Previous Article | Next Article 
Molecular and Cellular Biology, January 2000, p. 468-477, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Eukaryotic Translation Initiation Factor 4E (eIF4E)
Binding Site and the Middle One-Third of eIF4GI Constitute the Core
Domain for Cap-Dependent Translation, and the C-Terminal One-Third
Functions as a Modulatory Region
Shigenobu
Morino,1
Hiroaki
Imataka,1
Yuri V.
Svitkin,1
Tatyana V.
Pestova,2 and
Nahum
Sonenberg1,*
Department of Biochemistry and McGill Cancer
Center, McGill University, Montreal, Quebec H3G 1Y6,
Canada,1 and Department of Microbiology
and Immunology, State University of New York Health Science Center at
Brooklyn, Brooklyn, New York 112032
Received 30 August 1999/Accepted 6 October 1999
The mammalian eukaryotic initiation factor 4GI (eIF4GI) may be
divided into three roughly equal regions; an amino-terminal one-third
(amino acids [aa] 1 to 634), which contains the poly(A) binding
protein (PABP) and eIF4E binding sites; a middle third (aa 635 to
1039), which binds eIF4A and eIF3; and a carboxy-terminal third (aa
1040 to 1560), which harbors a second eIF4A binding site and a docking
sequence for the Ser/Thr kinase Mnk1. Previous reports demonstrated
that the middle one-third of eIF4GI is sufficient for cap-independent
translation. To delineate the eIF4GI core sequence required for
cap-dependent translation, various truncated versions of eIF4GI were
examined in an in vitro ribosome binding assay with
-globin mRNA. A
sequence of 540 aa encompassing aa 550 to 1090, which contains the
eIF4E binding site and the middle region of eIF4GI, is the minimal
sequence required for cap-dependent translation. In agreement with
this, a point mutation in eIF4GI which abolished eIF4A binding in the
middle region completely inhibited ribosomal binding. However, the
eIF4GI C-terminal third region, which does not have a counterpart in
yeast, modulates the activity of the core sequence. When the eIF4A
binding site in the C-terminal region of eIF4GI was mutated, ribosome
binding was decreased three- to fourfold. These data indicate that the interaction of eIF4A with the middle region of eIF4GI is necessary for
translation, whereas the interaction of eIF4A with the C-terminal region plays a modulatory role.
*
Corresponding author. Mailing address: Department of
Biochemistry and McGill Cancer Center, McGill University, Montreal,
Quebec H3G 1Y6, Canada. Phone: (514) 398-7274. Fax: (514) 398-1287. E-mail: nsonen{at}med.mcgill.ca.
Molecular and Cellular Biology, January 2000, p. 468-477, Vol. 20, No. 2
0270-7306/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Fujita, Y., Oe, M., Tutsumino, T., Morino, S., Imataka, H., Tomoo, K., Ishida, T.
(2009). Domain-dependent Interaction of Eukaryotic Initiation Factor eIF4A for Binding to Middle and C-terminal Domains of eIF4G. J Biochem
146: 359-368
[Abstract]
[Full Text]
-
Yanagiya, A., Svitkin, Y. V., Shibata, S., Mikami, S., Imataka, H., Sonenberg, N.
(2009). Requirement of RNA Binding of Mammalian Eukaryotic Translation Initiation Factor 4GI (eIF4GI) for Efficient Interaction of eIF4E with the mRNA Cap. Mol. Cell. Biol.
29: 1661-1669
[Abstract]
[Full Text]
-
Martineau, Y., Derry, M. C., Wang, X., Yanagiya, A., Berlanga, J. J., Shyu, A.-B., Imataka, H., Gehring, K., Sonenberg, N.
(2008). Poly(A)-Binding Protein-Interacting Protein 1 Binds to Eukaryotic Translation Initiation Factor 3 To Stimulate Translation. Mol. Cell. Biol.
