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Journal of Virology, January 2001, p. 323-340, Vol. 75, No. 1
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.1.323-340.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

Essential Role Played by the C-Terminal Domain of Glycoprotein I in Envelopment of Varicella-Zoster Virus in the trans-Golgi Network: Interactions of Glycoproteins with Tegument

Zuo-Hong Wang,1 Michael D. Gershon,2 Octavian Lungu,3 Zhenglun Zhu,2,dagger Suzanne Mallory,4 Ann M. Arvin,4 and Anne A. Gershon5,*

Institute of Human Nutrition1 and Departments of Anatomy and Cell Biology,2 Microbiology,3 and Pediatrics,5 College of Physicians and Surgeons, Columbia University, New York, New York 10032, and Departments of Pediatrics and Microbiology/Immunology, Stanford University School of Medicine, Stanford, California 943054

Received 14 August 2000/Accepted 28 September 2000

Varicella-zoster virus (VZV) is enveloped in the trans-Golgi network (TGN). Here we report that glycoprotein I (gI) is required within the TGN for VZV envelopment. Enveloping membranous TGN cisternae were microscopically identified in cells infected with intact VZV. These sacs curved around, and ultimately enclosed, nucleocapsids. Tegument coated the concave face of these sacs, which formed the viral envelope, but the convex surface was tegument-free. TGN cisternae of cells infected with VZV mutants lacking gI (gIDelta ) or its C (gIDelta C)- or N-terminal (gIDelta N)-terminal domains were uniformly tegument coated and adhered to one another, forming bizarre membranous stacks. Viral envelopment was compromised, and no virions were delivered to post-Golgi structures. The TGN was not gI-immunoreactive in cells infected with the gIDelta or gIDelta N mutants, but it was in cells infected with gIDelta C (because the ectodomains of gI and gE interact). The presence in the TGN of gI lacking a C-terminal domain, therefore, was not sufficient to maintain enveloping cisternae. In cells infected with intact VZV or with gIDelta , gIDelta N, or gIDelta C mutants, ORF10p immunoreactivity was concentrated on the cytosolic face of TGN membranes, suggesting that it interacts with the cytosolic domains of glycoproteins. Because of the gE-gI interaction, cotransfected cells that expressed gE or gI were able to target truncated forms of the other to the TGN. Our data suggest that the C-terminal domain of gI is required to segregate viral and cellular proteins in enveloping TGN cisternae.

* Corresponding author. Mailing address: Department of Pediatrics, Columbia University, College of Physicians and Surgeons, 630 W. 168th St., New York, NY 10032. Phone: (212) 305-9445. Fax: (212) 342-5218. E-mail: aag1{at}columbia.edu.

dagger Present address: Department of Medicine, Harvard Medical School, Boston, Mass.

Journal of Virology, January 2001, p. 323-340, Vol. 75, No. 1
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.1.323-340.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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