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• Research Paper Volume 11, Issue 12 pp 4032-4049

  Long-time qingyan formula extract treatment exerts estrogenic activities on reproductive tissues without side effects in ovariectomized rats and via active ER to ERE-independent gene regulation

  Relevance score: 14.118582

  Hong-Xia Zheng, Yuan Zhao, Ying Xu, Zi-Jia Zhang, Jing-jing Zhu, Yuan-Fang Fan, Na Lin

  Keywords: reproductive target tissue, estrogenic effect, estrogen receptors, estrogen receptor antagonist ICI182,780

  Published in Aging on June 19, 2019

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  The reproductive tissues are negatively influenced by estrogens in hormone therapy. Qingyan formula ethanol extract (QYFE)’s estrogenic effects and safety on reproductive tissues after long-term administration and its mechanism via estrogen receptor (ER) pathway haven’t been studied. Here, we characterized its estrogenic effects using ovariectomized rats together with in vitro studies for further molecular characterization. Ovariectomized rats were treated with QYFE at doses of 0.7, 1.4, and 2.8g/kg for 12 weeks. The results showed QYFE has a potent estrogenic activity, as indicated by restoring the disappeared estrous cycle, antagonizing the atrophy of uterus, vagina and mammary gland, and the estrogen decline in circulation caused by ovariectomy. In addition, QYFE upregulated ERα and ERβ expressions and had a less stimulatory effect on PCNA and ki-67 antigen in reproductive tissues compared with estradiol valerate. QYFE components can bind to ERα and ERβ, significantly increased ERα/β-ERE luciferase reporter gene expression, upregulated the expressions of ERs, PR and pS2 in MCF-7 cells at protein and gene level. All these activities were significantly inhibited by the ER antagonist ICI182,780. QYFE’s estrogenic activity maybe mediated by stimulating biosynthesis of estrogen and increasing the quantity of ERs in target tissue and via active ER to ERE-independent gene regulation.

  

  The effect of QYFE on the estrous cycle in ovariectomized (OVX) rats. EV refers to estradiol valerate, QYFE to Qing Yan Formula 70% ethanol extract. Representative photomicrographs taken at 200-X magnification. (I) OVX rats untreated; (II) Shan; (III) OVX rats treated with estradiol valerate (EV); (IV) OVX rats treated with 2.8g/kg QYFE.

  
  
  

  

  The effects of QYFE on index of uterine and adrenal gland, and sex hormone in circulation. The uterus index (A), adrenal gland index (B), serum levels of estradiol (E₂) (C), luteinzing hormone (LH) (D) and follicle-stimulating hormone (FSH) (E) for OVX rats were measured at the end of the 12-week treatment period. Data are the mean and standard deviation (SD) of samples from 10 rats. P values are for the one-way analysis of variance (ANOVA). ^***p < 0.001, compared with the sham group; #p < 0.05, ##p < 0.01, ###p < 0.001, compared with the OVX group.

  
  
  

  

  The effects of QYFE treatment on the histology of uterus, vagina and mammary gland in the OVX rats. Representative photomicrographs taken at 200-X magnification of uterine, 400-X magnification of vaginal and mammary gland sections in ovariectomized (OVX) rats. (A–C) are the histology of the uterus, vagina and mammary gland, respectively in OVX rats. The treatment groups in OVX rats are shown: (I) Untreated ovariectomized (OVX) rat; (II) sham-operated rat; (III) OVX rat treated with estradiol valerate (EV); and OVX rat treated with (IV) 0.7 g/kg, (V) 1.4 g/kg, and (VI) 2.8 g/kg QYFE.

  
  
  

  

  The effects of QYFE treatment on the expression of estrogen receptor (ER) α and estrogen receptor (ER) β in the uterus, vagina and mammary gland. (A) ERα and ERβ expression was assessed by quantitative immunohistochemistry. Representative photomicrographs taken at 200-X magnification of uterus and 400-X magnification of vagina and mammary gland sections from each treatment group are shown: (I) Untreated ovariectomized (OVX) rat; (II) sham-operated rat; (III) OVX rat treated with estradiol valerate (EV); and OVX rat treated with (IV) 0.7 g/kg, (V) 1.4 g/kg, and (VI) 2.8 g/kg QYFE. Data are the mean standard deviation (SD) of samples from 10 rats. ^*** p< 0.001, compared with the sham-operated group; ###p < 0.001, ##p < 0.01, and #p < 0.05, compared with the OVX group. (B) Comparative Statistical analysis of ERα and ERβ upregulation to OVX group (▲) p< 0.05, compared with ERα protein relative increase of QEFE to untreated OVX.

  
  
  

  

  The effects of QYFE on expression of PCNA or Ki67 in the uterus, vagina and mammary gland in OVX rats. PCNA and Ki67 expression was assessed by quantitative immunohistochemistry. Representative photomicrographs taken at 200-X magnification of uterus (A) and 400-X magnification of vagina (B) and mammary gland (C) sections from each treatment group are shown: (I) Untreated ovariectomized (OVX) rat; (II) sham-operated rat; (III) OVX rat treated with estradiol valerate (EV); and OVX rat treated with (IV) 0.7 g/kg, (V) 1.4 g/kg, and (VI) 2.8 g/kg QYFE. Data are the mean standard deviation (SD) of samples from 10 rats. ^**P<0.01, ^***P<0.001, compared with sham; #p<0.05, ##p<0.01, ###p<0.001, compared with OVX group;△p<0.05, △△p<0.01, △△△p<0.001, compared with EV group

  
  
  

  

  The effects of QYFE on the expression of estrogen receptor (ER) α and estrogen receptor (ER) β at protein levels in uterus, vagina, and mammary gland of rats. (A) Western blot analysis was carried out as described in Materials and Methods. Representative blots are shown above, and quantitative analysis is shown below. Values given are the mean standard deviation (SD) of three independent experiments. ^*** p < 0.001, and ^** p < 0.01, compared with sham-operated; ###p<0.001, ##p< 0.01 and #p< 0.05, compared with the ovariectomized (OVX) group; (▲) p< 0.05, compared with ERα protein relative increase to Control. (B) Comparative Statistical analysis of ERα and ERβ upregulation to OVX group. (▲) p< 0.05, compared with ERα protein relative increase of QEFE to untreated OVX.

  
  
  

  

  Effect of QYFE on viability of MCF-7 cells and MDA-MB-231 cell. Cell proliferation was carried out as described in the Materials and Methods. Results are expressed relative to the growth of cells treated with 1% dimethylsulfoxide (DMSO). Data are the mean ± standard deviation of quadruplicate analyses, expressed relative to that of treatment with 0.1% DMSO. ^***p < 0.001, ^*p < 0.05 compared to Con; ###p < 0.001, compared to QYFE or 0.01 μM 17β-estradiol (E₂).

  
  
  

  

  Effect of QYFE on ability of ERα and ERβ binding. Each data point represents the mean±standard of triplicate samples.^*p < 0.05,^**p < 0.01,^***p < 0.001 compared to Con.

  
  
  

  

  Effect of QYFE on the protein levels of estrogen receptors (ER) α and ERβ, PR and ps2 in MCF-7 cell. Western blotting analysis was carried out as described in the Methods ^*P<0.05, ^**P<0.01, ^***P<0.001, compared with con; ^#P<0.05, ^##P<0.01, ^###P<0.001, compared with 17β-estradiol (E₂/) QYFE.

  
  
  

  

  Effect of QYFE on the the gene expressions of estrogen receptor (ER) α, ER β, PR and pS2 in MCF-7 cells. Real-time PCR analysis was carried out as described in the Methods.^*P<0.05,^**P<0.01, ^***P<0.001compared to Con; ^#P<0.05, ^##P<0.01, ^###P<0.001 compared to 17β-estradiol (E₂) or QYFE.

  
  
  

  

  Effects of QYFE on the activation of estrogen receptors (ER) α and ERβ in HEK293T cells. The effect of QYFE on estrogen receptors α and β activity in the transiently transfected HEK293T-ERα and HEK293T-ERβ cells was investigated by measuring reporter gene-coupled luciferase activity. ^***P<0.001 compared to Con; ^#P<0.05, ^##P<0.01, ^###P<0.001 compared to 17β- estradiol or QYFE.

