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. 1986 Aug;6(8):3005–3009. doi: 10.1128/mcb.6.8.3005

Nonhomologous recombination in the parvovirus chromosome: role for a CTATTTCT motif.

A Hogan, E A Faust
PMCID: PMC367873  PMID: 3023957

Abstract

The mechanism of nonhomologous recombination in murine cells infected with the parvovirus minute virus of mice (MVM) has been investigated by analysis of DNA sequences at recombination junctions in naturally occurring deletion variants of the virus. We report here that nonhomologous recombination in the MVM chromosome is characterized by short homologies, by insertion at recombination junctions of foreign DNA sequences that are enriched for preferred eucaryotic topoisomerase I cleavage sites, and by an association with a common DNA sequence motif of the type 5'-CTATTTCT-3'. Additional analyses of broken MVM chromosomes provided evidence for specific enzymatic cleavage within 5'-CTTATC-3' and 5'-CTATTC-3' sequences. The results indicate that the 5'-CTATTTCT-3' motif is an important genetic element for nonhomologous recombination in the parvovirus chromosome.

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Selected References

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  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. Babineau D., Vetter D., Andrews B. J., Gronostajski R. M., Proteau G. A., Beatty L. G., Sadowski P. D. The FLP protein of the 2-micron plasmid of yeast. Purification of the protein from Escherichia coli cells expressing the cloned FLP gene. J Biol Chem. 1985 Oct 5;260(22):12313–12319. [PubMed] [Google Scholar]
  6. Bernstein L. B., Mount S. M., Weiner A. M. Pseudogenes for human small nuclear RNA U3 appear to arise by integration of self-primed reverse transcripts of the RNA into new chromosomal sites. Cell. 1983 Feb;32(2):461–472. doi: 10.1016/0092-8674(83)90466-x. [DOI] [PubMed] [Google Scholar]
  7. Bullock P., Champoux J. J., Botchan M. Association of crossover points with topoisomerase I cleavage sites: a model for nonhomologous recombination. Science. 1985 Nov 22;230(4728):954–958. doi: 10.1126/science.2997924. [DOI] [PubMed] [Google Scholar]
  8. Bullock P., Forrester W., Botchan M. DNA sequence studies of simian virus 40 chromosomal excision and integration in rat cells. J Mol Biol. 1984 Mar 25;174(1):55–84. doi: 10.1016/0022-2836(84)90365-6. [DOI] [PubMed] [Google Scholar]
  9. Chow M., Bodnar J. W., Polvino-Bodnar M., Ward D. C. Identification and characterization of a protein covalently bound to DNA of minute virus of mice. J Virol. 1986 Mar;57(3):1094–1104. doi: 10.1128/jvi.57.3.1094-1104.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Craig N. L., Nash H. A. The mechanism of phage lambda site-specific recombination: site-specific breakage of DNA by Int topoisomerase. Cell. 1983 Dec;35(3 Pt 2):795–803. doi: 10.1016/0092-8674(83)90112-5. [DOI] [PubMed] [Google Scholar]
  11. Desiderio S. V., Yancopoulos G. D., Paskind M., Thomas E., Boss M. A., Landau N., Alt F. W., Baltimore D. Insertion of N regions into heavy-chain genes is correlated with expression of terminal deoxytransferase in B cells. Nature. 1984 Oct 25;311(5988):752–755. doi: 10.1038/311752a0. [DOI] [PubMed] [Google Scholar]
  12. Efstratiadis A., Posakony J. W., Maniatis T., Lawn R. M., O'Connell C., Spritz R. A., DeRiel J. K., Forget B. G., Weissman S. M., Slightom J. L. The structure and evolution of the human beta-globin gene family. Cell. 1980 Oct;21(3):653–668. doi: 10.1016/0092-8674(80)90429-8. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Faust E. A., Ward D. C. Incomplete genomes of the parvovirus minute virus of mice: selective conservation of genome termini, including the origin for DNA replication. J Virol. 1979 Oct;32(1):276–292. doi: 10.1128/jvi.32.1.276-292.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Gerondakis S., Cory S., Adams J. M. Translocation of the myc cellular oncogene to the immunoglobulin heavy chain locus in murine plasmacytomas is an imprecise reciprocal exchange. Cell. 1984 Apr;36(4):973–982. doi: 10.1016/0092-8674(84)90047-3. [DOI] [PubMed] [Google Scholar]
  16. Gronostajski R. M., Sadowski P. D. Determination of DNA sequences essential for FLP-mediated recombination by a novel method. J Biol Chem. 1985 Oct 5;260(22):12320–12327. [PubMed] [Google Scholar]
  17. Hogan A., Faust E. A. Short direct repeats mediate spontaneous high-frequency deletions in DNA of minute virus of mice. Mol Cell Biol. 1984 Oct;4(10):2239–2242. doi: 10.1128/mcb.4.10.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ikeda H., Shiozaki M. Nonhomologous recombination mediated by Escherichia coli DNA gyrase: possible involvement of DNA replication. Cold Spring Harb Symp Quant Biol. 1984;49:401–409. doi: 10.1101/sqb.1984.049.01.046. [DOI] [PubMed] [Google Scholar]
  19. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  20. Revie D., Tseng B. Y., Grafstrom R. H., Goulian M. Covalent association of protein with replicative form DNA of parvovirus H-1. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5539–5543. doi: 10.1073/pnas.76.11.5539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roth D. B., Porter T. N., Wilson J. H. Mechanisms of nonhomologous recombination in mammalian cells. Mol Cell Biol. 1985 Oct;5(10):2599–2607. doi: 10.1128/mcb.5.10.2599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Sanhueza S., Eisenberg S. Cleavage of single-stranded DNA by the varphiX174 A protein: The A-single-stranded DNA covalent linkage. Proc Natl Acad Sci U S A. 1984 Jul;81(14):4285–4289. doi: 10.1073/pnas.81.14.4285. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Senapathy P., Carter B. J. Molecular cloning of adeno-associated virus variant genomes and generation of infectious virus by recombination in mammalian cells. J Biol Chem. 1984 Apr 10;259(7):4661–4666. [PubMed] [Google Scholar]
  25. Senecoff J. F., Bruckner R. C., Cox M. M. The FLP recombinase of the yeast 2-micron plasmid: characterization of its recombination site. Proc Natl Acad Sci U S A. 1985 Nov;82(21):7270–7274. doi: 10.1073/pnas.82.21.7270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stark G. R., Wahl G. M. Gene amplification. Annu Rev Biochem. 1984;53:447–491. doi: 10.1146/annurev.bi.53.070184.002311. [DOI] [PubMed] [Google Scholar]
  27. Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. Frameshift mutations and the genetic code. This paper is dedicated to Professor Theodosius Dobzhansky on the occasion of his 66th birthday. Cold Spring Harb Symp Quant Biol. 1966;31:77–84. doi: 10.1101/sqb.1966.031.01.014. [DOI] [PubMed] [Google Scholar]

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