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. 1978 Oct;28(1):199–211. doi: 10.1128/jvi.28.1.199-211.1978

Initiation and maintenance of persistent infection by respiratory syncytial virus.

C R P'ringle, P V Shirodaria, P Cash, D J Chiswell, P Malloy
PMCID: PMC354259  PMID: 702647

Abstract

Propagation of cells infected with temperature-sensitive (ts) mutants of respiratory syncytial (RS) virus at nonpermissive temperature (39 degrees C) resulted in cytolytic, abortive, or persistent infection, depending on the mutant used to initiate infection. Five mutants from complementation group B produced cytolytic or abortive infections, whereas a single mutant (ts1) from group D and a noncomplbmenting mutant produced persistent infections. The persistently infected culture initiated by mutant ts1 (RS ts1/BS-C-1) has been maintained in serial culture for greater than 100 transfers, and infectious-center assays and immunofluorescent staining indicated that all cells harbored the RS virus genome. RS ts1/BS-C-1 cultures were resistant to superinfection by homologous and some heterologous viruses, and interferon-like activity against some heterologous viruses was present in the culture medium. Small amounts (0.002 to 0.2 PFU/cell) of infectious virus were present in the culture fluid, but autointerfering defective particles were not detected. This released virus formed small plaques and produced persistent infection of BS-C-1 cells at 37 degrees C. The RS ts1/BS-C-1 cells contained abundant RS virus antigen internally, but little at the surface, although the cells showed enhanced agglutinability by concanavalin A. Nucleocapsids and the 41,000-molecular-weight nucleoprotein were present in extracts of both nucleated and enucleated cells. No infectious RS virus was obtained by transfection of DNA from RS tsl/BS-C-1 cells to susceptible BS-C-1 or feline embryo cells under conditions allowing efficient transfection of a foamy virus proviral DNA. It was concluded that persistent infection was maintained in part by a non-ts variant of RS virus partially defective in maturation. The karyotype of the RS ts1/BS-C-1 culture differed from that of unifected cells.

