The bone morphogenetic protein system and the regulation of ovarian follicle development in mammals

Zygote

Volumn 24, Issue 1, 2016, Pages 1-17

  Rossi, Rodrigo O D S ^b   Costa, José J N ^b   Silva, Anderson W B ^b   Saraiva, Márcia V A ^b   Van Den Hurk, Robert ^b   Silva, José R V ^a  

^a FEDERAL UNIVERSITY OF CEARÁ   (Brazil)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Folliculogenesis, Oogenesis; Ovary; Transforming growth factor

Indexed keywords

BONE MORPHOGENETIC PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR;

ANIMAL; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMAL; METABOLISM; OOCYTE DEVELOPMENT; OVARY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; FEMALE; MAMMALS; OOGENESIS; OVARY; SIGNAL TRANSDUCTION;

EID: 84921886197     PISSN: 09671994     EISSN: 14698730     Source Type: Journal    
DOI: 10.1017/S096719941400077X     Document Type: Article

References (135)

1. Abir, R., Ben-Haroush, A., Melamed, N., Felz, C., Krissi, H., Fisch, B. (2008). Expression of bone morphogenetic proteins 4 and 7 and their receptors IA, IB, and II in human ovaries from fetuses and adults. Fertil. Steril. 89, 1430-40.
2. Akiyama, I., Yoshino, O., Osuga, Y., Shi, J., Hirota, Y., Hirata, T., Harada, M., Koga, K., Fujimoto, A., Yano, T., Taketani, Y. (2012). The localization and regulation of proprotein convertase subtilisin/kexin (PCSK) 6 in human ovary. Am. J. Reprod. Immunol. 68, 491-8.
3. Akiyama, I., Yoshino, O., Osuga, Y. Shi, J., Takamura, M., Harada, M., Koga, K., Hirota, Y., Hirata, T., Fujii, T., Saito, S. (2014). The role of bone morphogenetic protein 6 in accumulation and regulation of neutrophils in the human ovary. Reprod. Sci. 21, 772-7.
4. Araújo, V.R., Silva, C.M.G., Magalhães, D.M., Silva, G.M., Baó, S.N., Silva, J.R.V., Figueiredo, J.R., Rodrigues, A.P.R. (2010a). Effect of bone morphogenetic protein-7 (BMP-7) on in vitro survival of caprine preantral follicles. Pesq. Vet. Bras. 30, 305-10.
5. Araújo, V.R., Lima-Verde, I.B., Name, K.P.O., Bao, S.N., Campello, C.C., Silva, J.R.V., Rodrigues, A.P.R., Figueiredo, J.R. (2010b). Bone morphogenetic protein-6 (BMP-6) induces atresia in goat primordial follicles cultured in vitro. Pesq. Vet. Bras. 30, 770-6.
6. Artini, P.G., Monteleone, P., Toldin, M.R.P., Matteucci, C., Ruggiero, M., Cela, V., Genazzani, A.R. (2007). Growth factors and folliculogenesis in polycystic ovary patients. Expert. Rev. Endocrinol. Metab. 2, 215-7.
7. Attisano, L., Wrana, J.L., Montalvo, E., Massagué, J. (1996). Activation of signalling by the activin receptor complex. Mol. Cell Biol. 16, 1066-73.
8. Berkholtz, C.B., Lai, B.E., Woodruff, T.K., Shea, L.D. (2006). Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochem. Cell Biol. 126, 583-92.
9. Bodin, L., Di Pasquale, E., Fabre, S., Bontoux, M., Monget, P., Persani, L., Mulsant, P. (2007). A novel mutation in the bone morphogenetic protein 15 gene causing defective protein secretion is associated with both increased ovulation rate and sterility in Lacaune sheep. Endocrinology 148, 393-400.
10. Bragdon, B., Moseychuk, O., Saldanha, S., King, D., Julian, J., Nohe, A. (2011). Bone morphogenetic proteins: a critical review. Cell Signal. 23, 609-20.
11. Brankin, V., Quinn, R.L., Webb, R., Hunter, M.G. (2005) BMP-2 and-6 modulate porcine theca cell function alone and co-cultured with granulosa cells. Domest. Anim. Endocrinol. 29, 593-604.
12. Caixeta, E.S., Sutton McDowall, M.L., Gilchrist, R.B., Thompson, C.A.P., Machado, M.F., Lima, P.F., Buratini, J. (2013). Bone morphogenetic protein 15 and fibroblast growth factor 10 enhance cumulus expansion, glucose uptake, and expression of genes in the ovulatory cascade during in vitro maturation of bovine cumulus-oocyte complexes. Reproduction 146, 27-3.
13. Canty-Laird, E., Carré, G.A., Mandon-Pépin, B., Kadler, K.E., Fabre, S. (2010). First evidence of bone morphogenetic protein 1 expression and activity in sheep ovarian follicles. Biol. Reprod. 83, 138-46.