28: 6658-6667
[Abstract]
[Full Text]
-
Schutz, P., Bumann, M., Oberholzer, A. E., Bieniossek, C., Trachsel, H., Altmann, M., Baumann, U.
(2008). Crystal structure of the yeast eIF4A-eIF4G complex: An RNA-helicase controlled by protein-protein interactions. Proc. Natl. Acad. Sci. USA
105: 9564-9569
[Abstract]
[Full Text]
-
Kempf, B. J., Barton, D. J.
(2008). Poly(rC) Binding Proteins and the 5' Cloverleaf of Uncapped Poliovirus mRNA Function during De Novo Assembly of Polysomes. J. Virol.
82: 5835-5846
[Abstract]
[Full Text]
-
Suzuki, C., Garces, R. G., Edmonds, K. A., Hiller, S., Hyberts, S. G., Marintchev, A., Wagner, G.
(2008). PDCD4 inhibits translation initiation by binding to eIF4A using both its MA3 domains. Proc. Natl. Acad. Sci. USA
105: 3274-3279
[Abstract]
[Full Text]
-
Hinton, T. M., Coldwell, M. J., Carpenter, G. A., Morley, S. J., Pain, V. M.
(2007). Functional Analysis of Individual Binding Activities of the Scaffold Protein eIF4G. J. Biol. Chem.
282: 1695-1708
[Abstract]
[Full Text]
-
LaRonde-LeBlanc, N., Santhanam, A. N., Baker, A. R., Wlodawer, A., Colburn, N. H.
(2007). Structural Basis for Inhibition of Translation by the Tumor Suppressor Pdcd4. Mol. Cell. Biol.
27: 147-156
[Abstract]
[Full Text]
-
Coldwell, M. J., Morley, S. J.
(2006). Specific Isoforms of Translation Initiation Factor 4GI Show Differences in Translational Activity. Mol. Cell. Biol.
26: 8448-8460
[Abstract]
[Full Text]
-
Miyakawa, S., Oguro, A., Ohtsu, T., Imataka, H., Sonenberg, N., Nakamura, Y.
(2006). RNA aptamers to mammalian initiation factor 4G inhibit cap-dependent translation by blocking the formation of initiation factor complexes. RNA
12: 1825-1834
[Abstract]
[Full Text]
-
Cheng, S., Gallie, D. R.
(2006). Wheat Eukaryotic Initiation Factor 4B Organizes Assembly of RNA and eIFiso4G, eIF4A, and Poly(A)-binding Protein. J. Biol. Chem.
281: 24351-24364
[Abstract]
[Full Text]
-
Karim, M. M., Svitkin, Y. V., Kahvejian, A., De Crescenzo, G., Costa-Mattioli, M., Sonenberg, N.
(2006). A mechanism of translational repression by competition of Paip2 with eIF4G for poly(A) binding protein (PABP) binding. Proc. Natl. Acad. Sci. USA
103: 9494-9499
[Abstract]
[Full Text]
-
Jivotovskaya, A. V., Valasek, L., Hinnebusch, A. G., Nielsen, K. H.
(2006). Eukaryotic Translation Initiation Factor 3 (eIF3) and eIF2 Can Promote mRNA Binding to 40S Subunits Independently of eIF4G in Yeast. Mol. Cell. Biol.
26: 1355-1372
[Abstract]
[Full Text]
-
DERRY, M.C., YANAGIYA, A., MARTINEAU, Y., SONENBERG, N.
(2006). Regulation of Poly(A)-binding Protein through PABP-interacting Proteins. Cold Spring Harb Symp Quant Biol
71: 537-543
[Abstract]
-
Svitkin, Y. V., Herdy, B., Costa-Mattioli, M., Gingras, A.-C., Raught, B., Sonenberg, N.
(2005). Eukaryotic Translation Initiation Factor 4E Availability Controls the Switch between Cap-Dependent and Internal Ribosomal Entry Site-Mediated Translation. Mol. Cell. Biol.
