Global Gene Expression Analysis in Human Uterine Epithelial Cells Defines New Targets of Glucocorticoid and Estradiol Antagonism1
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In preparation for embryo implantation and pregnancy, the uterine epithelium undergoes a genomic and biological transition that mediates adhesion and invasion of the blastocyst. These events resemble an inflammatory response, and the immune system likely takes an active role in the establishment and maintenance of pregnancy. Although glucocorticoids are primary mediators of the immune system, the functional role of glucocorticoid signaling in the uterine epithelium is not well defined. To investigate the dynamic relationship between glucocorticoids and reproductive hormones, we performed whole-genome microarray analysis in a human uterine endometrial cancer cell line (ECC1 cells) treated with the synthetic glucocorticoid dexamethasone (Dex) alone or in combination with estradiol (E₂). Over 10,000 genes were significantly regulated in the presence of Dex and/or E₂. Surprisingly, unique targets of Dex and E₂ together represented the largest group of regulated genes. Ingenuity pathway analysis found both overlapping and independent regulated networks for each hormone. Several hundred genes were found to be coregulated by Dex and E₂, including several that were antagonistically regulated. The effects of glucocorticoids and E₂ are mediated primarily through the glucocorticoid receptor (NR3C1) and estrogen receptor (ESR1), respectively. In silico promoter analysis revealed that NR3C1 and ESR1 response elements are enriched in antagonistically regulated genes, and signaling through these receptors was required for antagonism. Glucocorticoid and E₂ antagonism of target genes may represent a critical junction between the immune system and female reproductive system. Moreover, identification and ontology analysis of glucocorticoid-regulated genes in a uterine epithelial-like cell line suggests that glucocorticoid signaling regulates important biological functions, including immune cell trafficking and embryonic development.
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Dexamethasone treatment uniquely regulates expression of genes in mouse uterus and human uterine cell lines with functions related to signaling, embryonic development, and cellular growth and proliferation.
“Dexamethasone treatment uniquely regulates the expression of genes in the mouse uterus and in human uterine cell lines with functions that are related to signaling, embryonic development, and cellular growth and proliferation [52,53,54]”
From Stress and the HPA Axis: Balancing Homeostasis and Fertility. (2017) · cites this paper as [52]
Cites
Gene regulation by steroid hormones
Beato, M. (1989) · Cell · doi:10.1016/0092-8674(89)90237-7 · Cited by 3,383 · see citing works
Boivin, J., Bunting, L., Collins, J. A., & Nygren, K. G. (2007) · Human Reproduction · doi:10.1093/humrep/dem046 · Cited by 2,437 · see citing works
JASPAR: an open-access database for eukaryotic transcription factor binding profiles
Sandelin, A. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh012 · Cited by 1,763 · see citing works
Regulatory T cells mediate maternal tolerance to the fetus
Aluvihare, V. R., Kallikourdis, M., & Betz, A. G. (2004) · Nature Immunology · doi:10.1038/ni1037 · Cited by 1,661 · see citing works
Roadmap to embryo implantation: clues from mouse models
Wang, H., & Dey, S. K. (2006) · Nature Reviews Genetics · doi:10.1038/nrg1808 · Cited by 1,302 · see citing works
(1991) · PubMed · Cited by 1,101 · see citing works
DNA binding of the glucocorticoid receptor is not essential for survival
Reichardt, H. M., Kaestner, K. H., Tuckermann, J., Kretz, O., Wessely, O., Bock, R., Gass, P., Schmid, W., Herrlich, P., Angel, P., et al. (1998) · Cell · doi:10.1016/s0092-8674(00)81183-6 · Cited by 1,068 · see citing works
Cole, T. J., Blendy, J. A., Monaghan, A. P., Krieglstein, K., Schmid, W., Aguzzi, A., Fantuzzi, G., Hummler, E., Unsicker, K., & Schütz, G. (1995) · Genes & Development · doi:10.1101/gad.9.13.1608 · Cited by 946 · see citing works
Bryne, J. C., Valen, E., Tang, M. E., Marstrand, T. T., Winther, O., da Piedade, I., Krogh, A., Lenhard, B., & Sandelin, A. (2007) · Nucleic Acids Research · doi:10.1093/nar/gkm955 · Cited by 692 · see citing works
Surjit, M., Ganti, K. P., Mukherji, A., Ye, T., Hua, G., Metzger, D., Li, M., & Chambon, P. (2011) · Cell · doi:10.1016/j.cell.2011.03.027 · Cited by 551 · cited 1× · see citing works
“Furthermore, the glucocorticoid receptor is able to mediate direct transcriptional repression through binding negative GRE sequences (nGREs), of which three nGRE sequences have been identified [41].”
BackgroundPearce, D., & Yamamoto, K. R. (1993) · Science · doi:10.1126/science.8382376 · Cited by 451 · see citing works
Sakai, D. D., Helms, S. R., Carlstedt‐Duke, J., Gustafsson, J.-Α., ROTTMAN, F. M., & Yamamoto, K. R. (1988) · Genes & Development · doi:10.1101/gad.2.9.1144 · Cited by 448 · see citing works
D'Adamio, F., Zollo, O., Moraca, R., Ayroldi, E., Bruscoli, S., Bartoli, A., Cannarile, L., Migliorati, G., & Riccardi, C. (1997) · Immunity · doi:10.1016/s1074-7613(00)80398-2 · Cited by 444 · see citing works
Left–right asymmetric expression of the TGFβ-family member lefty in mouse embryos
Meno, C., Saijoh, Y., Fujii, H., Ikeda, M., Yokoyama, T., Yokoyama, M., Toyoda, Y., & Hamada, H. (1996) · Nature · doi:10.1038/381151a0 · Cited by 437 · see citing works
Uterine DCs are crucial for decidua formation during embryo implantation in mice
Plaks, V., Birnberg, T., Berkutzki, T., Sela, S., BenYashar, A., Kalchenko, V., Mor, G., Keshet, E., Dekel, N., Neeman, M., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci36682 · Cited by 381 · see citing works
Busillo, J. M., & Cidlowski, J. A. (2013) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2012.11.005 · Cited by 339 · see citing works
Self-citationInterleukin-1 beta regulates human cytotrophoblast metalloproteinase activity and invasion in vitro.
Librach, C. L., Feigenbaum, S. L., Bass, K. E., Cui, T. Y., Verastas, N., Sadovsky, Y., Quigley, J. P., French, D. L., & Fisher, S. J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)32529-2 · Cited by 304 · see citing works
Seminal fluid signaling in the female reproductive tract: Lessons from rodents and pigs1
Robertson, S. A. (2007) · Journal of Animal Science · doi:10.2527/jas.2006-578 · Cited by 262 · see citing works
Apoptosis in endometrial glandular and stromal cells in women with and without endometriosis
Dmowski, W. P., Ding, J., Shen, J., Rana, N., Fernandez, B. B., & Braun, D. P. (2001) · Human Reproduction · doi:10.1093/humrep/16.9.1802 · Cited by 234 · see citing works
Robertson, S. A., Mayrhofer, G., & Seamark, R. F. (1992) · Biology of Reproduction · doi:10.1095/biolreprod46.6.1069 · Cited by 224 · see citing works
Quenby, S. M., Kalumbi, C., Bates, M. D., Farquharson, R. G., & Vince, G. (2005) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.05.012 · Cited by 220 · see citing works
Coactivation of GR and NFKB alters the repertoire of their binding sites and target genesPreprint
Rao, N., McCalman, M. T., Moulos, P., Françoijs, K., Chatziioannou, A. A., Kolisis, F. N., Alexis, Μ. N., Mitsiou, D. J., & Stunnenberg, H. G. (2011) · Genome Research · doi:10.1101/gr.118042.110 · Cited by 218 · see citing works
Glucocorticoids exert opposing effects on macrophage function dependent on their concentration
Lim, H., Müller, N., Herold, M. J., van den Brandt, J., & Reichardt, H. M. (2007) · Immunology · doi:10.1111/j.1365-2567.2007.02611.x · Cited by 218 · see citing works
Danilovich, N., Babu, P. S., Xing, W., Gerdes, M., Krishnamurthy, H., & Sairam, M. R. (2000) · Endocrinology · doi:10.1210/endo.141.11.7765 · Cited by 203 · see citing works
