10 Years of tension on chromatin: Results from single molecule force spectroscopy

Current Pharmaceutical Biotechnology

Volumn 10, Issue 5, 2009, Pages 474-485

  Chien, Fan Tso ^a   Van Noort, John ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HISTONE;

ACCURACY; ACETYLATION; ATOMIC FORCE MICROSCOPY; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CRYSTALLIZATION; DNA MICROARRAY; DYNAMICS; ELASTICITY; ELECTRON MICROSCOPY; ELECTROPHORESIS; GENE EXPRESSION REGULATION; NUCLEOSOME; OPTICAL TWEEZERS; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN MODIFICATION; REVIEW; SINGLE MOLECULE FORCE SPECTROSCOPY; SPECTROSCOPY; STOICHIOMETRY; TENSION; X RAY CRYSTALLOGRAPHY; CHEMISTRY; HUMAN; INSTRUMENTATION; METHODOLOGY; PROTEIN CONFORMATION; ULTRASTRUCTURE;

EUKARYOTA;

CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA; HISTONES; HUMANS; MICROSCOPY, ATOMIC FORCE; NUCLEOSOMES; OPTICAL TWEEZERS; PROTEIN CONFORMATION; PROTEIN FOLDING; SPECTRUM ANALYSIS;

EID: 70350435635     PISSN: 13892010     EISSN: 18734316     Source Type: Journal    
DOI: 10.2174/138920109788922128     Document Type: Review

References (81)

