Enzyme-mediated DNA looping

Annual Review of Biophysics and Biomolecular Structure

Volumn 33, Issue , 2004, Pages 1-24

  Halford, Stephen E ^a   Welsh, Abigail J ^a   Szczelkun, Mark D ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

DNA structure; DNA protein interaction; Molecular motor; Protein protein interaction; Restriction endonuclease

Indexed keywords

DNA; RESTRICTION ENDONUCLEASE;

BINDING SITE; COMPLEX FORMATION; DNA CLEAVAGE; DNA STRUCTURE; ENERGY; ENZYME ACTIVITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; REVIEW; TRANSLOCATION LINE;

BINDING SITES; DNA RESTRICTION ENZYMES; DNA-BINDING PROTEINS; MOLECULAR MOTOR PROTEINS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 2342640588     PISSN: 10568700     EISSN: None     Source Type: Book Series    
DOI: 10.1146/annurev.biophys.33.110502.132711     Document Type: Review

References (107)

1. Adzuma K, Mizuuchi K. 1989. Interaction of proteins located at a distance along DNA: mechanism of target immunity in the Mu DNA strand-transfer reaction. Cell 57:41-47
2. Aldaz H, Schuster E, Baker TA. 1996. The interwoven architecture of the Mu transposase couples DNA synapsis to catalysis. Cell 85:257-69
3. Allen DJ, Makhov A, Grilley M, Taylor J, Thresher R, et al. 1997. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 16:4467-76
4. Bates AD, Maxwell A. 1993. DNA Topology. Oxford, UK: Oxford Univ. Press. 114 pp.
5. Bath AJ, Milsom SE, Gormley NA, Halford SE. 2002. Many type IIs restriction endonucleases interact with two recognition sites before cleaving DNA. J. Biol. Chem. 277:4024-33
6. Benkovic SJ, Valentine AM, Salinas F. 2001. Replisome-mediated DNA replication. Annu. Rev. Biochem. 70:181-208
7. Berge T, Ellis DJ, Dryden DT, Edwardson JM, Henderson RM. 2000. Translocation-independent dimerization of the EcoKI endonuclease visualized by atomic force microscopy. Biophys. J. 79:479-84
8. Bianco PR, Kowalczykowski SC. 2000. Translocation step size and mechanism of the RecBC DNA helicase. Nature 405:368-72
9. Bickle TA, Krüger DH. 1993. Biology of DNA restriction. Microbiol. Rev. 57:434-50
10. Bilcock DT, Daniels LE, Bath AJ, Halford SE. 1999. Reactions of type II restriction endonucleases with 8-base pair recognition sites. J. Biol. Chem. 274:36379-86
11. Bilcock DT, Halford SE. 1999. DNA restriction dependent on two recognition sites: activities of the SfiI restriction-modification system in Escherichia coli. Mol. Microbiol. 31:1243-54
12. Bitinaite J, Wah DA, Aggarwal AK, Schildkraut I. 1998. FokI dimerization is required for DNA cleavage. Proc. Natl. Acad. Sci. USA 95:10564-69
13. Bourniquel AA, Bickle TA. 2002. Complex restriction enzymes: NTP-driven molecular motors. Biochimie 84:1047-59
14. Charvin G, Bensimon D, Croquette V. 2003. Single-molecule study of DNA unlinking by eukaryotic and prokaryotic type-II topoisomerases. Proc. Natl. Acad. Sci. USA 100:9820-25
15. Chen Y, Rice PA. 2003. New insights into site-specific recombination from Flp recombinase-DNA structures. Annu. Rev. Biophys. Biomol. Struct. 32:135-59
16. Connolly BA, Eckstein F, Pingoud A. 1984. The stereochemical course of the restriction endonuclease EcoRI-catalyzed reaction. J. Biol. Chem. 259:10760-63
17. Craig NL, Craigie R, Gellert M, Lambowitz AM, eds. 2002. Mobile DNA II. Washington, DC: ASM. 1204 pp.
18. Daniels LE, Wood KE, Scott DJ, Halford SE. 2003. Subunit assembly for DNA cleavage by restriction endonuclease SgrAI. J. Mol. Biol. 327:579-91
