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Journal of Virology, October 2005, p. 13047-13059, Vol. 79, No. 20
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.20.13047-13059.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Herpes Simplex Virus 1 Envelopment Follows Two Diverse Pathways

Helene Leuzinger,1 Urs Ziegler,3 Elisabeth M. Schraner,1 Cornel Fraefel,2 Daniel L. Glauser,2 Irma Heid,2 Mathias Ackermann,2 Martin Mueller,4 and Peter Wild1*

Electron Microscopy, Institute of Veterinary Anatomy,1 Institute of Virology,2 Institute of Anatomy, University of Zürich,3 Laboratory for Electron Microscopy, Institute of Physics, Swiss Federal Institute of Technology, Zürich, Switzerland4

Received 10 March 2005/ Accepted 11 July 2005

Herpesvirus envelopment is assumed to follow an uneconomical pathway including primary envelopment at the inner nuclear membrane, de-envelopment at the outer nuclear membrane, and reenvelopment at the trans-Golgi network. In contrast to the hypothesis of de-envelopment by fusion of the primary envelope with the outer nuclear membrane, virions were demonstrated to be transported from the perinuclear space to rough endoplasmic reticulum (RER) cisternae. Here we show by high-resolution microscopy that herpes simplex virus 1 envelopment follows two diverse pathways. First, nuclear envelopment includes budding of capsids at the inner nuclear membrane into the perinuclear space whereby tegument and a thick electron dense envelope are acquired. The substance responsible for the dense envelope is speculated to enable intraluminal transportation of virions via RER into Golgi cisternae. Within Golgi cisternae, virions are packaged into transport vacuoles containing one or several virions. Second, for cytoplasmic envelopment, capsids gain direct access from the nucleus to the cytoplasm via impaired nuclear pores. Cytoplasmic capsids could bud at the outer nuclear membrane, at membranes of RER, Golgi cisternae, and large vacuoles, and at banana-shaped membranous entities that were found to continue into Golgi membranes. Envelopes originating by budding at the outer nuclear membrane and RER membrane also acquire a dense substance. Budding at Golgi stacks, designated wrapping, results in single virions within small vacuoles that contain electron-dense substances between envelope and vacuolar membranes.

* Corresponding author. Mailing address: Electron Microscopy, Institutes of Veterinary Anatomy and of Virology, Winterthurerstrasse 260, CH-8057 Zürich, Switzerland. Phone: 41 1 635 87 84. Fax: 41 1 635 89 11. E-mail: pewild{at}vetanat.unizh.ch.

Journal of Virology, October 2005, p. 13047-13059, Vol. 79, No. 20
0022-538X/05/$08.00+0     doi:10.1128/JVI.79.20.13047-13059.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



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