Quantitative analysis of single-molecule force spectroscopy on folded chromatin fibers

Nucleic Acids Research

Volumn 43, Issue 7, 2015, Pages 3578-3590

  Meng, He ^a   Andresen, Kurt ^b   Van Noort, John ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b GETTYSBURG COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; CHROMATIN; NUCLEOSOME;

ARTICLE; CHROMATIN; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; FORCE; MOLECULAR MECHANICS; NUCLEOSOME; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; STATISTICAL MODEL; CHEMISTRY; PROCEDURES; PROTEIN FOLDING;

CHROMATIN; NUCLEOSOMES; PROTEIN FOLDING; SPECTRUM ANALYSIS;

EID: 84930505454     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkv215     Document Type: Article

References (59)

1. Li, B., Carey, M. and Workman, J.L. (2007) The role of chromatin during transcription. Cell, 128, 707-719.
2. Luger, K., Ma, A.W., Richmond, R.K., Sargent, D.F. and Richmond, T.J. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389, 251-260.
3. Makde, R.D., England, J.R., Yennawar, H.P. and Tan, S. (2010) Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature, 467, 562-566.
4. Brower-Toland, B.D., Smith, C.L., Yeh, R.C., Lis, J.T., Peterson, C.L. and Wang, M.D. (2002) Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. U.S.A., 99, 1960-1965.
5. Mihardja, S., Spakowitz, A.J., Zhang, Y. and Bustamante, C. (2006) Effect of force on mononucleosomal dynamics. Proc. Natl. Acad. Sci. U. S. A., 103, 15871-15876.
6. Böhm, V., Hieb, A.R., Andrews, A.J., Gansen, A., Rocker, A., Tóth, K., Luger, K. and Langowski, J. (2011) Nucleosome accessibility governed by the dimer/tetramer interface. Nucleic Acids Res., 39, 3093-3102.
7. Flaus, A. and Owen-Hughes, T. (2011) Mechanisms for ATP-dependent chromatin remodelling: the means to the end. FEBS J., 278, 3579-3595.
8. Rippe, K., Schrader, A., Riede, P., Strohner, R., Lehmann, E. and Längst, G. (2007) DNA sequence-and conformation-directed positioning of nucleosomes by chromatin-remodeling complexes. Proc. Natl. Acad. Sci. U.S.A., 104, 15635-15640.
9. van Vugt, J.J.F.A., de Jager, M., Murawska, M., Brehm, A., van Noort, J. and Logie, C. (2009) Multiple aspects of ATP-dependent nucleosome translocation by RSC and Mi-2 are directed by the underlying DNA sequence. PloS One, 4, e6345.
10. Neumann, H., Hancock, S.M., Buning, R., Routh, A., Chapman, L., Somers, J., Owen-Hughes, T., van Noort, J., Rhodes, D. and Chin, J.W. (2009) A method for genetically installing site-specifc acetylation in recombinant histones defnes the effects of H3 K56 acetylation. Mol. Cell, 36, 153-163.
11. North, J.A., Simon, M., Ferdinand, M.B., Shoffner, M.A., Picking, J.W., Howard, C.J., Mooney, A.M., van Noort, J., Poirier, M.G. and Ottesen, J.J. (2014) Histone H3 phosphorylation near the nucleosome dyad alters chromatin structure. Nucleic Acids Res., 42, 4922-4933.
12. Schalch, T., Duda, S., Sargent, D.F. and Richmond, T.J. (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fbre. Nature, 436, 138-141.
13. Robinson, P.J.J., Fairall, L., Huynh, V.A.T. and Rhodes, D. (2006) EM measurements defne the dimensions of the "30-nm" chromatin fber: evidence for a compact, interdigitated structure. Proc. Natl. Acad. Sci. U.S.A., 103, 6506-6511.
14. Routh, A., Sandin, S. and Rhodes, D. (2008) Nucleosome repeat length and linker histone stoichiometry determine chromatin fber structure. Proc. Natl. Acad. Sci. U.S.A., 105, 8872-8877.
15. Dorigo, B., Schalch, T., Kulangara, A., Duda, S., Schroeder, R.R. and Richmond, T.J. (2004) Nucleosome arrays reveal the two-start organization of the chromatin fber. Science, 306, 1571-1573.
16. Grigoryev, S.A., Arya, G., Correll, S., Woodcock, C.L. and Schlick, T. (2009) Evidence for heteromorphic chromatin fbers from analysis of nucleosome interactions. Proc. Natl. Acad. Sci. U.S.A., 106, 13317-13322.
17. Allahverdi, A., Yang, R., Korolev, N., Fan, Y., Davey, C.A., Liu, C.-F. and Nordenskiöld, L. (2011) The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res., 39, 1680-1691.
18. Hansen, J.C. (2002) Conformational dynamics of the chromatin fber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct., 31, 361-392.
19. Luger, K., Dechassa, M.L. and Tremethick, D.J. (2012) New insights into nucleosome and chromatin structure: an ordered state or a disordered affair? Nat. Rev. Mol. Cell Biol., 13, 436-447.
20. Lowary, P.T. and Widom, J. (1998) New DNA sequence rules for high affnity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol., 276, 19-42.
21. Nishino, Y., Eltsov, M., Joti, Y., Ito, K., Takata, H., Takahashi, Y., Hihara, S., Frangakis, A.S., Imamoto, N., Ishikawa, T. et al. (2012) Human mitotic chromosomes consist predominantly of irregularly folded nucleosome fbres without a 30-nm chromatin structure. EMBO J., 31, 1644-1653.
22. Valouev, A., Ichikawa, J., Tonthat, T., Stuart, J., Ranade, S., Peckham, H., Zeng, K., Malek, J.A., Costa, G. and McKernan, K. (2008) A high-resolution, nucleosome position map of C. elegans reveals a lack of universal sequence-dictated positioning. Genome Res., 18, 1051-1063.
23. Correll, S.J., Schubert, M.H. and Grigoryev, S.A. (2012) Short nucleosome repeats impose rotational modulations on chromatin fbre folding. EMBO J., 31, 2416-2426.
24. Li, G. and Reinberg, D. (2011) Chromatin higher-order structures and gene regulation. Curr. Opin. Genet. Dev., 21, 175-186.
25. Wong, H., Victor, J.-M. and Mozziconacci, J. (2007) An all-atom model of the chromatin fber containing linker histones reveals a versatile structure tuned by the nucleosomal repeat length. PloS One, 2, e877.
26. Kruithof, M. and van Noort, J. (2009) Hidden Markov analysis of nucleosome unwrapping under force. Biophys. J., 96, 3708-3715.
27. Mack, A.H., Schlingman, D.J., Ilagan, R.P., Regan, L. and Mochrie, S.G.J. (2012) Kinetics and thermodynamics of phenotype: unwinding and rewinding the nucleosome. J. Mol. Biol., 423, 687-701.
28. Sheinin, M.Y., Li, M., Soltani, M., Luger, K. and Wang, M.D. (2013) Torque modulates nucleosome stability and facilitates H2A/H2B dimer loss. Nat. Commun., 4, 2579.
29. Kulić, I., Mohrbach, H., Lobaskin, V., Thaokar, R. and Schiessel, H. (2005) Apparent persistence length renormalization of bent DNA. Phys. Rev. E, 72, 041905.
30. Simon, M., North, J.A., Shimko, J.C., Forties, R.A., Ferdinand, M.B., Manohar, M., Zhang, M., Fishel, R., Ottesen, J.J. and Poirier, M.G. (2011) Histone fold modifcations control nucleosome unwrapping and disassembly. Proc. Natl. Acad. Sci. U.S.A., 108, 12711-12716.
31. Cui, Y. and Bustamante, C. (2000) Pulling a single chromatin fber reveals the forces that maintain its higher-order structure. Proc. Natl. Acad. Sci. U.S.A., 97, 127-132.
32. Kruithof, M., Chien, F.-T., Routh, A., Logie, C., Rhodes, D. and van Noort, J. (2009) Single-molecule force spectroscopy reveals a highly compliant helical folding for the 30-nm chromatin fber. Nat. Struct. Mol. Biol., 16, 534-540.
33. Korolev, N., Allahverdi, A., Yang, Y., Fan, Y., Lyubartsev, A.P. and Nordenskiöld, L. (2010) Electrostatic origin of salt-induced nucleosome array compaction. Biophys. J., 99, 1896-1905.
34. Dobrovolskaia, I.V. and Arya, G. (2012) Dynamics of forced nucleosome unraveling and role of nonuniform histone-DNA interactions. Biophys. J., 103, 989-998.
35. Victor, J.M., Zlatanova, J., Barbi, M. and Mozziconacci, J. (2012) Pulling chromatin apart: unstacking or unwrapping? BMC Biophys., 5, 21.
36. Collepardo-Guevara, R. and Schlick, T. (2014) Chromatin fber polymorphism triggered by variations of DNA linker lengths. Proc. Natl. Acad. Sci. U.S.A., 111, 8061-8066.
37. Ben-Haïm, E., Lesne, A. and Victor, J.-M. (2001) Chromatin: a tunable spring at work inside chromosomes. Phys. Rev. E, 64, 051921.
