Review Article
The morpho-functional parameters of rat pituitary hormone producing cells after genistein treatment
Svetlana Trifunović * ,
Verica Milošević

Mac Vet Rev 2018; 41 (1): 5 - 19

10.1515/macvetrev-2017-0027

Received: 02 June 2017

Received in revised form: 17 July 2017

Accepted: 30 August 2017

Available Online First: 19 November 2017

Published on: 15 March 2018

Correspondence: Svetlana Trifunović, lanat@ibiss.bg.ac.rs
PDF HTML

Abstract

Phytoestrogens are a diverse group of steroid–like compounds that occur naturally in many plants. There are various types of phytoestrogens, including the best-researched isoflavones which are commonly found in soy. The consumption of soy products has many health benefits, including protection against breast cancer, prostate cancer, menopausal symptoms, heart disease and osteoporosis. In contrast, use of hormonally active compounds-isoflavones may unfortunately interfere with the endocrine system and can have far-reaching consequences. Genistein, the most abundant soy-bean derived isoflavone, possesses a ring system similar to estrogens and acts through an estrogen receptor (ER)-mediated mechanism, by increasing or decreasing the transcription of ER-dependent target genes. Also, genistein can act on cells through ER non-dependent mechanisms, such as tyrosine kinase inhibitor. The neuroendocrine systems are responsible for the control of homeostatic processes in the body, including reproduction, growth, metabolism and energy balance, and stress responsiveness. It is well known, that estrogen is important for development of the neuroendocrine system in both sexes. At the pituitary level, estrogen is known to affect the regulation of all hormone producing (HP) cells, by direct and/or indirect mechanisms. Due to structural and functional resemblance to estrogen, the question may arise of whether and how genistein affects the morphofunctional features of pituitary HP cells. This review deals with the consequences of genistein’s effects on morphological, stereological and hormonal features of HP cells within the anterior pituitary gland. Transparency on this issue is needed because isoflavones are presently highly consumed. Inter alia, genistein as well as other isoflavones, are present in various dietary supplements and generally promoted as an accepted alternative to estrogen replacement therapy. Potential isoflavone biomedical exploitation is not only limited to estrogen replacement therapy, so it should be treated in a wider context of different ageing symptoms remediation.

Keywords: genistein, pituitary gland, hormone producing cells


References

1. Patisaul, H.B., Jefferson, W. (2010). The pros and cons of phytoestrogens. Front Neuroendocrinol. 31, 400-419. https://doi.org/10.1016/j.yfrne.2010.03.003 PMid:20347861 PMCid:PMC3074428
2. Setchell, K.D., Borriello, S.P., Hulme, P., Kirk, D.N., Axelson, M. (1984). Nonsteroidal estrogens of dietary origin:possible roles in hormone-dependent disease. Am J Clin Nutr. 40, 569-578. PMid:6383008
3. Wet, L., Birac, P.M., Pratt, D.E. (1978). Separation of the isomeric isoflavones from soybeans by high-performance liquid chromatography. J Chromatogr. 150, 266–268.
https://doi.org/10.1016/S0021-9673(01)92130-2
4. Cheng, E., Story, C.D., Yoder, L., Hale, W.H., Burrough, W. (1953). Estrogenic activity of isoflavone derivatives extracted and prepared from soybean oil meal. Science 118, 164–165. https://doi.org/10.1126/science.118.3058.164 PMid:13076231
5. Batterham, T.J., Hart, N.K., Lamberton, J.A. (1965). Metabolism of oestrogenic isoflavones in sheep. Nature 4983, 509. https://doi.org/10.1038/206509a0
6. Kuiper, G.G., Lemmen, J.G., Carlsson, B., Corton, J.C., Safe, S.H., van der Saag, P.T., van der Burg, B., Gustafsson, J.A. (1998). Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139, 4252-4263. https://doi.org/10.1210/endo.139.10.6216 PMid:9751507
7. Lephart, E.D., West, T.W., Weber, K.S., Rhees, R.W., Setchell, K.D., Adlercreutz, H., Lund, T.D. (2002). Neurobehavioral effects of dietary soy phytoestrogens. Neurotoxicol Teratol. 24, 5-16. https://doi.org/10.1016/S0892-0362(01)00197-0
8. Kostelac, D., Rechkemmer, G., Briviba, K. (2003). Phytoestrogens modulate binding response of estrogen receptors alpha and beta to the estrogen response element. J Agric Food Chem. 51, 7632-7635. https://doi.org/10.1021/jf034427b PMid:14664520
9. Patisaul, H.B. (2005). Phytoestrogen action in the adult and developing brain. J Neuroendocrinol. 17, 57-64. https://doi.org/10.1111/j.1365-2826.2005.01268.|ax PMid:15720476
10. Setchell, K.D., Cassidy, A. (1999). Dietary isoflavones:biological effects and relevance to human health. J Nutr. 129, 758-767.
11. Adlercreutz, H., Mazur, W. (1997). Phyto-oestrogens and Western diseases. Ann Med. 29, 95-120. https://doi.org/10.3109/07⅚99709113696 PMid:91−5
12. Shemesh, M., Lindner, H. R., Ayalaoan, N. (1972). Affinity of rabbit uterine oestradiol receptor for phyto-oestrogens and its use in a competitive protein-binding radioassay for plasma coumestrol. J Reprod Fertil. 29, 1–9. https://doi.org/10.1530/jrf.0.0290001 PMid:5017011
13. Piontek, M., Hangels, K.J., Porschen, R., Strohmeyer, G. (1993). Anti-proliferative effect of tyrosine kinase inhibitors in epidermal growth factor stimulated growth of human gastric cancer cells. Anticancer Res. 13, 2119–2123. PMid:8297123
14. Boutin, J.A. (1994). Tyrosine protein kinase inhibition and cancer. Int J Biochem Cell Bio. 26, 1203–1226. https://doi.org/10.1016/0020-711X(94)90091-4
15. Kurzer, M.S., Xia, X. (1997). Dietary Phytoestrogens Annu Rev Nutr. 17, 353–381. https://doi.org/10.1146/annurev.nutr.17.1.353 PMid:9240932
16. Okura, A., Arakawa, H., Oka, H., Yoshinari, T., Monden, Y. (1988). Effect of genistein on topoisomerase activity and on the growth of [Val 12] Ha-ras-transformed NIH 3T3 cells. Biochem Biophys Res Commun. 157, 183–189. https://doi.org/10.1016/S0006-291X(88)80030-5
17. Hu, G.,X, Zhao, B.H., Chu, Y.H., Zhou, H.Y., Akingbemi, B.T., Zheng, Z.Q, Ge, R.S. (2010). Effects of genistein and equol on human and rat testicular 3beta-hydroxysteroid dehydrogenase and 17beta-hydroxysteroid dehydrogenase 3 activities. Asian J Androl. 12(4):519-526. https://doi.org/10.1038/aja.2010.18 PMid:20453869 PMCid:PMC3739362
18. Adlercreutz, H. (1990). Western diet and Western diseases:some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest Suppl. 201, 3-23.
https://doi.org/10.1080/003655190090Ↄ8 PMid:2173856
19. Wang, H., Li, J., Gao, Y., Xu, Y., Pan, Y., Tsuji, I., Sun, Z.J., Li, X.M. (2010). Xeno-oestrogens and phyto-oestrogens are alternative ligands for the androgen receptor. Asian J Androl. 12, 535-547. https://doi.org/10.1038/aja.2010.14 PMid:20436506 PMCid:PMC3739360
20. Lee, H.P., Gourley, L., Duffy, S.W., Estève, J., Lee, J., Day, N.E. (1991). Dietary effects on breast-cancer risk in Singapore. Lancet 337, 1197–1200.
https://doi.org/10.1016/0140-6736(91)92867-2
21. Adlercreutz, H., Honjo, H., Higashi, A., Fotsis, T., Hämäläinen, E., Hasegawa, T., Okada, H. (1991). Urinary excretion of lignans and isoflavonoid phytoestrogens in Japanese men and women consuming a traditional Japanese diet. Am J Clin Nutr. 54, 1093–1100. PMid:1659780
22. Ingram, D., Sanders, K., Kolybaba, M., Lopez, D. (1997). Case-control study of phyto-oestrogens and breast cancer. Lancet 350, 990-994.
https://doi.org/10.1016/S0140-6736(97)01339-1
23. Shimizu, H., Ross, R.K., Bernstein, L., Yatani, R., Henderson, B.E., Mack, T.M. (1991). Cancers of the prostate and breast among Japanese and white immigrants in Los Angeles County. Br J Cancer. 63, 963-966. https://doi.org/10.1038/bjc.1991.210 PMid:2069852 PMCid:PMC1972548
24. Watanabe, S., Koessel, S (1993). Colon cancer:an approach from molecular epidemiology. J Epidemiol. 3, 47-61. https://doi.org/10.2188/jea.3.47
25. Severson, R.K., Nomura, A.M., Grove, J.S., Stemmermann, G.N. (1989). A prospective study of demographics, diet, and prostate cancer among men of Japanese ancestry in Hawaii. Cancer Res. 49, 1857-1860. PMid:2924323
26. Anthony, M.S., Clarkson, T.B., Hughes, C.L.Jr., Morgan, T.M., Burke, G.L. (1996). Soybean isoflavones improve cardiovascular risk factors without affecting the reproductive system of peripubertal rhesus monkeys. J Nutr. 126, 43-50. PMid:8558324
27. Tikkanen, M.J., Wahala, K., Ojala, S., Vihma, V., Adlercreutz, H. (1998). Effect of soybean phytoestrogen intake on low density lipoprotein oxidation resistance. Proc Natl Acad Sci USA 95, 3106-3110. https://doi.org/10.1073/pnas.95.6.3106 PMid:9501223 PMCid:PMC19702
28. Raines, E.W., Ross, R. (1995). Biology of atherosclerotic plaque formation:possible role of growth factors in lesion development and the potential impact of soy. J Nutr. 125, 624-630.
29. Šošić-Jurjević, B., Filipović, B., Ajdžanović, V., Brkić, D., Ristić, N., Stojanoski, M.M., Nestorović, N., Trifunović, S., Sekulić. M (2007). Subcutaneously administrated genistein and daidzein decrease serum cholesterol and increase triglyceride levels in male middle-aged rats. Exp Biol Med. 232, 1222-1227. https://doi.org/10.3181/0703-BC-82 PMid:17895530
30. Filipović, B., Šošić-Jurjević, B., Ajdžanović, V., Brkić, D., Manojlović-Stojanoski, M., Milošević, V., Sekulić, M. (2010). Daidzein administration positively affects thyroid C cells and bone structure in orchidectomized middle-aged rats. Osteoporos Int. 21, 1609-1616. https://doi.org/10.1007/s00198-009-1092-x PMid:19↔40
31. Messina, M., Ho, S., Alekel, D.L. (2004) Skeletal benefits of soy isoflavones:a review of the clinical trial and epidemiologic data. Curr Opin Clin Nutr Metab Care. 7(6):649-658. https://doi.org/10.1097/00075197-200411000-00010
32. Dalais, F.S., Rice, G.E., Wahlqvist, M.L., Grehan, M., Murkies, A.L., Medley, G., Ayton, R., Strauss, B.J. (1998). Effects of dietary phytoestrogens in postmenopausal women. Climacteric 1, 124-129. https://doi.org/10.3109/13697139809085527 PMid:11907915
33. Miao Q., Li J., Miao S., Hu N., Zhang J., Zhang S., Xie Y., Wang J., Wang S. (2012). The bone-protective effect of genistein in the animal model of bilateral ovariectomy:Roles of phytoestrogens and PTH/PTHR1 against post-menopausal osteoporosis. Int J Mol Sci. 13(1):56–70. PMid:22312238
