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Biology of Reproduction 62, 370-377 (2000)
© 2000 Society for the Study of Reproduction, Inc.

Articles

Growth Differentiation Factor-9 Stimulates Proliferation but Suppresses the Follicle-Stimulating Hormone-Induced Differentiation of Cultured Granulosa Cells from Small Antral and Preovulatory Rat Follicles1

U.A. Vitta, M. Hayashia, C. Kleina, and A.J.W. Hsueh2,a

a Division of Reproductive Biology, Department of Gynecology and Obstetrics, Stanford University School of Medicine, Stanford, California 94305-5317

In addition to pituitary gonadotropins and paracrine factors, ovarian follicle development is also modulated by oocyte factors capable of stimulating granulosa cell proliferation but suppressing their differentiation. The nature of these oocyte factors is unclear. Because growth differentiation factor-9 (GDF-9) enhanced preantral follicle growth and was detected in the oocytes of early antral and preovulatory follicles, we hypothesized that this oocyte hormone could regulate the proliferation and differentiation of granulosa cells from these advanced follicles. Treatment with recombinant GDF-9, but not FSH, stimulated thymidine incorporation into cultured granulosa cells from both early antral and preovulatory follicles, accompanied by increases in granulosa cell number. Although GDF-9 treatment alone stimulated basal steroidogenesis in granulosa cells, cotreatment with GDF-9 suppressed FSH-stimulated progesterone and estradiol production. In addition, GDF-9 cotreatment attentuated FSH-induced LH receptor formation. The inhibitory effects of GDF-9 on FSH-induced granulosa cell differentiation were accompanied by decreases in the FSH-induced cAMP production. These data suggested that GDF-9 is a proliferation factor for granulosa cells from early antral and preovulatory follicles but suppresses FSH-induced differentiation of the same cells. Thus, oocyte-derived GDF-9 could account, at least partially, for the oocyte factor(s) previously reported to control cumulus and granulosa cell differentiation.

First decision: 19 August 1999.

1 This study was supported by NIH Grant HD31398 and the Specialized Cooperative Centers Program in Reproduction Research.

2 Correspondence: Aaron J.W. Hsueh, Division of Reproductive Biology, Department of Gynecology and Obstetrics, Stanford University School of Medicine, Room A344, Stanford, CA 94305-5317. FAX: 650 725 7102; aaron.hsueh{at}stanford.edu




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T. El-Hefnawy and A. J. Zeleznik
Synergism Between FSH and Activin in the Regulation of Proliferating Cell Nuclear Antigen (PCNA) and Cyclin D2 Expression in Rat Granulosa Cells
Endocrinology, October 1, 2001; 142(10): 4357 - 4362.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
I. M. Joyce, F. L. Pendola, M. O'Brien, and J. J. Eppig
Regulation of Prostaglandin-Endoperoxide Synthase 2 Messenger Ribonucleic Acid Expression in Mouse Granulosa Cells during Ovulation
Endocrinology, July 1, 2001; 142(7): 3187 - 3197.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. Yan, P. Wang, J. DeMayo, F. J. DeMayo, J. A. Elvin, C. Carino, S. V. Prasad, S. S. Skinner, B. S. Dunbar, J. L. Dube, et al.
Synergistic Roles of Bone Morphogenetic Protein 15 and Growth Differentiation Factor 9 in Ovarian Function
Mol. Endocrinol., June 1, 2001; 15(6): 854 - 866.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. S. Richards
Perspective: The Ovarian Follicle--A Perspective in 2001
Endocrinology, June 1, 2001; 142(6): 2184 - 2193.
[Full Text] [PDF]

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 Biol. Reprod.Home page
T. Wilson, X.-Y. Wu, J. L. Juengel, I. K. Ross, J. M. Lumsden, E. A. Lord, K. G. Dodds, G. A. Walling, J. C. McEwan, A. R. O'Connell, et al.
Highly Prolific Booroola Sheep Have a Mutation in the Intracellular Kinase Domain of Bone Morphogenetic Protein IB Receptor (ALK-6) That Is Expressed in Both Oocytes and Granulosa Cells
Biol Reprod, April 1, 2001; 64(4): 1225 - 1235.
[Abstract] [Full Text]

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 Biol. Reprod.Home page
I. M. Joyce, A. T. Clark, F. L. Pendola, and J. J. Eppig
Comparison of Recombinant Growth Differentiation Factor-9 and Oocyte Regulation of KIT Ligand Messenger Ribonucleic Acid Expression in Mouse Ovarian Follicles
Biol Reprod, December 1, 2000; 63(6): 1669 - 1675.
[Abstract] [Full Text]

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 EndocrinologyHome page
U. A. Vitt, E. A. McGee, M. Hayashi, and A. J. W. Hsueh
In Vivo Treatment with GDF-9 Stimulates Primordial and Primary Follicle Progression and Theca Cell Marker CYP17 in Ovaries of Immature Rats
Endocrinology, October 1, 2000; 141(10): 3814 - 3820.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
E. V. Solovyeva, M. Hayashi, K. Margi, C. Barkats, C. Klein, A. Amsterdam, A. J.W. Hsueh, and A. Tsafriri
Growth Differentiation Factor-9 Stimulates Rat Theca-Interstitial Cell Androgen Biosynthesis
Biol Reprod, October 1, 2000; 63(4): 1214 - 1218.
[Abstract] [Full Text]

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 J. Biol. Chem.Home page
F. Otsuka, Z. Yao, T.-h. Lee, S. Yamamoto, G. F. Erickson, and S. Shimasaki
Bone Morphogenetic Protein-15. IDENTIFICATION OF TARGET CELLS AND BIOLOGICAL FUNCTIONS
J. Biol. Chem., December 8, 2000; 275(50): 39523 - 39528.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
F. Otsuka, S. Yamamoto, G. F. Erickson, and S. Shimasaki
Bone Morphogenetic Protein-15 Inhibits Follicle-stimulating Hormone (FSH) Action by Suppressing FSH Receptor Expression
J. Biol. Chem., March 30, 2001; 276(14): 11387 - 11392.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
F. Otsuka, R. K. Moore, and S. Shimasaki
Biological Function and Cellular Mechanism of Bone Morphogenetic Protein-6 in the Ovary
J. Biol. Chem., August 24, 2001; 276(35): 32889 - 32895.
[Abstract] [Full Text] [PDF]


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