Egress of Alphaherpesviruses: Comparative Ultrastructural Study

doi:10.1128/JVI.75.8.3675-3684.2001

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Journal of Virology, April 2001, p. 3675-3684, Vol. 75, No. 8
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.8.3675-3684.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Egress of Alphaherpesviruses: Comparative Ultrastructural Study

Harald Granzow,¹^,^* Barbara G. Klupp,² Walter Fuchs,² Jutta Veits,² Nikolaus Osterrieder,² and Thomas C. Mettenleiter²

Institutes of Infectology¹ and Molecular Biology,² Friedrich-Loeffler-Institutes, Federal Research Centre for Virus Diseases of Animals, D-17498 Insel Riems, Germany

Received 27 November 2000/Accepted 23 January 2001

Egress of four important alphaherpesviruses, equine herpesvirus 1 (EHV-1), herpes simplex virus type 1 (HSV-1), infectiouslaryngotracheitis virus (ILTV), and pseudorabies virus (PrV),was investigated by electron microscopy of infected cell linesof different origins. In all virus-cell systems analyzed, similarobservations were made concerning the different stages of virionmorphogenesis. After intranuclear assembly, nucleocapsids budat the inner leaflet of the nuclear membrane, resulting in envelopedparticles in the perinuclear space that contain a sharply borderedrim of tegument and a smooth envelope surface. Egress from theperinuclear cisterna primarily occurs by fusion of the primaryenvelope with the outer leaflet of the nuclear membrane, whichhas been visualized for HSV-1 and EHV-1 for the first time. Theresulting intracytoplasmic naked nucleocapsids are enveloped atmembranes of the trans-Golgi network (TGN), as shown by immunogoldlabeling with a TGN-specific antiserum. Virions containing theirfinal envelope differ in morphology from particles within theperinuclear cisterna by visible surface projections and a diffusetegument. Particularly striking was the addition of a large amountof tegument material to ILTV capsids in the cytoplasm. Extracellularvirions were morphologically identical to virions within Golgi-derivedvesicles, but distinct from virions in the perinuclear space.Studies with gB- and gH-deleted PrV mutants indicated that thesetwo glycoproteins, which are essential for virus entry and directcell-to-cell spread, are dispensable for egress. Taken together,our studies indicate that the deenvelopment-reenvelopment processof herpesvirus maturation also occurs in EHV-1, HSV-1, and ILTVand that membrane fusion processes occurring during egress aresubstantially different from those during entry and direct viralcell-to-cellspread.

^* Corresponding author. Mailing address: Institute of Infectology, Friedrich-Loeffler-Institutes, Federal Research Centre forVirus Diseases of Animals, Boddenblick 5A, D-17498 Insel Riems,Germany. Phone: 49-38351-7206. Fax: 49-38351-7151. E-mail: Harald.Granzow{at}rie.bfav.de.

Journal of Virology, April 2001, p. 3675-3684, Vol. 75, No. 8
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.8.3675-3684.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

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