14. Cao, X.K., Wang, J., Lan, X.Y., Lei, C.Z., Zhang, C.L., Qi, X.L., Chen, H. (2013). Genetic variants in BMP8B gene are associated with growth traits in Chinese native cattle. Gene 532, 108-13.
15. Celestino, J.J.H., Lima-Verde, I.B., Bruno, J.B., Matos, M.H.T., Chaves, R.N., Saraiva, M.V.A., Silva, C.M., Faustino, L.R., Rossetto, R., Lopes, C.A., Donato, M.A., Peixoto, C.A., Campello, C.C., Silva, J.R., Figueiredo, J.R. (2011). Steady state level of bone morphogenetic protein-15 in goat ovaries and its influence on in vitro development and survival of preantral follicles. Mol. Cell Endocrinol. 338, 1-9.
16. Chang, H., Brown, C.W., Matzuk, M.M. (2002). Genetic analysis of the mammalian transforming growth factorbeta superfamily. Endocr. Rev. 23, 787-823.
17. Chang, H.M., Cheng, J.C., Taylor, E., Leung, P.C. (2014). Oocyte-derived BMP15 but not GDF9 down-regulates connexin 43 expression and decreases gap junction intercellular communication activity in immortalized human granulosa cells. Mol. Hum. Reprod. 20, 373-83.
18. Chen, Y., Zhao, S., Qiao, J., Liu, P., Lian, Y., Zheng, X. (2009). Expression of bone morphogenetic protein-15 in human oocyte and cumulus granulosa cells primed with recombinant follicle-stimulating hormone followed by human chorionic gonadotropin. Fertil. Steril. 92, 2045-6.
19. Chhabra, A., Zijerdi, D., Zhang, J., Kline, A., Balian, G., Hurwitz, S. (2005). BMP-14 deficiency inhibits long bone fracture healing: a biochemical, histologic, and radiographic assessment. J. Orthop. Trauma. 19, 629-34.
20. Childs, A.J., Kinnell, H.L., Collins, C.S., Hogg, K., Bayne, R.A., Green, S.J., McNeilly, A.S., Anderson, R.A. (2010). BMP signaling in the human fetal ovary is developmentally regulated and promotes primordial germ cell apoptosis. Stem Cells 28, 1368-78.
21. Constam, D.B., Robertson, E.J. (2000). SPC4/PACE4 regulates a TGFbeta signaling network during axis formation. Genes Dev. 14, 1146-55.
22. Costa, J.J.N., Passos, M.J., Leitao, C.C.F., Vasconcelos, G.L., Saraiva, M.V.A., Figueiredo, J.R., van den Hurk, R., Silva, J.R. (2012). Levels ofmRNA for bonemorphogenetic proteins, their receptors and SMADs in goat ovarian follicles grown in vivo and in vitro. Reprod. Fertil. Dev. 24, 723-32.
23. Crawford, J.L., Mcnatty, K.P. (2012). The ratio of growth differentiation factor 9: bone morphogenetic protein 15 mRNA expression is tightly co-regulated and differs between species over a wide range of ovulation rates. Mol. Cell Endocrinol. 348, 339-43.
24. Dathe, K., Kjaer, K.W., Brehm, A., Meinecke, P., Nürnberg, P., Neto, J.C., Brunoni, D., Tommerup, N., Ott, C.E., Klopocki, E., Seemann, P., Mundlos, S. (2009). Duplications involving a conserved regulatory element downstream of BMP2 are associated with brachydactyly type A2. Am. J. Hum. Genet. 84, 483-92.
25. Derynck, R., Gelbart, W.M., Harland, R.M., Heldin, C.H., Kern, S.E., Massagué, J., Melton, D.A., Mlodzik, M., Padgett, R.W., Roberts, A.B., Smith, J., Thomsen, G.H., Vogelstein, B., Wang, X.F. (1996). Nomenclature: vertebrate mediators of TGF-family signals. Cell 87, 173.
26. Ding, X., Zhang, X., Mu, Y., Li, Y., Hao, J. (2013) Effects of BMP4/SMAD signaling pathway on mouse primordial follicle growth and survival via up-regulation of Sohlh2 and c-kit. Mol. Reprod. Dev. 80, 70-8.
27. Ducy, P., Karsenty, G. (2000). The family of bone morphogenetic proteins. Kidney Inter. 57, 2207-14.
28. Dudley, B., Palumbo, C., Nalepka, J., Molyneaux, K. (2010). BMP signaling controls formation of a primordial germ cell niche within the early genital ridges. Dev. Biol. 343, 84-93.
29. Edwards, S.J., Reader, K.L., Lun, S., Western, A., Lawrence, S., McNatty, K.P., Juengel, J.L. (2008). The cooperative effect of growth and differentiation factor-9 and bone morphogenetic protein (BMP)-15 on granulosa cell function is modulated primarily through BMP receptor II. Endocrinology 149, 1026-30.