19. Deibert M, Grazulis S, Siksnys V, Huber R. 2000. Tetrameric restriction enzyme trapped in action: structure of NgoMIV endonuclease in complex with cognate DNA. Nat. Struct. Biol. 7:792-99
20. Dreier J, MacWilliams MP, Bickle TA. 1996. DNA cleavage by the type IC restriction-modification enzyme EcoR124II. J. Mol. Biol. 264:722-33
21. Dryden DTF, Murray NE, Rao DN. 2001. Nucleoside triphosphate-dependent restriction enzymes. Nucleic Acids Res. 29:3728-41
22. Dybvig K, Sitaraman R, French CT. 1998. A family of phase-variable restriction enzymes with differing specificities generated by high-frequency gene rearrangements. Proc. Natl. Acad. Sci. USA 95:13923-28
23. Echols H. 1986. Multiple DNA-protein interactions governing high-precision DNA transactions. Science 233:1050-56
24. Ellis DJ, Dryden DT, Berge T, Edwardson JM, Henderson RM. 1999. Direct observation of DNA translocation and cleavage by the EcoKI endonuclease using atomic force microscopy. Nat. Struct. Biol. 6:15-17
25. Embleton ML, Siksnys V, Halford SE. 2001. DNA cleavage reactions by type II restriction enzymes that require two copies of their recognition sites. J. Mol. Biol. 311:503-14
26. Embleton ML, Williams S A, Watson MA, Halford SE. 1999. Specificity from the synapsis of DNA elements by the SfiI endonuclease. J. Mol. Biol. 289:785-97
27. Endlich B, Linn S. 1985. The DNA restriction endonuclease of Escherichia coli B. I. Studies of the DNA translocation and the ATPase activities. J. Biol. Chem. 260:5720-28
28. Forde NR, Izhaky D, Woodcock GR, Wuite GJ, Bustamante C. 2002. Using mechanical force to probe the mechanism of pausing and arrest during continuous elongation by Escherichia coli RNA polymerase. Proc. Natl. Acad. Sci. USA 99:11682-87
29. Friedhoff P, Lurz R, Lueder G, Pingoud A. 2001. Sau3AI: a monomeric type II restriction endonuclease that dimerizes on the DNA and thereby induces DNA loops. J. Biol. Chem. 276:23581-88
30. Gormley NA, Bath AJ, Halford SE. 2000. Reactions of BglI and other type II restriction endonucleases with discontinuous recognition sites. J. Biol. Chem. 275:6928-36
31. Gormley NA, Hillberg AL, Halford SE. 2002. The type IIs restriction endonuclease BspMI is a tetramer that acts concertedly at two copies of an asymmetric DNA sequence. J. Biol. Chem. 277:4034-41
32. Gowers DM, Halford SE. 2003. Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J. 22:1410-18
33. Grasby JA, Connolly BA. 1992. Stereochemical outcome of the hydrolysis reaction catalyzed by the EcoRV restriction endonuclease. Biochemistry 31:7855-61
34. Grazulis S, Deibert M, Rimeseliene R, Skirgaila R, Sasnauskas G, et al. 2002. Crystal structure of the Bse634I restriction endonuclease: comparison of two enzymes recognizing the same DNA sequence. Nucleic Acids Res. 30:876-85
35. Halford SE. 2001. Hopping, jumping and looping by restriction enzymes. Biochem. Soc. Trans. 29:363-73
36. Halford SE, Szczelkun MD. 2002. How to get from A to B: strategies for analysing protein motion on DNA. Eur. Biophys. J. 31:257-67
37. Havas K, Flaus A, Phelan M, Kingston R, Wade PA, et al. 2000. Generation of superhelical torsion by ATP-dependent chromatin remodeling activities. Cell 103:1133-42
38. Hochschild A. 1990. Protein-protein interactions and DNA loop formation. In DNA Topology and Its Biological Effects, ed. JC Wang, NR Cozzarelli, pp. 107-38. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press
39. Huai Q, Colandene JD, Topal MD, Ke H. 2001. Structure of NaeI-DNA complex reveals dual-mode DNA recognition and complete dimer rearrangement. Nat. Struct. Biol. 8:665-69
