Advertisement

Studies of DNA-Protein Interactions at the Single Molecule Level with Magnetic Tweezers

  • J.-F. Allemand
  • D. Bensimon
  • G. Charvin
  • V. Croquette
  • G. Lia
  • T. Lionnet
  • K.C. Neuman
  • O.A. Saleh
  • H. Yokota
Part of the Lecture Notes in Physics book series (LNP, volume 711)

Abstract

The development of tools to manipulate and study single biomolecules (DNA, RNA, proteins) has opened a new vista on the study of their mechanical properties and their joint interactions. In this short review we will focus on (single and double stranded) DNA and its interactions with various classes of proteins: structural DNA binding proteins such as gene repressors (e.g., the Galactose Repressor, GalR) and mechano-chemical enzymes that alter the DNA’s topology (topoisomerases), unwind it (helicases) or translocate it (FtsK). We will show how the new tools at our disposal can be used to gain an unprecedented description of the binding properties (on and off-times) and the enzymes’ kinetic constants that are often out of reach of more classical, bulk techniques.

Keywords

Single Molecule Persistence Length Single Molecule Level Magnetic Tweezer Single Biomolecule 
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.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    C. Bustamante, S.B. Smith, J. Liphardt, and D. Smith (2000). Curr. Op. Structural Biology, 10, pp. 279–285.CrossRefGoogle Scholar
  2. 2.
    T.R. Strick, M.-N. Dessinges, G. Charvin, N.H. Dekker, J.-F. Allemand, D. Bensimon, and V. Croquette (2003). Stretching of macromolecules and proteins. Rep. Prog. Phys., 66, pp. 1–45.CrossRefADSGoogle Scholar
  3. 3.
    G. Lia, D. Bensimon, V. Croquette, J.F. Allemand, D. Dunlap, D.E.A. Lewis, S. Adhya, and L. Finzi (2003). Supercoiling and denaturation in gal repressorheat unstable nucleoid protein (hu)-mediated dna looping. Proc. Natl. Acad. Sci. (USA), 100, pp. 11373–11377.CrossRefADSGoogle Scholar
  4. 4.
    J. Liphardt, B. Onoa, S.B. Smith, I. Tinoco Jr., and C. Bustamante (2001). Reversible unfolding of single RNA molecules by mechanical force. Science, 292, pp. 733–737.CrossRefADSGoogle Scholar
  5. 5.
    J.F. Marko and E.D. Siggia. Driving proteins off DNA using applied tension (1997). Biophys. J., 73, pp. 2173–2178.ADSCrossRefGoogle Scholar
  6. 6.
    J.-F. Allemand, D. Bensimon, R. Lavery, and V. Croquette. Stretched and overwound DNA form a Pauling-like structure with exposed bases (1998). Proc. Natl. Acad. Sci. USA, 95, pp. 14152–14157.CrossRefADSGoogle Scholar
  7. 7.
    M.-N. Dessinges, B. Maier, Y. Zhang, M. Peliti, D. Bensimon, and V. Croquette (2002). Stretching ssdna, a model polyelectrolyte. Phys. Rev. Lett., 89, pp. 248102.CrossRefADSGoogle Scholar
  8. 8.
    J.-F. Allemand, T. Strick, V. Croquette, and D. Bensimon (2000). Twisting and stretching single dna molecules. Prog. Biophys. Molec. Biol., 74, pp. 115–140.CrossRefGoogle Scholar
  9. 9.
    F. Gittes and C.F. Schmidt CF (1998). Signals and noise in micromechanical measurements. Methods in Cell Biology, 55, pp. 129–156.CrossRefGoogle Scholar
  10. 10.
    J.F. Marko and E. Siggia (1995). Statistical mechanics of supercoiled DNA. Phys. Rev. E, 52(3), pp. 2912–2938.CrossRefADSMathSciNetGoogle Scholar
  11. 11.
    C. Bouchiat, M.D. Wang, S.M. Block, J.-F. Allemand, T.R. Strick, and V. Croquette (1999). Estimating the persitence length of a worm-like chain molecule from force-extension measurements. Biophys. J., 76, pp. 409–413.CrossRefGoogle Scholar
  12. 12.
    T. Strick, J.-F. Allemand, D. Bensimon, and V. Croquette (1998). The behavior of supercoiled DNA. Biophys. J., 74, pp. 2016–2028.ADSCrossRefGoogle Scholar
  13. 13.
    H. Kramer, M. Niemoller, M. Amouyal, B. Revet, B. von Wilcken-Bergmann, and B. Muller-Hill (1987). Lac repressor forms loops with linear dna carrying two suitably spaced lac operators. EMBO Journal, 6, pp. 1481–1491.Google Scholar
  14. 14.
    N. Mandal, W. Su, R. Haber, S. Adhya, and H. Echols (1990). Dna looping in cellular repression of transcription of the galactose operon. Genes and Development, 4, pp. 410–418.CrossRefGoogle Scholar
  15. 15.
    A.K. Vershon, S.M. Liao, W.R. McClure, and R.T. Sauer (1987). Interaction of the bacteriophage p22 arc repressor with operator dna. J. Mol. Biol., 195, pp. 323–331.CrossRefGoogle Scholar
  16. 16.
    J.P. Hunt and B. Magasanik (1985). Transcription of glna by purified escherichia coli components: Core rna polymerase and products of glnf, glng and glnl. Proc. Natl. Acad. Sci. (USA), 85, pp. 8453–8457.CrossRefADSGoogle Scholar
  17. 17.
    T. Schlick and W.K. Olson (1992). Supercoiled DNA energetics and dynamics by computer simulation. J. Mol. Biol., 223, pp. 1089–1119.CrossRefGoogle Scholar
  18. 18.
    R. Tjian and T. Maniatis (1994). Transcriptional activation: a complex puzzle with few easy pieces. Cell, 77, pp. 5–8.CrossRefGoogle Scholar
  19. 19.
    D. Ristic, C. Wyman, C. Paulusma, and R. Kanaar (2001). The architecture of the human rad54-dna complex provides evidence for protein translocation along dna. Proc. Natl. Acad. Sci. (USA), 98, pp. 8454–8460.CrossRefADSGoogle Scholar
  20. 20.
    S. Pathania, M. Jayaram, and R.M. Harshey (2002). Path of dna within the mu transposome. transposase interactions bridging two mu ends and the enhancer trap five dna supercoils. Cell, 109, pp. 425–436.CrossRefGoogle Scholar
  21. 21.
    G.I. Bell (1978). Science, 200, pp. 618–627.CrossRefADSGoogle Scholar
  22. 22.
    D. Bensimon (1996). Force: a new structural control parameter? Structure, 4, pp. 885–889.CrossRefGoogle Scholar
  23. 23.
    I. Tinoco Jr. and C. Bustamante (2002). Biophys. Chem., 101–102, pp. 513–533.CrossRefGoogle Scholar
  24. 24.
    K. Virnik, Y.L. Lyubchenko, M.A. Karymov, P. Dahlgren, M.Y. Tolstorukov, S. Semsey, V.B. Zhurkin, and S. Adhya (2003). “antiparallel” dna loop in gal repressosome visualized by atomic force microscopy. J. Mol. Biol., 334, pp. 53–63.CrossRefGoogle Scholar
  25. 25.
    D. Shore and R.L. Baldwin (1983). J. Mol. Biol., 170, pp. 957–981.CrossRefGoogle Scholar
  26. 26.
    J. Roca and J.C. Wang (1994). DNA transport by a type II DNA topoisomerase: evidence in favor of a two-gate model. Cell, 77, pp. 609–616.CrossRefGoogle Scholar
  27. 27.
    J. J. Champoux (2001). DNA topoisomerases: structure, function, and mechanism. Annu. Rev. Biochem., 70, pp. 369–413.CrossRefGoogle Scholar
  28. 28.
    J. Roca and J.C. Wang (1992). The capture of a DNA double helix by an ATP-dependent protein clamp: a key step in DNA transport by type II DNA topoisomerase. Cell., 71, pp. 833–840.CrossRefGoogle Scholar
  29. 29.
    J. C. Wang (2002). Cellular roles of DNA topoisomerases: a molecular perspective. Nat. Rev. Mol. Cell. Biol., 3(6), pp. 430–40.CrossRefGoogle Scholar
  30. 30.
    V.V. Rybenkov, C. Ullsperger, A.V. Vologodskii, and N.R. Cozzarelli (1997). Simplification of DNA topology below equilibrium values by type II topoisomerases. Science, 277, pp. 690–693.CrossRefGoogle Scholar
  31. 31.
    J.E. Lindsley and J.C. Wang (1993). On the coupling betzeen ATP usage and DNA transport by yeast DNA topoisomerase II. J. Biol. Chem., 268, pp. 8096–8104.Google Scholar
  32. 32.
    T.T. Harkins and J.E. Lindsley (1998). Pre-steady-state analysis of ATP hydrolysis by saccharomyces cerevisiae DNA topoisomerase II. 1. A DNA-dependent burst in ATP hydrolysis. Biochemistry, 37, pp. 7292–7298.CrossRefGoogle Scholar
  33. 33.
    T.T. Harkins, T.J. Lewis, and J.E. Lindsley (1998). Pre-steady-state analysis of ATP hydrolysis by saccharomyces cerevisiae DNA topoisomerase II. 2. Kinetic mechanism for the sequential hydrolysis of two ATP. Biochemistry, 37, pp. 7299–7312.CrossRefGoogle Scholar
  34. 34.
    C.L. Baird, T.T. Harkins, S.K. Morris, and J.E. Lindsley (1999). Topoisomerase II drives DNA transport by hydrolyzing one ATP. Proc. Natl. Acad. Sci. USA, 96(24), pp. 13685–90.CrossRefADSGoogle Scholar
  35. 35.
    T.R. Strick, V. Croquette, and D. Bensimon (2000). Single-molecule analysis of DNA uncoiling by a type II topoisomerase. Nature, 404, pp. 901–904.CrossRefADSGoogle Scholar
  36. 36.
    T. Strick, J.F. Allemand, D. Bensimon, A. Bensimon, and V. Croquette (1996). The elasticity of a single supercoiled DNA molecule. Science, 271, pp. 1835–1837.CrossRefADSGoogle Scholar
  37. 37.
    N. Crisona, T.R. Strick, D. Bensimon, V. Croquette, and N. Cozzarelli (2000). Preferential relaxation of positively supercoiled DNA by E.coli topoisomerase VI in single-molecule and ensemble measurements. Genes & Developement, 14, pp. 2881–2892.CrossRefGoogle Scholar
  38. 38.
    M.D. Stone, Z. Bryant, N.J. Crisona, S.B. Smith, A. Vologodskii, C. Bustamante, and N. R. Cozzarelli (2003). Chirality sensing by escherichia coli topoisomerase IV and the mechanism of type II topoisomerases. Proc. Natl. Acad. Sci. USA, 100(15), pp. 8654–9.CrossRefADSGoogle Scholar
  39. 39.
    G. Charvin, V. Croquette, and D. Bensimon (2003). Single molecule study of dna unlinking by eukaryotic and prokaryotic type II topoisomerases. PNAS, 100(17), pp. 9820–9825.CrossRefADSGoogle Scholar
  40. 40.
    T.M. Lohman and K.P. Bjornson (1996). Mechanisms of helicase-catalysed unwinding. Annu. Rev. Biochem., 65, pp. 169–214.CrossRefGoogle Scholar
  41. 41.
    A. Sancar (1994). Mechanisms of dna excision-repair. Science, 266, pp. 1954–1956.CrossRefADSGoogle Scholar
  42. 42.
    G.T. Runyon and T.M. Lohman (1989). Escherichia Coli helicase ii (uvrd) protein can completely unwind fully duplex linear and nicked circular dna. J. Biol. Chem., 264, pp. 17502–17512.Google Scholar
  43. 43.
    S.W. Matson (1986). Escherichia Coli helicase ii (uvrd gene product) translocates unidirectionnaly in a 3′to 5′ direction. J. Biol. Chem., 261, pp. 10169–10175.Google Scholar
  44. 44.
    M.-N. Dessinges, T. Lionnet, X. Xi, D. Bensimon, and V. Croquette (2004). Single molecule assay reveals strand switching and enhanced processivity of uvrd. Proc. Nat. Acad. USA, 101, pp. 6439–6444.CrossRefADSGoogle Scholar
  45. 45.
