A relationship between the helical twist of DNA and the ordered positioning of nucleosomes in all eukaryotic cells (original) (raw)

Abstract

A large number of measurements of nucleosome repeat lengths are analyzed and are found to exhibit preferential quantization to a set of values related by integral multiples of the helical twist of DNA. This implies that the nucleosomal DNA content is preferentially quantized, which in turn implies that linker DNA lengths are preferentially quantized. This study confirms and extends previous observations in the literature that had suggested, but not firmly established, that linker lengths might be quantized. The quantization of repeat lengths applies even for very long repeat lengths. This suggests a model for the origin of the quantization, in which the quantization arises from the requirements of higher-order chromatin structure.

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Selected References

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  1. Bavykin S. G., Usachenko S. I., Zalensky A. O., Mirzabekov A. D. Structure of nucleosomes and organization of internucleosomal DNA in chromatin. J Mol Biol. 1990 Apr 5;212(3):495–511. doi: 10.1016/0022-2836(90)90328-J. [DOI] [PubMed] [Google Scholar]
  2. Drew H. R., Calladine C. R. Sequence-specific positioning of core histones on an 860 base-pair DNA. Experiment and theory. J Mol Biol. 1987 May 5;195(1):143–173. doi: 10.1016/0022-2836(87)90333-0. [DOI] [PubMed] [Google Scholar]
  3. Felsenfeld G., McGhee J. D. Structure of the 30 nm chromatin fiber. Cell. 1986 Feb 14;44(3):375–377. doi: 10.1016/0092-8674(86)90456-3. [DOI] [PubMed] [Google Scholar]
  4. 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]
  5. Hayes J. J., Tullius T. D., Wolffe A. P. The structure of DNA in a nucleosome. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7405–7409. doi: 10.1073/pnas.87.19.7405. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Karpov V. L., Bavykin S. G., Preobrazhenskaya O. V., Belyavsky A. V., Mirzabekov A. D. Alignment of nucleosomes along DNA and organization of spacer DNA in Drosophila chromatin. Nucleic Acids Res. 1982 Jul 24;10(14):4321–4337. doi: 10.1093/nar/10.14.4321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Kornberg R. D., Stryer L. Statistical distributions of nucleosomes: nonrandom locations by a stochastic mechanism. Nucleic Acids Res. 1988 Jul 25;16(14A):6677–6690. doi: 10.1093/nar/16.14.6677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Lohr D. The salt dependence of chicken and yeast chromatin structure. Effects on internucleosomal organization and relation to active chromatin. J Biol Chem. 1986 Jul 25;261(21):9904–9914. [PubMed] [Google Scholar]
  9. Lohr D., Van Holde K. E. Organization of spacer DNA in chromatin. Proc Natl Acad Sci U S A. 1979 Dec;76(12):6326–6330. doi: 10.1073/pnas.76.12.6326. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Prunell A., Kornberg R. D. Variable center to center distance of nucleosomes in chromatin. J Mol Biol. 1982 Jan 25;154(3):515–523. doi: 10.1016/s0022-2836(82)80010-7. [DOI] [PubMed] [Google Scholar]
  11. Ramsay N., Felsenfeld G., Rushton B. M., McGhee J. D. A 145-base pair DNA sequence that positions itself precisely and asymmetrically on the nucleosome core. EMBO J. 1984 Nov;3(11):2605–2611. doi: 10.1002/j.1460-2075.1984.tb02181.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Rhodes D., Klug A. Helical periodicity of DNA determined by enzyme digestion. Nature. 1980 Aug 7;286(5773):573–578. doi: 10.1038/286573a0. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Shore D., Baldwin R. L. Energetics of DNA twisting. I. Relation between twist and cyclization probability. J Mol Biol. 1983 Nov 15;170(4):957–981. doi: 10.1016/s0022-2836(83)80198-3. [DOI] [PubMed] [Google Scholar]
  15. Simpson R. T., Stafford D. W. Structural features of a phased nucleosome core particle. Proc Natl Acad Sci U S A. 1983 Jan;80(1):51–55. doi: 10.1073/pnas.80.1.51. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Strauss F., Prunell A. Nucleosome spacing in rat liver chromatin. A study with exonuclease III. Nucleic Acids Res. 1982 Apr 10;10(7):2275–2293. doi: 10.1093/nar/10.7.2275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Strauss F., Prunell A. Organization of internucleosomal DNA in rat liver chromatin. EMBO J. 1983;2(1):51–56. doi: 10.1002/j.1460-2075.1983.tb01379.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]