1. Luger, K.; Mader, A.; Richmond, R.; Sargent, D. and Richmond, T. (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature, 389, 251-260. (Pubitemid 27406632)
2. Sheng, S.; Czajkowsky, D. and Shao, Z. (2006) Localization of linker histone in chromatosomes by cryo-atomic force microscopy. Biophys. J., 91, L35-L37. (Pubitemid 44174236)
3. Finch, J. T. and Klug, A. (1976) Solenoidal model for superstructure in chromatin. Proc. Natl. Acad. Sci. USA, 73, 1897-1901.
4. Thoma, F.; Koller, T. and Klug, A. (1979) Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J. Cell Biol., 83, 403-427. (Pubitemid 10205723)
5. d'Erme, M.; Yang, G.; Sheagly, E.; Palitti, F. and Bustamante, C. (2001) Effect of poly(adp-ribosyl)ation and Mg2+ ions on chromatin structure revealed by scanning force microscopy. Biochemistry, 40, 10947-10955.
6. Strick, R.; Strissel, P.; Gavrilov, K. and Levi-Setti, R. (2001) Cation-chromatin binding as shown by ion microscopy is essential for the structural integrity of chromosomes. J. Cell Biol., 155, 899-910. (Pubitemid 34286242)
7. Müller, W. G.; Rieder, D.; Karpova, T. S.; John, S.; Trajanoski, Z. and McNally, J. G. (2007) Organization of chromatin and histone modifications at a transcription site. J. Cell Biol., 177, 957-967. (Pubitemid 46955701)
8. Conconi, A. (2005) The yeast rDNA locus: a model system to study DNA repair in chromatin. DNA Repair (Amst), 4, 897-908.
9. Roca, J. (2009) Topoisomerase II: a fitted mechanism for the chromatin landscape. Nucleic Acids Res., 37, 721-730.
10. Chaban, Y.; Ezeokonkwo, C.; Chung, W.-H.; Zhang, F.; Kornberg, R. D.; Maier-Davis, B.; Lorch, Y. and Asturias, F. J. (2008) Structure of a RSC-nucleosome complex and insights into chromatin remodeling. Nat. Struct. Mol. Biol., 15, 1272-1277.
11. Gerlich, D.; Hirota, T.; Koch, B.; Peters, J.-M. and Ellenberg, J. (2006) Condensin I stabilizes chromosomes mechanically through a dynamic interaction in live cells. Curr. Biol., 16, 333-344.
12. Milne, T. A.; Zhao, K. and Hess, J. L. (2009) Chromatin Immuno Precipitation (ChIP) for analysis of histone modifications and chromatin-associated proteins. Methods Mol. Biol., 538, 1-15.
13. Lavelle, C. (2009) Forces and torques in the nucleus: chromatin under mechanical constraints. Biochem. Cell Biol., 87, 307-322.
14. Wang, M. D.; Schnitzer, M. J.; Yin, H.; Landick, R.; Gelles, J. and Block, S. M. (1998) Force and velocity measured for single molecules of RNA polymerase. Science, 282, 902-907. (Pubitemid 28507515)
15. Hamdan, S. M.; Loparo, J. J.; Takahashi, M.; Richardson, C. C. and van Oijen, A. M. (2009) Dynamics of DNA replication loops reveal temporal control of lagging-strand synthesis. Nature, 457, 336-339.
16. Zhang, Y.; Smith, C.; Saha, A.; Grill, S.; Mihardja, S.; Smith, S.; Cairns, B.; Peterson, C. and Bustamante, C. (2006) DNA translocation and loop formation mechanism of chromatin remodeling by SWI/SNF and RSC. Mol. Cell, 24, 559-568. (Pubitemid 350284224)
17. Leschziner, A.; Saha, A.; Wittmeyer, J.; Zhang, Y.; Bustamante, C.; Cairns, B. and Nogales, E. (2007) Conformational flexibility in the chromatin remodeler RSC observed by electron microscopy and the orthogonal tilt reconstruction method. Proc. Natl. Acad. Sci. USA, 104, 4913-4918. (Pubitemid 47186151)
18. Hansen, J. C. (2002) Conformational dynamics of the chromatin fiber in solution: determinants, mechanisms, and functions. Annu. Rev. Biophys. Biomol. Struct., 31, 361-392.
19. Tremethick, D. (2007). Higher-order structures of chromatin: the elusive 30 nm fiber. Cell, 128, 651-654.
20. Horn, P. and Peterson, C. (2002) Chromatin higher order folding- wrapping up transcription. Science, 297, 1824-1827.
21. van Holde, K. and Zlatanova, J. (2007) Chromatin fiber structure: where is the problem now? Semin Cell Dev. Biol., 18, 651-658. (Pubitemid 350026429)
22. Robinson, P. and Rhodes, D. (2006) Structure of the '30 nm' chromatin fibre: a key role for the linker histone. Curr. Opin. Struct. Biol., 16, 336-343.
23. Widom, J. and Klug, A. (1985) Structure of the 300. A chromatin filament: X-ray diffraction from oriented samples. Cell, 43, 207-213. (Pubitemid 16199706)
24. Woodcock, C.L.; Frado, L.L. and Rattner, J.B. (1984) The higher-order structure of chromatin: evidence for a helical ribbon arrangement. J. Cell Biol., 99, 42-52.
25. Woodcock, C.; Grigoryev, S.; Horowitz, R. and Whitaker, N. (1993) A chromatin folding model that incorporates linker variability generates fibers resembling the native structures. Proc. Natl. Acad. Sci. USA, 90, 9021-9025. (Pubitemid 23306443)
26. Olins, A. L.; Carlson, R. D. and Olins, D. E. (1975) Visualization of chromatin substructure: upsilon bodies. J. Cell Biol., 64, 528-537.
27. Olins, A. L.; Senior, M. B. and Olins, D. E. (1976) Ultrastructural features of chromatin nu bodies. J. Cell Biol., 68, 787-793.
28. Leuba, S.; Bennink, M. and Zlatanova, J. (2004) Single-molecule analysis of chromatin. Meth. Enzymol., 376, 73-105.
29. Robinson, P.; Fairall, L.; Huynh, V. and Rhodes, D. (2006) EM measurements define the dimensions of the "30-nm" chromatin fiber: evidence for a compact, interdigitated structure. Proc. Natl. Acad. Sci. USA, 103, 6506-6511.
30. Felsenfeld, G. and McGhee, J.D. (1986) Structure of the 30 nm chromatin fiber. Cell, 44, 375-377.
31. Schalch, T.; Duda, S.; Sargent, D. and Richmond, T. (2005) X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature, 436, 138-141. (Pubitemid 40966200)
32. Dorigo, B.; Schalch, T.; Kulangara, A.; Duda, S.; Schroeder, R. and Richmond, T. (2004) Nucleosome arrays reveal the two-start organization of the chromatin fiber. Science, 306, 1571-1573. (Pubitemid 39564956)
33. Bednar, J.; Horowitz, R.; Grigoryev, S.; Carruthers, L.; Hansen, J.; Koster, A. and Woodcock, C. (1998) Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc. Natl. Acad. Sci. USA, 95, 14173-14178. (Pubitemid 28549340)
34. Ausió, J. (2000) Analytical ultracentrifugation and the characterization of chromatin structure. Biophys. Chem., 86, 141-153.
35. Butler, P. J. and Thomas, J. O. (1980) Changes in chromatin folding in solution. J. Mol. Biol., 140, 505-529.
36. 2. solubility and binding studies, transition to and characterization of the higher-order structure. J. Mol. Biol., 177, 373-398.
37. Rabbani, A.; Iskandar, M. and Ausió, J. (1999) Daunomycin-induced unfolding and aggregation of chromatin. J. Biol. Chem., 274, 18401-18406.
38. Dorigo, B.; Schalch, T.; Bystricky, K. and Richmond, T. J. (2003) Chromatin fiber folding: requirement for the histone H4 N-terminal tail. J. Mol. Biol., 327, 85-96. (Pubitemid 36293304)
39. Shogren-Knaak, M.; Ishii, H.; Sun, J.-M.; Pazin, M. J.; Davie, J. R. and Peterson, C. L. (2006) Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 311, 844-847. (Pubitemid 43228847)
40. Brower-Toland, B.; Smith, C.; Yeh, R.; Lis, J.; Peterson, C. and Wang, M. (2002) Mechanical disruption of individual nucleosomes reveals a reversible multistage release of DNA. Proc. Natl. Acad. Sci. USA, 99, 1960-1965. (Pubitemid 34168997)
41. Brower-Toland, B.; Wacker, D. A.; Fulbright, R. M.; Lis, J. T.; Kraus, W. L. and Wang, M. D. (2005) Specific contributions of histone tails and their acetylation to the mechanical stability of nucleosomes. J. Mol. Biol., 346, 135-146.
42. Bennink, M.; Leuba, S.; Leno, G.; Zlatanova, J.; de Grooth, B. and Greve, J. (2001) Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers. Nat. Struct. Biol., 8, 606-610.
43. Cui, Y. and Bustamante, C. (2000) Pulling a single chromatin fiber reveals the forces that maintain its higher-order structure. Proc. Natl. Acad. Sci. USA, 97, 127-132. (Pubitemid 30055795)
44. 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. (Pubitemid 41379524)
45. Kruithof, M.; Chien, F.; de Jager, M. and van Noort, S. (2007) Sub-piconewton dynamic force spectroscopy using magnetic tweezers. Biophys. J., 94, 2343-2348.
46. Strick, T. R.; Allemand, J. F.; Bensimon, D. and Croquette, V. (1998) Behavior of supercoiled DNA. Biophys. J., 74, 2016-2028.
47. Ladoux, B.; Quivy, J. P.; Doyle, P.; du Roure, O.; Almouzni, G. and Viovy, J. L. (2000) Fast kinetics of chromatin assembly revealed by single-molecule videomicroscopy and scanning force microscopy. Proc. Natl. Acad. Sci. USA, 97, 14251-14256.
48. Fotiadis, D.; Scheuring, S.; Müller, S. A.; Engel, A. and Müller, D. J. (2002) Imaging and manipulation of biological structures with the AFM. Micron, 33, 385-397.
49. Leuba, S. H.; and Zlatanova, J. (2002) Single-molecule studies of chromatin fibers: a personal report. Arch. Histol. Cytol., 65, 391-403.
50. Moffitt, J. R.; Chemla, Y. R.; Smith, S. B. and Bustamante, C. (2008) Recent advances in optical tweezers. Annu. Rev. Biochem., 77, 205-228.
51. Neuman, K. C. and Nagy, A. (2008) Single-molecule force spectroscopy: optical tweezers, magnetic tweezers and atomic force microscopy. Nat. Methods, 5, 491-505. (Pubitemid 351761756)
52. Mihardja, S.; Spakowitz, A.; Zhang, Y. and Bustamante, C. (2006) Effect of force on mononucleosomal dynamics. Proc. Natl. Acad. Sci. USA, 103, 15871-15876.
53. Kruithof, M. and van Noort, J. (2009) Hidden Markov analysis of nucleosome unwrapping under force. Biophys. J., 96, 3708-3715.
54. Kulic, I.; Mohrbach, H.; Lobaskin, V.; Thaokar, R. and Schiessel, H. (2005) Apparent persistence length renormalization of bent DNA. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 72, 041905. (Pubitemid 43273102)
55. Poirier, M. G.; Bussiek, M.; Langowski, J. and Widom, J.(2008) Spontaneous access to DNA target sites in folded chromatin fibers. J. Mol. Biol., 379, 772-786.
56. Koopmans, W.; Brehm, A.; Logie, C.; Schmidt, T. and van Noort, S. (2007) Single-pair FRET microscopy reveals mononucleosome dynamics. J. Fluoresc., 17, 785-795 (Pubitemid 350075697)
