Activities of gyrase and topoisomerase IV on positively supercoiled DNA

Abstract Although bacterial gyrase and topoisomerase IV have critical interactions with positively supercoiled DNA, little is known about the actions of these enzymes on overwound substrates. Therefore, the abilities of Bacillus anthracis and Escherichia coli gyrase and topoisomerase IV to relax and cleave positively supercoiled DNA were analyzed. Gyrase removed positive supercoils ∼10-fold more rapidly and more processively than it introduced negative supercoils into relaxed DNA. In time-resolved single-molecule measurements, gyrase relaxed overwound DNA with burst rates of ∼100 supercoils per second (average burst size was 6.2 supercoils). Efficient positive supercoil removal required the GyrA-box, which is necessary for DNA wrapping. Topoisomerase IV also was able to distinguish DNA geometry during strand passage and relaxed positively supercoiled substrates ∼3-fold faster than negatively supercoiled molecules. Gyrase maintained lower levels of cleavage complexes with positively supercoiled (compared with negatively supercoiled) DNA, whereas topoisomerase IV generated similar levels with both substrates. Results indicate that gyrase is better suited than topoisomerase IV to safely remove positive supercoils that accumulate ahead of replication forks. They also suggest that the wrapping mechanism of gyrase may have evolved to promote rapid removal of positive supercoils, rather than induction of negative supercoils.

[1]  D. Klostermeier,et al.  DNA gyrase with a single catalytic tyrosine can catalyze DNA supercoiling by a nicking-closing mechanism , 2016, Nucleic acids research.

[2]  Aakash Basu,et al.  Structural Dynamics and Mechanochemical Coupling in DNA Gyrase. , 2016, Journal of molecular biology.

[3]  N. Osheroff,et al.  Fluoroquinolone interactions with Mycobacterium tuberculosis gyrase: Enhancing drug activity against wild-type and resistant gyrase , 2016, Proceedings of the National Academy of Sciences.

[4]  D. Sherratt,et al.  The Localization and Action of Topoisomerase IV in Escherichia coli Chromosome Segregation Is Coordinated by the SMC Complex, MukBEF , 2015, Cell reports.

[5]  G. Jacoby,et al.  Mechanisms of drug resistance: quinolone resistance , 2015, Annals of the New York Academy of Sciences.

[6]  N. Osheroff,et al.  Catalytic Core of Human Topoisomerase IIα: Insights into Enzyme–DNA Interactions and Drug Mechanism , 2014, Biochemistry.

[7]  N. Osheroff,et al.  Role of the Water–Metal Ion Bridge in Mediating Interactions between Quinolones and Escherichia coli Topoisomerase IV , 2014, Biochemistry.

[8]  D. Klostermeier,et al.  The mechanism of negative DNA supercoiling: a cascade of DNA-induced conformational changes prepares gyrase for strand passage. , 2014, DNA Repair.

[9]  N. Osheroff,et al.  Mechanism of Quinolone Action and Resistance , 2014, Biochemistry.

[10]  D. Bates,et al.  Regulation of Sister Chromosome Cohesion by the Replication Fork Tracking Protein SeqA , 2013, PLoS genetics.

[11]  Patrick Schultz,et al.  Structural insight into negative DNA supercoiling by DNA gyrase, a bacterial type 2A DNA topoisomerase , 2013, Nucleic acids research.

[12]  Ronald J. Baskin,et al.  DNA Unwinding Heterogeneity by RecBCD Results from Static Molecules Able to Equilibrate , 2013, Nature.

[13]  N. Osheroff,et al.  Chiral Discrimination and Writhe-dependent Relaxation Mechanism of Human Topoisomerase IIα*♦ , 2013, The Journal of Biological Chemistry.

[14]  C. Dekker,et al.  Dynamics of DNA Supercoils , 2012, Science.

[15]  Sandra J. Aedo,et al.  Isolation and Quantitation of Topoisomerase Complexes Accumulated on Escherichia coli Chromosomal DNA , 2012, Antimicrobial Agents and Chemotherapy.

[16]  D. Dunlap,et al.  Physiological levels of salt and polyamines favor writhe and limit twist in DNA. , 2012, Macromolecules.

[17]  S. Neukirch,et al.  Competition between curls and plectonemes near the buckling transition of stretched supercoiled DNA. , 2012, Physical review. E, Statistical, nonlinear, and soft matter physics.

[18]  N. Osheroff,et al.  Drug interactions with Bacillus anthracis topoisomerase IV: biochemical basis for quinolone action and resistance. , 2012, Biochemistry.

[19]  B. Schmidt,et al.  All tangled up: how cells direct, manage and exploit topoisomerase function , 2011, Nature Reviews Molecular Cell Biology.

[20]  Y. Timsit.  Local sensing of global DNA topology: from crossover geometry to type II topoisomerase processivity , 2011, Nucleic acids research.

[21]  Ashley H. Hardin,et al.  Direct measurement of DNA bending by type IIA topoisomerases: implications for non-equilibrium topology simplification , 2011, Nucleic acids research.

[22]  M. Bjornsti,et al.  Cellular Strategies for Regulating DNA Supercoiling: A Single-Molecule Perspective , 2010, Cell.

[23]  C. Turnbough,et al.  Characterization of the Enzymes Encoded by the Anthrose Biosynthetic Operon of Bacillus anthracis , 2010, Journal of bacteriology.

[24]  M. Palumbo,et al.  In front of and behind the replication fork: bacterial type IIA topoisomerases , 2010, Cellular and Molecular Life Sciences.

[25]  Xilin Zhao,et al.  Quinolones: Action and Resistance Updated , 2009, Current topics in medicinal chemistry.

[26]  K. Neuman,et al.  Mechanisms of chiral discrimination by topoisomerase IV , 2009, Proceedings of the National Academy of Sciences.

[27]  H. Chan,et al.  The why and how of DNA unlinking , 2009, Nucleic acids research.

[28]  N. Osheroff,et al.  Bimodal recognition of DNA geometry by human topoisomerase II alpha: preferential relaxation of positively supercoiled DNA requires elements in the C-terminal domain. , 2008, Biochemistry.

[29]  N. Osheroff,et al.  The DNA cleavage reaction of topoisomerase II: wolf in sheep's clothing , 2008, Nucleic acids research.

[30]  N. Ribeck,et al.  Multiplexed single-molecule measurements with magnetic tweezers. , 2008, The Review of scientific instruments.

[31]  D. Sherratt,et al.  Modulation of Escherichia coli sister chromosome cohesion by topoisomerase IV. , 2008, Genes & development.

[32]  Michael D. Stone,et al.  Multiple modes of Escherichia coli DNA gyrase activity revealed by force and torque , 2007, Nature Structural &Molecular Biology.

[33]  N. Osheroff,et al.  Ability of viral topoisomerase II to discern the handedness of supercoiled DNA: bimodal recognition of DNA geometry by type II enzymes. , 2006, Biochemistry.

[34]  Tsai-Kun Li,et al.  Distribution of gyrase and topoisomerase IV on bacterial nucleoid: implications for nucleoid organization , 2006, Nucleic acids research.

[35]  P. Graumann,et al.  Differential and Dynamic Localization of Topoisomerases in Bacillus subtilis , 2006, Journal of bacteriology.

[36]  N. Osheroff,et al.  The geometry of DNA supercoils modulates topoisomerase-mediated DNA cleavage and enzyme response to anticancer drugs. , 2006, Biochemistry.

[37]  H. Hiasa,et al.  The “GyrA-box” Is Required for the Ability of DNA Gyrase to Wrap DNA and Catalyze the Supercoiling Reaction* , 2006, Journal of Biological Chemistry.

[38]  Michael D. Stone,et al.  Mechanochemical analysis of DNA gyrase using rotor bead tracking , 2006, Nature.

[39]  N. Osheroff,et al.  Human topoisomerase IIalpha rapidly relaxes positively supercoiled DNA: implications for enzyme action ahead of replication forks. , 2005, The Journal of biological chemistry.

[40]  J. Berger,et al.  The structural basis for substrate specificity in DNA topoisomerase IV. , 2005, Journal of molecular biology.

[41]  L. Gutmann,et al.  Activities of Different Fluoroquinolones against Bacillus anthracis Mutants Selected In Vitro and Harboring Topoisomerase Mutations , 2004, Antimicrobial Agents and Chemotherapy.

[42]  J. Schvartzman,et al.  A topological view of the replicon , 2004, EMBO reports.

[43]  Michael D. Stone,et al.  Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  L. Price,et al.  In Vitro Selection and Characterization of Bacillus anthracis Mutants with High-Level Resistance to Ciprofloxacin , 2003, Antimicrobial Agents and Chemotherapy.

[45]  A. C. Rodríguez,et al.  Studies of a Positive Supercoiling Machine , 2002, The Journal of Biological Chemistry.

[46]  JAMES C. Wang,et al.  Cellular roles of DNA topoisomerases: a molecular perspective , 2002, Nature Reviews Molecular Cell Biology.

[47]  Anthony Maxwell,et al.  Identification of four GyrA residues involved in the DNA breakage-reunion reaction of DNA gyrase. , 2002, Journal of molecular biology.

[48]  I. Brook,et al.  In vitro resistance of Bacillus anthracis Sterne to doxycycline, macrolides and quinolones. , 2001, International journal of antimicrobial agents.

[49]  N. Cozzarelli,et al.  Mechanism of topology simplification by type II DNA topoisomerases , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[50]  N. L. Williams,et al.  Locking the ATP-operated clamp of DNA gyrase: probing the mechanism of strand passage. , 2001, Journal of molecular biology.

[51]  N. Osheroff,et al.  Type II topoisomerases as targets for quinolone antibacterials: turning Dr. Jekyll into Mr. Hyde. , 2001, Current pharmaceutical design.

[52]  N. Cozzarelli,et al.  Preferential relaxation of positively supercoiled DNA by E. coli topoisomerase IV in single-molecule and ensemble measurements. , 2000, Genes & development.

[53]  N R Cozzarelli,et al.  Analysis of topoisomerase function in bacterial replication fork movement: use of DNA microarrays. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[54]  D. Hooper,et al.  Selective Targeting of Topoisomerase IV and DNA Gyrase in Staphylococcus aureus: Different Patterns of Quinolone- Induced Inhibition of DNA Synthesis , 2000, Antimicrobial Agents and Chemotherapy.

[55]  A. Khodursky,et al.  Roles of Topoisomerases in Maintaining Steady-state DNA Supercoiling in Escherichia coli * , 2000, The Journal of Biological Chemistry.

[56]  A. Maxwell,et al.  A model for the mechanism of strand passage by DNA gyrase. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[57]  L. Fisher,et al.  Streptococcus pneumoniae DNA Gyrase and Topoisomerase IV: Overexpression, Purification, and Differential Inhibition by Fluoroquinolones , 1999, Antimicrobial Agents and Chemotherapy.

[58]  H. Hiasa,et al.  DNA gyrase and topoisomerase IV: biochemical activities, physiological roles during chromosome replication, and drug sensitivities. , 1998, Biochimica et biophysica acta.

[59]  B. Peter,et al.  The Structure of Supercoiled Intermediates in DNA Replication , 1998, Cell.

[60]  T. Strick,et al.  Behavior of supercoiled DNA. , 1998, Biophysical journal.

[61]  L. Fisher,et al.  Targeting of DNA gyrase in Streptococcus pneumoniae by sparfloxacin: selective targeting of gyrase or topoisomerase IV by quinolones , 1997, Antimicrobial agents and chemotherapy.

[62]  A. Maxwell,et al.  Conversion of DNA gyrase into a conventional type II topoisomerase. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[63]  N. Cozzarelli,et al.  Contrasting Enzymatic Activities of Topoisomerase IV and DNA Gyrase from Escherichia coli* , 1996, The Journal of Biological Chemistry.

[64]  J. Ambler,et al.  Involvement of topoisomerase IV and DNA gyrase as ciprofloxacin targets in Streptococcus pneumoniae , 1996, Antimicrobial agents and chemotherapy.

[65]  A. Khodursky,et al.  Topoisomerase IV is a target of quinolones in Escherichia coli. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[66]  N. Cozzarelli,et al.  Roles of topoisomerase IV and DNA gyrase in DNA unlinking during replication in Escherichia coli. , 1995, Genes & development.

[67]  H. Hiasa,et al.  Topoisomerase IV can support oriC DNA replication in vitro. , 1994, The Journal of biological chemistry.

[68]  W. L. Fangman,et al.  A question of time: Replication origins of eukaryotic chromosomes , 1992, Cell.

[69]  M Frank-Kamenetskii,et al.  Conformational and thermodynamic properties of supercoiled DNA. , 1992, Journal of molecular biology.

[70]  R. J. Reece,et al.  The C-terminal domain of the Escherichia coli DNA gyrase A subunit is a DNA-binding protein. , 1991, Nucleic acids research.

[71]  H. Niki,et al.  New topoisomerase essential for chromosome segregation in E. coli , 1990, Cell.

[72]  A D Bates,et al.  DNA gyrase can supercoil DNA circles as small as 174 base pairs. , 1989, The EMBO journal.

[73]  Leroy F. Liu,et al.  Transcription generates positively and negatively supercoiled domains in the template , 1988, Cell.

[74]  J. Wang,et al.  Supercoiling of the DNA template during transcription. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[75]  K. Marians.  DNA gyrase-catalyzed decatenation of multiply linked DNA dimers. , 1987, The Journal of biological chemistry.

[76]  N. Cozzarelli,et al.  A simple topological method for describing stereoisomers of DNA catenanes and knots. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[77]  P. Brown,et al.  A sign inversion mechanism for enzymatic supercoiling of DNA. , 1979, Science.

[78]  M. Gellert,et al.  DNA gyrase: subunit structure and ATPase activity of the purified enzyme. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[79]  Leroy F. Liu,et al.  DNA-DNA gyrase complex: the wrapping of the DNA duplex outside the enzyme , 1978, Cell.

[80]  J. Wang,et al.  Micrococcus luteus DNA gyrase: active components and a model for its supercoiling of DNA. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[81]  N. Cozzarelli,et al.  Purification of subunits of Escherichia coli DNA gyrase and reconstitution of enzymatic activity. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[82]  H. Bernstein,et al.  DNA elongation rates and growing point distributions of wild-type phage T4 and a DNA-delay amber mutant. , 1976, Journal of molecular biology.

[83]  K. Neuman,et al.  Single-molecule measurements of topoisomerase activity with magnetic tweezers. , 2011, Methods in molecular biology.

[84]  D. J. Clarke,et al.  DNA Topoisomerases , 2009, Methods in Molecular Biology™.

[85]  J. Champoux.  DNA topoisomerases: structure, function, and mechanism. , 2001, Annual review of biochemistry.

[86]  L. Liu,et al.  Tumor cell death induced by topoisomerase-targeting drugs. , 2001, Annual review of pharmacology and toxicology.

[87]  L. Liu,et al.  Topoisomerase-targeting antitumor drugs: mechanisms of cytotoxicity and resistance. , 1992, Important advances in oncology.

[88]  F. Crick,et al.  Supercoiled DNA. , 1980, Scientific American.