40. Huang J, Schlick T, Vologodskii A. 2001. Dynamics of site juxtaposition in supercoiled DNA. Proc. Natl. Acad. Sci. USA 98:968-73
41. Janscak P, Abadjieva A, Firman K. 1996. The type I restriction endonuclease R.Eco R1241: over-production and biochemical properties. J. Mol. Biol. 257:977-91
42. Janscak P, Bickle TA. 2000. DNA supercoiling during ATP-dependent DNA translocation by the type I restriction enzyme Eco AI. J. Mol. Biol. 295:1089-99
43. Janscak P, Sandmeier U, Szczelkun MD, Bickle TA. 2001. Subunit assembly and mode of DNA cleavage of the type III restriction endonucleases EcoP1I and Eco P15I. J. Mol. Biol. 306:417-31
44. Jian H, Schlick T, Vologodskii A. 1998. Internal motion of supercoiled DNA: Brownian dynamic simulations of site juxtaposition. J. Mol. Biol. 284:287-96
45. Jeltsch A, Alves J, Wolfes H, Maass G, Pingoud A. 1994. Pausing of the restriction endonuclease EcoRI during linear diffusion on DNA. Biochemistry 33:10215-19
46. Kingston IJ, Gormley NA, Halford SE. 2003. DNA supercoiling enables the Type IIS restriction enzyme BspMI to recognise the relative orientation of two DNA sequences. Nucleic Acids Res. 31:5221-28
47. Klenin KV, Langowski J. 2001. Intrachain reactions of supercoiled DNA simulated by Brownian dynamics. Biophys. J. 81:1924-29
48. Kong H, Lin LF, Porter N, Stickel S, Byrd D, et al. 2000. Functional analysis of putative restriction-modification system genes in the Helicobacter pylori J99 genome. Nucleic Acids Res. 28:3216-23
49. Kong H, Smith CL. 1998. Does BcgI, a unique restriction endonuclease, require two sites for cleavage? Biol. Chem. 379:605-9
50. Krüger DH, Barcak GJ, Reuter M, Smith HO. 1988. EcoRII can be activated to cleave refractory DNA recognition sites. Nucleic Acids Res. 11:3997-4008
51. Kull FJ. 2000. Motor proteins of the kinesin superfamily: structure and mechanism. Essays Biochem. 35:61-73
52. Lagunavicius A, Sasnauskas G, Halford SE, Siksnys V. 2003. The metal-independent type IIs restriction enzyme BfiI is a dimer that binds two DNA sites but has only one catalytic centre. J. Mol. Biol. 326:1051-64
53. Liu LF, Wang JC. 1987. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84:7024-27
54. Lloyd G, Landini P, Busby S. 2001. Activation and repression of transcription initiation in bacteria. Essays Biochem. 37:17-31
55. Masse E, Drolet M. 1999. Relaxation of transcription-induced negative supercoiling is an essential function of Escherichia coli DNA topoisomerase I. J. Biol. Chem. 274:16654-58
56. Meisel A, Mackeldanz P, Bickle TA, Krüger DH, Schroeder C. 1995. Type III restriction endonucleases translocate DNA in a reaction driven by recognition site-specific ATP hydrolysis. EMBO J. 14:2958-66
57. Milsom SE, Halford SE, Embleton ML, Szczelkun MD. 2001. Analysis of DNA looping interactions by type II restriction enzymes that require two copies of their recognition sites. J. Mol. Biol. 311:515-27
58. Mizuuchi K, Adzuma K. 1991. Inversion of the phosphate chirality at the target site of Mu DNA strand transfer: evidence for a one-step transesterification mechanism. Cell 66:129-40
59. Mizuuchi K, Nobbs TJ, Halford SE, Adzuma K, Qin J. 1999. A new method for determining the stereochemistry of DNA cleavage reactions: application to the SfiI and HpaII restriction endonucleases and to the MuA transposase. Biochemistry 38:4640-48
60. Mucke M, Grelle G, Behlke J, Kraft R, Krüger DH, Reuter M. 2002. EcoRII: a restriction enzyme evolving recombination functions? EMBO J. 21:5262-68
