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Journal of Virology, October 2007, p. 10792-10803, Vol. 81, No. 19
0022-538X/07/$08.00+0     doi:10.1128/JVI.00196-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Emerin Is Hyperphosphorylated and Redistributed in Herpes Simplex Virus Type 1-Infected Cells in a Manner Dependent on both UL34 and US3{triangledown}

Natalie Leach,1 Susan L. Bjerke,2 Desire K. Christensen,2 Jacques M. Bouchard,2 Fan Mou,3 Richard Park,3 Joel Baines,3 Tokuko Haraguchi,4 and Richard J. Roller2*

Program in Molecular and Cellular Biology, University of Iowa, Iowa City, Iowa 52242,1 Department of Microbiology, University of Iowa, Iowa City, Iowa 52242,2 Department of Microbiology and Immunology, Cornell University, Ithaca, New York 14853,3 CREST Research Project, Kansai Advanced Research Center, National Institute of Information and Communications Technology, 588-2 Iwaoka, Iwaoka-cho, Nishi-ku, Kobe 651-2492, Japan4

Received 29 January 2007/ Accepted 5 July 2007

Cells infected with wild-type herpes simplex virus type 1 (HSV-1) show disruption of the organization of the nuclear lamina that underlies the nuclear envelope. This disruption is reflected in changes in the localization and phosphorylation of lamin proteins. Here, we show that HSV-1 infection causes relocalization of the LEM domain protein emerin. In cells infected with wild-type virus, emerin becomes more mobile in the nuclear membrane, and in cells infected with viruses that fail to express UL34 protein (pUL34) and US3 protein (pUS3), emerin no longer colocalizes with lamins, suggesting that infection causes a loss of connection between emerin and the lamina. Infection causes hyperphosphorylation of emerin in a manner dependent upon both pUL34 and pUS3. Some emerin hyperphosphorylation can be inhibited by the protein kinase C{delta} (PKC{delta}) inhibitor rottlerin. Emerin and pUL34 interact physically, as shown by pull-down and coimmunoprecipitation assays. Emerin expression is not, however, necessary for infection, since virus growth is not impaired in cells derived from emerin-null transgenic mice. The results suggest a model in which pUS3 and PKC{delta} that has been recruited by pUL34 hyperphosphorylate emerin, leading to disruption of its connections with lamin proteins and contributing to the disruption of the nuclear lamina. Changes in emerin localization, nuclear shape, and lamin organization characteristic of cells infected with wild-type HSV-1 also occur in cells infected with recombinant virus that does not make viral capsids, suggesting that these changes occur independently of capsid envelopment.

* Corresponding author. Mailing address: Department of Microbiology, The University of Iowa, 3-432 Bowen Science Building, Iowa City, IA 52242. Phone: (319) 335-9958. Fax: (319) 335-9006. E-mail: richard-roller{at}uiowa.edu

{triangledown} Published ahead of print on 25 July 2007.

Journal of Virology, October 2007, p. 10792-10803, Vol. 81, No. 19
0022-538X/07/$08.00+0     doi:10.1128/JVI.00196-07
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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