DOI QR코드

DOI QR Code

Effect of Vitamin D3 on Biosynthesis of Estrogen in Porcine Granulosa Cells via Modulation of Steroidogenic Enzymes

  • Hong, So-Hye (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • Lee, Jae-Eon (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • An, Sung-Min (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • Shin, Ye Young (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • Hwang, Dae Youn (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • Yang, Seung Yun (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University) ;
  • Cho, Seong-Keun (Animal Science, College of Natural Resources & Life Science, Pusan National University) ;
  • An, Beum-Soo (Department of Biomaterials Science, College of Natural Resources & Life Science, Pusan National University)
  • Received : 2016.11.15
  • Accepted : 2016.12.13
  • Published : 2017.01.15

Abstract

Vitamin D3 is a fat-soluble secosteroid responsible for enhancing intestinal absorption of calcium, iron, and other materials. Vitamin D3 deficiency, therefore, can cause health problems such as metabolic diseases, and bone disorder. Female sex hormones including estrogen and progesterone are biosynthesized mainly in the granulosa cells of ovary. In this study, we isolated granulosa cells from porcine ovary and cultured for the experiments. In order to examine the effect of vitamin D3 on the ovarian granulosa cells, the mRNA and protein levels of genes were analyzed by real-time PCR and Western blot assay. The production of estrogen from the granulosa cells was also measured by the ELISA assay. Genes associated with follicle growth were not significantly altered by vitamin D3. However, it increases expression of genes involved in the estrogen-biosynthesis. Further, estrogen concentrations in porcine granulosa cell-cultured media increased in response to vitamin D3. These results showed that vitamin D3 is a powerful regulator of sex steroid hormone production in porcine granulosa cells, suggesting that vitamin D deficiency may result in inappropriate sexual development of industrial animals and eventually economic loss.

Keywords

References

  1. Holick, M.F. (1994) McCollum Award Lecture, 1994: vitamin D--new horizons for the 21st century. Am. J. Clin. Nutr., 60, 619-630. https://doi.org/10.1093/ajcn/60.4.619
  2. Bell, T.D., Demay, M.B. and Burnett-Bowie, S.A. (2010) The biology and pathology of vitamin D control in bone. J. Cell. Biochem., 111, 7-13. https://doi.org/10.1002/jcb.22661
  3. Hollis, B.W. (1996) Assessment of vitamin D nutritional and hormonal status: what to measure and how to do it. Calcif. Tissue Int., 58, 4-5. https://doi.org/10.1007/BF02509538
  4. DeLuca, H.M., Holick, M.F., Schnoes, H.K., Suda, T. and Cousins, R.J. (1971) Isolation and identification of 1, 25-dihydroxycholecalciferol. A metabolite of vitamin D active in intestine. Biochemistry, 10, 2799-2804. https://doi.org/10.1021/bi00790a023
  5. DeLuca, H.F. (2004) Overview of general physiologic features and functions of vitamin D. Am. J. Clin. Nutr., 80, 1689S-1696S. https://doi.org/10.1093/ajcn/80.6.1689S
  6. Hewison, M. (2008) Vitamin D and innate immunity. Curr. Opin. Investig. Drugs, 9, 485-490.
  7. Hart, P.H. (2012) Vitamin D supplementation, moderate sun exposure, and control of immune diseases. Discov. Med., 13, 397-404.
  8. Ponsonby, A.L., McMichael, A. and van der Mei, I. (2002) Ultraviolet radiation and autoimmune disease: insights from epidemiological research. Toxicology, 181,71-78.
  9. Bolland, M.J., Grey, A., Gamble, G.D. and Reid, I.R. (2014) The effect of vitamin D supplementation on skeletal, vascular, or cancer outcomes: a trial sequential meta-analysis. Lancet Diabetes Endocrinol., 2, 307-320. https://doi.org/10.1016/S2213-8587(13)70212-2
  10. Forman, J.P., Scott, J.B., Ng, K., Drake, B.F., Suarez, E.G., Hayden, D.L., Bennett, G.G., Chandler, P.D., Hollis, B.W., Emmons, K.M., Giovannucci, E.L., Fuchs, C.S. and Chan, A.T. (2013) Effect of vitamin D supplementation on blood pressure in blacks. Hypertension, 61, 779-785. https://doi.org/10.1161/HYPERTENSIONAHA.111.00659
  11. Kang, E.J., Lee, J.E., An, S.M., Lee, J.H., Kwon, H.S., Kim, B.C., Kim, S.J., Kim, J.M., Hwang, D.Y., Jung, Y.J., Yang, S.Y., Kim, S.C. and An, B.S. (2015) The effects of vitamin D3 on lipogenesis in the liver and adipose tissue of pregnant rats. Int. J. Mol. Med., 36, 1151-1158. https://doi.org/10.3892/ijmm.2015.2300
  12. Pike, J.W., Meyer, M.B. and Martowicz, M.L. (2009) New techniques in transcription research extend our understanding of the molecular actions of the vitamin D hormone. IBMS BoneKEy, 6, 169-180. https://doi.org/10.1138/20090376
  13. Zhang, R. and Naughton, D.P. (2010) Vitamin D in health and disease: current perspectives. Nutr. J., 9, 65. https://doi.org/10.1186/1475-2891-9-65
  14. Zarnani, A.H., Shahbazi, M., Salek-Moghaddam, A., Zareie, M., Tavakoli, M., Ghasemi, J., Rezania, S., Moravej, A., Torkabadi, E., Rabbani, H. and Jeddi-Tehrani, M. (2010) Vitamin D3 receptor is expressed in the endometrium of cycling mice throughout the estrous cycle. Fertil. Steril., 93, 2738-2743. https://doi.org/10.1016/j.fertnstert.2009.09.045
  15. Avila, E., Diaz, L., Halhali, A. and Larrea, F. (2004) Regulation of 25-hydroxyvitamin D 3 1${\alpha}$-hydroxylase, 1, 25-dihydroxyvitamin D3 24-hydroxylase and vitamin D receptor gene expression by 8-bromo cyclic AMP in cultured human syncytiotrophoblast cells. J. Steroid Biochem. Mol. Biol., 89, 115-119.
  16. Irani, M. and Merhi, Z. (2014) Role of vitamin D in ovarian physiology and its implication in reproduction: a systematic review. Fertil. Steril., 102, 460-468. https://doi.org/10.1016/j.fertnstert.2014.04.046
  17. Kotsuji, F. and Tominaga, T. (1994) The role of granulosa and theca cell interactions in ovarian structure and function. Microsc. Res. Tech., 27, 97-107. https://doi.org/10.1002/jemt.1070270204
  18. Eppig, J.J., Wigglesworth, K. and Pendola, F.L. (2002) The mammalian oocyte orchestrates the rate of ovarian follicular development. Proc. Natl. Acad. Sci. U.S.A., 99, 2890-2894. https://doi.org/10.1073/pnas.052658699
  19. Payne, A.H. and Hales, D.B. (2004) Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. Endocr. Rev., 25, 947-970. https://doi.org/10.1210/er.2003-0030
  20. Peluso, C., Fonseca, F.L., Rodart, I.F., Cavalcanti, V., Gastaldo, G., Christofolini, D.M., Barbosa, C.P. and Bianco, B. (2014) AMH: An ovarian reserve biomarker in assisted reproduction. Clin. Chim. Acta, 437, 175-182. https://doi.org/10.1016/j.cca.2014.07.029
  21. Tao, Y.X. and Segaloff, D.L. (2009) Follicle stimulating hormone receptor mutations and reproductive disorders. Prog. Mol. Biol. Transl. Sci., 89,115-131.
  22. Georges, A., Auguste, A., Bessiere, L., Vanet, A., Todeschini, A.L. and Veitia, R.A. (2013) FOXL2: a central transcription factor of the ovary. J. Mol. Endocrinol., 52, R17-R33. https://doi.org/10.1530/JME-13-0159
  23. Hanukoglu, I. (1992) Steroidogenic enzymes: structure, function, and role in regulation of steroid hormone biosynthesis. J. Steroid Biochem. Mol. Biol., 43, 779-804. https://doi.org/10.1016/0960-0760(92)90307-5
  24. Zhu, B.T. and Conney, A.H. (1998) Functional role of estrogen metabolism in target cells: review and perspectives. Carcinogenesis, 19, 1-27. https://doi.org/10.1093/carcin/19.1.1
  25. Gruber, C.J., Tschugguel, W., Schneeberger, C. and Huber, J.C. (2002) Production and actions of estrogens. N. Engl. J. Med., 346, 340-352. https://doi.org/10.1056/NEJMra000471
  26. Hong S.H., Lee, J.E., Kim, H.S., Jung, Y.J., Hwang, D., Lee, J.H., Yang, S.Y., Kim, S.C., Cho, S.K. and An, B.S. (2016) Effect of vitamin D3 on production of progesterone in porcine granulosa cells by regulation of steroidogenic enzymes. J. Biomed. Res., 30, 203-208.
  27. Brody, S. and Wiqvist, N. (1961) Ovarian hormones and uterine growth: Effects of estradiol and progesterone on cell growth and cell division in the rat uterus. Endocrinology, 68, 971-977. https://doi.org/10.1210/endo-68-6-971
  28. Okada, H. (1993) Metabolism, structure and biological activity of sex steroids. Nihon Naibunpi Gakkai Zasshi, 69, 67-79.
  29. Distler, W. (1993) The role of sex steroids for genesis of breast and endometrial cancer. Gynakologe, 26, 94-99.
  30. Yoshiki, N. and Aso, T. (1997) The regulation mechanism of the female menstrual cycle. Nippon Rinsho, 55, 2840-2848.
  31. Wojtusik, J. and Johnson, P.A. (2012) Vitamin D regulates anti-Mullerian hormone expression in granulosa cells of the hen. Biol. Reprod., 86, 91.
  32. Merhi, Z., Doswell, A., Krebs, K. and Cipolla, M. (2014) Vitamin D alters genes involved in follicular development and steroidogenesis in human cumulus granulosa cells. J. Clin. Endocrinol. Metab., 99, E1137-E1145. https://doi.org/10.1210/jc.2013-4161

Cited by

  1. Inhibition of di(2-ethylhexyl) phthalate (DEHP)-induced endocrine disruption by co-treatment of vitamins C and E and their mechanism of action vol.81, pp.16, 2018, https://doi.org/10.1080/15287394.2018.1473262