Oocyte expression, secretion and somatic cell interaction of mouse bone morphogenetic protein 15 during the peri-ovulatory period

Reproduction, Fertility and Development

Volumn 27, Issue 5, 2015, Pages 801-811

  Mester, Brigitta ^a   Ritter, Lesley J ^b   Pitman, Janet L ^a   Bibby, Adrian H ^a   Gilchrist, Robert B ^b   McNatty, Kenneth P ^a   Juengel, Jennifer L ^c   McIntosh, C Joy ^a  

^a VICTORIA UNIVERSITY OF WELLINGTON   (New Zealand)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c Reproductive Biology Invermay Agricultural Centre   (New Zealand)

Author keywords

Cumulus; follicle; granulosa; growth differentiation factor 9; in vitro maturation.

Indexed keywords

BONE MORPHOGENETIC PROTEIN 15; CHORIONIC GONADOTROPIN; GROWTH DIFFERENTIATION FACTOR 9; LUTEINIZING HORMONE; MESSENGER RNA; SERIC GONADOTROPIN; CHORIONIC GONADOTROPIN, PREGNANT MARE SERUM GONADOTROPIN DRUG COMBINATION; DRUG COMBINATION; GDF9 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CUMULUS CELL; FEMALE; GENE EXPRESSION; GONADOTROPIN BLOOD LEVEL; GRANULOSA CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; LUTEINIZING HORMONE RELEASE; MOUSE; NONHUMAN; OOCYTE; OVARY FOLLICLE CELL; OVULATION; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PROCESSING; PROTEIN SECRETION; QUANTITATIVE ANALYSIS; SOMATIC CELL; UPREGULATION; ANIMAL; DRUG COMBINATION; DRUG EFFECTS; METABOLISM;

MAMMALIA; MUS;

ANIMALS; BONE MORPHOGENETIC PROTEIN 15; CHORIONIC GONADOTROPIN; CUMULUS CELLS; DRUG COMBINATIONS; FEMALE; GONADOTROPINS, EQUINE; GRANULOSA CELLS; GROWTH DIFFERENTIATION FACTOR 9; MICE; OOCYTES; OVULATION;

EID: 84904793848     PISSN: 10313613     EISSN: 14485990     Source Type: Journal    
DOI: 10.1071/RD13336     Document Type: Article

References (51)

1. Aaltonen, J., Laitinen, M. P., Vuojolainen, K., Jaatinen, R., Horelli-Kuitunen, N., Seppa, L., Louhio, H., Tuuri, T., Sjoberg, J., Butzow, R., Hovatta, O., Dale, L., and Ritvos, O. (1999). Human growth differentiation factor 9 (GDF-9) and its novel homolog GDF-9B are expressed in oocytes during early folliculogenesis. J. Clin. Endocrinol. Metab. 84, 2744-2750.
2. Bodensteiner, K. J., Clay, C. M., Moeller, C. L., and Sawyer, H. R. (1999). Molecular cloning of the ovine growth/differentiation factor-9 gene and expression of growth/differentiation factor-9 in ovine and bovine ovaries. Biol. Reprod. 60, 381-386. doi:10.1095/BIOLREPROD60.2.381
3. 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. G., Faustino, L. R., Rossetto, R., Lopes, C. A. P., Donato, M. A. M., Peixoto, C. A., Campello, C. C., Silva, J. R. V., and 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. doi:10.1016/J.MCE.2011.02.007
4. Chu, T., Dufort, I., and Sirard, M. A. (2012). Effect of ovarian stimulation on oocyte gene expression in cattle. Theriogenology 77, 1928-1938. doi:10.1016/J.THERIOGENOLOGY.2012.01.015
5. Crawford, J. L., and 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, 339-343. doi:10.1016/J.MCE.2011.09.033
6. Di Pasquale, E., Beck-Peccoz, P., and Persani, L. (2004). Hypergonadotropic ovarian failure associated with an inherited mutation of human bone morphogenetic protein-15 (BMP15) gene. Am. J. Hum. Genet. 75, 106-111. doi:10.1086/422103
7. Dong, J., Albertini, D., Nishimori, K., Kumar, T., Lu, N., and Matzuk, M. (1996). Growth differentiation factor-9 is required during early ovarian folliculogenesis. Nature 383, 531-535. doi:10.1038/383531A0
8. Dube, J. L., Wang, P., Elvin, J., Lyons, K. M., Celeste, A. J., and Matzuk, M. M. (1998). The bone morphogenetic protein 15 gene is X-linked and expressed in oocytes. Mol. Endocrinol. 12, 1809-1817.
9. Duffy, D. M. (2003). Growth differentiation factor-9 is expressed by the primate follicle throughout the periovulatory interval. Biol. Reprod. 69, 725-732. doi:10.1095/BIOLREPROD.103.015891
10. Eckery, D. C., Whale, L. J., Lawrence, S. B., Wylde, K. A., McNatty, K. P., and Juengel, J. L. (2002). Expression of mRNA encoding growth differentiation factor 9 and bone morphogenetic protein 15 during follicular formation and growth in a marsupial, the brushtail possum (Trichosurus vulpecula). Mol. Cell. Endocrinol. 192, 115-126. doi:10.1016/S0303-7207(02)00085-0
11. Galloway, S. M., McNatty, K. P., Cambridge, L. M., Laitinen, M. P. E., Juengel, J. L., Jokiranta, T. S., McLaren, R. J., Luiro, K., Dodds, K. G., Montgomery, G. W., Beattie, A. E., Davis, G. H., and Ritvos, O. (2000). Mutations in an oocyte-derived growth factor gene (BMP15) cause increased ovulation rate and infertility in a dosage-sensitive manner. Nat. Genet. 25, 279-283. doi:10.1038/77033
12. Gilchrist, R. B., and Thompson, J. G. (2007). Oocyte maturation: emerging concepts and technologies to improve developmental potential in vitro. Theriogenology 67, 6-15. doi:10.1016/J.THERIOGENOLOGY.2006. 09.027
13. Gilchrist, R. B., Lane, M., and Thompson, J. G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159-177. doi:10.1093/HUMUPD/DMM040
14. Guéripel, X., Brun, V., and Gougeon, A. (2006). Oocyte bone morphogenetic protein 15, but not growth differentiation factor 9, is increased during gonadotropin-induced follicular development in the immature mouse and is associated with cumulus oophorus expansion. Biol. Reprod. 75, 836-843. doi:10.1095/BIOLREPROD.106.055574
15. Hanrahan, J. P., Gregan, S. M., Mulsant, P., Mullen, M., Davis, G. H., Powell, R., and Galloway, S. M. (2004). 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. 70, 900-909. doi:10.1095/BIOLREPROD.103.023093
16. Hashimoto, O., Moore, R. K., and Shimasaki, S. (2005). Posttranslational processing of mouse and human BMP-15: potential implication in the determination of ovulation quota. Proc. Natl Acad. Sci. USA 102, 5426-5431. doi:10.1073/PNAS.0409533102
17. Hosoe, M., Kaneyama, K., Ushizawa, K., Hayashi, K.-g., and Takahashi, T. (2011). Quantitative analysis of bone morphogenetic protein 15 (BMP15) and growth differentiation factor 9 (GDF9) gene expression in calf and adult bovine ovaries. Reprod. Biol. Endocrinol. 9, 33. doi:10.1186/1477-7827-9-33
18. Hussein, T. S., Froiland, D. A., Amato, F., Thompson, J. G., and Gilchrist, R. B. (2005). Oocytes prevent cumulus cell apoptosis by maintaining a morphogenic paracrine gradient of bone morphogenetic proteins. J. Cell Sci. 118, 5257-5268. doi:10.1242/JCS.02644
19. Hussein, T. S., Thompson, J. G., and Gilchrist, R. B. (2006). Oocyte-secreted factors enhance oocyte developmental competence. Dev. Biol. 296, 514-521. doi:10.1016/J.YDBIO.2006.06.026
20. Hussein, T. S., Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2011). Temporal effects of exogenous oocyte-secreted factors on bovine oocyte developmental competence during IVM. Reprod. Fertil. Dev. 23, 576-584. doi:10.1071/RD10323
21. Juengel, J. L., and McNatty, K. P. (2005). The role of proteins of the transforming growth factor-b superfamily in the intraovarian regulation of follicular development. Hum. Reprod. Update 11, 144-161. doi:10.1093/HUMUPD/DMH061
22. Juengel, J. L., Hudson, N. L., Berg, M., Hamel, K., Smith, P., Lawrence, S. B., Whiting, L., and McNatty, K. P. (2009). Effects of active immunization against growth differentiation factor 9 and/or bone morphogenetic protein 15 on ovarian function in cattle. Reproduction 138, 107-114. doi:10.1530/REP-09-0009
23. Laitinen, M., Vuojolainen, K., Jaatinen, R., Ketola, I., Aaltonen, J., Lehtonen, E., Heikinheimo, M., and Ritvos, O. (1998). A novel growth differentiation factor-9 (GDF-9) related factor is co-expressed with GDF-9 in mouse oocytes during folliculogenesis. Mech. Dev. 78, 135-140. doi:10.1016/S0925-4773(98)00161-0
24. Li, R., Norman, R. J., Armstrong, D. T., and Gilchrist, R. B. (2000). Oocytesecreted factor(s) determine functional differences between bovine mural granulosa cells and cumulus cells. Biol. Reprod. 63, 839-845. doi:10.1095/BIOLREPROD63.3.839
25. Li, H. K., Kuo, T. Y., Yang, H. S., Chen, L. R., Li, S. S., and Huang, H. W. (2008). Differential gene expression of bone morphogenetic protein 15 and growth differentiation factor 9 during in vitro maturation of porcine oocytes and early embryos. Anim. Reprod. Sci. 103, 312-322. doi:10.1016/J.ANIREPROSCI.2006.12.017
26. Liao, W. X., Moore, R. K., Otsuka, F., and Shimasaki, S. (2003). 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. 278, 3713-3719. doi:10.1074/JBC.M210598200
27. Lin, J. Y., Pitman-Crawford, J. L., Bibby, A. H., Hudson, N. L., McIntosh, C. J., Juengel, J. L., and McNatty, K. P. (2012). Effects of species differences on oocyte regulation of granulosa cell function. Reproduction 144, 557-567. doi:10.1530/REP-12-0267
28. Livak, K. J., and Schmittgen, T. D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408. doi:10.1006/METH.2001.1262
29. McGrath, S. A., Esquela, A. F., and Lee, S. J. (1995). Oocyte-specific expression of growth/differentiation factor-9. Mol. Endocrinol. 9, 131-136.
30. McIntosh, C. J., Lun, S., Lawrence, S., Western, A. H., McNatty, K. P., and Juengel, J. L. (2008). The proregion of mouse BMP15 regulates the cooperative interactions of BMP15 and GDF9. Biol. Reprod. 79, 889-896. doi:10.1095/BIOLREPROD.108.068163
31. McIntosh, C. J., Lawrence, S., Smith, P., Juengel, J. L., and 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. doi:10.1530/REP-11-0336
32. McMahon, H. E., Sharma, S., and Shimasaki, S. (2008). Phosphorylation of bone morphogenetic protein-15 and growth and differentiation factor-9 plays a critical role in determining agonistic or antagonistic functions. Endocrinology 149, 812-817. doi:10.1210/EN.2007-1439
33. 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., and Laitinen, M. P. (2005). Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129, 473-480. doi:10.1530/REP.1.0511
34. McNatty, K. P., Lawrence, S., Groome, N. P., Meerasahib, M. F., Hudson, N. L., Whiting, L., Heath, D. A., and Juengel, J. L. (2006). Meat and Livestock Association Plenary Lecture 2005. Oocyte signalling molecules and their effects on reproduction in ruminants. Reprod. Fertil. Dev. 18, 403-412. doi:10.1071/RD05104
35. Monti, M., and Redi, C. (2009). Oogenesis specific genes (Nobox, Oct4, Bmp15, Gdf9, Oogenesin1 and Oogenesin2) are differentially expressed during natural and gonadotropin-induced mouse follicular development. Mol. Reprod. Dev. 76, 994-1003. doi:10.1002/MRD.21059
36. Mottershead, D. G., Ritter, L. J., and Gilchrist, R. B. (2012). Signalling pathways mediating specific synergistic interactions between GDF9 and BMP15. Mol. Hum. Reprod. 18, 121-128. doi:10.1093/MOLEHR/GAR056
37. Otsuka, F., Moore, R. K., and Shimasaki, S. (2001). Biological function and cellular mechanism of bone morphogenetic protein-6 in the ovary. J. Biol. Chem. 276, 32 889-32 895. doi:10.1074/JBC.M103212200
38. Paradis, F., Novak, S., Murdoch, G. K., Dyck, M. K., Dixon, W. T., and Foxcroft, G. R. (2009). 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 138, 115-129. doi:10.1530/REP-08-0538
39. Parrish, E. M., Siletz, A., Xu, M., Woodruff, T. K., and Shea, L. D. (2011). Gene expression in mouse ovarian follicle development in vivo versus an ex vivo alginate culture system. Reproduction 142, 309-318. doi:10.1530/REP-10-0481
40. Pedersen, T., and Peters, H. (1968). Proposal for a classification of oocytes and follicles in the mouse ovary. J. Reprod. Fertil. 17, 555-557. doi:10.1530/JRF.0.0170555
41. Peng, J., Li, Q., Wigglesworth, K., Rangarajan, A., Kattamuri, C., Peterson, R. T., Eppig, J. J., Thompson, T. B., and 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, E776-E785. doi:10.1073/PNAS.1218020110
42. Sánchez, F., Adriaenssens, T., Romero, S., and Smitz, J. (2010). Different follicle-stimulating hormone exposure regimens during antral follicle growth alter gene expression in the cumulus-oocyte complex in mice. Biol. Reprod. 83, 514-524. doi:10.1095/BIOLREPROD. 109.083311
43. Silva, J. R., van den Hurk, R., van Tol, H. T., Roelen, B. A., and Figueiredo, J. R. (2005). Expression of growth differentiation factor 9 (GDF9), bone morphogenetic protein 15 (BMP15), andBMPreceptors in the ovaries of goats. Mol. Reprod. Dev. 70, 11-19. doi:10.1002/MRD.20127
44. Simpson, C. M., Stanton, P. G., Walton, K. L., Chan, K. L., Ritter, L. J., Gilchrist, R. B., and Harrison, C. A. (2012). Activation of latent human GDF9 by a single residue change (Gly 391 Arg) in the mature domain. Endocrinology 142, 309-318. doi:10.1210/EN.2011-1632
45. Tisdall, D. J., Hudson, N., Smith, P., and McNatty, K. P. (1994). Localization of ovine follistatin and alpha and beta A inhibin mRNA in the sheep ovary during the oestrous cycle. J. Mol. Endocrinol. 12, 181-193. doi:10.1677/JME.0.0120181
46. Wang, J., and Roy, S. K. (2004). Growth differentiation factor-9 and stem cell factor promote primordial follicle formation in the hamster: modulation by follicle-stimulating hormone. Biol. Reprod. 70, 577-585. doi:10.1095/BIOLREPROD.103.023234
47. Watson, L. N., Mottershead, D. G., Dunning, K. R., Robker, R. L., Gilchrist, R. B., and Russell, D. L. (2012). Heparan sulfate proteoglycans regulate responses to oocyte paracrine signals in ovarian follicle morphogenesis. Endocrinology 153, 4544-4555. doi:10.1210/EN.2012-1181
48. Wigglesworth, K., Lee, K.-B., O'Brien, M. J., Peng, J., Matzuk, M. M., and Eppig, J. J. (2013). Bidirectional communication between oocytes and ovarian follicular somatic cells is required for meiotic arrest of mammalian oocytes. Proc. Natl Acad. Sci. USA 110, E3723-E3729. doi:10.1073/PNAS.1314829110
49. Yan, C., Wang, P., DeMayo, J., DeMayo, F. J., Elvin, J. A., Carino, C., Prasad, S. V., Skinner, S. S., Dunbar, B. S., and Dube, J. L. (2001). Synergistic roles of bone morphogenetic protein 15 and growth differentiation factor 9 in ovarian function. Mol. Endocrinol. 15, 854-866.
50. Yeo, C. X., Gilchrist, R. B., Thompson, J. G., and Lane, M. (2008). Exogenous growth differentiation factor 9 in oocyte maturation media enhances subsequent embryo development and fetal viability in mice. Hum. Reprod. 23, 67-73. doi:10.1093/HUMREP/DEM140
51. Yoshino, O., McMahon, H. E., Sharma, S., and 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, 10 678-10 683. doi:10.1073/PNAS.0600507103