Previous Article | Next Article 
Journal of Virology, August 2000, p. 7064-7071, Vol. 74, No. 15
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Efficient Translation of Rotavirus mRNA Requires Simultaneous
Interaction of NSP3 with the Eukaryotic Translation Initiation
Factor eIF4G and the mRNA 3' End
Patrice
Vende,
Maria
Piron,
Nathalie
Castagné, and
Didier
Poncet*
Laboratoire de Virologie et Immunologie
Moléculaires INRA, C.R.J.J., 78352 Jouy-en-Josas Cedex,
France
Received 17 February 2000/Accepted 5 May 2000
In contrast to the vast majority of cellular proteins, rotavirus
proteins are translated from capped but nonpolyadenylated mRNAs. The viral nonstructural protein NSP3 specifically
binds the 3'-end consensus sequence of viral mRNAs and
interacts with the eukaryotic translation initiation factor eIF4G. Here
we show that expression of NSP3 in mammalian cells allows the efficient translation of virus-like mRNA. A synergistic effect between
the cap structure and the 3' end of rotavirus mRNA was
observed in NSP3-expressing cells. The enhancement of viral
mRNA translation by NSP3 was also observed in a rabbit
reticulocyte lysate translation system supplemented with recombinant
NSP3. The use of NSP3 mutants indicates that its RNA- and eIF4G-binding
domains are both required to enhance the translation of viral
mRNA. The results reported here show that NSP3 forms a link
between viral mRNA and the cellular translation machinery and
hence is a functional analogue of cellular poly(A)-binding protein.
*
Corresponding author. Mailing address: Laboratoire de
Virologie et Immunologie Moléculaires INRA, C.R.J.J., Domaine de
Vilvert, 78352 Jouy-en-Josas Cedex, France. Phone: 33-(0)1 34 65 26 11. Fax: 33-(0)1 34 65 26 21. E-mail:
poncet{at}biotec.jouy.inra.fr.

Present address: Laboratory of Infectious Diseases, National
Institute of Allergy and Infectious Diseases, National Institutes
of Health, Bethesda, MD
20892.

Present address: Medicina Interna-Hepatologia, Hospitals Generals
Vall d'Hebron, 08035 Barcelona,
Spain.
Journal of Virology, August 2000, p. 7064-7071, Vol. 74, No. 15
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Blakqori, G., van Knippenberg, I., Elliott, R. M.
(2009). Bunyamwera Orthobunyavirus S-Segment Untranslated Regions Mediate Poly(A) Tail-Independent Translation. J. Virol.
83: 3637-3646
[Abstract]
[Full Text]
-
Polacek, C., Friebe, P., Harris, E.
(2009). Poly(A)-binding protein binds to the non-polyadenylated 3' untranslated region of dengue virus and modulates translation efficiency. J. Gen. Virol.
90: 687-692
[Abstract]
[Full Text]
-
Harb, M., Becker, M. M., Vitour, D., Baron, C. H., Vende, P., Brown, S. C., Bolte, S., Arold, S. T., Poncet, D.
(2008). Nuclear Localization of Cytoplasmic Poly(A)-Binding Protein upon Rotavirus Infection Involves the Interaction of NSP3 with eIF4G and RoXaN. J. Virol.
82: 11283-11293
[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]
-
Cakmakci, N. G., Lerner, R. S., Wagner, E. J., Zheng, L., Marzluff, W. F.
(2008). SLIP1, a Factor Required for Activation of Histone mRNA Translation by the Stem-Loop Binding Protein. Mol. Cell. Biol.
28: 1182-1194
[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]
-
Whitlow, Z. W., Connor, J. H., Lyles, D. S.
(2006). Preferential Translation of Vesicular Stomatitis Virus mRNAs Is Conferred by Transcription from the Viral Genome. J. Virol.
80: 11733-11742
[Abstract]
[Full Text]
-
Serrano, P., Pulido, M. R., Saiz, M., Martinez-Salas, E.
(2006). The 3' end of the foot-and-mouth disease virus genome establishes two distinct long-range RNA-RNA interactions with the 5' end region.. J. Gen. Virol.
87: 3013-3022
[Abstract]
[Full Text]
-
Montero, H., Arias, C. F., Lopez, S.
(2006). Rotavirus Nonstructural Protein NSP3 Is Not Required for Viral Protein Synthesis.. J. Virol.
80: 9031-9038
[Abstract]
[Full Text]
-
LeFebvre, A. K., Korneeva, N. L., Trutschl, M., Cvek, U., Duzan, R. D., Bradley, C. A., Hershey, J. W. B., Rhoads, R. E.
(2006). Translation Initiation Factor eIF4G-1 Binds to eIF3 through the eIF3e Subunit. J. Biol. Chem.
281: 22917-22932
[Abstract]
[Full Text]
-
Thivierge, K., Nicaise, V., Dufresne, P. J., Cotton, S., Laliberte, J.-F., Le Gall, O., Fortin, M. G.
(2005). Plant Virus RNAs. Coordinated Recruitment of Conserved Host Functions by (+) ssRNA Viruses during Early Infection Events. Plant Physiol.
138: 1822-1827
[Abstract]
[Full Text]
-
Chiu, W.-W., Kinney, R. M., Dreher, T. W.
(2005). Control of Translation by the 5'- and 3'-Terminal Regions of the Dengue Virus Genome. J. Virol.
79: 8303-8315
[Abstract]
[Full Text]
-
Krab, I. M., Caldwell, C., Gallie, D. R., Bol, J. F.
(2005). Coat protein enhances translational efficiency of Alfalfa mosaic virus RNAs and interacts with the eIF4G component of initiation factor eIF4F. J. Gen. Virol.
86: 1841-1849
[Abstract]
[Full Text]
-
Alvarez, D. E., Lodeiro, M. F., Luduena, S. J., Pietrasanta, L. I., Gamarnik, A. V.
(2005). Long-Range RNA-RNA Interactions Circularize the Dengue Virus Genome. J. Virol.
79: 6631-6643
[Abstract]
[Full Text]
-
Smith, J. A., Schmechel, S. C., Williams, B. R. G., Silverman, R. H., Schiff, L. A.
(2005). Involvement of the Interferon-Regulated Antiviral Proteins PKR and RNase L in Reovirus-Induced Shutoff of Cellular Translation. J. Virol.
79: 2240-2250
[Abstract]
[Full Text]
-
Matsuda, D., Bauer, L., Tinnesand, K., Dreher, T. W.
(2004). Expression of the Two Nested Overlapping Reading Frames of Turnip Yellow Mosaic Virus RNA Is Enhanced by a 5' Cap and by 5' and 3' Viral Sequences. J. Virol.
78: 9325-9335
[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]
-
Neeleman, L., Linthorst, H. J. M., Bol, J. F.
(2004). Efficient translation of alfamovirus RNAs requires the binding of coat protein dimers to the 3' termini of the viral RNAs. J. Gen. Virol.
85: 231-240
[Abstract]
[Full Text]
-
Burgui, I., Aragon, T., Ortin, J., Nieto, A.
(2003). PABP1 and eIF4GI associate with influenza virus NS1 protein in viral mRNA translation initiation complexes. J. Gen. Virol.
84: 3263-3274
[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]
-
Mitzel, D. N., Weisend, C. M., White, M. W., Hardy, M. E.
(2003). Translational regulation of rotavirus gene expression. J. Gen. Virol.
84: 383-391
[Abstract]
[Full Text]
-
Sanchez, R., Marzluff, W. F.
(2002). The Stem-Loop Binding Protein Is Required for Efficient Translation of Histone mRNA In Vivo and In Vitro. Mol. Cell. Biol.
22: 7093-7104
[Abstract]
[Full Text]
-
Bushell, M., Sarnow, P.
(2002). Hijacking the translation apparatus by RNA viruses. JCB
158: 395-399
[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]
-
Mossel, E. C., Ramig, R. F.
(2002). Rotavirus Genome Segment 7 (NSP3) Is a Determinant of Extraintestinal Spread in the Neonatal Mouse. J. Virol.
76: 6502-6509
[Abstract]
[Full Text]
-
Zeenko, V. V., Ryabova, L. A., Spirin, A. S., Rothnie, H. M., Hess, D., Browning, K. S., Hohn, T.
(2002). Eukaryotic Elongation Factor 1A Interacts with the Upstream Pseudoknot Domain in the 3' Untranslated Region of Tobacco Mosaic Virus RNA. J. Virol.
76: 5678-5691
[Abstract]
[Full Text]
-
Neeleman, L., Olsthoorn, R. C. L., Linthorst, H. J. M., Bol, J. F.
(2001). Translation of a nonpolyadenylated viral RNA is enhanced by binding of viral coat protein or polyadenylation of the RNA. Proc. Natl. Acad. Sci. USA
10.1073/pnas.251542798v1
[Abstract]
[Full Text]
-
Patton, J. T., Taraporewala, Z., Chen, D., Chizhikov, V., Jones, M., Elhelu, A., Collins, M., Kearney, K., Wagner, M., Hoshino, Y., Gouvea, V.
(2001). Effect of Intragenic Rearrangement and Changes in the 3' Consensus Sequence on NSP1 Expression and Rotavirus Replication. J. Virol.
75: 2076-2086
[Abstract]
[Full Text]
-
Thole, V., Garcia, M.-L., van Rossum, C. M. A., Neeleman, L., Brederode, F. T., Linthorst, H. J. M., Bol, J. F.
(2001). RNAs 1 and 2 of Alfalfa mosaic virus, expressed in transgenic plants, start to replicate only after infection of the plants with RNA 3. J. Gen. Virol.
82: 25-28
[Abstract]
[Full Text]
-
KAHVEJIAN, A., ROY, G., SONENBERG, N.
(2001). The mRNA Closed-loop Model: The Function of PABP and PABP-interacting Proteins in mRNA Translation. Cold Spring Harb Symp Quant Biol
66: 293-300
[Abstract]
-
Schuck, P., Taraporewala, Z., McPhie, P., Patton, J. T.
(2001). Rotavirus Nonstructural Protein NSP2 Self-assembles into Octamers That Undergo Ligand-induced Conformational Changes. J. Biol. Chem.
276: 9679-9687
[Abstract]
[Full Text]
-
Neeleman, L., Olsthoorn, R. C. L., Linthorst, H. J. M., Bol, J. F.
(2001). Translation of a nonpolyadenylated viral RNA is enhanced by binding of viral coat protein or polyadenylation of the RNA. Proc. Natl. Acad. Sci. USA
98: 14286-14291
[Abstract]
[Full Text]