Abstract
In all living cells, DNA is homeostatically underwound relative to its lowest energy conformation, resulting in egative supercoiling. This underwinding of DNA is critical to the metabolism of DNA and, thus, is vital to cell survival. Enzymes called topoisomerases regulate and maintain the supercoiled state of DNA and are critical to the successful replication of the genome. These enzymes are major targets for drugs used in the treatment of bacterial infections and cancer. One puzzling phenomenon of the topoisomerase mechanism is how these enzymes, orders of magnitude smaller than their substrate, can search, recognize and act at a local level to affect global DNA topology. While the homeostatic state of DNA supercoiling in cells is negative, both positive and negative supercoils exist transiently. Because of the right-handed nature of the DNA helix, the positive and negative supercoils are not equivalent. Several computational and theoretical models have been developed in an effort to describe the features of both positively and negatively supercoiled DNA. These models have accurately predicted some of the phenomena observed in vivo. However, the over-simplifying assumptions cannot account for the different biological activities of positively and negatively supercoiled DNA. This review will discuss the models in place and the mathematical and energetic properties of this elegant molecule and the “machines that push it around.”
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References
Adrian M., ten Heggeler-Bordier B., Wahli W., Stasiak A.Z., Stasiak A., and Dubochet J. (1990). Direct visualization of supercoiled DNA molecules in solution. EMBO J. 9, 4551–4554.
Allemand J.F., Bensimon D., Lavery R., and Croquette V. (1998). Stretched and overwound DNA forms a Pauling-like structure with exposed bases. Proc. Natl. Acad. Sci. USA 95, 14152–14157.
Anderson P. and Bauer W. (1978) Supercoiling in closed circular DNA: dependence upon ion type and concentration. Biochemistry. 17, 594–601.
Anderson V.E. and Osheroff N. (2001). Type II topoisomerases as targets for quinolone antibacterials: turning Dr. Jekyll into Mr. Hyde. Curr. Pharm. Des. 7, 337–353.
Arai Y., Yasuda R., Akashi K., Harada Y., Miyata H., Kinosita K.J., and Itoh H. (1999). Tying a molecular knot with optical tweezers. Nature 399, 446–448.
Arsuaga J., Vazquez M., Trigueros S., Sumners de W., and Roca J. (2002). Knotting probability of DNA molecules confined in restricted volumes: DNA knotting in phage capsids. Proc. Natl. Acad. Sci. USA 99, 5373–5377.
Bacolla A. and Wells R.D. (2004). Non-B DNA conformations, genomic rearrange ments, and human disease. J. Biol. Chem. 279, 47411–47414.
Baldwin G.S., Brooks N.J., Robson R.E., Wynveen A., Goldar A., Leikin S., Seddon J.M., and Kornyshev A.A. (2008) DNA double helices recognize mutual sequence homology in a protein free environment. J. Phys. Chem. B. 112, 1060–1064.
Bates A.D. and Maxwell A. (2007). Energy coupling in type II topoisomerases: why do they hydrolyze ATP? Biochemistry 46, 7929–7941.
Bednar J., Furrer P., Stasiak A., Dubochet J., Egelman E.H., and Bates A.D. (1994). The twist, writhe and overall shape of supercoiled DNA change during counterion-induced transition from a loosely to a tightly interwound superhelix. J. Mol. Biol. 235, 825–847.
Belova G.I., Prasad R., Kozyavkin S.A., Lake J.A., Wilson S.H., and Slesarev A.I. (2001). A type IB topoisomerase with DNA repair activities. Proc. Natl. Acad. Sci. USA. 98, 6015–6020.
Belova G.I., Prasad R., Nazimov I.V., Wilson S.H., and Slesarev A.I. (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.
Benham C.J. (1979). Torsional stress and local denaturation in supercoiled DNA. Proc. Natl. Acad. Sci. USA 76, 3870–3874.
Benham C.J. (1992). Energetics of the strand separation transition in superhelical DNA. J. Mol. Biol. 225, 835–847.
Benham C.J. and Mielke S.P. (2005). DNA mechanics. Ann. Rev. Biomed. Eng. 7, 21–53.
Berman H.M., Westbrook J., Feng Z., Gilliland G., Bhat T.N., Weissig H., Shindyalov I.N., and Bourne P.E. (2000). The Protein Data Bank. Nucleic Acids Res. 28, 235–242.
Boles T.C., White J.H., and Cozzarelli N.R. (1990). Structure of plectonemically supercoiled DNA. J. Mol. Biol. 213, 931–951.
Bryant Z., Stone M.D., Gore J., Smith S.B., Cozzarelli N.R., and Bustamante C. (2003). Structural transitions and elasticity from torque measurements on DNA. Nature 424, 338–341.
Buck G.R. and Zechiedrich E.L. (2004). DNA disentangling by type-2 topoisomerases. J. Mol. Biol. 340, 933–939.
Burnier Y., Weber C., Flammini A., and Stasiak A. (2007). Local selection rules that can determine specific pathways of DNA unknotting by type II DNA topoisomerases. Nucleic Acids Res. 35, 5223–5231.
Bustamante C., Bryant Z., and Smith S.B. (2003). Ten years of tension: single-molecule DNA mechanics. Nature 421, 423–427.
