Ribosome loading onto the mRNA cap is driven by conformational coupling between eIF4G and eIF4E

Cell

Volumn 115, Issue 6, 2003, Pages 739-750

  Gross, John D ^a,d   Moerke, Nathan J ^a   Von Der Haar, Tobias ^b   Lugovskoy, Alexey A ^a   Sachs, Alan B ^c   McCarthy, John E G ^b   Wagner, Gerhard ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; INITIATION FACTOR 4E; INITIATION FACTOR 4G;

ALLOSTERISM; AMINO TERMINAL SEQUENCE; ARTICLE; MOLECULAR BIOLOGY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; RIBOSOME; RNA CAPPING; RNA CONFORMATION;

EUKARYOTA;

EID: 0347281686     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(03)00975-9     Document Type: Article

References (56)

1. Altmann M., Handschin C., Trachsel H. mRNA cap-binding protein. cloning of the gene encoding protein synthesis initiation factor eIF-4E from Saccharomyces cerevisiae Mol. Cell. Biol. 7:1987;998-1003.
2. Altmann M., Schmitz N., Berset C., Trachsel H. A novel inhibitor of cap-dependent translation initiation in yeast-p20 competes with eIF4E for binding to eIF4E. EMBO J. 16:1997;1114-1121.
3. Asano K., Shalev A., Phan L., Nielsen K., Clayton J., Valasek L., Donahue T.F., Hinnebusch A.G. Multiple roles for the C-terminal domain of eIF5 in translation initiation complex assembly and GTPase activation. EMBO J. 20:2001;2326-2337.
4. Battiste J.L., Wagner G. Utilization of site-directed spin labeling and high-resolution heteronuclearnuclear magnetic resonance for global fold determination of large proteins with limited nuclear overhauser effect data. Biochemistry. 39:2000;5355-5365.
5. Benne R., Hershey J.W.B. Purification and characterization of initiation factor IF-E3 from rabbit reticulocytes. Proc. Natl. Acad. Sci. USA. 73:1976;3005-3009.
6. Berset C., Zurbriggen A., Djafarzadeh S., Altmann M., Trachsel H. RNA-binding activity of translation initiation factor eIF4G1 from Saccharomyces cerevisiae. RNA. 9:2003;871-880.
7. Boeke J.D., Trueheart J., Natsoulis G., Fink G.R. 5-fluoroorotic acid as a selective agent in yeast molecular genetics. Methods Enzymol. 154:1987;164-165.
8. Brunger A.T. X-PLOR Version 3.851. a system for X-ray crystallography and NMR:1996;Yale University Press, New Haven, CT.
9. Carberry S.E., Darzynkiewicz E., Goss D.J. A comparison of the binding of methylated cap analogues to wheat germ protein synthesis initiation factors 4F and (Iso)4F. Biochemistry. 30:1991;1624-1627.
10. Cornilescu G., Delaglio F., Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR. 13:1999;289-302.
11. Dever T.E. Gene-specific regulation by general translation factors. Cell. 108:2002;545-556.
12. Dunbrack R.L., Karplus M. Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J. Mol. Biol. 230:1993;543-574.
13. Etchison D., Milburn S.C., Edery I., Sonenberg N. Inhibition of HeLa cell protein synthesis following poliovirus infection correlates with the proteolysis of a 220,000 Da polypeptide associated with eukaryotic initiation factor 3 and a cap binding complex. J. Biol. Chem. 257:1982;14806-14810.
14. Fletcher C.M., McGuire A.M., Gingras A.-C., Li H., Matsuo H., Sonenberg N., Wagner G. 4E binding proteins inhibit the translation factor eIF4E without folded structure. Biochemistry. 37:1998;9-15.
15. Gallie D.R. The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev. 5:1991;2108-2116.
16. Gingras A.-C., Gygi S.P., Raught B., Polakiewicz R.D., Abraham R.T., Hoekstra M.F., Aebersold R., Sonenberg N. Regulation of 4E-BP1 phosphorylation. a novel two-step mechanism Genes Dev. 13:1999;1422-1437. a.
17. Gingras A.-C., Raught B., Sonenberg N. eIF4 initiation factors. effectors of mRNA recruitment to ribosomes and regulators of translation Annu. Rev. Biochem. 68:1999;913-963. b.
18. Gingras A.-C., Raught B., Gygi S.P., Niedzwiecka A., Miron M., Burley S.K., Polakiewicz R.D., Wyslouch-Ciesznska A., Aebersold R., Sonenberg N. Hierarchical phosphorylation of the translation inihibitor 4E-BP1. Genes Dev. 15:2001;2852-2864.
