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Originally published In Press as doi:10.1074/jbc.C700030200 on April 26, 2007

J. Biol. Chem., Vol. 282, Issue 24, 17335-17339, June 15, 2007
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Regulation of GREB1 Transcription by Estrogen Receptor {alpha} through a Multipartite Enhancer Spread Over 20 kb of Upstream Flanking Sequences*Formula

Julie Deschênes{ddagger}12, Véronique Bourdeau{ddagger}13, John H. White§4, and Sylvie Mader{ddagger}5

From the {ddagger}Institute for Research in Immunology and Cancer and Department of Biochemistry, Université de Montréal, Montréal, Québec H3C 3J7, Canada and the Departments of §Physiology and Medicine, McGill University, Montréal, Québec H3A 1A4, Canada

Received for publication, February 21, 2007 , and in revised form, April 24, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS AND DISCUSSION
 REFERENCES
 
Estrogen receptors activate transcription in part through direct interactions with specific DNA motifs, called estrogen response elements (EREs). Here we show that the strong and sustained induction of the gene regulated in breast cancer 1 (GREB1), a gene of unknown function that has been previously suggested to play a role in the effects of estradiol on breast cancer cell proliferation (Rae, J. M., Johnson, M. D., Scheys, J. O., Cordero, K. E., Larios, J. M., and Lippman, M. E. (2005) Breast Cancer Res. Treat 92, 141–149), is mediated by binding of estrogen receptor {alpha} (ER{alpha}) to three consensus EREs spread over ~20 kb of upstream flanking sequences. In addition to ER{alpha}, coactivator SRC-3, acetylated histones and phosphorylated RNA polymerase II (P-polII) were detected on all three EREs in the presence of estrogen, while basal recruitment of ER{alpha} and P-polII was observed only on the proximal element. Chromatin loops were formed between each ERE and the GREB1 transcriptional start site in the presence of estrogen but not of a total antiestrogen. Furthermore, estradiol induced physical association between EREs, suggesting that these elements function as a potent multipartite enhancer to regulate GREB1 transcription.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
EXPERIMENTAL PROCEDURES
 RESULTS AND DISCUSSION
 REFERENCES
 
Estrogens are steroid hormones that have pleiotropic physiological actions in numerous target tissues including the reproductive system (1–3) but also play an important role in cancers, in particular breast cancer (4, 5). Estrogens act through two receptors, ER{alpha}6 and ERbeta, members of the nuclear receptor superfamily of ligand-inducible transcription factors (6, 7). ER{alpha} is expressed or overexpressed in two-thirds of breast tumors (8), and blockade of estrogen signaling through antiestrogens, which are competitive inhibitors of ERs, is an effective treatment of the majority of ER{alpha}-positive breast tumors (9, 10). Functional genomic approaches have led to the identification of a variety of estrogen target genes in ER{alpha}-positive breast cancer cell lines (11–17). Some estrogen target genes, such as those encoding cyclin D1 (CCND1), c-myc (MYC), and E2F transcription factors have been shown to mediate the proliferative effects of estrogen in breast cancer cell lines (18–21). It has also been recently suggested that the gene regulated in breast cancer 1, GREB1 (22), whose function remains unknown, contributes to the growth-promoting effects of estrogens in MCF-7 cells (23).

ERs can bind to specific DNA motifs, called estrogen response elements (EREs) through a central conserved DNA binding domain (24). Consensus EREs, which were defined by compiling natural response elements in estrogen-responsive genes and correspond to the highest affinity binding site in vitro, are 15-bp palindromes composed of two PuGGTCA motifs spaced by 3 bp (25, 26). Although most high affinity EREs were initially characterized in the proximal regulatory sequences of target genes, recent studies have indicated that elements binding ER{alpha} can be found at large distances from transcriptional start sites (TSS). Our genome-wide mapping of high affinity EREs combined with characterization of elements by chromatin immunoprecipitation identified functional ER{alpha} binding sites up to 10 kb from TSS (27). In addition, genome-wide mapping of chromatin fragments bound by ER{alpha} revealed sites located much further from adjacent genes, and use of chromatin conformation capture (3C) assays showed that some of these elements can form chromatin loops with promoters located at distances of up to 100 kb (15, 17). Often, ER{alpha} binds several chromatin regions within this range of distances from the TSS of estrogen-regulated genes, raising the possibility of cooperativity between widely separated enhancer units for transcriptional regulation of target genes. This may result in the formation of multiple chromatin loops with the TSS of these target genes and possibly between enhancers themselves.

