A novel inhibitor of cap-dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E

EMBO Journal

Volumn 16, Issue 5, 1997, Pages 1114-1121

  Altmann, Michael ^a   Schmitz, Nicole ^a   Berset, Catherine ^a   Trachsel, Hans ^a  

^a UNIVERSITY OF BERN   (Switzerland)

Author keywords

4E BPS; eIF4E; eIF4G; Saccharomyces cerevisiae; Translation initiation

Indexed keywords

CAPPED RNA; FUNGAL PROTEIN; INITIATION FACTOR; MESSENGER RNA; PROTEIN SUBUNIT; RNA BINDING PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING SITE; CONTROLLED STUDY; FUNGUS GROWTH; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA STRUCTURE; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TOBACCO MOSAIC VIRUS; TRANSLATION INITIATION;

AMINO ACID SEQUENCE; BINDING SITES; BLOTTING, WESTERN; CELL DIVISION; ELECTROPHORESIS, POLYACRYLAMIDE GEL; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4F; EUKARYOTIC INITIATION FACTOR-4G; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; MOLECULAR SEQUENCE DATA; NUCLEAR CAP-BINDING PROTEIN COMPLEX; PEPTIDE INITIATION FACTORS; PHOSPHOPROTEINS; PROTEIN BIOSYNTHESIS; RECOMBINANT FUSION PROTEINS; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID;

FUNGI; NICOTIANA TABACUM; SACCHAROMYCES CEREVISIAE; TOBACCO MOSAIC VIRUS;

EID: 0031041015     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.5.1114     Document Type: Article

References (39)

