Estrogen Receptor β Modulates Apoptosis Complexes and the Inflammasome to Drive the Pathogenesis of Endometriosis
Open accessAbstract
Alterations in estrogen-mediated cellular signaling play an essential role in the pathogenesis of endometriosis. In addition to higher estrogen receptor (ER) β levels, enhanced ERβ activity was detected in endometriotic tissues, and the inhibition of enhanced ERβ activity by an ERβ-selective antagonist suppressed mouse ectopic lesion growth. Notably, gain of ERβ function stimulated the progression of endometriosis. As a mechanism to evade endogenous immune surveillance for cell survival, ERβ interacts with cellular apoptotic machinery in the cytoplasm to inhibit TNF-α-induced apoptosis. ERβ also interacts with components of the cytoplasmic inflammasome to increase interleukin-1β and thus enhance its cellular adhesion and proliferation properties. Furthermore, this gain of ERβ function enhances epithelial-mesenchymal transition signaling, thereby increasing the invasion activity of endometriotic tissues for establishment of ectopic lesions. Collectively, we reveal how endometrial tissue generated by retrograde menstruation can escape immune surveillance and develop into sustained ectopic lesions via gain of ERβ function.
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Aberrantly high ESR2 levels regulate several pathological processes in endometriotic tissue including proliferation, inhibition of apoptosis, inflammation and pain transmission.
“Aberrantly high ESR2 levels regulate several pathological processes in endometriotic tissue including proliferation, inhibition of apoptosis, inflammation and pain transmission”
From Endometriosis and nuclear receptors (2019) · cites this paper as Han et al., 2015
The Introduction reports elevated ERβ (ESR2) in endometriotic tissue, and the Results report increased proliferation, reduced apoptosis, and altered inflammatory signaling with ERβ gain of function (page numbers not provided). The paper mentions pelvic pain as a symptom in the Introduction, but the passages found do not link ERβ to pain transmission. (LLM, conf=0.88)
Experimental — accuracy not yet measuredIn a mouse model of endometriosis expressing high levels of ESR2 in lesions, inhibition of ESR2 activity by an ESR2-selective estrogen antagonist suppresses lesion growth, whereas gain of ESR2 function stimulates progression of endometriosis.
“The inhibition of ESR2 activity by an ESR2-selective estrogen antagonist suppresses lesion growth in these animals, whereas gain of ESR2 function stimulates the progression of endometriosis”
From Endometriosis and nuclear receptors (2019) · cites this paper as Han et al., 2015
ERβ is the predominant isoform in patients with endometriosis.
“ERβ is the predominant isoform in patients with endometriosis [7,8].”
From Polymorphisms in the 3<a:math xmlns:a="http://www.w3.org/1998/Math/MathML" id="M1"> <a:msup> <a:mrow/> <a:mrow> <a:mo>′</a:mo> </a:mrow> </a:msup> </a:math>UTR Region of ESR2 and CYP19A1 Genes and Its Influence on Allele-Specific Gene Expression in Endometriosis (2020) · cites this paper as [8]
Progesterone resistance may explain non-response to estroprogestins or progestins.
“Progesterone resistance may of course explain this unexpected issue [18,19,20,21,22].”
From Endometriosis and Medical Therapy: From Progestogens to Progesterone Resistance to GnRH Antagonists: A Review (2021) · cites this paper as [19]
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Cites
Mutation of the mouse klotho gene leads to a syndrome resembling ageing
Kuro-o, M., Matsumura, Y., Aizawa, H., Kawaguchi, H., Suga, T., Utsugi, T., Ohyama, Y., Kurabayashi, M., Kaname, T., Kume, E., et al. (1997) · Nature · doi:10.1038/36285 · Cited by 3,837 · see citing works
Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes
Micheau, O., & Tschopp, J. (2003) · Cell · doi:10.1016/s0092-8674(03)00521-x · Cited by 2,738 · see citing works
Giudice, L. C. (2010) · New England Journal of Medicine · doi:10.1056/nejmcp1000274 · Cited by 1,924 · see citing works
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772 · see citing works
