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. 1997 Sep 15;25(18):3559–3563. doi: 10.1093/nar/25.18.3559

Transcription factor access to chromatin.

M Beato 1, K Eisfeld 1
PMCID: PMC146956  PMID: 9278473

Abstract

The question of how sequence-specific transcription factors access their cognate sites in nucleosomally organized DNA is discussed on the basis of genomic footprinting data and chromatin reconstitution experiments. A classification of factors into two categories is proposed: (i) initiator factors which are able to bind their target sequences within regular nucleosomes and initiate events leading to chromatin remodelling and transactivation; (ii) effector factors which are unable to bind regular nucleosomes and depend on initiator factors or on a pre-set nucleosomal structure for accessing their target sequences in chromatin. Studies with the MMTV promoter suggest that the extent and number of protein-DNA contacts determine whether a factor belongs to one or the other category. Initiator factors have only a few DNA contacts clustered on one side of the double helix, whereas effector factors have extensive contacts distributed throughout the whole circumference of the DNA helix. Thus, the nature of DNA recognition confers to sequence-specific factors their specific place in the sequential hierarchy of gene regulatory events.

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Selected References

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  1. 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]
  2. 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]
  3. 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]
  4. Bartsch J., Truss M., Bode J., Beato M. Moderate increase in histone acetylation activates the mouse mammary tumor virus promoter and remodels its nucleosome structure. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10741–10746. doi: 10.1073/pnas.93.20.10741. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Beato M., Herrlich P., Schütz G. Steroid hormone receptors: many actors in search of a plot. Cell. 1995 Dec 15;83(6):851–857. doi: 10.1016/0092-8674(95)90201-5. [DOI] [PubMed] [Google Scholar]
  6. Becker P., Renkawitz R., Schütz G. Tissue-specific DNaseI hypersensitive sites in the 5'-flanking sequences of the tryptophan oxygenase and the tyrosine aminotransferase genes. EMBO J. 1984 Sep;3(9):2015–2020. doi: 10.1002/j.1460-2075.1984.tb02084.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Benyajati C., Ewel A., McKeon J., Chovav M., Juan E. Characterization and purification of Adh distal promoter factor 2, Adf-2, a cell-specific and promoter-specific repressor in Drosophila. Nucleic Acids Res. 1992 Sep 11;20(17):4481–4489. doi: 10.1093/nar/20.17.4481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Blomquist P., Li Q., Wrange O. The affinity of nuclear factor 1 for its DNA site is drastically reduced by nucleosome organization irrespective of its rotational or translational position. J Biol Chem. 1996 Jan 5;271(1):153–159. doi: 10.1074/jbc.271.1.153. [DOI] [PubMed] [Google Scholar]
  9. Burch J. B., Weintraub H. Temporal order of chromatin structural changes associated with activation of the major chicken vitellogenin gene. Cell. 1983 May;33(1):65–76. doi: 10.1016/0092-8674(83)90335-5. [DOI] [PubMed] [Google Scholar]
  10. Carr K. D., Richard-Foy H. Glucocorticoids locally disrupt an array of positioned nucleosomes on the rat tyrosine aminotransferase promoter in hepatoma cells. Proc Natl Acad Sci U S A. 1990 Dec;87(23):9300–9304. doi: 10.1073/pnas.87.23.9300. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chalepakis G., Arnemann J., Slater E., Brüller H. J., Gross B., Beato M. Differential gene activation by glucocorticoids and progestins through the hormone regulatory element of mouse mammary tumor virus. Cell. 1988 May 6;53(3):371–382. doi: 10.1016/0092-8674(88)90157-2. [DOI] [PubMed] [Google Scholar]
