An Interlocked Dimer of the Protelomerase TelK Distorts DNA Structure for the Formation of Hairpin Telomeres

Molecular Cell

Volumn 27, Issue 6, 2007, Pages 901-913

  Aihara, Hideki ^a   Huang, Wai Mun ^b   Ellenberger, Tom ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

Author keywords

DNA; MICROBIO

Indexed keywords

BACTERIAL ENZYME; DIMER; DNA; PALINDROMIC DNA; PROTELOMERASE TELK; UNCLASSIFIED DRUG;

ARTICLE; BACTERIOPHAGE; BASE PAIRING; CRYSTAL STRUCTURE; DNA CLEAVAGE; DNA STRUCTURE; ENZYME STRUCTURE; ENZYME SUBSTRATE; KLEBSIELLA OXYTOCA; PROTEIN DNA INTERACTION; PROTEIN FOLDING; TELOMERE;

AMINO ACID SEQUENCE; BACTERIOPHAGES; BINDING SITES; DIMERIZATION; DNA; DNA REPLICATION; ELECTROSTATICS; ENZYME PRECURSORS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; SUBSTRATE SPECIFICITY; TELOMERASE; TELOMERE; VIRAL PROTEINS; X-RAY DIFFRACTION;

KLEBSIELLA OXYTOCA; PROKARYOTA;

EID: 34748841408     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.07.026     Document Type: Article

References (87)

