Circadian gene PER1 senses progesterone signal during human endometrial decidualization

in Journal of Endocrinology
Authors:
Ying Zhang Department of Obstetrics and Gynecology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei, China
Hubei Clinical Research Center for Prenatal Diagnosis and Birth Health, Wuhan, Hubei, China
Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Nan Meng Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Haili Bao Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Yufei Jiang Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Ningjie Yang Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Kejia Wu Department of Obstetrics and Gynecology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei, China
Hubei Clinical Research Center for Prenatal Diagnosis and Birth Health, Wuhan, Hubei, China

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Jinxiang Wu Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China

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Haibin Wang Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China
Reproductive Medical Center, The First Affiliated Hospital of Xiamen University, Xiamen, Fujian, China

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Shuangbo Kong Fujian Provincial Key Laboratory of Reproductive Health Research, School of Medicine, Xiamen University, Xiamen, Fujian, China
Reproductive Medical Center, The First Affiliated Hospital of Xiamen University, Xiamen, Fujian, China

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Yuanzhen Zhang Department of Obstetrics and Gynecology, Zhongnan Hospital of Wuhan University, Wuhan, Hubei, China
Hubei Clinical Research Center for Prenatal Diagnosis and Birth Health, Wuhan, Hubei, China

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Correspondence should be addressed to Y Zhang or S Kong or H Wang: zhangyuanzhen@vip.sina.com or shuangbo_kong@163.com or haibin.wang@vip.163.com
DOI:
https://doi.org/10.1530/JOE-19-0284
Volume/Issue:
Volume 243: Issue 3
Article Type:
Research Article
Page Range:
229–242
Online Publication Date:
Dec 2019
Copyright:
© 2019 Society for Endocrinology 2019
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Progesterone is an important hormone for female reproduction; however, how the fluctuation of progesterone acts upon reproductive processes remains largely unknown. Mounting evidence indicates a pivotal role of the circadian clock in sensing hormone dynamics for homeostatic regulation of physiological functions. Therefore, we sought to determine whether clock genes respond to progesterone signaling in female reproductive system. In this study, we tested the hypothesis that the circadian system could respond to progesterone signaling during human endometrial decidual transformation. The expression of the circadian gene PER1 increased immediately and remained elevated during human endometrial decidualization. The progesterone receptor activated PER1 transcription by directly binding to its promoter from the onset of the stromal proliferation-differentiation transition. PER1 knockout significantly downregulated the expression of some PGR target genes, and attenuated human endometrial decidual transformation by expediting FOXO1 protein degradation. In conclusion, progesterone could control the female reproductive process through sustained feedback from the circadian gene PER1, which is probably involved to P4-PR signaling responsiveness in the initiation and maintenance of decidualization.

Supplementary Materials

    • Supplementary Fig. 1 (A, B) IGFBP1 and PRL mRNA levels in immortalized HESCs after treatment with MPA plus db-cAMP at 0, 2, 4 and 6 days (n=3 per independent experiment). The values are normalized to the GAPDH expression level. Analysis was performed with one-way ANOVA and Bonferroni’s post hoc test. **P <0.01. (C, D, E) IGFBP1 and PRL protein levels in immortalized HESCs after treatment with MPA plus db-cAMP at 0, 2, 4, 6 and 8 days (n=3 per independent experiment). The values are normalized to the GAPDH expression level. Analysis was performed between the undifferentiated group and the decidualized group using two-way repeated measures ANOVA with Bonferroni’s post hoc test. **P <0.01, ***P <0.001.
    • Supplementary Fig. 2 (A, B) IGFBP1 and PRL mRNA levels in the control (empty vector) and PGR-KO cell lines after treatment with MPA plus db-cAMP at 0, 2, 4 and 6 days (n=3 per independent experiment). The values are normalized to the GAPDH expression level. Analysis was performed between the control group and the PGR-KO group using two-way repeated measures ANOVA with Bonferroni’s post hoc test. *P <0.05. (C) After primary HESCs were seeded for 1 day, immunofluorescence staining was performed for vimentin and cytokeratin. Scale bars, 100 μM. (D, E, F, G) PRL, IGFBP1 and FOXO1 protein levels in control (empty vector) and PER1-KO cells after treatment with MPA plus db-cAMP at 0, 2, 4, 6 and 8 days (n=3 per independent experiment). The values are normalized to the GAPDH expression level. Analysis was performed between the control group and the PER1-KO group using two-way repeated measures ANOVA with Bonferroni’s post hoc test. *P <0.05, **P <0.01, ***P <0.001.

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Print ISSN:
0022-0795
Online ISSN:
1479-6805
Copyright:
© 2019 Society for Endocrinology 2019
Page(s):
14
Article Type:
Research Article
Received Date:
05 Sep 2019
Accepted Date:
12 Sep 2019
Print Publication Date:
01 Dec 2019
Online Publication Date:
Dec 2019
Keywords:
clock gene; decidualization; endometrium; PER1; progesterone receptor