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Mol Cell Biol. Nov 1995; 15(11): 6013–6024.
PMCID: PMC230853

Role of chromatin and Xenopus laevis heat shock transcription factor in regulation of transcription from the X. laevis hsp70 promoter in vivo.


Xenopus laevis oocytes activate transcription from the Xenopus hsp70 promoter within a chromatin template in response to heat shock. Expression of exogenous Xenopus heat shock transcription factor 1 (XHSF1) causes the activation of the wild-type hsp70 promoter within chromatin. XHSF1 activates transcription at normal growth temperatures (18 degrees C), but heat shock (34 degrees C) facilitates transcriptional activation. Titration of chromatin in vivo leads to constitutive transcription from the wild-type hsp70 promoter. The Y box elements within the hsp70 promoter facilitate transcription in the presence or absence of chromatin. The presence of the Y box elements prevents the assembly of canonical nucleosomal arrays over the promoter and facilitates transcription. In a mutant hsp70 promoter lacking Y boxes, exogenous XHSF1 activates transcription from a chromatin template much more efficiently under heat shock conditions. Activation of transcription from the mutant promoter by exogenous XHSF1 correlates with the disappearance of a canonical nucleosomal array over the promoter. Chromatin structure on a mutant hsp70 promoter lacking Y boxes can restrict XHSF1 access; however, on both mutant and wild-type promoters, chromatin assembly can also restrict the function of the basal transcriptional machinery. We suggest that chromatin assembly has a physiological role in establishing a transcriptionally repressed state on the Xenopus hsp70 promoter in vivo.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Adams CC, Workman JL. Binding of disparate transcriptional activators to nucleosomal DNA is inherently cooperative. Mol Cell Biol. 1995 Mar;15(3):1405–1421. [PMC free article] [PubMed]
  • Almouzni G, Méchali M, Wolffe AP. Competition between transcription complex assembly and chromatin assembly on replicating DNA. EMBO J. 1990 Feb;9(2):573–582. [PMC free article] [PubMed]
  • Almouzni G, Wolffe AP. Replication-coupled chromatin assembly is required for the repression of basal transcription in vivo. Genes Dev. 1993 Oct;7(10):2033–2047. [PubMed]
  • Almouzni G, Wolffe AP. Constraints on transcriptional activator function contribute to transcriptional quiescence during early Xenopus embryogenesis. EMBO J. 1995 Apr 18;14(8):1752–1765. [PMC free article] [PubMed]
  • Baxevanis AD, Arents G, Moudrianakis EN, Landsman D. A variety of DNA-binding and multimeric proteins contain the histone fold motif. Nucleic Acids Res. 1995 Jul 25;23(14):2685–2691. [PMC free article] [PubMed]
  • Becker PB, Rabindran SK, 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. [PMC free article] [PubMed]
  • Becker PB, Wu C. Cell-free system for assembly of transcriptionally repressed chromatin from Drosophila embryos. Mol Cell Biol. 1992 May;12(5):2241–2249. [PMC free article] [PubMed]
  • Bienz M. Xenopus hsp 70 genes are constitutively expressed in injected oocytes. EMBO J. 1984 Nov;3(11):2477–2483. [PMC free article] [PubMed]
  • Bienz M. Developmental control of the heat shock response in Xenopus. Proc Natl Acad Sci U S A. 1984 May;81(10):3138–3142. [PMC free article] [PubMed]
  • Bienz M. A CCAAT box confers cell-type-specific regulation on the Xenopus hsp70 gene in oocytes. Cell. 1986 Sep 26;46(7):1037–1042. [PubMed]
  • Bienz M, Gurdon JB. The heat-shock response in Xenopus oocytes is controlled at the translational level. Cell. 1982 Jul;29(3):811–819. [PubMed]
  • Bienz M, Pelham HR. Heat shock regulatory elements function as an inducible enhancer in the Xenopus hsp70 gene and when linked to a heterologous promoter. Cell. 1986 Jun 6;45(5):753–760. [PubMed]
  • Cho H, Wolffe AP. Xenopus laevis B4, an intron-containing oocyte-specific linker histone-encoding gene. Gene. 1994 Jun 10;143(2):233–238. [PubMed]
  • Clos J, Westwood JT, Becker PB, 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. [PubMed]
  • Dingwall C, Allan J. Accumulation of the isolated carboxy-terminal domain of histone H1 in the Xenopus oocyte nucleus. EMBO J. 1984 Sep;3(9):1933–1937. [PMC free article] [PubMed]
  • Dorn A, Bollekens J, Staub A, Benoist C, Mathis D. A multiplicity of CCAAT box-binding proteins. Cell. 1987 Sep 11;50(6):863–872. [PubMed]
  • Evans JP, Kay BK. Biochemical fractionation of oocytes. Methods Cell Biol. 1991;36:133–148. [PubMed]
  • Gallo GJ, Schuetz TJ, Kingston RE. Regulation of heat shock factor in Schizosaccharomyces pombe more closely resembles regulation in mammals than in Saccharomyces cerevisiae. Mol Cell Biol. 1991 Jan;11(1):281–288. [PMC free article] [PubMed]
  • Gargiulo G, Razvi F, Ruberti I, Mohr I, Worcel A. Chromatin-specific hypersensitive sites are assembled on a Xenopus histone gene injected into Xenopus oocytes. J Mol Biol. 1985 Feb 5;181(3):333–349. [PubMed]
  • Gargiulo G, Worcel A. Analysis of the chromatin assembled in germinal vesicles of Xenopus oocytes. J Mol Biol. 1983 Nov 5;170(3):699–722. [PubMed]
  • Gariglio P, Buss J, Green MH. Sarkosyl activation of RNA polymerase activity in mitotic mouse cells. FEBS Lett. 1974 Aug 30;44(3):330–333. [PubMed]
  • Giardina C, Pérez-Riba M, Lis JT. Promoter melting and TFIID complexes on Drosophila genes in vivo. Genes Dev. 1992 Nov;6(11):2190–2200. [PubMed]
  • Gilmour DS, Lis JT. In vivo interactions of RNA polymerase II with genes of Drosophila melanogaster. Mol Cell Biol. 1985 Aug;5(8):2009–2018. [PMC free article] [PubMed]
  • Gilmour DS, Lis JT. RNA polymerase II interacts with the promoter region of the noninduced hsp70 gene in Drosophila melanogaster cells. Mol Cell Biol. 1986 Nov;6(11):3984–3989. [PMC free article] [PubMed]
  • Graves BJ, Johnson PF, McKnight SL. Homologous recognition of a promoter domain common to the MSV LTR and the HSV tk gene. Cell. 1986 Feb 28;44(4):565–576. [PubMed]
  • Gross DS, Adams CC, 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. [PMC free article] [PubMed]
  • Gross DS, English KE, Collins KW, Lee SW. 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. [PubMed]
  • Hayes J, Tullius TD, Wolffe AP. A protein-protein interaction is essential for stable complex formation on a 5 S RNA gene. J Biol Chem. 1989 Apr 15;264(11):6009–6012. [PubMed]
  • Heikkila JJ, Kloc M, Bury J, Schultz GA, Browder LW. Acquisition of the heat-shock response and thermotolerance during early development of Xenopus laevis. Dev Biol. 1985 Feb;107(2):483–489. [PubMed]
  • Hensold JO, Hunt CR, Calderwood SK, Housman DE, Kingston RE. DNA binding of heat shock factor to the heat shock element is insufficient for transcriptional activation in murine erythroleukemia cells. Mol Cell Biol. 1990 Apr;10(4):1600–1608. [PMC free article] [PubMed]
  • Hooft van Huijsduijnen R, Li XY, Black D, Matthes H, Benoist C, Mathis D. Co-evolution from yeast to mouse: cDNA cloning of the two NF-Y (CP-1/CBF) subunits. EMBO J. 1990 Oct;9(10):3119–3127. [PMC free article] [PubMed]
  • Horrell A, Shuttleworth J, Colman A. Transcript levels and translational control of hsp70 synthesis in Xenopus oocytes. Genes Dev. 1987 Jul;1(5):433–444. [PubMed]
  • Jakobsen BK, Pelham HR. Constitutive binding of yeast heat shock factor to DNA in vivo. Mol Cell Biol. 1988 Nov;8(11):5040–5042. [PMC free article] [PubMed]
  • Jurivich DA, Sistonen L, Kroes RA, Morimoto RI. Effect of sodium salicylate on the human heat shock response. Science. 1992 Mar 6;255(5049):1243–1245. [PubMed]
  • King ML, Davis R. Do Xenopus oocytes have a heat shock response? Dev Biol. 1987 Feb;119(2):532–539. [PubMed]
  • Landsberger N, Ranjan M, Almouzni G, Stump D, Wolffe AP. The heat shock response in Xenopus oocytes, embryos, and somatic cells: a regulatory role for chromatin. Dev Biol. 1995 Jul;170(1):62–74. [PubMed]
  • Lis J, Wu C. Protein traffic on the heat shock promoter: parking, stalling, and trucking along. Cell. 1993 Jul 16;74(1):1–4. [PubMed]
  • McNabb DS, Xing Y, Guarente L. Cloning of yeast HAP5: a novel subunit of a heterotrimeric complex required for CCAAT binding. Genes Dev. 1995 Jan 1;9(1):47–58. [PubMed]
  • Milos PM, Zaret KS. A ubiquitous factor is required for C/EBP-related proteins to form stable transcription complexes on an albumin promoter segment in vitro. Genes Dev. 1992 Jun;6(6):991–1004. [PubMed]
  • Morimoto RI. Cells in stress: transcriptional activation of heat shock genes. Science. 1993 Mar 5;259(5100):1409–1410. [PubMed]
  • O'Brien T, Lis JT. RNA polymerase II pauses at the 5' end of the transcriptionally induced Drosophila hsp70 gene. Mol Cell Biol. 1991 Oct;11(10):5285–5290. [PMC free article] [PubMed]
  • Olesen JT, Guarente L. The HAP2 subunit of yeast CCAAT transcriptional activator contains adjacent domains for subunit association and DNA recognition: model for the HAP2/3/4 complex. Genes Dev. 1990 Oct;4(10):1714–1729. [PubMed]
  • Ovsenek N, Heikkila JJ. DNA sequence-specific binding activity of the heat-shock transcription factor is heat-inducible before the midblastula transition of early Xenopus development. Development. 1990 Oct;110(2):427–433. [PubMed]
  • Pederson DS, 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. [PMC free article] [PubMed]
  • Perlmann T, Wrange O. Inhibition of chromatin assembly in Xenopus oocytes correlates with derepression of the mouse mammary tumor virus promoter. Mol Cell Biol. 1991 Oct;11(10):5259–5265. [PMC free article] [PubMed]
  • Rabindran SK, Giorgi G, Clos J, Wu C. Molecular cloning and expression of a human heat shock factor, HSF1. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6906–6910. [PMC free article] [PubMed]
  • Rabindran SK, Haroun RI, Clos J, Wisniewski J, Wu C. Regulation of heat shock factor trimer formation: role of a conserved leucine zipper. Science. 1993 Jan 8;259(5092):230–234. [PubMed]
  • Ranjan M, Tafuri SR, Wolffe AP. Masking mRNA from translation in somatic cells. Genes Dev. 1993 Sep;7(9):1725–1736. [PubMed]
  • Rougvie AE, Lis JT. The RNA polymerase II molecule at the 5' end of the uninduced hsp70 gene of D. melanogaster is transcriptionally engaged. Cell. 1988 Sep 9;54(6):795–804. [PubMed]
  • Ryoji M, Worcel A. Chromatin assembly in Xenopus oocytes: in vivo studies. Cell. 1984 May;37(1):21–32. [PubMed]
  • Sarge KD, Murphy SP, Morimoto RI. Activation of heat shock gene transcription by heat shock factor 1 involves oligomerization, acquisition of DNA-binding activity, and nuclear localization and can occur in the absence of stress. Mol Cell Biol. 1993 Mar;13(3):1392–1407. [PMC free article] [PubMed]
  • Schuetz TJ, Gallo GJ, Sheldon L, Tempst P, Kingston RE. Isolation of a cDNA for HSF2: evidence for two heat shock factor genes in humans. Proc Natl Acad Sci U S A. 1991 Aug 15;88(16):6911–6915. [PMC free article] [PubMed]
  • 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. [PMC free article] [PubMed]
  • Shimamura A, Tremethick D, Worcel A. Characterization of the repressed 5S DNA minichromosomes assembled in vitro with a high-speed supernatant of Xenopus laevis oocytes. Mol Cell Biol. 1988 Oct;8(10):4257–4269. [PMC free article] [PubMed]
  • Sinha S, Maity SN, Lu J, de Crombrugghe B. Recombinant rat CBF-C, the third subunit of CBF/NFY, allows formation of a protein-DNA complex with CBF-A and CBF-B and with yeast HAP2 and HAP3. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1624–1628. [PMC free article] [PubMed]
  • Sorger PK. Yeast heat shock factor contains separable transient and sustained response transcriptional activators. Cell. 1990 Aug 24;62(4):793–805. [PubMed]
  • Sorger PK, Nelson HC. Trimerization of a yeast transcriptional activator via a coiled-coil motif. Cell. 1989 Dec 1;59(5):807–813. [PubMed]
  • Sorger PK, Pelham HR. Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell. 1988 Sep 9;54(6):855–864. [PubMed]
  • Stump DG, Landsberger N, Wolffe AP. The cDNA encoding Xenopus laevis heat-shock factor 1 (XHSF1): nucleotide and deduced amino-acid sequences, and properties of the encoded protein. Gene. 1995 Jul 28;160(2):207–211. [PubMed]
  • Tafuri SR, Wolffe AP. Selective recruitment of masked maternal mRNA from messenger ribonucleoprotein particles containing FRGY2 (mRNP4). J Biol Chem. 1993 Nov 15;268(32):24255–24261. [PubMed]
  • Taylor IC, Workman JL, Schuetz TJ, Kingston RE. 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. [PubMed]
  • Toyoda T, Wolffe AP. In vitro transcription by RNA polymerase II in extracts of Xenopus oocytes, eggs, and somatic cells. Anal Biochem. 1992 Jun;203(2):340–347. [PubMed]
  • Tsukiyama T, Becker PB, 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. [PubMed]
  • Ura K, Hayes JJ, Wolffe AP. 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. [PMC free article] [PubMed]
  • Varga-Weisz PD, Blank TA, Becker PB. Energy-dependent chromatin accessibility and nucleosome mobility in a cell-free system. EMBO J. 1995 May 15;14(10):2209–2216. [PMC free article] [PubMed]
  • Wall G, Varga-Weisz PD, Sandaltzopoulos R, Becker PB. 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. [PMC free article] [PubMed]
  • Wolffe AP. Structural and functional properties of the evolutionarily ancient Y-box family of nucleic acid binding proteins. Bioessays. 1994 Apr;16(4):245–251. [PubMed]
  • Wolffe AP, Perlman AJ, Tata JR. Transient paralysis by heat shock of hormonal regulation of gene expression. EMBO J. 1984 Dec 1;3(12):2763–2770. [PMC free article] [PubMed]
  • Wolffe AP, Tafuri S, Ranjan M, Familari M. The Y-box factors: a family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biol. 1992 Apr;4(4):290–298. [PubMed]
  • Wright KL, Vilen BJ, Itoh-Lindstrom Y, Moore TL, Li G, Criscitiello M, Cogswell P, Clarke JB, Ting JP. CCAAT box binding protein NF-Y facilitates in vivo recruitment of upstream DNA binding transcription factors. EMBO J. 1994 Sep 1;13(17):4042–4053. [PMC free article] [PubMed]
  • Young D, Carroll D. Regular arrangement of nucleosomes on 5S rRNA genes in Xenopus laevis. Mol Cell Biol. 1983 Apr;3(4):720–730. [PMC free article] [PubMed]

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