1887

Journal of General Virology header logo

Volume 78, Issue 1

Mouse hepatitis virus strain A59 is released from opposite sides of different epithelial cell types Free

Abstract

Coronaviruses infect humans and animals through epithelial cells of the gastrointestinal and respiratory tracts that serve as their primary target. When studying infections in cultured polarized epithelial cells, we found previously that coronaviruses are released from specific plasma-membrane domains; thus, mouse hepatitis virus (strain A59; MHV-A59) leaves murine epithelial kidney cells from the baso- lateral surface, whereas release of transmissible gastroenteritis virus from porcine epithelial kidney cells is confined to the apical membrane. This observation begged the question whether a particular coronavirus is consistently shed through the same membrane, irrespective of the nature of the epithelial cell. We therefore extended our studies with MHV-A59 to Madin-Darby canine kidney (MDCK) strain I and human colon carcinoma (Caco-2) cells, both of which are naturally refractory to MHV-A59 but were made susceptible to infection by transfection with recombinant MHV receptor cDNA. The release of MHV-A59 from Caco cells occurred preferentially from the basolateral side, consistent with our previous observations. In contrast, release from MDCK cells occurred almost exclusively from the apical surface. Because of this difference, we studied MHV-A59 infection of MDCK cells in more detail. The virus entered the cells preferentially from the apical side, a situation similar to that in murine epithelial cells, where the highest density of MHV receptor glycoprotein was found. The results from this and previous studies show that targeting of vesicles containing MHV-A59 to a specific side of epithelial cells may vary in different epithelial cell types.

  • Published Online:
© Society for General Microbiology Ltd 1997
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-1-61
1997-01-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/1/9010286.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-1-61&mimeType=html&fmt=ahah

References

  1. Blau D. M., Compans R. W. 1995; Entry and release of measles virus are polarized in epithelial cells. Virology 210:91–99
     [Google Scholar]
  2. Brown W. J., Constantinescu E., Farquhar M. G. 1984; Redistribution of mannose-6-phosphate receptors induced by tunicamycin and chloroquine. Journal of Cell Biology 99:320–326
     [Google Scholar]
  3. Caplan M. J., Stow J. L., Newman A. P., Madri J., Anderson C., Farquhar M. G., Palade G. E., Jamieson J. D. 1987; Dependence on pH of polarized sorting of secreted proteins. Nature 329:632–635
     [Google Scholar]
  4. Cavanagh D. 1995; The coronavirus surface glycoprotein. In The Coronaviridae pp 73–113 Siddell S. G. Edited by New York: Plenum Press;
     [Google Scholar]
  5. Cerneus D. P., Strous G. J., van der Ende A. 1993; Bidirectional transcytosis determines the steady state distribution of the transferrin receptor at opposite plasma membrane domains of BeWo cells. Journal of Cell Biology 122:1223–1230
     [Google Scholar]
  6. Compans R. W., Srinivas R. V. 1991; Protein sorting in polarized epithelial cells. Current Topics in Microbiology and Immunology 170:141–181
     [Google Scholar]
  7. De Almeida J. B., Stow J. L. 1991; Disruption of microtubules alters polarity of basement membrane proteoglycan secretion in epithelial cells. American Journal of Physiology 260:C691–C700
     [Google Scholar]
  8. Dveksler G. S., Dieffenbach C. W., Cardellichio C. B., McCuaig K., Pensiero M. N., Jiang G. S., Beauchemin N., Holmes K. V. 1993; Several members of the mouse carcinoembryonic antigen-related glycoprotein family are functional receptors for the coronavirus mouse hepatitis virus-A59. Journal of Virology 67:1–8
     [Google Scholar]
  9. Eaton S., Simons K. 1995; Apical, basal, and lateral cues for epithelial polarization. Cell 82:5–8
     [Google Scholar]
  10. Fuller S. D., von Bonsdorff C.-H., Simons K. 1984; Vesicular stomatitis virus infects and matures only through the basolateral surface of the polarized epithelial cell line, MDCK. Cell 38:65–77
     [Google Scholar]
  11. Gagneten S., Gout O., Dubois-Dalcq M., Rottier P. J. M., Rossen J. W. A., Holmes K. V. 1995; Interaction of mouse hepatitis virus (MHV) spike glycoprotein with receptor glycoprotein MHVR is required for infection with an MHV strain that expresses the hemagglutinin- esterase glycoprotein. Journal of Virology 69:889–895
     [Google Scholar]
  12. Gottlieb T. A., Beaudry T. A. G., Rizzolo L., Coleman A., Rindler M., Adesnik M., Sabatini D. D. 1986; Secretion of endogenous and exogenous proteins from polarized MDCK cell monolayers. Proceedings of the National Academy of Sciences USA: 832100–2104
     [Google Scholar]
  13. Holmes K. V. 1990; Coronaviridae and their replication. In Virology, 2nd edn.. pp 841–856 Fields B. N., Knipe D. M., Chanock R. M., Hirsch M. S., Melnick J. L., Monath T. P., Roizman B. Edited by New York: Raven Press;
     [Google Scholar]
  14. Klumperman J., Krijnse-Locker J., Meijer A., Horzinek M. C., Geuze H. J., Rottier P. J. M. 1994; Coronavirus M proteins accumulate in the Golgi complex beyond the site of virion budding. Journal of Virology 68:6523–6534
     [Google Scholar]
  15. Kondor-Koch C., Bravo R., Fuller S. D., Cutler D., Garoff H. 1985; Exocytic pathways exist to both the apical and the basolateral cell surfaces of the polarized epithelial cell MDCK. Cell 43:297–306
     [Google Scholar]
  16. Krijnse-Locker J., Ericsson M., Rottier P. J. M., Griffiths G. 1994; Characterization of the budding compartment of mouse hepatitis virus: evidence that transport from the RER to the Golgi complex requires only one vesicular transport step. Journal of Cell Biology 124:55–70
     [Google Scholar]
  17. Low S. H., Wong S. H., Tang B. L., Hong W. 1994; Effects of NH4Cl and nocadozole on polarized fibronectin secretion vary amongst different epithelial cell types. Molecular Membrane Biology 11:45–54
     [Google Scholar]
  18. Matter K., Mellman I. 1994; Mechanisms of cell polarity: sorting and transport in epithelial cells. Current Opinion in Cell Biology 6:545–554
     [Google Scholar]
  19. Mays R. W., Beck K. A., Nelson W. J. 1994; Organization and function of the cytoskeleton in polarized epithelial cells: a component of the protein sorting machinery. Current Opinion in Cell Biology 6:16–24
     [Google Scholar]
  20. Mostov K. E., Cardone M. H. 1995; Regulat ion of protein traffic in polarized epithelial cells. Bioessays 17:129–138
     [Google Scholar]
  21. Rindler M. J., Traber M. G. 1988; A specific sorting signal is not required for the polarized secretion of newly synthesized proteins from cultured intestinal epithelial cells. Journal of Cell Biology 107:471–479
     [Google Scholar]
  22. Rodriguez-Boulan E., Sabatini D. D. 1978; Asymmetric budding of viruses in epithelial monolayers : a model system for study of epithelial polarity. Proceedings of the National Academy of Sciences USA: 755071–5075
     [Google Scholar]
  23. Rossen J. W. A., Bekker C. P. J., Voorhout W. F., Strous G. J. A. M., van der Ende A., Rottier P. J. M. 1994; Entry and release of transmissible gastroenteritis coronavirus are restricted to apical surfaces of polarized epithelial cells. Journal of Virology 68:7966–7973
     [Google Scholar]
  24. Rossen J. W. A., Bekker C. P. J., Voorhout W. F., Horzinek M. C., Strous G. J. A. M., van der Ende A., Rottier P. J. M. 1995a; .Coronaviruses in polarized epithelial cells. Advances in Experimental Medicine and Biology 380:135–138
     [Google Scholar]
  25. Rossen J. W. A., Horzinek M. C., Rottier P. J. M. 1995b; Coronavirus infection of polarized epithelial cells. Trends in Microbiology 3:486–490
     [Google Scholar]
  26. Rossen J. W. A., Voorhout W. F., Horzinek M. C., van der Ende A., Strous G. J. A. M., Rottier P. J. M. 1995c; MHV-A59 enters polarized murine epithelial cells through the apical surface but is released basolaterally. Virology 210:54–66
     [Google Scholar]
  27. Rottier P. J. M., Spaan W. J. M., Horzinek M. C., van der Zeijst B. A. M. 1981; Translation of three mouse hepatitis virus strain A59 subgenomic RNAs in Xenopus laevis oocytes. Journal of Virology 38:20–26
     [Google Scholar]
  28. Simons K., Wandinger-Ness A. 1990; Polarized sorting in epithelia. Cell 62:207–210
     [Google Scholar]
  29. Spaan W. J. M., Rottier P. J. M., Horzinek M. C., van der Zeijst B. A. M. 1981; Isolation and identification of virus-specific mRNAs in cells infected with mouse hepatitis virus (MHV-A59). Virology 108:424–434
     [Google Scholar]
  30. Tooze J., Tooze S. A., Warren G. 1984; Replication of coronavirus MHV-A59 in sac cells: determination of the first site of budding of progeny virions. European Journal of Cell Biology 33:281–293
     [Google Scholar]
  31. Tooze J., Tooze S. A., Fuller S. D. 1987; Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans - Golgi network of AtT20 cells. Journal of Cell Biology 105:1215–1226
     [Google Scholar]
  32. Traber M. G., Kayden H. J., Rindler M. J. 1987; Polarized secretion of newly synthesized lipoproteins by the Caco-2 human intestinal cell line. Journal of Lipid Research 28:1350–1363
     [Google Scholar]
  33. Tucker S. P., Compans R. W. 1993; Virus infection of polarized epithelial cells. Advances in Virus Research 42:187–247
     [Google Scholar]
  34. Tucker S. P., Melsen L. R., Compans R. W. 1992; Migration of polarized epithelial cells through permeable membrane substrates of defined pore size. European Journal of Cell Biology 58:280–290
     [Google Scholar]
  35. Van Meer G., Simons K. 1982; Viruses budding from either the apical or basolateral plasma membrane domain of MDCK cells have unique phospholipid compositions. EMBO Journal 1:847–852
     [Google Scholar]
  36. Weaver S. C., Tesh R. B., Guzman H. 1992; Ultrastructural aspects of replication of New Jersey serotype of vesicular stomatitis virus in a suspected sand fly vector, Lutzomyia shannoni (Diptera: Psychodidae). American Journal of Tropical Medicine and Hygiene 46:201–210
     [Google Scholar]
  37. Williams R. K., Jiang G.-S., Snyder S. W., Frana M. F., Holmes K. V. 1990; Purification of the 110-kilodalton glycoprotein receptor for mouse hepatitis virus (MHV)-A59 from mouse liver and identification of a nonfunctional, homologous protein in MHV-resistant SJL/J mice. Journal of Virology 64:3817–3823
     [Google Scholar]
  38. Yokomori K., Lai M. M. C. 1992; The receptor for mouse hepatitis virus in the resistant mouse strain SJL is functional: implications for the requirement of a second factor for viral infection. Journal of Virology 66:6931–6938
     [Google Scholar]
  39. Yokomori K., Assanaka M., Stohlman S. A., Lai M. M. C. 1993; A spike protein-dependent cellular factor other than the viral receptor is required for mouse hepatitis virus entry. Virology 196:45–56
     [Google Scholar]
  40. Zurzolo C., Polistina C., Saini M., Gentile R., Aloj L., Migliaccio G., Bonatti S., Nitsch L. 1992; Opposite polarity of virus budding and of viral envelope glycoprotein distribution in epithelial cells derived from different tissues. Journal of Cell Biology 117:551–564
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-78-1-61
Loading
Mouse hepatitis virus strain A59 is released from opposite sides of different epithelial cell types
J. Gen. Virol. 78, 61 (1997); https://doi.org/10.1099/0022-1317-78-1-61
/content/journal/jgv/10.1099/0022-1317-78-1-61
/content/journal/jgv/10.1099/0022-1317-78-1-61
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error