Steroidogenic Enzyme and Key Decidualization Marker Dysregulation in Endometrial Stromal Cells from Women with Versus Without Endometriosis1

Aghajanova, L.; Hamilton, A.; Kwintkiewicz, J.; Vo, K.C.; Giudice, L.C.

doi:10.1095/biolreprod.108.070300

Cited by 169Endometriosis Research and TreatmentReproductive System and PregnancyEstrogen and related hormone effects

Steroidogenic Enzyme and Key Decidualization Marker Dysregulation in Endometrial Stromal Cells from Women with Versus Without Endometriosis1

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Aghajanova, L., Hamilton, A., Kwintkiewicz, J., Vo, K.C., Giudice, L.C.·2009·Biology of Reproduction

DOI 10.1095/biolreprod.108.070300PMC PMC2704986

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Abstract

Identification of mechanisms underlying endometriosis pathogenesis will facilitate understanding and treatment of infertility and pain associated with this disorder. Herein, we investigated the expression of steroidogenic pathway enzymes and key decidualization biomarkers in endometrial tissue and in eutopic endometrial stromal fibroblasts (hESFs) from women with vs. those without endometriosis, and subsequently treated in vitro with 8-bromo-cAMP (8-Br-cAMP) or progesterone (P4). Real-time quantitative PCR, immunohistochemistry, ELISA, and radiometric aromatase activity assay were used. The results demonstrate significantly increased (14.5-fold; P=0.037) expression of aromatase in eutopic endometrium of women with disease. In 8-Br-cAMP-treated hESF from eutopic endometrium of women with endometriosis, the balance in estradiol (E2) and P4 biosynthetic and metabolizing enzymes is disturbed (decreased HSD3B1 and HSD17B2, and increased HSD17B1 and aromatase), with the equilibrium being shifted towards an E2-enriched milieu. However, hESF from the same group of women treated with P4 did not demonstrate such responsiveness. Lower expression of IGFBP1 and prolactin mRNA and protein was observed in hESF from women with vs. those without endometriosis in response to 8-Br-cAMP, but not P4, suggesting a blunted response of these decidual biomarkers to activation of the PKA pathway in eutopic endometrium in women with disease. The dichotomy of 8-Br-cAMP regulation of select steroidogenic enzymes leading to an enriched E2 milieu within the endometrium and a blunted response of decidual biomarkers to this decidualizing agent of hESF from women with endometriosis suggests resistance to full decidualization of the stromal fibroblasts and mechanisms underlying implantation failure and the pathophysiology of this disorder.

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Hormone therapies that lower estradiol or act on progesterone reduce pain in women with endometriosis.
“The fact that hormonal treatments that reduce estradiol levels or influence progesterone alleviate pain in women with endometriosis supports the conclusion that estradiol contributes to pain symptoms and that progestogens may contribute to decreased symptoms (Fedele et al., 2008;Huang, 2008;Aghajanova et al., 2009).”
From Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications (2011) · cites this paper as Aghajanova et al., 2009
The Discussion (page unavailable in our copy) describes aromatase inhibitors as an alternative treatment for endometriosis-related pelvic pain, supporting the estradiol-lowering treatment part of the claim. It does not say that these treatments alleviate pain, nor does it report pain relief from treatments acting on progesterone; its progesterone findings concern stromal cells treated in vitro. (LLM, conf=0.84)
Experimental — accuracy not yet measured
Expression of P450 aromatase is increased in adenomyotic tissue and in ectopic and eutopic endometrium of women with endometriosis.
“The expression of the P450 aromatase is increased in adenomyotic tissue and in the ectopic and eutopic endometrium of women with endometriosis [35–41].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [40]
Similarity of molecular biology of TIAR in various tissues with that described in endometriosis strongly suggests that this represents the common underlying mechanisms of both processes.
“The similarity of the molecular biology of TIAR in various tissues with that described in endometriosis [39–41, 59–62] strongly suggests that this represents the common underlying mechanisms of both processes”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [40]

