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Dynamics and Mechanism of DNA-Bending Proteins in Binding Site Recognition

  • Anjum Ansari
  • Serguei V. Kuznetsov
Chapter
Part of the Biological and Medical Physics, Biomedical Engineering book series (BIOMEDICAL)

Abstract

The three-dimensional shape of biological macromolecules (proteins, DNA, and RNA), is determined by a myriad of “weak” noncovalent interactions (ionic, hydrophobic, van der Waals, and hydrogen bonds), each of which can be disrupted by thermal fluctuations, leading to constantly changing conformations accessible to the macromolecule [1]. These conformational fluctuations are essential to biology and are central to molecular recognition, in which two or more interacting macromolecules rely on complementary shapes and charge distributions to form a multitude of weak intermolecular bonds that lead to higher-order complexes. An overarching goal in molecular biophysics is to elucidate the underlying energetics of these interactions, by measuring the dynamics of conformational fluctuations in the macromolecular complexes.

Keywords

Forster Resonance Energy Transfer Persistence Length Cocrystal Structure Integration Host Factor Crick Base Pair 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

We thank the present and former members of the Ansari laboratory: Paula Vivas, Yogambigai Velmurugu and Ranjani Narayanan, for their help and for many discussions. We are grateful to James Maher and Phoebe Rice for critical reading of the manuscript and for their incisive comments and suggestions. We are especially indebted to Phoebe Rice for her offer and help in making all illustrations of protein structures shown in this chapter. A.A acknowledges support from the National Science Foundation (MCB-0721937). S.V.K. acknowledges support from the American Heart Association (AHA 0730254N).

References

  1. 1.
    Alberts B, Bray D, Lewis J, Raff M, Roberts K, Watson JD (1989) Molecular biology of the cell. Garland, New YorkGoogle Scholar
  2. 2.
    Riggs AD, Bourgeois S, Cohn M (1970) The lac repressor-operator interaction. 3. Kinetic studies. J Mol Biol 53:401–417CrossRefGoogle Scholar
  3. 3.
    Berg OG, Winter RB, von Hippel PH (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 20:6929–6948CrossRefGoogle Scholar
  4. 4.
    Winter RB, Berg OG, von Hippel PH (1981) Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor–operator interaction: kinetic measurements and conclusions. Biochemistry 20:6961–6977CrossRefGoogle Scholar
  5. 5.
    von Hippel PH, Berg OG (1989) Facilitated target location in biological systems. J Biol Chem 264:675–678Google Scholar
  6. 6.
    Stanford NP, Szczelkun MD, Marko JF, Halford SE (2000) One- and three-dimensional pathways for proteins to reach specific DNA sites. EMBO J 19:6546–6557CrossRefGoogle Scholar
  7. 7.
    Halford SE, Marko JF (2004) How do site-specific DNA-binding proteins find their targets? Nucleic Acids Res 32:3040–3052CrossRefGoogle Scholar
  8. 8.
    Spolar RS, Record MT Jr (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263:777–784ADSCrossRefGoogle Scholar
  9. 9.
    Garvie CW, Wolberger C (2001) Recognition of specific DNA sequences. Mol Cell 8:937–946CrossRefGoogle Scholar
  10. 10.
    Kalodimos CG, Biris N, Bonvin AM, Levandoski MM, Guennuegues M, Boelens R, Kaptein R (2004) Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes. Science 305:386–389ADSCrossRefGoogle Scholar
  11. 11.
    von Hippel PH (2004) Biochemistry. Completing the view of transcriptional regulation. Science 305:350–352CrossRefGoogle Scholar
  12. 12.
    Slutsky M, Mirny LA (2004) Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys J 87:4021–4035CrossRefGoogle Scholar
  13. 13.
    Rice PA (2008) Introduction. In: Correll CC, Rice PA, Correll CC (eds) Protein-nucleic acid interactions. Royal Society of Chemistry, CambridgeCrossRefGoogle Scholar
  14. 14.
    Beamer LJ, Pabo CO (1992) Refined 1.8 A crystal structure of the lambda repressor-operator complex. J Mol Biol 227:177–196CrossRefGoogle Scholar
  15. 15.
    Aggarwal AK, Rodgers DW, Drottar M, Ptashne M, Harrison SC (1988) Recognition of a DNA operator by the repressor of phage 434: a view at high resolution. Science 242:899–907ADSCrossRefGoogle Scholar
  16. 16.
    Otwinowski Z, Schevitz RW, Zhang RG, Lawson CL, Joachimiak A, Marmorstein RQ, Luisi BF, Sigler PB (1988) Crystal structure of trp repressor/operator complex at atomic resolution. Nature 335:321–329ADSCrossRefGoogle Scholar
  17. 17.
    Ellenberger TE, Brandl CJ, Struhl K, Harrison SC (1992) The GCN4 basic region leucine zipper binds DNA as a dimer of uninterrupted alpha helices: crystal structure of the protein–DNA complex. Cell 71:1223–1237CrossRefGoogle Scholar
  18. 18.
    Foster MP, Wuttke DS, Radhakrishnan I, Case DA, Gottesfeld JM, Wright PE (1997) Domain packing and dynamics in the DNA complex of the N-terminal zinc fingers of TFIIIA. Nat Struct Biol 4:605–608CrossRefGoogle Scholar
  19. 19.
    Lawson CL, Berman HM (2008) Indirect readout of DNA sequence by proteins. In: Rice PA, Correll CC (eds) Protein-nucleic acid interactions. Royal Society of Chemistry, CambridgeGoogle Scholar
  20. 20.
    Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389:251–260ADSCrossRefGoogle Scholar
  21. 21.
    Richmond TJ, Davey CA (2003) The structure of DNA in the nucleosome core. Nature 423:145–150ADSCrossRefGoogle Scholar
  22. 22.
    Werner MH, Gronenborn AM, Clore GM (1996) Intercalation, DNA kinking, and the control of transcription. Science 271:778–784ADSCrossRefGoogle Scholar
  23. 23.
    Rice PA, Yang S, Mizuuchi K, Nash HA (1996) Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn. Cell 87:1295–1306CrossRefGoogle Scholar
  24. 24.
    Mouw KM, Rice PA (2007) Shaping the Borrelia burgdorferi genome: crystal structure and binding properties of the DNA-bending Hbb. Mol Microbiol 63:1319–1330CrossRefGoogle Scholar
  25. 25.