30. Erickson, G.F., Shimasaki, S. (2001). The physiology of folliculogenesis: the role of novel growth factors. Fertil. Steril. 76, 943-9.
31. Erickson, G.F., Shimasaki, S. (2003) The spatiotemporal expression pattern of the bone morphogenetic protein family in rat ovary cell types during the estrous cycle. Reprod. Biol. Endocrinol. 1, 1-20.
32. Fatehi, A.N., van den Hurk, R., Colenbrander, B., Daemen, A.J., van Tol, H.T., Monteiro, R.M., Roelen, B.A., Bevers, M.M. (2005). Expression of bone morphogenetic protein 2 (BMP-2), 4 (BMP-4) and BMP receptors in the bovine ovary but absence of effects of BMP-2 and BMP-4 during IVM on bovine oocyte nuclear maturation and subsequent embryo development. Theriogenology 63, 872-89.
33. Frank, S., Stark, J., Hardy, K. (2008). Follicle dynamics and anovulation in polycystic ovary syndrome. Hum. Reprod. 14, 367-78.
34. Frota, I.M., Leitaõ, C.C., Costa, J.J., van den Hurk, R., Saraiva, M.V.A., Figueiredo, J.R., Silva, J.R. (2013). Levels of BMP-6 mRNA in goat ovarian follicles and in vitro effects of BMP-6 on secondary follicle development. Zygote 21, 270-8.
35. Frota, I.M.A., Leitaõ, C.C.F., Costa, J.J.N., van den Hurk, R., Brito, I.R., Saraiva, M.V.A., Figueiredo, J.R., Silva, J.R.V. (2011). Effects of BMP-7 and FSH on the development of goat preantral follicles and levels of mRNA for FSH-R, BMP-7 and BMP receptors after in-vitro culture. Anim. Reprod. 8, 25-31.
36. Galloway, S.M., McNatty, K.P., Cambridge, L.M., Laitinen, M.P., Juengel, J.L., Jokiranta, T.S., McLaren, R.J., Luiro, K., Dodds, K.G., Montgomery, G.W., Beattie, A.E., Davis, G.H., Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nature Genet. 25, 279-83.
37. Gilchrist, R.B., Lane, M., Thompson, J.G. (2008). Oocytesecreted factors: regulators of cumulus cell function and oocyte quality function and oocyte quality. Hum. Reprod. Update 14, 159-77.
38. Gitelman, S.E., Kobrin, M.S., Ye, J.Q., Lopez, A.R., Lee, A., Derynck, R. (1994). Recombinant Vgr-1/BMP-6-expressing tumors induce fibrosis and endochondral bone formation in vivo. J. Cell Biol. 126, 1595-609.
39. Glister, C., Kemp, C.F., Knight, P.G. (2004). 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 127, 239-54.
40. Goto, K., Kamiya, Y., Imamura, T., Miyazono, K., Miyazawa, K. (2007). Selective inhibitory effects of Smad6 on bone morphogenetic protein type I receptors. J. Biol. Chem. 282, 20603-11.
41. Hahn, S.A., Schutte, M., Hoque, A.T., Moskaluk, C.A., Costa, L.T., Rozenblum, E., Weinstein, C.L., Fischer, A., Yeo, C.J., Hruban, R.H., Kern, S.E. (1996). DPC4, a candidate tumor suppressor gene at human chromosome 18. Science 271, 350-3.
42. Hannan, N.R., Jamshidi, P., Pera, M.F., Wolvetang, E.J. (2009). BMP-11 and myostatin support undifferentiated growth of human embryonic stem cells in feeder-free cultures. Clon. Stem Cells. 11, 427-35.
43. Hardy, G., Kramer, B. (2000). Spatial and temporal localisation of bone morphogenetic protein-3 (osteogenin) in the developing rat submandibular gland. J. S. Afr. Dent. Assoc. 55, 136-41.
44. Ho, C.C., Bernard, D.J. (2009). Bone morphogenetic protein 2 signals via BMPR1A to regulate murine folliclestimulating hormone beta subunit transcription. Biol. Reprod. 81, 133-41.
45. Hsieh, M., Zamah, A.M., Conti, M. (2009). Epidermal growth factor-like growth factors in the follicular fluid: role in oocyte development andmaturation. Semin. Reprod. Med. 27, 52-61.
46. Huet, C., Monget, P., Pisselet, C., Hennequet, C., Locatelli, A., Monniaux, D. (1998). Chronology of events accompanying follicular atresia in hypophysectomized ewes. Changes in levels of steroidogenic enzymes, connexin 43, insulin-like growth factor II/mannose 6 phosphate receptor, extracellular matrix components, and matrix metalloproteinases. Biol. Reprod. 58, 175-85.
47. Huet, C., Monget, P., Pisselet, C., Monniaux, D. (1997). Changes in extracellular matrix components and steroidogenic enzymes during growth and atresia of antral ovarian follicles in the sheep. Biol. Reprod. 56, 1025-34.
48. Hussein, T.S., Thompson, J.G., Gilchrist, R.B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514-21.
49. Hutt, K.J., Albertini, D.F. (2007). An oocentric view of folliculogenesis and embryogenesis. Reprod. Biomed. Online 14, 758-64.
50. Inagaki, K., Otsuka, F., Miyoshi, T., Yamashita, M., Takahashi, M., Goto, J., Suzuki, J., Makino, H. (2009). p38-Mitogenactivated protein kinase stimulated steroidogenesis in granulosa cell-oocyte cocultures: role of bone morphogenetic proteins 2 and 4. Endocrinology 150, 1921-30.
51. Israel, D.I., Nove, J., Kerns, K.M., Moutsatsos, I.K., Kaufman, R.J. (1992). Expression and characterization of bone morphogenetic protein-2 in Chinese hamster ovary cells. Growth Factors 7, 139-50.
52. Juengel, J.L., Hudson, N.L., Heath, D.A., Smith, P., Reader, K.L., Lawrence, S.B., O'Connell, A.R., Laitinen, M.P., Cranfield, M., Groome, N.P., Ritvos, O., McNatty, K.P. (2002). Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 67, 1777-89.
53. Juengel, J.L., McNatty, K.P. (2005). The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11, 143-60.
54. Juengel, J.L., Reader, K.L., Bibby, A.H., Lun, S., Ross, I., Haydon, L.J. and McNatty, K.P. (2006). The role of bone morphogenetic proteins 2, 4, 6 and 7 during ovarian follicular development in sheep: contrast to rat. Reproduction 131, 501-13.
55. Kayamori, T., Kosaka, N., Miyamoto, A., Shimizu, T. (2009). The differential pathways of bone morphogenetic protein (BMP)-4 and-7 in the suppression of the bovine granulosa cell apoptosis. Mol. Cell Biochem. 323, 161-8.
56. Kayani, A.R., Glister, C., Knight, P.G. (2009). Evidence for an inhibitory role of bone morphogenetic protein(s) in the follicular-luteal transition in cattle. Reproduction 137, 67-78.
57. Kedem, A., Fisch, B., Garor, R., Ben-Zaken, A., Gizunterman, T., Felz, C., Ben-Haroush, A., Kravarusic, D., Abir, R. (2011). Growth differentiating factor 9 (GDF9) and bone morphogenetic protein 15 both activate development of human primordial follicles in vitro, with seemingly more beneficial effects of GDF9. J. Clin. Endocrinol. Metab. 96, 1246-54.
58. Khalaf, M., Morera, J., Bourret, A., Reznik, Y., Denoual, C., Herlicoviez, M., Mittre, H., Benhaim, A. (2013). BMP system expression in GCs from polycystic ovary syndrome women and the in vitro effects of BMP4, BMP6, and BMP7 on GC steroidogenesis. Eur. J. Endocrinol. 168, 437-44.
59. Kingsley, D.M. (1994). The TGF-superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8, 133-46.
60. Knight, P.G., Glister, C. (2006). TGF-beta superfamily members and ovarian follicle development. Reproduction 132, 191-206.
61. Kristensen, S.G., Andersen, K., Clement, C.A., Franks, S., Hardy, K., Andersen, C.Y. (2014). Expression of TGF-beta superfamily growth factors, their receptors, the associated SMADs and antagonists in five isolated size-matched populations of pre-antral follicles from normal human ovaries. Mol. Hum. Reprod. 20, 293-308.
62. Lawson, K.A., Dunn, N.R., Roelen, B.A.J., Zeinstra, L.M., Davis, A.M., Wright, C.V.E., Korving, J.P.W.F.M., Hogan, B.L.M. (1999). BMP4 is required for the generation of primordial germ cells in the mouse embryo. Genes Dev. 13, 424-36.
63. Lee, W.S., Otsuka, F., Moore, R.K., Shimasaki, S. (2001). Effect of bonemorphogenetic protein-7 on folliculogenesis and ovulation in the rat. Biol. Reprod. 65, 994-9.
64. Lee, M.M., Misra, M., Donahoe, P.K., MacLaughlin, D.T. (2003). MIS/AMH in the assessment of cryptorchidism and intersex conditions. Mol. Cell Endocrinol. 211, 91-8.
65. Lee, W.S., Yoon, S.J., Yoon, T.K., Cha, K.Y., Lee, S.K., Shimasaki, S., Lee, S., Lee, K.A. (2004). Effects of bone morphogenetic protein-7 (BMP-7) on primordial follicular growth in the mouse ovary. Mol. Reprod. Dev. 69, 159-63.
66. Lee, K.B., Khivansara, V., Santos, M.M., Lamba, P., Yuen, T., Sealfon, S.C., Bernard, D.J. (2007). Bone morphogenetic protein 2 and activin A synergistically stimulate folliclestimulating hormone b subunit transcription. J. Mol. Endocrinol. 38, 315-30.
67. Lembong, J.M.A., Yakoby, N., Shvartsman, S.Y. (2008). Spatial regulation of BMP signaling by patterned receptor expression. Tissue Eng. Part A 14, 1469-77.
68. Lima, I.M.T., Brito, I.R., Rossetto, R., Duarte, A.B.G., Rodrigues, G.Q., Saraiva, M.V.A., Costa, J.J., Donato, M.A., Peixoto, C.A., Silva, J.R., Figueiredo, J.R., Rodrigues, A.P. (2012). BMPRIB and BMPRII mRNA expression levels in goat ovarian follicles and the in vitro effects of BMP-15 on preantral follicle development. Cell Tissue Res. 348, 225-38.
69. Luckenbach, J.A., Dickey, J.T., Swanson, P. (2011). Folliclestimulating hormone regulation of ovarian transcripts for steroidogenesis-related proteins and cell survival, growth and differentiation factors in vitro during early secondary oocyte growth in coho salmon. Gen. Comp. Endocrinol. 171, 52-63.
70. Macias, D., Ganañ, Y., Sampath, T.K., Piedra, M.E., Ros, M.A., Hurle, J.M. (1997). Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124, 1109-17.
71. Martínez-Glez, V., Valencia, M., Caparrós-Martín, J.A., Aglan, M., Temtamy, S., Tenorio, J., Pulido, V., Lindert, U., Rohrbach, M., Eyre, D., Giunta, C., Lapunzina, P., Ruiz-Perez, V.L. (2012). Identification of a mutation causing deficient BMP1/mTLD proteolytic activity in autosomal recessive osteogenesis imperfecta. Hum. Mutat. 33, 343-50.
72. Massagué, J. (1998). TGF-signal transduction. Annu. Rev. Biochem. 67, 753-91.
73. Massagué, J., Wotton, D. (2000). Transcriptional control by the TGF-beta/Smad signaling system. Embo J. 19, 1745-54.
74. Massagué, J., Seoane, J., Wotton, D. (2005). Smad transcription factors. Genes Dev. 19, 2783-810.
75. McIntosh, C.J., Lawrence, S., Smith, P., Juengel, J.L., McNatty, K.P. (2012). Active immunization against the proregions of GDF9 or BMP15 alters ovulation rate and litter size in mice. Reproduction 143, 195-201.
76. McNatty, K.P., Smith, P., Moore, L.G., Reader, K., Lun, S., Hanrahan, J.P., Groome, N.P., Laitinen, M., Ritvos, O., Juengel, J.L. (2005). Oocyte-expressed genes affecting ovulation rate. Mol. Cell Endocrinol. 234, 57-66.
77. Miyagi, M., Mikawa, S., Sato, T., Hasegawa, T., Kobayashi, S., Matsuyama, Y., Sato, K. (2012). BMP2, BMP4, noggin, BMPRIA, BMPRIB, and BMPRII are differentially expressed in the adult rat spinal cord. Neuroscience 203, 12-26.
78. Miyoshi, T., Otsuka, F., Inagaki, K., Otani, H., Takeda, M., Suzuki, J., Goto, J., Ogura, T., Makino, H. (2007). Differential regulation of steroidogenesis by bone morphogenetic proteins in granulosa cells: involvement of extracellularly regulated kinase signaling and oocyte actions in follicle-stimulating hormone-induced estrogen production. Endocrinology 148, 337-45.
79. Miyoshi, T., Otsuka, F., Suzuki, J., Takeda, M., Inagaki, K., Kano, Y., Otani, H., Mimura, Y., Ogura, T., Makino, H. (2006). Mutual regulation of follicle-stimulating hormone signaling and bone morphogenetic protein system in human granulosa cells. Biol. Reprod. 74, 1073-82.
80. Mulsant, P., Lecerf, F., Fabre, S., Schibler, L., Monget, P., Lanneluc, I., Pisselet, C., Riquet, J., Monniaux, D., Callebaut, I., Cribiu, E., Thimonier, J., Teyssier, J., Bodin, L., Cognié, Y. Chitour, N., Elsen, J.M. (2001). Mutation in bonemorphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. P. Natl. Acad. Sci. USA 98, 5104-9.
81. Nicol, L., Faure, M.O., McNeilly, J.R., Fontaine, J., Taragnat, C., McNeilly, A.S. (2008). Bone morphogenetic protein-4 interacts with activin and GnRH to modulate gonadotrophin secretion in LbT2 gonadotrophs. J. Endocrinol. 196, 497-507.
82. Nikaido, M., Tada, M., Saji, T. and Ueno, N. (1997). Conservation of BMP signaling in zebrafish mesoderm patterning. Mech. Dev. 61, 75-88.
