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. 1987 May;61(5):1517–1523. doi: 10.1128/jvi.61.5.1517-1523.1987

Defective interfering virus associated with A/Chicken/Pennsylvania/83 influenza virus.

T M Chambers, R G Webster
PMCID: PMC254130  PMID: 3573146

Abstract

The A/Chicken/Pennsylvania/1/83 influenza virus, isolated from a respiratory infection of chickens, is an avirulent H5N2 virus containing subgenomic RNAs (W.J. Bean, Y. Kawaoka, J.M. Wood, J.E. Pearson, and R.G. Webster, J. Virol. 54:151-160, 1985). We show here that defective interfering particles are present in this virus population. The virus had a low ratio of plaque-forming to hemagglutinating units and produced interference with standard virus multiplication in infectious center reduction assays. Subgenomic RNAs were identified as internally deleted polymerase RNAs. We have confirmed that this virus protects chickens from lethal H5N2 influenza virus infection. This protective effect appeared to be due to the inhibition of virulent virus multiplication. Additionally, subgenomic RNAs derived from polymerase RNAs were detected in 5 of 18 RNA preparations from animal influenza virus isolates. Therefore, defective interfering particles are sometimes produced in natural influenza virus infections, not just under laboratory conditions. These particles may be capable of suppressing the pathogenic effect of virulent virus infections in nature.

