Abstract
The cytoplasmic domains of viral glycoproteins are often involved in specific interactions with internal viral components. These interactions can concentrate glycoproteins at virus budding sites and drive efficient virus budding, or can determine virion morphology. To investigate the role of the vesicular stomatitis virus (VSV) glycoprotein (G) cytoplasmic and transmembrane domains in budding, we recovered recombinant VSVs expressing chimeric G proteins with the transmembrane and cytoplasmic domains derived from the human CD4 protein. These unrelated foreign sequences were capable of supporting efficient VSV budding. Further analysis of G protein cytoplasmic domain deletion mutants showed that a cytoplasmic domain of only 1 amino acid did not drive efficient budding, whereas 9 amino acids did. Additional studies in agreement with the CD4-chimera experiments indicated the requirement for a short cytoplasmic domain on VSV G without the requirement for a specific sequence in that domain. We propose a model for VSV budding in which a relatively non-specific interaction of a cytoplasmic domain with a pocket or groove in the viral nucleocapsid or matrix proteins generates a glycoprotein array that promotes viral budding.
Full Text
The Full Text of this article is available as a PDF (335.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Barge A., Gaudin Y., Coulon P., Ruigrok R. W. Vesicular stomatitis virus M protein may be inside the ribonucleocapsid coil. J Virol. 1993 Dec;67(12):7246–7253. doi: 10.1128/jvi.67.12.7246-7253.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bruss V., Ganem D. The role of envelope proteins in hepatitis B virus assembly. Proc Natl Acad Sci U S A. 1991 Feb 1;88(3):1059–1063. doi: 10.1073/pnas.88.3.1059. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Buonocore L., Turi T. G., Crise B., Rose J. K. Stimulation of heterologous protein degradation by the Vpu protein of HIV-1 requires the transmembrane and cytoplasmic domains of CD4. Virology. 1994 Oct;204(1):482–486. doi: 10.1006/viro.1994.1560. [DOI] [PubMed] [Google Scholar]
- Chong L. D., Rose J. K. Membrane association of functional vesicular stomatitis virus matrix protein in vivo. J Virol. 1993 Jan;67(1):407–414. doi: 10.1128/jvi.67.1.407-414.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cosson P. Direct interaction between the envelope and matrix proteins of HIV-1. EMBO J. 1996 Nov 1;15(21):5783–5788. [PMC free article] [PubMed] [Google Scholar]
- Enami M., Enami K. Influenza virus hemagglutinin and neuraminidase glycoproteins stimulate the membrane association of the matrix protein. J Virol. 1996 Oct;70(10):6653–6657. doi: 10.1128/jvi.70.10.6653-6657.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fuerst T. R., Niles E. G., Studier F. W., Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122–8126. doi: 10.1073/pnas.83.21.8122. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jin H., Leser G. P., Lamb R. A. The influenza virus hemagglutinin cytoplasmic tail is not essential for virus assembly or infectivity. EMBO J. 1994 Nov 15;13(22):5504–5515. doi: 10.1002/j.1460-2075.1994.tb06885.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jin H., Leser G. P., Zhang J., Lamb R. A. Influenza virus hemagglutinin and neuraminidase cytoplasmic tails control particle shape. EMBO J. 1997 Mar 17;16(6):1236–1247. doi: 10.1093/emboj/16.6.1236. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johnson J. E., Schnell M. J., Buonocore L., Rose J. K. Specific targeting to CD4+ cells of recombinant vesicular stomatitis viruses encoding human immunodeficiency virus envelope proteins. J Virol. 1997 Jul;71(7):5060–5068. doi: 10.1128/jvi.71.7.5060-5068.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Knipe D. M., Baltimore D., Lodish H. F. Maturation of viral proteins in cells infected with temperature-sensitive mutants of vesicular stomatitis virus. J Virol. 1977 Mar;21(3):1149–1158. doi: 10.1128/jvi.21.3.1149-1158.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lawson N. D., Stillman E. A., Whitt M. A., Rose J. K. Recombinant vesicular stomatitis viruses from DNA. Proc Natl Acad Sci U S A. 1995 May 9;92(10):4477–4481. doi: 10.1073/pnas.92.10.4477. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lee S., Owen K. E., Choi H. K., Lee H., Lu G., Wengler G., Brown D. T., Rossmann M. G., Kuhn R. J. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure. 1996 May 15;4(5):531–541. doi: 10.1016/s0969-2126(96)00059-7. [DOI] [PubMed] [Google Scholar]
- Lefrancois L., Lyles D. S. The interaction of antibody with the major surface glycoprotein of vesicular stomatitis virus. II. Monoclonal antibodies of nonneutralizing and cross-reactive epitopes of Indiana and New Jersey serotypes. Virology. 1982 Aug;121(1):168–174. doi: 10.1016/0042-6822(82)90126-x. [DOI] [PubMed] [Google Scholar]
- Li Y., Drone C., Sat E., Ghosh H. P. Mutational analysis of the vesicular stomatitis virus glycoprotein G for membrane fusion domains. J Virol. 1993 Jul;67(7):4070–4077. doi: 10.1128/jvi.67.7.4070-4077.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lopez S., Yao J. S., Kuhn R. J., Strauss E. G., Strauss J. H. Nucleocapsid-glycoprotein interactions required for assembly of alphaviruses. J Virol. 1994 Mar;68(3):1316–1323. doi: 10.1128/jvi.68.3.1316-1323.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mebatsion T., Conzelmann K. K. Specific infection of CD4+ target cells by recombinant rabies virus pseudotypes carrying the HIV-1 envelope spike protein. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11366–11370. doi: 10.1073/pnas.93.21.11366. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mebatsion T., Konig M., Conzelmann K. K. Budding of rabies virus particles in the absence of the spike glycoprotein. Cell. 1996 Mar 22;84(6):941–951. doi: 10.1016/s0092-8674(00)81072-7. [DOI] [PubMed] [Google Scholar]
- Mitnaul L. J., Castrucci M. R., Murti K. G., Kawaoka Y. The cytoplasmic tail of influenza A virus neuraminidase (NA) affects NA incorporation into virions, virion morphology, and virulence in mice but is not essential for virus replication. J Virol. 1996 Feb;70(2):873–879. doi: 10.1128/jvi.70.2.873-879.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Odell D., Wanas E., Yan J., Ghosh H. P. Influence of membrane anchoring and cytoplasmic domains on the fusogenic activity of vesicular stomatitis virus glycoprotein G. J Virol. 1997 Oct;71(10):7996–8000. doi: 10.1128/jvi.71.10.7996-8000.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Owens R. J., Rose J. K. Cytoplasmic domain requirement for incorporation of a foreign envelope protein into vesicular stomatitis virus. J Virol. 1993 Jan;67(1):360–365. doi: 10.1128/jvi.67.1.360-365.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raja N. U., Vincent M. J., Jabbar M. A. Analysis of endoproteolytic cleavage and intracellular transport of human immunodeficiency virus type 1 envelope glycoproteins using mutant CD4 molecules bearing the transmembrane endoplasmic reticulum retention signal. J Gen Virol. 1993 Oct;74(Pt 10):2085–2097. doi: 10.1099/0022-1317-74-10-2085. [DOI] [PubMed] [Google Scholar]
- Rose J. K., Buonocore L., Whitt M. A. A new cationic liposome reagent mediating nearly quantitative transfection of animal cells. Biotechniques. 1991 Apr;10(4):520–525. [PubMed] [Google Scholar]
- Schnell M. J., Buonocore L., Kretzschmar E., Johnson E., Rose J. K. Foreign glycoproteins expressed from recombinant vesicular stomatitis viruses are incorporated efficiently into virus particles. Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11359–11365. doi: 10.1073/pnas.93.21.11359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnell M. J., Buonocore L., Whitt M. A., Rose J. K. The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J Virol. 1996 Apr;70(4):2318–2323. doi: 10.1128/jvi.70.4.2318-2323.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnell M. J., Johnson J. E., Buonocore L., Rose J. K. Construction of a novel virus that targets HIV-1-infected cells and controls HIV-1 infection. Cell. 1997 Sep 5;90(5):849–857. doi: 10.1016/s0092-8674(00)80350-5. [DOI] [PubMed] [Google Scholar]
- Schnitzer T. J., Dickson C., Weiss R. A. Morphological and biochemical characterization of viral particles produced by the tsO45 mutant of vesicular stomatitis virus at restrictive temperature. J Virol. 1979 Jan;29(1):185–195. doi: 10.1128/jvi.29.1.185-195.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnitzer T. J., Lodish H. F. Noninfectious vesicular stomatitis virus particles deficient in the viral nucleocapsid. J Virol. 1979 Feb;29(2):443–447. doi: 10.1128/jvi.29.2.443-447.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schubert M., Joshi B., Blondel D., Harmison G. G. Insertion of the human immunodeficiency virus CD4 receptor into the envelope of vesicular stomatitis virus particles. J Virol. 1992 Mar;66(3):1579–1589. doi: 10.1128/jvi.66.3.1579-1589.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Simons K., Garoff H. The budding mechanisms of enveloped animal viruses. J Gen Virol. 1980 Sep;50(1):1–21. doi: 10.1099/0022-1317-50-1-1. [DOI] [PubMed] [Google Scholar]
- Skoging U., Vihinen M., Nilsson L., Liljeström P. Aromatic interactions define the binding of the alphavirus spike to its nucleocapsid. Structure. 1996 May 15;4(5):519–529. doi: 10.1016/s0969-2126(96)00058-5. [DOI] [PubMed] [Google Scholar]
- Stephens E. B., Compans R. W. Assembly of animal viruses at cellular membranes. Annu Rev Microbiol. 1988;42:489–516. doi: 10.1146/annurev.mi.42.100188.002421. [DOI] [PubMed] [Google Scholar]
- Suomalainen M., Liljeström P., Garoff H. Spike protein-nucleocapsid interactions drive the budding of alphaviruses. J Virol. 1992 Aug;66(8):4737–4747. doi: 10.1128/jvi.66.8.4737-4747.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whelan S. P., Ball L. A., Barr J. N., Wertz G. T. Efficient recovery of infectious vesicular stomatitis virus entirely from cDNA clones. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8388–8392. doi: 10.1073/pnas.92.18.8388. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Whitt M. A., Chong L., Rose J. K. Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant. J Virol. 1989 Sep;63(9):3569–3578. doi: 10.1128/jvi.63.9.3569-3578.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson C. M. Staining of proteins on gels: comparisons of dyes and procedures. Methods Enzymol. 1983;91:236–247. doi: 10.1016/s0076-6879(83)91020-0. [DOI] [PubMed] [Google Scholar]
- Zhao H., Lindqvist B., Garoff H., von Bonsdorff C. H., Liljeström P. A tyrosine-based motif in the cytoplasmic domain of the alphavirus envelope protein is essential for budding. EMBO J. 1994 Sep 15;13(18):4204–4211. doi: 10.1002/j.1460-2075.1994.tb06740.x. [DOI] [PMC free article] [PubMed] [Google Scholar]