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 Miranda-Saksena, M.
Right arrow Articles by Cunningham, A. L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Miranda-Saksena, M.
Right arrow Articles by Cunningham, A. L.

 Previous Article  |  Next Article 

Journal of Virology, February 2000, p. 1827-1839, Vol. 74, No. 4
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Anterograde Transport of Herpes Simplex Virus Type 1 in Cultured, Dissociated Human and Rat Dorsal Root Ganglion Neurons

Monica Miranda-Saksena,1 Patricia Armati,2 Ross A. Boadle,3 David J. Holland,1 and Anthony L. Cunningham1,*

Centre for Virus Research, Westmead Millennium Institute, Westmead Hospital and University of Sydney,1 and Westmead Millennium Institute & Electron Microscope Laboratory, ICPMR, Westmead Hospital,3 Westmead, New South Wales 2145, and School of Biological Sciences, University of Sydney, Camperdown, New South Wales 2050,2 Australia

Received 21 June 1999/Accepted 10 November 1999

The mechanism of anterograde transport of herpes simplex virus was studied in cultured dissociated human and rat dorsal root ganglion neurons. The neurons were infected with HSV-1 to examine the distribution of capsid (VP5), tegument (VP16), and glycoproteins (gC and gB) at 2, 6, 10, 13, 17, and 24 h postinfection (p.i.) with or without nocodazole (a microtubule depolymerizer) or brefeldin A (a Golgi inhibitor). Retrogradely transported VP5 was detected in the cytoplasm of the cell body up to the nuclear membrane at 2 h p.i. It was first detected de novo in the nucleus and cytoplasm at 10 h p.i., the axon hillock at 13 h p.i., and the axon at 15 to 17 h p.i. gC and gB were first detected de novo in the cytoplasm and the axon hillock at 10 h p.i. and then in the axon at 13 h p.i., which was always earlier than the detection of VP5. De novo-synthesized VP16 was first detected in the cytoplasm at 10 to 13 h p.i. and in the axon at 16 to 17 h p.i. Nocodazole inhibited the transport of all antigens, VP5, VP16, and gC or gB. The kinetics of inhibition of VP5 and gC could be dissociated. Brefeldin A inhibited the transport of gC or gB and VP16 but not VP5 into axons. Transmission immunoelectron microscopy confirmed that there were unenveloped nucleocapsids in the axon with or without brefeldin A. These findings demonstrate that glycoproteins and capsids, associated with tegument proteins, are transported by different pathways with slightly differing kinetics from the nucleus to the axon. Furthermore, axonal anterograde transport of the nucleocapsid can proceed despite the loss of most VP16.

* Corresponding author. Mailing address: Centre for Virus Research, Westmead Millennium Institute, Westmead Hospital and University of Sydney, Westmead, New South Wales 2145, Australia. Phone: (61) 29845 6344. Fax: (61) 29845 8300. E-mail: tonyc{at}westgate.wh.usyd.edu.au.

