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Published 23 July 2001. doi:10.1083/jcb.200104124
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© The Rockefeller University Press, 0021-9525/2001/7/389 $5.00
The Journal of Cell Biology, Volume 154, Number 2, July 23, 2001 389-402

Article

 Vaccinia virus utilizes microtubules for movement to the cell surface

Michael Hollinshead, Gaener Rodger, Henriette Van Eijl, Mansun Law, Ruth Hollinshead, David J.T. Vaux and Geoffrey L. Smith

Sir William Dunn School of Pathology, University of Oxford, Oxford OX1 3RE, United Kingdom

Address correspondence to Geoffrey L. Smith, The Wright-Fleming Institute, Imperial College School of Medicine, St. Mary's Campus, Norfolk Place, London W2 1PG, UK. Tel.: 44-207-594-3972. Fax: 44-207-594-3973. E-mail: glsmith{at}ic.ac.uk

Vaccinia virus (VV) egress has been studied using confocal, video, and electron microscopy. Previously, intracellular-enveloped virus (IEV) particles were proposed to induce the polymerization of actin tails, which propel IEV particles to the cell surface. However, data presented support an alternative model in which microtubules transport virions to the cell surface and actin tails form beneath cell-associated enveloped virus (CEV) particles at the cell surface. Thus, VV is unique in using both microtubules and actin filaments for egress. The following data support this proposal. (a) Microscopy detected actin tails at the surface but not the center of cells. (b) VV mutants lacking the A33R, A34R, or A36R proteins are unable to induce actin tail formation but produce CEV and extracellular-enveloped virus. (c) CEV formation is inhibited by nocodazole but not cytochalasin D or 4-amino-5-(4-methylphenyl)-7-(t-butyl)pyrazolo(3,4-d)pyrimidine (PP1). (d) IEV particles tagged with the enhanced green fluorescent protein fused to the VV B5R protein moved inside cells at 60 µm/min. This movement was stop-start, was along defined pathways, and was inhibited reversibly by nocodazole. This velocity was 20-fold greater than VV movement on actin tails and consonant with the rate of movement of organelles along microtubules.

Key Words: vaccinia virus; green fluorescent protein; actin tails; confocal and electron microscopy; microtubules


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