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Effect of Soyabean Isoflavones Exposure on Onset of Puberty, Serum Hormone Concentration and Gene Expression in Hypothalamus, Pituitary Gland and Ovary of Female Bama Miniature Pigs

  • Fan, Juexin (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Zhang, Bin (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Li, Lili (Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock, Key Laboratory for Agro-Ecological Processes of Subtropical Region, Institute of Subtropical Agriculture, The Chinese Academy of Sciences) ;
  • Xiao, Chaowu (Nutrition Research Division, Food Directorate) ;
  • Oladele, Oso Abimbola (Department of Animal Nutrition, College of Animal Science and Livestock Production, Federal University of Agriculture) ;
  • Jiang, Guoli (Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock, Key Laboratory for Agro-Ecological Processes of Subtropical Region, Institute of Subtropical Agriculture, The Chinese Academy of Sciences) ;
  • Ding, Hao (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Wang, Shengping (Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock, Key Laboratory for Agro-Ecological Processes of Subtropical Region, Institute of Subtropical Agriculture, The Chinese Academy of Sciences) ;
  • Xing, Yueteng (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Xiao, Dingfu (College of Animal Science and Technology, Hunan Agricultural University) ;
  • Yin, Yulong (Scientific Observing and Experimental Station of Animal Nutrition and Feed Science in South-Central, Ministry of Agriculture, Hunan Provincial Engineering Research Center of Healthy Livestock, Key Laboratory for Agro-Ecological Processes of Subtropical Region, Institute of Subtropical Agriculture, The Chinese Academy of Sciences)
  • Received : 2015.03.04
  • Accepted : 2015.06.11
  • Published : 2015.11.01

Abstract

This study was to investigate the effect of soyabean isoflavones (SIF) on onset of puberty, serum hormone concentration, and gene expression in hypothalamus, pituitary and ovary of female Bama miniature pigs. Fifty five, 35-days old pigs were randomly assigned into 5 treatment groups consisting of 11 pigs per treatment. Results showed that dietary supplementation of varying dosage (0, 250, 500, and 1,250 mg/kg) of SIF induced puberty delay of the pigs with the age of puberty of pigs fed basal diet supplemented with 1,250 mg/kg SIF was significantly higher (p<0.05) compared to control. Supplementation of SIF or estradiol valerate (EV) reduced (p<0.05) serum gonadotrophin releasing hormone and luteinizing hormone concentration, but increased follicle-stimulating hormone concentration in pigs at 4 months of age. The expression of KiSS-1 metastasis-suppressor (KISS1), steroidogenic acute regulatory protein (StAR) and 3-beta-hydroxysteroid dehydrogenase/delta-5-delta-4 isomerase ($3{\beta}-HSD$) was reduced (p<0.01) in SIF-supplemented groups. Expression of gonadotropin-releasing hormone receptor in the pituitary of miniature pigs was reduced (p<0.05) compared to the control when exposed to 250, 1,250 mg/kg SIF and EV. Pigs on 250 mg/kg SIF and EV also showed reduced (p<0.05) expression of cytochrome P450 19A1 compared to the control. Our results indicated that dietary supplementation of SIF induced puberty delay, which may be due to down-regulation of key genes that play vital roles in the synthesis of steroid hormones.

Keywords

References

  1. Bateman, H. L. and H. B. Patisaul. 2008. Disrupted female reproductive physiology following neonatal exposure to phytoestrogens or estrogen specific ligands is associated with decreased gnrh activation and kisspeptin fiber density in the hypothalamus. Neurotoxicology 29:988-997. https://doi.org/10.1016/j.neuro.2008.06.008
  2. Cassidy, A., S. Bingham, and K. Setchell. 1995. Biological effects of isoflavones in young women: Importance of the chemical composition of soyabean products. Br. J. Nutr. 74:587-601. https://doi.org/10.1079/BJN19950160
  3. Ciechanowska, M., M. Lapot, K. Mateusiak, and F. Przekop. 2010. Neuroendocrine regulation of gnrh release and expression of gnrh and gnrh receptor genes in the hypothalamus-pituitary unit in different physiological states. Reprod. Biol. 10:85-124. https://doi.org/10.1016/S1642-431X(12)60054-0
  4. Clapper, J. and A. Tomlin. 2012. Effects of the phytoestrogen genistein on the porcine anterior pituitary insulin-like growth factor system. Domest. Anim. Endocrinol. 42:173-182. https://doi.org/10.1016/j.domaniend.2011.11.007
  5. Dickerson, S. M. and A. C. Gore. 2007. Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev. Endocr. Metab. Disord. 8:143-159. https://doi.org/10.1007/s11154-007-9048-y
  6. Doerge, D. R. and D. M. Sheehan. 2002. Goitrogenic and estrogenic activity of soy isoflavones. Environ. Health Perspect. 110(Suppl. 3):349-353.
  7. Edson, M. A., A. K. Nagaraja, and M. M. Matzuk. 2009. The mammalian ovary from genesis to revelation. Endocr. Rev. 30:624-712. https://doi.org/10.1210/er.2009-0012
  8. Fu, W. J., J. Hu, T. Spencer, R. Carroll, and G. Wu. 2006. Statistical models in assessing fold change of gene expression in real-time RT-PCR experiments. Comput. Biol. Chem. 30:21-26. https://doi.org/10.1016/j.compbiolchem.2005.10.005
  9. Hwang, C. S., H. S. Kwak, H. J. Lim, S. H. Lee, Y. S. Kang, T. B. Choe, H. G. Hur, and K. O. Han. 2006. Isoflavone metabolites and their in vitro dual functions: They can act as an estrogenic agonist or antagonist depending on the estrogen concentration. J. Steroid Biochem. Mol. Biol. 101:246-253. https://doi.org/10.1016/j.jsbmb.2006.06.020
  10. Jefferson, W. N., E. Padilla-Banks, and R. R. Newbold. 2005. Adverse effects on female development and reproduction in cd-1 mice following neonatal exposure to the phytoestrogen genistein at environmentally relevant doses. Biol. Reprod. 73:798-806. https://doi.org/10.1095/biolreprod.105.041277
  11. Jefferson, W. N. and C. J. Williams. 2011. Circulating levels of genistein in the neonate, apart from dose and route, predict future adverse female reproductive outcomes. Reprod. Toxicol. 31:272-279. https://doi.org/10.1016/j.reprotox.2010.10.001
  12. Ju, X. H., H. J. Xu, Y. H. Yong, L. L. An, Y. M. Xu, P. R. Jiao, and M. Liao. 2014. Heat stress upregulates the expression of TLR4 and its alternative splicing variant in bama miniature pigs. J. Integr. Agric. 13:2479-2487. https://doi.org/10.1016/S2095-3119(13)60574-2
  13. Lehman, M. N., C. M. Merkley, L. M. Coolen, and R. L. Goodman. 2010. Anatomy of the kisspeptin neural network in mammals. Brain Res. 1364:90-102. https://doi.org/10.1016/j.brainres.2010.09.020
  14. Li, D. F., J. L. Nelssen, P. G. Reddy, F. Blecha, R. Klemm, and R. D. Goodband. 1991. Interrelationship between hypersensitivity to soybean proteins and growth performance in early-weaned pigs. J. Anim. Sci. 69:4062-4069. https://doi.org/10.2527/1991.69104062x
  15. Losa, S. M., K. L. Todd, A. W. Sullivan, J. Cao, J. A. Mickens, and H. B. Patisaul. 2011. Neonatal exposure to genistein adversely impacts the ontogeny of hypothalamic kisspeptin signaling pathways and ovarian development in the peripubertal female rat. Reprod. Toxicol. 31:280-289. https://doi.org/10.1016/j.reprotox.2010.10.002
  16. Lu, S. S., C. P. Lau, Y. F. Tung, S. W. Huang, Y. H. Chen, H. C. Shih, S. C. Tsai, C. C. Lu, S. W. Wang, J. J. Chen, E. J. Chien, C. H. Chien, and P. S. Wang. 1996. Lactate stimulates progesterone secretion via an increase in cAMP production in exercised female rats. Am. J. Physiol. 271:E910-915.
  17. Nahoko I., U. Yoshihisa, T. Yoko, N. Tomoko, K. Masatoshi, N. Yousuke, W. Youki, M. Shiori, T. Junko, I. Naoko, M. Fuko, O. Satoshi, M. Kei-ichiro, T. Hiroko. 2014. KISS1 gene expression in the developing brain of female pigs in pre- and peripubertal periods. J. Reprod. Dev. 60:312-316. https://doi.org/10.1262/jrd.2013-129
  18. Oakley, A. E., D. K. Clifton, and R. A. Steiner. 2009. Kisspeptin signaling in the brain. Endocr. Rev. 30:713-743. https://doi.org/10.1210/er.2009-0005
  19. Ohno, S., Y. Nakajima, K. Inoue, H. Nakazawa, and S. Nakajin. 2003. Genistein administration decreases serum corticosterone and testosterone levels in rats. Life Sci. 74:733-742. https://doi.org/10.1016/j.lfs.2003.04.006
  20. Persky, V. W., R. T. Chatterton, L. V. Van Horn, M. D. Grant, P. Langenberg, and J. Marvin. 1992. Hormone levels in vegetarian and nonvegetarian teenage girls: Potential implications for breast cancer risk. Cancer Res. 52:578-583.
  21. Setchell, K. D., L. Zimmer-Nechemias, J. Cai, and J. E. Heubi. 1998. Isoflavone content of infant formulas and the metabolic fate of these phytoestrogens in early life. Am. J. Clin. Nutr. 68:1453s-1461s. https://doi.org/10.1093/ajcn/68.6.1453S
  22. Soede, N. M., P. Langendijk, and B. Kemp. 2011. Reproductive cycles in pigs. Anim. Reprod. Sci. 124:251-258. https://doi.org/10.1016/j.anireprosci.2011.02.025
  23. Sterle, J. A. and W. R. Lamberson. 1996. Effects of exposure to an estrual female on attainment of puberty in gilts. Theriogenology 45:733-744. https://doi.org/10.1016/0093-691X(96)00003-9
  24. Stocco, D. M. 2001. StAR protein and the regulation of steroid hormone biosynthesis. Annu. Rev. Physiol. 63:193-213. https://doi.org/10.1146/annurev.physiol.63.1.193
  25. Strom, B. L., R. Schinnar, E. E. Ziegler, K. T. Barnhart, M. D. Sammel, G. A. Macones, V. A. Stallings, J. M. Drulis, S. E. Nelson, and S. A. Hanson. 2001. Exposure to soy-based formula in infancy and endocrinological and reproductive outcomes in young adulthood. Jama 286:807-814. https://doi.org/10.1001/jama.286.7.807
  26. Takeyoshi, M., M. Sawaki, S. Noda, T. Muroi, and K. Yamasaki. 2002. Effect of gonadotropin-releasing hormone antagonist on ovarian and uterine weights in immature female rats. Reprod. Toxicol. 16:367-369. https://doi.org/10.1016/S0890-6238(02)00043-6
  27. Thackray, V. G., P. L. Mellon, and D. Coss. 2010. Hormones in synergy: Regulation of the pituitary gonadotropin genes. Mol. Cell. Endocrinol. 314:192-203. https://doi.org/10.1016/j.mce.2009.09.003
  28. Tiemann, U., F. Schneider, J. Vanselow, and W. Tomek. 2007. In vitro exposure of porcine granulosa cells to the phytoestrogens genistein and daidzein: Effects on the biosynthesis of reproductive steroid hormones. Reprod. Toxicol. 24:317-325. https://doi.org/10.1016/j.reprotox.2007.07.008
  29. Tomikawa, J., T. Homma, S. Tajima, T. Shibata, Y. Inamoto, K. Takase, N. Inoue, S. Ohkura, Y. Uenoyama, K. Maeda, and H. Tsukamura. 2010. Molecular characterization and estrogen regulation of hypothalamic KISS1 gene in the pig. Biol. Reprod. 82:313-319. https://doi.org/10.1095/biolreprod.109.079863
  30. Wang, D. F., N. Y. Zhang, Y. Z. Peng, and D. S. Qi. 2010. Interaction of zearalenone and soybean isoflavone on the development of reproductive organs, reproductive hormones and estrogen receptor expression in prepubertal gilts. Anim. Reprod. Sci. 122:317-323. https://doi.org/10.1016/j.anireprosci.2010.10.002
  31. Wang, Y., W. Man Gho, F. L. Chan, S. Chen, and L. K. Leung. 2008. The red clover (Trifolium pratense) isoflavone biochanin A inhibits aromatase activity and expression. Br. J. Nutr. 99:303-310.
  32. Yan, G. R., C. L. Xiao, G. W. He, X. F. Yin, N. P. Chen, Y. Cao, and Q. Y. He. 2010. Global phosphoproteomic effects of natural tyrosine kinase inhibitor, genistein, on signaling pathways. Proteomics 10:976-986.
  33. Yin, Y. L., Z. Y. Deng, H. L. Huang, T. J. Li, and H. Y. Zhong. 2004. The effect of arabinoxylanase and protease supplementation on nutritional value of diets containing wheat bran or rice bran in growing pig. J. Anim. Feed Sci. 13:445-461.
  34. Yuan, X. X., B. Zhang, L. L. Li, C. W. Xiao, J. X. Fan, M. M. Geng, and Y. L. Yin. 2012. Effects of soybean isoflavones on reproductive parameters in Chinese mini-pig boars. J. Anim. Sci. Biotechnol. 3:31. https://doi.org/10.1186/2049-1891-3-31

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