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. 1995 Aug 1;14(15):3752–3765. doi: 10.1002/j.1460-2075.1995.tb00045.x

A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones.

K Ura 1, J J Hayes 1, A P Wolffe 1
PMCID: PMC394450  PMID: 7641694

Abstract

Nucleosome mobility facilitates the transcription of chromatin templates containing only histone octamers. Inclusion of linker histones in chromatin inhibits nucleosome mobility, directs nucleosome positioning and represses transcription. Transcriptional repression by linker histone occurs preferentially on templates associated with histone octamers relative to naked DNA. Mobile nucleosomes and the restriction of mobility by linker histones might be expected to exert a major influence on the accessibility of chromatin to regulatory molecules.

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Selected References

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

  1. Allan J., Hartman P. G., Crane-Robinson C., Aviles F. X. The structure of histone H1 and its location in chromatin. Nature. 1980 Dec 25;288(5792):675–679. doi: 10.1038/288675a0. [DOI] [PubMed] [Google Scholar]
  2. Almouzni G., Méchali M. Assembly of spaced chromatin involvement of ATP and DNA topoisomerase activity. EMBO J. 1988 Dec 20;7(13):4355–4365. doi: 10.1002/j.1460-2075.1988.tb03334.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Almouzni G., Méchali M., Wolffe A. P. Competition between transcription complex assembly and chromatin assembly on replicating DNA. EMBO J. 1990 Feb;9(2):573–582. doi: 10.1002/j.1460-2075.1990.tb08145.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Almouzni G., Méchali M., Wolffe A. P. Transcription complex disruption caused by a transition in chromatin structure. Mol Cell Biol. 1991 Feb;11(2):655–665. doi: 10.1128/mcb.11.2.655. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Birkenmeier E. H., Brown D. D., Jordan E. A nuclear extract of Xenopus laevis oocytes that accurately transcribes 5S RNA genes. Cell. 1978 Nov;15(3):1077–1086. doi: 10.1016/0092-8674(78)90291-x. [DOI] [PubMed] [Google Scholar]
  6. Bogenhagen D. F., Wormington W. M., Brown D. D. Stable transcription complexes of Xenopus 5S RNA genes: a means to maintain the differentiated state. Cell. 1982 Feb;28(2):413–421. doi: 10.1016/0092-8674(82)90359-2. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Bouvet P., Dimitrov S., Wolffe A. P. Specific regulation of Xenopus chromosomal 5S rRNA gene transcription in vivo by histone H1. Genes Dev. 1994 May 15;8(10):1147–1159. doi: 10.1101/gad.8.10.1147. [DOI] [PubMed] [Google Scholar]
  9. Bresnick E. H., Bustin M., Marsaud V., Richard-Foy H., Hager G. L. The transcriptionally-active MMTV promoter is depleted of histone H1. Nucleic Acids Res. 1992 Jan 25;20(2):273–278. doi: 10.1093/nar/20.2.273. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Brown D. D. The role of stable complexes that repress and activate eucaryotic genes. Cell. 1984 Jun;37(2):359–365. doi: 10.1016/0092-8674(84)90366-0. [DOI] [PubMed] [Google Scholar]
  11. Chipev C. C., Wolffe A. P. Chromosomal organization of Xenopus laevis oocyte and somatic 5S rRNA genes in vivo. Mol Cell Biol. 1992 Jan;12(1):45–55. doi: 10.1128/mcb.12.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Clark D. J., Wolffe A. P. Superhelical stress and nucleosome-mediated repression of 5S RNA gene transcription in vitro. EMBO J. 1991 Nov;10(11):3419–3428. doi: 10.1002/j.1460-2075.1991.tb04906.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clark K. L., Halay E. D., Lai E., Burley S. K. Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature. 1993 Jul 29;364(6436):412–420. doi: 10.1038/364412a0. [DOI] [PubMed] [Google Scholar]
  14. Croston G. E., Kerrigan L. A., Lira L. M., Marshak D. R., Kadonaga J. T. Sequence-specific antirepression of histone H1-mediated inhibition of basal RNA polymerase II transcription. Science. 1991 Feb 8;251(4994):643–649. doi: 10.1126/science.1899487. [DOI] [PubMed] [Google Scholar]
  15. Dimitrov S., Almouzni G., Dasso M., Wolffe A. P. Chromatin transitions during early Xenopus embryogenesis: changes in histone H4 acetylation and in linker histone type. Dev Biol. 1993 Nov;160(1):214–227. doi: 10.1006/dbio.1993.1299. [DOI] [PubMed] [Google Scholar]
