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 Brideau, A. D.
Right arrow Articles by Enquist, L. W.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Brideau, A. D.
Right arrow Articles by Enquist, L. W.

 Previous Article  |  Next Article 

Journal of Virology, May 2000, p. 4549-4561, Vol. 74, No. 10
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Directional Transneuronal Infection by Pseudorabies Virus Is Dependent on an Acidic Internalization Motif in the Us9 Cytoplasmic Tail

Amy D. Brideau, Marlies G. Eldridge, and Lynn W. Enquist*

Department of Molecular Biology, Princeton University, Princeton, New Jersey 08544

Received 12 November 1999/Accepted 24 February 2000

The Us9 gene is conserved among most alphaherpesviruses. In pseudorabies virus (PRV), the Us9 protein is a 98-amino-acid, type II membrane protein found in the virion envelope. It localizes to the trans-Golgi network (TGN) region in infected and transfected cells and is maintained in this compartment by endocytosis from the plasma membrane. Viruses with Us9 deleted have no observable defects in tissue culture yet have reduced virulence and restricted spread to retinorecipient neurons in the rodent brain. In this report, we demonstrate that Us9-promoted transneuronal spread in vivo is dependent on a conserved acidic motif previously shown to be essential for the maintenance of Us9 in the TGN region and recycling from the plasma membrane. Mutant viruses with the acidic motif deleted have an anterograde spread defect indistinguishable from that of Us9 null viruses. Transneuronal spread, however, is not dependent on a dileucine endocytosis motif in the Us9 cytoplasmic tail. Through alanine scanning mutagenesis of the acidic motif, we have identified two conserved tyrosine residues that are essential for Us9-mediated spread as well as two serine residues, comprising putative consensus casein kinase II sites, that modulate the rate of PRV transneuronal spread in vivo.

* Corresponding author. Mailing address: Department of Molecular Biology, Princeton University, Princeton, NJ 08544. Phone: (609) 258-2415. Fax: (609) 258-1035. E-mail: Lenquist{at}molbio.princeton.edu.

Journal of Virology, May 2000, p. 4549-4561, Vol. 74, No. 10
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


This article has been cited by other articles:

  • Lyman, M. G., Kemp, C. D., Taylor, M. P., Enquist, L. W. (2009). Comparison of the Pseudorabies Virus Us9 Protein with Homologs from Other Veterinary and Human Alphaherpesviruses. J. Virol. 83: 6978-6986 [Abstract] [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]  
  • Lyman, M. G., Curanovic, D., Brideau, A. D., Enquist, L. W. (2008). Fusion of Enhanced Green Fluorescent Protein to the Pseudorabies Virus Axonal Sorting Protein Us9 Blocks Anterograde Spread of Infection in Mammalian Neurons. J. Virol. 82: 10308-10311 [Abstract] [Full Text]  
  • Fuchs, W., Granzow, H., Klopfleisch, R., Klupp, B. G., Mettenleiter, T. C. (2006). The UL4 gene of pseudorabies virus encodes a minor infected-cell protein that is dispensable for virus replication. J. Gen. Virol. 87: 2517-2525 [Abstract] [Full Text]  
  • Klopfleisch, R., Klupp, B. G., Fuchs, W., Kopp, M., Teifke, J. P., Mettenleiter, T. C. (2006). Influence of pseudorabies virus proteins on neuroinvasion and neurovirulence in mice.. J. Virol. 80: 5571-5576 [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]  
  • Chowdhury, S. I., Mahmood, S., Simon, J., Al-Mubarak, A., Zhou, Y. (2006). The Us9 Gene of Bovine Herpesvirus 1 (BHV-1) Effectively Complements a Us9-Null Strain of BHV-5 for Anterograde Transport, Neurovirulence, and Neuroinvasiveness in a Rabbit Model. J. Virol. 80: 4396-4405 [Abstract] [Full Text]  
  • Wang, F., Tang, W., McGraw, H. M., Bennett, J., Enquist, L. W., Friedman, H. M. (2005). Herpes Simplex Virus Type 1 Glycoprotein E Is Required for Axonal Localization of Capsid, Tegument, and Membrane Glycoproteins. J. Virol. 79: 13362-13372 [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]  
  • Ch'ng, T. H., Enquist, L.W. (2005). Neuron-to-Cell Spread of Pseudorabies Virus in a Compartmented Neuronal Culture System. J. Virol. 79: 10875-10889 [Abstract] [Full Text]  
  • Fuchs, W., Granzow, H., Klopfleisch, R., Klupp, B. G., Rosenkranz, D., Mettenleiter, T. C. (2005). The UL7 Gene of Pseudorabies Virus Encodes a Nonessential Structural Protein Which Is Involved in Virion Formation and Egress. J. Virol. 79: 11291-11299 [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]  
  • Ficinska, J., Van Minnebruggen, G., Nauwynck, H. J., Bienkowska-Szewczyk, K., Favoreel, H. W. (2005). Pseudorabies Virus Glycoprotein gD Contains a Functional Endocytosis Motif That Acts in Concert with an Endocytosis Motif in gB To Drive Internalization of Antibody-Antigen Complexes from the Surface of Infected Monocytes. J. Virol. 79: 7248-7254 [Abstract] [Full Text]  
  • Koshizuka, T., Kawaguchi, Y., Nishiyama, Y. (2005). Herpes simplex virus type 2 membrane protein UL56 associates with the kinesin motor protein KIF1A. J. Gen. Virol. 86: 527-533 [Abstract] [Full Text]  
  • Foster, T. P., Melancon, J. M., Olivier, T. L., Kousoulas, K. G. (2004). Herpes Simplex Virus Type 1 Glycoprotein K and the UL20 Protein Are Interdependent for Intracellular Trafficking and trans-Golgi Network Localization. J. Virol. 78: 13262-13277 [Abstract] [Full Text]  
  • Klopfleisch, R., Teifke, J. P., Fuchs, W., Kopp, M., Klupp, B. G., Mettenleiter, T. C. (2004). Influence of Tegument Proteins of Pseudorabies Virus on Neuroinvasion and Transneuronal Spread in the Nervous System of Adult Mice after Intranasal Inoculation. J. Virol. 78: 2956-2966 [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]  
  • Pickard, G. E., Smeraski, C. A., Tomlinson, C. C., Banfield, B. W., Kaufman, J., Wilcox, C. L., Enquist, L. W., Sollars, P. J. (2002). Intravitreal Injection of the Attenuated Pseudorabies Virus PRV Bartha Results in Infection of the Hamster Suprachiasmatic Nucleus Only by Retrograde Transsynaptic Transport via Autonomic Circuits. J. Neurosci. 22: 2701-2710 [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]  
  • Johnson, D. C., Huber, M. T. (2002). Directed Egress of Animal Viruses Promotes Cell-to-Cell Spread. J. Virol. 76: 1-8 [Full Text]  
  • Johnson, D. C., Webb, M., Wisner, T. W., Brunetti, C. (2001). Herpes Simplex Virus gE/gI Sorts Nascent Virions to Epithelial Cell Junctions, Promoting Virus Spread. J. Virol. 75: 821-833 [Abstract] [Full Text]  
  • Tomishima, M.J., Enquist, L.W. (2001). A conserved {alpha}-herpesvirus protein necessary for axonal localization of viral membrane proteins. JCB 154: 741-752 [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»