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. 1997 Dec 1;16(23):7130–7145. doi: 10.1093/emboj/16.23.7130

Structural and functional features of a specific nucleosome containing a recognition element for the thyroid hormone receptor.

J Wong 1, Q Li 1, B Z Levi 1, Y B Shi 1, A P Wolffe 1
PMCID: PMC1170314  PMID: 9384590

Abstract

The Xenopus thyroid hormone receptor betaA (TRbetaA) gene contains an important thyroid hormone response element (TRE) that is assembled into a positioned nucleosome. We determine the translational position of the nucleosome containing the TRE and the rotational positioning of the double helix with respect to the histone surface. Histone H1 is incorporated into the nucleosome leading to an asymmetric protection to micrococcal nuclease cleavage of linker DNA relative to the nucleosome core. Histone H1 association is without significant consequence for the binding of the heterodimer of thyroid hormone receptor and 9-cis retinoic acid receptor (TR/RXR) to nucleosomal DNA in vitro, or for the regulation of TRbetaA gene transcription following microinjection into the oocyte nucleus. Small alterations of 3 and 6 bp in the translational positioning of the TRE in chromatin are also without effect on the transcriptional activity of the TRbetaA gene, whereas a small change in the rotational position of the TRE (3 bp) relative to the histone surface significantly reduces the binding of TR/RXR to the nucleosome and decreases transcriptional activation directed by TR/RXR. Our results indicate that the specific architecture of the nucleosome containing the TRE may have regulatory significance for expression of the TRbetaA gene.

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Selected References

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  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. Almer A., Hörz W. Nuclease hypersensitive regions with adjacent positioned nucleosomes mark the gene boundaries of the PHO5/PHO3 locus in yeast. EMBO J. 1986 Oct;5(10):2681–2687. doi: 10.1002/j.1460-2075.1986.tb04551.x. [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. Almouzni G., Wolffe A. P. Replication-coupled chromatin assembly is required for the repression of basal transcription in vivo. Genes Dev. 1993 Oct;7(10):2033–2047. doi: 10.1101/gad.7.10.2033. [DOI] [PubMed] [Google Scholar]
  5. Archer T. K., Cordingley M. G., Wolford R. G., Hager G. L. Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Feb;11(2):688–698. doi: 10.1128/mcb.11.2.688. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Arents G., Burlingame R. W., Wang B. C., Love W. E., Moudrianakis E. N. The nucleosomal core histone octamer at 3.1 A resolution: a tripartite protein assembly and a left-handed superhelix. Proc Natl Acad Sci U S A. 1991 Nov 15;88(22):10148–10152. doi: 10.1073/pnas.88.22.10148. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Arents G., Moudrianakis E. N. Topography of the histone octamer surface: repeating structural motifs utilized in the docking of nucleosomal DNA. Proc Natl Acad Sci U S A. 1993 Nov 15;90(22):10489–10493. doi: 10.1073/pnas.90.22.10489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Barettino D., Vivanco Ruiz M. M., Stunnenberg H. G. Characterization of the ligand-dependent transactivation domain of thyroid hormone receptor. EMBO J. 1994 Jul 1;13(13):3039–3049. doi: 10.1002/j.1460-2075.1994.tb06603.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. 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]
  10. Blumberg B., Mangelsdorf D. J., Dyck J. A., Bittner D. A., Evans R. M., De Robertis E. M. Multiple retinoid-responsive receptors in a single cell: families of retinoid "X" receptors and retinoic acid receptors in the Xenopus egg. Proc Natl Acad Sci U S A. 1992 Mar 15;89(6):2321–2325. doi: 10.1073/pnas.89.6.2321. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Bouvet P., Wolffe A. P. A role for transcription and FRGY2 in masking maternal mRNA within Xenopus oocytes. Cell. 1994 Jun 17;77(6):931–941. doi: 10.1016/0092-8674(94)90141-4. [DOI] [PubMed] [Google Scholar]
  13. Calladine C. R., Drew H. R. Principles of sequence-dependent flexure of DNA. J Mol Biol. 1986 Dec 20;192(4):907–918. doi: 10.1016/0022-2836(86)90036-7. [DOI] [PubMed] [Google Scholar]
  14. Chávez S., Beato M. Nucleosome-mediated synergism between transcription factors on the mouse mammary tumor virus promoter. Proc Natl Acad Sci U S A. 1997 Apr 1;94(7):2885–2890. doi: 10.1073/pnas.94.7.2885. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. 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]
  17. Crane-Robinson C. Where is the globular domain of linker histone located on the nucleosome? Trends Biochem Sci. 1997 Mar;22(3):75–77. doi: 10.1016/s0968-0004(97)01013-x. [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. 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]
  20. Fragoso G., John S., Roberts M. S., Hager G. L. Nucleosome positioning on the MMTV LTR results from the frequency-biased occupancy of multiple frames. Genes Dev. 1995 Aug 1;9(15):1933–1947. doi: 10.1101/gad.9.15.1933. [DOI] [PubMed] [Google Scholar]
  21. 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]
  22. Glass C. K. Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocr Rev. 1994 Jun;15(3):391–407. doi: 10.1210/edrv-15-3-391. [DOI] [PubMed] [Google Scholar]
  23. Godde J. S., Nakatani Y., Wolffe A. P. The amino-terminal tails of the core histones and the translational position of the TATA box determine TBP/TFIIA association with nucleosomal DNA. Nucleic Acids Res. 1995 Nov 25;23(22):4557–4564. doi: 10.1093/nar/23.22.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Godde J. S., Wolffe A. P. Disruption of reconstituted nucleosomes. The effect of particle concentration, MgCl2 and KCl concentration, the histone tails, and temperature. J Biol Chem. 1995 Nov 17;270(46):27399–27402. doi: 10.1074/jbc.270.46.27399. [DOI] [PubMed] [Google Scholar]
  25. Godde J. S., Wolffe A. P. Nucleosome assembly on CTG triplet repeats. J Biol Chem. 1996 Jun 21;271(25):15222–15229. doi: 10.1074/jbc.271.25.15222. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Hayes J. J., Bashkin J., Tullius T. D., Wolffe A. P. The histone core exerts a dominant constraint on the structure of DNA in a nucleosome. Biochemistry. 1991 Aug 27;30(34):8434–8440. doi: 10.1021/bi00098a022. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Hayes J. J. Site-directed cleavage of DNA by a linker histone--Fe(II) EDTA conjugate: localization of a globular domain binding site within a nucleosome. Biochemistry. 1996 Sep 17;35(37):11931–11937. doi: 10.1021/bi961590+. [DOI] [PubMed] [Google Scholar]
  30. 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]
  31. 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]
  32. 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]
  33. Heinzel T., Lavinsky R. M., Mullen T. M., Söderstrom M., Laherty C. D., Torchia J., Yang W. M., Brard G., Ngo S. D., Davie J. R. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature. 1997 May 1;387(6628):43–48. doi: 10.1038/387043a0. [DOI] [PubMed] [Google Scholar]
  34. Juan L. J., Utley R. T., Adams C. C., Vettese-Dadey M., Workman J. L. Differential repression of transcription factor binding by histone H1 is regulated by the core histone amino termini. EMBO J. 1994 Dec 15;13(24):6031–6040. doi: 10.1002/j.1460-2075.1994.tb06949.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Juan L. J., Utley R. T., Vignali M., Bohm L., Workman J. L. H1-mediated repression of transcription factor binding to a stably positioned nucleosome. J Biol Chem. 1997 Feb 7;272(6):3635–3640. doi: 10.1074/jbc.272.6.3635. [DOI] [PubMed] [Google Scholar]
  36. 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]
  37. Li Q., Wrange O. Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning. Mol Cell Biol. 1995 Aug;15(8):4375–4384. doi: 10.1128/mcb.15.8.4375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. 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]
  39. 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]
  40. Nagy L., Kao H. Y., Chakravarti D., Lin R. J., Hassig C. A., Ayer D. E., Schreiber S. L., Evans R. M. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell. 1997 May 2;89(3):373–380. doi: 10.1016/s0092-8674(00)80218-4. [DOI] [PubMed] [Google Scholar]
  41. Nightingale K. P., Pruss D., Wolffe A. P. A single high affinity binding site for histone H1 in a nucleosome containing the Xenopus borealis 5 S ribosomal RNA gene. J Biol Chem. 1996 Mar 22;271(12):7090–7094. doi: 10.1074/jbc.271.12.7090. [DOI] [PubMed] [Google Scholar]
  42. Nightingale K., Dimitrov S., Reeves R., Wolffe A. P. Evidence for a shared structural role for HMG1 and linker histones B4 and H1 in organizing chromatin. EMBO J. 1996 Feb 1;15(3):548–561. [PMC free article] [PubMed] [Google Scholar]
  43. 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]
  44. Ogryzko V. V., Schiltz R. L., Russanova V., Howard B. H., Nakatani Y. The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell. 1996 Nov 29;87(5):953–959. doi: 10.1016/s0092-8674(00)82001-2. [DOI] [PubMed] [Google Scholar]
  45. Perlmann T., Wrange O. Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. EMBO J. 1988 Oct;7(10):3073–3079. doi: 10.1002/j.1460-2075.1988.tb03172.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Piña B., Barettino D., Truss M., Beato M. Structural features of a regulatory nucleosome. J Mol Biol. 1990 Dec 20;216(4):975–990. doi: 10.1016/S0022-2836(99)80015-1. [DOI] [PubMed] [Google Scholar]
  47. Piña B., Brüggemeier U., Beato M. Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter. Cell. 1990 Mar 9;60(5):719–731. doi: 10.1016/0092-8674(90)90087-u. [DOI] [PubMed] [Google Scholar]
  48. Prunell A. Nucleosome reconstitution on plasmid-inserted poly(dA) . poly(dT). EMBO J. 1982;1(2):173–179. doi: 10.1002/j.1460-2075.1982.tb01143.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Pruss D., Bartholomew B., Persinger J., Hayes J., Arents G., Moudrianakis E. N., Wolffe A. P. An asymmetric model for the nucleosome: a binding site for linker histones inside the DNA gyres. Science. 1996 Oct 25;274(5287):614–617. doi: 10.1126/science.274.5287.614. [DOI] [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. Pruss D., Wolffe A. P. Histone-DNA contacts in a nucleosome core containing a Xenopus 5S rRNA gene. Biochemistry. 1993 Jul 13;32(27):6810–6814. doi: 10.1021/bi00078a002. [DOI] [PubMed] [Google Scholar]
  52. 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]
  53. Ranjan M., Wong J., Shi Y. B. Transcriptional repression of Xenopus TR beta gene is mediated by a thyroid hormone response element located near the start site. J Biol Chem. 1994 Oct 7;269(40):24699–24705. [PubMed] [Google Scholar]
  54. 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]
  55. Richard-Foy H., Hager G. L. Sequence-specific positioning of nucleosomes over the steroid-inducible MMTV promoter. EMBO J. 1987 Aug;6(8):2321–2328. doi: 10.1002/j.1460-2075.1987.tb02507.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Roberts M. S., Fragoso G., Hager G. L. Nucleosomes reconstituted in vitro on mouse mammary tumor virus B region DNA occupy multiple translational and rotational frames. Biochemistry. 1995 Sep 26;34(38):12470–12480. doi: 10.1021/bi00038a046. [DOI] [PubMed] [Google Scholar]
  57. 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]
  58. Sap J., Muñoz A., Schmitt J., Stunnenberg H., Vennström B. Repression of transcription mediated at a thyroid hormone response element by the v-erb-A oncogene product. Nature. 1989 Jul 20;340(6230):242–244. doi: 10.1038/340242a0. [DOI] [PubMed] [Google Scholar]
  59. Schild C., Claret F. X., Wahli W., Wolffe A. P. A nucleosome-dependent static loop potentiates estrogen-regulated transcription from the Xenopus vitellogenin B1 promoter in vitro. EMBO J. 1993 Feb;12(2):423–433. doi: 10.1002/j.1460-2075.1993.tb05674.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Shen X., Gorovsky M. A. Linker histone H1 regulates specific gene expression but not global transcription in vivo. Cell. 1996 Aug 9;86(3):475–483. doi: 10.1016/s0092-8674(00)80120-8. [DOI] [PubMed] [Google Scholar]
  61. 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]
  62. Shrader T. E., Crothers D. M. Artificial nucleosome positioning sequences. Proc Natl Acad Sci U S A. 1989 Oct;86(19):7418–7422. doi: 10.1073/pnas.86.19.7418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Simpson R. T. Nucleosome positioning can affect the function of a cis-acting DNA element in vivo. Nature. 1990 Jan 25;343(6256):387–389. doi: 10.1038/343387a0. [DOI] [PubMed] [Google Scholar]
  64. 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]
  65. 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]
  66. 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]
  67. Straka C., Hörz W. A functional role for nucleosomes in the repression of a yeast promoter. EMBO J. 1991 Feb;10(2):361–368. doi: 10.1002/j.1460-2075.1991.tb07957.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. 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]
  69. Thoma F. Nucleosome positioning. Biochim Biophys Acta. 1992 Feb 28;1130(1):1–19. doi: 10.1016/0167-4781(92)90455-9. [DOI] [PubMed] [Google Scholar]
  70. Truss M., Bartsch J., Schelbert A., Haché R. J., Beato M. Hormone induces binding of receptors and transcription factors to a rearranged nucleosome on the MMTV promoter in vivo. EMBO J. 1995 Apr 18;14(8):1737–1751. doi: 10.1002/j.1460-2075.1995.tb07163.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Ura K., Hayes J. J., Wolffe A. P. A positive role for nucleosome mobility in the transcriptional activity of chromatin templates: restriction by linker histones. EMBO J. 1995 Aug 1;14(15):3752–3765. doi: 10.1002/j.1460-2075.1995.tb00045.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Ura K., Kurumizaka H., Dimitrov S., Almouzni G., Wolffe A. P. Histone acetylation: influence on transcription, nucleosome mobility and positioning, and linker histone-dependent transcriptional repression. EMBO J. 1997 Apr 15;16(8):2096–2107. doi: 10.1093/emboj/16.8.2096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Verdin E., Paras P., Jr, Van Lint C. Chromatin disruption in the promoter of human immunodeficiency virus type 1 during transcriptional activation. EMBO J. 1993 Aug;12(8):3249–3259. doi: 10.1002/j.1460-2075.1993.tb05994.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. 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]
  75. Wolffe A. P., Drew H. R. Initiation of transcription on nucleosomal templates. Proc Natl Acad Sci U S A. 1989 Dec;86(24):9817–9821. doi: 10.1073/pnas.86.24.9817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Wolffe A. P. Nucleosome positioning and modification: chromatin structures that potentiate transcription. Trends Biochem Sci. 1994 Jun;19(6):240–244. doi: 10.1016/0968-0004(94)90148-1. [DOI] [PubMed] [Google Scholar]
  77. Wong J., Shi Y. B., Wolffe A. P. A role for nucleosome assembly in both silencing and activation of the Xenopus TR beta A gene by the thyroid hormone receptor. Genes Dev. 1995 Nov 1;9(21):2696–2711. doi: 10.1101/gad.9.21.2696. [DOI] [PubMed] [Google Scholar]
  78. Wong J., Shi Y. B., Wolffe A. P. Determinants of chromatin disruption and transcriptional regulation instigated by the thyroid hormone receptor: hormone-regulated chromatin disruption is not sufficient for transcriptional activation. EMBO J. 1997 Jun 2;16(11):3158–3171. doi: 10.1093/emboj/16.11.3158. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Yang X. J., Ogryzko V. V., Nishikawa J., Howard B. H., Nakatani Y. A p300/CBP-associated factor that competes with the adenoviral oncoprotein E1A. Nature. 1996 Jul 25;382(6589):319–324. doi: 10.1038/382319a0. [DOI] [PubMed] [Google Scholar]

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