Cited by 350Epigenetics and DNA MethylationEndometriosis Research and TreatmentEstrogen and related hormone effects

The DOI matches its Crossref record; 42 of the 43 references it cites were found in a registry or an index.

Promoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1

Xue, Qing, Lin, Zhihong, Cheng, You-Hong, Huang, Chiang-Ching, Marsh, Erica, Yin, Ping, Milad, Magdy P., Confino, Edmond, Reierstad, Scott, Innes, Joy, Bulun, Serdar E.·2007·Biology of Reproduction

DOI 10.1095/biolreprod.107.061804

Open this paper in CoChat — free account

Abstract

Steroid receptors in the stromal cells of endometrium and its disease counterpart tissue endometriosis play critical physiologic roles. We found that mRNA and protein levels of estrogen receptor 2 (ESR2) were strikingly higher, whereas levels of estrogen receptor 1 (ESR1), total progesterone receptor (PGR), and progesterone receptor B (PGR B) were significantly lower in endometriotic versus endometrial stromal cells. Because ESR2 displayed the most striking levels of differential expression between endometriotic and endometrial cells, and the mechanisms for this difference are unknown, we tested the hypothesis that alteration in DNA methylation is a mechanism responsible for severely increased ESR2 mRNA levels in endometriotic cells. We identified a CpG island occupying the promoter region (-197/+359) of the ESR2 gene. Bisulfite sequencing of this region showed significantly higher methylation in primary endometrial cells (n = 8 subjects) versus endometriotic cells (n = 8 subjects). The demethylating agent 5-aza-2'-deoxycytidine significantly increased ESR2 mRNA levels in endometrial cells. Mechanistically, we employed serial deletion mutants of the ESR2 promoter fused to the luciferase reporter gene and transiently transfected into both endometriotic and endometrial cells. We demonstrated that the critical region (-197/+372) that confers promoter activity also bears the CpG island, and the activity of the ESR2 promoter was strongly inactivated by in vitro methylation. Taken together, methylation of a CpG island at the ESR2 promoter region is a primary mechanism responsible for differential expression of ESR2 in endometriosis and endometrium. These findings may be applied to a number of areas ranging from diagnosis to the treatment of endometriosis.

Integrity signals

Registry

Crossref · 10.1095/biolreprod.107.061804

Cites

42 of 42 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Cloning of a novel receptor expressed in rat prostate and ovary.
Kuiper, G. G. J. M., Enmark, E., Pelto‐Huikko, M., Nilsson, S., & Gustafsson, J.-Α. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.12.5925 · Cited by 4,802
Comparison of the Ligand Binding Specificity and Transcript Tissue Distribution of Estrogen Receptors α and β
Kuiper, G. G. J. M., Carlsson, B., Grandien, K., Enmark, E., Häggblad, J., Nilsson, S., & Gustafsson, J.-A. (1997) · Endocrinology · doi:10.1210/endo.138.3.4979 · Cited by 4,442
Endometriosis
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
Methylated DNA and MeCP2 recruit histone deacetylase to repress transcription
Jones, P. L., Veenstra, G. J. C., Wade, P. A., Vermaak, D., Kass, S. U., Landsberger, N., Strouboulis, J., & Wolffe, A. P. (1998) · Nature Genetics · doi:10.1038/561 · Cited by 2,791
Human oestrogen receptor cDNA: sequence, expression and homology to v-erb-A
Green, S., Walter, P., Kumar, V., Krust, A., Bornert, J., Argos, P., & Chambon, P. (1986) · Nature · doi:10.1038/320134a0 · Cited by 2,320
ERβ: Identification and characterization of a novel human estrogen receptor
Mosselman, S., Polman, J., & Dijkema, R. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00782-x · Cited by 2,269
Generation and reproductive phenotypes of mice lacking estrogen receptor β
Krege, J. H., Hodgin, J. B., Couse, J. F., Enmark, E., Warner, M. N., Mahler, J. F., Sar, M., Korach, K. S., Gustafsson, J.-Α., & Smithies, O. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15677 · Cited by 1,717
EPIDEMIOLOGY OF ENDOMETRIOSIS
Eskenazi, B., & Warner, M. L. (1997) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/s0889-8545(05)70302-8 · Cited by 1,617
The Estrogen Receptor β-Isoform (ERβ) of the Human Estrogen Receptor Modulates ERα Transcriptional Activity and Is a Key Regulator of the Cellular Response to Estrogens and Antiestrogens1
Hall, J. M., & McDonnell, D. P. (1999) · Endocrinology · doi:10.1210/endo.140.12.7179 · Cited by 1,078
Estrogen Receptors α and β Form Heterodimers on DNA
Cowley, S. M., Hoare, S., Mosselman, S., & Parker, M. G. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.32.19858 · Cited by 689

Show all 43 references

Sorted by citations

Items 101–200 of 350

The Increase of Circulating PD-1- and PD-L1-Expressing Lymphocytes in Endometriosis: Correlation with Clinical and Laboratory Parameters
Walankiewicz, M., Grywalska, E., Polak, G., Korona‐Głowniak, I., Witt, E., Surdacka, A., Kotarski, J., & Roliński, J. (2018) · Mediators of Inflammation · doi:10.1155/2018/7041342 · Cited by 48
The p160/Steroid Receptor Coactivator Family: Potent Arbiters of Uterine Physiology and Dysfunction1
Szwarc, M. M., Kommagani, R., Lessey, B. A., & Lydon, J. P. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.125021 · Cited by 49
DNA methylation of HOXA10 in eutopic and ectopic endometrium
Andersson, K. L., Bussani, C., Fambrini, M., Polverino, V., Taddei, G., Gemzell‐Danielsson, K., & Scarselli, G. F. (2014) · Human Reproduction · doi:10.1093/humrep/deu161 · Cited by 47
DNA methylation patterns of steroid receptor genes ESR1, ESR2 and PGR in deep endometriosis compromising the rectum
MEYER, J. L., ZIMBARDI, D., PODGAEC, S., AMORIM, R. L., ABRÃO, M. S., & RAINHO, C. A. (2014) · International Journal of Molecular Medicine · doi:10.3892/ijmm.2014.1637 · Cited by 47
Effect of cyclic AMP and estrogen/progesterone on the transcription of DNA methyltransferases during the decidualization of human endometrial stromal cells
Logan, P. C., Ponnampalam, A. P., STEINER, M. C., & Mitchell, M. D. (2012) · Molecular Human Reproduction · doi:10.1093/molehr/gas062 · Cited by 46
Dysfunctional signaling underlying endometriosis: current state of knowledge
Cho, Y. J., Lee, S. H., Park, J. W., Han, M. S., Park, M. J., & Han, S. J. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0227 · Cited by 49
Mitochondrial translocation of estrogen receptor Β affords resistance to oxidative insult-induced apoptosis and contributes to the pathogenesis of endometriosis
Liao, T.-L., Lee, Y.-C., Tzeng, C.-R., Wang, Y.-P., Chang, H.-Y., Lin, Y.-F., & Kao, S.-H. (2019) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2019.01.022 · Cited by 44
Infertility workup: identifying endometriosis
Pirtea, P., Vulliémoz, N. R., de Ziegler, D., & Ayoubi, J. M. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.03.015 · Cited by 46
An Alkylphenol Mix Promotes Seminoma Derived Cell Proliferation through an ERalpha36-Mediated Mechanism
Ajj, H., Chesnel, A., Pinel, S., Plénat, F., Flament, S., & Dumond, H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0061758 · Cited by 44
Immunoreactivity of progesterone receptor isoform B and nuclear factor kappa-B as biomarkers for recurrence of ovarian endometriomas
Shen, F., Wang, Y., Lu, Y., Yuan, L., Liu, X., & Guo, S. (2008) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2008.04.040 · Cited by 44
Aberrant DNA methylation suppresses expression of estrogen receptor 1 (ESR1) in ovarian endometrioma
Maekawa, R., Mihara, Y., Sato, S., Okada, M., Tamura, I., Shinagawa, M., Shirafuta, Y., Takagi, H., Taketani, T., Tamura, H., et al. (2019) · Journal of Ovarian Research · doi:10.1186/s13048-019-0489-1 · Cited by 44
Melatonin inhibits endometriosis development by disrupting mitochondrial function and regulating tiRNAs
Park, S., Ham, J., Yang, C., Park, W., Park, H., An, G., Song, J., Hong, T., Park, S. J., Kim, H. S., et al. (2022) · Journal of Pineal Research · doi:10.1111/jpi.12842 · Cited by 42
Novel estrogen-related genes and potential biomarkers of ovarian endometriosis identified by differential expression analysis.
Vouk, K., Šmuc, T., Guggenberger, C., Ribič-pucelj, M., Šinkovec, J., Husen, B., Thole, H., Houba, P. H. J., Thaete, C., Adamski, J., et al. (2011) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.010 · Cited by 40
Pathological functions of hypoxia in endometriosis
Hsiao, K.-Y. (2015) · Frontiers in Bioscience · doi:10.2741/e736 · Cited by 61
Estrogen- and Progesterone (P4)-Mediated Epigenetic Modifications of Endometrial Stromal Cells (EnSCs) and/or Mesenchymal Stem/Stromal Cells (MSCs) in the Etiopathogenesis of Endometriosis
Szukiewicz, D., Stangret, A., Ruiz‐Ruiz, C., Olivares, E. G., Şoriţău, O., Șușman, S., & Szewczyk, G. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-020-10115-5 · Cited by 42
Involvement of estrogen receptor-related receptors in human ovarian endometriosis.
Cavallini, A., Resta, L., Caringella, A., Naro, E. D., Lippolis, C., & Loverro, G. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.04.032 · Cited by 34
Endometrial expression of estrogen receptor β and its splice variants in patients with and without endometriosis
Juhasz‐Böss, I., Fischer, C., Lattrich, C., Skrzypczak, M., Malik, E., Ortmann, O., & Treeck, O. (2010) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-010-1768-7 · Cited by 41
Dienogest, a synthetic progestin, down-regulates expression of CYP19A1 and inflammatory and neuroangiogenesis factors through progesterone receptor isoforms A and B in endometriotic cells
Ichioka, M., Mita, S., Shimizu, Y., Imada, K., Kiyono, T., Bono, Y., & Kyo, S. (2014) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2014.12.008 · Cited by 38
Activated Platelets Induce Estrogen Receptor β Expression in Endometriotic Stromal Cells
Zhang, Q., Ding, D., Liu, X., & Guo, S.-W. (2015) · Gynecologic and Obstetric Investigation · doi:10.1159/000377629 · Cited by 38
Protopanaxadiol improves endometriosis associated infertility and miscarriage in sex hormones receptors-dependent and independent manners
Lai, Z., Yang, H., Shi, J.-W., Shen, H., Wang, Y., Chang, K., Zhang, T., Ye, J., Sun, J., Qiu, X., et al. (2021) · International Journal of Biological Sciences · doi:10.7150/ijbs.58657 · Cited by 36
Aberrant expression and localization of deoxyribonucleic acid methyltransferase 3B in endometriotic stromal cells
Dyson, M. T., Kakinuma, T., Pavone, M. E., Monsivais, D., Navarro, A., Malpani, S. S., Ono, M., & Bulun, S. E. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.06.046 · Cited by 37
Self-citation
Effect of simvastatin on baboon endometriosis†
Taylor, H. S., Alderman, M. H., D’Hooghe, T. M., Fazleabas, A. T., & Dulęba, A. J. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox058 · Cited by 38
BPA modulates the WDR5/TET2 complex to regulate ERβ expression in eutopic endometrium and drives the development of endometriosis
Xue, W., Yao, X., Ting, G., Jin, L., Huimin, L., Qiao, Y., Zhou, C., Ming, Z., & Yuanzhen, Z. (2020) · Environmental Pollution · doi:10.1016/j.envpol.2020.115748 · Cited by 39
Activated glucocorticoid and eicosanoid pathways in endometriosis
Monsivais, D., Bray, J. D., Su, E. J., Pavone, M. E., Dyson, M. T., Navarro, A., Kakinuma, T., & Bulun, S. E. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.03.030 · Cited by 37
Self-citation
Global endometrial DNA methylation analysis reveals insights into mQTL regulation and associated endometriosis disease risk and endometrial function
Mortlock, S., Houshdaran, S., Kosti, I., Rahmioğlu, N., NEZHAT, C. R., Vitonis, A. F., Andrews, S. V., Grosjean, P., Paranjpe, M. D., Horne, A. W., et al. (2023) · Communications Biology · doi:10.1038/s42003-023-05070-z · Cited by 40
Silencing of SRA1 Regulates ER Expression and Attenuates the Growth of Stromal Cells in Ovarian Endometriosis
Lin, K., Zhan, H., Ma, J., Xu, K., Wu, R., Zhou, C., & Lin, J. (2016) · Reproductive Sciences · doi:10.1177/1933719116670036 · Cited by 39
Effects of sex steroids on the pattern of methylation and expression of the promoter region of estrogen and androgen receptors in people with gender dysphoria under cross-sex hormone treatment
Aranda, G. B., Fernández‐Rebollo, E., Pradas-Juni, M., Hanzu, F. A., Kalko, S. G., Halperín, I., & Mora, M. (2017) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2017.05.010 · Cited by 36
Postnatal exposure to endosulfan affects uterine development and fertility
Milesi, M. M., Durando, M., Lorenz, V., Gastiazoro, M. P., & Varayoud, J. (2020) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2020.110855 · Cited by 36
Current Knowledge on Endometriosis Etiology: A Systematic Review of Literature
Михалева, Л. М., Radzinsky, V. E., Orazov, M. R., Николаевна, Х. Т., Sorokina, A. V., Александрович, М. С., Владимировна, В. С., Shustova, V. B., & Sinelnikov, M. Y. (2021) · International Journal of Women s Health · doi:10.2147/ijwh.s306135 · Cited by 37
Insight into the Potential Mechanisms of Endocrine Disruption by Dietary Phytoestrogens in the Context of the Etiopathogenesis of Endometriosis
Szukiewicz, D. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241512195 · Cited by 39
Expression of DNA methyltransferases in the mouse uterus during early pregnancy and susceptibility to dietary folate deficiency
Ding, Y., He, J., Liu, X. Q., Chen, X., Long, C., & Wang, Y. X. (2012) · Reproduction · doi:10.1530/rep-12-0006 · Cited by 35
Uterine ERα epigenetic modifications are induced by the endocrine disruptor endosulfan in female rats with impaired fertility
Milesi, M. M., Varayoud, J., Ramos, J. G., & Luque, E. H. (2017) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.05.028 · Cited by 36
Phytoestrogens for the Management of Endometriosis: Findings and Issues
Cai, X., Liu, M., Zhang, B., Zhao, S., & Jiang, S. (2021) · Pharmaceuticals · doi:10.3390/ph14060569 · Cited by 36
COX-2 gene promoter DNA methylation status in eutopic and ectopic endometrium of Egyptian women with endometriosis
Zidan, H. E., Rezk, N. A., Alnemr, A. A. A., & el Ghany, A. M. A. (2015) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2015.06.093 · Cited by 35
Cutting SRC-1 down to size in endometriosis
Dyson, M. T., & Bulun, S. E. (2012) · Nature Medicine · doi:10.1038/nm.2855 · Cited by 34
Self-citation
Expression of oestrogen receptor β isoforms is regulated by transcriptional and post-transcriptional mechanisms
Smith, L., Coleman, L., Cummings, M., Satheesha, S., Shaw, S. O., Speirs, V., & Hughes, T. A. (2010) · Biochemical Journal · doi:10.1042/bj20100373 · Cited by 34
Aberrant histone modification in endometriosis
Nasu, K. (2014) · Frontiers in bioscience · doi:10.2741/4276 · Cited by 33
Advances in targeting estrogen synthesis and receptors in patients with endometriosis
Clemenza, S., Vannuccini, S., Ruotolo, A., Capezzuoli, T., & Petraglia, F. (2022) · Expert Opinion on Investigational Drugs · doi:10.1080/13543784.2022.2152325 · Cited by 34
DNA-Binding Ability of NF-κB is Affected Differently by ERα and ERβ and Its Activation Results in Inhibition of Estrogen Responsiveness
Guzeloglu‐Kayisli, O., Halis, G., Taskiran, S. A., Kayisli, U. A., & Arici, A. M. (2008) · Reproductive Sciences · doi:10.1177/1933719108317583 · Cited by 32
Epigenetic Disorder May Cause Downregulation of HOXA10 in the Eutopic Endometrium of Fertile Women With Endometriosis
Lü, H., Yang, X., Zhang, Y., Lu, R., & Wang, X. (2012) · Reproductive Sciences · doi:10.1177/1933719112451146 · Cited by 33
Genome‐wide analysis of DNA methylation in endometriosis using Illumina Human Methylation 450 K BeadChips
Wang, L., Zhao, J., Li, Y., Wang, Z., & Kang, S. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23127 · Cited by 33
Lipoxin A4 regulates expression of the estrogen receptor and inhibits 17β-estradiol induced p38 mitogen-activated protein kinase phosphorylation in human endometriotic stromal cells
Chen, S., Wu, R., Su, L., Zhou, W., Zhu, M.-B., & Chen, Q. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.03.029 · Cited by 31
The Endometriotic Tissue Lining the Internal Surface of Endometrioma: Hormonal, Genetic, Epigenetic Status, and Gene Expression Profile
Sanchez, A. M., Viganò, P., Somigliana, E., Cioffi, R., Panina‐Bordignon, P., & Candiani, M. (2014) · Reproductive Sciences · doi:10.1177/1933719114529374 · Cited by 30
Arginine methyltransferases mediate an epigenetic ovarian response to endometriosis
Baumann, C., Olson, M. R., Wang, K., Fazleabas, A. T., & Fuente, R. D. L. (2015) · Reproduction · doi:10.1530/rep-15-0212 · Cited by 29
MicroRNAs in Endometriosis: Insights into Inflammation and Progesterone Resistance
Hon, J.-X., Wahab, N. A., Karim, A., Mokhtar, N. M., & Mokhtar, M. H. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms241915001 · Cited by 33
Endometriosis Malignant Transformation: Epigenetics as a Probable Mechanism in Ovarian Tumorigenesis
He, J., Chang, W., Feng, C., Cui, M., & Xu, T. (2018) · International Journal of Genomics · doi:10.1155/2018/1465348 · Cited by 28
A DNA Methylation Perspective on Infertility
Shacfe, G., Turko, R., Syed, H., Masoud, I., Tahmaz, Y., Samhan, L. M., AlKattan, K. M., Shafqat, A., & Yaqinuddin, A. (2023) · Genes · doi:10.3390/genes14122132 · Cited by 34
Clinicopathologic and Immunohistochemical Features of Ovarian Clear Cell Carcinomas in Comparison With Type I and Type II Tumors
Zannoni, G. F., Morassi, F., Prisco, M. G., Stefano, I. D., Vellone, V. G., Arena, V., Scambia, G., & Gallo, D. (2012) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e3182518557 · Cited by 28
Overexpression of lysine-specific demethylase 1 in ovarian endometriomas and its inhibition reduces cellular proliferation, cell cycle progression, and invasiveness
Ding, D., Liu, X., & Guo, S. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2013.11.033 · Cited by 28
Sex Steroid Hormones and Reproductive Disorders
