DNA looping provides for "intersegmental Hopping" by proteins: A mechanism for long-range site localization

Journal of Molecular Biology

Volumn 426, Issue 21, 2014, Pages 3539-3552

  Pollak, Adam J ^a   Chin, Aaron T ^a   Brown, Frank L H ^a   Reich, Norbert O ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA methyltransferase; DNA structure; facilitated diffusion; intersegmental transfer; processivity

Indexed keywords

DNA ADENINE METHYLTRANSFERASE; DNA BINDING PROTEIN; REGULATOR PROTEIN; RESTRICTION ENDONUCLEASE; TRANSCRIPTION FACTOR; ADENINE; DNA; PROTEIN BINDING; SITE SPECIFIC DNA METHYLTRANSFERASE (ADENINE SPECIFIC);

ARTICLE; DNA BINDING; DNA CONFORMATION; DNA FLANKING REGION; DNA LOOPING; DNA METHYLATION; DNA STRAND; ENZYME MODIFICATION; GENE CONTROL; GENE LOCATION; INTERACTIONS WITH DNA; NUCLEOTIDE BINDING SITE; POLYACRYLAMIDE GEL ELECTROPHORESIS; BINDING SITE; CHEMISTRY; CONFORMATION; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GENOME;

BACTERIA (MICROORGANISMS);

ADENINE; BINDING SITES; DNA; DNA METHYLATION; DNA RESTRICTION ENZYMES; ESCHERICHIA COLI; GENOME; MOLECULAR CONFORMATION; PROTEIN BINDING; SITE-SPECIFIC DNA-METHYLTRANSFERASE (ADENINE-SPECIFIC);

EID: 84907843278     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.08.002     Document Type: Article

References (59)

