Translation of vascular endothelial growth factor mRNA by internal ribosome entry: Implications for translation under hypoxia

Molecular and Cellular Biology

Volumn 18, Issue 6, 1998, Pages 3112-3119

  Stein, Ilan ^a   Itin, Ahuva ^a   Einat, Paz ^b   Skaliter, Rami ^b   Grossman, Zehava ^b   Keshet, Eli ^a  

^a HEBREW UNIVERSITY   (Israel)

^b QBI Enterprises Ltd   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; VASCULOTROPIN;

ANIMAL CELL; ARTICLE; CELL HYPOXIA; DNA SEQUENCE; GENE ACTIVITY; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RIBOSOME; RNA TRANSLATION; TRANSLATION REGULATION;

ANIMALIA;

EID: 0031869662     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.6.3112     Document Type: Article

References (40)

1. Aiello, L. P., R. L. Avery, P. G. Arrigg, B. A. Keyt, H. D. Jampel, S. T. Shah, L. R. Pasquale, H. Thieme, M. A. Iwamoto, J. E. Park, et al. 1994. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N. Engl. J. Med. 331:1480-1487.
2. Alon, T., I. Hemo, A. Itin, J. Pe'er, J. Stone, and E. Keshet. 1995. Vascular endothelial growth factor acts as a survival factor lor newly formed retinal vessels and has implications for retinopathy of prematurity. Nat. Med. 1:1024-1028.
3. Benda, P., J. Lightbody, G. Sato, L. Levine, and W. Sweet. 1968. Differentiated rat glial cell strain in tissue culture. Science 161:370-374.
4. Bernstein, J., O. Sella, S.-U. Le, and O. Elroy-Stein. 1997. PDGF2/c-sis mRNA leader contains a differentiation-linked internal ribosomal entry site (D-IRES). J. Biol. Chem. 272:9356-9362.
5. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
6. Carmeliet, P., V. Ferreira, G. Breier, S. Pollefeyt, L. Kieckens, M. Gertsenstein, M. Fahrig, A. Vandenhoeck, K. Harpal, C. Eberhardt, C. Declercq, J. Pawling, L. Moons, D. Collen, W. Risau, and A. Nagy. 1996. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380:435-439.
7. Chirgwin, J. M., A. E. Przybyla, R. J. McDonald, and W. J. Rutter. 1979. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
8. Ehrenfeld, E. 1996. Initiation of translation by picornavirus RNAs, p. 549-573. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N.Y.
9. Ferrara, N., K. Carver Moore, H. Chen, M. Dowd, L. Lu, K. S. O'Shea, L. Powell Braxton, K. J. Hillan, and M. W. Moore. 1996. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380:439-142.
10. Forsythe, J. A., B. H. Jiang, N. V. Iyer, F. Agani, S. W. Leung, R. D. Koos, and G. L. Semenza. 1996. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell. Biol. 16:4604-4613.
11. Frangakis, M. V., and H. K. Kimelberg. 1984. Dissociation of neonatal rat brain by dispase for preparation of primary astrocyte cultures. Neurochem. Res. 9:1689-1698.
12. Gan, W., and R. E. Rhoads. 1996. Internal initiation of translation directed by the 5′-untranslated region of the mRNA for eIF4G, a factor involved in the picornavirus-induced switch from cap-dependent to internal initiation. J. Biol. Chem. 271:623-626.
13. Ikeda, E., M. G. Achen, G. Breier, and W. Risau. 1995. Hypoxia-induced transcriptional activation and increased mRNA stability of vascular endothelial growth factor in C6 glioma cells. J. Biol. Chem. 270:19761-19766.
14. Jackson, R. J. 1996. A comparative view of initiation site selection mechanisms, p. 71-112. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
15. Jang, S. K., H.-G. 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.
16. Jang, S. K., M. V. Davies, R. J. Kaufman, and E. Wimmer. 1989. Initiation of protein synthesis by internal entry of ribosomes into the 5′ nontranslated region of encephalomyocarditis virus RNA in vivo. J. Virol. 63:1651-1660.
17. Jordan, M., A. Schallhorn, and F. M. Wurm. 1996. Transfecting mammalian cells: optimization of critical parameters affecting calcium-phosphate precipitate formation. Nucleic Acids Res. 24:596-601.
18. Kevil, C. G., A. De Benedetti, D. K. Payne, L. L. Coe, F. S. Laroux, and J. S. Alexander. 1996. Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int. J. Cancer 65:785-790.