    Kalodimos CG, Bonvin AM, Salinas RK, Wechselberger R, Boelens R, Kaptein R (2002) Plasticity in protein-DNA recognition: lac repressor interacts with its natural operator 01 through alternative conformations of its DNA-binding domain. EMBO J 21:2866–2876CrossRefGoogle Scholar
  26. 26.
    Kim Y, Geiger JH, Hahn S, Sigler PB (1993) Crystal structure of a yeast TBP/TATA-box complex. Nature 365:512–520ADSCrossRefGoogle Scholar
  27. 27.
    Winkler FK, Banner DW, Oefner C, Tsernoglou D, Brown RS, Heathman SP, Bryan RK, Martin PD, Petratos K, Wilson KS (1993) The crystal structure of EcoRV endonuclease and of its complexes with cognate and non-cognate DNA fragments. EMBO J 12:1781–1795Google Scholar
  28. 28.
    Obmolova G, Ban C, Hsieh P, Yang W (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407:703–710ADSCrossRefGoogle Scholar
  29. 29.
    Lamers MH, Perrakis A, Enzlin JH, Winterwerp HH, de Wind N, Sixma TK (2000) The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature 407:711–717ADSCrossRefGoogle Scholar
  30. 30.
    Howard J (2001) Mechanics of motor proteins and the cytoskeleton. Sinauer Associates, SunderlandGoogle Scholar
  31. 31.
    Hogan M, Dattagupta N, Crothers DM (1978) Transient electric dichroism of rod-like DNA molecules. Proc Natl Acad Sci USA 75:195–199ADSCrossRefGoogle Scholar
  32. 32.
    Hagerman PJ (1981) Investigation of the flexibility of DNA using transient electric birefringence. Biopolymers 20:1503–1535CrossRefGoogle Scholar
  33. 33.
    Hogan M, LeGrange J, Austin B (1983) Dependence of DNA helix flexibility on base composition. Nature 304:752–754ADSCrossRefGoogle Scholar
  34. 34.
    Shore D, Langowski J, Baldwin RL (1981) DNA flexibility studied by covalent closure of short fragments into circles. Proc Natl Acad Sci USA 78:4833–4837ADSCrossRefGoogle Scholar
  35. 35.
    Levene SD, Crothers DM (1986) Ring closure probabilities for DNA fragments by Monte Carlo simulation. J Mol Biol 189:61–72CrossRefGoogle Scholar
  36. 36.
    Crothers DM, Drak J, Kahn JD, Levene SD (1992) DNA bending, flexibility, and helical repeat by cyclization kinetics. Methods Enzymol 212:3–29CrossRefGoogle Scholar
  37. 37.
    Bustamante C, Marko JF, Siggia ED, Smith S (1994) Entropic elasticity of lambda-phage DNA. Science 265:1599–1600ADSCrossRefGoogle Scholar
  38. 38.
    Bustamante C, Smith SB, Liphardt J, Smith D (2000) Single-molecule studies of DNA mechanics. Curr Opin Struct Biol 10:279–285CrossRefGoogle Scholar
  39. 39.
    Marko JF, Siggia ED (1995) Stretching DNA. Macromolecules 28:8759–8770ADSCrossRefGoogle Scholar
  40. 40.
    Baumann CG, Smith SB, Bloomfield VA, Bustamante C (1997) Ionic effects on the elasticity of single DNA molecules. Proc Natl Acad Sci USA 94:6185–6190ADSCrossRefGoogle Scholar
  41. 41.
    Roychoudhury M, Sitlani A, Lapham J, Crothers DM (2000) Global structure and mechanical properties of a 10-bp nucleosome positioning motif. Proc Natl Acad Sci USA 97:13608–13613ADSCrossRefGoogle Scholar
  42. 42.
    Zhang Y, Crothers DM (2003) High-throughput approach for detection of DNA bending and flexibility based on cyclization. Proc Natl Acad Sci USA 100:3161–3166ADSCrossRefGoogle Scholar
  43. 43.
    Satchwell SC, Drew HR, Travers AA (1986) Sequence periodicities in chicken nucleosome core DNA. J Mol Biol 191:659–675CrossRefGoogle Scholar
  44. 44.
    Widom J (2001) Role of DNA sequence in nucleosome stability and dynamics. Q Rev Biophys 34:269–324CrossRefGoogle Scholar
  45. 45.
    Drew HR, Travers AA (1985) DNA bending and its relation to nucleosome positioning. J Mol Biol 186:773–790CrossRefGoogle Scholar
  46. 46.
    Lowary PT, Widom J (1997) Nucleosome packaging and nucleosome positioning of genomic DNA. Proc Natl Acad Sci USA 94:1183–1188ADSCrossRefGoogle Scholar
  47. 47.
    Lowary PT, Widom J (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J Mol Biol 276:19–42CrossRefGoogle Scholar
  48. 48.
    Segal E, Fondufe-Mittendorf Y, Chen L, Thastrom A, Field Y, Moore IK, Wang JP, Widom J (2006) A genomic code for nucleosome positioning. Nature 442:772–778ADSCrossRefGoogle Scholar
  49. 49.
    Anderson JE, Ptashne M, Harrison SC (1987) Structure of the repressor-operator complex of bacteriophage 434. Nature 326:846–852ADSCrossRefGoogle Scholar
  50. 50.
    Koudelka GB, Harrison SC, Ptashne M (1987) Effect of non-contacted bases on the affinity of 434 operator for 434 repressor and Cro. Nature 326:886–888ADSCrossRefGoogle Scholar
  51. 51.
    Hogan ME, Austin RH (1987) Importance of DNA stiffness in protein-DNA binding specificity. Nature 329:263–266ADSCrossRefGoogle Scholar
  52. 52.
    Zimmerman JM, Maher LJ 3rd (2003) Solution measurement of DNA curvature in papillomavirus E2 binding sites. Nucleic Acids Res 31:5134–5139CrossRefGoogle Scholar
  53. 53.
    Zhang Y, Xi Z, Hegde RS, Shakked Z, Crothers DM (2004) Predicting indirect readout effects in protein-DNA interactions. Proc Natl Acad Sci USA 101:8337–8341ADSCrossRefGoogle Scholar
  54. 54.
