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Introduction and Historical Perspective

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DNA Topoisomerases and Cancer

Part of the book series: Cancer Drug Discovery and Development ((CDD&D))

Abstract

The discoveries of DNA supercoiling and DNA topoisomerases have been two of the most important breakthroughs in biology in the last century. Negative supercoiling is a critical feature of bacterial genomes and transient supercoiling is produced in all organisms by DNA binding proteins and/or various DNA tracking processes. DNA topoisomerases are major elements in cellular life and the plethora of natural antibiotics and antitumor drugs that target these enzymes testify for their importance. DNA topoisomerases I and II, catalyzing DNA strand transfer via single or double-strand breaks in DNA molecules respectively, originated and evolved to solve topological problems raised by the plectonemic coiling of two DNA strands in the double helix, and specialized topoisomerases acquired the ability to produce supercoiling. The first DNA topoisomerases were discovered in Escherichia coli (protein ω, DNA gyrase, Topo III, and Topo IV) and eukaryotic cells (Topo IB, Topo II, Topo III). Later on, new families and subfamilies of DNA topoisomerases were discovered in Archaea, the third domain of life (reverse gyrase, Topo V, Topo VI), challenging the prokaryote/eukaryote dichotomy. DNA topoisomerases are now classified into five families of homologous proteins (Topo IA, IB, IC, Topo IIA, IIB) based on structural similarities. These families have been divided into subfamilies, some of them characterized by unique enzymatic properties (gyrase, reverse gyrase). The distribution of these families and subfamilies do not overlap with the universal tree of life, and some subfamilies are specific for viruses. This suggests that viruses played an important role in the origin and distribution of DNA topoisomerases among cellular organisms.

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References

  • Adachi Y, Luke M, Laemmli UK (1991) Chromosome assembly in vitro : Topoisomerase II is required for condensation Cell 64:137–148

    Google Scholar 

  • Aggarwal M, Brosh RM (2009) WRN helicase defective in the premature aging disorder Werner syndrome genetically interacts with topoisomerase 3 and restores the top3 slow growth phenotype of sgs1 top3. Aging (Albany NY) 1(2):219–233

    Google Scholar 

  • Allemand F, Mathy N, Brechemier-Baey D, Condon C (2005) The 5S rRNA maturase, ribonuclease M5, is a Toprim domain family member. Nucleic Acids Res 33(13):4368–4376

    PubMed Central  CAS  PubMed  Google Scholar 

  • Anquetin G, Rouquayrol M, Mahmoudi N, Santillana-Hayat M, Gozalbes R, Greiner J, Farhati K, Derouin F (2004) Synthesis of new fluoroquinolones and evaluation of their in vitro activity on Toxoplasma gondii and Plasmodium spp. Guedj R, Vierling P. Bioorg Med Chem Lett 14(11):2773–2776

    CAS  PubMed  Google Scholar 

  • Aravind L, Leipe DD, Koonin EV (1998) Toprim a conserved catalytic domain in type IA and II topoisomerases, DnaG-type primases, OLD family nucleases and RecR proteins. Nucleic Acids Res 26:4205–4213

    PubMed Central  CAS  PubMed  Google Scholar 

  • Atomi H, Matsumi R, Imanaka T (2004) Reverse gyrase is not a prerequisite for hyperthermophilic life. J Bacteriol 186:4829–4833

    PubMed Central  CAS  PubMed  Google Scholar 

  • Baldi MJ, Benedetti P, Mattoccia E, Tocchini-Valentini GP (1980) In vitro catenation and decatenation of DNA and a novel eucaryotic ATP-dependent topoisomerase. Cell 20:461–467

    CAS  PubMed  Google Scholar 

  • Baxter J, Diffley JF (2008) Topoisomerase II inactivation prevents the completion of DNA replication in budding yeast. Mol Cell 30(6):790–802

    CAS  PubMed  Google Scholar 

  • Belmont AS (2006) Mitotic chromosome structure and condensation. Curr Opin Cell Biol 18(6):632–638

    CAS  PubMed  Google Scholar 

  • Belova GI, Prasad R, Nazimov IV, Wilson SH, Slesarev AI (2002) The domain organization and properties of individual domains of DNA topoisomerase V, a type 1B topoisomerase with DNA repair activities. J Biol Chem 277:4959–4965

    CAS  PubMed  Google Scholar 

  • Benarroch D, Claverie JM, Raoult D, Shuman S (2006) Characterization of mimivirus DNA topoisomerase IB suggests horizontal gene transfer between eukaryal viruses and bacteria. J Virol 80:314–321

    PubMed Central  CAS  PubMed  Google Scholar 

  • Benedetti P, Baldi MI, Mattoccia E, Tocchini-Valentini GP (1983) Purification and characterization of Xenopus laevis topoisomerase II. EMBO J 2(8):1303–1308

    PubMed Central  CAS  PubMed  Google Scholar 

  • Berger JM, Gamblin SJ, Harrison SC, Wang JC (1996) Structure and mechanism of DNA topoisomerase II. Nature 379(6562):225–232

    CAS  PubMed  Google Scholar 

  • Berger JM, Fass D, Wang JC, Harrison SC (1998) Structural similarities between topoisomerases that cleave one or both DNA strands. Proc Natl Acad Sci USA 95(14):7876–7881

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bergerat A, Gadelle D, Forterre P (1994) Purification of a DNA topoisomerase II from the hyperthermophilic archaeon Sulfolobus shibatae. A thermostable enzyme with both bacterial and eucaryal features. J Biol Chem 269(44):27663–27669

    CAS  PubMed  Google Scholar 

  • Bergerat A, de Massy B, Gadelle D, Varoutas PC, Nicolas A, Forterre P (1997) An atypical topoisomerase II from Archaea with implications for meiotic recombination. Nature 386:414–417

    CAS  PubMed  Google Scholar 

  • Bodley AL, Chakraborty AK, Xie S, Burri C, Shapiro TA (2003) An unusual type IB topoisomerase from African trypanosomes. Proc Natl Acad Sci USA 100(13):7539–7544

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brochier C, Forterre P, Gribaldo S (2004) Archaeal phylogeny based on proteins of the transcription and translation machineries: tackling the Methanopyrus kandleri paradox. Genome Biol 5(3):R17

    PubMed Central  PubMed  Google Scholar 

  • Brochier-Armanet C, Forterre P (2007) Widespread distribution of archaeal reverse gyrase in thermophilic bacteria suggests a complex history of vertical inheritance and lateral gene transfers. Archaea 2:83–93

    PubMed Central  CAS  PubMed  Google Scholar 

  • Brochier-Armanet C, Boussau B, Gribaldo S, Forterre P (2008a) Mesophilic Crenarchaeota: proposal for a third archaeal phylum, the Thaumarchaeota. Nat Rev Microbiol 6:245–252

    CAS  PubMed  Google Scholar 

  • Brochier-Armanet C, Gribaldo S, Forterre P (2008b) A DNA topoisomerase IB in Thaumarchaeota testifies for the presence of this enzyme in the last common ancestor of Archaea and Eucarya. Biol Direct 3:54

    PubMed Central  PubMed  Google Scholar 

  • Brown PO, Cozzarelli NR (1979) A sign inversion mechanism for enzymatic supercoiling of DNA. Science 206(4422):1081–1083

    CAS  PubMed  Google Scholar 

  • Buhler C, Lebbink JH, Bocs C, Ladenstein R, Forterre P (2001) DNA topoisomerase VI generates ATP-dependent double-strand breaks with two-nucleotide overhangs. J Biol Chem 276:37215–37222

    CAS  PubMed  Google Scholar 

  • Cairns J (1963a) The bacterial chromosome and its manner of replication as seen by autoradiography. J Mol Biol 6:208–213

    CAS  PubMed  Google Scholar 

  • Cairns J (1963b) The chromosome of E. coli. Cold Spring Harbour Symp Quant Biol 28 (1963b) 43–46

    Google Scholar 

  • Capp C, Qian Y, Sage H, Huber H, Hsieh TS (2010) Separate and combined biochemical activities of the subunits of a naturally split reverse gyrase. J Biol Chem 2010 285(51):39637–39645

    PubMed Central  CAS  PubMed  Google Scholar 

  • Champoux JJ, Bean MD (1980) Topoisomerase and the swivel problem. In: Alberts BM (eds) Mechanistic studies of DNA réplication and genetic recombination. ICN-UCLA Symposia on Molecular and Cellular Biology, Vol 19, pp 809–815 Academic Press, New York

    Google Scholar 

  • Champoux JJ, Dulbecco R (1972) An activity from mammalian cells that untwists superhelical DNA-a possible swivel for DNA replication (polyoma-ethidium bromide-mouse-embryo cells-dye binding assay). Proc Natl Acad Sci USA 69:143–146

    PubMed Central  CAS  PubMed  Google Scholar 

  • Charbonnier F, Forterre P (1994) Comparison of plasmid DNA topology among mesophilic and thermophilic eubacteria and archaebacteria. J Bacteriol 176:1251–1259

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen GL, Yang L, Rowe TC, Halligan BD, Tewey KM, Liu LF (1984) Nonintercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J Biol Chem 259(21):13560–13566

    CAS  PubMed  Google Scholar 

  • Chen L, Huang L (2006) Oligonucleotide cleavage and rejoining by topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus: temperature dependence and strand annealing-promoted DNA religation. Mol Microbiol 60:783–794

    CAS  PubMed  Google Scholar 

  • Cheng C, Kussie P, Pavletich N, Shuman S (1998) Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92:841–850

    CAS  PubMed  Google Scholar 

  • Cheung KJ, Badarinarayana V, Selinger DW, Janse D, Church GM (2003) A microarray-based antibiotic screen identifies a regulatory role for supercoiling in the osmotic stress response of Escherichia coli. Genome Res. 13(2):206–215

    PubMed Central  CAS  PubMed  Google Scholar 

  • Cho HS, Lee SS, Kim KD, Hwang I, Lim JS, Park YI, Pai HS (2004) DNA gyrase is involved in chloroplast nucleoid partitioning. Plant Cell 16(10):2665–2682

    PubMed Central  CAS  PubMed  Google Scholar 

  • Confalonieri F, Elie C, Nadal M, de La Tour C, Forterre P, Duguet M (1993) Reverse gyrase: a helicase-like domain and a type I topoisomerase in the same polypeptide. Proc Natl Acad Sci USA 90:4753–4757

    PubMed Central  CAS  PubMed  Google Scholar 

  • Conti C, Seiler JA, Pommier Y. (2007) The mammalian DNA replication elongation checkpoint: implication of Chk1 and relationship with origin firing as determined by single DNA molecule and single cell analyses. Cell Cycle. 6:2760–2767

    CAS  PubMed  Google Scholar 

  • Corbett KD, Berger JM (2003) Structure of the topoisomerase VI-B subunit: implications for type II topoisomerase mechanism and evolution. EMBO J 22:151–163

    PubMed Central  CAS  PubMed  Google Scholar 

  • Corbett KD, Shultzaberger RK, Berger JM (2004) The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc Natl Acad Sci USA 101(19):7293–7298

    PubMed Central  CAS  PubMed  Google Scholar 

  • Corbett KD, Benedetti P, Berger JM (2007) Holoenzyme assembly and ATP-mediated conformational dynamics of topoisomerase VI. Nat Struct Mol Biol 14:611–619

    CAS  PubMed  Google Scholar 

  • D’Amaro A, Rossi M, Ciaramella M (2007) Reverse gyrase: an unusual DNA manipulator of hyperthermophilic organisms. J Biochem 56:103–109

    Google Scholar 

  • Dai P, Wang Y, Ye R, Chen L, Huang L (2003) DNA topoisomerase III from the hyperthermophilic archaeon Sulfolobus solfataricus with specific DNA cleavage activity. J Bacteriol 185:5500–5507

    PubMed Central  CAS  PubMed  Google Scholar 

  • Das BB, Ganguly A, Majumder HK (2008) DNA topoisomerases of Leishmania: the potential targets for anti-leishmanial therapy. Adv Exp Med Biol 625:103–115 Review

    CAS  PubMed  Google Scholar 

  • Dar MA, Sharma A, Mondal N, Dhar SK (2007) Molecular cloning of apicoplast-targeted Plasmodium falciparum DNA gyrase genes: unique intrinsic ATPase activity and ATP-independent dimerization of PfGyrB subunit. Eukaryot Cell 6(3):398–412

    PubMed Central  CAS  PubMed  Google Scholar 

  • De Massy B, Rocco V, Nicolas A. The nucleotide mapping of DNA double-strand breaks at the CYS3 initiation site of meiotic recombination in Saccharomyces cerevisiae. EMBO J 1995 Sep 15;14(18):4589–98

    Google Scholar 

  • Declais AC, Marsault J, Confalonieri F, de La Tour CB, Duguet M (2000) Reverse gyrase, the two domains intimately cooperate to promote positive supercoiling, J Biol Chem 275:19498–19504

    CAS  PubMed  Google Scholar 

  • Dickey JS, Van Etten JL, Osheroff N (2005) DNA methylation impacts the cleavage activity of Chlorella virus topoisomerase II. Biochemistry 44:15378–15386

    CAS  PubMed  Google Scholar 

  • DiGate RJ, Marians KJ (1989) Molecular cloning and DNA sequence analysis of Escherichia coli topB, the gene encoding topoisomerase III. J Biol Chem 264:17924–17930

    Google Scholar 

  • DiGate RJ, Marians KJ (1992) Escherichia coli topoisomerase III-catalyzed cleavage of RNA. J Biol Chem 267:20532–20535

    CAS  PubMed  Google Scholar 

  • DiNardo S, Voelkel KA, Sternglanz R, Reynolds AE, Wright A (1982) Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31:43–51

    Google Scholar 

  • DiNardo S, Voelkel K, Sternglanz R (1984) DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc Natl Acad Sci USA 81(9):2616–2620

    PubMed Central  CAS  PubMed  Google Scholar 

  • Dong KC, Berger JM (2007) Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450(7173):1201–1205

    CAS  PubMed  Google Scholar 

  • Drlica K, Worcel A (1975) Conformational transitions in the Escherichia coli chromosome: analysis by viscometry and sedimentation. J Mol Biol 98(2):393–411

    CAS  PubMed  Google Scholar 

  • Dröge P, Nordheim A (1991) Transcription-induced conformational change in a topologically closed DNA domain. Nucleic Acids Res 19(11):2941–2946

    PubMed Central  PubMed  Google Scholar 

  • Drolet M (2006) Growth inhibition mediated by excess negative supercoiling: the interplay between transcription elongation, R-loop formation and DNA topology. Mol Microbiol 59(3):723–730

    CAS  PubMed  Google Scholar 

  • Duguet M, Serre MC, Bouthier de La Tour C (2006) A universal type IA topoisomerase fold. J Mol Biol 359:805–812

    CAS  PubMed  Google Scholar 

  • Dutta R, Inouye M (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25:24–28

    CAS  PubMed  Google Scholar 

  • Edgell DR, Doolittle WF (1997) Archaea and the origin(s) of DNA replication proteins. Cell 89:995–998

    CAS  PubMed  Google Scholar 

  • Espeli O, Lee C, Marians KJ (2003) A physical and functional interaction between Escherichia coli FtsK and topoisomerase IV. J Biol Chem 278(45):44639–44644

    CAS  PubMed  Google Scholar 

  • Filée J, Forterre P, Sen-Lin T, Laurent J (2002) Evolution of DNA polymerase families: evidences for multiple gene exchange between cellular and viral proteins. J Mol Evol 54:763–773

    PubMed  Google Scholar 

  • Fischer MG, Allen MJ, Wilson WH, Suttle CA (2010) Giant virus with a remarkable complement of genes infects marine zooplankton. Proc Natl Acad Sci USA 107(45):19508–11953

    PubMed Central  CAS  PubMed  Google Scholar 

  • Forterre P (1999) Displacement of cellular proteins by functional analogues from plasmids or viruses could explain puzzling phylogenies of many DNA informational proteins. Mol Microbiol 33(3):457–465

    CAS  PubMed  Google Scholar 

  • Forterre P (2002a) A hot story from comparative genomics: reverse gyrase is the only hyperthermophile-specific protein. Trends Genet 18:236–237

    CAS  PubMed  Google Scholar 

  • Forterre P (2002b) The origin of DNA genomes and DNA replication proteins. Curr Opin Microbiol 5:525

    CAS  PubMed  Google Scholar 

  • Forterre P (2005) The two ages of the RNA world, and the transition to the DNA world: a story of viruses and cells. Biochimie 87:793–803

    CAS  PubMed  Google Scholar 

  • Forterre P (2006) Three RNA cells for ribosomal lineages and three DNA viruses to replicate their genomes: a hypothesis for the origin of cellular domain. Proc Natl Acad Sci USA 103:3669–3674

    PubMed Central  CAS  PubMed  Google Scholar 

  • Forterre P (2006) DNA topoisomerase V: a new fold of mysterious origin. Trends Biotechnol 24:245–247

    CAS  PubMed  Google Scholar 

  • Forterre P, Gadelle D (2009) Phylogenomics of DNA topoisomerases: their origin and putative roles in the emergence of modern organisms. Nucleic Acids Res 37(3):679–692

    PubMed Central  CAS  PubMed  Google Scholar 

  • Forterre P, Gribaldo S (2010) Bacteria with a eukaryotic touch: a glimpse of ancient evolution? Proc Natl Acad Sci USA 107(29):12739–12740

    PubMed Central  CAS  PubMed  Google Scholar 

  • Forterre P, Gribaldo S, Gadelle D, Serre MC (2007) Origin and evolution of DNA topoisomerases. Biochimie 4:427–446

    Google Scholar 

  • Forterre P, Mirambeau G, Jaxel C, Nadal M, Duguet M (1985) High positive supercoiling in vitro catalyzed by an ATP and polyethylene glycol-stimulated topoisomerase from Sulfolobus acidocaldarius. EMBO J 4:2123–2128

    PubMed Central  CAS  PubMed  Google Scholar 

  • Francke B, Margolin J (1981) Effect of novobiocin and other DNA gyrase inhibitors on virus replication and DNA synthesis in herpes simplex virus type 1-infected BHK cells. J Gen Virol 52(Pt 2):401–404

    CAS  PubMed  Google Scholar 

  • Freeland SJ, Knight RD, Landweber LF (1999) Do proteins predate DNA? Science 286:690–692

    CAS  PubMed  Google Scholar 

  • French SL, Sikes ML, Hontz RD, Osheim YN, Lambert TE, El Hage A, Smith MM, Tollervey D, Smith JS, Beyer AL (2011) Distinguishing the Roles of Topoisomerases I and II in Relief of Transcription-Induced Torsional Stress in Yeast rRNA Genes. Mol Cell Biol 31(3):482–494

    PubMed Central  CAS  PubMed  Google Scholar 

  • Fuller FB (1971) The writhing number of a space curve. Proc Natl Acad Sci USA 68:815–819

    PubMed Central  CAS  PubMed  Google Scholar 

  • Funnell BE, Baker TA, Kornberg A. (1987) In vitro assembly of a prepriming complex at the origin of the Escherichia coli chromosome. J Biol Chem. 262:10327–10334

    CAS  PubMed  Google Scholar 

  • Gadelle, Bocs DC, Graille M, Forterre P (2005) Inhibition of archaeal growth and DNA topoisomerase VI activities by the Hsp90 inhibitor radicicol. Nucleic Acids Res 33:2310–2317

    Google Scholar 

  • Gadelle D, Graille M, Forterre P (2006) The HSP90 and DNA topoisomerase VI inhibitor radicicol also inhibits human type II DNA topoisomerase. Biochem Pharmacol 72:1207–1216

    CAS  PubMed  Google Scholar 

  • Gadelle D, Filée J, Buhler C, Forterre P (2003) Phylogenomics of type II DNA topoisomerases. Bioessays 3:232–242

    Google Scholar 

  • Garnier F, Nadal M (2008) Transcriptional analysis of the two reverse gyrase encoding genes of Sulfolobus solfataricus P2 in relation to the growth phases and temperature conditions. Extremophiles 12(6):799–809

    CAS  PubMed  Google Scholar 

  • García-Estrada C, Prada CF, Fernández-Rubio C, Rojo-Vázquez F, Balaña-Fouce R (2010) DNA topoisomerases in apicomplexan parasites: promising targets for drug discovery. Proc Biol Sci 277(1689):1777–1778

    PubMed Central  PubMed  Google Scholar 

  • Ganguly A, Del Toro Duany Y, Rudolph MG, Klostermeier D (2011) The latch modulates nucleotide and DNA binding to the helicase-like domain of Thermotoga maritima reverse gyrase and is required for positive DNA supercoiling. Nucleic Acids Res 39:1789–1800

    Google Scholar 

  • Gellert M, Mizuuchi K, O’Dea MH, Itoh T, Tomizawa JI (1977) Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc Natl Acad Sci USA 74:4772–4776

    Google Scholar 

  • Gellert M, O’Dea MH, Itoh T, Tomizawa J (1976) Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci USA 73(12):4474–4478

    Google Scholar 

  • Germond JE, Hirt B, Oudet P, Gross-Bellark M, Chambon P (1975) Folding of the DNA double helix in chromatin-like structures from simian virus 40. Proc Natl Acad Sci USA 72(5):1843–1847

    PubMed Central  CAS  PubMed  Google Scholar 

  • Giaever G, Lynn R, Goto T, Wang JC (1986) The complete nucleotide sequence of the structural gene TOP2 of yeast DNA topoisomerase II. J Biol Chem 261(27):12448–12454

    CAS  PubMed  Google Scholar 

  • Graille M, Cladière L, Durand D, Lecointe F, Gadelle D, Quevillon-Cheruel S, Vachette P, Forterre P, van Tilbeurgh H (2008) Crystal structure of an intact type II DNA topoisomerase: insights into DNA transfer mechanisms. Structure 16:360–370

    CAS  PubMed  Google Scholar 

  • Griffith JD (1976) Visualization of prokaryotic DNA in a regularly condensed chromatin-like fiber. Proc Natl Acad Sci USA 73(2):563–567

    PubMed Central  CAS  PubMed  Google Scholar 

  • Guipaud O, Forterre P (2001) DNA gyrase from Thermotoga maritima. Methods Enzymol 334:162–171

    CAS  PubMed  Google Scholar 

  • Guipaud O, Marguet E, Noll KM, de la Tour CB, Forterre P (1997) Both DNA gyrase and reverse gyrase are present in the hyperthermophilic bacterium Thermotoga maritime. Proc Natl Acad Sci USA 94:10606–10611

    PubMed Central  CAS  PubMed  Google Scholar 

  • Halligan BD, Edwards KA, Liu LF (1985) Purification and characterization of a type II DNA topoisomerase from bovine calf thymus. J Biol Chem 260(4):2475–2482

    CAS  PubMed  Google Scholar 

  • Hartung F, Puchta H (2001) Molecular characterization of homologues of both subunits A (SPO11) and B of the archaebacterial topoisomerase 6 in plants. Gene 271:81–86

    CAS  PubMed  Google Scholar 

  • Hartung F, Angelis KJ, Meister A, Schubert I, Melzer M, Puchta H (2002) An archaebacterial topoisomerase homolog not present in other eukaryotes is indispensable for cell proliferation of plants. Curr Biol 12:1787–1791

    CAS  PubMed  Google Scholar 

  • Hayama R, Marians KJ (2010) Physical and functional interaction between the condensin MukB and the decatenase topoisomerase IV in Escherichia coli. Proc Natl Acad Sci USA 107(44):18826–18831

    Google Scholar 

  • Higgins NP, Peebles CL, Sugino A, Cozzarelli NR (1978) Purification of subunits of Escherichia coli DNA gyrase and reconstitution of enzymatic activity. Proc Natl Acad Sci USA 75:1773–1777

    Google Scholar 

  • Holmes ML, Dyall-Smith ML (1991) Mutations in DNA gyrase result in novobiocin resistance in halophilic archaebacteria. J Bacteriol 173:642–648

    Google Scholar 

  • Hsiang YH, Hertzberg R, Hecht S, Liu LF (1985) Camptothecin induces protein-linked DNA breaks via mammalian DNA topoisomerase I. J Biol Chem 260(27):14873–14878

    CAS  PubMed  Google Scholar 

  • Hsieh LS, Rouviere-Yaniv J, Drlica K (1991) Bacterial DNA supercoiling and [ATP]/[ADP] ratio: changes associated with salt shock. J Bacteriol 173(12):3914–3917

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hsieh LS, Burger RM, Drlica K (1991) Bacterial DNA supercoiling and [ATP]/[ADP]. Changes associated with a transition to anaerobic growth. J Mol Biol 219(3):443–450

    CAS  PubMed  Google Scholar 

  • Hsieh TJ, Farh L, Huang WM, Chan NL (2004) Structure of the topoisomerase IV C-terminal domain: a broken beta-propeller implies a role as geometry facilitator in catalysis. J Biol Chem 279:55587–55593

    CAS  PubMed  Google Scholar 

  • Hsieh TS, Plank JL (2006) Reverse gyrase functions as a DNA renaturase: annealing of complementary single-stranded circles and positive supercoiling of a bubble substrate. J Biol Chem 281:5640–5647

    CAS  PubMed  Google Scholar 

  • Hsieh TJ, Yen TJ, Lin TS, Chang HT, Huang SY, Hsu CH, Farh L, Chan NL (2010) Twisting of the DNA-binding surface by a beta-strand-bearing proline modulates DNA gyrase activity. Nucleic Acids Res 38(12):4173–81

    PubMed Central  CAS  PubMed  Google Scholar 

  • Huang WM, Joss L, Hsieh T, Casjens S. Protelomerase uses a topoisomerase IB/Y-recombinase type mechanism to generate DNA hairpin ends. J Mol Biol 2004 Mar 12;337(1):77–92

    Google Scholar 

  • Jain P, Nagaraja V (2005) An atypical type II topoisomerase from Mycobacterium smegmatis with positive supercoiling activity. Mol Microbiol 58:1392–1405

    CAS  PubMed  Google Scholar 

  • Jaxel C, Nadal M, Mirambeau G, Forterre P, Takahashi M, Duguet M. (1989) Reverse gyrase binding to DNA alters the double helix structure and produces single-strand cleavage in the absence of ATP. EMBO J. 8:3135–3139

    PubMed Central  CAS  PubMed  Google Scholar 

  • Jo K, Topal MD (1995) DNA topoisomerase and recombinase activities in Nae I restriction endonuclease. Science 267:1817–1820

    CAS  PubMed  Google Scholar 

  • Kampmann M, Stock D. (2004) Reverse gyrase has heat-protective DNA chaperone activity independent of supercoiling. Nucleic Acids Res. 32:3537–3545

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kato J, Nishimura Y, Imamura R, Niki H, Hiraga S, Suzuki H (1990) New topoisomerase essential for chromosome segregation in E. coli. Cell 63(2):393–404. Erratum in: Cell 1991

    Google Scholar 

  • Kato J, Suzuki H, Ikeda H (1992) Purification and characterization of DNA topoisomerase IV in Escherichia coli. J Biol Chem 267:25676–25684

    Google Scholar 

  • Keeney S, Giroux CN, Kleckner N (1997) Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family. Cell 88:375–384

    CAS  PubMed  Google Scholar 

  • Keller W (1975) Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc Natl Acad Sci USA 72:4876–4880

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kikuchi A, Asai K (1984) Reverse gyrase-a topoisomerase which introduces positive superhelical turns into DNA. Nature 309:677–681

    CAS  PubMed  Google Scholar 

  • Kim RA, Wang JC (1989) Function of DNA topoisomerases as replication swivels in Saccharomyces cerevisiae. J Mol Biol 208:257–267

    CAS  PubMed  Google Scholar 

  • Kirkegaard K, Wang JC (1978) Escherichia coli DNA topoisomerase I catalyzed linking of single-stranded rings of complementary base sequences. Nucleic Acids Res 5:3811–3820

    Google Scholar 

  • Khodursky AB, Peter BJ, Schmid MB, DeRisi J, Botstein D, Brown PO, Cozzarelli NR (2000) Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. Proc Natl Acad Sci USA 97(17):9419–9424

    PubMed Central  CAS  PubMed  Google Scholar 

  • Koonin EV. (2003) Comparative genomics, minimal gene-sets and the last universal common ancestor. Nat Rev Microbiol. 1:127–136

    CAS  PubMed  Google Scholar 

  • Koonin EV, Senkevitch TG, Dolja VV (2006) The ancient Virus World and evolution of cells. Biol Direct 1:19

    Google Scholar 

  • Koepsel RR, Murray RW, Rosenblum WD, Khan SA (1985) The replication initiator protein of plasmid pT181 has sequence-specific endonuclease and topoisomerase-like activities. Proc Natl Acad Sci USA 82(20):6845–9684

    PubMed Central  CAS  PubMed  Google Scholar 

  • Koster DA, Croquette V, Dekker C, Shuman S, Dekker NH (2005) Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434:671–674

    CAS  PubMed  Google Scholar 

  • Kovalsky OI, Kozyavkin SA, Slesarev AI. (1990) Archaebacterial reverse gyrase cleavage-site specificity is similar to that of eubacterial DNA topoisomerases I. Nucleic Acids Res. 18:2801–2805

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kozyavkin SA, Pushkin AV, Eiserling FA, Stetter KO, Lake JA, Slesarev AI (1995) DNA enzymology above 100 degrees C Topoisomerase V unlinks circular DNA at 80–122 degrees C. J Biol Chem 270:13593–13595

    CAS  PubMed  Google Scholar 

  • Kramlinger VM, Hiasa H (2006) The “GyrA-box” is required for the ability of DNA gyrase to wrap DNA and catalyze the supercoiling reaction. J Biol Chem 281:3738–3742

    CAS  PubMed  Google Scholar 

  • Kreuzer KN, Cozzarelli NR (1980) Formation and resolution of DNA catenanes by DNA gyrase. Cell 20(1):245–254

    CAS  PubMed  Google Scholar 

  • Krogh BO, Shuman S (2002) A poxvirus-like type IB topoisomerase family in bacteria. Proc Natl Acad Sci USA 99:1853–1858

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lazcano A, Guerrero R, Margulis L, Oró J (1988) The evolutionary transition from RNA to DNA in early cells. J Mol Evol 27:283–290

    CAS  PubMed  Google Scholar 

  • Lebowitz J (1990) Through the looking glass: the discovery of supercoiled DNA. Trends Biochem Sci 15:202–207

    CAS  PubMed  Google Scholar 

  • Leipe DD, Aravind L, Koonin EV (1999) Did DNA replication evolve twice independently? Nucleic Acids Res 27:3389–3401

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li Y, Stewart NK, Berger AJ, Vos S, Schoeffler AJ, Berger JM, Chait BT, Oakley MG (2010) Escherichia coli condensin MukB stimulates topoisomerase IV activity by a direct physical interaction. Proc Natl Acad Sci USA 107(44):18832–18837

    PubMed Central  CAS  PubMed  Google Scholar 

  • Li Z, Hiasa H, DiGate R (2006) Characterization of a unique type IA topoisomerase in Bacillus cereus. Mol Microbiol 60(1):140–151

    CAS  PubMed  Google Scholar 

  • Lindsley JE (1996) Intradimerically tethered DNA topoisomerase II is catalytically active in DNA transport. Proc Natl Acad Sci USA 93:2975–2980

    Google Scholar 

  • Lima CD, Mondragón A. Mechanism of type II DNA topoisomerases: a tale of two gates. Structure 1994 Jun 15;2(6):559–60

    Google Scholar 

  • Lima CD, Wang JC, Mondragon A (1994) Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367:138–146

    CAS  PubMed  Google Scholar 

  • Liu J, Wu TC, Lichten M (1995) The location and structure of double-strand DNA breaks induced during yeast meiosis: evidence for a covalently linked DNA-protein intermediate. EMBO J 14(18):4599–4608

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu LF, Wang JC (1978a) Micrococcus luteus DNA gyrase: active components and a model for its supercoiling of DNA. Proc Natl Acad Sci USA 75(5):2098–102

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu LF, Wang JC (1978b) DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell 15(3):979–984

    CAS  PubMed  Google Scholar 

  • Liu LF, Wang JC (1987) Supercoiling of the DNA template during transcription. Proc Natl Acad Sci USA 84(20):7024–7027

    PubMed Central  CAS  PubMed  Google Scholar 

  • Liu LF, Liu CC, Alberts BM (1979) T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature 28:456–461

    Google Scholar 

  • Liu LF, Liu CC, Alberts BM (1980) Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell 19:697–707

    CAS  PubMed  Google Scholar 

  • Ljungman M, Hanawalt PC. (1992) Localized torsional tension in the DNA of human cells. Proc Natl Acad Sci USA 89:6055–6059

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lopez-Garcia P, Forterre P, Van der Oost J, Erauso G (2000) Plasmid pGS5 from the hyperthermophilic archaeon Archaeoglobus profundus is negatively supercoiled. J Bacteriol 182:4998–5000

    PubMed Central  CAS  PubMed  Google Scholar 

  • Lockshon D, Morris DR (1983) Positively supercoiled plasmid DNA is produced by treatment of Escherichia coli with DNA gyrase inhibitors. Nucleic Acids Res 11:2999–3017

    Google Scholar 

  • Low RL, Orton S, Friedman DB. (2003) A truncated form of DNA topoisomerase IIbeta associates with the mtDNA genome in mammalian mitochondria. Eur J Biochem:4173–4186

    Google Scholar 

  • Lundin D, Gribaldo S, Torrents E, Sjöberg BM, Poole AM. (2010) Ribonucleotide reduction – horizontal transfer of a required function spans all three domains. BMC Evol Biol.10:383–387

    PubMed Central  CAS  PubMed  Google Scholar 

  • Malik SB, Ramesh MA, Hulstrand AM, Logsdon JM (2007) Protist homologs of the meiotic Spo11 gene and topoisomerase VI reveal an evolutionary history of gene duplication and lineage-specific loss. Mol Biol Evol 24:2827–2841

    CAS  PubMed  Google Scholar 

  • Mankouri HW, Hickson ID (2007) The RecQ helicase-topoisomerase III-Rmi1 complex: a DNA structure-specific “dissolvasome”? Trends Biochem Sci 32:538–546

    CAS  PubMed  Google Scholar 

  • Marguet E, Forterre P (1994) DNA stability at temperatures typical for hyperthermophiles. Nucleic Acids Res 22(9):1681–1686

    PubMed Central  CAS  PubMed  Google Scholar 

  • Marsin S, Marguet E, Forterre P (2000) Topoisomerase activity of the hyperthermophilic replication initiator protein Rep75. Nucleic Acids Res 28:2251–2255

    PubMed Central  CAS  PubMed  Google Scholar 

  • Miller KG, Liu LF, Englund PT (1981) A homogeneous type II DNA topoisomerase from HeLa cell nuclei. J Biol Chem 256:9334–9339

    CAS  PubMed  Google Scholar 

  • Mizuuchi K, Fisher LM, O’Dea MH, Gellert M (1980) DNA gyrase action involves the introduction of transient double-strand breaks into DNA. Proc Natl Acad Sci USA 77:1847–1851

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mizuuchi K, Nash HA (1976) Restriction assay for integrative recombination of bacteriophage lambda DNA in vitro: requirement for closed circular DNA substrate. Proc Natl Acad Sci USA 73:3524–3528

    PubMed Central  CAS  PubMed  Google Scholar 

  • Mondragon A, DiGate R (1999) The structure of Escherichia coli DNA topoisomerase III. Structure 7:1373–1383

    CAS  PubMed  Google Scholar 

  • Morrison A, Cozzarelli NR (1979) Site-specific cleavage of DNA by E. coli DNA gyrase. Cell 17:175–84

    CAS  PubMed  Google Scholar 

  • Musgrave D, Forterre P, Slesarev A. (2000) Negative constrained DNA supercoiling in archaeal nucleosomes. Mol Microbiol. 35:341–349

    CAS  PubMed  Google Scholar 

  • Mushegian AR, Koonin EV (1996) A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc Natl Acad Sci USA 93:10268–10273

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nadal M, Mirambeau G, Forterre P, Reiter WD, Duguet M (1986) Positively supercoiled DNA in a virus-like particle of an archaebacterium. Nature 321:256–258

    CAS  Google Scholar 

  • Nadal M (2007) Reverse gyrase: an insight into the role of DNA-topoisomerases. Biochimie 89:447–455

    CAS  PubMed  Google Scholar 

  • Nakasu S, Kikuchi A (1985) Reverse gyrase dependent type I topoisomerase from Sulfolobus. EMBO J 4:2705–2710

    PubMed Central  CAS  PubMed  Google Scholar 

  • Napoli A, Valenti A, Salerno V, Nadal M, Garnier F, Rossi M, Ciaramella M (2004) Reverse gyrase recruitment to DNA after UV light irradiation in Sulfolobus solfataricus. J Biol Chem 279(32):33192–33198

    CAS  PubMed  Google Scholar 

  • Nelson EM, Tewey KM, Liu LF (1984) Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4′-(9-acridinylamino)-methanesulfon-m-anisidide. Proc Natl Acad Sci USA 81(5):1361–1365

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nichols MD, DeAngelis K, Keck JL, Berger JM (1999) Structure and function of an archaeal topoisomerase VI subunit with homology to the meiotic recombination factor Spo11. EMBO J 18:6177–6188

    PubMed Central  CAS  PubMed  Google Scholar 

  • Nitiss JL.(2009) DNA topoisomerase II and its growing repertoire of biological functions. Nat Rev Cancer.9:327–37

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pace NR (2006) Time for a change. Nature, 441(7091):289

    CAS  PubMed  Google Scholar 

  • Pansegrau W, Schröder W, Lanka E (1994) Concerted action of three distinct domains in the DNA cleaving-joining reaction catalyzed by relaxase (TraI) of conjugative plasmid RP4. J Biol Chem 269:2782–2789

    CAS  PubMed  Google Scholar 

  • Pavlov AR, Belova GI, Kozyavkin SA, Slesarev AI (2002) Helix-hairpin-helix motifs confer salt resistance and processivity on chimeric DNA polymerases. Proc Natl Acad Sci USA 99(21):13510–13515

    PubMed Central  CAS  PubMed  Google Scholar 

  • Peter BJ, Arsuaga J, Breier AM, Khodursky AB, Brown PO, Cozzarelli NR (2004) Genomic transcriptional response to loss of chromosomal supercoiling in Escherichia coli. Genome Biol 5(11):R87

    PubMed Central  PubMed  Google Scholar 

  • Plank JL, Wu J, Hsieh TS. (2006) Topoisomerase IIIa and Bloom’s helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc Natl Acad Sci USA 103:11118–11123

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pommier Y, Leo E, Zhang H, Marchand C (2010) DNA topoisomerases and their poisoning by anticancer and antibacterial drugs. Chem Biol 17:421–433

    CAS  PubMed  Google Scholar 

  • Poole AM, Logan DT (2005) Modern mRNA proofreading and repair: clues that the last universal common ancestor possessed an RNA genome? Mol Biol Evol 22:1444–1455

    CAS  PubMed  Google Scholar 

  • Pruss GJ, Drlica K (1986) Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc Natl Acad Sci USA 83:8952–8956

    PubMed Central  CAS  PubMed  Google Scholar 

  • Pruss GJ, Drlica K (1989) DNA supercoiling and prokaryotic transcription. Cell 56(4):521–522

    CAS  PubMed  Google Scholar 

  • Pruss GJ, Manes SH, Drlica K (1982) Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31:35–342

    CAS  PubMed  Google Scholar 

  • Radloff R, Bauer W, Vinograd J (1967) A dye-buoyant-density method for the detection and isolation of closed circular duplex DNA: the closed circular DNA in HeLa cells. Proc Natl Acad Sci USA 57:1514–1521

    PubMed Central  CAS  PubMed  Google Scholar 

  • Raghu Ram EV, Kumar A, Biswas S, Kumar A, Chaubey S, Siddiqi MI, Habib S (2007) Nuclear gyrB encodes a functional subunit of the Plasmodium falciparum gyrase that is involved in apicoplast DNA replication. Mol Biochem Parasitol 154:30–39

    CAS  PubMed  Google Scholar 

  • Raoult D, Audic S, Robert C, Abergel C, Renesto P, Ogata H, La Scola B, Suzan M, Claverie JM (2004) The 1.2-megabase genome sequence of Mimivirus. Science 306:1344–1350

    CAS  PubMed  Google Scholar 

  • Roca J, Wang JC (1992) The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerases. Cell 71:833–840

    Google Scholar 

  • Roca J, Wang JC (1994) DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate mechanism. Cell 77:609–616

    CAS  PubMed  Google Scholar 

  • Rodríguez AC, Stock D (2002) Crystal structure of reverse gyrase: insights into the positive supercoiling of DNA. EMBO J 21:418–426

    PubMed Central  PubMed  Google Scholar 

  • Ross W, Rowe T, Glisson B, Yalowich J, Liu L (1984) Role of topoisomerase II in mediating epipodophyllotoxin-induced DNA cleavage. Cancer Res 44:5857–5860

    CAS  PubMed  Google Scholar 

  • Roth TF, Helinski DR (1967) Evidence for circular DNA forms of a bacterial plasmid. Proc Natl Acad Sci USA 58:650–657

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ruthenburg AJ, Graybosch DM, Huetsch JC, Verdine GL (2005) A superhelical spiral in the Escherichia coli DNA gyrase A C-terminal domain imparts unidirectional supercoiling bias. J Biol Chem. 280:26177–84

    CAS  PubMed  Google Scholar 

  • Salceda J, Fernández X, Roca J (2006) Topoisomerase II, not topoisomerase I, is the proficient relaxase of nucleosomal DNA. EMBO J 25:2575–2583

    PubMed Central  CAS  PubMed  Google Scholar 

  • Schmid MB, Sawitzke JA. (1993) Multiple bacterial topoisomerases: specialization or redundancy? Bioessays 15:445–449

    CAS  PubMed  Google Scholar 

  • Schoeffler AJ, Berger JM (2008) DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys 41:41–101

    CAS  PubMed  Google Scholar 

  • Scocca JR, Shapiro TA (2008) A mitochondrial topoisomerase IA essential for late theta structure resolution in African trypanosomes. Mol Microbiol 67:820–829

    CAS  PubMed  Google Scholar 

  • Seki M, Nakagawa T, Seki T, Kato G, Tada S, Takahashi Y, Yoshimura A, Kobayashi T, Aoki A, Otsuki M, Habermann FA, Tanabe H, Ishii Y and Enomoto T (2006) Bloom helicase and DNA topoisomerase IIIa are involved in the dissolution of sister chromatids. Mol Cell Biol 26:6299–6307

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sekiguchi J, Shuman S (1997) Site-specific ribonuclease activity of eukaryotic DNA topoisomerase I. Mol Cell 1:89–97

    CAS  PubMed  Google Scholar 

  • Shimamoto A, Nishikawa K, Kitao S, Furuichi Y (2000) Human RecQ5b, a large isomer of RecQ5 DNA helicase, localizes in the nucleoplasm and interacts with topoisomerases 3a and 3b. Nucleic Acids Res 28:1647–1655

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sinden RR, Carlson JO, Pettijohn DE (1980) Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell 21:773–783

    CAS  PubMed  Google Scholar 

  • Sioud M, Possot O, Elie C, Sibold L, Forterre P (1988) Coumarin and quinolone action in archaebacteria: evidence for the presence of a DNA gyrase-like enzyme. J Bacteriol 170:946–953

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sioud M, Forterre P (1989) Ciprofloxacin and etoposide (VP16) produce a similar pattern of DNA cleavage in a plasmid of an archaebacterium. Biochemistry 28:3638–3641

    CAS  PubMed  Google Scholar 

  • Slesarev AI, Kozyavkin SA (1990) DNA substrate specificity of reverse gyrase from extremely thermophilic archaebacteria. J Biomol Struct Dyn. 7:935–942

    CAS  PubMed  Google Scholar 

  • Slesarev AI, Zaitzev DA, Kopylov VM, Stetter KO, Kozyavkin SA (1991) DNA topoisomerase III from extremely thermophilic archaebacteria. ATP-independent type I topoisomerase from Desulfurococcus amylolyticus drives extensive unwinding of closed circular DNA at high temperature. J Biol Chem 266:12321–12328

    CAS  PubMed  Google Scholar 

  • Slesarev AI, Stetter KO, Lake JA, Gellert M, Krah R, Kozyavkin SA (1993) DNA topoisomerase V is a relative of eukaryotic topoisomerase I from a hyperthermophilic prokaryote. Nature 364:735–737

    CAS  PubMed  Google Scholar 

  • Schmidt BH, Burgin AB, Deweese JE, Osheroff N, Berger JM (2010) A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465:641–644

    PubMed Central  CAS  PubMed  Google Scholar 

  • Staczek P, Higgins NP (1998) Gyrase and Topo IV modulate chromosome domain size in vivo.Mol Microbiol 29:1435–1448

    Google Scholar 

  • Sugimoto-Shirasu K, Roberts GR, Stacey NJ, McCann MC, Maxwell A, Roberts K (2005) RHL1 is an essential component of the plant DNA topoisomerase VI complex and is required for ploidy-dependent cell growth. Proc Natl Acad Sci USA 102:18736–18741

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sugimoto-Shirasu K, Stacey NJ, Corsar J, Roberts K, McCann MC (2002) DNA topoisomerase VI is essential for endoreduplication in Arabidopsis. Curr Biol 12:1782–1786

    CAS  PubMed  Google Scholar 

  • Sugino A, Peebles CL, Kreuzer KN, Cozzarelli NR (1977) Mechanism of action of nalidixic acid: purification of Escherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme. Proc Natl Acad Sci USA 74:4767–4771

    PubMed Central  CAS  PubMed  Google Scholar 

  • Srivenugopal KS, Lockshon D, Morris DR (1984) Escherichia coli DNA topoisomerase III: purification and characterization of a new type I enzyme. Biochemistry 23(9):1899–1906

    CAS  PubMed  Google Scholar 

  • Postow L, Hardy CD, Arsuaga J, Cozzarelli NR (2004) Topological domain structure of the Escherichia coli chromosome. Genes Dev 18(14):1766–1779

    PubMed Central  CAS  PubMed  Google Scholar 

  • Krasilnikov AS, Podtelezhnikov A, Vologodskii A, Mirkin SM (1999) Large-scale effects of transcriptional DNA supercoiling in vivo. J Mol Biol 292(5):1149–1156

    CAS  PubMed  Google Scholar 

  • Taneja B, Patel A, Slesarev A, Mondragon A (2006) Structure of the N-terminal fragment of topoisomerase V reveals a new family of topoisomerases. EMBO J 25:398–408

    PubMed Central  CAS  PubMed  Google Scholar 

  • Taneja B, Schnurr B, Slesarev A, Marko JF, Mondragón A (2007) Topoisomerase V relaxes supercoiled DNA by a constrained swiveling mechanism. Proc Natl Acad Sci USA 104 (37):14670–14675

    Google Scholar 

  • Temime-Smaali N, Guittat L, Wenner T, Bayart E, Douarre C, Gomez D, Giraud-Panis MJ, Londono-Vallejo A, Gilson E, Amor-Guéret M, Riou JF (2008) Topoisomerase IIIalpha is required for normal proliferation and telomere stability in alternative lengthening of telomeres. EMBO J 27(10):1513–1524

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tewey KM, Chen GL, Nelson EM, Liu LF (1984) Intercalative antitumor drugs interfere with the breakage-reunion reaction of mammalian DNA topoisomerase II. J Biol Chem 259(14):9182–9187

    CAS  PubMed  Google Scholar 

  • Tewey KM, Rowe TC, Yang L, Halligan BD, Liu LF (1984) Adriamycin-induced DNA damage mediated by mammalian DNA topoisomerase II. Science 226(4673):466–468

    CAS  PubMed  Google Scholar 

  • Tretter EM, Lerman JC, Berger JM (2010) A naturally chimeric type IIA topoisomerase in Aquifex aeolicus highlights an evolutionary path for the emergence of functional paralogs. Proc Natl Acad Sci USA 107:22055–22059

    PubMed Central  CAS  PubMed  Google Scholar 

  • Tse-Dinh YC (1985) Regulation of the Escherichia coli DNA topoisomerase I gene by DNA supercoiling. Nucleic Acids Res 13:4751–4763

    PubMed Central  CAS  PubMed  Google Scholar 

  • Uemura T, Morikawa K, Yanagida M (1986) The nucleotide sequence of the fission yeast DNA topoisomerase II gene: structural and functional relationships to other DNA topoisomerases. EMBO J 5:2355–2361

    PubMed Central  CAS  PubMed  Google Scholar 

  • Uemura T, Ohkura H, Adachi Y, Morino K, Shiozaki K, Yanagida M (1987) DNA topoisomerase II is required for condensation and separation of mitotic chromosomes in S. pombe. Cell 50:917–925

    Google Scholar 

  • Ullsperger C, Cozzarelli NR (1996) Contrasting enzymatic activities of topoisomerase IV and DNA gyrase from Escherichia coli. J Biol Chem 271:31549–31555

    Google Scholar 

  • Valenti A, Perugino G, D’Amaro A, Cacace A, Napoli A, Rossi M, Ciaramella M (2008) Dissection of reverse gyrase activities: insight into the evolution of a thermostable molecular machine Nucleic Acids Res 36:4587–4597

    PubMed Central  CAS  PubMed  Google Scholar 

  • Valenti A, Perugino G, Nohmi T, Rossi M, Ciaramella M (2009) Inhibition of translesion DNA polymerase by archaeal reverse gyrase. Nucleic Acids Res 37:4287–4295

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vijayan V, Zuzow R, O’Shea EK (2009) Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc Natl Acad Sci USA 106:22564–22568

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vinograd J, Lebowitz J, Radloff R, Watson R, Laipis P (1965) The twisted circular form of polyoma viral DNA. Proc Natl Acad Sci USA 53:1104–1111

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vinograd J, Lebowitz J (1966) Physical and topological properties of circular DNA. J Gen Physiol 49:103–125

    PubMed Central  CAS  PubMed  Google Scholar 

  • Vinograd J, Lebowitz J, Watson R (1968) Early and late helix-coil transitions in closed circular DNA. The number of superhelical turns in polyoma DNA. J Mol Biol 33(1):173–197

    CAS  PubMed  Google Scholar 

  • Wall MK, Mitchenall LA, Maxwell A (2004) Arabidopsis thaliana DNA gyrase is targeted to chloroplasts and mitochondria. Proc Natl Acad Sci USA 101:7821–7826

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wallis JW, Chrebet G, Brodsky G, Rolfe M, Rothstein R (1989) A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409–419

    CAS  PubMed  Google Scholar 

  • Wang JC (1971) Interaction between DNA and an Escherichia coli protein omega. J Mol Biol 55:523–533

    CAS  PubMed  Google Scholar 

  • Wang JC (1991) DNA topoisomerases: why so many? J Biol Chem 266:6659–6662

    CAS  PubMed  Google Scholar 

  • Wang JC (2009a) Untangling the double-helix: DNA entanglement and the action of the DNA topoisomerases. Cold Spring Harbor, New York, Cold Spring Harbor Laboratory Press

    Google Scholar 

  • Wang JC (2009b) A journey in the world of DNA rings and beyond. Annu Rev Biochem 78:31–54

    CAS  PubMed  Google Scholar 

  • Wang Y, Lyu YL, Wang JC (2002) Dual localization of human DNA topoisomerase IIIalpha to mitochondria and nucleus. Proc Natl Acad Sci USA 99:12114–12119

    PubMed Central  CAS  PubMed  Google Scholar 

  • Warburton PE, Earnshaw WC (1997) Untangling the role of DNA topoisomerase II. In: Mitotic chromosome structure and function. Bioessays 19:97–99. Review

    CAS  PubMed  Google Scholar 

  • Watson JD, Crick FH (1953a) Genetical implications of the structure of deoxyribonucleic acid. Nature 171:964–967

    CAS  PubMed  Google Scholar 

  • Watson JD, Crick FH (1953b) The structure of DNA. Cold Spring Harb Symp Quant Biol 18:123–131

    CAS  PubMed  Google Scholar 

  • Weil R, Vinograd J (1963) The cyclic helix and cyclic coil forms of polyoma viral DNA. Proc Natl Acad Sci USA 50:730–738

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wyckoff E, Natalie D, Nolan JM, Lee M, Hsieh T (1989) Structure of the Drosophila DNA topoisomerase II gene. Nucleotide sequence and homology among topoisomerases II. J Mol Biol. 205:1–13

    CAS  PubMed  Google Scholar 

  • Woese CR, Fox GE (1977) Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 74:5088–5090

    PubMed Central  CAS  PubMed  Google Scholar 

  • Woese CR, Kandler O, Wheelis ML (1990) Towards a natural system of organisms: proposal for the domains Archaea, Bacteria, and Eucarya. Proc Natl Acad Sci USA 87: 4576–4579

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wu D, Hugenholtz P, Mavromatis K, Pukall R, Dalin E, Ivanova NN, Kunin V, Goodwin L, Wu M, Tindall BJ, Hooper SD, Pati A, Lykidis A, Spring S, Anderson IJ, D’haeseleer P, Zemla A, Singer M, Lapidus A, Nolan M, Copeland A, Han C, Chen F, Cheng JF, Lucas S, Kerfeld C, Lang E, Gronow S, Chain P, Bruce D, Rubin EM, Kyrpides NC, Klenk HP, Eisen JA (2009) A phylogeny-driven genomic encyclopaedia of Bacteria and Archaea. Nature 462:1056–1060

    PubMed Central  CAS  PubMed  Google Scholar 

  • Wu L, Hickson ID (2006) DNA helicases required for homologous recombination and repair of damaged replication forks. Annu Rev Genet 40:279–306

    Google Scholar 

  • Yamada T, Satoh S, Ishikawa H, Fujiwara A, Kawasaki T, Fujie M, Ogata H (2010) A jumbo phage infecting the phytopathogen Ralstonia solanacearum defines a new lineage of the Myoviridae family. Virology 398:135–147

    CAS  PubMed  Google Scholar 

  • Yamashiro K, Yamagishi A (2005) Characterization of the DNA gyrase from the thermoacidophilic archaeon Thermoplasma acidophilum. J Bacteriol 187:8531–8536

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yang W (2010) Topoisomerases and site-specific recombinases: similarities in structure and mechanism. Crit Rev Biochem Mol Biol 45:520–534

    CAS  PubMed  Google Scholar 

  • Yin Y, Cheong H, Friedrichsen D, Zhao Y, Hu J, Mora-Garcia S, Chory J (2002) A crucial role for the putative Arabidopsis topoisomerase VI in plant growth and development. Proc Natl Acad Sci USA 99:10191–10196

    PubMed Central  CAS  PubMed  Google Scholar 

  • Zechiedrich EL, Khodursky AB, Bachellier S, Schneider R, Chen D, Lilley DM, Cozzarelli NR (2000) Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J Biol Chem 275:8103–8113

    CAS  PubMed  Google Scholar 

  • Zhang H, Barceló JM, Lee B, Kohlhagen G, Zimonjic DB, Popescu NC, Pommier Y (2001) Human mitochondrial topoisomerase I. Proc Natl Acad Sci USA 98:10608–10613

    Google Scholar 

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Acknowledgment

I thank Daniele Gadelle and Marc Nadal for some references and critical comments on some aspect of this manuscript. I am grateful to Anna Bizard for the two-D gels in Fig. 1.3 and Sugimoto-Shirasu for the spectacular pictures of Arabidopsis wild type and Topo IIB mutant.

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Forterre, P. (2012). Introduction and Historical Perspective. In: Pommier, Y. (eds) DNA Topoisomerases and Cancer. Cancer Drug Discovery and Development. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-0323-4_1

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