1. Antao V.P., and Tinoco Jr. I. Thermodynamic parameters for loop formation in RNA and DNA hairpin tetraloops. Nucleic Acids Res. 20 (1992) 819-824
2. Bankhead T., and Chaconas G. Mixing active-site components: a recipe for the unique enzymatic activity of a telomere resolvase. Proc. Natl. Acad. Sci. USA 101 (2004) 13768-13773
3. Bao K., and Cohen S.N. Terminal proteins essential for the replication of linear plasmids and chromosomes in Streptomyces. Genes Dev. 15 (2001) 1518-1527
4. Baumann P., and Cech T.R. Pot1, the putative telomere end-binding protein in fission yeast and humans. Science 292 (2001) 1171-1175
5. Bilaud T., Brun C., Ancelin K., Koering C.E., Laroche T., and Gilson E. Telomeric localization of TRF2, a novel human telobox protein. Nat. Genet. 17 (1997) 236-239
6. Biswas T., Aihara H., Radman-Livaja M., Filman D., Landy A., and Ellenberger T. A structural basis for allosteric control of DNA recombination by λ integrase. Nature 435 (2005) 1059-1066
7. Blackburn E.H. Structure and function of telomeres. Nature 350 (1991) 569-573
8. Bonnet G., Krichevsky O., and Libchaber A. Kinetics of conformational fluctuations in DNA hairpin-loops. Proc. Natl. Acad. Sci. USA 95 (1998) 8602-8606
9. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR System: a new software suite for macromolecular structure determination. Acta Crystallogr. D Biol. Crystallogr. 54 (1998) 905-921
10. Casjens S. Evolution of the linear DNA replicons of the Borrelia spirochetes. Curr. Opin. Microbiol. 2 (1999) 529-534
11. Casjens S., Murphy M., DeLange M., Sampson L., van Vugt R., and Huang W.M. Telomeres of the linear chromosomes of Lyme disease spirochaetes: nucleotide sequence and possible exchange with linear plasmid telomeres. Mol. Microbiol. 26 (1997) 581-596
12. Casjens S.R., Gilcrease E.B., Huang W.M., Bunny K.L., Pedulla M.L., Ford M.E., Houtz J.M., Hatfull G.F., and Hendrix R.W. The pKO2 linear plasmid prophage of Klebsiella oxytoca. J. Bacteriol. 186 (2004) 1818-1832
13. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
14. Champoux J.J. DNA is linked to the rat liver DNA nicking-closing enzyme by a phosphodiester bond to tyrosine. J. Biol. Chem. 256 (1981) 4805-4809
15. Champoux J.J. DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem. 70 (2001) 369-413
16. Chen Y., and Rice P.A. New insight into site-specific recombination from Flp recombinase-DNA structures. Annu. Rev. Biophys. Biomol. Struct. 32 (2003) 135-159
17. Chou S.H., Chin K.H., and Wang A.H. Unusual DNA duplex and hairpin motifs. Nucleic Acids Res. 31 (2003) 2461-2474
18. Cooper J.P., Nimmo E.R., Allshire R.C., and Cech T.R. Regulation of telomere length and function by a Myb-domain protein in fission yeast. Nature 385 (1997) 744-747
19. Craig N.L., and Nash H.A. The mechanism of phage λ site-specific recombination: site-specific breakage of DNA by Int topoisomerase. Cell 35 (1983) 795-803
20. Davies D.R., and Hol W.G. The power of vanadate in crystallographic investigations of phosphoryl transfer enzymes. FEBS Lett. 577 (2004) 315-321
21. Davies D.R., Goryshin I.Y., Reznikoff W.S., and Rayment I. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289 (2000) 77-85
22. De LaFortelle E., and Bricogne G. Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276 (1997) 472-499
23. DeLano, W.L. (2002). The PyMOL Molecular Graphics System (http://www.pymol.org/).
24. Delaroque N., Muller D.G., Bothe G., Pohl T., Knippers R., and Boland W. The complete DNA sequence of the Ectocarpus siliculosus virus EsV-1 genome. Virology 287 (2001) 112-132
25. Deneke J., Ziegelin G., Lurz R., and Lanka E. The protelomerase of temperate Escherichia coli phage N15 has cleaving-joining activity. Proc. Natl. Acad. Sci. USA 97 (2000) 7721-7726
26. Doublie S. Production of selenomethionyl proteins in prokaryotic and eukaryotic expression systems. Methods Mol. Biol. 363 (2007) 91-108
27. Goodner B., Hinkle G., Gattung S., Miller N., Blanchard M., Qurollo B., Goldman B.S., Cao Y., Askenazi M., Halling C., et al. Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294 (2001) 2323-2328
28. Greider C.W., and Blackburn E.H. Identification of a specific telomere terminal transferase activity in Tetrahymena extracts. Cell 43 (1985) 405-413
29. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., and de Lange T. Mammalian telomeres end in a large duplex loop. Cell 97 (1999) 503-514
30. Groft C.M., Uljon S.N., Wang R., and Werner M.H. Structural homology between the Rap30 DNA-binding domain and linker histone H5: implications for preinitiation complex assembly. Proc. Natl. Acad. Sci. USA 95 (1998) 9117-9122
31. Guzman L.M., Belin D., Carson M.J., and Beckwith J. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J. Bacteriol. 177 (1995) 4121-4130
32. Hertwig S., Klein I., Lurz R., Lanka E., and Appel B. PY54, a linear plasmid prophage of Yersinia enterocolitica with covalently closed ends. Mol. Microbiol. 48 (2003) 989-1003
33. Hinnebusch J., and Barbour A.G. Linear plasmids of Borrelia burgdorferi have a telomeric structure and sequence similar to those of a eukaryotic virus. J. Bacteriol. 173 (1991) 7233-7239
34. Hinnebusch J., Bergstrom S., and Barbour A.G. Cloning and sequence analysis of linear plasmid telomeres of the bacterium Borrelia burgdorferi. Mol. Microbiol. 4 (1990) 811-820
35. Hirochika H., and Sakaguchi K. Analysis of linear plasmids isolated from Streptomyces: association of protein with the ends of the plasmid DNA. Plasmid 7 (1982) 59-65
36. Holm L., and Sander C. Touring protein fold space with Dali/FSSP. Nucleic Acids Res. 26 (1998) 316-319
37. Huang W.M., Joss L., Hsieh T., and Casjens S. Protelomerase uses a topoisomerase IB/Y-recombinase type mechanism to generate DNA hairpin ends. J. Mol. Biol. 337 (2004) 77-92
38. Interthal H., Quigley P.M., Hol W.G., and Champoux J.J. The role of lysine 532 in the catalytic mechanism of human topoisomerase I. J. Biol. Chem. 279 (2004) 2984-2992
39. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard M. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47 (1991) 110-119
40. Kobryn K., and Chaconas G. The circle is broken: telomere resolution in linear replicons. Curr. Opin. Microbiol. 4 (2001) 558-564
41. Kobryn K., and Chaconas G. ResT, a telomere resolvase encoded by the Lyme disease spirochete. Mol. Cell 9 (2002) 195-201
42. Krogh B.O., and Shuman S. Catalytic mechanism of DNA topoisomerase IB. Mol. Cell 5 (2000) 1035-1041
43. Kwon H.J., Tirumalai R., Landy A., and Ellenberger T. Flexibility in DNA recombination: structure of the λ integrase catalytic core. Science 276 (1997) 126-131
44. Lavery R., and Sklenar H. Defining the structure of irregular nucleic acids: conventions and principles. J. Biomol. Struct. Dyn. 6 (1989) 655-667
45. Levis R.W., Ganesan R., Houtchens K., Tolar L.A., and Sheen F.M. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75 (1993) 1083-1093
46. Lin Y.S., Kieser H.M., Hopwood D.A., and Chen C.W. The chromosomal DNA of Streptomyces lividans 66 is linear. Mol. Microbiol. 10 (1993) 923-933
47. Lobocka M.B., Svarchevsky A.N., Rybchin V.N., and Yarmolinsky M.B. Characterization of the primary immunity region of the Escherichia coli linear plasmid prophage N15. J. Bacteriol. 178 (1996) 2902-2910
48. Lu X.J., and Olson W.K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31 (2003) 5108-5121
49. MacDonald D., Demarre G., Bouvier M., Mazel D., and Gopaul D.N. Structural basis for broad DNA-specificity in integron recombination. Nature 440 (2006) 1157-1162
50. McClintock B. The stability of broken ends of chromosomes in Zea mays. Genetics 26 (1941) 234-282
51. Mellado R.P., Penalva M.A., Inciarte M.R., and Salas M. The protein covalently linked to the 5′ termini of the DNA of Bacillus subtilis phage φ{symbol} 29 is involved in the initiation of DNA replication. Virology 104 (1980) 84-96
52. Mizuuchi K., and Adzuma K. Inversion of the phosphate chirality at the target site of Mu DNA strand transfer: evidence for a one-step transesterification mechanism. Cell 66 (1991) 129-140
53. Müller H.J. The remaking of chromosomes. Collect. Net Woods Hole 13 (1938) 181-198
54. Mumm J.P., Landy A., and Gelles J. Viewing single λ site-specific recombination events from start to finish. EMBO J. 25 (2006) 4586-4595
55. Nash H.A., and Robertson C.A. Heteroduplex substrates for bacteriophage λ site-specific recombination: cleavage and strand transfer products. EMBO J. 8 (1989) 3523-3533
56. Nunes-Duby S.E., Matsumoto L., and Landy A. Site-specific recombination intermediates trapped with suicide substrates. Cell 50 (1987) 779-788
57. Nunes-Duby S.E., Kwon H.J., Tirumalai R.S., Ellenberger T., and Landy A. Similarities and differences among 105 members of the Int family of site-specific recombinases. Nucleic Acids Res. 26 (1998) 391-406
58. Oakey H.J., Cullen B.R., and Owens L. The complete nucleotide sequence of the Vibrio harveyi bacteriophage VHML. J. Appl. Microbiol. 93 (2002) 1089-1098
59. Olovnikov A.M. A theory of marginotomy. The incomplete copying of template margin in enzymic synthesis of polynucleotides and biological significance of the phenomenon. J. Theor. Biol. 41 (1973) 181-190
60. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
61. Pardue M.L., and DeBaryshe P.G. Drosophila telomeres: two transposable elements with important roles in chromosomes. Genetica 107 (1999) 189-196
62. Pargellis C.A., Nunes-Duby S.E., de Vargas L.M., and Landy A. Suicide recombination substrates yield covalent λ integrase-DNA complexes and lead to identification of the active site tyrosine. J. Biol. Chem. 263 (1988) 7678-7685
63. Parkinson G.N., Lee M.P., and Neidle S. Crystal structure of parallel quadruplexes from human telomeric DNA. Nature 417 (2002) 876-880
64. Picardeau M., Lobry J.R., and Hinnebusch B.J. Physical mapping of an origin of bidirectional replication at the centre of the Borrelia burgdorferi linear chromosome. Mol. Microbiol. 32 (1999) 437-445
65. Pieters J.M., Mellema J.R., van den Elst H., van der Marel G.A., van Boom J.H., and Altona C. Thermodynamics of the various forms of the dodecamer d(ATTACCGGTAAT) and of its constituent hexamers from proton NMR chemical shifts and UV melting curves: three-state and four-state thermodynamic models. Biopolymers 28 (1989) 717-740
66. Ravin N.V., Strakhova T.S., and Kuprianov V.V. The protelomerase of the phage-plasmid N15 is responsible for its maintenance in linear form. J. Mol. Biol. 312 (2001) 899-906
67. Ravin N.V., Kuprianov V.V., Gilcrease E.B., and Casjens S.R. Bidirectional replication from an internal ori site of the linear N15 plasmid prophage. Nucleic Acids Res. 31 (2003) 6552-6560
68. Redinbo M.R., Stewart L., Kuhn P., Champoux J.J., and Hol W.G. Crystal structures of human topoisomerase I in covalent and noncovalent complexes with DNA. Science 279 (1998) 1504-1513
69. Rekosh D.M., Russell W.C., Bellet A.J., and Robinson A.J. Identification of a protein linked to the ends of adenovirus DNA. Cell 11 (1977) 283-295
70. Rice P.A., and Baker T.A. Comparative architecture of transposase and integrase complexes. Nat. Struct. Biol. 8 (2001) 302-307
71. Rybchin V.N., and Svarchevsky A.N. The plasmid prophage N15: a linear DNA with covalently closed ends. Mol. Microbiol. 33 (1999) 895-903
72. Senior M.M., Jones R.A., and Breslauer K.J. Influence of loop residues on the relative stabilities of DNA hairpin structures. Proc. Natl. Acad. Sci. USA 85 (1988) 6242-6246
73. Sinden R.R., and Pettijohn D.E. Cruciform transitions in DNA. J. Biol. Chem. 259 (1984) 6593-6600
74. Smith S., and de Lange T. TRF1, a mammalian telomeric protein. Trends Genet. 13 (1997) 21-26
75. Smith F.W., and Feigon J. Quadruplex structure of Oxytricha telomeric DNA oligonucleotides. Nature 356 (1992) 164-168
76. Stewart L., Redinbo M.R., Qiu X., Hol W.G., and Champoux J.J. A model for the mechanism of human topoisomerase I. Science 279 (1998) 1534-1541
77. Szostak J.W., and Blackburn E.H. Cloning yeast telomeres on linear plasmid vectors. Cell 29 (1982) 245-255
78. Terwilliger T.C. Automated structure solution, density modification and model building. Acta Crystallogr. D Biol. Crystallogr. 58 (2002) 1937-1940
79. Tirumalai R.S., Kwon H.J., Cardente E.H., Ellenberger T., and Landy A. Recognition of core-type DNA sites by λ integrase. J. Mol. Biol. 279 (1998) 513-527
80. Tourand Y., Kobryn K., and Chaconas G. Sequence-specific recognition but position-dependent cleavage of two distinct telomeres by the Borrelia burgdorferi telomere resolvase, ResT. Mol. Microbiol. 48 (2003) 901-911
81. Van Duyne G.D. A structural view of cre-loxp site-specific recombination. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 87-104
82. van Gent D.C., Mizuuchi K., and Gellert M. Similarities between initiation of V(D)J recombination and retroviral integration. Science 271 (1996) 1592-1594
83. van Steensel B., Smogorzewska A., and de Lange T. TRF2 protects human telomeres from end-to-end fusions. Cell 92 (1998) 401-413
84. Watson J.D. Origin of concatemeric T7 DNA. Nat. New Biol. 239 (1972) 197-201
85. Wemmer D.E., Chou S.H., Hare D.R., and Reid B.R. Duplex-hairpin transitions in DNA: NMR studies on CGCGTATACGCG. Nucleic Acids Res. 13 (1985) 3755-3772
86. Whiteson K.L., Chen Y., Chopra N., Raymond A.C., and Rice P.A. Identification of a potential general acid/base in the reversible phosphoryl transfer reactions catalyzed by tyrosine recombinases: Flp H305. Chem. Biol. 14 (2007) 121-129
87. Zhu X.D., Pan G., Luetke K., and Sadowski P.D. Homology requirements for ligation and strand exchange by the FLP recombinase. J. Biol. Chem. 270 (1995) 11646-11653