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 Elliott, G.
Right arrow Articles by O'Hare, P.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Elliott, G.
Right arrow Articles by O'Hare, P.

 Previous Article  |  Next Article 

J Virol, August 1998, p. 6448-6455, Vol. 72, No. 8
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.

Herpes Simplex Virus Type 1 Tegument Protein VP22 Induces the Stabilization and Hyperacetylation of Microtubules

Gillian Elliott* and Peter O'Hare

Marie Curie Research Institute, Oxted, Surrey RH8 OTL, United Kingdom

Received 27 March 1998/Accepted 5 May 1998

The role of the herpes simplex virus type 1 tegument protein VP22 during infection is as yet undefined. We have previously shown that VP22 has the unusual property of efficient intercellular transport, such that the protein spreads from single expressing cells into large numbers of surrounding cells. We also noted that in cells expressing VP22 by transient transfection, the protein localizes in a distinctive cytoplasmic filamentous pattern. Here we show that this pattern represents a colocalization between VP22 and cellular microtubules. Moreover, we show that VP22 reorganizes microtubules into thick bundles which are easily distinguishable from nonbundled microtubules. These bundles are highly resistant to microtubule-depolymerizing agents such as nocodazole and incubation at 4°C, suggesting that VP22 has the capacity to stabilize the microtubule network. In addition, we show that the microtubules contained in these bundles are modified by acetylation, a marker for microtubule stability. Analysis of infected cells by both immunofluorescence and measurement of microtubule acetylation further showed that colocalization between VP22 and microtubules, and induction of microtubule acetylation, also occurs during infection. Taken together, these results suggest that VP22 exhibits the properties of a classical microtubule-associated protein (MAP) during both transfection and infection. This is the first demonstration of a MAP encoded by an animal virus.

* Corresponding author. Mailing address: Marie Curie Research Institute, The Chart, Oxted, Surrey RH8 OTL, United Kingdom. Phone: 1883 722306. Fax: 1883 714375. E-mail: g.elliott{at}mcri.ac.uk.

J Virol, August 1998, p. 6448-6455, Vol. 72, No. 8
0022-538X/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Stylianou, J., Maringer, K., Cook, R., Bernard, E., Elliott, G. (2009). Virion Incorporation of the Herpes Simplex Virus Type 1 Tegument Protein VP22 Occurs via Glycoprotein E-Specific Recruitment to the Late Secretory Pathway. J. Virol. 83: 5204-5218 [Abstract] [Full Text]  
  • Roohvand, F., Maillard, P., Lavergne, J.-P., Boulant, S., Walic, M., Andreo, U., Goueslain, L., Helle, F., Mallet, A., McLauchlan, J., Budkowska, A. (2009). Initiation of Hepatitis C Virus Infection Requires the Dynamic Microtubule Network: ROLE OF THE VIRAL NUCLEOCAPSID PROTEIN. J. Biol. Chem. 284: 13778-13791 [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]  
  • Nagel, C.-H., Dohner, K., Fathollahy, M., Strive, T., Borst, E. M., Messerle, M., Sodeik, B. (2008). Nuclear Egress and Envelopment of Herpes Simplex Virus Capsids Analyzed with Dual-Color Fluorescence HSV1(17+). J. Virol. 82: 3109-3124 [Abstract] [Full Text]  
  • Vanover, J., Sun, J., Deka, S., Kintner, J., Duffourc, M. M., Schoborg, R. V. (2008). Herpes simplex virus co-infection-induced Chlamydia trachomatis persistence is not mediated by any known persistence inducer or anti-chlamydial pathway. Microbiology 154: 971-978 [Abstract] [Full Text]  
  • Lin, S.-F., Gao, S. P., Price, D. L., Li, S., Chou, T.-C., Singh, P., Huang, Y.-Y., Fong, Y., Wong, R. J. (2008). Synergy of a Herpes Oncolytic Virus and Paclitaxel for Anaplastic Thyroid Cancer. Clin. Cancer Res. 14: 1519-1528 [Abstract] [Full Text]  
  • Sciortino, M. T., Taddeo, B., Giuffre-Cuculletto, M., Medici, M. A., Mastino, A., Roizman, B. (2007). Replication-Competent Herpes Simplex Virus 1 Isolates Selected from Cells Transfected with a Bacterial Artificial Chromosome DNA Lacking Only the UL49 Gene Vary with Respect to the Defect in the UL41 Gene Encoding Host Shutoff RNase. J. Virol. 81: 10924-10932 [Abstract] [Full Text]  
  • Cilloniz, C., Jackson, W., Grose, C., Czechowski, D., Hay, J., Ruyechan, W. T. (2007). The Varicella-Zoster Virus (VZV) ORF9 Protein Interacts with the IE62 Major VZV Transactivator. J. Virol. 81: 761-774 [Abstract] [Full Text]  
  • Duffy, C., LaVail, J. H., Tauscher, A. N., Wills, E. G., Blaho, J. A., Baines, J. D. (2006). Characterization of a UL49-Null Mutant: VP22 of Herpes Simplex Virus Type 1 Facilitates Viral Spread in Cultured Cells and the Mouse Cornea.. J. Virol. 80: 8664-8675 [Abstract] [Full Text]  
  • Warren, J. C., Rutkowski, A., Cassimeris, L. (2006). Infection with Replication-deficient Adenovirus Induces Changes in the Dynamic Instability of Host Cell Microtubules. Mol. Biol. Cell 17: 3557-3568 [Abstract] [Full Text]  
  • Potel, C., Elliott, G. (2005). Phosphorylation of the Herpes Simplex Virus Tegument Protein VP22 Has No Effect on Incorporation of VP22 into the Virus but Is Involved in Optimal Expression and Virion Packaging of ICP0. J. Virol. 79: 14057-14068 [Abstract] [Full Text]  
  • Hafezi, W., Bernard, E., Cook, R., Elliott, G. (2005). Herpes Simplex Virus Tegument Protein VP22 Contains an Internal VP16 Interaction Domain and a C-Terminal Domain That Are Both Required for VP22 Assembly into the Virus Particle. J. Virol. 79: 13082-13093 [Abstract] [Full Text]  
  • Mouzakitis, G., McLauchlan, J., Barreca, C., Kueltzo, L., O'Hare, P. (2005). Characterization of VP22 in Herpes Simplex Virus-Infected Cells. J. Virol. 79: 12185-12198 [Abstract] [Full Text]  
  • Elliott, G., Hafezi, W., Whiteley, A., Bernard, E. (2005). Deletion of the Herpes Simplex Virus VP22-Encoding Gene (UL49) Alters the Expression, Localization, and Virion Incorporation of ICP0. J. Virol. 79: 9735-9745 [Abstract] [Full Text]  
  • del Rio, T., DeCoste, C. J., Enquist, L.W. (2005). Actin Is a Component of the Compensation Mechanism in Pseudorabies Virus Virions Lacking the Major Tegument Protein VP22. J. Virol. 79: 8614-8619 [Abstract] [Full Text]  
  • Ruthel, G., Demmin, G. L., Kallstrom, G., Javid, M. P., Badie, S. S., Will, A. B., Nelle, T., Schokman, R., Nguyen, T. L., Carra, J. H., Bavari, S., Aman, M. J. (2005). Association of Ebola Virus Matrix Protein VP40 with Microtubules. J. Virol. 79: 4709-4719 [Abstract] [Full Text]  
  • Yedowitz, J. C., Kotsakis, A., Schlegel, E. F. M., Blaho, J. A. (2005). Nuclear Localizations of the Herpes Simplex Virus Type 1 Tegument Proteins VP13/14, vhs, and VP16 Precede VP22-Dependent Microtubule Reorganization and VP22 Nuclear Import. J. Virol. 79: 4730-4743 [Abstract] [Full Text]  
  • Pyka, J., Glogowska, A., Dralle, H., Hoang-Vu, C., Klonisch, T. (2005). Cytoplasmic Domain of proEGF Affects Distribution and Post-Translational Modification of Microtubuli and Increases Microtubule-Associated Proteins 1b and 2 Production in Human Thyroid Carcinoma Cells. Cancer Res. 65: 1343-1351 [Abstract] [Full Text]  
  • Naranatt, P. P., Krishnan, H. H., Smith, M. S., Chandran, B. (2005). Kaposi's Sarcoma-Associated Herpesvirus Modulates Microtubule Dynamics via RhoA-GTP-Diaphanous 2 Signaling and Utilizes the Dynein Motors To Deliver Its DNA to the Nucleus. J. Virol. 79: 1191-1206 [Abstract] [Full Text]  
  • Jouvenet, N., Monaghan, P., Way, M., Wileman, T. (2004). Transport of African Swine Fever Virus from Assembly Sites to the Plasma Membrane Is Dependent on Microtubules and Conventional Kinesin. J. Virol. 78: 7990-8001 [Abstract] [Full Text]  
  • Chiou, C.-T., Hu, C.-C. A., Chen, P.-H., Liao, C.-L., Lin, Y.-L., Wang, J.-J. (2003). Association of Japanese encephalitis virus NS3 protein with microtubules and tumour susceptibility gene 101 (TSG101) protein. J. Gen. Virol. 84: 2795-2805 [Abstract] [Full Text]  
  • van Leeuwen, H., Okuwaki, M., Hong, R., Chakravarti, D., Nagata, K., O'Hare, P. (2003). Herpes simplex virus type 1 tegument protein VP22 interacts with TAF-I proteins and inhibits nucleosome assembly but not regulation of histone acetylation by INHAT. J. Gen. Virol. 84: 2501-2510 [Abstract] [Full Text]  
  • Brignati, M. J., Loomis, J. S., Wills, J. W., Courtney, R. J. (2003). Membrane Association of VP22, a Herpes Simplex Virus Type 1 Tegument Protein. J. Virol. 77: 4888-4898 [Abstract] [Full Text]  
  • Hutchinson, I., Whiteley, A., Browne, H., Elliott, G. (2002). Sequential Localization of Two Herpes Simplex Virus Tegument Proteins to Punctate Nuclear Dots Adjacent to ICP0 Domains. J. Virol. 76: 10365-10373 [Abstract] [Full Text]  
  • Dohner, K., Wolfstein, A., Prank, U., Echeverri, C., Dujardin, D., Vallee, R., Sodeik, B. (2002). Function of Dynein and Dynactin in Herpes Simplex Virus Capsid Transport. Mol. Biol. Cell 13: 2795-2809 [Abstract] [Full Text]  
  • Martin, A., O'Hare, P., McLauchlan, J., Elliott, G. (2002). Herpes Simplex Virus Tegument Protein VP22 Contains Overlapping Domains for Cytoplasmic Localization, Microtubule Interaction, and Chromatin Binding. J. Virol. 76: 4961-4970 [Abstract] [Full Text]  
  • Willard, M. (2002). Rapid Directional Translocations in Virus Replication. J. Virol. 76: 5220-5232 [Abstract] [Full Text]  
  • Parker, J. S. L., Broering, T. J., Kim, J., Higgins, D. E., Nibert, M. L. (2002). Reovirus Core Protein {micro}2 Determines the Filamentous Morphology of Viral Inclusion Bodies by Interacting with and Stabilizing Microtubules. J. Virol. 76: 4483-4496 [Abstract] [Full Text]  
  • del Rio, T., Werner, H. C., Enquist, L. W. (2002). The Pseudorabies Virus VP22 Homologue (UL49) Is Dispensable for Virus Growth In Vitro and Has No Effect on Virulence and Neuronal Spread in Rodents. J. Virol. 76: 774-782 [Abstract] [Full Text]  
  • Geiss, B. J., Tavis, J. E., Metzger, L. M., Leib, D. A., Morrison, L. A. (2001). Temporal Regulation of Herpes Simplex Virus Type 2 VP22 Expression and Phosphorylation. J. Virol. 75: 10721-10729 [Abstract] [Full Text]  
  • Ren, X., Harms, J. S., Splitter, G. A. (2001). Tyrosine Phosphorylation of Bovine Herpesvirus 1 Tegument Protein VP22 Correlates with the Incorporation of VP22 into Virions. J. Virol. 75: 9010-9017 [Abstract] [Full Text]  
  • Kotsakis, A., Pomeranz, L. E., Blouin, A., Blaho, J. A. (2001). Microtubule Reorganization during Herpes Simplex Virus Type 1 Infection Facilitates the Nuclear Localization of VP22, a Major Virion Tegument Protein. J. Virol. 75: 8697-8711 [Abstract] [Full Text]  
  • Mossman, K. L., Macgregor, P. F., Rozmus, J. J., Goryachev, A. B., Edwards, A. M., Smiley, J. R. (2001). Herpes Simplex Virus Triggers and Then Disarms a Host Antiviral Response. J. Virol. 75: 750-758 [Abstract] [Full Text]  
  • Cho, E., Park, J., Yoo, O., Kim, K. (2001). Translocation and accumulation of exogeneous hepatitis B virus preS surface proteins in the cell nucleus. J. Cell Sci. 114: 1115-1123 [Abstract]  
  • Zhang, M., Zeng, C. Q.-Y., Morris, A. P., Estes, M. K. (2000). A Functional NSP4 Enterotoxin Peptide Secreted from Rotavirus-Infected Cells. J. Virol. 74: 11663-11670 [Abstract] [Full Text]  
  • Pomeranz, L. E., Blaho, J. A. (2000). Assembly of Infectious Herpes Simplex Virus Type 1 Virions in the Absence of Full-Length VP22. J. Virol. 74: 10041-10054 [Abstract] [Full Text]  
  • Lai, Z., Han, I., Zirzow, G., Brady, R. O., Reiser, J. (2000). Intercellular delivery of a herpes simplex virus VP22 fusion protein from cells infected with lentiviral vectors. Proc. Natl. Acad. Sci. USA 97: 11297-11302 [Abstract] [Full Text]  
  • Dorange, F., El Mehdaoui, S., Pichon, C., Coursaget, P., Vautherot, J.-F. (2000). Marek's disease virus (MDV) homologues of herpes simplex virus type 1 UL49 (VP22) and UL48 (VP16) genes: high-level expression and characterization of MDV-1 VP22 and VP16. J. Gen. Virol. 81: 2219-2230 [Abstract] [Full Text]  
  • Harms, J. S., Ren, X., Oliveira, S. C., Splitter, G. A. (2000). Distinctions between Bovine Herpesvirus 1 and Herpes Simplex Virus Type 1 VP22 Tegument Protein Subcellular Associations. J. Virol. 74: 3301-3312 [Abstract] [Full Text]  
  • Elliott, G., O'Hare, P. (2000). Cytoplasm-to-Nucleus Translocation of a Herpesvirus Tegument Protein during Cell Division. J. Virol. 74: 2131-2141 [Abstract] [Full Text]  
  • Brewis, N., Phelan, A., Webb, J., Drew, J., Elliott, G., O'Hare, P. (2000). Evaluation of VP22 Spread in Tissue Culture. J. Virol. 74: 1051-1056 [Abstract] [Full Text]  
  • Pomeranz, L. E., Blaho, J. A. (1999). Modified VP22 Localizes to the Cell Nucleus during Synchronized Herpes Simplex Virus Type 1 Infection. J. Virol. 73: 6769-6781 [Abstract] [Full Text]  
  • Elliott, G., O'Reilly, D., O'Hare, P. (1999). Identification of Phosphorylation Sites within the Herpes Simplex Virus Tegument Protein VP22. J. Virol. 73: 6203-6206 [Abstract] [Full Text]  
  • Elliott, G., O'Hare, P. (1999). Live-Cell Analysis of a Green Fluorescent Protein-Tagged Herpes Simplex Virus Infection. J. Virol. 73: 4110-4119 [Abstract] [Full Text]  
  • Kueltzo, L. A., Normand, N., O'Hare, P., Middaugh, C. R. (2000). Conformational Lability of Herpesvirus Protein VP22. J. Biol. Chem. 275: 33213-33221 [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»