  
  
  

• Research Paper Volume 9, Issue 1 pp 156-172

  Salvia miltiorrhiza bunge increases estrogen level without side effects on reproductive tissues in immature/ovariectomized mice

  Relevance score: 11.957275

  Ying Xu, Ting Chen, Xin Li, Ya-kun Qu, Jin-na An, Hong-xia Zheng, Zi-jia Zhang, Na Lin

  Keywords: Salvia miltiorrhiza bunge, reproductive target tissue, estrogenic effect, estrogen receptors, estrogen receptor antagonist ICI182, 780

  Published in Aging on December 20, 2016

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  Salvia miltiorrhiza bunge(SM) is a popular herb for alleviating menopausal symptoms, although the scientific evidence of applying SM to estrogen replacement therapy is limited. In this study, we characterized the estrogenic activity of SM using in vivo models of immature and ovariectomized (OVX) mice and performed in vitro studies focusing on the estrogen receptor (ER) pathway for further molecular characterizations. SM treatments demonstrated significant estrogenic activity by promoting the development of uterus and vagina in immature mice, restoring the estrus cycle and reversing the atrophy of reproductive tissues in OVX mice, as well as increasing the expressions of ERα and ERβ at protein and mRNA level in the reproductive tissues. Meanwhile, SM significantly increased estradiol in serum, and decreased follicle-stimulating hormone (FSH) and luteinizing hormone (LH) in the circulation of immature and OVX mice. SM could stimulate the binding effect of ERα and ERβ, and significantly induce ERα/β-estrogen response element (ERE) luciferase reporter gene expression. All these activities were inhibited by the ER antagonist ICI182, 780. This study demonstrates SM exerts estrogenic effects by stimulating biosynthesis of estrogen and increasing ERs in target tissues without side effects on reproductive tissues and through ER-ERE-dependent pathway.

  

  The effect of Salvia miltiorrhiza bunge (SM) on the estrous cycle. ICI refers to the estrogen antagonist ICI182, 780 and E₂ to 17β -estradiol. (A) The estrous cycle of the Immature mice, (i) the control group with untreated; (ii) Treated with estradiol (E₂) ; (iii) Treated with Salvia miltiorrhiza bunge (SM) and (iV) Treated with Salvia miltiorrhiza bunge (SM) with estrogen receptor antagonist (ICI182, 780). (B) The estrous cycle of the OVX mice, (i) Ovariectomized (OVX) mice untreated; (ii) Sham group with untreated; (iii) Treated with Salvia miltiorrhiza bunge (SM) and (iV) Treated with Salvia miltiorrhiza bunge (SM) with estrogen receptor antagonist (ICI182, 780).

  
  
  

  

  The effects of SM on uterine, body weights and adrenal gland. (A) The uterine weights of immature mice were measured at the end of the 7-day treatment period. (B) The uterus index for ovariectomized (OVX) mice was measured at the end of the 4-week treatment period. (C) Body weights of OVX mice were measured once per week for 4 weeks. (D) The adrenal gland index of ovariectomized (OVX) mice was measured at the end of the 4-week treatment period. Data are the mean and standard deviation (SD) of samples from 10 mice. P values are for the one-way analysis of variance (ANOVA) comparing the treatment group with untreated mice. (A) ***P < 0.001, **P < 0.01 and *P < 0.05 compared with the Con group; ^###P < 0.001 compared with the SM group or E₂ group; (B, C, D) ***P < 0.001 and *P < 0.05 compared with the Sham group; ^###P < 0.001 and ^#P < 0.05 compared with the OVX group;^∆∆∆P < 0.001, ^∆∆P < 0.01, and ^∆P < 0.05 compared with the SM group or E₂ group.

  
  
  

  

  The effects of SM on serum estradiol (E₂), luteinizing hormone (LH) and follicle-stimulating hormone (FSH) in immature and ovariectomized (OVX) mice. (A) Serum levels of E₂, LH and FSH from immature mice and (B) serum levels of E₂, LH and FSH from ovariectomized (OVX) mice were measured at the end of the treatment period. Data are the mean and standard deviation (SD) of samples from 10 mice. P values are for the one-way analysis of variance (ANOVA) comparing treatment groups with untreated mice. (A) ***P < 0.001, **P < 0.01 and *P < 0.05 compared with the Con group; ^###P < 0.001; ^##P < 0.01 and ^#P < 0.05 compared with the SM group or E₂ group; (B) ***P < 0.001; **P < 0.01 and *P < 0.05 compared with the Sham group; ^###P < 0.001 and ^##P < 0.01 compared with the OVX group;^∆∆∆P < 0.001, ^∆∆P < 0.01, and ^∆P < 0.05 compared with the SM group or E₂ group.

  
  
  

  

  The effects of SM on the histology of the uterus and vagina in immature and ovariectomized (OVX) mice. Representative photomicrographs taken at 200-X magnifiation of uterine in immature mice; 100-X magnifiation of uterine in ovariectomized (OVX) mice and 400-X magnifiation of vaginal sections. (A, B) are the histology of the uterus and vagina in immature mice. (C, D) are the histology of the uterus and vagina in ovariectomized (OVX) mice. The treatment groups in immature mice are shown: (i) control group; (ii) treated with E₂; (iii) treated with E₂ and ICI; (iv) treated with SM at 1.6 g/kg; (v) treated with SM at 1.6 g/kg and ICI, (vi) treated with SM at 3.2 g/kg; (vii) treated with SM at 3.2 g/kg and ICI. The treatment groups in OVX mice are shown: (i) sham-operated mice; (ii) untreated OVX mice; (iii) treated with E₂; (iv) treated with E₂ and ICI, (v) treated with SM at 1.6 g/kg; (vi) treated with SM at 1.6 g/kg and ICI; (vii) treated with SM at 3.2 g/kg; (viii) treated with SM at 3.2 g/kg and ICI.

  
  
  

  

  The effects of SM on the expressions of estrogen receptor ERα and β in the uterus and vagina. ERs expressions were assessed by immunohistochemistry. Representative photomicrographs taken at 200-X magnifiation of uterine in immature mice; 100-X magnifiation of uterine in ovariectomized (OVX) mice and 400-X magnifiation of vaginal sections. (A) show expression of ERs in immature mice. Treatment groups are shown: (i) control group; (ii) treated with E₂; (iii) treated with E₂ and ICI; (iv) treated with SM at 1.6 g/kg; (v) treated with SM at 1.6 g/kg and ICI, (vi) treated with SM at 3.2 g/kg; (vii) treated with SM at 3.2 g/kg and ICI. (B) show the expression of ERs in the ovariectomized (OVX) mice. Treatment groups are shown: (i) sham-operated mice; (ii) untreated OVX mice; (iii) treated with E₂; (iv) treated with E₂ and ICI, (v) treated with SM at 1.6 g/kg; (vi) treated with SM at 1.6 g/kg and ICI; (vii) treated with SM at 3.2 g/kg; (viii) treated with SM at 3.2 g/kg and ICI. Data are the mean and standard deviation from 10 mice. P values are for the one-way analysis of variance comparing the treatment group with untreated mice. (A) ***P < 0.001, **P < 0.01 and *P < 0.05 compared with the Con group; ^###P < 0.001 and ^##P < 0.01compared with the SM group or E₂ group; ^▴▴P < 0.01 and ^▴P < 0.05 compared with the ERα. (B) ***P < 0.001 compared with the Sham group; ^###P < 0.001 and ^##P < 0.05 compared with the OVX group;^∆∆∆P < 0.001 compared with the SM group or E₂ group.

  
  
  

  

  The effects of SM on the protein and gene expression of estrogen receptor ERα and ERβ in the uterus and vagina of mice. Western-blot (A, C) and Realtime PCR (B, D) analysis was carried out as described in the Methods. Representative blots are shown above, and quantitative analyses are shown below. P values are for one-way analysis of variance (ANOVA) comparing treatment groups with untreated mice. (A, B) ***P < 0.001, **P < 0.01 and *P < 0.05 compared with the Con group; ^###P < 0.001 and ^##P < 0.01compared with the SM group or E₂ group; ^▴▴P < 0.01 compared with the ERα. (C, D) ***P < 0.001 compared with the Sham group; ^###P < 0.001, ^##P < 0.01and ^#P < 0.05 compared with the OVX group;^∆∆∆P < 0.001 and ^∆∆P < 0.01compared with the SM group or E₂ group.

  
  
  

  

  Effect of SM on viability of MCF-7 cells. Cell proliferation was carried out as described in the Materials and Methods. Results are expressed relative to the growth of cells treated with 1% dimethylsulfoxide (DMSO). Data are the mean ± standard deviation of quadruplicate analyses, expressed relative to that of treatment with 0.1% DMSO. ***p < 0.001, *p < 0.05 compared to Con; ^###p < 0.001, compared to SM or 0.01 μM E₂.

  
  
  

  

  Effect of SM on ability of ERα binding (A) and ERβ (B). Each data point represents the mean ±standard of triplicate samples. ***p < 0.001 compared to Con.

  
  
  

  

  Activity of SM on estrogen receptor ERα (A) and ERβ (B) -estrogen response element (ERE) luciferases reporter gene expression. Data are the mean ± standard deviation of quadruplicate analyses, expressed relative to that of treatment with 0.1% DMSO. P values are for one-way analysis of variance (ANOVA) comparing treatment groups with untreated mice. ***P < 0.01, **P < 0.01 and *P < 0.05 compared with Con group; ^###p < 0.001, compared to SM or 0.01 μM E₂.