Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1968 Jan 1;36(1):197–230.

THE PENETRATION OF REOVIRUS RNA AND INITIATION OF ITS GENETIC FUNCTION IN L-STRAIN FIBROBLASTS

Samuel C Silverstein 1, Samuel Dales 1
PMCID: PMC2107329  PMID: 19806702

Abstract

Reovirus type 3 is phagocytized by L cells and rapidly sequestered inside lysosomes. Hydrolases within these organelles are capable of stripping the viral coat proteins, but they fail to degrade the double-stranded RNA genome. These observations support the view that sojourn of reovirus in lysosomes, when the lytic enzymes uncoat its genome, is an obligatory step in the sequence of infection. Although the mechanism for transferring the uncoated RNA out of lysosomes remains to be elucidated, evidence is presented suggesting that progeny genomes are bound to site(s) possessing the fine structure of viral inclusions or factories. It appears that both the synthesis of single- and double-stranded viral RNA and the morphogenesis of progeny virus particles occur in such factories.

Full Text

The Full Text of this article is available as a PDF (2.5 MB).

Selected References

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

  1. BERNHARD W., TOURNIER P. Ultrastructural cytochemistry applied to the study of virus infection. Cold Spring Harb Symp Quant Biol. 1962;27:67–82. doi: 10.1101/sqb.1962.027.001.010. [DOI] [PubMed] [Google Scholar]
  2. Baltimore D., Girard M., Darnell J. E. Aspects of the synthesis of poliovirus RNA and the formation of virus particles. Virology. 1966 Jun;29(2):179–189. doi: 10.1016/0042-6822(66)90024-9. [DOI] [PubMed] [Google Scholar]
  3. Bishop J. M., Koch G. Purification and characterization of poliovirus-induced infectious double-stranded ribonucleic acid. J Biol Chem. 1967 Apr 25;242(8):1736–1743. [PubMed] [Google Scholar]
  4. Bowers W. E., Finkenstaedt J. T., de Duve C. Lysosomes in lymphoid tissue. I. The measurement of hydrolytic activities in whole homogenates. J Cell Biol. 1967 Feb;32(2):325–337. doi: 10.1083/jcb.32.2.325. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. CARO L. G., VAN TUBERGEN R. P., KOLB J. A. High-resolution autoradiography. I. Methods. J Cell Biol. 1962 Nov;15:173–188. doi: 10.1083/jcb.15.2.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DALES S. ASSOCIATION BETWEEN THE SPINDLE APPARATUS AND REOVIRUS. Proc Natl Acad Sci U S A. 1963 Aug;50:268–275. doi: 10.1073/pnas.50.2.268. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. DALES S., GOMATOS P. J., HSU K. C. THE UPTAKE AND DEVELOPMENT OF REOVIRUS IN STRAIN L CELLS FOLLOWED WITH LABELED VIRAL RIBONUCLEIC ACID AND FERRITIN-ANTIBODY CONJUGATES. Virology. 1965 Feb;25:193–211. doi: 10.1016/0042-6822(65)90199-6. [DOI] [PubMed] [Google Scholar]
  8. DALES S., SIMINOVITCH L. The development of vaccinia virus in Earle's L strain cells as examined by electron microscopy. J Biophys Biochem Cytol. 1961 Aug;10:475–503. doi: 10.1083/jcb.10.4.475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Dales S. Effects of streptovitacin A on the initial events in the replication of vaccinia and reovirus. Proc Natl Acad Sci U S A. 1965 Aug;54(2):462–468. doi: 10.1073/pnas.54.2.462. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. EAGLE H. Amino acid metabolism in mammalian cell cultures. Science. 1959 Aug 21;130(3373):432–437. doi: 10.1126/science.130.3373.432. [DOI] [PubMed] [Google Scholar]
  11. Farquhar M. G., Palade G. E. Cell junctions in amphibian skin. J Cell Biol. 1965 Jul;26(1):263–291. doi: 10.1083/jcb.26.1.263. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Flanagan J. F. Hydrolytic enzymes in KB cells infected with poliovirus and herpes simplex virus. J Bacteriol. 1966 Feb;91(2):789–797. doi: 10.1128/jb.91.2.789-797.1966. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. GEIDUSCHEK E. P., MOOHR J. W., WEISS S. B. The secondary structure of complementary RNA. Proc Natl Acad Sci U S A. 1962 Jun 15;48:1078–1086. doi: 10.1073/pnas.48.6.1078. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gomatos P. J., Tamm I. THE SECONDARY STRUCTURE OF REOVIRUS RNA. Proc Natl Acad Sci U S A. 1963 May;49(5):707–714. doi: 10.1073/pnas.49.5.707. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. HOMMA M., GRAHAM A. F. INTRACELLULAR FATE OF MENGO VIRUS RIBONUCLEIC ACID. J Bacteriol. 1965 Jan;89:64–73. doi: 10.1128/jb.89.1.64-73.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. KAVERIN N. V. A NON-PROTEIN-SYNTHESIS-DEPENDENT STAGE OF LATENT PERIOD AND TIME OF PHOTOSENSITIVITY LOSS OF VIRUS IN ITS INTERACTION WITH THE CELL. Acta Virol. 1965 May;9:193–199. [PubMed] [Google Scholar]
  17. Kates J. R., McAuslan B. R. Messenger RNA synthesis by a "coated" viral genome. Proc Natl Acad Sci U S A. 1967 Feb;57(2):314–320. doi: 10.1073/pnas.57.2.314. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kates J. R., McAuslan B. R. Poxvirus DNA-dependent RNA polymerase. Proc Natl Acad Sci U S A. 1967 Jul;58(1):134–141. doi: 10.1073/pnas.58.1.134. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kudo H., Graham A. F. Synthesis of reovirus ribonucleic acid in L cells. J Bacteriol. 1965 Oct;90(4):936–945. doi: 10.1128/jb.90.4.936-945.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. LANGRIDGE R., GOMATOS P. J. The structure of RNA. Reovirus RNA and transfer RNA have similar three-dimensional structures, which differ from DNA. Science. 1963 Aug 23;141(3582):694–698. doi: 10.1126/science.141.3582.694. [DOI] [PubMed] [Google Scholar]
  21. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  22. LUCK D. J. Formation of mitochondria in Neurospora crassa. A quantitative radioautographic study. J Cell Biol. 1963 Mar;16:483–499. doi: 10.1083/jcb.16.3.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MANDELL J. D., HERSHEY A. D. A fractionating column for analysis of nucleic acids. Anal Biochem. 1960 Jun;1:66–77. doi: 10.1016/0003-2697(60)90020-8. [DOI] [PubMed] [Google Scholar]
  24. MARTIN A. P., NEUFELD H. A., LUCAS F. V., STOTZ E. Characterization of uterine peroxidase. J Biol Chem. 1958 Jul;233(1):206–208. [PubMed] [Google Scholar]
  25. McClain M. E., Spendlove R. S., Lennette E. H. Infectivity assay of Reoviruses: comparison of immunofluorescent cell count and plaque methods. J Immunol. 1967 Jun;98(6):1301–1308. [PubMed] [Google Scholar]
  26. Mego J. L., Bertini F., McQueen J. D. The use of formaldehyde-treated 131-I-albumin in the study of digestive vacuoles and some properties of these particles from mouse liver. J Cell Biol. 1967 Mar;32(3):699–707. doi: 10.1083/jcb.32.3.699. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. NIELSEN S. O., LEHNINGER A. L. Phosphorylation coupled to the oxidation of ferrocytochrome c. J Biol Chem. 1955 Aug;215(2):555–570. [PubMed] [Google Scholar]
  28. Prevec L., Graham A. F. Reovirus-specific polyribosomes in infected L-cells. Science. 1966 Oct 28;154(3748):522–523. [PubMed] [Google Scholar]
  29. RHIM J. S., JORDAN L. E., MAYOR H. D. Cytochemical, fluorescent-antibody and electron microscopic studies on the growth of reovirus (ECHO 10) in tissue culture. Virology. 1962 Jun;17:342–355. doi: 10.1016/0042-6822(62)90125-3. [DOI] [PubMed] [Google Scholar]
  30. SHATKIN A. J. ACTINOMYCIN AND THE DIFFERENTIAL SYNTHESIS OF REOVIRUS AND L CELL RNA. Biochem Biophys Res Commun. 1965 May 3;19:506–510. doi: 10.1016/0006-291x(65)90154-3. [DOI] [PubMed] [Google Scholar]
  31. SILVERSTEIN S. C., MARCUS P. I. EARLY STAGES OF NEWCASTLE DISEASE VIRUS-HELA CELL INTERACTION: AN ELECTRON MICROSCOPIC STUDY. Virology. 1964 Jul;23:370–380. doi: 10.1016/0042-6822(64)90259-4. [DOI] [PubMed] [Google Scholar]
  32. SIMINOVITCH L., GRAHAM A. F., LESLEY S. M., NEVILL A. Propagation of L strain mouse cells in suspension. Exp Cell Res. 1957 Apr;12(2):299–308. doi: 10.1016/0014-4827(57)90143-x. [DOI] [PubMed] [Google Scholar]
  33. Shatkin A. J. Inactivity of purified reovirus RNA as a template for E. coli polymerases in vitro. Proc Natl Acad Sci U S A. 1965 Dec;54(6):1721–1728. doi: 10.1073/pnas.54.6.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Shatkin A. J., Rada B. Reovirus-directed ribonucleic acid synthesis in infected L cells. J Virol. 1967 Feb;1(1):24–35. doi: 10.1128/jvi.1.1.24-35.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Stanley W. M., Jr, Bock R. M. Isolation and physical properties of the ribosomal ribonucleic acid of Escherichia coli. Biochemistry. 1965 Jul;4(7):1302–1311. doi: 10.1021/bi00883a014. [DOI] [PubMed] [Google Scholar]
  36. WHEELOCK E. F. The role of protein synthesis in the eclipse period of newcastle disease virus multiplication in HeLa cells as studied with puromycin. Proc Natl Acad Sci U S A. 1962 Aug;48:1358–1366. doi: 10.1073/pnas.48.8.1358. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Watanabe Y., Kudo H., Graham A. F. Selective inhibition of reovirus ribonucleic acid synthesis by cycloheximide. J Virol. 1967 Feb;1(1):36–44. doi: 10.1128/jvi.1.1.36-44.1967. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES