Next Article 
Microbiology and Molecular Biology Reviews, June 2000, p. 239-280, Vol. 64, No. 2
1092-2172/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Translational Control of Viral Gene Expression
in Eukaryotes
Michael
Gale Jr.,1,*
Seng-Lai
Tan,2 and
Michael G.
Katze2
University of Texas Southwestern Medical
Center, Dallas, Texas,1 and
University of Washington, Seattle, Washington2
As obligate intracellular parasites, viruses rely exclusively on the translational machinery of the host cell for the synthesis of viral proteins. This relationship has imposed numerous challenges on both the infecting virus and the host cell. Importantly, viruses must compete with the endogenous transcripts of the host cell for the translation of viral mRNA. Eukaryotic viruses have thus evolved diverse mechanisms to ensure translational efficiency of viral mRNA above and beyond that of cellular mRNA. Mechanisms that facilitate the efficient and selective translation of viral mRNA may be inherent in the structure of the viral nucleic acid itself and can involve the recruitment and/or modification of specific host factors. These processes serve to redirect the translation apparatus to favor viral transcripts, and they often come at the expense of the host cell. Accordingly, eukaryotic cells have developed antiviral countermeasures to target the translational machinery and disrupt protein synthesis during the course of virus infection. Not to be outdone, many viruses have answered these countermeasures with their own mechanisms to disrupt cellular antiviral pathways, thereby ensuring the uncompromised translation of virion proteins. Here we review the varied and complex translational programs employed by eukaryotic viruses. We discuss how these translational strategies have been incorporated into the virus life cycle and examine how such programming contributes to the pathogenesis of the host cell.
*
Corresponding author. Mailing address: Department of
Microbiology, University of Texas Southwestern Medical Center, 5323 Harry Hines Blvd., Dallas, TX 75390-9048. Phone: (214) 648-5940. Fax: (214) 648-5905. E-mail: mgale{at}mednet.swmed.edu.
Microbiology and Molecular Biology Reviews, June 2000, p. 239-280, Vol. 64, No. 2
1092-2172/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Abrahamyan, L. G., Chatel-Chaix, L., Ajamian, L., Milev, M. P., Monette, A., Clement, J.-F., Song, R., Lehmann, M., DesGroseillers, L., Laughrea, M., Boccaccio, G., Mouland, A. J.
(2010). Novel Staufen1 ribonucleoproteins prevent formation of stress granules but favour encapsidation of HIV-1 genomic RNA. J. Cell Sci.
123: 369-383
[Abstract]
[Full Text]
-
Wang, X., Liao, Y., Yap, P. L., Png, K. J., Tam, J. P., Liu, D. X.
(2009). Inhibition of Protein Kinase R Activation and Upregulation of GADD34 Expression Play a Synergistic Role in Facilitating Coronavirus Replication by Maintaining De Novo Protein Synthesis in Virus-Infected Cells. J. Virol.
83: 12462-12472
[Abstract]
[Full Text]
-
Wylie, K. M., Schrimpf, J. E., Morrison, L. A.
(2009). Increased eIF2{alpha} Phosphorylation Attenuates Replication of Herpes Simplex Virus 2 vhs Mutants in Mouse Embryonic Fibroblasts and Correlates with Reduced Accumulation of the PKR Antagonist ICP34.5. J. Virol.
83: 9151-9162
[Abstract]
[Full Text]
-
Daher, A., Laraki, G., Singh, M., Melendez-Pena, C. E., Bannwarth, S., Peters, A. H. F. M., Meurs, E. F., Braun, R. E., Patel, R. C., Gatignol, A.
(2009). TRBP Control of PACT-Induced Phosphorylation of Protein Kinase R Is Reversed by Stress. Mol. Cell. Biol.
29: 254-265
[Abstract]
[Full Text]
-
Powell, M. L., Napthine, S., Jackson, R. J., Brierley, I., Brown, T. D. K.
(2008). Characterization of the termination-reinitiation strategy employed in the expression of influenza B virus BM2 protein. RNA
14: 2394-2406
[Abstract]
[Full Text]
-
Ricci, E. P., Herbreteau, C. H., Decimo, D., Schaupp, A., Datta, S. A.K., Rein, A., Darlix, J.-L., Ohlmann, T.
(2008). In vitro expression of the HIV-2 genomic RNA is controlled by three distinct internal ribosome entry segments that are regulated by the HIV protease and the Gag polyprotein. RNA
14: 1443-1455
[Abstract]
[Full Text]
-
Yeam, I., Cavatorta, J. R., Ripoll, D. R., Kang, B.-C., Jahn, M. M.
(2007). Functional Dissection of Naturally Occurring Amino Acid Substitutions in eIF4E That Confers Recessive Potyvirus Resistance in Plants. Plant Cell
19: 2913-2928
[Abstract]
[Full Text]
-
Assenberg, R., Ren, J., Verma, A., Walter, T. S., Alderton, D., Hurrelbrink, R. J., Fuller, S. D., Bressanelli, S., Owens, R. J., Stuart, D. I., Grimes, J. M.
(2007). Crystal structure of the Murray Valley encephalitis virus NS5 methyltransferase domain in complex with cap analogues. J. Gen. Virol.
88: 2228-2236
[Abstract]
[Full Text]
-
Chan, E. Y., Qian, W.-J., Diamond, D. L., Liu, T., Gritsenko, M. A., Monroe, M. E., Camp, D. G. II, Smith, R. D., Katze, M. G.
(2007). Quantitative Analysis of Human Immunodeficiency Virus Type 1-Infected CD4+ Cell Proteome: Dysregulated Cell Cycle Progression and Nuclear Transport Coincide with Robust Virus Production. J. Virol.
81: 7571-7583
[Abstract]
[Full Text]
-
Sanz, M. A., Castello, A., Carrasco, L.
(2007). Viral Translation Is Coupled to Transcription in Sindbis Virus-Infected Cells. J. Virol.
81: 7061-7068
[Abstract]
[Full Text]
-
Anderson, J. L., Johnson, A. T., Howard, J. L., Purcell, D. F. J.
(2007). Both Linear and Discontinuous Ribosome Scanning Are Used for Translation Initiation from Bicistronic Human Immunodeficiency Virus Type 1 env mRNAs. J. Virol.
81: 4664-4676
[Abstract]
[Full Text]
-
Yi, G., Gopinath, K., Kao, C. C.
(2007). Selective Repression of Translation by the Brome Mosaic Virus 1a RNA Replication Protein. J. Virol.
81: 1601-1609
[Abstract]
[Full Text]
-
Nakatsu, Y., Takeda, M., Ohno, S., Koga, R., Yanagi, Y.
(2006). Translational Inhibition and Increased Interferon Induction in Cells Infected with C Protein-Deficient Measles Virus. J. Virol.
80: 11861-11867
[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]
-
Khan, M. A., Miyoshi, H., Ray, S., Natsuaki, T., Suehiro, N., Goss, D. J.
(2006). Interaction of Genome-linked Protein (VPg) of Turnip Mosaic Virus with Wheat Germ Translation Initiation Factors eIFiso4E and eIFiso4F. J. Biol. Chem.
281: 28002-28010
[Abstract]
[Full Text]
-
Edgil, D., Polacek, C., Harris, E.
(2006). Dengue Virus Utilizes a Novel Strategy for Translation Initiation When Cap-Dependent Translation Is Inhibited. J. Virol.
80: 2976-2986
[Abstract]
[Full Text]
-
Takeda, M., Ohno, S., Seki, F., Nakatsu, Y., Tahara, M., Yanagi, Y.
(2005). Long Untranslated Regions of the Measles Virus M and F Genes Control Virus Replication and Cytopathogenicity. J. Virol.
