Skip to main content
PMC home page
The EMBO Journal logoLink to The EMBO Journal
. 1995 May 15;14(10):2209–2216. doi: 10.1002/j.1460-2075.1995.tb07215.x

Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system.

P D Varga-Weisz 1, T A Blank 1, P B Becker 1
PMCID: PMC398327  PMID: 7774579

Abstract

Chromatin structure must be flexible to allow the binding of regulatory proteins and to accommodate different levels of gene activity. Chromatin assembled in a cell-free system derived from Drosophila embryos contains an activity that hydrolyses ATP to render entire nucleosome arrays mobile. Nucleosome movements, most likely their sliding, occurred even in the presence of the linker histone H1. The dynamic state of chromatin in the presence of the activity and ATP globally increased the accessibility of nucleosomal DNA to incoming proteins. This unprecedented demonstration of energy-dependent nucleosome mobility identifies a new principle which is likely to be fundamental to the mechanism of chromatin remodelling and the binding of regulatory proteins.

Full text

PDF
2215

Images in this article

2210Image
on p.2210
2211Image
on p.2211
2211Image
on p.2211
2212Image
on p.2212

Selected References

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

  1. Adams C. C., Workman J. L. Nucleosome displacement in transcription. Cell. 1993 Feb 12;72(3):305–308. doi: 10.1016/0092-8674(93)90109-4. [DOI] [PubMed] [Google Scholar]
  2. Allan J., Cowling G. J., Harborne N., Cattini P., Craigie R., Gould H. Regulation of the higher-order structure of chromatin by histones H1 and H5. J Cell Biol. 1981 Aug;90(2):279–288. doi: 10.1083/jcb.90.2.279. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Almer A., Rudolph H., Hinnen A., Hörz W. Removal of positioned nucleosomes from the yeast PHO5 promoter upon PHO5 induction releases additional upstream activating DNA elements. EMBO J. 1986 Oct;5(10):2689–2696. doi: 10.1002/j.1460-2075.1986.tb04552.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Archer T. K., Lefebvre P., Wolford R. G., Hager G. L. Transcription factor loading on the MMTV promoter: a bimodal mechanism for promoter activation. Science. 1992 Mar 20;255(5051):1573–1576. doi: 10.1126/science.1347958. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Beard P. Mobility of histones on the chromosome of simian virus 40. Cell. 1978 Nov;15(3):955–967. doi: 10.1016/0092-8674(78)90279-9. [DOI] [PubMed] [Google Scholar]
  7. Becker P. B. The establishment of active promoters in chromatin. Bioessays. 1994 Aug;16(8):541–547. doi: 10.1002/bies.950160807. [DOI] [PubMed] [Google Scholar]
  8. Becker P. B., Tsukiyama T., Wu C. Chromatin assembly extracts from Drosophila embryos. Methods Cell Biol. 1994;44:207–223. doi: 10.1016/s0091-679x(08)60915-2. [DOI] [PubMed] [Google Scholar]
  9. Becker P. B., Wu C. Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. Mol Cell Biol. 1992 May;12(5):2241–2249. doi: 10.1128/mcb.12.5.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Clos J., Westwood J. T., Becker P. B., Wilson S., Lambert K., Wu C. Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell. 1990 Nov 30;63(5):1085–1097. doi: 10.1016/0092-8674(90)90511-c. [DOI] [PubMed] [Google Scholar]
  11. Craig E. A., McCarthy B. J. Four Drosophila heat shock genes at 67B: characterization of recombinant plasmids. Nucleic Acids Res. 1980 Oct 10;8(19):4441–4457. doi: 10.1093/nar/8.19.4441. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Farkas G., Gausz J., Galloni M., Reuter G., Gyurkovics H., Karch F. The Trithorax-like gene encodes the Drosophila GAGA factor. Nature. 1994 Oct 27;371(6500):806–808. doi: 10.1038/371806a0. [DOI] [PubMed] [Google Scholar]
  13. Hansen J. C., Ausio J. Chromatin dynamics and the modulation of genetic activity. Trends Biochem Sci. 1992 May;17(5):187–191. doi: 10.1016/0968-0004(92)90264-a. [DOI] [PubMed] [Google Scholar]
  14. Imbalzano A. N., Kwon H., Green M. R., Kingston R. E. Facilitated binding of TATA-binding protein to nucleosomal DNA. Nature. 1994 Aug 11;370(6489):481–485. doi: 10.1038/370481a0. [DOI] [PubMed] [Google Scholar]
  15. Kwon H., Imbalzano A. N., Khavari P. A., Kingston R. E., Green M. R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature. 1994 Aug 11;370(6489):477–481. doi: 10.1038/370477a0. [DOI] [PubMed] [Google Scholar]
  16. Laurent B. C., Treich I., Carlson M. The yeast SNF2/SWI2 protein has DNA-stimulated ATPase activity required for transcriptional activation. Genes Dev. 1993 Apr;7(4):583–591. doi: 10.1101/gad.7.4.583. [DOI] [PubMed] [Google Scholar]
  17. Lu Q., Wallrath L. L., Granok H., Elgin S. C. (CT)n (GA)n repeats and heat shock elements have distinct roles in chromatin structure and transcriptional activation of the Drosophila hsp26 gene. Mol Cell Biol. 1993 May;13(5):2802–2814. doi: 10.1128/mcb.13.5.2802. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Meersseman G., Pennings S., Bradbury E. M. Mobile nucleosomes--a general behavior. EMBO J. 1992 Aug;11(8):2951–2959. doi: 10.1002/j.1460-2075.1992.tb05365.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Minocha A., Long B. H. Inhibition of the DNA catenation activity of type II topoisomerase by VP16-213 and VM26. Biochem Biophys Res Commun. 1984 Jul 18;122(1):165–170. doi: 10.1016/0006-291x(84)90454-6. [DOI] [PubMed] [Google Scholar]
  20. Nelson E. M., Tewey K. M., Liu L. F. Mechanism of antitumor drug action: poisoning of mammalian DNA topoisomerase II on DNA by 4'-(9-acridinylamino)-methanesulfon-m-anisidide. Proc Natl Acad Sci U S A. 1984 Mar;81(5):1361–1365. doi: 10.1073/pnas.81.5.1361. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Nelson P. P., Albright S. C., Wiseman J. M., Garrard W. T. Reassociation of histone H1 with nucleosomes. J Biol Chem. 1979 Nov 25;254(22):11751–11760. [PubMed] [Google Scholar]
  22. Pennings S., Meersseman G., Bradbury E. M. Linker histones H1 and H5 prevent the mobility of positioned nucleosomes. Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10275–10279. doi: 10.1073/pnas.91.22.10275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pennings S., Meersseman G., Bradbury E. M. Mobility of positioned nucleosomes on 5 S rDNA. J Mol Biol. 1991 Jul 5;220(1):101–110. doi: 10.1016/0022-2836(91)90384-i. [DOI] [PubMed] [Google Scholar]
  24. Peterson C. L., Herskowitz I. Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription. Cell. 1992 Feb 7;68(3):573–583. doi: 10.1016/0092-8674(92)90192-f. [DOI] [PubMed] [Google Scholar]
  25. Reik A., Schütz G., Stewart A. F. Glucocorticoids are required for establishment and maintenance of an alteration in chromatin structure: induction leads to a reversible disruption of nucleosomes over an enhancer. EMBO J. 1991 Sep;10(9):2569–2576. doi: 10.1002/j.1460-2075.1991.tb07797.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sandaltzopoulos R., Blank T., Becker P. B. Transcriptional repression by nucleosomes but not H1 in reconstituted preblastoderm Drosophila chromatin. EMBO J. 1994 Jan 15;13(2):373–379. doi: 10.1002/j.1460-2075.1994.tb06271.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Segers A., Muyldermans S., Wyns L. The interaction of histone H5 and its globular domain with core particles, depleted chromatosomes, polynucleosomes, and a DNA decamer. J Biol Chem. 1991 Jan 25;266(3):1502–1508. [PubMed] [Google Scholar]
  28. Svaren J., Hörz W. Histones, nucleosomes and transcription. Curr Opin Genet Dev. 1993 Apr;3(2):219–225. doi: 10.1016/0959-437x(93)90026-l. [DOI] [PubMed] [Google Scholar]
  29. Tamkun J. W., Deuring R., Scott M. P., Kissinger M., Pattatucci A. M., Kaufman T. C., Kennison J. A. brahma: a regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2/SWI2. Cell. 1992 Feb 7;68(3):561–572. doi: 10.1016/0092-8674(92)90191-e. [DOI] [PubMed] [Google Scholar]
  30. Taylor I. C., Workman J. L., Schuetz T. J., Kingston R. E. Facilitated binding of GAL4 and heat shock factor to nucleosomal templates: differential function of DNA-binding domains. Genes Dev. 1991 Jul;5(7):1285–1298. doi: 10.1101/gad.5.7.1285. [DOI] [PubMed] [Google Scholar]
  31. Travers A. A. The reprogramming of transcriptional competence. Cell. 1992 May 15;69(4):573–575. doi: 10.1016/0092-8674(92)90218-2. [DOI] [PubMed] [Google Scholar]
  32. Tsukiyama T., Becker P. B., Wu C. ATP-dependent nucleosome disruption at a heat-shock promoter mediated by binding of GAGA transcription factor. Nature. 1994 Feb 10;367(6463):525–532. doi: 10.1038/367525a0. [DOI] [PubMed] [Google Scholar]
  33. Wall G., Varga-Weisz P. D., Sandaltzopoulos R., Becker P. B. Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. EMBO J. 1995 Apr 18;14(8):1727–1736. doi: 10.1002/j.1460-2075.1995.tb07162.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Wallrath L. L., Lu Q., Granok H., Elgin S. C. Architectural variations of inducible eukaryotic promoters: preset and remodeling chromatin structures. Bioessays. 1994 Mar;16(3):165–170. doi: 10.1002/bies.950160306. [DOI] [PubMed] [Google Scholar]
  35. Wolffe A. P. Transcription: in tune with the histones. Cell. 1994 Apr 8;77(1):13–16. doi: 10.1016/0092-8674(94)90229-1. [DOI] [PubMed] [Google Scholar]

Articles from The EMBO Journal are provided here courtesy of Nature Publishing Group

RESOURCES