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. 1976 Aug;19(2):685–708. doi: 10.1128/jvi.19.2.685-708.1976

Genome structure of incomplete particles of adenovirus.

E Daniell
PMCID: PMC354903  PMID: 957486

Abstract

Incomplete particles arising during productive growth of adenovirus were separated from infectious particles by density gradient centrifugation. The DNA contained in particles of low density was characterized by restriction enzyme analysis and by electron microscopy and heteroduplexing techniques. The DNA is heterogeneous in length, ranging in size from 15% of the normal genome to full length. Many individual molecules contain long, inverted terminal repetitions, which consist of the sequences extending from the normal left-hand end of the viral genome inward; the normal right end sequences appear to be missing from these molecules. The region of the genome reiterated in these molecules is that which has been implicated in transformation of rat cells by adenovirus (Gallimore, Sharp, and Sambrook, 1974; Graham, van der Eb, and Heijneker, 1974). A model for adenovirus replication is presented that accounts for the aberrant structures observed.

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Selected References

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  1. 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]
  2. Chow L. T., Davidson N. Electron microscope study of the structures of lambdadv DNAs. J Mol Biol. 1974 Jun 15;86(1):69–89. doi: 10.1016/s0022-2836(74)80008-2. [DOI] [PubMed] [Google Scholar]
  3. Denhardt D. T. A membrane-filter technique for the detection of complementary DNA. Biochem Biophys Res Commun. 1966 Jun 13;23(5):641–646. doi: 10.1016/0006-291x(66)90447-5. [DOI] [PubMed] [Google Scholar]
  4. Englund P. T. Analysis of nucleotide sequences at 3' termini of duplex deoxyribonucleic acid with the use of the T4 deoxyribonucleic acid polymerase. J Biol Chem. 1971 May 25;246(10):3269–3276. [PubMed] [Google Scholar]
  5. Fuke M., Thomas C. A., Jr Isolation of open-circular DNA molecules by retention in agar gels. J Mol Biol. 1970 Sep 14;52(2):395–397. doi: 10.1016/0022-2836(70)90040-9. [DOI] [PubMed] [Google Scholar]
  6. Gallimore P. H. Viral DNA in transformed cells. II. A study of the sequences of adenovirus 2 DNA IN NINE LINES OF TRANSFORMED RAT CELLS USING SPECIFIC FRAGMENTS OF THE VIRAL GENOME;. J Mol Biol. 1974 Oct 15;89(1):49–72. doi: 10.1016/0022-2836(74)90162-4. [DOI] [PubMed] [Google Scholar]
  7. Garon C. F., Berry K. W., Rose J. A. A unique form of terminal redundancy in adenovirus DNA molecules. Proc Natl Acad Sci U S A. 1972 Sep;69(9):2391–2395. doi: 10.1073/pnas.69.9.2391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Garon C. F., Berry K. W., Rose J. A. Arrangement of sequences in the inverted terminal repetition of adenovirus 18 DNA. Proc Natl Acad Sci U S A. 1975 Aug;72(8):3039–3043. doi: 10.1073/pnas.72.8.3039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Graham F. L., van der Eb A. J., Heijneker H. L. Size and location of the transforming region in human adenovirus type 5 DNA. Nature. 1974 Oct 25;251(5477):687–691. doi: 10.1038/251687a0. [DOI] [PubMed] [Google Scholar]
  10. Horwitz M. S. Location of the origin of DNA replication in adenovirus Type 2. J Virol. 1974 May;13(5):1046–1054. doi: 10.1128/jvi.13.5.1046-1054.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Huang A. S. Defective interfering viruses. Annu Rev Microbiol. 1973;27:101–117. doi: 10.1146/annurev.mi.27.100173.000533. [DOI] [PubMed] [Google Scholar]
  12. Igarashi K., Niiyama Y., Tsukamoto K., Kurokawa T., Sugino Y. Biochemical studies on bovine adenovirus type 3. II. Incomplete virus. J Virol. 1975 Sep;16(3):634–641. doi: 10.1128/jvi.16.3.634-641.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lavelle G., Patch C., Khoury G., Rose J. Isolation and partial characterization of single-stranded adenoviral DNA produced during synthesis of adenovirus type 2 DNA. J Virol. 1975 Oct;16(4):775–782. doi: 10.1128/jvi.16.4.775-782.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Maizel J. V., Jr, White D. O., Scharff M. D. The polypeptides of adenovirus. II. Soluble proteins, cores, top components and the structure of the virion. Virology. 1968 Sep;36(1):126–136. doi: 10.1016/0042-6822(68)90122-0. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Mulder C., Arrand J. R., Delius H., Keller W., Pettersson U., Roberts R. J., Sharp P. A. Cleavage maps of DNA from adenovirus types 2 and 5 by restriction endonucleases EcoRI and HpaI. Cold Spring Harb Symp Quant Biol. 1975;39(Pt 1):397–400. doi: 10.1101/sqb.1974.039.01.051. [DOI] [PubMed] [Google Scholar]