61. Nelson P. 1999. Transport of torsional stress in DNA. Proc. Natl. Acad. Sci. USA 96:14342-47
62. Nobbs TJ, Halford SE. 1995. DNA cleavage at two recognition sites by the SfiI restriction endonuclease: salt dependence of cis and trans interactions between distant DNA sites. J. Mol. Biol. 252:399-411
63. Nobbs TJ, Szczelkun MD, Wentzell LM, Halford SE. 1998. DNA excision by the SfiI restriction endonuclease. J. Mol. Biol. 281:419-32
64. Ogata K, Sato K, Tahirov T. 2003. Eukaryotic transcriptional regulatory complexes: cooperativity from near and afar. Curr. Opin. Struct. Biol. 13:40-48
65. Ostrander EA, Benedetti P, Wang JC. 1990. Template supercoiling by a chimera of yeast GAL4 protein and phage T7 RNA polymerase. Science 249:1261-65
66. Panne D, Raleigh EA, Bickle TA. 1999. The McrBC endonuclease translocates DNA in a reaction dependent on GTP hydrolysis. J. Mol. Biol. 290:49-60
67. Peakman LJ, Antognozzi M, Bickle TA, Janscak P, Szczelkun MD. 2003. S-Adenosyl methionine prevents promiscuous DNA cleavage by the EcoP1I type III restriction enzyme. J. Mol. Biol. 333:321-35
68. Pingoud A, Jeltsch A. 2001. Structure and function of type II restriction endonucleases. Nucleic Acids Res. 29:3705-27
69. Powell LM, Dryden DT, Murray NE. 1998. Sequence-specific DNA binding by EcoKI, a type IA DNA restriction enzyme. J. Mol. Biol. 283:963-76
70. Rippe K. 2001. Making contacts on a nucleic acid polymer. Trends Biochem. Sci. 26:733-40
71. Rippe K, von Hippel PH, Langowski J. 1995. Action at a distance: DNA-looping and initiation of transcription. Trends Biochem. Sci. 20:500-6
72. Ristic D, Wyman C, Paulusma C, Kanaar R. 2001 The architecture of the human Rad54-DNA complex provides evidence for protein translocation along DNA. Proc. Natl. Acad. Sci. USA 98:8454-60
73. Roberts RJ, Belfort M, Bestor T, Bhagwat AS, Bickle TA, et al. 2003. A nomenclature for restriction enzymes, DNA methyl-transferases, homing endonucleases and their genes. Nucleic Acids Res. 31:1805-12
74. Roberts RJ, Vincze T, Posfai J, Macelis D. 2003. REBASE: restriction enzymes and methylases. Nucleic Acids Res. 31:418-20
75. Rosamond J, Endlich B, Linn S. 1979. Electron microscopic studies of the mechanism of action of the restriction endonuclease of Escherichia coli B. J. Mol. Biol. 129:619-35
76. Sarkar A, Leger JF, Chatenay D, Marko JF. 2001. Structural transitions in DNA driven by external force and torque. Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 63:051903
77. Sasnauskas G, Halford SE, Siksnys V. 2003. How the BfiI restriction enzyme uses one active site to cut two DNA strands. Proc. Natl. Acad. Sci. USA 100:6410-15
78. Schleif R. 1992. DNA looping. Annu. Rev. Biochem. 61:199-223
79. Schneider R, Lurz R, Lüder G, Tolksdorf C, Travers A, Muskhelishvili G. 2001. An architectural role of the Escherichia coli chromatin protein FIS in organising DNA. Nucleic Acids. Res. 29:5107-14
80. Siksnys V, Skirgalia R, Sasnauskas G, Urbanke C, Cherny D, et al. 1999. The Cfr10I restriction enzyme is functional as a tetramer. J. Mol. Biol. 291:1105-18
81. Singleton MR, Scaife S, Wigley DB. 2001. Structural analysis of DNA replication fork reversal by RecG. Cell 107:79-89
82. Soundararajan M, Chang Z, Morgan RD, Heslop P, Connolly BA. 2002. DNA binding and recognition by the IIs restriction endonuclease MboII. J. Biol. Chem. 277:887-95
83. Stanford NP, Szczelkun MD, Marko JF, Halford SE. 2000. One- and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J. 19:6546-57
84. Stewart FJ, Raleigh EA. 1998. Dependence of McrBC cleavage on distance between recognition elements. Biol. Chem. 379:611-16
85. Stone MD, Bryant Z, Crisona NJ, Smith SB, Vologodskii A, et al. 2003. Chirality sensing by Escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl. Acad. Sci. USA 100:8654-59
86. Svejstrup JQ. 2002. Transcription repair coupling factor: a very pushy enzyme. Mol. Cell. 9:1151-52
87. Szczelkun MD. 2002. Kinetic models of translocation, head-on collision, and DNA cleavage by type I restriction endonucleases. Biochemistry 41:2067-74
88. Szczelkun MD, Dillingham MS, Janscak P, Firman K, Halford SE. 1996. Repercussions of DNA tracking by the type IC restriction endonuclease EcoR124I on linear, circular and catenated substrates. EMBO J. 15:6335-47
89. Szczelkun MD, Halford SE. 1996. Recombination by resolvase to analyse DNA communications by the SfiI restriction endonuclease. EMBO J. 15:1460-69
90. Taylor JD, Goodall AJ, Vermote CL, Halford SE. 1990. Fidelity of DNA recognition by the EcoRV restriction-modification system in vivo. Biochemistry 29:10727-33
91. Terry BJ, Jack WE, Modrich P. 1985. Facilitated diffusion during catalysis by EcoRI endonuclease. Nonspecific interactions in EcoRI catalysis. J. Biol. Chem. 260:13130-37
92. Tsao YP, Wu HY, Liu LF. 1989. Transcription-driven supercoiling of DNA: direct biochemical evidence from in vitro studies. Cell 56:111-18
93. Vanamee ES, Santagata S, Aggarwal AK. 2001. FokI requires two specific DNA sites for cleavage. J. Mol. Biol. 309:69-78
94. Van Duyne GD. 2001. A structural view of Cre-loxP site-specific recombination. Annu. Rev. Biophys. Biomol. Struct. 30:87-104
95. Van Komen S, Petukhova G, Sigurdsson S, Stratton S, Sung P. 2000. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell 6:563-72
96. Vologodskii A, Cozzarelli NR. 1996. Effect of supercoiling on the juxtaposition and relative orientation of DNA sites. Biophys. J. 70:2548-56
97. von Hippel PH, Berg OG. 1989. Facilitated target location in biological systems. J. Biol. Chem. 264:675-78
98. Wah DA, Bitinaite J, Schildkraut I, Aggarwal AK. 1998. Structure of FokI has implications for DNA cleavage. Proc. Natl. Acad. Sci. USA 95:10564-69
99. Wah DA, Hirsch JA, Dorner LF, Schildkraut I, Aggarwal AK. 1997. Structure of the multimodular endonuclease FokI bound to DNA. Nature 388:97-100
100. Wang JC, Giaever GN. 1988. Action at a distance along a DNA. Science 240:300-4
101. Wang Z, Droge P. 1997. Long-range effects in a supercoiled DNA domain generated by transcription in vitro. J. Mol. Biol. 271:499-510
102. Watson MA, Gowers DM, Halford SE. 2000. Alternative geometries of DNA looping: an analysis using the SfiI endonuclease. J. Mol. Biol. 298:461-75
103. Wentzell LM, Halford SE. 1998. DNA looping by the SfiI restriction endonuclease. J. Mol. Biol. 281:433-44
104. Wentzell LM, Nobbs TJ, Halford SE. 1995. The SfiI restriction endonuclease makes a four-strand DNA break at two copies of its recognition sequence. J. Mol. Biol. 248:581-95
105. Whitehouse I, Stockdale C, Flaus A, Szczelkun MD, Owen-Hughes T. 2003. Evidence for DNA translocation by the ISWI chromatin-remodeling enzyme. Mol. Cell Biol. 23(6):1935-45
106. Williams SA, Halford SE. 2002. Communications between catalytic sites in the protein-DNA synapse by the SfiI endonuclease. J. Mol. Biol. 318:387-94
107. Yuan R, Hamilton DL, Burckhardt J. 1980. DNA translocation by the restriction enzyme from E. coli K. Cell 20:237-44