Fox-2 Mediates Epithelial Cell-Specific Fibroblast Growth Factor Receptor 2 Exon Choice

REFERENCES

• Baraniak, A. P., E. L. Lasda, E. J. Wagner, and M. A. Garcia-Blanco. 2003. A stem structure in fibroblast growth factor receptor 2 transcripts mediates cell-type-specific splicing by approximating intronic control elements. Mol. Cell. Biol. 23:9327–9337.
   PubMed Web of Science ®Google Scholar
• Brudno, M., M. S. Gelfand, S. Spengler, M. Zorn, I. Dubchak, and J. G. Conboy. 2001. Computational analysis of candidate intron regulatory elements for tissue-specific alternative pre-mRNA splicing. Nucleic Acids Res. 29:2338–2348.
   PubMed Web of Science ®Google Scholar
• Burns, R. C., T. J. Fairbanks, F. Sala, S. De Langhe, A. Mailleux, J. P. Thiery, C. Dickson, N. Itoh, D. Warburton, K. D. Anderson, and S. Bellusci. 2004. Requirement for fibroblast growth factor 10 or fibroblast growth factor receptor 2-IIIb signaling for cecal development in mouse. Dev. Biol. 265:61–74.
   PubMedGoogle Scholar
• Carstens, R. P., J. V. Eaton, H. R. Krigman, P. J. Walther, and M. A. Garcia-Blanco. 1997. Alternative splicing of fibroblast growth factor receptor 2 (FGF-R2) in human prostate cancer. Oncogene 15:3059–3065.
   PubMed Web of Science ®Google Scholar
• Carstens, R. P., W. L. McKeehan, and M. A. Garcia-Blanco. 1998. An intronic sequence element mediates both activation and repression of rat fibroblast growth factor receptor 2 pre-mRNA splicing. Mol. Cell. Biol. 18:2205–2217.
   PubMed Web of Science ®Google Scholar
• Carstens, R. P., E. J. Wagner, and M. A. Garcia-Blanco. 2000. An intronic splicing silencer causes skipping of the IIIb exon of fibroblast growth factor receptor 2 through involvement of polypyrimidine tract binding protein. Mol. Cell. Biol. 20:7388–7400.
   PubMedGoogle Scholar
• Champion-Arnaud, P., C. Ronsin, E. Gilbert, M. C. Gesnel, E. Houssaint, and R. Breathnach. 1991. Multiple mRNAs code for proteins related to the BEK fibroblast growth factor receptor. Oncogene 6:979–987.
   PubMedGoogle Scholar
• Deguillien, M., S. C. Huang, M. Moriniere, N. Dreumont, E. J. Benz, Jr., and F. Baklouti. 2001. Multiple cis elements regulate an alternative splicing event at 4.1R pre-mRNA during erythroid differentiation. Blood 98:3809–3816.
   PubMedGoogle Scholar
• Del Gatto, F., and R. Breathnach. 1995. Exon and intron sequences, respectively, repress and activate splicing of a fibroblast growth factor receptor 2 alternative exon. Mol. Cell. Biol. 15:4825–4834.
   PubMedGoogle Scholar
• Del Gatto, F., M. C. Gesnel, and R. Breathnach. 1996. The exon sequence TAGG can inhibit splicing. Nucleic Acids Res. 24:2017–2021.
   PubMedGoogle Scholar
• Del Gatto, F., A. Plet, M. C. Gesnel, C. Fort, and R. Breathnach. 1997. Multiple interdependent sequence elements control splicing of a fibroblast growth factor receptor 2 alternative exon. Mol. Cell. Biol. 17:5106–5116.
   PubMedGoogle Scholar
• Del Gatto-Konczak, F., C. F. Bourgeois, C. Le Guiner, L. Kister, M. C. Gesnel, J. Stevenin, and R. Breathnach. 2000. The RNA-binding protein TIA-1 is a novel mammalian splicing regulator acting through intron sequences adjacent to a 5′ splice site. Mol. Cell. Biol. 20:6287–6299.
   PubMed Web of Science ®Google Scholar
• Del Gatto-Konczak, F., M. Olive, M. C. Gesnel, and R. Breathnach. 1999. hnRNP A1 recruited to an exon in vivo can function as an exon splicing silencer. Mol. Cell. Biol. 19:251–260.
   PubMedGoogle Scholar
• Dell, K. R., and L. T. Williams. 1992. A novel form of fibroblast growth factor receptor 2. Alternative splicing of the third immunoglobulin-like domain confers ligand binding specificity. J. Biol. Chem. 267:21225–21229.
   PubMedGoogle Scholar
• De Moerlooze, L., B. Spencer-Dene, J. Revest, M. Hajihosseini, I. Rosewell, and C. Dickson. 2000. An important role for the IIIb isoform of fibroblast growth factor receptor 2 (FGFR2) in mesenchymal-epithelial signalling during mouse organogenesis. Development 127:483–492.
   PubMed Web of Science ®Google Scholar
• Hajihosseini, M. K., S. Wilson, L. De Moerlooze, and C. Dickson. 2001. A splicing switch and gain-of-function mutation in FgfR2-IIIc hemizygotes causes Apert/Pfeiffer-syndrome-like phenotypes. Proc. Natl. Acad. Sci. USA 98:3855–3860.
   PubMedGoogle Scholar
• Hedjran, F., J. M. Yeakley, G. S. Huh, R. O. Hynes, and M. G. Rosenfeld. 1997. Control of alternative pre-mRNA splicing by distributed pentameric repeats. Proc. Natl. Acad. Sci. USA 94:12343–12347.
   PubMedGoogle Scholar
• Hovhannisyan, R. H., and R. P. Carstens. 2005. A novel intronic cis element, ISE/ISS-3, regulates rat fibroblast growth factor receptor 2 splicing through activation of an upstream exon and repression of a downstream exon containing a noncanonical branch point sequence. Mol. Cell. Biol. 25:250–263.
   PubMedGoogle Scholar
• Huh, G. S., and R. O. Hynes. 1994. Regulation of alternative pre-mRNA splicing by a novel repeated hexanucleotide element. Genes Dev. 8:1561–1574.
   PubMed Web of Science ®Google Scholar
• Jin, Y., H. Suzuki, S. Maegawa, H. Endo, S. Sugano, K. Hashimoto, K. Yasuda, and K. Inoue. 2003. A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J. 22:905–912.
   PubMed Web of Science ®Google Scholar
• Jones, R. B., R. P. Carstens, Y. Luo, and W. L. McKeehan. 2001. 5′- and 3′-terminal nucleotides in the FGFR2 ISAR splicing element core have overlapping roles in exon IIIb activation and exon IIIc repression. Nucleic Acids Res. 29:3557–3565.
   PubMedGoogle Scholar
• Kang, Y., and J. Massague. 2004. Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118:277–279.
   PubMed Web of Science ®Google Scholar
• Kawamoto, S. 1996. Neuron-specific alternative splicing of nonmuscle myosin II heavy chain-B pre-mRNA requires a cis-acting intron sequence. J. Biol. Chem. 271:17613–17616.
   PubMed Web of Science ®Google Scholar
• Kiehl, T. R., H. Shibata, T. Vo, D. P. Huynh, and S. M. Pulst. 2001. Identification and expression of a mouse ortholog of A2BP1. Mamm. Genome 12:595–601.
   PubMedGoogle Scholar
• Lieberman, A. P., D. L. Friedlich, G. Harmison, B. W. Howell, C. L. Jordan, S. M. Breedlove, and K. H. Fischbeck. 2001. Androgens regulate the mammalian homologues of invertebrate sex determination genes tra-2 and fox-1. Biochem. Biophys. Res. Commun. 282:499–506.
   PubMedGoogle Scholar
• Lim, L. P., and P. A. Sharp. 1998. Alternative splicing of the fibronectin EIIIB exon depends on specific TGCATG repeats. Mol. Cell. Biol. 18:3900–3906.
   PubMedGoogle Scholar
• Miki, T., D. P. Bottaro, T. P. Fleming, C. L. Smith, W. H. Burgess, A. M. Chan, and S. A. Aaronson. 1992. Determination of ligand-binding specificity by alternative splicing: two distinct growth factor receptors encoded by a single gene. Proc. Natl. Acad. Sci. USA 89:246–250.
   PubMed Web of Science ®Google Scholar
• Minovitsky, S., S. L. Gee, S. Schokrpur, I. Dubchak, and J. G. Conboy. 2005. The splicing regulatory element, UGCAUG, is phylogenetically and spatially conserved in introns that flank tissue-specific alternative exons. Nucleic Acids Res. 33:714–724.
   PubMedGoogle Scholar
• Mistry, N., W. Harrington, E. Lasda, E. J. Wagner, and M. A. Garcia-Blanco. 2003. Of urchins and men: evolution of an alternative splicing unit in fibroblast growth factor receptor genes. RNA 9:209–217.
   PubMedGoogle Scholar
• Modafferi, E. F., and D. L. Black. 1997. A complex intronic splicing enhancer from the c-src pre-mRNA activates inclusion of a heterologous exon. Mol. Cell. Biol. 17:6537–6545.
   PubMedGoogle Scholar
• Morriss-Kay, G. M., S. Iseki, and D. Johnson. 2001. Genetic control of the cell proliferation-differentiation balance in the developing skull vault: roles of fibroblast growth factor receptor signalling pathways. Novartis Found. Symp. 232:102–116.
   PubMedGoogle Scholar
• Muh, S. J., R. H. Hovhannisyan, and R. P. Carstens. 2002. A non-sequence-specific double-stranded RNA structural element regulates splicing of two mutually exclusive exons of fibroblast growth factor receptor 2 (FGFR2). J. Biol. Chem. 277:50143–50154.
   PubMedGoogle Scholar
• Nakahata, S., and S. Kawamoto. 2005. Tissue-dependent isoforms of mammalian Fox-1 homologs are associated with tissue-specific splicing activities. Nucleic Acids Res. 33:2078–2089.
   PubMed Web of Science ®Google Scholar
• Norris, J. D., D. Fan, A. Sherk, and D. P. McDonnell. 2002. A negative coregulator for the human ER. Mol. Endocrinol. 16:459–468.
   PubMedGoogle Scholar
• Oldridge, M., E. H. Zackai, D. M. McDonald-McGinn, S. Iseki, G. M. Morriss-Kay, S. R. Twigg, D. Johnson, S. A. Wall, W. Jiang, C. Theda, E. W. Jabs, and A. O. Wilkie. 1999. De novo alu-element insertions in FGFR2 identify a distinct pathological basis for Apert syndrome. Am. J. Hum. Genet. 64:446–461.
   PubMedGoogle Scholar
• Orr-Urtreger, A., M. T. Bedford, T. Burakova, E. Arman, Y. Zimmer, A. Yayon, D. Givol, and P. Lonai. 1993. Developmental localization of the splicing alternatives of fibroblast growth factor receptor-2 (FGFR2). Dev. Biol. 158:475–486.
   PubMed Web of Science ®Google Scholar
• Savagner, P., A. M. Valles, J. Jouanneau, K. M. Yamada, and J. P. Thiery. 1994. Alternative splicing in fibroblast growth factor receptor 2 is associated with induced epithelial-mesenchymal transition in rat bladder carcinoma cells. Mol. Biol. Cell 5:851–862.
   PubMed Web of Science ®Google Scholar
• Shibata, H., D. P. Huynh, and S. M. Pulst. 2000. A novel protein with RNA-binding motifs interacts with ataxin-2. Hum. Mol. Genet. 9:1303–1313.
   PubMedGoogle Scholar
• Sune, C., and M. A. Garcia-Blanco. 1995. Transcriptional trans activation by human immunodeficiency virus type 1 Tat requires specific coactivators that are not basal factors. J. Virol. 69:3098–3107.
   PubMed Web of Science ®Google Scholar
• Thiery, J. P. 2003. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 15:740–746.
   PubMed Web of Science ®Google Scholar
• Underwood, J. G., P. L. Boutz, J. D. Dougherty, P. Stoilov, and D. L. Black. 2005. Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol. Cell. Biol. 25:10005–10016.
   PubMed Web of Science ®Google Scholar
• Wagner, E. J., A. Baines, T. Albrecht, R. M. Brazas, and M. A. Garcia-Blanco. 2004. Imaging alternative splicing in living cells. Methods Mol. Biol. 257:29–46.
   PubMedGoogle Scholar
• Wagner, E. J., A. P. Baraniak, O. M. Sessions, D. Mauger, E. Moskowitz, and M. A. Garcia-Blanco. 2005. Characterization of the intronic splicing silencers flanking FGFR2 exon IIIb. J. Biol. Chem. 280:14017–14027.
   PubMedGoogle Scholar
• Wagner, E. J., M. L. Curtis, N. D. Robson, A. P. Baraniak, P. S. Eis, and M. A. Garcia-Blanco. 2003. Quantification of alternatively spliced FGFR2 RNAs using the RNA invasive cleavage assay. RNA 9:1552–1561.
   PubMedGoogle Scholar
• Wagner, E. J., and M. A. Garcia-Blanco. 2001. Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol. 21:3281–3288.
   PubMed Web of Science ®Google Scholar
• Wagner, E. J., and M. A. Garcia-Blanco. 2002. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol. Cell 10:943–949.
   PubMed Web of Science ®Google Scholar
• Wilkie, A. O., M. Oldridge, Z. Tang, and R. E. Maxson, Jr. 2001. Craniosynostosis and related limb anomalies. Novartis Found. Symp. 232:122–133.
   PubMedGoogle Scholar
• Wollerton, M. C., C. Gooding, E. J. Wagner, M. A. Garcia-Blanco, and C. W. Smith. 2004. Autoregulation of polypyrimidine tract binding protein by alternative splicing leading to nonsense-mediated decay. Mol. Cell 13:91–100.
   PubMed Web of Science ®Google Scholar
• Yan, G., Y. Fukabori, G. McBride, S. Nikolaropolous, and W. L. McKeehan. 1993. Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy. Mol. Cell. Biol. 13:4513–4522.
   PubMed Web of Science ®Google Scholar
• Yang, J., S. A. Mani, J. L. Donaher, S. Ramaswamy, R. A. Itzykson, C. Come, P. Savagner, I. Gitelman, A. Richardson, and R. A. Weinberg. 2004. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 117:927–939.
   PubMed Web of Science ®Google Scholar
• Yasumoto, H., A. Matsubara, K. Mutaguchi, T. Usui, and W. L. McKeehan. 2004. Restoration of fibroblast growth factor receptor 2 suppresses growth and tumorigenicity of malignant human prostate carcinoma PC-3 cells. Prostate 61:236–242.
   PubMed Web of Science ®Google Scholar
• Yayon, A., Y. Zimmer, G. H. Shen, A. Avivi, Y. Yarden, and D. Givol. 1992. A confined variable region confers ligand specificity on fibroblast growth factor receptors: implications for the origin of the immunoglobulin fold. EMBO J. 11:1885–1890.
   PubMedGoogle Scholar
• Yeakley, J. M., J. B. Fan, D. Doucet, L. Luo, E. Wickham, Z. Ye, M. S. Chee, and X. D. Fu. 2002. Profiling alternative splicing on fiber-optic arrays. Nat. Biotechnol. 20:353–358.
   PubMed Web of Science ®Google Scholar
• Yu, K., A. B. Herr, G. Waksman, and D. M. Ornitz. 2000. Loss of fibroblast growth factor receptor 2 ligand-binding specificity in Apert syndrome. Proc. Natl. Acad. Sci. USA 97:14536–14541.
   PubMed Web of Science ®Google Scholar