    Kim SS, Tam JK, Wang AF, Hegde RS (2000) The structural basis of DNA target discrimi­nation by papillomavirus E2 proteins. J Biol Chem 275:31245–31254CrossRefGoogle Scholar
  55. 55.
    Hardwidge PR, Zimmerman JM, Maher LJ 3rd (2000) Design and calibration of a semi-synthetic DNA phasing assay. Nucleic Acids Res 28:E102CrossRefGoogle Scholar
  56. 56.
    Crick FH, Klug A (1975) Kinky helix. Nature 255:530–533ADSCrossRefGoogle Scholar
  57. 57.
    Hogan ME, Rooney TF, Austin RH (1987) Evidence for kinks in DNA folding in the nucleosome. Nature 328:554–557ADSCrossRefGoogle Scholar
  58. 58.
    Cloutier TE, Widom J (2004) Spontaneous sharp bending of double-stranded DNA. Mol Cell 14:355–362CrossRefGoogle Scholar
  59. 59.
    Cloutier TE, Widom J (2005) DNA twisting flexibility and the formation of sharply looped protein-DNA complexes. Proc Natl Acad Sci USA 102:3645–3650ADSCrossRefGoogle Scholar
  60. 60.
    Yan J, Marko JF (2004) Localized single-stranded bubble mechanism for cyclization of short double helix DNA. Phys Rev Lett 93:108108ADSCrossRefGoogle Scholar
  61. 61.
    Wiggins PA, Phillips R, Nelson PC (2005) Exact theory of kinkable elastic polymers. Phys Rev E 71:021909MathSciNetADSCrossRefGoogle Scholar
  62. 62.
    Du Q, Smith C, Shiffeldrim N, Vologodskaia M, Vologodskii A (2005) Cyclization of short DNA fragments and bending fluctuations of the double helix. Proc Natl Acad Sci USA 102:5397–5402ADSCrossRefGoogle Scholar
  63. 63.
    Forties RA, Bundschuh R, Poirier MG (2009) The flexibility of locally melted DNA. Nucleic Acids Res 37:4580–4586CrossRefGoogle Scholar
  64. 64.
    Du Q, Kotlyar A, Vologodskii A (2008) Kinking the double helix by bending deformation. Nucleic Acids Res 36:1120–1128CrossRefGoogle Scholar
  65. 65.
    Demurtas D, Amzallag A, Rawdon EJ, Maddocks JH, Dubochet J, Stasiak A (2009) Bending modes of DNA directly addressed by cryo-electron microscopy of DNA minicircles. Nucleic Acids Res 37:2882–2893CrossRefGoogle Scholar
  66. 66.
    Wiggins PA, van der Heijden T, Moreno-Herrero F, Spakowitz A, Phillips R, Widom J, Dekker C, Nelson PC (2006) High flexibility of DNA on short length scales probed by atomic force microscopy. Nat Nanotechnol 1:137–141ADSCrossRefGoogle Scholar
  67. 67.
    Yuan C, Chen H, Lou XW, Archer LA (2008) DNA bending stiffness on small length scales. Phys Rev Lett 100:018102ADSCrossRefGoogle Scholar
  68. 68.
    Frank-Kamenetskii F (1971) Simplification of the empirical relationship between melting temperature of DNA, its GC content and concentration of sodium ions in solution. Biopolymers 10:2623–2624CrossRefGoogle Scholar
  69. 69.
    Wartell RM, Benight AS (1982) Fluctuational base-pair opening in DNA at temperatures below the helix-coil transition region. Biopolymers 21:2069–2081CrossRefGoogle Scholar
  70. 70.
    Protozanova E, Yakovchuk P, Frank-Kamenetskii MD (2004) Stacked–unstacked equilibrium at the nick site of DNA. J Mol Biol 342:775–785CrossRefGoogle Scholar
  71. 71.
    Coman D, Russu IM (2005) A nuclear magnetic resonance investigation of the energetics of basepair opening pathways in DNA. Biophys J 89:3285–3292CrossRefGoogle Scholar
  72. 72.
    Mills JB, Hagerman PJ (2004) Origin of the intrinsic rigidity of DNA. Nucleic Acids Res 32:4055–4059CrossRefGoogle Scholar
  73. 73.
    Yakovchuk P, Protozanova E, Frank-Kamenetskii MD (2006) Base-stacking and base-pairing contributions into thermal stability of the DNA double helix. Nucleic Acids Res 34:564–574CrossRefGoogle Scholar
  74. 74.
    SantaLucia J Jr (1998) A unified view of polymer, dumbbell, and oligonucleotide DNA nearest-neighbor thermodynamics. Proc Natl Acad Sci USA 95:1460–1465ADSCrossRefGoogle Scholar
  75. 75.
    Olson WK, Gorin AA, Lu XJ, Hock LM, Zhurkin VB (1998) DNA sequence-dependent deformability deduced from protein-DNA crystal complexes. Proc Natl Acad Sci USA 95:11163–11168ADSCrossRefGoogle Scholar
  76. 76.
    Olson WK, Zhurkin VB (2000) Modeling DNA deformations. Curr Opin Struct Biol 10:286–297CrossRefGoogle Scholar
  77. 77.
    Perez-Howard GM, Weil PA, Beechem JM (1995) Yeast TATA binding protein interaction with DNA: fluorescence determination of oligomeric state, equilibrium binding, on-rate, and dissociation kinetics. Biochemistry 34:8005–8017CrossRefGoogle Scholar
  78. 78.
    Parkhurst KM, Brenowitz M, Parkhurst LJ (1996) Simultaneous binding and bending of promoter DNA by the TATA binding protein: real time kinetic measurements. Biochemistry 35:7459–7465CrossRefGoogle Scholar
  79. 79.
    Dhavan GM, Crothers DM, Chance MR, Brenowitz M (2002) Concerted binding and bending of DNA by Escherichia coli integration host factor. J Mol Biol 315:1027–1037CrossRefGoogle Scholar
  80. 80.
    Hiller DA, Fogg JM, Martin AM, Beechem JM, Reich NO, Perona JJ (2003) Simultaneous DNA binding and bending by EcoRV endonuclease observed by real-time fluorescence. Biochemistry 42:14375–14385CrossRefGoogle Scholar
  81. 81.
    Sugimura S, Crothers DM (2006) Stepwise binding and bending of DNA by Escherichia coli integration host factor. Proc Natl Acad Sci USA 103:18510–18514ADSCrossRefGoogle Scholar
  82. 82.
