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. 1993 Jun;67(6):3319–3325. doi: 10.1128/jvi.67.6.3319-3325.1993

Dissociation of progeny vaccinia virus from the cell membrane is regulated by a viral envelope glycoprotein: effect of a point mutation in the lectin homology domain of the A34R gene.

R Blasco 1, J R Sisler 1, B Moss 1
PMCID: PMC237674  PMID: 8497053

Abstract

Vaccinia virus strains vary considerably in the amounts of extracellular enveloped virus (EEV) that they release from infected cells. The IHD-J strain produces up to 40 times more EEV than does the related WR strain and consequently generates elongated comet-shaped virus plaques instead of sharply defined round ones in susceptible monolayer cells under liquid medium. The difference in EEV formation is due to the retention of enveloped WR virions on the cell surface (R. Blasco and B. Moss, J. Virol. 66:4170-4179, 1992). By using WR and IHD-J DNA fragments for marker transfer and analyzing the progeny virus by the comet formation assay, we determined that gene A34R and at least one other gene regulate the release of cell-associated virions. Replacement of the A34R gene of WR with the corresponding gene from IHD-J increased the amount of EEV produced by 10-fold and conferred the ability to form distinctive comet-shaped plaques. Gene A34R encodes an EEV-specific glycoprotein with homology to C-type animal lectins (S.A. Duncan and G.L. Smith, J. Virol. 66:1610-1621, 1992). The nucleotide sequences of the A34R genes of WR and IHD-J strains differed in six positions, of which four were silent. One of the codon mutations (Lys-151-->Glu), which is located in the putative carbohydrate recognition domain, was sufficient to transfer a comet-forming phenotype to WR virus. These data indicate that the A34R-encoded glycoprotein is involved, through its lectin homology domain, in the retention of progeny virus on the surface of parental cells and raise the possibility that the protein also has a role in virus attachment to uninfected cells.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aguado B., Selmes I. P., Smith G. L. Nucleotide sequence of 21.8 kbp of variola major virus strain Harvey and comparison with vaccinia virus. J Gen Virol. 1992 Nov;73(Pt 11):2887–2902. doi: 10.1099/0022-1317-73-11-2887. [DOI] [PubMed] [Google Scholar]
  2. Blasco R., Moss B. 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. J Virol. 1991 Nov;65(11):5910–5920. doi: 10.1128/jvi.65.11.5910-5920.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blasco R., Moss B. Role of cell-associated enveloped vaccinia virus in cell-to-cell spread. J Virol. 1992 Jul;66(7):4170–4179. doi: 10.1128/jvi.66.7.4170-4179.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Boulter E. A., Appleyard G. Differences between extracellular and intracellular forms of poxvirus and their implications. Prog Med Virol. 1973;16:86–108. [PubMed] [Google Scholar]
  5. DeFilippes F. M. Restriction enzyme mapping of vaccinia virus DNA. J Virol. 1982 Jul;43(1):136–149. doi: 10.1128/jvi.43.1.136-149.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Drickamer K. Two distinct classes of carbohydrate-recognition domains in animal lectins. J Biol Chem. 1988 Jul 15;263(20):9557–9560. [PubMed] [Google Scholar]
  7. Duncan S. A., Smith G. L. Identification and characterization of an extracellular envelope glycoprotein affecting vaccinia virus egress. J Virol. 1992 Mar;66(3):1610–1621. doi: 10.1128/jvi.66.3.1610-1621.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Engelstad M., Howard S. T., Smith G. L. A constitutively expressed vaccinia gene encodes a 42-kDa glycoprotein related to complement control factors that forms part of the extracellular virus envelope. Virology. 1992 Jun;188(2):801–810. doi: 10.1016/0042-6822(92)90535-w. [DOI] [PubMed] [Google Scholar]
  9. Fathi Z., Sridhar P., Pacha R. F., Condit R. C. Efficient targeted insertion of an unselected marker into the vaccinia virus genome. Virology. 1986 Nov;155(1):97–105. doi: 10.1016/0042-6822(86)90171-6. [DOI] [PubMed] [Google Scholar]
  10. Goebel S. J., Johnson G. P., Perkus M. E., Davis S. W., Winslow J. P., Paoletti E. The complete DNA sequence of vaccinia virus. Virology. 1990 Nov;179(1):247-66, 517-63. doi: 10.1016/0042-6822(90)90294-2. [DOI] [PubMed] [Google Scholar]
