Skip to main content
Molecular and Cellular Biology logoLink to Molecular and Cellular Biology
. 1996 Dec;16(12):7004–7017. doi: 10.1128/mcb.16.12.7004

Heat shock factor gains access to the yeast HSC82 promoter independently of other sequence-specific factors and antagonizes nucleosomal repression of basal and induced transcription.

A M Erkine 1, C C Adams 1, T Diken 1, D S Gross 1
PMCID: PMC231704  PMID: 8943356

Abstract

Transcription in eukaryotic cells occurs in the context of chromatin. Binding of sequence-specific regulatory factors must contend with the presence of nucleosomes for establishment of a committed preinitiation complex. Here we demonstrate that the high-affinity binding site for heat shock transcription factor (HSF) is occupied independently of other cis-regulatory elements and is critically required for preventing nucleosomal assembly over the yeast HSC82 core promoter under both noninducing (basal) and inducing conditions. Chromosomal mutation of this sequence, termed HSE1, erases the HSF footprint and abolishes both transcription and in vivo occupancy of the TATA box. Moreover, it dramatically reduces promoter chromatin accessibility to DNase I and TaqI, as the nuclease-hypersensitive region is replaced by a localized nucleosome. By comparison, in situ mutagenesis of two other promoter elements engaged in stable protein-DNA interactions in vivo, the GRF2/REB1 site and the TATA box, despite reducing transcription three- to fivefold, does not compromise the nucleosome-free state of the promoter. The GRF2-binding factor appears to facilitate the binding of proteins to both HSE1 and TATA, as these sequences, while still occupied, are less protected from in vivo dimethyl sulfate methylation in a deltaGRF2 strain. Finally, deletion of a consensus upstream repressor sequence (URS1), positioned immediately upstream of the GRF2-HSE1 region and only weakly occupied in chromatin, has no expression phenotype, even under meiotic conditions. However, deletion of URS1, like mutation of GRF2, shifts the translational setting of an upstream nucleosomal array flanking the promoter region. Taken together, our results argue that HSF, independent of and dominant among sequence-specific factors binding to the HSC82 upstream region, antagonizes nucleosomal repression and creates an accessible chromatin structure conducive to preinitiation complex assembly and transcriptional activation.

Full Text

The Full Text of this article is available as a PDF (719.2 KB).

Selected References

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

  1. Adams C. C., Gross D. S. The yeast heat shock response is induced by conversion of cells to spheroplasts and by potent transcriptional inhibitors. J Bacteriol. 1991 Dec;173(23):7429–7435. doi: 10.1128/jb.173.23.7429-7435.1991. [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. 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]
  4. Axelrod J. D., Reagan M. S., Majors J. GAL4 disrupts a repressing nucleosome during activation of GAL1 transcription in vivo. Genes Dev. 1993 May;7(5):857–869. doi: 10.1101/gad.7.5.857. [DOI] [PubMed] [Google Scholar]
  5. Becker P. B., Rabindran S. K., Wu C. Heat shock-regulated transcription in vitro from a reconstituted chromatin template. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4109–4113. doi: 10.1073/pnas.88.10.4109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Borkovich K. A., Farrelly F. W., Finkelstein D. B., Taulien J., Lindquist S. hsp82 is an essential protein that is required in higher concentrations for growth of cells at higher temperatures. Mol Cell Biol. 1989 Sep;9(9):3919–3930. doi: 10.1128/mcb.9.9.3919. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bowdish K. S., Yuan H. E., Mitchell A. P. Positive control of yeast meiotic genes by the negative regulator UME6. Mol Cell Biol. 1995 Jun;15(6):2955–2961. doi: 10.1128/mcb.15.6.2955. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Boyes J., Felsenfeld G. Tissue-specific factors additively increase the probability of the all-or-none formation of a hypersensitive site. EMBO J. 1996 May 15;15(10):2496–2507. [PMC free article] [PubMed] [Google Scholar]
  9. Buratowski S. The basics of basal transcription by RNA polymerase II. Cell. 1994 Apr 8;77(1):1–3. doi: 10.1016/0092-8674(94)90226-7. [DOI] [PubMed] [Google Scholar]
  10. Carmen A. A., Holland M. J. The upstream repression sequence from the yeast enolase gene ENO1 is a complex regulatory element that binds multiple trans-acting factors including REB1. J Biol Chem. 1994 Apr 1;269(13):9790–9797. [PubMed] [Google Scholar]
  11. 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]
  12. Chatterjee S., Struhl K. Connecting a promoter-bound protein to TBP bypasses the need for a transcriptional activation domain. Nature. 1995 Apr 27;374(6525):820–822. doi: 10.1038/374820a0. [DOI] [PubMed] [Google Scholar]
  13. Drazinic C. M., Smerage J. B., López M. C., Baker H. V. Activation mechanism of the multifunctional transcription factor repressor-activator protein 1 (Rap1p). Mol Cell Biol. 1996 Jun;16(6):3187–3196. doi: 10.1128/mcb.16.6.3187. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Erkine A. M., Adams C. C., Gao M., Gross D. S. Multiple protein-DNA interactions over the yeast HSC82 heat shock gene promoter. Nucleic Acids Res. 1995 May 25;23(10):1822–1829. doi: 10.1093/nar/23.10.1822. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Erkine A. M., Szent-Gyorgyi C., Simmons S. F., Gross D. S. The upstream sequences of the HSP82 and HSC82 genes of Saccharomyces cerevisiae: regulatory elements and nucleosome positioning motifs. Yeast. 1995 May;11(6):573–580. doi: 10.1002/yea.320110607. [DOI] [PubMed] [Google Scholar]
  17. Fascher K. D., Schmitz J., Hörz W. Role of trans-activating proteins in the generation of active chromatin at the PHO5 promoter in S. cerevisiae. EMBO J. 1990 Aug;9(8):2523–2528. doi: 10.1002/j.1460-2075.1990.tb07432.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Fascher K. D., Schmitz J., Hörz W. Structural and functional requirements for the chromatin transition at the PHO5 promoter in Saccharomyces cerevisiae upon PHO5 activation. J Mol Biol. 1993 Jun 5;231(3):658–667. doi: 10.1006/jmbi.1993.1317. [DOI] [PubMed] [Google Scholar]
  19. 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]
  20. 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]
  21. Fernandes M., Xiao H., Lis J. T. Binding of heat shock factor to and transcriptional activation of heat shock genes in Drosophila. Nucleic Acids Res. 1995 Dec 11;23(23):4799–4804. doi: 10.1093/nar/23.23.4799. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Fernandes M., Xiao H., Lis J. T. Fine structure analyses of the Drosophila and Saccharomyces heat shock factor--heat shock element interactions. Nucleic Acids Res. 1994 Jan 25;22(2):167–173. doi: 10.1093/nar/22.2.167. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Giardina C., Lis J. T. Dynamic protein-DNA architecture of a yeast heat shock promoter. Mol Cell Biol. 1995 May;15(5):2737–2744. doi: 10.1128/mcb.15.5.2737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Goodson M. L., Sarge K. D. Heat-inducible DNA binding of purified heat shock transcription factor 1. J Biol Chem. 1995 Feb 10;270(6):2447–2450. doi: 10.1074/jbc.270.6.2447. [DOI] [PubMed] [Google Scholar]
  25. Gross D. S., Adams C. C., Lee S., Stentz B. A critical role for heat shock transcription factor in establishing a nucleosome-free region over the TATA-initiation site of the yeast HSP82 heat shock gene. EMBO J. 1993 Oct;12(10):3931–3945. doi: 10.1002/j.1460-2075.1993.tb06071.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Gross D. S., English K. E., Collins K. W., Lee S. W. Genomic footprinting of the yeast HSP82 promoter reveals marked distortion of the DNA helix and constitutive occupancy of heat shock and TATA elements. J Mol Biol. 1990 Dec 5;216(3):611–631. doi: 10.1016/0022-2836(90)90387-2. [DOI] [PubMed] [Google Scholar]
  27. Gross D. S., Garrard W. T. Nuclease hypersensitive sites in chromatin. Annu Rev Biochem. 1988;57:159–197. doi: 10.1146/annurev.bi.57.070188.001111. [DOI] [PubMed] [Google Scholar]
  28. Grunstein M. Histone function in transcription. Annu Rev Cell Biol. 1990;6:643–678. doi: 10.1146/annurev.cb.06.110190.003235. [DOI] [PubMed] [Google Scholar]
  29. Hirschhorn J. N., Brown S. A., Clark C. D., Winston F. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 1992 Dec;6(12A):2288–2298. doi: 10.1101/gad.6.12a.2288. [DOI] [PubMed] [Google Scholar]
  30. Jakobsen B. K., Pelham H. R. Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol. 1988 Nov;8(11):5040–5042. doi: 10.1128/mcb.8.11.5040. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Jenuwein T., Forrester W. C., Qiu R. G., Grosschedl R. The immunoglobulin mu enhancer core establishes local factor access in nuclear chromatin independent of transcriptional stimulation. Genes Dev. 1993 Oct;7(10):2016–2032. doi: 10.1101/gad.7.10.2016. [DOI] [PubMed] [Google Scholar]
  32. Kim J. L., Nikolov D. B., Burley S. K. Co-crystal structure of TBP recognizing the minor groove of a TATA element. Nature. 1993 Oct 7;365(6446):520–527. doi: 10.1038/365520a0. [DOI] [PubMed] [Google Scholar]
  33. Kingston R. E., Bunker C. A., Imbalzano A. N. Repression and activation by multiprotein complexes that alter chromatin structure. Genes Dev. 1996 Apr 15;10(8):905–920. doi: 10.1101/gad.10.8.905. [DOI] [PubMed] [Google Scholar]
  34. Klages N., Strubin M. Stimulation of RNA polymerase II transcription initiation by recruitment of TBP in vivo. Nature. 1995 Apr 27;374(6525):822–823. doi: 10.1038/374822a0. [DOI] [PubMed] [Google Scholar]
  35. Klein C., Struhl K. Increased recruitment of TATA-binding protein to the promoter by transcriptional activation domains in vivo. Science. 1994 Oct 14;266(5183):280–282. doi: 10.1126/science.7939664. [DOI] [PubMed] [Google Scholar]
  36. Knezetic J. A., Luse D. S. The presence of nucleosomes on a DNA template prevents initiation by RNA polymerase II in vitro. Cell. 1986 Apr 11;45(1):95–104. doi: 10.1016/0092-8674(86)90541-6. [DOI] [PubMed] [Google Scholar]
  37. Kornberg R. D., Lorch Y. Irresistible force meets immovable object: transcription and the nucleosome. Cell. 1991 Nov 29;67(5):833–836. doi: 10.1016/0092-8674(91)90354-2. [DOI] [PubMed] [Google Scholar]
  38. Kurtz S., Rossi J., Petko L., Lindquist S. An ancient developmental induction: heat-shock proteins induced in sporulation and oogenesis. Science. 1986 Mar 7;231(4742):1154–1157. doi: 10.1126/science.3511530. [DOI] [PubMed] [Google Scholar]
  39. Landsberger N., Wolffe A. P. Role of chromatin and Xenopus laevis heat shock transcription factor in regulation of transcription from the X. laevis hsp70 promoter in vivo. Mol Cell Biol. 1995 Nov;15(11):6013–6024. doi: 10.1128/mcb.15.11.6013. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. 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]
  41. Lee M. S., Garrard W. T. Uncoupling gene activity from chromatin structure: promoter mutations can inactivate transcription of the yeast HSP82 gene without eliminating nucleosome-free regions. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9166–9170. doi: 10.1073/pnas.89.19.9166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lee S., Gross D. S. Conditional silencing: the HMRE mating-type silencer exerts a rapidly reversible position effect on the yeast HSP82 heat shock gene. Mol Cell Biol. 1993 Feb;13(2):727–738. doi: 10.1128/mcb.13.2.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Liaw P. C., Brandl C. J. Defining the sequence specificity of the Saccharomyces cerevisiae DNA binding protein REB1p by selecting binding sites from random-sequence oligonucleotides. Yeast. 1994 Jun;10(6):771–787. doi: 10.1002/yea.320100608. [DOI] [PubMed] [Google Scholar]
  44. Lis J., Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell. 1993 Jul 16;74(1):1–4. doi: 10.1016/0092-8674(93)90286-y. [DOI] [PubMed] [Google Scholar]
  45. Lorch Y., LaPointe J. W., Kornberg R. D. Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones. Cell. 1987 Apr 24;49(2):203–210. doi: 10.1016/0092-8674(87)90561-7. [DOI] [PubMed] [Google Scholar]
  46. Lu Q., Wallrath L. L., Allan B. D., Glaser R. L., Lis J. T., Elgin S. C. Promoter sequence containing (CT)n.(GA)n repeats is critical for the formation of the DNase I hypersensitive sites in the Drosophila hsp26 gene. J Mol Biol. 1992 Jun 20;225(4):985–998. doi: 10.1016/0022-2836(92)90099-6. [DOI] [PubMed] [Google Scholar]
  47. Lu Q., Wallrath L. L., Emanuel P. A., Elgin S. C., Gilmour D. S. Insensitivity of the present hsp26 chromatin structure to a TATA box mutation in Drosophila. J Biol Chem. 1994 Jun 3;269(22):15906–15911. [PubMed] [Google Scholar]
  48. 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]
  49. Luche R. M., Sumrada R., Cooper T. G. A cis-acting element present in multiple genes serves as a repressor protein binding site for the yeast CAR1 gene. Mol Cell Biol. 1990 Aug;10(8):3884–3895. doi: 10.1128/mcb.10.8.3884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. McDaniel D., Caplan A. J., Lee M. S., Adams C. C., Fishel B. R., Gross D. S., Garrard W. T. Basal-level expression of the yeast HSP82 gene requires a heat shock regulatory element. Mol Cell Biol. 1989 Nov;9(11):4789–4798. doi: 10.1128/mcb.9.11.4789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Mitchell A. P. Control of meiotic gene expression in Saccharomyces cerevisiae. Microbiol Rev. 1994 Mar;58(1):56–70. doi: 10.1128/mr.58.1.56-70.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Morrow B. E., Ju Q., Warner J. R. A bipartite DNA-binding domain in yeast Reb1p. Mol Cell Biol. 1993 Feb;13(2):1173–1182. doi: 10.1128/mcb.13.2.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Morse R. H. Nucleosome disruption by transcription factor binding in yeast. Science. 1993 Dec 3;262(5139):1563–1566. doi: 10.1126/science.8248805. [DOI] [PubMed] [Google Scholar]
  54. Park H. O., Craig E. A. Positive and negative regulation of basal expression of a yeast HSP70 gene. Mol Cell Biol. 1989 May;9(5):2025–2033. doi: 10.1128/mcb.9.5.2025. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Pazin M. J., Kamakaka R. T., Kadonaga J. T. ATP-dependent nucleosome reconfiguration and transcriptional activation from preassembled chromatin templates. Science. 1994 Dec 23;266(5193):2007–2011. doi: 10.1126/science.7801129. [DOI] [PubMed] [Google Scholar]
  56. Pederson D. S., Fidrych T. Heat shock factor can activate transcription while bound to nucleosomal DNA in Saccharomyces cerevisiae. Mol Cell Biol. 1994 Jan;14(1):189–199. doi: 10.1128/mcb.14.1.189. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Peterson C. L., Tamkun J. W. The SWI-SNF complex: a chromatin remodeling machine? Trends Biochem Sci. 1995 Apr;20(4):143–146. doi: 10.1016/s0968-0004(00)88990-2. [DOI] [PubMed] [Google Scholar]
  58. Poon D., Bai Y., Campbell A. M., Bjorklund S., Kim Y. J., Zhou S., Kornberg R. D., Weil P. A. Identification and characterization of a TFIID-like multiprotein complex from Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8224–8228. doi: 10.1073/pnas.92.18.8224. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Prioleau M. N., Huet J., Sentenac A., Méchali M. Competition between chromatin and transcription complex assembly regulates gene expression during early development. Cell. 1994 May 6;77(3):439–449. doi: 10.1016/0092-8674(94)90158-9. [DOI] [PubMed] [Google Scholar]
  60. Shopland L. S., Hirayoshi K., Fernandes M., Lis J. T. HSF access to heat shock elements in vivo depends critically on promoter architecture defined by GAGA factor, TFIID, and RNA polymerase II binding sites. Genes Dev. 1995 Nov 15;9(22):2756–2769. doi: 10.1101/gad.9.22.2756. [DOI] [PubMed] [Google Scholar]
  61. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Sorger P. K., Lewis M. J., Pelham H. R. Heat shock factor is regulated differently in yeast and HeLa cells. Nature. 1987 Sep 3;329(6134):81–84. doi: 10.1038/329081a0. [DOI] [PubMed] [Google Scholar]
  63. Sorger P. K., Nelson H. C. Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell. 1989 Dec 1;59(5):807–813. doi: 10.1016/0092-8674(89)90604-1. [DOI] [PubMed] [Google Scholar]
  64. 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]
  65. Sumrada R. A., Cooper T. G. Ubiquitous upstream repression sequences control activation of the inducible arginase gene in yeast. Proc Natl Acad Sci U S A. 1987 Jun;84(12):3997–4001. doi: 10.1073/pnas.84.12.3997. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Szent-Gyorgyi C. A bipartite operator interacts with a heat shock element to mediate early meiotic induction of Saccharomyces cerevisiae HSP82. Mol Cell Biol. 1995 Dec;15(12):6754–6769. doi: 10.1128/mcb.15.12.6754. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. 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]
  68. Tjian R., Maniatis T. Transcriptional activation: a complex puzzle with few easy pieces. Cell. 1994 Apr 8;77(1):5–8. doi: 10.1016/0092-8674(94)90227-5. [DOI] [PubMed] [Google Scholar]
  69. 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]
  70. 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]
  71. 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]
  72. Werner-Washburne M., Becker J., Kosic-Smithers J., Craig E. A. Yeast Hsp70 RNA levels vary in response to the physiological status of the cell. J Bacteriol. 1989 May;171(5):2680–2688. doi: 10.1128/jb.171.5.2680-2688.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. 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]
  74. Workman J. L., Buchman A. R. Multiple functions of nucleosomes and regulatory factors in transcription. Trends Biochem Sci. 1993 Mar;18(3):90–95. doi: 10.1016/0968-0004(93)90160-o. [DOI] [PubMed] [Google Scholar]
  75. Workman J. L., Roeder R. G. Binding of transcription factor TFIID to the major late promoter during in vitro nucleosome assembly potentiates subsequent initiation by RNA polymerase II. Cell. 1987 Nov 20;51(4):613–622. doi: 10.1016/0092-8674(87)90130-9. [DOI] [PubMed] [Google Scholar]
  76. Workman J. L., Roeder R. G., Kingston R. E. An upstream transcription factor, USF (MLTF), facilitates the formation of preinitiation complexes during in vitro chromatin assembly. EMBO J. 1990 Apr;9(4):1299–1308. doi: 10.1002/j.1460-2075.1990.tb08239.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Xiao H., Friesen J. D., Lis J. T. Recruiting TATA-binding protein to a promoter: transcriptional activation without an upstream activator. Mol Cell Biol. 1995 Oct;15(10):5757–5761. doi: 10.1128/mcb.15.10.5757. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Molecular and Cellular Biology are provided here courtesy of Taylor & Francis

RESOURCES