19. He H., von der Haar T., Singh C.R., Ii M., Li B., Hinnebusch A.G., McCarthy J.E., Asano K. The yeast eukaryotic initiation factor 4G (eIF4G) HEAT domain interacts with eIF1 and eIF5 and is involved in stringent AUG selection. Mol. Cell. Biol. 23:2003;5431-5445.
20. Haghighat A., Sonenberg N. eIF4G dramatically enhances the binding of eIF4E to the mRNA 5′-cap structure. J. Biol. Chem. 272:1997;21677-21680.
21. Haghighat A., Mader S., Pause A., Sonenberg N. Repression of cap-dependent translation by 4E-binding protein 1. competition with p220 fo rbinding to eukaryotic initation factor-4E EMBO J. 14:1995;5701-5709.
22. Hentze M.W. eIF4G. a multipurpose ribosome adapter Science. 275:1997;500-501.
23. Hershey J.W.B., Merrick W.C. The pathway and mechanism of initiation of protein synthesis. Sonenberg N., Hershey J.W.B., Mathews M.B. Translational Control of Gene Expression. 2000;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
24. Hershey P.E.C., McWhirter S.M., Gross J.D., Wagner G., Alber T., Sachs A.B. The cap-binding protein eIF4E promotes folding of a functional domain of yeast translation initiation factor eIF4G1. J. Biol. Chem. 274:1999;21297-21304.
25. Iizuka N., Najita L., Franzusoff A., Sarnow P. Cap-dependent and cap-independent translation by internal initiation of mRNAs in cell extracts prepared from Saccharomyces cerevisiae. Mol. Cell. Biol. 14:1994;7322-7330.
26. Jacobson A. Poly(A) metabolism and translation. the closed loop model Hershey J.W.B., Matthews M.B., Sonenberg N. Translational Control. 1996;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
27. Karim M.M., Hughes J.M.X., Warwicker J., Scheper G.C., Proud C.G., McCarthy J.E.G. A quantitative molecular model for modulation of mammalian translation by the eIF4E-binding protein 1. J. Biol. Chem. 276:2001;20750-20757.
28. Koradi R., Billeter M., Wüthrich K. Molmol. a program for display and analysis of macromolecular structures J. Mol. Graph. 14:1996;51-55.
29. Lamphear B.J., Kirchweger R., Skern T., Rhoads R.E. Mapping of functional domains in eukaryotic protein synthesis initiation factor 4G (eIF4G) with picornaviral proteases. J. Biol. Chem. 270:1995;21975-21983.
30. Laskowski R.A., MacArthur R.W., Moss D.S., Thorton J.M. Procheck. a program to check the sterochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291.
31. Lee K.A.W., Sonenberg N. Inactivation of cap-binding proteins accompanies the shut-off of host protein synthesis by poliovirus. Proc. Natl. Acad. Sci. USA. 79:1982;3447-3451.
32. Luo Y., Goss D.J. Homeostasis in mRNA initiation. J. Biol. Chem. 276:2001;43083-43086.
33. Mader S., Lee H., Pause A., Sonenberg N. The translation initiation factor eIF4E binds to a common motif shared by the translation factor eIF4E and the translational repressors 4E-binding proteins. Mol. Cell. Biol. 15:1995;4990-4997.
34. Marcotrigiano J., Gingras A.-C., Sonenberg N., Burley S.K. Cocrystal structure of the messenger RNA 5′ cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell. 89:1997;951-961.
35. Marcotrigiano J., Gingras A.-C., Sonenberg N., Burley S.K. Cap-dependent translation initiation in eukaryotes is regulated by a molecular mimic of eIF4G. Mol. Cell. 3:1999;707-716.
36. Matsuo H., Li H., McGuire A.M., Fletcher C.M., Gingras A.-C., Sonenberg N., Wagner G. Structure of translation factor eIF4E bound to m7GDP and interaction with 4E-binding protein. Nat Struct Biol. 4:1997;717-724.
37. Niedzwiecka A., Marcotrigiano J., Stepinski J., Jankowska-Anyszka M., Wyslouch-Cieszynska A., Dadlez M., Gingras A.-C., Mak P., Darzynkiewicz E., Sonenberg N.et al. Biophysical studies of eIF4E cap-binding protein. recognition of mRNA 5′ cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins J. Mol. Biol. 319:2002;615-635.
