Cellular roles of DNA topoisomerases: a molecular perspective (original) (raw)

• Wang, J. C. DNA topoisomerases. Annu. Rev. Biochem. 65, 635–692 (1996).
  Article CAS PubMed Google Scholar
• Nitiss, J. L. Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta 1400, 63–81 (1998).A comprehensive review of the cellular functions of eukaryotic DNA topoisomerases.
  Article CAS PubMed Google Scholar
• Champoux, J. J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369–413 (2001).
  Article CAS PubMed Google Scholar
• Wang, J. C. Interaction between DNA and an Escherichia coli protein ω. J. Mol. Biol. 55, 523–533 (1971).This reports the discovery of the first DNA topoisomerase, and proposes the transesterification mechanism of DNA strand breakage and rejoining.
  Article CAS PubMed Google Scholar
• Kirkegaard, K. & Wang, J. C. Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J. Mol. Biol. 185, 625–637 (1985).
  Article CAS PubMed Google Scholar
• Tse, Y. & Wang, J. C. E. coli and M. luteus DNA topoisomerase I can catalyze catenation or decatenation of double-stranded DNA rings. Cell 22, 269–276 (1980).
  Article CAS PubMed Google Scholar
• Lima, C. D., Wang, J. C. & Mondragon, A. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138–146 (1994).
  Article CAS PubMed Google Scholar
• Brown, P. O. & Cozzarelli, N. R. Catenation and knotting of duplex DNA by type 1 topoisomerases: a mechanistic parallel with type 2 topoisomerases. Proc. Natl Acad. Sci. USA 78, 843–847 (1981).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, J. C. Moving one DNA double helix through another by a type II DNA topoisomerase: the story of a simple molecular machine. Q. Rev. Biophys. 31, 107–144 (1998).
  Article CAS PubMed Google Scholar
• Bergerat, A. et al. An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386, 414–417 (1997).A report on the discovery of the type IIB topoisomerase.
  Article CAS PubMed Google Scholar
• Forterre, P. Genomics and early cellular evolution. The origin of the DNA world. C. R. Acad. Sci. III 324, 1067–1076 (2001).
  Article CAS PubMed Google Scholar
• Berger, J. M., Gamblin, S. J., Harrison, S. C. & Wang, J. C. Structure and mechanism of DNA topoisomerase II. Nature 379, 225–232 (1996).
  Article CAS PubMed Google Scholar
• Nichols, M. D., DeAngelis, K., Keck, J. L. & Berger, J. M. Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J. 18, 6177–6188 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Kampranis, S. C., Bates, A. D. & Maxwell, A. A model for the mechanism of strand passage by DNA gyrase. Proc. Natl Acad. Sci. USA 96, 8414–8419 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Cook, P. R. The organization of replication and transcription. Science 284, 1790–1795 (1999).
  Article CAS PubMed Google Scholar
• Postow, L., Crisona, N. J., Peter, B. J., Hardy, C. D. & Cozzarelli, N. R. Topological challenges to DNA replication: conformations at the fork. Proc. Natl Acad. Sci. USA 98, 8219–8226 (2001).A detailed review of the topological problems of DNA chain elongation during replication, and their plausible solutions by the DNA topoisomerases, especially the type II enzymes. Much of the discussions, however, deal with cases in which rotation of the replication machinery is unconstrained.
  Article CAS PubMed PubMed Central Google Scholar
• Harmon, F. G., DiGate, R. J. & Kowalczykowski, S. C. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol. Cell 3, 611–620 (1999).
  Article CAS PubMed Google Scholar
• Kim, R. A. & Wang, J. C. Function of DNA topoisomerases as replication swivels in Saccharomyces cerevisiae. J. Mol. Biol. 208, 257–267 (1989).
  Article CAS PubMed Google Scholar
• Zhang, C. X., Chen, A. D., Gettel, N. J. & Hsieh, T. S. Essential functions of DNA topoisomerase I in Drosophila melanogaster. Dev. Biol. 222, 27–40 (2000).An elegant study of the cellular roles of DNA topoisomerase I through its controlled expression from a heat-shock-gene promoter.
  Article CAS PubMed Google Scholar
• Hiasa, H. & Marians, K. J. Topoisomerase III, but not topoisomerase I, can support nascent chain elongation during θ-type DNA replication. J. Biol. Chem. 269, 32655–32659 (1994).
  CAS PubMed Google Scholar
• Redinbo, M. R., Stewart, L., Kuhn, P., Champoux, J. J. & Hol, W. G. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504–1513 (1998).
  Article CAS PubMed Google Scholar
• 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 25, 659–669 (1981).The first demonstration of the formation of multiple intertwined pairs of newly replicated DNA rings in the absence of activities that can resolve them.
  Article CAS PubMed Google Scholar
• Hiasa, H., DiGate, R. J. & Marians, K. J. Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J. Biol. Chem. 269, 2093–2099 (1994).
  CAS PubMed Google Scholar
• Spell, R. M. & Holm, C. Nature and distribution of chromosomal intertwinings in Saccharomyces cerevisiae. Mol. Cell. Biol. 14, 1465–1476 (1994).This report shows clearly that chromosome loss and/or breakage in the absence of a type II DNA topoisomerase is particularly severe for larger chromosomes.
  Article CAS PubMed PubMed Central Google Scholar
• Crooke, E., Hwang, D. S., Skarstad, K., Thony, B. & Kornberg, A. E. coli minichromosome replication: regulation of initiation at oriC. Res. Microbiol. 142, 127–130 (1991).
  Article CAS PubMed Google Scholar
• Liu, L. F. & Wang, J. C. Supercoiling of the DNA template during transcription. Proc. Natl Acad. Sci. USA 84, 7024–7027 (1987).This proposes a 'twin-supercoiled-domain' model when rotation of a transcription assembly in the cellular milieu is hindered, and discusses how various DNA topoisomerases might act to remove the positive and negative supercoils that are generated in the DNA template.
  Article CAS PubMed PubMed Central Google Scholar
• Norris, V. Hypothesis: chromosome separation in Escherichia coli involves autocatalytic gene expression, transertion and membrane-domain formation. Mol. Microbiol. 16, 1051–1057 (1995).
  Article CAS PubMed Google Scholar
• Lodge, J. K., Kazic, T. & Berg, D. E. Formation of supercoiling domains in plasmid pBR322. J. Bacteriol. 171, 2181–2187 (1989).
  Article CAS PubMed PubMed Central Google Scholar
• Cook, D. N., Ma, D., Pon, N. G. & Hearst, J. E. Dynamics of DNA supercoiling by transcription in Escherichia coli. Proc. Natl Acad. Sci. USA 89, 10603–10607 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Lynch, A. S. & Wang, J. C. Anchoring of DNA to the bacterial cytoplasmic membrane through cotranscriptional synthesis of polypeptides encoding membrane proteins or proteins for export: a mechanism of plasmid hypernegative supercoiling in mutants deficient in DNA topoisomerase I. J. Bacteriol. 175, 1645–1655 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Drolet, M. et al. Overexpression of RNase H partially complements the growth defect of an Escherichia coli ΔtopA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc. Natl Acad. Sci. USA 92, 3526–3530 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Pruss, G. J., Manes, S. H. & Drlica, K. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31, 35–42 (1982).
  Article CAS PubMed Google Scholar
• DiNardo, S., Voelkel, K. A., Sternglanz, R., Reynolds, A. E. & Wright, A. Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31, 43–51 (1982).
  Article CAS PubMed Google Scholar
• Richardson, S. M., Higgins, C. F. & Lilley, D. M. The genetic control of DNA supercoiling in Salmonella typhimurium. EMBO J. 3, 1745–1752 (1984).
  Article CAS PubMed PubMed Central Google Scholar
• Bhriain, N. N. & Dorman, C. J. Isolation and characterization of a topA mutant of Shigella flexneri. Mol. Microbiol. 7, 351–358 (1993).
  Article Google Scholar
• Kato, J. et al. New topoisomerase essential for chromosome segregation in E. coli. Cell 63, 393–404 (1990).
  Article CAS PubMed Google Scholar
• Iborra, F. J., Jackson, D. A. & Cook, P. R. Coupled transcription and translation within nuclei of mammalian cells. Science 293, 1139–1142 (2001).
  Article CAS PubMed Google Scholar
• Shaiu, W. L. & Hsieh, T. S. Targeting to transcriptionally active loci by the hydrophilic N-terminal domain of Drosophila DNA topoisomerase I. Mol. Cell. Biol. 18, 4358–4367 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Uemura, T. & Yanagida, M. Isolation of type I and II DNA topoisomerase mutants from fission yeast: single and double mutants show different phenotypes in cell growth and chromatin organization. EMBO J. 3, 1737–1744 (1984).
  Article CAS PubMed PubMed Central Google Scholar
• Thrash, C., Bankier, A. T., Barrell, B. G. & Sternglanz, R. Cloning, characterization, and sequence of the yeast DNA topoisomerase I gene. Proc. Natl Acad. Sci. USA 82, 4374–4378 (1985).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, M. D. et al. Force and velocity measured for single molecules of RNA polymerase. Science 282, 902–907 (1998).
  Article CAS PubMed Google Scholar
• Matera, A. G. Nuclear bodies: multifaceted subdomains of the interchromatin space. Trends Cell Biol. 9, 302–309 (1999).
  Article CAS PubMed Google Scholar
• Misteli, T. Protein dynamics: implications for nuclear architecture and gene expression. Science 291, 843–847 (2001).
  Article CAS PubMed Google Scholar
• Felsenfeld, G., Clark, D. & Studitsky, V. Transcription through nucleosomes. Biophys. Chem. 86, 231–237 (2000).
  Article CAS PubMed Google Scholar
• Mondal, N. & Parvin, J. D. DNA topoisomerase IIα is required for RNA polymerase II transcription on chromatin templates. Nature 413, 435–438 (2001).
  Article CAS PubMed Google Scholar
• Merino, A., Madden, K. R., Lane, W. S., Champoux, J. J. & Reinberg, D. DNA topoisomerase I is involved in both repression and activation of transcription. Nature 365, 227–232 (1993).
  Article CAS PubMed Google Scholar
• Kretzschmar, M., Meisterernst, M. & Roeder, R. G. Identification of human DNA topoisomerase I as a cofactor for activator-dependent transcription by RNA polymerase II. Proc. Natl Acad. Sci. USA 90, 11508–11512 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Shykind, B. M., Kim, J., Stewart, L., Champoux, J. J. & Sharp, P. A. Topoisomerase I enhances TFIID–TFIIA complex assembly during activation of transcription. Genes Dev. 11, 397–407 (1997).
  Article CAS PubMed Google Scholar
• Wang, J. C. DNA topoisomerases: why so many? J. Biol. Chem. 266, 6659–6662 (1991).
  CAS PubMed Google Scholar
• Wang, J. C., Caron, P. R. & Kim, R. A. The role of DNA topoisomerases in recombination and genome stability: a double-edged sword? Cell 62, 403–406 (1990).
  Article CAS PubMed Google Scholar
• Keeney, S., Giroux, C. N. & Kleckner, N. Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88, 375–384 (1997).
  Article CAS PubMed Google Scholar
• Cox, M. M. et al. The importance of repairing stalled replication forks. Nature 404, 37–41 (2000).
  Article CAS PubMed Google Scholar
• Kuzminov, A. DNA replication meets genetic exchange: chromosomal damage and its repair by homologous recombination. Proc. Natl Acad. Sci. USA 98, 8461–8468 (2001).A summary of a recent colloquium on the roles of recombination in DNA replication. This issue of the journal contains many other contributions to the colloquium, including reference 16.
  Article CAS PubMed PubMed Central Google Scholar
• Zhu, Q., Pongpech, P. & DiGate, R. J. Type I topoisomerase activity is required for proper chromosomal segregation in Escherichia coli. Proc. Natl Acad. Sci. USA 98, 9766–9771 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Wallis, J. W., Chrebet, G., Brodsky, G., Rolfe, M. & Rothstein, R. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58, 409–419 (1989).The first report of a type IA DNA topoisomerase in eukaryotes.
  Article CAS PubMed Google Scholar
• Maftahi, M. et al. The top3+ gene is essential in Schizosaccharomyces pombe and the lethality associated with its loss is caused by Rad12 helicase activity. Nucleic Acids Res. 27, 4715–4724 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Goodwin, A., Wang, S. W., Toda, T., Norbury, C. & Hickson, I. D. Topoisomerase III is essential for accurate nuclear division in Schizosaccharomyces pombe. Nucleic Acids Res. 27, 4050–4058 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Gangloff, S., McDonald, J. P., Bendixen, C., Arthur, L. & Rothstein, R. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14, 8391–8398. (1994).This study reported the identification of the first suppressor of top3 and established physical and functional interactions between a type IA DNA topoisomerase and a RecQ family helicase.