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 1,692 · see citing works
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 · see citing works
ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis
Tobiume, K., Matsuzawa, A., Takahashi, T., Nishitoh, H., Morita, K., Takeda, K., Minowa, O., Miyazono, K., Noda, T., & Ichijo, H. (2001) · EMBO Reports · doi:10.1093/embo-reports/kve046 · Cited by 1,213 · see citing works
Caspase‐1‐induced pyroptotic cell death
Miao, E. A., Rajan, J. V., & Aderem, A. A. (2011) · Immunological Reviews · doi:10.1111/j.1600-065x.2011.01044.x · Cited by 1,139 · see citing works
Impact of endometriosis on women’s lives: a qualitative study
Moradi, M., Parker, M. A., Sneddon, A., López, V., & Ellwood, D. A. (2014) · BMC Women s Health · doi:10.1186/1472-6874-14-123 · Cited by 525 · see citing works
Progesterone 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 · see citing works
Regulation of the Apaf-1–caspase-9 apoptosome
Bratton, S. B., & Salvesen, G. S. (2010) · Journal of Cell Science · doi:10.1242/jcs.073643 · Cited by 434 · see citing works
Pathophysiology and Immune Dysfunction in Endometriosis
Ahn, S. H., Monsanto, S. P., Miller, C. D., Singh, S. S., Thomas, R., & Tayade, C. (2015) · BioMed Research International · doi:10.1155/2015/795976 · Cited by 398 · see citing works
Cre-mediated recombination in cell lineages that express the progesterone receptor
Soyal, S. M., Mukherjee, A., Lee, K. Y.-S., Li, J., Li, H., DeMayo, F. J., & Lydon, J. P. (2005) · genesis · doi:10.1002/gene.20098 · Cited by 380 · see citing works
Self-citationTobiume, K., Saitoh, M., & Ichijo, H. (2002) · Journal of Cellular Physiology · doi:10.1002/jcp.10080 · Cited by 362 · see citing works
Estrogen receptors α and β in the rodent mammary gland
Saji, S., Jensen, E. V., Nilsson, S. V., Rylander‐Rudqvist, T., Warner, M. N., & Gustafsson, J.-Α. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.1.337 · Cited by 357 · see citing works
Endometriosis: cost estimates and methodological perspective
Simoens, S., Hummelshoj, L., & D'Hooghe, T. (2007) · Human Reproduction Update · doi:10.1093/humupd/dmm010 · Cited by 357 · see citing works
Ligand-independent activation of steroid hormone receptors
Weigel, N. L., & Zhang, Y. (1998) · Journal of Molecular Medicine · doi:10.1007/s001090050241 · Cited by 351 · see citing works
Willingham, S. B., Allen, I. C., Bergstralh, D. T., Brickey, W. J., Huang, M. T.-H., Taxman, D. J., Duncan, J. A., & Ting, J. P. ‐. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0900138 · Cited by 348 · see citing works
<i>Endometriosis and Infertility</i>: <i>Epidemiology and Evidence‐based Treatments</i>
Ozkan, S., Murk, W., & Arici, A. (2008) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1434.007 · Cited by 347 · see citing works
Promoter Methylation Regulates Estrogen Receptor 2 in Human Endometrium and Endometriosis1
Xue, Q., Lin, Z., Cheng, Y.-H., Huang, C.-C., Marsh, E., Yin, P., Milad, M. P., Confino, E., Reierstad, S., Innes, J., et al. (2007) · Biology of Reproduction · doi:10.1095/biolreprod.107.061804 · Cited by 346 · see citing works
Hatai, T., Matsuzawa, A., Inoshita, S., Mochida, Y., Kuroda, T., Sakamaki, K., Kuida, K., Yonehara, S., Ichijo, H., & Takeda, K. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003412200 · Cited by 332 · see citing works
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 307 · see citing works
A Novel Immortalized Human Endometrial Stromal Cell Line with Normal Progestational Response
Krikun, G., Mor, G., Alvero, A. B., Guller, S. M., Schatz, F., Sapi, E., Rahman, M. M., Caze, R., Qumsiyeh, M. Β., & Lockwood, C. J. (2004) · Endocrinology · doi:10.1210/en.2003-1606 · Cited by 285 · see citing works
Holoch, K., & Lessey, B. A. (2010) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0b013e3181db7d71 · Cited by 258 · see citing works
Compton, D. R., Sheng, S., Carlson, K. E., Rebacz, N. A., Lee, I. Y., Katzenellenbogen, B. S., & Katzenellenbogen, J. A. (2004) · Journal of Medicinal Chemistry · doi:10.1021/jm049631k · Cited by 184 · see citing works
Dual suppression of estrogenic and inflammatory activities for targeting of endometriosis
