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Molecular Endocrinology 13 (6): 1035-1048
Copyright © 1999 by The Endocrine Society

Paracrine Actions Of Growth Differentiation Factor-9 in the Mammalian Ovary

Julia A. Elvin, Amander T. Clark, Pei Wang, Neil M. Wolfman and Martin M. Matzuk

Department of Pathology (J.A.E., A.T.C., P.W., M.M.M.) Department of Molecular and Human Genetics (J.A.E., M.M.M.), and Department of Cell Biology (M.M.M.) Baylor College of Medicine Houston, Texas 77030
Genetics Institute (N.M.W.) Cambridge, Massachusetts 02140

Although the transforming growth factor-ß (TGF-ß) superfamily is the largest family of secreted growth factors, surprisingly few downstream target genes in their signaling pathways have been identified. Likewise, the identities of oocyte-derived secreted factors, which regulate important oocyte-somatic cell interactions, remain largely unknown. For example, oocytes are known to secrete paracrine growth factor(s) which are necessary for cumulus expansion, induction of hyaluronic acid synthesis, and suppression of LH receptor (LHR) mRNA synthesis. Our previous studies demonstrated that absence of the TGF-ß family member, growth differentiation factor-9 (GDF-9), blocks ovarian folliculogenesis at the primary follicle stage leading to infertility. In the present study, we demonstrate that mouse GDF-9 protein is expressed in all oocytes beginning at the type 3a follicle stage including antral follicles. To explore the biological functions of GDF-9 in the later stages of folliculogenesis and cumulus expansion, we produced mature, glycosylated, recombinant mouse GDF-9 using a Chinese hamster ovary cell expression system. A granulosa cell culture system was established to determine the role of GDF-9 in the regulation of several key ovarian gene products using semiquantitative RT-PCR. We find that recombinant GDF-9 induces hyaluronan synthase 2 (HAS2), cyclooxygenase 2 (COX-2), and steroidogenic acute regulator protein (StAR) mRNA synthesis but suppresses urokinase plasminogen activator (uPA) and LHR mRNA synthesis. Consistent with the induction of StAR mRNA by GDF-9, recombinant GDF-9 increases granulosa cell progesterone synthesis in the absence of FSH. Since induction of HAS2 and suppression of the protease uPA in cumulus cells are key events in the production of the hyaluronic acid-rich extracellular matrix which is produced during cumulus expansion, we determined whether GDF-9 could mimic this process. Using oocytectomized cumulus cell-oocyte complexes, we show that recombinant GDF-9 induces cumulus expansion in vitro. These studies demonstrate that GDF-9 can bind to receptors on granulosa cells to regulate the expression of a number of gene products. Thus, in addition to playing a critical function as a growth and differentiation factor during early folliculogenesis, GDF-9 functions as an oocyte-secreted paracrine factor to regulate several key granulosa cell enzymes involved in cumulus expansion and maintenance of an optimal oocyte microenvironment, processes which are essential for normal ovulation, fertilization, and female reproduction.




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K. E. Latham, K. Wigglesworth, M. McMenamin, and J. J. Eppig
Stage-Dependent Effects of Oocytes and Growth Differentiation Factor 9 on Mouse Granulosa Cell Development: Advance Programming and Subsequent Control of the Transition from Preantral Secondary Follicles to Early Antral Tertiary Follicles
Biol Reprod, May 1, 2004; 70(5): 1253 - 1262.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
F.-C. Ke, L.-C. Chuang, M.-T. Lee, Y. J. Chen, S.-W. Lin, P. S. Wang, D. M. Stocco, and J.-J. Hwang
The Modulatory Role of Transforming Growth Factor {beta}1 and Androstenedione on Follicle-Stimulating Hormone-Induced Gelatinase Secretion and Steroidogenesis in Rat Granulosa Cells
Biol Reprod, May 1, 2004; 70(5): 1292 - 1298.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
C. J. Jorgez, M. Klysik, S. P. Jamin, R. R. Behringer, and M. M. Matzuk
Granulosa Cell-Specific Inactivation of Follistatin Causes Female Fertility Defects
Mol. Endocrinol., April 1, 2004; 18(4): 953 - 967.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
Y. Kalma, I. Granot, D. Galiani, A. Barash, and N. Dekel
Luteinizing Hormone-Induced Connexin 43 Down-Regulation: Inhibition of Translation
Endocrinology, April 1, 2004; 145(4): 1617 - 1624.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
A. Salustri, C. Garlanda, E. Hirsch, M. De Acetis, A. Maccagno, B. Bottazzi, A. Doni, A. Bastone, G. Mantovani, P. B. Peccoz, et al.
PTX3 plays a key role in the organization of the cumulus oophorus extracellular matrix and in in vivo fertilization
Development, April 1, 2004; 131(7): 1577 - 1586.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. Mukhopadhyay, A. Asari, M. S. Rugg, A. J. Day, and C. Fulop
Specificity of the Tumor Necrosis Factor-induced Protein 6-mediated Heavy Chain Transfer from Inter-{alpha}-trypsin Inhibitor to Hyaluronan: IMPLICATIONS FOR THE ASSEMBLY OF THE CUMULUS EXTRACELLULAR MATRIX
J. Biol. Chem., March 19, 2004; 279(12): 11119 - 11128.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
S. Mazerbourg, C. Klein, J. Roh, N. Kaivo-Oja, D. G. Mottershead, O. Korchynskyi, O. Ritvos, and A. J. W. Hsueh
Growth Differentiation Factor-9 Signaling Is Mediated by the Type I Receptor, Activin Receptor-Like Kinase 5
Mol. Endocrinol., March 1, 2004; 18(3): 653 - 665.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
S. K. Bristol and T. K. Woodruff
Follicle-Restricted Compartmentalization of Transforming Growth Factor {beta} Superfamily Ligands in the Feline Ovary
Biol Reprod, March 1, 2004; 70(3): 846 - 859.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
S. Shimasaki, R. K. Moore, F. Otsuka, and G. F. Erickson
The Bone Morphogenetic Protein System In Mammalian Reproduction
Endocr. Rev., February 1, 2004; 25(1): 72 - 101.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
C. Glister, C F. Kemp, and P. G Knight
Bone morphogenetic protein (BMP) ligands and receptors in bovine ovarian follicle cells: actions of BMP-4, -6 and -7 on granulosa cells and differential modulation of Smad-1 phosphorylation by follistatin
Reproduction, February 1, 2004; 127(2): 239 - 254.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
N. Minami, A. Aizawa, R. Ihara, M. Miyamoto, A. Ohashi, and H. Imai
Oogenesin Is a Novel Mouse Protein Expressed in Oocytes and Early Cleavage-Stage Embryos
Biol Reprod, November 1, 2003; 69(5): 1736 - 1742.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
D. L. Russell, K. M. H. Doyle, S. A. Ochsner, J. D. Sandy, and J. S. Richards
Processing and Localization of ADAMTS-1 and Proteolytic Cleavage of Versican during Cumulus Matrix Expansion and Ovulation
J. Biol. Chem., October 24, 2003; 278(43): 42330 - 42339.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. H. Burns, G. E. Owens, S. C. Ogbonna, J. H. Nilson, and M. M. Matzuk
Expression Profiling Analyses of Gonadotropin Responses and Tumor Development in the Absence of Inhibins
Endocrinology, October 1, 2003; 144(10): 4492 - 4507.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
A. Balla, N. Danilovich, Y. Yang, and M. R. Sairam
Dynamics of Ovarian Development in the FORKO Immature Mouse: Structural and Functional Implications for Ovarian Reserve
Biol Reprod, October 1, 2003; 69(4): 1281 - 1293.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
K. L. Loveland, M. Bakker, T. Meehan, E. Christy, V. von Schonfeldt, A. Drummond, and D. de Kretser
Expression of Bambi Is Widespread in Juvenile and Adult Rat Tissues and Is Regulated in Male Germ Cells
Endocrinology, September 1, 2003; 144(9): 4180 - 4186.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
D. M. Duffy
Growth Differentiation Factor-9 Is Expressed by the Primate Follicle Throughout the Periovulatory Interval
Biol Reprod, August 1, 2003; 69(2): 725 - 732.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
S. A. Ochsner, D. L. Russell, A. J. Day, R. M. Breyer, and J. S. Richards
Decreased Expression of Tumor Necrosis Factor-{alpha}-Stimulated Gene 6 in Cumulus Cells of the Cyclooxygenase-2 and EP2 Null Mice
Endocrinology, March 1, 2003; 144(3): 1008 - 1019.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
D. L. Russell, S. A. Ochsner, M. Hsieh, S. Mulders, and J. S. Richards
Hormone-Regulated Expression and Localization of Versican in the Rodent Ovary
Endocrinology, March 1, 2003; 144(3): 1020 - 1031.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
C. Glister, N. P. Groome, and P. G. Knight
Oocyte-Mediated Suppression of Follicle-Stimulating Hormone- and Insulin-Like Growth Factor-Induced Secretion of Steroids and Inhibin-Related Proteins by Bovine Granulosa Cells In Vitro: Possible Role of Transforming Growth Factor {alpha}
Biol Reprod, March 1, 2003; 68(3): 758 - 765.
[Abstract] [Full Text] [PDF]

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 Proc. Natl. Acad. Sci. USAHome page
N. Suzumori, K. H. Burns, W. Yan, and M. M. Matzuk
RFPL4 interacts with oocyte proteins of the ubiquitin-proteasome degradation pathway
PNAS, January 21, 2003; 100(2): 550 - 555.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
S. Jabara, L. K. Christenson, C. Y. Wang, J. M. McAllister, N. B. Javitt, A. Dunaif, and J. F. Strauss III
Stromal Cells of the Human Postmenopausal Ovary Display a Distinctive Biochemical and Molecular Phenotype
J. Clin. Endocrinol. Metab., January 1, 2003; 88(1): 484 - 492.
[Abstract] [Full Text] [PDF]

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 Endocr. Rev.Home page
H. Chang, C. W. Brown, and M. M. Matzuk
Genetic Analysis of the Mammalian Transforming Growth Factor-{beta} Superfamily
Endocr. Rev., December 1, 2002; 23(6): 787 - 823.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
L. L. Espey and J. S. Richards
Temporal and Spatial Patterns of Ovarian Gene Transcription Following an Ovulatory Dose of Gonadotropin in the Rat
Biol Reprod, December 1, 2002; 67(6): 1662 - 1670.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
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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 EndocrinologyHome page
A. E. Stock, N. Bouchard, K. Brown, A. P. Spicer, C. B. Underhill, M. Dore, and J. Sirois
Induction of Hyaluronan Synthase 2 by Human Chorionic Gonadotropin in Mural Granulosa Cells of Equine Preovulatory Follicles
Endocrinology, November 1, 2002; 143(11): 4375 - 4384.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
N. C. Zachos, R. B. Billiar, E. D. Albrecht, and G. J. Pepe
Developmental Regulation of Baboon Fetal Ovarian Maturation by Estrogen
Biol Reprod, October 1, 2002; 67(4): 1148 - 1156.
[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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 Biol. Reprod.Home page
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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 Biol. Reprod.Home page
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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 J. Clin. Endocrinol. Metab.Home page
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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 Mol. Endocrinol.Home page
S. Varani, J. A. Elvin, C. Yan, J. DeMayo, F. J. DeMayo, H. F. Horton, M. C. Byrne, and M. M. Matzuk
Knockout of Pentraxin 3, a Downstream Target of Growth Differentiation Factor-9, Causes Female Subfertility
Mol. Endocrinol., June 1, 2002; 16(6): 1154 - 1167.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
W. Yan, A. Rajkovic, M. M. Viveiros, K. H. Burns, J. J. Eppig, and M. M. Matzuk
Identification of Gasz, an Evolutionarily Conserved Gene Expressed Exclusively in Germ Cells and Encoding a Protein with Four Ankyrin Repeats, a Sterile-{alpha} Motif, and a Basic Leucine Zipper
Mol. Endocrinol., June 1, 2002; 16(6): 1168 - 1184.
[Abstract] [Full Text] [PDF]


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