Previous Article | Next Article 
Journal of Virology, December 2002, p. 12877-12889, Vol. 76, No. 24
0022-538X/02/$04.00+0 DOI: 10.1128/JVI.76.24.12877-12889.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
ICP27 Interacts with the RNA Export Factor Aly/REF To Direct Herpes Simplex Virus Type 1 Intronless mRNAs to the TAP Export Pathway
I-Hsiung Brandon Chen, Kathryn S. Sciabica, and Rozanne M. Sandri-Goldin*
Department of Microbiology and Molecular Genetics, College of Medicine, University of California, Irvine, California 92697-4025
Received 8 July 2002/
Accepted 9 September 2002
Herpes simplex virus type 1 (HSV-1) protein ICP27 facilitates the export of viral intronless mRNAs. ICP27 shuttles between the nucleus and cytoplasm, which has been shown to require a leucine-rich nuclear export sequence (NES). ICP27 export was reported to be sensitive to the CRM1 inhibitor leptomycin B (LMB) in HSV-1-infected cells but not in Xenopus oocytes, where ICP27 interacts with the export factor Aly/REF to access the TAP export pathway. Here, we show that ICP27 interacts with Aly/REF in HSV-1-infected mammalian cells and that Aly/REF stimulates export of viral intronless RNAs but does not cross-link to these RNAs. During infection, Aly/REF was no longer associated with splicing factor SC35 but moved into structures that colocalized with ICP27, suggesting that ICP27 recruits Aly/REF from spliceosomes to viral intronless RNAs. Further, ICP27 was found to interact in vivo with TAP but not with CRM1. In vitro export assays showed that ICP27 export was not sensitive to LMB but was blocked by a dominant-negative TAP deletion mutant lacking the nucleoporin interaction domain. These data suggest that ICP27 uses the TAP pathway to export viral RNAs. Interestingly, the leucine-rich N-terminal sequence was required for efficient export, even though ICP27 export was LMB insensitive. Thus, this region is required for efficient ICP27 export but does not function as a CRM1-dependent NES.
* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, Medical Sciences I, B240, College of Medicine, University of California, Irvine, CA 92697-4025. Phone: (949) 824-7570. Fax: (949) 824-9054. E-mail:
rmsandri{at}uci.edu.
Journal of Virology, December 2002, p. 12877-12889, Vol. 76, No. 24
0022-538X/02/$04.00+0 DOI: 10.1128/JVI.76.24.12877-12889.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.
This article has been cited by other articles:
-
Corbin-Lickfett, K. A., Chen, I-H. B., Cocco, M. J., Sandri-Goldin, R. M.
(2009). The HSV-1 ICP27 RGG box specifically binds flexible, GC-rich sequences but not G-quartet structures. Nucleic Acids Res
0: gkp793v1-gkp793
[Abstract]
[Full Text]
-
Souki, S. K., Sandri-Goldin, R. M.
(2009). Arginine Methylation of the ICP27 RGG Box Regulates the Functional Interactions of ICP27 with SRPK1 and Aly/REF during Herpes Simplex Virus 1 Infection. J. Virol.
83: 8970-8975
[Abstract]
[Full Text]
-
Ricci, E. P., Mure, F., Gruffat, H., Decimo, D., Medina-Palazon, C., Ohlmann, T., Manet, E.
(2009). Translation of intronless RNAs is strongly stimulated by the Epstein-Barr virus mRNA export factor EB2. Nucleic Acids Res
37: 4932-4943
[Abstract]
[Full Text]
-
Johnson, L. A., Li, L., Sandri-Goldin, R. M.
(2009). The Cellular RNA Export Receptor TAP/NXF1 Is Required for ICP27-Mediated Export of Herpes Simplex Virus 1 RNA, but the TREX Complex Adaptor Protein Aly/REF Appears To Be Dispensable. J. Virol.
83: 6335-6346
[Abstract]
[Full Text]
-
Colgan, K. J., Boyne, J. R., Whitehouse, A.
(2009). Uncoupling of hTREX demonstrates that UAP56 and hTHO-complex recruitment onto herpesvirus saimiri intronless transcripts is required for replication. J. Gen. Virol.
90: 1455-1460
[Abstract]
[Full Text]
-
Souki, S. K., Gershon, P. D., Sandri-Goldin, R. M.
(2009). Arginine Methylation of the ICP27 RGG Box Regulates ICP27 Export and Is Required for Efficient Herpes Simplex Virus 1 Replication. J. Virol.
83: 5309-5320
[Abstract]
[Full Text]
-
Gillis, P. A., Okagaki, L. H., Rice, S. A.
(2009). Herpes Simplex Virus Type 1 ICP27 Induces p38 Mitogen-Activated Protein Kinase Signaling and Apoptosis in HeLa Cells. J. Virol.
83: 1767-1777
[Abstract]
[Full Text]
-
Johnson, L. A., Sandri-Goldin, R. M.
(2009). Efficient Nuclear Export of Herpes Simplex Virus 1 Transcripts Requires both RNA Binding by ICP27 and ICP27 Interaction with TAP/NXF1. J. Virol.
83: 1184-1192
[Abstract]
[Full Text]
-
Schneider, J., Dauber, B., Melen, K., Julkunen, I., Wolff, T.
(2009). Analysis of Influenza B Virus NS1 Protein Trafficking Reveals a Novel Interaction with Nuclear Speckle Domains. J. Virol.
83: 701-711
[Abstract]
[Full Text]
-
Duffy, C., Mbong, E. F., Baines, J. D.
(2009). VP22 of Herpes Simplex Virus 1 Promotes Protein Synthesis at Late Times in Infection and Accumulation of a Subset of Viral mRNAs at Early Times in Infection. J. Virol.
83: 1009-1017
[Abstract]
[Full Text]
-
Wang, W., Cui, Z.-Q., Han, H., Zhang, Z.-P., Wei, H.-P., Zhou, Y.-F., Chen, Z., Zhang, X.-E.
(2008). Imaging and characterizing influenza A virus mRNA transport in living cells. Nucleic Acids Res
36: 4913-4928
[Abstract]
[Full Text]
-
Sedlackova, L., Perkins, K. D., Lengyel, J., Strain, A. K., van Santen, V. L., Rice, S. A.
(2008). Herpes Simplex Virus Type 1 ICP27 Regulates Expression of a Variant, Secreted Form of Glycoprotein C by an Intron Retention Mechanism. J. Virol.
82: 7443-7455
[Abstract]
[Full Text]
-
Fontaine-Rodriguez, E. C., Knipe, D. M.
(2008). Herpes Simplex Virus ICP27 Increases Translation of a Subset of Viral Late mRNAs. J. Virol.
82: 3538-3545
[Abstract]
[Full Text]
-
Majerciak, V., Yamanegi, K., Allemand, E., Kruhlak, M., Krainer, A. R., Zheng, Z.-M.
(2008). Kaposi's Sarcoma-Associated Herpesvirus ORF57 Functions as a Viral Splicing Factor and Promotes Expression of Intron-Containing Viral Lytic Genes in Spliceosome-Mediated RNA Splicing. J. Virol.
82: 2792-2801
[Abstract]
[Full Text]
-
Nekorchuk, M., Han, Z., Hsieh, T.-T., Swaminathan, S.
(2007). Kaposi's Sarcoma-Associated Herpesvirus ORF57 Protein Enhances mRNA Accumulation Independently of Effects on Nuclear RNA Export. J. Virol.
81: 9990-9998
[Abstract]
[Full Text]
-
Nojima, T., Hirose, T., Kimura, H., Hagiwara, M.
(2007). The Interaction between Cap-binding Complex and RNA Export Factor Is Required for Intronless mRNA Export. J. Biol. Chem.
282: 15645-15651
[Abstract]
[Full Text]
-
Han, Z., Marendy, E., Wang, Y.-D., Yuan, J., Sample, J. T., Swaminathan, S.
(2007). Multiple Roles of Epstein-Barr Virus SM Protein in Lytic Replication. J. Virol.
81: 4058-4069
[Abstract]
[Full Text]
-
Donnelly, M., Verhagen, J., Elliott, G.
(2007). RNA Binding by the Herpes Simplex Virus Type 1 Nucleocytoplasmic Shuttling Protein UL47 Is Mediated by an N-Terminal Arginine-Rich Domain That Also Functions as Its Nuclear Localization Signal. J. Virol.
81: 2283-2296
[Abstract]
[Full Text]
-
Hargett, D., Rice, S., Bachenheimer, S. L.
(2006). Herpes Simplex Virus Type 1 ICP27-Dependent Activation of NF-{kappa}B. J. Virol.
80: 10565-10578
[Abstract]
[Full Text]
-
Corcoran, J. A., Hsu, W.-L., Smiley, J. R.
(2006). Herpes Simplex Virus ICP27 Is Required for Virus-Induced Stabilization of the ARE-Containing IEX-1 mRNA Encoded by the Human IER3 Gene. J. Virol.
80: 9720-9729
[Abstract]
[Full Text]
-
Han, Z., Swaminathan, S.
(2006). Kaposi's Sarcoma-Associated Herpesvirus Lytic Gene ORF57 Is Essential for Infectious Virion Production.. J. Virol.
80: 5251-5260
[Abstract]
[Full Text]
-
Sanchez, V., Spector, D. H.
(2006). Cyclin-Dependent Kinase Activity Is Required for Efficient Expression and Posttranslational Modification of Human Cytomegalovirus Proteins and for Production of Extracellular Particles.. J. Virol.
80: 5886-5896
[Abstract]
[Full Text]
-
Dai-Ju, J. Q., Li, L., Johnson, L. A., Sandri-Goldin, R. M.
(2006). ICP27 Interacts with the C-Terminal Domain of RNA Polymerase II and Facilitates Its Recruitment to Herpes Simplex Virus 1 Transcription Sites, Where It Undergoes Proteasomal Degradation during Infection.. J. Virol.
80: 3567-3581
[Abstract]
[Full Text]
-
Lischka, P., Toth, Z., Thomas, M., Mueller, R., Stamminger, T.
(2006). The UL69 Transactivator Protein of Human Cytomegalovirus Interacts with DEXD/H-Box RNA Helicase UAP56 To Promote Cytoplasmic Accumulation of Unspliced RNA.. Mol. Cell. Biol.
26: 1631-1643
[Abstract]
[Full Text]
-
Toth, Z., Lischka, P., Stamminger, T.
(2006). RNA-binding of the human cytomegalovirus transactivator protein UL69, mediated by arginine-rich motifs, is not required for nuclear export of unspliced RNA. Nucleic Acids Res
34: 1237-1249
[Abstract]
[Full Text]
-
Larralde, O., Smith, R. W. P., Wilkie, G. S., Malik, P., Gray, N. K., Clements, J. B.
(2006). Direct Stimulation of Translation by the Multifunctional Herpesvirus ICP27 Protein. J. Virol.
80: 1588-1591
[Abstract]
[Full Text]
-
Guang, S., Felthauser, A. M., Mertz, J. E.
(2005). Binding of hnRNP L to the Pre-mRNA Processing Enhancer of the Herpes Simplex Virus Thymidine Kinase Gene Enhances both Polyadenylation and Nucleocytoplasmic Export of Intronless mRNAs. Mol. Cell. Biol.
25: 6303-6313
[Abstract]
[Full Text]
-
Hargett, D., McLean, T., Bachenheimer, S. L.
(2005). Herpes Simplex Virus ICP27 Activation of Stress Kinases JNK and p38. J. Virol.
79: 8348-8360
[Abstract]
[Full Text]
-
Chen, I-H. B., Li, L., Silva, L., Sandri-Goldin, R. M.
(2005). ICP27 Recruits Aly/REF but Not TAP/NXF1 to Herpes Simplex Virus Type 1 Transcription Sites although TAP/NXF1 Is Required for ICP27 Export. J. Virol.
79: 3949-3961
[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]
-
Uhrig, J. F., Canto, T., Marshall, D., MacFarlane, S. A.
(2004). Relocalization of Nuclear ALY Proteins to the Cytoplasm by the Tomato Bushy Stunt Virus P19 Pathogenicity Protein. Plant Physiol.
135: 2411-2423
[Abstract]
[Full Text]
-
Malik, P., Blackbourn, D. J., Clements, J. B.
(2004). The Evolutionarily Conserved Kaposi's Sarcoma-associated Herpesvirus ORF57 Protein Interacts with REF Protein and Acts as an RNA Export Factor. J. Biol. Chem.
279: 33001-33011
[Abstract]
[Full Text]
-
Sandri-Goldin, R. M.
(2004). Viral Regulation of mRNA Export. J. Virol.
78: 4389-4396
[Full Text]
-
Pearson, A., Knipe, D. M., Coen, D. M.
(2004). ICP27 Selectively Regulates the Cytoplasmic Localization of a Subset of Viral Transcripts in Herpes Simplex Virus Type 1-Infected Cells. J. Virol.
78: 23-32
[Abstract]
[Full Text]
-
Perkins, K. D., Gregonis, J., Borge, S., Rice, S. A.
(2003). Transactivation of a Viral Target Gene by Herpes Simplex Virus ICP27 Is Posttranscriptional and Does Not Require the Endogenous Promoter or Polyadenylation Site. J. Virol.
77: 9872-9884
[Abstract]
[Full Text]
-
Sokolowski, M., Scott, J. E., Heaney, R. P., Patel, A. H., Clements, J. B.
(2003). Identification of Herpes Simplex Virus RNAs That Interact Specifically with Regulatory Protein ICP27 in Vivo. J. Biol. Chem.
278: 33540-33549
[Abstract]
[Full Text]