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. 1981 Feb;37(2):620–627. doi: 10.1128/jvi.37.2.620-627.1981

Subgenomic viral DNA species synthesized in simian cells by human and simian adenoviruses.

E Daniell
PMCID: PMC171049  PMID: 6261009

Abstract

DNA synthesized after infection of simian tissue culture cells (BSC-1 or CV-1) with human adenovirus type 2 or 5 or with simian adenovirus 7 was characterized. It was demonstrated that as much as 40% of the virus-specific DNA in nuclei of infected monkey cells consists of subgenomic pieces. No subgenomic viral DNA species were detected in the nuclei of human (HeLa) cells infected with these adenovirus types. Restriction analysis showed that these short viral DNA molecules contain normal amounts of the sequences from the ends of the viral genome, whereas internal regions are underrepresented. The production of subgenomic DNAs is not correlated with semipermissive infection. Although adenovirus types 2 and 5 are restricted in monkey cells, these cells are fully permissive for simian adenovirus 7. HR404, an adenovirus type 5 mutant which is not restricted in monkey cells, produced the same percentage of subgenomic DNAs as did its wild type (restricted) parent, and coinfection of monkey cells with adenovirus type 5 DNAs. The array of predominant size classes among the heterogeneously sized short DNAs is serotype specific. Extensive plaque purification and comparison of wild-type adenovirus type 5 with several viral mutants indicated that the distribution of aberrant sizes of DNA is characteristic of the virus and not a result of random replicative errors and then enrichment of particular species.

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Selected References

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

  1. Baum S. G. Persistent adenovirus infections of nonpermissive monkey cells. J Virol. 1977 Aug;23(2):412–420. doi: 10.1128/jvi.23.2.412-420.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Burlingham B. T., Brown D. T., Doerfler W. Incomplete particles of adenovirus. I. Characteristics of the DNA associated with incomplete adenovirions of types 2 and 12. Virology. 1974 Aug;60(2):419–430. doi: 10.1016/0042-6822(74)90336-5. [DOI] [PubMed] [Google Scholar]
  3. Burnett J. P., Harrington J. A. Simian adenovirus SA7 DNA: chemical, physical, and biological studies. Proc Natl Acad Sci U S A. 1968 Jul;60(3):1023–1029. doi: 10.1073/pnas.60.3.1023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. DULBECCO R., FREEMAN G. Plaque production by the polyoma virus. Virology. 1959 Jul;8(3):396–397. doi: 10.1016/0042-6822(59)90043-1. [DOI] [PubMed] [Google Scholar]
  5. Daniell E. Genome structure of incomplete particles of adenovirus. J Virol. 1976 Aug;19(2):685–708. doi: 10.1128/jvi.19.2.685-708.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Daniell E., Mullenbach T. Synthesis of defective viral DNA in HeLa cells infected with adenovirus type 3. J Virol. 1978 Apr;26(1):61–70. doi: 10.1128/jvi.26.1.61-70.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Edvardsson B., Ustacelebi S., Williams J., Philipson L. Assembly intermediates among adenovirus type 5 temperature-sensitive mutants. J Virol. 1978 Feb;25(2):641–651. doi: 10.1128/jvi.25.2.641-651.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Ensinger M. J., Ginsberg H. S. Selection and preliminary characterization of temperature-sensitive mutants of type 5 adenovirus. J Virol. 1972 Sep;10(3):328–339. doi: 10.1128/jvi.10.3.328-339.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Eron L. Post-transcriptional restriction of human adenovirus expression in monkey cells. J Virol. 1975 May;15(5):1256–1261. doi: 10.1128/jvi.15.5.1256-1261.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Estes M. K. Characterization of DNA-protein complexes from simian adenovirus SA7. J Virol. 1978 Mar;25(3):917–922. doi: 10.1128/jvi.25.3.917-922.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Everitt E., Meador S. A., Levine A. S. Synthesis and processing of the precursor to the major core protein of adenovirus type 2. J Virol. 1977 Jan;21(1):199–214. doi: 10.1128/jvi.21.1.199-214.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fox R. I., Baum S. G. Synthesis of viral ribonucleic acid during restricted adenovirus infection. J Virol. 1972 Aug;10(2):220–227. doi: 10.1128/jvi.10.2.220-227.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Friedman M. P., Lyons M. J., Ginsberg H. S. Biochemical consequences of type 2 adenovirus and Simian virus 40 double infections of African green monkey kidney cells. J Virol. 1970 May;5(5):586–597. doi: 10.1128/jvi.5.5.586-597.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Grodzicker T., Anderson C., Sharp P. A., Sambrook J. Conditional lethal mutants of adenovirus 2-simian virus 40 hybrids. I. Host range mutants of Ad2+ND1. J Virol. 1974 Jun;13(6):1237–1244. doi: 10.1128/jvi.13.6.1237-1244.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hashimoto K., Nakajima K., Oda K., Shimojo H. Complementation of translational defect for growth of human adenovirus type 2 in Simian cells by a Simian virus 40-induced factor. J Mol Biol. 1973 Dec 5;81(2):207–223. doi: 10.1016/0022-2836(73)90190-3. [DOI] [PubMed] [Google Scholar]
  16. Holland J. J., Villarreal L. P., Breindl M. Factors involved in the generation and replication of rhabdovirus defective T particles. J Virol. 1976 Mar;17(3):805–815. doi: 10.1128/jvi.17.3.805-815.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Horwitz M. S., Brayton C., Baum S. G. Synthesis of type 2 adenovirus DNA in the presence of cycloheximide. J Virol. 1973 Apr;11(4):544–551. doi: 10.1128/jvi.11.4.544-551.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. JENSEN F. C., GIRARDI A. J., GILDEN R. V., KOPROWSKI H. INFECTION OF HUMAN AND SIMIAN TISSUE CULTURES WITH ROUS SARCOMA VIRUS. Proc Natl Acad Sci U S A. 1964 Jul;52:53–59. doi: 10.1073/pnas.52.1.53. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ketner G., Kelly T. J., Jr Integrated simian virus 40 sequences in transformed cell DNA: analysis using restriction endonucleases. Proc Natl Acad Sci U S A. 1976 Apr;73(4):1102–1106. doi: 10.1073/pnas.73.4.1102. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Klessig D. F., Anderson C. W. Block to multiplication of adenovirus serotype 2 in monkey cells. J Virol. 1975 Dec;16(6):1650–1668. doi: 10.1128/jvi.16.6.1650-1668.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Klessig D. F., Hassell J. A. Characterization of a variant of human adenovirus type 2 which multiples efficiently in simian cells. J Virol. 1978 Dec;28(3):945–956. doi: 10.1128/jvi.28.3.945-956.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Klessig D. F. Isolation of a variant of human adenovirus serotype 2 that multiplies efficiently on monkey cells. J Virol. 1977 Mar;21(3):1243–1246. doi: 10.1128/jvi.21.3.1243-1246.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lazzarini R. A., Weber G. H., Johnson L. D., Stamminger G. M. Covalently linked message and anti-message (genomic) RNA from a defective vesicular stomatitis virus particle. J Mol Biol. 1975 Sep 25;97(3):289–307. doi: 10.1016/s0022-2836(75)80042-8. [DOI] [PubMed] [Google Scholar]
  24. Lucas J. J., Ginsberg H. S. Transcription and transport of virus-specific ribonucleic acids in African green monkey kidney cells abortively infected with type 2 adenovirus. J Virol. 1972 Dec;10(6):1109–1117. doi: 10.1128/jvi.10.6.1109-1117.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Mak S. Defective virions in human adenovirus type 12. J Virol. 1971 Apr;7(4):426–433. doi: 10.1128/jvi.7.4.426-433.1971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Maniatis T., Jeffrey A., Kleid D. G. Nucleotide sequence of the rightward operator of phage lambda. Proc Natl Acad Sci U S A. 1975 Mar;72(3):1184–1188. doi: 10.1073/pnas.72.3.1184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Perrault J., Holland J. Variability of vesicular stomatitis virus autointerference with different host cells and virus serotypes. Virology. 1972 Oct;50(1):148–158. doi: 10.1016/0042-6822(72)90355-8. [DOI] [PubMed] [Google Scholar]
  28. Perrault J., Leavitt R. W. Characterization of snap-back RNAs in vesicular stomatitis defective interfering virus particles. J Gen Virol. 1978 Jan;38(1):21–34. doi: 10.1099/0022-1317-38-1-21. [DOI] [PubMed] [Google Scholar]
  29. Perrault J., Leavitt R. W. Inverted complementary terminal sequences in single-stranded RNAs and snap-back RNAs from vesicular stomatitis defective interfering particles. J Gen Virol. 1978 Jan;38(1):35–50. doi: 10.1099/0022-1317-38-1-35. [DOI] [PubMed] [Google Scholar]
  30. Prage L., Höglund S., Philipson L. Structural proteins of adenoviruses. 8. Characterization of incomplete particles of adenovirus type 3. Virology. 1972 Sep;49(3):745–757. doi: 10.1016/0042-6822(72)90531-4. [DOI] [PubMed] [Google Scholar]
  31. Price J. A., Norkin L. C. Defective virions of simian adenovirus 7 produced by one passage at high multiplicity of infection. Virology. 1978 Nov;91(1):194–197. doi: 10.1016/0042-6822(78)90367-7. [DOI] [PubMed] [Google Scholar]
  32. RABSON A. S., O'CONOR G. T., BEREZESKY I. K., PAUL F. J. ENHANCEMENT OF ADENOVIRUS GROWTH IN AFRICAN GREEN MONKEY KIDNEY CELL CULTURES BY SV40. Proc Soc Exp Biol Med. 1964 May;116:187–190. doi: 10.3181/00379727-116-29197. [DOI] [PubMed] [Google Scholar]
  33. Reich P. R., Baum S. G., Rose J. A., Rowe W. P., Weissman S. M. Nucleic acid homology studies of adenovirus type 7-SV40 interactions. Proc Natl Acad Sci U S A. 1966 Feb;55(2):336–341. doi: 10.1073/pnas.55.2.336. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. 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]
  35. Russel W. C., Newman C., Williams J. F. Characterization of temperature-sensitive mutants of adenovirus type 5--serology. J Gen Virol. 1972 Dec;17(3):265–279. doi: 10.1099/0022-1317-17-3-265. [DOI] [PubMed] [Google Scholar]
  36. Schaller J. P., Yohn D. S. Transformation potentials of the noninfectious (defective) component in pools of adenoviruses type 12 and simian adenovirus 7. J Virol. 1974 Aug;14(2):392–401. doi: 10.1128/jvi.14.2.392-401.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  38. Sussenbach J. S., Kuijk M. G. Studies on the mechanism of replication of adenovirus DNA. V. The location of termini of replication. Virology. 1977 Mar;77(1):149–157. doi: 10.1016/0042-6822(77)90414-7. [DOI] [PubMed] [Google Scholar]
  39. Wadell G., Hammarskjöld M. L., Varsanyi T. Incomplete virus particles of adenovirus type 16. J Gen Virol. 1973 Sep;20(3):287–302. doi: 10.1099/0022-1317-20-3-287. [DOI] [PubMed] [Google Scholar]
  40. Wilkie N. M., Ustacelebi S., Williams J. F. Characterization of temperature-sensitive mutants of adenovirus type 5: nucleic acid synthesis. Virology. 1973 Feb;51(2):499–503. doi: 10.1016/0042-6822(73)90450-9. [DOI] [PubMed] [Google Scholar]
  41. Williams J. F. Enhancement of adenovirus plaque formation on HeLa cells by magnesium chloride. J Gen Virol. 1970 Dec;9(3):251–255. doi: 10.1099/0022-1317-9-3-251. [DOI] [PubMed] [Google Scholar]

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