Micromanipulation studies of chromatin fibers in Xenopus egg extracts reveal ATP-dependent chromatin assembly dynamics

Molecular Biology of the Cell

Volumn 18, Issue 2, 2007, Pages 464-474

  Yan, Jie ^a,b   Maresca, Thomas J ^c   Skoko, Dunja ^a   Adams, Christian D ^d   Xiao, Botao ^a   Christensen, Morten O ^a,e   Heald, Rebecca ^c   Marko, John F ^f  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d UNIVERSITY OF WISCONSIN MADISON   (United States)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DNA; HISTONE;

ANIMAL CELL; ARTICLE; CELL MANIPULATION; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN STRUCTURE; CONTROLLED STUDY; EGG; ENERGY TRANSFER; ENERGY YIELD; INTERPHASE; MICROMANIPULATION; MOLECULAR DYNAMICS; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROTEIN DNA INTERACTION; XENOPUS;

ADENOSINE TRIPHOSPHATE; ANIMALS; CELL EXTRACTS; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; HYDROLYSIS; MAGNETICS; MICROMANIPULATION; NUCLEOSOMES; OVUM; XENOPUS;

EID: 33846804071     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-09-0800     Document Type: Article

References (59)

1. Almouzni, G., and Wolffe, A. P. (1993). Nuclear assembly, structure, and function: the use of Xenopus in vitro systems. Exp. Cell Res. 205, 1-15.
2. Bancaud, A., et al. (2006). Structural plasticity of single chromatin fibers revealed by torsional manipulation. Nat. Struct. Mol. Biol. 13, 444-450.
3. Belmont, A. (2003). Dynamics of chromatin, proteins, and bodies within the cell nucleus. Curr. Opin. Cell Biol. 15, 304-310.
4. Bennink, M. L., Leuba, S. H., Leno, G. H., Zlatanova, J., de Grooth, B. G., and Greve, J. (2001). Unfolding individual nucleosomes by stretching single chromatin fibers with optical tweezers. Nat. Struct. Biol. 8, 606-610.
5. Berg, H. C. (1993). Random Walks in Biology, Princeton, NJ: Princeton University Press.
6. Bonte, E., and Becker, P. B. (1999). Preparation of chromatin assembly extracts from preblastoderm Drosophila embryos. Methods Mol. Biol. 119, 187-194.
7. Brower-Toland, B., and Wang, M. D. (2004). Use of optical trapping techniques to study single-nucleosome dynamics. Methods Enzymol. 376, 62-72.
8. 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. USA 99, 1960-1965.
9. Brown, D. T., Izard, T., and Misteli, T. (2006). Mapping the interaction surface of linker histone H1(0) with the nucleosome of native chromarin in vivo. Nat. Struct. Mol. Biol. 13, 250-255.
10. Bustamante, C., Marko, J. F., Siggia, E. D., and Smith, S. (1994). Entropic elasticity of lambda-phage DNA. Science 265, 1599-1600.
11. Bustamante, C., Smith, S. B., Liphardt, J., and Smith, D. (2000). Single-molecule studies of DNA mechanics. Curr. Opin. Struct. Biol. 10, 279-285.
12. Chen, D., Dundr, M., Wang, C., Leung, A., Lamond, A., Misteli, T., and Huang, S. (2005). Condensed mitotic chromatin is accessible to transcription factors and chromatin structural proteins. J. Cell Biol. 168, 41-54.
13. 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.
14. Cotton, R. W., and Hamkalo, B. A. (1981). Nucleosome dissociation at physiological ionic strengths. Nucleic Acids Res. 9, 445-457.
15. 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.
16. Dilworth, S. M., Black, S. J., and Laskey, R. A. (1987). Two complexes that contain histones are required for nucleosome assembly in vitro: role of nucleoplasmin and N1 in Xenopus egg extracts. Cell 51, 1009-1018.
17. Evans, E. (2001). Probing the relation between force-lifetime- and chemistry in single molecular bonds. Annu. Rev. Biophys. Biomol. Struct. 30, 105-128.
18. Felsenfeld, G. (1996). Chromarin unfolds. Cell 86, 13-19.
19. Gautier, T., Abbott, D. W., Molla, A., Verdel, A., Ausio, J., and Dimitrov, S. (2004). Histone variant H2ABbd confers lower stability to the nucleosome. EMBO Rep. 5, 715-720.
20. Gemmen, G. J., Sim, R., Haushalter, K. A., Ke, P. C., Kadonaga, J. T., and Smith, D. E. (2005). Forced unraveling of nucleosomes assembled on heterogeneous DNA using core histones, NAP-1, and ACF. J. Mol. Biol. 351, 89-99.
21. Glikin, G. C., Ruberti, I., and Worcel, A. (1984). Chromatin assembly in Xenopus oocytes: in vitro studies. Cell 37, 33-41.
22. Gottesfeld, J. M., and Luger, K. (2001). Energetics and affinity of the histone octamer for defined DNA sequences. Biochemistry 40, 10927-10933.
23. Hirano, T., and Mitchison, T. J. (1991). Cell cycle control of higher-order chromatin assembly around naked DNA in vitro. J. Cell Biol. 115, 1479-1489.
24. Hirano, T., and Mitchison, T. J. (1994). A heterodimeric coiled-coil protein required for mitotic chromosome condensation in vitro. Cell 79, 449-458.
25. Ito, T., Bulger, M., Kobayashi, R., and Kadonaga, J. T. (1996). Drosophila NAP-1 is a core histone chaperone that functions in ATP-facilitated assembly of regularly spaced nucleosomal arrays. Mol. Cell. Biol. 16, 3112-3124.
26. 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.
27. Kleckner, N., Zickler, D., Jones, G. H., Dekker, J., Padmore, R., Henle, J., and Hutchinson, J. (2004). A mechanical basis for chromosome function. Proc. Natl. Acad. Sci. USA 101, 12592-12597.
28. Kleinschmidt, J. A., Seiter, A., and Zentgraf, H. (1990). Nucleosome assembly in vitro: separate histone transfer and synergistic interaction of native histone complexes purified from nuclei of Xenopus laevis oocytes. EMBO J. 9, 1309-1318.
29. Kulic, I. M., and Schiessel, H. (2004). DNA spools under tension. Phys. Rev. Lett. 92, 228101.
30. 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.
31. 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.
32. Laskey, R. A., Mills, A. D., Philpott, A., Leno, G. H., Dilworth, S. M., and Dingwall, C. (1993). The role of nucleoplasmin in chromatin assembly and disassembly. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 339, 263-269; discussion, 268-269.
33. Leuba, S. H., Karymov, M. A., Tomschik, M., Ramjit, R., Smith, P., and Zlatanova, J. (2003). Assembly of single chromatin fibers depends on the tension in the DNA molecule: magnetic tweezers study. Proc. Natl. Acad. Sci. USA 100, 495-500.
34. Levi, V., Ruan, Q., Plutz, M., Belmont, A. S., and Gratton, E. (2005). Chromatin dynamics in interphase cells revealed by tracking in a two-photon excitation microscope. Biophys. J. 89, 4275-4285.
35. MacCallum, D. E., Losada, A., Kobayashi, R., and Hirano, T. (2002). ISWI remodeling complexes in Xenopus egg extracts: identification as major chromosomal components that are regulated by INCENP-aurora B. Mol. Biol. Cell 13, 25-39.
36. Maier, B., Bensimon, D., and Croquette, V. (2000). Replication by a single DNA polymerase of a stretched single-stranded DNA. Proc. Natl. Acad. Sci. USA 97, 12002-12007.
37. Maresca, T. J., Freedman, B. S., and Heald, R. (2005). Histone H1 is essential for mitotic chromosome architecture and segregation in Xenopus laevis egg extracts. J. Cell Biol. 169, 859-869.
38. Marko, J. F., and Siggia, E. D. (1995). Stretching DNA. Macromolecules 28, 8759-8770.
