Computational study of remodeling in a nucleosomal array

Abstract

Chromatin remodeling complexes utilize the energy of ATP hydrolysis to change the packing state of chromatin, e.g. by catalysing the sliding of nucleosomes along DNA. Here we present simple models to describe experimental data of changes in DNA accessibility along a synthetic, repetitive array of nucleosomes during remodeling by the ACF enzyme or its isolated ATPase subunit, ISWI. We find substantial qualitative differences between the remodeling activities of ISWI and ACF. To understand better the observed behavior for the ACF remodeler, we study more microscopic models of nucleosomal arrays.

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References

  1. 1.

    K. Luger, A.W. Mäder, R.K. Richmond, D.F. Sargent, T.J. Richmond, Nature 389, 251 (1997).

    ADS  Article  Google Scholar 

  2. 2.

    R. Blossey, H. Schiessel, FEBS J. 278, 3619 (2011).

    Article  Google Scholar 

  3. 3.

    K.J. Polach, J. Widom, J. Mol. Biol. 254, 130 (1995).

    Article  Google Scholar 

  4. 4.

    J.D. Anderson, J. Widom, J. Mol. Biol. 296, 979 (2000).

    Article  Google Scholar 

  5. 5.

    J.D. Anderson, P.T. Lowary, J. Widom, J. Mol. Biol. 307, 977 (2001).

    Article  Google Scholar 

  6. 6.

    G. Li, M. Levitus, C. Bustamante, J. Widom, Nat. Struct. Mol. Biol. 12, 46 (2005).

    Article  Google Scholar 

  7. 7.

    L. Kelbauskas, N. Chan, R. Bash, J. Yodh, N. Woodbury, D. Lohr, Biochemistry 46, 2239 (2007).

    Article  Google Scholar 

  8. 8.

    A. Gansen, A. Valeri, F. Hauger, S. Felekyan, S. Kalinin, K. Toth, J. Langowski, C.A.M. Seidel, Proc. Natl. Acad. Sci. U.S.A. 106, 15308 (2009).

    ADS  Article  Google Scholar 

  9. 9.

    W.J.A. Koopmans, R. Buning, T. Schmidt, J. van Noort, Biophys. J. 97, 195 (2009).

    ADS  Article  Google Scholar 

  10. 10.

    R. Prinsen, H. Schiessel, Biochimie 92, 1722 (2010).

    Article  Google Scholar 

  11. 11.

    H.S. Tims, K. Gurunathan, M. Levitus, J. Widom, J. Mol. Biol. 411, 430 (2011).

    Article  Google Scholar 

  12. 12.

    I. Jimenez-Useche, C. Yuan, Biophys. J. 103, 2502 (2012).

    ADS  Article  Google Scholar 

  13. 13.

    S. Pennings, G. Meersseman, E.M. Bradbury, J. Mol. Biol. 220, 101 (1991).

    Article  Google Scholar 

  14. 14.

    G. Meersseman, S. Pennings, E.M. Bradbury, EMBO J. 11, 2951 (1992).

    Google Scholar 

  15. 15.

    S. Pennings, G. Meersseman, E.M. Bradbury, Proc. Natl. Acad. Sci. U.S.A. 91, 10275 (1994).

    ADS  Article  Google Scholar 

  16. 16.

    A. Flaus, T.J. Richmond, J. Mol. Biol. 275, 427 (1998).

    Article  Google Scholar 

  17. 17.

    J.M. Gottesfeld, J.M. Belitsky, C. Melander, P.B. Dervan, K. Luger, J. Mol. Biol. 321, 249 (2002).

    Article  Google Scholar 

  18. 18.

    S. Pisano, E. Marchioni, A. Galati, R. Mechelli, M. Savino, S. Cacchione, J. Mol. Biol. 369, 1153 (2007).

    Article  Google Scholar 

  19. 19.

    A. Flaus, T. Owen-Hughes, Biopolymers 68, 563 (2003).

    Article  Google Scholar 

  20. 20.

    H. Schiessel, J. Phys.: Condens. Matter 15, R699 (2003).

    ADS  Google Scholar 

  21. 21.

    H. Schiessel, J. Widom, R.F. Bruinsma, W.M. Gelbart, Phys. Rev. Lett. 86, 4414 (2001).

    ADS  Article  Google Scholar 

  22. 22.

    I.M. Kulić, H. Schiessel, Biophys. J. 84, 3197 (2003).

    ADS  Article  Google Scholar 

  23. 23.

    I.M. Kulić, H. Schiessel, Phys. Rev. Lett. 91, 148103 (2003).

    ADS  Article  Google Scholar 

  24. 24.

    F. Mohammad-Rafiee, I.M. Kulić, H. Schiessel, J. Mol. Biol. 344, 47 (2004).

    Article  Google Scholar 

  25. 25.

    A. Fathizadeh, A.B. Besya, M.R. Ejtehadi, H. Schiessel, Eur. Phys. J. E 36, 21 (2013).

    Article  Google Scholar 

  26. 26.

    A. Flaus, D.M.A. Martin, G.J. Barton, T. Owen-Hughes, Nucl. Acids Res. 34, 2887 (2006).

    Article  Google Scholar 

  27. 27.

    C.R. Clapier, B.R. Cairns, Annu. Rev. Biochem. 78, 273 (2009).

    Article  Google Scholar 

  28. 28.

    A.E. Leschziner, Curr. Opin. Struct. Biol. 21, 709 (2011).

    Article  Google Scholar 

  29. 29.

    G.J. Narlikar, R. Sundaramoorthy, T. Owen-Hughes, Cell 154, 490 (2013).

    Article  Google Scholar 

  30. 30.

    P.D. Varga-Weisz, M. Wilm, E. Bonte, K. Dumas, M. Mann, P.B. Becker, Nature 388, 598 (1997).

    ADS  Article  Google Scholar 

  31. 31.

    J.G. Yang, T.S. Madrid, E. Sevastopoulos, G.J. Narlikar, Nat. Struct. Mol. Biol. 13, 1078 (2006).

    Article  Google Scholar 

  32. 32.

    L.R. Racki, J.G. Yang, N. Naber, P.D. Partensky, A. Acevedo, T.J. Purcell, R. Cooke, Y. Cheng, G.J. Narlikar, Nature 462, 1016 (2009).

    ADS  Article  Google Scholar 

  33. 33.

    T.R. Blosser, J.G. Yang, M.D. Stone, G.J. Narlikar, X. Zhyang, Nature 462, 1022 (2009).

    ADS  Article  Google Scholar 

  34. 34.

    S.E. Torigoe, D.L. Urwin, H. Ishii, D.E. Smith, J.T. Kadonaga, Mol. Cell 43, 638 (2011).

    Article  Google Scholar 

  35. 35.

    A.-M. Florescu, H. Schiessel, R. Blossey, Phys. Rev. Lett. 109, 118103 (2012).

    ADS  Article  Google Scholar 

  36. 36.

    P. Korber, P.B. Becker, Essays Biochem. 58, 63 (2010).

    Article  Google Scholar 

  37. 37.

    G. Lanzani, H. Schiessel, EPL 97, 38002 (2012).

    ADS  Article  Google Scholar 

  38. 38.

    V.K. Maier, M. Chioda, D. Rhodes, P.B. Becker, EMBO J. 27, 817 (2008).

    Article  Google Scholar 

  39. 39.

    H. Klinker, F. Mueller-Planitz, R. Yang, I. Forné, C.-F. Liu, L. Nordenskiöld, P.B. Becker, PLoS ONE 9, e88411 (2014).

    ADS  Article  Google Scholar 

  40. 40.

    A. Eberharter, S. Ferrari, G. Längst, T. Straub, A. Imhof, P. Varga-Weisz, M. Wilm, P.B. Becker, EMBO J. 20, 3781 (2001).

    Article  Google Scholar 

  41. 41.

    X. He, H.-Y. Fan, G.J. Narlikar, R.E. Kingston, J. Biol. Chem. 281, 28636 (2006).

    Article  Google Scholar 

  42. 42.

    P.T. Lowary, J. Widom, J. Mol. Biol. 276, 19 (1998).

    Article  Google Scholar 

  43. 43.

    K.J. Polach, J. Widom, Methods Enzymol. 304, 278 (1999).

    Article  Google Scholar 

  44. 44.

    P.D. Gregory, S. Barbaric, W. Hörz, Methods Mol Biol. 119, 417 (1999).

    Google Scholar 

  45. 45.

    C. Logie, C.L. Peterson, EMBO J. 16, 6772 (1997).

    Article  Google Scholar 

  46. 46.

    G.J. Narlikar, M.L. Phelan, R.E. Kingston, Mol. Cell 8, 1219 (2001).

    Article  Google Scholar 

  47. 47.

    A.R. Khaki, C. Field, S. Malik, A. Niedziela-Majka, S.A. Leavitt, R. Wang, M. Hung, R. Sakowicz, K.M. Brendza, C.J. Fischer, J. Mol. Biol. 400, 345 (2010).

    Article  Google Scholar 

  48. 48.

    G. Al-Ani, K. Briggs, S.S. Malik, M. Conner, Y. Azumi, C.J. Fischer, Biochemistry 53, 4334 (2014).

    Article  Google Scholar 

  49. 49.

    R. Kornberg, L. Stryer, Nucl. Acids Res. 16, 6677 (1988).

    Article  Google Scholar 

  50. 50.

    E. Segal, Y. Fondufe-Mittendorf, L. Chen, A.C. Thaström, Y. Field, I.K. Moore, J.-P.Z. Wang, J. Widom, Nature 442, 772 (2006).

    ADS  Article  Google Scholar 

  51. 51.

    P.D. Partensky, G.J. Narlikar, J. Mol. Biol. 391, 12 (2009).

    Article  Google Scholar 

  52. 52.

    L. Tonks, Phys. Rev. 50, 955 (1936).

    ADS  Article  Google Scholar 

  53. 53.

    G. Chevereau, L. Palmeira, C. Thermes, A. Arneodo, C. Vaillant, Phys. Rev. Lett. 103, 188103 (2009).

    ADS  Article  Google Scholar 

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Correspondence to Helmut Schiessel.

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Schram, R.D., Klinker, H., Becker, P.B. et al. Computational study of remodeling in a nucleosomal array. Eur. Phys. J. E 38, 85 (2015). https://doi.org/10.1140/epje/i2015-15085-4

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Keywords

  • Living systems: Biological Matter