미성숙한 암컷 흰쥐 시상하부의 신경회로에 미치는 Genistein의 직접 작용 : 에스트로겐 수용체 베타아형 경로?

Direct Action of Genistein on the Hypothalamic Neuronal Circuits in Prepubertal Female Rats : Estrogen Receptor Beta($ER{\beta}$) Pathway?

  • 허현진 (상명대학교 그린생명과학과) ;
  • 이성호 (상명대학교 그린생명과학과)
  • Heo, Hyun-Jin (Dept. of Green Life Science, Sangmyung University) ;
  • Lee, Sung-Ho (Dept. of Green Life Science, Sangmyung University)
  • 투고 : 2011.04.29
  • 심사 : 2011.06.16
  • 발행 : 2011.06.30

초록

콩이나 적포도주의 식물성 에스트로겐(phytoestrogen)은 건강에 부정적이기보다는 긍정적인 효과를 갖는 것으로 알려져 있는데, 특히 콩류 섭취는 유방암이나 골다공증, 그리고 심혈관계 질환 예방과 높은 상관관계가 있는 것으로 보인다. 그러나 콩류, 특히 그 주성분인 genistein(GS)이 상기한 긍정적인 효과 외에도 여성의 생식계에 잠재적으로 부정적인 영향을 미칠 가능성에 대한 의문이 계속되어왔다. 선행 연구에서 본 연구자들은 사춘기 전에 genistein(GS)을 경구 투여했을 때 암컷 흰쥐의 생식계가 활성화되어 사춘기 개시가 조기에 유도되고, 암컷 성체에 GS를 뇌실내로 미세주입했을 때 kisspeptin-GnRH 뉴런회로 활성화가 일어남을 관찰하였다. 본 연구에서는 사춘기 전 암컷 흰쥐에서의 시상하부 특이적인 GS 투여 효과와 이에 관여하는 에스트로겐 수용체 아형($ER{\alpha}$$ER{\beta}$)을 조사하였다. 사춘기 전암컷 흰쥐(SD strain, PND 30)를 마취시킨 후 GS(3.4 ${\mu}g$/animal)를 1회 뇌실내로 미세 주입하고, 2시간 후 희생시켰다. 시상하부내 생식조절 유전자 발현을 조사하기 위해, RNA를 추출한 후 semi-quantitative reverse transcription polymerasechain reaction(RT-PCR)을 시행하였다. GS 투여는 KiSS-1 유전자 발현의 상위조절자인 mTOR(1:$0.361{\pm}0.058$ AU, p<0.001)발현을 유의하게 감소시켰고, GnRH 분비의 상위조절자인 GAD67(1:$1.285{\pm}0.099$ AU, p<0.05) 발현을 유의하게 증가시켰다. GS 투여는 KiSS-1(1:$1.458{\pm}0.078$ AU, p<0.001) mRNA 수준을 유의하게 증가시켰지만, kisspeptin 수용체인 GPR-54(1:$1.29{\pm}0.08$ AU) mRNA 수준은 변화가 없었고, GnRH(1:$0.379{\pm}0.196$ AU, p<0.05)의 경우는 유의하게 감소시켰다. GS투여군에서 $ER{\alpha}$(1:$1.180{\pm}0.390$ AU) 발현은 대조군 대비 차이가 없었지만, $ER{\beta}$(1:$4.209{\pm}0.796$ AU, p<0.01) 발현은 유의하게 증가했다. 본 연구결과는 사춘기 전 암컷 흰쥐에서 GS의 단기 노출이 시상하부의 GnRH 조절시스템을 직접 변화시킴을 보여준 것으로, 이러한 GS의 시상하부 특이적 효과에 $ER{\beta}$ 경로가 관여함을 강력히 시사한다. 이는 잘 알려진 $ER{\beta}$ 경로를 매개로 하는 GS의 유방암 억제 효과와 일치한다.

Some phytoestrogens in soy and red wine, for example, might have beneficiary rather than adverse effects. In particular, dietary soy intake seems to be highly correlated with protection of breast cancer, osteoporosis and cardiovascular disorders. However, questions persist on the potential adverse effects of the main soy constituent genistein (GS) on female reproductive physiology. Previously we found that prepubertal exposure to GS could activate the reproductive system of immature female rats leading to precocious puberty onset, and intracerebroventricularly (ICV) injected GS could directly activate hypothalamic kisspeptin-GnRH neuronal circuits in adult female rats. The present study was performed to examine the hypothalamus-specific GS effects in prepubertal female rats and which subtype of estrogen receptor is mediated in this GS effect. Prepubertal female rats (PND 30) were anaesthetized, treated with single dose of GS (3.4 ${\mu}g$/animal), and sacrificed at 2 hrs post-injection. To determine the transcriptional changes of reproductive hormone-related genes in hypothalamus, total RNAs were extracted and applied to the semi-quantitative reverse transcription polymerase chain reaction (RT-PCR). ICV infusion of GS significantly lowered the transcriptional activities of mTOR (1:$0.361{\pm}0.058$ AU, p<0.001) but increased that of GAD67 (1:$1.285{\pm}0.099$ AU, p<0.05), which are known to act as an upstream modulator of kisspeptin and GnRH neuronal activities in the hypothalamus, respectively. GS administration enhanced significantly the mRNA levels of KiSS-1(1:$1.458{\pm}0.078$ AU, p<0.001), and exerted no effect on the mRNA level of kisspeptin receptor GPR-54 (1:$1.29{\pm}0.08$ AU). GnRH gene expression was significantly decreased in GS-treated group compared to control group (1:$0.379{\pm}0.196$ AU, p<0.05). There was no difference in the mRNA level of $ER{\alpha}$ in the GS-treated group compare to control group (1:$1.180{\pm}0.390$ AU, Fig. 3A). However, icv infusion of GS significantly increased the transcriptional activities of $ER{\beta}$ (1:$4.209{\pm}0.796$ AU, p<0.01, Fig. 3B). Taken together, the present study indicated that the acute exposure to GS could directly alter the hypothalamic GnRH modulating system in prepubertal female rats. Our study strongly suggested the involvement of $ER{\beta}$ pathway in GS's hypothalamus-specific action, and this idea is consistent with the GS's well-known $ER{\beta}$-mediated protective action in breast cancer.