Robertson, S. A., Mau, V. J., Tremellen, K. P., & Seamark, R. F. (1996) · Reproduction · doi:10.1530/jrf.0.1070265 · Cited by 200 · see citing works
Fahey, J. V., Schaefer, T. M., Channon, J. Y., & Wira, C. R. (2005) · Human Reproduction · doi:10.1093/humrep/deh806 · Cited by 192 · see citing works
Peri-implantation glucocorticoid administration for assisted reproductive technology cycles
Boomsma, C. M., Keay, S. D., & Macklon, N. (2012) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd005996.pub3 · Cited by 176 · see citing works
Females Live Longer than Males: Role of Oxidative Stress
Viña, J., Gambini, J., López-Grueso, R., Abdelaziz, K. M., Jové, M., & Borrás, C. (2011) · Current Pharmaceutical Design · doi:10.2174/138161211798764942 · Cited by 170 · see citing works
Giles, K. M., Ross, K. A., Rossi, A. G., Hotchin, N. A., Haslett, C., & Dransfield, I. (2001) · The Journal of Immunology · doi:10.4049/jimmunol.167.2.976 · Cited by 165 · see citing works
Baxter, J. D., & Tomkins, G. M. (1970) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.65.3.709 · Cited by 163 · see citing works
Munck, A. U., & Koritz, S. B. (1962) · Biochimica et Biophysica Acta · doi:10.1016/0006-3002(62)91124-1 · Cited by 160 · see citing works
Microarray analysis of uterine gene expression in mouse and human pregnancy.
Bethin, K., Nagai, Y., Sladek, R., Asada, M., Sadovsky, Y., Hudson, T., & Muglia, L. (2003) · Molecular Endocrinology · doi:10.1210/me.2003-0007 · Cited by 146 · see citing works
The balance between cytotoxic NK cells and regulatory NK cells in human pregnancy
Saito, S., Nakashima, A., Subaru, M.-H., & Shiozaki, A. (2007) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2007.04.007 · Cited by 146 · see citing works
Dual Role for Glucocorticoids in Cardiomyocyte Hypertrophy and Apoptosis
Ren, R., Oakley, R. H., Cruz‐Topete, D., & Cidlowski, J. A. (2012) · Endocrinology · doi:10.1210/en.2012-1563 · Cited by 133 · see citing works
Self-citationSimón, C., Valbuena, D., Krüssel, J.-S., Bernal, A., Murphy, C. R., Shaw, T., Pellicer, A., & Polan, M. L. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00275-1 · Cited by 130 · see citing works
Inflammatory events in endometrial adenocarcinoma
Wallace, A. E., Gibson, D. A., Saunders, P. T. K., & Jabbour, H. N. (2010) · Journal of Endocrinology · doi:10.1677/joe-10-0072 · Cited by 128 · see citing works
Immune regulation of conception and embryo implantation—all about quality control?
Robertson, S. A. (2010) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2010.01.008 · Cited by 127 · see citing works
Glucocorticoid Receptors and the Role of Glucocorticoids in Fetal Lung Development
Ballard, P. L., & Ballard, R. A. (1972) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.69.9.2668 · Cited by 127 · see citing works
Mo, B., Vendrov, A. E., Palomino, W. A., DuPont, B. R., Apparao, K. B. C., & Lessey, B. A. (2006) · Biology of Reproduction · doi:10.1095/biolreprod.106.051870 · Cited by 111 · see citing works
Jacobs, A. L., Sehgal, P. B., Julian, J. A., & Carson, D. D. (1992) · Endocrinology · doi:10.1210/endo.131.3.1505448 · Cited by 107 · see citing works
Effect of Mineralo- and Glucocorticoids on Fasted Adrenalectomized Dogs Subjected to Electroshock.
Swingle, W. W., DaVanzo, J. P., GLENISTER, D. W., Wagle, G., Osborne, M., & Rowen, R. J. (1960) · Experimental Biology and Medicine · doi:10.3181/00379727-104-25773 · Cited by 102 · see citing works
Yates, F. E., Leeman, S. E., GLENISTER, D. W., & Dallman, M. F. (1961) · Endocrinology · doi:10.1210/endo-69-1-67 · Cited by 98 · see citing works
Rabin, D. S., Johnson, E. O., Brandon, D. D., Liapi, C. A., & Chrousos, G. P. (1990) · Biology of Reproduction · doi:10.1095/biolreprod42.1.74 · Cited by 98 · see citing works
Immunological responses to semen in the female genital tract
Schuberth, H., Taylor, U., Zerbe, H., Waberski, D., Hunter, R. H. F., & Rath, D. (2008) · Theriogenology · doi:10.1016/j.theriogenology.2008.07.020 · Cited by 93 · see citing works
Sanford, T. R., De, M., & Wood, G. W. (1992) · Reproduction · doi:10.1530/jrf.0.0940213 · Cited by 93 · see citing works
Cushingʼs Syndrome in Pregnancy
Pickard, J. A., Jochen, A., SADUR, C. N., & Hofeldt, F. D. (1990) · Obstetrical & Gynecological Survey · doi:10.1097/00006254-199002000-00002 · Cited by 84 · see citing works
The balance between cytotxic NK cells and regulatory NK cells in human pregnancy
滋, 齋. (2007) · Journal of Reproductive Immunology · Cited by 77 · see citing works
Ponce, C., Torres, M. J., Galleguillos, C., Hugo Sovino, S., Boric, M. A., Fuentes, A., & Johnson, M. C. (2009) · Reproduction · doi:10.1530/rep-08-0407 · Cited by 76 · see citing works
Role of Histamine in Implantation: Dexamethasone Inhibits Estradiol-Induced Implantation in the Rat1
Johnson, D. C., & Dey, S. K. (1980) · Biology of Reproduction · doi:10.1093/biolreprod/22.5.1136 · Cited by 74 · cited 1× · see citing works
“Exogenous administration of the synthetic glucocorticoid dexamethasone (Dex) in rats and mice blocks estrogen-induced uterine growth and differentiation, leading to diminished rates of embryo implantation [21–23].”
BackgroundCrocker, I. P., Barratt, S. L., Kaur, M., & Baker, P. N. (2001) · Placenta · doi:10.1053/plac.2001.0733 · Cited by 73 · see citing works
Ostrowski, M. C., Huang, A.-L., Kessel, M., Wolford, R. G., & Hager, G. L. (1984) · The EMBO Journal · doi:10.1002/j.1460-2075.1984.tb02064.x · Cited by 70 · see citing works
Grant‐Tschudy, K. S., & Wira, C. R. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.103.015495 · Cited by 69 · see citing works
Sherwin, J. R. A., Freeman, T. C., Stephens, R. J., Kimber, S., Smith, A. G., Chambers, I., Smith, S. K., & Sharkey, A. M. (2004) · Molecular Endocrinology · doi:10.1210/me.2004-0110 · Cited by 68 · see citing works
Pan, H., Zhu, L., Deng, Y., & Pollard, J. W. (2006) · Endocrinology · doi:10.1210/en.2006-0140 · Cited by 68 · see citing works
Sexuality and fertility in women with Addison's disease.