83. Nilsson, E.E., Skinner, M.K. (2003). Bone morphogenetic protein-4 acts as an ovarian follicle survival factor and promotes primordial follicle development. Biol. Reprod. 69, 1265-72.
84. Ohta, Y., Nakagawa, K., Imai, Y., Katagiri, T., Koike, T., Takaoka, K. (2008). Cyclic AMP enhances Smad-mediated BMP signaling through PKA-CREB pathway. J. Bone Miner. Metab. 26, 478-84.
85. Otsuka, F, Moore, KR & Shimasaki, S. (2001). Biological function and cellular mechanisms of bone morphogenetic protein-6 in the ovary. J. Biol. Chem. 276, 32889-95.
86. Otsuka, F., Shimasaki, S. (2002). A negative feedback system between oocyte bone morphogenetic protein 15 and granulosa cell kit ligand: its role in regulating granulosa cell mitosis. Proc. Natl. Acad. Sci. USA 99, 8060-5.
87. Otsuka, F., McTavish, K., Shimasaki, S. (2011). Integral role of GDF-9 and BMP-15 in ovarian function. Mol. Reprod. Dev. 78, 9-21.
88. Otsuka, F., Yao, Z., Lee, T., Yamamoto, S., Erickson, G.F., Shimasaki, S. (2000). Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem. 275, 39523-8.
89. Padhy, N., Sathya, M.L., Varma, T.R. (2009). Antral follicle size in the downregulated cycle and is relation to in vitro fertilization outcome. J. Hum. Reprod. Sci. 2, 68-71.
90. Park, S.S., Park, M.J., Joo, B.S., Joo, J.K., Son, J.B., Lee, K.S. (2012). Improvement of ovarian response and oocyte quality of aged female by administration of bone morphogenetic protein-6 in a mouse model. Reprod. Biol. Endocrinol. 10, 117.
91. Passos, M.J., Vasconcelos, G.L., Silva, A.W., Brito, I.R., Saraiva, M.V., Magalhães, D.M., Costa, J.J., Donato, M.A., Ribeiro, R.P., Cunha, E.V., Peixoto, C.A., Campello, C.C., Figueiredo, J.R., van den Hurk, R., Silva, J.R. (2013). Accelerated growth of bovine preantral follicles in vitro after stimulation with both FSH and BMP-15 is accompanied by ultrastructural changes and increased atresia. Theriogenology 79, 1269-77.
92. Peng, J., Li, Q., Wigglesworth, K., Rangarajan, A., Kattamuri, C., Peterson, R.T., Eppig, J.J., Thompson, T.B., Matzuk, M.M. (2013). Growth differentiation factor 9: bone morphogenetic protein 15 heterodimers are potent regulators of ovarian functions. Proc. Natl. Acad. Sci. USA 110, 776-85.
93. Pierre, A., Pisselet, C., Dupont, J., Bontoux, M., Monget, P. (2005). Bone morphogenetic protein 5 expression in the rat ovary: biological effects on granulosa cell proliferation and steroidogenesis. Biol. Reprod. 73, 1102-8.
94. Qiao, J., Feng, H.L. (2011). Extra-and intra-ovarian factors in polycystic ovary syndrome: impact on oocyte maturation and embryo developmental competence. Hum. Reprod. Update 17, 17-33.
95. Ross, A.J., Tilman, C., Yao, H., MacLaughlin, D., Capel, B. (2003). AMH induces mesonephric cell migration in XX gonads. Mol. Cell Endocrinol. 211, 1-7.
96. Saitou, M., Yamaji, M. (2010). Germ cell specification in mice: Signaling, transcription regulation, and epigenetic consequences. Reproduction 139, 931-42.
97. Samad, T.A., Rebbapragada, A., Bell, E., Zhang, Y., Sidis, Y., Jeong, S.J., Campagna, J.A., Perusini, S., Fabrizio, D.A., Schneyer, A.L., Lin, H.Y., Brivanlou, A.H., Attisano, L., Woolf, C.J. (2005). DRAGON, a bone morphogenetic protein co-receptor. J. Biol. Chem. 280, 14122-9.
98. Sánchez, F., Adriaenssens, T., Romero, S., Smitz, J. (2009). Quantification of oocyte-specific transcripts in follicle-enclosed oocytes during antral development and maturation in vitro. Mol. Hum. Reprod. 15, 539-50.
99. Savage, C., Das, P., Finelli, A.L., Townsend, S.R., Sun, C.Y., Baird, S.E., Padgett, R.W. (1996). Caenorhabditis elegans genes sma-2, sma-3, and sma-4 define a conserved family of transforming growth factor-pathway components. Proc. Natl. Acad. Sci. USA 93, 790-4.
100. Seidah, N.G., Chretien, M. (1999). Proprotein and prohormone convertases: a family of subtilases generating diverse bioactive polypeptides. Brain Res. 848, 45-62.
101. Selvaraju, S., Folger, J.K., Gupta, P.S., Ireland, J.J., Smith, G.W. (2013). Stage-specific expression and effect of bone morphogenetic protein 2 on bovine granulosa cell estradiol production: regulation by cocaine and amphetamine regulated transcript. Domest. Anim. Endocrinol. 44, 115-20.
102. Sekelsky, J.J., Newfeld, S.J., Raftery, L.A., Chartoff, E.H., Gelbart, W.M. (1995). Genetic characterization and cloning of mothers against dpp, a gene required for decapentaplegic function in Drosophila melanogaster. Genetics 139, 1347-58.
103. Shi, J., Yoshino, O., Osuga, Y., Akiyama, I., Harada, M., Koga, K., Fujimoto, A., Yano, T., Taketani, Y. (2012). Growth differentiation factor 3 is induced by bone morphogenetic protein 6 (BMP-6) and BMP-7 and increases luteinizing hormone receptor messenger RNA expression in human granulosa cells. Fertil. Steril. 97, 979-83.
104. Shi, J., Yoshino, O., Osuga, Y., Nishii, O., Yano, T., Taketani, Y. (2010). Bone morphogenetic protein 7 (BMP-7) increases the expression of follicle-stimulating hormone (FSH) receptor in human granulosa cells. Fertil. Steril. 93, 1273-9.
105. Shimasaki, S., Zachow, R.J., Li, D., Kim, H., Iemura, S., Ueno, N., Sampath, K., Chang, R.J., Erickson, G.F. (1999). A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. USA 96, 7282-7.
106. Shimasaki, S., Moore, R.K., Otsuka, F., Erickson, G.F. (2004). The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25, 72-101.
107. Shimizu, T., Yokoo, M., Miyake, Y., Sasada, H., Sato, E. (2004). Differential expression of bone morphogenetic protein 4-6 (BMP-4,-5, and-6) and growth differentiation factor-9 (GDF-9) during ovarian development in neonatal pigs. Domest. Anim. Endocrinol. 27, 397-405.
108. Silva, J.R.V., van den Hurk, R., van Tol, H.T., Roelen, B.A., Figueiredo, J.R. (2006). The Kit ligand/c-Kit receptor system in goat ovaries: gene expression and protein localization. Zygote 14, 317-28.
109. Silva, J.R.V., van den Hurk, R., van Tol, H.T.A., Roelen, B.A.J., Figueiredo, J.R. (2005). Expression of growth differentiation factor-9 (GDF-9), bone morphogenetic protein 15 (BMP-15) and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 70, 11-9.
110. Song, K., Krause, C., Shi, S., Patterson, M., Suto, R., Grgurevic, L., Vukicevic, S., van Dinther, M., Falb, D., Ten Dijke, P., Alaoui-Ismaili, M.H. (2010). Identification of a key residue mediating bone morphogenetic protein (BMP)-6 resistance to noggin inhibition allows for engineered BMPs with superior agonist activity. J. Biol. Chem. 285, 12169-80.
111. Souza, C.J., Campbell, B.K., McNeilly, A.S., Baird, D.T. (2002) Effect of bone morphogenetic protein 2 (BMP2) on oestradiol and inhibin A production by sheep granulosa cells, and localization of BMP receptors in the ovary by immunohistochemistry. Reproduction 123, 363-9.
112. Sugimura, S., Ritter, L.J., Sutton-McDowall, M.L., Mottershead, D.G., Thompson, J.G., Gilchrist, R.B. (2014). Amphiregulin co-operates with bone morphogenetic protein 15 to increase bovine oocyte developmental competence: effects on gap junctionmediated metabolite supply. Mol. Hum. Reprod. 20, 499-513.
113. Sugiyama, R., Fuzitou, A., Takahashi, C., Akutagawa, O., Ito, H., Nakagawa, K., Sugiyama, R., Isaka, K. (2010). Bone morphogenetic protein 2 may be a good predictor of success in oocyte fertilization during assisted reproductive technology. Hum. Cell 23, 83-8.
114. Takebayashi, K., Takakura, K., Wang, H., Kimura, F., Kasahara, K., Noda, Y. (2000). Mutation analysis of the growth differentiation factor-9 and-9B genes in patients with premature ovarian failure and polycystic ovary syndrome. Fertil. Steril. 74: 976-9.
115. Tandon, M., Gokul, K., Ali, S.A., Chen, Z., Lian, J., Stein, G.S., Pratap, J. (2012). Runx2 mediates epigenetic silencing of the bone morphogenetic protein-3B (BMP-3B/GDF10) in lung cancer cells. Mol. Cancer. 18, 11-27.
116. Tanno, T., Noel, P., Miller, J.L. (2010). Growth differentiation factor 15 in erythroid health and disease. Curr. Opin. Hematol. 17, 184-90.
117. Teixeira Filho, F.L., Baracat, E.C., Lee, T.H., Suh, C.S., Matsui, M., Chang, R.J., Shimasaki, S., Erickson, G.F. (2002). Aberrant expression of growth differentiation factor-9 in oocytes of women with polycystic ovary syndrome. J Clin. Endocrinol. Metab. 87, 1337-44.
118. Urist, M.R. (1965). Bone: formation by autoinduction. Science 150, 893-9.
119. Vitt, U.A., Hsu, S.Y., Hsueh, A.J.W. (2001). Evolution and classification of cystine knot-containing hormones and related extracellular signaling molecules. Mol. Endocrinol. 15, 681-94.
120. Wang, E.A., Rosen, V., D'Alessandro, J.S., Bauduy, M., Cordes, P., Harada, T., Israel, D., Hewick, R.M., Kerns, K.M., Lapan, P., Luxenberg, D.P., McQuaid, D., Moutsatsos, I.K., Nove, J., Wozney, J.M. (1990). Recombinant human bone morphogenetic protein induces bone formation. Proc. Natl. Acad. Sci. USA 87, 2220-4.
121. West, F.D., Roche-Rios, M.I., Abraham, S., Rao, R.R., Natrajan, M.S., Bacanamwo, M., Stice, S.L. (2010). KIT ligand and bone morphogenetic protein signaling enhances human embryonic stem cell to germlike cell differentiation. Hum. Reprod. 25, 168-78.
122. Wieser, R., Wrana, J.L., Massagué, J. (1995). GS domain mutations that constitutively activate T-R-I, the downstream signaling component in the TGF-receptor complex. EMBO J. 14, 2199-208.
123. Williams, L.A., Bhargav, D., Diwan, A.D. (2008). Unveiling the Bmp13 enigma: redundant morphogen or crucial regulator Int. J. Biol. Sci. 4, 318-29.
124. Wilson, T., Wu, X.Y., Juengel, J.L., Ross, I.K., Lumsden, J.M., Lord, E.A. (2001). 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. 64, 1225-35.
125. Witthuhn, B.A., Bernlohr, D.A. (2001) Upregulation of bone morphogenetic protein GDF-3/Vgr-2 expression in adipose tissue of FABP4/aP2 null mice. Cytokine 14, 129-35.
126. Wrana, J.L., Attisano, L., Wieser, R., Ventura, F., Massagué, J. (1994). Mechanism of activation of the TGF-receptor. Nature 370, 341-7.
127. Wu, Y.T., Tang, L., Cai, J., Lu, X.E., Xu, J., Zhu, X.M., Luo, Q., Huang, H.F. (2007). High bone morphogenetic protein-15 level in follicular fluid is associated with high quality oocyte and subsequent embryonic development. Hum. Reprod. 22, 1526-31.
128. Wu, Y.T., Wang, T.T., Chen, X.J., Zhu, X.M., Dong, M.Y., Sheng, J.Z., Xu, C.M., Huang, H.F. (2012). Bone morphogenetic protein-15 in follicle fluid combined with agemay differentiate between successful and unsuccessful poor ovarian responders. Reprod. Biol. Endocrinol. 10, 1-6.
129. Xia, Y., Yu, P.B., Sidis, Y., Beppu, H., Bloch, K.D., Schneyer, A.L., Lin, H.Y. (2007). Repulsive guidance molecule RGMa alters utilization of bone morphogenetic protein (BMP) type II receptors by BMP2 and BMP4. J. Biol. Chem. 282, 18129-40.
130. Yeh, L.C., Lee, J.C. (2010). Effects of cartilage-derived morphogenetic protein-3 on the expression of chondrogenic and osteoblastic markers in the pluripotent mesenchymal C3H10T1/2 cell line. Growth Factors 28, 117-28.
131. Ying, Y., Zhao, G.Q. (2001). Cooperation of endodermderived BMP2 and extraembryonic ectoderm-derived BMP4 in primordial germ cell generation in the mouse. Dev. Biol. 232, 484-92.
132. Ying, Y., Liu, X.M., Marble, A., Lawson, K.A., Zhao, G.Q. (2000). Requirement of BMP8b for the generation of primordial germ cells in the mouse. Mol. Endocrinol. 14, 1053-63.
133. Yoshimura, Y., Wallach, E.E. (1987). Studies of the mechanism(s) of mammalian ovulation. Fert. Steril. 47, 22-34.
134. Yoshino, O., McMahon, H.E., Sharma, S., Shimasaki, S. (2006). A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc. Natl. Acad. Sci. USA 103, 10678-83.
135. Zhao, G.Q., Hogan, B.L. (1996). Evidence that mouse Bmp8a (Op2) and Bmp8b are duplicated genes that play a role in spermatogenesis and placental development. Mech. Dev. 57, 159-68.