The dynamics of individual nucleosomes controls the chromatin condensation pathway: Direct atomic force microscopy visualization of variant chromatin

Biophysical Journal

Volumn 97, Issue 2, 2009, Pages 544-553

  Montel, Fabien ^a,b   Menoni, Hervé ^b   Castelnovo, Martin ^a,b   Bednar, Jan ^c,d,e   Dimitrov, Stefan ^f   Angelov, Dimitar ^b   Faivre Moskalenko, Cendrine ^a,b  

^a Laboratoire Joliot Curie   (France)

^b UNIVERSITÉ DE LYON   (France)

^c CNRS   (France)

^d CHARLES UNIVERSITY   (Czech Republic)

^e INSTITUTE OF PHYSIOLOGY   (Czech Republic)

^f UNIV GRENOBLE ALPES   (France)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE H2A; PROTEIN H2A BBD; PROTEIN H2A BBD DDH2A; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; CELL INTERACTION; CELL NUCLEUS; CHROMATIN; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA SEQUENCE; IMAGE ANALYSIS; MOLECULAR IMAGING; NONHUMAN; NUCLEOSOME; PROTEIN PURIFICATION; PROTEIN VARIANT; SIGNAL TRANSDUCTION; THEORETICAL MODEL; X CHROMATIN;

EID: 68949136888     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.04.042     Document Type: Article

References (36)

