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Steroidogenic Factor 1: A Key Determinant of Endocrine Development and Function

Departments of Medicine and Pharmacology and the Howard Hughes Medical Institute (K.L.P.), Duke University Medical Center, Durham, North Carolina 27710; and the Banting and Best Department of Medical Research (B.P.S.), University of Toronto, Toronto, Canada M5G 1L6

I. Introduction

II. The Initial Identification of SF-1 as a Key Determinant of Steroid Hormone Biosynthesis

A. Overview of steroidogenesis

B. SF-1 and the regulation of steroidogenesis

C. Cloning and structural characterization of SF-1

1. Structural features of SF-1

2. Multiple transcripts are encoded by the gene encoding SF-1

3. The gene encoding SF-1 is evolutionarily conserved in vertebrates and invertebrates

III. Characterization of Sites of SF-1 Expression and Identification of Its Target Genes

A. Profiles of SF-1 expression

1. Adult steroidogenic tissues

2. Embryonic steroidogenic tissues

3. Other sites of SF-1 expression

B. Target genes regulated by SF-1

1. Steroidogenic cells

2. Sertoli cells

3. Gonadotropes

4. VMH

IV. The Roles Of SF-1 in Vivo: Targeted Gene Disruption to Create SF-1 Knockout Mice

A. General features of the SF-1 knockout mice

B. Primary steroidogenic tissues in SF-1 knockout mice

C. Pituitary and hypothalamic defects in SF-1 knockout mice

V. Perspectives and Future Directions

A. What are the roles of the various transcripts encoded by the Ftz-F1 gene?

B. Does a ligand mediate SF-1 transcriptional activation?

C. Where does SF-1 fit within hierarchical cascades of endocrine development?

1. Which other genes also contribute to tissue-selective expression of SF-1 target genes?

2. Which target genes of SF-1 mediate its key roles in maintaining the adrenal glands, gonads, and VMH?

3. What mechanisms regulate the expression of SF-1?

4. How is SF-1 related to other genes whose disruptions lead to phenotypes that resemble the SF-1 knockout mice?

D. Do other transcription factors/nuclear receptors serve dual roles in development and maintenance of the differentiated phenotype?

VI. Conclusion

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				D. L. Liu, W. Z. Liu, Q. L. Li, H. M. Wang, D. Qian, E. Treuter, and C. Zhu Expression and Functional Analysis of Liver Receptor Homologue 1 as a Potential Steroidogenic Factor in Rat Ovary Biol Reprod, August 1, 2003; 69(2): 508 - 517. [Abstract] [Full Text] [PDF]

				A. K. Ghosh, R. Steele, and R. B. Ray Modulation of Human Luteinizing Hormone {beta} Gene Transcription by MIP-2A J. Biol. Chem., June 20, 2003; 278(26): 24033 - 24038. [Abstract] [Full Text] [PDF]

				K. Mukai, F. Mitani, H. Nagasawa, R. Suzuki, T. Suzuki, M. Suematsu, and Y. Ishimura An Inverse Correlation between Expression of a Preprocathepsin B-related Protein with Cysteine-rich Sequences and Steroid 11beta -Hydroxylase in Adrenocortical Cells J. Biol. Chem., May 2, 2003; 278(19): 17084 - 17092. [Abstract] [Full Text] [PDF]

				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]

				S. Catalano, V. Pezzi, A. Chimento, C. Giordano, A. Carpino, M. Young, M. J. McPhaul, and S. Ando Triiodothyronine Decreases the Activity of the Proximal Promoter (PII) of the Aromatase Gene in the Mouse Sertoli Cell Line, TM4 Mol. Endocrinol., May 1, 2003; 17(5): 923 - 934. [Abstract] [Full Text] [PDF]

				Y. Yoshiura, B. Senthilkumaran, M. Watanabe, Y. Oba, T. Kobayashi, and Y. Nagahama Synergistic Expression of Ad4BP/SF-1 and Cytochrome P-450 Aromatase (Ovarian Type) in the Ovary of Nile Tilapia, Oreochromis niloticus, During Vitellogenesis Suggests Transcriptional Interaction Biol Reprod, May 1, 2003; 68(5): 1545 - 1553. [Abstract] [Full Text] [PDF]

				N. Y. Gevry, E. Lalli, P. Sassone-Corsi, and B. D. Murphy Regulation of Niemann-Pick C1 Gene Expression by the 3'5'-Cyclic Adenosine Monophosphate Pathway in Steroidogenic Cells Mol. Endocrinol., April 1, 2003; 17(4): 704 - 715. [Abstract] [Full Text] [PDF]

				A.-M. Pulichino, S. Vallette-Kasic, J. P.-Y. Tsai, C. Couture, Y. Gauthier, and J. Drouin Tpit determines alternate fates during pituitary cell differentiation Genes & Dev., March 15, 2003; 17(6): 738 - 747. [Abstract] [Full Text] [PDF]

				T. Suzuki, M. Kasahara, H. Yoshioka, K.-i. Morohashi, and K. Umesono LXXLL-Related Motifs in Dax-1 Have Target Specificity for the Orphan Nuclear Receptors Ad4BP/SF-1 and LRH-1 Mol. Cell. Biol., January 1, 2003; 23(1): 238 - 249. [Abstract] [Full Text]

				X. Yan, J.-F. Mouillet, Q. Ou, and Y. Sadovsky A Novel Domain within the DEAD-Box Protein DP103 Is Essential for Transcriptional Repression and Helicase Activity Mol. Cell. Biol., January 1, 2003; 23(1): 414 - 423. [Abstract] [Full Text]

				D. A. Schreihofer, D. F. Rowe, E. F. Rissman, E. M. Scordalakes, J.-a. Gustafsson, and M. A. Shupnik Estrogen Receptor-{alpha} (ER{alpha}), But Not ER{beta}, Modulates Estrogen Stimulation of the ER{alpha}-Truncated Variant, TERP-1 Endocrinology, November 1, 2002; 143(11): 4196 - 4202. [Abstract] [Full Text] [PDF]

				S. P. Scherrer, D. A. Rice, and L. L. Heckert Expression of Steroidogenic Factor 1 in the Testis Requires an Interactive Array of Elements Within Its Proximal Promoter Biol Reprod, November 1, 2002; 67(5): 1509 - 1521. [Abstract] [Full Text] [PDF]

				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]

				M. Desclozeaux, I. N. Krylova, F. Horn, R. J. Fletterick, and H. A. Ingraham Phosphorylation and Intramolecular Stabilization of the Ligand Binding Domain in the Nuclear Receptor Steroidogenic Factor 1 Mol. Cell. Biol., October 15, 2002; 22(20): 7193 - 7203. [Abstract] [Full Text] [PDF]

				F. Gizard, B. Lavallee, F. DeWitte, E. Teissier, B. Staels, and D. W. Hum The Transcriptional Regulating Protein of 132 kDa (TReP-132) Enhances P450scc Gene Transcription through Interaction with Steroidogenic Factor-1 in Human Adrenal Cells J. Biol. Chem., October 11, 2002; 277(42): 39144 - 39155. [Abstract] [Full Text] [PDF]

				C. Frigeri, J. Tsao, M. Cordova, and B. P. Schimmer A Polymorphic Form of Steroidogenic Factor-1 Is Associated with Adrenocorticotropin Resistance in Y1 Mouse Adrenocortical Tumor Cell Mutants Endocrinology, October 1, 2002; 143(10): 4031 - 4037. [Abstract] [Full Text] [PDF]

				J. Y. L. Chiang Bile Acid Regulation of Gene Expression: Roles of Nuclear Hormone Receptors Endocr. Rev., August 1, 2002; 23(4): 443 - 463. [Abstract] [Full Text] [PDF]

				S. Kiiveri, J. Liu, M. Westerholm-Ormio, N. Narita, D. B. Wilson, R. Voutilainen, and M. Heikinheimo Differential Expression of GATA-4 and GATA-6 in Fetal and Adult Mouse and Human Adrenal Tissue Endocrinology, August 1, 2002; 143(8): 3136 - 3143. [Abstract] [Full Text] [PDF]

				J. C. Achermann, G. Ozisik, J. J. Meeks, and J. L. Jameson Genetic Causes of Human Reproductive Disease J. Clin. Endocrinol. Metab., June 1, 2002; 87(6): 2447 - 2454. [Full Text] [PDF]

				S. B. Rosenberg and P. L. Mellon An Otx-Related Homeodomain Protein Binds an LH{beta} Promoter Element Important for Activation During Gonadotrope Maturation Mol. Endocrinol., June 1, 2002; 16(6): 1280 - 1298. [Abstract] [Full Text] [PDF]

				C. D. Clyne, C. J. Speed, J. Zhou, and E. R. Simpson Liver Receptor Homologue-1 (LRH-1) Regulates Expression of Aromatase in Preadipocytes J. Biol. Chem., May 31, 2002; 277(23): 20591 - 20597. [Abstract] [Full Text] [PDF]

				B. Borud, T. Hoang, M. Bakke, A. L. Jacob, J. Lund, and G. Mellgren The Nuclear Receptor Coactivators p300/CBP/Cointegrator-Associated Protein (p/CIP) and Transcription Intermediary Factor 2 (TIF2) Differentially Regulate PKA-Stimulated Transcriptional Activity of Steroidogenic Factor 1 Mol. Endocrinol., April 1, 2002; 16(4): 757 - 773. [Abstract] [Full Text] [PDF]

				J. C. Achermann, G. Ozisik, M. Ito, U. A. Orun, K. Harmanci, B. Gurakan, and J. L. Jameson Gonadal Determination and Adrenal Development Are Regulated by the Orphan Nuclear Receptor Steroidogenic Factor-1, in a Dose-Dependent Manner J. Clin. Endocrinol. Metab., April 1, 2002; 87(4): 1829 - 1833. [Abstract] [Full Text] [PDF]

				J. H.-C. Shen and H. A. Ingraham Regulation of the Orphan Nuclear Receptor Steroidogenic Factor 1 by Sox Proteins Mol. Endocrinol., March 1, 2002; 16(3): 529 - 540. [Abstract] [Full Text] [PDF]

				L. Peng and A. H. Payne AP-2gamma and the Homeodomain Protein Distal-less 3 Are Required for Placental-specific Expression of the Murine 3beta -Hydroxysteroid Dehydrogenase VI Gene, Hsd3b6 J. Biol. Chem., March 1, 2002; 277(10): 7945 - 7954. [Abstract] [Full Text] [PDF]

				G. Majdic, M. Young, E. Gomez-Sanchez, P. Anderson, L. S. Szczepaniak, R. L. Dobbins, J. D. McGarry, and K. L. Parker Knockout Mice Lacking Steroidogenic Factor 1 Are a Novel Genetic Model of Hypothalamic Obesity Endocrinology, February 1, 2002; 143(2): 607 - 614. [Abstract] [Full Text] [PDF]

				P. S. Babu, D. L. Bavers, F. Beuschlein, S. Shah, B. Jeffs, J. L. Jameson, and G. D. Hammer Interaction Between Dax-1 and Steroidogenic Factor-1 in Vivo: Increased Adrenal Responsiveness to ACTH in the Absence of Dax-1 Endocrinology, February 1, 2002; 143(2): 665 - 673. [Abstract] [Full Text] [PDF]

				M. Tena-Sempere, M. L. Barreiro, L. C. Gonzalez, F. Gaytan, F.-P. Zhang, J. E. Caminos, L. Pinilla, F. F. Casanueva, C. Dieguez, and E. Aguilar Novel Expression and Functional Role of Ghrelin in Rat Testis Endocrinology, February 1, 2002; 143(2): 717 - 725. [Abstract] [Full Text] [PDF]

				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]

				D. Lopez, W. Shea-Eaton, M. D. Sanchez, and M. P. McLean DAX-1 Represses the High-Density Lipoprotein Receptor Through Interaction with Positive Regulators Sterol Regulatory Element-Binding Protein-1a and Steroidogenic Factor-1 Endocrinology, December 1, 2001; 142(12): 5097 - 5106. [Abstract] [Full Text] [PDF]

				M. J. Young, C. D. Clyne, T. J. Cole, and J. W. Funder Cardiac Steroidogenesis in the Normal and Failing Heart J. Clin. Endocrinol. Metab., November 1, 2001; 86(11): 5121 - 5126. [Abstract] [Full Text] [PDF]