  16. Dimitrov S., Dasso M. C., Wolffe A. P. Remodeling sperm chromatin in Xenopus laevis egg extracts: the role of core histone phosphorylation and linker histone B4 in chromatin assembly. J Cell Biol. 1994 Aug;126(3):591–601. doi: 10.1083/jcb.126.3.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dimitrov S., Wolffe A. P. Chromatin and nuclear assembly: experimental approaches towards the reconstitution of transcriptionally active and silent states. Biochim Biophys Acta. 1995 Jan 2;1260(1):1–13. doi: 10.1016/0167-4781(94)00182-3. [DOI] [PubMed] [Google Scholar]
  18. Dong F., Hansen J. C., van Holde K. E. DNA and protein determinants of nucleosome positioning on sea urchin 5S rRNA gene sequences in vitro. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5724–5728. doi: 10.1073/pnas.87.15.5724. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Dong F., van Holde K. E. Nucleosome positioning is determined by the (H3-H4)2 tetramer. Proc Natl Acad Sci U S A. 1991 Dec 1;88(23):10596–10600. doi: 10.1073/pnas.88.23.10596. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Drew H. R., Travers A. A. DNA bending and its relation to nucleosome positioning. J Mol Biol. 1985 Dec 20;186(4):773–790. doi: 10.1016/0022-2836(85)90396-1. [DOI] [PubMed] [Google Scholar]
  21. Engelke D. R., Ng S. Y., Shastry B. S., Roeder R. G. Specific interaction of a purified transcription factor with an internal control region of 5S RNA genes. Cell. 1980 Mar;19(3):717–728. doi: 10.1016/s0092-8674(80)80048-1. [DOI] [PubMed] [Google Scholar]
  22. Fedor M. J., Lue N. F., Kornberg R. D. Statistical positioning of nucleosomes by specific protein-binding to an upstream activating sequence in yeast. J Mol Biol. 1988 Nov 5;204(1):109–127. doi: 10.1016/0022-2836(88)90603-1. [DOI] [PubMed] [Google Scholar]
  23. Felsenfeld G. Chromatin as an essential part of the transcriptional mechanism. Nature. 1992 Jan 16;355(6357):219–224. doi: 10.1038/355219a0. [DOI] [PubMed] [Google Scholar]
  24. Graziano V., Gerchman S. E., Schneider D. K., Ramakrishnan V. Histone H1 is located in the interior of the chromatin 30-nm filament. Nature. 1994 Mar 24;368(6469):351–354. doi: 10.1038/368351a0. [DOI] [PubMed] [Google Scholar]
  25. Hansen J. C., Ausio J., Stanik V. H., van Holde K. E. Homogeneous reconstituted oligonucleosomes, evidence for salt-dependent folding in the absence of histone H1. Biochemistry. 1989 Nov 14;28(23):9129–9136. doi: 10.1021/bi00449a026. [DOI] [PubMed] [Google Scholar]
  26. Hansen J. C., Wolffe A. P. A role for histones H2A/H2B in chromatin folding and transcriptional repression. Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2339–2343. doi: 10.1073/pnas.91.6.2339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hansen J. C., Wolffe A. P. Influence of chromatin folding on transcription initiation and elongation by RNA polymerase III. Biochemistry. 1992 Sep 1;31(34):7977–7988. doi: 10.1021/bi00149a032. [DOI] [PubMed] [Google Scholar]
  28. Hansen J. C., van Holde K. E., Lohr D. The mechanism of nucleosome assembly onto oligomers of the sea urchin 5 S DNA positioning sequence. J Biol Chem. 1991 Mar 5;266(7):4276–4282. [PubMed] [Google Scholar]
  29. Hayes J. J., Clark D. J., Wolffe A. P. Histone contributions to the structure of DNA in the nucleosome. Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6829–6833. doi: 10.1073/pnas.88.15.6829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hayes J. J., Pruss D., Wolffe A. P. Contacts of the globular domain of histone H5 and core histones with DNA in a "chromatosome". Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7817–7821. doi: 10.1073/pnas.91.16.7817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hayes J. J., Tullius T. D. Structure of the TFIIIA-5 S DNA complex. J Mol Biol. 1992 Sep 20;227(2):407–417. doi: 10.1016/0022-2836(92)90897-s. [DOI] [PubMed] [Google Scholar]
  32. 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]
  33. Hayes J. J., Wolffe A. P. Histones H2A/H2B inhibit the interaction of transcription factor IIIA with the Xenopus borealis somatic 5S RNA gene in a nucleosome. Proc Natl Acad Sci U S A. 1992 Feb 15;89(4):1229–1233. doi: 10.1073/pnas.89.4.1229. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Hayes J. J., Wolffe A. P. Preferential and asymmetric interaction of linker histones with 5S DNA in the nucleosome. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6415–6419. doi: 10.1073/pnas.90.14.6415. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Juan L. J., Walter P. P., Taylor I. C., Kingston R. E., Workman J. L. Nucleosome cores and histone H1 in the binding of GAL4 derivatives and the reactivation of transcription from nucleosome templates in vitro. Cold Spring Harb Symp Quant Biol. 1993;58:213–223. doi: 10.1101/sqb.1993.058.01.026. [DOI] [PubMed] [Google Scholar]
  36. Kamakaka R. T., Bulger M., Kadonaga J. T. Potentiation of RNA polymerase II transcription by Gal4-VP16 during but not after DNA replication and chromatin assembly. Genes Dev. 1993 Sep;7(9):1779–1795. doi: 10.1101/gad.7.9.1779. [DOI] [PubMed] [Google Scholar]
  37. Kandolf H. The H1A histone variant is an in vivo repressor of oocyte-type 5S gene transcription in Xenopus laevis embryos. Proc Natl Acad Sci U S A. 1994 Jul 19;91(15):7257–7261. doi: 10.1073/pnas.91.15.7257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lassar A. B., Martin P. L., Roeder R. G. Transcription of class III genes: formation of preinitiation complexes. Science. 1983 Nov 18;222(4625):740–748. doi: 10.1126/science.6356356. [DOI] [PubMed] [Google Scholar]
  39. Laybourn P. J., Kadonaga J. T. Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II. Science. 1991 Oct 11;254(5029):238–245. doi: 10.1126/science.254.5029.238. [DOI] [PubMed] [Google Scholar]
  40. Lee D. Y., Hayes J. J., Pruss D., Wolffe A. P. A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell. 1993 Jan 15;72(1):73–84. doi: 10.1016/0092-8674(93)90051-q. [DOI] [PubMed] [Google Scholar]
  41. Li Q., Wrange O. Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. Genes Dev. 1993 Dec;7(12A):2471–2482. doi: 10.1101/gad.7.12a.2471. [DOI] [PubMed] [Google Scholar]
  42. 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]
  43. McGhee J. D., Nickol J. M., Felsenfeld G., Rau D. C. Higher order structure of chromatin: orientation of nucleosomes within the 30 nm chromatin solenoid is independent of species and spacer length. Cell. 1983 Jul;33(3):831–841. doi: 10.1016/0092-8674(83)90025-9. [DOI] [PubMed] [Google Scholar]
  44. McPherson C. E., Shim E. Y., Friedman D. S., Zaret K. S. An active tissue-specific enhancer and bound transcription factors existing in a precisely positioned nucleosomal array. Cell. 1993 Oct 22;75(2):387–398. doi: 10.1016/0092-8674(93)80079-t. [DOI] [PubMed] [Google Scholar]
  45. Meersseman G., Pennings S., Bradbury E. M. Chromatosome positioning on assembled long chromatin. Linker histones affect nucleosome placement on 5 S rDNA. J Mol Biol. 1991 Jul 5;220(1):89–100. doi: 10.1016/0022-2836(91)90383-h. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Norton V. G., Imai B. S., Yau P., Bradbury E. M. Histone acetylation reduces nucleosome core particle linking number change. Cell. 1989 May 5;57(3):449–457. doi: 10.1016/0092-8674(89)90920-3. [DOI] [PubMed] [Google Scholar]
  48. O'Neill T. E., Roberge M., Bradbury E. M. Nucleosome arrays inhibit both initiation and elongation of transcripts by bacteriophage T7 RNA polymerase. J Mol Biol. 1992 Jan 5;223(1):67–78. doi: 10.1016/0022-2836(92)90716-w. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Pruss D., Hayes J. J., Wolffe A. P. Nucleosomal anatomy--where are the histones? Bioessays. 1995 Feb;17(2):161–170. doi: 10.1002/bies.950170211. [DOI] [PubMed] [Google Scholar]
  51. Ramakrishnan V., Finch J. T., Graziano V., Lee P. L., Sweet R. M. Crystal structure of globular domain of histone H5 and its implications for nucleosome binding. Nature. 1993 Mar 18;362(6417):219–223. doi: 10.1038/362219a0. [DOI] [PubMed] [Google Scholar]
  52. Reeves R., Nissen M. S. Interaction of high mobility group-I (Y) nonhistone proteins with nucleosome core particles. J Biol Chem. 1993 Oct 5;268(28):21137–21146. [PubMed] [Google Scholar]
  53. 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]
  54. 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]
