Czech J. Anim. Sci., 2008, 53(1):1-8 | DOI: 10.17221/2718-CJAS
Effects of genistein and genistin on in vitro maturation of pig oocytes
- 1 Department of Veterinary Sciences, Czech University of Life Sciences in Prague, Prague-Suchdol, Czech Republic
- 2 Institute of Animal Science, Prague-Uhříněves, Czech Republic
The objective of the study was to verify the hypothesis that GEN (genistein - phytoestrogen and an inhibitor of tyrosine protein kinase - TPK) effects on pig oocyte maturation and cumular cell expansion under in vitro conditions are connected with its estrogenic activity. Oocytes were cultivated for 24 hours up to the stage of the first meiotic metaphase (MI). Three different doses of GEN (13, 40, 80 µg/ml of medium) and also three doses of GIN, genistin, an analogue of GEN without effects on TPK, (80, 160 and 240 µg/ml of medium) were tested. To verify the reversibility of GEN effects, the oocytes were first cultivated for 24 hours with 80 µg of GEN per 1 ml of medium and then for another 24 hours without any GEN. GEN blocked pig oocyte maturation at the stage of the germinal vesicle (GV), depending on the dose. After rinsing out the GEN the oocyte maturation recovered, but with abnormalities (32%). GIN in a concentration of 80 µg/ml of medium induced a significant blockage at the GV stage (18%). With an increase in the GIN concentration, the number of oocytes blocked at the GV stage significantly decreased, but the abnormal maturation increased (up to 31%). GEN inhibited the cumular cell expansion in proportion to its dose. GIN had a less pronounced effect. As GEN and GIN effects demonstrate similar patterns, it is probable that estrogenic activity is involved.
Keywords: phytoestrogen; isoflavone; oocyte maturation; pig; estrogenic effect; tyrosine protein kinase
Published: January 31, 2008 Show citation
References
- Akiyama T., Ishida J., Nakagawa S., Ogawara H., Watanabe S., Itoh N., Shibuya M., Fukami Y. (1987): Genistein, a specific inhibitor of tyrosine-specific protein kinases. J. Biol. Chem., 262, 5592-5595.
Go to original source...
- Barrett J. (1996): Phytoestrogens. Friends or foes? Environ. Health Perspect., 104, 478-482.
Go to original source...
Go to PubMed...
- Beker-Van Woudenberg A.R., Van Tol H.T.A., Roelen B.A.J., Colenbrander B., Bevers M.M. (2004): Estradiol and its membrane-impermeable conjugate (estradiolbovine serum albumin) during in vitro maturation of bovine oocytes: effects on nuclear and cytoplasmic maturation, cytoskeleton, and embryo quality. Biol. Reprod., 70, 1465-1474.
Go to original source...
Go to PubMed...
- Benassayag C., Perrot-Applanat M., Ferre F. (2002): Phytoestrogens as modulators of steroid action in target cells. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci., 777, 233-248.
Go to original source...
Go to PubMed...
- Bennetts H.W., Underwood E.J., Shier F.L. (1946): A breeding problem of sheep in the south-west division of Western Australia. J. Dept. Agric. West. Aust., 23, 1-12.
- Bing Y.Z., Nagai T., Rodriguez-Martinez H. (2001): Effects of cysteamine, FSH and estradiol-17 beta on in vitro maturation of porcine oocytes. Theriogenology, 55, 867-876.
Go to original source...
Go to PubMed...
- Boker L.K., Van der Schouw Y.T., De Kleijn M.J., Jacques P.F., Grobbee D.E., Peeters P.H. (2002): Intake of dietary phytoestrogens by Dutch women. J. Nutr., 132, 1319-1328.
Go to original source...
Go to PubMed...
- Bolego C., Poli A., Cignarella A., Paoletti R. (2003): Phytoestrogens: pharmacological and therapeutic perspectives. Curr. Drug Targets, 4, 77-87.
Go to original source...
Go to PubMed...
- Burton J.L., Wells M. (2002): The effect of phytoestrogens on the female genital tract. J. Clin. Pathol., 55, 401-407.
Go to original source...
Go to PubMed...
- Cassidy A. (2003): Potential risks and benefits of phytoestrogen-rich diets. Int. J. Vitam. Nutr. Res., 73, 120-126.
Go to original source...
Go to PubMed...
- Eichenlaub-Ritter U., Winterscheidt U., Vogt E., Shen Y., Tinneberg H.R., Sorensen R. (2007): 2-Methoxyestradiol induces spindle aberrations, chromosome congression failure, and nondisjunction in mouse oocytes. Biol. Reprod., 76, 784-793.
Go to original source...
Go to PubMed...
