Abstract
The vaccinia virus (VV) A27L gene encodes a 14 kDa protein that is required for the formation of intracellular enveloped virus (IEV) and, consequently, normal sized plaques. Data presented here show that A27L plays an additional role in VV assembly. When cells were infected with the VV WR32-7/Ind 14K, under conditions that repress A27L expression, transport of intracellular mature virus (IMV) from virus factories was inhibited and some IMV was found in aberrant association with virus crescents. In contrast, other VV mutants (vΔB5R and vΔF13L) that are defective in IEV formation produce IMV particles that are transported out of virus factories. This indicated a specific role for A27L in IMV transport. Induction of A27L expression at 10 h post-infection promoted the dispersal of clustered IMV particles, but only when microtubules were intact. Formation of IEV particles was also impaired when cells were infected with WR32-7/14K, a VV strain expressing a mutated form of the A27L protein; however, this mutation did not inhibit intracellular transport of IMV particles. Collectively, these data define two novel aspects of VV morphogenesis. Firstly, A27L is required for both IMV transport and the process of envelopment that leads to IEV formation. Secondly, movement of IMV particles between the virus factory and the site of IEV formation is microtubule-dependent.
References
52
Referenced
66
10.1016/0248-4900(93)90134-Z
/ Biology of the Cell / African swine fever virus interaction with microtubules by Alves de Matos (1993)10.1016/0042-6822(87)90444-2
/ Virology / Resistance of vaccinia virus to rifampicin conferred by a single nucleotide substitution near the predicted NH2 terminus of a gene encoding an Mr 62,000 polypeptide by Baldick (1987)10.1128/JVI.65.11.5910-5920.1991
/ Journal of Virology / Extracellular vaccinia virus formation and cell-to-cell virus transmission are prevented by deletion of the gene encoding the 37,000-Dalton outer envelope protein by Blasco (1991)10.1016/0168-1702(88)90042-1
/ Virus Research / Association of African swine fever virus with the cytoskeleton by Carvalho (1988)10.1128/JVI.72.2.1577-1585.1998
/ Journal of Virology / A27L mediates vaccinia virus interaction with cell surface heparan sulfate by Chung (1998)10.1038/378636a0
/ Nature / Actin-based motility of vaccinia virus by Cudmore (1995)10.1242/jcs.109.7.1739
/ Journal of Cell Science / Vaccinia virus: a model system for actin–membrane interactions by Cudmore (1996)10.1016/0042-6822(68)90286-9
/ Virology / Vaccinia as a model for membrane biogenesis by Dales (1968)10.1083/jcb.10.4.475
/ Journal of Biophysical and Biochemical Cytology / The development of vaccinia virus in Earles L strain cells as examined by electron microscopy by Dales (1961)10.1016/0042-6822(87)90480-6
/ Virology / Isolation and characterization of attenuated mutants of vaccinia virus by Dallo (1987)10.1016/0042-6822(87)90481-8
/ Virology / A 14K envelope protein of vaccinia virus with an important role in virus–host cell interactions is altered during virus persistence and determines the plaque size phenotype of the virus by Dallo (1987)10.1128/JVI.64.10.4884-4892.1990
/ Journal of Virology / Fusion of intra- and extracellular forms of vaccinia virus with the cell membrane by Doms (1990)10.1128/JVI.66.3.1610-1621.1992
/ Journal of Virology / Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress by Duncan (1992)10.1016/0042-6822(92)90535-W
/ Virology / A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope by Engelstad (1992)10.1128/JVI.63.11.4507-4514.1989
/ Journal of Virology / A single point mutation of Ala-25 to Asp in the 14,000-Mr envelope protein of vaccinia virus induces a size change that leads to the small plaque size phenotype of the virus by Gong (1989)10.1016/0042-6822(90)90381-Z
/ Virology / Vaccinia virus induces cell fusion at acid pH and this activity is mediated by the N-terminus of the 14-kDa virus envelope protein by Gong (1990)10.1128/JVI.72.6.5108-5120.1998
/ Journal of Virology / Analysis of a vaccinia virus mutant expressing a non-palmitoylated form of p37, a mediator of virion envelopment by Grosenbach (1998){'key': 'R18', 'first-page': '355', 'article-title': 'Immunofluorescence microscopy of the cytoskeleton: double and triple immunofluorescence', 'volume-title': 'Cell Biology: A Laboratory Handbook', 'author': 'Herzog', 'year': '1994'}
/ Cell Biology: A Laboratory Handbook / Immunofluorescence microscopy of the cytoskeleton: double and triple immunofluorescence by Herzog (1994)10.1128/JVI.44.2.647-657.1982
/ Journal of Virology / A phosphorylated basic vaccinia virus virion polypeptide of molecular weight 11,000 is exposed on the surface of mature particles and interacts with actin-containing cytoskeletal elements by Hiller (1982)10.1128/JVI.55.3.651-659.1985
/ Journal of Virology / Golgi-derived membranes that contain an acylated viral polypeptide are used for vaccinia virus envelopment by Hiller (1985)10.1016/0042-6822(79)90533-6
/ Virology / Interaction of assembled progeny pox viruses with the cellular cytoskeleton by Hiller (1979)10.1128/JVI.39.3.903-913.1981
/ Journal of Virology / Characterization of intracellular and extracellular vaccinia virus variants: N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release by Hiller (1981)10.1128/JVI.58.3.757-764.1986
/ Journal of Virology / Localization and fine structure of a vaccinia virus gene encoding an envelope antigen by Hirt (1986)10.1128/JVI.73.2.1503-1517.1999
/ Journal of Virology / Vaccinia virus intracellular mature virions contain only one lipid membrane by Hollinshead (1999)10.1128/JVI.66.12.7217-7224.1992
/ Journal of Virology / Characterization of a vaccinia virus-encoded 42-Kilodalton class I membrane glycoprotein component of the extracellular virus envelope by Isaacs (1992)10.1128/JVI.70.11.7485-7497.1996
/ Journal of Virology / Identification of the major membrane and core proteins of vaccinia virus by two-dimensional electrophoresis by Jensen (1996)10.1016/S0022-2836(64)80066-8
/ Journal of Molecular Biology / The replication and coating of vaccinia DNA by Joklik (1964)10.1128/JVI.72.3.2429-2438.1998
/ Journal of Virology / The extracellular domain of vaccinia virus protein B5R affects plaque phenotype, extracellular enveloped virus release, and intracellular actin tail formation by Mathew (1998)10.1016/0042-6822(76)90059-3
/ Virology / Vaccinia virus reexamined: development and release by Morgan (1976)10.1128/JVI.61.8.2642-2647.1987
/ Journal of Virology / Virus attenuation and identification of structural proteins of vaccinia virus that are selectively modified during virus persistence by Paez (1987)10.1006/viro.1994.1542
/ Virology / Vaccinia virus gene A36R encodes a Mr 43–50 K protein on the surface of extracellular enveloped virus by Parkinson (1994)10.1099/0022-1317-32-1-63
/ Journal of General Virology / Presence of haemagglutinin in the envelope of extracellular vaccinia virus particles by Payne (1976)10.1016/0042-6822(90)90477-9
/ Virology / Inducible gene expression from vaccinia virus vectors by Rodriguez (1990a)10.1093/nar/18.18.5347
/ Nucleic Acids Research / IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress by Rodriguez (1990b)10.1128/JVI.61.2.395-404.1987
/ Journal of Virology / A 14,000-Mr envelope protein of vaccinia virus is involved in cell fusion and forms covalently linked trimers by Rodriguez (1987)10.1128/JVI.67.6.3435-3440.1993
/ Journal of Virology / The vaccinia virus 14-kilodalton fusion protein forms a stable complex with the processed protein encoded by the vaccinia virus A17L gene by Rodriguez (1993)10.1128/JVI.69.8.4640-4648.1995
/ Journal of Virology / Vaccinia virus A17L gene product is essential for an early step in virion morphogenesis by Rodriguez (1995)10.1128/JVI.71.3.1821-1833.1997
/ Journal of Virology / Characterization of early stages in vaccinia virus membrane biogenesis: implications of the 21-kilodalton protein and a newly identified 15-kilodalton envelope protein by Rodriguez (1997)10.1128/JVI.70.6.3753-3762.1996
/ Journal of Virology / Extracellular vaccinia virus envelope glycoprotein encoded by the A33R gene by Roper (1996)10.1128/JVI.72.5.4192-4204.1998
/ Journal of Virology / The envelope protein encoded by the A33R gene is required for formation of actin-containing microvilli and efficient cell-to-cell spread of vaccinia virus by Roper (1998)10.1099/0022-1317-79-6-1415
/ Journal of General Virology / Roles of vaccinia virus EEV-specific proteins in intracellular actin tail formation and low pH-induced cell-cell fusion by Sanderson (1998)10.1128/JVI.68.1.130-147.1994
/ Journal of Virology / Assembly of vaccinia virus: the second wrapping cisterna is derived from the trans Golgi network by Schmelz (1994)10.1016/0042-6822(86)90309-0
/ Virology / Nucleotide sequence of the vaccinia virus hemagglutinin gene by Shida (1986)10.1083/jcb.121.3.521
/ Journal of Cell Biology / Assembly of vaccinia virus: role of the intermediate compartment between the endoplasmic reticulum and the Golgi stacks by Sodeik (1993)10.1128/JVI.18.2.636-643.1976
/ Journal of Virology / High-voltage electron microscope study of the release of vaccinia virus from whole cells by Stokes (1976)10.1006/viro.1994.1406
/ Virology / N-terminal amino acid sequences of vaccinia virus structural proteins by Takahashi (1994)10.1016/0042-6822(86)90264-3
/ Virology / Vaccinia virus rifampicin-resistance locus specifies a late 63,000 Da gene product by Tartaglia (1986){'key': 'R48', 'first-page': '163', 'article-title': 'Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes', 'volume': '60', 'author': 'Tooze', 'year': '1993', 'journal-title': 'European Journal of Cell Biology'}
/ European Journal of Cell Biology / Progeny vaccinia and human cytomegalovirus particles utilize early endosomal cisternae for their envelopes by Tooze (1993)10.1128/JVI.70.5.2797-2808.1996
/ Journal of Virology / Vaccinia virus A17L open reading frame encodes an essential component of nascent viral membranes that is required to initiate morphogenesis by Wolffe (1996)10.1128/JVI.71.5.3904-3915.1997
/ Journal of Virology / The A34R glycoprotein gene is required for induction of specialized actin-containing microvilli and efficient cell-to-cell transmission of vaccinia virus by Wolffe (1997)10.1006/viro.1998.9103
/ Virology / Role for the vaccinia virus A36R outer envelope protein in the formation of virus-tipped actin-containing microvilli and cell-to-cell virus spread by Wolffe (1998)10.1016/0042-6822(92)90467-4
/ Virology / Immature viral envelope formation is interrupted at the same stage by lac operator-mediated repression of vaccinia virus gene D13L and by the drug rifampicin by Zhang (1992)
Dates
Type | When |
---|---|
Created | 10 years ago (Aug. 26, 2015, 10:49 a.m.) |
Deposited | 3 years, 3 months ago (May 20, 2022, 7:23 p.m.) |
Indexed | 1 year, 2 months ago (June 11, 2024, 5:54 p.m.) |
Issued | 25 years, 8 months ago (Jan. 1, 2000) |
Published | 25 years, 8 months ago (Jan. 1, 2000) |
Published Print | 25 years, 8 months ago (Jan. 1, 2000) |
@article{Sanderson_2000, title={The vaccinia virus A27L protein is needed for the microtubule-dependent transport of intracellular mature virus particles}, volume={81}, ISSN={1465-2080}, url={http://dx.doi.org/10.1099/0022-1317-81-1-47}, DOI={10.1099/0022-1317-81-1-47}, number={1}, journal={Microbiology}, publisher={Microbiology Society}, author={Sanderson, Christopher M. and Hollinshead, Michael and Smith, Geoffrey L.}, year={2000}, month=jan, pages={47–58} }