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J. Biol. Chem., Vol. 279, Issue 27, 28522-28530, July 2, 2004

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Herpes Simplex Virus Type 1 Capsid Protein VP26 Interacts with Dynein Light Chains RP3 and Tctex1 and Plays a Role in Retrograde Cellular Transport^*

Mark W. Douglas, Russell J. Diefenbach¶, Fred L. Homa||**, Monica Miranda-Saksena, Frazer J. Rixon, Valerio Vittone, Karen Byth, and Anthony L. Cunningham

From the Centre for Virus Research, Westmead Millennium Institute, University of Sydney and Westmead Hospital, P. O. Box 412, Westmead 2145, New South Wales, Australia, ^||Infectious Disease Biology, Pharmacia Corp., Kalamazoo, Michigan 49001, and MRC Virology Unit, Institute of Virology, Glasgow G11 5JR, Scotland, United Kingdom

Cytoplasmic dynein is the major molecular motor involved in minus-end-directed cellular transport along microtubules. There is increasing evidence that the retrograde transport of herpes simplex virus type 1 along sensory axons is mediated by cytoplasmic dynein, but the viral and cellular proteins involved are not known. Here we report that the herpes simplex virus outer capsid protein VP26 interacts with dynein light chains RP3 and Tctex1 and is sufficient to mediate retrograde transport of viral capsids in a cellular model. A library of herpes simplex virus capsid and tegument structural genes was constructed and tested for interactions with dynein subunits in a yeast two-hybrid system. A strong interaction was detected between VP26 and the homologous 14-kDa dynein light chains RP3 and Tctex1. In vitro pull-down assays confirmed binding of VP26 to RP3, Tctex1, and intact cytoplasmic dynein complexes. Recombinant herpes simplex virus capsids were constructed either with or without VP26. In pull-down assays VP26+ capsids bound to RP3; VP26-capsids did not. To investigate intracellular transport, the recombinant viral capsids were microinjected into living cells and incubated at 37 °C. After 1 h VP26+ capsids were observed to co-localize with RP3, Tctex1, and microtubules. After 2 or 4 h VP26+ capsids had moved closer to the cell nucleus, whereas VP26-capsids remained in a random distribution. We propose that VP26 mediates binding of incoming herpes simplex virus capsids to cytoplasmic dynein during cellular infection, through interactions with dynein light chains.

Received for publication, October 24, 2003 , and in revised form, April 22, 2004.

^* This work was supported by National Health and Medical Research Council Grants 107374 and 253617 (to A. L. C. and R. J. D.) and Post-graduate Medical Scholarship 165713 (to M. W. D.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Both authors contributed equally to this work.

^** Present address: Dept. of Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261.

^¶ To whom correspondence should be addressed: Centre for Virus Research, Westmead Millennium Institute, P. O. Box 412, Westmead 2145, New South Wales, Australia. Tel.: 61-2-9845-9111; Fax: 61-2-9845-9103; E-mail: russell_diefenbach{at}wmi.usyd.edu.au.

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