Abstract
The distribution of terminal-sequence orientations in the viral DNA of bovine parvovirus (BPV), an autonomous parvovirus, was studied by end labeling and restriction enzyme digestion and also by cloning. The left (3') end of the minus strand of BPV was found in two alternative sequence orientations (designated as flip and flop, which are reverse complements of each other), with a 10-fold excess of flip. This is in contrast to the autonomous rodent parvoviruses which encapsidate minus-strand DNA with only the flip orientation at this end. The right (5') end of the minus strand of BPV contained both sequence orientations with equal frequencies, as in the rodent parvoviruses. Sequence inversions were also detected at both ends of the plus strand, which makes up about 10% of the encapsidated BPV DNA. Each terminus of BPV DNA had a characteristic ratio of flip to flop forms, and this ratio was restored in the progeny DNA resulting from transfection with genomic clones of different defined terminal conformations. Replicative-form DNA showed the same distribution of terminal-sequence orientations as the reannealed plus and minus virion DNAs, suggesting that the distribution of flip and flop forms observed in virion DNA is not due to selective encapsidation, but rather to the specific distribution of replicative forms. The current replication model for autonomous parvoviruses, which was based on the available data for the rodent parvoviruses, cannot account for the observed distribution of BPV DNA. An alternative model is suggested.
Full text
PDFImages in this article
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Astell C. R., Chow M. B., Ward D. C. Sequence analysis of the termini of virion and replicative forms of minute virus of mice DNA suggests a modified rolling hairpin model for autonomous parvovirus DNA replication. J Virol. 1985 Apr;54(1):171–177. doi: 10.1128/jvi.54.1.171-177.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Astell C. R., Gardiner E. M., Tattersall P. DNA sequence of the lymphotropic variant of minute virus of mice, MVM(i), and comparison with the DNA sequence of the fibrotropic prototype strain. J Virol. 1986 Feb;57(2):656–669. doi: 10.1128/jvi.57.2.656-669.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Astell C. R., Smith M., Chow M. B., Ward D. C. Structure of the 3' hairpin termini of four rodent parvovirus genomes: nucleotide sequence homology at origins of DNA replication. Cell. 1979 Jul;17(3):691–703. doi: 10.1016/0092-8674(79)90276-9. [DOI] [PubMed] [Google Scholar]
- Astell C. R., Thomson M., Merchlinsky M., Ward D. C. The complete DNA sequence of minute virus of mice, an autonomous parvovirus. Nucleic Acids Res. 1983 Feb 25;11(4):999–1018. doi: 10.1093/nar/11.4.999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bates R. C., Snyder C. E., Banerjee P. T., Mitra S. Autonomous parvovirus LuIII encapsidates equal amounts of plus and minus DNA strands. J Virol. 1984 Feb;49(2):319–324. doi: 10.1128/jvi.49.2.319-324.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berns K. I., Bohenzky R. A. Adeno-associated viruses: an update. Adv Virus Res. 1987;32:243–306. doi: 10.1016/s0065-3527(08)60479-0. [DOI] [PubMed] [Google Scholar]
- Berns K. I., Labow M. A. Parvovirus gene regulation. J Gen Virol. 1987 Mar;68(Pt 3):601–614. doi: 10.1099/0022-1317-68-3-601. [DOI] [PubMed] [Google Scholar]
- Biggin M. D., Gibson T. J., Hong G. F. Buffer gradient gels and 35S label as an aid to rapid DNA sequence determination. Proc Natl Acad Sci U S A. 1983 Jul;80(13):3963–3965. doi: 10.1073/pnas.80.13.3963. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cavalier-Smith T. Palindromic base sequences and replication of eukaryote chromosome ends. Nature. 1974 Aug 9;250(5466):467–470. doi: 10.1038/250467a0. [DOI] [PubMed] [Google Scholar]
