Hairpin telomere resolvases

Microbiology Spectrum

Volumn 2, Issue 6, 2014, Pages

  Kobryn, Kerri ^a   Chaconas, George ^b,c  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RECOMBINASE;

BACTERIOPHAGE; BACTERIUM; ENZYME ACTIVE SITE; ENZYMOLOGY; GENETIC VARIATION; GENETICS; METABOLISM; TELOMERE;

BACTERIA; BACTERIOPHAGES; CATALYTIC DOMAIN; GENETIC VARIATION; RECOMBINASES; TELOMERE;

EID: 84958215166     PISSN: None     EISSN: 21650497     Source Type: Journal    
DOI: 10.1128/microbiolspec.MDNA3-0023-2014     Document Type: Article

References (75)

1. Chaconas G. 2005. Hairpin telomeres and genome plasticity in Borrelia: all mixed up in the end. Mol Microbiol 58:625-635.
2. Chaconas G, Kobryn K. 2010. Structure, function, and evolution of linear replicons in Borrelia. Annu Rev Microbiol 64:185-202.
3. Deneke J, Ziegelin G, Lurz R, Lanka E. 2000. The protelomerase of temperate Escherichia coli phage N15 has cleaving-joining activity. Proc Natl Acad Sci U S A 97:7721-7726.
4. Huang WM, Joss L, Hsieh T, Casjens S. 2004. Protelomerase uses a topoisomerase IB/Y-recombinase type mechanism to generate DNA hairpin ends. J Mol Biol 337:77-92.
5. Hertwig S, Klein I, Lurz R, Lanka E, Appel B. 2003. PY54, a linear plasmid prophage of Yersinia enterocolitica with covalently closed ends. Mol Microbiol 48:989-1003.
6. Kobryn K, Chaconas G. 2002. ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol Cell 9:195-201.
7. Moriarty TJ, Chaconas G. 2009. Identification of the determinant conferring permissive substrate usage in the telomere resolvase, ResT. J Biol Chem 284:23293-23301.
8. Huang WM, DaGloria J, Fox H, Ruan Q, Tillou J, Shi K, Aihara H, Aron J, Casjens S. 2012. Linear chromosome-generating system of Agrobacterium tumefaciens C58: protelomerase generates and protects hairpin ends. J Biol Chem 287:25551-25563.
9. Ramirez-Bahena MH, Vial L, Lassalle F, Diel B, Chapulliot D, Daubin V, Nesme X, Muller D. 2014. Single acquisition of protelomerase gave rise to speciation of a large and diverse clade within the Agrobacterium/Rhizobium supercluster characterized by the presence of a linear chromid. Mol Phylogenet Evol 73: 202-207.
10. Chaconas G, Stewart PE, Tilly K, Bono JL, Rosa P. 2001. Telomere resolution in the Lyme disease spirochete. EMBO J 20:3229-3237.
11. Tourand Y, Kobryn K, Chaconas G. 2003. Sequence-specific recognition but position-dependent cleavage of two distinct telomeres by the Borrelia burgdorferi telomere resolvase, ResT. Mol Microbiol 48:901-911.
12. Bankhead T, Chaconas G. 2004. Mixing active site components: A recipe for the unique enzymatic activity of a telomere resolvase. Proc Natl Acad Sci U S A 101:13768-13773.
13. Deneke J, Burgin AB, Wilson SL, Chaconas G. 2004. Catalytic residues of the telomere resolvaseResT: a pattern similar to, but distinct fromtyrosine recombinases and type IB topoisomerases. J Biol Chem 279:53699-53706.
14. Kobryn K, Burgin AB, Chaconas G. 2005. Uncoupling the chemical steps of telomere resolution by ResT. J Biol Chem 280:26788-26795.
15. Kobryn K, Chaconas G. 2005. Fusion of hairpin telomeres by the B. burgdorferi telomere resolvase ResT: Implications for shaping a genome in flux. Mol Cell 17:783-791.
16. Bankhead T, Kobryn K, Chaconas G. 2006. Unexpected twist: harnessing the energy in positive supercoils to control telomere resolution. Mol Microbiol 62:895-905.
17. Tourand Y, Bankhead T, Wilson SL, Putteet-Driver AD, Barbour AG, Byram R, Rosa PA, Chaconas G. 2006. Differential telomere processing by Borrelia telomere resolvases in vitro but not in vivo. J Bacteriol 188:7378-7386.
18. Tourand Y, Lee L, Chaconas G. 2007. Telomere resolution by Borrelia burgdorferi ResT through the collaborative efforts of tethered DNA binding domains. Mol Microbiol 64:580-590.
19. Lefas G, Chaconas G. 2009. High-throughput screening identifies three inhibitor classes of the telomere resolvase from the Lyme disease spirochete. Antimicrob Agents Chemother 53:4441-4449.
20. Tourand Y, Deneke J, Moriarty TJ, Chaconas G. 2009. Characterization and in vitro reaction properties of 19 unique hairpin telomeres from the linear plasmids of the Lyme disease spirochete. J Biol Chem 284:7264-7272.
21. Kobryn K, Briffotaux J, Karpov V. 2009. Holliday junction formation by the Borrelia burgdorferi telomere resolvase, ResT: implications for the origin of genome linearity. Mol Microbiol 71:1117-1130.
22. Briffotaux J, Kobryn K. 2010. Preventing broken borrelia telomeres: Rest couples dual hairpin telomere formation to product release. J Biol Chem 285: 41010-41018.
23. Mir T, Huang SH, Kobryn K. 2013. The telomere resolvase of the Lyme disease spirochete, Borrelia burgdorferi, promotes DNA single-strand annealing and strand exchange. Nucleic Acids Res 41:10438-10448.
24. Deneke J, Ziegelin G, Lurz R, Lanka E. 2002. Phage N15 telomere resolution: Target requirements for recognition and processing by the protelomerase. J Biol Chem 277:10410-10419.
25. Aihara H, Huang WM, Ellenberger T. 2007. An interlocked dimer of the protelomerase TelK distorts DNA structure for the formation of hairpin telomeres. Mol Cell 27:901-913.
26. Shi K, Huang WM, Aihara H. 2013. An enzyme-catalyzed multistep DNA refolding mechanism in hairpin telomere formation. PLoS Biol 11: e1001472.
27. Shuman S. 1998. Vaccinia virus DNA topoisomerase: a model eukaryotic type IB enzyme. Biochim Biophys Acta 1400:321-337.
28. Van Duyne GD. 2002. A structural view of tyrosine recombinase site-specific recombination, p 93-117. In Craig NL, Craigie R, Gellert M, Lambowitz AM (ed), Mobile DNA II. ASM Press, Washington, DC.
29. Grindley ND, Whiteson KL, Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75:567-605.
30. Lee J, Tonozuka T, Jayaram M. 1997. Mechanism of active site exclusion in a site-specific recombinase: role of the DNA substrate in conferring half-of-the-sites activity. Genes Dev 11:3061-3071.
31. Voziyanov Y, Pathania S, Jayaram M. 1999. A general model for site-specific recombination by the integrase family recombinases. Nucleic Acids Res 27:930-941.
32. Conway AB, Chen Y, Rice PA. 2003. Structural plasticity of the Flp-Holliday junction complex. J Mol Biol 326:425-434.
33. Burgin AB, Jr, Nash HA. 1995. Suicide substrates reveal properties of the homology-dependent steps during integrative recombination of bacteriophage lambda. Curr Biol 5:1312-1321.
34. Barre FX, Aroyo M, Colloms SD, Helfrich A, Cornet F, Sherratt DJ. 2000. FtsK functions in the processing of a Holliday junction intermediate during bacterial chromosome segregation. Genes Dev 14:2976-2988.
35. Rybchin VN, Svarchevsky AN. 1999. The plasmid prophage N15: a linear DNA with covalently closed ends. Mol Microbiol 33:895-903.
36. Krogh BO, Shuman S. 2000. Catalytic mechanism of DNA topoisomerase IB. Mol Cell 5:1035-1041.
37. Krogh BO, Shuman S. 2002. Proton relay mechanism of general acid catalysis by DNA topoisomerase IB. J Biol Chem 277:5711-5714.
38. Burgin AB. 2001. Synthesis and use of DNA containing a 5'-bridging phosphorothioate as a suicide substrate for type I DNA topoisomerases. Methods Mol Biol 95:119-128.
39. Van Duyne GD. 2001. A structural view of cre-loxp site-specific recombination. Annu Rev Biophys Biomol Struct 30:87-104.
40. Chen Y, Rice PA. 2003. The role of the conserved Trp330 in Flpmediated recombination. Functional and structural analysis. J Biol Chem 278:24800-24807.
41. Whiteson KL, Chen Y, Chopra N, Raymond AC, 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.
42. Davies DR, Mushtaq A, Interthal H, Champoux JJ, Hol WG. 2006. The structure of the transition state of the heterodimeric topoisomerase I of Leishmania donovani as a vanadate complex with nicked DNA. J Mol Biol 357:1202-1210.
43. Kobryn K. 2007. The linear hairpin replicons of Borrelia burgdorferi, p 117-140. In Meinhardt F, Klassen R (ed), Microbial Linear Plasmids. Springer, Berlin Heidelberg.
44. Casjens S, Palmer N, van Vugt R, Huang WH, Stevenson B, Rosa P, Lathigra R, Sutton G, Peterson J, Dodson RJ, Haft D, Hickey E, Gwinn M, White O, Fraser CM. 2000. A bacterial genome in flux: the twelve linear and nine circular extrachromosomal DNAs in an infectious isolate of the Lyme disease spirochete Borrelia burgdorferi. Mol Microbiol 35:490-516.
45. Fraser CM, Casjens S, Huang WM, Sutton GG, Clayton R, Lathigra R, White O, Ketchum KA, Dodson R, Hickey EK, Gwinn M, Dougherty B, Tomb JF, Fleischmann RD, Richardson D, Peterson J, Kerlavage AR, Quackenbush J, Salzberg S, Hanson M, van Vugt R, Palmer N, Adams MD, Gocayne J, Weidman J, Utterback T, Watthey L, McDonald L, Artiach P, Bowman C, Garland S, Fujii C, Cotton MD, Horst K, Roberts K, Hatch B, Smith HO, Venter JC. 1997. Genomic sequence of a Lyme disease spirochaete, Borrelia burgdorferi. Nature 390:580-586.
46. Casjens SR, Mongodin EF, Qiu WG, Luft BJ, Schutzer SE, Gilcrease EB, Huang WM, Vujadinovic M, Aron JK, Vargas LC, Freeman S, Radune D, Weidman JF, Dimitrov GI, Khouri HM, Sosa JE, Halpin RA, Dunn JJ, Fraser CM. 2012. Genome stability of Lyme disease spirochetes: comparative genomics of Borrelia burgdorferi plasmids. PloS One 7: e33280.
47. Huang WM, Robertson M, Aron J, Casjens S. 2004. Telomere exchange between linear replicons of Borrelia burgdorferi. J Bacteriol 186:4134-4141.
48. Casjens S, Murphy M, DeLange M, Sampson L, van Vugt R, Huang WM. 1997. Telomeres of the linear chromosomes of Lyme disease spirochaetes: nucleotide sequence and possible exchange with linear plasmid telomeres. Mol Microbiol 26:581-596.
49. Terekhova D, Iyer R, Wormser GP, Schwartz I. 2006. Comparative genome hybridization reveals substantial variation among clinical isolates of Borrelia burgdorferi sensu stricto with different pathogenic properties. J Bacteriol 188:6124-6134.
50. Davies DR, Goryshin IY, ReznikoffWS, Rayment I. 2000. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289:77-85.
51. Lovell S, Goryshin IY, ReznikoffWR, Rayment I. 2002. Two-metal active site binding of a Tn5 transposase synaptic complex. Nat Struct Biol 9:278-281.
52. Ason B, ReznikoffWS. 2002. Mutational analysis of the base flipping event found in Tn5 transposition. J Biol Chem 277:11284-11291.
53. Allingham JS, Wardle SJ, Haniford DB. 2001. Determinants for hairpin formation in Tn10 transposition. EMBO J 20:2931-2942.
54. Bischerour J, Chalmers R. 2007. Base-flipping dynamics in a DNA hairpin processing reaction. Nucleic Acids Res 35:2584-2595.
55. Bischerour J, Chalmers R. 2009. Base flipping in tn10 transposition: an active flip and capture mechanism. PloS One 4:e6201.
56. Ghosh K, Lau CK, Gupta K, Van Duyne GD. 2005. Preferential synapsis of loxP sites drives ordered strand exchange in Cre-loxP site-specific recombination. Nat Chem Biol 1:275-282.
57. Hoess RH, Wierzbicki A, Abremski K. 1986. The role of the loxP spacer region in P1 site-specific recombination. Nucleic Acids Res 14:2287-2300.
58. Lee L, Chu LC, Sadowski PD. 2003. Cre induces an asymmetric DNA bend in its target loxP site. J Biol Chem 278:23118-23129.
59. Lee L, Sadowski PD. 2003. Sequence of the loxP site determines the order of strand exchange by the Cre recombinase. J Mol Biol 326:397-412.
60. SenecoffJF, Cox MM. 1986. Directionality in FLP protein-promoted site-specific recombination is mediated by DNA-DNA pairing. J Biol Chem 261:7380-7386.
61. Cui T, Moro-oka N, Ohsumi K, Kodama K, Ohshima T, Ogasawara N, Mori H, Wanner B, Niki H, Horiuchi T. 2007. Escherichia coli with a linear genome. EMBO Rep 8:181-187.
62. Aussel L, Barre FX, Aroyo M, Stasiak A, Stasiak AZ, Sherratt D. 2002. FtsK Is a DNA motor protein that activates chromosome dimer resolution by switching the catalytic state of the XerC and XerD recombinases. Cell 108:195-205.
63. Bigot S, Saleh OA, Lesterlin C, Pages C, El Karoui M, Dennis C, Grigoriev M, Allemand JF, Barre FX, Cornet F. 2005. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J 24:3770-3780.
64. Kuzminov A. 1999. Recombinational repair of DNA damage in Escherichia coli and bacteriophage lambda. Microbiol Mol Biol Rev 63:751-813.
65. Coutte L, Botkin DJ, Gao L, Norris SJ. 2009. Detailed analysis of sequence changes occurring during vlsE antigenic variation in the mouse model of Borrelia burgdorferi infection. PLoS Pathog 5:e1000293.
66. Dresser AR, Hardy P-O, Chaconas G. 2009. Investigation of the role of DNA replication, recombination and repair genes in antigenic switching at the vlsE locus in Borrelia burgdorferi: an essential role for the RuvAB branch migrase. PLoS Pathog 5:e1000680.
67. Lin T, Gao L, Edmondson DG, Jacobs MB, Philipp MT, Norris SJ. 2009. Central role of the Holliday junction helicase RuvAB in vlsE recombination and infectivity of Borrelia burgdorferi. PLoS Pathog 12: e1000679.
68. Byram R, Stewart PE, Rosa P. 2004. The essential nature of the ubiquitous 26-kilobase circular replicon of Borrelia burgdorferi. J Bacteriol 186:3561-3569.
69. Bandy NJ, Salman-Dilgimen A, Chaconas G. 2014. Construction and characterization of a B. burgdorferi strain with conditional expression of the essential telomere resolvase, ResT. Journal of Bacteriology 196:2396-2404.
70. Hinnebusch J, Barbour AG. 1991. Linear plasmids of Borrelia burgdorferi have a telomeric structure and sequence similar to those of a eukaryotic virus. J Bacteriol 173:7233-7239.
71. Hinnebusch J, Bergstrom S, Barbour AG. 1990. Cloning and sequence analysis of linear plasmid telomeres of the bacterium Borrelia burgdorferi. Mol Microbiol 4:811-820.
72. Zhang JR, Hardham JM, Barbour AG, Norris SJ. 1997. Antigenic variation in Lyme disease borreliae by promiscuous recombination of VMP-like sequence cassettes. Cell 89:275-285.
73. Froelich-Ammon SJ, OsheroffN. 1995. Topoisomerase poisons: harnessing the dark side of enzyme mechanism. J Biol Chem270:21429-21432.
74. Pinder DJ, Blake CE, Lindsey JC, Leach DR. 1998. Replication strand preference for deletions associated with DNA palindromes. Mol Microbiol 28:719-727.
75. Leach DR, Okely EA, Pinder DJ. 1997. Repair by recombination of DNA containing a palindromic sequence. Mol Microbiol 26:597-606.