Previous Article | Next Article 
Molecular and Cellular Biology, July 2001, p. 4097-4109, Vol. 21, No. 13
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.13.4097-4109.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Eukaryotic Initiation Factor 4G-Poly(A) Binding Protein
Interaction Is Required for Poly(A) Tail-Mediated Stimulation of
Picornavirus Internal Ribosome Entry Segment-Driven Translation but Not
for X-Mediated Stimulation of Hepatitis C Virus
Translation
Yanne M.
Michel,
Andrew M.
Borman,
Sylvie
Paulous, and
Katherine M.
Kean*
U.P. Régulation de la Traduction
Eucaryote et Virale, CNRS URA 1966, Institut Pasteur, 75724 Paris
Cedex 15, France
Received 8 November 2000/Returned for modification 20 December
2000/Accepted 4 April 2001
Efficient translation of most eukaryotic mRNAs results from
synergistic cooperation between the 5' m7GpppN cap and the
3' poly(A) tail. In contrast to such mRNAs, the polyadenylated genomic
RNAs of picornaviruses are not capped, and translation is initiated
internally, driven by an extensive sequence termed IRES (for internal
ribosome entry segment). Here we have used our recently described
poly(A)-dependent rabbit reticulocyte lysate cell-free translation
system to study the role of mRNA polyadenylation in IRES-driven
translation. Polyadenylation significantly stimulated translation
driven by representatives of each of the three types of picornaviral
IRES (poliovirus, encephalomyocarditis virus, and hepatitis A virus,
respectively). This did not result from a poly(A)-dependent alteration
of mRNA stability in our in vitro translation system but was very
sensitive to salt concentration. Disruption of the eukaryotic
initiation factor 4G-poly(A) binding protein (eIF4G-PABP) interaction
or cleavage of eIF4G abolished or severely reduced poly(A)
tail-mediated stimulation of picornavirus IRES-driven translation. In
contrast, translation driven by the flaviviral hepatitis C virus (HCV)
IRES was not stimulated by polyadenylation but rather by the authentic
viral RNA 3' end: the highly structured X region. X region-mediated
stimulation of HCV IRES activity was not affected by disruption of the
eIF4G-PABP interaction. These data demonstrate that the protein-protein
interactions required for synergistic cooperativity on capped and
polyadenylated cellular mRNAs mediate 3'-end stimulation of
picornaviral IRES activity but not HCV IRES activity. Their
implications for the picornavirus infectious cycle and for the
increasing number of identified cellular IRES-carrying mRNAs are discussed.
*
Corresponding author. Mailing address: U.P.
Régulation de la Traduction Eucaryote et Virale, CNRS URA 1966, Institut Pasteur, 25 rue du Dr. Roux, 75724 Paris Cedex 15, France.
Phone: (33) 1-40-61-33-55. Fax: (33) 1-40-61-30-45. E-mail:
kathiemb{at}pasteur.fr.
Molecular and Cellular Biology, July 2001, p. 4097-4109, Vol. 21, No. 13
0270-7306/01/$04.00+0 DOI: 10.1128/MCB.21.13.4097-4109.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Romero-Lopez, C., Berzal-Herranz, A.
(2009). A long-range RNA-RNA interaction between the 5' and 3' ends of the HCV genome. RNA
15: 1740-1752
[Abstract]
[Full Text]
-
Bonderoff, J. M., LaRey, J. L., Lloyd, R. E.
(2008). Cleavage of Poly(A)-Binding Protein by Poliovirus 3C Proteinase Inhibits Viral Internal Ribosome Entry Site-Mediated Translation. J. Virol.
82: 9389-9399
[Abstract]
[Full Text]
-
Thoma, C., Fraterman, S., Gentzel, M., Wilm, M., Hentze, M. W.
(2008). Translation initiation by the c-myc mRNA internal ribosome entry sequence and the poly(A) tail. RNA
14: 1579-1589
[Abstract]
[Full Text]
-
Martinez-Salas, E., Pacheco, A., Serrano, P., Fernandez, N.
(2008). New insights into internal ribosome entry site elements relevant for viral gene expression. J. Gen. Virol.
89: 611-626
[Abstract]
[Full Text]
-
Svitkin, Y. V., Costa-Mattioli, M., Herdy, B., Perreault, S., Sonenberg, N.
(2007). Stimulation of picornavirus replication by the poly(A) tail in a cell-free extract is largely independent of the poly(A) binding protein (PABP). RNA
13: 2330-2340
[Abstract]
[Full Text]
-
Beauchemin, C., Laliberte, J.-F.
(2007). The Poly(A) Binding Protein Is Internalized in Virus-Induced Vesicles or Redistributed to the Nucleolus during Turnip Mosaic Virus Infection. J. Virol.
81: 10905-10913
[Abstract]
[Full Text]
-
Zhang, B., Morace, G., Gauss-Muller, V., Kusov, Y.
(2007). Poly(A) binding protein, C-terminally truncated by the hepatitis A virus proteinase 3C, inhibits viral translation. Nucleic Acids Res
35: 5975-5984
[Abstract]
[Full Text]
-
Bradrick, S. S., Dobrikova, E. Y., Kaiser, C., Shveygert, M., Gromeier, M.
(2007). Poly(A)-binding protein is differentially required for translation mediated by viral internal ribosome entry sites. RNA
13: 1582-1593
[Abstract]
[Full Text]
-
Tellinghuisen, T. L., Evans, M. J., von Hahn, T., You, S., Rice, C. M.
(2007). Studying Hepatitis C Virus: Making the Best of a Bad Virus. J. Virol.
81: 8853-8867
[Full Text]
-
Jackson, R. J., Standart, N.
(2007). How Do MicroRNAs Regulate Gene Expression?. Sci Signal
2007: re1-re1
[Abstract]
[Full Text]
-
Song, Y., Friebe, P., Tzima, E., Junemann, C., Bartenschlager, R., Niepmann, M.
(2006). The Hepatitis C Virus RNA 3'-Untranslated Region Strongly Enhances Translation Directed by the Internal Ribosome Entry Site. J. Virol.
80: 11579-11588
[Abstract]
[Full Text]
-
Castello, A., Alvarez, E., Carrasco, L.
(2006). Differential Cleavage of eIF4GI and eIF4GII in Mammalian Cells: EFFECTS ON TRANSLATION. J. Biol. Chem.
281: 33206-33216
[Abstract]
[Full Text]
-
Bradrick, S. S., Walters, R. W., Gromeier, M.
(2006). The hepatitis C virus 3'-untranslated region or a poly(A) tract promote efficient translation subsequent to the initiation phase. Nucleic Acids Res
34: 1293-1303
[Abstract]
[Full Text]
-
Johnson, R. F., Feng, M., Liu, P., Millership, J. J., Yount, B., Baric, R. S., Leibowitz, J. L.
(2005). Effect of Mutations in the Mouse Hepatitis Virus 3'(+)42 Protein Binding Element on RNA Replication. J. Virol.
79: 14570-14585
[Abstract]
[Full Text]
-
ISKEN, O., GRASSMANN, C. W., YU, H., BEHRENS, S.-E.
(2004). Complex signals in the genomic 3' nontranslated region of bovine viral diarrhea virus coordinate translation and replication of the viral RNA. RNA
10: 1637-1652
[Abstract]
[Full Text]
-
Fabian, M. R., White, K. A.
(2004). 5'-3' RNA-RNA Interaction Facilitates Cap- and Poly(A) Tail-independent Translation of Tomato Bushy Stunt Virus mRNA: A POTENTIAL COMMON MECHANISM FOR TOMBUSVIRIDAE. J. Biol. Chem.
279: 28862-28872
[Abstract]
[Full Text]
-
Cristofari, G., Ivanyi-Nagy, R., Gabus, C., Boulant, S., Lavergne, J.-P., Penin, F., Darlix, J.-L.
(2004). The hepatitis C virus Core protein is a potent nucleic acid chaperone that directs dimerization of the viral (+) strand RNA in vitro. Nucleic Acids Res
32: 2623-2631
[Abstract]
[Full Text]
-
Koloteva-Levine, N., Pinchasi, D., Pereman, I., Zur, A., Brandeis, M., Elroy-Stein, O.
(2004). The Apc5 Subunit of the Anaphase-Promoting Complex/Cyclosome Interacts with Poly(A) Binding Protein and Represses Internal Ribosome Entry Site-Mediated Translation. Mol. Cell. Biol.