- Fritsche S., Steinhart H. (1999): Occurrence of hormonally active compounds in food: A review. Eur. Food Res. Technol., 209, 153-179.
Go to original source...
- Gallo D., Cantelmo F., Distefano M., Ferlini C., Zannoni G.F., Riva A., Morazzoni P., Bombardelli E., Mancuso S., Scambia G. (1999): Reproductive effects of dietary soy in female Wistar rats. Food Chem. Toxicol., 37, 493-502.
Go to original source...
Go to PubMed...
- Greiner L.L., Stahly T.S., Stabel T.J. (2001): The effect of dietary soy genistein on pig growth and viral replication during a viral challenge. J. Anim. Sci., 79, 1272-1279.
Go to original source...
Go to PubMed...
- Jeľová M., Scsuková S., Nagyová E., Vránová J., Procházka R., Kolena J. (2001): Effect of intraovarian factors on porcine follicular cells: cumulus expansion, granulosa and cumulus cell progesterone production. Anim. Reprod. Sci., 65, 115-126.
Go to original source...
Go to PubMed...
- Ju Y.H., Allred K.F., Allred C.D., Helferich W.G. (2006a): Genistein stimulates growth of human breast cancer cells in a novel, postmenopausal animal model, with low plasma estradiol concentrations. Carcinogenesis, 27, 1292-1299.
Go to original source...
Go to PubMed...
- Ju Y.H., Fultz J., Allred K.F., Doerge D.R., Helferich W.G. (2006b): Effects of dietary daidzein and its metabolite, equol, at physiological concentrations on the growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in ovariectomized athymic mice. Carcinogenesis, 27, 856-863.
Go to original source...
Go to PubMed...
- Jung T., Fulka J. Jr, Lee C., Moor R.M. (1993): Effects of the protein phosphorylation inhibitor genistein on maturation of pig oocytes in vitro. J. Reprod. Fertil., 98, 529-535.
Go to original source...
Go to PubMed...
- Kayisli U.A., Aksu C.A., Berkkanoglu M., Arici A. (2002): Estrogenicity of isoflavones on human endometrial stromal and glandular cells. J. Clin. Endocrinol. Metab., 87, 5539-5544.
Go to original source...
Go to PubMed...
- Knight D.C., Eden J.A. (1996): A review of the clinical effects of phytoestrogens. Obstet. Gynecol., 87, 897-904.
- Leopold A.S., Erwin M., Oh J., Browning B. (1976): Phytoestrogens: adverse effects on reproduction in California quail. Science, 191, 98-100.
Go to original source...
Go to PubMed...
- Li Q., Niwa K., Hunter M.G. (2004): Effects of 17betaestradiol on in vitro maturation of pig oocytes in protein-free medium. J. Reprod. Dev., 50, 305-313.
Go to original source...
Go to PubMed...
- Linassier C., Pierre M., Lepecq J.B., Pierre J. (1990): Mechanisms of action in Nih-3t3 cells of genistein, an inhibitor of EGF receptor tyrosine kinase-activity. Biochem. Pharmacol., 39, 187-193.
Go to original source...
Go to PubMed...
- Liu L.J., Yang T.M., Simon S.A. (2004): The protein tyrosine kinase inhibitor, genistein, decreases excitability of nociceptive neurons. Pain, 112, 131-141.
Go to original source...
Go to PubMed...
- Makarevich A., Sirotkin A., Taradajnik T., Chrenek P. (1997): Effects of genistein and lavendustin on reproductive processes in domestic animals in vitro. J. Steroid Biochem. Mol. Biol., 63, 329-337.
Go to original source...
Go to PubMed...
- Markovits J., Linassier C., Fosse P., Couprie J., Pierre J., Jacqueminsablon A., Saucier J.M., Lepecq J.B., Larsen A.K. (1989): Inhibitory effects of the tyrosine kinase inhibitor genistein on mammalian DNA topoisomerase-Ii. Cancer Res., 49, 5111-5117.
- Moore K.L., Kinsey W.H. (1994): Identification of an Ablrelated protein-tyrosine kinase in the cortex of the seaurchin egg - possible role at fertilization. Dev. Biol., 164, 444-455.
Go to original source...
Go to PubMed...
- Moravcová J., Kleinová T. (2002): Phytoestrogens in nutrition - do they bring benefit or involve risk? Chem. Listy, 96, 282-289.
- Petrová I., Rajmon R., Sedmiková M., Kuthanová Z., Jílek F. et al. (2005): Improvement of developmental competence of aged porcine oocytes by means of the synergistic effect of insulin-like growth factor-1 (IGF-1) and epidermal growth factor (EGF). Czech J. Anim. Sci., 50, 300-310.
Go to original source...
- Procházka R., Kalab P., Nagyová E. (2003): Epidermal growth factor-receptor tyrosine kinase activity regulates expansion of porcine oocyte-cumulus cell complexes in vitro. Biol. Reprod., 68, 797-803.
Go to original source...
Go to PubMed...
- Reinli K., Block G. (1996): Phytoestrogen content of foods - a compendium of literature values. Nutr. Cancer, 26, 123-148.
Go to original source...
Go to PubMed...
- Rhen T., Cidlowski J.A. (2004): Steroid hormone action. In: Strauss J.F., Barbieri R.L., Mastroianni L.Ju, Ladd K.M. Yen and Jaffe's reproductive endocrinology - physiology, pathophysio-logy, and clinical management. Elsevier, Amsterdam, 155-174.
- Rosselli M., Reinhart K., Imthurn B., Keller P.J., Dubey R.K. (2000): Cellular and biochemical mechanisms by which environmental oestrogens influence reproductive function. Hum. Reprod. Update, 6, 332-350.
Go to original source...
Go to PubMed...
- Scambia G., Gallo D., Foti E. (2002): Use of phytoestrogens in menopause. J. Endocrinol. Invest., 25, 668- 669.
Go to original source...
Go to PubMed...
- Schiff R., Massarweh S.A., Shou J., Bharwani L., Arpino G., Rimawi M., Osborne C.K. (2005): Advanced concepts in estrogen receptor biology and breast cancer endocrine resistance: implicated role of growth factor signaling and estrogen receptor coregulators. Cancer Chemother. Pharmacol., 56, 10-20.
Go to original source...
Go to PubMed...
- Setchell K.D.R., Gosselin S.J., Welsh M.B., Johnston J.O., Balistreri W.F., Kramer L.W., Dresser B.L., Tarr M.J. (1987): Dietary estrogens - a probable cause of infertility and liver-disease in captive cheetahs. Gastroenterology, 93, 225-233.
Go to original source...
Go to PubMed...
- Singh B., Barbe G.J., Armstrong D.T. (1993): Factors influencing resumption of meiotic maturation and cumulus expansion of porcine oocyte-cumulus cell complexes in vitro. Mol. Reprod. Dev., 36, 113-119.
Go to original source...
Go to PubMed...
- Smith D.M., Tenney D.Y. (1980): Effects of steroids on mouse oocyte maturation in vitro. J. Reprod. Fertil., 60, 331-338.
Go to original source...
Go to PubMed...
- Snedecor G.W., Cochran W.G. (1980): Statistical methods. 7th ed., Iowa State University Press., Iowa, USA. 1-506.
- Steer T.E., Johnson I.T., Gee J.M., Gibson G.R. (2003): Metabolism of the soybean isoflavone glycoside genistin in vitro by human gut bacteria and the effect of prebiotics. Brit. J. Nutr., 90, 635-642.
Go to original source...
Go to PubMed...
- Sun Q.Y., Luria A., Rubinstein S., Breitbart H. (1998): Protein kinase inhibitors induce the interphase transition by inactivating mitogen-activated protein kinase in mouse eggs. Zygote, 6, 277-284.
Go to original source...
Go to PubMed...
- Tatemoto H., Terada T. (1996): Activation of P34(Cdc2) kinase around the meiotic resumption in bovine oocytes cultured in vitro. Theriogenology, 45, 427-437.
Go to original source...
Go to PubMed...
- Tirone E., D'Alessandris C., Hascall V.C., Siracusa G., Salustri A. (1997): Hyaluronan synthesis by mouse cumulus cells is regulated by interactions between follicle-stimulating hormone (or epidermal growth factor) and a soluble oocyte factor (or transforming growth factor beta1). J. Biol. Chem., 272, 4787-4794.
Go to original source...
Go to PubMed...
- Van Cauwenberge A., Alexandre H. (2000): Effect of genistein alone and in combination with okadaic acid on the cell cycle resumption of mouse oocytes. Int. J. Dev. Biol., 44, 409-420.
- Viglietti-Panzica C., Mura E., Panzica G. (2007): Effects of early embryonic exposure to genistein on male copulatory behavior and vasotocin system of Japanese quail. Horm. Behav., 51, 355-363.
Go to original source...
Go to PubMed...
- Wang T.T.Y., Sathyamoorthy N., Phang J.M. (1996): Molecular effects of genistein on estrogen receptor mediated pathways. Carcinogenesis, 17, 271-275.
Go to original source...
Go to PubMed...
This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International (CC BY NC 4.0), which permits non-comercial use, distribution, and reproduction in any medium, provided the original publication is properly cited. No use, distribution or reproduction is permitted which does not comply with these terms.