    Hoopes BC, LeBlanc JF, Hawley DK (1992) Kinetic analysis of yeast TFIID-TATA box complex formation suggests a multi-step pathway. J Biol Chem 267:11539–11547Google Scholar
  83. 83.
    Petri V, Hsieh M, Brenowitz M (1995) Thermodynamic and kinetic characterization of the binding of the TATA binding protein to the adenovirus E4 promoter. Biochemistry 34:9977–9984CrossRefGoogle Scholar
  84. 84.
    Berg OG, Ehrenberg M (1982) Association kinetics with coupled three- and one-dimensional diffusion. Chain-length dependence of the association rate of specific DNA sites. Biophys Chem 15:41–51ADSCrossRefGoogle Scholar
  85. 85.
    Parkhurst KM, Richards RM, Brenowitz M, Parkhurst LJ (1999) Intermediate species ­possessing bent DNA are present along the pathway to formation of a final TBP-TATA complex. J Mol Biol 289:1327–1341CrossRefGoogle Scholar
  86. 86.
    Delgadillo RF, Whittington JE, Parkhurst LK, Parkhurst LJ (2009) The TATA-binding ­protein core domain in solution variably bends TATA sequences via a three-step binding mechanism (dagger). Biochemistry 48:1801–1809CrossRefGoogle Scholar
  87. 87.
    Tolic-Norrelykke SF, Rasmussen MB, Pavone FS, Berg-Sorensen K, Oddershede LB (2006) Stepwise bending of DNA by a single TATA-box binding protein. Biophys J 90:3694–3703CrossRefGoogle Scholar
  88. 88.
    Jacobs-Palmer E, Hingorani MM (2007) The effects of nucleotides on MutS-DNA binding kinetics clarify the role of MutS ATPase activity in mismatch repair. J Mol Biol 366:1087–1098CrossRefGoogle Scholar
  89. 89.
    Erskine SG, Baldwin GS, Halford SE (1997) Rapid-reaction analysis of plasmid DNA cleavage­ by the EcoRV restriction endonuclease. Biochemistry 36:7567–7576CrossRefGoogle Scholar
  90. 90.
    Hopkins BB, Reich NO (2004) Simultaneous DNA binding, bending, and base flipping: ­evidence for a novel M.EcoRI methyltransferase-DNA complex. J Biol Chem 279:37049–37060CrossRefGoogle Scholar
  91. 91.
    van den Broek B, Noom MC, Wuite GJ (2005) DNA-tension dependence of restriction enzyme activity reveals mechanochemical properties of the reaction pathway. Nucleic Acids Res 33:2676–2684CrossRefGoogle Scholar
  92. 92.
    Ali BM, Amit R, Braslavsky I, Oppenheim AB, Gileadi O, Stavans J (2001) Compaction of single DNA molecules induced by binding of integration host factor (IHF). Proc Natl Acad Sci USA 98:10658–10663ADSCrossRefGoogle Scholar
  93. 93.
    Skoko D, Wong B, Johnson RC, Marko JF (2004) Micromechanical analysis of the binding of DNA-bending proteins HMGB1, NHP6A, and HU reveals their ability to form highly stable DNA-protein complexes. Biochemistry 43:13867–13874CrossRefGoogle Scholar
  94. 94.
    McCauley M, Hardwidge PR, Maher LJ 3rd, Williams MC (2005) Dual binding modes for an HMG domain from human HMGB2 on DNA. Biophys J 89:353–364CrossRefGoogle Scholar
  95. 95.
    Skoko D, Yoo D, Bai H, Schnurr B, Yan J, McLeod SM, Marko JF, Johnson RC (2006) Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid ­protein Fis. J Mol Biol 364:777–798CrossRefGoogle Scholar
  96. 96.
    Zhang J, McCauley MJ, Maher LJ 3rd, Williams MC, Israeloff NE (2009) Mechanism of DNA flexibility enhancement by HMGB proteins. Nucleic Acids Res 37:1107–1114CrossRefGoogle Scholar
  97. 97.
    Dixit S, Singh-Zocchi M, Hanne J, Zocchi G (2005) Mechanics of binding of a single integration-host-factor protein to DNA. Phys Rev Lett 94:118101ADSCrossRefGoogle Scholar
  98. 98.
    Reinhard BM, Sheikholeslami S, Mastroianni A, Alivisatos AP, Liphardt J (2007) Use of plasmon coupling to reveal the dynamics of DNA bending and cleavage by single EcoRV restriction enzymes. Proc Natl Acad Sci USA 104:2667–2672ADSCrossRefGoogle Scholar
  99. 99.
    Riggs AD, Bourgeois S, Newby RF, Cohn M (1968) DNA binding of the lac repressor. J Mol Biol 34:365–368CrossRefGoogle Scholar
  100. 100.
    Dyer RB, Gai F, Woodruff WH, Gilmanshin R, Callender RH (1998) Infrared studies of fast events in protein folding. Acc Chem Res 31:709–716CrossRefGoogle Scholar
  101. 101.
    Hofrichter J (2001) Laser temperature-jump methods for studying folding dynamics. In: Murphy KP (ed) Methods in molecular biology. Humana Press, Totowa, NJGoogle Scholar
  102. 102.
    Kubelka J (2009) Time-resolved methods in biophysics. 9. Laser temperature-jump methods for investigating biomolecular dynamics. Photochem Photobiol Sci 8:499–512CrossRefGoogle Scholar
  103. 103.
    Munoz V, Thompson PA, Hofrichter J, Eaton WA (1997) Folding dynamics and mechanism of beta-hairpin formation. Nature 390:196–199ADSCrossRefGoogle Scholar
  104. 104.
    Gruebele M, Sabelko J, Ballew R, Ervin J (1998) Laser temperature jump induced protein refolding. Acc Chem Res 31:699–707CrossRefGoogle Scholar
  105. 105.
    Thompson PA, Munoz V, Jas GS, Henry ER, Eaton WA, Hofrichter J (2000) The helix-coil kinetics of a heteropeptide. J Phys Chem B 104:378–389CrossRefGoogle Scholar
  106. 106.
    Qiu L, Pabit SA, Roitberg AE, Hagen SJ (2002) Smaller and faster: the 20-residue Trp-cage protein folds in 4 micros. J Am Chem Soc 124:12952–12953CrossRefGoogle Scholar
  107. 107.
    Hauser K, Krejtschi C, Huang R, Wu L, Keiderling TA (2008) Site-specific relaxation kinetics of a tryptophan zipper hairpin peptide using temperature-jump IR spectroscopy and isotopic labeling. J Am Chem Soc 130:2984–2992CrossRefGoogle Scholar
  108. 108.
    Ansari A, Kuznetsov SV, Shen Y (2001) Configurational diffusion down a folding funnel describes the dynamics of DNA hairpins. Proc Natl Acad Sci USA 98:7771–7776ADSCrossRefGoogle Scholar
  109. 109.
    Proctor DJ, Ma H, Kierzek E, Kierzek R, Gruebele M, Bevilacqua PC (2004) Thermodynamics and kinetics of YNMG RNA hairpins: incorporation of 8-bromoguanosine leads to stabilization by enhancement of the folding rate. J Am Chem Soc 43:14004–14014Google Scholar
  110. 110.
    Brauns EB, Dyer RB (2005) Time-resolved infrared spectroscopy of RNA folding. Biophys J 89:3523–3530CrossRefGoogle Scholar
  111. 111.
    Kuznetsov SV, Ren C, Woodson SA, Ansari A (2008) Loop dependence of the stability and dynamics of nucleic acid hairpins. Nucleic Acids Res 36:1098–1112CrossRefGoogle Scholar
  112. 112.
    Bonnet G, Tyagi S, Libchaber A, Kramer FR (1999) Thermodynamic basis of the enhanced specificity of structured DNA probes. Proc Natl Acad Sci USA 96:6171–6176ADSCrossRefGoogle Scholar
  113. 113.
    Kim HD, Nienhaus GU, Ha T, Orr JW, Williamson JR, Chu S (2002) Mg2+-dependent ­conformational change of RNA studied by fluorescence correlation and FRET on immobilized single molecules. Proc Natl Acad Sci USA 99:4284–4289ADSCrossRefGoogle Scholar
  114. 114.
    Altan-Bonnet G, Libchaber A, Krichevsky O (2003) Bubble dynamics in double-stranded DNA. Phys Rev Lett 90:138101ADSCrossRefGoogle Scholar
  115. 115.
    Li G, Levitus M, Bustamante C, Widom J (2005) Rapid spontaneous accessibility of nucleosomal DNA. Nat Struct Mol Biol 12:46–53CrossRefGoogle Scholar
  116. 116.
    Kubelka J, Eaton WA, Hofrichter J (2003) Experimental tests of villin subdomain folding simulations. J Mol Biol 329:625–630CrossRefGoogle Scholar
  117. 117.
    Qiu L, Hagen SJ (2004) A limiting speed for protein folding at low solvent viscosity. J Am Chem Soc 126:3398–3399CrossRefGoogle Scholar
  118. 118.
    Kuznetsov SV, Kozlov AG, Lohman TM, Ansari A (2006) Microsecond dynamics of protein-DNA interactions: direct observation of the wrapping/unwrapping kinetics of single-stranded DNA around the E. coli SSB tetramer. J Mol Biol 359:55–65CrossRefGoogle Scholar
  119. 119.
    Hawkins ME, Pfleiderer W, Balis FM, Porter D, Knutson JR (1997) Fluorescence properties of pteridine nucleoside analogs as monomers and incorporated into oligonucleotides. Anal Biochem 244:86–95CrossRefGoogle Scholar
  120. 120.
    Martin GT, Ujvari A, Liu C (2003) Evaluation of fluorescence spectroscopy methods for ­mapping melted regions of DNA along the transcription pathway. Methods Enzymol 371:13–33CrossRefGoogle Scholar
  121. 121.
    Wojtuszewski K, Hawkins ME, Cole JL, Mukerji I (2001) HU binding to DNA: evidence for multiple complex formation and DNA bending. Biochemistry 40:2588–2598CrossRefGoogle Scholar
  122. 122.
    Kuznetsov SV, Sugimura S, Vivas P, Crothers DM, Ansari A (2006) Direct observation of DNA bending/unbending kinetics in complex with DNA-bending protein IHF. Proc Natl Acad Sci USA 103:18515–18520ADSCrossRefGoogle Scholar
  123. 123.
    Vivas P, Kuznetsov SV, Ansari A (2008) New insights into the transition pathway from nonspecific to specific complex of DNA with Escherichia coli integration host factor. J Phys Chem B 112:5997–6007CrossRefGoogle Scholar
  124. 124.
    Swinger KK, Lemberg KM, Zhang Y, Rice PA (2003) Flexible DNA bending in HU-DNA cocrystal structures. EMBO J 22:3749–3760CrossRefGoogle Scholar
  125. 125.
    Grove A, Galeone A, Mayol L, Geiduschek EP (1996) On the connection between inherent DNA flexure and preferred binding of hydroxymethyluracil-containing DNA by the type II DNA-binding protein TF1. J Mol Biol 260:196–206CrossRefGoogle Scholar
  126. 126.
    Grove A, Galeone A, Mayol L, Geiduschek EP (1996) Localized DNA flexibility contributes to target site selection by DNA-bending proteins. J Mol Biol 260:120–125CrossRefGoogle Scholar
  127. 127.
    Swinger KK, Rice PA (2004) IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 14:28–35CrossRefGoogle Scholar
  128. 128.
    Swinger KK, Rice PA (2007) Structure-based analysis of HU-DNA binding. J Mol Biol 365:1005–1016CrossRefGoogle Scholar
  129. 129.
    Aeling KA, Opel ML, Steffen NR, Tretyachenko-Ladokhina V, Hatfield GW, Lathrop RH, Senear DF (2006) Indirect recognition in sequence-specific DNA binding by Escherichia coli integration host factor: the role of DNA deformation energy. J Biol Chem 281:39236–39248CrossRefGoogle Scholar
  130. 130.
    Nash HA, Robertson CA (1981) Purification and properties of the Escherichia coli protein factor required for lambda integrative recombination. J Biol Chem 256:9246–9253Google Scholar
  131. 131.
    Winkelman JW, Hatfield GW (1990) Characterization of the integration host factor binding site in the ilvPG1 promoter region of the ilvGMEDA operon of Escherichia coli. J Biol Chem 265:10055–10060Google Scholar
  132. 132.
