This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Simpson-Holley, M.
Right arrow Articles by Knipe, D. M.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Simpson-Holley, M.
Right arrow Articles by Knipe, D. M.

 Previous Article  |  Next Article 

Journal of Virology, June 2004, p. 5591-5600, Vol. 78, No. 11
0022-538X/04/$08.00+0     DOI: 10.1128/JVI.78.11.5591-5600.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.

Herpes Simplex Virus 1 UL31 and UL34 Gene Products Promote the Late Maturation of Viral Replication Compartments to the Nuclear Periphery

Martha Simpson-Holley,1 Joel Baines,2 Richard Roller,3 and David M. Knipe1*

Department of Microbiology and Molecular Genetics, Harvard Medical School, Boston, Massachusetts 02115,1 Department of Microbiology and Immunology, Cornell University, Ithaca, New York 14853,2 Department of Microbiology, University of Iowa, Iowa City, Iowa 522423

Received 16 November 2003/ Accepted 16 January 2004

Herpes simplex virus 1 (HSV-1) forms replication compartments (RCs), domains in which viral DNA replication, late-gene transcription, and encapsidation take place, in the host cell nucleus. The formation of these domains leads to compression and marginalization of host cell chromatin, which forms a dense layer surrounding the viral RCs and constitutes a potential barrier to viral nuclear egress or primary envelopment at the inner nuclear membrane. Surrounding the chromatin layer is the nuclear lamina, a further host cell barrier to egress. In this study, we describe an additional phase in RC maturation that involves disruption of the host chromatin and nuclear lamina so that the RC can approach the nuclear envelope. During this phase, the structure of the chromatin layer is altered so that it no longer forms a continuous layer around the RCs but instead is fragmented, forming islands between which RCs extend to reach the nuclear periphery. Coincident with these changes, the nuclear lamina components lamin A/C and lamin-associated protein 2 appear to be redistributed via a mechanism involving the UL31 and UL34 gene products. Viruses in which the UL31 or UL34 gene has been deleted are unable to undergo this phase of chromatin reorganization and lamina alterations and instead form RCs which are bounded by an intact host cell chromatin layer and nuclear lamina. We postulate that these defects in chromatin restructuring and lamina reorganization explain the previously documented growth defects of these mutant viruses.

* Corresponding author. Mailing address: Department of Microbiology and Molecular Genetics, Harvard Medical School, 200 Longwood Ave., Boston, MA 02115. Phone: (617) 432-1934. Fax: (617) 432-0223. E-mail: david_knipe{at}hms.harvard.edu.

Journal of Virology, June 2004, p. 5591-5600, Vol. 78, No. 11
0022-538X/04/$08.00+0     DOI: 10.1128/JVI.78.11.5591-5600.2004
Copyright © 2004, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Wisner, T. W., Wright, C. C., Kato, A., Kawaguchi, Y., Mou, F., Baines, J. D., Roller, R. J., Johnson, D. C. (2009). Herpesvirus gB-Induced Fusion between the Virion Envelope and Outer Nuclear Membrane during Virus Egress Is Regulated by the Viral US3 Kinase. J. Virol. 83: 3115-3126 [Abstract] [Full Text]  
  • Cliffe, A. R., Nash, A. A., Dutia, B. M. (2009). Selective Uptake of Small RNA Molecules in the Virion of Murine Gammaherpesvirus 68. J. Virol. 83: 2321-2326 [Abstract] [Full Text]  
  • Cliffe, A. R., Knipe, D. M. (2008). Herpes Simplex Virus ICP0 Promotes both Histone Removal and Acetylation on Viral DNA during Lytic Infection. J. Virol. 82: 12030-12038 [Abstract] [Full Text]  
  • Nitzsche, A., Paulus, C., Nevels, M. (2008). Temporal Dynamics of Cytomegalovirus Chromatin Assembly in Productively Infected Human Cells. J. Virol. 82: 11167-11180 [Abstract] [Full Text]  
  • Hofemeister, H., O'Hare, P. (2008). Nuclear Pore Composition and Gating in Herpes Simplex Virus-Infected Cells. J. Virol. 82: 8392-8399 [Abstract] [Full Text]  
  • Conn, K. L., Hendzel, M. J., Schang, L. M. (2008). Linker Histones Are Mobilized during Infection with Herpes Simplex Virus Type 1. J. Virol. 82: 8629-8646 [Abstract] [Full Text]  
  • Mou, F., Wills, E. G., Park, R., Baines, J. D. (2008). Effects of Lamin A/C, Lamin B1, and Viral US3 Kinase Activity on Viral Infectivity, Virion Egress, and the Targeting of Herpes Simplex Virus UL34-Encoded Protein to the Inner Nuclear Membrane. J. Virol. 82: 8094-8104 [Abstract] [Full Text]  
  • Yamauchi, Y., Kiriyama, K., Kimura, H., Nishiyama, Y. (2008). Herpes simplex virus induces extensive modification and dynamic relocalisation of the nuclear mitotic apparatus (NuMA) protein in interphase cells. J. Cell Sci. 121: 2087-2096 [Abstract] [Full Text]  
  • Liang, L., Roizman, B. (2008). Expression of Gamma Interferon-Dependent Genes Is Blocked Independently by Virion Host Shutoff RNase and by US3 Protein Kinase. J. Virol. 82: 4688-4696 [Abstract] [Full Text]  
  • Bertrand, L., Pearson, A. (2008). The conserved N-terminal domain of herpes simplex virus 1 UL24 protein is sufficient to induce the spatial redistribution of nucleolin. J. Gen. Virol. 89: 1142-1151 [Abstract] [Full Text]  
  • Leach, N., Bjerke, S. L., Christensen, D. K., Bouchard, J. M., Mou, F., Park, R., Baines, J., Haraguchi, T., Roller, R. J. (2007). Emerin Is Hyperphosphorylated and Redistributed in Herpes Simplex Virus Type 1-Infected Cells in a Manner Dependent on both UL34 and US3. J. Virol. 81: 10792-10803 [Abstract] [Full Text]  
  • Mou, F., Forest, T., Baines, J. D. (2007). US3 of Herpes Simplex Virus Type 1 Encodes a Promiscuous Protein Kinase That Phosphorylates and Alters Localization of Lamin A/C in Infected Cells. J. Virol. 81: 6459-6470 [Abstract] [Full Text]  
  • Farnsworth, A., Wisner, T. W., Webb, M., Roller, R., Cohen, G., Eisenberg, R., Johnson, D. C. (2007). Herpes simplex virus glycoproteins gB and gH function in fusion between the virion envelope and the outer nuclear membrane. Proc. Natl. Acad. Sci. USA 104: 10187-10192 [Abstract] [Full Text]  
  • Morris, J. B., Hofemeister, H., O'Hare, P. (2007). Herpes Simplex Virus Infection Induces Phosphorylation and Delocalization of Emerin, a Key Inner Nuclear Membrane Protein. J. Virol. 81: 4429-4437 [Abstract] [Full Text]  
  • Baines, J. D., Hsieh, C.-E., Wills, E., Mannella, C., Marko, M. (2007). Electron Tomography of Nascent Herpes Simplex Virus Virions. J. Virol. 81: 2726-2735 [Abstract] [Full Text]  
  • Arumugaswami, V., Wu, T.-T., Martinez-Guzman, D., Jia, Q., Deng, H., Reyes, N., Sun, R. (2006). ORF18 Is a Transfactor That Is Essential for Late Gene Transcription of a Gammaherpesvirus. J. Virol. 80: 9730-9740 [Abstract] [Full Text]  
  • Remillard-Labrosse, G., Guay, G., Lippe, R. (2006). Reconstitution of Herpes Simplex Virus Type 1 Nuclear Capsid Egress In Vitro. J. Virol. 80: 9741-9753 [Abstract] [Full Text]  
  • AuCoin, D. P., Smith, G. B., Meiering, C. D., Mocarski, E. S. (2006). Betaherpesvirus-Conserved Cytomegalovirus Tegument Protein ppUL32 (pp150) Controls Cytoplasmic Events during Virion Maturation.. J. Virol. 80: 8199-8210 [Abstract] [Full Text]  
  • Wilkinson, D. E., Weller, S. K. (2006). Herpes simplex virus type I disrupts the ATR-dependent DNA-damage response during lytic infection. J. Cell Sci. 119: 2695-2703 [Abstract] [Full Text]  
  • Poon, A. P. W., Benetti, L., Roizman, B. (2006). US3 and US3.5 Protein Kinases of Herpes Simplex Virus 1 Differ with Respect to Their Functions in Blocking Apoptosis and in Virion Maturation and Egress.. J. Virol. 80: 3752-3764 [Abstract] [Full Text]  
  • Kato, A., Yamamoto, M., Ohno, T., Tanaka, M., Sata, T., Nishiyama, Y., Kawaguchi, Y. (2006). Herpes Simplex Virus 1-Encoded Protein Kinase UL13 Phosphorylates Viral Us3 Protein Kinase and Regulates Nuclear Localization of Viral Envelopment Factors UL34 and UL31. J. Virol. 80: 1476-1486 [Abstract] [Full Text]  
  • Lotzerich, M., Ruzsics, Z., Koszinowski, U. H. (2006). Functional Domains of Murine Cytomegalovirus Nuclear Egress Protein M53/p38. J. Virol. 80: 73-84 [Abstract] [Full Text]  
  • Park, R., Baines, J. D. (2006). Herpes Simplex Virus Type 1 Infection Induces Activation and Recruitment of Protein Kinase C to the Nuclear Membrane and Increased Phosphorylation of Lamin B. J. Virol. 80: 494-504 [Abstract] [Full Text]  
  • Simpson-Holley, M., Colgrove, R. C., Nalepa, G., Harper, J. W., Knipe, D. M. (2005). Identification and Functional Evaluation of Cellular and Viral Factors Involved in the Alteration of Nuclear Architecture during Herpes Simplex Virus 1 Infection. J. Virol. 79: 12840-12851 [Abstract] [Full Text]  
  • Farina, A., Feederle, R., Raffa, S., Gonnella, R., Santarelli, R., Frati, L., Angeloni, A., Torrisi, M. R., Faggioni, A., Delecluse, H.-J. (2005). BFRF1 of Epstein-Barr Virus Is Essential for Efficient Primary Viral Envelopment and Egress. J. Virol. 79: 3703-3712 [Abstract] [Full Text]  
  • Gonnella, R., Farina, A., Santarelli, R., Raffa, S., Feederle, R., Bei, R., Granato, M., Modesti, A., Frati, L., Delecluse, H.-J., Torrisi, M. R., Angeloni, A., Faggioni, A. (2005). Characterization and Intracellular Localization of the Epstein-Barr Virus Protein BFLF2: Interactions with BFRF1 and with the Nuclear Lamina. J. Virol. 79: 3713-3727 [Abstract] [Full Text]  
  • Liang, L., Baines, J. D. (2005). Identification of an Essential Domain in the Herpes Simplex Virus 1 UL34 Protein That Is Necessary and Sufficient To Interact with UL31 Protein. J. Virol. 79: 3797-3806 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»