  55. Schlissel M. S., Brown D. D. The transcriptional regulation of Xenopus 5s RNA genes in chromatin: the roles of active stable transcription complexes and histone H1. Cell. 1984 Jul;37(3):903–913. doi: 10.1016/0092-8674(84)90425-2. [DOI] [PubMed] [Google Scholar]
  56. Schwabe J. W., Travers A. A. What is evolution playing at? Curr Biol. 1993 Sep 1;3(9):628–630. doi: 10.1016/0960-9822(93)90016-h. [DOI] [PubMed] [Google Scholar]
  57. Shimamura A., Sapp M., Rodriguez-Campos A., Worcel A. Histone H1 represses transcription from minichromosomes assembled in vitro. Mol Cell Biol. 1989 Dec;9(12):5573–5584. doi: 10.1128/mcb.9.12.5573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Shrader T. E., Crothers D. M. Effects of DNA sequence and histone-histone interactions on nucleosome placement. J Mol Biol. 1990 Nov 5;216(1):69–84. doi: 10.1016/S0022-2836(05)80061-0. [DOI] [PubMed] [Google Scholar]
  59. Simpson R. T. Nucleosome positioning: occurrence, mechanisms, and functional consequences. Prog Nucleic Acid Res Mol Biol. 1991;40:143–184. doi: 10.1016/s0079-6603(08)60841-7. [DOI] [PubMed] [Google Scholar]
  60. 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]
  61. Simpson R. T. Structure of the chromatosome, a chromatin particle containing 160 base pairs of DNA and all the histones. Biochemistry. 1978 Dec 12;17(25):5524–5531. doi: 10.1021/bi00618a030. [DOI] [PubMed] [Google Scholar]
  62. Simpson R. T., Thoma F., Brubaker J. M. Chromatin reconstituted from tandemly repeated cloned DNA fragments and core histones: a model system for study of higher order structure. Cell. 1985 Oct;42(3):799–808. doi: 10.1016/0092-8674(85)90276-4. [DOI] [PubMed] [Google Scholar]
  63. Smith S., Stillman B. Stepwise assembly of chromatin during DNA replication in vitro. EMBO J. 1991 Apr;10(4):971–980. doi: 10.1002/j.1460-2075.1991.tb08031.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Tatchell K., Van Holde K. E. Reconstitution of chromatin core particles. Biochemistry. 1977 Nov 29;16(24):5295–5303. doi: 10.1021/bi00643a021. [DOI] [PubMed] [Google Scholar]
  65. Travers A. A. Chromatin structure and dynamics. Bioessays. 1994 Sep;16(9):657–662. doi: 10.1002/bies.950160911. [DOI] [PubMed] [Google Scholar]
  66. 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]
  67. Varga-Weisz P. D., Blank T. A., Becker P. B. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system. EMBO J. 1995 May 15;14(10):2209–2216. doi: 10.1002/j.1460-2075.1995.tb07215.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. 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]
  69. Weintraub H. Assembly and propagation of repressed and depressed chromosomal states. Cell. 1985 Oct;42(3):705–711. doi: 10.1016/0092-8674(85)90267-3. [DOI] [PubMed] [Google Scholar]
  70. Weintraub H. Histone-H1-dependent chromatin superstructures and the suppression of gene activity. Cell. 1984 Aug;38(1):17–27. doi: 10.1016/0092-8674(84)90522-1. [DOI] [PubMed] [Google Scholar]
  71. 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]
  72. Wolffe A. P. Dominant and specific repression of Xenopus oocyte 5S RNA genes and satellite I DNA by histone H1. EMBO J. 1989 Feb;8(2):527–537. doi: 10.1002/j.1460-2075.1989.tb03407.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Wolffe A. P., Jordan E., Brown D. D. A bacteriophage RNA polymerase transcribes through a Xenopus 5S RNA gene transcription complex without disrupting it. Cell. 1986 Feb 14;44(3):381–389. doi: 10.1016/0092-8674(86)90459-9. [DOI] [PubMed] [Google Scholar]
  74. Wolffe A. P. The transcription of chromatin templates. Curr Opin Genet Dev. 1994 Apr;4(2):245–254. doi: 10.1016/s0959-437x(05)80051-6. [DOI] [PubMed] [Google Scholar]
  75. 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]
  76. 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]
  77. Yao J., Lowary P. T., Widom J. Direct detection of linker DNA bending in defined-length oligomers of chromatin. Proc Natl Acad Sci U S A. 1990 Oct;87(19):7603–7607. doi: 10.1073/pnas.87.19.7603. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Yao J., Lowary P. T., Widom J. Linker DNA bending induced by the core histones of chromatin. Biochemistry. 1991 Aug 27;30(34):8408–8414. doi: 10.1021/bi00098a019. [DOI] [PubMed] [Google Scholar]

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