    Polaczek P, Kwan K, Liberies DA, Campbell JL (1997) Role of architectural elements in combinatorial regulation of initiation of DNA replication in Escherichia coli. Mol Microbiol 26:261–275CrossRefGoogle Scholar
  133. 133.
    Xin W, Feiss M (1993) Function of IHF in lambda DNA packaging. I. Identification of the strong binding site for integration host factor and the locus for intrinsic bending in cosB. J Mol Biol 230:492–504CrossRefGoogle Scholar
  134. 134.
    Goodrich JA, Schwartz ML, McClure WR (1990) Searching for and predicting the activity of sites for DNA binding proteins: compilation and analysis of the binding sites for Escherichia coli integration host factor (IHF). Nucleic Acids Res 18:4993–5000CrossRefGoogle Scholar
  135. 135.
    Hales LM, Gumport RI, Gardner JF (1994) Determining the DNA sequence elements required for binding integration host factor to two different target sites. J Bacteriol 176:2999–3006Google Scholar
  136. 136.
    Hales LM, Gumport RI, Gardner JF (1996) Examining the contribution of a dA+dT element to the conformation of Escherichia coli integration host factor-DNA complexes. Nucleic Acids Res 24:1780–1786CrossRefGoogle Scholar
  137. 137.
    Lavoie BD, Chaconas G (1993) Site-specific HU binding in the Mu transpososome: conversion of a sequence-independent DNA-binding protein into a chemical nuclease. Genes Dev 7:2510–2519CrossRefGoogle Scholar
  138. 138.
    Lavoie BD, Shaw GS, Millner A, Chaconas G (1996) Anatomy of a flexer-DNA complex inside a higher-order transposition intermediate. Cell 85:761–771CrossRefGoogle Scholar
  139. 139.
    Aki T, Adhya S (1997) Repressor induced site-specific binding of HU for transcriptional regulation. EMBO J 16:3666–3674CrossRefGoogle Scholar
  140. 140.
    Lyubchenko YL, Shlyakhtenko LS, Aki T, Adhya S (1997) Atomic force microscopic ­demonstration of DNA looping by GalR and HU. Nucleic Acids Res 25:873–876CrossRefGoogle Scholar
  141. 141.
    Boubrik F, Rouviere-Yaniv J (1995) Increased sensitivity to gamma irradiation in bacteria lacking protein HU. Proc Natl Acad Sci USA 92:3958–3962ADSCrossRefGoogle Scholar
  142. 142.
    Li S, Waters R (1998) Escherichia coli strains lacking protein HU are UV sensitive due to a role for HU in homologous recombination. J Bacteriol 180:3750–3756Google Scholar
  143. 143.
    Kamashev D, Balandina A, Rouviere-Yaniv J (1999) The binding motif recognized by HU on both nicked and cruciform DNA. EMBO J 18:5434–5444CrossRefGoogle Scholar
  144. 144.
    Castaing B, Zelwer C, Laval J, Boiteux S (1995) HU protein of Escherichia coli binds speci­fically to DNA that contains single-strand breaks or gaps. J Biol Chem 270:10291–10296CrossRefGoogle Scholar
  145. 145.
    Kobryn K, Naigamwalla DZ, Chaconas G (2000) Site-specific DNA binding and bending by the Borrelia burgdorferi Hbb protein. Mol Microbiol 37:145–155CrossRefGoogle Scholar
  146. 146.
    Johnson JB, Stella S, Heiss JK (2008) Bending and compaction of DNA by proteins. In: Rice PA, Correll CC (eds) Protein-nucleic acid interactions. Royal Society of Chemistry, CambridgeGoogle Scholar
  147. 147.
    van Noort J, Verbrugge S, Goosen N, Dekker C, Dame RT (2004) Dual architectural roles of HU: formation of flexible hinges and rigid filaments. Proc Natl Acad Sci USA 101:6969–6974ADSCrossRefGoogle Scholar
  148. 148.
    Sagi D, Friedman N, Vorgias C, Oppenheim AB, Stavans J (2004) Modulation of DNA conformations through the formation of alternative high-order HU-DNA complexes. J Mol Biol 341:419–428CrossRefGoogle Scholar
  149. 149.
    Tanaka I, Appelt K, Dijk J, White SW, Wilson KS (1984) 3-A resolution structure of a ­protein with histone-like properties in prokaryotes. Nature 310:376–381ADSCrossRefGoogle Scholar
  150. 150.
    Vis H, Mariani M, Vorgias CE, Wilson KS, Kaptein R, Boelens R (1995) Solution structure of the HU protein from Bacillus stearothermophilus. J Mol Biol 254:692–703CrossRefGoogle Scholar
  151. 151.
    Boelens R, Vis H, Vorgias CE, Wilson KS, Kaptein R (1996) Structure and dynamics of the DNA binding protein HU from Bacillus stearothermophilus by NMR spectroscopy. Biopolymers 40:553–559CrossRefGoogle Scholar
  152. 152.
    White SW, Wilson KS, Appelt K, Tanaka I (1999) The high-resolution structure of DNA-binding protein HU from Bacillus stearothermophilus. Acta Crystallogr D Biol Crystallogr 55:801–809CrossRefGoogle Scholar
  153. 153.
    Fernandez S, Rojo F, Alonso JC (1997) The Bacillus subtilis chromatin-associated protein Hbsu is involved in DNA repair and recombination. Mol Microbiol 23:1169–1179CrossRefGoogle Scholar
  154. 154.
    Kamashev D, Rouviere-Yaniv J (2000) The histone-like protein HU binds specifically to DNA recombination and repair intermediates. EMBO J 19:6527–6535CrossRefGoogle Scholar
  155. 155.
    Grove A, Saavedra TC (2002) The role of surface-exposed lysines in wrapping DNA about the bacterial histone-like protein HU. Biochemistry 41:7597–7603CrossRefGoogle Scholar
  156. 156.
    Grove A (2003) Surface salt bridges modulate DNA wrapping by the type II DNA-binding protein TF1. Biochemistry 42:8739–8747CrossRefGoogle Scholar
  157. 157.
    Kamau E, Tsihlis ND, Simmons LA, Grove A (2005) Surface salt bridges modulate the DNA site size of bacterial histone-like HU proteins. Biochem J 390:49–55CrossRefGoogle Scholar
  158. 158.
    Record MT Jr, Anderson CF, Lohman TM (1978) Thermodynamic analysis of ion effects on the binding and conformational equilibria of proteins and nucleic acids: the roles of ion association or release, screening, and ion effects on water activity. Q Rev Biophys 11:103–178CrossRefGoogle Scholar
  159. 159.
    Manning GS (1978) The molecular theory of polyelectrolyte solutions with applications to the electrostatic properties of polynucleotides. Q Rev Biophys 11:179–246CrossRefGoogle Scholar
  160. 160.
    Lohman TM, Mascotti DP (1992) Thermodynamics of ligand-nucleic acid interactions. Methods Enzymol 212:400–424CrossRefGoogle Scholar
  161. 161.
    Bloomfield VA, Crothers DM, Tinoco IJ (2000) Nucleic acids: structures, properties, and functions. University Science Books, Sausalito, CAGoogle Scholar
  162. 162.
    Holbrook JA, Tsodikov OV, Saecker RM, Record MT Jr (2001) Specific and non-specific interactions of integration host factor with DNA: thermodynamic evidence for disruption of multiple IHF surface salt-bridges coupled to DNA binding. J Mol Biol 310:379–401CrossRefGoogle Scholar
  163. 163.
    Saecker RM, Record MT Jr (2002) Protein surface salt bridges and paths for DNA wrapping. Curr Opin Struct Biol 12:311–319CrossRefGoogle Scholar
  164. 164.
    Vander Meulen KA, Saecker RM, Record MT Jr (2008) Formation of a wrapped DNA-protein interface: experimental characterization and analysis of the large contributions of ions and water to the thermodynamics of binding IHF to H′ DNA. J Mol Biol 377:9–27CrossRefGoogle Scholar
  165. 165.
    Lohman TM, Overman LB, Ferrari ME, Kozlov AG (1996) A highly salt-dependent enthalpy change for Escherichia coli SSB protein-nucleic acid binding due to ion-protein interactions. Biochemistry 35:5272–5279CrossRefGoogle Scholar
  166. 166.
    Cui T, Wei S, Brew K, Leng F (2005) Energetics of binding the mammalian high mobility group protein HMGA2 to poly(dA-dT)2 and poly(dA)-poly(dT). J Mol Biol 352:629–645CrossRefGoogle Scholar
  167. 167.
    Jen-Jacobson L, Engler LE, Jacobson LA (2000) Structural and thermodynamic strategies for site-specific DNA binding proteins. Structure 8:1015–1023CrossRefGoogle Scholar
  168. 168.
    Privalov PL, Dragan AI, Crane-Robinson C, Breslauer KJ, Remeta DP, Minetti CA (2007) What drives proteins into the major or minor grooves of DNA? J Mol Biol 365:1–9CrossRefGoogle Scholar
  169. 169.
    Dragan AI, Read CM, Makeyeva EN, Milgotina EI, Churchill ME, Crane-Robinson C, Privalov PL (2004) DNA binding and bending by HMG boxes: energetic determinants of specificity. J Mol Biol 343:371–393CrossRefGoogle Scholar
  170. 170.
    Khrapunov S, Brenowitz M, Rice PA, Catalano CE (2006) Binding then bending: a mechanism for wrapping DNA. Proc Natl Acad Sci USA 103:19217–19218ADSCrossRefGoogle Scholar
  171. 171.
    Lorenz M, Hillisch A, Goodman SD, Diekmann S (1999) Global structure similarities of intact and nicked DNA complexed with IHF measured in solution by fluorescence resonance energy transfer. Nucleic Acids Res 27:4619–4625CrossRefGoogle Scholar
  172. 172.
    Hillisch A, Lorenz M, Diekmann S (2001) Recent advances in FRET: distance determination in protein-DNA complexes. Curr Opin Struct Biol 11:201–207CrossRefGoogle Scholar
  173. 173.
    Holbrook JA, Capp MW, Saecker RM, Record MT Jr (1999) Enthalpy and heat capacity changes for formation of an oligomeric DNA duplex: interpretation in terms of coupled processes of formation and association of single-stranded helices. Biochemistry 38:8409–8422CrossRefGoogle Scholar
  174. 174.
    Bosch D, Campillo M, Pardo L (2003) Binding of proteins to the minor groove of DNA: what are the structural and energetic determinants for kinking a basepair step? J Comput Chem 24:682–691CrossRefGoogle Scholar
  175. 175.
    Gueron M, Leroy JL (1995) Studies of base pair kinetics by NMR measurement of proton exchange. Methods Enzymol 261:383–413CrossRefGoogle Scholar
  176. 176.
    Dhavan GM, Lapham J, Yang S, Crothers DM (1999) Decreased imino proton exchange and base-pair opening in the IHF-DNA complex measured by NMR. J Mol Biol 288:659–671CrossRefGoogle Scholar
  177. 177.
    Yan J, Kawamura R, Marko JF (2005) Statistics of loop formation along double helix DNAs. Phys Rev E Stat Nonlin Soft Matter Phys 71:061905CrossRefGoogle Scholar
  178. 178.
    Lankas F, Lavery R, Maddocks JH (2006) Kinking occurs during molecular dynamics simulations of small DNA minicircles. Structure 14:1527–1534CrossRefGoogle Scholar
  179. 179.
    Maher LJ 3rd (2006) DNA kinks available...if needed. Structure 14:1479–1480MathSciNetCrossRefGoogle Scholar
  180. 180.
    Leger JF, Robert J, Bourdieu L, Chatenay D, Marko JF (1998) RecA binding to a single double-stranded DNA molecule: a possible role of DNA conformational fluctuations. Proc Natl Acad Sci USA 95:12295–12299ADSCrossRefGoogle Scholar
  181. 181.
    deHaseth PL, Zupancic ML, Record MT Jr (1998) RNA polymerase-promoter interactions: the comings and goings of RNA polymerase. J Bacteriol 180:3019–3025Google Scholar
  182. 182.
    deHaseth PL, Nilsen TW (2004) Molecular biology. When a part is as good as the whole. Science 303:1307–1308CrossRefGoogle Scholar
  183. 183.
    Young BA, Gruber TM, Gross CA (2004) Minimal machinery of RNA polymerase holoenzyme sufficient for promoter melting. Science 303:1382–1384ADSCrossRefGoogle Scholar
  184. 184.
