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Published online 10 July 2006. doi:10.1083/jcb.200510156
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 174, Number 2, 267-275
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Article

{alpha}-Herpesvirus glycoprotein D interaction with sensory neurons triggers formation of varicosities that serve as virus exit sites



Nick De Regge1, Hans J. Nauwynck1, Kristin Geenen1, Claude Krummenacher3, Gary H. Cohen3, Roselyn J. Eisenberg4, Thomas C. Mettenleiter5, and Herman W. Favoreel1,2

1 Laboratory of Virology and 2 Laboratory of Immunology, Faculty of Veterinary Medicine, Ghent University, 9820 Merelbeke, Belgium
3 Department of Microbiology, School of Dental Medicine, and 4 Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104
5 Friedrich-Loeffler-Institut, Federal Research Institute for Animal Health, Institute of Molecular Biology, D-17493 Greifswald–Insel Riems, Germany

Correspondence to Herman W. Favoreel: Herman.Favoreel{at}UGent.be

{alpha}-Herpesviruses constitute closely related neurotropic viruses, including herpes simplex virus in man and pseudorabies virus (PRV) in pigs. Peripheral sensory neurons, such as trigeminal ganglion (TG) neurons, are predominant target cells for virus spread and lifelong latent infections. We report that in vitro infection of swine TG neurons with the homologous swine {alpha}-herpesvirus PRV results in the appearance of numerous synaptophysin-positive synaptic boutons (varicosities) along the axons. Nonneuronal cells that were juxtaposed to these varicosities became preferentially infected with PRV, suggesting that varicosities serve as axonal exit sites for the virus. Viral envelope glycoprotein D (gD) was found to be necessary and sufficient for the induction of varicosities. Inhibition of Cdc42 Rho GTPase and p38 mitogen-activated protein kinase signaling pathways strongly suppressed gD-induced varicosity formation. These data represent a novel aspect of the cell biology of {alpha}-herpesvirus infections of sensory neurons, demonstrating that virus attachment/entry is associated with signaling events and neuronal changes that may prepare efficient egress of progeny virus.

Abbreviations used in this paper: BoHV, bovine herpesvirus; ERK, extracellular signal–regulated kinase; gD, glycoprotein D; HSV, herpes simplex virus; PFU, plaque-forming unit; PRV, pseudorabies virus; TG, trigeminal ganglion; WT, wild-type.


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