转化生长因子-β参与调控小鼠卵巢原始卵泡库维持与激活的研究
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摘要
正常生理情况下,雌性哺乳动物的每一个动情周期都只有极少数的原始卵泡被募集激活进入到生长卵泡发育阶段,而绝大多数的原始卵泡处于静止状态。然而为什么原始卵泡库每个排卵周期仅仅部分启动仍是未解之谜。虽然近年来的研究表明PTEN/PI3K和TSC/mTROC信号通路协同参与调控原始卵泡库的激活,但是基因敲除的表型并不符合生理状况,因此这一问题有待进一步的研究。本实验主要探讨了生殖细胞分泌的转化生长因子-p(TGF-β)对小鼠原始卵泡库维持与激活的调节机制。
首先,我们发现在小鼠围产期卵巢中,TGF-β1及其受体TGF-βR1表达于出生前卵巢的合胞体生殖细胞,以及出生后的原始卵泡和初级卵泡的生殖细胞。从初级卵泡开始在颗粒细胞也有表达。而蛋白免疫印迹实验表明出生前卵巢TGF-β1及其受体TGF-βR1是低水平表达,在出生后逐渐上升,在4dpp至7dpp期间又显著下降。
体外培养的实验结果表明,TGF-β信号通路的激动剂TGF-β1可以显著抑制原始卵泡的生长,并造成生殖细胞总数量的减少。而抑制剂SD208不影响卵巢中生殖细胞的总数,但是却显著促进原始卵泡的生长,更多的原始卵泡激活进入到生长卵泡发育阶段。而RNA干扰TGF-β信号通路的受体TGF-βR1表达的实验也表明,削弱TGF-β信号通路可以显著促进卵巢中原始卵泡的激活,更多数量的原始卵泡被激活进入到生长卵泡阶段。另外拯救实验也表明,卵巢中存在TGF-β信号通路抑制剂SD208的情况下,如果不断向卵巢中添加不同浓度的TGF-β1蛋白纯品,则可以部分逆转SD208造成的促进原始卵泡激活的现象。
原始卵泡的生长包括了生殖细胞的生长和体细胞的增殖。我们检测了不同处理组卵巢的增殖和凋亡情况。实验结果表明TGF-β1可以显著促进卵巢原始卵泡的凋亡并且抑制卵巢体细胞的增殖,而SD208不影响卵巢生殖细胞的凋亡但是却显著促进卵巢体细胞的增殖。
同时我们也探讨了TGF-β调节原始卵泡启动生长的相关机制。我们利用蛋白免疫印迹实验检测了TGF-β信号通路对PI3K-AKT-FOXO3a信号通路和TSC/mTROC信号通路下游蛋白的磷酸化水平的影响。实验结果表明TGF-P信号通路不影响AKT、FOXO3a的磷酸化变化,但是TGF-β1可以显著下调TSC/mTROC下游的S6K1/rpS6信号通路中的p-S6K1(T389)、 p-rpS6(S235/6)和p-rpS6(S240/4)的磷酸化水平,而SD208显著上调p-S6K1(T389)、 p-rpS6(S235/6)和p-rpS6(S240/4)的磷酸化水平。这些结果提示我们TGF-β信号通路可能通过调节TSC/mTROC信号通路来参与调控小鼠原始卵泡的激活,并且TSC/mTROC信号通路的特异性抑制剂雷帕霉素(Rapamycin)可以部分逆转TGF-β信号通路抑制剂SD208促进原始卵泡生长激活的作用。
综上所述,我们发现TGF-β信号通路可以通过调控TSC/mTROC信号通路从而调控小鼠卵巢原始卵泡库的维持与激活。
Naturally, only a few follicles enter the growing follicle pool from primordial follicles each wave in mammalian ovary. However, why only a few follicles enter the growing follicle pool every time remains unknown. Recent studies using knockout mice model have showed that early follicle oocyte growth depends on signaling from the tuberous sclerosis complex (TSC), the mammalian target of rapamycin complex1(mTORCl), phosphatase and tensin homolog deleted on chromosome10(PTEN), and phosphatidylinositol3kinase (PI3K) pathways. However, whether transforming growth factor beta (TGF-β) has function on them is unknown. This study aims to identify the physiological roles of TGF-P signaling during primordial follicle activation.
First of all, TGF-β1and TGF-P receptor type I (TGF-PR1) expressed in the oocytes of cysts, primordial and primary follicles in18.5days post coitus (dpc),1days post parturition (dpp) and4dpp mouse ovaries and started expressing in the cuboidal granulosa cells of primary follicles. Western blot results revealed that the protein levels of TGF-β1and TGF-βR1sharply decreased between4dpp and7dpp mouse ovaries.
We found that the growth of primordial follicle oocytes in TGF-β1-treated ovaries was inhibited, while the growth of oocytes in SD208(a specific inhibitor of TGF-βR1)-treated ovaries was accelerated with an in vitro ovary culture system. Furthermore, TGF-β1dose-dependently rescued the abnormal primordial follicle activation in SD208-treated ovaries.
To determine the cause of rapid oocyte growth, we found that there was dramatically less proliferation of granulosa cells and more TUNEL-positive oocytes in TGF-β1-treated ovaries and significantly more proliferation in SD208-treated ovaries as shown by5-bromo-2'-deoxyuridine (BrdU) incorporation assays and immunohistochemical staining for proliferating cell nuclear antigen (PCNA) and TUNEL assays.
To investigate the molecular mechanisms underlying the accelerated enlargement of oocytes, we found that the phosphorylation levels of Akt (S473) and FOXO3a (Thr32) in SD208-treated ovaries were similar to control and TGF-β1-treated ovaries. However, the phosphorylation of S6K1at its threonine389(p-S6K1, T389) and the phosphorylation of rpS6at its serine235and236(p-rpS6, S235/6) and at its serine240and244(p-rpS6, S240/4) were elevated in SD208-treated ovaries but reduced in TGF-β1-treated ovaries compared with control ovaries. In other words, TGF-P signaling may regulate primordial follicle growth through activation of p70S6kinase1(S6K1)/ribosomal protein S6(rpS6) signaling in mouse ovaries.
In conclusion, our results suggest that TGF-P signaling plays an important physiological role in the maintenance of the dormant pool of primordial follicles, which functions through activation of S6K1/rpS6signaling in mouse ovaries.
首先,我们发现在小鼠围产期卵巢中,TGF-β1及其受体TGF-βR1表达于出生前卵巢的合胞体生殖细胞,以及出生后的原始卵泡和初级卵泡的生殖细胞。从初级卵泡开始在颗粒细胞也有表达。而蛋白免疫印迹实验表明出生前卵巢TGF-β1及其受体TGF-βR1是低水平表达,在出生后逐渐上升,在4dpp至7dpp期间又显著下降。
体外培养的实验结果表明,TGF-β信号通路的激动剂TGF-β1可以显著抑制原始卵泡的生长,并造成生殖细胞总数量的减少。而抑制剂SD208不影响卵巢中生殖细胞的总数,但是却显著促进原始卵泡的生长,更多的原始卵泡激活进入到生长卵泡发育阶段。而RNA干扰TGF-β信号通路的受体TGF-βR1表达的实验也表明,削弱TGF-β信号通路可以显著促进卵巢中原始卵泡的激活,更多数量的原始卵泡被激活进入到生长卵泡阶段。另外拯救实验也表明,卵巢中存在TGF-β信号通路抑制剂SD208的情况下,如果不断向卵巢中添加不同浓度的TGF-β1蛋白纯品,则可以部分逆转SD208造成的促进原始卵泡激活的现象。
原始卵泡的生长包括了生殖细胞的生长和体细胞的增殖。我们检测了不同处理组卵巢的增殖和凋亡情况。实验结果表明TGF-β1可以显著促进卵巢原始卵泡的凋亡并且抑制卵巢体细胞的增殖,而SD208不影响卵巢生殖细胞的凋亡但是却显著促进卵巢体细胞的增殖。
同时我们也探讨了TGF-β调节原始卵泡启动生长的相关机制。我们利用蛋白免疫印迹实验检测了TGF-β信号通路对PI3K-AKT-FOXO3a信号通路和TSC/mTROC信号通路下游蛋白的磷酸化水平的影响。实验结果表明TGF-P信号通路不影响AKT、FOXO3a的磷酸化变化,但是TGF-β1可以显著下调TSC/mTROC下游的S6K1/rpS6信号通路中的p-S6K1(T389)、 p-rpS6(S235/6)和p-rpS6(S240/4)的磷酸化水平,而SD208显著上调p-S6K1(T389)、 p-rpS6(S235/6)和p-rpS6(S240/4)的磷酸化水平。这些结果提示我们TGF-β信号通路可能通过调节TSC/mTROC信号通路来参与调控小鼠原始卵泡的激活,并且TSC/mTROC信号通路的特异性抑制剂雷帕霉素(Rapamycin)可以部分逆转TGF-β信号通路抑制剂SD208促进原始卵泡生长激活的作用。
