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Journal of Virology, October 2002, p. 9934-9951, Vol. 76, No. 19
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.19.9934-9951.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.

In Rat Dorsal Root Ganglion Neurons, Herpes Simplex Virus Type 1 Tegument Forms in the Cytoplasm of the Cell Body

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

Centre for Virus Research,1 Electron Microscope Laboratory, Institute of Clinical Pathology and Medical Research, Westmead Millennium Institute, Westmead Hospital and University of Sydney, Westmead, New South Wales 2145,2 School of Biological Sciences, University of Sydney, Camperdown, New South Wales 2050, Australia3

Received 15 January 2002/ Accepted 12 June 2002

The herpes simplex virus type 1 (HSV-1) tegument is the least understood component of the virion, and the mechanism of tegument assembly and incorporation into virions during viral egress has not yet been elucidated. In the present study, the addition of tegument proteins (VP13/14, VP16, VP22, and US9) and envelope glycoproteins (gD and gH) to herpes simplex virions in the cell body of rat dorsal root ganglion neurons was examined by immunoelectron microscopy. All tegument proteins were detected diffusely spread in the nucleus within 10 to 12 h and, at these times, nucleocapsids were observed budding from the nucleus. The majority (96%) of these nucleocapsids had no detectable label for tegument and glycoproteins despite the presence of tegument proteins in the nucleus and glycoproteins adjacent to the nuclear membrane. Immunolabeling for tegument proteins and glycoproteins was found abundantly in the cytoplasm of the cell body in multiple discrete vesicular areas: on unenveloped, enveloped, or partially enveloped capsids adjacent to these vesicles and in extracellular virions. These vesicles and intracytoplasmic and extracellular virions also labeled with Golgi markers, giantin, mannosidase II, and TGN38. Treatment with brefeldin A from 2 to 24 h postinfection markedly inhibited incorporation into virions of VP22 and US9 but to a lesser degree with VP16 and VP13/14. These results suggest that, in the cell body of neurons, most tegument proteins are incorporated into unenveloped nucleocapsids prior to envelopment in the Golgi and the trans-Golgi network. These findings give further support to the deenvelopment-reenvelopment hypothesis for viral egress. Finally, the addition of tegument proteins to unenveloped nucleocapsids in the cell body allows access to these unenveloped nucleocapsids to one of two pathways: egress through the cell body or transport into the axon.

* Corresponding author. Mailing address: Centre for Virus Research, Westmead Millennium Institute, Westmead Hospital/University of Sydney, Westmead, New South Wales 2145, Australia. Phone: (61) 2-9845-9000. Fax: (61) 2-9845-8100. E-mail: tony_cunningham{at}wmi.usyd.edu.au.

Journal of Virology, October 2002, p. 9934-9951, Vol. 76, No. 19
0022-538X/02/$04.00+0     DOI: 10.1128/JVI.76.19.9934-9951.2002
Copyright © 2002, American Society for Microbiology. All Rights Reserved.



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