Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5' cap in yeast involves a site partially shared by p20

EMBO Journal

Volumn 17, Issue 16, 1998, Pages 4798-4808

  Ptushkina, Marina ^a   Von der Haar, Tobias ^a   Vasilescu, Simona ^a   Frank, Ronald ^b   Birkenhäger, Ralf ^a   McCarthy, John E G ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Cooperativity; eIF4E and eIF4G; Interaction sites; Regulation by 4E binding proteins; Yeast gene expression

Indexed keywords

CELL PROTEIN; INITIATION FACTOR 4E; MESSENGER RNA; RNA BINDING PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHROMATOGRAPHY; CONTROLLED STUDY; GENE MUTATION; NONHUMAN; POLYSOME; PRIORITY JOURNAL; PROTEIN RNA BINDING; PROTEIN SYNTHESIS; RNA TRANSLATION; TEMPERATURE SENSITIVITY; YEAST;

AMINO ACID SEQUENCE; ANTIBODIES, MONOCLONAL; BINDING SITES; EUKARYOTIC INITIATION FACTOR-4E; EUKARYOTIC INITIATION FACTOR-4G; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR CAP-BINDING PROTEIN COMPLEX; PEPTIDE INITIATION FACTORS; PEPTIDE MAPPING; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA CAPS; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 0032541425     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.16.4798     Document Type: Article

References (46)

1. Altmann,M., Edery,I., Trachsel,H. and Sonenberg,N. (1988) Site-directed mutagenesis of the tryptophan residues in yeast eukaryotic initiation factor 4E. J. Biol. Chem., 263, 17229-17323.
2. Altmann,M., Müller,P.P., Pelletier,J., Sonenberg,N. and Trachsel,H. (1989) A mammalian translation initiation factor can substitute for its yeast homologue in vivo. J. Biol. Chem., 264, 12145-12147.
3. Altmann,M., Schmitz,N., Berset,C. and Trachsel,H. (1997) A novel inhibitor of cap-dependent translation initiation in yeast: p20 competes with eIF4G for binding to eIF4E. EMBO J., 16, 1114-1121.
4. Belev,T.N., Singh,M. and McCarthy,J.E.G. (1991) A fully modular vector system for the optimisation of gene expression in Escherichia coli. Plasmid, 26, 147-150.
5. Browning,K.S. (1996) The plant translational apparatus. Plant Mol. Biol., 32, 107-144.
6. 7GpppG to human protein-synthesis initiation factor-4E. Biochemistry, 28, 8078-8083.
7. Craig,A.W.B., Haghighat,A., Yu,A.T.K. and Sonenberg,N. (1998) Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature, 392, 520-523.
8. De la Cruz,J., Iost,I., Kressler,D. and Linder,P. (1997) The p20 and DED1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA, 94, 5201-5206.
9. Edery,I., Lee,K.A.W. and Sonenberg,N. (1987) In Illan,I. (ed.), Translational Regulation of Gene Expression. Plenum Press, New York,NY, pp. 335-366.
10. Frank,R. (1992) Spot-synthesis: an easy technique for the positionally addressable, parallel chemical synthesis on a membrane support. Tetrahedron, 48, 9217-9232.
11. 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.
12. Gradi,A., Imataka,H., Svitkin,Y.V., Rom,E., Raught,B., Morino,S. and Sonenberg,N. (1998) A novel functional human eukaryotic translation initiation factor 4G. Mol. Cell. Biol., 18, 334-342.
13. Grossman,A.D., Erickson,J.W. and Gross,C.A. (1984) The htpR gene product of E.coli is a sigma factor for heat-shock promoters. Cell, 38, 383-390.
14. Haghighat,A. and Sonenberg,N. (1997) eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J. Biol. Chem., 272, 21677-21680.
15. Haile,D.J., Hentze,M.W., Roualt,T.A., Harford,J.B. and Klausner,R.D. (1989) Regulation of interaction of the iron-responsive element binding-protein with iron-responsive RNA elements. Mol. Cell. Biol., 9, 5055-5061.
16. Harlow,E. and Lane,D. (1988) Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
17. Laemmli,E.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
18. 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. J. Biol. Chem., 270, 21975-21983.
19. Lang,V., Zanchin,N., Lünsdorf,H., Tuite,M.F. and McCarthy,J.E.G. (1994) Initiation factor eIF-4E of Saccharomyces cerevisiae: distribution within the cell, binding to mRNA and consequences of its overproduction. J. Biol. Chem., 269, 6117-6123.
20. Lanker,S., Muller,P.R. 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.
21. Le,H., Tanguay,R.L., Balasta,M.L., Wei,C.-C., Browning,K.S., Metz,A.M., Goss,DJ. and Gallie,D.R. (1997) Translation initiation factors eIF-iso4G and eIF-4B interact with the poly(A)-binding protein and increase its RNA binding activity. J. Biol. Chem., 272, 16247-16255.
22. Mader,S., Lee,H., Pause,A. and Sonenberg,N. (1995) The translation of initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4γ and the translational repressors 4E-binding proteins. Mol. Cell. Biol., 15, 4990-4997.
23. Marcotrigiano,J., Gingras,A.-C., Sonenberg,N. and Burley,S.K. (1997) Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell, 89, 951-961.
24. 7GDP and interaction with 4E-binding protein. Nature Struct. Biol., 4, 717-724.
25. McCarthy,J.E.G. (1998) Posttranscriptional control of gene expression in yeast. Microbiol. Mol. Biol. Rev., in press.
26. McCarthy,J.E.G. and Kollmus,H. (1995) Cytoplasmic mRNA-protein interactions in eukaryotic gene expression. Trends Biochem. Sci., 20 191-197.
27. Merrick,W.C. and Hershey,J.W.B. (1996) The pathway and mechanism of eukaryotic protein synthesis. In Hershey,J.W.B., Matthews,M.B. and Sonenberg,N. (eds), Translational Control. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 31-70.
28. Mikaelian,I. and Sergeant,A. (1992) A general and fast method to generate multiple site directed mutations. Nucleic Acids Res., 20, 376.
29. Morino,S., Hazama,H., Ozaki,M., Teraoka,Y., Shibata,S., Doi,M., Ueda,H., Ishida,T. and Uesugi,S. (1996) Analysis of the mRNA capbinding ability of human eukaryotic initiation factor-4E by use of recombinant wild-type and mutant forms. Eur. J. Biochem., 238, 597-601.
30. Morley,S.J., Curtis,P.S. and Pain,V.M. (1997) eIF4G: Translation's mystery factor begins to yield its secrets. RNA, 3, 1085-1104.
31. Oliveira,C.C., van den Heuvel,J.J. and McCarthy,J.E.G. (1993) Inhibition of translational initiation in Saccharomyces cerevisiae by secondary structure: the role of the stability and position of stem-loops in the mRNA leader. Mol. Microbiol., 9, 521-532.
32. Pause,A., Belsham,G.J., Gingras,A.-C., Donzé,O., Lin,T.-A., Lawrence,J.C.,Jr and Sonenberg,N. (1994) Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′-cap function. Nature, 371, 762-767.
33. Ptashne,M. (1967) Specific binding of the λ phage repressor to λ DNA. Nature, 214, 232-234.
34. Ptushkina,M., Fierro-Monti,I., van den Heuvel,J., Vasilescu,S., Birkenhäger,R., Mita,K. and McCarthy,J.E.G. (1996) Schizosaccharomyces pombe has a novel eukaryotic initiation factor 4F complex containing a cap-binding protein with the human eIF4E C-terminal motif KSGST. J. Biol. Chem., 271, 32818-32824.
35. 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.
36. Sagliocco,F., Vega Laso,M.R., Zhu,D., Tuite,M.F., McCarthy,J.E.G. and Brown,A.J.P. (1993) The influence of 5′ secondary structures upon ribosome binding to mRNA during translation in yeast. J. Biol. Chem., 268, 26522-26530.
37. Sambrook,J., Fritsch,E.F. and Maniatis,T. (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
38. Sayle,R.A. and Milner-White,E.J. (1995) RASMOL: biomolecular graphics for all. Trends Biochem. Sci., 20, 374-376.
39. Sherman,F., Fink,G.R. and Hicks,J.B. (1986) Laboratory Course Manual for Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
40. Sonenberg,N. (1996) mRNA 5′ Cap-binding protein eIF4E and control of cell growth. In Hershey,J.W.B., Matthews,M.B. and Sonenberg,N. (eds), Translational Control, Cold Spring Harbour Laboratory Press, Cold Spring Harbour, NY, pp. 245-269.
41. Tarun,S.Z. and Sachs,A.B. (1996) Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. EMBO J., 15, 7168-7177.
42. Tarun,S.Z., Wells,S.E., Deardorff,J.A. and Sachs,A.B. (1997) Translation initiation factor eIF4G mediates in vitro poly(A) tail-dependent translation. Proc. Natl Acad. Sci. USA, 94, 9045-9051.
43. Ueda,H., Maruyama,H., Doi,M., Inoue,M., Ishida,T., Morioka,H., Tanaka,T., Nishikawa,S. and Uesugi,E. (1991) Expression of a synthetic gene for human cap binding-protein (human IF-4E) in Escherichia coli and fluorescence studies on interaction with messenger-RNA cap structure analogs. J. Biochem. (Tokyo), 109, 882-889.
44. Vasilescu,S., Ptushkina,M., Linz,B., Müller,P.P. and McCarthy,J.E.G. (1996) Mutants of eukaryotic initiation factor eIF-4E with altered mRNA cap binding specificity reprogram mRNA selection by ribosomes in Saccharomyces cerevisiae. J. Biol. Chem., 271, 7030-7037.
45. 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.
46. Zhong,T. and Arndt,K.T. (1993) The yeast SISI protein, a DnaJ homolog, is required for the initiation of translation. Cell, 73, 1175-1186.