综上所述,我们发现TGF-β信号通路可以通过调控TSC/mTROC信号通路从而调控小鼠卵巢原始卵泡库的维持与激活。
Naturally, only a few follicles enter the growing follicle pool from primordial follicles each wave in mammalian ovary. However, why only a few follicles enter the growing follicle pool every time remains unknown. Recent studies using knockout mice model have showed that early follicle oocyte growth depends on signaling from the tuberous sclerosis complex (TSC), the mammalian target of rapamycin complex1(mTORCl), phosphatase and tensin homolog deleted on chromosome10(PTEN), and phosphatidylinositol3kinase (PI3K) pathways. However, whether transforming growth factor beta (TGF-β) has function on them is unknown. This study aims to identify the physiological roles of TGF-P signaling during primordial follicle activation.
First of all, TGF-β1and TGF-P receptor type I (TGF-PR1) expressed in the oocytes of cysts, primordial and primary follicles in18.5days post coitus (dpc),1days post parturition (dpp) and4dpp mouse ovaries and started expressing in the cuboidal granulosa cells of primary follicles. Western blot results revealed that the protein levels of TGF-β1and TGF-βR1sharply decreased between4dpp and7dpp mouse ovaries.
We found that the growth of primordial follicle oocytes in TGF-β1-treated ovaries was inhibited, while the growth of oocytes in SD208(a specific inhibitor of TGF-βR1)-treated ovaries was accelerated with an in vitro ovary culture system. Furthermore, TGF-β1dose-dependently rescued the abnormal primordial follicle activation in SD208-treated ovaries.
To determine the cause of rapid oocyte growth, we found that there was dramatically less proliferation of granulosa cells and more TUNEL-positive oocytes in TGF-β1-treated ovaries and significantly more proliferation in SD208-treated ovaries as shown by5-bromo-2'-deoxyuridine (BrdU) incorporation assays and immunohistochemical staining for proliferating cell nuclear antigen (PCNA) and TUNEL assays.
To investigate the molecular mechanisms underlying the accelerated enlargement of oocytes, we found that the phosphorylation levels of Akt (S473) and FOXO3a (Thr32) in SD208-treated ovaries were similar to control and TGF-β1-treated ovaries. However, the phosphorylation of S6K1at its threonine389(p-S6K1, T389) and the phosphorylation of rpS6at its serine235and236(p-rpS6, S235/6) and at its serine240and244(p-rpS6, S240/4) were elevated in SD208-treated ovaries but reduced in TGF-β1-treated ovaries compared with control ovaries. In other words, TGF-P signaling may regulate primordial follicle growth through activation of p70S6kinase1(S6K1)/ribosomal protein S6(rpS6) signaling in mouse ovaries.
In conclusion, our results suggest that TGF-P signaling plays an important physiological role in the maintenance of the dormant pool of primordial follicles, which functions through activation of S6K1/rpS6signaling in mouse ovaries.
引文
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