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
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.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
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?
In the citing paper
“In addition, ERβ is also hypermethylated and silenced in normal endometrial stromal cells [71].”
From The Pathogenesis of Adenomyosis vis-à-vis Endometriosis (2020) · cites this paper as [71]
In the citing paper
“Higher expression of estrogen receptor amplifies estrogenic effects and the proliferative capacity of endometrial cells.26,27”
From Altered genome-wide methylation in endometriosis (2014) · cites this paper as [27]
Citations
Cites
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
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
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
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
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
Cited by
Sorted by citations
Endometriosis: pathogenesis and treatment
Vercellini, P., Viganò, P., Somigliana, E., & Fedele, L. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2013.255 · Cited by 1,940
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772
Self-citationEndometriosis is a chronic systemic disease: Clinical challenges and novel innovations
Taylor, H. S., Kotlyar, A. M., & Flores, V. A. (2021) · The Lancet · doi:10.1016/s0140-6736(21)00389-5 · Cited by 1,425
Bulun, S. E., Yilmaz, B. D., Sison, C., Miyazaki, K., Bernardi, L., Liu, S., Kohlmeier, A., Yin, P., Milad, M., & Wei, J. (2019) · Endocrine Reviews · doi:10.1210/er.2018-00242 · Cited by 844
Self-citationProgesterone action in endometrial cancer, endometriosis, uterine fibroids, and breast cancer
Kim, J. J., Kurita, T., & Bulun, S. E. (2013) · Endocrine Reviews · doi:10.1210/er.2012-1043 · Cited by 520
Self-citationProgesterone and Estrogen Signaling in the Endometrium: What Goes Wrong in Endometriosis?
Marquardt, R. M., Kim, T. H., Shin, J., & Jeong, J. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20153822 · Cited by 527
The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights
Laganà, A. S., Garzon, S., Götte, M., Viganò, P., Franchi, M. P., Ghezzi, F., & Martin, D. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20225615 · Cited by 503
The Origin and Pathogenesis of Endometriosis
Wang, Y., Nicholes, K., & Shih, I. (2019) · Annual Review of Pathology Mechanisms of Disease · doi:10.1146/annurev-pathmechdis-012419-032654 · Cited by 483
Han, S. J., Jung, S. Y., Wu, S.-P., Hawkins, S. M., Park, M. J., Kyo, S., Qin, J., Lydon, J. P., Tsai, S. Y., Tsai, M.-J., et al. (2015) · Cell · doi:10.1016/j.cell.2015.10.034 · Cited by 380
Hormonal treatments for endometriosis: The endocrine background
Vannuccini, S., Clemenza, S., Rossi, M., & Petraglia, F. (2022) · Reviews in Endocrine and Metabolic Disorders · doi:10.1007/s11154-021-09666-w · Cited by 336
“Changes in promoter methylation may be a cause for the increased ERβ/ERα ratio in endometriotic cells, since regions of the ERα promoter become hypermethylated leading to a decreased expression, whereas a CpG island in the ERβ promoter becomes hypomethylated causing an increased expression [41, 42] (Fig.”
BackgroundProgesterone resistance in endometriosis: origins, consequences and interventions
Patel, B. G., Rudnicki, M., Yu, J., Shu, Y., & Taylor, R. N. (2017) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.1111/aogs.13156 · Cited by 336
Guo, S.-W. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap064 · Cited by 328
Estrogen Receptor β: An Overview and Update
Zhao, C., Dahlman‐Wright, K., & Gustafsson, J.-Α. (2008) · Nuclear Receptor Signaling · doi:10.1621/nrs.06003 · Cited by 311
Role of Estrogen Receptor-β in Endometriosis
Bulun, S., Monsavais, D., Pavone, M., Dyson, M., Xue, Q., Attar, E., Tokunaga, H., & Su, E. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0031-1299596 · Cited by 321
Self-citationRole of estrogen receptors in health and disease
Chen, P., Li, B., & Ou-Yang, L. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.839005 · Cited by 339
Estrogen Receptors and Endometriosis
Chantalat, É., Valera, M., Vaysse, C., Noirrit‐Esclassan, E., Rusidzé, M., Weyl, A., Vergriete, K., Buscail, É., Lluel, P., Fontaine, C., et al. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21082815 · Cited by 335
Estrogen receptors and human disease: an update
Burns, K. A., & Korach, K. (2012) · Archives of Toxicology · doi:10.1007/s00204-012-0868-5 · Cited by 287
Endometriosis and nuclear receptors
Yilmaz, B. D., & Bulun, S. E. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz005 · Cited by 243
Self-citationEstrogen Receptor-β, Estrogen Receptor-α, and Progesterone Resistance in Endometriosis
Bulun, S., Cheng, Y.-H., Pavone, M., Xue, Q., Attar, E., Trukhacheva, E., Tokunaga, H., Utsunomiya, H., Yin, P., Luo, X., et al. (2010) · Seminars in Reproductive Medicine · doi:10.1055/s-0029-1242991 · Cited by 243
Self-citationEndometriosis and adenomyosis: shared pathophysiology
Bulun, S. E., Yildiz, S., Adli, M., Chakravarti, D., Parker, J. B., Milad, M., Yang, L., Chaudhari, A., Tsai, S., Wei, J. J., et al. (2023) · Fertility and Sterility · doi:10.1016/j.fertnstert.2023.03.006 · Cited by 216
Self-citationAdenomyosis pathogenesis: insights from next-generation sequencing
Bulun, S. E., Yıldız, Ş., Adli, M., & Wei, J. (2021) · Human Reproduction Update · doi:10.1093/humupd/dmab017 · Cited by 216
Self-citationRegulation of Inflammation Pathways and Inflammasome by Sex Steroid Hormones in Endometriosis
García-Gómez, E., Vázquez-Martínez, E. R., Reyes-Mayoral, C., Cruz-Orozco, O., Camacho‐Arroyo, I., & Cerbón, M. A. (2020) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00935 · Cited by 202
Huhtinen, K., Desai, R., Ståhle, M., Salminen, A., Handelsman, D. J., Perheentupa, A., & Poutanen, M. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1154 · Cited by 195
Greaves, E., Cousins, F., Murray, A., Esnal-Zufiaurre, A., Fassbender, A., Horne, A., & Saunders, P. (2014) · American Journal of Pathology · doi:10.1016/j.ajpath.2014.03.011 · Cited by 170
Kinase signalling pathways in endometriosis: potential targets for non-hormonal therapeutics
McKinnon, B. D., Kocbek, V., Nirgianakis, K., Bersinger, N. A., & Mueller, M. D. (2016) · Human Reproduction Update · doi:10.1093/humupd/dmv060 · Cited by 195
Endometrial receptivity in women of advanced age: an underrated factor in infertility
Pathare, A. D. S., Loid, M., Saare, M., Gidlöf, S. B., Esteki, M. Z., Acharya, G., Peters, M., & Salumets, A. (2023) · Human Reproduction Update · doi:10.1093/humupd/dmad019 · Cited by 194
Zama, A. M., & Uzumcu, M. (2009) · Endocrinology · doi:10.1210/en.2009-0499 · Cited by 181
Molecular and Cellular Pathogenesis of Endometriosis
Klemmt, P. A. B., & Starzinski‐Powitz, A. (2017) · Current Women s Health Reviews · doi:10.2174/1573404813666170306163448 · Cited by 182
Aghajanova, L., Hamilton, A., Kwintkiewicz, J., Vo, K. C., & Giudice, L. C. (2009) · Biology of Reproduction · doi:10.1095/biolreprod.108.070300 · Cited by 168
Epigenetic effects of endocrine-disrupting chemicals on female reproduction: An ovarian perspective
Zama, A. M., & Uzumcu, M. (2010) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2010.06.003 · Cited by 168
The Pathogenesis of Adenomyosis vis-à-vis Endometriosis
Guo, S.-W. (2020) · Journal of Clinical Medicine · doi:10.3390/jcm9020485 · Cited by 165
“In addition, ERβ is also hypermethylated and silenced in normal endometrial stromal cells [71].”
BackgroundEstrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153
Burns, K. A., Rodriguez, K., Hewitt, S., Janardhan, K., Young, S., & Korach, K. (2012) · Endocrinology · doi:10.1210/en.2012-1294 · Cited by 143
Yamagata, Y., Asada, H., Tamura, I., Lee, L., Maekawa, R., Taniguchi, K., Taketani, T., Matsuoka, A., Tamura, H., & Sugino, N. (2009) · Human Reproduction · doi:10.1093/humrep/dep015 · Cited by 151
Szczepańska, M., Wirstlein, P. K., Skrzypczak, J., & Jagodziński, P. P. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-1 · Cited by 151
Estrogen receptor β: the guardian of the endometrium
Hapangama, D. K., Kamal, A. M., & Bulmer, J. N. (2015) · Human Reproduction Update · doi:10.1093/humupd/dmu053 · Cited by 145
Trukhacheva, E., Lin, Z., Reierstad, S., Cheng, Y.-H., Milad, M., & Bulun, S. E. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-1466 · Cited by 143
Self-citationDevelopmental programming: prenatal androgen excess disrupts ovarian steroid receptor balance
Ortega, H. H., Salvetti, N. R., & Padmanabhan, V. (2009) · Reproduction · doi:10.1530/rep-08-0491 · Cited by 133
Mei, J., Zhu, X., Jin, L.-P., Duan, Z., Li, D., & Li, M. (2015) · Human Reproduction · doi:10.1093/humrep/dev100 · Cited by 126
Epigenetic Dysregulation in Endometriosis: Implications for Pathophysiology and Therapeutics
Marquardt, R. M., Tran, D. N., Lessey, B. A., Rahman, M. S., & Jeong, J. (2023) · Endocrine Reviews · doi:10.1210/endrev/bnad020 · Cited by 137
Progesterone Receptor Status Predicts Response to Progestin Therapy in Endometriosis
Flores, V. A., Vanhie, A., Dang, T., & Taylor, H. S. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01227 · Cited by 118
Proestling, K., Birner, P., Gamperl, S., Nirtl, N., Márton, E., Yerlikaya‐Schatten, G., Wenzl, R. J., Streubel, B., & Husslein, H. (2015) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-015-0063-7 · Cited by 116
Molecular aspects of development and regulation of endometriosis
Aznaurova, Y. B., M.B.Zhumataev, M. B. Z., Roberts, T. K., Aliper, A. M., & Zhavoronkov, A. A. (2014) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-12-50 · Cited by 116
Lu, Y., Nie, J., Liu, X., Zheng, Y., & Guo, S. (2010) · Human Reproduction · doi:10.1093/humrep/dep472 · Cited by 111
Hayashi, A., Tanabe, A., Kawabe, S., Hayashi, M., Yuguchi, H., Yamashita, Y., Okuda, K., & Ohmichi, M. (2012) · Journal of Ovarian Research · doi:10.1186/1757-2215-5-31 · Cited by 116
Liu, X., Zhang, Q., & Guo, S.-W. (2018) · Reproductive Sciences · doi:10.1177/1933719117718275 · Cited by 110
Estrogen biosynthesis and signaling in endometriosis
Huhtinen, K., Ståhle, M., Perheentupa, A., & Poutanen, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.08.022 · Cited by 107
Epithelial Mutations in Endometriosis: Link to Ovarian Cancer
Bulun, S. E., Wan, Y., & Matei, D. E. (2019) · Endocrinology · doi:10.1210/en.2018-00794 · Cited by 105
Self-citationDNA methylation in endometriosis (Review)
KOUKOURA, O., SIFAKIS, S., & SPANDIDOS, D. A. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.4925 · Cited by 103
Endometriosis is characterized by a distinct pattern of histone 3 and histone 4 lysine modifications
Monteiro, J. B., Colón-Díaz, M., García, M., Gutierrez, S., Colón, M., Seto, E., Laboy, J., & Flores, I. (2014) · Reproductive Sciences · doi:10.1177/1933719113497267 · Cited by 98
Han, S. J., & O’Malley, B. W. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu002 · Cited by 98
Aghajanova, L., Tatsumi, K., Horcajadas, J. A., Zamah, A. M., Esteban, F. J., Herndon, C. N., Conti, M., & Giudice, L. C. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.110.086181 · Cited by 99
Hormonal therapy for endometriosis: from molecular research to bedside
Tosti, C., Biscione, A., Morgante, G., Bifulco, G., Luisi, S., & Petraglia, F. (2017) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2016.05.032 · Cited by 96
Borghese, B., Barbaux, S., Mondon, F., Santulli, P., Pierre, G., Vinci, G., Chapron, C., & Vaiman, D. (2010) · Molecular Endocrinology · doi:10.1210/me.2010-0160 · Cited by 97
Genistein: Dual Role in Women’s Health
Yu, L. C., Rios, E., Castro, L., Liu, J., Yan, Y., & Dixon, D. (2021) · Nutrients · doi:10.3390/nu13093048 · Cited by 95
Cancer-associated mutations in endometriosis: shedding light on the pathogenesis and pathophysiology
Guo, S.-W. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmz047 · Cited by 96
Velarde, M. C., Aghajanova, L., NEZHAT, C. R., & Giudice, L. C. (2009) · Endocrinology · doi:10.1210/en.2009-0389 · Cited by 92
Monsivais, D., Dyson, M. T., Yin, P., Coon, J. S., Navarro, A., Feng, G., Malpani, S. S., Ono, M., Ercan, C. M., Wei, J. J., et al. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1421 · Cited by 91
Self-citationHypoxia: The force of endometriosis
Wu, M., Hsiao, K., & Tsai, S. (2019) · Journal of Obstetrics and Gynaecology Research · doi:10.1111/jog.13900 · Cited by 88
Nasu, K., Kawano, Y., Tsukamoto, Y., Takano, M., Takai, N., Li, H., Furukawa, Y., Abe, W., Moriyama, M., & Narahara, H. (2011) · Journal of obstetrics and gynaecology research · doi:10.1111/j.1447-0756.2011.01663.x · Cited by 89
Kawano, Y., Nasu, K., Li, H., Tsuno, A., Abe, W., Takai, N., & Narahara, H. (2011) · Human Reproduction · doi:10.1093/humrep/der203 · Cited by 88
Li, Y., Adur, M. K., Kannan, A., Dávila, J., Zhao, Y., Nowak, R. A., Bagchi, M. K., Bagchi, I. C., & Li, Q. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165347 · Cited by 90
Expression Pattern of Stemness-Related Genes in Human Endometrial and Endometriotic Tissues
Forte, A., Schettino, M. T., Finicelli, M., Cipollaro, M., Colacurci, N., Cobellis, L., & Galderisi, U. (2009) · Molecular Medicine · doi:10.2119/molmed.2009.00068 · Cited by 86
The non-human primate model of endometriosis: research and implications for fecundity
Braundmeier, A. G., & Fazleabas, A. T. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap057 · Cited by 85
Aromatase and endometriosis: estrogens play a role
Ferrero, S., Remorgida, V., Maganza, C., Venturini, P. L., Salvatore, S., Papaleo, E., Candiani, M., & Maggiore, U. L. R. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12411 · Cited by 84
Yotova, I., Hsu, E., Do, C., Gaba, A., Sczabolcs, M., Dekan, S., Kenner, L., Wenzl, R., & Tycko, B. (2017) · PLOS ONE · doi:10.1371/journal.pone.0170859 · Cited by 81
Local estrogen formation and its regulation in endometriosis
Mori, T., Ito, F., Koshiba, A., Kataoka, H., Takaoka, O., Okimura, H., Khan, K. N., & Kitawaki, J. (2019) · Reproductive Medicine and Biology · doi:10.1002/rmb2.12285 · Cited by 84
Altered genome-wide methylation in endometriosis
Naqvi, H., Ilagan, Y., Krikun, G., & Taylor, H. S. (2014) · Reproductive Sciences · doi:10.1177/1933719114532841 · Cited by 82
Human Endometrial DNA Methylome Is Cycle-Dependent and Is Associated With Gene Expression Regulation
Houshdaran, S., Zelenko, Z., Irwin, J. C., & Giudice, L. C. (2014) · Molecular Endocrinology · doi:10.1210/me.2013-1340 · Cited by 81
Differential regulation of Akt phosphorylation in endometriosis.
Cinar, O., Seval, Y., Uz, Y. H., Cakmak, H., Ulukus, M., Kayisli, U., & Arıcı, A. (2009) · Reproductive Biomedicine Online · doi:10.1016/j.rbmo.2009.10.001 · Cited by 82
Greaves, E., Collins, F., Esnal-Zufiaurre, A., Giakoumelou, S., Horne, A. W., & Saunders, P. T. K. (2014) · Endocrinology · doi:10.1210/en.2014-1086 · Cited by 77
Role of Oxidative Stress in Epigenetic Modification in Endometriosis
Ito, F., Yamada, Y., 重光, 愛., Akinishi, M., Kaniwa, H., Miyake, R., Yamanaka, S., & Kobayashi, H. (2017) · Reproductive Sciences · doi:10.1177/1933719117704909 · Cited by 79
Daidzein-rich isoflavone aglycones inhibit cell growth and inflammation in endometriosis
Takaoka, O., Mori, T., Ito, F., Okimura, H., Kataoka, H., Tanaka, Y., Koshiba, A., Kusuki, I., Shigehiro, S., Amami, T., et al. (2018) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2018.04.004 · Cited by 81
Potential link between estrogen receptor-alpha gene hypomethylation and uterine fibroid formation.
Asada, H., Yamagata, Y., Taketani, T., Matsuoka, A., Tamura, H., Hattori, N., Ohgane, J., Hattori, N., Shiota, K., & Sugino, N. (2008) · Molecular human reproduction · doi:10.1093/molehr/gan045 · Cited by 73
Genome-wide DNA methylation profiling in cultured eutopic and ectopic endometrial stromal cells
Yamagata, Y., Nishino, K., Takaki, E., Sato, S., Maekawa, R., Nakai, A., & Sugino, N. (2014) · PLoS ONE · doi:10.1371/journal.pone.0083612 · Cited by 70
Regulation of estrogen receptor beta activity and implications in health and disease
Swedenborg, E., Power, K. A., Cai, W., Pongratz, I., & Rüegg, J. (2009) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-009-0118-z · Cited by 69
The influence of menstrual cycle and endometriosis on endometrial methylome
Saare, M., Modhukur, V., Suhorutshenko, M., Rajashekar, B., Rekker, K., Sõritsa, D., Karro, H., Soplepmann, P., Sõritsa, A., Lindgren, C. M., et al. (2016) · Clinical Epigenetics · doi:10.1186/s13148-015-0168-z · Cited by 68
Liu, M.-H., Liu, X., Zhang, Y., & Guo, S. (2012) · Reproductive Sciences · doi:10.1177/1933719111424453 · Cited by 68
Roy, D., Morgan, M., Yoo, C., Deoraj, A., Roy, S., Yadav, V., Garoub, M. M., Assaggaf, H. M., & Doke, M. (2015) · International Journal of Molecular Sciences · doi:10.3390/ijms161025285 · Cited by 67
Epigenetic regulation and T-cell responses in endometriosis – something other than autoimmunity
Szukiewicz, D. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.943839 · Cited by 65
Hsiao, K.-Y., Wu, M.-H., Chang, N., Yang, S.-H., Wu, C.-W., Sun, H. S., & Tsai, S.-J. (2015) · Molecular Human Reproduction · doi:10.1093/molehr/gav054 · Cited by 64
van Kaam, K. J. A. F., Delvoux, B., Romano, A., D’Hooghe, T., Dunselman, G. A. J., & Groothuis, P. G. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.01.031 · Cited by 64
Machine Learning Classifiers for Endometriosis Using Transcriptomics and Methylomics Data
Akter, S., Xu, D. H., Nagel, S. C., Bromfield, J. J., Pelch, K. E., Wilshire, G., & Joshi, T. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00766 · Cited by 65
