Skip to main content
PMC home page
Journal of Virology logoLink to Journal of Virology
. 1997 Jul;71(7):5481–5486. doi: 10.1128/jvi.71.7.5481-5486.1997

Sendai virus efficiently infects cells via the asialoglycoprotein receptor and requires the presence of cleaved F0 precursor proteins for this alternative route of cell entry.

M Bitzer 1, U Lauer 1, C Baumann 1, M Spiegel 1, M Gregor 1, W J Neubert 1
PMCID: PMC191789  PMID: 9188621

Abstract

Biochemical evidence suggests that the asialoglycoprotein receptor (ASGP-R) can be used as an alternative receptor for a temperature-sensitive Sendai virus (SV) mutant. We now have investigated this possible alternative route of infection for SV wild-type (SV-wt) strain Fushimi by using a pair of cell lines which differ only with regard to ASGP-R expression. Infection studies after enzymatic destruction of conventional sialic acid-containing SV receptors (SA-R) revealed that only ASGP-R-expressing cells could be infected by SV-wt. This alternative route of cell entry could be completely blocked by incubation of cells with ASGP-R-specific antibodies prior to infection. Furthermore, cleavage of SV-F0 precursor protein into the subunits F1 and F2 was necessary to establish infection via ASGP-R, suggesting a fusion-mediated cell entry after binding of SV-wt to the ASGP-R on host cells. Interestingly, infection via ASGP-R was found to be nearly as efficient as infection via conventional sialic acid-containing SV receptors. A possible physiological role of the ASGP-R-mediated route of SV infection is discussed.

Full Text

The Full Text of this article is available as a PDF (483.5 KB).

Selected References

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

  1. Bagai S., Sarkar D. P. Fusion-mediated microinjection of lysozyme into HepG2 cells through hemagglutinin neuraminidase-depleted Sendai virus envelopes. J Biol Chem. 1994 Jan 21;269(3):1966–1972. [PubMed] [Google Scholar]
  2. Bagai S., Sarkar D. P. Reconstituted Sendai virus envelopes as biological carriers: dual role of F protein in binding and fusion with liver cells. Biochim Biophys Acta. 1993 Oct 10;1152(1):15–25. doi: 10.1016/0005-2736(93)90226-p. [DOI] [PubMed] [Google Scholar]
  3. Becker S., Spiess M., Klenk H. D. The asialoglycoprotein receptor is a potential liver-specific receptor for Marburg virus. J Gen Virol. 1995 Feb;76(Pt 2):393–399. doi: 10.1099/0022-1317-76-2-393. [DOI] [PubMed] [Google Scholar]
  4. Chowdhury N. R., Wu C. H., Wu G. Y., Yerneni P. C., Bommineni V. R., Chowdhury J. R. Fate of DNA targeted to the liver by asialoglycoprotein receptor-mediated endocytosis in vivo. Prolonged persistence in cytoplasmic vesicles after partial hepatectomy. J Biol Chem. 1993 May 25;268(15):11265–11271. [PubMed] [Google Scholar]
  5. Feldmann H., Nichol S. T., Klenk H. D., Peters C. J., Sanchez A. Characterization of filoviruses based on differences in structure and antigenicity of the virion glycoprotein. Virology. 1994 Mar;199(2):469–473. doi: 10.1006/viro.1994.1147. [DOI] [PubMed] [Google Scholar]
  6. Fuhrer C., Geffen I., Huggel K., Spiess M. The two subunits of the asialoglycoprotein receptor contain different sorting information. J Biol Chem. 1994 Feb 4;269(5):3277–3282. [PubMed] [Google Scholar]
  7. Garcin D., Pelet T., Calain P., Roux L., Curran J., Kolakofsky D. A highly recombinogenic system for the recovery of infectious Sendai paramyxovirus from cDNA: generation of a novel copy-back nondefective interfering virus. EMBO J. 1995 Dec 15;14(24):6087–6094. doi: 10.1002/j.1460-2075.1995.tb00299.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Geffen I., Spiess M. Asialoglycoprotein receptor. Int Rev Cytol. 1992;137B:181–219. doi: 10.1016/s0074-7696(08)62605-4. [DOI] [PubMed] [Google Scholar]
  9. Homma M., Ouchi M. Trypsin action on the growth of Sendai virus in tissue culture cells. 3. Structural difference of Sendai viruses grown in eggs and tissue culture cells. J Virol. 1973 Dec;12(6):1457–1465. doi: 10.1128/jvi.12.6.1457-1465.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Lamb R. A. Paramyxovirus fusion: a hypothesis for changes. Virology. 1993 Nov;197(1):1–11. doi: 10.1006/viro.1993.1561. [DOI] [PubMed] [Google Scholar]
  11. Markwell M. A., Paulson J. C. Sendai virus utilizes specific sialyloligosaccharides as host cell receptor determinants. Proc Natl Acad Sci U S A. 1980 Oct;77(10):5693–5697. doi: 10.1073/pnas.77.10.5693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Markwell M. A., Portner A., Schwartz A. L. An alternative route of infection for viruses: entry by means of the asialoglycoprotein receptor of a Sendai virus mutant lacking its attachment protein. Proc Natl Acad Sci U S A. 1985 Feb;82(4):978–982. doi: 10.1073/pnas.82.4.978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Massion P. P., Funari C. C., Ueki I., Ikeda S., McDonald D. M., Nadel J. A. Parainfluenza (Sendai) virus infects ciliated cells and secretory cells but not basal cells of rat tracheal epithelium. Am J Respir Cell Mol Biol. 1993 Oct;9(4):361–370. doi: 10.1165/ajrcmb/9.4.361. [DOI] [PubMed] [Google Scholar]
  14. Neubert W. J., Hofschneider P. H. Transient rescue of Sendai-6/94 cl virus from the persistently infected cell line Cl-E-8 by cocultivation. Virology. 1983 Mar;125(2):445–453. doi: 10.1016/0042-6822(83)90215-5. [DOI] [PubMed] [Google Scholar]
  15. Portner A., Marx P. A., Kingsbury D. W. Isolation and characterization of Sendai virus temperature-sensitive mutants. J Virol. 1974 Feb;13(2):298–304. doi: 10.1128/jvi.13.2.298-304.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Portner A., Scroggs R. A., Marx P. S., Kingsbury D. W. A temperature-sensitive mutant of Sendai virus with an altered hemagglutinin-neuraminidase polypeptide: consequences for virus assembly and cytopathology. Virology. 1975 Sep;67(1):179–187. doi: 10.1016/0042-6822(75)90415-8. [DOI] [PubMed] [Google Scholar]
  17. Scheid A., Choppin P. W. Identification of biological activities of paramyxovirus glycoproteins. Activation of cell fusion, hemolysis, and infectivity of proteolytic cleavage of an inactive precursor protein of Sendai virus. Virology. 1974 Feb;57(2):475–490. doi: 10.1016/0042-6822(74)90187-1. [DOI] [PubMed] [Google Scholar]
  18. Seglen P. O. Inhibitors of lysosomal function. Methods Enzymol. 1983;96:737–764. doi: 10.1016/s0076-6879(83)96063-9. [DOI] [PubMed] [Google Scholar]
  19. Shia M. A., Lodish H. F. The two subunits of the human asialoglycoprotein receptor have different fates when expressed alone in fibroblasts. Proc Natl Acad Sci U S A. 1989 Feb;86(4):1158–1162. doi: 10.1073/pnas.86.4.1158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Sigmund M., Einberger H., Neubert W. J. Simple method for rapid and highly sensitive detection of antiviral-antibodies in serum and cerebrospinal fluid of small laboratory animals. J Virol Methods. 1988 Dec;22(2-3):231–238. doi: 10.1016/0166-0934(88)90105-x. [DOI] [PubMed] [Google Scholar]
  21. Stockert R. J., Morell A. G., Scheinberg I. H. Hepatic binding protein: the protective role of its sialic acid residues. Science. 1977 Aug 12;197(4304):667–668. doi: 10.1126/science.877581. [DOI] [PubMed] [Google Scholar]
  22. Stockert R. J., Morell A. G. Second messenger modulation of the asialoglycoprotein receptor. J Biol Chem. 1990 Feb 5;265(4):1841–1846. [PubMed] [Google Scholar]
  23. Stockert R. J. The asialoglycoprotein receptor: relationships between structure, function, and expression. Physiol Rev. 1995 Jul;75(3):591–609. doi: 10.1152/physrev.1995.75.3.591. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. Tuffereau C., Portner A., Roux L. The role of haemagglutinin-neuraminidase glycoprotein cell surface expression in the survival of Sendai virus-infected BHK-21 cells. J Gen Virol. 1985 Nov;66(Pt 11):2313–2318. doi: 10.1099/0022-1317-66-11-2313. [DOI] [PubMed] [Google Scholar]
  27. VOGEL J., SHELOKOV A. Adsorption-hemagglutination test for influenza virus in monkey kidney tissue culture. Science. 1957 Aug 23;126(3269):358–359. doi: 10.1126/science.126.3269.358-a. [DOI] [PubMed] [Google Scholar]
  28. Wu G. Y., Wu C. H. Delivery systems for gene therapy. Biotherapy. 1991;3(1):87–95. doi: 10.1007/BF02175102. [DOI] [PubMed] [Google Scholar]
  29. Wu G. Y., Wu C. H. Targeted delivery and expression of foreign genes in hepatocytes. Targeted Diagn Ther. 1991;4:127–149. [PubMed] [Google Scholar]
  30. Yoshima H., Nakanishi M., Okada Y., Kobata A. Carbohydrate structures of HVJ (Sendai virus) glycoproteins. J Biol Chem. 1981 Jun 10;256(11):5355–5361. [PubMed] [Google Scholar]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES