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Molecular Endocrinology 15 (6): 854-866
Copyright © 2001 by The Endocrine Society

Synergistic Roles of Bone Morphogenetic Protein 15 and Growth Differentiation Factor 9 in Ovarian Function

Changning Yan, Pei Wang, Janet DeMayo, Francesco J. DeMayo, Julia A. Elvin, Cecilia Carino, Sarvamangala V. Prasad, Sheri S. Skinner, Bonnie S. Dunbar, Jennifer L. Dube, Anthony J. Celeste and Martin M. Matzuk

Departments of Pathology (C.Y., M.M.M.), Molecular and Cellular Biology (P.W., J.D., F.J.D., C.C., S.V.P., S.S.S., B.S.D., M.M.M.), and Molecular and Human Genetics (J.A.E., M.M.M.) Baylor College of Medicine Houston, Texas, 77030
Department of Tissue Growth and Repair (J.L.D., A.J.C.) Genetics Institute, Inc. Cambridge, Massachusetts 02140

Knockout mouse technology has been used over the last decade to define the essential roles of ovarian-expressed genes and uncover genetic interactions. In particular, we have used this technology to study the function of multiple members of the transforming growth factor-ß superfamily including inhibins, activins, and growth differentiation factor 9 (GDF-9 or Gdf9). Knockout mice lacking GDF-9 are infertile due to a block in folliculogenesis at the primary follicle stage. In addition, recombinant GDF-9 regulates multiple cumulus granulosa cell functions in the periovulatory period including hyaluronic acid synthesis and cumulus expansion. We have also cloned an oocyte-specific homolog of GDF-9 from mice and humans, which is termed bone morphogenetic protein 15 (BMP-15 or Bmp15). To define the function of BMP-15 in mice, we generated embryonic stem cells and knockout mice, which have a null mutation in this X-linked gene. Male chimeric and Bmp15 null mice are normal and fertile. In contrast to Bmp15 null males and Gdf9 knockout females, Bmp15 null females (Bmp15-/-) are subfertile and usually have minimal ovarian histopathological defects, but demonstrate decreased ovulation and fertilization rates. To further decipher possible direct or indirect genetic interactions between GDF-9 and BMP-15, we have generated double mutant mice lacking one or both alleles of these related homologs. Double homozygote females (Bmp15-/-Gdf9-/-) display oocyte loss and cysts and resemble Gdf9-/- mutants. In contrast, Bmp15-/-Gdf9+/- female mice have more severe fertility defects than Bmp15-/- females, which appear to be due to abnormalities in ovarian folliculogenesis, cumulus cell physiology, and fertilization. Thus, the dosage of intact Bmp15 and Gdf9 alleles directly influences the destiny of the oocyte during folliculogenesis and in the periovulatory period. These studies have important implications for human fertility control and the maintenance of fertility and normal ovarian physiology.




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K. P McNatty, J. L Juengel, K. L Reader, S. Lun, S. Myllymaa, S. B Lawrence, A. Western, M. F Meerasahib, D. G Mottershead, N. P Groome, et al.
Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function
Reproduction, April 1, 2005; 129(4): 473 - 480.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
K. P McNatty, J. L Juengel, K. L Reader, S. Lun, S. Myllymaa, S. B Lawrence, A. Western, M. F Meerasahib, D. G Mottershead, N. P Groome, et al.
Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants
Reproduction, April 1, 2005; 129(4): 481 - 487.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
J. D. Hennebold, K. Mah, W. Perez, J. E. Vance, R. L. Stouffer, C. Morisseau, B. D. Hammock, and E. Y. Adashi
Identification and Characterization of an Ovary-Selective Isoform of Epoxide Hydrolase
Biol Reprod, April 1, 2005; 72(4): 968 - 975.
[Abstract] [Full Text] [PDF]

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 Hum Reprod UpdateHome page
J.L. Juengel and K.P. McNatty
The role of proteins of the transforming growth factor-{beta} superfamily in the intraovarian regulation of follicular development
Hum. Reprod. Update, March 1, 2005; 11(2): 144 - 161.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
F. H. Thomas, J.-F. Ethier, S. Shimasaki, and B. C. Vanderhyden
Follicle-Stimulating Hormone Regulates Oocyte Growth by Modulation of Expression of Oocyte and Granulosa Cell Factors
Endocrinology, February 1, 2005; 146(2): 941 - 949.
[Abstract] [Full Text] [PDF]

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 Hum ReprodHome page
L.J. McKenzie, S.A. Pangas, S.A. Carson, E. Kovanci, P. Cisneros, J.E. Buster, P. Amato, and M.M. Matzuk
Human cumulus granulosa cell gene expression: a predictor of fertilization and embryo selection in women undergoing IVF
Hum. Reprod., December 1, 2004; 19(12): 2869 - 2874.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
M. Donnison and P. L. Pfeffer
Isolation of Genes Associated with Developmentally Competent Bovine Oocytes and Quantitation of Their Levels During Development
Biol Reprod, December 1, 2004; 71(6): 1813 - 1821.
[Abstract] [Full Text] [PDF]

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 J. Clin. Endocrinol. Metab.Home page
G. A. R. Maciel, E. C. Baracat, J. A. Benda, S. M. Markham, K. Hensinger, R. J. Chang, and G. F. Erickson
Stockpiling of Transitional and Classic Primary Follicles in Ovaries of Women with Polycystic Ovary Syndrome
J. Clin. Endocrinol. Metab., November 1, 2004; 89(11): 5321 - 5327.
[Abstract] [Full Text] [PDF]

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 ReproductionHome page
K P McNatty, L G Moore, N L Hudson, L D Quirke, S B Lawrence, K Reader, J P Hanrahan, P Smith, N P Groome, M Laitinen, et al.
The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology
Reproduction, October 1, 2004; 128(4): 379 - 386.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
S. Pennetier, S. Uzbekova, C. Perreau, P. Papillier, P. Mermillod, and R. Dalbies-Tran
Spatio-Temporal Expression of the Germ Cell Marker Genes MATER, ZAR1, GDF9, BMP15,andVASA in Adult Bovine Tissues, Oocytes, and Preimplantation Embryos
Biol Reprod, October 1, 2004; 71(4): 1359 - 1366.
[Abstract] [Full Text] [PDF]

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 Physiol. GenomicsHome page
J. Yao, X. Ren, J. J. Ireland, P. M. Coussens, T. P. L. Smith, and G. W. Smith
Generation of a bovine oocyte cDNA library and microarray: resources for identification of genes important for follicular development and early embryogenesis
Physiol Genomics, September 16, 2004; 19(1): 84 - 92.
[Abstract] [Full Text] [PDF]

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 Mol. Endocrinol.Home page
D. Tomic, K. P. Miller, H. A. Kenny, T. K. Woodruff, P. Hoyer, and J. A. Flaws
Ovarian Follicle Development Requires Smad3
Mol. Endocrinol., September 1, 2004; 18(9): 2224 - 2240.
[Abstract] [Full Text] [PDF]

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 Biol. Reprod.Home page
R.B. Gilchrist, L.J. Ritter, M. Cranfield, L.A. Jeffery, F. Amato, S.J. Scott, S. Myllymaa, N. Kaivo-Oja, H. Lankinen, D.G. Mottershead, et al.
Immunoneutralization of Growth Differentiation Factor 9 Reveals It Partially Accounts for Mouse Oocyte Mitogenic Activity
Biol Reprod, September 1, 2004; 71(3): 732 - 739.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
S. Sudo, O. Avsian-Kretchmer, L. S. Wang, and A. J. W. Hsueh
Protein Related to DAN and Cerberus Is a Bone Morphogenetic Protein Antagonist That Participates in Ovarian Paracrine Regulation
J. Biol. Chem., May 28, 2004; 279(22): 23134 - 23141.
[Abstract] [Full Text] [PDF]

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 Hum Reprod UpdateHome page
J. D. Hennebold
Characterization of the ovarian transcriptome through the use of differential analysis of gene expression methodologies
Hum. Reprod. Update, May 1, 2004; 10(3): 227 - 239.
[Abstract] [Full Text] [PDF]

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 J. Biol. Chem.Home page
W. X. Liao, R. K. Moore, and S. Shimasaki
Functional and Molecular Characterization of Naturally Occurring Mutations in the Oocyte-secreted Factors Bone Morphogenetic Protein-15 and Growth and Differentiation Factor-9
J. Biol. Chem., April 23, 2004; 279(17): 17391 - 17396.
[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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 Biol. Reprod.Home page
J. P. Hanrahan, S. M. Gregan, P. Mulsant, M. Mullen, G. H. Davis, R. Powell, and S. M. Galloway
Mutations in the Genes for Oocyte-Derived Growth Factors GDF9 and BMP15 Are Associated with Both Increased Ovulation Rate and Sterility in Cambridge and Belclare Sheep (Ovis aries)
Biol Reprod, April 1, 2004; 70(4): 900 - 909.
[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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 Biol. Reprod.Home page
J. L. Juengel, N. L. Hudson, L. Whiting, and K. P. McNatty
Effects of Immunization Against Bone Morphogenetic Protein 15 and Growth Differentiation Factor 9 on Ovulation Rate, Fertilization, and Pregnancy in Ewes
Biol Reprod, March 1, 2004; 70(3): 557 - 561.
[Abstract] [Full Text] [PDF]

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 DevelopmentHome page
D. Schmidt, C. E. Ovitt, K. Anlag, S. Fehsenfeld, L. Gredsted, A.-C. Treier, and M. Treier
The murine winged-helix transcription factor Foxl2 is required for granulosa cell differentiation and ovary maintenance
Development, February 15, 2004; 131(4): 933 - 942.
[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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 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
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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 Biol. Reprod.Home page
Y. Yang, A. Balla, N. Danilovich, and M. R. Sairam
Developmental and Molecular Aberrations Associated with Deterioration of Oogenesis During Complete or Partial Follicle-Stimulating Hormone Receptor Deficiency in Mice
Biol Reprod, October 1, 2003; 69(4): 1294 - 1302.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
T. G. Shepherd and M. W. Nachtigal
Identification of a Putative Autocrine Bone Morphogenetic Protein-Signaling Pathway in Human Ovarian Surface Epithelium and Ovarian Cancer Cells
Endocrinology, August 1, 2003; 144(8): 3306 - 3314.
[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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 Biol. Reprod.Home page
B. Mandon-Pepin, A. Oustry-Vaiman, B. Vigier, F. Piumi, E. Cribiu, and C. Cotinot
Expression Profiles and Chromosomal Localization of Genes Controlling Meiosis and Follicular Development in the Sheep Ovary
Biol Reprod, March 1, 2003; 68(3): 985 - 995.
[Abstract] [Full Text] [PDF]


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