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Endocrine Reviews 25 (1): 72-101
Copyright © 2004 by The Endocrine Society

The Bone Morphogenetic Protein System In Mammalian Reproduction

Shunichi Shimasaki, R. Kelly Moore, Fumio Otsuka and Gregory F. Erickson

Department of Reproductive Medicine, University of California San Diego, School of Medicine, La Jolla, California 92093-0633

Correspondence: Address all correspondence and requests for reprints to: Shunichi Shimasaki, Ph.D., Department of Reproductive Medicine, University of California San Diego, 9500 Gilman Drive, La Jolla, California 92093-0633. E-mail: sshimasaki{at}ucsd.edu

Using molecular, cellular, and genetic approaches, recent studies examining the role of the bone morphogenetic protein (BMP) family of growth factors in the reproductive system have led to significant breakthroughs in our understanding of mammalian reproduction and fertility. Gene expression studies have revealed that key components of the BMP system (ligands, receptors, signaling molecules, and binding proteins) exhibit coordinated spatial and temporal expression patterns in fundamental cell types throughout the reproductive system. Availability of recombinant BMPs has enabled functional studies that have demonstrated important biological activities of BMPs in controlling cellular proliferation, differentiation, and apoptosis in reproductive tissues. The physiological importance of the BMP system for mammalian reproduction has been further highlighted by the elucidation of the aberrant reproductive phenotypes of animals with naturally occurring mutations or targeted deletions of certain BMP family genes. Collectively, these studies have established the concept that the BMP system plays a crucial role in fertility in female and male mammals. The purpose of this article is to review the evidence underpinning the importance of the BMP system in mammalian reproduction.




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EndocrinologyHome page
E. Clelland, G. Kohli, R. K. Campbell, S. Sharma, S. Shimasaki, and C. Peng
Bone Morphogenetic Protein-15 in the Zebrafish Ovary: Complementary Deoxyribonucleic Acid Cloning, Genomic Organization, Tissue Distribution, and Role in Oocyte Maturation
Endocrinology, January 1, 2006; 147(1): 201 - 209.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
R. W. Cook, T. B. Thompson, S. P. Kurup, T. S. Jardetzky, and T. K. Woodruff
Structural Basis for a Functional Antagonist in the Transforming Growth Factor {beta} Superfamily
J. Biol. Chem., December 2, 2005; 280(48): 40177 - 40186.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
Y. Kano, F. Otsuka, M. Takeda, J. Suzuki, K. Inagaki, T. Miyoshi, M. Miyamoto, H. Otani, T. Ogura, and H. Makino
Regulatory Roles of Bone Morphogenetic Proteins and Glucocorticoids in Catecholamine Production by Rat Pheochromocytoma Cells
Endocrinology, December 1, 2005; 146(12): 5332 - 5340.
[Abstract] [Full Text] [PDF]


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J. Cell Sci.Home page
T. S. Hussein, D. A. Froiland, F. Amato, J. G. Thompson, and R. B. Gilchrist
Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins
J. Cell Sci., November 15, 2005; 118(22): 5257 - 5268.
[Abstract] [Full Text] [PDF]


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ReproductionHome page
T R. Kumar
What have we learned about gonadotropin function from gonadotropin subunit and receptor knockout mice?
Reproduction, September 1, 2005; 130(3): 293 - 302.
[Abstract] [Full Text] [PDF]


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ReproductionHome page
J Buratini Jr, A B Teixeira, I B Costa, V F Glapinski, M G L Pinto, I C Giometti, C M Barros, M Cao, E S Nicola, and C A Price
Expression of fibroblast growth factor-8 and regulation of cognate receptors, fibroblast growth factor receptor-3c and -4, in bovine antral follicles
Reproduction, September 1, 2005; 130(3): 343 - 350.
[Abstract] [Full Text] [PDF]


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ReproductionHome page
I Demeestere, J Centner, C Gervy, Y Englert, and A Delbaere
Impact of various endocrine and paracrine factors on in vitro culture of preantral follicles in rodents
Reproduction, August 1, 2005; 130(2): 147 - 156.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
F. Otsuka, R. K. Moore, X. Wang, S. Sharma, T. Miyoshi, and S. Shimasaki
Essential Role of the Oocyte in Estrogen Amplification of Follicle-Stimulating Hormone Signaling in Granulosa Cells
Endocrinology, August 1, 2005; 146(8): 3362 - 3367.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
Y. Xia, Y. Sidis, A. Mukherjee, T. A. Samad, G. Brenner, C. J. Woolf, H. Y. Lin, and A. Schneyer
Localization and Action of Dragon (Repulsive Guidance Molecule b), a Novel Bone Morphogenetic Protein Coreceptor, throughout the Reproductive Axis
Endocrinology, August 1, 2005; 146(8): 3614 - 3621.
[Abstract] [Full Text] [PDF]


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J EndocrinolHome page
M-O Faure, L Nicol, S Fabre, J Fontaine, N Mohoric, A McNeilly, and C Taragnat
BMP-4 inhibits follicle-stimulating hormone secretion in ewe pituitary
J. Endocrinol., July 1, 2005; 186(1): 109 - 121.
[Abstract] [Full Text] [PDF]


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Hum Reprod UpdateHome page
N. Josso, C. Belville, N. di Clemente, and J.-Y. Picard
AMH and AMH receptor defects in persistent Mullerian duct syndrome
Hum. Reprod. Update, July 1, 2005; 11(4): 351 - 356.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
R. A. Dragovic, L. J. Ritter, S. J. Schulz, F. Amato, D. T. Armstrong, and R. B. Gilchrist
Role of Oocyte-Secreted Growth Differentiation Factor 9 in the Regulation of Mouse Cumulus Expansion
Endocrinology, June 1, 2005; 146(6): 2798 - 2806.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
O. Hashimoto, R. K. Moore, and S. Shimasaki
Posttranslational processing of mouse and human BMP-15: Potential implication in the determination of ovulation quota
PNAS, April 12, 2005; 102(15): 5426 - 5431.
[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
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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Mol. Endocrinol.Home page
B. D. Cherrington, T. A. Farmerie, C. A. Lents, J. D. Cantlon, M. S. Roberson, and C. M. Clay
Activin Responsiveness of the Murine Gonadotropin-Releasing Hormone Receptor Gene Is Mediated by a Composite Enhancer Containing Spatially Distinct Regulatory Elements
Mol. Endocrinol., April 1, 2005; 19(4): 898 - 912.
[Abstract] [Full Text] [PDF]


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EndocrinologyHome page
C. Glister, S. L. Richards, and P. G. Knight
Bone Morphogenetic Proteins (BMP) -4, -6, and -7 Potently Suppress Basal and Luteinizing Hormone-Induced Androgen Production by Bovine Theca Interna Cells in Primary Culture: Could Ovarian Hyperandrogenic Dysfunction Be Caused by a Defect in Thecal BMP Signaling?
Endocrinology, April 1, 2005; 146(4): 1883 - 1892.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
Y. Park, E. T. Maizels, Z. J. Feiger, H. Alam, C. A. Peters, T. K. Woodruff, T. G. Unterman, E. J. Lee, J. L. Jameson, and M. Hunzicker-Dunn
Induction of Cyclin D2 in Rat Granulosa Cells Requires FSH-dependent Relief from FOXO1 Repression Coupled with Positive Signals from Smad
J. Biol. Chem., March 11, 2005; 280(10): 9135 - 9148.
[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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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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EndocrinologyHome page
M. Takeda, F. Otsuka, K. Nakamura, K. Inagaki, J. Suzuki, D. Miura, H. Fujio, H. Matsubara, H. Date, T. Ohe, et al.
Characterization of the Bone Morphogenetic Protein (BMP) System in Human Pulmonary Arterial Smooth Muscle Cells Isolated from a Sporadic Case of Primary Pulmonary Hypertension: Roles of BMP Type IB Receptor (Activin Receptor-Like Kinase-6) in the Mitotic Action
Endocrinology, September 1, 2004; 145(9): 4344 - 4354.
[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. A. Pangas, C. J. Jorgez, and M. M. Matzuk
Growth Differentiation Factor 9 Regulates Expression of the Bone Morphogenetic Protein Antagonist Gremlin
J. Biol. Chem., July 30, 2004; 279(31): 32281 - 32286.
[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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