25: 10556-10565
[Abstract]
[Full Text]
-
Hundsdoerfer, P., Thoma, C., Hentze, M. W.
(2005). Eukaryotic translation initiation factor 4GI and p97 promote cellular internal ribosome entry sequence-driven translation. Proc. Natl. Acad. Sci. USA
102: 13421-13426
[Abstract]
[Full Text]
-
Oberer, M., Marintchev, A., Wagner, G.
(2005). Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev.
19: 2212-2223
[Abstract]
[Full Text]
-
Singh, C. R., Curtis, C., Yamamoto, Y., Hall, N. S., Kruse, D. S., He, H., Hannig, E. M., Asano, K.
(2005). Eukaryotic Translation Initiation Factor 5 Is Critical for Integrity of the Scanning Preinitiation Complex and Accurate Control of GCN4 Translation. Mol. Cell. Biol.
25: 5480-5491
[Abstract]
[Full Text]
-
Kim, W. J., Back, S. H., Kim, V., Ryu, I., Jang, S. K.
(2005). Sequestration of TRAF2 into Stress Granules Interrupts Tumor Necrosis Factor Signaling under Stress Conditions. Mol. Cell. Biol.
25: 2450-2462
[Abstract]
[Full Text]
-
ZAKOWICZ, H., YANG, H.-S., STARK, C., WLODAWER, A., LARONDE-LEBLANC, N., COLBURN, N. H.
(2005). Mutational analysis of the DEAD-box RNA helicase eIF4AII characterizes its interaction with transformation suppressor Pdcd4 and eIF4GI. RNA
11: 261-274
[Abstract]
[Full Text]
-
Korneeva, N. L., First, E. A., Benoit, C. A., Rhoads, R. E.
(2005). Interaction between the NH2-terminal Domain of eIF4A and the Central Domain of eIF4G Modulates RNA-stimulated ATPase Activity. J. Biol. Chem.
280: 1872-1881
[Abstract]
[Full Text]
-
MOCHIZUKI, K., OGURO, A., OHTSU, T., SONENBERG, N., NAKAMURA, Y.
(2005). High affinity RNA for mammalian initiation factor 4E interferes with mRNA-cap binding and inhibits translation. RNA
11: 77-89
[Abstract]
[Full Text]
-
Harris, M. N., Ozpolat, B., Abdi, F., Gu, S., Legler, A., Mawuenyega, K. G., Tirado-Gomez, M., Lopez-Berestein, G., Chen, X.
(2004). Comparative proteomic analysis of all-trans-retinoic acid treatment reveals systematic posttranscriptional control mechanisms in acute promyelocytic leukemia. Blood
104: 1314-1323
[Abstract]
[Full Text]
-
Yang, H.-S., Cho, M.-H., Zakowicz, H., Hegamyer, G., Sonenberg, N., Colburn, N. H.
(2004). A Novel Function of the MA-3 Domains in Transformation and Translation Suppressor Pdcd4 Is Essential for Its Binding to Eukaryotic Translation Initiation Factor 4A. Mol. Cell. Biol.
24: 3894-3906
[Abstract]
[Full Text]
-
Willcocks, M. M., Carter, M. J., Roberts, L. O.
(2004). Cleavage of eukaryotic initiation factor eIF4G and inhibition of host-cell protein synthesis during feline calicivirus infection. J. Gen. Virol.
85: 1125-1130
[Abstract]
[Full Text]
-
Gradi, A., Foeger, N., Strong, R., Svitkin, Y. V., Sonenberg, N., Skern, T., Belsham, G. J.
(2004). Cleavage of Eukaryotic Translation Initiation Factor 4GII within Foot-and-Mouth Disease Virus-Infected Cells: Identification of the L-Protease Cleavage Site In Vitro. J. Virol.
78: 3271-3278
[Abstract]
[Full Text]
-
Kasuno, K., Takabuchi, S., Fukuda, K., Kizaka-Kondoh, S., Yodoi, J., Adachi, T., Semenza, G. L., Hirota, K.
