev. Cell 5:351–358.
   PubMed Web of Science ®Google Scholar
• Iorio, M. V., M. Ferracin, C. G. Liu, A. Veronese, R. Spizzo, S. Sabbioni, E. Magri, M. Pedriali, M. Fabbri, M. Campiglio, S. Menard, J. P. Palazzo, A. Rosenberg, P. Musiani, S. Volinia, I. Nenci, G. A. Calin, P. Querzoli, M. Negrini, and C. M. Croce. 2005. MicroRNA gene expression deregulation in human breast cancer. Cancer Res. 65:7065–7070.
   PubMed Web of Science ®Google Scholar
• Kang, Y., W. He, S. Tulley, G. P. Gupta, I. Serganova, C. R. Chen, K. Manova-Todorova, R. Blasberg, W. L. Gerald, and J. Massague. 2005. Breast cancer bone metastasis mediated by the Smad tumor suppressor pathway. Proc. Natl. Acad. Sci. USA 102:13909–13914.
   PubMed Web of Science ®Google Scholar
• Kertesz, M., N. Iovino, U. Unnerstall, U. Gaul, and E. Segal. 2007. The role of site accessibility in microRNA target recognition. Nat. Genet. 39:1278–1284.
   PubMed Web of Science ®Google Scholar
• Kluiver, J., A. van den Berg, D. de Jong, T. Blokzijl, G. Harms, E. Bouwman, S. Jacobs, S. Poppema, and B. J. Kroesen. 2007. Regulation of pri-microRNA BIC transcription and processing in Burkitt lymphoma. Oncogene 26:3769–3776.
   PubMed Web of Science ®Google Scholar
• Korpal, M., E. S. Lee, G. Hu, and Y. Kang. 2008. The miR-200 family inhibits epithelial-mesenchymal transition and cancer cell migration by direct targeting of E-cadherin transcriptional repressors ZEB1 and ZEB2. J. Biol. Chem. 283:14910–14914.
   PubMed Web of Science ®Google Scholar
• Kulshreshtha, R., M. Ferracin, S. E. Wojcik, R. Garzon, H. Alder, F. J. Agosto-Perez, R. Davuluri, C. G. Liu, C. M. Croce, M. Negrini, G. A. Calin, and M. Ivan. 2007. A microRNA signature of hypoxia. Mol. Cell. Biol. 27:1859–1867.
   PubMed Web of Science ®Google Scholar
• Kusanagi, K., H. Inoue, Y. Ishidou, H. K. Mishima, M. Kawabata, and K. Miyazono. 2000. Characterization of a bone morphogenetic protein-responsive Smad-binding element. Mol. Biol. Cell 11:555–565.
   PubMed Web of Science ®Google Scholar
• Lee, Y., C. Ahn, J. Han, H. Choi, J. Kim, J. Yim, J. Lee, P. Provost, O. Radmark, S. Kim, and V. N. Kim. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–419.
   PubMed Web of Science ®Google Scholar
• Lewis, B. P., C. B. Burge, and D. P. Bartel. 2005. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120:15–20.
   PubMed Web of Science ®Google Scholar
• Lewis, B. P., I. H. Shih, M. W. Jones-Rhoades, D. P. Bartel, and C. B. Burge. 2003. Prediction of mammalian microRNA targets. Cell 115:787–798.
   PubMed Web of Science ®Google Scholar
• Long, D., R. Lee, P. Williams, C. Y. Chan, V. Ambros, and Y. Ding. 2007. Potent effect of target structure on microRNA function. Nat. Struct. Mol. Biol. 14:287–294.
   PubMed Web of Science ®Google Scholar
• Ma, L., J. Teruya-Feldstein, and R. A. Weinberg. 2007. Tumour invasion and metastasis initiated by microRNA-10b in breast cancer. Nature 449:682–688.
   PubMed Web of Science ®Google Scholar
• Matys, V., E. Fricke, R. Geffers, E. Gossling, M. Haubrock, R. Hehl, K. Hornischer, D. Karas, A. E. Kel, O. V. Kel-Margoulis, D. U. Kloos, S. Land, B. Lewicki-Potapov, H. Michael, R. Munch, I. Reuter, S. Rotert, H. Saxel, M. Scheer, S. Thiele, and E. Wingender. 2003. TRANSFAC: transcriptional regulation, from patterns to profiles. Nucleic Acids Res. 31:374–378.