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  1. Belshe R. B., Richardson L. S., Schnitzer T. J., Prevar D. A., Camargo E., Chanock R. M. Further characterization of the complementation group B temperature-sensitive mutant of respiratory syncytial virus. J Virol. 1977 Oct;24(1):8–12. doi: 10.1128/jvi.24.1.8-12.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Cash P., Wunner W. H., Pringle C. R. A comparison of the polypeptides of human and bovine respiratory syncytial viruses and murine pneumonia virus. Virology. 1977 Oct 15;82(2):369–379. doi: 10.1016/0042-6822(77)90012-5. [DOI] [PubMed] [Google Scholar]
  3. Faulkner G. P., Shirodaria P. V., Follett E. A., Pringle C. R. Respiratory syncytial virus ts mutants and nuclear immunofluorescence. J Virol. 1976 Nov;20(2):487–500. doi: 10.1128/jvi.20.2.487-500.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Follett E. A. A convenient method for enucleating cells in quantity. Exp Cell Res. 1974 Mar 15;84(1):72–78. doi: 10.1016/0014-4827(74)90381-4. [DOI] [PubMed] [Google Scholar]
  5. Follett E. A., Pringle C. R., Pennington T. H. Virus development in enucleate cells: echovirus, poliovirus, pseudorabies virus, reovirus, respiratory syncytial virus and Semliki Forest virus. J Gen Virol. 1975 Feb;26(2):183–196. doi: 10.1099/0022-1317-26-2-183. [DOI] [PubMed] [Google Scholar]
  6. Gimenez H. B., Pringle C. R. Seven complementation groups of respiratory syncytial virus temperature-sensitive mutants. J Virol. 1978 Sep;27(3):459–464. doi: 10.1128/jvi.27.3.459-464.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gould E. A., Linton P. E. The production of a temperature-sensitive persistent measles virus infection. J Gen Virol. 1975 Jul;28(1):21–28. doi: 10.1099/0022-1317-28-1-21. [DOI] [PubMed] [Google Scholar]
  8. Hallum J. V., Thacore H. R., Youngner J. S. Factors affecting the sensitivity of different viruses to interferon. J Virol. 1970 Aug;6(2):156–162. doi: 10.1128/jvi.6.2.156-162.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hill B. T., Whatley S. A simple, rapid microassay for DNA. FEBS Lett. 1975 Aug 1;56(1):20–23. doi: 10.1016/0014-5793(75)80102-5. [DOI] [PubMed] [Google Scholar]
  10. Holland J. J., Villarreal L. P., Welsh R. M., Oldstone M. B., Kohne D., Lazzarini R., Scolnick E. Long-term persistent vesicular stomatitis virus and rabies virus infection of cells in vitro. J Gen Virol. 1976 Nov;33(2):193–211. doi: 10.1099/0022-1317-33-2-193. [DOI] [PubMed] [Google Scholar]
  11. Holmes A. R., Rasmussen L., Merigan T. C. Factors affecting the interferon sensitivity of human cytomegalovirus. Intervirology. 1978;9(1):48–55. doi: 10.1159/000148920. [DOI] [PubMed] [Google Scholar]
  12. Mudd J. A., Leavitt R. W., Kingsbury D. T., Holland J. J. Natural selection of mutants of vesicular stomatitis virus by cultured cells of Drosophila melanogaster. J Gen Virol. 1973 Sep;20(3):341–351. doi: 10.1099/0022-1317-20-3-341. [DOI] [PubMed] [Google Scholar]
  13. Nishiyama Y. Studies of L cells persistently infected with VSV: factors involved in the regulation of persistent infection. J Gen Virol. 1977 May;35(2):265–279. doi: 10.1099/0022-1317-35-2-265. [DOI] [PubMed] [Google Scholar]
  14. Poste G., Reeve P. Agglutination of normal cells by plant lectins following infection with nononcogenic viruses. Nat New Biol. 1972 May 24;237(73):113–114. doi: 10.1038/newbio237113a0. [DOI] [PubMed] [Google Scholar]
  15. Preble O. T., Youngner J. S. Selection of temperature-sensitive mutants during persistent infection: role in maintenance of persistent Newcastle disease virus infections of L cells. J Virol. 1973 Sep;12(3):481–491. doi: 10.1128/jvi.12.3.481-491.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Preble O. T., Youngner J. S. Temperature-sensitive viruses and the etiology of chronic and inapparent infections. J Infect Dis. 1975 Apr;131(4):467–473. doi: 10.1093/infdis/131.4.467. [DOI] [PubMed] [Google Scholar]
  17. Pringle C. R. Enucleation as a technique in the study of virus-host interactions. Curr Top Microbiol Immunol. 1977;76:49–82. doi: 10.1007/978-3-642-66653-7_2. [DOI] [PubMed] [Google Scholar]
  18. Rima R. K., Martin S. J. Persistent infection of tissue culture cells by RNA viruses. Med Microbiol Immunol. 1976 Jun 1;162(2):89–119. doi: 10.1007/BF02121320. [DOI] [PubMed] [Google Scholar]
  19. Russell W. C., Newman C., Williamson D. H. A simple cytochemical technique for demonstration of DNA in cells infected with mycoplasmas and viruses. Nature. 1975 Feb 6;253(5491):461–462. doi: 10.1038/253461a0. [DOI] [PubMed] [Google Scholar]
  20. Simpson R. W., Iinuma M. Recovery of infectious proviral DNA from mammalian cells infected with respiratory syncytial virus. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3230–3234. doi: 10.1073/pnas.72.8.3230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Stow N. D., Wilkie N. M. An improved technique for obtaining enhanced infectivity with herpes simplex virus type 1 DNA. J Gen Virol. 1976 Dec;33(3):447–458. doi: 10.1099/0022-1317-33-3-447. [DOI] [PubMed] [Google Scholar]
  22. WALKER D. L. THE VIRAL CARRIER STATE IN ANIMAL CELL CULTURES. Prog Med Virol. 1964;6:111–148. [PubMed] [Google Scholar]
  23. Wunner W. H., Pringle C. R. Respiratory syncytial virus proteins. Virology. 1976 Aug;73(1):228–243. doi: 10.1016/0042-6822(76)90077-5. [DOI] [PubMed] [Google Scholar]
  24. Youngner J. S., Dubovi E. J., Quagliana D. O., Kelly M., Preble O. T. Role of temperature-sensitive mutants in persistent infections initiated with vesicular stomatitis virus. J Virol. 1976 Jul;19(1):90–101. doi: 10.1128/jvi.19.1.90-101.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Youngner J. S., Quagliana D. O. Temperature-sensitive mutants of vesicular stomatitis virus are conditionally defective particles that interfere with and are rescued by wild-type virus. J Virol. 1976 Jul;19(1):102–107. doi: 10.1128/jvi.19.1.102-107.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Zakstelskaya L. Y., Almeida J. D., Bradstreet C. M. The morphological characterisation of respiratory syncytial virus by a simple electron microscope technique. Acta Virol. 1967 Sep;11(5):420–423. [PubMed] [Google Scholar]
  27. Zarling J. M., Tevethia S. S. Expression of concanavalin A binding sites in rabbit kidney cells infected with vaccinia virus. Virology. 1971 Jul;45(1):313–316. doi: 10.1016/0042-6822(71)90140-1. [DOI] [PubMed] [Google Scholar]

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