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Analysis of the mechanism of DNA recombination using tangles

Published online by Cambridge University Press:  17 March 2009

De Witt Sumners ,
Claus Ernst ,
Sylvia J. Spengler  and
Nicholas R. Cozzarelli
De Witt Sumners
Affiliation:
Department of Mathematics, Florida State University, Tallahassee FLUSA Program in Mathematics and Molecular Biology, University of California, Berkeley CAUSA
Claus Ernst
Affiliation:
Department of Mathematics, Western Kentucky University, Bowling Green KYUSA
Sylvia J. Spengler
Affiliation:
Program in Mathematics and Molecular Biology, University of California, Berkeley CAUSA
Nicholas R. Cozzarelli
Affiliation:
Program in Mathematics and Molecular Biology, University of California, Berkeley CAUSA Department of Molecular and Cell Biology, University of California, Berkeley CAUSA
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Extract

The DNA of all organisms has a complex and essential topology. The three topological properties of naturally occurring DNA are supercoiling, catenation, and knotting. Although these properties are denned rigorously only for closed circular DNA, even linear DNA in vivo can have topological properties because it is divided into topologically separate subdomains (Drlica 1987; Roberge & Gasser, 1992). The essentiality of topological properties is demonstrated by the lethal consequence of interfering with topoisomerases, the enzymes that regulate the level of DNA supercoiling and that unlink DNA during its replication (reviewed in Wang, 1991; Bjornsti, 1991; Drlica, 1992; Ullsperger et al. 1995).

Type
Research Article
Information
Quarterly Reviews of Biophysics , Volume 28 , Issue 3 , August 1995 , pp. 253 - 313
Copyright
Copyright © Cambridge University Press 1995

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References

Abremski, K. & Hoess, R. (1985). Phage Pi Cre-loxP site-specific recombination. Effects of DNA supercoiling on catenation and knotting of recombinant products. J. molec. Biol. 184, 211–220.CrossRefGoogle Scholar
Abremski, K., Frommer, B. & Hoess, R. H. (1986). Linking-number changes in the DNA substrate during Cre-mediated loxP site-specific recombination. J. molec. Biol. 192, 17–26.CrossRefGoogle ScholarPubMed
Adams, D. E., Bliska, J. B. & Cozzarelli, N. R. (1992 a). Cre-lox recombination in Escherichia coli cells: mechanistic differences from the in vitro reaction. J. molec. Biol. 226, 661–673.CrossRefGoogle ScholarPubMed
Adams, D. E., Shekhtman, E. M., Zechiedrich, E. L., Schmid, M. B. & Cozzarelli, N. R. (1992 b). The role of topoisomerase IV in partitioning bacterial replicons and the structure of catenated intermediates in DNA replication. Cell 71, 277–288.CrossRefGoogle Scholar
Beatty, L. G., Babineau-Clary, D., Hogrefe, C. & Sadowski, P. D. (1986). FLP sitespecific recombinase of yeast 2-μm plasmid: topological features of the reaction. J. molec. Biol. 188, 529–544.CrossRefGoogle Scholar
Benjamin, H. W., Matzuk, M. M., Krasnow, M. A. & Cozzarelli, N. R. (1985). Recombination site selection by Tn3 resolvase: topological tests of a tracking mechanism. Cell 40, 147–158.CrossRefGoogle ScholarPubMed
Benjamin, H. W. & Cozzarelli, N. R. (1986). DNA-directed synapsis in recombination: slithering and random collision of sites. In Genetic Chemistry: The Molecular Basis of Heredity, pp. 107–126. Houston: Robert A. Welch Foundation.Google Scholar
Benjamin, H. W. & Cozzarelli, N. R. (1988). Isolation and characterization of the Tn3 resolvase synaptic intermediate. EMBO J. 7, 1897–1905.CrossRefGoogle ScholarPubMed
Benjamin, H. W. & Cozzarelli, N. R. (1990). Geometric arrangements of Tn3 resolvase sites. J. biol. Chem. 265, 6441–6447.CrossRefGoogle ScholarPubMed
Bjornsti, M.-A. (1991). DNA topoisomerases. Curr. Biol. 1, 99–103.Google Scholar
Bliska, J. B. & Cozzarelli, N. R. (1987). Use of site-specific recombination as a probe of DNA structure and metabolism in vivo, J. molec. Biol. 194, 205–218.CrossRefGoogle ScholarPubMed
Boles, T. C.White, J. H. & Cozzarelli, N. R. (1990). Structure of plectonemically supercoiled DNA. J. molec. Biol. 213, 931–951.CrossRefGoogle ScholarPubMed
Boocock, M. R., Brown, J. L. & Sherratt, D. J. (1987). Topological specificity in Tn3 resolvase catalysis. In DNA Replication and Recombination, UCLA Symposia on Molecular and Cellular Biology, New Series (ed. McMacken, R. and Kelly, T. J.), pp. 703–718. New York: Alan R. Liss, Inc.Google Scholar
Burde, G. & Zieschang, H. (1985). Knots. Berlin: de Gruyter.Google Scholar
Câlugâreanu, G. (1961). Sur les classes d'isotopie des noeuds tridimensionnels et leurs invariants. Czech math. J. 11, 588–625.Google Scholar
Conway, J. H. (1970). On enumerations of knots and links and some of their related properties. In Computational Problems in Abstract Algebra : Proc. Conf. Oxford 1967, pp. 329–358. Oxford: Pergamon.Google Scholar
Cozzarelli, N. R., Krasnow, M. A., Gerrard, S. P. & White, J. H. (1984). A topological treatment of recombination and topoisomerases. Cold Spring Harb. Symp. quant. Biol. 49, 383–400.CrossRefGoogle ScholarPubMed
Craig, N. (1988). The mechanism of conservative site-specific recombination. A. Rev. Genet. 22, 77–105.CrossRefGoogle ScholarPubMed
Craig, N. L. & Nash, H. W. (1983). The mechanism of phage lambda site-specific recombination: collision versus sliding in att site juxtaposition. In Mechanisms of DNA Replication and Recombination (ed. Cozzarelli, N.), pp. 617–636. New York: Alan R. Liss, Inc.Google Scholar
Crisona, N. J., Kanaar, R., Gonzalez, T. N., Zechiedrich, E. L., Klippel, A. & Cozzarelli, N. R. (1994). Processive recombination by wild-type Gin and an enhancer-independent mutant: insight into the mechanisms of recombination selectivity and strand exchange. J. molec. Biol. 243, 437–457.CrossRefGoogle Scholar
Dean, F. B., Stasiak, A., Koller, T. & Cozzarelli, N. R. (1985). Duplex DNA knots produced by Escherichia coli topoisomerase I: Structure and requirements for formation. J. biol. Chem. 260, 4975–4983.CrossRefGoogle ScholarPubMed
Drlica, K. (1987). The nucleoid. In Escherichia coli and Salmonella typhimurium, Cellular and Molecular Biology (ed. Neidhardt, F. C.), pp. 91–103. American Society for Microbiology, Washington DC.Google Scholar
Drlica, K. (1992). Control of bacterial DNA supercoiling. Molec. Microbiol. 6, 425–433.CrossRefGoogle ScholarPubMed
Dröge, P. & Cozzarelli, N. R. (1989). Recombination of knotted substrates by Tn3 resolvase. Proc. natn. Acad. Sci. U.S.A. 86, 6062–6066.CrossRefGoogle ScholarPubMed
Dröge, P. & Cozzarelli, N. R. (1992). Topological structure of DNA knots and catenanes. Meth. Enzym. 212, 120–130.CrossRefGoogle Scholar
Dungan, J. M. (1988). Topological mechanism of site specific recombination by Tn3 resolvase. Ph.D. thesis, University of California at Berkeley.Google Scholar
ERNST, C. (1995). Tangle equations. J. Knot Theory and its Ramifications. (In the Press.)Google Scholar
Ernst, C. & Sumners, D. W. (1987). The growth of the number of prime knots. Math. Proc. Camb. phil. Soc. 102, 303–315.CrossRefGoogle Scholar
Ernst, C. & Sumners, D. W. (1990). A calculus for rational tangles: applications to DNA recombination. Math. Proc. Camb. phil. Soc. 108, 489–515.CrossRefGoogle Scholar
Fuller, F. B. (1971). The writhing number of a space curve. Proc. natn. Acad. Sci. U.S.A. 68, 815–819.CrossRefGoogle ScholarPubMed
Gellert, M. & Nash, H. A. (1987). Communication between segments of DNA during site-specific recombination. Nature, Lond. 325, 401–404.CrossRefGoogle ScholarPubMed
Griffith, J. D. & Nash, H. A. (1985). Genetic rearrangement of DNA induces knots with a unique topology: Implications for the mechanism of synapsis and crossing over. Proc. natn. Acad. Sci. U.S.A. 82, 3124–3128.CrossRefGoogle ScholarPubMed
Hatfull, G. F. & Grindley, N. D. F. (1988). Resolvases and DNA-invertases: a family of enzymes active in site-specific recombination. In Genetic Recombination (ed. Kucherlapati, R. and Smith, G. R.), pp. 357–396. Washington, D.C.: American Society for Microbiology.Google Scholar
Heichman, K. A. & Johnson, R. C. (1990). The Hin invertasome: protein-mediated joining of distant recombination sites at the enhancer. Science, N.Y. 249, 511–517.CrossRefGoogle ScholarPubMed
Heichman, K. A., Moskowitz, I. P. G. & Johnson, R. C. (1991). Configuration of DNA strands and mechanism of strand exchange in the Hin invertasome as revealed by analysis of recombinant knots. Genes & Dev. 5, 1622–1634.CrossRefGoogle Scholar
Horowitz, D. S. & Wang, J. C. (1984). Torsional rigidity of DNA and length dependence of the free energy of DNA supercoiling. J. molec. Biol. 173, 75–91.CrossRefGoogle ScholarPubMed
Jenkins, J. (1989). Knotter. M.Sc. thesis, University of California at Berkeley.Google Scholar
Johnson, R. C. (1991). Mechanism of site-specific DNA inversion in bacteria. Curr. Op. in Genet. Dev. 1, 400–411.CrossRefGoogle ScholarPubMed
Kahmann, R., Mertens, G., Klippel, A., Brauer, B., Rudt, F. & Koch, C. (1987). The mechanism of G inversion. In DNA Replication and Recombination, UCLA Symposia on Molecular and Cellular Biology, New Series (ed. McMacken, R. and Kelly, T. J.), pp. 681–690. New York: Alan R. Liss, Inc.Google Scholar
Kanaar, R. & Cozzarelli, N. R. (1992). Roles of supercoiled DNA structure in DNA transactions. Curr. Opin. Struct. Biol. 2, 369–379.CrossRefGoogle Scholar
Kanaar, R., Van De Putte, P. & Cozzarelli, N. R. (1989). Gin-mediated recombination of catenated and knotted substrates: implications for the mechanism of interaction between cis-acting sites. Cell 58, 147–159.CrossRefGoogle ScholarPubMed
Kanaar, R., Klippel, A., Shekhtman, E., Dungan, J. M., Kahmann, R. & Cozzarelli, N. R. (1990). Processive recombination by the phage Mu Gin system: implications for the mechanisms of DNA strand exchange, DNA site alignment, and enhancer action. Cell 62, 353–366.CrossRefGoogle ScholarPubMed
Kanaar, R., Van De Putte, P. & Cozzarelli, N. R. (1988). Gin-mediated DNA inversion: product structure and the mechanism of strand exchange. Proc. natn. Acad. Sci. U.S.A. 85, 752–756.CrossRefGoogle ScholarPubMed
Kanaar, R. & Van De Putte, P. (1987). Topological aspects of site-specific DNAinversion. BioEssays 7, 195–200.CrossRefGoogle Scholar
Keller, W. (1975). Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc. natn. Acad. Sci. U.S.A. 72, 4876–4880.CrossRefGoogle ScholarPubMed
Klippel, A., Cloppenborg, K. & Kahmann, R. (1988). Isolation and characterization of unusual gin mutants. EMBO J. 7, 3983–3989.CrossRefGoogle Scholar
Klippel, A., Kanaar, R., Kahmann, R. & Cozzarelli, N. R. (1993). Analysis of strand exchange and DNA binding of enhancer-independent Gin recombinase mutants. EMBO J. 12, 1047–1057.CrossRefGoogle ScholarPubMed
Koch, C., Mertens, G., Rudt, F., Kahmann, R., Kanaar, R., Plasterk, R. H. A., Van De Putte, P., Sandulache, R. & Kamp, D. (1987). The invertible G segment. In Phage Mu (ed. Symonds, N.Toussaint, A.van de Putte, P., and Howe, M. M.), Cold Spring Harbor N. Y.: Cold Spring Harbor Laboratory.Google Scholar
Krasnow, M. A., Matzuk, M. M., Dungan, J. D., Benjamin, H. W. & Cozzarelli, N. R. (1983). Site-specific recombination by Tn3 resolvase: models for pairing of recombination sites. In Mechanisms of DNA Replication and Recombination, UCLA Symposia on Molecular and Cellular Biology, New Series (ed. Cozzarelli, N. R.), pp. 637–659. New York: Alan R. Liss, Inc.Google Scholar
Landy, A., Leong, J. M., Nunes-Duby, S. E., Oser, A. B., Lesser, C. F., Youderian, P. & Susskind, M. M. (1986). Structural and regulatory divergence among sitespecific recombination genes of lambdoid phage. J. molec. Biol. 189, 603–616.Google Scholar
Lilley, D. M. J. & Clegg, R. M. (1993). The structure of branched DNA species. Q. Rev. Biophys. 26, 131–175.CrossRefGoogle ScholarPubMed
Liu, L. F., Depew, R. E. & Wang, J. C. (1976). Knotted single-stranded DNA rings: a novel topological isomer of circular single-stranded DNA formed by treatment with Escherichia coli omega protein. J. molec. Biol. 106, 439–452.CrossRefGoogle Scholar
Liu, L. F., Liu, C.-C. & Alberts, B. M. (1980). Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19, 697–707.CrossRefGoogle Scholar
Mizuuchi, K., Gellert, M., Weisberg, R. A. & Nash, H. A. (1980). Catenation and supercoiling in the products of bacteriophage lambda integrative recombination in vitro. J. molec. Biol. 141, 485–494.CrossRefGoogle ScholarPubMed
Nash, H. A. (1990). Bending and supercoiling of DNA at the attachment site of bacteriophage λ. Trends Biochem. Sci. 15, 222–227.CrossRefGoogle ScholarPubMed
Nash, H. A. (1981). Integration and excision of bacteriophage λ: the mechanism of conservative site-specific recombination. A. Rev. Genet. 15, 143–167.CrossRefGoogle Scholar
Nash, H. A. & Pollock, T. J. (1983). Site-specific recombination of bacteriophage lambda. The change in topological linking number associated with exchange of DNA strands. J. molec. Biol. 170, 19–38.CrossRefGoogle Scholar
Ochiai, M. & Yamada, S. (1992). Knot Theory by Computer. This is a program on the Internet: the address there is http://archives.math.utk.edu/11/software/mac/topology.Google Scholar
Pohl, W. F. (1968). The self-linking number of a closed space curve. J. Math. Mech. 17, 975–986.Google Scholar
Reed, R. R. (1981). Transposon-mediated site-specific recombination: A defined in vitro system. Cell 25, 713–719.CrossRefGoogle ScholarPubMed
Roberge, M. & Gasser, S. (1992). DNA loops: structural and functional properties of scaffold-attached regions. Molec. Microbiol. 6, 419–423.CrossRefGoogle ScholarPubMed
Roca, J., Berger, J. M. & Wang, J. C. (1993). On the simultaneous binding of eukaryotic DNA topoisomerase II to a pair of double stranded DNA helices. J. biol. Chem. 268, 14250–14255.CrossRefGoogle ScholarPubMed
Rolfsen, D. (1990). Knots and Links. Berkeley, CA: Publish or Perish, Inc.Google Scholar
Sadowski, P. D. (1993). Site-specific genetic recombination: hops, flips, and flops. FASEB J. 7, 760–767.CrossRefGoogle ScholarPubMed
Sherratt, D., Dyson, P., Boocock, M., Brown, L., Sumners, D., Stewart, G. & Clary, P. (1984). Site-specific recombination in transposition and plasmid stability. Cold Spring Harb. Symp. quant. Biol. 49, 227–233.CrossRefGoogle ScholarPubMed
Spengler, S. J., Stasiak, A. & Cozzarelli, N. R. (1985). The stereostructure of knots and catenanes produced by phage λ integrative recombination: implications for mechanism and DNA structure. Cell 42, 325–334.CrossRefGoogle ScholarPubMed
Stark, W. M., Sherratt, D. J. & Boocock, M. R. (1989). Site-specific recombination by Tn3 resolvase: topological changes in the forward and reverse reactions. Cell 58, 779–790.CrossRefGoogle Scholar
Stark, W. M., Grindley, N. D. F., Hatfull, G. F. & Boocock, M. R. (1991). Resolvase-catalysed reactions between res sites differing in the central dinucleotide of subsite I. EMBO J. 10, 3541–3548.CrossRefGoogle ScholarPubMed
Stark, W. M., Boocock, M. R. & Sherratt, D. J. (1992). Catalysis by site-specific recombinases. Trends Genet. 8, 432–439.CrossRefGoogle ScholarPubMed
Sumners, D. W. (1990). Untangling DNA. Mathematical Intelligencer 12, 71–80.CrossRefGoogle Scholar
Sumners, D. W. (1992). Knot theory and DNA. In New Scientific Applications of Geometry and Topology (ed. Sumners, D. W.), pp. 39–72. Providence: American Mathematical Society.CrossRefGoogle Scholar
Sundin, O. & Varshavsky, A. (1980). Terminal stages of SV40 DNA replication proceed via multiply intertwined catenated dimers. Cell 21, 103–114.CrossRefGoogle ScholarPubMed
Ullsperger, C. J., Vologodskii, A. V. & Cozzarelli, N. R. (1995). Unlinking of DNA by topoisomerases during DNA replication. Nucl. Acids molec. Biol. (In the Press.)CrossRefGoogle Scholar
Van De Putte, P. & Goosen, N. (1992). DNA inversion in phage and bacteria. Trends Genet. 8, 457–462.CrossRefGoogle ScholarPubMed
Wang, J. C. (1991). DNA topoisomerases: Why so many? J. biol. Chem. 266, 6659–6662.CrossRefGoogle ScholarPubMed
Wasserman, S. A. & Cozzarelli, N. R. (1985). Determination of the stereostructure of the product of Tn3 resolvase by a general method. Proc. natn. Acad. Sci. U.S.A. 82, 1079–1083.CrossRefGoogle ScholarPubMed
Wasserman, S. A. & Cozzarelli, N. R. (1986). Biochemical topology: applications to DNA recombination and replication. Science, N. Y. 232, 951–960.CrossRefGoogle ScholarPubMed
Wasserman, S. A. & Cozzarelli, N. R. (1991). Supercoiled DNA-directed knotting by T4 topoisomerase. J. biol. Chem. 266, 20567–20573.CrossRefGoogle ScholarPubMed
Wasserman, S. A., Dungan, J. M. & Cozzarelli, N. R. (1985). Discovery of a predicted DNA knot substantiates a model for site-specific recombination. Science, N.Y. 229, 171–174.CrossRefGoogle Scholar
Welsh, D. J. A. (1991). On the number of knots and links. Coll. Math. Soc.Janos Bolyai 60, 713–718.Google Scholar
White, J. H. (1969). Self-linking and the Gauss integral in higher dimensions. Am. J. Math. 91, 693–728.CrossRefGoogle Scholar
White, J. H. (1989). An introduction to the geometry and topology of DNA structure. In Mathematical Methods for DNA Sequences (ed. Waterman, M. S.), pp. 225–253. Boca Raton U.S.A.: CRC Press.Google Scholar
White, J. H. & Cozzarelli, N. R. (1984). A simple topological method for describing stereoisomers of DNA catenanes and knots. Proc. natn. Acad. Sci. U.S.A. 81, 3322–3326.CrossRefGoogle ScholarPubMed
White, J. H., Millett, K. C. & Cozzarelli, N. R. (1987). Description of the topological entanglement of DNA catenanes and knots by a powerful method involving strand passage and recombination. J. molec. Biol. 197, 585–603.CrossRefGoogle ScholarPubMed
Zechiedrich, E. L. & Osheroff, N. (1990). Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 9, 4555–45O2.CrossRefGoogle ScholarPubMed