Abstract
Steroidogenic factor 1 (SF-1), an orphan member of the intracellular receptor superfamily, plays an essential role in the development and function of multiple endocrine organs. It is expressed in all steroidogenic tissues where it regulates the P450 steroidogenic genes to generate physiologically active steroids. Although many of the functions of SF-1 in vivo have been defined, an unresolved question is whether a ligand modulates its transcriptional activity. Here, we show that 25-, 26-, or 27-hydroxycholesterol, known suppressors of cholesterol biosynthesis, enhance SF-1-dependent transcriptional activity. This activation is dependent upon the SF-1 activation function domain, and, is specific for SF-1 as several other receptors do not respond to these molecules. The oxysterols activate at concentrations comparable to those previously shown to inhibit cholesterol biosynthesis, and, can be derived from cholesterol by P450c27, an enzyme expressed within steroidogenic tissues. Recent studies have shown that the nuclear receptor LXR also is activated by oxysterols. We demonstrate that different oxysterols differ in their rank order potency for these two receptors, with 25-hydroxycholesterol preferentially activating SF-1 and 22(R)-hydroxycholesterol preferentially activating LXR. These results suggest that specific oxysterols may mediate transcriptional activation via different intracellular receptors. Finally, ligand-dependent transactivation of SF-1 by oxysterols may play an important role in enhancing steroidogenesis in vivo.
MeSH Terms
Amino Acid Sequence
Animals
Binding Sites
Cell Line
Chlorocebus aethiops
DNA-Binding Proteins/biosynthesis,drug effects,physiology
Fushi Tarazu Transcription Factors
Green Fluorescent Proteins
Homeodomain Proteins
Humans
Hydroxycholesterols/pharmacology
Kinetics
Luminescent Proteins/biosynthesis
Molecular Sequence Data
Receptors, Cytoplasmic and Nuclear/biosynthesis,drug effects,physiology
Receptors, Thyroid Hormone/physiology
Recombinant Fusion Proteins/metabolism
Sequence Homology, Amino Acid
Steroidogenic Factor 1
Transcription Factors/biosynthesis,drug effects,physiology
Transcription, Genetic/drug effects
Transfection
Chemicals
DNA-Binding Proteins
Fushi Tarazu Transcription Factors
Homeodomain Proteins
Hydroxycholesterols
Luminescent Proteins
NR5A1 protein, human
Receptors, Cytoplasmic and Nuclear
Receptors, Thyroid Hormone
Recombinant Fusion Proteins
Steroidogenic Factor 1
Transcription Factors
cholest-5-ene-3 beta,26-diol
Green Fluorescent Proteins
22-hydroxycholesterol
27-hydroxycholesterol
25-hydroxycholesterol
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lala D S
Departments of Orphan Nuclear Receptor and Retinoid Research, Ligand Pharmaceuticals, 10255 Science Center Drive, San Diego, CA 92121, USA.
Syka P M
Lazarchik S B
Mangelsdorf D J
Parker K L
Heyman R A
References (30)
30 references, click to expand
-
A cell-specific nuclear receptor is essential for adrenal and gonadal development and sexual differentiation.
Cell. 1994 May 20;77(4):481-90
PMID: 8187173
-
SREBP-1, a membrane-bound transcription factor released by sterol-regulated proteolysis.
Cell. 1994 Apr 8;77(1):53-62
PMID: 8156598
-
The nuclear receptor steroidogenic factor 1 acts at multiple levels of the reproductive axis.
Genes Dev. 1994 Oct 1;8(19):2302-12
PMID: 7958897
-
Role of steroidogenic acute regulatory protein in adrenal and gonadal steroidogenesis.
Science. 1995 Mar 24;267(5205):1828-31
PMID: 7892608
-
LXR, a nuclear receptor that defines a distinct retinoid response pathway.
Genes Dev. 1995 May 1;9(9):1033-45
PMID: 7744246
-
Identification of a nuclear receptor that is activated by farnesol metabolites.
Cell. 1995 Jun 2;81(5):687-93
PMID: 7774010
-
A cell-specific nuclear receptor regulates the steroid hydroxylases.
Steroids. 1995 Jan;60(1):10-4
PMID: 7792792
-
Low density lipoprotein (LDL) cholesterol is converted to 27-hydroxycholesterol in human fibroblasts. Evidence that 27-hydroxycholesterol can be an important intracellular mediator between LDL and the suppression of cholesterol production.
J Biol Chem. 1995 Jun 23;270(25):15102-10
PMID: 7797494
-
A novel nonhepatic hydroxycholesterol 7 alpha-hydroxylase that is markedly stimulated by interleukin-1 beta. Characterization in the immature rat ovary.
J Biol Chem. 1995 Aug 11;270(32):18888-96
PMID: 7642545
-
Use of an 18O2 inhalation technique and mass isotopomer distribution analysis to study oxygenation of cholesterol in rat. Evidence for in vivo formation of 7-oxo-, 7 beta-hydroxy-, 24-hydroxy-, and 25-hydroxycholesterol.
J Biol Chem. 1995 Sep 1;270(35):20278-84
PMID: 7657597
-
Structure of the human steroidogenic acute regulatory protein (StAR) gene: StAR stimulates mitochondrial cholesterol 27-hydroxylase activity.
Biochemistry. 1995 Oct 3;34(39):12506-12
PMID: 7547998
-
Autoregulatory loop in the regulation of the mammalian ftz-f1 gene.
J Biol Chem. 1996 Apr 5;271(14):8243-9
PMID: 8626518
-
Steroidogenic factor 1-dependent promoter activity of the human steroidogenic acute regulatory protein (StAR) gene.
Biochemistry. 1996 Jul 16;35(28):9052-9
PMID: 8703908
-
An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha.
Nature. 1996 Oct 24;383(6602):728-31
PMID: 8878485
-
The isolation of crystalline 22R-hydroxycholesterol and 20 alpha, 22R-dihydroxycholesterol from bovine adrenals.
Biochem Biophys Res Commun. 1970 Jul 13;40(1):161-5
PMID: 5456952
-
Biosynthesis of cholest-5-ene-3beta, 24-diol (cerebrosterol) by bovine cerebral cortical microsomes.
J Neurochem. 1973 Jul;21(1):51-60
PMID: 4146460
-
Biological activity of some oxygenated sterols.
Science. 1978 Aug 11;201(4355):498-501
PMID: 663671
-
Side chain cleavage of hydroxylated sterols by bovine adrenal cortex mitochondria: observation of 25-hydroxylase activity during incubation at pH 7.80.
J Steroid Biochem. 1980 May;13(5):539-43
PMID: 7392630
-
26-Hydroxycholesterol. Identification and quantitation in human serum.
J Biol Chem. 1981 Dec 25;256(24):12644-6
PMID: 7309726
-
Identification of regulatory oxysterols, 24(S),25-epoxycholesterol and 25-hydroxycholesterol, in cultured fibroblasts.
J Biol Chem. 1985 Nov 25;260(27):14571-9
PMID: 4055791
-
Oxysterol regulators of 3-hydroxy-3-methylglutaryl-CoA reductase in liver. Effect of dietary cholesterol.
J Biol Chem. 1989 Apr 25;264(12):6863-9
PMID: 2708346
-
Cloning, structure, and expression of the mitochondrial cytochrome P-450 sterol 26-hydroxylase, a bile acid biosynthetic enzyme.
J Biol Chem. 1989 May 15;264(14):8222-9
PMID: 2722778
-
Cloning and regulation of cholesterol 7 alpha-hydroxylase, the rate-limiting enzyme in bile acid biosynthesis.
J Biol Chem. 1990 May 15;265(14):8190-7
PMID: 2335522
-
Generation of regulatory oxysterols: 26-hydroxylation of cholesterol by ovarian mitochondria.
Endocrinology. 1990 Aug;127(2):738-46
PMID: 2373053
-
Characterization of human sterol 27-hydroxylase. A mitochondrial cytochrome P-450 that catalyzes multiple oxidation reaction in bile acid biosynthesis.
J Biol Chem. 1991 Apr 25;266(12):7774-8
PMID: 1708392
-
Cholesterol biosynthesis and metabolism.
Cardiovasc Drugs Ther. 1992 Apr;6(2):103-10
PMID: 1390320
-
Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I.
Mol Endocrinol. 1992 Aug;6(8):1249-58
PMID: 1406703
-
Identification of residues in the estrogen receptor that confer differential sensitivity to estrogen and hydroxytamoxifen.
Mol Endocrinol. 1993 Feb;7(2):232-40
PMID: 8469236
-
Characterization of the mouse FTZ-F1 gene, which encodes a key regulator of steroid hydroxylase gene expression.
Mol Endocrinol. 1993 Jul;7(7):852-60
PMID: 8413309
-
Activation function 2 (AF-2) of retinoic acid receptor and 9-cis retinoic acid receptor: presence of a conserved autonomous constitutive activating domain and influence of the nature of the response element on AF-2 activity.
EMBO J. 1994 Nov 15;13(22):5370-82
PMID: 7957103