1. O.G. Berg, R.B. Winter, and P.H. von Hippel Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory Biochemistry 20 1981 6929 6948
2. S.E. Halford An end to 40 years of mistakes in DNA-protein association kinetics? Biochem Soc Trans 37 2009 343 348
3. P. Hammar, P. Leroy, A. Mahmutovic, E.G. Marklund, O.G. Berg, and J. Elf The lac repressor displays facilitated diffusion in living cells Science 336 2012 1595 1598
4. J. Iwahara, and G.M. Clore Detecting transient intermediates in macromolecular binding by paramagnetic NMR Nature 440 2006 1227 1230
5. A. Esadze, and J. Iwahara Stopped-flow fluorescence kinetic study of protein sliding and intersegmental transfer in the target DNA search process J Mol Biol 426 2014 230 244
6. H.X. Zhou Rapid search for specific sites on DNA through conformational switch of non-specifically bound proteins Proc Natl Acad Sci USA 108 2011 8651 8656
7. M. Hedglin, and P.J. O'Brien Hopping enables a DNA repair glycosylase to search both strands and bypass a bound protein ACS Chem Biol 5 2010 427 436
8. J.D. Schonhoft, and J.T. Stivers Timing facilitated site transfer of an enzyme on DNA Nat Chem Biol 8 2012 205 210
9. G.W. Li, O.G. Berg, and J. Elf Effect of macromolecular crowding and DNA looping on gene regulation kinetics Nat Phys 5 2009 294 297
10. 6-methyl-adenine: an epigenetic signal for DNA-protein interactions Nat Rev Microbiol 4 2006 183 192
11. D.M. Heithoff, R.L. Sinsheimer, D.A. Low, and M.J. Mahan An essential role for DNA adenine methylation in bacterial virulence Science 284 1999 967 970
12. N.P. Stanford, M.D. Szczelkun, J.F. Marko, and S.E. Halford One- and three-dimensional pathways for proteins to reach specific DNA sites EMBO J 19 2000 6546 6557
13. R.H. Porecha, and J.T. Stivers Uracil DNA glycosylase uses DNA hopping and short-range sliding to trap extrahelical uracils Proc Natl Acad Sci USA 105 2008 10791 10796
14. S.E. Halford, and J.F. Marko How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res 32 2004 3040 3052
15. T. Hu, A.Y. Grosberg, and B.I. Shklovskii How proteins search for their specific sites on DNA: the role of DNA confirmation Biophys J 90 2006 2731 2744
16. A.J. Pollak, and N.O. Reich Proximal recognition sites facilitate intrasite hopping by DNA adenine methyltransferase: mechanistic exploration of epigenetic gene regulation J Biol Chem 287 2012 22873 22881
17. A. Fersht Structure and mechanism in protein science 1998 W. H. Freeman New York
18. J. Langowski, J. Alves, A. Pingoud, and G. Maass Does the specific recognition of DNA by the restriction endonuclease EcoRI involve a linear diffusion step? Investigation of the processivity of the EcoRI endonuclease Nucleic Acids Res 11 1983 501 513
19. S.N. Peterson, and N.O. Reich GATC flanking sequences regulate Dam activity: evidence for how Dam specificity may influence pap expression J Mol Biol 355 2006 459 472
20. O.P. Ryabinina, I.G. Minko, M.R. Lasarev, A.K. McCullough, and R.S. Lloyd Modulation of the processive abasic site lyase activity of a pyrimidine dimer glycosylase DNA Repair 10 2011 1014 1022
21. D. Shore, J. Langowski, and R.L. Baldwin DNA flexibility studied by covalent closure of short fragments into circles Proc Natl Acad Sci USA 78 1981 4833 4837
22. L. Ringrose, and S. Chabanis Quantitative comparison of DNA looping in vitro and in vivo: chromatin increases effective DNA flexibility at short distances EMBO J 18 1999 6630 6641
23. J. Shimada, and H. Yamakawa Ring closure probabilities for twisted wormlike chains. Application to DNA Macromolecules 17 1984 689 698
24. P.J. Hagerman, and V.A. Ramadevi Application of the method of phage T4 DNA ligase-catalyzed ring-closure to the study of DNA structure J Mol Biol 212 1990 351 362
25. S. Geggier, and A. Vologodskii Sequence dependence of DNA bending rigidity Proc Natl Acad Sci USA 107 2010 15421 15426
26. C.G. Baumann, S.B. Smith, V.A. Bloomfield, and C. Bustamante Ionic effects on the elasticity of single DNA molecules Proc Natl Acad Sci USA 94 1997 6185 6190
27. L.M. Wentzell, and S.E. Halford DNA looping by the Sfi I restriction endonuclease J Mol Biol 281 1998 433 444
28. L.E. Catto, S. Ganguly, S.E. Milsom, A.J. Welsh, and S.E. Halford Protein assembly and DNA looping by the FokI restriction endonuclease Nucleic Acids Res 34 2006 1711 1720
29. P. Friedhoff, R. Lurz, G. Luder, and A. Pingoud Sau3AI, a monomeric type II restriction endonuclease that dimerizes on the DNA and thereby induces DNA loops J Biol Chem 276 2001 23581 23588
30. S.R. Coffin, and N.O. Reich Escherichia coli DNA adenine methyltransferase: intrasite processivity and substrate-induced dimerization and activation Biochemistry 48 2009 7399 7410
31. J.R. Horton, K. Liebert, M. Bekes, A. Jeltsch, and X. Cheng Structure and substrate recognition of Escherichia coli DNA adenine methyltransferase J Mol Biol 358 2006 559 570
32. D. Vuzman, A. Azia, and Y. Levy Searching DNA via a "monkey bar" mechanism: the significance of disordered tails J Mol Biol 396 2010 674 684
33. J. Iwahara, M. Zweckstetter, and G.M. Clore NMR structural and kinetic characterization of a homeodomain diffusing and hopping on nonspecific DNA Proc Natl Acad Sci USA 103 2006 15062 15067
34. M. Doucleft, and G.M. Clore Global jumping and domain-specific intersegmental transfer between DNA cognate site of the same multidomain transcription factor Oct-1 Proc Natl Acad Sci USA 105 2008 13871 13876
35. J. Iwahara, and G.M. Clore Direct observations of enhanced translocations of a homeodomain between DNA cognate sites by NMR exchange spectroscopy J Am Chem Soc 128 2006 404 405
36. H. Tjong, and H.X. Zhou DISPLAR: an accurate method for predicting DNA-binding sites on protein surface Nucleic Acids Res 35 2007 1465 1477
37. N.Y. Sidorova, T. Scott, and D.C. Rau DNA concentration dependent dissociation of EcoRI: direct transfer or reaction during hopping Biophys J 104 2013 1296 13039
38. B. van den Broek, M.A. Lomholt, S.M.J. Kalisch, R. Metzler, and G.J.L. Wuite How DNA coiling enhances target localization by proteins Proc Natl Acad Sci USA 105 2008 1578 15742
39. D.M. Gowers, and S.E. Halford Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling EMBO J 22 2003 1410 1418
40. M. Hedglin, Y. Zhang, and P.J. O'Brien Isolating contributions from intersegmental transfer to DNA searching by alkyladenine DNA glycosylase J Biol Chem 288 2013 24550 24559
41. D.C. Rau, and N.Y. Sidorova Diffusion of the restriction nuclease EcoRI along DNA J Mol Biol 395 2010 408 416
42. B.J. Terry, W.E. Jack, and P. Modrich Facilitated diffusion during catalysis by EcoRI endonucleases. Non-specific interactions in EcoRI catalysis J Biol Chem 260 1985 13130 13137
43. H.S. Koo, H.M. Wu, and D.M. Crothers DNA bending at adenine thymine tracts Nature 320 1986 501 506
44. H.S. Koo, J. Drak, J.A. Rice, and D.M. Crothers Determination of the extent of DNA bending by an adenine-thymine tract Biochemistry 29 1990 4227 4234
45. S.S. Zinkel, and D.M. Crothers DNA bend direction by phase sensitive detection Nature 328 1987 178 181
46. J.D. Kahn, and D.M. Crothers Protein-induced bending and DNA cyclization Proc Natl Acad Sci USA 89 1992 6343 6347
47. R. Stefl, H. Wu, S. Ravindranathan, V. Sklenar, and J. Feigon DNA A-tract bending in three dimensions: solving the dA4T4 vs. dT4A4 conundrum Proc Natl Acad Sci USA 101 2004 1177 1182
48. K. Vlahovicek, L. Kajan, and S. Pongor DNA analysis servers: plot.it, bend.it, model.it and IS Nucleic Acids Res 31 2003 3686 3687
49. J.I. Friedman, and J.T. Stivers Detection of damaged DNA bases by DNA glycosylase enzymes Biochemistry 49 2010 4957 4967
50. S. Ghaemmaghami, W.K. Huh, K. Bower, R.W. Howson, A. Belle, and N. Dephoure Global analysis of protein expression in yeast Nature 425 2003 737 741
51. J. Elf, G.W. Li, and X.S. Xie Probing transcription factor dynamics at the single-molecule level in a living cell Science 316 2007 1191 1194
52. D.M. Gowers, G.G. Wilson, and S.E. Halford Measurement of the contributions of 1D and 3D pathways to the translocation of a protein along DNA Proc Natl Acad Sci USA 102 2005 15883 15888
53. D.T. Bilcock, L.E. Daniels, A.J. Bath, and S.E. Halford Reactions of type II restriction endonucleases with 8-base pair recognition sites J Biol Chem 274 1999 36379 36386
54. N.A. Gormley, A.J. Bath, and S.E. Halford Reactions of BglI and other type II restriction endonucleases with discontinuous recognition sites J Biol Chem 275 2000 6928 6936
55. G. Sasnauskas, L. Zakrys, M. Zaremba, R. Cosstick, J.W. Gaynor, and S.E. Halford A novel mechanism for the scission of double-stranded DNA: BfiI cuts both 3′-5′ and 5′-3′ strands by rotating a single active site Nucleic Acids Res 38 2010 2399 2410
56. G. Sasnauskas, G. Kostiuk, G. Tamulaitis, and V. Siksynys Target site cleavage by the monomeric restriction enzyme BcnI requires translocation to a random DNA sequence and a switch in enzyme orientation Nucleic Acids Res 39 2011 8844 8856
57. A.D. Hernday, B.A. Braaten, and D.A. Low The mechanism by which DNA adenine methylase and papI activate the pap epigenetic switch Mol Cell 12 2003 947 957
58. A. Pluciennik, and P. Modrich Protein roadblocks and helix discontinuities are barriers to the initiation of mismatch repair Proc Natl Acad Sci USA 104 2007 12709 12713
59. T.A. Kunkel, and D.A. Erie DNA mismatch repair Annu Rev Biochem 74 2005 681 710