Skip to main content
NCBI home page
Journal of Virology logoLink to Journal of Virology
. 1993 Mar;67(3):1579–1589. doi: 10.1128/jvi.67.3.1579-1589.1993

Asymmetric resolution of a parvovirus palindrome in vitro.

S F Cotmore 1, J P Nüesch 1, P Tattersall 1
PMCID: PMC237529  PMID: 8437230

Abstract

Cell extracts from murine A9 or human HeLa cells containing wild-type copies the NS1 polypeptide of minute virus of mice (MVM), produced from a recombinant vaccinia virus, can support the resolution of viral 3' termini from palindromic junction fragments of dimeric, replicative-form MVM DNA. Resolution resulted in the generation of two new viral termini, one associated with each arm of the junction palindrome. Telomeres were created in two configurations, "extended" forms, which were covalently associated with NS1 molecules, and smaller "turn-around" forms in which a single arm of the palindrome terminated at the axis of dyad symmetry in a covalent bond which cross-linked the two strands. The in vitro resolution reaction was asymmetric, generating predominantly extended-form termini from one arm of the palindrome but predominantly turn-around forms from the other. This asymmetry was independent of the type of cell used to prepare the in vitro extract or the orientation of the palindrome in the plasmid and was obtained for all cloned junction sequences of 156 bp or more. Two modified forms of the duplex junction fragment, which appeared to be intermediates in the resolution process since they were nicked, covalently linked to NS1, and associated with newly synthesized DNA, were identified. The structures of these intermediates suggest that resolution is initiated by preferential nicking at one of the two candidate resolution sites. The asymmetric nature of this resolution reaction is discussed in terms of current models of MVM DNA replication.

Full text

PDF
1579

Images in this article

1582Image
on p.1582
1582Image
on p.1582
1584Image
on p.1584
1585Image
on p.1585
1585Image
on p.1585
1587Image
on p.1587