Fauser, B. C. J. M., Laven, J. S. E., Tarlatzis, B. C., Moley, K. H., Critchley, H., Taylor, R. N., Berga, S. L., Mermelstein, P. G., Devroey, P., Gianaroli, L., et al. (2011) · Reproductive Sciences · doi:10.1177/1933719111405068 · Cited by 30
Systematic review on the DNA methylation role in endometriosis: current evidence and perspectives
Ducreux, B., Patrat, C., Firmin, J., Ferreux, L., Chapron, C., Marcellin, L., Parpex, G., Bourdon, M., Vaiman, D., Santulli, P., et al. (2025) · Clinical Epigenetics · doi:10.1186/s13148-025-01828-w · Cited by 32
The Estrogen Receptor-β Expression in De Quervain’s Disease
Shen, P., Wang, P.-H., Wu, P., Wu, K.-C., Hsieh, J., & Jou, I. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161125968 · Cited by 27
Endometriosis and ovulatory menstruation: beyond the Sampson principle
Bulun, S. E. (2025) · Journal of Clinical Investigation · doi:10.1172/jci188787 · Cited by 29
Self-citation
Genetic Polymorphisms of DNMT3L Involved in Hypermethylation of Chromosomal Ends Are Associated with Greater Risk of Developing Ovarian Endometriosis
Borghese, B., Santulli, P., Héquet, D., Pierre, G., de Ziegler, D., Vaiman, D., & Chapron, C. (2012) · American Journal Of Pathology · doi:10.1016/j.ajpath.2012.01.009 · Cited by 26
Epigenetic control of embryo–uterine crosstalk at peri-implantation
Kong, S., Zhou, C., Bao, H., Ni, Z., Liu, M., He, B., Huang, L., Sun, Y., Wang, H., & Lu, J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03245-8 · Cited by 28
Epigenetic dysregulation of endometriosis susceptibility genes (Review)
Koike, N., Higashiura, Y., Akasaka, J., Uekuri, C., Ito, F., & Kobayashi, H. (2015) · Molecular Medicine Reports · doi:10.3892/mmr.2015.3635 · Cited by 25
GenomeForest: An Ensemble Machine Learning Classifier for Endometriosis.
Akter, S., Xu, D., Nagel, S. C., Bromfield, J. J., Pelch, K. E., Wilshire, G., & Joshi, T. (2020) · PubMed Central · Cited by 24
Zearalenone affects the growth of endometriosis via estrogen signaling and inflammatory pathways
Yan, W., Liu, Y., Song, S., Kang, J., Zhang, Y., Lu, L., Wei, S., Xu, Q., Zhang, W., Liu, X., et al. (2022) · Ecotoxicology and Environmental Safety · doi:10.1016/j.ecoenv.2022.113826 · Cited by 26
Emerging drugs for endometriosis
Guo, S. (2008) · Expert Opinion on Emerging Drugs · doi:10.1517/14728210802548360 · Cited by 25
Hypomethylation of the GSTM1 promoter is associated with ovarian endometriosis
Zhao, J., Wang, L., Li, Y., Zhao, W., & Kang, S. (2019) · Human Reproduction · doi:10.1093/humrep/dez039 · Cited by 23
Interferon Signaling in the Endometrium and in Endometriosis
Park, Y., & Han, S. J. (2022) · Biomolecules · doi:10.3390/biom12111554 · Cited by 25
Various types of adenomyosis and endometriosis: in search of optimal management
Guo, S. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2023.03.021 · Cited by 24
Functional Characterization of a Genetic Polymorphism in the Promoter of the ESR2 Gene
Philips, S., Richter, A., Oesterreich, S., Rae, J. M., Flockhart, D. A., Perumal, N. B., & Skaar, T. C. (2011) · Hormones and Cancer · doi:10.1007/s12672-011-0086-2 · Cited by 21
A systematic review of epigenetics of endometriosis
Bedrick, B. S., Courtright, L., Zhang, J., Snow, M., Landsteiner, I., Nylander, E. M., Vaught, K. C. C., Segars, J. H., & Singh, B. (2024) · F&S Reviews · doi:10.1016/j.xfnr.2024.01.003 · Cited by 23
The Genetic Background of Endometriosis: Can ESR2 and CYP19A1 Genes Be a Potential Risk Factor for Its Development?
Smolarz, B., Szyłło, K., & Romanowicz, H. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21218235 · Cited by 23
Genome-wide DNA methylation profiling in ectopic and eutopic of endometrial tissues
Barjaste, N., Shahhoseini, M., Afsharian, P., Sharifi‐Zarchi, A., & Masoudi‐Nejad, A. (2019) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-019-01508-8 · Cited by 21
Construction of lncRNA-related competing endogenous RNA network and identification of hub genes in recurrent implantation failure
Huang, J., Song, N., Xia, L., Tian, L., Tan, J., Chen, Q., Zhu, J., & Wu, Q. (2021) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-021-00778-1 · Cited by 22
Regulation of estrogen receptor β1 expression in breast cancer by epigenetic modification of the 5′ regulatory region
Al-nakhle, H. H., Smith, L., Bell, S. M., Burns, P. A., Cummings, M., Hanby, A. M., Lane, S., Parker, M. D., Hughes, T. A., & Speirs, V. (2013) · International Journal of Oncology · doi:10.3892/ijo.2013.2112 · Cited by 20