  17. Niiyama Y., Igarashi K., Tsukamoto K., Kurokawa T., Sugino Y. Biochemical studies on bovine adenovirus type 3. I. Purification and properties. J Virol. 1975 Sep;16(3):621–633. doi: 10.1128/jvi.16.3.621-633.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pearson G. D., Hanawalt P. C. Isolation of DNA replication complexes from uninfected and adenovirus-infected HeLa cells. J Mol Biol. 1971 Nov 28;62(1):65–80. doi: 10.1016/0022-2836(71)90131-8. [DOI] [PubMed] [Google Scholar]
  19. Pettersson U. Letter: Some unusual properties of replicating adenovirus type 2 DNA. J Mol Biol. 1973 Dec 25;81(4):521–527. doi: 10.1016/0022-2836(73)90521-4. [DOI] [PubMed] [Google Scholar]
  20. Pettersson U., Sambrook J. Amount of viral DNA in the genome of cells transformed by adenovirus type 2. J Mol Biol. 1973 Jan;73(1):125–130. doi: 10.1016/0022-2836(73)90164-2. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Rainbow A. J., Mak S. Functional heterogeneity of virions in human adenovirus types 2 and 12. J Virol. 1970 Feb;5(2):188–193. doi: 10.1128/jvi.5.2.188-193.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Robberson D. L., Fried M. Sequence arrangements in clonal isolates of polyoma defective DNA. Proc Natl Acad Sci U S A. 1974 Sep;71(9):3497–3501. doi: 10.1073/pnas.71.9.3497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Roberts R. J., Arrand J. R., Keller W. The length of the terminal repetition in adenovirus-2 DNA. Proc Natl Acad Sci U S A. 1974 Oct;71(10):3829–3833. doi: 10.1073/pnas.71.10.3829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Robin J., Bourgaux-Ramoisy D., Bourgaux P. Single-stranded regions in replicating DNA of adenovirus type 2. J Gen Virol. 1973 Aug;20(2):233–237. doi: 10.1099/0022-1317-20-2-233. [DOI] [PubMed] [Google Scholar]
  26. Robinson A. J., Younghusband H. B., Bellett A. J. A circula DNA-protein complex from adenoviruses. Virology. 1973 Nov;56(1):54–69. doi: 10.1016/0042-6822(73)90287-0. [DOI] [PubMed] [Google Scholar]
  27. Rosenwirth B., Tjia S., Westphal M., Doerfler W. Incomplete particles of adenovirus. II. Kinetics of formation and polypeptide composition of adenovirus type 2. Virology. 1974 Aug;60(2):431–437. doi: 10.1016/0042-6822(74)90337-7. [DOI] [PubMed] [Google Scholar]
  28. Sambrook J., Williams J., Sharp P. A., Grodzicker T. Physical mapping of temperature-sensitive mutations of adenoviruses. J Mol Biol. 1975 Sep 25;97(3):369–390. doi: 10.1016/s0022-2836(75)80046-5. [DOI] [PubMed] [Google Scholar]
  29. Sauer G., Koprowski H., Defendi V. The genetic heterogeneity of simian virus 40. Proc Natl Acad Sci U S A. 1967 Aug;58(2):599–606. doi: 10.1073/pnas.58.2.599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. 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]
  31. Schilling R., Weingärtner B., Winnacker E. L. Adenovirus type 2 DNA replication. II. Termini of DNA replication. J Virol. 1975 Oct;16(4):767–774. doi: 10.1128/jvi.16.4.767-774.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Sharp P. A., Sugden B., Sambrook J. Detection of two restriction endonuclease activities in Haemophilus parainfluenzae using analytical agarose--ethidium bromide electrophoresis. Biochemistry. 1973 Jul 31;12(16):3055–3063. doi: 10.1021/bi00740a018. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Southern E. M. Long range periodicities in mouse satellite DNA. J Mol Biol. 1975 May 5;94(1):51–69. doi: 10.1016/0022-2836(75)90404-0. [DOI] [PubMed] [Google Scholar]
  35. Steenbergh P. H., Sussenbach J. S., Roberts R. J., Jansz H. S. The 3'-terminal nucleotide sequences of adenovirus types 2 and 5 DNA. J Virol. 1975 Feb;15(2):268–272. doi: 10.1128/jvi.15.2.268-272.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sussenbach J. S., Ellens D. J., Jansz H. S. Studies on the mechanism of replication of adenovirus DNA. II. The nature of single-stranded DNA in replicative intermediates. J Virol. 1973 Nov;12(5):1131–1138. doi: 10.1128/jvi.12.5.1131-1138.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Tolun A., Pettersson U. Termination sites for adenovirus type 2 DNA replication. J Virol. 1975 Oct;16(4):759–766. doi: 10.1128/jvi.16.4.759-766.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. Wolfson J., Dressler D. Adenovirus-2 DNA contains an inverted terminal repetition. Proc Natl Acad Sci U S A. 1972 Oct;69(10):3054–3057. doi: 10.1073/pnas.69.10.3054. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Yoshiike K. Studies on DNA from low-density particles of SV40. I. Heterogeneous defective virions produced by successive undiluted passages. Virology. 1968 Mar;34(3):391–401. doi: 10.1016/0042-6822(68)90059-7. [DOI] [PubMed] [Google Scholar]
  41. van der Eb A. J. Intermediates in type 5 adenovirus DNA replication. Virology. 1973 Jan;51(1):11–23. doi: 10.1016/0042-6822(73)90361-9. [DOI] [PubMed] [Google Scholar]

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