34. Adlercreutz, C.H., Goldin, B.R., Gorbach, S.L., Hockerstedt, K.A., Watanabe, S., Hamalainen, E.K., Markkanen, M.H., Makela, T.H., Wahala, K.T., Adlercreutz, T. (1995). Soybean phytoestrogen intake and cancer risk. J Nutr. 125, 757-770.
35. Ajdžanović, V., Šosić-Jurjević, B., Filipović, B., Trifunović, S., Manojlović-Stojanoski, M., Sekulić, M., Milosević, V. (2009). Genistein-induced histomorphometric and hormone secreting changes in the adrenal cortex in middle-aged rats. Exp Biol Med (Maywood). 234, 148-156. https://doi.org/10.3181/0807-RM-231 PMid:19064942
36. Banerje, S., Li, Y., Wang, Z., Sarkar, F.H. (2008) Multi-target therapy of cancer by genistein Cancer Lett. 269(2):226–242. https://doi.org/10.1016/j.canlet.2008.03.052 PMid:18492603 PMCid:PMC2575691
37. Jefferson, W.N., Couse, J.F., Padilla-Banks, E., Korach, K.S., Newbold, R.R. (2002). Neonatal exposure to genistein induces estrogen receptor (ER) alpha expression and multioocyte follicles in the maturing mouse ovary:evidence for ER beta-mediated and nonestrogenic actions. Biol Reprod. 67, 1285-1296. https://doi.org/10.1095/biolreprod67.4.1285 PMid:12297547
38. Jefferson,W.N., Padilla-Banks, E., Newbold, R.R. (2007). Disruption of the developing female reproductive system by phytoestrogens:genistein as an example. Mol Nutr Food Res. 51, 832-844. https://doi.org/10.1002/mnfr.200600258 PMid:17604387
39. Medigović, I.M., Živanović, J.B., Ajdžanović, V.Z., Nikolić-Kokić, A.L., Stanković, S.D., Trifunović, S.L., Milošević, V.Lj., Nestorović, N.M. (2015). Effects of soy phytoestrogens on pituitary-ovarian function in middle-aged female rats. Endocrine 50, 764-776. https://doi.org/10.1007/s12020-015-0691-x PMid:26215277
40. Lindner, H.R. (1976). Occurrence of anabolic agents in plants and their importance. Environ Qual Safety Suppl. pp. 151–158.
41. Allred, C.D., Allred, K.F., Ju, Y.H., Virant, S.M., Helferich, W.G. (2001). Soy diets containing varying amounts of genistein stimulate growth of estrogen-dependent (MCF-7) tumors in a dose-dependent manner. Cancer Res. 61, 5045-5050. PMid:11431339
42. Ju, Y.H., Allred, C.D., Allred, K.F., Karko, K.L., Doerge, D.R., Helferich, W.G. (2001). Physiological concentrations of dietary genistein dose-dependently stimulate growth of estrogen-dependent hum and breast cancer (MCF-7) tumors implanted in athymic nude mice. J Nutr. 131, 2957-2962. PMid:11694625
43. Unfer, V., Casini, M.L., Costabile, L., Mignosa, M., Gerli, S., Di Renzo, G.C. (2004). Endometrial effects of long-term treatment with phytoestrogens:a randomized, double-blind, placebo-controlled study. Fertil Steril. 82, 145-148. https://doi.org/10.1016/j.fertnstert.2003.11.041 PMid:15237003
44. Nohynek, G.J., Borgert, C.J., Dietrich, D., Rozman, K.K. (2013). Endocrine disruption:fact or urban legend?Toxicol Lett. 223, 295-305. https://doi.org/10.1016/j.toxlet.2013.10.022 PMid:24177261
45. Goldin, B.R., Brauner, E., Adlercreutz, H., Ausman, L.M., Lichtenstein, A.H. (2005). Hormonal response to diets high in soy or animal protein without and with isoflavones in moderately hypercholesterolemic subjects. Nutr Cancer. 51, 1-6. https://doi.org/10.1207/s15327914nc5101_1 PMid:15749623
46. Jabbar, M.A., Larrea, J., Shaw, R.A. (1997). Abnormal thyroid function tests in infants with congenital hypothyroidism:the influence of soy-based formula. J Am Coll Nutr. 16, 280-282. https://doi.org/10.1080/07315724.1997.10718686 PMid:9176836
47. Divi, R.L., Chang, H.C., Doerge, D.R. (1997). Anti-thyroid isoflavones from soybean:isolation, characterization, and mechanisms of action. Biochem Pharmacol. 54, 1087-1096. https://doi.org/10.1016/S0006-2952(97)00301-8