Zhao, Y., Gong, P., Chen, Y., Nwachukwu, J. C., Srinivasan, S., Ko, C., Bagchi, M. K., Taylor, R. N., Korach, K. S., Nettles, K. W., et al. (2015) · Science Translational Medicine · doi:10.1126/scitranslmed.3010626 · Cited by 170 · see citing works
Vanderschueren, D., Herck, E. V., Nijs, J., EDERVEEN, A. G. H., Coster, R. D., & Bouillon, R. (1997) · Endocrinology · doi:10.1210/endo.138.6.5216 · Cited by 151 · see citing works
Han, S. J., Hawkins, S. M., Begum, K., Jung, S. Y., Kovanci, E., Qin, J., Lydon, J. P., DeMayo, F. J., & O'Malley, B. W. (2012) · Nature Medicine · doi:10.1038/nm.2826 · Cited by 149 · see citing works
Self-citationWei, Q., Guo, P., Mu, K., Zhang, Y., Zhao, W., Huai, W., Qiu, Y., Li, T., Ma, X., Liu, Y., et al. (2015) · Laboratory Investigation · doi:10.1038/labinvest.2015.63 · Cited by 146 · see citing works
Burns, K. A., Rodriguez, K., Hewitt, S., Janardhan, K., Young, S., & Korach, K. (2012) · Endocrinology · doi:10.1210/en.2012-1294 · Cited by 143 · see citing works
Pellegrini, C., Gori, I., Achtari, C., Hornung, D., Chardonnens, E., Wunder, D. M., Fiche, M., & Canny, G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.06.056 · Cited by 139 · see citing works
Compton, D. R., Sheng, S., Carlson, K. E., Rebacz, N. A., Lee, I. Y., Katzenellenbogen, B. S., & Katzenellenbogen, J. A. (2005) · Journal of Medicinal Chemistry · doi:10.1021/jm058162z · Cited by 137 · see citing works
Estrogen Receptor Knockout Mice as a Model for Endocrine Research
Walker, V. R., & Korach, K. S. (2004) · ILAR Journal · doi:10.1093/ilar.45.4.455 · Cited by 128 · see citing works
Small Molecule Inhibition of the Steroid Receptor Coactivators, SRC-3 and SRC-1
Wang, Y., Lonard, D. M., Yu, Y., Chow, D., Palzkill, T. G., & O’Malley, B. W. (2011) · Molecular Endocrinology · doi:10.1210/me.2011-1222 · Cited by 121 · see citing works
Self-citationIncreased Production of 17β-Estradiol in Endometriosis Lesions Is the Result of Impaired Metabolism
Delvoux, B., Groothuis, P. G., D’Hooghe, T. M., Kyama, C. M., Dunselman, G. A. J., & Romano, A. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-2218 · Cited by 120 · see citing works
Harris, H. A., Bruner‐Tran, K. L., Zhang, X., Osteen, K. G., & Lyttle, C. R. (2004) · Human Reproduction · doi:10.1093/humrep/deh711 · Cited by 119 · see citing works
Han, S. J., & O’Malley, B. W. (2014) · Human Reproduction Update · doi:10.1093/humupd/dmu002 · Cited by 98 · see citing works
Self-citationMonsivais, 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 · see citing works
Cao, W. G., Morin, M., Metz, C. N., Maheux, R., & Akoum, A. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.038331 · Cited by 91 · see citing works
17βE2 promotes cell proliferation in endometriosis by decreasing PTEN via NFκB-dependent pathway
Zhang, H., Ζhao, X., Liu, S., Li, J., Wen, Z., & Li, M. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.11.009 · Cited by 85 · see citing works
Cheng, C., Licence, D. R., Cook, E., Luo, F., Arends, M. J., Smith, S. K., Print, C. G., & Jones, D. S. (2011) · The Journal of Pathology · doi:10.1002/path.2852 · Cited by 63 · see citing works
Sillem, M., Prifti, S., Monga, B., Arslic‐Schmitt, T., & Runnebaum, B. (1999) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/s0301-2115(99)00114-1 · Cited by 56 · see citing works
Creation of immortalised epithelial cells from ovarian endometrioma
Bono, Y., Kyo, S., Takakura, M., Maida, Y., Mizumoto, Y., Nakamura, M., Nomura, K., Kiyono, T., & Inoue, M. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.26 · Cited by 55 · see citing works
Self-citationInvolvement of resistance to apoptosis in the pathogenesis of endometriosis.
Nasu, K., Yuge, A., Tsuno, A., Nishida, M., & Narahara, H. (2009) · PubMed · doi:10.14670/hh-24.1181 · Cited by 46 · see citing works
Acién, P., Velasco, I., Gutiérrez, M., & Martínez-Beltrán, M. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.11.188 · Cited by 41 · see citing works
The genetics and biochemistry of endometriosis
Burney, R. O. (2013) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0b013e3283630d56 · Cited by 34 · see citing works
Danazol and benign intracranial hypertension.
Shah, A. M., Roberts, T., McQueen, I. N., Graham, J., & Walker, K. (1987) · BMJ · doi:10.1136/bmj.294.6583.1323 · Cited by 27 · see citing works
Apoptosis Resistance in Endometriosis
Salmassi, A., Acar-Perk, B., Schmutzler, A. G., Koch, K., Püngel, F., Jonat, W., & Mettler, L. (2011) · Europe PMC (PubMed Central) · doi:10.5681/bi.2011.017 · Cited by 10 · see citing works
An estrogen receptor alpha activity indicator model in mice
Han, S. J., O’Malley, B. W., & DeMayo, F. J. (2009) · genesis · doi:10.1002/dvg.20572 · Cited by 9 · see citing works
Self-citationENDOMETRIOSIS AND RETROGRADE MENSTRUATION Case Report and Review
Hughesdon, P. E. (1958) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1958.tb08588.x · Cited by 7 · see citing works
Endometriosis and retrograde menstruation
Kruitwagen, R. F. P. M. (1991) · Radboud Repository (Radboud University) · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Zondervan, K. T., Becker, C. M., & Missmer, S. A. (2020) · New England Journal of Medicine · doi:10.1056/nejmra1810764 · Cited by 2,249 · see citing works
Zondervan, K. T., Becker, C. M., Koga, K., Missmer, S. A., Taylor, R. N., & Viganò, P. (2018) · Nature Reviews Disease Primers · doi:10.1038/s41572-018-0008-5 · Cited by 1,257 · see citing works
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 · see citing works
The Immunopathophysiology of Endometriosis
Symons, L. K., Miller, J. E., Kay, V. R., Marks, R. M., Liblik, K., Koti, M., & Tayade, C. (2018) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2018.07.004 · Cited by 583 · see citing works
Progesterone 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 510 · see citing works
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 492 · see citing works
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 466 · see citing works
Fertile ground: human endometrial programming and lessons in health and disease
Evans, J., Salamonsen, L. A., Winship, A., Menkhorst, E. M., Nie, G., Gargett, C. E., & Dimitriadis, E. (2016) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2016.116 · Cited by 371 · see citing works
Role 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 · see citing works
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 · see citing works
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 315 · see citing works
Nuclear receptors outside the nucleus: extranuclear signalling by steroid receptors
Levin, E. R., & Hammes, S. R. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.122 · Cited by 277 · see citing works
Estrogen-Receptor Expression and Function in Female Reproductive Disease
Tang, Z.-R., Zhang, R., Lian, Z., Deng, S., & Yu, K. (2019) · Cells · doi:10.3390/cells8101123 · Cited by 278 · see citing works
Endometriosis and nuclear receptors
Yilmaz, B. D., & Bulun, S. E. (2019) · Human Reproduction Update · doi:10.1093/humupd/dmz005 · Cited by 243 · see citing works
Estrogen Receptor Function: Impact on the Human Endometrium
Yu, K., Huang, Z., Xu, X.-L., Li, J., Fu, X., & Deng, S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.827724 · Cited by 236 · see citing works
Chadchan, S. B., Cheng, M., Parnell, L. A., Yin, Y., Schriefer, A. E., Mysorekar, I. U., & Kommagani, R. (2019) · Human Reproduction · doi:10.1093/humrep/dez041 · Cited by 202 · see citing works
Regulation 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 198 · see citing works
Intricate Connections between the Microbiota and Endometriosis
Jiang, I., Yong, P. J., Allaire, C., & Bedaiwy, M. A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22115644 · Cited by 188 · see citing works
Endometriosis: where are we and where are we going?
Greene, A. D., Lang, S. A., Kendziorski, J. A., Sroga-Rios, J. M., Herzog, T. J., & Burns, K. A. (2016) · Reproduction · doi:10.1530/rep-16-0052 · Cited by 187 · see citing works
Immune-inflammation gene signatures in endometriosis patients
Ahn, S. H., Khalaj, K., Young, S. L., Lessey, B. A., Koti, M., & Tayade, C. (2016) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.07.005 · Cited by 187 · see citing works
Immunological changes associated with adenomyosis: a systematic review
Bourdon, M., Santulli, P., Jeljeli, M. M., Vannuccini, S., Marcellin, L., Doridot, L., Petraglia, F., Batteux, F., & Chapron, C. (2020) · Human Reproduction Update · doi:10.1093/humupd/dmaa038 · Cited by 189 · see citing works
Donnez, J., & Dolmans, M.-M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10051085 · Cited by 182 · see citing works
Progesterone Actions and Resistance in Gynecological Disorders
MacLean, J. A., & Hayashi, K. (2022) · Cells · doi:10.3390/cells11040647 · Cited by 195 · see citing works
Muraoka, A., Suzuki, M. M., Hamaguchi, T., Watanabe, S., Iijima, K., Murofushi, Y., Shinjo, K., Osuka, S., Hariyama, Y., Ito, M., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.add1531 · Cited by 177 · see citing works
Self-citationMolecular and Cellular Pathogenesis of Endometriosis
Klemmt, P. A. B., & Starzinski‐Powitz, A. (2017) · Current Women s Health Reviews · doi:10.2174/1573404813666170306163448 · Cited by 175 · see citing works
Hung, S. W., Zhang, R., Tan, Z., Chung, J. P. W., Zhang, T., & Wang, C. C. (2021) · Medicinal Research Reviews · doi:10.1002/med.21802 · Cited by 171 · see citing works
Peritoneal immune microenvironment of endometriosis: Role and therapeutic perspectives
Chen, S., Liu, Y., Zhong, Z., Wei, C., Liu, Y., & Zhu, X. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1134663 · Cited by 172 · see citing works
Yang, H., Zhou, W., Chang, K., Mei, J., Huang, L., Wang, M., Meng, Y., Ha, S., Li, D., & Li, M. (2017) · Reproduction · doi:10.1530/rep-17-0342 · Cited by 145 · see citing works
Pathogenesis of Endometriosis: New Insights into Prospective Therapies
Kapoor, R., Stratopoulou, C. A., & Dolmans, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111700 · Cited by 144 · see citing works
Gou, Y., Li, X., Li, P., Zhang, H., Xu, T., Wang, H., Wang, B., Ma, X., Xue, J., & Zhang, Z. (2019) · Human Reproduction · doi:10.1093/humrep/dez019 · Cited by 133 · see citing works
Estrogen Receptor Beta (ERβ): A Ligand Activated Tumor Suppressor
Mal, R., Magner, A., David, J., Datta, J., Vallabhaneni, M., Kassem, M. A. M., Manouchehri, J. M., Willingham, N., Stover, D. G., VanDeusen, J. B., et al. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.587386 · Cited by 131 · see citing works
The role of estrogen receptor beta in breast cancer
Zhou, Y., & Liu, X. (2020) · Biomarker Research · doi:10.1186/s40364-020-00223-2 · Cited by 122 · see citing works
Can Endometriosis-Related Oxidative Stress Pave the Way for New Treatment Targets?
Cacciottola, L., Donnez, J., & Dolmans, M.-M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22137138 · Cited by 118 · see citing works
Endometrial stromal cell ferroptosis promotes angiogenesis in endometriosis
Li, G., Lin, Y., Zhang, Y., Gu, N.-H., Yang, B. X., Shan, S., Liu, N., Ouyang, J., Yang, Y., Sun, F., et al. (2022) · Cell Death Discovery · doi:10.1038/s41420-022-00821-z · Cited by 115 · see citing works
Nelson, A. W., Groen, A. J., Miller, J. L., Warren, A. Y., Holmes, K. A., Tarulli, G. A., Tilley, W. D., Katzenellenbogen, B. S., Hawse, J. R., Gnanapragasam, V. J., et al. (2016) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2016.11.016 · Cited by 116 · see citing works
Burns, K. A., Thomas, S. Y., Hamilton, K. J., Young, S. L., Cook, D. N., & Korach, K. S. (2017) · Endocrinology · doi:10.1210/en.2017-00562 · Cited by 115 · see citing works
The Role of Peritoneal Macrophages in Endometriosis
Ramírez-Pavez, T. N., Martinez‐Esparza, M., Ruiz‐Alcaraz, A. J., Marín‐Sánchez, P., Machado‐Linde, F., & García–Peñarrubia, P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms221910792 · Cited by 113 · see citing works
Gut microbiota–derived short-chain fatty acids protect against the progression of endometriosis
Chadchan, S. B., Popli, P., Ambati, C. R., Tycksen, E., Han, S. J., Bulun, S. E., Putluri, N., Biest, S. W., & Kommagani, R. (2021) · Life Science Alliance · doi:10.26508/lsa.202101224 · Cited by 116 · see citing works