  Article CAS PubMed PubMed Central Google Scholar
• Bennett, R. J., Sharp, J. A. & Wang, J. C. Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisiae. J. Biol. Chem. 273, 9644–9650 (1998).
  Article CAS PubMed Google Scholar
• van Brabant, A. J., Stan, R. & Ellis, N. A. DNA helicases, genomic instability, and human genetic disease. Annu. Rev. Genomics Hum. Genet. 1, 409–459 (2000).
  Article CAS PubMed Google Scholar
• Shen, J. C. & Loeb, L. A. The Werner syndrome gene: the molecular basis of RecQ helicase-deficiency diseases. Trends Genet. 16, 213–220 (2000).
  Article CAS PubMed Google Scholar
• Wu, L. & Hickson, I. D. RecQ helicases and topoisomerases: components of a conserved complex for the regulation of genetic recombination. Cell. Mol. Life Sci. 58, 894–901 (2001).
  Article CAS PubMed Google Scholar
• Kitao, S., Lindor, N. M., Shiratori, M., Furuichi, Y. & Shimamoto, A. Rothmund-Thomson syndrome responsible gene, RECQL4: genomic structure and products. Genomics 61, 268–276 (1999).
  Article CAS PubMed Google Scholar
• Bennett, R. J., Noirot-Gros, M. F. & Wang, J. C. Interaction between yeast Sgs1 helicase and DNA topoisomerase III. J. Biol. Chem. 275, 26898–26905 (2000).
  CAS PubMed Google Scholar
• Fricke, W. M., Kaliraman, V. & Brill, S. J. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J. Biol. Chem. 276, 8848–8855 (2001).
  Article CAS PubMed Google Scholar
• Shimamoto, A., Nishikawa, K., Kitao, S. & Furuichi, Y. Human RecQ5β, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3α and 3β. Nucleic Acids Res. 28, 1647–1655 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Gangloff, S., de Massy, B., Arthur, L., Rothstein, R. & Fabre, F. The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J. 18, 1701–1711 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Kaliraman, V., Mullen, J. R., Fricke, W. M., Bastin-Shanower, S. A. & Brill, S. J. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15, 2730–2740 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Keeney, S. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52, 1–53 (2001).
  Article CAS PubMed Google Scholar
• Buhler, C., Gadelle, D., Forterre, P., Wang, J. C. & Bergerat, A. Reconstitution of DNA topoisomerase VI of the thermophilic archaeon Sulfolobus shibatae from subunits separately overexpressed in Escherichia coli. Nucleic Acids Res. 26, 5157–5162 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Koshland, D. & Strunnikov, A. Mitotic chromosome condensation. Annu. Rev. Cell Dev. Biol. 12, 305–333 (1996).
  Article CAS PubMed Google Scholar
• Gordon, G. S. & Wright, A. DNA segregation in bacteria. Annu. Rev. Microbiol. 54, 681–708 (2000).
  Article CAS PubMed Google Scholar
• Nordstrom, K. & Dasgupta, S. Partitioning of the Escherichia coli chromosome: superhelicity and condensation. Biochimie 83, 41–48 (2001).
  Article CAS PubMed Google Scholar
• Losada, A. & Hirano, T. Shaping the metaphase chromosome: coordination of cohesion and condensation. Bioessays 23, 924–935 (2001).
  Article CAS PubMed Google Scholar
• Uemura, T. et al. DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50, 917–925 (1987).
  Article CAS PubMed Google Scholar
• Durrieu, F. et al. DNA topoisomerase IIα interacts with CAD nuclease and is involved in chromatin condensation during apoptotic execution. Curr. Biol. 10, 923–926 (2000).
  Article CAS PubMed Google Scholar
• Castano, I. B., Heath-Pagliuso, S., Sadoff, B. U., Fitzhugh, D. J. & Christman, M. F. A novel family of TRF (DNA topoisomerase I-related function) genes required for proper nuclear segregation. Nucleic Acids Res. 24, 2404–2410 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Castano, I. B., Brzoska, P. M., Sadoff, B. U., Chen, H. & Christman, M. F. Mitotic chromosome condensation in the rDNA requires TRF4 and DNA topoisomerase I in Saccharomyces cerevisiae. Genes Dev. 10, 2564–2576 (1996).
