Translation of CUG- but not AUG-initiated forms of human fibroblast growth factor 2 is activated in transformed and stressed cells

Journal of Cell Biology

Volumn 135, Issue 5, 1996, Pages 1391-1402

  Vagner, Stéphan ^a   Touriol, Christian ^a   Galy, Bruno ^a   Audigier, Sylvie ^a   Gensac, Marie Claire ^a   Amalric, François ^b   Bayard, Francis ^a   Prats, Hervé ^a   Prats, Anne Catherine ^a  

^a CHU RANGUEIL   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; MESSENGER RNA;

ARTICLE; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CROSS LINKING; FIBROBLAST CULTURE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; SKIN FIBROBLAST; TRANSLATION REGULATION;

EID: 0030474826     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.135.5.1391     Document Type: Article

References (60)

1. Bensaid, M., F. Malecaze, H. Prats, F. Bayard, and J.P. Tauber. 1989. Autocrine regulation of bovine retinal capillary endothelial cells (BREC) proliferation by BREC derived fibroblast growth factor. Exp. Eye Res. 45:801-813.
2. Berlioz, C. and J.L. Darlix. 1995. An internal ribosomal entry mechanism promotes translation of murine leukemia virus gag polyprotein precursors. J. Viral. 69:2214-2222.
3. Bikfalvi, A., S. Klein, G. Pintucci, N. Quarto, P. Mignatti, and D. B. Rifkin. 1995. Differential modulation of cell phenotype by different molecular weight forms of basic fibroblast growth factor: possible intracellular signaling by the high molecular weight forms. J. Cell. Biol. 129:233-243.
4. Borman, A., M.T. Howell, J.G. Patton, and R.J. Jackson. 1993. The involvement of a spliceosome component in internal initiation of human rhinovirus RNA translation. J. Gen. Virol. 74:1775-1788.
5. Borovjagin, A., T. Pestova, and I. Shatsky. 1994. Pyrimidine tract binding protein strongly stimulates in vitro encephalomyocarditis virus RNA translation at the level of preinitiation complex formation. FEBS Lett. 351:299-302.
6. Brigstock, D.R., J. Sasse, and M. Klagsbrun. 1991. Subcellular distribution of basic fibroblast growth factor in human hepatoma cells. Growth Fact. 4:189-196.
7. Bugler, B., F. Amalric, and H. Prats. 1991. Alternative initiation of translation determines cytoplasmic or nuclear localization of basic fibroblast growth factor. Mol. Cell Biol. 11:573-577.
8. Coffin, J.D., R.Z. Florkiewicz, J. Neumann, T. Mort-Hopkins, G.W. Dorn II, P. Lightfoot, R. German, P.N. Howles, A. Kier, B.A. O'Toole et al. 1995. Abnormal hone growth and selective translational regulation in basic fibroblast growth factor (FGF-2) transgenic mice. Mol. Biol. Cell 6:1861-1873.
9. Couderc, B., H. Prats, F. Bayard, and F. Amalric. 1991. Potential oncogenic effects of basic fibroblast growth factor requires cooperation between CUG and AUG-initiated forms. Cell Regul. 2:709-718.
10. DcBenedetti, A., and R.E. Rhoads. 1990. Overexpression of eukaryotic protein synthesis initiation factor 4E in HeLa cells results in aberrant growth and morphology. Proc. Natl. Acad. Sci. USA. 87:8212-8216.
11. Florkiewicz, R.Z., and A. Sommer. 1989. Human basic fibroblast growth factor gene encodes four polypeptides: three initiate translation from non-AUG codons. Proc. Natl. Acad. Sci. USA. 86:3978-3981.
12. Florkiewicz, R.Z., F. Shibata, T. Barankiewicz, A. Baird, A.M. Gonzalez, E. Florkiewicz, and N. Shah. 1991. Basic fibroblast growth factor gene expression. In The Fibroblast Growth Factor Family. Vol. 638. A. Baird and M. Klagsbrun, editors. Annals of the New York Academy of Sciences. New York 109-126.
13. Fumagalli, S., N.F. Totty, J. Justin Huan, and S.A. Courtneidge. 1994. A target for Src in mitosis. Nature (Lond.). 368:871-874.
14. Gay, C.G., and J.A. Winkles. 1991. Interleukin 1 regulates heparin-binding growth factor 2 gene expression in vascular smooth cells. Proc. Natl. Acad. Sci. USA. 88:296-300.
15. Hellen, C.U.T., G.W. Witherell, M. Schmid, S.H. Shin, T.V. Pestova, A. Gil, and E. Wimmer. 1993. A cytoplasmic 57-kDa protein that is required for translation of picornavirus RNA by internal ribosome entry is identical to the nuclear pyrimidine tract-binding protein. Proc. Natl. Acad. Sci. USA. 90:7642-7646.
16. Jackson, R.J. 1991. Initiation without an end. Nature (Lond.). 353:14-15.
17. Jang, S.K., and E. Wimmer. 1990. Cap-independent translation of encephalomyocarditis virus RNA: structural elements of the internal ribosomal entry site and involvement of a cellular 57-kD RNA-binding protein. Genes Dev. 4:1560-1572.
18. Jang, S.K., H. Krausslich, M.J.H. Nicklin, G.M. Duke, A.C. Palmenberg, and E. Wimmer. 1988. A segment of the 5′ nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 62:2636-2643.
19. Kaminski, A., S.L. Hunt, J.G. Patton, and R.J. Jackson. 1995. Direct evidence that polypyrimidine tract binding protein (PTB) is essential for internal initiation of translation of encephalomyocarditis virus RNA. RNA. 1:924-938.
20. Kandel, J., E. Bossy-Wetzel, F. Radvanyi, M. Klagsbrun, J. Folkman, and D. Hanahan. 1991. Neovascularisation is associated with a switch to the export of bFGF in the multistep development of fibrosarcoma. Cell. 66:1095-1104.
21. Kevil, C., P. Carter, B. Hu, and A. DcBenedelti. 1995. Translational enhancement of FGF-2 by eIF-4 factors, and alternate utilization of CUG and AUG codons for translation initiation. Oncogene. 11:2239-2348.
22. Kozak, M. 1978. How do eucaryotic ribosomes select initiation regions in messenger RNA? Cell. 15:1109-1123.
23. Kozak, M. 1990. Downstream secondary structure facilitates recognition of initiator codons by eukaryotic rihosomes. Proc. Natl. Acad. Sci. USA. 87:8301-8305.
24. Lazaris-Karatzas, A., K.S. Montine, and N. Sonenberg. 1990. Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature (Lond.). 345:544-547.
25. Macejak, D.J., and P. Sarnow. 1991. Internal initiation of translation mediated by the 5′ leader of a cellular mRNA. Nature (Lond.). 353:90-94.
26. Meerovitch, K., J. Pelletier, and N. Sonenberg. 1989. A cellular protein that binds to the 5′-noncoding region of poliovirus RNA: implications for internal translation initiation. Genes Dev. 3:1026-1034.
27. Meerovitch, K., Y.V. Svitkin, H.S. Lee, F. Lejbkowicz, D.J. Kenan, E.K.L. Chan, V.I. Agol, J.D. Keene, and N. Sonenberg. 1993. La autoantigen enhances and corrects aberrant translation of poliovirus RNA in reticulocyte lysate. J. Virol. 67:3798-3807.
28. Mignatti, P., T. Morimoto, and D.B. Rifkin. 1991. Basic fibroblast growth factor (bFGF) released by single isolated cells stimulates their migration in an autocrine manner. Proc. Natl. Acad. Sci. USA. 88:11007-11011.
29. Mignatti, P., T. Morimoto, and D.B. Rifkin. 1992. Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J. Cell Physiol. 151:81-93.
30. Nakayama, H., H. Yokoi, and J. Fujita. 1992. Quantification of mRNA by non-radioactive RT-PCR and CCD imaging system. Nucleic Acids Res. 20:4939.
31. Oh, S.-K., M.P. Scott, and P. Sarnow. 1992. Homeotic gene Antennapedia mRNA contains 5′-noncoding sequences that confer translational initiation by internal ribosome binding. Genes Dev. 6:1643-1353.
32. Panniers, R., E.B. Steward, W.C. Merrick, and E.C. Henshaw. 1985. Mechanism of inhibition of polypeptide chain initiation in heat-shocked Ehrlich cells involves reduction of eukaryotic initiation factor 4F activity. J. Biol. Chem. 260:9648-9653.
33. Patton, J.G., S.A. Meyer, P. Tempst, and B. Nadal-Ginard. 1991. Characteriza-tion and molecular cloning of polypyrimidine trad-binding protein: a component of a complex necessary for pre-mRNA splicing. Genes Dev. 5:1237-1251.
34. Pelletier, J., and N. Sonenberg. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature (Lond.) 334:320-325.
35. Pertovaara, L., O. Saksela, and K. Alitalo. 1993. Enhanced bFGF gene expression in response to transforming growth factor-b stimulation in AKR-2B cells. Growth Fact. 9:81-86.
36. Prats, A.C., S. Vagner, H. Prats, and F. Amalric. 1992. Cis-acting elements involved in the alternative translation initiation process of human basic fibroblast growth factor. Mol. Cell. Biol. 12:4795-4805.
37. Prats, H., M. Kaghad, A.C. Prats, M. Klagsbrun, J.M. Lélias, P. Liauzun, P. Chalon, J.P. Tauber, F. Amalric, J.A. Smith, and D. Caput. 1989. High molecular mass forms of basic fibroblast growth factor are initiated by alternative CUG codons. Proc. Natl. Acad. Sci. USA. 86:1836-1840.
38. Quarto, N., D. Talarico, R. Florkiewicz, and D.B. Rifkin. 1991. Selective expression of high molecular weight basic fibroblast growth factor confers a unique phenotype to NIH 3T3 cells. Cell Regul. 2:699-708.
39. Renko, M., N. Quarto, T. Morimoto, and D.B. Rifkin. 1990. Nuclear and cytoplasmic localization of different basic fibroblast growth factor species. J. Cell. Physiol. 144:108-114.
40. Reynolds, J.E., A. Kaminski, H.J. Kettinen, K. Grace, B.E. Clarke, A.R. Carroll, D.J. Rowlands, and R.J. Jackson. 1995. Unique features of internal initiation of hepatitis C virus RNA translation. EMBO (Eur. Mol. Biol. Organ.) J. 14:6010-6020.
41. Rifkin, D.B., and D. Moscatelli. 1989. Recent developments in the cell biology of fibroblast growth factor. J. Cell Biol. 109:1-6.
42. Rousseau, D., R. Kaspar, I. Rosenwald, L. Gehrke, and N. Sonenberg. 1996. Translation initiation of onrithine decarboxylase and nucleocytoplasmic transport of cyclin D1 mRNA are increased in cells overexpressing eukaryotic initiation factor 4E. Proc. Natl. Acad. Sci. USA. 93:1065-1070.
43. Sonenberg, N. 1988. Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation. Prog. Nucleic Acid Res. Mol. Biol. 35:173-297.
44. Stachowiak, M.K., J. Moffett, A. Joy, E. Puchacz, R. Florkiewicz, and E.K. Stachowiak. 1994. Regulation of bFGF gene expression and subcellular distribution of bFGF protein in adrenal medullary cells. J. Cell Biol. 127:203-223.