38. Kulić, I. and Schiessel, H. (2004) DNA Spools under Tension. Physical Review Letters, 92, 228101.
39. Schiessel, H. (2006) The nucleosome: a transparent, slippery, sticky and yet stable DNA-protein complex. Eur. Phys. J. E Soft Matter, 19, 251-262.
40. Sudhanshu, B., Mihardja, S., Koslover, E.F., Mehraeen, S., Bustamante, C. and Spakowitz, A.J. (2011) Tension-dependent structural deformation alters single-molecule transition kinetics. Proc. Natl. Acad. Sci. U.S.A., 108, 1885-1890.
41. Kruithof, M., Chien, F., de Jager, M. and van Noort, J. (2008) Subpiconewton dynamic force spectroscopy using magnetic tweezers. Biophys. J., 94, 2343-2348.
42. Klaue, D. and Seidel, R. (2009) Torsional stiffness of single superparamagnetic microspheres in an external magnetic feld. Phys. Rev. Lett., 102, 028302.
43. De Vlaminck, I., Henighan, T., van Loenhout, M.T.J., Burnham, D.R. and Dekker, C. (2012) Magnetic forces and DNA mechanics in multiplexed magnetic tweezers. PloS One, 7, e41432.
44. Carter, B.C., Vershinin, M. and Gross, S.P. (2008) A comparison of step-detection methods: how well can you do? Biophys. J., 94, 306-319.
45. Bintu, L., Ishibashi, T., Dangkulwanich, M., Wu, Y.-Y., Lubkowska, L., Kashlev, M. and Bustamante, C. (2012) Nucleosomal elements that control the topography of the barrier to transcription. Cell, 151, 738-749.
46. Claudet, C., Angelov, D., Bouvet, P., Dimitrov, S. and Bednar, J. (2005) Histone octamer instability under single molecule experiment conditions. J. Biol. Chem., 280, 19958-19965.
47. Odijk, T. (1993) Physics of tightly curved semifexible polymer chains. Macromolecules, 26, 6897-6902.
48. Bustamante, C., Smith, S.B., Liphardt, J. and Smith, D. (2000) Single-molecule studies of DNA mechanics. Curr. Opin. Struct. Biol., 10, 279-285.
49. Collepardo-Guevara, R. and Schlick, T. (2011) The effect of linker histone's nucleosome binding affnity on chromatin unfolding mechanisms. Biophys. J., 101, 1670-1680.
50. Bassett, A., Cooper, S., Wu, C. and Travers, A. (2009) The folding and unfolding of eukaryotic chromatin. Curr. Opin. Genet. Dev., 19, 159-165.
51. Bancaud, A., Conde e Silva, N., Barbi, M., Wagner, G., Allemand, J.-F., Mozziconacci, J., Lavelle, C., Croquette, V., Victor, J.-M., Prunell, A. et al. (2006) Structural plasticity of single chromatin fbers revealed by torsional manipulation. Nat. Struct. Mol. Biol., 13, 444-450.
52. Pope, L.H., Bennink, M.L., van Leijenhorst-Groener, K.A., Nikova, D., Greve, J. and Marko, J.F. (2005) Single chromatin fber stretching reveals physically distinct populations of disassembly events. Biophys. J., 88, 3572-3583.
53. Cocco, S., Marko, J.F., Monasson, R., Sarkar, A. and Yan, J. (2003) Force-extension behavior of folding polymers. Eur. Phys. J. E Soft Matter, 10, 249-263.
54. Kimura, H. and Cook, P.R. (2001) Kinetics of core histones in living human cells: little exchange of H3 and H4 and some rapid exchange of H2B. J. Cell Biol., 153, 1341-1353.
55. Jamai, A., Imoberdorf, R.M. and Strubin, M. (2007) Continuous histone H2B and transcription-dependent histone H3 exchange in yeast cells outside of replication. Mol. Cell, 25, 345-355.
56. Koopmans, W.J.A., Buning, R., Schmidt, T. and van Noort, J. (2009) spFRET using alternating excitation and FCS reveals progressive DNA unwrapping in nucleosomes. Biophys. J., 97, 195-204.
57. Poirier, M.G., Oh, E., Tims, H.S. and Widom, J. (2009) Dynamics and function of compact nucleosome arrays. Nat. Struct. Mol. Biol., 16, 938-944.
58. Koslover, E.F., Fuller, C.J., Straight, A.F. and Spakowitz, A.J. (2010) Local geometry and elasticity in compact chromatin structure. Biophys. J., 99, 3941-3950.
59. Kepper, N., Ettig, R., Stehr, R., Marnach, S., Wedemann, G. and Rippe, K. (2011) Force spectroscopy of chromatin fbers: extracting energetics and structural information from Monte Carlo simulations. Biopolymers, 95, 435-447.