Bustamante C., Marko J.F., Siggia E.D., and Smith S. (1994). Entropic elasticity of lambda-phage DNA. Science 265, 1599–1600.
Calladine C.R. and Drew H.R. (1984) A base-centred explanation of the B-to-A transition in DNA. J. Mol. Biol. 178, 773–782.
Camilloni G., Di Martino E., Caserta M., and di Mauro E. (1988). Eukaryotic DNA topoisomerase I reaction is topology dependent. Nucleic Acids Res. 14, 7071–7085.
Camilloni G., Martino E., Di Mauro E., and Caserta M. (1989). Regulation of the function of eukaryotic DNA topoisomerase I: topological conditions for inactivity. Proc. Natl. Acad. Sci. USA 86, 3080–3084.
Champoux J.J. (2001). DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70, 369–413.
Champoux J.J. (2002). Type IA DNA topoisomerases: strictly one step at a time. Proc. Natl. Acad. Sci. USA. 99, 11998–12000.
Changela A., DiGate R.J., and Mondragon A. (2001). Crystal structure of a complex of a type IA DNA topoisomerase with a single-stranded DNA molecule. Nature 411, 1077–1081.
Charvin G., Bensimon D., and Croquette V. (2003). Single-molecule study of DNA unlinking by eukaryotic and prokaryotic type-II topoisomerases. Proc. Natl. Acad. Sci. USA 100, 9820–9825.
Charvin G., Strick T.R., Bensimon D., and Croquette V. (2005a). Topoisomerase IV bends and overtwists DNA upon binding. Biophys. J. 89, 384–392.
Charvin G., Strick T.R., Bensimon D., and Croquette V. (2005b). Tracking topoisomerase activity at the single-molecule level. Ann. Rev. Biophys. Biomol. Struct. 34, 201–219.
Cherny D.I. and Jovin T.M. (2001). Electron and scanning force microscopy studies of alterations in supercoiled DNA tertiary structure. J. Mol. Biol. 313, 295–307.
Cloutier T.E. and Widom J. (2004). Spontaneous sharp bending of double-stranded DNA. Mol. Cell 14, 355–362.
Cloutier T.E. and Widom J. (2005). DNA twisting flexibility and the formation of sharply looped protein-DNA complexes. Proc. Natl. Acad. Sci. USA 102, 3645–3650.
Corbett K.D. and Berger J.M. (2004). Structure, molecular mechanisms, and evolutionary relationships in DNA topoisomerases. Ann. Rev. Biophys. Biomol. Struct. 33, 95–118.
Corbett K.D., Schoeffler A.J., Thomsen N.D., and Berger J.M. (2005). The structural basis for substrate specificity in DNA topoisomerase IV. J. Mol. Biol. 351, 545–561.
Corbett K.D., Shultzaberger R.K., and Berger J.M. (2004). The C-terminal domain of DNA gyrase A adopts a DNA-bending beta-pinwheel fold. Proc. Natl. Acad. Sci. USA 101, 7293–7298.
Cozzarelli N.R., Boles T.C., and White J.H. (1990). Primer on the topology and geometry of DNA supercoiling. In DNA topology and its biological effects. Cozzarelli N.R. and Wang, J.C. (eds.) Cold Spring Harbor Laboratory Press.
Crick F.H. and Klug A. (1975). Kinky helix. Nature 255, 530–533.
Crisona N.J. and Cozzarelli N.R. (2006). Alteration of Escherichia coli topoisomerase IV conformation upon enzyme binding to positively supercoiled DNA. J. Biol. Chem. 281, 18927–18932.
Crisona N.J., Strick T.R., Bensimon D., Croquette V., and Cozzarelli N.R. (2000). Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. Genes Dev. 14, 2881–2892.
Crooke E., Hwang D.S., Skarstad K., Thony B., and Kornberg A. (1991). E. coli minichromosome replication: regulation of initiation at oriC. Res. Microbiol. 142, 127–130.
Crothers D.M., Drak J., Kahn J.D., and Levene S.D. (1992). DNA bending, flexibility, and helical repeat by cyclization kinetics. Methods Enzymol. 212, 3–29.
Czapla L., Swigon D. and Olson W.K. (2006) Sequence-Dependent Effects in the Cyclization of Short DNA. J. Chem. Theory Comput. 2, 685–695.
Deibler R.W., Mann J.K., Sumners D.W.L., and Zechiedrich L. (2007). Hinmediated DNA knotting and recombination promote replicon dysfunction and mutation. BMC Mol. Biol. 8, 44
Dekker N.H., Rybenkov V.V., Duguet M., Crisona N.J., Cozzarelli N.R., Bensimon D., and Croquette V. (2002). The mechanism of type IA topoisomerases. Proc. Natl. Acad. Sci. USA 99, 12126–12131.
Deutsch J.M. (1988). Theoretical studies of DNA during gel electrophoresis. Science 240, 922–924.
Dickerson R.E. (1998). DNA bending: the prevalence of kinkiness and the virtues of normality. Nucleic Acids Res. 26, 1906–1926.
Dong K.C. and Berger J.M. (2007). Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450, 1201–1205.
Drake F.H., Hofmann G.A., Bartus H.F., Mattern M.R., Crooke S.T., and Mirabelli C.K. (1989). Biochemical and pharmacological properties of p170 and p180 forms of topoisomerase II. Biochemistry 28, 8154–8160.
