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Mol Cell Biol. 1993 August; 13(8): 4513-4522

Exon switching and activation of stromal and embryonic fibroblast growth factor (FGF)-FGF receptor genes in prostate epithelial cells accompany stromal independence and malignancy.

W. Alton Jones Cell Science Center, Inc., Lake Placid, New York 12946.

ABSTRACT

Stroma and the heparin-binding fibroblast growth factor (FGF) family influence normal epithelial cell growth and differentiation in embryonic and adult tissues. The role of stromal cells and the expression of isoforms of the FGF ligand and receptor family were examined during malignant progression of epithelial cells from a differentiated, slowly growing, nonmalignant model rat prostate tumor. In syngeneic hosts, a mixture of stromal and epithelial cells resulted in nonmalignant tumors which were differentiated and slowly growing. In the absence of the stromal cells, epithelial cells progressed to malignant tumors which were independent of the stroma and undifferentiated. The independence of the malignant epithelial cells from stromal cells was accompanied by a switch from exclusive expression of exon IIIb to exclusive expression of exon IIIc in the FGF receptor 2 (FGF-R2) gene. The FGF-R2(IIIb) isoform displays high affinity for stromal cell-derived FGF-7, whereas the FGF-R2(IIIc) isoform does not recognize FGF-7 but has high affinity for the FGF-2 member of the FGF ligand family. The switch from expression of exclusively exon IIIb to exclusively exon IIIc in the resident FGF-R2 gene was followed by activation of the FGF-2 ligand gene, the normally stromal cell FGF-R1 gene, and embryonic FGF-3 and FGF-5 ligand genes in malignant epithelial cells. Multiple autocrine and potentially intracrine ligand-receptor loops resulting from these alterations within the FGF-FGF-R family may underlie the autonomy of malignant tumor cells.

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• (2001). Poster Abstracts. J. Nutr. 131: 191S-199 [Full Text]  
• Carstens, R. P., Wagner, E. J., Garcia-Blanco, M. A. (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 [Abstract] [Full Text]  
• Alizadeh, M., Gelfman, C. M., Bench, S. R., Hjelmeland, L. M. (2000). Expression and Splicing of FGF Receptor mRNAs during APRE-19 Cell Differentiation In Vitro. IOVS 41: 2357-2362 [Abstract] [Full Text]  
• Moore, T. M., Garg, R., Johnson, C., Coptcoat, M. J., Ridley, A. J., Morris, J. D. H. (2000). PSK, a Novel STE20-like Kinase Derived from Prostatic Carcinoma That Activates the c-Jun N-terminal Kinase Mitogen-activated Protein Kinase Pathway and Regulates Actin Cytoskeletal Organization. J. Biol. Chem. 275: 4311-4322 [Abstract] [Full Text]  
• Olumi, A. F., Grossfeld, G. D., Hayward, S. W., Carroll, P. R., Tlsty, T. D., Cunha, G. R. (1999). Carcinoma-associated Fibroblasts Direct Tumor Progression of Initiated Human Prostatic Epithelium. Cancer Res. 59: 5002-5011 [Abstract] [Full Text]  
• Chott, A., Sun, Z., Morganstern, D., Pan, J., Li, T., Susani, M., Mosberger, I., Upton, M. P., Bubley, G. J., Balk, S. P. (1999). Tyrosine Kinases Expressed in Vivo by Human Prostate Cancer Bone Marrow Metastases and Loss of the Type 1 Insulin-Like Growth Factor Receptor. Am. J. Pathol. 155: 1271-1279 [Abstract] [Full Text]  
• Gu, D.-l., Gonzalez, A. M., Printz, M. A., Doukas, J., Ying, W., D'Andrea, M., Hoganson, D. K., Curiel, D. T., Douglas, J. T., Sosnowski, B. A., Baird, A., Aukerman, S. L., Pierce, G. F. (1999). Fibroblast Growth Factor 2 Retargeted Adenovirus Has Redirected Cellular Tropism: Evidence for Reduced Toxicity and Enhanced AntitumorActivity in Mice. Cancer Res. 59: 2608-2614 [Abstract] [Full Text]  
• Lu, W., Luo, Y., Kan, M., McKeehan, W. L. (1999). Fibroblast Growth Factor-10. A SECOND CANDIDATE STROMAL TO EPITHELIAL CELL ANDROMEDIN IN PROSTATE. J. Biol. Chem. 274: 12827-12834 [Abstract] [Full Text]  
• Heberlein, C., Friel, J., Laker, C., von Laer, D., Bergholz, U., Bogel, M., Ashman, L. K., Klingler, K., Ostertag, W. (1999). Downregulation of c-kit (Stem Cell Factor Receptor) in Transformed Hematopoietic Precursor Cells by Stroma Cells. Blood 93: 554-563 [Abstract] [Full Text]  
• Thomson, A., Cunha, G. (1999). Prostatic growth and development are regulated by FGF10. Development 126: 3693-3701 [Abstract]  
• Asa, S. L., Ezzat, S. (1998). The Cytogenesis and Pathogenesis of Pituitary Adenomas. Endocr. Rev. 19: 798-827 [Abstract] [Full Text]  
• Lopez-Otin, C., Diamandis, E. P. (1998). Breast and Prostate Cancer: An Analysis of Common Epidemiological, Genetic, and Biochemical Features. Endocr. Rev. 19: 365-396 [Abstract] [Full Text]  
• Carstens, R. P., McKeehan, W. L., Garcia-Blanco, M. A. (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 [Abstract] [Full Text]  
• Russell, P. J., Bennett, S., Stricker, P. (1998). Growth factor involvement in progression of prostate cancer. Clin. Chem. 44: 705-723 [Abstract] [Full Text]  
• Wang, F., Kan, M., McKeehan, K., Jang, J.-H., Feng, S., McKeehan, W. L. (1997). A Homeo-interaction Sequence in the Ectodomain of the Fibroblast Growth Factor Receptor. J. Biol. Chem. 272: 23887-23895 [Abstract] [Full Text]  
• Pilcher, B. K., Gaither-Ganim, J., Parks, W. C., Welgus, H. G. (1997). Cell Type-specific Inhibition of Keratinocyte Collagenase-1 Expression by Basic Fibroblast Growth Factor and Keratinocyte Growth Factor. A COMMON RECEPTOR PATHWAY. J. Biol. Chem. 272: 18147-18154 [Abstract] [Full Text]  
• Bikfalvi, A., Klein, S., Pintucci, G., Rifkin, D. B. (1997). Biological Roles of Fibroblast Growth Factor-2. Endocr. Rev. 18: 26-45 [Abstract] [Full Text]  
• Ornitz, D. M., Xu, J., Colvin, J. S., McEwen, D. G., MacArthur, C. A., Coulier, F., Gao, G., Goldfarb, M. (1996). Receptor Specificity of the Fibroblast Growth Factor Family. J. Biol. Chem. 271: 15292-15297 [Abstract] [Full Text]  
• Wang, F., Kan, M., Xu, J., Yan, G., McKeehan, W. L. (1995). Ligand-specific Structural Domains in the Fibroblast Growth Factor Receptor. J. Biol. Chem. 270: 10222-10230 [Abstract] [Full Text]  
• Nurcombe, V., Smart, C. E., Chipperfield, H., Cool, S. M., Boilly, B., Hondermarck, H. (2000). The Proliferative and Migratory Activities of Breast Cancer Cells Can Be Differentially Regulated by Heparan Sulfates. J. Biol. Chem. 275: 30009-30018 [Abstract] [Full Text]  
• Jones, R. B., Wang, F., Luo, Y., Yu, C., Jin, C., Suzuki, T., Kan, M., McKeehan, W. L. (2001). The Nonsense-mediated Decay Pathway and Mutually Exclusive Expression of Alternatively Spliced FGFR2IIIb and -IIIc mRNAs. J. Biol. Chem. 276: 4158-4167 [Abstract] [Full Text]