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. 1981 Mar;78(3):1461–1465. doi: 10.1073/pnas.78.3.1461

Structure of chromatin and the linking number of DNA.

A Worcel, S Strogatz, D Riley
PMCID: PMC319150  PMID: 6940168

Abstract

Recent observations suggest that the basic supranucleosomal structure of chromatin is a zigzag helical ribbon with a repeat unit made of two nucleosomes connected by a relaxed spacer DNA. A remarkable feature of one particular ribbon is that it solves the apparent paradox between the number of DNA turns per nucleosome and the total linking number of a nucleosome-containing closed circular DNA molecule. We show here that the repeat unit of the proposed structure, which contains two nucleosomes with -1 3/4 DNA turns per nucleosome and one spacer crossover per repeat, contributes -2 to the linking number of closed circular DNA. Space-filling models show that the cylindrical 250-A chromatin fiber can be generated by twisting the ribbon.

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Selected References

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  1. Benyajati C., Worcel A. Isolation, characterization, and structure of the folded interphase genome of Drosophila melanogaster. Cell. 1976 Nov;9(3):393–407. doi: 10.1016/0092-8674(76)90084-2. [DOI] [PubMed] [Google Scholar]
  2. Bonner W. M., Pollard H. B. The presence of F3-F2a1 dimers and F1 oligomers in chromatin. Biochem Biophys Res Commun. 1975 May 5;64(1):282–288. doi: 10.1016/0006-291x(75)90250-8. [DOI] [PubMed] [Google Scholar]
  3. Boulikas T., Wiseman J. M., Garrard W. T. Points of contact between histone H1 and the histone octamer. Proc Natl Acad Sci U S A. 1980 Jan;77(1):127–131. doi: 10.1073/pnas.77.1.127. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Compton J. L., Bellard M., Chambon P. Biochemical evidence of variability in the DNA repeat length in the chromatin of higher eukaryotes. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4382–4386. doi: 10.1073/pnas.73.12.4382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cook P. R., Brazell I. A. Supercoils in human DNA. J Cell Sci. 1975 Nov;19(2):261–279. doi: 10.1242/jcs.19.2.261. [DOI] [PubMed] [Google Scholar]
  6. Crick F. H. Linking numbers and nucleosomes. Proc Natl Acad Sci U S A. 1976 Aug;73(8):2639–2643. doi: 10.1073/pnas.73.8.2639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dubochet J., Noll M. Nucleosome arcs and helices. Science. 1978 Oct 20;202(4365):280–286. doi: 10.1126/science.694532. [DOI] [PubMed] [Google Scholar]
  8. Felsenfeld G. Chromatin. Nature. 1978 Jan 12;271(5641):115–122. doi: 10.1038/271115a0. [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., Lutter L. C., Rhodes D., Brown R. S., Rushton B., Levitt M., Klug A. Structure of nucleosome core particles of chromatin. Nature. 1977 Sep 1;269(5623):29–36. doi: 10.1038/269029a0. [DOI] [PubMed] [Google Scholar]
  11. Fuller F. B. Decomposition of the linking number of a closed ribbon: A problem from molecular biology. Proc Natl Acad Sci U S A. 1978 Aug;75(8):3557–3561. doi: 10.1073/pnas.75.8.3557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Fuller F. B. The writhing number of a space curve. Proc Natl Acad Sci U S A. 1971 Apr;68(4):815–819. doi: 10.1073/pnas.68.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Germond J. E., Hirt B., Oudet P., Gross-Bellark M., Chambon P. Folding of the DNA double helix in chromatin-like structures from simian virus 40. Proc Natl Acad Sci U S A. 1975 May;72(5):1843–1847. doi: 10.1073/pnas.72.5.1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hinton D. M., Bode V. C. Ethidium binding affinity of circular lambda deoxyribonucleic acid determined fluorometrically. J Biol Chem. 1975 Feb 10;250(3):1061–1070. [PubMed] [Google Scholar]
  15. Keller W. Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. Proc Natl Acad Sci U S A. 1975 Dec;72(12):4876–4880. doi: 10.1073/pnas.72.12.4876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Liu L. F., Liu C. C., Alberts B. M. Type II DNA topoisomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break. Cell. 1980 Mar;19(3):697–707. doi: 10.1016/s0092-8674(80)80046-8. [DOI] [PubMed] [Google Scholar]
  17. 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]
  18. Lutter L. C. Precise location of DNase I cutting sites in the nucleosome core determined by high resolution gel electrophoresis. Nucleic Acids Res. 1979 Jan;6(1):41–56. doi: 10.1093/nar/6.1.41. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Miller O. L., Jr, Bakken A. H. Morphological studies of transcription. Acta Endocrinol Suppl (Copenh) 1972;168:155–177. doi: 10.1530/acta.0.071s155. [DOI] [PubMed] [Google Scholar]
  20. Mizuuchi K., Fisher L. M., O'Dea M. H., Gellert M. DNA gyrase action involves the introduction of transient double-strand breaks into DNA. Proc Natl Acad Sci U S A. 1980 Apr;77(4):1847–1851. doi: 10.1073/pnas.77.4.1847. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Noll M. Internal structure of the chromatin subunit. Nucleic Acids Res. 1974 Nov;1(11):1573–1578. doi: 10.1093/nar/1.11.1573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Olins A. L., Olins D. E. Spheroid chromatin units (v bodies). Science. 1974 Jan 25;183(4122):330–332. doi: 10.1126/science.183.4122.330. [DOI] [PubMed] [Google Scholar]
  23. Olins D. E., Wright E. B. Glutaraldehyde fixation of isolated eucaryotic nuclei. Evidence for histone-histone proximity. J Cell Biol. 1973 Nov;59(2 Pt 1):304–317. doi: 10.1083/jcb.59.2.304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Oudet P., Gross-Bellard M., Chambon P. Electron microscopic and biochemical evidence that chromatin structure is a repeating unit. Cell. 1975 Apr;4(4):281–300. doi: 10.1016/0092-8674(75)90149-x. [DOI] [PubMed] [Google Scholar]
  25. Prunell A., Kornberg R. D., Lutter L., Klug A., Levitt M., Crick F. H. Periodicity of deoxyribonuclease I digestion of chromatin. Science. 1979 May 25;204(4395):855–858. doi: 10.1126/science.441739. [DOI] [PubMed] [Google Scholar]
  26. Rattner J. B., Hamkalo B. A. Higher order structure in metaphase chromosomes. I. The 250 A fiber. Chromosoma. 1978 Dec 6;69(3):363–372. doi: 10.1007/BF00332139. [DOI] [PubMed] [Google Scholar]
  27. Renz M., Nehls P., Hozier J. Involvement of histone H1 in the organization of the chromosome fiber. Proc Natl Acad Sci U S A. 1977 May;74(5):1879–1883. doi: 10.1073/pnas.74.5.1879. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Riley D., Weintraub H. Conservative segregation of parental histones during replication in the presence of cycloheximide. Proc Natl Acad Sci U S A. 1979 Jan;76(1):328–332. doi: 10.1073/pnas.76.1.328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shure M., Vinograd J. The number of superhelical turns in native virion SV40 DNA and minicol DNA determined by the band counting method. Cell. 1976 Jun;8(2):215–226. doi: 10.1016/0092-8674(76)90005-2. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. Varshavsky A. J., Sundin O., Bohn M. A stretch of "late" SV40 viral DNA about 400 bp long which includes the origin of replication is specifically exposed in SV40 minichromosomes. Cell. 1979 Feb;16(2):453–466. doi: 10.1016/0092-8674(79)90021-7. [DOI] [PubMed] [Google Scholar]
  33. Vinograd J., Lebowitz J., Watson R. Early and late helix-coil transitions in closed circular DNA. The number of superhelical turns in polyoma DNA. J Mol Biol. 1968 Apr 14;33(1):173–197. doi: 10.1016/0022-2836(68)90287-8. [DOI] [PubMed] [Google Scholar]
  34. Wang J. C. Helical repeat of DNA in solution. Proc Natl Acad Sci U S A. 1979 Jan;76(1):200–203. doi: 10.1073/pnas.76.1.200. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weintraub H., Worcel A., Alberts B. A model for chromatin based upon two symmetrically paired half-nucleosomes. Cell. 1976 Nov;9(3):409–417. doi: 10.1016/0092-8674(76)90085-4. [DOI] [PubMed] [Google Scholar]
  36. Whitlock J. P., Jr, Simpson R. T. Removal of histone H1 exposes a fifty base pair DNA segment between nucleosomes. Biochemistry. 1976 Jul 27;15(15):3307–3314. doi: 10.1021/bi00660a022. [DOI] [PubMed] [Google Scholar]
  37. Worcel A., Benyajati C. Higher order coiling of DNA in chromatin. Cell. 1977 Sep;12(1):83–100. doi: 10.1016/0092-8674(77)90187-8. [DOI] [PubMed] [Google Scholar]
  38. Worcel A., Burgi E. On the structure of the folded chromosome of Escherichia coli. J Mol Biol. 1972 Nov 14;71(2):127–147. doi: 10.1016/0022-2836(72)90342-7. [DOI] [PubMed] [Google Scholar]
  39. Worcel A., Han S., Wong M. L. Assembly of newly replicated chromatin. Cell. 1978 Nov;15(3):969–977. doi: 10.1016/0092-8674(78)90280-5. [DOI] [PubMed] [Google Scholar]
  40. Wu C., Bingham P. M., Livak K. J., Holmgren R., Elgin S. C. The chromatin structure of specific genes: I. Evidence for higher order domains of defined DNA sequence. Cell. 1979 Apr;16(4):797–806. doi: 10.1016/0092-8674(79)90095-3. [DOI] [PubMed] [Google Scholar]
  41. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature. 1980 Aug 28;286(5776):854–860. doi: 10.1038/286854a0. [DOI] [PubMed] [Google Scholar]

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