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Molecular Endocrinology 14 (8): 1283-1300
Copyright © 2000 by The Endocrine Society

Follicle-Stimulating Hormone (FSH) Stimulates Phosphorylation and Activation of Protein Kinase B (PKB/Akt) and Serum and Glucocorticoid-Induced Kinase (Sgk): Evidence for A Kinase-Independent Signaling by FSH in Granulosa Cells

Ignacio J. Gonzalez-Robayna, Allison E. Falender, Scott Ochsner, Gary L. Firestone and JoAnne S. Richards

Department of Molecular and Cellular Biology (I.J.G.R., A.E.F., S.O., J.S.R.) Baylor College of Medicine Houston, Texas 77030
Department of Molecular and Cell Biology (G.L.F.) University of California Berkeley Berkeley, California 94720

FSH stimulates in ovarian granulosa cells diverse, differentiation-dependent responses that implicate activation of specific cellular signaling cascades. In these studies three kinases were investigated to determine their relationship to FSH, cAMP, and A kinase signaling: protein kinase B (PKB/Akt), serum and glucocorticoid-induced kinase (Sgk), and p38 mitogen-activated protein kinase (p38MAPK). The phosphorylation (activation) of these kinases was analyzed by using selective agonists/inhibitors: forskolin/H89 for cAMP-dependent protein kinase (A kinase), insulin-like growth factor I (IGF-I)/LY294002 and wortmannin for phosphatidylinositol-dependent kinase (PI3-K), and phorbol myristate (PMA)/GF109203X for diacylglycerol and Ca++-dependent kinases (C kinases). An inhibitor (PD98059) of MEK1, which regulates extracellular regulated kinases (ERKs), and SB203580, which inhibits p38MAPK, were also used. In addition, we analyzed the expression of the recently described, cAMP-regulated guanine nucleotide exchange factors (cAMP-GEFI and GEFII) that impact Ras-related GTPases and Raf kinases, known regulators of various protein kinase cascades. We provide evidence that FSH, forskolin, and 8-bromo-cAMP stimulate phosphorylation of PKB by mechanisms involving PI3-K (LY294002/wortmannin sensitive) not A kinase (H89 insensitive), a pattern of response mimicking that of IGF-I. In contrast, FSH induction and phosphorylation of Sgk protein requires A kinase (H89 sensitive) but also involves PI3-K (LY294002 sensitive) as well as p38MAPK (SB203580 sensitive) pathways. PMA (C kinase) abolished FSH-mediated (but not IGF-I-mediated) phosphorylation of PKB at a step(s) upstream of PI3-K and independent of A kinase. Lastly, FSH-mediated phosphorylation of p38MAPK is negatively affected by A kinase and PI3-K, suggesting that it may be downstream of specific members of the cAMP-GEF/Rap/Raf pathway. We propose that cAMP activation of A kinase is obligatory for transcription of Sgk in granulosa cells whereas cAMP (IGF-I-like)-mediated phosphorylation (activation) of PKB and Sgk (via PI3-K), as well as p38MAPK, involves other cellular events. These results provide new and exciting evidence that cAMP acts in granulosa cells by A kinase-dependent and -independent mechanisms, each of which controls specific kinase cascades.




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R. Roberts, A. Iatropoulou, D. Ciantar, J. Stark, D. L. Becker, S. Franks, and K. Hardy
Follicle-Stimulating Hormone Affects Metaphase I Chromosome Alignment and Increases Aneuploidy in Mouse Oocytes Matured in Vitro
Biol Reprod, January 1, 2005; 72(1): 107 - 118.
[Abstract] [Full Text] [PDF]


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J EndocrinolHome page
E C Chin, T E Harris, and D R E Abayasekara
Changes in cAMP-dependent protein kinase (PKA) and progesterone secretion in luteinizing human granulosa cells
J. Endocrinol., October 1, 2004; 183(1): 39 - 50.
[Abstract] [Full Text] [PDF]


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J EndocrinolHome page
E C Chin and D R E Abayasekara
Progesterone secretion by luteinizing human granulosa cells: a possible cAMP-dependent but PKA-independent mechanism involved in its regulation
J. Endocrinol., October 1, 2004; 183(1): 51 - 60.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Lung Cell. Mol. Physiol.Home page
C. P. Thomas, J. R. Campbell, P. J. Wright, and R. F. Husted
cAMP-stimulated Na+ transport in H441 distal lung epithelial cells: role of PKA, phosphatidylinositol 3-kinase, and sgk1
Am J Physiol Lung Cell Mol Physiol, October 1, 2004; 287(4): L843 - L851.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
C. A. Nechamen, R. M. Thomas, B. D. Cohen, G. Acevedo, P. I. Poulikakos, J. R. Testa, and J. A. Dias
Human Follicle-Stimulating Hormone (FSH) Receptor Interacts with the Adaptor Protein APPL1 in HEK 293 Cells: Potential Involvement of the PI3K Pathway in FSH Signaling
Biol Reprod, August 1, 2004; 71(2): 629 - 636.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
L. G. Villa-Diaz and T. Miyano
Activation of p38 MAPK During Porcine Oocyte Maturation
Biol Reprod, August 1, 2004; 71(2): 691 - 696.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
M. A. Cunningham, Q. Zhu, and J. M. Hammond
FoxO1a Can Alter Cell Cycle Progression by Regulating the Nuclear Localization of p27kip in Granulosa Cells
Mol. Endocrinol., July 1, 2004; 18(7): 1756 - 1767.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Gastrointest. Liver Physiol.Home page
M. Palmada, M. Dieter, A. Speil, C. Bohmer, A. F. Mack, H. J. Wagner, K. Klingel, R. Kandolf, H. Murer, J. Biber, et al.
Regulation of intestinal phosphate cotransporter NaPi IIb by ubiquitin ligase Nedd4-2 and by serum- and glucocorticoid-dependent kinase 1
Am J Physiol Gastrointest Liver Physiol, July 1, 2004; 287(1): G143 - G150.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
N. Sekar and J. D. Veldhuis
Involvement of Sp1 and SREBP-1a in transcriptional activation of the LDL receptor gene by insulin and LH in cultured porcine granulosa-luteal cells
Am J Physiol Endocrinol Metab, July 1, 2004; 287(1): E128 - E135.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
R. Roberts, J. Stark, A. Iatropoulou, D. L. Becker, S. Franks, and K. Hardy
Energy Substrate Metabolism of Mouse Cumulus-Oocyte Complexes: Response to Follicle-Stimulating Hormone Is Mediated by the Phosphatidylinositol 3-Kinase Pathway and Is Associated with Oocyte Maturation
Biol Reprod, July 1, 2004; 71(1): 199 - 209.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
H. Alam, E. T. Maizels, Y. Park, S. Ghaey, Z. J. Feiger, N. S. Chandel, and M. Hunzicker-Dunn
Follicle-stimulating Hormone Activation of Hypoxia-inducible Factor-1 by the Phosphatidylinositol 3-Kinase/AKT/Ras Homolog Enriched in Brain (Rheb)/Mammalian Target of Rapamycin (mTOR) Pathway Is Necessary for Induction of Select Protein Markers of Follicular Differentiation
J. Biol. Chem., May 7, 2004; 279(19): 19431 - 19440.
[Abstract] [Full Text] [PDF]


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Mol Hum ReprodHome page
R. Sasson, E. Rimon, A. Dantes, T. Cohen, V. Shinder, A. Land-Bracha, and A. Amsterdam
Gonadotrophin-induced gene regulation in human granulosa cells obtained from IVF patients. Modulation of steroidogenic genes, cytoskeletal genes and genes coding for apoptotic signalling and protein kinases
Mol. Hum. Reprod., May 1, 2004; 10(5): 299 - 311.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
P. P. Kayampilly and K. M. J. Menon
Inhibition of Extracellular Signal-Regulated Protein Kinase-2 Phosphorylation by Dihydrotestosterone Reduces Follicle-Stimulating Hormone-Mediated Cyclin D2 Messenger Ribonucleic Acid Expression in Rat Granulosa Cells
Endocrinology, April 1, 2004; 145(4): 1786 - 1793.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
H. Morinaga, T. Yanase, M. Nomura, T. Okabe, K. Goto, N. Harada, and H. Nawata
A Benzimidazole Fungicide, Benomyl, and Its Metabolite, Carbendazim, Induce Aromatase Activity in a Human Ovarian Granulose-Like Tumor Cell Line (KGN)
Endocrinology, April 1, 2004; 145(4): 1860 - 1869.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
P. Yang and S. K. Roy
Follicle Stimulating Hormone-Induced DNA Synthesis in the Granulosa Cells of Hamster Preantral Follicles Involves Activation of Cyclin-Dependent Kinase-4 Rather Than Cyclin D2 Synthesis
Biol Reprod, February 1, 2004; 70(2): 509 - 517.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
M. A. Cunningham, Q. Zhu, T. G. Unterman, and J. M. Hammond
Follicle-Stimulating Hormone Promotes Nuclear Exclusion of the Forkhead Transcription Factor FoxO1a via Phosphatidylinositol 3-Kinase in Porcine Granulosa Cells
Endocrinology, December 1, 2003; 144(12): 5585 - 5594.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
S. A. Ochsner, A. J. Day, M. S. Rugg, R. M. Breyer, R. H. Gomer, and J. S. Richards
Disrupted Function of Tumor Necrosis Factor-{alpha}-Stimulated Gene 6 Blocks Cumulus Cell-Oocyte Complex Expansion
Endocrinology, October 1, 2003; 144(10): 4376 - 4384.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
M. Hsieh, S. M. Mulders, R. R. Friis, A. Dharmarajan, and J. S. Richards
Expression and Localization of Secreted Frizzled-Related Protein-4 in the Rodent Ovary: Evidence for Selective Up-Regulation in Luteinized Granulosa Cells
Endocrinology, October 1, 2003; 144(10): 4597 - 4606.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
A. J. Zeleznik, D. Saxena, and L. Little-Ihrig
Protein Kinase B Is Obligatory for Follicle-Stimulating Hormone-Induced Granulosa Cell Differentiation
Endocrinology, September 1, 2003; 144(9): 3985 - 3994.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
A. E. Falender, R. Lanz, D. Malenfant, L. Belanger, and J. S. Richards
Differential Expression of Steroidogenic Factor-1 and FTF/LRH-1 in the Rodent Ovary
Endocrinology, August 1, 2003; 144(8): 3598 - 3610.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
A. Ulloa-Aguirre, C. Timossi, J. Barrios-de-Tomasi, A. Maldonado, and P. Nayudu
Impact of Carbohydrate Heterogeneity in Function of Follicle-Stimulating Hormone: Studies Derived from in Vitro and in Vivo Models
Biol Reprod, August 1, 2003; 69(2): 379 - 389.
[Abstract] [Full Text] [PDF]


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FASEB J.Home page
R. SASSON, A. DANTES, K. TAJIMA, and A. AMSTERDAM
Novel genes modulated by FSH in normal and immortalized FSH-responsive cells: new insights into the mechanism of FSH action
FASEB J, July 1, 2003; 17(10): 1256 - 1266.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. M. Suh, J. H. Song, D. W. Kim, H. Kim, H. K. Chung, J. H. Hwang, J. M. Kim, E. S. Hwang, J. Chung, J.-H. Han, et al.
Regulation of the Phosphatidylinositol 3-Kinase, Akt/Protein Kinase B, FRAP/Mammalian Target of Rapamycin, and Ribosomal S6 Kinase 1 Signaling Pathways by Thyroid-stimulating Hormone (TSH) and Stimulating type TSH Receptor Antibodies in the Thyroid Gland
J. Biol. Chem., June 6, 2003; 278(24): 21960 - 21971.
[Abstract] [Full Text] [PDF]


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Mol Hum ReprodHome page
O. Yoshino, Y. Osuga, Y. Hirota, K. Koga, T. Yano, O. Tsutsumi, and Y. Taketani
Akt as a possible intracellular mediator for decidualization in human endometrial stromal cells
Mol. Hum. Reprod., May 1, 2003; 9(5): 265 - 269.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
C. Mukasa, M. Nomura, T. Tanaka, K. Tanaka, Y. Nishi, T. Okabe, K. Goto, T. Yanase, and H. Nawata
Activin Signaling through Type IB Activin Receptor Stimulates Aromatase Activity in the Ovarian Granulosa Cell-Like Human Granulosa (KGN) Cells
Endocrinology, April 1, 2003; 144(4): 1603 - 1611.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
D. L. Russell, K. M. H. Doyle, I. Gonzales-Robayna, C. Pipaon, and J. S. Richards
Egr-1 Induction in Rat Granulosa Cells by Follicle-Stimulating Hormone and Luteinizing Hormone: Combinatorial Regulation By Transcription Factors Cyclic Adenosine 3',5'-Monophosphate Regulatory Element Binding Protein, Serum Response Factor, Sp1, and Early Growth Response Factor-1
Mol. Endocrinol., April 1, 2003; 17(4): 520 - 533.
[Abstract] [Full Text] [PDF]


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Mol. Endocrinol.Home page
C. Lukas-Croisier, C. Lasala, J. Nicaud, P. Bedecarras, T. R. Kumar, M. Dutertre, M. M. Matzuk, J.-Y. Picard, N. Josso, and R. Rey
Follicle-Stimulating Hormone Increases Testicular Anti-Mullerian Hormone (AMH) Production through Sertoli Cell Proliferation and a Nonclassical Cyclic Adenosine 5'-Monophosphate-Mediated Activation of the AMH Gene
Mol. Endocrinol., April 1, 2003; 17(4): 550 - 561.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
C. Boehmer, V. Wilhelm, M. Palmada, S. Wallisch, G. Henke, H. Brinkmeier, P. Cohen, B. Pieske, and F. Lang
Serum and glucocorticoid inducible kinases in the regulation of the cardiac sodium channel SCN5A
Cardiovasc Res, March 15, 2003; 57(4): 1079 - 1084.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
G. W. Sun, H. Kobayashi, M. Suzuki, N. Kanayama, and T. Terao
Follicle-Stimulating Hormone and Insulin-Like Growth Factor I Synergistically Induce Up-Regulation of Cartilage Link Protein (Crtl1) via Activation of Phosphatidylinositol-Dependent Kinase/Akt in Rat Granulosa Cells
Endocrinology, March 1, 2003; 144(3): 793 - 801.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
J. Cottom, L. M. Salvador, E. T. Maizels, S. Reierstad, Y. Park, D. W. Carr, M. A. Davare, J. W. Hell, S. S. Palmer, P. Dent, et al.
Follicle-stimulating Hormone Activates Extracellular Signal-regulated Kinase but Not Extracellular Signal-regulated Kinase Kinase through a 100-kDa Phosphotyrosine Phosphatase
J. Biol. Chem., February 21, 2003; 278(9): 7167 - 7179.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
Y. Wang and W. Ge
Involvement of Cyclic Adenosine 3',5'-Monophosphate in the Differential Regulation of Activin {beta}A and {beta}B Expression by Gonadotropin in the Zebrafish Ovarian Follicle Cells
Endocrinology, February 1, 2003; 144(2): 491 - 499.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
C. R. O. Carvalho, J. B. C. Carvalheira, M. H. M. Lima, S. F. Zimmerman, L. C. Caperuto, A. Amanso, A. L. Gasparetti, V. Meneghetti, L. F. Zimmerman, L. A. Velloso, et al.
Novel Signal Transduction Pathway for Luteinizing Hormone and Its Interaction with Insulin: Activation of Janus Kinase/Signal Transducer and Activator of Transcription and Phosphoinositol 3-Kinase/Akt Pathways
Endocrinology, February 1, 2003; 144(2): 638 - 647.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
R. J. Phillips, J. Bailey, S. C. Robson, and G. N. Europe-Finner
Differential Expression of the Adenylyl Cyclase-Stimulatory Guanosine Triphosphate-Binding Protein Gs{alpha} in the Human Myometrium during Pregnancy and Labor Involves Transcriptional Regulation by Cyclic Adenosine 3',5'-Monophosphate and Binding of Phosphorylated Nuclear Proteins to Multiple GC Boxes within the Promoter
J. Clin. Endocrinol. Metab., December 1, 2002; 87(12): 5675 - 5685.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Cell Physiol.Home page
T. Kagawa, L. Varticovski, Y. Sai, and I. M. Arias
Mechanism by which cAMP activates PI3-kinase and increases bile acid secretion in WIF-B9 cells
Am J Physiol Cell Physiol, December 1, 2002; 283(6): C1655 - C1666.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
M. Conti
Specificity of the Cyclic Adenosine 3',5'-Monophosphate Signal in Granulosa Cell Function
Biol Reprod, December 1, 2002; 67(6): 1653 - 1661.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
O. A. Itani, K. Z. Liu, K. L. Cornish, J. R. Campbell, and C. P. Thomas
Glucocorticoids stimulate human sgk1 gene expression by activation of a GRE in its 5'-flanking region
Am J Physiol Endocrinol Metab, November 1, 2002; 283(5): E971 - E979.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
W. Liu, C. Chin-Chance, E.-J. Lee, and W. L. Lowe Jr.
Activation of Phosphatidylinositol 3-Kinase Contributes to Insulin-Like Growth Factor I-Mediated Inhibition of Pancreatic {beta}-Cell Death
Endocrinology, October 1, 2002; 143(10): 3802 - 3812.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
A.L. Johnson, E.V. Solovieva, and J.T. Bridgham
Relationship Between Steroidogenic Acute Regulatory Protein Expression and Progesterone Production in Hen Granulosa Cells During Follicle Development
Biol Reprod, October 1, 2002; 67(4): 1313 - 1320.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
U. K. Misra, G. Akabani, and S. V. Pizzo
The Role of cAMP-dependent Signaling in Receptor-recognized Forms of alpha 2-Macroglobulin-induced Cellular Proliferation
J. Biol. Chem., September 20, 2002; 277(39): 36509 - 36520.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
V. M. Laurich, A. M. Trbovich, F. H. O'Neill, C. P. Houk, P. M. Sluss, A. H. Payne, P. K. Donahoe, and J. Teixeira
Mullerian Inhibiting Substance Blocks the Protein Kinase A-Induced Expression of Cytochrome P450 17{alpha}-Hydroxylase/C17-20 Lyase mRNA in a Mouse Leydig Cell Line Independent of cAMP Responsive Element Binding Protein Phosphorylation
Endocrinology, September 1, 2002; 143(9): 3351 - 3360.
[Abstract] [Full Text] [PDF]


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Biol. Reprod.Home page
S. Eimerl and J. Orly
Regulation of Steroidogenic Genes by Insulin-Like Growth Factor-1 and Follicle-Stimulating Hormone: Differential Responses of Cytochrome P450 Side-Chain Cleavage, Steroidogenic Acute Regulatory Protein, and 3{beta}-Hydroxysteroid Dehydrogenase/Isomerase in Rat Granulosa Cells
Biol Reprod, September 1, 2002; 67(3): 900 - 910.
[Abstract] [Full Text] [PDF]




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