Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1990 Oct;87(19):7603–7607. doi: 10.1073/pnas.87.19.7603

Direct detection of linker DNA bending in defined-length oligomers of chromatin.

J Yao 1, P T Lowary 1, J Widom 1
PMCID: PMC54796  PMID: 2217191

Abstract

Linker DNA, which connects between nucleosomes in chromatin, is short and, therefore, may be essentially straight and inflexible. We have carried out hydrodynamic and electron microscopic studies of dinucleosomes--fragments of chromatin containing just two nucleosomes--to test the ability of linker DNA to bend. We find that ionic conditions that stabilize the folding of long chromatin cause linker DNA in dinucleosomes to bend, bringing the two nucleosomes into contact. The results uphold a key prediction of the solenoid model of chromosome folding and suggest a mechanism by which proteins that are separated along the DNA can interact by direct contact.

Full text

PDF
7603

Images in this article

7606Image
on p.7606
7606Image
on p.7606

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. Bates D. L., Butler P. J., Pearson E. C., Thomas J. O. Stability of the higher-order structure of chicken-erythrocyte chromatin in solution. Eur J Biochem. 1981 Oct;119(3):469–476. doi: 10.1111/j.1432-1033.1981.tb05631.x. [DOI] [PubMed] [Google Scholar]
  3. Bates D. L., Thomas J. O. Histones H1 and H5: one or two molecules per nucleosome? Nucleic Acids Res. 1981 Nov 25;9(22):5883–5894. doi: 10.1093/nar/9.22.5883. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Belmont A., Nicolini C. Polyelectrolyte theory and chromatin-DNA quaternary structure: role of ionic strength and H1 histone. J Theor Biol. 1981 May 21;90(2):169–179. doi: 10.1016/0022-5193(81)90040-0. [DOI] [PubMed] [Google Scholar]
  5. Bordas J., Perez-Grau L., Koch M. H., Vega M. C., Nave C. The superstructure of chromatin and its condensation mechanism. I. Synchrotron radiation X-ray scattering results. Eur Biophys J. 1986;13(3):157–173. doi: 10.1007/BF00542560. [DOI] [PubMed] [Google Scholar]
  6. Burch J. B., Martinson H. G. The roles of H1, the histone core and DNA length in the unfolding of nucleosomes at low ionic strength. Nucleic Acids Res. 1980 Nov 11;8(21):4969–4987. doi: 10.1093/nar/8.21.4969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Butler P. J., Thomas J. O. Changes in chromatin folding in solution. J Mol Biol. 1980 Jul 15;140(4):505–529. doi: 10.1016/0022-2836(80)90268-5. [DOI] [PubMed] [Google Scholar]
  8. Clark D. J., Thomas J. O. Differences in the binding of H1 variants to DNA. Cooperativity and linker-length related distribution. Eur J Biochem. 1988 Dec 1;178(1):225–233. doi: 10.1111/j.1432-1033.1988.tb14447.x. [DOI] [PubMed] [Google Scholar]
  9. Finch J. T., Klug A. Solenoidal model for superstructure in chromatin. Proc Natl Acad Sci U S A. 1976 Jun;73(6):1897–1901. doi: 10.1073/pnas.73.6.1897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Finch J. T., Noll M., Kornberg R. D. Electron microscopy of defined lengths of chromatin. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3320–3322. doi: 10.1073/pnas.72.9.3320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gordon V. C., Knobler C. M., Olins D. E., Schumaker V. N. Conformational changes of the chromatin subunit. Proc Natl Acad Sci U S A. 1978 Feb;75(2):660–663. doi: 10.1073/pnas.75.2.660. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hagerman P. J. Flexibility of DNA. Annu Rev Biophys Biophys Chem. 1988;17:265–286. doi: 10.1146/annurev.bb.17.060188.001405. [DOI] [PubMed] [Google Scholar]
  13. Hagerman P. J. Investigation of the flexibility of DNA using transient electric birefringence. Biopolymers. 1981 Jul;20(7):1503–1535. doi: 10.1002/bip.1981.360200710. [DOI] [PubMed] [Google Scholar]
  14. Hirai M., Niimura N., Zama M., Mita K., Ichimura S., Tokunaga F., Ishikawa Y. Interparticle interactions and structural changes of nucleosome core particles in low-salt solution. Biochemistry. 1988 Oct 4;27(20):7924–7931. doi: 10.1021/bi00420a051. [DOI] [PubMed] [Google Scholar]
  15. Libertini L. J., Small E. W. Salt induced transitions of chromatin core particles studied by tyrosine fluorescence anisotropy. Nucleic Acids Res. 1980 Aug 25;8(16):3517–3534. doi: 10.1093/nar/8.16.3517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Manning G. S. Self-attraction and natural curvature in null DNA. J Biomol Struct Dyn. 1989 Aug;7(1):41–61. doi: 10.1080/07391102.1989.10507751. [DOI] [PubMed] [Google Scholar]
  17. Marion C., Bezot P., Hesse-Bezot C., Roux B., Bernengo J. C. Conformation of chromatin oligomers. A new argument for a change with the hexanucleosome. Eur J Biochem. 1981 Nov;120(1):169–176. doi: 10.1111/j.1432-1033.1981.tb05685.x. [DOI] [PubMed] [Google Scholar]
  18. Olins A. L., Carlson R. D., Wright E. B., Olins D. E. Chromatin nu bodies: isolation, subfractionation and physical characterization. Nucleic Acids Res. 1976 Dec;3(12):3271–3291. doi: 10.1093/nar/3.12.3271. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Osipova T. N., Pospelov V. A., Svetlikova S. B., Vorob'ev V. I. The role of histone H1 in compaction of nucleosomes. Sedimentation behaviour of oligonucleosomes in solution. Eur J Biochem. 1980 Dec;113(1):183–188. doi: 10.1111/j.1432-1033.1980.tb06153.x. [DOI] [PubMed] [Google Scholar]
  20. Renz M., Day L. A. Transition from noncooperative to cooperative and selective binding of histone H1 to DNA. Biochemistry. 1976 Jul 27;15(15):3220–3228. doi: 10.1021/bi00660a010. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Satchwell S. C., Travers A. A. Asymmetry and polarity of nucleosomes in chicken erythrocyte chromatin. EMBO J. 1989 Jan;8(1):229–238. doi: 10.1002/j.1460-2075.1989.tb03368.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Schmitz K. S., Ramsay-Shaw B. Chromatin conformation: a systematic analysis of helical parameters from hydrodynamic data. Biopolymers. 1977 Dec;16(12):2619–2633. doi: 10.1002/bip.1977.360161204. [DOI] [PubMed] [Google Scholar]
  24. Smerdon M. J., Isenberg I. Conformational changes in subfractions of calf thymus histone H1. Biochemistry. 1976 Sep 21;15(19):4233–4242. doi: 10.1021/bi00664a016. [DOI] [PubMed] [Google Scholar]
  25. Smith M. F., Athey B. D., Williams S. P., Langmore J. P. Radial density distribution of chromatin: evidence that chromatin fibers have solid centers. J Cell Biol. 1990 Feb;110(2):245–254. doi: 10.1083/jcb.110.2.245. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sogo J. M., Thoma F. Electron microscopy of chromatin. Methods Enzymol. 1989;170:142–165. doi: 10.1016/0076-6879(89)70045-8. [DOI] [PubMed] [Google Scholar]
  27. Thoma F., Koller T., Klug A. Involvement of histone H1 in the organization of the nucleosome and of the salt-dependent superstructures of chromatin. J Cell Biol. 1979 Nov;83(2 Pt 1):403–427. doi: 10.1083/jcb.83.2.403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Thomas J. O., Rees C. Exchange of histones H1 and H5 between chromatin fragments. A preference of H5 for higher-order structures. Eur J Biochem. 1983 Jul 15;134(1):109–115. doi: 10.1111/j.1432-1033.1983.tb07538.x. [DOI] [PubMed] [Google Scholar]
  29. Varshavsky A. J., Bakayev V. V., Georgiev G. P. Heterogeneity of chromatin subunits in vitro and location of histone H1. Nucleic Acids Res. 1976 Feb;3(2):477–492. doi: 10.1093/nar/3.2.477. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Widom J., Klug A. Structure of the 300A chromatin filament: X-ray diffraction from oriented samples. Cell. 1985 Nov;43(1):207–213. doi: 10.1016/0092-8674(85)90025-x. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Widom J. Toward a unified model of chromatin folding. Annu Rev Biophys Biophys Chem. 1989;18:365–395. doi: 10.1146/annurev.bb.18.060189.002053. [DOI] [PubMed] [Google Scholar]
  33. Williams S. P., Athey B. D., Muglia L. J., Schappe R. S., Gough A. H., Langmore J. P. Chromatin fibers are left-handed double helices with diameter and mass per unit length that depend on linker length. Biophys J. 1986 Jan;49(1):233–248. doi: 10.1016/S0006-3495(86)83637-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wittig B., Wittig S. Nucleosome mono, di, tri-, and tetramers from chicken embryo chromatin. Nucleic Acids Res. 1977 Nov;4(11):3901–3917. doi: 10.1093/nar/4.11.3901. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES