Skip to main content
NCBI home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1980 Nov 25;8(22):5255–5266. doi: 10.1093/nar/8.22.5255

An examination of models for chromatin transcription.

H J Gould, G J Cowling, N R Harborne, J Allan
PMCID: PMC324299  PMID: 7465413

Abstract

Structural studies have revealed that chromatin is composed of repeating units or nucleosomes having two distinct domains, the nucleosome core and the linker region. The nucleosome core comprises 146 base pairs of DNA wound in one and three quarter turns around an octamer of histones made up of two symmetrical tetramers (1). It may be inferred on topological grounds that this structure must be perturbed during chromatin transcription and replication since the histone core bridges the supercoil which blocks the passage of polymerase along the template and prevents the unwinding of DNA required for enzymatic copying. A number of mechanisms for freeing the DNA template may be envisaged, and one detailed model, based on symmetrical dissociation of the histone tetramers, has been proposed (2). Here we present evidence against such unpairing or indeed any detachment of histones from the octamer during chromatin transcription, and we give reasons for favouring a transcriptional mechanism based upon the separation of the octamer from at least one of the DNA.

Full text

PDF
5255

Images in this article

5258Image
on p.5258

Selected References

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

  1. Allan J., Staynov D. Z., Gould H. Reversible dissociation of linker histone from chromatin with preservation of internucleosomal repeat. Proc Natl Acad Sci U S A. 1980 Feb;77(2):885–889. doi: 10.1073/pnas.77.2.885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Axel R., Cedar H., Felsenfield G. The structure of the globin genes in chromatin. Biochemistry. 1975 Jun 3;14(11):2489–2495. doi: 10.1021/bi00682a031. [DOI] [PubMed] [Google Scholar]
  3. Brutlag D., Schlehuber C., Bonner J. Properties of formaldehyde-treated nucleohistone. Biochemistry. 1969 Aug;8(8):3214–3218. doi: 10.1021/bi00836a013. [DOI] [PubMed] [Google Scholar]
  4. Camerini-Otero R. D., Felsenfeld G. Histone H3 disulfide dimers and nucleosome structure. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5519–5523. doi: 10.1073/pnas.74.12.5519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cedar H. Transcription of DNA and chromatin with calf thymus RNA polymerase B in vitro. J Mol Biol. 1975 Jun 25;95(2):257–269. doi: 10.1016/0022-2836(75)90394-0. [DOI] [PubMed] [Google Scholar]
  6. Crémisi C., Chestier A., Dauguet C., Yaniv M. Transcription of SV 40 nucleoprotein complexes in vitro. Biochem Biophys Res Commun. 1977 Sep 9;78(1):74–82. doi: 10.1016/0006-291x(77)91223-2. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Gariglio P., Llopis R., Oudet P., Chambon P. The template of the isolated native simian virus 40 transcriptional complexes is a minichromosome. J Mol Biol. 1979 Jun 15;131(1):75–105. doi: 10.1016/0022-2836(79)90302-4. [DOI] [PubMed] [Google Scholar]
  9. Germond J. E., Bellard M., Oudet P., Chambon P. Stability of nucleosomes in native and reconstituted chromatins. Nucleic Acids Res. 1976 Nov;3(11):3173–3192. doi: 10.1093/nar/3.11.3173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Germond J. E., Bellard M., Oudet P., Chambon P. Stability of nucleosomes in native and reconstituted chromatins. Nucleic Acids Res. 1976 Nov;3(11):3173–3192. doi: 10.1093/nar/3.11.3173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gottesfeld J. M., Melton D. A. The length of nucleosome-associated DNA is the same in both transcribed and nontranscribed regions of chromatin. Nature. 1978 May 25;273(5660):317–319. doi: 10.1038/273317a0. [DOI] [PubMed] [Google Scholar]
  12. Kobashi K. Catalytic oxidation of sulfhydryl groups by o-phenanthroline copper complex. Biochim Biophys Acta. 1968 May;158(2):239–245. doi: 10.1016/0304-4165(68)90136-0. [DOI] [PubMed] [Google Scholar]
  13. Lacy E., Axel R. Analysis of DNA of isolated chromatin subunits. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3978–3982. doi: 10.1073/pnas.72.10.3978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Lomant A. J., Fairbanks G. Chemical probes of extended biological structures: synthesis and properties of the cleavable protein cross-linking reagent [35S]dithiobis(succinimidyl propionate). J Mol Biol. 1976 Jun 14;104(1):243–261. doi: 10.1016/0022-2836(76)90011-5. [DOI] [PubMed] [Google Scholar]
  16. Martinson H. G., True R., Lau C. K., Mehrabian M. Histon-histone interactions within chromatin. Preliminary location of multiple contact sites between histones 2A, 2B, and 4. Biochemistry. 1979 Mar 20;18(6):1075–1082. doi: 10.1021/bi00573a022. [DOI] [PubMed] [Google Scholar]
  17. Mathis D. J., Oudet P., Wasylyk B., Chambon P. Effect of histone acetylation on structure and in vitro transcription of chromatin. Nucleic Acids Res. 1978 Oct;5(10):3523–3547. doi: 10.1093/nar/5.10.3523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. McGhee J. D., Felsenfeld G. Nucleosome structure. Annu Rev Biochem. 1980;49:1115–1156. doi: 10.1146/annurev.bi.49.070180.005343. [DOI] [PubMed] [Google Scholar]
  19. Meneguzzi G., Chenciner N., Milanesi G. Transcription of nucleosomal DNA in SV40 minichromosomes by eukaryotic and prokaryotic RNA polymerases. Nucleic Acids Res. 1979 Jun 25;6(8):2947–2960. doi: 10.1093/nar/6.8.2947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Meneguzzi G., Pignatti P. F., Milanesi G. Transcription of polyoma virus DNA after interaction with nuclear proteins in vitro. Biochem Biophys Res Commun. 1976 Sep 20;72(2):626–633. doi: 10.1016/s0006-291x(76)80086-1. [DOI] [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. Palter K. B., Alberts B. M. The use of DNA-cellulose for analyzing histone-DNA interactions. Discovery of nucleosome-like histone binding to single-stranded DNA. J Biol Chem. 1979 Nov 10;254(21):11160–11169. [PubMed] [Google Scholar]
  23. Spadafora C., Oudet P., Chambon P. Rearrangement of chromatin structure induced by increasing ionic strength and temperature. Eur J Biochem. 1979 Oct;100(1):225–235. doi: 10.1111/j.1432-1033.1979.tb02053.x. [DOI] [PubMed] [Google Scholar]
  24. Staynov D. Z., Pinder J. C., Gratzer W. B. Molecular weight determination of nucleic acids by gel electrophoresis in non-aqueous solution. Nat New Biol. 1972 Jan 26;235(56):108–110. doi: 10.1038/newbio235108a0. [DOI] [PubMed] [Google Scholar]
  25. Stein A. DNA folding by histones: the kinetics of chromatin core particle reassembly and the interaction of nucleosomes with histones. J Mol Biol. 1979 May 15;130(2):103–134. doi: 10.1016/0022-2836(79)90421-2. [DOI] [PubMed] [Google Scholar]
  26. Thomas J. O., Kornberg R. D. An octamer of histones in chromatin and free in solution. Proc Natl Acad Sci U S A. 1975 Jul;72(7):2626–2630. doi: 10.1073/pnas.72.7.2626. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Tien Kuo M., Sahasrabuddhe C. G., Saunders G. F. Presence of messenger specifying sequences in the DNA of chromatin subunits. Proc Natl Acad Sci U S A. 1976 May;73(5):1572–1575. doi: 10.1073/pnas.73.5.1572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. 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]
  29. Voordouw G., Eisenberg H. Binding of additional histones to chromatin core particles. Nature. 1978 Jun 8;273(5662):446–448. doi: 10.1038/273446a0. [DOI] [PubMed] [Google Scholar]
  30. Wasylyk B., Chambon P. Studies on the mechanism of transcription of nucleosomal complexes. Eur J Biochem. 1980 Jan;103(2):219–226. doi: 10.1111/j.1432-1033.1980.tb04306.x. [DOI] [PubMed] [Google Scholar]
  31. Wasylyk B., Chambon P. Transcription by eukaryotic RNA polymerases A and B of chromatin assembled in vitro. Eur J Biochem. 1979 Aug 1;98(2):317–327. doi: 10.1111/j.1432-1033.1979.tb13191.x. [DOI] [PubMed] [Google Scholar]
  32. Wasylyk B., Thevenin G., Oudet P., Chambon P. Transcription of in vitro assembled chromatin by Escherichia coli RNA polymerase. J Mol Biol. 1979 Mar 5;128(3):411–440. doi: 10.1016/0022-2836(79)90095-0. [DOI] [PubMed] [Google Scholar]
  33. Weber K., Osborn M. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J Biol Chem. 1969 Aug 25;244(16):4406–4412. [PubMed] [Google Scholar]
  34. 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]
  35. Williamson P., Felsenfeld G. Transcription of histone-covered T7 DNA by Escherichia coli RNA polymerase. Biochemistry. 1978 Dec 26;17(26):5695–5705. doi: 10.1021/bi00619a015. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES