Skip to main content
PMC home page
Biophysical Journal logoLink to Biophysical Journal
. 2002 Jan;82(1 Pt 1):345–356. doi: 10.1016/S0006-3495(02)75399-X

Salt-induced conformation and interaction changes of nucleosome core particles.

Stéphanie Mangenot 1, Amélie Leforestier 1, Patrice Vachette 1, Dominique Durand 1, Françoise Livolant 1
PMCID: PMC1302474  PMID: 11751321

Abstract

Small angle x-ray scattering was used to follow changes in the conformation and interactions of nucleosome core particles (NCP) as a function of the monovalent salt concentration C(s). The maximal extension (D(max)) of the NCP (145 +/- 3-bp DNA) increases from 137 +/- 5 A to 165 +/- 5 A when C(s) rises from 10 to 50 mM and remains constant with further increases of C(s) up to 200 mM. In view of the very weak increase of the R(g) value in the same C(s) range, we attribute this D(max) variation to tail extension, a proposal confirmed by simulations of the entire I(q) curves, considering an ideal solution of particles with tails either condensed or extended. This tail extension is observed at higher salt values when particles contain longer DNA fragments (165 +/- 10 bp). The maximal extension of the tails always coincides with the screening of repulsive interactions between particles. The second virial coefficient becomes smaller than the hard sphere virial coefficient and eventually becomes negative (net attractive interactions) for NCP(145). Addition of salt simultaneously screens Coulombic repulsive interactions between NCP and Coulombic attractive interactions between tails and DNA inside the NCP. We discuss how the coupling of these two phenomena may be of biological relevance.

Full Text

The Full Text of this article is available as a PDF (360.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Ausio J., Dong F., van Holde K. E. Use of selectively trypsinized nucleosome core particles to analyze the role of the histone "tails" in the stabilization of the nucleosome. J Mol Biol. 1989 Apr 5;206(3):451–463. doi: 10.1016/0022-2836(89)90493-2. [DOI] [PubMed] [Google Scholar]
  2. Ausio J., Seger D., Eisenberg H. Nucleosome core particle stability and conformational change. Effect of temperature, particle and NaCl concentrations, and crosslinking of histone H3 sulfhydryl groups. J Mol Biol. 1984 Jun 15;176(1):77–104. doi: 10.1016/0022-2836(84)90383-8. [DOI] [PubMed] [Google Scholar]
  3. Ausio J., van Holde K. E. Histone hyperacetylation: its effects on nucleosome conformation and stability. Biochemistry. 1986 Mar 25;25(6):1421–1428. doi: 10.1021/bi00354a035. [DOI] [PubMed] [Google Scholar]
  4. Ballestar E., Boix-Chornet M., Franco L. Conformational changes in the nucleosome followed by the selective accessibility of histone glutamines in the transglutaminase reaction: effects of ionic strength. Biochemistry. 2001 Feb 20;40(7):1922–1929. doi: 10.1021/bi001575b. [DOI] [PubMed] [Google Scholar]
  5. Ballestar E., Franco L. Use of the transglutaminase reaction to study the dissociation of histone N-terminal tails from DNA in nucleosome core particles. Biochemistry. 1997 May 20;36(20):5963–5969. doi: 10.1021/bi9626620. [DOI] [PubMed] [Google Scholar]
  6. Banères J. L., Martin A., Parello J. The N tails of histones H3 and H4 adopt a highly structured conformation in the nucleosome. J Mol Biol. 1997 Oct 31;273(3):503–508. doi: 10.1006/jmbi.1997.1297. [DOI] [PubMed] [Google Scholar]
  7. Cary P. D., Moss T., Bradbury E. M. High-resolution proton-magnetic-resonance studies of chromatin core particles. Eur J Biochem. 1978 Sep 1;89(2):475–482. doi: 10.1111/j.1432-1033.1978.tb12551.x. [DOI] [PubMed] [Google Scholar]
  8. Clark D. J., Kimura T. Electrostatic mechanism of chromatin folding. J Mol Biol. 1990 Feb 20;211(4):883–896. doi: 10.1016/0022-2836(90)90081-V. [DOI] [PubMed] [Google Scholar]
  9. De Lucia F., Alilat M., Sivolob A., Prunell A. Nucleosome dynamics. III. Histone tail-dependent fluctuation of nucleosomes between open and closed DNA conformations. Implications for chromatin dynamics and the linking number paradox. A relaxation study of mononucleosomes on DNA minicircles. J Mol Biol. 1999 Jan 22;285(3):1101–1119. doi: 10.1006/jmbi.1998.2382. [DOI] [PubMed] [Google Scholar]
  10. Dong F., Nelson C., Ausio J. Analysis of the changes in the structure and hydration of the nucleosome core particle at moderate ionic strengths. Biochemistry. 1990 Nov 27;29(47):10710–10716. doi: 10.1021/bi00499a020. [DOI] [PubMed] [Google Scholar]
  11. Fletcher T. M., Hansen J. C. Core histone tail domains mediate oligonucleosome folding and nucleosomal DNA organization through distinct molecular mechanisms. J Biol Chem. 1995 Oct 27;270(43):25359–25362. doi: 10.1074/jbc.270.43.25359. [DOI] [PubMed] [Google Scholar]
  12. Fletcher T. M., Hansen J. C. The nucleosomal array: structure/function relationships. Crit Rev Eukaryot Gene Expr. 1996;6(2-3):149–188. doi: 10.1615/critreveukargeneexpr.v6.i2-3.40. [DOI] [PubMed] [Google Scholar]
  13. Garcia-Ramirez M., Dong F., Ausio J. Role of the histone "tails" in the folding of oligonucleosomes depleted of histone H1. J Biol Chem. 1992 Sep 25;267(27):19587–19595. [PubMed] [Google Scholar]
  14. Greulich K. O., Ausio J., Eisenberg H. Nucleosome core particle structure and structural changes in solution. J Mol Biol. 1985 Nov 5;186(1):167–173. doi: 10.1016/0022-2836(85)90266-9. [DOI] [PubMed] [Google Scholar]
  15. Harp J. M., Hanson B. L., Timm D. E., Bunick G. J. Asymmetries in the nucleosome core particle at 2.5 A resolution. Acta Crystallogr D Biol Crystallogr. 2000 Dec;56(Pt 12):1513–1534. doi: 10.1107/s0907444900011847. [DOI] [PubMed] [Google Scholar]
  16. Hilliard P. R., Jr, Smith R. M., Rill R. L. Natural abundance carbon-13 nuclear magnetic resonance studies of histone and DNA dynamics in nucleosome cores. J Biol Chem. 1986 May 5;261(13):5992–5998. [PubMed] [Google Scholar]
  17. Imai B. S., Yau P., Baldwin J. P., Ibel K., May R. P., Bradbury E. M. Hyperacetylation of core histones does not cause unfolding of nucleosomes. Neutron scatter data accords with disc shape of the nucleosome. J Biol Chem. 1986 Jul 5;261(19):8784–8792. [PubMed] [Google Scholar]
  18. Inoko Y., Yamamoto M., Fujiwara S., Ueki T. X-ray scattering study of the shape of the DNA region in nucleosome core particle with synchrotron radiation. J Biochem. 1992 Mar;111(3):310–316. doi: 10.1093/oxfordjournals.jbchem.a123755. [DOI] [PubMed] [Google Scholar]
  19. Kornberg R. D., Lorch Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell. 1999 Aug 6;98(3):285–294. doi: 10.1016/s0092-8674(00)81958-3. [DOI] [PubMed] [Google Scholar]
  20. Leforestier A., Dubochet J., Livolant F. Bilayers of nucleosome core particles. Biophys J. 2001 Oct;81(4):2414–2421. doi: 10.1016/S0006-3495(01)75888-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Leforestier A., Livolant F. Liquid crystalline ordering of nucleosome core particles under macromolecular crowding conditions: evidence for a discotic columnar hexagonal phase. Biophys J. 1997 Oct;73(4):1771–1776. doi: 10.1016/S0006-3495(97)78207-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Libertini L. J., Ausió J., van Holde K. E., Small E. W. Histone hyperacetylation. Its effects on nucleosome core particle transitions. Biophys J. 1988 Apr;53(4):477–487. doi: 10.1016/S0006-3495(88)83126-6. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Livolant F., Leforestier A. Chiral discotic columnar germs of nucleosome core particles. Biophys J. 2000 May;78(5):2716–2729. doi: 10.1016/S0006-3495(00)76816-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Luger K., Mäder A. W., Richmond R. K., Sargent D. F., Richmond T. J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature. 1997 Sep 18;389(6648):251–260. doi: 10.1038/38444. [DOI] [PubMed] [Google Scholar]
  25. Luger K., Richmond T. J. The histone tails of the nucleosome. Curr Opin Genet Dev. 1998 Apr;8(2):140–146. doi: 10.1016/s0959-437x(98)80134-2. [DOI] [PubMed] [Google Scholar]
  26. Mutskov V., Gerber D., Angelov D., Ausio J., Workman J., Dimitrov S. Persistent interactions of core histone tails with nucleosomal DNA following acetylation and transcription factor binding. Mol Cell Biol. 1998 Nov;18(11):6293–6304. doi: 10.1128/mcb.18.11.6293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Oliva R., Bazett-Jones D. P., Locklear L., Dixon G. H. Histone hyperacetylation can induce unfolding of the nucleosome core particle. Nucleic Acids Res. 1990 May 11;18(9):2739–2747. doi: 10.1093/nar/18.9.2739. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Petsev D. N., Vekilov P. G. Evidence for non-DLVO hydration interactions in solutions of the protein apoferritin. Phys Rev Lett. 2000 Feb 7;84(6):1339–1342. doi: 10.1103/PhysRevLett.84.1339. [DOI] [PubMed] [Google Scholar]
  29. Pérez J., Vachette P., Russo D., Desmadril M., Durand D. Heat-induced unfolding of neocarzinostatin, a small all-beta protein investigated by small-angle X-ray scattering. J Mol Biol. 2001 May 11;308(4):721–743. doi: 10.1006/jmbi.2001.4611. [DOI] [PubMed] [Google Scholar]
  30. Richmond T. J., Finch J. T., Rushton B., Rhodes D., Klug A. Structure of the nucleosome core particle at 7 A resolution. Nature. 1984 Oct 11;311(5986):532–537. doi: 10.1038/311532a0. [DOI] [PubMed] [Google Scholar]
  31. Smith R. M., Rill R. L. Mobile histone tails in nucleosomes. Assignments of mobile segments and investigations of their role in chromatin folding. J Biol Chem. 1989 Jun 25;264(18):10574–10581. [PubMed] [Google Scholar]
  32. Tardieu A., Vérétout F., Krop B., Slingsby C. Protein interactions in the calf eye lens: interactions between beta-crystallins are repulsive whereas in gamma-crystallins they are attractive. Eur Biophys J. 1992;21(1):1–12. doi: 10.1007/BF00195438. [DOI] [PubMed] [Google Scholar]
  33. Walker I. O. Differential dissociation of histone tails from core chromatin. Biochemistry. 1984 Nov 6;23(23):5622–5628. doi: 10.1021/bi00318a037. [DOI] [PubMed] [Google Scholar]
  34. Wang X., Moore S. C., Laszckzak M., Ausió J. Acetylation increases the alpha-helical content of the histone tails of the nucleosome. J Biol Chem. 2000 Nov 10;275(45):35013–35020. doi: 10.1074/jbc.M004998200. [DOI] [PubMed] [Google Scholar]
  35. Widom J. Physicochemical studies of the folding of the 100 A nucleosome filament into the 300 A filament. Cation dependence. J Mol Biol. 1986 Aug 5;190(3):411–424. doi: 10.1016/0022-2836(86)90012-4. [DOI] [PubMed] [Google Scholar]
  36. Yager T. D., McMurray C. T., van Holde K. E. Salt-induced release of DNA from nucleosome core particles. Biochemistry. 1989 Mar 7;28(5):2271–2281. doi: 10.1021/bi00431a045. [DOI] [PubMed] [Google Scholar]

Articles from Biophysical Journal are provided here courtesy of The Biophysical Society

RESOURCES