Self-citationResearch advances in endometriosis-related signaling pathways: A review
Zhang, M., Xu, T., Tong, D., Li, S., Yu, X., Liu, B., Jiang, L., & Liu, K. (2023) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2023.114909 · Cited by 119 · see citing works
Effects of Estrogen on the Gastrointestinal Tract
Nie, X., Xie, R., & Tuo, B. (2018) · Digestive Diseases and Sciences · doi:10.1007/s10620-018-4939-1 · Cited by 106 · see citing works
Ovarian hormones-autophagy-immunity axis in menstruation and endometriosis
Shen, H., Zhang, T., Yang, H., Lai, Z., Zhou, W., Mei, J., Shi, J., Zhu, R., Xu, F., Li, D., et al. (2021) · Theranostics · doi:10.7150/thno.55241 · Cited by 107 · see citing works
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 103 · see citing works
Ma, J., Zhang, L., Zhan, H., Mo, Y., Ren, Z., Shao, A., & Lin, J. (2021) · Cell & Bioscience · doi:10.1186/s13578-021-00637-x · Cited by 104 · see citing works
Gou, Y., Wang, H., Wang, T., Wang, H., Wang, B., Jiao, N., Yu, Y., Cao, Y., Wang, H., & Zhang, Z. (2022) · Immunology · doi:10.1111/imm.13574 · Cited by 101 · see citing works
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 · see citing works
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 88 · see citing works
Villainous role of estrogen in macrophage-nerve interaction in endometriosis
Liang, Y., Xie, H., Wu, J., Liu, D., & Yao, S. (2018) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-018-0441-z · Cited by 87 · see citing works
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 · see citing works
Endometriosis-Associated Angiogenesis and Anti-angiogenic Therapy for Endometriosis
Chung, M. S., & Han, S. J. (2022) · Frontiers in Global Women s Health · doi:10.3389/fgwh.2022.856316 · Cited by 89 · see citing works
Self-citationPepe, G., Braga, D., Renzi, T. A., Villa, A., Bolego, C., D’Avila, F., Barlassina, C., Maggi, A., Locati, M., & Vegeto, E. (2017) · Scientific Reports · doi:10.1038/srep44270 · Cited by 80 · see citing works
Nuclear Receptors in the Control of the NLRP3 Inflammasome Pathway
Duez, H., & Pourcet, B. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.630536 · Cited by 80 · see citing works
Chen, M., Zhou, Y., Xu, H. A., Hill, C. N., Ewing, R. M., He, D., Zhang, X., & Wang, Y. (2020) · Scientific Reports · doi:10.1038/s41598-020-65606-9 · Cited by 78 · see citing works
Polyphenols as a Diet Therapy Concept for Endometriosis—Current Opinion and Future Perspectives
Gołąbek-Grenda, A., Kowalska, K., & Olejnik, A. M. (2021) · Nutrients · doi:10.3390/nu13041347 · Cited by 93 · see citing works
Innate immunity and the sensing of infection, damage and danger in the female genital tract
Sheldon, I. M., Owens, S. E., & Turner, M. L. (2016) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2016.07.002 · Cited by 79 · see citing works
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 · see citing works
Estradiol promotes EMT in endometriosis via MALAT1/miR200s sponge function
Du, Y., Zhang, Z., Xiong, W., Li, N., Liu, H., He, H., Li, Q., Liu, Y., & Zhang, L. (2018) · Reproduction · doi:10.1530/rep-18-0424 · Cited by 73 · see citing works
Genomic Function of Estrogen Receptor β in Endometriosis
Han, S. J., Lee, J. E., Cho, Y. J., Park, M. J., & O’Malley, B. W. (2019) · Endocrinology · doi:10.1210/en.2019-00442 · Cited by 73 · see citing works
Self-citationHeard, M. E., Melnyk, S. B., Simmen, F. A., Yang, Y., Pabona, J. M. P., & Simmen, R. C. M. (2016) · Endocrinology · doi:10.1210/en.2016-1092 · Cited by 71 · see citing works
The estrogen–macrophage interplay in the homeostasis of the female reproductive tract
Pepe, G., Locati, M., Torre, S. D., Mornata, F., Cignarella, A., Maggi, A. C., & Vegeto, E. (2018) · Human Reproduction Update · doi:10.1093/humupd/dmy026 · Cited by 72 · see citing works
Endometriosis and cardiovascular disease
Marchandot, B., Curtiaud, A., Matsushita, K., Trimaille, A., Host, A., Faller, É., Garbin, O., Akladios, C. Y., Jesel, L., & Morel, O. (2022) · European Heart Journal Open · doi:10.1093/ehjopen/oeac001 · Cited by 72 · see citing works
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 64 · see citing works
Interleukin-1/-33 Signaling Pathways as Therapeutic Targets for Endometriosis
Kato, T., Yasuda, K., Matsushita, K., Ishii, K. J., Hirota, S., Yoshimoto, T., & Shibahara, H. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.02021 · Cited by 61 · see citing works
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 · see citing works
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 · see citing works
Li, W.-N., Wu, M., & Tsai, S. (2020) · Reproduction · doi:10.1530/rep-20-0267 · Cited by 64 · see citing works
Self-citationZheng, W., Wu, J., Gu, J., Weng, H., Wang, J., Wang, T., Liang, X., & Cao, L. (2020) · Frontiers in Pharmacology · doi:10.3389/fphar.2020.00147 · Cited by 59 · see citing works
Structure, Function, and Evaluation of the Female Reproductive Tract
Lessey, B. A., & Young, S. L. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00009-3 · Cited by 58 · see citing works
Noncanonical farnesoid X receptor signaling inhibits apoptosis and impedes liver fibrosis
Wang, H., Ge, C., Zhou, J., Guo, Y., Cui, S., Huang, N., Yan, T., Cao, L., Che, Y., Zheng, Q., et al. (2018) · EBioMedicine · doi:10.1016/j.ebiom.2018.10.028 · Cited by 55 · see citing works
Nothnick, W. B., & Alali, Z. (2016) · F1000Research · doi:10.12688/f1000research.7504.1 · Cited by 55 · see citing works
Fusco, R., D’Amico, R., Cordaro, M., Gugliandolo, E., Siracusa, R., Peritore, A. F., Crupi, R., Impellizzeri, D., Cuzzocrea, S., & Paola, R. D. (2018) · Oncotarget · doi:10.18632/oncotarget.25823 · Cited by 53 · see citing works
Meng, X., Liu, J., Wang, H., Peng, C., & Wang, D. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110486 · Cited by 53 · see citing works
Geng, R., Huang, X., Li, L., Guo, X., Wang, Q., Zheng, Y., & Guo, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.1037504 · Cited by 54 · see citing works
Fan, W., Yuan, Z., Li, M., Zhang, Y., & Nan, F. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1226687 · Cited by 55 · see citing works
NLRP3 inflammasome activation by estrogen promotes the progression of human endometrial cancer
Liu, S.-G., Wu, X., Teng, H., Xin, X., Feng, D., Chi, S., Wang, X., & Wang, H. (2019) · OncoTargets and Therapy · doi:10.2147/ott.s218240 · Cited by 52 · see citing works
The Endometriotic Tumor Microenvironment in Ovarian Cancer
Wendel, J. R. H., Wang, X., & Hawkins, S. M. (2018) · Cancers · doi:10.3390/cancers10080261 · Cited by 51 · see citing works
Self-citationEffectiveness of NLRP3 Inhibitor as a Non-Hormonal Treatment for ovarian endometriosis
Murakami, M., Osuka, S., Muraoka, A., Hayashi, S., Bayasula, Kasahara, Y., Sonehara, R., Hariyama, Y., Shinjo, K., Tanaka, H., et al. (2022) · Reproductive Biology and Endocrinology · doi:10.1186/s12958-022-00924-3 · Cited by 49 · see citing works
Role of the gut microbiota in the pathogenesis of endometriosis: a review
Guo, C., & Zhang, C. (2024) · Frontiers in Microbiology · doi:10.3389/fmicb.2024.1363455 · Cited by 56 · see citing works
Brain inflammasomes in stroke and depressive disorders: Regulation by oestrogen
Slowik, A., Lammerding, L., Hoffmann, S., & Beyer, C. (2017) · Journal of Neuroendocrinology · doi:10.1111/jne.12482 · Cited by 49 · see citing works
Endometriosis as an immune-mediated disease: pathogenetic mechanisms and therapeutic strategies
Shifon, S., Викторовна, Т. Т., Veretel’nikova, T. V., Пасман, Н. М., & Chernykh, E. R. (2025) · Frontiers in Immunology · doi:10.3389/fimmu.2025.1727183 · Cited by 54 · see citing works
Reversal of fortune: estrogen receptor-β in endometriosis
Simmen, R. C. M., & Kelley, A. S. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0080 · Cited by 46 · see citing works
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 48 · see citing works
Self-citationLiao, 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 · see citing works
Ameliorative effects of luteolin against endometriosis progression in vitro and in vivo
Park, S., Lim, W., You, S., & Song, G. (2019) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2019.02.006 · Cited by 44 · see citing works
The gut microbiota: a double-edged sword in endometriosis
Talwar, C., Singh, V., & Kommagani, R. (2022) · Biology of Reproduction · doi:10.1093/biolre/ioac147 · Cited by 44 · see citing works
Pattern-recognition receptors in endometriosis: A narrative review
Guo, B., Chen, J. H., Zhang, J. H., Fang, Y., Liu, X. J., Zhang, J., Zhu, H. Q., & Zhan, L. (2023) · Frontiers in Immunology · doi:10.3389/fimmu.2023.1161606 · Cited by 43 · see citing works
Nicuolo, F. D., Castellani, R., Nardone, A. D. C., Barbaro, G., Paciullo, C., Pontecorvi, A., Scambia, G., & Simone, N. D. (2021) · Molecules · doi:10.3390/molecules26020288 · Cited by 42 · see citing works
Kobayashi, H., Kimura, M., Maruyama, S., Nagayasu, M., & Imanaka, S. (2020) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2020.12.044 · Cited by 40 · see citing works
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 41 · see citing works
Stephens, V. R., Rumph, J. T., Ameli, S., Bruner‐Tran, K. L., & Osteen, K. G. (2022) · Frontiers in Physiology · doi:10.3389/fphys.2021.807685 · Cited by 40 · see citing works
Understanding endometriosis from an immunomicroenvironmental perspective
Fan, D., Wang, X., Shi, Z., Jiang, Y., Zheng, B., Xu, L., & Zhou, S. (2023) · Chinese Medical Journal · doi:10.1097/cm9.0000000000002649 · Cited by 39 · see citing works
Pollution and endometriosis: A deep dive into the environmental impacts on women's health
Vallée, A., Ceccaldi, P., Carbonnel, M., Féki, A., & Ayoubi, J. (2023) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.17687 · Cited by 48 · see citing works
Effects of the gut microbiota and its metabolite short-chain fatty acids on endometriosis
Liu, M., Peng, R., Tian, C., Shi, J., Ma, J., Shi, R., Xiao, Q., Zhao, R., & Guan, H. (2024) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2024.1373004 · Cited by 39 · see citing works
Developmental Toxicant Exposure Is Associated with Transgenerational Adenomyosis in a Murine Model
Bruner‐Tran, K. L., Dulęba, A. J., Taylor, H. S., & Osteen, K. G. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.138370 · Cited by 39 · see citing works
Bufalin suppresses endometriosis progression by inducing pyroptosis and apoptosis
Cho, Y. J., Lee, J. E., Park, M. J., O’Malley, B. W., & Han, S. J. (2018) · Journal of Endocrinology · doi:10.1530/joe-17-0700 · Cited by 37 · see citing works
Self-citationCui, S., Hu, H.-J., Chen, A., Cui, M.-J., Pan, X., Zhang, P., Wang, G.-J., Wang, H., & Hao, H. (2022) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2022.08.019 · Cited by 39 · see citing works
Kowalczyk, W., Waliszczak, G., Jach, R., & Dulińska-Litewka, J. (2021) · Cancers · doi:10.3390/cancers13194779 · Cited by 37 · see citing works
Taylor, H. S., Dun, E. C., & Chwalisz, K. (2019) · Pain Management · doi:10.2217/pmt-2019-0010 · Cited by 38 · see citing works
Estrogen receptor β activation inhibits colitis by promoting NLRP6-mediated autophagy
Fan, W., Ding, C., Liu, S., Gao, X., Shen, X., Boevre, M. D., Gao, Z., Li, M., Zhang, S., Miao, Y., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111454 · Cited by 37 · see citing works
Vitamin D and reproductive disorders: a comprehensive review with a focus on endometriosis
Farhangnia, P., Noormohammadi, M., & Delbandi, A. (2024) · Reproductive Health · doi:10.1186/s12978-024-01797-y · Cited by 43 · see citing works
Endometriosis: An Immunologist’s Perspective
Garmendia, J. V., Sanctis, C. V. D., Hajdúch, M., & Sanctis, J. B. D. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26115193 · Cited by 48 · see citing works
- Authors
- 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., DeMayo, F. J., & O’Malley, B. W.
- Affiliations
- Baylor College of Medicine (US)
- Kanazawa University (JP)
- Corresponding author
- O’Malley, Bert W.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-11
- Volume
- 163
- Issue
- 4
- Pages
- 960-974
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4640214
- OpenAlex
- W2169528901
- Cited by
- 380
- References
- 51
- Citations by year
- 2026: 29 · 2025: 40 · 2024: 42 · 2023: 47 · 2022: 40 · 2021: 41 · 2020: 42 · 2019: 38 · 2018: 28 · 2017: 15 · 2016: 17 · 2015: 1
- FWCI
- 23.20
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Cancer Institute (P30CA123125)
- National Institute of Diabetes and Digestive and Kidney Diseases (U19 DK-62434, P01DK059820, U19DK062434)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54 HD-0077495, R01HD082786, R01HD07857, R01HD08188, U54HD007495, R01HD042311, R03HD077495, K12HD050128, R01HD008188, R01HD007857)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Keywords
- endometriosis, estrogen receptor beta, apoptosis, inflammasome, IL-1β, TNF-induced apoptosis, epithelial-mesenchymal transition, immune evasion, retrograde menstruation, ectopic lesions
- MeSH terms
- Animals, Cell Adhesion, Endometriosis, Female, Humans, Immunologic Surveillance, Menstruation, Tumor Necrosis Factor-alpha, Apoptosis, Estrogen Receptor alpha, Estrogen Receptor beta, Cell Proliferation, Mice, Interleukin-1beta, Inflammasomes
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