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Molecular Endocrinology, Vol 10, 147-158, Copyright © 1996 by Endocrine Society

ARTICLES

The orphan nuclear receptor steroidogenic factor-1 regulates the cyclic adenosine 3',5'-monophosphate-mediated transcriptional activation of rat cytochrome P450c17 (17 alpha-hydroxylase/c17-20 lyase)

P Zhang and SH Mellon
Department of Obstetrics & Gynecology, University of California, San Francisco 94143-0556, USA.

The rat steroid cytochrome P450 17 alpha-hydroxylase/c17-20 lyase (rP450c17) gene is transcriptionally regulated in steroidogenic tissues. Previous studies showed that one DNA element located between - 75 and -50 base pairs (bp) upstream from the transcriptional initiation site mediated both the basal and cAMP-regulated transcription of rP450c17. Using a series of mutant oligonucleotides in gel mobility shift assays and in functional assays, it is now shown that a core sequence of 12 bp, located at -58/-69 bp, is essential for nuclear protein binding and transcriptional activation. Mutant oligonucleotides cloned into a luciferase reporter gene construct containing a heterologous thymidine kinase promoter, transfected into mouse Leydig MA-10 and adrenocortical Y-1 cells, gave results consistent with those of gel shift assays. Mutants that abolished binding of the nuclear protein to DNA abolished the basal transcription of the gene as well as the responsiveness to cAMP, whereas those mutants that did not abolish binding of the nuclear protein to DNA still showed strong basal transcription as well as responsiveness to cAMP. Comparison of the binding sequence with the consensus binding site for the orphan nuclear receptor steroidogenic factor-1 (SF-1) showed that eight of nine bases were identical. However, the sequence from rP450c17 includes an additional three bases at the 5'-end, not previously demonstrated to be important for SF-1 binding. Recombinant rat SF-1 protein expressed in Escherichia coli binds to this sequence, and antibodies raised against rat SF-1 abolish binding of both recombinant SF-1 and the nuclear protein from Y-1 and MA-10 cells. These observations demonstrate that this region of the rP450c17 gene is responsible for both the basal transcription and cAMP inducibility and is bound by the orphan nuclear receptor SF-1. It is further shown that SF-1 can be phosphorylated in vitro by protein kinase A. This phosphorylation occurs at serine and threonine residues and results in decreased binding to the rP450c17 - 58/-69 element. Since SF-1 mediates cAMP-induced transcriptional regulation of the rat P450c17 gene, phosphorylation of SF-1 via protein kinase A is likely to play a regulatory role in transcriptional activation.


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R. K. Srivastava, Y. N. Lee, K. Noguchi, Y. G. Park, M. J. C. Ellis, J.-S. Jeong, S. N. Kim, and Y. S. Cho-Chung
The RIIbeta regulatory subunit of protein kinase A binds to cAMP response element: An alternative cAMP signaling pathway
PNAS, June 9, 1998; 95(12): 6687 - 6692.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. L. Jacob and J. Lund
Mutations in the Activation Function-2 Core Domain of Steroidogenic Factor-1 Dominantly Suppresses PKA-dependent Transactivation of the Bovine CYP17 Gene
J. Biol. Chem., May 29, 1998; 273(22): 13391 - 13394.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
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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 EndocrinologyHome page
J. M. Burrin, S. J. B. Aylwin, J. G. Holdstock, and U. Sahye
Mechanism of Action of Pituitary Adenylate Cyclase-Activating Polypeptide on Human Glycoprotein Hormone {alpha}-Subunit Transcription in {alpha}T3-1 Gonadotropes
Endocrinology, April 1, 1998; 139(4): 1731 - 1737.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Monte, F. DeWitte, and D. W. Hum
Regulation of the Human P450scc Gene by Steroidogenic Factor 1 Is Mediated by CBP/p300
J. Biol. Chem., February 20, 1998; 273(8): 4585 - 4591.
[Abstract] [Full Text] [PDF]

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 Reproductive SciencesHome page
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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 EndocrinologyHome page
Y. Li and L. F. Lau
Adrenocorticotropic Hormone Regulates the Activities of the Orphan Nuclear Receptor Nur77 through Modulation of Phosphorylation
Endocrinology, October 1, 1997; 138(10): 4138 - 4146.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
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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 Mol. Endocrinol.Home page
F. M. Cammas, G. D. Pullinger, S. Barker, and A. J. L. Clark
The Mouse Adrenocorticotropin Receptor Gene: Cloning and Characterization of Its Promoter and Evidence for a Role for the Orphan Nuclear Receptor Steroidogenic Factor 1
Mol. Endocrinol., June 1, 1997; 11(7): 867 - 876.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
D. Liu, Y. Le Drean, M. Ekker, F. Xiong, and C. L. Hew
Teleost FTZ-F1 Homolog and Its Splicing Variant Determine the Expression of the Salmon Gonadotropin II{beta} Subunit Gene
Mol. Endocrinol., June 1, 1997; 11(7): 877 - 890.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
P. Zhang and S. H. Mellon
Multiple Orphan Nuclear Receptors Converge to Regulate Rat P450c17 Gene Transcription: Novel Mechanisms for Orphan Nuclear Receptor Action
Mol. Endocrinol., June 1, 1997; 11(7): 891 - 904.
[Abstract] [Full Text]

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 EndocrinologyHome page
R. Borroni, Z. Liu, E. R. Simpson, and M. M. Hinshelwood
A Putative Binding Site for Sp1 Is Involved in Transcriptional Regulation of CYP17 Gene Expression in Bovine Ovary
Endocrinology, May 1, 1997; 138(5): 2011 - 2020.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. L. Carlone and J. S. Richards
Functional Interactions, Phosphorylation, and Levels of 3',5'-Cyclic Adenosine Monophosphate-Regulatory Element Binding Protein and Steroidogenic Factor-1 Mediate Hormone-Regulated and Constitutive Expression of Aromatase in Gonadal Cells
Mol. Endocrinol., March 1, 1997; 11(3): 292 - 304.
[Abstract] [Full Text]

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 EndocrinologyHome page
N. Pilon, I. Daneau, C. Brisson, J.-F. Ethier, J. G. Lussier, and D. W. Silversides
Porcine and Bovine Steroidogenic Acute Regulatory Protein (StAR) Gene Expression during Gestation
Endocrinology, March 1, 1997; 138(3): 1085 - 1091.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
H. Rodriguez, D. W. Hum, B. Staels, and W. L. Miller
Transcription of the Human Genes for Cytochrome P450scc and P450c17 Is Regulated Differently in Human Adrenal NCI-H295 Cells Than in Mouse Adrenal Y1 Cells
J. Clin. Endocrinol. Metab., February 1, 1997; 82(2): 365 - 371.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
Z. Liu and E. R. Simpson
Steroidogenic Factor 1 (SF-1) and SP1 Are Required for Regulation of Bovine CYP11A Gene Expression in Bovine Luteal Cells and Adrenal Y1 Cells
Mol. Endocrinol., February 1, 1997; 11(2): 127 - 137.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
B. Staels, G. Martin, M. Martinez, C. Albert, J. Peinado-Onsurbe, R. Saladin, D. W. Hum, M. Reina, S. Vilaro, and J. Auwerx
Expression and Regulation of the Lipoprotein Lipase Gene in Human Adrenal Cortex
J. Biol. Chem., July 19, 1996; 271(29): 17425 - 17432.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
T. Mizutani, K. Yamada, T. Minegishi, and K. Miyamoto
Transcriptional Regulation of Rat Scavenger Receptor Class B Type I Gene
J. Biol. Chem., July 14, 2000; 275(29): 22512 - 22519.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
H. Pincas, J.-N. Laverriere, and R. Counis
Pituitary Adenylate Cyclase-activating Polypeptide and Cyclic Adenosine 3',5'-Monophosphate Stimulate the Promoter Activity of the Rat Gonadotropin-releasing Hormone Receptor Gene via a Bipartite Response Element in Gonadotrope-derived Cells
J. Biol. Chem., June 22, 2001; 276(26): 23562 - 23571.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. L. Gyles, C. J. Burns, B. J. Whitehouse, D. Sugden, P. J. Marsh, S. J. Persaud, and P. M. Jones
ERKs Regulate Cyclic AMP-induced Steroid Synthesis through Transcription of the Steroidogenic Acute Regulatory (StAR) Gene
J. Biol. Chem., September 7, 2001; 276(37): 34888 - 34895.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
A. L. Jacob, J. Lund, P. Martinez, and L. Hedin
Acetylation of Steroidogenic Factor 1 Protein Regulates Its Transcriptional Activity and Recruits the Coactivator GCN5
J. Biol. Chem., September 28, 2001; 276(40): 37659 - 37664.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
K. Tamura, Y. E. Chen, M. Horiuchi, Q. Chen, L. Daviet, Z. Yang, L. Daviet, M. Lopez-Ilasaca, H. Mu, R. E. Pratt, et al.
LXRalpha functions as a cAMP-responsive transcriptional regulator of gene expression
PNAS, July 18, 2000; 97(15): 8513 - 8518.
[Abstract] [Full Text] [PDF]


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