79: 14346-14354
[Abstract]
[Full Text]
-
McInerney, G. M., Kedersha, N. L., Kaufman, R. J., Anderson, P., Liljestrom, P.
(2005). Importance of eIF2{alpha} Phosphorylation and Stress Granule Assembly in Alphavirus Translation Regulation. Mol. Biol. Cell
16: 3753-3763
[Abstract]
[Full Text]
-
Santi, N., Song, H., Vakharia, V. N., Evensen, O.
(2005). Infectious Pancreatic Necrosis Virus VP5 Is Dispensable for Virulence and Persistence. J. Virol.
79: 9206-9216
[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]
-
Yu, Y., Kudchodkar, S. B., Alwine, J. C.
(2005). Effects of Simian Virus 40 Large and Small Tumor Antigens on Mammalian Target of Rapamycin Signaling: Small Tumor Antigen Mediates Hypophosphorylation of eIF4E-Binding Protein 1 Late in Infection. J. Virol.
79: 6882-6889
[Abstract]
[Full Text]
-
Deas, T. S., Binduga-Gajewska, I., Tilgner, M., Ren, P., Stein, D. A., Moulton, H. M., Iversen, P. L., Kauffman, E. B., Kramer, L. D., Shi, P.-Y.
(2005). Inhibition of Flavivirus Infections by Antisense Oligomers Specifically Suppressing Viral Translation and RNA Replication. J. Virol.
79: 4599-4609
[Abstract]
[Full Text]
-
Connor, J. H., Lyles, D. S.
(2005). Inhibition of Host and Viral Translation during Vesicular Stomatitis Virus Infection: eIF2 IS RESPONSIBLE FOR THE INHIBITION OF VIRAL BUT NOT HOST TRANSLATION. J. Biol. Chem.
280: 13512-13519
[Abstract]
[Full Text]
-
Ellison, K. S., Maranchuk, R. A., Mottet, K. L., Smiley, J. R.
(2005). Control of VP16 Translation by the Herpes Simplex Virus Type 1 Immediate-Early Protein ICP27. J. Virol.
79: 4120-4131
[Abstract]
[Full Text]
-
Chen, A., Kao, Y. F., Brown, C. M.
(2005). Translation of the first upstream ORF in the hepatitis B virus pregenomic RNA modulates translation at the core and polymerase initiation codons. Nucleic Acids Res
33: 1169-1181
[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]
-
Tatsuta, M., Mizumoto, H., Kaido, M., Mise, K., Okuno, T.
(2005). The Red Clover Necrotic Mosaic Virus RNA2 trans-Activator Is Also a cis-Acting RNA2 Replication Element. J. Virol.
79: 978-986
[Abstract]
[Full Text]
-
Sen, N., Cao, F., Tavis, J. E.
(2004). Translation of Duck Hepatitis B Virus Reverse Transcriptase by Ribosomal Shunting. J. Virol.
78: 11751-11757
[Abstract]
[Full Text]
-
tenOever, B. R., Sharma, S., Zou, W., Sun, Q., Grandvaux, N., Julkunen, I., Hemmi, H., Yamamoto, M., Akira, S., Yeh, W.-C., Lin, R., Hiscott, J.
(2004). Activation of TBK1 and IKK{varepsilon} Kinases by Vesicular Stomatitis Virus Infection and the Role of Viral Ribonucleoprotein in the Development of Interferon Antiviral Immunity. J. Virol.
78: 10636-10649
[Abstract]
[Full Text]
-
Guenther, R. H., Sit, T. L., Gracz, H. S., Dolan, M. A., Townsend, H. L., Liu, G., Newman, W. H., Agris, P. F., Lommel, S. A.
(2004). Structural characterization of an intermolecular RNA-RNA interaction involved in the transcription regulation element of a bipartite plant virus. Nucleic Acids Res
32: 2819-2828
[Abstract]
[Full Text]
-
de Breyne, S., Monney, R. S., Curran, J.
(2004). Proteolytic Processing and Translation Initiation: TWO INDEPENDENT MECHANISMS FOR THE EXPRESSION OF THE SENDAI VIRUS Y PROTEINS. J. Biol. Chem.
279: 16571-16580
[Abstract]
[Full Text]
-
Kazemi, S., Papadopoulou, S., Li, S., Su, Q., Wang, S., Yoshimura, A., Matlashewski, G., Dever, T. E., Koromilas, A. E.
(2004). Control of {alpha} Subunit of Eukaryotic Translation Initiation Factor 2 (eIF2{alpha}) Phosphorylation by the Human Papillomavirus Type 18 E6 Oncoprotein: Implications for eIF2{alpha}-Dependent Gene Expression and Cell Death. Mol. Cell. Biol.
24: 3415-3429
[Abstract]
[Full Text]
-
Gazo, B. M., Murphy, P., Gatchel, J. R., Browning, K. S.
(2004). A Novel Interaction of Cap-binding Protein Complexes Eukaryotic Initiation Factor (eIF) 4F and eIF(iso)4F with a Region in the 3'-Untranslated Region of Satellite Tobacco Necrosis Virus. J. Biol. Chem.
279: 13584-13592
[Abstract]
[Full Text]
-
VAN EDEN, M. E., BYRD, M. P., SHERRILL, K. W., LLOYD, R. E.
(2004). Demonstrating internal ribosome entry sites in eukaryotic mRNAs using stringent RNA test procedures. RNA
10: 720-730
[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]
-
VAN EDEN, M. E., BYRD, M. P., SHERRILL, K. W., LLOYD, R. E.
(2004). Translation of cellular inhibitor of apoptosis protein 1 (c-IAP1) mRNA is IRES mediated and regulated during cell stress. RNA
10: 469-481
[Abstract]
[Full Text]
-
RONFORT, C., DE BREYNE, S., SANDRIN, V., DARLIX, J.-L., OHLMANN, T.
(2004). Characterization of two distinct RNA domains that regulate translation of the Drosophila gypsy retroelement. RNA
10: 504-515
[Abstract]
[Full Text]
-
Das, S., Ward, S. V., Markle, D., Samuel, C. E.
(2004). DNA Damage-binding Proteins and Heterogeneous Nuclear Ribonucleoprotein A1 Function as Constitutive KCS Element Components of the Interferon-inducible RNA-dependent Protein Kinase Promoter. J. Biol. Chem.
279: 7313-7321
[Abstract]
[Full Text]
-
Boot, H. J., Pritz-Verschuren, S. B. E.
(2004). Modifications of the 3'-UTR stem-loop of infectious bursal disease virus are allowed without influencing replication or virulence. Nucleic Acids Res
32: 211-222
[Abstract]
[Full Text]
-
Bink, H. H. J., Schirawski, J., Haenni, A.-L., Pleij, C. W. A.
(2003). The 5'-Proximal Hairpin of Turnip Yellow Mosaic Virus RNA: Its Role in Translation and Encapsidation. J. Virol.
77: 7452-7458
[Abstract]
[Full Text]
-
He, Y., Yan, W., Coito, C., Li, Y., Gale, M. Jr, Katze, M. G.
(2003). The regulation of hepatitis C virus (HCV) internal ribosome-entry site-mediated translation by HCV replicons and nonstructural proteins. J. Gen. Virol.
84: 535-543
[Abstract]
[Full Text]
-
de Breyne, S., Simonet, V., Pelet, T., Curran, J.
(2003). Identification of a cis-acting element required for shunt-mediated translational initiation of the Sendai virus Y proteins. Nucleic Acids Res
31: 608-618
[Abstract]
[Full Text]
-
Han, B., Zhang, J.-T.
(2002). Regulation of Gene Expression by Internal Ribosome Entry Sites or Cryptic Promoters: the eIF4G Story. Mol. Cell. Biol.
22: 7372-7384
[Abstract]
[Full Text]
-
Connor, J. H., Lyles, D. S.
(2002). Vesicular Stomatitis Virus Infection Alters the eIF4F Translation Initiation Complex and Causes Dephosphorylation of the eIF4E Binding Protein 4E-BP1. J. Virol.
76: 10177-10187
[Abstract]
[Full Text]
-
Kash, J. C., Cunningham, D. M., Smit, M. W., Park, Y., Fritz, D., Wilusz, J., Katze, M. G.
(2002). Selective Translation of Eukaryotic mRNAs: Functional Molecular Analysis of GRSF-1, a Positive Regulator of Influenza Virus Protein Synthesis. J. Virol.
76: 10417-10426
[Abstract]
[Full Text]
-
Mahalingam, S., Meanger, J., Foster, P. S., Lidbury, B. A.
(2002). The viral manipulation of the host cellular and immune environments to enhance propagation and survival: a focus on RNA viruses. J. Leukoc. Biol.
72: 429-439
[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]
-
Dorokhov, Y. L., Skulachev, M. V., Ivanov, P. A., Zvereva, S. D., Tjulkina, L. G., Merits, A., Gleba, Y. Y., Hohn, T., Atabekov, J. G.
(2002). Polypurine (A)-rich sequences promote cross-kingdom conservation of internal ribosome entry. Proc. Natl. Acad. Sci. USA
99: 5301-5306
[Abstract]
[Full Text]
-
Koh, D. C.-Y., Liu, D. X., Wong, S.-M.
(2002). A Six-Nucleotide Segment within the 3' Untranslated Region of Hibiscus Chlorotic Ringspot Virus Plays an Essential Role in Translational Enhancement. J. Virol.
76: 1144-1153
[Abstract]
[Full Text]
-
Salvatore, M., Basler, C. F., Parisien, J.-P., Horvath, C. M., Bourmakina, S., Zheng, H., Muster, T., Palese, P., Garcia-Sastre, A.
(2002). Effects of Influenza A Virus NS1 Protein on Protein Expression: the NS1 Protein Enhances Translation and Is Not Required for Shutoff of Host Protein Synthesis. J. Virol.
76: 1206-1212
[Abstract]
[Full Text]
-
Schneider, R., Kozak, M.
(2001). New Ways of Initiating Translation in Eukaryotes?. Mol. Cell. Biol.
21: 8238-8246
[Full Text]
-
Samuel, C. E.
(2001). Antiviral Actions of Interferons. Clin. Microbiol. Rev.
14: 778-809
[Abstract]
[Full Text]
-
Keene, J. D.
(2001). Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. USA
98: 7018-7024
[Abstract]
[Full Text]
-
He, Y., Tan, S.-L., Tareen, S. U., Vijaysri, S., Langland, J. O., Jacobs, B. L., Katze, M. G.
(2001). Regulation of mRNA Translation and Cellular Signaling by Hepatitis C Virus Nonstructural Protein NS5A. J. Virol.
75: 5090-5098
[Abstract]
[Full Text]
-
Zhao, W. D., Wimmer, E.
(2001). Genetic Analysis of a Poliovirus/Hepatitis C Virus Chimera: New Structure for Domain II of the Internal Ribosomal Entry Site of Hepatitis C Virus. J. Virol.
75: 3719-3730
[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]
-
Daher, A., Longuet, M., Dorin, D., Bois, F., Segeral, E., Bannwarth, S., Battisti, P.-L., Purcell, D. F., Benarous, R., Vaquero, C., Meurs, E. F., Gatignol, A.
(2001). Two Dimerization Domains in the Trans-activation Response RNA-binding Protein (TRBP) Individually Reverse the Protein Kinase R Inhibition of HIV-1 Long Terminal Repeat Expression. J. Biol. Chem.
276: 33899-33905
[Abstract]
[Full Text]