  12. Chasman D. I., Lue N. F., Buchman A. R., LaPointe J. W., Lorch Y., Kornberg R. D. A yeast protein that influences the chromatin structure of UASG and functions as a powerful auxiliary gene activator. Genes Dev. 1990 Apr;4(4):503–514. doi: 10.1101/gad.4.4.503. [DOI] [PubMed] [Google Scholar]
  13. Chen H., Li B., Workman J. L. A histone-binding protein, nucleoplasmin, stimulates transcription factor binding to nucleosomes and factor-induced nucleosome disassembly. EMBO J. 1994 Jan 15;13(2):380–390. doi: 10.1002/j.1460-2075.1994.tb06272.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Demarchi F., D'Agaro P., Falaschi A., Giacca M. In vivo footprinting analysis of constitutive and inducible protein-DNA interactions at the long terminal repeat of human immunodeficiency virus type 1. J Virol. 1993 Dec;67(12):7450–7460. doi: 10.1128/jvi.67.12.7450-7460.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Elgin S. C. The formation and function of DNase I hypersensitive sites in the process of gene activation. J Biol Chem. 1988 Dec 25;263(36):19259–19262. [PubMed] [Google Scholar]
  16. Fedor M. J., Kornberg R. D. Upstream activation sequence-dependent alteration of chromatin structure and transcription activation of the yeast GAL1-GAL10 genes. Mol Cell Biol. 1989 Apr;9(4):1721–1732. doi: 10.1128/mcb.9.4.1721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. 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]
  18. FitzGerald P. C., Simpson R. T. Effects of sequence alterations in a DNA segment containing the 5 S RNA gene from Lytechinus variegatus on positioning of a nucleosome core particle in vitro. J Biol Chem. 1985 Dec 5;260(28):15318–15324. [PubMed] [Google Scholar]
  19. 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]
  20. Ghosh D. Glucocorticoid receptor-binding site in the human immunodeficiency virus long terminal repeat. J Virol. 1992 Jan;66(1):586–590. doi: 10.1128/jvi.66.1.586-590.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. 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]
  22. Grosschedl R., Giese K., Pagel J. HMG domain proteins: architectural elements in the assembly of nucleoprotein structures. Trends Genet. 1994 Mar;10(3):94–100. doi: 10.1016/0168-9525(94)90232-1. [DOI] [PubMed] [Google Scholar]
  23. Gualdi R., Bossard P., Zheng M., Hamada Y., Coleman J. R., Zaret K. S. Hepatic specification of the gut endoderm in vitro: cell signaling and transcriptional control. Genes Dev. 1996 Jul 1;10(13):1670–1682. doi: 10.1101/gad.10.13.1670. [DOI] [PubMed] [Google Scholar]
  24. 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]
  25. 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]
  26. 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]
  27. Herrera R. E., Shaw P. E., Nordheim A. Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature. 1989 Jul 6;340(6228):68–70. doi: 10.1038/340068a0. [DOI] [PubMed] [Google Scholar]
  28. 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]
  29. Ioshikhes I., Bolshoy A., Derenshteyn K., Borodovsky M., Trifonov E. N. Nucleosome DNA sequence pattern revealed by multiple alignment of experimentally mapped sequences. J Mol Biol. 1996 Sep 20;262(2):129–139. doi: 10.1006/jmbi.1996.0503. [DOI] [PubMed] [Google Scholar]
  30. Ioshikhes I., Trifonov E. N. Nucleosomal DNA sequence database. Nucleic Acids Res. 1993 Oct 25;21(21):4857–4859. doi: 10.1093/nar/21.21.4857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Iyer V., Struhl K. Poly(dA:dT), a ubiquitous promoter element that stimulates transcription via its intrinsic DNA structure. EMBO J. 1995 Jun 1;14(11):2570–2579. doi: 10.1002/j.1460-2075.1995.tb07255.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Jackson J. R., Benyajati C. DNA-histone interactions are sufficient to position a single nucleosome juxtaposing Drosophila Adh adult enhancer and distal promoter. Nucleic Acids Res. 1993 Feb 25;21(4):957–967. doi: 10.1093/nar/21.4.957. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Jantzen K., Fritton H. P., Igo-Kemenes T., Espel E., Janich S., Cato A. C., Mugele K., Beato M. Partial overlapping of binding sequences for steroid hormone receptors and DNaseI hypersensitive sites in the rabbit uteroglobin gene region. Nucleic Acids Res. 1987 Jun 11;15(11):4535–4552. doi: 10.1093/nar/15.11.4535. [DOI] [PMC free article] [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. Koch K. A., Thiele D. J. Autoactivation by a Candida glabrata copper metalloregulatory transcription factor requires critical minor groove interactions. Mol Cell Biol. 1996 Feb;16(2):724–734. doi: 10.1128/mcb.16.2.724. [DOI] [PMC free article] [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 B., Adams C. C., Workman J. L. Nucleosome binding by the constitutive transcription factor Sp1. J Biol Chem. 1994 Mar 11;269(10):7756–7763. [PubMed] [Google Scholar]
  38. 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]
  39. Lohr D., Torchia T., Hopper J. The regulatory protein GAL80 is a determinant of the chromatin structure of the yeast GAL1-10 control region. J Biol Chem. 1987 Nov 15;262(32):15589–15597. [PubMed] [Google Scholar]
  40. Luisi B. F., Xu W. X., Otwinowski Z., Freedman L. P., Yamamoto K. R., Sigler P. B. Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA. Nature. 1991 Aug 8;352(6335):497–505. doi: 10.1038/352497a0. [DOI] [PubMed] [Google Scholar]
  41. 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]
  42. 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]
  43. Miksicek R., Heber A., Schmid W., Danesch U., Posseckert G., Beato M., Schütz G. Glucocorticoid responsiveness of the transcriptional enhancer of Moloney murine sarcoma virus. Cell. 1986 Jul 18;46(2):283–290. doi: 10.1016/0092-8674(86)90745-2. [DOI] [PubMed] [Google Scholar]
  44. Mutskov V. J., Russanova V. R., Dimitrov S. I., Pashev I. G. Histones associated with non-nucleosomal rat ribosomal genes are acetylated while those bound to nucleosome-organized gene copies are not. J Biol Chem. 1996 May 17;271(20):11852–11857. doi: 10.1074/jbc.271.20.11852. [DOI] [PubMed] [Google Scholar]
  45. Pazin M. J., Sheridan P. L., Cannon K., Cao Z., Keck J. G., Kadonaga J. T., Jones K. A. NF-kappa B-mediated chromatin reconfiguration and transcriptional activation of the HIV-1 enhancer in vitro. Genes Dev. 1996 Jan 1;10(1):37–49. doi: 10.1101/gad.10.1.37. [DOI] [PubMed] [Google Scholar]
  46. Perlmann T. Glucocorticoid receptor DNA-binding specificity is increased by the organization of DNA in nucleosomes. Proc Natl Acad Sci U S A. 1992 May 1;89(9):3884–3888. doi: 10.1073/pnas.89.9.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. 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]
  48. Pham T. A., McDonnell D. P., Tsai M. J., O'Malley B. W. Modulation of progesterone receptor binding to progesterone response elements by positioned nucleosomes. Biochemistry. 1992 Feb 11;31(5):1570–1578. doi: 10.1021/bi00120a039. [DOI] [PubMed] [Google Scholar]
  49. 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]
  50. Piña B., Haché R. J., Arnemann J., Chalepakis G., Slater E. P., Beato M. Hormonal induction of transfected genes depends on DNA topology. Mol Cell Biol. 1990 Feb;10(2):625–633. doi: 10.1128/mcb.10.2.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Polach K. J., Widom J. A model for the cooperative binding of eukaryotic regulatory proteins to nucleosomal target sites. J Mol Biol. 1996 May 24;258(5):800–812. doi: 10.1006/jmbi.1996.0288. [DOI] [PubMed] [Google Scholar]
  52. Polach K. J., Widom J. Mechanism of protein access to specific DNA sequences in chromatin: a dynamic equilibrium model for gene regulation. J Mol Biol. 1995 Nov 24;254(2):130–149. doi: 10.1006/jmbi.1995.0606. [DOI] [PubMed] [Google Scholar]
  53. 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]
  54. Rhodes D. Structural analysis of a triple complex between the histone octamer, a Xenopus gene for 5S RNA and transcription factor IIIA. EMBO J. 1985 Dec 16;4(13A):3473–3482. doi: 10.1002/j.1460-2075.1985.tb04106.x. [DOI] [PMC free article] [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. Scheidereit C., Beato M. Contacts between hormone receptor and DNA double helix within a glucocorticoid regulatory element of mouse mammary tumor virus. Proc Natl Acad Sci U S A. 1984 May;81(10):3029–3033. doi: 10.1073/pnas.81.10.3029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. 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]
  58. 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]
  59. Stünkel W., Kober I., Kauer M., Taimor G., Seifart K. H. Human TFIIIA alone is sufficient to prevent nucleosomal repression of a homologous 5S gene. Nucleic Acids Res. 1995 Jan 11;23(1):109–116. doi: 10.1093/nar/23.1.109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Svaren J., Schmitz J., Hörz W. The transactivation domain of Pho4 is required for nucleosome disruption at the PHO5 promoter. EMBO J. 1994 Oct 17;13(20):4856–4862. doi: 10.1002/j.1460-2075.1994.tb06812.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. 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]
  62. 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]
  63. Thomas G. H., Elgin S. C. Protein/DNA architecture of the DNase I hypersensitive region of the Drosophila hsp26 promoter. EMBO J. 1988 Jul;7(7):2191–2201. doi: 10.1002/j.1460-2075.1988.tb03058.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. 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]
  65. Truss M., Beato M. Steroid hormone receptors: interaction with deoxyribonucleic acid and transcription factors. Endocr Rev. 1993 Aug;14(4):459–479. doi: 10.1210/edrv-14-4-459. [DOI] [PubMed] [Google Scholar]
  66. Truss M., Chalepakis G., Beato M. Contacts between steroid hormone receptors and thymines in DNA: an interference method. Proc Natl Acad Sci U S A. 1990 Sep;87(18):7180–7184. doi: 10.1073/pnas.87.18.7180. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. 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]
  68. 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]
  69. Ura K., Nightingale K., Wolffe A. P. Differential association of HMG1 and linker histones B4 and H1 with dinucleosomal DNA: structural transitions and transcriptional repression. EMBO J. 1996 Sep 16;15(18):4959–4969. [PMC free article] [PubMed] [Google Scholar]
  70. Van Lint C., Emiliani S., Ott M., Verdin E. Transcriptional activation and chromatin remodeling of the HIV-1 promoter in response to histone acetylation. EMBO J. 1996 Mar 1;15(5):1112–1120. [PMC free article] [PubMed] [Google Scholar]
  71. Venter U., Svaren J., Schmitz J., Schmid A., Hörz W. A nucleosome precludes binding of the transcription factor Pho4 in vivo to a critical target site in the PHO5 promoter. EMBO J. 1994 Oct 17;13(20):4848–4855. doi: 10.1002/j.1460-2075.1994.tb06811.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. 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]
  73. 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]
  74. Walter P. P., Owen-Hughes T. A., Côté J., Workman J. L. Stimulation of transcription factor binding and histone displacement by nucleosome assembly protein 1 and nucleoplasmin requires disruption of the histone octamer. Mol Cell Biol. 1995 Nov;15(11):6178–6187. doi: 10.1128/mcb.15.11.6178. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. 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]
  76. 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]
  77. Zaret K. S., Yamamoto K. R. Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element. Cell. 1984 Aug;38(1):29–38. doi: 10.1016/0092-8674(84)90523-3. [DOI] [PubMed] [Google Scholar]
  78. Zhu Z., Thiele D. J. A specialized nucleosome modulates transcription factor access to a C. glabrata metal responsive promoter. Cell. 1996 Nov 1;87(3):459–470. doi: 10.1016/s0092-8674(00)81366-5. [DOI] [PubMed] [Google Scholar]
  79. de Vries E., van Driel W., van den Heuvel S. J., van der Vliet P. C. Contactpoint analysis of the HeLa nuclear factor I recognition site reveals symmetrical binding at one side of the DNA helix. EMBO J. 1987 Jan;6(1):161–168. doi: 10.1002/j.1460-2075.1987.tb04734.x. [DOI] [PMC free article] [PubMed] [Google Scholar]

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