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Departments of Medicine and Pharmacology Duke University
Medical Center (K.M.C., Y.I., S.-C.S., K.L.P.) Durham, North
Carolina 27710
Department of Cell Biology and
Biochemistry Texas Tech University Health Science Center
(D.M.S.) Lubbock, Texas 79430
Department of
Biochemistry University of Louisville School of Medicine
(B.J.C.) Louisville, Kentucky 40292
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ABSTRACT |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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Recent studies have implicated the steroidogenic acute regulatory protein (StAR) as an essential component of the acute response of steroidogenic cells to trophic hormone. StAR is a 30-kDa mitochondrial phosphoprotein whose expression is restricted to steroidogenic cells, where it is rapidly induced by trophic hormone in a manner that correlates with the acute stimulation of steroidogenesis (3, 4). In transient transfection experiments in both steroidogenic and nonsteroidogenic cells, StAR expression directly stimulated pregnenolone production (4, 5, 6). The onset of StAR expression during mouse embryonic development correlated closely with the onset of steroid hydroxylase expression and with the beginning of steroid hormone biosynthesis (5). Definitive proof for an essential role of StAR in regulated steroidogenesis came from studies of patients with lipoid congenital adrenal hyperplasia, a congenital disorder characterized by global defects in steroidogenesis (7). Analyses of patients with this disorder revealed mutations in the StAR gene that preclude the expression of functional StAR protein (8). These findings provided compelling biochemical and genetic evidence for the essential role of StAR in regulated steroidogenesis and strongly suggested that StAR mediates the acute regulation of steroid hormone biosynthesis.
To further our understanding of the mechanisms that regulate StAR gene expression, we recently isolated the mouse StAR gene and determined its structural organization and sequence (5). We further showed that StAR messenger RNA (mRNA) levels within steroidogenic cells were markedly increased by cAMP, suggesting that cAMP may induce StAR transcription. To extend these studies, we now characterize the mechanisms that regulate StAR expression in steroidogenic cells. Our results show that the 5'-flanking sequences of StAR can direct cell-specific and hormone-induced expression. They further implicate steroidogenic factor-1 (SF-1; also called adrenal-4-binding protein), an orphan nuclear receptor that plays key roles at multiple levels of the hypothalamic-pituitary-steroidogenic organ axis. Collectively, these results provide novel insights into the mechanisms that control the expression of this essential component of regulated steroidogenesis.
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RESULTS |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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3.6 kilobases of the
StAR 5'-flanking region (Fig. 1
). These
sequences are numbered relative to the transcription initiation site,
which was determined by primer extension analysis (Fig. 2). Unlike many tissue-specific and hormonally
responsive genes, neither a canonical TATA box nor a consensus
cAMP-responsive element (CRE) can be identified within this region. We
previously noted a sequence at -135 (CCAAGGTGG, bottom strand) that
resembles the consensus binding motif for the orphan nuclear receptor
SF-1 (5). Further examination of the 5'-flanking sequence revealed two
other potential binding sites for nuclear hormone receptors: the
inverted repeat (AGGTCA GGACCT) located at -890 and a
region at -42 (AGGCTG, bottom strand) that somewhat resembles the SF-1
consensus motif.
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, the StAR 5'-flanking region directed
high levels of luciferase expression in two steroidogenic cell lines
(mouse Y1 adrenocortical and MA-10 Leydig cells) and low levels of
expression in two nonsteroidogenic cell lines (mouse L-TK-
fibroblast and 
T3 gonadotrope cells). The finding that StAR promoter
activity is restricted to steroidogenic cells demonstrates that the 966
bp of the StAR 5'-flanking region are sufficient to direct
appropriate cell-selective expression in transient transfection
analyses.
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(cross-hatched bars), treatment with cAMP
significantly induced promoter activity in the steroidogenic Y1
adrenocortical and MA-10 Leydig cells. Significant increases were also
observed in the very low levels of expression in L cells. These results
demonstrate that the proximal 966 bp of the StAR promoter are
sufficient for hormone-induced expression in steroidogenic and
nonsteroidogenic cells. Studies with a reporter construct
containing 3.6 kilobases of StAR 5'-flanking region showed
that these additional sequences did not significantly increase basal or
hormone-induced promoter activity over that seen with the proximal 966
bp (data not shown). We, therefore, concentrated our analyses of
StAR gene regulation on the proximal 966 bp of the
5'-flanking region shown to be capable of directing both cell-selective
and hormone-induced expression.
Elements Required for StAR Promoter Activity Are Located within 253
bp of the Transcription Initiation Site
We next performed 5'-deletion analyses to identify specific
sequences within the StAR 5'-flanking region that regulate
constitutive and hormone-induced promoter activity. Plasmids containing
progressively decreasing amounts of StAR 5'-flanking region
upstream of the human GH (hGH) reporter gene were transiently
transfected into MA-10 Leydig and Y1 adrenocortical cells, with or
without cAMP treatment, and promoter activity was measured by RIA for
hGH (MA-10 cells) or by Northern blotting analyses of hGH transcripts
(Y1 cells). As shown in Fig. 4A, progressive deletion of
sequences from -966 to -426 and from -426 to -254 did not
significantly impair basal or cAMP-induced promoter activity. In fact,
there was a progressive increase in both basal and cAMP-induced
activity, suggesting that a negative regulatory element may lie between
-966 and -254. These results demonstrate that sequences within this
region do not positively regulate StAR expression in MA-10 cells.
Further deletion of the promoter from -254 to -113 considerably
diminished basal StAR promoter activity to levels that did not differ
significantly from the those of the promoterless negative control.
Moreover, there was no response to cAMP treatment in cells transfected
with the -113 construct. Similar results were obtained when the same
plasmids were transiently transfected into Y1 adrenocortical cells
(Fig. 4B). In addition, hGH transcripts expressed from the 5'-deletion
plasmids were of the predicted size, strongly suggesting that they
arose from the authentic initiation site. These results strongly
suggest that the region between -254 and -113 contains an important
positive regulator of StAR expression in both MA-10 Leydig cells and Y1
adrenocortical cells. Interestingly, this region contains the putative
SF-1 binding site at -135.
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), suggesting that hormonal
effects reflect increased StAR transcription. Consistent with this
model, trophic hormone induction of StAR mRNA levels was abolished when
cells were treated with actinomycin D to prevent the synthesis of new
transcripts (Fig. 5). However, treatment of the cells
with cycloheximide did not prevent the cAMP-related increases in StAR
mRNA, indicating that cAMP induction of StAR mRNA is direct and does
not require de novo protein synthesis.
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, a probe containing the SF-1 motif located at -135
formed a prominent shifted complex that was competed in a
dose-dependent manner by unlabeled oligonucleotides containing the
homologous sequence (CCAAGGTGG), but not by unlabeled oligonucleotides
containing a mutated SF-1-binding site
(CCATATTAT). Moreover, preincubation of the
nuclear extract with a polyclonal antiserum specific for the
DNA-binding domain of SF-1 completely abolished complex formation (Fig. 6). Even though it was not identified as an important regulator of StAR
expression in our 5'-deletion studies, the potential SF-1 motif at -42
also competed with the SF-1-related complex. Given that the region
between -254 and -113 is important for StAR promoter activity, the
finding that SF-1 interacts specifically with the -135 element is
consistent with the model in which SF-1 regulates StAR gene
expression.
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, mutation of the -135 SF-1-binding site decreased basal promoter
activity in Y1 adrenocortical cells to 50% of the level of the
wild-type promoter (Fig. 7), revealing a role for this
element in StAR promoter activity. No further impairment was seen when
the -42 SF-1 site was also mutated. However, both mutated plasmids
exhibited full levels of induction in response to cAMP, suggesting that
hormone induction and regulation by SF-1 occur through different
promoter elements. Similar qualitative results were obtained when
mutated StAR promoter/hGH plasmids were transiently transfected in
MA-10 Leydig cells (data not shown). Collectively, the 5'-deletion and
site-directed mutagenesis studies thus define an important role for the
SF-1 binding motif at -135 in StAR gene expression.
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, StAR transcripts were readily detected
in the genital ridges of wild-type embryos on both E10.5 and E11.5, but
could not be detected in the urogenital ridges of Ftz-F1
knockout mice. To the extent that the developing gonads were still
intact at these relatively early stages of gonadogenesis, these results
implicate SF-1 as an essential regulator of StAR expression in
vivo.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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Our analyses of StAR promoter activity raise several interesting points. Perhaps most significantly, both transfection studies and analyses of knockout mice implicate the orphan nuclear receptor SF-1 in StAR gene regulation. Although cotransfection of Y1 cells with an SF-1 expression plasmid only slightly increased the promoter activity of the mouse StAR 5'-flanking sequences (data not shown), this modest induction probably reflects the fact that Y1 cells endogenously express high levels of SF-1. Consistent with this model, a similar role for SF-1 in the promoter activity of the human StAR gene has recently been proposed based on SF-1 induction of promoter activity of the human 5'-flanking sequences in transient transfection experiments in nonsteroidogenic cells (13).
Initially identified as an essential regulator of the cytochrome P450 steroid hydroxylases (14, 15), analyses of knockout mice established that SF-1 plays essential roles at multiple levels of the hypothalamic-pituitary-steroidogenic organ axis, establishing it as a key factor in reproduction (12, 16–19; reviewed in ref. 20). Although it is not entirely unexpected that SF-1 regulates StAR gene expression in view of its global roles in steroidogenesis and reproduction, the link between SF-1 and StAR identifies yet another target gene by which SF-1 determines steroidogenic competence.
Another important finding is that the StAR 5'-flanking region directs hormone-induced expression. Unlike many genes that are induced by cAMP, increases in StAR promoter activity apparently do not result from interactions between the transcriptional regulator cAMP-response element binding protein and its cognate CRE (21), as no sequence resembling the consensus CRE is found in the 5'-flanking region of the mouse (this report) or human (13) StAR genes. Nonetheless, our promoter analyses strongly suggest that StAR induction by cAMP at least partly involves transcriptional activation. In this respect, the StAR gene resembles those of several of the steroid hydroxylases, which also are induced by cAMP in the absence of a classical CRE (21). Although SF-1-binding sites have been implicated in the hormonal regulation of several steroid hydroxylases (reviewed in Ref.22), our site-directed mutagenesis studies demonstrate that the SF-1 sites in the StAR promoter are dispensable for hormone induction. Thus, an important goal for future studies will be to identify the precise region(s) of the StAR gene that underlies increased transcription in response to hormone induction.
Another key component of StAR expression is its tissue specificity, with expression in steroidogenic cells of the adrenal cortex and gonads, but not in those of the placenta. Our own studies indicate that the orphan nuclear receptor SF-1 is a key regulator of cell specificity. It is, nonetheless, clear that other mechanisms also must limit StAR expression to the steroidogenic cells of the adrenal cortex and gonads, as SF-1 is also expressed by pituitary gonadotropes and the ventromedial hypothalamic nucleus, regions that do not express StAR (5). Of interest in this regard, mutation of the SF-1 binding element does not impair StAR promoter activity as drastically as does deletion of the region from -254 to -113. It thus appears that other important regulatory elements reside within this part of the StAR 5'-flanking region. An important goal for future studies will be to identify and characterize these other regulatory elements, perhaps leading to a better understanding of the precise mechanisms that regulate this essential component of regulated steroidogenesis.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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Plasmids
Plasmids were made using previously isolated sequences of the
StAR 5'-flanking region (5). Full-length and 5'-deletion
plasmids with the indicated amounts of 5'-flanking sequences were
cloned into a promoterless plasmid containing the hGH structural gene
using PCR-based strategies and convenient restriction sites. Other
plasmids used the same 5'-flanking sequences upstream of a luciferase
reporter gene in the pGL2 basic plasmid (Promega). Mutated plasmids
were generated by PCR-based strategies or double stranded site-directed
mutagenesis. The SF-1 site at -135 was mutated from wild-type
CCAAGGTGG (bottom strand) to TACGTAGTT (bottom strand). The
SF-1 site at -42 was mutated from wild-type AGGCTG (bottom strand) to
TACGTA (bottom strand).
Primer Extension Analysis
The transcription initiation site of StAR was mapped with the
Drosophila Embryo Nuclear Extract In Vitro
Transcription System (Promega) according to the manufacturer’s
protocol. Total RNA was isolated from Y1 adrenocortical cells by the
guanidinium isothiocyanate method using a standard protocol (23). A
primer complementary to 110–130 bp of the complementary DNA (cDNA) was
used to extend a 130-nucleotide fragment, whose size was estimated
relative to the migration of end-labeled, HaeIII-digested
X DNA.
Cell Culture
Mouse Y1 adrenocortical, MA-10 Leydig, L-TK-
fibroblast, and T3 gonadotrope cells were cultured and transfected
in triplicate by the CaPO4 precipitation technique (23) or
by lipofectamine (4), using 0.5–2.5 µg of the reporter gene. Levels
of hGH were assayed by RIA or Northern analysis 48 h after
transfection. In experiments with cAMP stimulation, cells were treated
with either 8-Br-cAMP for 12 h (Y1 studies) or
(Bu)2cAMP for 2–24 h (MA-10 studies). Total RNA was
isolated by the guanidinium isothiocyanate method using a standard
protocol and subjected to Northern blot analyses using standard methods
(23).
Reverse Transcription-PCR
MA-10 Leydig cells were either treated or untreated for 2 h
with 1 mM (Bu)2cAMP alone plus 10 µg/ml
actinomycin D or plus 7 µg/ml cycloheximide. Total RNA was extracted
using the Trizol reagent (Life Technologies, Gaithersburg, MA) and
semiquantitative reverse transcription-PCR was used to measure StAR
mRNA levels. Random hexamer oligonucleotides (Pharmacia-LKB,
Piscataway, NJ) were used for the RT reaction, which contained
deoxy-NTPs, RNAsin, 2.5 mM MgCl2, 200 U Moloney
murine leukemia virus-reverse transcriptase (Life Technologies) and 1
µg total RNA. For amplification of the cDNA, the reaction was
"spiked" with [32P]deoxy-CTP to radiolabel the
amplification products. After 25 cycles of amplification, the PCR
products were separated on a 2% agarose gel, the gel was dried and
exposed to a phosphoscreen, and the products were visualized and
quantitated using a Molecular Dynamics PSF PhosphoImager (Sunnyvale,
CA). StAR mRNA levels were normalized to ß-actin mRNA levels to
determine the effect of treatment on StAR expression.
Gel Mobility Shift Assays
Complementary oligonucleotides corresponding to each of the
putative SF-1 sequences were synthesized, annealed, and end labeled by
Klenow fill-in reaction; these duplex oligonucleotides included SF-1-1
(5'-CCTCCCACCTTGGCCA-3', positions -142 to -126) and
SF-1-2 (5'-TGCACAGCCTTCCACG-3', positions -49 to -34). Gel
mobility shift assays were performed essentially as previously
described (14). Briefly, labeled probes were incubated with 10 µg Y1
adrenocortical cell nuclear extract and 4 µg
poly[d(I-C)]-poly-[d(I-C)] as nonspecific competitor. Where
indicated, either unlabeled oligonucleotide competitors or antiserum
specific for SF-1 were preincubated with the nuclear extract before
probe addition. Samples were analyzed by electrophoresis on a 4%
nondenaturing polyacrylamide gel. Gels were dried and exposed to x-ray
film overnight.
In Situ Hybridization
Serial sagittal sections (6 µm) were deparaffinized and
hybridized overnight at 50–55 C using an in situ
hybridization kit according to recommended protocol.
35S-Labeled complementary RNA probes were prepared using T3
and T7 polymerases according to the protocol supplied with a kit
purchased from Novagen (Madison, WI). After washes at high stringency,
the slides were dipped in Kodak NTB-2 emulsion (Eastman Kodak,
Rochester, NY) diluted 1:1. Exposures were carried out for 3–4 weeks.
After exposure, slides were developed in Kodak D-19, fixed, and
counterstained with methyl green. Both sense and antisense probes
derived from the mouse StAR cDNA (5) were used, and all hybridizations
included a control section of adult mouse adrenal gland.
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ACKNOWLEDGMENTS |
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T3 cells; Drs. Deepak Lala, Cameron Scarlett, Jerry Strauss,
and Walter Miller for helpful discussions; and Jeana Meade, LeeAnn
Baity, and Rebecca Combs for superb technical assistance. |
FOOTNOTES |
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This work was supported by the Howard Hughes Medical Institute; NIH Grants HL-48460 (to K.L.P.), HD-17481 (to D.M.S.), and DK-51656-01 (to B.J.C.); and NIEHS Grant ES06832-03 (to B.J.C.).
Received for publication February 19, 1996. Revision received October 17, 1996. Accepted for publication November 5, 1996.
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMATERIALS AND METHODSREFERENCES |
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C. P. Houk, E. J. Pearson, N. Martinelle, P. K. Donahoe, and J. Teixeira Feedback Inhibition of Steroidogenic Acute Regulatory Protein Expression in Vitro and in Vivo by Androgens Endocrinology, March 1, 2004; 145(3): 1269 - 1275. [Abstract] [Full Text] [PDF]
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B. Borud, G. Mellgren, J. Lund, and M. Bakke Cloning and Characterization of a Novel Zinc Finger Protein that Modulates the Transcriptional Activity of Nuclear Receptors Mol. Endocrinol., November 1, 2003; 17(11): 2303 - 2319. [Abstract] [Full Text] [PDF]
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T. Sugawara, H. Shimizu, N. Hoshi, A. Nakajima, and S. Fujimoto Steroidogenic Acute Regulatory Protein-binding Protein Cloned by a Yeast Two-hybrid System J. Biol. Chem., October 24, 2003; 278(43): 42487 - 42494. [Abstract] [Full Text] [PDF]
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L. J. Whale, D. C. Eckery, and J. L. Juengel Determination of Steroidogenic Potential of Ovarian Cells of the Brushtail Possum (Trichosurus vulpecula) Biol Reprod, September 1, 2003; 69(3): 947 - 958. [Abstract] [Full Text] [PDF]
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S. Gambaryan, E. Butt, K. Marcus, M. Glazova, A. Palmetshofer, G. Guillon, and A. Smolenski cGMP-dependent Protein Kinase Type II Regulates Basal Level of Aldosterone Production by Zona Glomerulosa Cells without Increasing Expression of the Steroidogenic Acute Regulatory Protein Gene J. Biol. Chem., August 8, 2003; 278(32): 29640 - 29648. [Abstract] [Full Text] [PDF]
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X. Wang, M. T. Dyson, Y. Jo, and D. M. Stocco Inhibition of Cyclooxygenase-2 Activity Enhances Steroidogenesis and Steroidogenic Acute Regulatory Gene Expression in MA-10 Mouse Leydig Cells Endocrinology, August 1, 2003; 144(8): 3368 - 3375. [Abstract] [Full Text] [PDF]
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T. Yazawa, T. Mizutani, K. Yamada, H. Kawata, T. Sekiguchi, M. Yoshino, T. Kajitani, Z. Shou, and K. Miyamoto Involvement of Cyclic Adenosine 5'-Monophosphate Response Element-Binding Protein, Steroidogenic Factor 1, and Dax-1 in the Regulation of Gonadotropin-Inducible Ovarian Transcription Factor 1 Gene Expression by Follicle-Stimulating Hormone in Ovarian Granulosa Cells Endocrinology, May 1, 2003; 144(5): 1920 - 1930. [Abstract] [Full Text] [PDF]
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H. Schwarzenbach, P. R. Manna, D. M. Stocco, G. Chakrabarti, and A. K. Mukhopadhyay Stimulatory Effect of Progesterone on the Expression of Steroidogenic Acute Regulatory Protein in MA-10 Leydig Cells Biol Reprod, March 1, 2003; 68(3): 1054 - 1063. [Abstract] [Full Text] [PDF]
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P. R. Manna, I. T. Huhtaniemi, X.-J. Wang, D. W. Eubank, and D. M. Stocco Mechanisms of Epidermal Growth Factor Signaling: Regulation of Steroid Biosynthesis and the Steroidogenic Acute Regulatory Protein in Mouse Leydig Tumor Cells Biol Reprod, November 1, 2002; 67(5): 1393 - 1404. [Abstract] [Full Text] [PDF]
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H. Takemori, Y. Katoh, N. Horike, J. Doi, and M. Okamoto ACTH-induced Nucleocytoplasmic Translocation of Salt-inducible Kinase. IMPLICATION IN THE PROTEIN KINASE A-ACTIVATED GENE TRANSCRIPTION IN MOUSE ADRENOCORTICAL TUMOR CELLS J. Biol. Chem., October 25, 2002; 277(44): 42334 - 42343. [Abstract] [Full Text] [PDF]
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H. Osman, C. Murigande, A. Nadakal, and A. M. Capponi Repression of DAX-1 and Induction of SF-1 Expression. TWO MECHANISMS CONTRIBUTING TO THE ACTIVATION OF ALDOSTERONE BIOSYNTHESIS IN ADRENAL GLOMERULOSA CELLS J. Biol. Chem., October 18, 2002; 277(43): 41259 - 41267. [Abstract] [Full Text] [PDF]
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J. J. Tremblay, F. Hamel, and R. S. Viger Protein Kinase A-Dependent Cooperation between GATA and CCAAT/Enhancer-Binding Protein Transcription Factors Regulates Steroidogenic Acute Regulatory Protein Promoter Activity Endocrinology, October 1, 2002; 143(10): 3935 - 3945. [Abstract] [Full Text] [PDF]
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M. Jakacka, M. Ito, F. Martinson, T. Ishikawa, E. J. Lee, and J. L. Jameson An Estrogen Receptor (ER){alpha} Deoxyribonucleic Acid-Binding Domain Knock-In Mutation Provides Evidence for Nonclassical ER Pathway Signaling in Vivo Mol. Endocrinol., October 1, 2002; 16(10): 2188 - 2201. [Abstract] [Full Text] [PDF]
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J. von Hofsten, J. Karlsson, I. Jones, and P.-E. Olsson Expression and Regulation of Fushi Tarazu Factor-1 and Steroidogenic Genes During Reproduction in Arctic Char (Salvelinus alpinus) Biol Reprod, October 1, 2002; 67(4): 1297 - 1304. [Abstract] [Full Text] [PDF]
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P. R. Manna, M. T. Dyson, D. W. Eubank, B. J. Clark, E. Lalli, P. Sassone-Corsi, A. J. Zeleznik, and D. M. Stocco Regulation of Steroidogenesis and the Steroidogenic Acute Regulatory Protein by a Member of the cAMP Response-Element Binding Protein Family Mol. Endocrinol., January 1, 2002; 16(1): 184 - 199. [Abstract] [Full Text] [PDF]
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R. AEsoy, G. Mellgren, K.-I. Morohashi, and J. Lund Activation of cAMP-Dependent Protein Kinase Increases the Protein Level of Steroidogenic Factor-1 Endocrinology, January 1, 2002; 143(1): 295 - 303. [Abstract] [Full Text] [PDF]
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D. M. Stocco Tracking the Role of a StAR in the Sky of the New Millennium Mol. Endocrinol., August 1, 2001; 15(8): 1245 - 1254. [Abstract] [Full Text] [PDF]
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B. D. Murphy, E. Lalli, L. P. Walsh, Z. Liu, J. Soh, D. M. Stocco, and P. Sassone-Corsi Heat Shock Interferes with Steroidogenesis by Reducing Transcription of the Steroidogenic Acute Regulatory Protein Gene Mol. Endocrinol., August 1, 2001; 15(8): 1255 - 1263. [Abstract] [Full Text] [PDF]
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T. Sugawara, S. Abe, N. Sakuragi, Y. Fujimoto, E. Nomura, K. Fujieda, M. Saito, and S. Fujimoto RIP 140 Modulates Transcription of the Steroidogenic Acute Regulatory Protein Gene through Interactions with Both SF-1 and DAX-1 Endocrinology, August 1, 2001; 142(8): 3570 - 3577. [Abstract] [Full Text] [PDF]
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A. L. Johnson and J. T. Bridgham Regulation of Steroidogenic Acute Regulatory Protein and Luteinizing Hormone Receptor Messenger Ribonucleic Acid in Hen Granulosa Cells Endocrinology, July 1, 2001; 142(7): 3116 - 3124. [Abstract] [Full Text] [PDF]
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C. Mauduit, I. Goddard, V. Besset, E. Tabone, C. Rey, F. Gasnier, F. Dacheux, and M. Benahmed Leukemia Inhibitory Factor Antagonizes Gonadotropin Induced-Testosterone Synthesis in Cultured Porcine Leydig Cells: Sites of Action Endocrinology, June 1, 2001; 142(6): 2509 - 2520. [Abstract] [Full Text] [PDF]
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P. de Santa Barbara, C. Méjean, B. Moniot, M.-H. Malclès, P. Berta, and B. Boizet-Bonhoure Steroidogenic Factor-1 Contributes to the Cyclic-Adenosine Monophosphate Down-Regulation of Human SRY Gene Expression Biol Reprod, March 1, 2001; 64(3): 775 - 783. [Abstract] [Full Text]
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C. Aigueperse, P. Val, C. Pacot, C. Darne, E. Lalli, P. Sassone-Corsi, G. Veyssiere, C. Jean, and A. Martinez SF-1 (Steroidogenic Factor-1), C/EBP{beta} (CCAAT/Enhancer Binding Protein), and Ubiquitous Transcription Factors NF1 (Nuclear Factor 1) and Sp1 (Selective Promoter Factor 1) Are Required for Regulation of the Mouse Aldose Reductase-Like Gene (AKR1B7) Expression in Adrenocortical Cells Mol. Endocrinol., January 1, 2001; 15(1): 93 - 111. [Abstract] [Full Text]
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L. K. Christenson, T. F. Osborne, J. M. McAllister, and J. F. Strauss III Conditional Response of the Human Steroidogenic Acute Regulatory Protein Gene Promoter to Sterol Regulatory Element Binding Protein-1a Endocrinology, January 1, 2001; 142(1): 28 - 36. [Abstract] [Full Text] [PDF]
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P. R. Manna, J. Kero, M. Tena-Sempere, P. Pakarinen, D. M. Stocco, and I. T. Huhtaniemi Assessment of Mechanisms of Thyroid Hormone Action in Mouse Leydig Cells: Regulation of the Steroidogenic Acute Regulatory Protein, Steroidogenesis, and Luteinizing Hormone Receptor Function Endocrinology, January 1, 2001; 142(1): 319 - 331. [Abstract] [Full Text] [PDF]
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G. Zhang, J. C. Garmey, and J. D. Veldhuis Interactive Stimulation by Luteinizing Hormone and Insulin of the Steroidogenic Acute Regulatory (StAR) Protein and 17{alpha}-Hydroxylase/17, 20-Lyase (CYP17) Genes in Porcine Theca Cells Endocrinology, August 1, 2000; 141(8): 2735 - 2742. [Abstract] [Full Text] [PDF]
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T. Sugawara, M. Saito, and S. Fujimoto Sp1 and SF-1 Interact and Cooperate in the Regulation of Human Steroidogenic Acute Regulatory Protein Gene Expression Endocrinology, August 1, 2000; 141(8): 2895 - 2903. [Abstract] [Full Text] [PDF]
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 J. K. Wickenheisser, P. G. Quinn, V. L. Nelson, R. S. Legro, J. F. Strauss III, and J. M. McAllister. Differential Activity of the Cytochrome P450 17{alpha}-Hydroxylase and Steroidogenic Acute Regulatory Protein Gene Promoters in Normal and Polycystic Ovary Syndrome Theca Cells J. Clin. Endocrinol. Metab., June 1, 2000; 85(6): 2304 - 2311. [Abstract] [Full Text]
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C. Le Roy, J. Y. Li, D. M. Stocco, D. Langlois, and J. M. Saez Regulation by Adrenocorticotropin (ACTH), Angiotensin II, Transforming Growth Factor-{beta}, and Insulin-Like Growth Factor I of Bovine Adrenal Cell Steroidogenic Capacity and Expression of ACTH Receptor, Steroidogenic Acute Regulatory Protein, Cytochrome P450c17, and 3{beta}-Hydroxysteroid Dehydrogenase Endocrinology, May 1, 2000; 141(5): 1599 - 1607. [Abstract] [Full Text] [PDF]
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C. R. Wooton-Kee and B. J. Clark Steroidogenic Factor-1 Influences Protein-Deoxyribonucleic Acid Interactions within the Cyclic Adenosine 3',5'-Monophosphate-Responsive Regions of the Murine Steroidogenic Acute Regulatory Protein Gene Endocrinology, April 1, 2000; 141(4): 1345 - 1355. [Abstract] [Full Text] [PDF]
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B. J. Clark and R. Combs Angiotensin II and Cyclic Adenosine 3',5'-Monophosphate Induce Human Steroidogenic Acute Regulatory Protein Transcription through a Common Steroidogenic Factor-1 Element Endocrinology, October 1, 1999; 140(10): 4390 - 4398. [Abstract] [Full Text]
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L. K. Christenson, P. F. Johnson, J. M. McAllister, and J. F. Strauss III CCAAT/Enhancer-binding Proteins Regulate Expression of the Human Steroidogenic Acute Regulatory Protein (StAR) Gene J. Biol. Chem., September 10, 1999; 274(37): 26591 - 26598. [Abstract] [Full Text] [PDF]
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K. Kawabe, T. Shikayama, H. Tsuboi, S. Oka, K. Oba, T. Yanase, H. Nawata, and K.-i. Morohashi Dax-1 as One of the Target Genes of Ad4BP/SF-1 Mol. Endocrinol., August 1, 1999; 13(8): 1267 - 1284. [Abstract] [Full Text]
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E. Silverman, S. Eimerl, and J. Orly CCAAT Enhancer-binding Protein beta and GATA-4 Binding Regions within the Promoter of the Steroidogenic Acute Regulatory Protein (StAR) Gene Are Required for Transcription in Rat Ovarian Cells J. Biol. Chem., June 18, 1999; 274(25): 17987 - 17996. [Abstract] [Full Text] [PDF]
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A. J. Reinhart, S. C. Williams, B. J. Clark, and D. M. Stocco SF-1 (Steroidogenic Factor-1) and C/EBP{beta} (CCAAT/Enhancer Binding Protein-{beta}) Cooperate to Regulate the Murine StAR (Steroidogenic Acute Regulatory) Promoter Mol. Endocrinol., May 1, 1999; 13(5): 729 - 741. [Abstract] [Full Text]
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M. Kanzaki and P. L. Morris Growth Hormone Regulates Steroidogenic Acute Regulatory Protein Expression and Steroidogenesis in Leydig Cell Progenitors Endocrinology, April 1, 1999; 140(4): 1681 - 1686. [Abstract] [Full Text]
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P. R. Manna, P. Pakarinen, T. El-Hefnawy, and I. T. Huhtaniemi Functional Assessment of the Calcium Messenger System in Cultured Mouse Leydig Tumor Cells: Regulation of Human Chorionic Gonadotropin-Induced Expression of the Steroidogenic Acute Regulatory Protein Endocrinology, April 1, 1999; 140(4): 1739 - 1751. [Abstract] [Full Text]
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R. Mamluk, Y. Greber, and R. Meidan Hormonal Regulation of Messenger Ribonucleic Acid Expression for Steroidogenic Factor-1, Steroidogenic Acute Regulatory Protein, and Cytochrome P450 Side-Chain Cleavage in Bovine Luteal Cells Biol Reprod, March 1, 1999; 60(3): 628 - 634. [Abstract] [Full Text]
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 K.-i. Morohashi, H. Tsuboi-Asai, S. Matsushita, M. Suda, M. Nakashima, H. Sasano, Y. Hataba, C.-L. Li, J. Fukata, J. Irie, et al. Structural and Functional Abnormalities in the Spleen of an mFtz-F1 Gene-Disrupted Mouse Blood, March 1, 1999; 93(5): 1586 - 1594. [Abstract] [Full Text] [PDF]
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P. R. Manna, M. Tena-Sempere, and I. T. Huhtaniemi Molecular Mechanisms of Thyroid Hormone-stimulated Steroidogenesis in Mouse Leydig Tumor Cells. INVOLVEMENT OF THE STEROIDOGENIC ACUTE REGULATORY () PROTEIN J. Biol. Chem., February 26, 1999; 274(9): 5909 - 5918. [Abstract] [Full Text] [PDF]
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H. A. LaVoie, J. C. Garmey, and J. D. Veldhuis Mechanisms of Insulin-Like Growth Factor I Augmentation of Follicle-Stimulating Hormone-Induced Porcine Steroidogenic Acute Regulatory Protein Gene Promoter Activity in Granulosa Cells Endocrinology, January 1, 1999; 140(1): 146 - 153. [Abstract] [Full Text]
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T. W. Sandhoff, D. B. Hales, K. H. Hales, and M. P. McLean Transcriptional Regulation of the Rat Steroidogenic Acute Regulatory Protein Gene by Steroidogenic Factor 1 Endocrinology, December 1, 1998; 139(12): 4820 - 4831. [Abstract] [Full Text] [PDF]
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L. K. Christenson, J. M. McAllister, K. O. Martin, N. B. Javitt, T. F. Osborne, and J. F. Strauss III Oxysterol Regulation of Steroidogenic Acute Regulatory Protein Gene Expression. STRUCTURAL SPECIFICITY AND TRANSCRIPTIONAL AND POSTTRANSCRIPTIONAL ACTIONS J. Biol. Chem., November 13, 1998; 273(46): 30729 - 30735. [Abstract] [Full Text] [PDF]
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E. Lalli, M. H. Melner, D. M. Stocco, and P. Sassone-Corsi DAX-1 Blocks Steroid Production at Multiple Levels Endocrinology, October 1, 1998; 139(10): 4237 - 4243. [Abstract] [Full Text] [PDF]
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N. Cherradi, Y. Brandenburger, M. F. Rossier, M. B. Vallotton, D. M. Stocco, and A. M. Capponi Atrial Natriuretic Peptide Inhibits Calcium-Induced Steroidogenic Acute Regulatory Protein Gene Transcription in Adrenal Glomerulosa Cells Mol. Endocrinol., July 1, 1998; 12(7): 962 - 972. [Abstract] [Full Text]
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C. Mauduit, F. Gasnier, C. Rey, M.-A. Chauvin, D. M. Stocco, P. Louisot, and M. Benahmed Tumor Necrosis Factor-{alpha} Inhibits Leydig Cell Steroidogenesis through a Decrease in Steroidogenic Acute Regulatory Protein Expression Endocrinology, June 1, 1998; 139(6): 2863 - 2868. [Abstract] [Full Text] [PDF]
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 P. A. Crawford, C. Dorn, Y. Sadovsky, and J. Milbrandt Nuclear Receptor DAX-1 Recruits Nuclear Receptor Corepressor N-CoR to Steroidogenic Factor 1 Mol. Cell. Biol., May 1, 1998; 18(5): 2949 - 2956. [Abstract] [Full Text]
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 Y. Sadovsky and P. A. Crawford Developmental and Physiologic Roles of the Nuclear Receptor Steroidogenic Factor-I in the Reproductive System Reproductive Sciences, January 1, 1998; 5(1): 6 - 12. [Abstract] [PDF]
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D. Nalbant, S. C. Williams, D. M. Stocco, and S. A. Khan Luteinizing Hormone-Dependent Gene Regulation in Leydig Cells May Be Mediated by CCAAT/Enhancer-Binding Protein-{beta} Endocrinology, January 1, 1998; 139(1): 272 - 279. [Abstract] [Full Text] [PDF]
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G. Cao, C. K. Garcia, K. L. Wyne, R. A. Schultz, K. L. Parker, and H. H. Hobbs Structure and Localization of the Human Gene Encoding SR-BI/CLA-1. EVIDENCE FOR TRANSCRIPTIONAL CONTROL BY STEROIDOGENIC FACTOR 1 J. Biol. Chem., December 26, 1997; 272(52): 33068 - 33076. [Abstract] [Full Text] [PDF]
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B. J. Clark, R. Combs, K. H. Hales, D. B. Hales, and D. M. Stocco Inhibition of Transcription Affects Synthesis of Steroidogenic Acute Regulatory Protein and Steroidogenesis in MA-10 Mouse Leydig Tumor Cells Endocrinology, November 1, 1997; 138(11): 4893 - 4901. [Abstract] [Full Text] [PDF]
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 K. L. Parker and B. P. Schimmer Steroidogenic Factor 1: A Key Determinant of Endocrine Development and Function Endocr. Rev., June 1, 1997; 18(3): 361 - 377. [Abstract] [Full Text]
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X. Wang, L. P. Walsh, A. J. Reinhart, and D. M. Stocco The Role of Arachidonic Acid in Steroidogenesis and Steroidogenic Acute Regulatory (StAR) Gene and Protein Expression J. Biol. Chem., June 23, 2000; 275(26): 20204 - 20209. [Abstract] [Full Text] [PDF]
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M. E. Reyland, R. M. Evans, and E. K. White Lipoproteins Regulate Expression of the Steroidogenic Acute Regulatory Protein (StAR) in Mouse Adrenocortical Cells J. Biol. Chem., November 17, 2000; 275(47): 36637 - 36644. [Abstract] [Full Text] [PDF]
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