Epigenetics of Estrogen and Progesterone Receptors in Endometriosis
Chen, H., Malentacchi, F., Fambrini, M., Harrath, A. H., Huang, H., & Petraglia, F. (2020) · Reproductive Sciences · doi:10.1007/s43032-020-00226-2 · Cited by 66
Monsivais, D., Dyson, M. T., Yin, P., Navarro, A., Coon, J. S., Pavone, M. E., & Bulun, S. E. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.01.012 · Cited by 62
Self-citationLi, W.-N., Wu, M., & Tsai, S. (2020) · Reproduction · doi:10.1530/rep-20-0267 · Cited by 66
Forte, A., Cipollaro, M., & Galderisi, U. (2013) · Clinical Science · doi:10.1042/cs20130099 · Cited by 63
Sutrisno, S., Aprina, H., Simanungkalit, H. M., Andriyani, A., Barlıanto, W., Sujuti, H., Santoso, S., Dwijayasa, P. M., Wahyuni, E. S., & Mustofa, E. (2017) · Journal of Traditional and Complementary Medicine · doi:10.1016/j.jtcme.2017.03.002 · Cited by 60
The elusive and controversial roles of estrogen and progesterone receptors in human endometriosis.
Shao, R., Cao, S., Wang, X., Feng, Y., & Billig, H. (2014) · Europe PMC (PubMed Central) · Cited by 55
Expression and regulation of DNA methyltransferases in human endometrium
Vincent, Z. L., Farquhar, C. M., Mitchell, M. D., & Ponnampalam, A. P. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.09.030 · Cited by 55
Nothnick, W. B., & Alali, Z. (2016) · F1000Research · doi:10.12688/f1000research.7504.1 · Cited by 55
Ding, Y., Long, C., Liu, X., Chen, X., Guo, L.-R., Xia, Y., He, J., & Wang, Y. (2012) · PLoS ONE · doi:10.1371/journal.pone.0045364 · Cited by 54
Zanatta, A., Pereira, R., da Rocha, A. M., Cogliati, B., Baracat, E. C., Taylor, H. S., Motta, E. L. A., & Serafini, P. C. (2014) · Reproductive Sciences · doi:10.1177/1933719114549846 · Cited by 54
Wang, D., Chen, Q., Zhang, C., Ren, F., & Li, T. (2012) · European journal of medical research · doi:10.1186/2047-783x-17-12 · Cited by 56
Logan, P. C., Yango, P., & Tran, N. D. (2017) · Reproductive Sciences · doi:10.1177/1933719117704905 · Cited by 54
Endometriosis research in the -omics era
Goulielmos, G. N., Matalliotakis, M., Matalliotaki, C., Eliopoulos, E., Matalliotakis, I., & Zervou, M. I. (2020) · Gene · doi:10.1016/j.gene.2020.144545 · Cited by 50
Epigenetic aberration of gene expression in endometriosis
Izawa, M. (2013) · Frontiers in Bioscience · doi:10.2741/e669 · Cited by 49
Arosh, J. A., Lee, J., Starzinski‐Powitz, A., & Banu, S. K. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.03.023 · Cited by 48
Xenoestrogen regulation of ERα/ERβ balance in hormone-associated cancers
Acconcia, F., Fiocchetti, M., & Marino, M. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.10.033 · Cited by 49
Gołąbek-Grenda, A., & Olejnik, A. M. (2022) · Cellular Signalling · doi:10.1016/j.cellsig.2022.110375 · Cited by 53
Metadata
- 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.
- 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
- 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
