Vaccinia virus utilizes microtubules for movement to the cell surface

doi:10.1083/jcb.200104124

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-envelopedvirus (IEV) particles were proposed to induce the polymerizationof actin tails, which propel IEV particles to the cell surface.However, data presented support an alternative model in whichmicrotubules transport virions to the cell surface and actintails form beneath cell-associated enveloped virus (CEV) particlesat the cell surface. Thus, VV is unique in using both microtubulesand actin filaments for egress. The following data support thisproposal. (a) Microscopy detected actin tails at the surfacebut not the center of cells. (b) VV mutants lacking the A33R,A34R, or A36R proteins are unable to induce actin tail formationbut produce CEV and extracellular-enveloped virus. (c) CEV formationis 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 fluorescentprotein fused to the VV B5R protein moved inside cells at 60µm/min. This movement was stop-start, was along definedpathways, and was inhibited reversibly by nocodazole. This velocitywas 20-fold greater than VV movement on actin tails and consonantwith 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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