    Travers A (2005) DNA dynamics: bubble ‘n’ flip for DNA cyclisation? Curr Biol 15:R377–379CrossRefGoogle Scholar
  185. 185.
    Vivas P (2009) Mechanism of integration host factor, a DNA-bending protein, probed with laser temperature-jump, in Physics. University of Illinois at Chicago, ChicagoGoogle Scholar
  186. 186.
    Kahn JD, Crothers DM (1992) Protein-induced bending and DNA cyclization. Proc Natl Acad Sci USA 89:6343–6347ADSCrossRefGoogle Scholar
  187. 187.
    Kahn JD, Yun E, Crothers DM (1994) Detection of localized DNA flexibility. Nature 368:163–166ADSCrossRefGoogle Scholar
  188. 188.
    Parvin JD, McCormick RJ, Sharp PA, Fisher DE (1995) Pre-bending of a promoter sequence enhances affinity for the TATA-binding factor. Nature 373:724–727ADSCrossRefGoogle Scholar
  189. 189.
    Starr DB, Hoopes BC, Hawley DK (1995) DNA bending is an important component of site-specific recognition by the TATA binding protein. J Mol Biol 250:434–446CrossRefGoogle Scholar
  190. 190.
    Sugimura S (2005) Kinetic and steady-state studies of binding and bending of lambda phage DNA by integration host factor. Ph.D. thesis, Chemistry Department, Yale University, New Haven, CTGoogle Scholar
  191. 191.
    Aymami J, Coll M, van der Marel GA, van Boom JH, Wang AH, Rich A (1990) Molecular structure of nicked DNA: a substrate for DNA repair enzymes. Proc Natl Acad Sci USA 87:2526–2530ADSCrossRefGoogle Scholar
  192. 192.
    Mills JB, Cooper JP, Hagerman PJ (1994) Electrophoretic evidence that single-stranded regions of one or more nucleotides dramatically increase the flexibility of DNA. Biochemistry 33:1797–1803CrossRefGoogle Scholar
  193. 193.
    Kozerski L, Mazurek AP, Kawecki R, Bocian W, Krajewski P, Bednarek E, Sitkowski J, Williamson MP, Moir AJ, Hansen PE (2001) A nicked duplex decamer DNA with a PEG(6) tether. Nucleic Acids Res 29:1132–1143CrossRefGoogle Scholar
  194. 194.
    Fersht A (1999) Structure and mechanism in protein science. W.H. Freeman & Co, New YorkGoogle Scholar
  195. 195.
    Ferreiro DU, Sanchez IE, de Prat Gay G (2008) Transition state for protein-DNA recognition. Proc Natl Acad Sci USA 105:10797–10802ADSCrossRefGoogle Scholar
  196. 196.
    Lynch TW, Read EK, Mattis AN, Gardner JF, Rice PA (2003) Integration host factor: putting a twist on protein-DNA recognition. J Mol Biol 330:493–502CrossRefGoogle Scholar
  197. 197.
    Mirzabekov AD, Rich A (1979) Asymmetric lateral distribution of unshielded phosphate groups in nucleosomal DNA and its role in DNA bending. Proc Natl Acad Sci USA 76:1118–1121ADSCrossRefGoogle Scholar
  198. 198.
    Manning GS, Ebralidse KK, Mirzabekov AD, Rich A (1989) An estimate of the extent of folding of nucleosomal DNA by laterally asymmetric neutralization of phosphate groups. J Biomol Struct Dyn 6:877–889CrossRefGoogle Scholar
  199. 199.
    Williams LD, Maher LJ 3rd (2000) Electrostatic mechanisms of DNA deformation. Annu Rev Biophys Biomol Struct 29:497–521CrossRefGoogle Scholar
  200. 200.
    Strauss JK, Maher LJ 3rd (1994) DNA bending by asymmetric phosphate neutralization. Science 266:1829–1834ADSCrossRefGoogle Scholar
  201. 201.
    Strauss JK, Roberts C, Nelson MG, Switzer C, Maher LJ 3rd (1996) DNA bending by hexamethylene-tethered ammonium ions. Proc Natl Acad Sci USA 93:9515–9520ADSCrossRefGoogle Scholar
  202. 202.
    Strauss-Soukup JK, Maher LJ 3rd (1998) Electrostatic effects in DNA bending by GCN4 mutants. Biochemistry 37:1060–1066CrossRefGoogle Scholar
  203. 203.
    McDonald RJ, Kahn JD, Maher LJ 3rd (2006) DNA bending by bHLH charge variants. Nucleic Acids Res 34:4846–4856CrossRefGoogle Scholar
  204. 204.
    Leonard DA, Rajaram N, Kerppola TK (1997) Structural basis of DNA bending and oriented heterodimer binding by the basic leucine zipper domains of Fos and Jun. Proc Natl Acad Sci USA 94:4913–4918ADSCrossRefGoogle Scholar
  205. 205.
    Ramirez-Carrozzi VR, Kerppola TK (2001) Long-range electrostatic interactions influence the orientation of Fos-Jun binding at AP-1 sites. J Mol Biol 305:411–427CrossRefGoogle Scholar
  206. 206.
    Blainey PC, van Oijen AM, Banerjee A, Verdine GL, Xie XS (2006) A base-excision DNA-repair protein finds intrahelical lesion bases by fast sliding in contact with DNA. Proc Natl Acad Sci USA 103:5752–5757ADSCrossRefGoogle Scholar
  207. 207.
    Wang YM, Austin RH, Cox EC (2006) Single molecule measurements of repressor protein 1D diffusion on DNA. Phys Rev Lett 97:048302ADSCrossRefGoogle Scholar
  208. 208.
    Tafvizi A, Huang F, Leith JS, Fersht AR, Mirny LA, van Oijen AM (2008) Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys J 95:L01–03CrossRefGoogle Scholar
  209. 209.
    Bonnet I, Biebricher A, Porte PL, Loverdo C, Benichou O, Voituriez R, Escude C, Wende W, Pingoud A, Desbiolles P (2008) Sliding and jumping of single EcoRV restriction enzymes on non-cognate DNA. Nucleic Acids Res 36:4118–4127CrossRefGoogle Scholar
  210. 210.
    Gorman J, Chowdhury A, Surtees JA, Shimada J, Reichman DR, Alani E, Greene EC (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol Cell 28:359–370CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  1. 1.Physics Department, M/C 273University of Illinois at ChicagoChicagoUSA

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