57. Hall, M. A.; Shundrovsky, A.; Bai, L.; Fulbright, R. M.; Lis, J. T. and Wang, M. D. (2009) High-resolution dynamic mapping of histone- DNA interactions in a nucleosome. Nat. Struct. Mol. Biol., 16, 124-129.
58. Shundrovsky, A.; Smith, C. L.; Lis, J. T.; Peterson, C. L. and Wang, M. D. (2006) Probing SWI/SNF remodeling of the nucleosome by unzipping single DNA molecules. Nat. Struct. Mol. Biol., 13, 549-554. (Pubitemid 43848910)
59. Laskey, R. A.; Mills, A. D. and Morris, N. R. (1977) Assembly of SV40 chromatin in a cell-free system from Xenopus eggs. Cell, 10, 237-243. (Pubitemid 8056265)
60. Gemmen, G.; Sim, R.; Haushalter, K.; Ke, P.; Kadonaga, J. and Smith, D. (2005) Forced unraveling of nucleosomes assembled on heterogeneous DNA using core histones, NAP-1, and ACF. J. Mol. Biol., 351, 89-99. (Pubitemid 40967057)
61. Huynh, V.; Robinson, P. and Rhodes, D. (2005) A method for the in vitro reconstitution of a defined "30 nm" chromatin fibre containing stoichiometric amounts of the linker histone. J. Mol. Biol., 345, 957-968.
62. Thåström, A.; Lowary, P. T.; Widlund, H. R.; Cao, H.; Kubista, M. and Widom, J.(1999) Sequence motifs and free energies of selected natural and non-natural nucleosome positioning DNA sequences. J. Mol. Biol., 288, 213-229. (Pubitemid 29209873)
63. Lowary, P. and Widom, J. (1998) New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol.Biol., 276, 19-42. (Pubitemid 28085408)
64. 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 fibers. Nat. Struct. Mol. Biol., 16, 534-540.
65. Bancaud, A.; e Silva, C.; Barbi, M.; Wagner, G.; Allemand, J.; Mozziconacci, J.; Lavelle, C.; Croquette, V.; Victor, J.; Prunell, A. and Viovy, J. (2006) Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat. Struct. Mol. Biol., 13, 444-450.
66. Dworkin-Rastl, E.; Kandolf, H. and Smith, R. C. (1994) The maternal histone H1 variant, H1M (B4 protein), is the predominant H1 histone in Xenopus pregastrula embryos. Dev. Biol., 161, 425-439. (Pubitemid 24077412)
67. An, W.; van Holde, K. and Zlatanova, J. (1998) The non-histone chromatin protein HMG1 protects linker DNA on the side opposite to that protected by linker histones. J. Biol. Chem., 273, 26289-26291.
68. Pope, L.; Bennink, M.; van Leijenhorst-Groener, K.; Nikova, D.; Greve, J. and Marko, J. (2005) Single chromatin fiber stretching reveals physically distinct populations of disassembly events. Biophys. J., 88, 3572-3583. (Pubitemid 40586605)
69. Yan, J.; Maresca, T. J.; Skoko, D.; Adams, C. D.; Xiao, B.; Christensen, M. O.; Heald, R. and Marko, J. F. (2007) Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics. Mol. Biol. Cell, 18, 464-474. (Pubitemid 46213216)
70. Robinson, P. J. J.; An, W.; Routh, A.; Martino, F.; Chapman, L.; Roeder, R. G. and Rhodes, D. (2008) 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J. Mol. Biol., 381, 816-825.
71. Roopa, T. and Shivashankar, G. V. (2006) Direct measurement of local chromatin fluidity using optical trap modulation force spectroscopy. Biophys. J., 91, 4632-4637. (Pubitemid 44904248)
72. Strahl, B. D. and Allis, C. D. (2000) The language of covalent histone modifications. Nature, 403, 41-45.
73. Langowski, J. and Heermann, D. W. (2007) Computational modeling of the chromatin fiber. Semin. Cell Dev. Biol., 18, 659-667.
74. Langowski, J. (2006) Polymer chain models of dna and chromatin. Eur. Phys. J. E Soft Matter, 19, 241-249.
75. Mergell, B.; Everaers, R. and Schiessel, H. (2004) Nucleosome interactions in chromatin: fiber stiffening and hairpin formation. Phys. Rev. E Stat., Nonlin. Soft Matter Phys., 70, 011915.
76. Stehr, R.; Kepper, N.; Rippe, K. and Wedemann, G. (2008) The effect of internucleosomal interaction on folding of the chromatin fiber. Biophys. J., 95, 3677-3691.
77. Depken, M.; and Schiessel, H. (2009) Nucleosome shape dictates chromatin fiber structure. Biophys. J., 96, 777-784.
78. Wong, H.; Victor, J. and Mozziconacci, J. (2007) An all-atom model of the chromatin fiber containing linker histones reveals a versatile structure tuned by the nucleosomal repeat length. PLoS ONE, 2, e877.
79. Garcia, H.; Grayson, P.; Han, L.; Inamdar, M.; Kondev, J.; Nelson, P.; Phillips, R.; Widom, J. and Wiggins, P. (2006) Biological consequences of tightly bent DNA: the other life of a macromolecular celebrity. Biopolymers, 85, 115-130. (Pubitemid 46306069)
80. McGinty, R. K.; Kim, J.; Chatterjee, C.; Roeder, R. G. and Muir, T. W. (2008) Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature, 453, 812-816.
81. Neumann, H.; Hancock, S.; Buning, R.; Routh, A.; Chapman, L.; Somers, J.; Owen-Hughes, T.; van Noort, J.; Rhodes, D. and Chin, J. (2009) Site-specifically acetylated histones define the structural and functional role of H3 K56 acetylation. Submitted for publication.