39. Marko, J. F., and Siggia, E. D. (1997a). Driving proteins off DNA using applied tension. Biophys. J. 73, 2173-2178.
40. Marko, J. F., and Siggia, E. D. (1997b). Polymer models of meiotic and mitotic chromosomes. Mol. Biol. Cell 8, 2217-2231.
41. Murray, A. W. (1991). Cell cycle extracts. Methods Cell Biol. 36, 581-605.
42. Park, Y. J., Chodaparambil, J. V., Bao, Y., McBryant, S. J., and Luger, K. (2005). Nucleosome assembly protein 1 exchanges histone H2A-H2B dimers and assists nucleosome sliding. J. Biol. Chem. 280, 1817-1825.
43. Pope, L. H., Bennink, M. L., and Greve, J. (2002). Optical tweezers stretching of chromatin. J. Muscle Res. Cell Motil. 23, 397-407.
44. Pope, L. H., Bennink, M. L., van Leijenhorst-Groener, K. A., Nikova, D., Greve, J., and Marko, J. F. (2005). Single chromatin fiber stretching reveals physically distinct populations of disassembly events. Biophys. J. 88, 3572-3583.
45. Rodriguez-Campos, A., Shimamura, A., and Worcel, A. (1989). Assembly and properties of chromatin containing histone H1. J. Mol. Biol. 209, 135-150.
46. Schaaf, P., and Talbot, J. (1989). Kinetics of random sequential adsorption. Phys. Rev. Lett. 62, 175-178.
47. Shimamura, A., Tremethick, D., and Worcel, A. (1988). Characterization of the repressed 5S DNA minichromosomes assembled in vitro with a high-speed supernatant of Xenopus laevis oocytes. Mol. Cell. Biol. 8, 4257-4269.
48. Shintomi, K., Iwabuchi, M., Saeki, H., Ura, K., Kishimoto, T., and Ohsumi, K. (2005). Nucleosome assembly protein-1 is a linker histone chaperone in Xenopus eggs. Proc. Natl. Acad. Sci. USA 102, 8210-8215.
49. Skoko, D., Wong, B., Johnson, R. C., and Marko, J. F. (2004). Micromechanical analysis of the binding of DNA-bending proteins HMGB1, NHP6A and HU reveals their ability to cooperatively form highly stable DNA-protein complexes. Biochemistry 43, 13867-13874.
50. Smith, S. B., Finzi, L., and Bustamante, C. (1992). Direct mechanical measurements of the elasticity of single DNA molecules by using magnetic beads. Science 258, 1122-1126.
51. Smythe, C., and Newport, J. W. (1991). Systems for the study of nuclear assembly, DNA replication, and nuclear breakdown in Xenopus laevis egg extracts. Methods Cell Biol. 35, 449-468.
52. Strick, T., Allemand, J., Croquette, V., and Bensimon, D. (2000). Twisting and stretching single DNA molecules. Prog. Biophys. Mol. Biol. 74, 115-140.
53. Strick, T. R., Allemand, J. F., Bensimon, D., Bensimon, A., and Croquette, V. (1996). The elasticity of a single supercoiled DNA molecule. Science 271, 1835-1837.
54. Strick, T. R., Allemand, J. F., Bensimon, D., and Croquette, V. (1998). Behavior of supercoiled DNA. Biophys. J. 74, 2016-2028.
55. Thastrom, A., Gottesfeld, J. M., Luger, K., and Widom, J. (2004). Histone-DNA binding free energy cannot be measured in dilution-driven dissociation experiments. Biochemistry 43, 736-741.
56. Wagner, G., Bancaud, A., Quivy, J. P., Clapier, C., Almouzni, G., and Viovy, J. L. (2005). Compaction kinetics on single DNAs: purified nucleosome reconstitution systems versus crude extract. Biophys. J. 89, 3647-3659.
57. 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.
58. Yan, J., Skoko, D., and Marko, J. F. (2004). Near-field-magnetic-tweezer manipulation of single DNA molecules. Phys. Rev. E 70, 011905
59. Yin, H., Wang, M. D., Svoboda, K., Landick, R., Block, S. M., and Gelles, J. (1995). Transcription against an applied force. Science 270, 1653-1657.