Estrogen-Induced CCN1 Is Critical for Establishment of Endometriosis-Like Lesions in Mice
Zhao, Y., Li, Q., Katzenellenbogen, B. S., Lau, L. F., Taylor, R. N., Bagchi, I. C., & Bagchi, M. K. (2014) · Molecular Endocrinology · doi:10.1210/me.2014-1080 · Cited by 21
Periconceptional undernutrition affects in utero methyltransferase expression and steroid hormone concentrations in uterine flushings and blood plasma during the peri-implantation period in domestic pigs
Franczak, A., Zglejc, K., Waszkiewicz, E., Wojciechowicz, B., Martyniak, M., Sobótka, W., Okrasa, S., & Kotwica, G. (2016) · Reproduction Fertility and Development · doi:10.1071/rd16124 · Cited by 21
Polymorphic variants of folate and choline metabolism genes and the risk of endometriosis-associated infertility
Szczepańska, M., Mostowska, A., Wirstlein, P. K., Lianeri, M., Marianowski, P., Skrzypczak, J., & Jagodziński, P. P. (2011) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2011.02.003 · Cited by 20
LPAR2 and LPAR4 are the Main Receptors Responsible for LPA Actions in Ovarian Endometriotic Cysts
Kowalczyk‐Zieba, I., Wocławek-Potocka, I., Waśniewski, T., Boruszewska, D., Grycmacher, K., Sinderewicz, E., Staszkiewicz‐Chodor, J., & Wołczyński, S. (2018) · Reproductive Sciences · doi:10.1177/1933719118766263 · Cited by 19
Epigenetic Regulation in Uterine Fibroids—The Role of Ten-Eleven Translocation Enzymes and Their Potential Therapeutic Application
Włodarczyk, M., Nowicka, G., Ciebiera, M., Ali, M. K., Yang, Q., & Al-Hendy, A. A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052720 · Cited by 19
Prospects for potential therapy targeting immune‑associated factors in endometriosis (Review)
Zhang, W., Li, K., Jian, A., Zhang, G., & Zhang, X. (2024) · Molecular Medicine Reports · doi:10.3892/mmr.2024.13422 · Cited by 25
Epigenetic Regulation of Estrogen Receptor Genes’ Expressions in Adipose Tissue in the Course of Obesity
Koźniewski, K., Wąsowski, M., Jonas, M. I., Lisik, W., Jonas, M., Binda, A., Jaworski, P., Tarnowski, W., Noszczyk, B. H., Puzianowska‐Kuźnicka, M., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23115989 · Cited by 19
Innovations in classical hormonal targets for endometriosis
Pluchino, N., Freschi, L., Wenger, J., & Streuli, I. (2015) · Expert Review of Clinical Pharmacology · doi:10.1586/17512433.2016.1129895 · Cited by 19
Endometriosis: Challenges in Clinical Molecular Diagnostics and Treatment
Chalma, P. R., Díaz-Landy, E. N., Antonio-Véjar, V., Tejedor, J. G. O., Reytor-González, C., Simancas‐Racines, D., & Ordóñez, G. D. B. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26093979 · Cited by 20
C-Jun NH2-Terminal Kinase and p38 Inhibition Suppresses Prostaglandin E2-Stimulated Aromatase and Estrogen Receptor Levels in Human Endometriosis
Zeng, C., Xu, J., Zhou, Y., Yang, H.-X., Zhou, Y., & Xue, Q. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-2031 · Cited by 18
Self-citation
Alternation of ten-eleven translocation 1, 2, and 3 expression in eutopic endometrium of women with endometriosis-associated infertility
Szczepańska, M., Wirstlein, P. K., Zawadzka, M., Wender-Ożegowska, E., & Jagodziński, P. P. (2018) · Gynecological Endocrinology · doi:10.1080/09513590.2018.1490403 · Cited by 18
Could DNA hydroxymethylation be crucial in influencing steroid hormone signaling in endometrial biology and endometriosis?
Mahajan, V., Farquhar, C. M., & Ponnampalam, A. P. (2019) · Molecular Reproduction and Development · doi:10.1002/mrd.23299 · Cited by 18
DNA methylation is correlated with gene expression during early pregnancy in Bos taurus
Walker, C. G., Littlejohn, M. D., Meier, S., Roche, J. R., & Mitchell, M. D. (2013) · Physiological Genomics · doi:10.1152/physiolgenomics.00145.2012 · Cited by 18
Spatial and temporal changes in the expression of steroid hormone receptors in mouse model of endometriosis
Mishra, A., Galvankar, M., Singh, N., Vaidya, S., Chaudhari, U. K., & Modi, D. N. (2020) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-020-01725-6 · Cited by 18
Transcription factor 21 regulates expression of ERβ and SF-1 via upstream stimulatory factor-2 in endometriotic tissues
Wu, P.-L., Zhou, Y., Zeng, C., Li, X., Dong, Z.-T., Zhou, Y.-F., Bulun, S. E., & Xue, Q. (2018) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2018.06.008 · Cited by 17
Self-citation
The Enigmatic Role of Serum & Glucocorticoid Inducible Kinase 1 in the Endometrium
