1887

Abstract

Summary

Three categories of cell lines are described which differ with respect to their permissiveness to mouse hepatitis virus (MHV), strain A59. Fully permissive L-2 cells gave rise to 100- to 1000-fold higher numbers of infectious centres than did semipermissive LM, LM-K or C-1300 cells, whereas non-permissive Vero or C-6 cells were refractory to MHV infection. On an infected cell basis, semi-permissive cells (LM, LM-K or C-1300) were as efficient in replicating viral RNA, protein and progeny virions as fully permissive L-2 cells. This result suggested that LM, LM-K and C-1300 cells were deficient in their ability to permit full expression (as compared to L-2 cells) of an early event in MHV infection. Assays of radiolabelled MHV binding to cells of all three categories (L-2, LM, LM-K and C-6) and of infectious MHV binding to L-2 and LM-K cells showed no correlation between virion binding and degree of permissiveness to MHV infection. Internalization of MHV virions into L-2 and LM-K cells, as assayed by proteinase K-resistant infectious centres, showed that, in both cases, maximum virion uptake was complete by approximately 40 min post-inoculation. Direct assays of infectious virion uptake showed similar numbers of internalized viruses (only a threefold difference between L-2 and LM-K cells, as compared to a 500-fold difference in infectious centres). Attempts to enhance MHV uptake into LM-K cells relative to L-2 cells, with DEAE-dextran or the cytoskeleton-disrupting drugs colchicine and cytochalasin B, were unsuccessful, further suggesting that the ability of LM-K cells to internalize the virus was not lacking. The results suggest that MHV infection of at least some semi-permissive cells, such as the LM-K line, is limited by a process which chronologically correlates with virion uncoating. Since LM-K cells have been shown previously to be resistant to membrane fusion in MHV infection, it is postulated that they may also restrict uncoating of MHV by limiting the degree of normal endosomal membrane fusion with the viral envelope.

Keyword(s): internalization , MHV and permissiveness
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-69-6-1125
1988-06-01
2022-01-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/69/6/JV0690061125.html?itemId=/content/journal/jgv/10.1099/0022-1317-69-6-1125&mimeType=html&fmt=ahah

References

  1. AUGUSTI-TOCCO G., SATO G. 1969; Establishment of functional clonal lines of neurons from mouse neuroblastoma. Proceedings of the National Academy of Sciences, U.S.A 64:311–315
    [Google Scholar]
  2. BAILEY C. A., MILLER D. K., LENARD J. 1984; Effects of DEAE-dextran on infection and hemolysis of VSV. Evidence that nonspecific electrostatic interactions mediate effective binding of VSV to cells. Virology 133:111–118
    [Google Scholar]
  3. BARIC R. S., STOHLMAN S. A., LAI M. M. C. 1983; Characterization of replicative intermediate RNA of mouse hepatitis virus: presence of leader RNA sequences on nascent chains. Journal of Virology 48:633–640
    [Google Scholar]
  4. BARIC R. S., STOHLMAN S. A., RAZAVI M. K., LAI M. M. C. 1985; Characterization of leader-related small RNAs in coronavirus-infected cells: further evidence for leader-primed mechanism of transcription. Virus Research 3:19–33
    [Google Scholar]
  5. BENDA P., LIGHTBODY I., SATO G., LEVINE L., SWEET S. 1968; Differentiated rat glial cell strain in tissue culture. Science 161:370–371
    [Google Scholar]
  6. BOYLE J. P., WEISMILLER D. G., HOLMES K. V. 1987; Genetic resistance to mouse hepatitis virus correlates with absence of virus-binding activity on target tissues. Journal of Virology 61:185–189
    [Google Scholar]
  7. BRAYTON P. R., LAI M. M. C, PATTON C. D., STOHLMAN S. A. 1982; Characterization of two RNA polymerase activities induced by mouse hepatitis virus. Journal of Virology 42:847–853
    [Google Scholar]
  8. BUCHANAN D., KAMARCK M., RUDDLE N. H. 1981; Development of a Protein A enzyme immunoassay for use in screening hybridomas. Journal of Immunological Methods 42:179–185
    [Google Scholar]
  9. CHEEVER F. S., DANIELS J. B., PAPPENHEIMER A. M., BAILEY O. T. 1949; A murine virus (JHM) causing disseminated encephalomyelitis with extensive destruction of myelin. I. Isolation and biologic properties of the virus. Journal of Experimental Medicine 90:181–194
    [Google Scholar]
  10. CHELEY S., ANDERSON R. 1984; A reproducible microanalytical method for the detection of specific RNA sequences by dot-blot hybridization. Analytical Biochemistry 137:15–19
    [Google Scholar]
  11. CHELEY S., ANDERSON R., CUPPLES M. J., LEE CHAN E. C. M., MORRIS V. L. 1981; Intracellular murine hepatitis virus-specific RNAs contain common sequences. Virology 112:596–604
    [Google Scholar]
  12. DALGLEISH A. G., BEVERLY P. C. L., CLAPHAM P. R., CRAWFORD D. H., GREAVES M. F., WEISS R. A. 1984; The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature, London 312:763–766
    [Google Scholar]
  13. DAVID-FERREIRA J. F., MANAKER R. A. 1965; An electron microscope study of the development of a mouse hepatitis virus in tissue culture cells. Journal of Cell Biology 24:57–78
    [Google Scholar]
  14. DIMMOCK N. J. 1982; Initial stages in infection with animal viruses. Journal of General Virology 59:1–22
    [Google Scholar]
  15. DOYLE L. P., HUTCHINGS L. M. 1946; A transmissible gastroenteritis in pigs. Journal of the American Veterinary Association 108:257–259
    [Google Scholar]
  16. GLEDHILL A. W., ANDREWES C. H. 1951; A hepatitis virus of mice. British Journal of Experimental Pathology 32:559–568
    [Google Scholar]
  17. HAMRE D., PROCKNOW J. J. 1966; A new virus isolated from the human respiratory tract. Proceedings of the Society for Experimental Biology and Medicine 121:190–193
    [Google Scholar]
  18. HASPEL M. V., LAMPERT P. W., OLDSTONE M. B. A. 1978; Temperature-sensitive mutants of mouse hepatitis virus produce a high incidence of demyelination. Proceedings of the National Academy of Sciences, U.S.A 75:4033–4036
    [Google Scholar]
  19. HELENLUS A., KARTENBECK J., SIMONS K., FRIES E. 1980; On the entry of Semliki Forest virus into BHK-21 cells. Journal of Cell Biology 84:404–420
    [Google Scholar]
  20. HIRANO N., GOTO N., OGAWA T., ONO K., MURAKAMI T., FUJIWARA K. 1980; Hydrocephalus in suckling rats infected intracerebrally with mouse hepatitis virus, MHV-A59. Microbiology and Immunology 24:825–834
    [Google Scholar]
  21. HOLZWORTH J. 1963; Some important disorders of cats. Cornell Veterinarian 53:157–160
    [Google Scholar]
  22. JONDAL M., KLEIN G. 1973; Surface markers on human B and T lymphocytes. II. Presence of Epstein-Barr virus receptors on B lymphocytes. Journal of Experimental Medicine 138:1365–1378
    [Google Scholar]
  23. KAYE H. S., YARBOROUGH W. B., REED C. J. 1975; Calf diarrhoea coronavirus. Lancet ii:509
    [Google Scholar]
  24. KIT S., DUBBS D. R., PIEKARSKI L. I., HSU T. C. 1963; Deletion of thymidine kinase activity from L cells resistant to bromodeoxyuridine. Experimental Cell Research 31:297–312
    [Google Scholar]
  25. KRONTIRIS T. G., SOEIRO R., FIELDS R. N. 1973; Host restriction of Friend leukemia virus. Role of the viral outer coat. Proceedings of the National Academy of Sciences, U.S.A 70:2549–2553
    [Google Scholar]
  26. KRZYSTYNIAK K., DUPUY J. M. 1984; Entry of mouse hepatitis virus 3 into cells. Journal of General Virology 65:227–231
    [Google Scholar]
  27. LAI M. M. C., STOHLMAN S. A. 1978; The RNA of mouse hepatitis virus. Journal of Virology 26:236–242
    [Google Scholar]
  28. LAI M. M. C, BRAYTON P. R., ARMEN R. C, PATTON C. D., PUGH C., STOHLMAN S. A. 1981; Mouse hepatitis virus A59 messenger RNA structure and genetic localization of the sequence divergence from the hepatotropic strain MHV-3. Journal of Virology 39:823–824
    [Google Scholar]
  29. LAI M. M. C, PATTON C. D., STOHLMAN S. A. 1982; Replication of mouse hepatitis virus: negative-stranded RNA and replicative form RNA are of genome-length. Journal of Virology 44:487–492
    [Google Scholar]
  30. LEIBOWITZ J. L., WILHELMSEN K. C., BOND C. W. 1981; The virus-specific intracellular RNA species of two murine coronaviruses: MHV-A59 and MHV-JHM. Virology 114:29–51
    [Google Scholar]
  31. LE PREVOST C, VTRELIZIER J. L., DUPUY J. M. 1975; Immunopathology of mouse hepatitis virus type 3 infection. III. Clinical and virological observation of a persistent viral infection. Journal of Immunology 115:640–643
    [Google Scholar]
  32. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. 1951; Protein measurement with the Folin phenol reagent. Journal of Biological Chemistry 193:265–275
    [Google Scholar]
  33. LUCAS A., FLINTOFF W., ANDERSON R., PERCY D., COULTER M., DALES S. 1977; In vivo and in vitro models of demyelinating diseases: tropism of the JHM strain of murine hepatitis virus for cells of glial origin. Cell 12:553–560
    [Google Scholar]
  34. LUCAS A., COULTER M., ANDERSON R., DALES S., FLINTOFF W. 1978; In vivo and in vitro models of demyelinating diseases. II. Persistence and host-regulated thermosensitivity in cells of neural derivation infected with mouse hepatitis and measles viruses. Virology 88:325–337
    [Google Scholar]
  35. MCINTOSH K., BECKER W. C., CHANOCK R. M. 1967; Growth in suckling mouse brain of ‘IBV-like’ viruses from patients with upper respiratory disease. Proceedings of the National Academy of Sciences, U.S.A 58:2268–2273
    [Google Scholar]
  36. MCLAREN L. C, HOLLAND J. J., SYVERTON J. T. 1959; The mammalian cell-virus relationship. I. Attachment of poliovirus to cultivated cells of primate and non-primate origin. Journal of Experimental Medicine 109:475–485
    [Google Scholar]
  37. MALLUCCI L. 1966; Effect of chloroquine on lysosomes and on growth of mouse hepatitis virus (MHV-3). Virology 28:355–362
    [Google Scholar]
  38. MALLUCCI L., EDWARDS B. 1982; Influence of the cytoskeleton on the expression of a mouse hepatitis virus (MHV-3) in peritoneal macrophages: acute and persistent infection. Journal of General Virology 63:217–221
    [Google Scholar]
  39. MANAKER R. A., PICZAK C. V., MILLER A. A., STANTON M. F. 1961; A hepatitis virus complicating studies with mouse leukemia. Journal of the National Cancer Institute 27:29–44
    [Google Scholar]
  40. MARSH M. 1984; The entry of enveloped viruses into cells by endocytosis. Biochemical Journal 218:1–10
    [Google Scholar]
  41. MARSH M., BOLZAU E., HELENIUS A. 1983; Penetration of Semliki Forest virus from acidic prelysosomal vacuoles. Cell 32:931–940
    [Google Scholar]
  42. MERCHANT D. J., HELLMAN K. B. 1962; Growth of L-M strain of mouse cells in a chemically defined medium. Proceedings of the Society for Experimental Biology and Medicine 110:194–198
    [Google Scholar]
  43. MIZZEN L., CHELEY S., RAO M., WOLF R., ANDERSON R. 1983; Fusion resistance and decreased infectability as major host cell determinants of corona virus persistence. Virology 128:407–417
    [Google Scholar]
  44. MIZZEN L., HILTON A., CHELEY S., ANDERSON R. 1985; Attenuation of murine coronavirus infection by ammonium chloride. Virology 142:387–388
    [Google Scholar]
  45. NAGASHIMA K., WEGE H., MEYERMANN R., TER MEULEN V. 1978; Demyelinating encephalomyelitis induced by long-term coronavirus infection in rats. A preliminary report. Acta neuropathologica 45:205–213
    [Google Scholar]
  46. PIRAINO F. 1967; The mechanism of genetic resistance of chick embryo cells to infection by Rous sarcoma virus-Bryan strain. Virology 32:700–707
    [Google Scholar]
  47. ROTHFELS K. H., AXELRAD A. A., SIMINOVITCH L., MCCULLOCH E. A., PARKER R. C. 1959; The origin of altered Cell lines from mouse, monkey and man as indicated by chromosome and transplantation studies. Canadian Cancer Conference 3:189–214
    [Google Scholar]
  48. SCHALK A. E., HAWN M. C. 1931; An apparently new respiratory disease of baby chicks. Journal of the American Veterinary Medical Association 78:413–422
    [Google Scholar]
  49. SHANK P. R., COHEN J. C, VARMUS H. E., YAMAMOTO K. R., RINGOLD G. M. 1978; Mapping of linear and circular forms of mouse mammary tumor virus DNA with restriction endonucleases: evidence for a large specific deletion occurring at high frequency during circularization. Proceedings of the National Academy of Sciences, U.S.A 75:2112–2116
    [Google Scholar]
  50. SHAPIRO I. M., VOLSKY D. J., SAEMUNDSEN A. K., ANISIMOVA E., KLEIN O. 1982; Infection of the human T-cell-derived leukemia line molt-4 by Epstein-Barr virus (EBV): induction of EBV-determined antigens and virus reproduction. Virology 120:171–181
    [Google Scholar]
  51. SIDDELL S. G., WEGE H., BARTHEL A., TER MEULEN V. 1980; Coronavirus JHM: cell-free synthesis of structural protein p60. Journal of Virology 33:10–17
    [Google Scholar]
  52. SORENSEN O., PERCY D., DALES S. 1980; In vivo and in vitro models of demyelinating diseases. III. JHM virus infection of rats. Archives of Neurology 37:478–484
    [Google Scholar]
  53. SPAAN W. J. M., ROTTIER P. J. M., HORZINEK M. C., VAN DER ZEUST B. A. M. 1982; Sequence relationships between the genome and the intracellular RNA species 1, 3, 6 and 7 of mouse hepatitis virus strain A59. Journal of Virology 42:432–439
    [Google Scholar]
  54. STECK F. T., RUBIN H. 1966; The mechanism of interference between an avian leukosis and Rous sarcoma virus. II. Early steps of infection by RSV of cells under conditions of interference. Virology 29:642–653
    [Google Scholar]
  55. TARDIEU M., BOESPFLUG O., BARBE T. 1986; Selective tropism of a neurotropic coronavirus for ependymal cells, neurons, and meningeal cells. Journal of Virology 60:574–582
    [Google Scholar]
  56. VAN DINTER S., FLINTOFF W. F. 1987; Rat glial C6 cells are defective in murine coronavirus internalization. Journal of General Virology 68:1677–1685
    [Google Scholar]
  57. WEGE H., MÜLLER A., TER MEULEN V. 1978; Genomic RNA of the murine coronavirus JHM. Journal of General Virology 41:217–227
    [Google Scholar]
  58. WEINER H. L., DRAYNA D., AVERILL D. R., FIELDS B. N. 1977; Molecular basis of reovirus virulence: role of the S1 gene. Proceedings of the National Academy of Sciences, U.S.A 74:5744–5748
    [Google Scholar]
  59. WEISS S. R., LEIBOWITZ I. L. 1983; Characterization of murine coronavirus RNA by hybridization with virus-specific cDNA probes. Journal of General Virology 64:127–133
    [Google Scholar]
  60. WRAY W., BOULIKAS T., WRAY V., HANCOCK R. 1981; Silver-staining of proteins in Polyacrylamide gels. Analytical Biochemistry 118:197–203
    [Google Scholar]
  61. WUNNER W. H., REAGAN K. J., KOPROWSKI H. 1984; Characterization of saturable binding sites for rabies virus. Journal of Virology 50:691–697
    [Google Scholar]
  62. YASUMURA Y., KAWAKITA Y. 1963; Studies on SV-40 in tissue culture. Nippon Rinsho (Japan 21:1209
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-69-6-1125
Loading
/content/journal/jgv/10.1099/0022-1317-69-6-1125
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