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. 1998 Jun;74(6):2815–2822. doi: 10.1016/S0006-3495(98)77988-3

Geometry and physics of catenanes applied to the study of DNA replication.

B Laurie 1, V Katritch 1, J Sogo 1, T Koller 1, J Dubochet 1, A Stasiak 1
PMCID: PMC1299622  PMID: 9635735

Abstract

The concept of ideal geometric configurations was recently applied to the classification and characterization of various knots. Different knots in their ideal form (i.e., the one requiring the shortest length of a constant-diameter tube to form a given knot) were shown to have an overall compactness proportional to the time-averaged compactness of thermally agitated knotted polymers forming corresponding knots. This was useful for predicting the relative speed of electrophoretic migration of different DNA knots. Here we characterize the ideal geometric configurations of catenanes (called links by mathematicians), i.e., closed curves in space that are topologically linked to each other. We demonstrate that the ideal configurations of different catenanes show interrelations very similar to those observed in the ideal configurations of knots. By analyzing literature data on electrophoretic separations of the torus-type of DNA catenanes with increasing complexity, we observed that their electrophoretic migration is roughly proportional to the overall compactness of ideal representations of the corresponding catenanes. This correlation does not apply, however, to electrophoretic migration of certain replication intermediates, believed up to now to represent the simplest torus-type catenanes. We propose, therefore, that freshly replicated circular DNA molecules, in addition to forming regular catenanes, may also form hemicatenanes.

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Selected References

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

  1. Adams D. E., Shekhtman E. M., Zechiedrich E. L., Schmid M. B., Cozzarelli N. R. The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell. 1992 Oct 16;71(2):277–288. doi: 10.1016/0092-8674(92)90356-h. [DOI] [PubMed] [Google Scholar]
  2. Bianchi M., DasGupta C., Radding C. M. Synapsis and the formation of paranemic joints by E. coli RecA protein. Cell. 1983 Oct;34(3):931–939. doi: 10.1016/0092-8674(83)90550-0. [DOI] [PubMed] [Google Scholar]
  3. Colloms S. D., Bath J., Sherratt D. J. Topological selectivity in Xer site-specific recombination. Cell. 1997 Mar 21;88(6):855–864. doi: 10.1016/s0092-8674(00)81931-5. [DOI] [PubMed] [Google Scholar]
  4. Crisona N. J., Kanaar R., Gonzalez T. N., Zechiedrich E. L., Klippel A., Cozzarelli N. R. Processive recombination by wild-type gin and an enhancer-independent mutant. Insight into the mechanisms of recombination selectivity and strand exchange. J Mol Biol. 1994 Oct 28;243(3):437–457. doi: 10.1006/jmbi.1994.1671. [DOI] [PubMed] [Google Scholar]
  5. Cunningham R. P., Wu A. M., Shibata T., DasGupta C., Radding C. M. Homologous pairing and topological linkage of DNA molecules by combined action of E. coli RecA protein and topoisomerase I. Cell. 1981 Apr;24(1):213–223. doi: 10.1016/0092-8674(81)90517-1. [DOI] [PubMed] [Google Scholar]
  6. Dean F. B., Stasiak A., Koller T., Cozzarelli N. R. Duplex DNA knots produced by Escherichia coli topoisomerase I. Structure and requirements for formation. J Biol Chem. 1985 Apr 25;260(8):4975–4983. [PubMed] [Google Scholar]
  7. Dressler D., Potter H. Molecular mechanisms in genetic recombination. Annu Rev Biochem. 1982;51:727–761. doi: 10.1146/annurev.bi.51.070182.003455. [DOI] [PubMed] [Google Scholar]
  8. Griffith J. D., Nash H. A. Genetic rearrangement of DNA induces knots with a unique topology: implications for the mechanism of synapsis and crossing-over. Proc Natl Acad Sci U S A. 1985 May;82(10):3124–3128. doi: 10.1073/pnas.82.10.3124. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kanaar R., Klippel A., Shekhtman E., Dungan J. M., Kahmann R., Cozzarelli N. R. Processive recombination by the phage Mu Gin system: implications for the mechanisms of DNA strand exchange, DNA site alignment, and enhancer action. Cell. 1990 Jul 27;62(2):353–366. doi: 10.1016/0092-8674(90)90372-l. [DOI] [PubMed] [Google Scholar]
  10. Krasnow M. A., Cozzarelli N. R. Site-specific relaxation and recombination by the Tn3 resolvase: recognition of the DNA path between oriented res sites. Cell. 1983 Apr;32(4):1313–1324. doi: 10.1016/0092-8674(83)90312-4. [DOI] [PubMed] [Google Scholar]
  11. Krasnow M. A., Stasiak A., Spengler S. J., Dean F., Koller T., Cozzarelli N. R. Determination of the absolute handedness of knots and catenanes of DNA. Nature. 1983 Aug 11;304(5926):559–560. doi: 10.1038/304559a0. [DOI] [PubMed] [Google Scholar]
  12. Sogo J. M., Stahl H., Koller T., Knippers R. Structure of replicating simian virus 40 minichromosomes. The replication fork, core histone segregation and terminal structures. J Mol Biol. 1986 May 5;189(1):189–204. doi: 10.1016/0022-2836(86)90390-6. [DOI] [PubMed] [Google Scholar]
  13. Spengler S. J., Stasiak A., Cozzarelli N. R. The stereostructure of knots and catenanes produced by phage lambda integrative recombination: implications for mechanism and DNA structure. Cell. 1985 Aug;42(1):325–334. doi: 10.1016/s0092-8674(85)80128-8. [DOI] [PubMed] [Google Scholar]
  14. Stasiak A., Katritch V., Bednar J., Michoud D., Dubochet J. Electrophoretic mobility of DNA knots. Nature. 1996 Nov 14;384(6605):122–122. doi: 10.1038/384122a0. [DOI] [PubMed] [Google Scholar]
  15. Sundin O., Varshavsky A. Arrest of segregation leads to accumulation of highly intertwined catenated dimers: dissection of the final stages of SV40 DNA replication. Cell. 1981 Sep;25(3):659–669. doi: 10.1016/0092-8674(81)90173-2. [DOI] [PubMed] [Google Scholar]
  16. Sundin O., Varshavsky A. Terminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers. Cell. 1980 Aug;21(1):103–114. doi: 10.1016/0092-8674(80)90118-x. [DOI] [PubMed] [Google Scholar]
  17. Vologodskii A. V., Crisona N. J., Laurie B., Pieranski P., Katritch V., Dubochet J., Stasiak A. Sedimentation and electrophoretic migration of DNA knots and catenanes. J Mol Biol. 1998 Apr 24;278(1):1–3. doi: 10.1006/jmbi.1998.1696. [DOI] [PubMed] [Google Scholar]
  18. Wasserman S. A., White J. H., Cozzarelli N. R. The helical repeat of double-stranded DNA varies as a function of catenation and supercoiling. Nature. 1988 Aug 4;334(6181):448–450. doi: 10.1038/334448a0. [DOI] [PubMed] [Google Scholar]
  19. West S. C., Countryman J. K., Howard-Flanders P. Enzymatic formation of biparental figure-eight molecules from plasmid DNA and their resolution in E. coli. Cell. 1983 Mar;32(3):817–829. doi: 10.1016/0092-8674(83)90068-5. [DOI] [PubMed] [Google Scholar]
  20. Zerbib D., Colloms S. D., Sherratt D. J., West S. C. Effect of DNA topology on Holliday junction resolution by Escherichia coli RuvC and bacteriophage T7 endonuclease I. J Mol Biol. 1997 Aug 1;270(5):663–673. doi: 10.1006/jmbi.1997.1157. [DOI] [PubMed] [Google Scholar]

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