Lang, F. J. W., Rajaxavier, J., Singh, Y., Brucker, S. Y., & Salker, M. S. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.556543 · Cited by 19
Sex Steroid Receptors in Polycystic Ovary Syndrome and Endometriosis: Insights from Laboratory Studies to Clinical Trials
Hamid, F. A., Abu, M., Karim, A. K. A., Ahmad, M., Aziz, N. A., Kamal, D. A. M., & Mokhtar, M. H. (2022) · Biomedicines · doi:10.3390/biomedicines10071705 · Cited by 17
Integrated analysis of genome-wide gene expression and DNA methylation profiles reveals candidate genes in ovary endometriosis
Lei, L., Xu, X., Gong, C., Lin, B., & Li, F. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1093683 · Cited by 17
Non-response to first-line hormonal treatment for symptomatic endometriosis: overcoming tunnel vision. A narrative review
Cetera, G. E., Merli, C. E. M., Facchin, F., Viganò, P., Pesce, E., Caprara, F., & Vercellini, P. (2023) · BMC Women s Health · doi:10.1186/s12905-023-02490-1 · Cited by 26
Expression and steroid hormone regulation of TETs and DNMTs in human endometrium
Mahajan, V., Osavlyuk, D., Logan, P. C., Amirapu, S., & Ponnampalam, A. P. (2020) · Reproduction · doi:10.1530/rep-19-0562 · Cited by 16
Multiple Beneficial Roles of Repressor of Estrogen Receptor Activity (REA) in Suppressing the Progression of Endometriosis
Zhao, Y., Chen, Y., Kuang, Y., Bagchi, M. K., Taylor, R. N., Katzenellenbogen, J. A., & Katzenellenbogen, B. S. (2015) · Endocrinology · doi:10.1210/en.2015-1324 · Cited by 17
Endometriosis — insights into a multifaceted entity
Amălinei, C., Păvăleanu, I., Lozneanu, L., Balan, R. A., Giuşcă, S. E., & Căruntu, I.-D. (2018) · Folia Histochemica et Cytobiologica · doi:10.5603/fhc.a2018.0013 · Cited by 17
MicroRNA22-5p targets ten-eleven translocation and regulates estrogen receptor 2 expression in infertile women with minimal/mild endometriosis during implantation window
Xiao, L. Y., Pei, T., Huang, W., Zhou, M., Fu, J., Tan, J., Liu, T., Song, Y., & Yang, S. (2020) · PLoS ONE · doi:10.1371/journal.pone.0234086 · Cited by 17
Circulating estradiol and its biologically active metabolites in endometriosis and in relation to pain symptoms
Émond, J.-P., Caron, P., Pušić, M. N., Turcotte, V., Simonyan, D., Vogler, A., Osredkar, J., Rižner, T. L., & Guillemette, C. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1034614 · Cited by 18
Gene expression profiles separate endometriosis lesion subtypes and indicate a sensitivity of endometrioma to estrogen suppressive treatments through elevated ESR2 expression
Marla, S., Mortlock, S., Heinosalo, T., POUTANEN, M. H., Montgomery, G. W., & McKinnon, B. D. (2023) · BMC Medicine · doi:10.1186/s12916-023-03166-1 · Cited by 17
Notch activity mediates oestrogen-induced stromal cell invasion in endometriosis
Li, N., Zhang, L., Li, Q., Du, Y., Liu, H., Liu, Y., & Xiong, W. (2018) · Reproduction · doi:10.1530/rep-18-0326 · Cited by 16
Insights from genomic studies on the role of sex steroids in the aetiology of endometriosis
Saunders, P. T. K. (2022) · Reproduction and Fertility · doi:10.1530/raf-21-0078 · Cited by 16
Endometriosis and ovarian cancer risk, an epigenetic connection
Brunty, S., Mitchell, B. L., Zgheib, N. B., & Santanam, N. (2020) · Annals of Translational Medicine · doi:10.21037/atm-20-2449 · Cited by 15
Effect of epigallocatechin‐3‐gallate on the status of DNA methylation of E‐cadherin promoter region on endometriosis mouse
Guan, Q., Shi, W., Zhou, L., Tao, A., & Li, L. (2020) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.14358 · Cited by 15
Characterization of the CpG Island Hypermethylated Phenotype Subclass in Primary Melanomas
Conway, K., Tsai, Y., Edmiston, S. N., Parker, J. S., Parrish, E., Hao, H., Kuan, P. F., SCOTT, G. A., Frank, J. S., Googe, P. B., et al. (2021) · Journal of Investigative Dermatology · doi:10.1016/j.jid.2021.11.017 · Cited by 15
Altered Gene Expression Profile in Vaginal Polypoid Endometriosis Resembles Peritoneal Endometriosis and Is Consistent with Increased Local Estrogen Production
Syrcle, S. M., Pelch, K. E., Schroder, A. L., Nichols, B. M., Mills, M. P., Barrier, B., Havey, A. D., & Nagel, S. C. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000320736 · Cited by 13
Corroborating evidence for aberrant expression of histone deacetylase 8 in endometriosis
Zheng, H., Liu, X., & Guo, S. (2023) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12527 · Cited by 14