Du Q., Kotlyar A., and Vologodskii A. (2008). Kinking the double helix by bending deformation. Nucleic Acids Res. 36, 1120–1128.
Du Q., Smith C., Shiffeldrim N., Vologodskaia M., and Vologodskii A. (2005). Cyclization of short DNA fragments and bending fluctuations of the double helix. Proc. Natl. Acad. Sci. USA 102, 5397–5402.
Dunaway M. and Dröge P. (1989). Transactivation of the Xenopus rRNA gene promoter by its enhancer. Nature 341, 657–659.
Drlica K., Malik M., Kerns R.J., Zhao X. (2008) Quinolone-mediated bacterial death. Antimicrob. Agents Chemother. 52, 385–392.
Embleton M.L., Vologodskii A.V., and Halford S.E. (2004). Dynamics of DNA loop capture by the SfiI restriction endonuclease on supercoiled and relaxed DNA. J. Mol. Biol. 339, 53–66.
Fogg J.M., Kolmakova N., Rees I., Magonov S., Hansma H., Perona J.J., and Zechiedrich E.L. (2006). Exploring writhe in supercoiled minicircle DNA. J. Phys: Condens. Matter 18, S145–S159.
Forterre P. (2006) DNA topoisomerase V: a new fold of mysterious origin. Trends Biotechnol. 24, 245–247.
Forterre P., Gribaldo S., Gadelle D., and Serre M.C. (2007) Origin and evolution of DNA topoisomerases. Biochimie. 89, 427–446.
Fujimoto B.S. and Schurr J.M. (1990). Dependence of the torsional rigidity of DNA on base composition. Nature 344, 175–178.
Fuller F.B. (1971). The writhing number of a space curve. Proc. Natl. Acad. Sci. USA 68, 815–819.
Fuller F.B. (1978). Decomposition of the linking of a closed ribbon: A problem of molecular biology. Proc. Natl. Acad. Sci. USA 75, 3557–3561.
Gellert M., Mizuuchi K., O’Dea M.H., and Nash H.A. (1976). DNA gyrase: An enzyme that introduces superhelical turns into DNA. Proc. Natl. Acad. Sci. USA 73, 3872–3876.
Gore J., Bryant Z., Nollmann M., Le M.U., Cozzarelli N.R., and Bustamante C. (2006). DNA overwinds when stretched. Nature 442, 836–839.
Gorin A.A, Zhurkin V.B., and Olson W.K. (1995) B-DNA twisting correlates with base-pair morphology. J. Mol. Biol. 247, 34–48.
Gowers D.M. and Halford S.E. (2003). Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J. 22, 1410–1418.
Grue P., Grasser A., Sehested M., Jensen P.B., Uhse A., Straub T., Ness W., and Boege F. (1998). Essential mitotic functions of DNA topoisomerase IIalpha are not adopted by topoisomerase IIbeta in human H69 cells. J. Biol. Chem. 273, 33660–33666.
Hagerman P.J. (1988). Flexibility of DNA. Ann. Rev. Biophys. Biophys. Chem. 17, 265–286.
Harris S.A., Laughton C.A., and Liverpool T.B. (2008). Mapping the phase diagram of the writhe of DNA nanocircles using atomistic molecular dynamics simulations. Nucleic Acids Res. 36, 21–29.
Harris S.A., Sands Z.A., and Laughton C.A. (2005). Molecular dynamics simulations of duplex stretching reveal the importance of entropy in determining the biomechanical properties of DNA. Biophys. J. 88, 1684–1691.
Heath P.J., Clendenning J.B., Fujimoto B.S., and Schurr J.M. (1996). Effect of bending strain on the torsion elastic constant of DNA. J. Mol. Biol. 260, 718–730.
Heck M.M. and Earnshaw W.C. (1986). Topoisomerase II: A specific marker for cell proliferation. J. Cell. Biol. 103, 2569–2581.
Hiasa H. and Marians K.J. (1996). Two distinct modes of topological processing during theta-type DNA replication. J. Biol. Chem. 271, 21529–21535.
Hiasa H., Yousef D.O., and Marians K.J. (1996). DNA strand cleavage is required for replication fork arrest by a frozen topoisomerase-quinolone-DNA ternary complex. J. Biol. Chem. 271, 26424–26429.
Hiller D.A., Rodriguez A.M., Perona J.J. Non-cognate enzyme-DNA complex: structural and kinetic analysis of EcoRV endonuclease bound to the EcoRI recognition site GAATTC. J. Mol. Biol. 354, 121–136.
Higgins N.P. and Cozzarelli N.R. (1982). The binding of gyrase to DNA: analysis by retention by nitrocellulose filters. Nucleic Acids Res. 10, 6833–6847.
Hopfield J.J. (1974). Kinetic proofreading: a new mechanism for reducing errors in biosynthetic processes requiring high specificity. Proc. Natl. Acad. Sci. USA 71, 4135–4139.
Horowitz D.S. and Wang J.C. (1984). Torsional rigidity of DNA and length dependence of the free energy of DNA supercoiling. J. Mol. Biol. 173, 75–91.
Keller W. and Wendel I. (1975). Stepwise relaxation of supercoiled SV40 DNA. Cold Spring Harbor Symposia on Quantitative Biology 39 (Part 1), 199–208.
Kikuchi A. and Asai K. (1984). Reverse gyrase–a topoisomerase which introduces positive superhelical turns into DNA. Nature 309, 677–681.
Kim J.L., Nikolov D.B., and Burley S.K. (1993a). Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature 365, 520–527.
Kim Y., Geiger J.H., Hahn S., and Sigler P.B. (1993b). Crystal structure of a yeast TBP/TATA-box complex. Nature 365, 512–520.
Kirkegaard K. and Wang J.C. (1985). Bacterial DNA topoisomerase I can relax positively supercoiled DNA containing a single-stranded loop. J. Mol. Biol. 185, 625–637.
Klenin K. and Langowski J. (2000). Computation of writhe in modeling of supercoiled DNA. Biopolymers 54, 307–317.
Klenin K., Langowski J., and Vologodskii A.V. (2002). Computational analysis of the chiral action of type II DNA topoisomerases. J. Mol. Biol. 320, 359–367.
Kondapi A.K., Mulpuri N., Mandraju R.K., Sasikaran B., and Subba Rao K. (2004) Analysis of age dependent changes of Topoisomerase II alpha and beta in rat brain. Int. J. Dev. Neurosci. 22, 19–30.
Koster D.A., Croquette V., Dekker C., Shuman S., and Dekker N.H. (2005). Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434, 671–674.
Koster D.A., Palle K., Bot E.S., Bjornsti M.A., Dekker N.H. (2007). Antitumour drugs impede DNA uncoiling by topoisomerase I. Nature. 448, 213–217.
Kramer P.R. and Sinden, R.R. (1997). Measurement of unrestrained negative supercoiling and topological domain size in living human cells. Biochemistry 36, 3151–3158.
Kreuzer K.N. and Alberts B.M. (1984). Site-specific recognition of bacteriophage T4 DNA by T4 type II DNA topoisomerase and Escherichia coli DNA gyrase. J. Biol. Chem. 259, 5339–5346.
Kreuzer K.N. and Cozzarelli N.R. (1979). Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J. Bacteriol. 140, 424–435.
Krogh S., Mortensen U.H., Westergaard O., and Bonven B.J. (1991). Eukaryotic topoisomerase I-DNA interaction is stabilized by helix curvature. Nucleic Acids Res. 19, 1235–1241.
LaMarr W.A., Sandman K.M., Reeve J.N., and Dedon P.C. (1997). Large scale preparation of positively supercoiled DNA using the archaeal histone HMf. Nucleic Acids Res. 25, 1660–1661.
Lankas F., Lavery R., and Maddocks J.H. (2006). Kinking occurs during molecular dynamics simulations of small DNA minicircles. Structure 14, 1527–1534.
Lee M.P., Sander M., and Hsieh T. (1989). Nuclease protection by Drosophila DNA topoisomerase II. Enzyme/DNA contacts at the strong topoisomerase II cleavage sites. J. Biol. Chem. 264, 21779–21787.
Leppard J.B. and Champoux J.J. (2005). Human DNA topoisomerase I: relaxation, roles, and damage control. Chromosoma 114, 75–85.
Levene S.D. and Crothers D.M. (1986). Topological distributions and the torsional rigidity of DNA. A Monte Carlo study of DNA circles. J. Mol. Biol. 189, 73–83.
Levitt M. (1983) Protein folding by restrained energy minimization and molecular dynamics. J. Mol. Biol. 170, 723–764.
Lewis M., Chang G., Horton N.C., Kercher M.A., Pace H.C., Schumacher M.A., Brennan R.G., and Lu P. (1996). Crystal structure of the lactose operon repressor and its complexes with DNA and inducer. Science 271, 1247–1254.
Lima C.D., Wang J.C., and Mondragon A. (1994). Three-dimensional structure of the 67 K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367, 138–146.
Lionnet T., Joubaud S., Lavery R., Bensimon D., and Croquette V. (2006). Wringing out DNA. Phys. Rev. Lett. 96, 178102.
Liu C.C., Burke R.L., Hibner U., Barry J., and Alberts B. (1979a). Probing DNA replication mechanisms with the T4 bacteriophage in vitro system. Cold Spring Harbor Symposia on Quantitative Biology 43 (Part 1), 469–487.
Liu D.J. and Day L.A. (1994). Pf1 virus structure: helical coat protein and DNA with paraxial phosphates. Science 265, 671–674.
Liu L.F., Liu C.C., and Alberts B.M. (1979b). T4 DNA topoisomerase: a new ATP-dependent enzyme essential for initiation of T4 bacteriophage DNA replication. Nature 281, 456–461.
Liu L.F. and Wang J.C. (1978). DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme. Cell 15, 979–984.
Liu L.F. and Wang J.C. (1987). Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84, 7024–7027.
Liu Z., Mann J.K., Zechiedrich E.L., and Chan H.S. (2006a). Topological information embodied in local juxtaposition geometry provides a statistical mechanical basis for unknotting by type-2 DNA topoisomerases. J. Mol. Biol. 361, 268–285.
Liu Z., Zechiedrich E.L., and Chan H.S. (2006b). Inferring global topology from local juxtaposition geometry: interlinking polymer rings and ramifications for topoisomerase action. Biophys. J. 90, 2344–2355.
Liu Z., Deibler R.W., Chan H.S., and Zechiedrich (2008). Hooked on DNA: the why and how of DNA untangling. Nucleic Acids Res. in press.
Liverpool T.B., Harris S.A., and Laughton C.A. (2008). Supercoiling and denaturation of DNA loops. Phys. Rev. Lett. 100, 238103.
Lockshon D. and Morris D.R. (1983). Positively supercoiled plasmid DNA is produced by treatment of Escherichia coli with DNA gyrase inhibitors. Nucleic Acids Res. 11, 2999–3017.
Luger K., Mader A.W., Richmond R.K., Sargent D.F., and Richmond T.J. (1997). Crystal structure of the nucleosome core particle at 2.8Å resolution. Nature 389, 251–260.
Lyubchenko Y.L. (2004). DNA structure and dynamics: an atomic force microscopy study. Cell Biochem. Biophys. 41, 75–98.
Madden K.R., Stewart L., and Champoux J.J. (1995). Preferential binding of human topoisomerase I to superhelical DNA. EMBO J. 14, 5399–5409.
Maher L.J., 3rd (1998). Mechanisms of DNA bending. Current Opin. Chem. Biol. 2, 688–694.
Maher L.J., 3rd (2006). DNA kinks available…if needed. Structure 14, 1479–1480.
Manning G.S. (1969a). Limiting laws and counterion condensation in polyelectrolyte solutions. I. Colligative properties. J. Chem. Phys. 51, 924–933.
Manning G.S. (1969b). Limiting laws and counterion condensation in polyelectrolyte solutions. II. Self-diffusion of the small ions. J. Chem. Phys. 51, 934–938.
Marko J.F. and Siggia E.D. (1994). Bending and Twisting Elasticity of DNA. Macromolecules 27, 981–988.
Martincic D. and Hande K.R. (2005). Topoisomerase II inhibitors. Cancer Chemother. Biol. Response Modif. 22, 101–121.
Marvin D.A., Spencer M., Wilkins M.H., and Hamilton L.D. (1958) A new configuration of deoxyribonucleic acid. Nature 182, 387–388.
McClellan J.A. and Lilley D.M. (1991). Structural alteration in alternating adenine-thymine sequences in positively supercoiled DNA. J. Mol. Biol. 219, 145–149.
McClendon A.K., Dickey J.S., and Osheroff N. (2006a). The geometry of DNA supercoils modulates topoisomerase-mediated DNA cleavage and enzyme response to anticancer drugs. Biochemistry. 45, 3040–3050.
McClendon A.K., Dickey J.S., and Osheroff N. (2006b). Ability of viral topoisomerase II to discern the handedness of supercoiled DNA: bimodal recognition of DNA geometry by type II enzymes. Biochemistry 45, 11674–11680.
McClendon A.K. and Osheroff N. (2007). DNA topoisomerase II, genotoxicity, and cancer. Mut. Res. 623, 83–97.
McClendon A.K., Rodriguez A.C., and Osheroff N. (2005). Human topoisomerase IIα rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. J. Biol. Chem. 280, 39337–39345.
Mizuuchi K., Gellert M., and Nash H.A. (1978). Involvement of supertwisted DNA in integrative recombination of bacteriophage lambda. J. Mol. Biol. 121, 375–392.
Mondragon A. and DiGate R. (1999). The structure of Escherichia coli DNA topoisomerase III. Structure 7, 1373–1383.
Muller M.T. (1985). Quantitation of eukaryotic topoisomerase I reactivity with DNA. Preferential cleavage of supercoiled DNA. Biochim. Biophys. Acta 824, 263–267.
Musgrave D., Zhang X., and Dinger M. (2002). Archaeal genome organization and stress responses: implications for the origin and evolution of cellular life. Astrobiology 2, 241–253.
Musgrave D.R., Sandman K.M., and Reeve J.N. (1991). DNA binding by the archaeal histone HMf results in positive supercoiling. Proc. Natl. Acad. Sci. USA 88, 10397–10401.
Ninio J. (1975). Kinetic amplification of enzyme discrimination. Biochimie 57, 587–595.
Nitiss J.L. (1998). Investigating the biological functions of DNA topoisomerases in eukaryotic cells. Biochim. Biophys. Acta. 1400, 63–81.
Nöllmann M., Crisona N.J., and Arimondo P.B. (2007). Thirty years of Escherichia coli DNA gyrase: from in vivo function to single-molecule mechanism. Biochimie 89, 490–499.
Nunes-Duby S.E., Smith-Mungo L.I., and Landy A. (1995). Single base-pair precision and structural rigidity in a small IHF-induced DNA loop. J. Mol. Biol. 253, 228–242.
Olson W.K. (1996). Simulating DNA at low resolution. Current Opin. Struct. Biol. 6, 242–256.
Olson W.K., Gorin A.A., Lu X.J., Hock L.M., and Zhurkin V.B. (1998). DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc. Natl. Acad. Sci. USA 95, 11163–11168.
Osheroff N. (1986). Eukaryotic topoisomerase II. Characterization of enzyme turnover. J. Biol. Chem. 261, 9944–9950.
Osheroff N. (1987). Role of the divalent cation in topoisomerase II mediated reactions. Biochemistry 26, 6402–6406.
Osheroff N., Shelton E.R., and Brutlag D.L. (1983). DNA topoisomerase II from Drosophila melanogaster. Relaxation of supercoiled DNA. J. Biol. Chem 258, 9536–9543.
Osheroff N. and Zechiedrich E.L. (1987). Calcium-promoted DNA cleavage by eukaryotic topoisomerase II: Trapping the covalent enzyme-DNA complex in an active form. Biochemistry 26, 4303–4309.
Pack G.R., Wong L., and Lamm G. (1999). Divalent cations and the electrostatic potential around DNA: Monte Carlo and Poisson-Boltzmann calculations. Biopolymers 49, 575–590.
Parvin J.D., McCormick R.J., Sharp P.A., and Fisher D.E. (1995). Pre-bending of a promoter sequence enhances affinity for the TATA-binding factor. Nature 373, 724–727.
Pauling L. and Corey R.B. (1953). A proposed structure for the nucleic acids. Proc. Natl. Acad. Sci. USA 39, 84–97.
Pavlicek J.W., Oussatcheva E.A., Sinden R.R., Potaman V.N., Sankey O.F., and Lyubchenko Y.L. (2004). Supercoiling-induced DNA bending. Biochemistry 43, 10664–10668.
Peng H. and Marians K. (1995). The interaction of Escherichia coli topoisomerase IV with DNA. J. Biol. Chem. 270, 25286–25290.
Pérez A., Lankas F., Luque F.J., Orozco M. (2008) Towards a molecular dynamics consensus view of B-DNA flexibility. Nucleic Acids Res. 36, 2379–2394.
Perry K. and Mondragon A. (2003). Structure of a complex between E. coli DNA topoisomerase I and single-stranded DNA. Structure 11, 1349–1358.
Pohl W.F. and Roberts G.W. (1978). Topological considerations in the theory of replication of DNA. J. Math. Biol. 6, 383–402.
Pommier Y. (2006). Topoisomerase I inhibitors: camptothecins and beyond. Nat. Rev. Cancer 6, 789–802.
Portugal J. and Rodriguez-Campos A. (1996). T7 RNA polymerase cannot transcribe through a highly knotted DNA template. Nucleic Acids Res. 24, 4890–4894.
Randall G.L., Pettitt B.M., Buck G., and Zechiedrich E.L. (2006). Electrostatics of DNA-DNA juxtapositions: consequences for type II topoisomerase function. J. Phys: Condens. Matter 18, S173–S185.
Redinbo M.R., Champoux J.J., and Hol W.G. (2000). Novel insights into catalytic mechanism from a crystal structure of human topoisomerase I in complex with DNA. Biochemistry 39, 6832–6840.
Redinbo M.R., Stewart L., Champoux J.J., and Hol W.G. (1999). Structural flexibility in human topoisomerase I revealed in multiple non-isomorphous crystal structures. J. Mol. Biol. 292, 685–696.
Redinbo M.R., Stewart L., Kuhn P., Champoux J.J., and Hol W.G. (1998). Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279, 1504–1513.
Reeve J.N., Sandman K., and Daniels C.J. (1997). Archaeal histones, nucleosomes, and transcription initiation. Cell 89, 999–1002.
Rice P.A., Yang S., Mizuuchi K., and Nash H.A. (1996). Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87, 1295–1306.
Richet E., Abcarian P., and Nash H.A. (1986). The interaction of recombination proteins with supercoiled DNA: defining the role of supercoiling in lambda integrative recombination. Cell 46, 1011–1021.
Rodley G.A., Scobie R.S., Bates R.H.T., and Lewitt R.M. (1976) A possible conformation for double-stranded polynucleotides. Proc. Natl. Acad. Sci. USA. 73, 2929–2963.
Rodriguez-Campos A. (1996). DNA knotting abolishes in vitro chromatin assembly. J. Biol. Chem. 271, 14150–14155.
Rodriguez A.C. (2002). Studies of a positive supercoiling machine. Nucleotide hydrolysis and a multifunctional “latch” in the mechanism of reverse gyrase. J. Biol. Chem. 277, 29865–29873.
Rybenkov V.V., Ullsperger C., Vologodskii A.V., and Cozzarelli N.R. (1997a). Simplification of DNA topology below equilibrium values by type II topoisomerases. Science 277, 690–693.
Rybenkov V.V., Vologodskii A.V., and Cozzarelli N.R. (1997b). The effect of ionic conditions on DNA helical repeat, effective diameter, and free energy of supercoiling. Nucleic Acids Res. 25, 1412–1418.
Saitta A.M., Soper P.D., Wasserman E., and Klein M.L. (1999). Influence of a knot on the strength of a polymer strand. Nature 399, 46–48.
Schoeffler A.J. and Berger J.M. (2005). Recent advances in understanding structure-function relationships in the type II topoisomerase mechanism. Biochem. Soc. Trans. 33, 1465–1470.
Schoeffler A.J. and Berger J.M. (2008). DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Quart. Rev. Biophys. 41, 41–101.
Schvartzman J.B. and Stasiak A. (2004). A topological view of the replicon. EMBO Rep. 5, 256–261.
Selvin P.R., Cook D.N., Pon N.G., Bauer W.R., Klein M.P., and Hearst J.E. (1992). Torsional rigidity of positively and negatively supercoiled DNA. Science 255, 82–85.
Shore D. and Baldwin R.L. (1983a). Energetics of DNA twisting. I. Relation between twist and cyclization probability. J. Mol. Biol. 170, 957–981.
Shore D. and Baldwin R.L. (1983b). Energetics of DNA twisting. II. Topoisomer analysis. J. Mol. Biol. 170, 983–1007.
Shore D., Langowski J., and Baldwin R.L. (1981). DNA flexibility studied by covalent closure of short fragments into circles. Proc. Natl. Acad. Sci USA 78, 4833–4837.
Sikorav J.L. and Jannink G. (1994). Kinetics of chromosome condensation in the presence of topoisomerases: a phantom chain model. Biophys. J. 66, 827–837.
Smith S.B., Finzi L., and Bustamante C. (1992). Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122–1126.
Snounou G. and Malcom A.D. (1983). Production of positively supercoiled DNA by netropsin. J. Mol. Biol. 167, 211–216.
Sperrazza J.M., Register J.C. 3rd., and Griffith J. (1984). Electron microscopy can be used to measure DNA supertwisting. Gene 31, 17–22.
Stewart L., Redinbo M.R., Qiu X., Hol W.G., and Champoux J.J. (1998). A model for the mechanism of human topoisomerase I. Science 279, 1534–1541.
Stivers J.T., Harris T.K., and Mildvan A.S. (1997). Vaccinia DNA topoisomerase I: evidence supporting a free rotation mechanism for DNA supercoil relaxation. Biochemistry 36, 5212–5222.
Stone M.D., Bryant Z., Crisona N.J., Smith S.B., Vologodskii A., Bustamante C., and Cozzarelli N.R. (2003). Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl. Acad. Sci. USA 100, 8654–8659.
Strick T.R., Allemand J.F., Bensimon D., Bensimon A., and Croquette V. (1996). The elasticity of a single supercoiled DNA molecule. Science 271, 1835–1837.
Strick T.R., Allemand J.F., Bensimon D., and Croquette V. (1998). Behavior of supercoiled DNA. Biophys. J. 74, 2016–2028.
Strick T.R., Allemand J.F., Bensimon D., and Croquette V. (2000a). Stress-induced structural transitions in DNA and proteins. Ann. Rev. Biophys. Biomol. Struct. 29, 523–543.
Strick T.R., Bensimon D., and Croquette V. (1999). Micro-mechanical measurement of the torsional modulus of DNA. Genetica 106, 57–62.
Strick T.R., Croquette V., and Bensimon D. (2000b). Single-molecule analysis of DNA uncoiling by a type II topoisomerase. Nature 404, 901–904.
Svozil D., Sponer J.E., Marchan I., Pérez A., Cheatham T.E. 3rd, Forti. F., Luque F.J., Orozco M., Sponer J. (2008) Geometrical and electronic structure variability of the sugar-phosphate backbone in nucleic acids. J. Phys. Chem. B 112, 8188–8197.
Taneja B., Patel A., Slesarev A., Mondragón A. (2006) Structure of the N-terminal fragment of topoisomerase V reveals a new family of topoisomerases. EMBO J. 25, 398–408.
Taneja B., Schnurr B., Slesarev A., Marko J.F., Mondragón A. (2007) Topoisomerase V relaxes supercoiled DNA by a constrained swiveling mechanism. Proc. Natl. Acad. Sci. USA. 104, 14670–14675.
Terry B.J., Jack W.E., and Modrich P. (1985). Facilitated diffusion during catalysis by EcoRI endonuclease. Nonspecific interactions in EcoRI catalysis. J. Biol. Chem. 260, 13130–13137.
Thomsen B., Bendixen C., Lund K., Andersen A.H., Sorensen B.S., and Westergaard O. (1990). Characterization of the interaction between topoisomerase II and DNA by transcriptional footprinting. J. Mol. Biol. 215, 237–244.
Timsit Y., Duplantier B., Jannink G., and Sikoravq J.-L. (1998). Symmetry and chirality in topoisomerases II-DNA crossover recognition. J. Mol. Biol. 284, 1289–1299.
Timsit Y. and Moras D. (1994). DNA self-fitting: the double helix directs the geometry of its supramolecular assembly. EMBO J. 13, 2737–2746.
Timsit Y., Shatzky-Schwartz M., and Shakked Z. (1999). Left-handed DNA crossovers. Implications for DNA-DNA recognition and structural alterations. J. Biomol. Struct. Dyn. 16, 775–785.
Tolstorukov M.Y., Colasanti A.V., McCandlish D.M., Olson W.K., Zhurkin V.B. (2007) A novel roll-and-slide mechanism of DNA folding in chromatin: implications for nucleosome positioning. J. Mol. Biol. 371, 725–738.
Travers A. and Muskhelishvili G. (2005). DNA supercoiling - a global transcriptional regulator for enterobacterial growth? Nat. Rev. Microbiol. 3, 157–169.
Trigueros S., Salceda J., Bermudez I., Fernandez X., and Roca J. (2004). Asymmetric removal of supercoils suggests how topoisomerase II simplifies DNA topology. J. Mol. Biol. 335, 723–731.
Ullsperger C. and Cozzarelli N.R. (1996). Contrasting enzymatic activities of topoisomerase IV and DNA gyrase from Escherichia coli. J. Biol. Chem. 271, 31549–31555.
Vinograd J. and Lebowitz J. (1966). Physical and topological properties of circular DNA. J. Gen. Physiol. 49, 103–125.
Vinograd J., Lebowitz J., Radloff R., Watson R., and Laipis P. (1965). The twisted circular form of polyoma viral DNA. Proc. Natl. Acad. Sci. USA 53, 1104–1111.
Vologodskii A.V. and Cozzarelli N.R. (1996). Effect of supercoiling on the juxtaposition and relative orientation of DNA sites. Biophys. J. 70, 2548–2556.
Vologodskii A.V., Levene S.D., Klenin K.V., Frank-Kamenetskii M., and Cozzarelli N.R. (1992). Conformational and thermodynamic properties of supercoiled DNA. J. Mol. Biol. 227, 1224–1243.
Vologodskii A.V., Lukashin A.V., Anshelevich V.V., and Frank-Kamenetskii M.D. (1979). Fluctuations in superhelical DNA. Nucleic Acids Res. 6, 967–982.
Vologodskii A.V., Zhang W., Rybenkov V.V., Podtelezhnikov A.A., Subramanian D., Griffith J.D., and Cozzarelli N.R. (2001). Mechanism of topology simplification by type II DNA topoisomerases. Proc. Natl. Acad. Sci. USA 98, 3045–3049.
von Hippel P.H. (2007). From “simple” DNA-protein interactions to the macromolecular machines of gene expression. Ann. Rev. Biophys. Biomol. Struct. 36, 79–105.
Wahle E. and Kornberg A. (1988). The partition locus of plasmid pSC101 is a specific binding site for DNA gyrase. EMBO J. 7, 1889–1895.
Wang G. and Vasquez K.M. (2006). Non-B DNA structure-induced genetic instability. Mut. Res. 598, 103–119.
Wang G. and Vasquez K.M. (2007). Z-DNA, an active element in the genome. Front. Biosci. 12, 4424–38.
Wang J.C. (1971). Interaction between DNA and an Escherichia coli protein ω. J. Mol. Biol. 55, 523–533.
Wang J.C. (1996). DNA topoisomerases. Annu. Rev. Biochem. 65, 635–692.
Wang J.C. (2002). Cellular roles of DNA topoisomerases: A molecular perspective. Nat. Rev. Mol. Cell Biol. 3, 430–440.
Watson J.D. and Crick F.H.C. (1953). Molecular structure of nucleic acids: A structure for deoxyribose nucleic acid. Nature 171, 737–738.
Weber C., Stasiak A., De Los Rios P., and Dietler G. (2006). Numerical simulation of gel electrophoresis of DNA knots in weak and strong electric fields. Biophys. J. 90, 3100–3105.
Wells R.D. (2007). Non-B DNA conformations, mutagenesis and disease. Trends Biochem. Sci. 32, 271–278.
Wells R.D., Dere R., Hebert M.L., Napierala M., and Son L.S. (2005). Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res. 33, 3785–3798.
White J.H. (1969). Self-linking and the Gauss integral in higher dimensions. Am. J. Math. 91, 693–728.
Whitson P.A., Hsieh W.T., Wells R.D., and Matthews K.S. (1987). Supercoiling facilitates lac operator-repressor-pseudooperator interactions. J. Biol. Chem. 262, 4943–4946.
Wolters Kluwer Health, Pharmaceutical Audit Suite (PHAST), January to December 2006.
Xu Y.C. and Bremer H. (1997). Winding of the DNA helix by divalent metal ions. Nucleic Acids Res. 25, 4067–4071.
Yan J., Magnasco M.O., and Marko J.F. (1999). A kinetic proofreading mechanism for disentanglement of DNA by topoisomerases. Nature 401, 932–935.
Yan J., Magnasco M.O., and Marko J.F. (2001). Kinetic proofreading can explain the supression of supercoiling of circular DNA molecules by type-II topoisomerases. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 63, 031909.
Yin H., Wang M.D., Svoboda K., Landick R., Block S.M., and Gelles J. (1995). Transcription against an applied force. Science 270, 1653–1657.
Zechiedrich E.L. and Cozzarelli N.R. (1995). Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. Genes Dev. 9, 2859–2869.
Zechiedrich E.L., Khodursky A.B., Bachellier S., Schneider R., Chen D., Lilley D.M., and Cozzarelli N.R. (2000). Roles of topoisomerases in maintaining steady-state DNA supercoiling in Escherichia coli. J. Biol. Chem. 275, 8103–8113.
Zechiedrich E.L., Khodursky A.B., and Cozzarelli N.R. (1997). Topoisomerase IV, not gyrase, decatenates products of site-specific recombination in Escherichia coli. Genes Dev. 11, 2580–2592.
Zechiedrich E.L. and Osheroff N. (1990). Eukaryotic topoisomerases recognize nucleic acid topology by preferentially interacting with DNA crossovers. EMBO J. 9, 4555–4562.
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Fogg, J.M., Catanese, D.J., Randall, G.L., Swick, M.C., Zechiedrich, L. (2009). Differences Between Positively and Negatively Supercoiled DNA that Topoisomerases May Distinguish. In: Benham, C., Harvey, S., Olson, W., Sumners, D., Swigon, D. (eds) Mathematics of DNA Structure, Function and Interactions. The IMA Volumes in Mathematics and its Applications, vol 150. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0670-0_5
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