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

Molecular and Cellular Endocrinology

Volumn 348, Issue 1, 2012, Pages 339-343

  Crawford, Janet L ^a   McNatty, Kenneth P ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

Author keywords

BMP15:GDF9 mRNA ratio; Ovulation rate; Species specificity

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; GROWTH DIFFERENTIAL FACTOR 9; GROWTH FACTOR; MESSENGER RNA; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; COW; FEMALE; GENE EXPRESSION; MOUSE; NONHUMAN; OOCYTE; OVULATION; PHENOTYPE; PRIORITY JOURNAL; RAT; RED DEER; SHEEP; SPECIES DIFFERENCE; SWINE;

ANIMALS; BONE MORPHOGENETIC PROTEIN 15; CATTLE; CUMULUS CELLS; DEER; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 9; MICE; MICE, INBRED C57BL; OOCYTES; OVULATION; RATS; RATS, SPRAGUE-DAWLEY; SHEEP; SPECIES SPECIFICITY; SWINE; TRANSCRIPTION, GENETIC;

EID: 80755145974     PISSN: 03037207     EISSN: 18728057     Source Type: Journal    
DOI: 10.1016/j.mce.2011.09.033     Document Type: Article

References (43)

1. Asher, G.W., Pearse, A.J. (2002). Managing reproductive preformance of farmed deer: the key to productivity. Proceedings of the Third World Deer Farming Congress, Austin, Texas, USA, 99-112.
2. Carabatsos M.J., Elvin J., Matzuk M.M., Albertini D.F. Characterization of oocyte and follicle development in growth differentiation factor-9-deficient mice. Dev. Biol. 1998, 204:373-384.
3. Crawford J.L., Heath D.A., Reader K.L., Quirke L.D., Hudson N.L., Juengel J.L., McNatty K.P. Oocytes in sheep homozygous for a mutation in bone morphogenetic protein receptor 1B express lower mRNA levels of bone morphogenetic protein 15 but not growth differentiation factor 9. Reproduction 2011, 142:53-61.
4. Dong J., Albertini D.F., Nishimori K., Kumar T.R., Lu N., Matzuk M.M. Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 1996, 383:531-535.
5. Dragovic R.A., Ritter L.J., Schulz S.J., Amato F., Armstrong D.T., Gilchrist R.B. Role of oocyte-secreted growth differentiation factor 9 in the regulation of mouse cumulus expansion. Endocrinology 2005, 146:2798-2806.
6. Edwards S.J., Reader K.L., Lun S., Western A., Lawrence S., McNatty K.P., Juengel J.L. 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 2008, 149:1026-1030.
7. Elvin J.A., Yan C., Wang P., Nishimori K., Matzuk M.M. Molecular characterization of the follicle defects in the growth differentiation factor 9-deficient ovary. Mol. Endocrinol. 1999, 13:1018-1034.
8. 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. Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 2000, 25:279-283.
9. Hanrahan J.P., Gregan S.M., Mulsant P., Mullen M., Davis G.H., Powell R., Galloway S.M. 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. 2004, 70:900-909.
10. Hashimoto O., Moore R.K., Shimasaki S. Posttranslational processing of mouse and human BMP-15: potential implication in the determination of ovulation quota. Proc. Natl. Acad. Sci. USA 2005, 102:5426-5431.
11. Hussein T.S., Froiland D.A., Amato F., Thompson J.G., Gilchrist R.B. Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell. Sci. 2005, 118:5257-5268.
12. Hussein T.S., Thompson J.G., Gilchrist R.B. Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 2006, 296:514-521.
13. 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. Growth differentiation factor 9 and bone morphogenetic protein 15 are essential for ovarian follicular development in sheep. Biol. Reprod. 2002, 67:1777-1789.
14. Juengel J.L., McNatty K.P. The role of proteins of the transforming growth factor-beta superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 2005, 11:143-160.
15. Komisarek J., Dorynek Z. Genetic aspects of twinning in cattle. J. Appl. Genet. 2002, 43:55-68.
16. Lee G.S., Kim H.S., Hwang W.S., Hyun S.H. Characterization of porcine growth differentiation factor-9 and its expression in oocyte maturation. Mol. Reprod. Dev. 2008, 75:707-714.
17. Liao W.X., Moore R.K., Otsuka F., Shimasaki S. 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. 2003, 278:3713-3719.
18. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001, 25:402-408.
19. McIntosh C.J., Lun S., Lawrence S., Western A.H., McNatty K.P., Juengel J.L. The proregion of mouse BMP15 regulates the cooperative interactions of BMP15 and GDF9. Biol. Reprod. 2008, 79:889-896.
20. McNatty K.P., Juengel J.L., Wilson T., Galloway S.M., Davis G.H., Hudson N.L., Moeller C.L., Cranfield M., Reader K.L., Laitinen M.P., Groome N.P., Sawyer H.R., Ritvos O. Oocyte-derived growth factors and ovulation rate in sheep. Reprod. Suppl. 2003, 61:339-351.
21. McNatty K.P., Moore L.G., Hudson N.L., Quirke L.D., Lawrence S.B., Reader K., Hanrahan J.P., Smith P., Groome N.P., Laitinen M., Ritvos O., Juengel J.L. The oocyte and its role in regulating ovulation rate: a new paradigm in reproductive biology. Reproduction 2004, 128:379-386.
22. McNatty K.P., Juengel J.L., Reader K.L., Lun S., Myllymaa S., Lawrence S.B., Western A., Meerasahib M.F., Mottershead D.G., Groome N.P., Ritvos O., Laitinen M.P. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 2005, 129:473-480.
23. McNatty K.P., Juengel J.L., Reader K.L., Lun S., Myllymaa S., Lawrence S.B., Western A., Meerasahib M.F., Mottershead D.G., Groome N.P., Ritvos O., Laitinen M.P. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function in ruminants. Reproduction 2005, 129:481-487.
24. 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. Oocyte-expressed genes affecting ovulation rate. Mol. Cell. Endocrinol. 2005, 234:57-66.
25. McNatty K.P., Lawrence S., Groome N.P., Meerasahib M.F., Hudson N.L., Whiting L., Heath D.A., Juengel J.L. Meat and Livestock Association Plenary Lecture 2005. Oocyte signalling molecules and their effects on reproduction in ruminants. Reprod. Fert. Devel. 2006, 18:403-412.
26. McNatty K.P., Heath D.A., Hudson N.L., Lun S., Juengel J.L., Moore L.G. Gonadotrophin-responsiveness of granulosa cells from bone morphogenetic protein 15 heterozygous mutant sheep. Reproduction 2009, 138:545-551.
27. McNatty K.P., Heath D.A., Hudson N.L., Reader K.L., Quirke L., Lun S., Juengel J.L. The conflict between hierarchical ovarian follicular development and superovulation treatment. Reproduction 2010, 140:287-294.
28. Mester, B., Bibby, A., Crawford, J.L., McNatty, K.P., Juengel, J.L., McIntosh, C.J., 2011. Spatio-temporal expression patterns of Bmp15 and Gdf9 mRNA in the mouse ovarian follicle. Society for Reproduction and Fertility, Brighton, UK, 10-13 July, Abstract O17.
29. Moore R.K., Erickson G.F., Shimasaki S. Are BMP-15 and GDF-9 primary determinants of ovulation quota in mammals?. Trends Endocrinol. Metab. 2004, 15:356-361.
30. Otsuka F., Yao Z., Lee T., Yamamoto S., Erickson G.F., Shimasaki S. Bone morphogenetic protein-15. Identification of target cells and biological functions. J. Biol. Chem. 2000, 275:39523-39528.
31. Paradis F., Novak S., Murdoch G.K., Dyck M.K., Dixon W.T., Foxcroft G.R. Temporal regulation of BMP2, BMP6, BMP15, GDF9, BMPR1A, BMPR1B, BMPR2 and TGFBR1 mRNA expression in the oocyte, granulosa and theca cells of developing preovulatory follicles in the pig. Reproduction 2009, 138:115-129.
32. Peters H., Byskov A.G., Himelstein-Braw R., Faber M. Follicular growth: the basic event in the mouse and human ovary. J. Reprod. Fertil. 1975, 45:559-566.
33. Prochazka R., Nemcova L., Nagyova E., Kanka J. Expression of growth differentiation factor 9 messenger RNA in procine growing and preovulatory ovarian follicles. Biol. Reprod. 2004, 71:1290-1295.
34. Russell D.L., Robker R.L. Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum. Reprod. Update 2007, 13:289-312.
35. Salustri A. Paracrine actions of oocytes in the mouse pre-ovulatory follicle. Int. J. Dev. Biol. 2000, 44:591-597.
36. Scaramuzzi R.J., Baird D.T., Campbell B.K., Driancourt M.A., Dupont J., Fortune J.E., Gilchrist R.B., Martin G.B., McNatty K.P., McNeilly A.S., Monget P., Monniaux D., Vinoles C., Webb R. Regulation of folliculogenesis and the determination of ovulation rate in ruminants. Reprod. Fertil. Dev. 2011, 23:444-467.
37. Sengle G., Charbonneau N.L., Ono R.N., Sasaki T., Alvarez J., Keene D.R., Bachinger H.P., Sakai L.Y. Targeting of bone morphogenetic protein growth factor complexes to fibrillin. J. Biol. Chem. 2008, 283:13874-13888.
38. Shimasaki S., Moore R.K., Otsuka F., Erickson G.F. The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 2004, 25:72-101.
39. Silva J.R., van den Hurk R., van Tol H.T., Roelen B.A., Fiqueiredo J.R. Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), and BMP receptors in the ovaries of goats. Mol. Reprod. Dev. 2005, 70:11-19.
40. Vanderhyden B.C., Macdonald E.A., Nagyova E., Dhawan A. Evaluation of members of the TGFbeta superfamily as candidates for the oocyte factors that control mouse cumulus expansion and steroidogenesis. Reprod. Suppl. 2003, 61:55-70.
41. Walton K.L., Makanji Y., Wilce M.C., Chan K.L., Robertson D.M., Harrison C.A. A common biosynthetic pathway governs the dimerization and secretion of inhibin and related transforming growth factor beta (TGFbeta) ligands. J. Biol. Chem. 2009, 284:9311-9320.
42. Yan C., Wang P., DeMayo J., DeMayo F.J., Elvin J.A., Carino C., Prasad S.V., Skinner S.S., Dunbar B.S., Dube J.L., Celeste A.J., Matzuk M.M. Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 2001, 15:854-866.
43. Yoshino O., McMahon H.E., Sharma S., Shimasaki S. A unique preovulatory expression pattern plays a key role in the physiological functions of BMP-15 in the mouse. Proc. Natl. Acad. Sci. USA 2006, 103:10678-10683.