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Selected References

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  1. Barrett A. D., Dimmock N. J. Defective interfering viruses and infections of animals. Curr Top Microbiol Immunol. 1986;128:55–84. doi: 10.1007/978-3-642-71272-2_2. [DOI] [PubMed] [Google Scholar]
  2. Bean W. J., Jr, Simpson R. W. Transcriptase activity and genome composition of defective influenza virus. J Virol. 1976 Apr;18(1):365–369. doi: 10.1128/jvi.18.1.365-369.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bean W. J., Jr, Sriram G., Webster R. G. Electrophoretic analysis of iodine-labeled influenza virus RNA segments. Anal Biochem. 1980 Feb;102(1):228–232. doi: 10.1016/0003-2697(80)90343-7. [DOI] [PubMed] [Google Scholar]
  4. Bean W. J., Kawaoka Y., Wood J. M., Pearson J. E., Webster R. G. Characterization of virulent and avirulent A/chicken/Pennsylvania/83 influenza A viruses: potential role of defective interfering RNAs in nature. J Virol. 1985 Apr;54(1):151–160. doi: 10.1128/jvi.54.1.151-160.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bishop D. H., Huddleston J. A., Brownlee G. G. The complete sequence of RNA segment 2 of influenza A/NT/60/68 P1 protein. Nucleic Acids Res. 1982 Feb 25;10(4):1335–1343. doi: 10.1093/nar/10.4.1335. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bishop D. H., Jones K. L., Huddleston J. A., Brownlee G. G. Influenza A virus evolution: complete sequences of influenza A/NT/60/68 RNA segment 3 and its predicted acidic P polypeptide compared with those of influenza A/PR/8/34. Virology. 1982 Jul 30;120(2):481–489. doi: 10.1016/0042-6822(82)90049-6. [DOI] [PubMed] [Google Scholar]
  7. Bosch F. X., Orlich M., Klenk H. D., Rott R. The structure of the hemagglutinin, a determinant for the pathogenicity of influenza viruses. Virology. 1979 May;95(1):197–207. doi: 10.1016/0042-6822(79)90414-8. [DOI] [PubMed] [Google Scholar]
  8. Carter M. J., Mahy B. W. Incomplete avian influenza A virus displays anomalous interference. Arch Virol. 1982;74(1):71–76. doi: 10.1007/BF01320784. [DOI] [PubMed] [Google Scholar]
  9. Carter M. J., Mahy B. W. Incomplete avian influenza virus contains a defective non-interfering component. Arch Virol. 1982;71(1):13–25. doi: 10.1007/BF01315172. [DOI] [PubMed] [Google Scholar]
  10. Cave D. R., Hagen F. S., Palma E. L., Huang A. S. Detection of vesicular stomatitis virus RNA and its defective-interfering particles in individual mouse brains. J Virol. 1984 Apr;50(1):86–91. doi: 10.1128/jvi.50.1.86-91.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cave D. R., Hendrickson F. M., Huang A. S. Defective interfering virus particles modulate virulence. J Virol. 1985 Aug;55(2):366–373. doi: 10.1128/jvi.55.2.366-373.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chanda P. K., Chambers T. M., Nayak D. P. In vitro transcription of defective interfering particles of influenza virus produces polyadenylic acid-containing complementary RNAs. J Virol. 1983 Jan;45(1):55–61. doi: 10.1128/jvi.45.1.55-61.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. De B. K., Nayak D. P. Defective interfering influenza viruses and host cells: establishment and maintenance of persistent influenza virus infection in MDBK and HeLa cells. J Virol. 1980 Dec;36(3):847–859. doi: 10.1128/jvi.36.3.847-859.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Deshpande K. L., Naeve C. W., Webster R. G. The neuraminidases of the virulent and avirulent A/Chicken/Pennsylvania/83 (H5N2) influenza A viruses: sequence and antigenic analyses. Virology. 1985 Nov;147(1):49–60. doi: 10.1016/0042-6822(85)90226-0. [DOI] [PubMed] [Google Scholar]
  15. Dimmock N. J., Beck S., McLain L. Protection of mice from lethal influenza: evidence that defective interfering virus modulates the immune response and not virus multiplication. J Gen Virol. 1986 May;67(Pt 5):839–850. doi: 10.1099/0022-1317-67-5-839. [DOI] [PubMed] [Google Scholar]
  16. Holland J. J., Doyle M. Attempts to detect homologous autointerference in vivo with influenza virus and vesicular stomatitis virus. Infect Immun. 1973 Apr;7(4):526–531. doi: 10.1128/iai.7.4.526-531.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Huang A. S., Baltimore D. Defective viral particles and viral disease processes. Nature. 1970 Apr 25;226(5243):325–327. doi: 10.1038/226325a0. [DOI] [PubMed] [Google Scholar]
  18. Huddleston J. A., Brownlee G. G. The sequence of the nucleoprotein gene of human influenza A virus, strain A/NT/60/68. Nucleic Acids Res. 1982 Feb 11;10(3):1029–1038. doi: 10.1093/nar/10.3.1029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Janda J. M., Davis A. R., Nayak D. P., De B. K. Diversity and generation of defective interfering influenza virus particles. Virology. 1979 May;95(1):48–58. doi: 10.1016/0042-6822(79)90400-8. [DOI] [PubMed] [Google Scholar]
  20. Jennings P. A., Finch J. T., Winter G., Robertson J. S. Does the higher order structure of the influenza virus ribonucleoprotein guide sequence rearrangements in influenza viral RNA? Cell. 1983 Sep;34(2):619–627. doi: 10.1016/0092-8674(83)90394-x. [DOI] [PubMed] [Google Scholar]
  21. Jones K. L., Huddleston J. A., Brownlee G. G. The sequence of RNA segment 1 of influenza virus A/NT/60/68 and its comparison with the corresponding segment of strains A/PR/8/34 and A/WSN/33. Nucleic Acids Res. 1983 Mar 11;11(5):1555–1566. doi: 10.1093/nar/11.5.1555. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Kawaoka Y., Naeve C. W., Webster R. G. Is virulence of H5N2 influenza viruses in chickens associated with loss of carbohydrate from the hemagglutinin? Virology. 1984 Dec;139(2):303–316. doi: 10.1016/0042-6822(84)90376-3. [DOI] [PubMed] [Google Scholar]
  23. Kawaoka Y., Webster R. G. Evolution of the A/Chicken/Pennsylvania/83 (H5N2) influenza virus. Virology. 1985 Oct 15;146(1):130–137. doi: 10.1016/0042-6822(85)90059-5. [DOI] [PubMed] [Google Scholar]
  24. Nayak D. P., Chambers T. M., Akkina R. K. Defective-interfering (DI) RNAs of influenza viruses: origin, structure, expression, and interference. Curr Top Microbiol Immunol. 1985;114:103–151. doi: 10.1007/978-3-642-70227-3_3. [DOI] [PubMed] [Google Scholar]
  25. Plotch S. J., Krug R. M. Influenza virion transcriptase: synthesis in vitro of large, polyadenylic acid-containing complementary RNA. J Virol. 1977 Jan;21(1):24–34. doi: 10.1128/jvi.21.1.24-34.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Rabinowitz S. G., Huprikar J. The influence of defective-interfering particles of the PR-8 strain of influenza A virus on the pathogenesis of pulmonary infection in mice. J Infect Dis. 1979 Sep;140(3):305–315. doi: 10.1093/infdis/140.3.305. [DOI] [PubMed] [Google Scholar]
  27. Sriram G., Bean W. J., Jr, Hinshaw V. S., Webster R. G. Genetic diversity among avian influenza viruses. Virology. 1980 Sep;105(2):592–599. doi: 10.1016/0042-6822(80)90059-8. [DOI] [PubMed] [Google Scholar]
  28. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. VON MAGNUS P. Propagation of the PR8 strain of influenza A virus in chick embryos. III. Properties of the incomplete virus produced in serial passages of undiluted virus. Acta Pathol Microbiol Scand. 1951;29(2):157–181. doi: 10.1111/j.1699-0463.1951.tb00114.x. [DOI] [PubMed] [Google Scholar]
  30. Wallace R. B., Shaffer J., Murphy R. F., Bonner J., Hirose T., Itakura K. Hybridization of synthetic oligodeoxyribonucleotides to phi chi 174 DNA: the effect of single base pair mismatch. Nucleic Acids Res. 1979 Aug 10;6(11):3543–3557. doi: 10.1093/nar/6.11.3543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Winter G., Fields S. Cloning of influenza cDNA ino M13: the sequence of the RNA segment encoding the A/PR/8/34 matrix protein. Nucleic Acids Res. 1980 May 10;8(9):1965–1974. doi: 10.1093/nar/8.9.1965. [DOI] [PMC free article] [PubMed] [Google Scholar]

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