GREB1 stands out as an estrogen target gene because of the presence in its flanking region of three consensus EREs spread over 20 kb of upstream sequences. We have previously observed in vivo recruitment of ER{alpha} to the EREs present at –1.5 and –9.5 kb (27). Here we address whether the three GREB1 consensus EREs are functional enhancers that cooperate for transcriptional induction of the GREB1 gene by ER{alpha} and present evidence for a complex chromatin loop structure that implicates all three EREs and the TSS.


   EXPERIMENTAL PROCEDURES
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
RESULTS AND DISCUSSION
 REFERENCES
 
Cell Culture—MCF-7 breast carcinoma cells and Ishikawa cells were maintained in {alpha}-minimal Eagle's medium (Wisent, St-Bruno, Quebec, Canada) supplemented with 10% fetal bovine serum (FBS) (Sigma-Aldrich, Oakville, Ontario, Canada). ZR75 and T47D were maintained in RPMI-1640 (Wisent) supplemented with 10% FBS. MDA-MB-231::ER{alpha} cells were maintained in Dulbecco's modified Eagle's medium (DMEM) (Wisent) supplemented with 5% FBS with 0.15 mg/ml of hygromycin (Sigma). Three days before experiments, cells were switched to phenol red-free DMEM (Wisent) containing 10% charcoal-treated FBS (FBS-T), 1% sodium pyruvate (Wisent), 1% penicillin/streptomycin (Wisent), and 1% L-glutamine (Wisent). The day before hormonal stimulation, the medium was changed to phenol red-free DMEM supplemented with 0.5% charcoal-treated FBS. Cells were then treated with 17-beta-estradiol (E2, 25 nM, Sigma), ICI 182,780 (ICI, 100 nM, Tocris, Ellisville, MO) or vehicle (0.1% ethanol) for variable periods of time as indicated in the figure legends.

RNA Extraction—Cells were seeded in 10-cm plates (MCF-7, T47D, ZR75, MDA-MB-231::ER{alpha}) or 6-cm plates (Ishikawa) at a density such that near confluence was obtained at the end of the treatment. Cells were treated with 25 nM E2, 100 nM ICI 182,780, or vehicle (ethanol) for different times, as indicated in the figure legends. For pretreatments with actinomycin D (2 µg/ml) or cycloheximide (10 µg/ml), incubation was initiated 1 h before hormonal treatment. siGenome siRNAs were transfected according to the instructions of the manufacturer (Dharmacon, Chicago, IL), medium was changed 24 h after transfection and hormonal stimulations were initiated after another 24 h. At the end of the treatments, medium was removed, cells were collected in 1 ml of TRI Reagent (Sigma), and total RNA was extracted as recommended by the manufacturer.

Reverse Transcription and Real-time PCR—Total RNA (2 µg) was reverse transcribed using the RevertAid H first minus strand cDNA synthesis kit (MBI Fermentas, Burlington, Ontario, Canada) as recommended by the manufacturer. The reverse transcription product was diluted 10 times prior to real-time PCR. Each real-time PCR amplification reaction contained the reverse transcription dilution (2 µl), forward and reverse primers (150–300 nM), MgCl2 (3–4.5 mM according to primer pairs), dNTP (0.2 mM), SYBR Green (0.33x, Invitrogen, Burlington, Ontario, Canada), buffer for Jump Start Taq and Jump Start Taq (0.5 unit, Sigma) in a final volume of 20 µl. After denaturation at 95 °C for 7 min, samples went through a one-degree annealing temperature touchdown of 7 cycles starting from 60 °C (30 s at 95 °C, 30 s at annealing temperature, 30 s at 72 °C) followed by 40 cycles of amplification (30 s at 95 °C, 30 s at 58 °C and 30 s at 72 °C). A dissociation protocol followed the amplification program to characterize the amplified product(s). PCR was performed using a RotorGene 3000 (Corbett, Australia) and analyzed using expression levels of the p36b4 gene for normalization. For each set of primers, non-template control reactions were performed as a negative control. Each sample was assayed in triplicate and each experiment was reproduced at least two times. A typical experiment is shown. All primer pairs were designed using the Primer3 software and chosen to span an intron. The primer sequences and individual conditions used for polymerase chain reaction amplification are available upon request.

Western Blot Analysis—Whole cell extracts and blot analysis were performed as described previously (28) using anti-ER{alpha} mouse monoclonal (B10, kind gift from Prof. P. Chambon) and anti-beta-actin mouse monoclonal antibody (AC-15, Sigma Diagnostics).

Chromatin Immunoprecipitation—For chromatin immunoprecipitation (ChIP) assays, cells in phenol red-free DMEM containing 0.5% FBS-T were treated with vehicle (ethanol), E2 or ICI for 45 min. Chromatin was cross-linked by treating cells with 1.5% formaldehyde for 10 min at room temperature and fragmented by sonication as reported previously (27), yielding fragments of average size ~400 bp. Antibodies against ER{alpha} (SC-543), SRC-3 (SC-7217), or normal IgG (rabbit: SC-2027, goat: SC-2028; mouse: SC-2025) were purchased from Santa Cruz Biotechnology, Inc. (Santa Cruz, CA), and antibodies against phosphorylated polymerase II (05-623) or acetylated histone H4 (06-598) were purchased from Upstate%20Biotechnology">Upstate Biotechnology, Inc. (Chicago, IL). The sequences of the primers used in ChIP assays (Sigma Genosis) are available upon request. Chromatin immunoprecipitation experiments were performed at least two times with similar results. A representative set of results is shown.

3C Assays—3C assays were performed essentially as described (29), with only minor modifications. In short, 3 days prior to the experiment, MCF-7 cells were switched to phenol red-free DMEM containing 10% FBS-T and repeated for 48 h at 9 million cells per 15-cm Petri dish. The serum concentration was decreased to 0.5% 24 h before treatment with E2 (25 nM), ICI (100 nM), or vehicle (ethanol) for 45 min. Culture medium was removed, and cells were fixed with 1.5% formaldehyde for 10 min at room temperature. Cells were then washed twice with cold phosphate-buffered saline solution, collected in 500 µl of collection buffer (100 mM Tris-HCl, pH 9.4, 10 mM dithiothreitol, and protease inhibitor mixture), washed with cold phosphate-buffered saline, and resuspended in ice-cold lysis buffer (10 mM Tris-HCl, pH 8.0, 10 mM NaCl, 0.2% Nonidet P-40, and protease inhibitor mixture). Nuclei were resuspended in 2 ml of Tango 1.2x buffer (MBI Fermentas) supplemented with SDS. Triton X-100 was added to sequester the SDS. The cross-linked DNA was digested overnight with 400 units of restriction enzyme MspI or XceI (MBI Fermentas) and then with another 100 units for 2 h at 37 °C. The restriction enzyme was inactivated by addition of SDS and incubation at 65 °C. Genomic DNA concentrations were measured in 30-µl aliquots for standardization between samples. The reactions were diluted with ligase buffer (50 mM Tris-HCl, pH 7.5, 10 mM MgCl2, 10 mM dithiothreitol, 1 mM ATP, and 25 µg/ml bovine serum albumin), supplemented with Triton X-100 (1% final concentration), and incubated for 1 h at 37 °C. The DNA was ligated using T4 ligase (New England Biolabs, Ipswich, MA) overnight at 16 °C. RNase was added, and samples were incubated overnight at 65 °C to reverse the cross-links. The following day, samples were incubated for 2 h at 45 °C with proteinase K, and the DNA was purified by phenol-chloroform extractions and ethanol precipitation. Chromatin loop formation was assessed by PCR amplification carried out using similar conditions as for real-time-PCR amplification but without SYBR Green and with two nested primer pairs for each predicted ligation event. PCR products were visualized on ethidium bromide agarose gels (2%) and confirmed by sequencing. Primer sequences are available upon request.


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 EXPERIMENTAL PROCEDURES
 RESULTS AND DISCUSSION
REFERENCES
 
To better characterize the mechanisms of regulation of the GREB1 gene by estrogen, we first assessed the influence of estradiol (E2) treatment on its expression in different ER+ cell lines (MCF-7, T47D, ZR45, MDA-MB-231::ER{alpha}, and Ishikawa). Transcriptional induction was detected in all ER+ cells with E2 treatment whereas the antiestrogen ICI 182,780 (ICI) reduced mRNA levels (supplemental Fig. 1A). Consistent with these findings, a strong correlation between higher GREB1 mRNA levels and ER{alpha} expression in breast tumors can be observed in various microarray studies compiled by Oncomine (supplemental Fig. 1B).

To confirm the involvement of ER{alpha} in transcriptional regulation by estrogen, we assessed the effect of siRNA-mediated suppression of ER{alpha} on GREB1 mRNA expression levels in MCF-7 cells. As shown in Fig. 1, levels of ER{alpha} proteins were reduced by the specific siRNA duplex (Fig. 1A) resulting in a substantial reduction of both basal and estrogen-stimulated levels of GREB1 mRNA (Fig. 1B), which together with the effect of ICI treatment indicates that ER{alpha} is important for both basal and activated GREB1 mRNA expression. To further verify that GREB1 is regulated at the transcriptional level by E2, MCF-7 cells were pretreated by the transcription inhibitor actinomycin D. This treatment prevented induction of GREB1 transcripts, indicating that E2 enhances GREB1 de novo transcription (Fig. 1C). On the other hand, the protein synthesis inhibitor cycloheximide had no effect on the induction by E2 in MCF-7 cells (GREB1, supplemental Fig. 2A), as reported (22), similar to what was observed with the E2 target gene encoding the progesterone receptor (PGR, supplemental Fig. 2A), while induction of the BRCA1 gene was abrogated by cycloheximide and that of pS2/TFF1 was largely attenuated as reported previously (30) (supplemental Fig. 2A). Kinetics of induction of GREB1 transcripts by E2 in MCF-7 cells resembled that of the PGR target gene, being both rapid (detectable at 2 h), and sustained over a 48 h period (supplemental Fig. 2B). On the other hand, induction of E2 targets MYC or FOS was more rapid but transient (supplemental Fig. 2C), while that of pS2/TFF1 was progressive and that of BRCA1 delayed in time (supplemental Fig. 2D). Together, these results indicate that GREB1 is a primary ER{alpha} target induced in an early, strong, and sustained manner by ER{alpha} in MCF-7 cells.

The 5'-flanking sequences of GREB1 contain three consensus EREs (Fig. 2A), and we have previously shown that two of the three GREB1 EREs strongly bound ER{alpha} in ChIP experiments in MCF-7 cells and in MDA-MB-231 cells stably transfected with ER{alpha} (27). Recruitment of ER{alpha} to the three EREs was also observed in a recent genome-wide mapping of ER{alpha} binding sites in the presence of estrogen (17). Here we show that in MCF-7 cells all three perfect EREs are bound with a cyclical temporal pattern after E2 stimulation (Fig. 2B), as observed previously for the pS2/TFF1 gene (31, 32). Note, however, that the basal levels of ER{alpha} recruited to the ERE at –1.5 kb from the GREB1 TSS were higher than those for other EREs. Only faint binding of ER{alpha} to the GREB1 TSS was observed under our experimental conditions. In addition, recruitment to the EREs of the ER{alpha} coactivator SRC-3 (Fig. 2C), acetylated histone H4 (Fig. 2D), as well as phosphorylated RNA polymerase II (P-polII) (Fig. 2C) was also detected by ChIP assays. Note that binding of P-polII was strong under basal conditions on the –1.5-kb ERE. Altogether, these data suggest that the two distal EREs are functional enhancers and that the proximal ERE contributes to the low basal, ICI-repressed activity of the promoter.


Figure 1
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  		FIGURE 1.
GREB1 is transcriptionally induced by ER{alpha}. A, siRNA-mediated depletion of ER{alpha} protein levels was verified by Western analysis with antibodies against ER{alpha} or beta-actin 72 h after transfection and stimulated with E2 during the last 24 h. B, siRNA-mediated depletion of ER{alpha} in MCF-7 cells reduces basal and E2-stimulated mRNA levels of GREB1. MCF-7 cells were transfected with siRNA against ER{alpha} or glyceraldehyde-3-phosphate dehydrogenase (GAPDH) for 72 h and stimulated with hormone during the last 24 h prior to RNA extraction. C, the transcriptional inhibitor actinomycin D abrogates the induction of GREB1 mRNA levels by E2. Cells were pretreated with actinomycin D (2 µg/ml) for 1 h before treatment with E2 for 4 h.

 


Figure 2
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  		FIGURE 2.
Consensus EREs recruit ER{alpha}, SRC-3, acetylated histones, and phosphorylated RNA polymerase II in the presence of estradiol. A, position of the three consensus EREs (cEREs) in the GREB1 upstream regulatory regions. B, cyclical recruitment of ER{alpha} on the three consensus EREs in GREB1 promoter. ChIP was performed using an antibody against ER{alpha} or IgG as negative control with MCF-7 cells treated with E2 (25 nM) or vehicle (ethanol) for different times (as indicated). C, ChIP of SRC-3 and P-PolII at 2 h. D, ChIP of acetylated H4 at 2 h. Results are representative of at least two experiments.

 
While ChIP data indicate recruitment of ER{alpha} and its coactivator SRC-3, acetylation of histone H4 and binding of P-polII to sites that are closer to the GREB1 TSS than to any other gene (the closest gene, E2F6, is located more than 45 kb away from ERE3), this does not conclusively demonstrate that these EREs play a role in direct transactivation of GREB1. To investigate whether all three EREs associate with the GREB1 TSS, we used a chromatin conformation capture (3C) assay (33), which detects physical proximity between distal DNA sites by ligation of restricted DNA fragments that are maintained juxtaposed by cross-linked DNA-protein complexes. Using restriction enzymes that cut at least once between consensus EREs and the GREB1 TSS, we observed PCR amplification of products resulting from the ligation of each of the three EREs and the TSS (Fig. 3A). Association of ERE1 (–1.5 kb) and the TSS was constitutive, which could reflect either the higher basal level of receptor and P-polII associated with this ERE (see Fig. 2C) or the short distance between the ERE and the TSS. However, the lack of chromatin loop formation in the presence of ICI suggests formation of a chromatin loop in the absence of hormone rather than random interactions between the two DNA fragments. No chromatin loops were detected with several regions located between the EREs and the TSS (Fig. 3A and data not shown) or between the TSS and a fragment at +1.5 kb downstream (data not shown), demonstrating that E2-induced chromatin looping with the TSS is specific for fragments containing the EREs. Note that the 3C PCR products obtained were sequenced to confirm product identity and that all primer sets for 3C detection led to amplification of a digested and re-ligated BAC clone overlapping this genomic region (data not shown). These results indicate that the consensus EREs in the GREB1 gene behave as E2-induced enhancers since they recruit ER{alpha}, SRC-3, and P-polII, are associated with acetylated histones, and interact with the TSS of GREB1 in the presence of E2.


Figure 3
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  		FIGURE 3.
Induction by estradiol treatment of chromatin loops associating the GREB1 enhancers and transcriptional start site. A, detection of chromatin loops formed between different regions of the GREB1 upstream sequences and the most 5' transcriptional start site. Chromatin conformation capture (3C) assays were performed in MCF-7 cells treated with E2 (25 nM), ICI (100 nM), or vehicle (ethanol) for 45 min. B, detection of chromatin loops formed between consensus EREs. Results are representative of three to four independent experiments performed either with the MspI or the XceI enzyme. Each chromatin loop was observed in between two and four independent assays.

 
The presence of three strong enhancers raises the question of whether these sequences associate with the TSS in a mutually exclusive and possibly sequential manner or if they may participate in reciprocal interactions as well. To investigate this question, we analyzed by 3C whether chromatin loop formation could take place between ERE enhancers themselves (Fig. 3B). PCR amplification resulting from chromatin loop formation between any combinations of two consensus EREs could be detected in the presence of E2 but not in its absence or in the presence of ICI. In addition, no interactions were detected with other intermediate regions (Fig. 3B and data not shown), demonstrating again the specificity of these interactions for the presence of EREs. These results suggest that EREs can physically associate with each other, either in a large complex with the TSS or in transient binary interactions (see model in supplementary Fig. 3).

Based on the above findings, we conclude that the 5'-flanking region of GREB1, a gene of as yet unknown function but that may play an important role in E2-induced cell proliferation (23), contains a strong, multipartite enhancer composed of three consensus EREs separated by 8 to ~20 kb of intervening sequences. Future studies will be necessary to assess whether this multipartite enhancer also interacts with additional ER{alpha} binding regions and with the TSS of other E2 target genes and whether transcriptional regulation by E2 often involves the association of several widely spread enhancer units.


   FOOTNOTES
 
* This work was supported in part by Canadian Institutes of Health Research (CIHR) Grant MOP-13147 (to S. M.). The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. Back

Formula The on-line version of this article (available at http://www.jbc.org) contains supplemental Figs. 1–3 and Refs. 34–39. Back

1 These authors contributed equally to this work. Back

2 Recipient of studentships from the Fonds de la Recherche en Santé du Québec (FRSQ) and the Faculté desÉtudes Supérieures de l'Université de Montréal. Back

3 Holder of a post-doctoral fellowship from the CIHR. Back

4 Chercheur-Boursier National of the FRSQ. Back

5 Chercheur-Boursier National of the FRSQ. Holder of the Canadian Imperial Bank of Commerce Breast Cancer Research Chair at Université de Montréal. To whom correspondence should be addressed: IRIC, Université de Montréal, C.P. 6128, Succursale Centre-Ville, Montréal, Quebec H3C 3J7, Canada. Tel.: 514-343-7166; Fax: 514-343-7780; E-mail: sylvie.mader{at}umontreal.ca.

6 The abbreviations used are: ER, estrogen receptor; ERE, estrogen response element; TSS, transcriptional start site; FBS, fetal bovine serum; DMEM, Dulbecco's modified Eagle's medium; siRNA, small interfering RNA; ChIP, chromatin immunoprecipitation; E2, estradiol; P-polII, phosphorylated RNA polymerase II; 3C, chromatine conformation capture. Back


   ACKNOWLEDGMENTS
 
We thank Drs. Raphael Metivier and Michael Witcher for discussions on the ChIP technique and Drs. Wouter de Laat, Hugo Wurtele, Pierre Chartrand, and Josée Dostie for advice on the 3C technique. We are also grateful to Marie-France Proteau for technical assistance and Walter Rocha for helpful discussions.



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