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Two chromatin remodeling activities cooperate during activation of hormone responsive promoters.

ABSTRACT: Steroid hormones regulate gene expression by interaction of their receptors with hormone responsive elements (HREs) and recruitment of kinases, chromatin remodeling complexes, and coregulators to their target promoters. Here we show that in breast cancer cells the BAF, but not the closely related PBAF complex, is required for progesterone induction of several target genes including MMTV, where it catalyzes localized displacement of histones H2A and H2B and subsequent NF1 binding. PCAF is also needed for induction of progesterone target genes and acetylates histone H3 at K14, an epigenetic mark that interacts with the BAF subunits by anchoring the complex to chromatin. In the absence of PCAF, full loading of target promoters with hormone receptors and BAF is precluded, and induction is compromised. Thus, activation of hormone-responsive promoters requires cooperation of at least two chromatin remodeling activities, BAF and PCAF.

SUBMITTER: Vicent GP

PROVIDER: S-EPMC2704372 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Two chromatin remodeling activities cooperate during activation of hormone responsive promoters.

Vicent Guillermo Pablo GP Zaurin Roser R Nacht A Silvina AS Li Ang A Font-Mateu Jofre J Le Dily Francois F Vermeulen Michiel M Mann Matthias M Beato Miguel M

PLoS genetics 20090717 7

Steroid hormones regulate gene expression by interaction of their receptors with hormone responsive elements (HREs) and recruitment of kinases, chromatin remodeling complexes, and coregulators to their target promoters. Here we show that in breast cancer cells the BAF, but not the closely related PBAF complex, is required for progesterone induction of several target genes including MMTV, where it catalyzes localized displacement of histones H2A and H2B and subsequent NF1 binding. PCAF is also ne ...[more]

PMID: 19609353

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Project description:Many of the physiological actions of GH are mediated by IGF-I, a secreted 70-residue peptide whose gene expression is induced by GH in the liver and other tissues via mechanisms that remain incompletely characterized but depend on the transcription factor Stat5b. Here we investigate the chromatin landscape of the IGF-I gene in the liver of pituitary-deficient young adult male rats and assess the impact of a single systemic GH injection. Despite minimal ongoing transcription in the absence of GH, both IGF-I promoters appear to reside in open chromatin environments, at least as inferred from relatively high levels of acetylation of core histones H3 and H4 when compared with adjacent intergenic DNA and from enhanced trimethylation of histone H3 at lysine 4. This landscape of open chromatin may reflect maturation of the liver. Surprisingly, in the absence of hormone, IGF-I promoter 1 appears poised to be activated, as evidenced by the presence of the transcriptional coactivator p300 and recruitment of RNA polymerase (Pol) II into a preinitiation complex. By contrast, chromatin surrounding IGF-I promoter 2 is devoid of both p300 and RNA Pol II. Systemic GH treatment causes an approximately 15-fold increase in transcription from each IGF-I promoter within 60 min of hormone administration, leading to a sustained accumulation of IGF-I mRNA. The coordinated induction of both IGF-I promoters by GH is accompanied by hyperacetylation of histones H3 and H4 in promoter-associated chromatin, a decline in monomethylation at lysine 4 of histone H3, and recruitment of RNA Pol II to IGF-I promoter 2. We conclude that GH actions induce rapid and dramatic changes in hepatic chromatin at the IGF-I locus and activate IGF-I gene transcription in the liver by distinct promoter-specific mechanisms: at promoter 1, GH causes RNA Pol II to be released from a previously recruited paused preinitiation complex, whereas at promoter 2, hormone treatment facilitates recruitment and then activation of RNA Pol II to initiate transcription.

Project description:Nitrate is the main source of nitrogen for plants and an essential component of fertilizers. Rapid transcriptional activation of genes encoding the high-affinity nitrate transport system (HATS) is an important strategy that plants use to cope with nitrogen deficiency. However, the specific transcriptional machineries involved in this process and the detailed transcriptional regulatory mechanism of the core HATS remain poorly understood. ZmCHB101 is the core subunit of the SWI/SNF-type ATP-dependent chromatin remodeling complex in maize. RNA-interference transgenic plants (ZmCHB101-RNAi) display abaxially curling leaves and impaired tassel and cob development. Here, we demonstrate that ZmCHB101 plays a pivotal regulatory role in nitrate-responsive gene expression. ZmCHB101-RNAi lines showed accelerated root growth and increased biomass under low nitrate conditions. An RNA sequencing analysis revealed that ZmCHB101 regulates the expression of genes involved in nitrate transport, including ZmNRT2.1 and ZmNRT2.2. The NIN-like protein (NLP) of maize, ZmNLP3.1, recognized the consensus nitrate-responsive cis-elements (NREs) in the promoter regions of ZmNRT2.1 and ZmNRT2.2, and activated the transcription of these genes in response to nitrate. Intriguingly, well-positioned nucleosomes were detected at NREs in the ZmNRT2.1 and ZmNRT2.2 gene promoters, and nucleosome densities were lower in ZmCHB101-RNAi lines than in wild-type plants, both in the absence and presence of nitrate. The ZmCHB101 protein bound to NREs and was involved in the maintenance of nucleosome occupancies at these sites, which may impact the binding of ZmNLP3.1 to NREs in the absence of nitrate. However, in the presence of nitrate, the binding affinity of ZmCHB101 for NREs decreased dramatically, leading to reduced nucleosome density at NREs and consequently increased ZmNLP3.1 binding. Our results provide novel insights into the role of chromatin remodeling proteins in the regulation of nitrate-responsive gene expression in plants.

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Two chromatin remodeling activities cooperate during activation of hormone responsive promoters.

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Two chromatin remodeling activities cooperate during activation of hormone responsive promoters.

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