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TRANSACTIVATION OF GLUCOCORTICOID-INDUCIBLE RAT ARYL SULFOTRANSFERASE (SULT1A1) GENE TRANSCRIPTION

Institute of Environmental Health Sciences, Wayne State University, Detroit, Michigan

(Received June 2, 2003; accepted July 30, 2003)

	Abstract

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The purpose of the current study was to establish the role of the glucocorticoid receptor (GR) and androgen receptor (AR) transcription factors in the transactivation of rat aryl sulfotransferase (SULT1A1) gene transcription and to identify the functional hormone-responsive element(s) in the SULT1A1 gene. A cis-acting inverted repeat with three intervening bases (IR3) was identified in the 5'-flanking of the SULT1A1 gene that mediates the transactivation of SULT1A1 gene transcription by both the GR and AR. CV-1 cells were cotransfected with SULT1A1-luciferase reporter plasmids and either wild-type or mutant GR or AR expression constructs. In cotransfectants expressing the wild-type GR, treatment with triamcinolone acetonide produced an 4- to 6-fold induction of luciferase activity in IR3-containing SULT1A1 reporter plasmids. IR3-containing SULT1A1 reporter constructs were also activated by treatment with the synthetic androgen R1881 in cells cotransfected with wild-type but not mutant AR. In primary cultured rat hepatocytes, androgen-inducible expression of IR3-containing SULT1A1 reporter plasmids required cotransfection with AR expression plasmid. Targeted disruption of the SULT1A1 IR3 by mutation of a conserved GT sequence in the 3' half-site of the element ablated GR and AR responsiveness. These results indicate that a proximal IR3 element in the 5'-flanking region of the rat SULT1A1 gene is sufficient for the transactivation of SULT1A1 gene transcription by the GR and AR, and that relative to the GR, functional AR activity is reduced in primary cultured rat hepatocytes.

SULT1A1 is more abundantly expressed in male relative to female rat liver (Liu and Klaassen, 1995), and definitive information on the molecular regulation of "male-predominant" rat hepatic SULT1A1 is just emerging. We previously reported that rat hepatic SULT1A1 gene transcription is inducible through a GR-mediated mechanism, and that sequences located within -84 base pairs of the SULT1A1 core promoter contain two candidate glucocorticoid receptor-responsive elements (GREs) (Duanmu et al., 2001). Several members of the steroid hormone class of receptors, such as the GR, AR, progesterone receptor, and mineralocorticoid receptor, share an ability to transactivate gene expression through common consensus response elements (Beato, 1989; Ham et al., 1998). Since the pattern of SULT1A1 expression in rat liver suggests a role for both the GR and AR in the control of SULT1A1 gene transcription, cotransfection analyses were used to localize the cis-acting sequences in the 5'-flanking region of rat SULT1A1 that mediate GR- and AR-inducible SULT1A1 gene transcription.

	Materials and Methods

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Materials. Triamcinolone acetonide, dexamethasone, dihydrotestosterone (DHT), and molecular biology-grade reagents were obtained from Sigma-Aldrich (St. Louis, MO). Synthetic androgen R1881 (methyltrienolone) was purchased from PerkinElmer Life Sciences (Boston, MA). Custom-synthesized oligonucleotides were obtained commercially from Integrated DNA Technologies, Inc. (Coralville, IA). CV-1 cells (No. CLL-70) were obtained from American Type Culture Collection (Manassas, VA). The wild-type and mutant GR cDNA expression constructs were generous gifts from Dr. Mark Danielsen of Georgetown University Medical Center (Washington, DC), as were the wild-type and DNA binding-defective mutant AR expression plasmids. The two GR expression mutants, GR-A (Glu-546 Gly) and GR-B (Arg-484 His), were deficient in glucocorticoid hormone binding and DNA binding, respectively (Danielsen et al., 1986). The pSG5 expression vector containing an SV40 promoter was obtained from Stratagene (La Jolla, CA).

Preparation of SULT1A1 Reporter Constructs. A fragment of the SULT1A1 5'-flanking region from -1892 to +56 inserted into the promoterless luciferase reporter plasmid pGL3-Basic was prepared as described previously (Duanmu et al., 2001). An IR3 sequence located within -84 nucleotides of the transcription start site of the SULT1A1 gene was identified as a candidate SULT1A1 GRE. A reference deletion construct containing nucleotides -84 to +56 of the SULT1A1 gene was generated by PCR using a 5'-primer that included an added SacI restriction site (-84SULT1A1 5'-primer 1: 5'-GAGCTCTGTTTCTGGAGAACAGCCA-3') and a 3'-PCR primer that included a XhoI restriction site (-84SULT1A1 3'-primer 2: 5'-CTCGAGTCCGGGTGCTCAGTGATA-3'). The PCR product was first ligated into the pGEM-T Easy vector (Promega, Madison, WI) and then subcloned into the SacI and XhoI sites of the pGL3-Basic luciferase reporter vector (Promega). Two additional mutant IR3 SULT1A1 constructs were prepared by PCR and cloned into the pGL3-Basic reporter vector. In the wild-type SULT1A1 IR3 construct, all SULT1A1 5'-flanking sequences upstream of the IR3 element were deleted (-75 SULT1A1). In -75(IR3m)SULT1A1, the GT dinucleotide in the 3' half-site of the SULT1A1 IR3 was changed to CA. The 5' primers for the -75 SULT1A1 and -75(IR3m)SULT1A1 constructs both contained SacI restriction sites and were designated as primer 3: 5'-GCGGAGCTCAGAACAGCCAGTCCTAGCA-3' for -75 SULT1A1 and primer 4: 5'-GCGGAGCTCAGAACAGCCACACCTAGCA-3' for -75(IR3m)SULT1A1. The bolded bases represent the IR3 motif, and the underscored bases are those that were changed to create the mutant IR3. The 3' primer 5: 5'-GCGCTCGAGTCCGGGTGCTCAGTGATA-3' was common to both the -75 SULT1A1 and -75(IR3m)SULT1A1 inserts and contained a XhoI restriction enzyme site to facilitate subcloning into the pGL3-Basic reporter vector. The SULT1A1 deletion and mutation test constructs that were used in transient transfections are depicted in Fig. 1. The sequences of all cloned inserts were verified by sequence analysis (Center for Molecular Medicine and Genetics DNA Sequencing Facility, Wayne State University, Detroit, MI).

View larger version (11K): [in this window] [in a new window]   FIG. 1. A schematic representation of SULT1A1 deletion and mutation reporter constructs that were used in transient transfections. The IR3 sequence in the -84 SULT1A1, -75 SULT1A1, and -75(IR3m)SULT1A1 constructs is indicated in bold type. In 75(IR3m)SULT1A1, the GT dinucleotide in the 3' half-site of the SULT1A1 IR3 was changed to CA (underscored).

Transient Transfections. Transient transfections in primary cultured rat hepatocytes were performed as described previously (Duanmu et al., 2002). Transient transfections in CV-1 cells were accomplished by following a previously described procedure with certain modifications (Urizar et al., 2000). CV-1 cells were cultured in Dulbeccco's modified Eagle's medium supplemented with 10% charcoal-stripped fetal bovine serum in 5% CO₂/air at 37°C. Cells (7 x 10⁴ cells/well) were plated in 24-well plates and allowed to reach 80% confluency. The cells were then transfected using 2 µl/well of Lipofectamine and 1 µl/well of Plus reagent (Invitrogen, Carlsbad, CA). Cells were cotransfected with 5 ng of GR or AR expression plasmid or pSG5 (control), together with 320 ng of pGL3-Basic luciferase reporter plasmid containing specified sequences from the rat SULT1A1 gene 5'-flanking region. The pRL-CMV plasmid, which expresses Renilla luciferase, was used to normalize for variations in transfection efficiency among samples, as previously described (Duanmu et al., 2001). The appropriate amount of pBluescript KS+ plasmid was added to individual transfection wells as required to render a constant amount of DNA (400 ng) in each transfection reaction. Three hours after transfection, the medium was replaced with fresh Dulbeccco's modified Eagle's medium containing 10% delipidated charcoal-stripped fetal calf serum. At 18 to 24 h after transfection, cells were treated with either DMSO vehicle (control), 10^-7 M triamcinolone acetonide, 10^-7 M dexamethasone, 10 ^-7 M R1881, or 10^-5 M dihydrotestosterone for 24 h. The cells were then harvested and assayed for luciferase activity. The Dual-Luciferase reporter assay system (Promega) and a Dynex model MLX luminometer (Dynex Technologies, Chantilly, VA) were used for luciferase assays. Luciferase assay results are expressed in the figures as normalized values of firefly luciferase chemiluminescence units divided by Renilla luciferase chemiluminescence units.

Statistical Analysis of the Data. Data were analyzed by one-way analysis of variance followed by the Newman-Keuls post hoc test, using Prism (version 3) software (GraphPad Software Inc., San Diego, CA).

	Results

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Our previous analysis of the SULT1A1 5'-flanking region in primary cultured rat hepatocytes suggested that either an everted repeat with three intervening bases or an IR3 element was the prime candidate for a functional GRE, and that the IR3 element (i.e., AGAACA GCC AGTCCT) retained features that were strikingly characteristic of a classical GRE (Duanmu et al., 2001). In support of the hypothesis that the IR3 is a functional GRE, we found that the IR3 was sufficient to support GR inducibility in SULT1A1 reporter plasmids (Fig. 2). In transient transfections conducted in primary cultured rat hepatocytes, deletion of all SULT1A1 5'-flanking sequences located distal to the IR3 (-75 SULT1A1) still conferred GR inducibility (Fig. 2). Moreover, in light of previous reports demonstrating that a short GT dinucleotide sequence in the 3' half-site is a generally conserved feature in most GREs and that the mutation of this critical GT to a CA sequence disrupts transactivation of gene expression by the GR (Nogami et al., 2002), we found that a similar mutation in the SULT1A1 IR3 3' half-site effectively abolished GR-inducible SULT1A1 expression (-75(IR3m)SULT1A1, Fig. 2). In contrast, treatment with the synthetic androgen R1881 failed to induce luciferase reporter activity in SULT1A1 IR3-containing plasmids (Fig. 2). Since ligand-activated AR should induce transcription in GRE-luciferase reporter plasmids, these results suggested that, relative to the GR, AR activity in primary cultured rat hepatocytes is diminished.

View larger version (19K): [in this window] [in a new window]   FIG. 2. Transient transfections in primary cultured rat hepatocytes. Glucocorticoid treatment transactivates SULT1A1 transcription at the IR3. Primary rat hepatocyte cultures were transiently transfected with -84 SULT1A1, -75 SULT1A1, or -75(IR3m)SULT1A1 luciferase reporter plasmid. After overlaying the transfected cultures with Matrigel (BD Biosciences, Franklin Lakes, NJ), cells were treated with either 0.1% DMSO (solvent control), dexamethasone (10-7 M), or synthetic androgen R1881 (10-7 M). After 24 h of treatment, cells were harvested for the determination of luciferase reporter activity. The data are representative of two independent experiments and are presented as the mean normalized luciferase activity ± S.D., n = 3 per treatment group. Within each treatment set (i.e., cultures transfected with the same reporter plasmid), groups that are marked by * are significantly different from all other groups (p < 0.05), whereas unmarked groups are not significantly different from one another.

Follow-up cotransfection analyses were performed in CV-1 cells using a panel of wild-type and mutant GR expression constructs that were previously characterized by Danielsen's research group (Danielsen et al., 1986). The wild-type GR cDNA expression construct contained the complete open reading frame for the mouse GR, whereas the GR-A (Glu-546 Gly) and GR-B (Arg-484 His) constructs expressed GR proteins that were deficient in hormone binding and DNA binding, respectively (Danielsen et al., 1986). Relative to DMSO-treated controls, triamcinolone acetonide-treated cotransfectants that expressed wild-type GR in the presence of IR3-containing SULT1A1 reporter plasmids (-84 SULT1A1 and -75 SULT1A1) displayed substantial increases in luciferase reporter activity, unlike the -75(IR3m)SULT1A1 reporter (Fig. 3). These results support a role for the IR3 element in the transactivation of SULT1A1 gene transcription by the GR. As expected, cotransfection with either of the mutant GR expression plasmids ablated the GR responsiveness in the -84 SULT1A1 and -75 SULT1A1 reporter plasmids (Fig. 3).

View larger version (21K): [in this window] [in a new window]   FIG. 3. Cotransfections of glucocorticoid receptor expression constructs with SULT1A1-5' reporter plasmids in CV-1 cells. CV-1 cells were cotransfected with one of the following expression plasmids: the control pSG5 plasmid, wild-type GR, mutant GR-A (Glu-546 Gly), or mutant GR-B(Arg-484 His) and one of the SULT1A1 luciferase reporter plasmids described in the legend to Fig. 1. At 18 to 24 h after transient transfection, cells were treated with either 0.1% DMSO (vehicle control) or triamcinolone acetonide (10-7 M). After 24 h of treatment, cells were harvested for the determination of luciferase activity. The data are representative of two independent experiments and are presented as the mean normalized luciferase activity ± S.D., n = 3 per treatment group. Within each treatment set (i.e., cultures transfected with the same reporter plasmid), groups that are marked by * are significantly different from all other groups (p < 0.05), whereas unmarked groups are not significantly different from one another.

To test whether or not ligand-activated AR can also transactivate SULT1A1 transcription through the IR3, parallel transient cotransfections in CV-1 cells were performed using SULT1A1 reporter plasmids and either wild-type or mutant (DNA binding defective) AR expression construct. Cotransfectants containing wild-type AR expression plasmid and IR3-containing SULT1A1 luciferase reporter produced robust increases in luciferase expression following treatment with the synthetic androgen R1881 (Fig. 4). As expected, cotransfectants containing either intact SULT1A1 IR3 luciferase reporters and a mutant AR expression plasmid or a mutant SULT1A1 IR3 reporter construct with a wild-type AR expression plasmid showed ablated androgen responsiveness of the reporter (Fig. 4).

View larger version (17K): [in this window] [in a new window]   FIG. 4. Cotransfections of androgen receptor expression constructs with SULT1A1-5' reporter plasmids in CV-1 cells. CV-1 cells were cotransfected with one of the following expression plasmids: either the control pSG5 plasmid or wild-type or DNA binding-defective mutant AR (ARmut) expression plasmid and one of the SULT1A1 reporter plasmids described in the legend to Fig. 1. At 18 to 24 h after transient cotransfection, cells were treated with either 0.1% DMSO (vehicle control) or R1881 (10-7 M). After 24 h of treatment, cells were harvested for the determination of luciferase activity. The data are representative of two independent experiments and are presented as the mean normalized luciferase activity ± S.D., n = 3 per treatment group. Within each treatment set (i.e., cultures transfected with the same reporter plasmid), groups that are marked by * are significantly different from all other groups (p < 0.05), whereas unmarked groups are not significantly different from one another.

In primary cultured rat hepatocytes, significant androgen-inducible transcription in SULT1A1 IR3 reporter constructs did not occur in the absence of cotransfection with AR expression plasmid (Fig. 5). In hepatocytes transfected with either the AR or pSG5, luciferase activity was substantially induced for the -75 SULT1A1 reporter plasmid following treatment with a GR-activating concentration of dexamethasone, as expected (Fig. 5). Treatment with DHT, even at a high concentration, failed to induce transcription from the IR3-containing SULT1A1 reporter (-75 SULT1A1). To circumvent the possibility that rapid metabolism in cultured hepatocytes leads to reduced bio-availability of DHT in our system, cells were treated with an AR-activating concentration of the synthetic androgen R1881. This approach produced a significant increase in -75 SULT1A1 reporter activity (Fig. 5). As expected, GR- and AR-mediated induction of SULT1A1 reporter expression was dependent upon an intact IR3 in SULT1A1 (Fig. 5).

View larger version (21K): [in this window] [in a new window]   FIG. 5. Transient cotransfections in primary cultured rat hepatocytes. Primary rat hepatocyte cultures were transiently cotransfected with either the control pSG5 plasmid or wild-type AR expression plasmid, and either -75 SULT1A1 or -75(IR3m)SULT1A1 luciferase reporter plasmid. After overlaying the transfected cultures with Matrigel, cells were treated with either 0.1% DMSO (solvent control), dexamethasone (10-7 M), dihydrotestosterone (10-5 M), or synthetic androgen R1881 (10-7 M). After 24 h of treatment, cells were harvested for the determination of luciferase reporter activity. The data are representative of two independent experiments and are presented as the mean normalized luciferase activity ± S.D., n = 3 per treatment group. Group means were compared using a one-way analysis of variance followed by the Newman-Keuls post hoc test. Groups that do not share a capital letter are significantly different from one another (p 0.05).

	Discussion

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Previous transient transfection studies in primary cultured rat hepatocytes revealed the presence of two candidate GREs in the 5'-flanking region of SULT1A1, including an everted repeat with three intervening bases and an IR3 element, both located within 84 nucleotides of the SULT1A1 transcription start site (Duanmu et al., 2001). In the present study, we demonstrated that an intact IR3 element (contained in -84 SULT1A1 and -75 SULT1A1 constructs) was sufficient to support transactivation by expressed GR. In addition, we noted that transfectants containing the longer -84 SULT1A1 reporter construct reproducibly displayed modestly greater levels of GR inducibility (relative to -75 SULT1A1 transfectants), suggesting that the longer -84 SULT1A1 fragment may contain added positive regulatory information that is important for achieving maximal levels of GR-inducible SULT1A1 transcription.

The GR and AR share an ability to transactivate gene expression through common responsive element sequences (Beato, 1989; Ham et al., 1998), and there is reason to implicate a role for the AR in the transcriptional control of rat hepatic SULT1A1 expression in vivo. SULT1A1 is more robustly expressed in male relative to female rat liver (Liu and Klaassen, 1995). In male rat liver, the expression of SULT1A1 increases with maturity and mirrors the age-related pattern of AR expression that has been reported for rat liver in vivo (Supakar and Roy, 1996). The precise reason for the need to cotransfect hepatocytes with AR expression plasmid to support androgen-inducible transactivation of SULT1A1 IR3-containing reporter constructs is unclear. The temporal course of AR mRNA and protein expression was examined by real-time reverse transcriptase-PCR and Western blot, respectively, and we were able to demonstrate measurable amounts of AR mRNA and protein in primary rat hepatocytes throughout 72 h of culture (data not shown). The GR and AR have been shown to activate target gene transcription through similar or identical response elements in vitro and in other biological systems (Beato, 1989; Danielsen et al., 1989; Umesono and Evans, 1989; Jianming and Danielsen, 1998). In corroboration of this observation, we were able to show in CV-1 cells that GR and AR expression plasmids can each effectively transactivate IR3-containing reporter plasmids.

A critical check-point in the control of tissue-specific target gene transcription occurs at the level of receptor interactions with other transcription factors and as a consequence of differences in coactivator or corepressor recruitment (Jianming and Danielsen, 1998). For example, Jianming and Danielsen (1998) demonstrated that the pRB protein selectively complexes with the AR but not the GR, and that the loss of pRB coactivator expression selectively reduces AR but not GR activity in transfected cells. However, we found that cotransfection of primary cultured rat hepatocytes with IR3-containing SULT1A1 reporter construct and increasing concentrations of pRB expression plasmid failed to activate endogenous AR-mediated gene expression in response to R1881 treatment (data not shown).

Gaining a thorough understanding of the molecular controls that govern SULT1A1 gene transcription has potential implications for drug and hormone metabolism in humans. SULT1A1 expression was previously observed to be induced by glucocorticoids in cultured bovine tracheobronchial epithelial cells (Beckmann et al., 1994; Schauss et al., 1995). These foundation studies implied a role for steroid receptors in the trans-species regulation of SULT1A1 transcription. However, Northern blot analyses of primary cultured human hepatocytes suggested that the human SULT1A1 gene is not glucocorticoid-inducible (Duanmu et al., 2002). Unlike the rat, the human SULT1A1 gene contains two alternative promoters and lacks a consensus GRE (Bernier et al., 1996), indicating that the transcriptional regulation of SULT1A1 by a classical GR-mediated mechanism is not conserved in the human.

The present series of transient transfection and cotransfection studies provides evidence for the regulation of glucocorticoid-inducible rat SULT1A1 gene transcription by the GR and AR transcription factors and shows that an IR3 element located in close proximity to the SULT1A1 core promoter functions as a cis-acting GR- and AR-responsive element. Relative to the GR, primary cultured rat hepatocytes displayed diminished transactivation of SULT1A1 gene transcription by endogenous AR, as a result of alterations in either essential coactivators, corepressors, or downstream signaling components in the AR transcription machinery. In the rat, the selective maintenance of glucocorticoid-over androgen-inducible SULT1A1 gene expression may be critical to the activation of xenobioticmetabolizing enzyme gene expression during episodes of hepatic stress or during developmental periods of fluctuating hormone levels.

	Acknowledgments

 
We especially thank Dr. Mark Danielsen of Georgetown University Medical Center for providing the wild-type and mutant glucocorticoid expression plasmids that were instrumental to this study. In addition, the contributions of research assistants Jeffrey R. Smigelski and Amy Weckle are recognized and appreciated.

	Footnotes

 
¹ Abbreviations used are: SULT1A1, aryl sulfotransferase; GRE, glucocorticoid receptor-responsive element; GR, glucocorticoid receptor; AR, androgen receptor; R1881, methyltrienolone; IR3, inverted repeat with three intervening bases; PCR, polymerase chain reaction; DMSO, dimethyl sulfoxide; DHT, dihydrotestosterone.

Address correspondence to: Dr. Melissa Runge-Morris, Institute of Environmental Health Sciences, Wayne State University, 2727 Second Avenue, Room 4000, Detroit, MI 48201. E-mail: M.Runge-Morris{at}wayne.edu

	References

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This Article Abstract Full Text (PDF) Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Fang, H.-L. Articles by Runge-Morris, M. Search for Related Content PubMed PubMed Citation Articles by Fang, H.-L. Articles by Runge-Morris, M.