45. Standart, N., and R.J. Jackson. 1994. Regulation of translation by specific protein/mRNA interactions. Biochimie (Paris). 76:867-879.
46. Svitkin, V.S., K. Meerovitch, H.S. Lee, J.N. Dholakia, D.J. Kenan, V.I. Agol, and N. Sonenberg. 1994. Internal translation initiation on poliovirus RNA: further characterization of La function in poliovirus translation in vitro. J. Virol. 68:1544-1550.
47. Taylor, S.J., and D. Shalloway. 1994. An RNA-binding protein associated with Src through its SH2 and SH3 domains in mitosis. Nature (Lond.). 368:867-871.
48. Toyoda, H., N. Koide, M. Kamiyama, K. Tobita, K. Mizumoto, and N. Imura. 1994. Host factors required for internal initiation of translation on poliovirus RNA. Arch. Virol. 138:1-15.
49. Tsukiyama-Kohara, K., N. Iizuka, M. Kohara, and A. Nomoto. 1992. Internal ribosome entry site within hepatitis C virus RNA. J. Virol. 66:1476-1483.
50. Ueba, T., T. Nosaka, J.A. Takahashi, F. Shibata, R.Z. Florkiewicz, B. Vogelstein, Y. Oda, H. Kikushi, and M. Hatanaka. 1994. Transcriptional regulation of basic fibroblast growth factor gene by p53 in human glioblastoma and hepatocellular carcinoma cells. Proc. Natl. Acad. Sci. USA. 91:9009-9013.
51. Vagner, S., M.C. Gensac, A. Maret, F. Bayard, F. Amalric, H. Prats, and A.C. Prats. 1995a Alternative translation of human fibroblast growth factor 2 mRNA occurs by internal entry of ribosomes. Mol. Cell. Biol. 15:35-44.
52. Vagner, S., A. Waysbort, M. Marenda, M.C. Gensac, F. Amalric, and A.C. Prats. 1995. Alternative translation initiation of the Moloney murine leukemia virus mRNA controlled by internal ribosome entry involving the p57/PTB splicing factor. J. Biol. Chem. 270:20376-20383.
53. Volk, T., I. Ioannidis, M. Hensel, H. DeGroot, and W.J. Kox. 1995. Endothelial damage induced by nitric oxide: synergism with reactive oxygen species. Biochem. Biophys. Res. Commun. 213:196-203.
54. Wagner, J.A. 1991. The fibroblasts growth factors: an emerging family of neural growth factors. Curr. Top. Microbiol. Immunol. 165:95-118.
55. Wang, A.M., M.V. Doyle, and D.F. Mark. 1989. Quantitation of mRNA by the polymerase chain reaction. Prof. Natl. Acad. Sci. USA. 86:9717-9721.
56. Wang, L.L., S. Richard, and A.S. Shaw. 1995. p62 association with RNA is regulated by tyrosine phosphorylation. J. Biol. Chem. 270:2010-2013.
57. Weich, H.A., N. Iberg, M. Klagsbrun, and J. Folkman. 1990. Expression of acidic and basic fibroblast growth factors in human and bovine vascular smooth muscle cells. Growth Fact. 2:313-320.
58. Witherell, G.W., and E. Wimmer. 1994. Encephalomyocarditis virus internal ribosomal entry site RNA-protein interactions. J. Virol. 68:3183-3192.
59. Wong, G., O. Müller, R. Clark, L. Conroy, M.F. Moran, P. Polakis, and F. McCormick. 1992. Molecular cloning and nucleic acid binding properties of the GAP-associated tyrosine phosphoprotein p62. Cell. 69:551-558.
60. Yanagisawa-Miwa, A., Y. Uchida, F. Nakamura, T. Tomaru, H. Kido, T. Kamijo, T. Sugimoto, K. Kaji, M. Utsuyama, C. Kurashima, and H. Ito. 1992. Salvage of infarcted myocardium by angiogenic action of basic fibroblast growth factor. Science (Wash. DC). 257:1401-1403.