38. Ohlmann T., Pain V.M., Wood W., Rau M., Morley S.J. The proteolytic cleavage of eukaryotic initiation factor (eIF) 4G is prevented by eIF4E binding protein (PHAS-I;4E-BP1) in reticulocyte lysate. EMBO J. 16:1997;844-855.
39. Oliveira C.C., van den Heuvel J.J., McCarthy J.E. Inhibition of translational initiation in Saccharomyces cerevisiae by secondary structure. the roles of the stability and position of stem-loops in the mRNA leader Mol. Microbiol. 9:1993;521-532.
40. Pause A., Belsham G.J., Gingras A.C., Donze O., Lin T.A., Lawrence J.C. Jr., Sonenberg N. Insulin-dependent stimulation of protein synthesis by phosphorylation of a regulator of 5′ cap function. Nature. 371:1994;762-767.
41. Pestova T.V., Shatsky I.N., Hellen C.U. Functional dissection of eukaryotic initiation factor 4F. the 4A subunit and the central domain of the 4G subunit are sufficient to mediate internal entry of 43S preinitiation complexes Mol. Cell. Biol. 16:1996;6870-6878.
42. Prevot D., Darlix J.-L., Ohlmann T. Conducting the initiation of protein synthesis. the role of eIF4G Biol. Cell. 95:2003;141-156.
43. Ptushkina M., von der Haar T., Vasilescu S., Frank R., Birkenhager R., McCarthy J.E. Cooperative modulation by eIF4G of eIF4E-binding to the mRNA 5′ cap in yeast involves a site partially shared by p20. EMBO J. 17:1998;4798-4808.
44. Ptushkina M., von der Haar T., Karim M.M., Hughes J.M., McCarthy J.E. Repressor binding to a dorsal regulatory site traps human eIF4E in a high cap-affinity state. EMBO J. 18:1999;4068-4075.
45. Raught B., Gingras A.-C., Sonenberg N. Regulation of ribosomal recruitment in eukaryotes. Sonenberg N., Hershey J.W.B., Mathews M.B. Translational Control of Gene Expression. 2000;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
46. Richter J.D. Influence of polyadenylation-induced translation on metazoan development and neuronal synaptic function. Sonenberg N., Hershey J.W.B., Mathews M.B. Translational Control of Gene Expression. 2000;785 Cold Spring Harbor Press, Cold Spring Harbor, NY.
47. Sachs A.B., Sarnow P., Hentze M.W. Starting at the beginning, middle and end, translation initiation in eucaryotes. Cell. 89:1997;831-838.
48. Scheper G.C., van Kollenburg B., Hu J., Luo J., Goss D.J., Proud C.G. Phosphorylation of eukaryotic initiation factor 4E markedly reduces its affinity for capped mRNA. J. Biol. Chem. 277:2002;3303-3309.
49. Sha M., Wang Y., Xiang T., van Heerden A., Browning K.S., Goss D.J. Interaction of wheat germ protein synthesis initiation factor eIF-(iso)4F and its subunits p28 and p86 with m7GTP and mRNA analogues. J. Biol. Chem. 270:1995;29904-29909.
50. Tarun S.Z., Sachs A.B. Binding of eukaryotic translation initiation factor 4E (eIF4E) to eIF4G represses translation of uncapped mRNA. Mol. Cell. Biol. 17:1997;6876-6886.
51. Uchida N., Hoshino S.-I., Imataka H., Sonenberg N., Katada T. A novel role fo the mammalian GSPT/eRF3 associating with poly(A)-binding protein in cap/poly(A)-dependent translation. J. Biol. Chem. 277:2002;50286-50292.
52. Vasilescu S., Ptushkina M., Linz B., Muller P.P., McCarthy J.E.G. Mutants of eukaryotic initiation factor eIF4E with altered mRNA cap binding specificity reprogram mRNA selection by ribosomes in Saccharomyces cerevisiae. J. Biol. Chem. 271:1996;7030-7037.
53. von der Haar T., McCarthy J.E.G. Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol. Microbiol. 2:2002;531-544.
54. von der Haar T., Ball P.D., McCarthy J.E.G. Stabilization of eukaryotic initiation factor 4E binding to the mRNA 5′-cap by domains of eIF4G. J. Biol. Chem. 275:2000;30551-30555.
55. Wei C.-C., Balasta M.L., Ren J., Goss D.J. Wheat germ poly(A) binding protein enhances the binding affinity of eukaryotic initiation factor 4F and (iso)4F for cap analogues. Biochemistry. 37:1998;1910-1916.
56. Wells S.E., Hillner P.E., Vale R.D., Sachs A.B. Circularization of mRNA by eukaryotic translation initiation factors. Mol. Cell. 2:1998;135-140.