19. Kozak, M. 1991. An analysis of vertebrate mRNA sequences: intimations of translational control. J. Cell Biol. 115:887-903.
20. Kraggerud, S. M., J. A. Sandvik, and E. O. Pettersen. 1995. Regulation of protein synthesis in human cells exposed to extreme hypoxia. Anticancer Res. 15:683-686.
21. Le, S.-Y., and J. V. Maizel, Jr. 1997. A common RNA structural motif involved in the internal initiation of translation of cellular mRNAs. Nucleic Acids Res. 25:362-369.
22. Levy, A. P., N. S. Levy, and M. A. Goldberg. 1996. Hypoxia-inducible protein binding to vascular endothelial growth factor mRNA and its modulation by the von Hippel-Lindau protein. J. Biol. Chem. 271:25492-25497.
23. Lindquist, S. 1986. The heat-shock response. Annu. Rev. Biochem. 55:1151-1191.
24. Macejak, D. G., and P. Sarnow. 1991. Internal initiation of translation mediated by the 5′ leader of a cellular mRNA. Nature 353:90-94.
25. Meyuhas, O., E. A. Thompson, Jr., and R. P. Perry. 1987. Glucocorticoids selectively inhibit translation of ribosomal protein mRNAs in P1798 lymphosarcoma cells. Mol. Cell. Biol. 7:2691-2699.
26. 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. 6:1643-1653.
27. Pain, V. M. 1996. Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem. 236:747-771.
28. Pe'er, J., D. Shweiki, A. Itin, I. Hemo, H. Gnessin, and E. Keshet. 1995. Hypoxia-induced expression of vascular endothelial growth factor by retinal cells is a common factor in neovascularizing ocular diseases. Lab. Invest. 72:638-645.
29. Pelletier, J., and N. Sonenberg. 1988. Internal initiation of translation of eukaryotic mRNA directed by a sequence derived from poliovirus RNA. Nature 334:320-325.
30. Plate, K. H., G. Breier, H. A. Weich, and W. Risau. 1992. Vascular endothelial growth factor is a potential tumour angiogenesis factor in human gliomas in vivo. Nature 359:845-848.
31. Senger, D. R., L. Van de Water, L. F. Brown, J. A. Nagy, K. T. Yeo, T. K. Yeo, B. Berse, R. W. Jackman, A. M. Dvorak, and H. F. Dvorak. 1993. Vascular permeability factor (VPF, VEGF) in tumor biology. Cancer Metastasis Rev. 12:303-324.
32. Shima, D. T., U. Deutsch, and P. A. D'Amore. 1995. Hypoxic induction of vascular endothelial growth factor (VEGF) in human epithelial cells is mediated by increases in mRNA stability. FEBS Lett. 370:203-208.
33. Shweiki, D., A. Itin, D. Soffer, and E. Keshet. 1992. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359:843-845.
34. Shweiki, D., M. Neeman, A. Itin, and E. Keshet. 1995. Induction of vascular endothelial growth factor expression by hypoxia and by glucose deficiency in multicell spheroids: implications for tumor angiogenesis. Proc. Natl. Acad. Sci. USA 92:768-772.
35. Sonenberg, N. 1996. mRNA 5′ cap-binding protein eIF4E and control of cell growth, p. 245-269. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
36. Stein, I., M. Neeman, D. Shweiki, A. Itin, and E. Keshet. 1995. Stabilization of vascular endothelial growth factor mRNA by hypoxia and hypoglycemia and coregulation with other ischemia-induced genes. Mol. Cell. Biol. 15:5363-5368.
37. Stone, J., A. Itin, T. Alon, J. Pe'er, H. Gnessin, T. Chan Ling, and E. Keshet. 1995. Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J. Neurosci. 15:4738-4747.
38. Teerink, H., H. O. Voorma, and A. A. M. Thomas. 1995. The human insulin-like growth factor II leader 1 contains an internal ribosomal entry site. Biochim. Biophys. Acta 1264:403-408.
39. Vagner, S., M. C. Gensac, A. Maret, F. Bayard, F. Amalric, H. Prats, and A. C. Prats. 1995. Alternative translation of human fibroblast growth factor 2 mRNA occurs by internal entry of ribosomes. Mol. Cell. Biol. 15:35-44.
40. Ye, X., P. Fong, N. Iizuka, D. Choate, and D. R. Cavener. 1997. Ultrabithorax and Antennapedia 5′ untranslated regions promote developmentally regulated internal translation initiation. Mol. Cell. Biol. 17:1714-1721.