Journal of Virology, February 2000, p. 1827-1839, Vol. 74, No. 4
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Honda, T., Horie, M., Daito, T., Ikuta, K., Tomonaga, K. (2009). Molecular Chaperone BiP Interacts with Borna Disease Virus Glycoprotein at the Cell Surface. J. Virol. 83: 12622-12625 [Abstract] [Full Text]  
  • Miranda-Saksena, M., Boadle, R. A., Aggarwal, A., Tijono, B., Rixon, F. J., Diefenbach, R. J., Cunningham, A. L. (2009). Herpes Simplex Virus Utilizes the Large Secretory Vesicle Pathway for Anterograde Transport of Tegument and Envelope Proteins and for Viral Exocytosis from Growth Cones of Human Fetal Axons. J. Virol. 83: 3187-3199 [Abstract] [Full Text]  
  • Lyman, M. G., Enquist, L. W. (2009). Herpesvirus Interactions with the Host Cytoskeleton. J. Virol. 83: 2058-2066 [Full Text]  
  • Snyder, A., Polcicova, K., Johnson, D. C. (2008). Herpes Simplex Virus gE/gI and US9 Proteins Promote Transport of both Capsids and Virion Glycoproteins in Neuronal Axons. J. Virol. 82: 10613-10624 [Abstract] [Full Text]  
  • Shanda, S. K., Wilson, D. W. (2008). UL36p Is Required for Efficient Transport of Membrane-Associated Herpes Simplex Virus Type 1 along Microtubules. J. Virol. 82: 7388-7394 [Abstract] [Full Text]  
  • Ch'ng, T. H., Spear, P. G., Struyf, F., Enquist, L. W. (2007). Glycoprotein D-Independent Spread of Pseudorabies Virus Infection in Cultured Peripheral Nervous System Neurons in a Compartmented System. J. Virol. 81: 10742-10757 [Abstract] [Full Text]  
  • Fang, M., Dai, X., Theilmann, D. A. (2007). Autographa californica Multiple Nucleopolyhedrovirus EXON0 (ORF141) Is Required for Efficient Egress of Nucleocapsids from the Nucleus. J. Virol. 81: 9859-9869 [Abstract] [Full Text]  
  • Snyder, A., Bruun, B., Browne, H. M., Johnson, D. C. (2007). A Herpes Simplex Virus gD-YFP Fusion Glycoprotein Is Transported Separately from Viral Capsids in Neuronal Axons. J. Virol. 81: 8337-8340 [Abstract] [Full Text]  
  • Snyder, A., Wisner, T. W., Johnson, D. C. (2006). Herpes Simplex Virus Capsids Are Transported in Neuronal Axons without an Envelope Containing the Viral Glycoproteins. J. Virol. 80: 11165-11177 [Abstract] [Full Text]  
  • Antinone, S. E., Smith, G. A. (2006). Two Modes of Herpesvirus Trafficking in Neurons: Membrane Acquisition Directs Motion. J. Virol. 80: 11235-11240 [Abstract] [Full Text]  
  • Satpute-Krishnan, P., DeGiorgis, J. A., Conley, M. P., Jang, M., Bearer, E. L. (2006). A peptide zipcode sufficient for anterograde transport within amyloid precursor protein. Proc. Natl. Acad. Sci. USA 103: 16532-16537 [Abstract] [Full Text]  
  • Lee, G. E., Murray, J. W., Wolkoff, A. W., Wilson, D. W. (2006). Reconstitution of Herpes Simplex Virus Microtubule-Dependent Trafficking In Vitro. J. Virol. 80: 4264-4275 [Abstract] [Full Text]  
  • Saksena, M. M., Wakisaka, H., Tijono, B., Boadle, R. A., Rixon, F., Takahashi, H., Cunningham, A. L. (2006). Herpes simplex virus type 1 accumulation, envelopment, and exit in growth cones and varicosities in mid-distal regions of axons.. J. Virol. 80: 3592-3606 [Abstract] [Full Text]  
  • Hood, C., Cunningham, A. L., Slobedman, B., Arvin, A. M., Sommer, M. H., Kinchington, P. R., Abendroth, A. (2006). Varicella-Zoster Virus ORF63 Inhibits Apoptosis of Primary Human Neurons. J. Virol. 80: 1025-1031 [Abstract] [Full Text]  
  • Luxton, G. W. G., Lee, J. I-H., Haverlock-Moyns, S., Schober, J. M., Smith, G. A. (2006). The Pseudorabies Virus VP1/2 Tegument Protein Is Required for Intracellular Capsid Transport. J. Virol. 80: 201-209 [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]  
  • Pomeranz, L. E., Reynolds, A. E., Hengartner, C. J. (2005). Molecular Biology of Pseudorabies Virus: Impact on Neurovirology and Veterinary Medicine. Microbiol. Mol. Biol. Rev. 69: 462-500 [Abstract] [Full Text]  
  • LaVail, J. H., Tauscher, A. N., Hicks, J. W., Harrabi, O., Melroe, G. T., Knipe, D. M. (2005). Genetic and Molecular In Vivo Analysis of Herpes Simplex Virus Assembly in Murine Visual System Neurons. J. Virol. 79: 11142-11150 [Abstract] [Full Text]  
  • Decman, V., Kinchington, P. R., Harvey, S. A. K., Hendricks, R. L. (2005). Gamma Interferon Can Block Herpes Simplex Virus Type 1 Reactivation from Latency, Even in the Presence of Late Gene Expression. J. Virol. 79: 10339-10347 [Abstract] [Full Text]  
  • Ch'ng, T. H., Enquist, L. W. (2005). Efficient Axonal Localization of Alphaherpesvirus Structural Proteins in Cultured Sympathetic Neurons Requires Viral Glycoprotein E. J. Virol. 79: 8835-8846 [Abstract] [Full Text]  
  • Turcotte, S., Letellier, J., Lippe, R. (2005). Herpes Simplex Virus Type 1 Capsids Transit by the trans-Golgi Network, Where Viral Glycoproteins Accumulate Independently of Capsid Egress. J. Virol. 79: 8847-8860 [Abstract] [Full Text]  
  • Luxton, G. W. G., Haverlock, S., Coller, K. E., Antinone, S. E., Pincetic, A., Smith, G. A. (2005). From the Cover: Targeting of herpesvirus capsid transport in axons is coupled to association with specific sets of tegument proteins. Proc. Natl. Acad. Sci. USA 102: 5832-5837 [Abstract] [Full Text]  
  • del Rio, T., Ch'ng, T. H., Flood, E. A., Gross, S. P., Enquist, L. W. (2005). Heterogeneity of a Fluorescent Tegument Component in Single Pseudorabies Virus Virions and Enveloped Axonal Assemblies. J. Virol. 79: 3903-3919 [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]  
  • Bosnjak, L., Miranda-Saksena, M., Koelle, D. M., Boadle, R. A., Jones, C. A., Cunningham, A. L. (2005). Herpes Simplex Virus Infection of Human Dendritic Cells Induces Apoptosis and Allows Cross-Presentation via Uninfected Dendritic Cells. J. Immunol. 174: 2220-2227 [Abstract] [Full Text]  
  • Smith, G. A., Pomeranz, L., Gross, S. P., Enquist, L. W. (2004). Local modulation of plus-end transport targets herpesvirus entry and egress in sensory axons. Proc. Natl. Acad. Sci. USA 101: 16034-16039 [Abstract] [Full Text]  
  • Douglas, M. W., Diefenbach, R. J., Homa, F. L., Miranda-Saksena, M., Rixon, F. J., Vittone, V., Byth, K., Cunningham, A. L. (2004). Herpes Simplex Virus Type 1 Capsid Protein VP26 Interacts with Dynein Light Chains RP3 and Tctex1 and Plays a Role in Retrograde Cellular Transport. J. Biol. Chem. 279: 28522-28530 [Abstract] [Full Text]  
  • Hood, C., Cunningham, A. L., Slobedman, B., Boadle, R. A., Abendroth, A. (2003). Varicella-Zoster Virus-Infected Human Sensory Neurons Are Resistant to Apoptosis, yet Human Foreskin Fibroblasts Are Susceptible: Evidence for a Cell-Type-Specific Apoptotic Response. J. Virol. 77: 12852-12864 [Abstract] [Full Text]  
  • Bajramovic, J. J., Munter, S., Syan, S., Nehrbass, U., Brahic, M., Gonzalez-Dunia, D. (2003). Borna Disease Virus Glycoprotein Is Required for Viral Dissemination in Neurons. J. Virol. 77: 12222-12231 [Abstract] [Full Text]  
  • Jones, C. A., Fernandez, M., Herc, K., Bosnjak, L., Miranda-Saksena, M., Boadle, R. A., Cunningham, A. (2003). Herpes Simplex Virus Type 2 Induces Rapid Cell Death and Functional Impairment of Murine Dendritic Cells In Vitro. J. Virol. 77: 11139-11149 [Abstract] [Full Text]  
  • Potel, C., Kaelin, K., Danglot, L., Triller, A., Vannier, C., Rozenberg, F. (2003). Herpes simplex virus type 1 glycoprotein B sorting in hippocampal neurons. J. Gen. Virol. 84: 2613-2624 [Abstract] [Full Text]  
  • LaVail, J. H., Tauscher, A. N., Aghaian, E., Harrabi, O., Sidhu, S. S. (2003). Axonal Transport and Sorting of Herpes Simplex Virus Components in a Mature Mouse Visual System. J. Virol. 77: 6117-6126 [Abstract] [Full Text]  
  • Koelle, D. M., Corey, L. (2003). Recent Progress in Herpes Simplex Virus Immunobiology and Vaccine Research. Clin. Microbiol. Rev. 16: 96-113 [Abstract] [Full Text]  
  • Miranda-Saksena, M., Boadle, R. A., Armati, P., Cunningham, A. L. (2002). In Rat Dorsal Root Ganglion Neurons, Herpes Simplex Virus Type 1 Tegument Forms in the Cytoplasm of the Cell Body. J. Virol. 76: 9934-9951 [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]  
  • Tomishima, M. J., Enquist, L. W. (2002). In Vivo Egress of an Alphaherpesvirus from Axons. J. Virol. 76: 8310-8317 [Abstract] [Full Text]  
  • Koshizuka, T., Goshima, F., Takakuwa, H., Nozawa, N., Daikoku, T., Koiwai, O., Nishiyama, Y. (2002). Identification and Characterization of the UL56 Gene Product of Herpes Simplex Virus Type 2. J. Virol. 76: 6718-6728 [Abstract] [Full Text]  
  • Chowdhury, S. I., Onderci, M., Bhattacharjee, P. S., Al-Mubarak, A., Weiss, M. L., Zhou, Y. (2002). Bovine Herpesvirus 5 (BHV-5) Us9 Is Essential for BHV-5 Neuropathogenesis. J. Virol. 76: 3839-3851 [Abstract] [Full Text]  
  • Diefenbach, R. J., Miranda-Saksena, M., Diefenbach, E., Holland, D. J., Boadle, R. A., Armati, P. J., Cunningham, A. L. (2002). Herpes Simplex Virus Tegument Protein US11 Interacts with Conventional Kinesin Heavy Chain. J. Virol. 76: 3282-3291 [Abstract] [Full Text]  
  • van Leeuwen, H., Elliott, G., O'Hare, P. (2002). Evidence of a Role for Nonmuscle Myosin II in Herpes Simplex Virus Type 1 Egress. J. Virol. 76: 3471-3481 [Abstract] [Full Text]  
  • Mikloska, Z., Cunningham, A. L. (2001). Alpha and Gamma Interferons Inhibit Herpes Simplex Virus Type 1 Infection and Spread in Epidermal Cells after Axonal Transmission. J. Virol. 75: 11821-11826 [Abstract] [Full Text]  
  • Dasgupta, A., Wilson, D. W. (2001). Evaluation of the primary effect of brefeldin A treatment upon herpes simplex virus assembly. J. Gen. Virol. 82: 1561-1567 [Abstract] [Full Text]  
  • Skepper, J. N., Whiteley, A., Browne, H., Minson, A. (2001). Herpes Simplex Virus Nucleocapsids Mature to Progeny Virions by an Envelopment {right-arrow} Deenvelopment {right-arrow} Reenvelopment Pathway. J. Virol. 75: 5697-5702 [Abstract] [Full Text]  
  • Harley, C. A., Dasgupta, A., Wilson, D. W. (2001). Characterization of Herpes Simplex Virus-Containing Organelles by Subcellular Fractionation: Role for Organelle Acidification in Assembly of Infectious Particles. J. Virol. 75: 1236-1251 [Abstract] [Full Text]  
  • Saldanha, C. E., Lubinski, J., Martin, C., Nagashunmugam, T., Wang, L., van der Keyl, H., Tal-Singer, R., Friedman, H. M. (2000). Herpes Simplex Virus Type 1 Glycoprotein E Domains Involved in Virus Spread and Disease. J. Virol. 74: 6712-6719 [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»