Abstract
A unique defective interfering (DI) particle, generated by a heat-resistant (HR) mutant of Indiana serotype vesicular stomatitis virus, was capable of inhibiting primary transcription by heterologous New Jersey serotype virions. The correlation between this phenomenon and the lowering of viral yields from doubly infected cells was investigated by the construction of chimeric DI particles containing the HR DI particle genome with a thermolabile polymerase. At the nonpermissive temperature, these DI particles were unable to self-transcribe, inhibit virion primary transcription, or reduce virion yield, but were able to be replicated. These results suggested that self-transcription of the HR DI particle genome was a prerequisite for heterotypic interference, but not for its own replication. Inhibition of virion primary transcription by HR DI ribonucleocapsids was also observed in vitro. At low HR DI to virion ribonucleocapsid ratios, the extent of inhibition was concentration dependent, whereas at high ratios, the amount of inhibition was concentration independent, approaching a limiting maximum value. A speculative mathematical model, which quantitatively accounts for these data, is presented. According to this model, the higher affinity for polymerase molecules by the HR DI ribonucleocapsids is explained in terms of dissociation events during transcription, which are more frequent in the longer virion ribonucleocapsids.
Full text
PDFSelected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bay P. H., Reichmann M. E. UV inactivation of the biological activity of defective interfering particles generated by vesicular stomatitis virus. J Virol. 1979 Dec;32(3):876–884. doi: 10.1128/jvi.32.3.876-884.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carroll A. R., Wagner R. R. Role of the membrane (M) protein in endogenous inhibition of in vitro transcription by vesicular stomatitis virus. J Virol. 1979 Jan;29(1):134–142. doi: 10.1128/jvi.29.1.134-142.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chow J. M., Schnitzlein W. M., Reichmann M. E. Expression of genetic information contained in the RNA of a defective interfering particle of vesicular stomatitis virus. Virology. 1977 Apr;77(2):579–588. doi: 10.1016/0042-6822(77)90483-4. [DOI] [PubMed] [Google Scholar]
- Clerx-Van Haaster C. M., Clewley J. P., Bishop D. H. Oligonucleotide sequence analyses indicate that vesicular stomatitis virus large defective interfering virus particle RNA is made by internal deletion: evidence for similar transcription polyadenylation signals for the synthesis of all vesicular stomatitis virus mRNA species. J Virol. 1980 Feb;33(2):807–817. doi: 10.1128/jvi.33.2.807-817.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clinton G. M., Little S. P., Hagen F. S., Huang A. S. The matrix (M) protein of vesicular stomatitis virus regulates transcription. Cell. 1978 Dec;15(4):1455–1462. doi: 10.1016/0092-8674(78)90069-7. [DOI] [PubMed] [Google Scholar]
- Colonno R. J., Lazzarini R. A., Keene J. D., Banerjee A. K. In vitro synthesis of messenger RNA by a defective interfering particle of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1977 May;74(5):1884–1888. doi: 10.1073/pnas.74.5.1884. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Epstein D. A., Herman R. C., Chien I., Lazzarini R. A. Defective interfering particle generated by internal deletion of the vesicular stomatitis virus genome. J Virol. 1980 Feb;33(2):818–829. doi: 10.1128/jvi.33.2.818-829.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hartford S. L., Lesnaw J. A., Flygare W. H., MacLeod R., Reichmann M. E. Physical properties of New Jersey serotype of vesicular stomatitis virus and its defective particles. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1202–1205. doi: 10.1073/pnas.72.3.1202. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang A. S., Manders E. K. Ribonucleic acid synthesis of vesicular stomatitis virus. IV. Transcription by standard virus in the presence of defective interfering particles. J Virol. 1972 Jun;9(6):909–916. doi: 10.1128/jvi.9.6.909-916.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang A. S. Viral pathogenesis and molecular biology. Bacteriol Rev. 1977 Dec;41(4):811–821. doi: 10.1128/br.41.4.811-821.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Huang A. S., Wagner R. R. Defective T particles of vesicular stomatitis virus. II. Biologic role in homologous interference. Virology. 1966 Oct;30(2):173–181. doi: 10.1016/0042-6822(66)90093-6. [DOI] [PubMed] [Google Scholar]
- Hunt D. M., Emerson S. U., Wagner R. R. RNA- temperature-sensitive mutants of vesicular stomatitis virus: L-protein thermosensitivity accounts for transcriptase restriction of group I mutants. J Virol. 1976 May;18(2):596–603. doi: 10.1128/jvi.18.2.596-603.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kang C. Y., Prevec L. Proteins of vesicular stomatitis virus. I. Polyacrylamide gel analysis of viral antigens. J Virol. 1969 Apr;3(4):404–413. doi: 10.1128/jvi.3.4.404-413.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Keene J. D., Schubert M., Lazzarini R. A. Terminal sequences of vesicular stomatitis virus RNA are both complementary and conserved. J Virol. 1979 Oct;32(1):167–174. doi: 10.1128/jvi.32.1.167-174.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lafay F. Envelope proteins of vesicular stomatitis virus: effect of temperature-sensitive mutations in complementation groups III and V. J Virol. 1974 Nov;14(5):1220–1228. doi: 10.1128/jvi.14.5.1220-1228.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Leamnson R. N., Reichmann M. E. The RNA of defective vesicular stomatitis virus particles in relation to viral cistrons. J Mol Biol. 1974 Jan 5;85(4):551–568. doi: 10.1016/0022-2836(74)90315-5. [DOI] [PubMed] [Google Scholar]
- Leppert M., Kort L., Kolakofsky D. Further characterization of Sendai virus DI-RNAs: a model for their generation. Cell. 1977 Oct;12(2):539–552. doi: 10.1016/0092-8674(77)90130-1. [DOI] [PubMed] [Google Scholar]
- Lewis J. B., Esche H., Smart J. E., Stillman B. W., Harter M. L., Mathews M. B. Organization and expression of the left third of the genome of adenovirus. Cold Spring Harb Symp Quant Biol. 1980;44(Pt 1):493–508. doi: 10.1101/sqb.1980.044.01.052. [DOI] [PubMed] [Google Scholar]
- Metzel P. S., Reichmann M. E. Characterization of vesicular stomatitis virus mutants by partial proteolysis. J Virol. 1981 Jan;37(1):248–255. doi: 10.1128/jvi.37.1.248-255.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Perrault J., Holland J. J. Absence of transcriptase activity or transcription-inhibiting ability in defective interfering particles of vesicular stomatitis virus. Virology. 1972 Oct;50(1):150–170. [PubMed] [Google Scholar]
- Perrault J., Semler B. L. Internal genome deletions in two distinct classes of defective interfering particles of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6191–6195. doi: 10.1073/pnas.76.12.6191. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Petric M., Prevec L. Vesicular stomatitis virus--a new interfering particle, intracellular structures, and virus-specific RNA. Virology. 1970 Aug;41(4):615–630. doi: 10.1016/0042-6822(70)90427-7. [DOI] [PubMed] [Google Scholar]
- Prevec L., Kang C. Y. Homotypic and heterotypic interference by defective particles of vesicular stomatitis virus. Nature. 1970 Oct 3;228(5266):25–27. doi: 10.1038/228025a0. [DOI] [PubMed] [Google Scholar]
- Pringle C. R. Genetic characteristics of conditional lethal mutants of vesicular stomatitis virus induced by 5-fluorouracil, 5-azacytidine, and ethyl methane sulfonate. J Virol. 1970 May;5(5):559–567. doi: 10.1128/jvi.5.5.559-567.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rao D. D., Huang A. S. Synthesis of a small RNA in cells coinfected by standard and defective interfering particles of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3742–3745. doi: 10.1073/pnas.76.8.3742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reichmann M. E., Bishop D. H., Brown F., Crick J., Holland J. J., Kang C. Y., Lazzarini R., Moyer S., Perrault J., Prevec L. Proposal for a uniform nomenclature for defective interfering viruses of vesicular stomatitis virus. J Virol. 1980 Jun;34(3):792–794. doi: 10.1128/jvi.34.3.792-794.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reichmann M. E., Pringle C. R., Follett E. A. Defective particles in BHK cells infected with temperature-sensitive mutants of vesicular stomatitis virus. J Virol. 1971 Aug;8(2):154–160. doi: 10.1128/jvi.8.2.154-160.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reichmann M. E., Schnitzlein W. M., Bishop D. H., Lazzerini R. A., Beatrice S. T., Wagner R. R. Classification of the New Jersey serotype of vesicular stomatitis virus into two subtypes. J Virol. 1978 Jan;25(1):446–449. doi: 10.1128/jvi.25.1.446-449.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reichmann M. E., Villarreal L. P., Kohne D., Lesnaw J., Holland J. J. RNA polymerase activity and poly(A) synthesizing activity in defective T particles of vesicular stomatitis virus. Virology. 1974 Mar;58(1):240–249. doi: 10.1016/0042-6822(74)90158-5. [DOI] [PubMed] [Google Scholar]
- Repik P., Flamand A., Bishop D. H. Synthesis of RNA by mutants of vesicular stomatitis virus (Indiana serotype) and the ability of wild-type VSV New Jersey to complement the VSV Indiana ts G I-114 transcription defect. J Virol. 1976 Oct;20(1):157–169. doi: 10.1128/jvi.20.1.157-169.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Repik P., Flamand A., Clark H. F., Obijeski J. F., Roy P., Bishop D. H. Detection of homologous RNA sequences among six rhabdovirus genomes. J Virol. 1974 Jan;13(1):250–252. doi: 10.1128/jvi.13.1.250-252.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schnitzlein W. M., Reichmann M. E. A possible effect of viral proteins on the specificity of interference by defective vesicular stomatitis virus particles. Virology. 1977 Jul 15;80(2):275–288. doi: 10.1016/s0042-6822(77)80004-4. [DOI] [PubMed] [Google Scholar]
- Schnitzlein W. M., Reichmann M. E. Inhibition of vesicular stomatitis virus replication by adenosine. Virology. 1980 May;103(1):123–137. doi: 10.1016/0042-6822(80)90131-2. [DOI] [PubMed] [Google Scholar]
- Schnitzlein W. M., Reichmann M. E. Interference and RNA homologies of New Jersey serotype isolates vesicular stomatitis virus and their defective particles. Virology. 1977 Apr;77(2):490–500. doi: 10.1016/0042-6822(77)90474-3. [DOI] [PubMed] [Google Scholar]
- Schnitzlein W. M., Reichmann M. E. The size and the cistronic origin of defective vesicular stomatitis virus particle RNAs in relation to homotypic and heterotypic interference. J Mol Biol. 1976 Mar 5;101(3):307–325. doi: 10.1016/0022-2836(76)90150-9. [DOI] [PubMed] [Google Scholar]
- Schubert M., Keene J. D., Lazzarini R. A., Emerson S. U. The complete sequence of a unique RNA species synthesized by a DI particle of VSV. Cell. 1978 Sep;15(1):103–112. doi: 10.1016/0092-8674(78)90086-7. [DOI] [PubMed] [Google Scholar]
- Semler B. L., Perrault J., Abelson J., Holland J. J. Sequence of a RNA templated by the 3'-OH RNA terminus of defective interfering particles of vesicular stomatitis virus. Proc Natl Acad Sci U S A. 1978 Oct;75(10):4704–4708. doi: 10.1073/pnas.75.10.4704. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Stamminger G., Lazzarini R. A. Analysis of the RNA of defective VSV particles. Cell. 1974 Sep;3(1):85–93. doi: 10.1016/0092-8674(74)90044-0. [DOI] [PubMed] [Google Scholar]
- Testa D., Chanda P. K., Banerjee A. K. Unique mode of transcription in vitro by Vesicular stomatitis virus. Cell. 1980 Aug;21(1):267–275. doi: 10.1016/0092-8674(80)90134-8. [DOI] [PubMed] [Google Scholar]
- Wagner R. R., Schnaitman T. A., Snyder R. M. Structural proteins of vesicular stomatitis viruses. J Virol. 1969 Apr;3(4):395–403. doi: 10.1128/jvi.3.4.395-403.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]