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Enveloped Virus Maturation at Restricted Membrane Domains

  • Richard W. Compans
Chapter

Abstract

Synthesis and assembly of the envelope proteins of lipid-containing viruses require the biosynthetic and transport processes involved in cellular membrane biogenesis, and such viruses have therefore been used extensively for investigation of these processes. With the exception of poxviruses, which assemble their membranes de novo in the cytoplasm, the assembly of enveloped viruses takes place on preformed cellular membranes. The precise location at which assembly occurs is a distinctive characteristic that is highly conserved among structurally similar viruses. Herpesvirus maturation occurs by budding at the inner nuclear membrane. Coronaviruses are assembled at the rough endoplasmic reticulum, and bunyaviruses bud at membranes of the Golgi complex. Virus particles of several other families are formed by budding at the plasma membrane. Polarized epithelial cells exhibit distinct apical and basolateral surface domains separated by tight junctions, and it has been observed that assembly of enveloped viruses occurs at one or the other of these membrane domains. Thus, with the exception of mitochondrial membranes, any membrane of the cell is known to be capable of serving as a virus maturation site.

Keywords

Influenza Virus MDCK Cell Basolateral Membrane Avian Influenza Virus Golgi Complex 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Rodriguez Boulan E, Sabatini DD (1978) Asymmetric budding of viruses in epithelial monolayers: A model system for study of epithelial polarity. Proc Natl Acad Sci USA 75:5071–5075PubMedCrossRefGoogle Scholar
  2. 2.
    Roth MG, Srinivas RV, Compans RW (1983) Basolateral maturation of retroviruses in polarized epithelial cells. J Virol 45:1065–1073PubMedGoogle Scholar
  3. 3.
    Rodriguez Boulan E, Pendergast M (1980) Polarized distribution of viral envelope proteins in the plasma membrane of infected epithelial cells. Cell 20:45–54PubMedCrossRefGoogle Scholar
  4. 4.
    Roth MG, Compans RW, Giusti L, Davis AR, Nayak DP, Gething M-J, Sambrook J (1983) Influenza virus hemagglutinin expression is polarized in cells infected with recombinant SV40 viruses carrying cloned hemagglutinin DNA. Cell 33:435–442PubMedCrossRefGoogle Scholar
  5. 5.
    Green RF, Meiss HK, Rodriguez Boulan E (1981) Glycosylation does not determine segregation of viral envelope proteins in the plasma membrane of epithelial cells. J Cell Biol 89:230–239PubMedCrossRefGoogle Scholar
  6. 6.
    Roth MG, Fitzpatrick JP, Compans RW (1979) Polarity of influenza and vesicular stomatitis virus maturation in MDCK cells: Lack of a requirement for glycosylation of viral glycoproteins. Proc Natl Acad Sci USA 76:6430–6434PubMedCrossRefGoogle Scholar
  7. 7.
    Doller EW, Holmes KV (1980) Different intracellular transportation of the envelope glycoproteins E1 and E2 of the coronavirus MHV. Abstr Am Soc Micro, p 267Google Scholar
  8. 8.
    De Guili C, Kawai S, Dales S, Hanafusa H (1975) Absence of surface projection on some noninfectious forms of RSV. Virology 66:253–260CrossRefGoogle Scholar
  9. 9.
    Schnitzer TJ, Dickson C, Weiss RA (1979) Morphological and biochemical characterization of viral particles produced by the ts045 mutant of vesicular stomatitis virus at restrictive temperature. J Virol 29:185–195PubMedGoogle Scholar
  10. 10.
    Rodriguez Boulan E, Paskiet KT, Sabatini DD (1983) Assembly of enveloped viruses in Madin-Darby canine kidney cells: Polarized budding from single attached cells and from clusters of cells in suspension. J Cell Biol 96:866–874PubMedCrossRefGoogle Scholar
  11. 11.
    Rose JK, Bergmann JE, Gallione CJ, Florkiewicz RZ (1983) Changes in the cytoplasmic sequence of VSV G protein alter its rate of transport to the plasma membrane. J Cell Biochem Supp 7B:356Google Scholar
  12. 12.
    Bergeron JJM, Kotwall GJ, Levine G, Bilan P, Rachubinski R, Hamilton M, Shore GC, Ghosh HP (1982) Intracellular transport of the transmembrane glycoprotein G of vesicular stomatitis virus through the Golgi apparatus as visualized by electron microscope radioautography. J Cell Biol 94:36–41PubMedCrossRefGoogle Scholar
  13. 13.
    Bergmann JE, Tokuyasu KT, Singer SJ (1981) Passage of an integral membrane protein, the vesicular stomatitis virus glycoprotein, through the Golgi apparatus en route to the plasma membrane. Proc Natl Acad Sci USA 78:1746–1750PubMedCrossRefGoogle Scholar
  14. 14.
    Rindler MJ, Ivanov IE, Rodriguez Boulan E, Sabatini DD (1981) Simultaneous budding of viruses with opposite polarity from doubly-infected MDCK cells. J Cell Biol 91:118aGoogle Scholar
  15. 15.
    Tartakoff AM (1983) Perturbation of vesicular traffic with the carboxylic ionophore monensin. Cell 32:1026–1028PubMedCrossRefGoogle Scholar
  16. 16.
    Alonso FV, Compans RW (1981) Differential effect of monensin on enveloped viruses that form at distinct plasma membrane domains. J Cell Biol 89:700–705PubMedCrossRefGoogle Scholar
  17. 17.
    Alonso-Caplen FV, Compans RW (1983) Modulation of glycosylation and transport of viral membrane glycoproteins by a sodium ionophore. J Cell Biol 97:659–668.PubMedCrossRefGoogle Scholar
  18. 18.
    Roth MG, Compans RW (1981) Delayed appearance of pseudotypes between vesicular stomatitis virus and influenza virus during mixed infection of MDCK cells. J Virol 40:848–860PubMedGoogle Scholar
  19. 19.
    Farquhar MG (1983) Multiple pathways of exocytosis, endocytosis, and membrane recycling: Validation of a Golgi route. Fed Proc 42:2407–2413PubMedGoogle Scholar
  20. 20.
    Rothman JE, Pettegrew HG, Fine RE (1980) Transport of the membrane glycoprotein of the vesicular stomatitis virus to the cell surface in two stages by clathrin-coated vesicles. J Cell Biol 86:162–171PubMedCrossRefGoogle Scholar
  21. 21.
    Roth MG, Compans RW (1980) Antibody-resistant spread of vesicular stomatitis virus infection in cell lines of epithelial origin. J Virol 35:547–550PubMedGoogle Scholar
  22. 22.
    Holmes KV, Choppin PW (1966) On the role of the response of the cell membrane in determining virus virulence. Contrasting effects of the parainfluenza SV5 in two cell types. J Exp Med 124:501–520PubMedCrossRefGoogle Scholar
  23. 23.
    Compans RW, Roth MG, Alonso FV, Srinivas RV, Herrler G, Melsen LR (1982) Do viral maturation sites influence disease processes? In Mackenzie JS (ed) Viral Disease in Southeast Asia and the Western Pacific, Academic Press, Australia, p 328Google Scholar
  24. 24.
    Basak S, Melsen LR, Alonso-Caplen FV, Compans RW (1983) Maturation sites of human and avian influenza viruses in polarized epithelial cells. In Laver WG (ed) The Origin of Pandemic Influenza Viruses. Elsevier, New York, pp 139–145Google Scholar
  25. 25.
    Webster RG, Yakhno M, Hinshaw VS, Bean WJ, Murti KG (1978) Intestinal influenza: Replication and characterization of influenza viruses in ducks. Virology 84:268–278PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag New York Inc. 1984

Authors and Affiliations

  • Richard W. Compans
    • 1
  1. 1.University of Alabama in BirminghamUSA

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