    G. Charvin, V. Croquette, and D. Bensimon (2002). On the relation betwen noise spectra and the distribution of time between steps for single molecular motors. Single Molecule, 3(1), pp. 43–48.CrossRefADSGoogle Scholar
  46. 46.
    O.A. Saleh, S. Bigot, F.-X. Barre, and J.-F. Allemand (2005). Analysis of DNA supercoil induction by FtsK indicates translocation without groove-tracking Nat. Struct. Mol. Biol., 12, 436–440.CrossRefGoogle Scholar
  47. 47.
    O.A. Saleh, C. Perals, F.-X. Barre, and J.-F. Allemand (2004). Fast, DNAsequence independent translocation by ftsk in a single-molecule experiment. EMBO J., 23, pp. 2430–2439.CrossRefGoogle Scholar
  48. 48.
    P.J. Pease, O. Levy, G.J. Cost, J. Gore, J.L. Ptacin, D. Sherratt, C. Bustamante, and N.R. Cozzarelli (2005). Sequence-directed DNA translocation by purified FtsK. Science, 307, pp. 586–590.CrossRefADSGoogle Scholar
  49. 49.
    S. Bigot, O.A. Saleh, C. Lesterlin, C. Pages, M.El Karoui, C. Dennis, M. Grigoriev, J.-F. Allemand, F.-X. Barre, and F. Cornet. KOPS: DNA motifs that control E. coli chromosome segregation by orienting the FtsK translocase. EMBO J., in press Google Scholar
  50. 50.
    M. Spies, P.R. Bianco, M.S. Dillingham, N. Handa, R.J. Baskin, S.C. Kowalczykowski (2003). A molecular throttle: the recombination hotspot chi controls DNA translocation by the RecBCD helicase. Cell, 114, pp. 647–654.CrossRefGoogle Scholar
  51. 51.
    A. Yildiz, J.N. Forkey, S.A. McKinney, T. Ha, Y.E. Goldman, and P.R. Selvin (2003). Myosin v walks hand-over-hand: single fluorophore imaging with 1.5 nm localization. Science, 300, pp. 2061–2065.CrossRefADSGoogle Scholar
  52. 52.
    X. Zhuang, L.E. Bartley, H.P. Babcock, R. Russel, T. Ha, D. Herschlag, and S. Chu (2000). Science, 288, pp. 2048–2051.CrossRefADSGoogle Scholar
  53. 53.
    S. Weiss (1999). Fluorescence spectroscopy of single biomolecules. Science, 283, pp. 1676–1683.CrossRefADSGoogle Scholar
  54. 54.
    T. Funatsu, Y. Harada, M. Tokunaga, K. Saito, and T. Yanagida (1995). Imaging of single fluorescent molecules and individual ATP turnovers by single myosin molecules in aqueous solution. Nature, 374, pp. 555–559.CrossRefADSGoogle Scholar
  55. 55.
    M.J. Lang, P.M. Fordyce, A.M. Engh, K.C. Neuman, and S.M. Block (2004). Simultaneous, coincident optical trapping and single-molecule fluorescence. Nat. Methods, 1(2), pp. 133–139.CrossRefGoogle Scholar
  56. 56.
    A. Ishijima, H. Kojima, T. Funatsu, M. Tokunaga, H. Higuchi, H. Tanaka, and T. Yanagida (1998). Simultaneous observation of individual ATPase and mechanical events by a single myosin molecule during interaction with actin. Cell, 92, pp. 161–171.CrossRefGoogle Scholar

Copyright information

© Springer 2007

Authors and Affiliations

  • J.-F. Allemand
    • 1
  • D. Bensimon
    • 1
  • G. Charvin
    • 1
  • V. Croquette
    • 1
  • G. Lia
    • 2
  • T. Lionnet
    • 1
  • K.C. Neuman
    • 1
  • O.A. Saleh
    • 3
  • H. Yokota
    • 4
  1. 1.Laboratoire de Physique Statistique and Department of BiologieEcole Normale Superieure, UMR 8550 CNRSParis Cedex 05France
  2. 2.Harvard University Chemistry and Chemical BiologyCambridgeUSA
  3. 3.Materials Department and Biomolecular Science and Engineering ProgramUniversity of California, Materials DeptUSA
  4. 4.Department of Molecular PhysiologyThe Tokyo Metropolition Institute of Medical ScienceTokyoJapan

Personalised recommendations