Authors: Xue, Q., Lin, Z., Cheng, Y.-H., Huang, C.-C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., & Bulun, S. E.
Affiliations: Northwestern University (US)
Peking University (CN)
Corresponding author: Bulun, Serdar E.
ORCID: Xue, Qing
Lin, Zhihong
Huang, Chiang-Ching
Marsh, Erica
Yin, Ping
Milad, Magdy P.
Bulun, Serdar E.
Venue: Biology of Reproduction
Publisher: Oxford University Press (OUP)
Published: 2007-10-01
Volume: 77
Issue: 4
Pages: 681-687
ISSN: 0006-3363 (ISSN-L)
1529-7268
DOI: 10.1095/biolreprod.107.061804
OpenAlex: W2164434026
Cited by: 346
References: 43
Citations by year: 2026: 15 · 2025: 13 · 2024: 20 · 2023: 30 · 2022: 19 · 2021: 24 · 2020: 23 · 2019: 25 · 2018: 16 · 2017: 15 · 2016: 14 · 2015: 22 · 2014: 27 · 2013: 14 · 2012: 24
FWCI: 4.10
Type: journal article
Language: en
Open access: closed
Locations: Biology of Reproduction (publishedVersion)
PubMed (publishedVersion)
BioOne Complete (BioOne) (submittedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD040093, U54-HD40093)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Life Sciences › Biochemistry, Genetics and Molecular Biology › Endocrinology › Estrogen and related hormone effects
Keywords: estrogen receptor 2, endometriosis, endometrium, DNA methylation, promoter methylation, CpG islands, endometrial stromal cells, estrogen receptor 1, progesterone receptor, gene expression regulation, decitabine, promoter deletion mutants
MeSH terms: Decitabine, Adult, Azacitidine, Cells, Cultured, Endometriosis, Endometrium, Female, Gene Expression Regulation, Humans, Promoter Regions, Genetic, Receptors, Progesterone, RNA, Messenger, Stromal Cells, CpG Islands, DNA Methylation, Estrogen Receptor alpha, Estrogen Receptor beta

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Promoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks