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Review Article

Topoisomerases and site-specific recombinases: similarities in structure and mechanism

Pages 520-534 | Received 30 Jun 2010, Accepted 02 Aug 2010, Published online: 18 Nov 2010

References

  • Allemand F, Mathy N, Brechemier-Baey D and Condon C. 2005. The 5S rRNA maturase, ribonuclease M5, is a Toprim domain family member. Nucleic Acids Res 33:4368–4376.
  • Aravind L, Leipe DD and 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.
  • Arnold PH, Blake DG, Grindley ND, Boocock MR and Stark WM. 1999. Mutants of Tn3 resolvase which do not require accessory binding sites for recombination activity. EMBO J 18:1407–1414.
  • Artymiuk PJ, Ceska TA, Suck D and Sayers JR. 1997. Prokaryotic 5′-3′ exonucleases share a common core structure with gamma-delta resolvase. Nucleic Acids Res 25:4224–4229.
  • Balendiran GK. 2009. Fibrates in the chemical action of daunorubicin. Curr Cancer Drug Targets 9:366–369.
  • Bates AD and Maxwell A. 1997. DNA topology: topoisomerases keep it simple. Curr Biol 7:R778–781.
  • Bates AD and Maxwell A. 2010. The role of ATP in the reactions of type II DNA topoisomerases. Biochem Soc Trans 38:438–442.
  • Benjamin HW and Cozzarelli NR. 1988. Isolation and characterization of the Tn3 resolvase synaptic intermediate. EMBO J 7:1897–1905.
  • Benjamin HW and Cozzarelli NR. 1990. Geometric arrangements of Tn3 resolvase sites. J Biol Chem 265:6441–6447.
  • Berger JM, Gamblin SJ, Harrison SC and Wang JC. 1996. Structure and mechanism of DNA topoisomerase II. Nature 379:225–232.
  • Biswas T, Aihara H, Radman-Livaja M, Filman D, Landy A and Ellenberger T. 2005. A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 435:1059–1066.
  • Boocock MR, Zhu X and Grindley ND. 1995. Catalytic residues of gamma delta resolvase act in cis. EMBO J 14:5129–5140.
  • Burke ME, Arnold PH, He J, Wenwieser SV, Rowland SJ, Boocock MR and Stark WM. 2004. Activating mutations of Tn3 resolvase marking interfaces important in recombination catalysis and its regulation. Mol Microbiol 51:937–948.
  • Burrus V, Marrero J and Waldor MK. 2006. The current ICE age: biology and evolution of SXT-related integrating conjugative elements. Plasmid 55:173–183.
  • Campbell A. 2007. Phage integration and chromosome structure. A personal history. Annu Rev Genet 41:1–11.
  • Castell SE, Jordan SL and Halford SE. 1986. Site-specific recombination and topoisomerization by Tn21 resolvase: role of metal ions. Nucleic Acids Res 14:7213–7226.
  • Champoux JJ. 1977. Strand breakage by the DNA untwisting enzyme results in covalent attachment of the enzyme to DNA. Proc Natl Acad Sci USA 74:3800–3804.
  • Champoux JJ. 2001. DNA topoisomerases: structure, function, and mechanism. Annu Rev Biochem 70:369–413.
  • Changela A, DiGate RJ 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.
  • Chen Y and Rice PA. 2003a. New insight into site-specific recombination from Flp recombinase-DNA structures. Annu Rev Biophys Biomol Struct 32:135–159.
  • Chen Y and Rice PA. 2003b. The role of the conserved Trp330 in Flp-mediated recombination. Functional and structural analysis. J Biol Chem 278:24800–24807.
  • Chen Y, Narendra U, Iype LE, Cox MM and Rice PA. 2000. Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol Cell 6:885–897.
  • Cheng C, Kussie P, Pavletich N and Shuman S. 1998. Conservation of structure and mechanism between eukaryotic topoisomerase I and site-specific recombinases. Cell 92:841–850.
  • Confalonieri F, Elie C, Nadal M, de La Tour C, Forterre P and 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.
  • Crick FH. 1976. Linking numbers and nucleosomes. Proc Natl Acad Sci USA 73:2639–2643.
  • Dhar G, Sanders ER and Johnson RC. 2004. Architecture of the hin synaptic complex during recombination: the recombinase subunits translocate with the DNA strands. Cell 119:33–45.
  • Dhar G, Heiss JK and Johnson RC. 2009. Mechanical constraints on Hin subunit rotation imposed by the Fis/enhancer system and DNA supercoiling during site-specific recombination. Mol Cell 34:746–759.
  • Domanico PL and Tse-Dinh YC. 1991. Mechanistic studies on E. coli DNA topoisomerase I: divalent ion effects. J Inorg Biochem 42:87–96.
  • Dong KC and Berger JM. 2007. Structural basis for gate-DNA recognition and bending by type IIA topoisomerases. Nature 450:1201–1205.
  • Forterre P, Gribaldo S, Gadelle D and Serre MC. 2007. Origin and evolution of DNA topoisomerases. Biochimie 89:427–446.
  • Gehman JD, Cocco MJ and Grindley ND. 2008. Chemical shift mapping of gammadelta resolvase dimer and activated tetramer: mechanistic implications for DNA strand exchange. Biochim Biophys Acta 1784:2086–2092.
  • Ghosh P, Kim AI and Hatfull GF. 2003. The orientation of mycobacteriophage Bxb1 integration is solely dependent on the central dinucleotide of attP and attB. Mol Cell 12:1101–1111.
  • Gibb B, Gupta K, Ghosh K, Sharp R, Chen J and Van Duyne GD. 2010. Requirements for catalysis in the Cre recombinase active site. Nucleic Acids Res 38:5817–5832.
  • Grindley ND. 1993. Analysis of a nucleoprotein complex: the synaptosome of gamma delta resolvase. Science 262:738–740.
  • Grindley ND, Whiteson KL and Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75:567–605.
  • Guo F, Gopaul DN and van Duyne GD. 1997. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389:40–46.
  • Hickman AB, Waninger S, Scocca JJ and Dyda F. 1997. Molecular organization in site-specific recombination: the catalytic domain of bacteriophage HP1 integrase at 2.7 A resolution. Cell 89:227–237.
  • Hickman AB, Chandler M and Dyda F. 2010. Integrating prokaryotes and eukaryotes: DNA transposases in light of structure. Crit Rev Biochem Mol Biol 45:50–69.
  • Hughes RE, Rice PA, Steitz TA and Grindley ND. 1993. Protein–protein interactions directing resolvase site-specific recombination: a structure-function analysis. EMBO J 12:1447–1458.
  • Jayaram M, Mehta S, Uzri D, Voziyanov Y and Velmurugan S. 2004. Site-specific recombination and partitioning systems in the stable high copy propagation of the 2-micron yeast plasmid. Prog Nucleic Acid Res Mol Biol 77:127–172.
  • Johnson RC, Bruist MF and Simon MI. 1986. Host protein requirements for in vitro site-specific DNA inversion. Cell 46:531–539.
  • Kamtekar S, Ho RS, Cocco MJ, Li W, Wenwieser SV, Boocock MR, Grindley ND and Steitz TA. 2006. Implications of structures of synaptic tetramers of gamma delta resolvase for the mechanism of recombination. Proc Natl Acad Sci USA 103:10642–10647.
  • Kanaar R, van de Putte P and Cozzarelli NR. 1988. Gin-mediated DNA inversion: product structure and the mechanism of strand exchange. Proc Natl Acad Sci USA 85:752–756.
  • Kato M, Ito T, Wagner G, Richardson CC and Ellenberger T. 2003. Modular architecture of the bacteriophage T7 primase couples RNA primer synthesis to DNA synthesis. Mol Cell 11:1349–1360.
  • Keck JL, Roche DD, Lynch AS and Berger JM. 2000. Structure of the RNA polymerase domain of E. coli primase. Science 287:2482–2486.
  • Kim AI, Ghosh P, Aaron MA, Bibb LA, Jain S and Hatfull GF. 2003. Mycobacteriophage Bxb1 integrates into the Mycobacterium smegmatis groEL1 gene. Mol Microbiol 50:463–473.
  • Koster DA, Croquette V, Dekker C, Shuman S and Dekker NH. 2005. Friction and torque govern the relaxation of DNA supercoils by eukaryotic topoisomerase IB. Nature 434:671–674.
  • Kreuzer KN and Cozzarelli NR. 1980. Formation and resolution of DNA catenanes by DNA gyrase. Cell 20:245–254.
  • Krogh BO and Shuman S. 2000. Catalytic mechanism of DNA topoisomerase IB. Mol Cell 5:1035–1041.
  • Kwon HJ, Tirumalai R, Landy A and Ellenberger T. 1997. Flexibility in DNA recombination: structure of the lambda integrase catalytic core. Science 276:126–131.
  • Laponogov I, Pan XS, Veselkov DA, McAuley KE, Fisher LM and Sanderson MR. Structural basis of gate-DNA breakage and resealing by type II topoisomerases. PLoS One 5:e11338.
  • Leschziner AE and Grindley ND. 2003. The architecture of the gammadelta resolvase crossover site synaptic complex revealed by using constrained DNA substrates. Mol Cell 12:775–781.
  • Li W, Kamtekar S, Xiong Y, Sarkis GJ, Grindley ND and Steitz TA. 2005. Structure of a synaptic gammadelta resolvase tetramer covalently linked to two cleaved DNAs. Science 309:1210–1215.
  • Liebert CA, Hall RM and Summers AO. 1999. Transposon Tn21, flagship of the floating genome. Microbiol Mol Biol Rev 63:507–522.
  • Lima CD, Wang JC and Mondragon A. 1994. Three-dimensional structure of the 67K N-terminal fragment of E. coli DNA topoisomerase I. Nature 367:138–146.
  • Liu LF, Liu CC and 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.
  • MacDonald D, Demarre G, Bouvier M, Mazel D and Gopaul DN. 2006. Structural basis for broad DNA-specificity in integron recombination. Nature 440:1157–1162.
  • Maxwell A and Lawson DM. 2003. The ATP-binding site of type II topoisomerases as a target for antibacterial drugs. Curr Top Med Chem 3:283–303.
  • McIlwraith MJ, Boocock MR and Stark WM. 1996. Site-specific recombination by Tn3 resolvase, photocrosslinked to its supercoiled DNA substrate. J Mol Biol 260:299–303.
  • McIlwraith MJ, Boocock MR and Stark WM. 1997. Tn3 resolvase catalyses multiple recombination events without intermediate rejoining of DNA ends. J Mol Biol 266:108–121.
  • Merickel SK, Haykinson MJ and Johnson RC. 1998. Communication between Hin recombinase and Fis regulatory subunits during coordinate activation of Hin-catalyzed site-specific DNA inversion. Genes Dev 12:2803–2816.
  • Merickel SK and Johnson RC. 2004. Topological analysis of Hin-catalysed DNA recombination in vivo and in vitro. Mol Microbiol 51:1143–1154.
  • Minkah N, Hwang Y, Perry K, Van Duyne GD, Hendrickson R, Lefkowitz EJ, Hannenhalli S and Bushman FD. 2007. Variola virus topoisomerase: DNA cleavage specificity and distribution of sites in Poxvirus genomes. Virology 365:60–69.
  • Mondragon A and DiGate R. 1999. The structure of Escherichia coli DNA topoisomerase III. Structure 7:1373–1383.
  • Mouw KW, Rowland SJ, Gajjar MM, Boocock MR, Stark WM and Rice PA. 2008. Architecture of a serine recombinase-DNA regulatory complex. Mol Cell 30:145–155.
  • Murley LL and Grindley ND. 1998. Architecture of the gamma delta resolvase synaptosome: oriented heterodimers identity interactions essential for synapsis and recombination. Cell 95:553–562.
  • Nash HA. 1981. Integration and excision of bacteriophage lambda: the mechanism of conservation site specific recombination. Annu Rev Genet 15:143–167.
  • Newman BJ and Grindley ND. 1984. Mutants of the gamma delta resolvase: a genetic analysis of the recombination function. Cell 38:463–469.
  • Nollmann M, He J, Byron O and Stark WM. 2004. Solution structure of the Tn3 resolvase-crossover site synaptic complex. Mol Cell 16:127–137.
  • Olorunniji FJ and Stark WM. 2010. Catalysis of site-specific recombination by Tn3 resolvase. Biochem Soc Trans 38:417–421.
  • Perry K, Hwang Y, Bushman FD and Van Duyne GD. 2006. Structural basis for specificity in the poxvirus topoisomerase. Mol Cell 23:343–354.
  • Perry K, Hwang Y, Bushman FD and Van Duyne GD. 2010. Insights from the structure of a smallpox virus topoisomerase-DNA transition state mimic. Structure 18:127–137.
  • Radman-Livaja M, Biswas T, Ellenberger T, Landy A and Aihara H. 2006. DNA arms do the legwork to ensure the directionality of lambda site-specific recombination. Curr Opin Struct Biol 16:42–50.
  • Redinbo MR, Stewart L, Kuhn P, Champoux JJ and Hol WG. 1998. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279:1504–1513.
  • Reed RR and Grindley ND. 1981. Transposon-mediated site-specific recombination in vitro: DNA cleavage and protein–DNA linkage at the recombination site. Cell 25:721–728.
  • Rezacova P, Borek D, Moy SF, Joachimiak A and Otwinowski Z. 2008. Crystal structure and putative function of small Toprim domain-containing protein from Bacillus stearothermophilus. Proteins 70:311–319.
  • Rice PA and Steitz TA. 1994. Model for a DNA-mediated synaptic complex suggested by crystal packing of gamma delta resolvase subunits. EMBO J 13:1514–1524.
  • Rowland SJ, Stark WM and Boocock MR. 2002. Sin recombinase from Staphylococcus aureus: synaptic complex architecture and transposon targeting. Mol Microbiol 44:607–619.
  • Rowland SJ, Boocock MR, McPherson AL, Mouw KW, Rice PA and Stark WM. 2009. Regulatory mutations in Sin recombinase support a structure-based model of the synaptosome. Mol Microbiol 74:282–298.
  • Sanders ER and Johnson RC. 2004. Stepwise dissection of the Hin-catalyzed recombination reaction from synapsis to resolution. J Mol Biol 340:753–766.
  • Sanderson MR, Freemont PS, Rice PA, Goldman A, Hatfull GF, Grindley ND and Steitz TA. 1990. The crystal structure of the catalytic domain of the site-specific recombination enzyme gamma delta resolvase at 2.7 A resolution. Cell 63:1323–1329.
  • Sarkis GJ, Murley LL, Leschziner AE, Boocock MR, Stark WM and Grindley ND. 2001. A model for the gamma delta resolvase synaptic complex. Mol Cell 8:623–631.
  • Schmidt BH, Burgin AB, Deweese JE, Osheroff N and Berger JM. 2010. A novel and unified two-metal mechanism for DNA cleavage by type II and IA topoisomerases. Nature 465:641–644.
  • Schoeffler AJ and Berger JM. 2008. DNA topoisomerases: harnessing and constraining energy to govern chromosome topology. Q Rev Biophys 41:41–101.
  • Sherratt DJ, Soballe B, Barre FX, Filipe S, Lau I, Massey T and Yates J. 2004. Recombination and chromosome segregation. Philos Trans R Soc Lond B Biol Sci 359:61–69.
  • Shuman S and Prescott J. 1990. Specific DNA cleavage and binding by vaccinia virus DNA topoisomerase I. J Biol Chem 265:17826–17836.
  • Simon M, Zieg J, Silverman M, Mandel G and Doolittle R. 1980. Phase variation: evolution of a controlling element. Science 209:1370–1374.
  • Smith MC, Brown WR, McEwan AR and Rowley PA. 2010. Site-specific recombination by phiC31 integrase and other large serine recombinases. Biochem Soc Trans 38:388–394.
  • Stark WM, Sherratt DJ and Boocock MR. 1989. Site-specific recombination by Tn3 resolvase: topological changes in the forward and reverse reactions. Cell 58:779–790.
  • Stark WM, Boocock MR and Sherratt DJ. 1992. Catalysis by site-specific recombinases. Trends Genet 8:432–439.
  • Stivers JT, Harris TK and Mildvan AS. 1997. Vaccinia DNA topoisomerase I: evidence supporting a free rotation mechanism for DNA supercoil relaxation. Biochemistry 36:5212–5222.
  • Subramanya HS, Arciszewska LK, Baker RA, Bird LE, Sherratt DJ and Wigley DB. 1997. Crystal structure of the site-specific recombinase, XerD. EMBO J 16:5178–5187.
  • Tse-Dinh YC, McCarron BG, Arentzen R and Chowdhry V. 1983. Mechanistic study of E. coli DNA topoisomerase I: cleavage of oligonucleotides. Nucleic Acids Res 11:8691–8701.
  • van de Putte P and Goosen N. 1992. DNA inversions in phages and bacteria. Trends Genet 8:457–462.
  • Van Duyne GD. 2001. A structural view of cre-loxp site-specific recombination. Annu Rev Biophys Biomol Struct 30:87–104.
  • Vologodskii AV and Cozzarelli NR. 1994. Conformational and thermodynamic properties of supercoiled DNA. Annu Rev Biophys Biomol Struct 23:609–643.
  • Wang JC. 1996. DNA topoisomerases. Annu Rev Biochem 65:635–692.
  • Wang JC. 2002. Cellular roles of DNA topoisomerases: a molecular perspective. Nat Rev Mol Cell Biol 3:430–440.
  • Wasserman SA, Dungan JM and Cozzarelli NR. 1985. Discovery of a predicted DNA knot substantiates a model for site-specific recombination. Science 229:171–174.
  • Whiteson KL, Chen Y, Chopra N, Raymond AC and Rice PA. 2007. Identification of a potential general acid/base in the reversible phosphoryl transfer reactions catalyzed by tyrosine recombinases: Flp H305. Chem Biol 14:121–129.
  • Yang W. 2010. Nucleases: diversity of structrue, function and mechanism. Q Rev Biophys: Sept 21, Epub ahead of print.
  • Yang W and Steitz TA. 1995. Crystal structure of the site-specific recombinase gamma delta resolvase complexed with a 34 bp cleavage site. Cell 82:193–207.
  • Yang Z and Champoux JJ. 2001. The role of histidine 632 in catalysis by human topoisomerase I. J Biol Chem 276:677–685.
  • Zhu CX and Tse-Dinh YC. 2000. The acidic triad conserved in type IA DNA topoisomerases is required for binding of Mg(II) and subsequent conformational change. J Biol Chem 275:5318–5322.
  • Zieg J, Silverman M, Hilmen M and Simon M. 1977. Recombinational switch for gene expression. Science 196:170–172.

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