1. Allen, M.L., Metz, A.M., Timmer, R.T., Rhoads, R.E. and Browning, K.S. (1992) Isolation and sequence of the cDNAs encoding the subunits of the isozyme form of wheat protein synthesis initiation factor 4F. J. Biol. Chem., 267, 23232-23236.
2. Altmann, M., Edery, I., Sonenberg, N. and Trachsel, H. (1985) Purification and characterization of protein synthesis initiation factor eIF-4E from the yeast Saccharomyces cerevisiae. Biochemistry, 24, 6085-6089.
3. Altmann, M., Krieger, M. and Trachsel, H. (1989a) Nucleotide sequence of the gene encoding a 20 kDa protein associated with the cap binding protein eIF-4E from Saccharomyces cerevisiae. Nucleic Acids Res., 17, 7520.
4. Altmann, M., Sonenberg, N. and Trachsel, H. (1989b) Translation in Saccharomyces cerevisiae: initiation factor 4E-dependent cell-tree system. Mol. Cell. Biol., 9, 4467-4472.
5. Altmann, M., Blum, S., Wilson, T.M. and Trachsel, H. (1990) The 5′-leader sequence of tobacco mosaic virus RNA mediates initiation-factor-4E-independent, but still initiation-factor-4A-dependent translation in yeast extracts. Gene, 91, 127-129.
6. Anderson, C.W., Baum, P.R. and Gesteland, R.F. (1973) Processing of adenovirus 2-induced proteins. J. Virol., 12, 241-252.
7. Barbet, N.C., Schneider, U., Helliwell, S.B., Stansfield, I., Tuite, M.F. and Hall, M.N. (1996) TOR controls translation initiation and early G1 progression in yeast. Mol. Biol. Cell, 7, 25-42.
8. Beretta, L., Gingras, A.C., Svitkin, Y.V. Hall, M.N. and Sonenberg, N. (1996) Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J., 15, 658-664.
9. Brenner, C., Nakayama, N., Goebl, M., Tanaka, K., Toh-e, A. and Matsumoto, K. (1988) CDC33 encodes mRNA cap-binding protein eIF-4E of Saccharomyces cerevisiae. Mol. Cell. Biol., 8, 3556-3559.
10. de Benedetti, A., Joshi, B., Graff, J.R. and Zimmer, S.G. (1994) CHO cells transformed by the translation factor eIF-4E display increased c-myc expression, but require overexpression of Max for tumorigenicity. Mol. Cell. Differ., 2, 347-371.
11. Edery, I., Hümbelin, M., Darveau, A., Lee, K.A.W., Milburn, S., Hershey, J.W.B., Trachsel, H. and Sonenberg, N. (1983) Involvement of eukaryotic initiation factor 4A in the cap recognition process. J. Biol. Chem., 258, 11398-11403.
12. Goyer, C., Altmann, M., Lee, H.S., Blanc, A., Deshmukh, M., Woolford, J.L., Trachsel, H. and Sonenberg, N. (1993) TIF4631 and TIF4632 -Two yeast genes encoding the high-molecular-weight subunits of the cap-binding protein complex (eukaryotic initiation factor-4F) contain an RNA recognition motif-like sequence and carry out an essential function. Mol. Cell. Biol., 13, 4860-4874.
13. Grifo, J.A., Tahara, S.M., Morgan, M.A., Shatkin, A.J. and Merrick, W.C. (1983) New initiation factor activity required for globin mRNA translation. J. Biol. Chem., 258, 5804-5810.
14. Haghighat, A., Mader, S., Pause, A. and Sonenberg, N. (1995) Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J., 14, 5701-5709.
15. Ito, H., Fukuda, Y., Murata, K. and Kimura, A. (1983) Transformation of intact yeast cells treated with alkali cations. J. Bacteriol., 153, 163-168.
16. Lamphear, B.J., Kirchweger, R., Skern, T. and Rhoads, R.E. (1995) Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases - Implications for cap-dependent and cap-independent translational initiation. J. Biol. Chem., 270, 21975-21983.
17. Lanker, S., Müller, P.P., Altmann, M. Goyer, C., Sonenberg, N. and Trachsel, H. (1992) Interactions of the eIF-4F subunits in the yeast Saccharomyces cerevisiae. J. Biol. Chem., 267, 21167-21171.
18. Lazaris-Karatzas, A., Montine, K.S. and Sonenberg, N. (1990) Malignant transformation by a eukaryotic initiation factor subunit that binds to mRNA 5′ cap. Nature, 345, 544-547.
19. Lin, T.A., Kong, X., Haystead, T.A.J., Pause, A., Belsham, G., Sonenberg, N. and Lawrence, J.C. (1994) PHAS-I as a link between mitogen-activated protein kinase and translation initiation. Science, 266, 653-656.
20. Mader, S. and Sonenberg, N. (1995) Cap binding complexes and cellular growth control. Biochimie, 77, 40-44.
21. Mader, S., Lee, H., Pause, A. and Sonenberg, N. (1995) The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4gamma and the translational repressors 4E-binding proteins. Mol. Cell. Biol., 15, 4990-4997.
22. Merrick, W.C. and Hershey, J.W.B. (1996) The pathway and mechanism of eukaryotic protein synthesis. In Hershey, J.W.B., Mathews, M.B. and Sonenberg, N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 31-69.
23. Ohlmann, T., Rau, M., Morley, S.J. and Pain, V.M. (1995) Proteolytic cleavage of initiation factor eIF-4gamma in the reticulocyte lysate inhibits translation of capped mRNAs but enhances that of uncapped mRNAs. Nucleic Acids Res., 23, 334-340.
24. Ohlmann, T., Rau, M., Pain, V.M. and Morley, S.J. (1996) The C-terminal domain of eukaryotic protein synthesis initiation factor (eIF) 4G is sufficient to support cap-independent translation in the absence of eIF4E. EMBO J., 15, 1371-1382.
25. Pain, V.M. (1996) Initiation of protein synthesis in eukaryotic cells. Eur. J. Biochem., 236, 747-771.
26. Pause, A., Belsham, G.J., Gingras, A.C., Donze, O., Lin, T.A., Lawrence, J.C. and Sonenberg, N. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature, 371, 762-767.
27. Rosenwald, I.B., Lazaris-Karatzas, A., Sonenberg, N. and Schmidt, E.V. (1993) Elevated levels of cyclin D1 protein in response to increased expression of eukaryotic initiation factor 4E. Mol. Cell. Biol., 13, 7358-7363.
28. Rozen, F., Edery, I., Meerovitch, K., Dever, T.E., Merrick, W.C. and Sonenberg, N. (1990) Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol., 10, 1134-1144.
29. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
30. Shantz, L.M. and Pegg, A.E. (1994) Overproduction of ornithine decarboxylase caused by relief of translational repression is associated with neoplastic transformation. Cancer Res., 54, 2313-2316.
31. Shatkin, A.J. (1985) mRNA cap binding proteins: essential factors for initiating translation. Cell, 40, 223-224.
32. Sleat, D.E., Gallie, D.R., Jefferson, R.A., Bevan, M.W., Turner, P.C. and Wilson, T.M.A. (1987) Characterization of the 5′-leader sequence of tobacco mosaic virus RNA as a general enhancer of translation in vitro. Gene, 217, 217-225.
33. Smith, M.R., Jaramillo, M., Liu, Y. Dever, T.E., Merrick, W.C., Kung, H. and Sonenberg, N. (1990) Translation initiation factors induce DNA synthesis and transform NIH 3T3 cells. New Biol., 2, 648-654.
34. Sonenberg, N. (1988) Cap-binding proteins of eukaryotic messenger RNA: functions in initiation and control of translation. Prog. Nucleic Acid Res. Mol. Biol., 35, 173-207.
35. Sonenberg, N., Morgan, M.A., Merrick W.C. and Shatkin, A.J. (1978) A polypeptide in eukaryotic initiation factors that crosslinks specifically to the 5′-terminal cap in mRNA. Proc. Natl Acad. Sci. USA, 75, 4843-4847.
36. 7G-cap binding protein with different effects on capped mRNA translation in extracts of uninfected and poliovirus-infected HeLa cells. J. Biol. Chem., 256, 7691-7694.
37. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA, 76, 4350-4354.
38. S6k pathway and is independent of mitogen-activated protein kinase. Proc. Natl Acad. Sci. USA, 93, 4076-4080.
39. Zanchin, N.I.T. and McCarthy, J.E.G. (1995) Characterization of the in vivo phosphorylation sites of the mRNA-cap-binding complex proteins eukaryotic initiation factor-4E and p20 in Saccharomyces cerevisiae. J. Biol. Chem., 270, 26505-26510.