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Journal of Virology, November 2001, p. 10923-10932, Vol. 75, No. 22
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.22.10923-10932.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.

The UL6 Gene Product Forms the Portal for Entry of DNA into the Herpes Simplex Virus Capsid

William W. Newcomb,1 Rachel M. Juhas,1 Darrell R. Thomsen,2 Fred L. Homa,2 April D. Burch,3 Sandra K. Weller,3 and Jay C. Brown1,*

Department of Microbiology and Cancer Center, University of Virginia Health System, Charlottesville, Virginia 229081; Infectious Disease Research, Pharmacia Corp., Kalamazoo, Michigan 490012; and Department of Microbiology, University of Connecticut Health Center, Farmington, Connecticut 060303

Received 5 June 2001/Accepted 21 August 2001

During replication of herpes simplex virus type 1 (HSV-1), viral DNA is synthesized in the infected cell nucleus, where DNA-free capsids are also assembled. Genome-length DNA molecules are then cut out of a larger, multigenome concatemer and packaged into capsids. Here we report the results of experiments carried out to test the idea that the HSV-1 UL6 gene product (pUL6) forms the portal through which viral DNA passes as it enters the capsid. Since DNA must enter at a unique site, immunoelectron microscopy experiments were undertaken to determine the location of pUL6. After specific immunogold staining of HSV-1 B capsids, pUL6 was found, by its attached gold label, at one of the 12 capsid vertices. Label was not observed at multiple vertices, at nonvertex sites, or in capsids lacking pUL6. In immunoblot experiments, the pUL6 copy number in purified B capsids was found to be 14.8 ± 2.6. Biochemical experiments to isolate pUL6 were carried out, beginning with insect cells infected with a recombinant baculovirus expressing the UL6 gene. After purification, pUL6 was found in the form of rings, which were observed in electron micrographs to have outside and inside diameters of 16.4 ± 1.1 and 5.0 ± 0.7 nm, respectively, and a height of 19.5 ± 1.9 nm. The particle weights of individual rings as determined by scanning transmission electron microscopy showed a majority population with a mass corresponding to an oligomeric state of 12. The results are interpreted to support the view that pUL6 forms the DNA entry portal, since it exists at a unique site in the capsid and forms a channel through which DNA can pass. The HSV-1 portal is the first identified in a virus infecting a eukaryote. In its dimensions and oligomeric state, the pUL6 portal resembles the connector or portal complexes employed for DNA encapsidation in double-stranded DNA bacteriophages such as phi 29, T4, and P22. This similarity supports the proposed evolutionary relationship between herpesviruses and double-stranded DNA phages and suggests the basic mechanism of DNA packaging is conserved.

* Corresponding author. Mailing address: Department of Microbiology, Box 800734, 1300 Jefferson Park Ave., University of Virginia Health System, Charlottesville, VA 22908. Phone: (434) 924-1814. Fax: (434) 982-1071. E-mail: JCB2G{at}VIRGINIA.EDU.

Journal of Virology, November 2001, p. 10923-10932, Vol. 75, No. 22
0022-538X/01/$04.00+0   DOI: 10.1128/JVI.75.22.10923-10932.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.


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