(2004). Nitric Oxide Induces Hypoxia-inducible Factor 1 Activation That Is Dependent on MAPK and Phosphatidylinositol 3-Kinase Signaling. J. Biol. Chem.
279: 2550-2558
[Abstract]
[Full Text]
-
Alvarez, E., Menendez-Arias, L., Carrasco, L.
(2003). The Eukaryotic Translation Initiation Factor 4GI Is Cleaved by Different Retroviral Proteases. J. Virol.
77: 12392-12400
[Abstract]
[Full Text]
-
He, H., von der Haar, T., Singh, C. R., Ii, M., Li, B., Hinnebusch, A. G., McCarthy, J. E. G., Asano, K.
(2003). 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: 5431-5445
[Abstract]
[Full Text]
-
OGURO, A., OHTSU, T., SVITKIN, Y. V., SONENBERG, N., NAKAMURA, Y.
(2003). RNA aptamers to initiation factor 4A helicase hinder cap-dependent translation by blocking ATP hydrolysis. RNA
9: 394-407
[Abstract]
[Full Text]
-
Yang, H.-S., Jansen, A. P., Komar, A. A., Zheng, X., Merrick, W. C., Costes, S., Lockett, S. J., Sonenberg, N., Colburn, N. H.
(2003). The Transformation Suppressor Pdcd4 Is a Novel Eukaryotic Translation Initiation Factor 4A Binding Protein That Inhibits Translation. Mol. Cell. Biol.
23: 26-37
[Abstract]
[Full Text]
-
Pestova, T. V., Kolupaeva, V. G.
(2002). The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev.
16: 2906-2922
[Abstract]
[Full Text]
-
Morley, S. J., Naegele, S.
(2002). Phosphorylation of Eukaryotic Initiation Factor (eIF) 4E Is Not Required for de Novo Protein Synthesis following Recovery from Hypertonic Stress in Human Kidney Cells. J. Biol. Chem.
277: 32855-32859
[Abstract]
[Full Text]
-
Byrd, M. P., Zamora, M., Lloyd, R. E.
(2002). Generation of Multiple Isoforms of Eukaryotic Translation Initiation Factor 4GI by Use of Alternate Translation Initiation Codons. Mol. Cell. Biol.
22: 4499-4511
[Abstract]
[Full Text]
-
Roy, G., De Crescenzo, G., Khaleghpour, K., Kahvejian, A., O'Connor-McCourt, M., Sonenberg, N.
(2002). Paip1 Interacts with Poly(A) Binding Protein through Two Independent Binding Motifs. Mol. Cell. Biol.
22: 3769-3782
[Abstract]
[Full Text]
-
Lachance, P. E. D., Miron, M., Raught, B., Sonenberg, N., Lasko, P.
(2002). Phosphorylation of Eukaryotic Translation Initiation Factor 4E Is Critical for Growth. Mol. Cell. Biol.
22: 1656-1663
[Abstract]
[Full Text]
-
Zamora, M., Marissen, W. E., Lloyd, R. E.
(2002). Multiple eIF4GI-Specific Protease Activities Present in Uninfected and Poliovirus-Infected Cells. J. Virol.
76: 165-177
[Abstract]
[Full Text]
-
Ventoso, I., Blanco, R., Perales, C., Carrasco, L.
(2001). HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation. Proc. Natl. Acad. Sci. USA
10.1073/pnas.231343498v1
[Abstract]
[Full Text]
-
Pestova, T. V., Kolupaeva, V. G., Lomakin, I. B., Pilipenko, E. V., Shatsky, I. N., Agol, V. I., Hellen, C. U. T.
(2001). Molecular mechanisms of translation initiation in eukaryotes. Proc. Natl. Acad. Sci. USA
98: 7029-7036
[Abstract]
[Full Text]
-
Gingras, A.-C., Raught, B., Sonenberg, N.
(2001). Regulation of translation initiation by FRAP/mTOR. Genes Dev.
15: 807-826
[Full Text]
-
Scheper, G. C., Morrice, N. A., Kleijn, M., Proud, C. G.
(2001). The Mitogen-Activated Protein Kinase Signal-Integrating Kinase Mnk2 Is a Eukaryotic Initiation Factor 4E Kinase with High Levels of Basal Activity in Mammalian Cells. Mol. Cell. Biol.
21: 743-754
[Abstract]
[Full Text]
-
ALI, I.K., JACKSON, R.J.
(2001). The Translation of Capped mRNAs Has an Absolute Requirement for the Central Domain of eIF4G but Not for the Cap-binding Initiation Factor eIF4E. Cold Spring Harb Symp Quant Biol
66: 377-388
[Abstract]
-
PESTOVA, T.V., HELLEN, C.U.T.
(2001). Functions of Eukaryotic Factors in Initiation of Translation. Cold Spring Harb Symp Quant Biol
66: 389-396
[Abstract]
-
Shah, O. J., Anthony, J. C., Kimball, S. R., Jefferson, L. S.
(2000). 4E-BP1 and S6K1: translational integration sites for nutritional and hormonal information in muscle. Am. J. Physiol. Endocrinol. Metab.
279: E715-E729
[Abstract]
[Full Text]
-
Lomakin, I. B., Hellen, C. U. T., Pestova, T. V.
(2000). Physical Association of Eukaryotic Initiation Factor 4G (eIF4G) with eIF4A Strongly Enhances Binding of eIF4G to the Internal Ribosomal Entry Site of Encephalomyocarditis Virus and Is Required for Internal Initiation of Translation. Mol. Cell. Biol.
20: 6019-6029
[Abstract]
[Full Text]
-
Pilipenko, E. V., Pestova, T. V., Kolupaeva, V. G., Khitrina, E. V., Poperechnaya, A. N., Agol, V. I., Hellen, C. U.T.
(2000). A cell cycle-dependent protein serves as a template-specific translation initiation factor. Genes Dev.
14: 2028-2045
[Abstract]
[Full Text]
-
Aravind, L., Koonin, E. V.
(2000). Eukaryote-specific Domains in Translation Initiation Factors: Implications for Translation Regulation and Evolution of the Translation System. Genome Res
10: 1172-1184
[Abstract]
[Full Text]
-
Li, W., Belsham, G. J., Proud, C. G.
(2001). Eukaryotic Initiation Factors 4A (eIF4A) and 4G (eIF4G) Mutually Interact in a 1:1 Ratio in Vivo. J. Biol. Chem.
276: 29111-29115
[Abstract]
[Full Text]
-
Korneeva, N. L., Lamphear, B. J., Hennigan, F. L. C., Merrick, W. C., Rhoads, R. E.
(2001). Characterization of the Two eIF4A-binding Sites on Human eIF4G-1. J. Biol. Chem.
276: 2872-2879
[Abstract]
[Full Text]
-
Burks, E. A., Bezerra, P. P., Le, H., Gallie, D. R., Browning, K. S.
(2001). Plant Initiation Factor 3 Subunit Composition Resembles Mammalian Initiation Factor 3 and Has a Novel Subunit. J. Biol. Chem.
276: 2122-2131
[Abstract]
[Full Text]
-
Korneeva, N. L., Lamphear, B. J., Hennigan, F. L. C., Rhoads, R. E.
(2000). Mutually Cooperative Binding of Eukaryotic Translation Initiation Factor (eIF) 3 and eIF4A to Human eIF4G-1. J. Biol. Chem.
275: 41369-41376
[Abstract]
[Full Text]
-
Ventoso, I., Blanco, R., Perales, C., Carrasco, L.
(2001). HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation. Proc. Natl. Acad. Sci. USA
98: 12966-12971
[Abstract]
[Full Text]