Selected References

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

  1. 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]
  2. 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]
  3. Astell C. R., Thomson M., Chow M. B., Ward D. C. Structure and replication of minute virus of mice DNA. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):751–762. doi: 10.1101/sqb.1983.047.01.086. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Ben-Asher E., Aloni Y. Transcription of minute virus of mice, an autonomous parvovirus, may be regulated by attenuation. J Virol. 1984 Oct;52(1):266–276. doi: 10.1128/jvi.52.1.266-276.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Berns K. I., Hauswirth W. W. Adeno-associated viruses. Adv Virus Res. 1979;25:407–449. doi: 10.1016/s0065-3527(08)60574-6. [DOI] [PubMed] [Google Scholar]
  7. Bohenzky R. A., LeFebvre R. B., Berns K. I. Sequence and symmetry requirements within the internal palindromic sequences of the adeno-associated virus terminal repeat. Virology. 1988 Oct;166(2):316–327. doi: 10.1016/0042-6822(88)90502-8. [DOI] [PubMed] [Google Scholar]
  8. 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]
  9. Cotmore S. F., Gunther M., Tattersall P. Evidence for a ligation step in the DNA replication of the autonomous parvovirus minute virus of mice. J Virol. 1989 Feb;63(2):1002–1006. doi: 10.1128/jvi.63.2.1002-1006.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Cotmore S. F., Nuesch J. P., Tattersall P. In vitro excision and replication of 5' telomeres of minute virus of mice DNA from cloned palindromic concatemer junctions. Virology. 1992 Sep;190(1):365–377. doi: 10.1016/0042-6822(92)91223-h. [DOI] [PubMed] [Google Scholar]
  11. Cotmore S. F., Tattersall P. A genome-linked copy of the NS-1 polypeptide is located on the outside of infectious parvovirus particles. J Virol. 1989 Sep;63(9):3902–3911. doi: 10.1128/jvi.63.9.3902-3911.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Cotmore S. F., Tattersall P. In vivo resolution of circular plasmids containing concatemer junction fragments from minute virus of mice DNA and their subsequent replication as linear molecules. J Virol. 1992 Jan;66(1):420–431. doi: 10.1128/jvi.66.1.420-431.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Cotmore S. F., Tattersall P. The NS-1 polypeptide of minute virus of mice is covalently attached to the 5' termini of duplex replicative-form DNA and progeny single strands. J Virol. 1988 Mar;62(3):851–860. doi: 10.1128/jvi.62.3.851-860.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Diffoot N., Shull B. C., Chen K. C., Stout E. R., Lederman M., Bates R. C. Identical ends are not required for the equal encapsidation of plus- and minus-strand parvovirus LuIII DNA. J Virol. 1989 Jul;63(7):3180–3184. doi: 10.1128/jvi.63.7.3180-3184.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Eisenberg S., Kornberg A. Purification and characterization of phiX174 gene A protein. A multifunctional enzyme of duplex DNA replication. J Biol Chem. 1979 Jun 25;254(12):5328–5332. [PubMed] [Google Scholar]
  17. Fuerst T. R., Niles E. G., Studier F. W., Moss B. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A. 1986 Nov;83(21):8122–8126. doi: 10.1073/pnas.83.21.8122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Gardiner E. M., Tattersall P. Evidence that developmentally regulated control of gene expression by a parvoviral allotropic determinant is particle mediated. J Virol. 1988 May;62(5):1713–1722. doi: 10.1128/jvi.62.5.1713-1722.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Im D. S., Muzyczka N. Factors that bind to adeno-associated virus terminal repeats. J Virol. 1989 Jul;63(7):3095–3104. doi: 10.1128/jvi.63.7.3095-3104.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Im D. S., Muzyczka N. Partial purification of adeno-associated virus Rep78, Rep52, and Rep40 and their biochemical characterization. J Virol. 1992 Feb;66(2):1119–1128. doi: 10.1128/jvi.66.2.1119-1128.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Im D. S., Muzyczka N. The AAV origin binding protein Rep68 is an ATP-dependent site-specific endonuclease with DNA helicase activity. Cell. 1990 May 4;61(3):447–457. doi: 10.1016/0092-8674(90)90526-k. [DOI] [PubMed] [Google Scholar]
  22. Lefebvre R. B., Riva S., Berns K. I. Conformation takes precedence over sequence in adeno-associated virus DNA replication. Mol Cell Biol. 1984 Jul;4(7):1416–1419. doi: 10.1128/mcb.4.7.1416. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lusby E. W., Berns K. I. Mapping of the 5' termini of two adeno-associated virus 2 RNAs in the left half of the genome. J Virol. 1982 Feb;41(2):518–526. doi: 10.1128/jvi.41.2.518-526.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. 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]
  25. Nüesch J. P., Cotmore S. F., Tattersall P. Expression of functional parvoviral NS1 from recombinant vaccinia virus: effects of mutations in the nucleotide-binding motif. Virology. 1992 Nov;191(1):406–416. doi: 10.1016/0042-6822(92)90202-z. [DOI] [PubMed] [Google Scholar]
  26. Owens R. A., Carter B. J. In vitro resolution of adeno-associated virus DNA hairpin termini by wild-type Rep protein is inhibited by a dominant-negative mutant of rep. J Virol. 1992 Feb;66(2):1236–1240. doi: 10.1128/jvi.66.2.1236-1240.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Owens R. A., Trempe J. P., Chejanovsky N., Carter B. J. Adeno-associated virus rep proteins produced in insect and mammalian expression systems: wild-type and dominant-negative mutant proteins bind to the viral replication origin. Virology. 1991 Sep;184(1):14–22. doi: 10.1016/0042-6822(91)90817-u. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Snyder R. O., Samulski R. J., Muzyczka N. In vitro resolution of covalently joined AAV chromosome ends. Cell. 1990 Jan 12;60(1):105–113. doi: 10.1016/0092-8674(90)90720-y. [DOI] [PubMed] [Google Scholar]
  30. Stillman B. W., Gluzman Y. Replication and supercoiling of simian virus 40 DNA in cell extracts from human cells. Mol Cell Biol. 1985 Aug;5(8):2051–2060. doi: 10.1128/mcb.5.8.2051. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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]
  32. 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]

Articles from Journal of Virology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES