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Molecular Endocrinology Vol. 6, No. 8 1249-1258
doi:10.1210/me.6.8.1249
Copyright © 1992 by the Endocrine Society.
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Molecular Endocrinology, Vol 6, 1249-1258, Copyright © 1992 by Endocrine Society

ARTICLES

Steroidogenic factor I, a key regulator of steroidogenic enzyme expression, is the mouse homolog of fushi tarazu-factor I

DS Lala, DA Rice and KL Parker
Department of Medicine, Howard Hughes Medical Institute, Duke University Medical Center, Durham, North Carolina 27710.

We proposed that a cell-selective regulatory protein coordinately regulates the expression of three enzymes that are required for the biosynthesis of corticosteroids: cholesterol side chain cleavage enzyme, steroid 21-hydroxylase, and the aldosterone synthase isozyme of steroid 11 beta-hydroxylase. In this report, we identify a 53- kilodalton protein, termed steroidogenic factor 1 (SF-1), that interacts with the related promoter elements from these steroidogenic enzymes, and we isolate and characterize a cDNA that very likely encodes this protein. We first showed that nuclear extracts from bovine adrenal glands interact with the mouse steroidogenic regulatory elements, forming complexes indistinguishable from those produced by nuclear extracts from mouse Y1 adrenocortical cells. These bovine adrenal extracts were subjected to sequential ion exchange and affinity chromatography to yield a highly enriched preparation of SF-1. The predominant protein in the affinity-purified preparation comigrated with shift activity and had a mol wt of 53,000; UV cross-linking experiments demonstrated directly that this 53-kilodalton protein interacted with the steroidogenic regulatory element. Even with this marked enrichment, affinity-purified SF-1 bound six steroidogenic regulatory elements. These results support strongly the model that a steroidogenic cell-selective protein interacts with related promoter elements from three steroidogenic enzymes to regulate their coordinate expression. The recognition sequence of SF-1 closely resembles those of nuclear hormone receptor family members, suggesting that SF-1 may belong to this supergene family. By screening a Y1 cell cDNA library with the DNA-binding region of the H-2RIIBP nuclear hormone receptor cDNA, we isolated a cDNA that is selectively expressed in steroidogenic cells. When expressed as a glutathione S-transferase fusion protein in Escherichia. coli, the protein encoded by this cDNA interacts with all six related steroidogenic regulatory elements with a binding specificity indistinguishable from that of SF-1. Surprisingly, the sequence of the putative DNA-binding domain of this cDNA matches exactly the corresponding sequence of the mouse homolog of the Drosophila transcription factor fushi tarazu-factor I. The demonstration that a member of the nuclear hormone receptor family interacts with the steroidogenic regulatory elements provides intriguing insights into possible mechanisms by which these essential genes are regulated.


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K. Gen, K. Okuzawa, N. Kumakura, S. Yamaguchi, and H. Kagawa
Correlation Between Messenger RNA Expression of Cytochrome P450 Aromatase and Its Enzyme Activity During Oocyte Development in the Red Seabream (Pagrus major)
Biol Reprod, October 1, 2001; 65(4): 1186 - 1194.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
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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 EndocrinologyHome page
S. B. Seminara and W. F. Crowley Jr.
Perspective: The Importance of Genetic Defects in Humans in Elucidating the Complexities of the Hypothalamic-Pituitary-Gonadal Axis
Endocrinology, June 1, 2001; 142(6): 2173 - 2177.
[Full Text] [PDF]

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 Mol. Endocrinol.Home page
L. L. Heckert
Activation of the Rat Follicle-Stimulating Hormone Receptor Promoter by Steroidogenic Factor 1 Is Blocked by Protein Kinase A and Requires Upstream Stimulatory Factor Binding to a Proximal E Box Element
Mol. Endocrinol., May 1, 2001; 15(5): 704 - 715.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
K. Yamada, T. Mizutani, Z. Shou, T. Yazawa, T. Sekiguchi, M. Yoshino, T. Inazu, and K. Miyamoto
Cloning and Functional Expression of an E Box-Binding Protein from Rat Granulosa Cells
Biol Reprod, May 1, 2001; 64(5): 1315 - 1319.
[Abstract] [Full Text]

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 EndocrinologyHome page
A. Fleming and D. Crews
Estradiol and Incubation Temperature Modulate Regulation of Steroidogenic Factor 1 in the Developing Gonad of the Red-Eared Slider Turtle
Endocrinology, April 1, 2001; 142(4): 1403 - 1411.
[Abstract] [Full Text]

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 EndocrinologyHome page
J. J. Tremblay and R. S. Viger
GATA Factors Differentially Activate Multiple Gonadal Promoters through Conserved GATA Regulatory Elements
Endocrinology, March 1, 2001; 142(3): 977 - 986.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
J. Levallet, P. Koskimies, N. Rahman, and I. Huhtaniemi
The Promoter of Murine Follicle-Stimulating Hormone Receptor: Functional Characterization and Regulation by Transcription Factor Steroidogenic Factor 1
Mol. Endocrinol., January 1, 2001; 15(1): 80 - 92.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
F. Adam, T. Sourisseau, R. Métivier, Y. Le Page, C. Desbois, D. Michel, and G. Salbert
COUP-TFI (Chicken Ovalbumin Upstream Promoter-Transcription Factor I) Regulates Cell Migration and Axogenesis in Differentiating P19 Embryonal Carcinoma Cells
Mol. Endocrinol., December 1, 2000; 14(12): 1918 - 1933.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
M. Higa, H. Kanda, T. Kitahashi, M. Ito, T. Shiba, and H. Ando
Quantitative Analysis of fushi tarazu Factor 1 Homolog Messenger Ribonucleic Acids in the Pituitary of Salmon at Different Prespawning Stages
Biol Reprod, December 1, 2000; 63(6): 1756 - 1763.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
A. Pask, M. B. Renfree, and J. A. Marshall Graves
The human sex-reversing ATRX gene has a homologue on the marsupial Y chromosome, ATRY: Implications for the evolution of mammalian sex determination
PNAS, November 2, 2000; (2000) 230424497.
[Abstract] [Full Text]

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 EndocrinologyHome page
X.-L. Wang, M. Bassett, Y. Zhang, S. Yin, C. Clyne, P. C. White, and W. E. Rainey
Transcriptional Regulation of Human 11{beta}-Hydroxylase (hCYP11B1)
Endocrinology, October 1, 2000; 141(10): 3587 - 3594.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
U. B. Kaiser, L. M. Halvorson, and M. T. Chen
Sp1, Steroidogenic Factor 1 (SF-1), and Early Growth Response Protein 1 (Egr-1) Binding Sites Form a Tripartite Gonadotropin-Releasing Hormone Response Element in the Rat Luteinizing Hormone-{beta} Gene Promoter: an Integral Role for SF-1
Mol. Endocrinol., August 1, 2000; 14(8): 1235 - 1245.
[Abstract] [Full Text]

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 Mol Hum ReprodHome page
D.R. Corley, X. Li, Z.M. Lei, and Ch.V. Rao
Potential regulation of GnRH gene by a steroidogenic factor-1-like protein
Mol. Hum. Reprod., August 1, 2000; 6(8): 671 - 676.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
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. Histochem. Cytochem.Home page
R. Y. Osamura, S. Tahara, R. Kurotani, N. Sanno, A. Matsuno, and A. Teramoto
Contributions of Immunohistochemistry and In Situ Hybridization to the Functional Analysis of Pituitary Adenomas
J. Histochem. Cytochem., April 1, 2000; 48(4): 445 - 458.
[Abstract] [Full Text]

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 EndocrinologyHome page
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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 Mol. Endocrinol.Home page
M. Ito, Y. Park, J. Weck, K. E. Mayo, and J. L. Jameson
Synergistic Activation of the Inhibin {alpha}-Promoter by Steroidogenic Factor-1 and Cyclic Adenosine 3',5'-Monophosphate
Mol. Endocrinol., January 1, 2000; 14(1): 66 - 81.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
S. D. Wijesuriya, G. Zhang, A. Dardis, and W. L. Miller
Transcriptional Regulatory Elements of the Human Gene for Cytochrome P450c21 (Steroid 21-Hydroxylase) Lie within Intron 35 of the Linked C4B Gene
J. Biol. Chem., December 31, 1999; 274(53): 38097 - 38106.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
V. Giguère
Orphan Nuclear Receptors: From Gene to Function
Endocr. Rev., October 1, 1999; 20(5): 689 - 725.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
G. Cao, L. Zhao, H. Stangl, T. Hasegawa, J. A. Richardson, K. L. Parker, and H. H. Hobbs
Developmental and Hormonal Regulation of Murine Scavenger Receptor, Class B, Type 1
Mol. Endocrinol., September 1, 1999; 13(9): 1460 - 1473.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
M. W. Wolfe
The Equine Luteinizing Hormone {beta}-Subunit Promoter Contains Two Functional Steroidogenic Factor-1 Response Elements
Mol. Endocrinol., September 1, 1999; 13(9): 1497 - 1510.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
L.-A. Li, E. F-L. Chiang, J.-C. Chen, N.-C. Hsu, Y.-J. Chen, and B.-c. Chung
Function of Steroidogenic Factor 1 Domains in Nuclear Localization, Transactivation, and Interaction with Transcription Factor TFIIB and c-Jun
Mol. Endocrinol., September 1, 1999; 13(9): 1588 - 1598.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
E. P. Fiedler, L. Jr. Plouffe, D. B. Hales, K. H. Hales, and I. Khan
Prostaglandin F2{alpha} Induces a Rapid Decline in Progesterone Production and Steroidogenic Acute Regulatory Protein Expression in Isolated Rat Corpus Luteum Without Altering Messenger Ribonucleic Acid Expression
Biol Reprod, September 1, 1999; 61(3): 643 - 650.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
P. Parma, E. Pailhoux, and C. Cotinot
Reverse Transcription-Polymerase Chain Reaction Analysis of Genes Involved in Gonadal Differentiation in Pigs
Biol Reprod, September 1, 1999; 61(3): 741 - 748.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
Y.-K. Lee, K. L. Parker, H.-S. Choi, and D. D. Moore
Activation of the Promoter of the Orphan Receptor SHP by Orphan Receptors That Bind DNA as Monomers
J. Biol. Chem., July 23, 1999; 274(30): 20869 - 20873.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. Mitani, K. Mukai, H. Miyamoto, M. Suematsu, and Y. Ishimura
Development of Functional Zonation in the Rat Adrenal Cortex
Endocrinology, July 1, 1999; 140(7): 3342 - 3353.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
M. Nitta, S. Ku, C. Brown, A. Y. Okamoto, and B. Shan
CPF: An orphan nuclear receptor that regulates liver-specific expression of the human cholesterol 7alpha -hydroxylase gene
PNAS, June 8, 1999; 96(12): 6660 - 6665.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
E. S. W. Ngan, P. K. W. Cheng, P. C. K. Leung, and B. K. C. Chow
Steroidogenic Factor-1 Interacts with a Gonadotrope-Specific Element within the First Exon of the Human Gonadotropin-Releasing Hormone Receptor Gene to Mediate Gonadotrope-Specific Expression
Endocrinology, June 1, 1999; 140(6): 2452 - 2462.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
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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 Mol. Endocrinol.Home page
M. W. Wolfe and G. B. Call
Early Growth Response Protein 1 Binds to the Luteinizing Hormone-{beta} Promoter and Mediates Gonadotropin-Releasing Hormone-Stimulated Gene Expression
Mol. Endocrinol., May 1, 1999; 13(5): 752 - 763.
[Abstract] [Full Text]

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 EndocrinologyHome page
D. Barkan, H. Jia, A. Dantes, L. Vardimon, A. Amsterdam, and M. Rubinstein
Leptin Modulates the Glucocorticoid-Induced Ovarian Steroidogenesis
Endocrinology, April 1, 1999; 140(4): 1731 - 1738.
[Abstract] [Full Text]

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 Genes Dev.Home page
A. Swain and R. Lovell-Badge
Mammalian sex determination: a molecular drama
Genes & Dev., April 1, 1999; 13(7): 755 - 767.
[Full Text]

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 EndocrinologyHome page
A. Martinez, A.-M. Lefrançois-Martinez, M. Manin, S. Guyot, C. Jean-Faucher, G. Veyssière, A. Kahn, and C. Jean
5'-Flanking and Intragenic Sequences Confer Androgenic and Developmental Regulation of Mouse Aldose Reductase-Like Gene in Vas Deferens and Adrenal in Transgenic Mice
Endocrinology, March 1, 1999; 140(3): 1338 - 1348.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
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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 J. Clin. Endocrinol. Metab.Home page
A. T. Reutens, J. C. Achermann, M. Ito, M. Ito, W.-X. Gu, R. L. Habiby, P. A. Donohoue, S. Pang, P. C. Hindmarsh, and J. L. Jameson
Clinical and Functional Effects of Mutations in the DAX-1 Gene in Patients with Adrenal Hypoplasia Congenita
J. Clin. Endocrinol. Metab., February 1, 1999; 84(2): 504 - 511.
[Abstract] [Full Text]

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 Mol. Endocrinol.Home page
L. M. Halvorson, U. B. Kaiser, and W. W. Chin
The Protein Kinase C System Acts through the Early Growth Response Protein 1 to Increase LH{beta} Gene Expression in Synergy with Steroidogenic Factor-1
Mol. Endocrinol., January 1, 1999; 13(1): 106 - 116.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
S. L. Asa and S. Ezzat
The Cytogenesis and Pathogenesis of Pituitary Adenomas
Endocr. Rev., December 1, 1998; 19(6): 798 - 827.
[Abstract] [Full Text]

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 EndocrinologyHome page
M. Young and M. J. McPhaul
A Steroidogenic Factor-1-Binding Site and Cyclic Adenosine 3',5'-Monophosphate Response Element-Like Elements Are Required for the Activity of the Rat Aromatase Promoter in Rat Leydig Tumor Cell Lines
Endocrinology, December 1, 1998; 139(12): 5082 - 5093.
[Abstract] [Full Text] [PDF]

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 Mol. Cell. Biol.Home page
P. De Santa Barbara, N. Bonneaud, B. Boizet, M. Desclozeaux, B. Moniot, P. Sudbeck, G. Scherer, F. Poulat, and P. Berta
Direct Interaction of SRY-Related Protein SOX9 and Steroidogenic Factor 1 Regulates Transcription of the Human Anti-Mullerian Hormone Gene
Mol. Cell. Biol., November 1, 1998; 18(11): 6653 - 6665.
[Abstract] [Full Text]


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