Pseudorabies virus, an α-herpesvirus, is capable of infecting the nervous system and spreading between synaptically connected neurons in diverse hosts. At least three viral membrane proteins (gE, gI, and Us9) are necessary for the spread of infection from presynaptic to postsynaptic neurons (anterograde spread) in infected rodents. To understand how these proteins effect anterograde spread between neurons, we analyzed the subcellular localization of viral proteins after infection of cultured rat sympathetic neurons with wild-type or mutant viruses. After Us9-null mutant infections but not gE-null mutant infections, only a subset of the viral structural proteins had entered axons. Surprisingly, capsid and tegument proteins but not viral membrane proteins were detected in axons. The spread of Us9 missense mutants in the rodent nervous system correlated with the amount of viral membrane proteins localized to axons. We conclude that the Us9 membrane protein controls axonal localization of diverse viral membrane proteins but not that of capsid or tegument proteins. The data support a model where virion subassemblies but not complete virions are transported in the axon. Our results provide new insight into the process of virion assembly and exit from neurons that leads to directional spread of herpesviruses in the nervous system.
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20 August 2001
Article|
August 13 2001
A conserved α-herpesvirus protein necessary for axonal localization of viral membrane proteins
M.J. Tomishima,
M.J. Tomishima
Department of Molecular Biology, Princeton University, Princeton, NJ 08544
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L.W. Enquist
L.W. Enquist
Department of Molecular Biology, Princeton University, Princeton, NJ 08544
Search for other works by this author on:
M.J. Tomishima
Department of Molecular Biology, Princeton University, Princeton, NJ 08544
L.W. Enquist
Department of Molecular Biology, Princeton University, Princeton, NJ 08544
Address correspondence to Lynn W. Enquist, 314 Schultz Laboratory, Department of Molecular Biology, Princeton University, Princeton, NJ 08544. Tel.: (609) 258-2415. Fax: (609) 258-1035. E-mail: [email protected]
*
Abbreviations used in this paper: GFP, green fluorescent protein; NgCAM, neural glycoprotein cell adhesion molecule; PNS, peripheral nervous system; PRV, pseudorabies virus; SCG, superior cervical ganglia.
Received:
November 29 2000
Revision Received:
June 05 2001
Accepted:
July 02 2001
Online ISSN: 1540-8140
Print ISSN: 0021-9525
The Rockefeller University Press
2001
J Cell Biol (2001) 154 (4): 741–752.
Article history
Received:
November 29 2000
Revision Received:
June 05 2001
Accepted:
July 02 2001
Citation
M.J. Tomishima, L.W. Enquist; A conserved α-herpesvirus protein necessary for axonal localization of viral membrane proteins . J Cell Biol 20 August 2001; 154 (4): 741–752. doi: https://doi.org/10.1083/jcb.200011146
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