1. van Holde, K. 1988. Chromatin. Springer-Verlag KG, Berlin.
2. Luger, K., A. W. Mader, R. K. Richmond, D. F. Sargent, and T. J. Richmond. 1997. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 389:251-260.
3. Schalch, T., S. Duda, D. F. Sargent, and T. J. Richmond. 2005. X-ray structure of a tetranucleosome and its implications for the chromatin fibre. Nature. 436:138-141.
4. Robinson, P. J., L. Fairall, V. A. Huynh, and D. Rhodes. 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.
5. Routh, A., S. Sandin, and D. Rhodes. 2008. Nucleosome repeat length and linker histone stoichiometry determine chromatin fiber structure. Proc. Natl. Acad. Sci. USA. 105:8872-8877.
6. Robinson, P. J., W. An, A. Routh, F. Martino, L. Chapman, et al. 2008. 30 nm chromatin fibre decompaction requires both H4-K16 acetylation and linker histone eviction. J. Mol. Biol. 381:816-825.
7. Sims, 3rd, R. J., and D. Reinberg. 2008. Is there a code embedded in proteins that is based on post-translational modifications? Nat. Rev. Mol. Cell Biol. 9:815-820.
8. Boulard, M., P. Bouvet, T. K. Kundu, and S. Dimitrov. 2007. Histone variant nucleosomes: structure, function and implication in disease. Subcell. Biochem. 41:71-89.
9. Gonzalez-Romero, R., J. Mendez, J. Ausio, and J. M. Eirin-Lopez. 2008. Quickly evolving histones, nucleosome stability and chromatin folding: All about histone H2A.Bbd. Gene. 413:1-7.
10. Chadwick, B. P., and H. F. Willard. 2001. A novel chromatin protein, distantly related to histone H2A, is largely excluded from the inactive X chromosome. J. Cell Biol. 152:375-384.
11. Bao, Y., K. Konesky, Y. J. Park, S. Rosu, P. N. Dyer, et al. 2004. Nucleosomes containing the histone variant H2A.Bbd organize only 118 base pairs of DNA. EMBO J. 23:3314-3324.
12. Doyen, C. M., F. Montel, T. Gautier, H. Menoni, C. Claudet, et al. 2006. Dissection of the unusual structural and functional properties of the variant H2A.Bbd nucleosome. EMBO J. 25:4234-4244.
13. Montel, F., E. Fontaine, P. St.-Jean, M. Castelnovo, and C. Faivre-Moskalenko. 2007. Atomic force microscopy imaging of SWI/SNF action: mapping the nucleosome remodeling and sliding. Biophys. J. 93:566-578.
14. Gautier, T., D. W. Abbott, A. Molla, A. Verdel, J. Ausio, et al. 2004. Histone variant H2ABbd confers lower stability to the nucleosome. EMBO Rep. 5:715-720.
15. Angelov, D., A. Verdel, W. An, V. Bondarenko, F. Hans, et al. 2004. SWI/SNF remodeling and p300-dependent transcription of histone variant H2ABbd nucleosomal arrays. EMBO J. 23:3815-3824.
16. Menoni, H., D. Gasparutto, A. Hamiche, J. Cadet, S. Dimitrov, et al. 2007. ATP-dependent chromatin remodeling is required for base excision repair in conventional but not in variant H2A.Bbd nucleosomes. Mol. Cell. Biol. 27:5949-5956.
17. Zhou, J., J. Y. Fan, D. Rangasamy, and D. J. Tremethick. 2007. The nucleosome surface regulates chromatin compaction and couples it with transcriptional repression. Nat. Struct. Mol. Biol. 14:1070-1076.
18. Huynh, V. A., P. J. Robinson, and D. Rhodes. 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.
19. Luger, K., T. J. Rechsteiner, and T. J. Richmond. 1999. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. 119:1-16.
20. Mutskov, V., D. Gerber, D. Angelov, J. Ausio, J. Workman, et al. 1998. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol. Cell. Biol. 18:6293-6304.
21. Lyubchenko, Y. L., P. I. Oden, D. Lampner, S. M. Lindsay, and K. A. Dunker. 1993. Atomic force microscopy of DNA and bacteriophage in air, water and propanol: the role of adhesion forces. Nucleic Acids Res. 21:1117-1123.
22. Gonzales, R. C., and P. Wintz. 1987. Digital Image Processing. 2nd ed. Addison-Wesley, Reading, MA.
23. Koch, M. H., P. Vachette, and D. I. Svergun. 2003. Small-angle scattering: a view on the properties, structures and structural changes of biological macromolecules in solution. Q. Rev. Biophys. 36:147-227.
24. Lowary, P. T., and J. Widom. 1998. New DNA sequence rules for high affinity binding to histone octamer and sequence-directed nucleosome positioning. J. Mol. Biol. 276:19-42.
25. Claudet, C., D. Angelov, P. Bouvet, S. Dimitrov, and J. Bednar. 2005. Histone octamer instability under single molecule experiment conditions. J. Biol. Chem. 280:19958-19965.
26. Zlatanova, J., and S. H. Leuba. 2003. Chromatin fibers, one-at-a-time. J. Mol. Biol. 331:1-19.
27. Dalal, Y., H. Wang, S. Lindsay, and S. Henikoff. 2007. Tetrameric structure of centromeric nucleosomes in interphase Drosophila cells. PLoS Biol. 5:e218.
28. Valle, F., M. Favre, P. De Los Rios, A. Rosa, and G. Dietler. 2005. Scaling exponents and probability distributions of DNA end-to-end distance. Phys. Rev. Lett. 95:158105.
29. Yodh, J. G., Y. L. Lyubchenko, L. S. Shlyakhtenko, N. Woodbury, and D. Lohr. 1999. Evidence for nonrandom behavior in 208-12 subsaturated nucleosomal array populations analyzed by AFM. Biochemistry. 38:15756-15763.
30. Poirier, M. G., M. Bussiek, J. Langowski, and J. Widom. 2008. Spontaneous access to DNA target sites in folded chromatin fibers. J. Mol. Biol. 379:772-786.
31. Kepert, J. F., J. Mazurkiewicz, G. L. Heuvelman, K. F. Toth, and K. Rippe. 2005. NAP1 modulates binding of linker histone H1 to chromatin and induces an extended chromatin fiber conformation. J. Biol. Chem. 280:34063-34072.
32. Lebedev, D. V., M. V. Filatov, A. I. Kuklin, A. K. Islamov, J. Stellbrink, et al. 2008. Structural hierarchy of chromatin in chicken erythrocyte nuclei based on small-angle neutron scattering: Fractal nature of the large-scale chromatin organization. Crystallogr. Rep. 53:110-115.
33. Akiyama, S., S. Takahashi, T. Kimura, K. Ishimori, I. Morishima, et al. 2002. Conformational landscape of cytochrome c folding studied by microsecond-resolved small-angle x-ray scattering. Proc. Natl. Acad. Sci. USA. 99:1329-1334.
34. Schiessel, H. 2006. The nucleosome: a transparent, slippery, sticky and yet stable DNA-protein complex. Eur. Phys, J. E. 19:251-262.
35. Wu, C., A. Bassett, and A. Travers. 2007. A variable topology for the 30-nm chromatin fibre. EMBO Rep. 8:1129-1134.
36. Shogren-Knaak, M., H. Ishii, J. M. Sun, M. J. Pazin, J. R. Davie, et al. 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science. 311:844-847.