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Division of Reproductive Biology, Department of Gynecology and
Obstetrics, Stanford University School of Medicine (M.H., E.A.M., G.M.,
C.K., A.J.W.H.), Stanford, California 94305-5317 and Scientific
Development Group
1 (U.M.R., M.v.D.), N.V.
Organon, Oss,
The Netherlands
Address all correspondence and requests for reprints to: Aaron J. W. Hsueh, Division of Reproductive Biology, Department of Gynecology and Obstetrics, Stanford University School of Medicine, Stanford California 94305-5317. E-mail: aaron.hsueh{at}stanford.edu
Transgenic mice with deletion of the GDF-9 (growth differentiation
factor-9) gene are characterized by the arrest of ovarian follicle
development at the primary stage. Based on the hypothesis that GDF-9 is
important for early follicle development, we isolated rat GDF-9
complementary DNA (cDNA) and generated recombinant GDF-9 protein to
study its physiological role. Using bacteria-derived GDF-9-glutathione
S-transferase (GST) fusion protein, specific antibodies to the mature
form of GDF-9 was generated. Immunohistochemical staining of ovarian
sections indicated the localization of GDF-9 protein in the oocyte of
primary, secondary and preantral follicles, whereas immunoblotting
demonstrated the secretion of GDF-9 by mammalian cells transfected with
GDF-9 cDNAs. Recombinant GDF-9 was shown to be an
N-glycosylated protein capable of stimulating early
follicle development. Growth of preantral follicles isolated from
immature rats was enhanced by treatment with either GDF-9 or FSH
whereas the combined treatment showed an additive effect. In addition,
treatment with GDF-9, like forskolin, also stimulated inhibin-
content in explants of neonatal ovaries. In contrast, the stimulatory
effects of GDF-9 were not mimicked by amino-terminal tagged GDF-9 that
was apparently not bioactive. Thus, the present study demonstrates the
important role of GDF-9 in early follicle growth and differentiation.
The availability of recombinant bioactive GDF-9 allows future studies
on the physiological role of GDF-9 in ovarian development in
vivo.
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W. X. Liao, R. K. Moore, F. Otsuka, and S. Shimasaki Effect of Intracellular Interactions on the Processing and Secretion of Bone Morphogenetic Protein-15 (BMP-15) and Growth and Differentiation Factor-9. IMPLICATION OF THE ABERRANT OVARIAN PHENOTYPE OF BMP-15 MUTANT SHEEP J. Biol. Chem., January 31, 2003; 278(6): 3713 - 3719. [Abstract] [Full Text] [PDF]
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J.-S. Roh, J. Bondestam, S. Mazerbourg, N. Kaivo-Oja, N. Groome, O. Ritvos, and A. J. W. Hsueh Growth Differentiation Factor-9 Stimulates Inhibin Production and Activates Smad2 in Cultured Rat Granulosa Cells Endocrinology, January 1, 2003; 144(1): 172 - 178. [Abstract] [Full Text] [PDF]
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J. L. Juengel, N. L. Hudson, D. A. Heath, P. Smith, K. L. Reader, S. B. Lawrence, A. R. O'Connell, M. P.E. Laitinen, M. Cranfield, N. P. Groome, et al. Growth Differentiation Factor 9 and Bone Morphogenetic Protein 15 Are Essential for Ovarian Follicular Development in Sheep Biol Reprod, December 1, 2002; 67(6): 1777 - 1789. [Abstract] [Full Text] [PDF]
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R. A. Taft, J. M. Denegre, F. L. Pendola, and J. J. Eppig Identification of Genes Encoding Mouse Oocyte Secretory and Transmembrane Proteins by a Signal Sequence Trap Biol Reprod, September 1, 2002; 67(3): 953 - 960. [Abstract] [Full Text] [PDF]
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E. E. Nilsson and M. K. Skinner Growth and Differentiation Factor-9 Stimulates Progression of Early Primary but Not Primordial Rat Ovarian Follicle Development Biol Reprod, September 1, 2002; 67(3): 1018 - 1024. [Abstract] [Full Text] [PDF]
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U. A. Vitt, S. Mazerbourg, C. Klein, and A. J.W. Hsueh Bone Morphogenetic Protein Receptor Type II Is a Receptor for Growth Differentiation Factor-9 Biol Reprod, August 1, 2002; 67(2): 473 - 480. [Abstract] [Full Text] [PDF]
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N. Yamamoto, L. K. Christenson, J. M. MCAllister, and J. F. Strauss III Growth Differentiation Factor-9 Inhibits 3'5'-Adenosine Monophosphate-Stimulated Steroidogenesis in Human Granulosa and Theca Cells J. Clin. Endocrinol. Metab., June 1, 2002; 87(6): 2849 - 2856. [Abstract] [Full Text] [PDF]
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R. Jaatinen, J. Bondestam, T. Raivio, K. Hilden, L. Dunkel, N. Groome, and O. Ritvos Activation of the Bone Morphogenetic Protein Signaling Pathway Induces Inhibin {beta}B-Subunit mRNA and Secreted Inhibin B Levels in Cultured Human Granulosa-Luteal Cells J. Clin. Endocrinol. Metab., March 1, 2002; 87(3): 1254 - 1261. [Abstract] [Full Text] [PDF]
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F. L. Teixeira Filho, E. C. Baracat, T. H. Lee, C. S. Suh, M. Matsui, R. J. Chang, S. Shimasaki, and G. F. Erickson Aberrant Expression of Growth Differentiation Factor-9 in Oocytes of Women with Polycystic Ovary Syndrome J. Clin. Endocrinol. Metab., March 1, 2002; 87(3): 1337 - 1344. [Abstract] [Full Text] [PDF]
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 J. J. Eppig, K. Wigglesworth, and F. L. Pendola The mammalian oocyte orchestrates the rate of ovarian follicular development PNAS, February 20, 2002; (2002) 52658699. [Abstract] [Full Text] [PDF]
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J. G. Hreinsson, J. E. Scott, C. Rasmussen, M. L. Swahn, A. J. W. Hsueh, and O. Hovatta Growth Differentiation Factor-9 Promotes the Growth, Development, and Survival of Human Ovarian Follicles in Organ Culture J. Clin. Endocrinol. Metab., January 1, 2002; 87(1): 316 - 321. [Abstract] [Full Text] [PDF]
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 J.M. van Montfrans, M.H.A. van Hooff, F. Martens, and C.B. Lambalk Basal FSH, estradiol and inhibin B concentrations in women with a previous Down's syndrome affected pregnancy Hum. Reprod., January 1, 2002; 17(1): 44 - 47. [Abstract] [Full Text] [PDF]
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A. L. L. Durlinger, M. J. G. Gruijters, P. Kramer, B. Karels, T. R. Kumar, M. M. Matzuk, U. M. Rose, F. H. de Jong, J. Th. J. Uilenbroek, J. A. Grootegoed, et al. Anti-Mullerian Hormone Attenuates the Effects of FSH on Follicle Development in the Mouse Ovary Endocrinology, November 1, 2001; 142(11): 4891 - 4899. [Abstract] [Full Text] [PDF]
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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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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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E. A. McGee, R. Smith, N. Spears, M. W. Nachtigal, H. Ingraham, and A. J.W. Hsueh Mullerian Inhibitory Substance Induces Growth of Rat Preantral Ovarian Follicles Biol Reprod, January 1, 2001; 64(1): 293 - 298. [Abstract] [Full Text]
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B. S. Dunbar, S. Prasad, C. Carino, and S. M. Skinner The Ovary as an Immune Target Reproductive Sciences, January 1, 2001; 8(1_suppl): S43 - S48. [Abstract] [PDF]
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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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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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R. Li, R. J. Norman, D. T. Armstrong, and R. B. Gilchrist Oocyte-Secreted Factor(s) Determine Functional Differences Between Bovine Mural Granulosa Cells and Cumulus Cells Biol Reprod, September 1, 2000; 63(3): 839 - 845. [Abstract] [Full Text]
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K. Oktay, G. Karlikaya, O. Akman, G. K. Ojakian, and M. Oktay Interaction of Extracellular Matrix and Activin-A in the Initiation of Follicle Growth in the Mouse Ovary Biol Reprod, August 1, 2000; 63(2): 457 - 461. [Abstract] [Full Text]
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E. A. McGee and A. J. W. Hsueh Initial and Cyclic Recruitment of Ovarian Follicles Endocr. Rev., April 1, 2000; 21(2): 200 - 214. [Abstract] [Full Text]
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J. J. Eppig and K. Wigglesworth Development of Mouse and Rat Oocytes in Chimeric Reaggregated Ovaries after Interspecific Exchange of Somatic and Germ Cell Components Biol Reprod, April 1, 2000; 63(4): 1014 - 1023. [Abstract] [Full Text]
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U.A. Vitt, M. Hayashi, C. Klein, and A.J.W. Hsueh Growth Differentiation Factor-9 Stimulates Proliferation but Suppresses the Follicle-Stimulating Hormone-Induced Differentiation of Cultured Granulosa Cells from Small Antral and Preovulatory Rat Follicles Biol Reprod, February 1, 2000; 62(2): 370 - 377. [Abstract] [Full Text]
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A. L. L. Durlinger, P. Kramer, B. Karels, F. H. de Jong, J. Th. J. Uilenbroek, J. A. Grootegoed, and A. P. N. Themmen Control of Primordial Follicle Recruitment by Anti-Mullerian Hormone in the Mouse Ovary Endocrinology, December 1, 1999; 140(12): 5789 - 5796. [Abstract] [Full Text]
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J. Aaltonen, M. P. Laitinen, K. Vuojolainen, R. Jaatinen, N. Horelli-Kuitunen, L. Seppä, H. Louhio, T. Tuuri, J. Sjöberg, R. Bützow, et al. Human Growth Differentiation Factor 9 (GDF-9) and Its Novel Homolog GDF-9B Are Expressed in Oocytes during Early Folliculogenesis J. Clin. Endocrinol. Metab., August 1, 1999; 84(8): 2744 - 2750. [Abstract] [Full Text]
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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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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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J. J. Eppig, K. Wigglesworth, and F. L. Pendola The mammalian oocyte orchestrates the rate of ovarian follicular development PNAS, March 5, 2002; 99(5): 2890 - 2894. [Abstract] [Full Text] [PDF]
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