24: 3577-3587
[Abstract]
[Full Text]
-
Vitour, D., Lindenbaum, P., Vende, P., Becker, M. M., Poncet, D.
(2004). RoXaN, a Novel Cellular Protein Containing TPR, LD, and Zinc Finger Motifs, Forms a Ternary Complex with Eukaryotic Initiation Factor 4G and Rotavirus NSP3. J. Virol.
78: 3851-3862
[Abstract]
[Full Text]
-
Leonard, S., Viel, C., Beauchemin, C., Daigneault, N., Fortin, M. G., Laliberte, J.-F.
(2004). Interaction of VPg-Pro of Turnip mosaic virus with the translation initiation factor 4E and the poly(A)-binding protein in planta. J. Gen. Virol.
85: 1055-1063
[Abstract]
[Full Text]
-
Dobrikova, E., Florez, P., Bradrick, S., Gromeier, M.
(2003). Activity of a type 1 picornavirus internal ribosomal entry site is determined by sequences within the 3' nontranslated region. Proc. Natl. Acad. Sci. USA
100: 15125-15130
[Abstract]
[Full Text]
-
Imbert, I., Dimitrova, M., Kien, F., Kieny, M. P., Schuster, C.
(2003). Hepatitis C virus IRES efficiency is unaffected by the genomic RNA 3'NTR even in the presence of viral structural or non-structural proteins. J. Gen. Virol.
84: 1549-1557
[Abstract]
[Full Text]
-
Paulous, S., Malnou, C. E., Michel, Y. M., Kean, K. M., Borman, A. M.
(2003). Comparison of the capacity of different viral internal ribosome entry segments to direct translation initiation in poly(A)-dependent reticulocyte lysates. Nucleic Acids Res
31: 722-733
[Abstract]
[Full Text]
-
Wang, H., Iacoangeli, A., Popp, S., Muslimov, I. A., Imataka, H., Sonenberg, N., Lomakin, I. B., Tiedge, H.
(2002). Dendritic BC1 RNA: Functional Role in Regulation of Translation Initiation. J. Neurosci.
22: 10232-10241
[Abstract]
[Full Text]
-
Kong, L. K., Sarnow, P.
(2002). Cytoplasmic Expression of mRNAs Containing the Internal Ribosome Entry Site and 3' Noncoding Region of Hepatitis C Virus: Effects of the 3' Leader on mRNA Translation and mRNA Stability. J. Virol.
76: 12457-12462
[Abstract]
[Full Text]
-
Lopez de Quinto, S., Saiz, M., de la Morena, D., Sobrino, F., Martinez-Salas, E.
(2002). IRES-driven translation is stimulated separately by the FMDV 3'-NCR and poly(A) sequences. Nucleic Acids Res
30: 4398-4405
[Abstract]
[Full Text]
-
Borman, A. M., Michel, Y. M., Malnou, C. E., Kean, K. M.
(2002). Free Poly(A) Stimulates Capped mRNA Translation in Vitro through the eIF4G-Poly(A)-binding Protein Interaction. J. Biol. Chem.
277: 36818-36824
[Abstract]
[Full Text]
-
Gauss-Muller, V., Kusov, Y. Y.
(2002). Replication of a hepatitis A virus replicon detected by genetic recombination in vivo. J. Gen. Virol.
83: 2183-2192
[Abstract]
[Full Text]
-
Leonard, S., Chisholm, J., Laliberte, J.-F., Sanfacon, H.
(2002). Interaction in vitro between the proteinase of Tomato ringspot virus (genus Nepovirus) and the eukaryotic translation initiation factor iso4E from Arabidopsis thaliana. J. Gen. Virol.
83: 2085-2089
[Abstract]
[Full Text]
-
McCormick, C. J., Rowlands, D. J., Harris, M.
(2002). Efficient delivery and regulable expression of hepatitis C virus full-length and minigenome constructs in hepatocyte-derived cell lines using baculovirus vectors. J. Gen. Virol.
83: 383-394
[Abstract]
[Full Text]
-
KIEFT, J.S., GRECH, A., ADAMS, P., DOUDNA, J.A.
(2001). Mechanisms of Internal Ribosome Entry in Translation Initiation. Cold Spring Harb Symp Quant Biol
66: 277-284
[Abstract]