DOI QR코드

DOI QR Code

Effects of Daidzein on mRNA Expression of Bone Morphogenetic Protein Receptor Type I and II Genes in the Ovine Granulosa Cells

  • Chen, A Qin (Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Fisheries University) ;
  • Xu, Zi Rong (College of Animal Science of Zhejiang University) ;
  • Yu, Song Dong (College of Animal Science of Zhejiang University) ;
  • Yang, Zhi Gang (Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Fisheries University)
  • Received : 2008.05.12
  • Accepted : 2008.11.22
  • Published : 2010.03.01

Abstract

Daidzein, a natural isoflavonoid phytoestrogen, structurally resembles estradiol (E2) and possesses estrogenic activity. This study was designed to test the hypothesis that daidzein may mimic the effects of E2 on ovine follicle development by regulation of the mRNA expression of bone morphogenetic protein receptor genes and thereby influence the reproductive system. Granulosa cells were cultured in serum-free McCoy's 5A medium with and without supplementation of daidzein. Results showed that daidzein (10-100 ng/ml) significantly increased the proliferation of ovine granulosa cells (p<0.05), but inhibited the growth of granulosa cells at a dose of 1,000 ng/ml (p<0.01). Daidzein inhibited progesterone production in a dose dependent manner; however, it did not affect estradiol production by granulosa cells. We also investigated the effects of daidzein on BMPRII, BMPRIB and ALK-5 mRNA expression in ovine granulosa cells by quantitative real-time PCR. Treatment of granulosa cells with daidzein increased significantly expression of these genes at 10-100 ng/ml. Thus, these data suggested that a low concentration of daidzein (10-100 ng/ml) had a direct stimulatory effect on ovine granulosa cells while a high concentration was toxic.

Keywords

Daidzein;Granulosa Cells;Cell Proliferation;BMP Receptor Genes

Acknowledgement

Supported by : Zhejiang Science and Technology Committee

References

  1. Knight, P. G. and C. Glister. 2006. TGF-$\beta$ superfamily members and ovarian follicle development. Reproduction 132:191-206 https://doi.org/10.1530/rep.1.01074
  2. Kotwica, J., M. Wrobel and J. Młynarczuk. 2006. The influence of polychlorinated- biphenyls (PCBs) and phytoestrogens in vitro on functioning of reproductive tract in cow. Reprod. Biol. 6 (Suppl.):189-194
  3. Liu, H. Y., C. Q. Zhang, C. T. Ge and J. X. Liu. 2007. Effects of daidzein on mRNA expression of gonadotropin receptors and P450 aromatase in ovarian follicles of white silky fowls. Asian-Aust. J. Anim. Sci. 20:1827-1831
  4. Monget, P., S. Fabre, P. Mulsant, F. Lecerf, J. Elsen, S. Mazerbourg, C. Pisselet and D. Monniaux. 2002. Regulation of ovarian folliculogenesis by IGF and BMP system in domestic animals. Domest. Anim. Enodcrinol. 23:139-154 https://doi.org/10.1016/S0739-7240(02)00152-2
  5. Murkies, A. L., G. Wilcox and S. R. Davis. 1998. Phytoestrogens. J. Clin. Endocrinol. Metab. 83:297-303 https://doi.org/10.1210/jc.83.2.297
  6. Reinli, K. and G. Block. 1996. Phytoestrogen content of foods-a compendium of literature values. Nutr. Cancer. 26:123-148 https://doi.org/10.1080/01635589609514470
  7. Whitten, P. L. and H. B. Patisaul. 2001. Cross-species and interassay comparisons of phytoestrogen action. Environ. Health. Persp. 109(Suppl.1):5-20
  8. Campbell, B. K., R. J. Scaramuzzi and R Webb. 1996. Induction and maintenance of oestradiol and immuno-reactive inhibin production with FSH by ovine granulosa cells cultured in serum free media. J. Reprod. Fert. 106:7-16 https://doi.org/10.1530/jrf.0.1060007
  9. Makarevich, A., A. Sirotkin, T. Taradajnik and P. Chrenek. 1997. Effects of genistein and lavendustin on reproductive processes in domestic animals in vitro. J. Steroid. Biochem. Mol. Biol. 63:329-337 https://doi.org/10.1016/S0960-0760(97)00092-7
  10. Jayawardana, B. C., T. Shimizu, H. Nishmoto, E. Kaneko, M. Tetsuka and A. Miyamoto. 2006. Hormonal regulation of expression of growth differentiation factor-9 receptor type I and II genes in the bovine ovarian follicle. Reproduction 131:545-553 https://doi.org/10.1530/rep.1.00885
  11. Yi, S. E., P. S. LaPolt, B. S. Yoon, J. Y. Chen, J. K. Lu and K. M. Lyons. 2001. The type I BMP receptor BMPRIB is essential for female reproductive function. Proc. Natl. Acad. Sci. USA. 98:7994-7999 https://doi.org/10.1073/pnas.141002798
  12. Im, K. S., H. J. Kim, K. M. Chung, H. S. Kim, K. W. Park and K. Niwa. 1995. Effect of granulosa and cumulus cells on in vitro development of the bovine follicular oocytes. Asian-Aust. J. Anim. Sci. 8:317-321
  13. Liu, H. Y., C. Q. Zhang and W. D. Zeng. 2006. Estrogenic and antioxidant effects of a phytoestrogen daidzein on ovarian germ cells in embryonic chickens. Dom. Anim. Endocrinol. 31:258-268 https://doi.org/10.1016/j.domaniend.2005.11.002
  14. Moore, R. K., F. Otsuka and S. Shimasaki. 2003. Molecular basis of bone morphogenetic protein-15 signaling in granulosa cells. J. Biol. Chem. 278:304-310 https://doi.org/10.1074/jbc.M207362200
  15. McNatty, K. P., J. L. Juengel, K. L. Reader, S. Lun, S. Myllymaa, S. B. Lawrence, A. Western, M. F. Meerasahib, D. G. Mottershead, N. P. Groome, O. Ritvos and M. P. E. Laitinen. 2005. Bone morphogenetic protein 15 and growth differentiation factor 9 co-operate to regulate granulosa cell function. Reproduction 129:473-480 https://doi.org/10.1530/rep.1.0511
  16. Shimasaki, S., R. K. Moore, F. Otsuka and G. F. Erickson. 2004. The bone morphogenetic protein system in mammalian reproduction. Endocr. Rev. 25:72-101 https://doi.org/10.1210/er.2003-0007
  17. Tang, X. Y., C. Q. Zhang, W. D. Zeng, Y. L. Mi and H. Y. Liu. 2006. Proliferation effects of the flavonoids daidzein and quercetin on cultured chicken primordial germ cells through antioxidant action. Cell. Biol. Int. 30:445-451 https://doi.org/10.1016/j.cellbi.2006.02.004
  18. Purinton, S. C. and C. E. Wood. 2002. Oestrogen augments the fetal ovine hypothalamus-pituitary-adrenal axis in response to hypotension. J. Phsiol. 544:919-929 https://doi.org/10.1113/jphysiol.2002.025635
  19. Edwards, S. J., K. L. Reader, S. Lun, A. Western, S. Lawrence, K. P. McNatty and J. L. Juengel. 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 149:1026-1030 https://doi.org/10.1210/en.2007-1328
  20. Groenevel, E. H. J. and E. H. Burge. 2000. Bone morphogenetic proteins in human bone regeneration. Eur. J. Endocrinol. 142: 9-21 https://doi.org/10.1530/eje.0.1420009
  21. Vitt, U. A., C. Klein and A. J. Hseuh. 2002b. Bone morphogenetic protein receptor type II is a receptor for growth differentiation factor-9. Biol. Reprod. 67:473-480 https://doi.org/10.1095/biolreprod67.2.473
  22. Rosselli, M., K. Reinhart, B. Imthurn, P. J. Keller and R. K. Dubey. 2000. Cellular and biochemical mechanisms by which environmental oestrogens influence reproductive function. Hum. Reprod. 6:332-350 https://doi.org/10.1093/humupd/6.4.332
  23. Mulsant, P., F. Lecerf, S. Fabre, L. Schibler, P. Monget, I. Lanneluc, C. Pisselet, J. Riquet, D. Monniaux, I. Callebaut, E. Cribiu, J. Thimonier, J. Teyssier, L. Bodin, Y. Cognie, N. Chitour and J. M. Elsen. 2001. Mutation in bone morphogenetic protein receptor-IB is associated with increased ovulation rate in Booroola Merino ewes. Proc. Natl. Acad. Sci. USA. 98:5104-5109 https://doi.org/10.1073/pnas.091577598
  24. Dusza, L., R. Ciereszko, D. J. Skarzynski, L. Nogowski, M. Opalka, B. Kaminska, A. Nynca, O. Kraszewska, M. Slomczynska, I. Woclawek-Potocka, A. Korzekwa, E. Pruszynska-Oszmalek and K. Szkudelska. 2006. Mechanism of phytoestrogen action in reproductive processes of mammals and birds. Biol. Reprod. 6(Suppl.1):151-174
  25. Souza, C., B. Campbell, A. McNeilly and D. T. Baird. 2002. The effect of bone morphogenetic protein (BMP2) on oestradiol and inhibin A production by sheep granulosa cells and localization of BMP receptors in the ovary by immunohistochmistry. Reproduction 123:363-369 https://doi.org/10.1530/rep.0.1230363
  26. Jia, C. L., N. Li, X. B. Zhao, X. P. Zhu and Z. H. Jia. 2005. Association of single nucleotide polymorphisms in exon 6 region of BMPRIB gene with litter size traits in sheep. Asian-Aust. J. Anim. Sci. 18:1375-1378
  27. Shimasaki, S., R. J. Zachow, D. Li, H. Kim, S. Iemura, N. Ueno, K. Sampath, R. J. Chang and G. F. Erickson. 1999. A functional bone morphogenetic protein system in the ovary. Proc. Natl. Acad. Sci. USA. 96:7282-7287 https://doi.org/10.1073/pnas.96.13.7282
  28. Nynca, A. and R. E. Ciereszko. 2006. Effect of genistein on steroidogenic response of granulosa cell populations from porcine preovulatory follicles. Reprod. Biol. 6:31-50
  29. Wood, G. E. and D. Giroux. 2003. Central nervous system prostaglandin endoperoxide synthase-1 and -2 responses to oestradiol and cerebral hypoperfusion in late- gestation fetal sheep. J. Physiol. 549:572-581
  30. Magee, P. and I. R. Rowlan. 2004. Phyto-oestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br. J. Nutr. 91:513-531 https://doi.org/10.1079/BJN20031075
  31. Totta, P., F. Acconcia, F. Virgili, A. Cassidy, P. D. Weingerg, G. Rimbach and M. Marino. 2005. Daidzein-sulfate metabolites affect transcriptional and antiproliferative activities of estrogen receptor-$\beta$ in cultured human cancer cells. J. Nutr. 135:2687-2693
  32. Vitt, U. A., E. A. McGee, M. Hayashi and A. J. Hsueh. 2002a. In vivo treatment with GDF9 stimulates primordial and primary follicle progression and theca cell marker CYP17 in ovaries of immature rats. Endocrinology 141:3814-3820 https://doi.org/10.1210/en.141.10.3814
  33. Beck, V., U. Rohr and A. Jungbaur. 2005. Phytoestrogens derived from red clover: An alternative to estrogen replacement therapy. J. Steroid. Biochem. Mol. Biol. 94:499-518 https://doi.org/10.1016/j.jsbmb.2004.12.038
  34. Suttner, A., N. A. Danilovich, W. J. Banz and T. A. Winters. 1998. The effects of the phytoestrogen daidzein on in situ apoptosis in primary porcine granulosa cells. Proceedings of the Sixth Word Soybean Research Conference, Global Soy Forum 99, Chicago, IL, Aug. 7, p. 686
  35. Evans, A. C. O. 2003. Ovarian follicle growth and consequences for fertility in sheep. Anim. Reprod. Sci.78:289-306 https://doi.org/10.1016/S0378-4320(03)00096-4
  36. Glister, C., C. F. Kemp and P. G. Knight. 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 127:239-254 https://doi.org/10.1530/rep.1.00090
  37. Souza, C., C. MacDougall, B. Campbell, A. McNeilly and D. Baird. 2001. The Booroola (FecB) phenotype is associated with a mutation in the bone morphogenetic receptor IB (BMPRIB) gene. J. Endocrinol. 169:R1-R6 https://doi.org/10.1677/joe.0.169R001
  38. Juengel, J. L., K. J. Bodensteiner, D. A. Heath, N. L. Hudson, C. L. Moeller, P. Smith, S. M. Galloway, G. H. Davis, H. R. Sawyer and K. P. Mcnatty. 2004. Physiology of GDF9 and BMP15 signaling molecules. Anim. Reprod. Sci. 82-83:447-460 https://doi.org/10.1016/j.anireprosci.2004.04.021
  39. Vinze, M., M. K. Sharma and D. Singh. 2004. Effect of follicular fluid proteins and gonadotropins on progesterone secretion by buffalo granulosa cells in vitro. Asian-Aust. J. Anim. Sci. 17:1496-1500
  40. Jia, T. L., H. Z. Wang, L. P. Xie, X. Y. Wang and R. Q. Zhang. 2003. Daidzein enhances osteoblast growth that may be mediated by increased bone morphogenetic protein (BMP) production. Biochem. Pharmacol. 65:709-715 https://doi.org/10.1016/S0006-2952(02)01585-X
  41. Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta delta C (T)) method. Methods 25:402-408 https://doi.org/10.1006/meth.2001.1262
  42. Kurzer, M. S. and X. Xu. 1999. Dietary phytoestrogens. Annu. Rev. Nutr. 17:353-381 https://doi.org/10.1146/annurev.nutr.17.1.353