48. Persky, V.W., Turyk, M.E., Wang, L., Freels, S., Chatterton, R.Jr., Barnes, S., Erdman, J.Jr., Sepkovic, D.W., Bradlow, H.L., Potter, S. (2002). Effect of soy protein on endogenous hormones in postmenopausal women. Am J Clin Nutr. 75, 145-153. PMid:11756072
49. Patisaul H., Jefferson W. (2010). The pros and cons of phytoestrogens Front Neuroendocrinol. 31(4):400–419. https://doi.org/10.1016/j.yfrne.2010.03.003 PMid:20347861 PMCid:PMC3074428
50. Cone R., Low M., Elmquist J., Cameron J. D. (2011). Anterior pituitary. In:Larsen PR, Kronenberg HM., Melmed S., Plonsky KS, (Eds.), Williams:Text book of Endocrinology. (pp. 81-176). Philadelphia:WB Saunders Company. PMCid:PMC1308188
51. Melmed, S., Kleinberg. (2011). Anterior pituitary. In:Larsen PR, Kronenberg HM., Melmed S., Plonsky KS, (Eds.), Williams:Text book of Endocrinology. (pp. 175-279). Philadelphia:WB Saunders Company.
52. Muller, E.E., Locatelli, V., Cocchi, D. (1999) Neuroendocrine control of growth hormone secretion. Physiol Rev. 79, 511-607. PMid:10221989
53. Whitnall, M.H. (1993). Regulation of the hypothalamic corticotropin-releasing hormone neurosecretory system. Progr Neurobiol. 40, 573–629.
https://doi.org/10.1016/0301-0082(93)90035-Q
54. Brooks, A. N. (1998). Natural and anthropogenic environmental oestrogens:the scientific basis for risk assessment. Comparative physiology of the reproductive endocrine system in laboratory rodents and humans. Pure Appl Chem. 70, 1633-1646. https://doi.org/10.1351/pac199870091633
55. Horvath, E., Kovacs, K. (1988). Fine structural cytology of the adenohypophysis in rat and man. J Electron Microsc Tech. 8, 401-432. https://doi.org/10.1002/jemt.1060080410 PMid:3058887
56. Dada, M.O., Campbell, G.T., Blake, C.A. (1984). Pars distalis cell quantification in normal adult male and female rats. J Endocrinol. 101, 87-94 https://doi.org/10.1677/joe.0.1010087
57. Milošević, V., Brkić, B., Velkovski, S.D., Sekulić, M., Lovren, M., Starčević, V., Severs W.B. (1998). Morphometric and functional changes of rat pituitary somatotropes and lactotropes after central administration of somatostatin. Pharmacology 57, 28–34. https://doi.org/10.1159/000028223 PMid:9670210
58. Milošević, V., Ajdžanović, V. (2014). Pituitary hormone-producing cells after estradiol application in rat models of menopause. Serbian Journal of Experimental and Clinical Research 15, 115-120. https://doi.org/10.5937/sjecr1403115M
59. Milosević, V., Sekulić, M., Brkić, B., Lovren, M., Starcević, V. (2000). Effect of centrally administered somatostatin on pituitary thyrotropes in male rats. Histochem J. 32, 565-569. https://doi.org/10.1023/A:1004158412915 PMid:11127978
60. Vankelecom, H. (2007). Non-hormonal cell types in the pituitary candidating for stem cell. Semin Cell Dev Biol. 18, 559-570. https://doi.org/10.1016/j.semcdb.2007.04.006 PMid:17509912
61. Vankelecom, H., Gremeaux, L. (2010). Stem cells in the pituitary gland:A burgeoning field. Gen Comp Endocrinol. 166, 478-488. https://doi.org/10.1016/j.ygcen.2009.11.007 PMid:19917287
62. Hauspie, A., Seuntjens, E.,Vankelecom, H., Denef, C. (2003). Stimulation of combinatorial expression of prolactin and glycoprotein hormone alpha-subunit genes by gonadotropin-releasing hormone and estradiol-17beta in single rat pituitary cells during aggregate cell culture. Endocrinology 144, 388-399. https://doi.org/10.1210/en.2002-220606 PMid:12488367
63. Mignot, M., Skinner, D.C. (2005). Colocalization of GH, TSH and prolactin, but not ACTH, with beta LH-immunoreactivity:evidence for pluripotential cells in the ovine pituitary. Cell Tissue Res. 319, 413-421. https://doi.org/10.1007/s00441-004-1009-0 PMid:15647919