   PubMed Web of Science ®Google Scholar
• Muckstein, U., H. Tafer, J. Hackermuller, S. H. Bernhart, P. F. Stadler, and I. L. Hofacker. 2006. Thermodynamics of RNA-RNA binding. Bioinformatics 22:1177–1182.
   PubMed Web of Science ®Google Scholar
• Nam, J. S., A. M. Suchar, M. J. Kang, C. H. Stuelten, B. Tang, A. M. Michalowska, L. W. Fisher, N. S. Fedarko, A. Jain, J. Pinkas, S. Lonning, and L. M. Wakefield. 2006. Bone sialoprotein mediates the tumor cell-targeted prometastatic activity of transforming growth factor beta in a mouse model of breast cancer. Cancer Res. 66:6327–6335.
   PubMed Web of Science ®Google Scholar
• Negrini, M., M. Ferracin, S. Sabbioni, and C. M. Croce. 2007. MicroRNAs in human cancer: from research to therapy. J. Cell Sci. 120:1833–1840.
   PubMed Web of Science ®Google Scholar
• O'Connell, R. M., K. D. Taganov, M. P. Boldin, G. Cheng, and D. Baltimore. 2007. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104:1604–1609.
   PubMed Web of Science ®Google Scholar
• Ozdamar, B., R. Bose, M. Barrios-Rodiles, H. R. Wang, Y. Zhang, and J. L. Wrana. 2005. Regulation of the polarity protein Par6 by TGFβ receptors controls epithelial cell plasticity. Science 307:1603–1609.
   PubMed Web of Science ®Google Scholar
• Park, S., D. Kim, S. Kaneko, K. M. Szewczyk, S. V. Nicosia, H. Yu, R. Jove, and J. Q. Cheng. 2005. Molecular cloning and characterization of the human AKT1 promoter uncovers its up-regulation by the Src/Stat3 pathway. J. Biol. Chem. 280:38932–38941.
   PubMedGoogle Scholar
• Park, S. M., A. B. Gaur, E. Lengyel, and M. E. Peter. 2008. The miR-200 family determines the epithelial phenotype of cancer cells by targeting the E-cadherin repressors ZEB1 and ZEB2. Genes Dev. 22:894–907.
   PubMed Web of Science ®Google Scholar
• Perez-Moreno, M., C. Jamora, and E. Fuchs. 2003. Sticky business: orchestrating cellular signals at adherens junctions. Cell 112:535–548.
   PubMed Web of Science ®Google Scholar
• Reinhart, B. J., F. J. Slack, M. Basson, A. E. Pasquinelli, J. C. Bettinger, A. E. Rougvie, H. R. Horvitz, and G. Ruvkun. 2000. The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403:901–906.
   PubMed Web of Science ®Google Scholar
• Roberts, A. B., and L. M. Wakefield. 2003. The two faces of transforming growth factor beta in carcinogenesis. Proc. Natl. Acad. Sci. USA 100:8621–8623.
   PubMed Web of Science ®Google Scholar
• Rodriguez, A., E. Vigorito, S. Clare, M. V. Warren, P. Couttet, D. R. Soond, S. van Dongen, R. J. Grocock, P. P. Das, E. A. Miska, D. Vetrie, K. Okkenhaug, A. J. Enright, G. Dougan, M. Turner, and A. Bradley. 2007. Requirement of bic/microRNA-155 for normal immune function. Science 316:608–611.
   PubMed Web of Science ®Google Scholar
• Skalsky, R. L., M. A. Samols, K. B. Plaisance, I. W. Boss, A. Riva, M. C. Lopez, H. V. Baker, and R. Renne. 2007. Kaposi's sarcoma-associated herpesvirus encodes an ortholog of miR-155. J. Virol. 81:12836–12845.
   PubMed Web of Science ®Google Scholar
• Stark, A., J. Brennecke, N. Bushati, R. B. Russell, and S. M. Cohen. 2005. Animal microRNAs confer robustness to gene expression and have a significant impact on 3′UTR evolution. Cell 123:1133–1146.
   PubMed Web of Science ®Google Scholar
• Tam, W. 2001. Identification and characterization of human BIC, a gene on chromosome 21 that encodes a noncoding RNA. Gene 274:157–167.
   PubMed Web of Science ®Google Scholar
• Tang, G. 2005. siRNA and miRNA: an insight into RISCs. Trends Biochem. Sci. 30:106–114.
   PubMed Web of Science ®Google Scholar
• Thai, T. H., D. P. Calado, S. Casola, K. M. Ansel, C. Xiao, Y. Xue, A. Murphy, D. Frendewey, D. Valenzuela, J. L. Kutok, M. Schmidt-Supprian, N. Rajewsky, G. Yancopoulos, A. Rao, and K. Rajewsky. 2007. Regulation of the germinal center response by microRNA-155. Science 316:604–608.
   PubMed Web of Science ®Google Scholar
• Vaezi, A., C. Bauer, V. Vasioukhin, and E. Fuchs. 2002. Actin cable dynamics and Rho/Rock orchestrate a polarized cytoskeletal architecture in the early steps of assembling a stratified epithelium. Dev. Cell 3:367–381.
   PubMed Web of Science ®Google Scholar
• Vigorito, E., K. L. Perks, C. Abreu-Goodger, S. Bunting, Z. Xiang, S. Kohlhaas, P. P. Das, E. A. Miska, A. Rodriguez, A. Bradley, K. G. Smith, C. Rada, A. J. Enright, K. M. Toellner, I. C. Maclennan, and M. Turner. 2007. MicroRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27:847–859.
   PubMed Web of Science ®Google Scholar
• Volinia, S., G. A. Calin, C. G. Liu, S. Ambs, A. Cimmino, F. Petrocca, R. Visone, M. Iorio, C. Roldo, M. Ferracin, R. L. Prueitt, N. Yanaihara, G. Lanza, A. Scarpa, A. Vecchione, M. Negrini, C. C. Harris, and C. M. Croce. 2006. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl. Acad. Sci. USA 103:2257–2261.
   PubMed Web of Science ®Google Scholar
• Wang, H. R., Y. Zhang, B. Ozdamar, A. A. Ogunjimi, E. Alexandrova, G. H. Thomsen, and J. L. Wrana. 2003. Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302:1775–1779.
   PubMed Web of Science ®Google Scholar
• Xie, W., J. C. Mertens, D. J. Reiss, D. L. Rimm, R. L. Camp, B. G. Haffty, and M. Reiss. 2002. Alterations of Smad signaling in human breast carcinoma are associated with poor outcome: a tissue microarray study. Cancer Res. 62:497–505.
   PubMed Web of Science ®Google Scholar
• Yanaihara, N., N. Caplen, E. Bowman, M. Seike, K. Kumamoto, M. Yi, R. M. Stephens, A. Okamoto, J. Yokota, T. Tanaka, G. A. Calin, C. G. Liu, C. M. Croce, and C. C. Harris. 2006. Unique microRNA molecular profiles in lung cancer diagnosis and prognosis. Cancer Cell 9:189–198.
   PubMed Web of Science ®Google Scholar
• Yang, H., W. Kong, L. He, J. J. Zhao, J. D. O'Donnell, J. Wang, R. M. Wenham, D. Coppola, P. A. Kruk, S. V. Nicosia, and J. Q. Cheng. 2008. MicroRNA expression profiling in human ovarian cancer: miR-214 induces cell survival and cisplatin resistance by targeting PTEN. Cancer Res. 68:425–433.
   PubMed Web of Science ®Google Scholar
• Yin, Q., X. Wang, J. McBride, C. Fewell, and E. K. Flemington. 2008. B-cell receptor activation induces BIC/MIR-155 expression through a conserved AP-1 element. J. Biol. Chem. 283:2654–2662.
   PubMed Web of Science ®Google Scholar
• Zavadil, J., and E. P. Bottinger. 2005. TGFβ and epithelial-to-mesenchymal transitions. Oncogene 24:5764–5774.
   PubMed Web of Science ®Google Scholar
• Zavadil, J., M. Narasimhan, M. Blumenberg, and R. J. Schneider. 2007. Transforming growth factor-β and microRNA:mRNA regulatory networks in epithelial plasticity. Cells Tissues Organs 185:157–161.
   PubMedGoogle Scholar