1887

Abstract

We have characterized the temporal appearance and accumulation of minute virus of mice (MVM) replicative forms (RF) in highly synchronized single rounds of infection using a combination of restriction endonuclease analysis and two-dimensional agarose gel electrophoresis. Between 4 and 12 h after release of infected cells into the S-phase, both monomer (mRF) and dimer RF (dRF) increased exponentially at similar rates such that the ratio of mRF relative to dRF remained unchanged. These DNA forms accumulated at a faster rate than MVM RNAs, suggesting that the number of DNA templates available for replication is limiting, not the expression of MVM gene products, and that the majority of DNA templates are likely to be destined for DNA amplification rather than transcription and further gene expression. During this exponential DNA amplification phase, approximately 65 % of mRF were in a fully extended form, whereas most of the remaining mRF were covalently closed in the left end and extended in the right end. Although MVM replication presumably generates right-hand turn-around mRF, only a low level of this form persists (5 to 10 % of total mRF) at all times examined, suggesting that this form must be quickly converted to the extended form. Greater than 90% of dRF, which have right-hand palindromes on both ends of the molecule, were extended on both ends. A significant proportion of dRF and higher concatemers are nicked in the left-hand palindrome, suggesting that resolution of dRF into two mRFs may occur via single-stranded nicks rather than a double-stranded cut. An additional replicative form, previously termed band X, has been identified as an RNA-DNA duplex. This band is formed predominantly intracellularly, before cell lysis but its biological significance remains unclear. Our results provide direct experimental support for many of the predictions of the current models of parvovirus replication and suggest that the kinetic hairpin transfer model should be adjusted to include a strand-transfer or similar mechanism for the resolution of dRF to account adequately for the production of left-end turn-around forms.

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1994-07-01
2024-04-23
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References

  1. Astell C. R., Thomson M., Chow M. D., Ward D. C. 1983; Structure and replication of minute virus of mice DNA. Cold Spring Harbor Symposia on Quantitative Biology 47:751–762
    [Google Scholar]
  2. Astell C. R., Chow M. D., Ward D. C. 1985; 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. Journal of Virology 54:171–177
    [Google Scholar]
  3. Bates R. C., Snyder C. E., Banerjee P. T., Mitra S. 1984; Autonomous parvovirus LuIIIencapsidates equal amounts of plus and minus DNA strands. Journal of Virology 49:319–324
    [Google Scholar]
  4. Cavalier-Smith T. 1974; Palindromic base sequences and replication of eukaryotic chromosome ends. Nature; London: 250467–470
    [Google Scholar]
  5. Chen K. C., Tyson J. J., Lederman M., Stout E. R., Bates R. C. 1989; A kinetic hairpin transfer model for parvoviral DNA replication. Journal of Molecular Biology 208:283–296
    [Google Scholar]
  6. Clemens K. E., Pintel D. J. 1988; The two transcription units of the autonomous parvovirus minute virus of mice are transcribed in a temporal order. Journal of Virology 62:1448–1451
    [Google Scholar]
  7. Cotmore S. F., Tattersall P. 1987; The autonomously replicating parvoviruses of vertebrates. Advances in Virus Research 33:91–174
    [Google Scholar]
  8. Cotmore S. F., Tattersall P. 1988; 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. Journal of Virology 62:851–860
    [Google Scholar]
  9. Cotmore S. F., Tattersall P. 1989; A genome-linked copy of the NS-1 polypeptide is located on the outside of infectious parvovirus particles. Journal of Virology 63:3902–3911
    [Google Scholar]
  10. Cotmore S. F., Tattersall P. 1992; In vivo resolution of circular plasmids containing concatemer junction fragments from minute virus of mice DNA and their subsequent replication as linear molecules. Journal of Virology 66:420–431
    [Google Scholar]
  11. Cotmore S. F., Gunther M., Tattersall P. 1989; Evidence for a ligation step in the DNA replication of the autonomous parvovirus minute virus of mice. Journal of Virology 63:1002–1006
    [Google Scholar]
  12. Cotmore S. F., Nuesch J. P. F., Tattersall P. 1992; In vitro excision and replication of 5′ telomeres of minute virus of mice DNA from cloned palindromic concatemer junctions. Virology 190:365–377
    [Google Scholar]
  13. Cotmore S. F., Nüesch J. P. F., Tattersall P. 1993; Asymmetric resolution of a parvovirus palindrome in vitro. Journal of Virology 67:1579–1589
    [Google Scholar]
  14. Doerig C., Mcmaster G., Sogo J., Bruggmann H., Beard P. 1986; Nucleoprotein complexes of MVM have a distinct structure different from that of chromatin. Journal of Virology 58:817–824
    [Google Scholar]
  15. Eisenberg S., Griffith J., Kornberg A. 1977; PhiX174 cistronA protein is a multifunctional enzyme in DNA replication. Proceedings of the National Academy of Sciences, U.S.A 74:3198–3202
    [Google Scholar]
  16. Faust E. A., Gloor G. 1984; Characterization of a metastable, partially replicated dimeric intermediate of minute virus of mice. Journal of Virology 49:621–625
    [Google Scholar]
  17. Faust E. A., Brudzynska K., Morgan J. 1989; Characterization of novel populations of MVM virions containing covalent DNA- protein complexes. Virology 168:128–137
    [Google Scholar]
  18. Feinberg A. P., Vogelstein B. 1983; A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Analytical Biochemistry 132:6–13
    [Google Scholar]
  19. Hirt B. 1967; Selective extraction of polyoma DNA from infected mouse cell cultures. Journal of Molecular Biology 26:365–369
    [Google Scholar]
  20. Lusby E., Bohenzky R., Berns K. I. 1981; Inverted terminal repetitions in adeno-associated virus DNA: independence of the orientation at either end of the genome. Journal of Virology 37:1083–1086
    [Google Scholar]
  21. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: A Laboratory Manual New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  22. Merchlinsky M. J. 1984 Studies on MVM DNA replication using an infectious molecular clone Ph.D. thesis Yale University:
    [Google Scholar]
  23. Muller D.-E., Siegl G. 1983; Maturation of parvovirus LuIII in a subcellular system. I. Optimal conditions for in vitro synthesis and encapsidation of viral DNA. Journal of General Virology 64:1043–1054
    [Google Scholar]
  24. Ogden R. C., Adams D. A. 1987; Electrophoresis in agarose and acrylamide gels. Methods in Enzymology 152:61–87
    [Google Scholar]
  25. Reinberg D., Zipursky S. L., Weisbeck P., Brown D., Hurwitz J. 1983; Studies on the phiX174 gene A protein-mediated termination of leading strand DNA synthesis. Journal of Biological Chemistry 258:529–537
    [Google Scholar]
  26. Schoborg R. V., Pintel D. J. 1991; Accumulation of MVM gene products is differentially regulated by transcription initiation, RNA processing and protein stability. Virology 181:22–34
    [Google Scholar]
  27. Straus S. E., Sebring E. D., Rose J. A. 1976; Concatemers of alternating plus and minus strands are intermediates in adeno- associated virus DNA synthesis. Proceedings of the National Academy of Sciences, U.S.A 73:742–746
    [Google Scholar]
  28. Tattersall P., Bratton J. 1983; Reciprocal productive and restrictive virus-cell interactions of immunosuppressive and prototype strains of minute virus of mice. Journal of Virology 46:944–955
    [Google Scholar]
  29. Tattersall P., Ward D. C. 1976; Rolling hairpin model for replication of parvovirus and linear chromosomal DNA. Nature; London: 263106
    [Google Scholar]
  30. Tullis G. E., Labeniec-Pintel L., Clemens K. E., Pintel D. 1988; Generation and characterization of a temperature sensitive mutation in the NS-1 gene of the autonomous parvovirus minute virus of mice. Journal of Virology 62:2736–2744
    [Google Scholar]
  31. Tullis G. E., Burger L. R., Pintel D. J. 1992; The trypsin- sensitive RVER domain in the capsid proteins of minute virus of mice is required for efficient cell binding and viral infection but not for proteolytic processing in vivo. Virology 191:846–857
    [Google Scholar]
  32. Tullis G. E., Burger L. R., Pintel D. J. 1993; The minor capsid protein VP1 of the autonomous parvovirus minute virus of mice is dispensable for encapsidation of progeny single-stranded DNA but is required for infectivity. Journal of Virology 67:131–141
    [Google Scholar]
  33. Tyson J. J., Chen K. C., Lederman M., Bates R. C. 1990; Analysis of the kinetic hairpin transfer model for parvoviral DNA replication. Journal of Theoretical Biology 144:155–169
    [Google Scholar]
  34. Ward D. C., Dadachanji D. K. 1978; Replication of minute virus of mice DNA. In Replication of Mammalian Parvoviruses pp. 297–313 Ward D. C., Tattersall P. J. Edited by New York: Cold Spring Harbor Laboratory;
    [Google Scholar]
  35. Willwand K., Kaaden O. R. 1990; Proteins of viral and cellular origin bind to the Aleutian disease virus (ADV) DNA 3′-terminal hairpin: presentation of a scheme for encapsidation of ADV DNA. Journal of Virology 64:1598–1605
    [Google Scholar]
  36. Willwand K., Hirt B. 1991; The minute virus of mice capsid specifically recognizes the 3′ hairpin structure of the viral replicative- form DNA: mapping of the binding site by hydroxyl radical footprinting. Journal of Virology 65:4629–4635
    [Google Scholar]
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