64. Mitchner, N.A., Garlick, C., Ben-Jonathan, N. (1998). Cellular distribution and gene regulation of estrogen receptors alpha and beta in the rat pituitary gland. Endocrinology 139, 3976-3983. https://doi.org/10.1210/endo.139.9.6181 PMid:9724053
65. Yin, P., Kawashima, K., Arita, J. (2002). Direct actions of estradiol on the anterior pituitary gland are required for hypothalamus-dependent lactotrope proliferation and secretory surges of luteinizing hormone but not of prolactin in female rats. Neuroendocrinology 75, 392-401. https://doi.org/10.1159/000059436 PMid:12065892
66. Milošević, V., StarčevićV., Šošić-Jurjević, B., Filipović, B., Trifunović, S., Ristić, N., Nestorović, N., Manojlović, M., Sekulić, M. (2007). Effect of estradiol or calcium treatment on mammotrophs of female middle-aged rats. Acta Vet. 57, 393-402. https://doi.org/10.2298/AVB0706393M
67. Trifunović, S., Manojlović-Stojanoski, M., Ajdzanović, V., Nestorović, N., Ristić, N., Medigović, I., MiloševićV. (2012). Genistein stimulates the hypothalamo-pituitary-adrenal axis in adult rats:morphological and hormonal study. Histol Histopathol. 27, 627-640. PMid:22419027
68. Trifunović, S., Manojlović-Stojanoski, M., Ajdžanović, V., Nestorović, N., Ristić, N., Medigović, I., Milošević, V. (2014). Effects of genistein on stereological and hormonal characteristics of the pituitary somatotrophs in rats. Endocrine 47, 869-877. https://doi.org/10.1007/s12020-014-0265-3 PMid:24752394
69. Sekulić, M., Lovren, M., Milosević, V. (1998). Immunoreactive TSH cells in the pituitary of female middle-aged rats after treatment with estradiol or calcium. Acta Histochem. 100, 185-191 https://doi.org/10.1016/S0065-1281(98)80026-3
70. von Bartheld CS1, Wouters FS, Quantitative techniques for imaging cells and tissues. Cell Tissue Res. 2015 Apr;360(1):1-4. https://doi.org/10.1007/s00441-015-2149-0 PMid:25773453 PMCid:PMC4380763
71. Childs, G.V. (2002). Development of gonadotropes may involve cyclic transdifferentiation of growth hormone cells. Arch Physiol Biochem. 110, 42–49. https://doi.org/10.1076/apab.110.1.42.906 PMid:11935399
72. TrifunovićS., Manojlović-Stojanoski M., RistićN., NestorovićN., MedigovićI., ŽivanovićJ., MiloševićV. (2016). Changes of growth hormone-releasing hormone and somatostatin neurons in the rat hypothalamus induced by genistein:a stereological study. Nutr Neurosci. 19(10):467-474. https://doi.org/10.1179/1476830514Y.0000000143
73. Shimizu, T., Kamegai, J., Tamura, H., Ishii, S., Sugihara, H., Oikawa, S. (2005). The estrogen receptor (ER) alpha, but not ER beta, gene is expressed in hypothalamic growth hormone-releasing hormone neurons of the adult female rat. Neurosci Res. 52, 121-125. https://doi.org/10.1016/j.neures.2005.02.002 PMid:15811559
74. Misztal, T., Wańkowska, M., Górski, K., Romanowicz, K. (2007). Central estrogen-like effect of genistein on growth hormone secretion in the ewe. Acta Neurobiol Exp (Wars). 67, 411-419.
75. Ajdžanović, V., Medigović, I., Živanović, J., Šošić-JurjevićB., Trifunović, S., Tanić, N., Miločević,V. (2014). Immunohistomorphometric and fluorescent characteristics of GH cells after treatment with genistein or daidzein in an animal model of andropause. Acta Vet. 64, 93-104. https://doi.org/10.2478/acve-2014-0010
76. Romanowicz, K., Misztal, T., Barcikowski, B. (2004). Genistein, a phytoestrogen, effectively modulates luteinizing hormone and prolactin secretion in ovariectomized ewes during seasonal anestrus. Neuroendocrinology 79, 73-81. https://doi.org/10.1159/000076630 PMid:15004429
77. Gonzalez, M., Reyes, R., Damas, C., Alonso, R., Bello, AR. (2008). Estrogen receptor alpha and beta in female rat pituitary cells, an immunochemical study. Gen Comp Endocrinol. 155, 857–868. https://doi.org/10.1016/j.ygcen.2007.10.007 PMid:18067893
78. Asnacios, A., Hamant, O. (2012). The mechanics behind cell polarity. Trends Cell Biol. 22, 584–591. https://doi.org/10.1016/j.tcb.2012.08.005 PMid:22980034
79. Medigović, I., Ristić, N., Trifunović, S., Manojlović-Stojanoski, M., Milošević, V., Zikić, D., Nestorović, N. (2012). Genistein affects ovarian folliculogenesis:a stereological study. Microsc Res Tech. 75, 1691-1699. https://doi.org/10.1002/jemt.22117 PMid:22927040
80. Ohno, S., Nakajima, Y., Inoue, K., Nakazawa, H., Nakajin, S. (2003). Genistein administration decreases serum corticosterone and testosteronelevels in rats. Life Sci. 74, 733–742. https://doi.org/10.1016/j.lfs.2003.04.006 PMid:14654166
81. Wójcik-Gładysz, A., Romanowicz, K., Misztal, T., Polkowska, J., Barcikowski,B. (2005). Effects of intracerebroventricular infusion ofgenistein on the secretory activity of the GnRH/LH axis in ovariectomized ewes. Anim Reprod Sci. 86, 221–235. https://doi.org/10.1016/j.anireprosci.2004.08.004 PMid:15766802
82. Polkowska, J., Ridderstråle, Y., Wankowska, M., Romanowicz, K., Misztal, T., Madej, A. (2004). Effects of intracerebroventricular infusion of genistein on gonadotrophin subunit mRNA and immunoreactivity of gonadotrophins and oestrogen receptor-alpha in the pituitary cells of the anoestrous ewe. J Chem Neuroanat. 28, 217–224.
https://doi.org/10.1016/j.jchemneu.2004.07.004 PMid:15531133
83. Bliedtner, A., Zierau, O., Albrecht, S., Liebhaber, S., Vollmer, G. (2010). Effects of genistein and estrogen receptor subtype-specific agonists in ArKO mice following different administration routes. Mol Cell Endocrinol. 314, 41–52. https://doi.org/10.1016/j.mce.2009.07.032 PMid:19686804
84. Childs, G.V., Ellison, D.G., Ramaley, J.A. (1982). Storage of anteriorlobe adrenocorticotropin in corticotropes and a subpopulation of gonadotropes during the stress-nonresponsive period in the neonatal male rat. Endocrinology 110, 1676-1692. https://doi.org/10.1210/endo-110-5-1676 PMid:6280971
85. Milošević, V., Ajdžanović, V., Sošic-Jurjevic, B., Filipovic, B., Brkic, M., Nestorovic, N., Sekulic, M. (2009). Morphofunctional characteristics of ACTH cells in middle-aged male rats after treatment with genistein. Gen Physiol Biophys 28, 94-97. https://doi.org/10.4149/gpb_2009_01_94 PMid:19390142
86. Zhang, Q.H., Hu, Y.Z., Zhou, S.S., Wang F.Z. (2001). Inhibitory effect,of,genistein on the proliferation of the anterior pituitary cells of rats. Sheng Li Xue Bao 53, 51-54. PMid:11354798
87. Hauger, R.L., Thrivikraman, K.V. Plotsky, P.M. (1994). Age-related alterations of hypothalamic-pituitary-adrenal axis function in male Fischer 344 rats. Endocrinology 134, 1528-1536. https://doi.org/10.1210/endo.134.3.8119195 PMid:8119195
88. Šošić-Jurjević, B., Filipović, B., Ajdžanović, V., Savin, S., Nestorović, N., Milošević, V., Sekulić, M. (2010). Suppressive effects of genistein and daidzein on pituitary-thyroid axis in orchidectomized middle-aged rats. Exp Biol Med (Maywood). 235, 590-598. https://doi.org/10.1258/ebm.2009.009279 PMid:20463299
89. Modaresi, M., Khorrami, H., Asadi-Samani, M. (2014). The effect of feeding with soybean on serum levels of TSH, T3 and T4 in male mice. J Herb Med Pharmacol. 3, 93-96.


Copyright

©2017 Trifunović S. This is an open-access article published under the terms of the Creative Commons Attribution License which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Acknowledgement

This research was supported by grants from the Ministry of Education and Science of the Republic of Serbia (No.173009).

Conflict of Interest Statement

The authors declared that they have no potential conflict of interest with respect to the authorship and/or publication of this article.

Citation Information

Macedonian Veterinary Review. Volume 41, Issue 1, Pages 5-19, p-ISSN 1409-7621, e-ISSN 1857-7415, DOI: 10.1515/macvetrev-2017-0027, 2018