- Chen K. C., Shull B. C., Moses E. A., Lederman M., Stout E. R., Bates R. C. Complete nucleotide sequence and genome organization of bovine parvovirus. J Virol. 1986 Dec;60(3):1085–1097. doi: 10.1128/jvi.60.3.1085-1097.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cotmore S. F., Tattersall P. Characterization and molecular cloning of a human parvovirus genome. Science. 1984 Dec 7;226(4679):1161–1165. doi: 10.1126/science.6095448. [DOI] [PubMed] [Google Scholar]
- Cotmore S. F., Tattersall P. The autonomously replicating parvoviruses of vertebrates. Adv Virus Res. 1987;33:91–174. doi: 10.1016/s0065-3527(08)60317-6. [DOI] [PubMed] [Google Scholar]
- Fife K. H., Berns K. I., Murray K. Structure and nucleotide sequence of the terminal regions of adeno-associated virus DNA. Virology. 1977 May 15;78(2):475–477. doi: 10.1016/0042-6822(77)90124-6. [DOI] [PubMed] [Google Scholar]
- Lusby E., Fife K. H., Berns K. I. Nucleotide sequence of the inverted terminal repetition in adeno-associated virus DNA. J Virol. 1980 May;34(2):402–409. doi: 10.1128/jvi.34.2.402-409.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muller D. E., Siegl G. Maturation of parvovirus LuIII in a subcellular system. I. Optimal conditions for in vitro synthesis and encapsidation of viral DNA. J Gen Virol. 1983 May;64(Pt 5):1043–1054. doi: 10.1099/0022-1317-64-5-1043. [DOI] [PubMed] [Google Scholar]
- Rhode S. L., 3rd, Klaassen B. DNA sequence of the 5' terminus containing the replication origin of parvovirus replicative form DNA. J Virol. 1982 Mar;41(3):990–999. doi: 10.1128/jvi.41.3.990-999.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Robertson A. T., Stout E. R., Bates R. C. Aphidicolin inhibition of the production of replicative-form DNA during bovine parvovirus infection. J Virol. 1984 Mar;49(3):652–657. doi: 10.1128/jvi.49.3.652-657.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roychoudhury R., Wu R. Terminal transferase-catalyzed addition of nucleotides to the 3' termini of DNA. Methods Enzymol. 1980;65(1):43–62. doi: 10.1016/s0076-6879(80)65009-5. [DOI] [PubMed] [Google Scholar]
- Sahli R., McMaster G. K., Hirt B. DNA sequence comparison between two tissue-specific variants of the autonomous parvovirus, minute virus of mice. Nucleic Acids Res. 1985 May 24;13(10):3617–3633. doi: 10.1093/nar/13.10.3617. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samulski R. J., Berns K. I., Tan M., Muzyczka N. Cloning of adeno-associated virus into pBR322: rescue of intact virus from the recombinant plasmid in human cells. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2077–2081. doi: 10.1073/pnas.79.6.2077. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Samulski R. J., Srivastava A., Berns K. I., Muzyczka N. Rescue of adeno-associated virus from recombinant plasmids: gene correction within the terminal repeats of AAV. Cell. 1983 May;33(1):135–143. doi: 10.1016/0092-8674(83)90342-2. [DOI] [PubMed] [Google Scholar]
- Shull B. C., Chen K. C., Lederman M., Stout E. R., Bates R. C. Genomic clones of bovine parvovirus: construction and effect of deletions and terminal sequence inversions on infectivity. J Virol. 1988 Feb;62(2):417–426. doi: 10.1128/jvi.62.2.417-426.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siegl G., Bates R. C., Berns K. I., Carter B. J., Kelly D. C., Kurstak E., Tattersall P. Characteristics and taxonomy of Parvoviridae. Intervirology. 1985;23(2):61–73. doi: 10.1159/000149587. [DOI] [PubMed] [Google Scholar]
- Straus S. E., Sebring E. D., Rose J. A. Concatemers of alternating plus and minus strands are intermediates in adenovirus-associated virus DNA synthesis. Proc Natl Acad Sci U S A. 1976 Mar;73(3):742–746. doi: 10.1073/pnas.73.3.742. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tattersall P., Ward D. C. Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature. 1976 Sep 9;263(5573):106–109. doi: 10.1038/263106a0. [DOI] [PubMed] [Google Scholar]