Glucocorticoid receptor-glucocorticoid response element binding stimulates nucleosome disruption by the SWI/SNF complex

The organization of DNA in chromatin is involved in repressing basal transcription of a number of inducible genes. Biochemically defined multiprotein complexes such as SWI/SNF (J. Côté, J. Quinn, J. L. Workman, and C. L. Peterson, Science 265:53-60, 1994) and nucleosome remodeling factor (T. Tsukiyama and C. Wu, Cell 83:1011-1020, 1995) disrupt nucleosomes in vitro and are thus candidates for complexes which cause chromatin decondensation during gene induction. In this study we show that the glucocorticoid receptor (GR), a hormone-inducible transcription factor, stimulates the nucleosome-disrupting activity of the SWI/SNF complex partially purified either from HeLa cells or from rat liver tissue. This GR-mediated stimulation of SWI/SNF nucleosome disruption depended on the presence of a glucocorticoid response element. The in vitro-reconstituted nucleosome probes used in these experiments harbored 95 bp of synthetic DNA-bending sequence in order to rotationally position the DNA. The GR-dependent stimulation of SWI/SNF-mediated nucleosome disruption, as evaluated by DNase I footprinting, was 2.7- to 3.8-fold for the human SWI/SNF complex and 2.5- to 3.2-fold for the rat SWI/SNF complex. When nuclear factor 1 (NF1) was used instead of GR, there was no stimulation of SWI/SNF activity in the presence of a mononucleosome containing an NF1 binding site. On the other hand, the SWI/SNF nucleosome disruption activity increased the access of NF1 for its nucleosomal binding site. No such effect was seen on binding of GR to its response element. Our results suggest that GR, but not NF1, is able to target the nucleosome-disrupting activity of the SWI/SNF complex.

[1]  M. Scott,et al.  The Drosophila snr1 and brm proteins are related to yeast SWI/SNF proteins and are components of a large protein complex. , 1995, Molecular biology of the cell.

[2]  M. Yaniv,et al.  A human homologue of Saccharomyces cerevisiae SNF2/SWI2 and Drosophila brm genes potentiates transcriptional activation by the glucocorticoid receptor. , 1993, The EMBO journal.

[3]  R. Kornberg,et al.  Nucleosomes inhibit the initiation of transcription but allow chain elongation with the displacement of histones , 1987, Cell.

[4]  Thomas C. Kaufman,et al.  brahma: A regulator of Drosophila homeotic genes structurally related to the yeast transcriptional activator SNF2 SWI2 , 1992, Cell.

[5]  M. Beato,et al.  Nucleosome positioning modulates accessibility of regulatory proteins to the mouse mammary tumor virus promoter , 1990, Cell.

[6]  H. Richard-Foy,et al.  Glucocorticoids locally disrupt an array of positioned nucleosomes on the rat tyrosine aminotransferase promoter in hepatoma cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[7]  J. Workman,et al.  Stimulation of GAL4 derivative binding to nucleosomal DNA by the yeast SWI/SNF complex. , 1994, Science.

[8]  J. Schmitz,et al.  Structural and functional requirements for the chromatin transition at the PHO5 promoter in Saccharomyces cerevisiae upon PHO5 activation. , 1993, Journal of molecular biology.

[9]  G. Hager,et al.  Transcription factor access is mediated by accurately positioned nucleosomes on the mouse mammary tumor virus promoter , 1991, Molecular and cellular biology.

[10]  O. Wrange,et al.  Accessibility of a glucocorticoid response element in a nucleosome depends on its rotational positioning , 1995, Molecular and cellular biology.

[11]  T. Perlmann,et al.  Specific glucocorticoid receptor binding to DNA reconstituted in a nucleosome. , 1988, The EMBO journal.

[12]  Paul A. Khavari,et al.  BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription , 1993, Nature.

[13]  H. Chiba,et al.  Two human homologues of Saccharomyces cerevisiae SWI2/SNF2 and Drosophila brahma are transcriptional coactivators cooperating with the estrogen receptor and the retinoic acid receptor. , 1994, Nucleic acids research.

[14]  B. Gloss,et al.  Cooperativity of glucocorticoid response elements located far upstream of the tyrosine aminotransferase gene , 1987, Cell.

[15]  A. Wolffe,et al.  Nucleosome positioning and modification: chromatin structures that potentiate transcription. , 1994, Trends in biochemical sciences.

[16]  H. Richard-Foy,et al.  Sequence‐specific positioning of nucleosomes over the steroid‐inducible MMTV promoter. , 1987, The EMBO journal.

[17]  J. Workman,et al.  Persistent Site-Specific Remodeling of a Nucleosome Array by Transient Action of the SWI/SNF Complex , 1996, Science.

[18]  C. Peterson Multiple SWItches to turn on chromatin? , 1996, Current opinion in genetics & development.

[19]  Steven A. Brown,et al.  Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. , 1992, Genes & development.

[20]  D. S. Gross,et al.  Nuclease hypersensitive sites in chromatin. , 1988, Annual review of biochemistry.

[21]  A. Reik,et al.  Glucocorticoids are required for establishment and maintenance of an alteration in chromatin structure: induction leads to a reversible disruption of nucleosomes over an enhancer. , 1991, The EMBO journal.

[22]  Carl Wu,et al.  Purification and properties of an ATP-dependent nucleosome remodeling factor , 1995, Cell.

[23]  Michael R. Green,et al.  Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex , 1994, Nature.

[24]  J. T. Kadonaga,et al.  Role of chromatin structure in the regulation of transcription by RNA polymerase II. , 1993, Current opinion in cell biology.

[25]  R. Sandaltzopoulos,et al.  Chromatin remodeling by GAGA factor and heat shock factor at the hypersensitive Drosophila hsp26 promoter in vitro. , 1995, The EMBO journal.

[26]  M. Grunstein Histone function in transcription. , 1990, Annual review of cell biology.

[27]  M. Scott,et al.  Five SWI/SNF gene products are components of a large multisubunit complex required for transcriptional enhancement. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. Workman,et al.  Transcriptional regulation by the immediate early protein of pseudorabies virus during in vitro nucleosome assembly , 1988, Cell.

[29]  I. Herskowitz,et al.  Roles of SWI1, SWI2, and SWI3 proteins for transcriptional enhancement by steroid receptors. , 1992, Science.

[30]  K. Yamamoto,et al.  Crystallographic analysis of the interaction of the glucocorticoid receptor with DNA , 2003, Nature.

[31]  U. Schibler,et al.  Tissue-specific in vitro transcription from the mouse albumin promoter , 1986, Cell.

[32]  G. Crabtree,et al.  brg1: a putative murine homologue of the Drosophila brahma gene, a homeotic gene regulator. , 1994, Developmental biology.

[33]  Jerry L. Workman,et al.  Nucleosome displacement in transcription , 1993, Cell.

[34]  R. Losa,et al.  A bacteriophage RNA polymerase transcribes in vitro through a nucleosome core without displacing it , 1987, Cell.

[35]  A. Wolffe,et al.  Replication-coupled chromatin assembly is required for the repression of basal transcription in vivo. , 1993, Genes & development.

[36]  Qiao Li,et al.  The Affinity of Nuclear Factor 1 for Its DNA Site Is Drastically Reduced by Nucleosome Organization Irrespective of Its Rotational or Translational Position (*) , 1996, The Journal of Biological Chemistry.

[37]  M. Yaniv,et al.  Purification and biochemical heterogeneity of the mammalian SWI‐SNF complex. , 1996, The EMBO journal.

[38]  M. A. Shea,et al.  Quantitative DNase footprint titration: a method for studying protein-DNA interactions. , 1986, Methods in enzymology.

[39]  M. Carlson,et al.  The SNF/SWI family of global transcriptional activators. , 1994, Current opinion in cell biology.

[40]  C. McCallum,et al.  Identification and characterization of Drosophila relatives of the yeast transcriptional activator SNF2/SWI2 , 1994, Molecular and cellular biology.

[41]  J. T. Kadonaga,et al.  Role of nucleosomal cores and histone H1 in regulation of transcription by RNA polymerase II. , 1991, Science.

[42]  B. O’Malley,et al.  Modulation of progesterone receptor binding to progesterone response elements by positioned nucleosomes. , 1992, Biochemistry.

[43]  I. Herskowitz,et al.  Characterization of the yeast SWI1, SWI2, and SWI3 genes, which encode a global activator of transcription , 1992, Cell.

[44]  J. Whitlock,et al.  Dioxin induces localized, graded changes in chromatin structure: implications for Cyp1A1 gene transcription , 1995, Molecular and cellular biology.

[45]  O. Wrange,et al.  Translational positioning of a nucleosomal glucocorticoid response element modulates glucocorticoid receptor affinity. , 1993, Genes & development.

[46]  R. Simpson,et al.  Nucleosome positioning: occurrence, mechanisms, and functional consequences. , 1991, Progress in nucleic acid research and molecular biology.

[47]  Toshio Tsukiyama,et al.  ISWI, a member of the SWl2/SNF2 ATPase family, encodes the 140 kDa subunit of the nucleosome remodeling factor , 1995, Cell.

[48]  L. Lutter Kinetic analysis of deoxyribonuclease I cleavages in the nucleosome core: evidence for a DNA superhelix. , 1978, Journal of molecular biology.

[49]  Michael R. Green,et al.  Facilitated binding of TATA-binding protein to nucleosomal DNA , 1994, Nature.

[50]  Keith R. Yamamoto,et al.  Reversible and persistent changes in chromatin structure accompany activation of a glucocorticoid-dependent enhancer element , 1984, Cell.

[51]  Donald F. Senear,et al.  [9] Quantitative DNase footprint titration: A method for studying protein-DNA interactions , 1986 .

[52]  B. Cairns,et al.  A multisubunit complex containing the SWI1/ADR6, SWI2/SNF2, SWI3, SNF5, and SNF6 gene products isolated from yeast. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[53]  A. Wolffe,et al.  Disruption of Reconstituted Nucleosomes , 1995, The Journal of Biological Chemistry.

[54]  D M Crothers,et al.  Artificial nucleosome positioning sequences. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[55]  J. Whitlock,et al.  Transcription-dependent and transcription-independent nucleosome disruption induced by dioxin. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[56]  M. Grunstein,et al.  Nucleosome loss activates CUP1 and HIS3 promoters to fully induced levels in the yeast Saccharomyces cerevisiae , 1992, Molecular and cellular biology.

[57]  R. Cortese,et al.  Amino‐terminal domain of NF1 binds to DNA as a dimer and activates adenovirus DNA replication. , 1990, The EMBO journal.

[58]  R. Young,et al.  RNA Polymerase II Holoenzyme Contains SWI/SNF Regulators Involved in Chromatin Remodeling , 1996, Cell.

[59]  G. Hager,et al.  Steroid-dependent interaction of transcription factors with the inducible promoter of mouse mammary tumor virus in vivo , 1987, Cell.

[60]  Craig L. Peterson,et al.  DNA-binding properties of the yeast SWI/SNF complex , 1996, Nature.

[61]  I. Herskowitz,et al.  A negative regulator of HO transcription, SIN1 (SPT2), is a nonspecific DNA-binding protein related to HMG1 , 1991, Molecular and cellular biology.

[62]  F. Winston,et al.  Evidence That Spt6p Controls Chromatin Structure by a Direct Interaction with Histones , 1996, Science.

[63]  A. Wolffe,et al.  The amino-terminal tails of the core histones and the translational position of the TATA box determine TBP/TFIIA association with nucleosomal DNA. , 1995, Nucleic acids research.

[64]  Alan P. Wolffe,et al.  Transcription: In tune with the histones , 1994, Cell.

[65]  M. Carlson,et al.  Functional interdependence of the yeast SNF2, SNF5, and SNF6 proteins in transcriptional activation. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[66]  B. O’Malley,et al.  Transactivation functions facilitate the disruption of chromatin structure by estrogen receptor derivatives in vivo. , 1991, The Journal of biological chemistry.