1887

Abstract

It has previously been shown that trypsinized triplelayered particles of rotavirus induce destabilization of liposomes and membrane vesicles in the absence of Ca , a condition which leads to solubilization of the outer capsid proteins of the virus. In this work, we have studied the relationship between outer capsid solubilization and permeabilization of membrane vesicles, monitoring particle and vesicle size simultaneously by changes in light scattering. Per- meabilization of intact cells induced by solubilized outer capsid proteins was monitored by following the rate of entry of ethidium bromide into the cells. Solubilized outer capsid proteins separated from double-layered particles induced vesicle permeabi- lization. Solubilization of the outer capsid preceded and was required for vesicle or cell permeabiliza- tion. Membrane damage induced by rotaviral outer proteins was not repaired upon addition of 1 mM Ca to the medium. Rotavirus infection and cell permeabilization were correlated in six different cell lines tested. This phenomenon might be related to the mechanism of virus entry into the cell. We propose a new model for rotavirus internalization based on the permeabilizing ability of outer capsid proteins and the cycling of trapped calcium in the endosomal compartment.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-78-11-2883
1997-11-01
2021-10-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/78/11/9367375.html?itemId=/content/journal/jgv/10.1099/0022-1317-78-11-2883&mimeType=html&fmt=ahah

References

  1. Bass D. M., Baylor M., Chen C., Upadhyayula U. 1995; Dansylcadaverine and cytochalasin D enhance rotavirus infection of murine L cells. Virology 212:429–437
    [Google Scholar]
  2. Carrasco L. 1995; Modification of membrane permeability by animal viruses. Advances in Virus Research 45:61–112
    [Google Scholar]
  3. Charpilienne A., Abad M. J., Michelangeli F., Alvarado F., Vasseur M., Cohen J., Ruiz M. C. 1997; Solubilized and cleaved VP7, the outer capsid protein of rotavirus, induces permeabilization of cell membrane vesicles. Journal of General Virology 78:1367–1371
    [Google Scholar]
  4. Crawford S. E., Labbé M., Cohen J., Burroughs M. H., Zhou Y. J., Estes M. K. 1994; Characterization of virus-like particles produced by the expression of rotavirus capsid proteins in insect cells. Journal of Virology 68: 5945–5952
    [Google Scholar]
  5. Diaz R., Wileman T. E., Anderson S. J., Stahl P. 1989; The use of permeabilized cells to study the ion requirements of receptor-ligand dissociation in endosomes. Biochemical Journal 260:127–134
    [Google Scholar]
  6. Dimmock N. J. 1982; Initial stages in infection with animal viruses. Journal of General Virology 59:1–22
    [Google Scholar]
  7. Estes M. K., Cohen J. 1989; Rotavirus gene structure and function. Microbiological Reviews 53:410–499
    [Google Scholar]
  8. Estes M. K., Graham D. Y., Mason R. B. 1981; Proteolytic enhancement of rotavirus infectivity: molecular mechanisms. Journal of Virology 39:879–888
    [Google Scholar]
  9. Falconer M. M., Gilbert J. M., Roper A. M., Greenberg H. B., Gavora J. S. 1995; Rotavirus-induced fusion from without in tissue culture cells. Journal of Virology 69: 5582–5591
    [Google Scholar]
  10. Fukuhara N., Yoshie O., Kitaoka S., Konno T. 1988; Role of VP3 in human rotavirus internalization after target cell attachment via VP7. Journal of Virology 62:2209–2218
    [Google Scholar]
  11. Greber U. F., Willetts M., Webster P., Helenius A. 1993; Stepwise dismantling of adenovirus 2 during entry into cells. Cell 75:477–86
    [Google Scholar]
  12. Greber U. F., Singh I., Helenius A. 1994; Mechanisms of virus uncoating. Trends in Microbiology 2:52–56
    [Google Scholar]
  13. Hauser H., Howell K., Dawson R. M. C., Bowyer D. E. 1980; Rabbit small intestinal brush border membrane preparation and lipid composition. Biochimica et Biophysica Acta 602:567–577
    [Google Scholar]
  14. Hoekstra D., Kok J. W. 1989; Entry mechanisms of enveloped viruses. Implications for fusion of intracellular membranes. Bioscience Reports 9:273–305
    [Google Scholar]
  15. Kalica A. R., Flores J., Greenberg H. B. 1983; Identification of the rotaviral gene that codes for hemagglutination and protease-enhanced plaque formation. Virology 125:194–205
    [Google Scholar]
  16. Kaljot K. T., Shaw R. D., Rubin D. H., Greenberg H. B. 1988; Infectious rotavirus enters cells by direct cell membrane penetration, not by endocytosis. Journal of Virology 62:1136–1144
    [Google Scholar]
  17. Kapikian A. Z., Chanock R. M. 1990; Rotaviruses. In Virology pp. 1353–1404 Fields B. N., Knipe D. M. Edited by New York: Raven Press;
    [Google Scholar]
  18. Labbé M., Charpilienne A., Crawford S. E., Estes M. K., Cohen J. 1991; Expression of rotavirus VP2 produces empty corelike particles. Journal of Virology 65:2946–2952
    [Google Scholar]
  19. Liprandi F., Rodriguez I., Pina C., Larralde G., Gorziglia M. 1991; VP4 monotype specificities among porcine rotavirus strains of the same VP4 serotype. Journal of Virology 65:1658–1661
    [Google Scholar]
  20. Ludert J. E., Michelangeli F., Gil F., Liprandi F., Esparza J. 1987; Penetration and uncoating of rotaviruses in cultured cells. Intervirology 27:95–101
    [Google Scholar]
  21. Ludert J. E., Feng N. G., Yu J. H., Broome R. L., Hoshino Y., Greenberg H. B. 1996; Genetic mapping indicates that VP4 is the rotavirus cell attachment protein in vitro and in vivo . Journal of Virology 70:487–493
    [Google Scholar]
  22. Mackow E. R., Barnett J. W., Chan H., Greenberg H. B. 1989; The rhesus rotavirus outer capsid protein VP4 functions as a hemagglutinin and is antigenically conserved when expressed by a baculovirus recombinant. Journal of Virology 63:1661–1668
    [Google Scholar]
  23. Matsui S. M., Offit P. A., Vo P. T., Mackow E. R., Benfield D. A., Shaw R. D., Padilla-Noriega L., Greenberg H. B. 1989; Passive protection against rotavirus-induced diarrhea by monoclonal antibodies to the heterotypic neutralization domain of VP7 and the VP8 fragment of VP4. Journal of Clinical Microbiology 27:780–782
    [Google Scholar]
  24. Nandi P., Charpilienne A., Cohen J. 1992; Interaction of rotavirus particles with liposomes. Journal of Virology 66: 3363–3367
    [Google Scholar]
  25. Offit P. A., Blavat G., Greenberg H. B., Clark H. F. 1986; Molecular basis for rotavirus virulence : role of gene segment 4. Journal of Virology 57:46–49
    [Google Scholar]
  26. Prasad B. V. V., Wang G. J., Clerx J. P., Chiu W. 1988; Threedimensional structure of rotavirus. Journal of Molecular Biology 199:269–275
    [Google Scholar]
  27. Prasad B. V. V., Burns J. W., Marietta E., Estes M. K., Chiu W. 1990; Localization of VP4 neutralization sites in rotavirus by threedimensional cryo-electron microscopy. Nature 343:476–479
    [Google Scholar]
  28. Ruggeri F. M., Greenberg H. B. 1991; Antibodies to the trypsin cleavage peptide VP8* neutralize rotavirus by inhibiting binding of virions to target cells in culture. Journal of Virology 65:2211–2219
    [Google Scholar]
  29. Ruiz M. C., Michelangeli F., Ludert J. E., Liprandi F., del Castillo J. R., Chemello M. E., Benaim G., Cohen E. 1991; Fluorometric quantification of cell death in monolayer cultures and cell suspensions. Journal of Biochemical and Biophysical Methods 23:237–248
    [Google Scholar]
  30. Ruiz M. C., Alonso Torre S. R., Charpilienne A., Vasseur M., Michelangeli F., Cohen J., Alvarado F. 1994; Rotavirus interaction with isolated membrane vesicles. Journal of Virology 68:4009–4016
    [Google Scholar]
  31. Ruiz M. C., Charpilienne A., Liprandi F., Gajardo R., Michelangeli F., Cohen J. 1996; Concentration of Ca2+ that solubilizes outer capsid proteins from rotavirus particles is dependent on the strain. Journal of Virology 70:4877–4883
    [Google Scholar]
  32. Suzuki H., Kitaoka S., Konno T., Sato T., Ishida N. 1985; Two modes of human rotavirus entry into MA104 cells. Journal of Virology 85:25–34
    [Google Scholar]
  33. Yeager M., Dryden K. A., Olson N. H., Greenberg H. B., Baker T. S. 1990; Three-dimensional structure of rhesus rotavirus by cryo-electron microscopy and image reconstruction. Journal of Cell Biology 110:2133–2144
    [Google Scholar]
  34. Yeager M., Berriman J. A., Baker T. S., Bellamy A. R. 1994; Three-dimensional structure of the rotavirus haemagglutinin VP4 by cryo-electron microscopy and difference map analysis. EMBO Journal 13:1011–1018
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-78-11-2883
Loading
/content/journal/jgv/10.1099/0022-1317-78-11-2883
Loading

Data & Media loading...

Most cited this month 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