  11. Hiller G., Eibl H., Weber K. Characterization of intracellular and extracellular vaccinia virus variants: N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine interferes with cytoplasmic virus dissemination and release. J Virol. 1981 Sep;39(3):903–913. doi: 10.1128/jvi.39.3.903-913.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hirt P., Hiller G., Wittek R. Localization and fine structure of a vaccinia virus gene encoding an envelope antigen. J Virol. 1986 Jun;58(3):757–764. doi: 10.1128/jvi.58.3.757-764.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Ichihashi Y., Matsumoto S., Dales S. Biogenesis of poxviruses: role of A-type inclusions and host cell membranes in virus dissemination. Virology. 1971 Dec;46(3):507–532. doi: 10.1016/0042-6822(71)90056-0. [DOI] [PubMed] [Google Scholar]
  14. Isaacs S. N., Wolffe E. J., Payne L. G., Moss B. Characterization of a vaccinia virus-encoded 42-kilodalton class I membrane glycoprotein component of the extracellular virus envelope. J Virol. 1992 Dec;66(12):7217–7224. doi: 10.1128/jvi.66.12.7217-7224.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Jones E. V., Puckett C., Moss B. DNA-dependent RNA polymerase subunits encoded within the vaccinia virus genome. J Virol. 1987 Jun;61(6):1765–1771. doi: 10.1128/jvi.61.6.1765-1771.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Morgan C. Vaccinia virus reexamined: development and release. Virology. 1976 Aug;73(1):43–58. doi: 10.1016/0042-6822(76)90059-3. [DOI] [PubMed] [Google Scholar]
  17. Payne L. G. Characterization of vaccinia virus glycoproteins by monoclonal antibody precipitation. Virology. 1992 Mar;187(1):251–260. doi: 10.1016/0042-6822(92)90313-e. [DOI] [PubMed] [Google Scholar]
  18. Payne L. G. Identification of the vaccinia hemagglutinin polypeptide from a cell system yielding large amounts of extracellular enveloped virus. J Virol. 1979 Jul;31(1):147–155. doi: 10.1128/jvi.31.1.147-155.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Payne L. G., Kristenson K. Mechanism of vaccinia virus release and its specific inhibition by N1-isonicotinoyl-N2-3-methyl-4-chlorobenzoylhydrazine. J Virol. 1979 Nov;32(2):614–622. doi: 10.1128/jvi.32.2.614-622.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Payne L. G., Kristensson K. Extracellular release of enveloped vaccinia virus from mouse nasal epithelial cells in vivo. J Gen Virol. 1985 Mar;66(Pt 3):643–646. doi: 10.1099/0022-1317-66-3-643. [DOI] [PubMed] [Google Scholar]
  21. Payne L. G. Significance of extracellular enveloped virus in the in vitro and in vivo dissemination of vaccinia. J Gen Virol. 1980 Sep;50(1):89–100. doi: 10.1099/0022-1317-50-1-89. [DOI] [PubMed] [Google Scholar]
  22. Payne L. Polypeptide composition of extracellular enveloped vaccinia virus. J Virol. 1978 Jul;27(1):28–37. doi: 10.1128/jvi.27.1.28-37.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Rodriguez J. F., Smith G. L. IPTG-dependent vaccinia virus: identification of a virus protein enabling virion envelopment by Golgi membrane and egress. Nucleic Acids Res. 1990 Sep 25;18(18):5347–5351. doi: 10.1093/nar/18.18.5347. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Schmutz C., Payne L. G., Gubser J., Wittek R. A mutation in the gene encoding the vaccinia virus 37,000-M(r) protein confers resistance to an inhibitor of virus envelopment and release. J Virol. 1991 Jul;65(7):3435–3442. doi: 10.1128/jvi.65.7.3435-3442.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Shida H. Nucleotide sequence of the vaccinia virus hemagglutinin gene. Virology. 1986 Apr 30;150(2):451–462. doi: 10.1016/0042-6822(86)90309-0. [DOI] [PubMed] [Google Scholar]
  26. Smith G. L., Chan Y. S., Howard S. T. Nucleotide sequence of 42 kbp of vaccinia virus strain WR from near the right inverted terminal repeat. J Gen Virol. 1991 Jun;72(Pt 6):1349–1376. doi: 10.1099/0022-1317-72-6-1349. [DOI] [PubMed] [Google Scholar]
  27. Weis W. I., Drickamer K., Hendrickson W. A. Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature. 1992 Nov 12;360(6400):127–134. doi: 10.1038/360127a0. [DOI] [PubMed] [Google Scholar]

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