키워드

참고문헌

  1. Bateman HL, Patisaul HB (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. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidium thiocyanate-phenolchloroform extraction. Anal Biochem 162:156-159.
  3. Chrzan BG, Bradford PG (2007) Phytoestrogens activate estrogen receptor beta1 and estrogenic responses in human breast and bone cancer cell lines. Mol Nutr Food Res 51:171-177. https://doi.org/10.1002/mnfr.200600091
  4. Fitzpatrick LA (2003) Soy isoflavones: hope or hype? Maturitas 44(supp l1):S21-S29. https://doi.org/10.1016/S0378-5122(02)00345-6
  5. Gingerich S, Krukoff TL (2005) Estrogen modulates endothelial and neuronal nitric oxide synthase expression via an estrogen receptor beta-dependent mechanism in hypothalamic slice cultures. Endocrinology 146:2933-2941. https://doi.org/10.1210/en.2004-1375
  6. Goldwyn S, Lazinsky A, Wei H (2000) Promotion of health by soy isoflavones: efficacy, benefit and safety concerns. Drug Metabol Drug Interact 17:261-289.
  7. Hoyer PB (2001) Reproductive toxicology: current and future directions. Biochem Pharmacol 62:1557-1564. https://doi.org/10.1016/S0006-2952(01)00814-0
  8. Jefferson WN, Padilla-Banks E, Newbold RR (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
  9. Johnson MS, Wolbers WB, Noble J, Fennell M, Mitchell R (1995) Effect of tyrosine kinase inhibitors on luteinizing hormone-releasing hormone (LHRH)-induced gonadotropin release from the anterior pituitary. Mol Cell Endocrinol 109:69-75. https://doi.org/10.1016/0303-7207(95)03484-O
  10. Kasuya E, Nyberg CL, Mogi K, Terasawa E (1999) A role of gamma-amino butyric acid (GABA) and glutamate in control of puberty in female rhesus monkeys: effect of an antisense oligodeoxynucleotide for GAD67 messenger ribonucleic acid and MK801 on luteinizing hormonereleasing hormone release. Endocrinology 140:705-712. https://doi.org/10.1210/en.140.2.705
  11. Kouki T, Kishitake M, Okamoto M, Oosuka I, Takebe M, Yamanouchi K (2003) Effects of neonatal treatment with phytoestrogens, genistein and daidzein, on sex difference in female rat brain function: estrous cycle and lordosis. Horm Behav 44:140-145. https://doi.org/10.1016/S0018-506X(03)00122-3
  12. Lamartiniere CA, Zhang JX, Cotroneo MS (1998) Genistein studies in rats: potential for breast cancer prevention and reproductive and developmental toxicity. Am J Clin Nutr 68(suppl):1400S-1405S. https://doi.org/10.1093/ajcn/68.6.1400S
  13. Lee K-Y, Lee S-H (2006a) Effect of genistein on the onset of puberty in female rats. Dev Reprod 10:55-61.
  14. Lee K-Y, Lee S-H (2006b) Effects of endocrine disruptors on the expression of estrogen receptors in ovary and uterus from immature rats. Dev Reprod 10:255-261.
  15. Lee W, Lee S-H (2010) Direct action of genistein on the hypothalamic neuronal circuits in female rats. Dev Reprod 14:35-41.
  16. Levy JR, Faber KA, Ayyash L, Hughes CL Jr (1995) The effect of prenatal exposure to the phytoestrogen genistein on sexual differentiation in rats. Proc Soc Exp Biol Med 208:60-66. https://doi.org/10.3181/00379727-208-43832
  17. Lyons G (2006) Viewpoint: Policy requirements for protecting wildlife from endocrine disruptors. Environ Health Perspect 114 Suppl 1:142-146. https://doi.org/10.1289/ehp.8070
  18. McCarty MF (2006) Isoflavones made simple - genistein's agonist activity for the beta-type estrogen receptor mediates their health benefits. Med Hypotheses 66:1093-1114. https://doi.org/10.1016/j.mehy.2004.11.046
  19. Messina M, Nagata C, Wu AH (2006) Estimated Asian adult soy protein and isoflavone intakes. Nutr Cancer 55:1-12. https://doi.org/10.1207/s15327914nc5501_1
  20. Misztal T, Gorski K, Romanowicz K (2008) Differential endocrine response in rams to intracerebroventricular infusion of genistein. Acta Neurobiol Exp (Wars) 68:43-50.
  21. Polkowska J, Ridderstråle Y, Wańkowska 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
  22. Roa J, Garcia-Galiano D, Varela L, Sanchez-Garrido MA, Pineda R, Castellano JM, Ruiz-Pino F, Romero M, Aguilar E, Lopez M, Gaytan F, Dieguez C, Pinilla L, Tena-Sempere M (2009) The mammalian target of rapamycin as novel central regulator of puberty onset via modulation of hypothalamic Kiss1 system. Endocrinology 150:5016-5026. https://doi.org/10.1210/en.2009-0096
  23. Takagi H, Shibutani M, Lee KY, Lee HC, Nishihara M, Uneyama C, Takigami S, Mitsumori K, Hirose M (2004) Lack of modifying effects of genistein on disruption of the reproductive system by perinatal dietary exposure to ethinylestradiol in rats. Reprod Toxicol 18:687-700. https://doi.org/10.1016/j.reprotox.2004.03.002
  24. Whitsett TG, Lamartiniere CA (2006) Genistein and resveratrol: mammary cancer chemoprevention and mechanisms of action in the rat. Expert Rev Anticancer Ther 6:1699-1706. https://doi.org/10.1586/14737140.6.12.1699
  25. Wojcik-Gładysz A, Romanowicz K, Misztal T, Polkowska J, Barcikowski B (2005) Effects of intracerebroventricular infusion of genistein 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
  26. Wozniak AL, Bulayeva NN, Watson CS (2005) Xenoestrogens at picomolar to nanomolar concentrations trigger membrane estrogen receptor-alpha-mediated Ca2+ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environ Health Perspect 113:431-439. https://doi.org/10.1289/ehp.7505