  Article CAS PubMed Google Scholar
• Hartsuiker, E., Bahler, J. & Kohli, J. The role of topoisomerase II in meiotic chromosome condensation and segregation in Schizosaccharomyces pombe. Mol. Biol. Cell 9, 2739–2750 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Miller, C. A., Beaucage, S. L. & Cohen, S. N. Role of DNA superhelicity in partitioning of the pSC101 plasmid. Cell 62, 127–133 (1990).
  Article CAS PubMed Google Scholar
• Conley, D. L. & Cohen, S. N. Effects of the pSC101 partition (par) locus on in vivo DNA supercoiling near the plasmid replication origin. Nucleic Acids Res. 23, 701–707 (1995).
  Article CAS PubMed PubMed Central Google Scholar
• Austin, S. J. & Eichorn, B. G. Random diffusion can account for _topA_-dependent suppression of partition defects in low-copy-number plasmids. J. Bacteriol. 174, 5190–5195 (1992).
  Article CAS PubMed PubMed Central Google Scholar
• Sawitzke, J. A. & Austin, S. Suppression of chromosome segregation defects of Escherichia coli muk mutants by mutations in topoisomerase I. Proc. Natl Acad. Sci. USA 97, 1671–1676 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Varga-Weisz, P. D. et al. Chromatin-remodelling factor CHRAC contains the ATPases ISWI and topoisomerase II. Nature 388, 598–602 (1997).
  Article CAS PubMed Google Scholar
• LeRoy, G., Loyola, A., Lane, W. S. & Reinberg, D. Purification and characterization of a human factor that assembles and remodels chromatin. J. Biol. Chem. 275, 14787–14790 (2000).
  Article CAS PubMed Google Scholar
• Warburton, P. E. & Earnshaw, W. C. Untangling the role of DNA topoisomerase II in mitotic chromosome structure and function. Bioessays 19, 97–99 (1997).
  Article CAS PubMed Google Scholar
• Gasser, S. M., Laroche, T., Falquet, J., Boy de la Tour, E. & Laemmli, U. K. Metaphase chromosome structure. Involvement of topoisomerase II. J. Mol. Biol. 188, 613–629 (1986).
  Article CAS PubMed Google Scholar
• Bhat, M. A., Philp, A. V., Glover, D. M. & Bellen, H. J. Chromatid segregation at anaphase requires the barren product, a novel chromosome-associated protein that interacts with topoisomerase II. Cell 87, 1103–1114 (1996).
  Article PubMed Google Scholar
• Christensen, M. O. et al. Dynamics of human DNA topoisomerases IIα and IIβ in living cells. J. Cell Biol. 157, 31–44 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Lewis, R. J., Tsai, F. T. & Wigley, D. B. Molecular mechanisms of drug inhibition of DNA gyrase. Bioessays 18, 661–671 (1996).
  Article CAS PubMed Google Scholar
• Maxwell, A. DNA gyrase as a drug target. Biochem. Soc. Trans. 27, 48–53 (1999).
  Article CAS PubMed Google Scholar
• Li, T. K. & Liu, L. F. Tumor cell death induced by topoisomerase-targeting drugs. Annu. Rev. Pharmacol. Toxicol. 41, 53–77 (2001).
  Article PubMed Google Scholar
• Vizan, J. L., Hernandez-Chico, C., del Castillo, I. & Moreno, F. The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated by E. coli DNA gyrase. EMBO J. 10, 467–476 (1991).
  Article CAS PubMed PubMed Central Google Scholar
• Miki, T., Park, J. A., Nagao, K., Murayama, N. & Horiuchi, T. Control of segregation of chromosomal DNA by sex factor F in Escherichia coli. Mutants of DNA gyrase subunit A suppress letD (ccdB) product growth inhibition. J. Mol. Biol. 225, 39–52 (1992).
  Article CAS PubMed Google Scholar
• Bernard, P. & Couturier, M. Cell killing by the F plasmid CcdB protein involves poisoning of DNA-topoisomerase II complexes. J. Mol. Biol. 226, 735–745 (1992).
  Article CAS PubMed Google Scholar
• Wang, H. et al. Stimulation of topoisomerase II-mediated DNA damage via a mechanism involving protein thiolation. Biochemistry 40, 3316–3323 (2001).
  Article CAS PubMed Google Scholar
• Yang, X., Li, W., Prescott, E. D., Burden, S. J. & Wang, J. C. DNA topoisomerase IIβ and neural development. Science 287, 131–134 (2000).
  Article CAS PubMed Google Scholar
• Krogh, B. O. & Shuman, S. A poxvirus-like type IB topoisomerase family in bacteria. Proc. Natl Acad. Sci. USA 99, 1853–1858 (2002).The first report of the presence of a type IB DNA topoisomerase in prokaryotes.
  Article CAS PubMed PubMed Central Google Scholar
• Zhang, H. et al. Human mitochondrial topoisomerase I. Proc. Natl Acad. Sci. USA 98, 10608–10613 (2001).A report of the discovery of the newest DNA topoisomerase gene in humans.
  Article CAS PubMed PubMed Central Google Scholar
• Morham, S. G., Kluckman, K. D., Voulomanos, N. & Smithies, O. Targeted disruption of the mouse topoisomerase I gene by camptothecin selection. Mol. Cell. Biol. 16, 6804–6809 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Li, W. & Wang, J. C. Mammalian DNA topoisomerase IIIα is essential in early embryogenesis. Proc. Natl Acad. Sci. USA 95, 1010–1013 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Kwan, K. Y. & Wang, J. C. Mice lacking DNA topoisomerase IIIβ develop to maturity but show a reduced mean lifespan. Proc. Natl Acad. Sci. USA 98, 5717–5721 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Szostak, J. W., Orr-Weaver, T. L., Rothstein, R. J. & Stahl, F. W. The double-strand-break repair model for recombination. Cell 33, 25–35 (1983).
  Article CAS PubMed Google Scholar
• Schwacha, A. & Kleckner, N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83, 783–791 (1995).An elegant study that establishes the formation of the double Holliday junction in meiotic recombination. The potential requirement for a type I DNA topoisomerase in resolving a subset of such structures was also raised. The idea that a type II DNA topoisomerase might be able to resolve some of the double Holliday junctions, however, differed from the view that is presented in this review.
  Article CAS PubMed Google Scholar
• Gilbertson, L. A. & Stahl, F. W. A test of the double-strand break repair model for meiotic recombination in Saccharomyces cerevisiae. Genetics 144, 27–41 (1996).
  CAS PubMed PubMed Central Google Scholar
• Zou, H. & Rothstein, R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90, 87–96 (1997).
  Article CAS PubMed Google Scholar
• Michel, B. Replication fork arrest and DNA recombination. Trends Biochem. Sci. 25, 173–178 (2000).
  Article CAS PubMed Google Scholar
• Sekiguchi, J., Seeman, N. C. & Shuman, S. Resolution of Holliday junctions by eukaryotic DNA topoisomerase I. Proc. Natl Acad. Sci. USA 93, 785–789 (1996).
  Article CAS PubMed PubMed Central Google Scholar
• Champoux, J. J. Renaturation of complementary single-stranded DNA circles: complete rewinding facilitated by the DNA untwisting enzyme. Proc. Natl Acad. Sci. USA 74, 5328–5332 (1977).
  Article CAS PubMed PubMed Central Google Scholar
• Bennett, R. J., Keck, J. L. & Wang, J. C. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J. Mol. Biol. 289, 235–248 (1999).
  Article CAS PubMed Google Scholar
• Karow, J. K., Constantinou, A., Li, J. L., West, S. C. & Hickson, I. D. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl Acad. Sci. USA 97, 6504–6508 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Doe, C. L., Dixon, J., Osman, F. & Whitby, M. C. Partial suppression of the fission yeast rqh1− phenotype by expression of a bacterial Holliday junction resolvase. EMBO J. 19, 2751–2762 (2000).
  Article CAS PubMed PubMed Central Google Scholar
• Chen, S. J. & Wang, J. C. Identification of active site residues in Escherichia coli DNA topoisomerase I. J. Biol. Chem. 273, 6050–6056 (1998).
  Article CAS PubMed Google Scholar
• Stivers, J. T., Shuman, S. & Mildvan, A. S. Vaccinia DNA topoisomerase I: single-turnover and steady-state kinetic analysis of the DNA strand cleavage and ligation reactions. Biochemistry 33, 327–339 (1994).
  Article CAS PubMed Google Scholar
• Wigley, D. B., Davies, G. J., Dodson, E. J., Maxwell, A. & Dodson, G. Crystal structure of an N-terminal fragment of the DNA gyrase B protein. Nature 351, 624–629 (1991).
  Article CAS PubMed Google Scholar