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. 1990 Oct;64(10):4672–4677. doi: 10.1128/jvi.64.10.4672-4677.1990

Altered budding site of a pantropic mutant of Sendai virus, F1-R, in polarized epithelial cells.

M Tashiro 1, M Yamakawa 1, K Tobita 1, J T Seto 1, H D Klenk 1, R Rott 1
PMCID: PMC247951  PMID: 2168957

Abstract

A protease activation mutant of Sendai virus, F1-R, causes a systemic infection in mice, whereas wild-type virus is exclusively pneumotropic (M. Tashiro, E. Pritzer, M. A. Khoshnan, M. Yamakawa, K. Kuroda, H.-D. Klenk, R. Rott, and J. T. Seto, Virology 165:577-583, 1988). Budding of F1-R has been observed bidirectionally at the apical and basolateral surfaces of the bronchial epithelium of mice and of MDCK cells, whereas wild-type virus buds apically (M. Tashiro, M. Yamakawa, K. Tobita, H.-D. Klenk, R. Rott, and J. T. Seto, J. Virol. 64:3627-3634, 1990). In this study, wild-type virus was shown to be produced primarily from the apical site of polarized MDCK cells grown on permeable membrane filters. Surface immunofluorescence and immunoprecipitation analyses revealed that transmembrane glycoproteins HN and F were expressed predominantly at the apical domain of the plasma membrane. On the other hand, infectious progeny of F1-R was released from the apical and basolateral surfaces, and HN and F were expressed at both regions of the cells. Since F1-R has amino acid substitutions in F and M proteins but none in HN, the altered budding of the virus and transport of the envelope glycoproteins might be attributed to interactions by F and M proteins. These findings suggest that in addition to proteolytic activation of the F glycoprotein, the differential site of budding, at the primary target of infection, is a determinant for organ tropism of Sendai virus in mice.

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Selected References

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  1. Balcarova-Ständer J., Pfeiffer S. E., Fuller S. D., Simons K. Development of cell surface polarity in the epithelial Madin-Darby canine kidney (MDCK) cell line. EMBO J. 1984 Nov;3(11):2687–2694. doi: 10.1002/j.1460-2075.1984.tb02194.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bergmann J. E., Fusco P. J. The M protein of vesicular stomatitis virus associates specifically with the basolateral membranes of polarized epithelial cells independently of the G protein. J Cell Biol. 1988 Nov;107(5):1707–1715. doi: 10.1083/jcb.107.5.1707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Choppin P. W., Scheid A. The role of viral glycoproteins in adsorption, penetration, and pathogenicity of viruses. Rev Infect Dis. 1980 Jan-Feb;2(1):40–61. doi: 10.1093/clinids/2.1.40. [DOI] [PubMed] [Google Scholar]
  4. Fuller S., von Bonsdorff C. H., Simons K. Vesicular stomatitis virus infects and matures only through the basolateral surface of the polarized epithelial cell line, MDCK. Cell. 1984 Aug;38(1):65–77. doi: 10.1016/0092-8674(84)90527-0. [DOI] [PubMed] [Google Scholar]
  5. Ishida N., Homma M. Sendai virus. Adv Virus Res. 1978;23:349–383. doi: 10.1016/s0065-3527(08)60103-7. [DOI] [PubMed] [Google Scholar]
  6. Middleton Y., Tashiro M., Thai T., Oh J., Seymour J., Pritzer E., Klenk H. D., Rott R., Seto J. T. Nucleotide sequence analyses of the genes encoding the HN, M, NP, P, and L proteins of two host range mutants of Sendai virus. Virology. 1990 Jun;176(2):656–657. doi: 10.1016/0042-6822(90)90040-x. [DOI] [PubMed] [Google Scholar]
  7. Nagai Y., Klenk H. D., Rott R. Proteolytic cleavage of the viral glycoproteins and its significance for the virulence of Newcastle disease virus. Virology. 1976 Jul 15;72(2):494–508. doi: 10.1016/0042-6822(76)90178-1. [DOI] [PubMed] [Google Scholar]
  8. Nayak D. P., Jabbar M. A. Structural domains and organizational conformation involved in the sorting and transport of influenza virus transmembrane proteins. Annu Rev Microbiol. 1989;43:465–501. doi: 10.1146/annurev.mi.43.100189.002341. [DOI] [PubMed] [Google Scholar]
  9. Orvell C., Grandien M. The effects of monoclonal antibodies on biologic activities of structural proteins of Sendai virus. J Immunol. 1982 Dec;129(6):2779–2787. [PubMed] [Google Scholar]
  10. Richardson J. C., Scalera V., Simmons N. L. Identification of two strains of MDCK cells which resemble separate nephron tubule segments. Biochim Biophys Acta. 1981 Feb 18;673(1):26–36. [PubMed] [Google Scholar]
  11. Rodriguez Boulan E., Sabatini D. D. Asymmetric budding of viruses in epithelial monlayers: a model system for study of epithelial polarity. Proc Natl Acad Sci U S A. 1978 Oct;75(10):5071–5075. doi: 10.1073/pnas.75.10.5071. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rose J. K., Doms R. W. Regulation of protein export from the endoplasmic reticulum. Annu Rev Cell Biol. 1988;4:257–288. doi: 10.1146/annurev.cb.04.110188.001353. [DOI] [PubMed] [Google Scholar]
  13. Simons K., Fuller S. D. Cell surface polarity in epithelia. Annu Rev Cell Biol. 1985;1:243–288. doi: 10.1146/annurev.cb.01.110185.001331. [DOI] [PubMed] [Google Scholar]
  14. 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]
  15. Tashiro M., Homma M. Evidence of proteolytic activation of Sendai virus in mouse lung. Arch Virol. 1983;77(2-4):127–137. doi: 10.1007/BF01309262. [DOI] [PubMed] [Google Scholar]
  16. Tashiro M., Homma M. Pneumotropism of Sendai virus in relation to protease-mediated activation in mouse lungs. Infect Immun. 1983 Feb;39(2):879–888. doi: 10.1128/iai.39.2.879-888.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Tashiro M., Pritzer E., Khoshnan M. A., Yamakawa M., Kuroda K., Klenk H. D., Rott R., Seto J. T. Characterization of a pantropic variant of Sendai virus derived from a host range mutant. Virology. 1988 Aug;165(2):577–583. doi: 10.1016/0042-6822(88)90601-0. [DOI] [PubMed] [Google Scholar]
  18. Tashiro M., Tobita K., Seto J. T., Rott R. Comparison of protective effects of serum antibody on respiratory and systemic infection of Sendai virus in mice. Arch Virol. 1989;107(1-2):85–96. doi: 10.1007/BF01313881. [DOI] [PubMed] [Google Scholar]
  19. Tashiro M., Yamakawa M., Tobita K., Klenk H. D., Rott R., Seto J. T. Organ tropism of Sendai virus in mice: proteolytic activation of the fusion glycoprotein in mouse organs and budding site at the bronchial epithelium. J Virol. 1990 Aug;64(8):3627–3634. doi: 10.1128/jvi.64.8.3627-3634.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tozawa H., Komatsu H., Ohkata K., Nakajima T., Watanabe M., Tanaka Y., Arifuku M. Neutralizing activity of the antibodies against two kinds of envelope glycoproteins of Sendai virus. Arch Virol. 1986;91(1-2):145–161. doi: 10.1007/BF01316735. [DOI] [PubMed] [Google Scholar]
  21. Yoshida T., Nagai Y'Yoshii S., Maeno K., Matsumoto T. Membrane (M) protein of HVJ (Sendai virus): its role in virus assembly. Virology. 1976 May;71(1):143–161. doi: 10.1016/0042-6822(76)90101-x. [DOI] [PubMed] [Google Scholar]
  22. Zuk A., Matlin K. S., Hay E. D. Type I collagen gel induces Madin-Darby canine kidney cells to become fusiform in shape and lose apical-basal polarity. J Cell Biol. 1989 Mar;108(3):903–919. doi: 10.1083/jcb.108.3.903. [DOI] [PMC free article] [PubMed] [Google Scholar]

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