Erichsen, M. M., Husebye, E., Michelsen, T., Dahl, A., & Løvås, K. (2010) · Journal of Clinical Endocrinology and Metabolism · doi:10.1210/jc.2010-0445 · Cited by 66 · see citing works
Rhen, T., Grissom, S., Afshari, C., & Cidlowski, J. A. (2003) · The FASEB Journal · doi:10.1096/fj.02-1099com · Cited by 66 · see citing works
Self-citationRecent advances in medically assisted conception. Report of a WHO Scientific Group.
(1992) · PubMed · Cited by 65 · see citing works
Successful pregnancy outcome following 19 consecutive miscarriages: Case report
Quenby, S. M. (2003) · Human Reproduction · doi:10.1093/humrep/deg502 · Cited by 57 · see citing works
Hong, S., Nah, H. Y., Lee, J. Y., Gye, M. C., Kim, C. H., & Kim, M. K. (2004) · Journal of Endocrinology · doi:10.1677/joe.0.1810157 · Cited by 57 · see citing works
Velardo, J. T., Hisaw, F., & Bever, A. T. (1956) · Endocrinology · doi:10.1210/endo-59-2-165 · Cited by 56 · see citing works
Differential glucocorticoid effects on proliferation and invasion of human trophoblast cell lines
Mandl, M., Ghaffari‐Tabrizi‐Wizsy, N., Haas, J., Nöhammer, G., & Desoyé, G. (2006) · Reproduction · doi:10.1530/rep.1.00976 · Cited by 55 · see citing works
RNA‐binding motif protein 24 regulates myogenin expression and promotes myogenic differentiation
Jin, D., Hidaka, K., Shirai, M., & Morisaki, T. (2010) · Genes to Cells · doi:10.1111/j.1365-2443.2010.01446.x · Cited by 50 · see citing works
Rosen, T., Krikun, G., Ma, Y., Wang, E.-Y., Lockwood, C. J., & Guller, S. M. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.10.5151 · Cited by 50 · see citing works
Whirledge, S., & Cidlowski, J. A. (2013) · Endocrinology · doi:10.1210/en.2012-1748 · Cited by 50 · see citing works
Self-citationMarca, A. L., Artenisio, A. C., Stabile, G., Rivasi, F., & Volpe, A. (2005) · Gynecological Endocrinology · doi:10.1080/09513590500402756 · Cited by 49 · see citing works
Ma, Y., Ryu, J. S., Dulay, A. T., Segal, M., & Guller, S. M. (2002) · Placenta · doi:10.1053/plac.2002.0863 · Cited by 45 · see citing works
Watanabe, H., Nonoguchi, K., Sakurai, T., Masuda, T., Itoh, K., & Fujita, J. (2005) · Molecular Human Reproduction · doi:10.1093/molehr/gah186 · Cited by 38 · see citing works
Whirledge, S., Dixon, D., & Cidlowski, J. A. (2012) · Hormones and Cancer · doi:10.1007/s12672-012-0103-0 · Cited by 35 · see citing works
Self-citationUterine DCs are essential for pregnancy
Pollard, J. W. (2008) · Journal of Clinical Investigation · doi:10.1172/jci37733 · Cited by 35 · see citing works
Rhen, T., & Cidlowski, J. A. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.045336 · Cited by 35 · see citing works
Self-citationTang, M., Naidu, D. G., Hearing, P., Handwerger, S., & TABIBZADEH, S. S. (2010) · Endocrinology · doi:10.1210/en.2009-1081 · Cited by 33 · see citing works
Successful Uterine Steroid Therapy in a Case with a History of Ten Miscarriages
Ogasawara, M., & Aoki, K. (2000) · American Journal of Reproductive Immunology · doi:10.1111/j.8755-8920.2000.440411.x · Cited by 32 · see citing works
Hodrea, J., Majai, G. E., Doró, Z., Zahuczky, G., Pap, A., Rajnavölgyi, É., & Fésüs, L. (2011) · Journal of Leukocyte Biology · doi:10.1189/jlb.0511243 · Cited by 31 · see citing works
Shiokawa, S., Yoshimura, Y., Sawa, H., Nagamatsu, S., Hanashi, H., Sakai, K., Ando, M., & Nakamura, Y. (1999) · Biology of Reproduction · doi:10.1095/biolreprod60.6.1468 · Cited by 28 · see citing works
Jeyasuria, P., Subedi, K., Suresh, A., & Condon, J. C. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.091652 · Cited by 25 · see citing works
Herrera-Luna, C. V., Budik, S., & Aurich, C. (2012) · Reproduction in Domestic Animals · doi:10.1111/j.1439-0531.2012.01993.x · Cited by 24 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Stress and the HPA Axis: Balancing Homeostasis and Fertility.
Joseph, D., & Whirledge, S. (2017) · International journal of molecular sciences · doi:10.3390/ijms18102224 · Cited by 290 · see citing works
Self-citationA Role for Glucocorticoids in Stress-Impaired Reproduction: Beyond the Hypothalamus and Pituitary
Whirledge, S., & Cidlowski, J. A. (2013) · Endocrinology · doi:10.1210/en.2013-1652 · Cited by 209 · see citing works
Self-citationGlucocorticoids and reproduction: Traffic control on the road to reproduction
Whirledge, S., & Cidlowski, J. A. (2017) · Trends in Endocrinology & Metabolism · doi:10.1016/j.tem.2017.02.005 · Cited by 178 · see citing works
Self-citationWest-Szymanski, D. C., Pan, D., Tonsing-Carter, E. Y., Hernandez, K. M., Pierce, C. F., Styke, S. C., Bowie, K. R., Garcia, T. I., Kocherginsky, M., & Conzen, S. D. (2016) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-15-0433 · Cited by 123 · see citing works
Deak, T., Quinn, M., Cidlowski, J. A., Victoria, N. C., Murphy, A. Z., & Sheridan, J. F. (2015) · Stress · doi:10.3109/10253890.2015.1053451 · Cited by 102 · see citing works
Self-citationQuinn, M. A., Xu, X., Ronfani, M., & Cidlowski, J. A. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.02.041 · Cited by 98 · see citing works
Self-citationHuman Glucocorticoid Receptor β Regulates Gluconeogenesis and Inflammation in Mouse Liver
He, B., Cruz‐Topete, D., Oakley, R. H., Xiao, X., & Cidlowski, J. A. (2015) · Molecular and Cellular Biology · doi:10.1128/mcb.00908-15 · Cited by 64 · see citing works
Self-citationTransitioning from Basic toward Systems Pharmacodynamic Models: Lessons from Corticosteroids
Ayyar, V. S., & Jusko, W. J. (2020) · Pharmacological Reviews · doi:10.1124/pr.119.018101 · Cited by 58 · see citing works
Sex differences in chronic stress responses and Alzheimer's disease
Yan, Y., Dominguez, S., Fisher, D. W., & Dong, H. (2018) · Neurobiology of Stress · doi:10.1016/j.ynstr.2018.03.002 · Cited by 54 · see citing works
Boucher, J. G., Husain, M., Rowan‐Carroll, A., Williams, A., Yauk, C. L., & Atlas, E. (2014) · Obesity · doi:10.1002/oby.20848 · Cited by 50 · see citing works
Ruíz, D., Padmanabhan, V., & Sargis, R. M. (2020) · Journal of the Endocrine Society · doi:10.1210/jendso/bvaa087 · Cited by 44 · see citing works
Quinn, M. A., & Cidlowski, J. A. (2015) · The FASEB Journal · doi:10.1096/fj.15-278309 · Cited by 41 · see citing works
Self-citationAlofe, O., Kisanga, E. P., Inayat‐Hussain, S. H., Fukumura, M., García-Milian, R., Perera, L., Vasiliou, V., & Whirledge, S. (2019) · Environment International · doi:10.1016/j.envint.2019.104969 · Cited by 38 · see citing works
Self-citationCruz‐Topete, D., He, B., Xu, X., & Cidlowski, J. A. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.725903 · Cited by 37 · see citing works
Self-citationBhaumik, S., Lockett, J., Cuffe, J. S. M., & Clifton, V. L. (2023) · Biology · doi:10.3390/biology12081104 · Cited by 39 · see citing works
Prokai, D., & Berga, S. L. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17122147 · Cited by 36 · see citing works
Kisanga, E. P., Tang, Z., Guller, S. M., & Whirledge, S. (2018) · American Journal of Reproductive Immunology · doi:10.1111/aji.12974 · Cited by 32 · see citing works
Self-citationLi, Q., Li, L., Hou, G.-M., Wang, Z., Hou, Y., Liu, Z.-H., Schatten, H., & Sun, Q. (2018) · Human Reproduction · doi:10.1093/humrep/dey322 · Cited by 29 · see citing works
Ayyar, V. S., DuBois, D. C., Nakamura, T., Almon, R. R., & Jusko, W. J. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.257527 · Cited by 29 · see citing works
Psychological Stress and Functional Endometrial Disorders: Update of Mechanism Insights
Wu, J., Lin, S., & Kong, S. (2021) · Frontiers in Endocrinology · doi:10.3389/fendo.2021.690255 · Cited by 28 · see citing works
Zhang, D., Li, Y., Peng, H., Liu, H., Cheng, Q., Cheng, X. Y., Zeng, P., Wu, P., Chen, H., Huang, Y., et al. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.113.116384 · Cited by 21 · see citing works
Coons, L. A., Hewitt, S. C., Burkholder, A., McDonnell, D. P., & Korach, K. S. (2017) · Endocrinology · doi:10.1210/en.2017-00468 · Cited by 20 · see citing works
Genistein Disrupts Glucocorticoid Receptor Signaling in Human Uterine Endometrial Ishikawa Cells
Whirledge, S., Senbanjo, L. T., & Cidlowski, J. A. (2014) · Environmental Health Perspectives · doi:10.1289/ehp.1408437 · Cited by 20 · see citing works
Self-citationRuiz‐Conca, M., Gardela, J., Martinez-Serrano, C. A., Wright, D., López‐Béjar, M., Rodríguez‐Martínez, H., & Álvarez‐Rodríguez, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21124437 · Cited by 18 · see citing works
Whirledge, S., & Cidlowski, J. A. (2019) · Elsevier eBooks · doi:10.1016/b978-0-323-47912-7.00005-6 · Cited by 19 · see citing works
Self-citationWhirledge, S., Kisanga, E. P., Taylor, R. N., & Cidlowski, J. A. (2017) · Endocrinology · doi:10.1210/en.2017-00361 · Cited by 17 · see citing works
Self-citationKieffer, T. E. C., Chin, P. Y., Green, E. S., Moldenhauer, L. M., Prins, J. R., & Robertson, S. A. (2020) · Molecular Human Reproduction · doi:10.1093/molehr/gaaa019 · Cited by 17 · see citing works
Dumeige, L., Storey, C., Decourtye, L., Nehlich, M., Lhadj, C., Viengchareun, S., Kappeler, L., Lombès, M., & Martinerie, L. (2017) · International Journal of Molecular Sciences · doi:10.3390/ijms18020457 · Cited by 16 · see citing works
Ayyar, V. S., DuBois, D. C., Almon, R. R., & Jusko, W. J. (2019) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.119.257543 · Cited by 15 · see citing works
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Plant, M., Armstrong, C., Ruggiero, A. D., Sherrill, C., Uberseder, B., Jeffries, R., Nevarez, J., Jorgensen, M. J., Kavanagh, K., & Quinn, M. A. (2020) · GeroScience · doi:10.1007/s11357-020-00219-8 · Cited by 13 · see citing works
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Xu, J., Zhao, A., Xin, P., Geng, J., Wang, B., & Xia, T. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/3854117 · Cited by 12 · see citing works
Chromatin organization as an indicator of glucocorticoid induced natural killer cell dysfunction
Misale, M. S., Janusek, L. W., Tell, D., & Mathews, H. L. (2017) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2017.09.004 · Cited by 11 · see citing works
Quinn, M. A., McCalla, A., He, B., Xu, X., & Cidlowski, J. A. (2019) · Communications Biology · doi:10.1038/s42003-019-0344-3 · Cited by 11 · see citing works
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Ruiz-Zambrana, Á., & Berga, S. L. (2020) · Clinical Obstetrics & Gynecology · doi:10.1097/grf.0000000000000573 · Cited by 11 · see citing works
Baida, G. E., Agarwal, S., Readhead, B., Dudley, J. T., & Budunova, I. V. (2020) · Oncotarget · doi:10.18632/oncotarget.27445 · Cited by 7 · see citing works
Nanjappa, M. K., Medrano, T. I., Lydon, J. P., Bigsby, R. M., & Cooke, P. S. (2015) · Biology of Reproduction · doi:10.1095/biolreprod.114.123463 · Cited by 7 · see citing works
Neonatal Genistein Exposure and Glucocorticoid Signaling in the Adult Mouse Uterus
Whirledge, S., Kisanga, E. P., Oakley, R. H., & Cidlowski, J. A. (2018) · Environmental Health Perspectives · doi:10.1289/ehp1575 · Cited by 6 · see citing works
Self-citationKitawaki, Y., Horie, A., Ikeda, A., Shitanaka, S., Yanai, A., Ohara, T., Nakakita, B., Sagae, Y., Okunomiya, A., Tani, H., et al. (2024) · Cell Communication and Signaling · doi:10.1186/s12964-024-01904-3 · Cited by 3 · see citing works
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Dai, C., Lin, B., Xing, X., & Liu, J. S. (2020) · arXiv (Cornell University) · doi:10.48550/arxiv.2007.01237 · Cited by 3 · see citing works
Stress and Implantation Failure
Deaton, J. L., Patel, B., Johnston-MacAnanny, E. B., Yu, J., Whirledge, S., Wilson, A., Wininger, J. D., Shu, Y., Taylor, R. N., & Berga, S. L. (2017) · Springer eBooks · doi:10.1007/978-3-319-71967-2_7 · Cited by 1 · see citing works
Self-citationLi, R., & DeMayo, F. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-801238-3.64635-4 · Cited by 1 · see citing works
Li, R., & DeMayo, F. J. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-21477-6.00392-8
- Authors
- Whirledge, S., Xu, X., & Cidlowski, J. A.
- Affiliations
- National Institutes of Health (US)
- Corresponding author
- Cidlowski, John A.
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-09-01
- Volume
- 89
- Issue
- 3
- Pages
- 66-66
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- PMC
- PMC4435104
- OpenAlex
- W2125514335
- Cited by
- 44
- References
- 76
- Citations by year
- 2025: 1 · 2024: 1 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 8 · 2019: 7 · 2018: 5 · 2017: 8 · 2016: 3 · 2015: 4 · 2014: 3 · 2013: 1
- FWCI
- 2.43
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Biology of Reproduction (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- Funders
- National Institutes of Health
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- glucocorticoid signaling, estradiol, uterine epithelium, endometrium, dexamethasone, glucocorticoid receptor, estrogen receptor alpha, gene expression regulation, pregnancy establishment, embryonic development, immune cell trafficking
- MeSH terms
- Cells, Cultured, Dexamethasone, Epithelial Cells, Estradiol, Female, Gene Expression Regulation, Glucocorticoids, Humans, Uterus, Gene Expression Profiling, Microarray Analysis, Gene Regulatory Networks
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