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DDE-Induced Changes in Aromatase Activity in Endometrial Stromal Cells in Culture
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Expression of 3b-Hydroxysteroid dehydrogenase and P450 side chain cleavage enzyme in the human uterine endometrium
Rhee, H. S., Oh, S. H., Ko, B. J., Han, D. M., Jeon, B. H., Park, H., Moon, H. B., & Kim, W. S. (2003) · Experimental & Molecular Medicine · doi:10.1038/emm.2003.22 · Cited by 28 · see citing works
Localization of type 1 17beta-hydroxysteroid dehydrogenase mRNA and protein in syncytiotrophoblasts and invasive cytotrophoblasts in the human term villi
Bonenfant, M., Pr, P., Drolet, R., & Tremblay, Y. (2000) · Journal of Endocrinology · doi:10.1677/joe.0.1650217 · Cited by 26 · see citing works
The effect of oral contraceptives on aromatase expression in the eutopic endometrium of patients with endometriosis
Maia, H., Casoy, J., Correia, T., Freitas, L., Pimentel, K., & Athayde, C. (2008) · Gynecological Endocrinology · doi:10.1080/09513590801890816 · Cited by 25 · see citing works
Mid-luteal endometrial intracrinology following controlled ovarian hyperstimulation involving use of a gonadotrophin releasing hormone antagonist
Vani, S., McDonald, S. E., Williams, A. R. W., Mason, J. I., Thong, K. J., & Critchley, H. (2007) · Human Reproduction · doi:10.1093/humrep/dem269 · Cited by 16 · see citing works
Androstenedione Up-Regulation of endometrial aromatase expression via local conversion to estrogen potential relevance to the pathogenesis of endometriosis
Bukulmez, O., Hardy, D., Carr, B., Auchus, R., Toloubeydokhti, T., Word, R., & Mendelson, C. (2009) · Obstetrical & Gynecological Survey · doi:10.1097/01.ogx.0000345377.28368.a5 · Cited by 2 · see citing works

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3 of the 78 references couldn’t be matched to a known paper.

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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 · see citing works
Cyclic Decidualization of the Human Endometrium in Reproductive Health and Failure
Gellersen, B., & Brosens, J. J. (2014) · Endocrine Reviews · doi:10.1210/er.2014-1045 · Cited by 1,149 · see citing works
Chronic pelvic pain and endometriosis: translational evidence of the relationship and implications
Stratton, P., & Berkley, K. J. (2011) · Human Reproduction Update · doi:10.1093/humupd/dmq050 · Cited by 442 · see citing works
The pathophysiology of endometriosis and adenomyosis, tissue injury and repair
Leyendecker, G., Wildt, L., & Mall, G. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-009-1191-0 · Cited by 418 · see citing works
“Other authors suggest that the endometrium in women with endometriosis is inherently altered [ 40 ].”
BackgroundResultInfluential
Endometriosis-associated infertility: From pathophysiology to tailored treatment
Bonavina, G., & Taylor, H. S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1020827 · Cited by 359 · see citing works
Endometrial receptivity in the eutopic endometrium of women with endometriosis: it is affected, and let me show you why
Lessey, B. A., & Kim, J. J. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.05.031 · Cited by 286 · see citing works
Functional MicroRNA Involved in Endometriosis
Hawkins, S. M., Creighton, C. J., Han, D. Y., Zariff, A., Anderson, M. L., Gunaratne, P. H., & Matzuk, M. M. (2011) · Molecular Endocrinology · doi:10.1210/me.2010-0371 · Cited by 264 · see citing works
MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis
Burney, R. O., Hamilton, A. E., Aghajanova, L., Vo, K. C., Nezhat, C. N., Lessey, B. A., & Giudice, L. C. (2009) · MHR: Basic science of reproductive medicine · doi:10.1093/molehr/gap068 · Cited by 254 · see citing works
Pathogenesis of endometriosis: Interaction between Endocrine and inflammatory pathways
Patel, B. G., Lenk, E. E., Lebovic, D. I., Shu, Y., Yu, J., & Taylor, R. N. (2018) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2018.01.006 · Cited by 195 · see citing works
Inflammatory pathways in endometrial disorders
Maybin, J. A., Critchley, H. O. D., & Jabbour, H. N. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2010.08.006 · Cited by 170 · see citing works
ARID1A Mutations and PI3K/AKT Pathway Alterations in Endometriosis and Endometriosis-Associated Ovarian Carcinomas
Samartzis, E. P., Noske, A., Dedes, K. J., Fink, D. A., & Imesch, P. (2013) · International Journal of Molecular Sciences · doi:10.3390/ijms140918824 · Cited by 172 · see citing works
Endometrial gene expression analysis at the time of embryo implantation in women with unexplained infertility
Altmäe, S., Martínez-Conejero, J. A., Salumets, A., Simón, C., Horcajadas, J. A., & Stavreus-Evers, A. C. (2009) · Molecular Human Reproduction · doi:10.1093/molehr/gap102 · Cited by 171 · see citing works
Endometrial biomarkers for the non-invasive diagnosis of endometriosis
Gupta, D., Hull, M. L., Fraser, I. S., Miller, L., Bossuyt, P. M., JOHNSON, N. P., & Nisenblat, V. (2016) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012165 · Cited by 174 · see citing works
Increased Activation of the PI3K/AKT Pathway Compromises Decidualization of Stromal Cells from Endometriosis
Yin, X., Pavone, M. E., Lu, Z., Wei, J., & Kim, J. J. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1527 · Cited by 171 · see citing works
Endometrial and endometriotic concentrations of estrone and estradiol are determined by local metabolism rather than circulating levels
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 · see citing works
Estrogen metabolism and action in endometriosis
Rižner, T. L. (2009) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2009.03.022 · Cited by 153 · see citing works
Progesterone Resistance in Endometriosis: an Acquired Property?
McKinnon, B. D., Mueller, M. D., & Montgomery, G. W. (2018) · Trends in Endocrinology and Metabolism · doi:10.1016/j.tem.2018.05.006 · Cited by 153 · see citing works
Molecular Evidence for Differences in Endometrium in Severe Versus Mild Endometriosis
Aghajanova, L., & Giudice, L. C. (2011) · Reproductive Sciences · doi:10.1177/1933719110386241 · Cited by 146 · see citing works
Self-citation
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Human Decidual Stromal Cells as a Component of the Implantation Niche and a Modulator of Maternal Immunity
Vinketova, К., Mourdjeva, M., & Oreshkova, T. (2016) · Journal of Pregnancy · doi:10.1155/2016/8689436 · Cited by 142 · see citing works
In vitro evidence that platelet-rich plasma stimulates cellular processes involved in endometrial regeneration
Aghajanova, L., Houshdaran, S., Balayan, S., Manvelyan, E., Irwin, J. C., Huddleston, H. G., & Giudice, L. C. (2018) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-018-1130-8 · Cited by 138 · see citing works
Self-citation
Thyroid-stimulating hormone receptor and thyroid hormone receptors are involved in human endometrial physiology
Aghajanova, L., Stavreus-Evers, A. C., Lindeberg, M., Landgren, B.-M., Sparre, L. S., & Hovatta, O. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2010.06.079 · Cited by 134 · see citing works
Self-citation
Risks of adverse pregnancy outcome in endometriosis
Brosens, I., Brosens, J. J., Fusi, L., Al-Sabbagh, M., Kuroda, K., & Benagiano, G. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.02.024 · Cited by 132 · see citing works
Endometrial stromal fibroblasts from women with polycystic ovary syndrome have impaired progesterone-mediated decidualization, aberrant cytokine profiles and promote enhanced immune cell migration in vitro
Piltonen, T. T., Chen, J. C., Khatun, M., Kangasniemi, M., Liakka, A., Spitzer, T., Tran, N., Huddleston, H., Irwin, J. C., & Giudice, L. C. (2015) · Human Reproduction · doi:10.1093/humrep/dev055 · Cited by 135 · see citing works
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Endometrial receptivity defects during IVF cycles with and without letrozole
Miller, P. B. W., Parnell, B. A., Bushnell, G., Tallman, N., Forstein, D. A., Higdon, H. L., Kitawaki, J., & Lessey, B. A. (2012) · Human Reproduction · doi:10.1093/humrep/der452 · Cited by 128 · see citing works
Impaired Down-Regulation of E-Cadherin and β-Catenin Protein Expression in Endometrial Epithelial Cells in the Mid-Secretory Endometrium of Infertile Patients with Endometriosis
Matsuzaki, S., Darcha, C., Maleysson, E., Canis, M. J., & Mage, G. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2713 · Cited by 116 · see citing works
Eutopic endometrium in women with endometriosis: ground zero for the study of implantation defects
Lessey, B., Lebovic, D., & Taylor, R. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1333476 · Cited by 113 · see citing works
Aberrant Endometrial DNA Methylome and Associated Gene Expression in Women with Endometriosis
Houshdaran, S., Nezhat, C. R., Vo, K. C., Zelenko, Z., Irwin, J. C., & Giudice, L. C. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.140434 · Cited by 113 · see citing works
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Comparative Transcriptome Analysis of Human Trophectoderm and Embryonic Stem Cell-Derived Trophoblasts Reveal Key Participants in Early Implantation1
Aghajanova, L., Shen, S., Rojas, A. M., Fisher, S. J., Irwin, J. C., & Giudice, L. C. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.092775 · Cited by 110 · see citing works
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Androgens and endometrium: new insights and new targets
Simitsidellis, I., Saunders, P. T. K., & Gibson, D. A. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2017.09.022 · Cited by 107 · see citing works
Abnormal activation of Ras/Raf/MAPK and RhoA/ROCKII signalling pathways in eutopic endometrial stromal cells of patients with endometriosis
Yotova, I., Quan, P., Leditznig, N., Beer, U., Wenzl, R. J., & Tschugguel, W. (2011) · Human Reproduction · doi:10.1093/humrep/der010 · Cited by 101 · see citing works
Unique Transcriptome, Pathways, and Networks in the Human Endometrial Fibroblast Response to Progesterone in Endometriosis
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 · see citing works
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Local remodeling of synthetic extracellular matrix microenvironments by co-cultured endometrial epithelial and stromal cells enables long-term dynamic physiological function
Cook, C. D., Hill, A. S., Guo, M. G., Stockdale, L., Papps, J. P., Isaacson, K., Lauffenburger, D. A., & Griffith, L. G. (2017) · Integrative Biology · doi:10.1039/c6ib00245e · Cited by 93 · see citing works
The Protein Kinase A Pathway-Regulated Transcriptome of Endometrial Stromal Fibroblasts Reveals Compromised Differentiation and Persistent Proliferative Potential in Endometriosis
Aghajanova, L., Horcajadas, J. A., Weeks, J. L., Esteban, F. J., NEZHAT, C. R., Conti, M., & Giudice, L. C. (2010) · Endocrinology · doi:10.1210/en.2009-0923 · Cited by 94 · see citing works
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Increased Mitogen-Activated Protein Kinase Kinase/Extracellularly Regulated Kinase Activity in Human Endometrial Stromal Fibroblasts of Women with Endometriosis Reduces 3′,5′-Cyclic Adenosine 5′-Monophosphate Inhibition of Cyclin D1
Velarde, M. C., Aghajanova, L., NEZHAT, C. R., & Giudice, L. C. (2009) · Endocrinology · doi:10.1210/en.2009-0389 · Cited by 92 · see citing works
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The Molecular and Cellular Mechanisms of Endometriosis: From Basic Pathophysiology to Clinical Implications
Mariadas, H., Chen, J.-H., & Chen, K.-H. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26062458 · Cited by 103 · see citing works
Absence of aromatase protein and mRNA expression in endometriosis
Colette, S., Lousse, J. C., Defrère, S., Curaba, M., Heilier, J.-F., Langendonckt, A. V., Mestdagt, M., Foidart, J. M., Loumaye, E., & Donnez, J. (2009) · Human Reproduction · doi:10.1093/humrep/dep199 · Cited by 86 · see citing works
The Progesterone Receptor Coactivator Hic-5 Is Involved in the Pathophysiology of Endometriosis
Aghajanova, L., Velarde, M. C., & Giudice, L. C. (2009) · Endocrinology · doi:10.1210/en.2009-0008 · Cited by 82 · see citing works
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The Bone Marrow-Derived Human Mesenchymal Stem Cell: Potential Progenitor of the Endometrial Stromal Fibroblast1
Aghajanova, L., Horcajadas, J. A., Esteban, F. J., & Giudice, L. C. (2010) · Biology of Reproduction · doi:10.1095/biolreprod.109.082867 · Cited by 83 · see citing works
Self-citation
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 80 · see citing works
Self-citation
Intra-tissue steroid profiling indicates differential progesterone and testosterone metabolism in the endometrium and endometriosis lesions
Huhtinen, K., Saloniemi-Heinonen, T., Keski-Rahkonen, P., Desai, R., Laajala, D., Ståhle, M., Häkkinen, M. R., Awosanya, M., Suvitie, P., Kujari, H., et al. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1913 · Cited by 75 · see citing works
Altered retinoid uptake and action contributes to cell survival in endometriosis
Pavone, M. E., Reierstad, S., Sun, H., Milad, M., Bulun, S. E., & Cheng, Y.-H. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-0459 · Cited by 74 · see citing works
Androgens, oestrogens and endometrium: a fine balance between perfection and pathology
Gibson, D. A., Simitsidellis, I., Collins, F., & Saunders, P. T. K. (2020) · Journal of Endocrinology · doi:10.1530/joe-20-0106 · Cited by 76 · see citing works
Pluripotent stem cell-derived endometrial stromal fibroblasts in a cyclic, hormone-responsive, coculture model of human decidua
Cheung, V. C., Peng, C., Marinić, M., Sakabe, N. J., Aneas, I., Lynch, V. J., Ober, C., Nóbrega, M. A., & Kessler, J. A. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109138 · Cited by 73 · see citing works
Physical therapy and psychological intervention normalize cortisol levels and improve vitality in women with endometriosis
Friggi Sebe Petrelluzzi, K., Garcia, M. C., Petta, C. A., Ribeiro, D. A., de Oliveira Monteiro, N. R., Céspedes, I. C., & Spadari, R. C. (2012) · Journal of Psychosomatic Obstetrics & Gynecology · doi:10.3109/0167482x.2012.729625 · Cited by 73 · see citing works
Angiogenesis lymphangiogenesis and neurogenesis in endometriosis
Hey‐Cunningham, A. J. (2013) · Frontiers in Bioscience-Elite · doi:10.2741/e682 · Cited by 68 · see citing works
Intracrine Regulation of Estrogen and Other Sex Steroid Levels in Endometrium and Non-gynecological Tissues; Pathology, Physiology, and Drug Discovery
Konings, G. F. J., Brentjens, L. S., Delvoux, B., Linnanen, T., Cornel, K. M. C., Koskimies, P., Bongers, M. Y., Kruitwagen, R. F. P. M., Xanthoulea, S., & Romano, A. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00940 · Cited by 65 · see citing works
Effects of BMAL1–SIRT1-positive cycle on estrogen synthesis in human ovarian granulosa cells: an implicative role of BMAL1 in PCOS
Zhang, J., Liu, J., Zhu, K., Hong, Y., Sun, Y. W., Zhao, X., Du, Y., & Chen, Z. (2016) · Endocrine · doi:10.1007/s12020-016-0961-2 · Cited by 62 · see citing works
Mucosal stromal fibroblasts markedly enhance HIV infection of CD4+ T cells
Neidleman, J. A., Chen, J. C., Kohgadai, N., Müller, J. A., Laustsen, A., Thavachelvam, K., Jang, K. S., Stürzel, C. M., Jones, J. J., Ochsenbauer, C., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006163 · Cited by 62 · see citing works
Self-citation
Clinical management of endometriosis‐associated infertility
Khine, Y. M., Taniguchi, F., & Harada, T. (2016) · Reproductive Medicine and Biology · doi:10.1007/s12522-016-0237-9 · Cited by 55 · see citing works
Progesterone Receptor B (PGR-B) Is Partially Methylated in Eutopic Endometrium From Infertile Women With Endometriosis
Rocha, C. V., Broi, M. G. D., Furtado, C. L. M., Navarro, P. A., Ferriani, R. A., & Meola, J. (2019) · Reproductive Sciences · doi:10.1177/1933719119828078 · Cited by 58 · see citing works
Transcriptome Analysis during Human Trophectoderm Specification Suggests New Roles of Metabolic and Epigenetic Genes
Assou, S., Boumela, I., Haouzi, D., Monzo, C., Déchaud, H., Kadoch, I.-J., & Hamamah, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039306 · Cited by 54 · see citing works
Transcriptome profiling of bovine inner cell mass and trophectoderm derived from in vivo generated blastocysts
Hosseini, S. M., Dufort, I., Caballero, J., Moulavi, F., Ghanaei, H., & Sirard, M. (2015) · BMC Developmental Biology · doi:10.1186/s12861-015-0096-3 · Cited by 54 · 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
Effect of bisphenol A on human endometrial stromal fibroblasts in vitro
Aghajanova, L., & Giudice, L. C. (2010) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2010.12.007 · Cited by 51 · see citing works
Self-citation
Reduced connexin 43 in eutopic endometrium and cultured endometrial stromal cells from subjects with endometriosis
Yu, J., Boicea, A., Barrett, K. L., James, C. O., Bagchi, I. C., Bagchi, M. K., Nezhat, C., Sidell, N., & Taylor, R. N. (2013) · Molecular Human Reproduction · doi:10.1093/molehr/gat087 · Cited by 47 · see citing works
Endometrial Intracrinology—Generation of an estrogen-dominated microenvironment in the secretory phase of women
Gibson, D. A., McInnes, K. J., Critchley, H. O. D., & Saunders, P. T. K. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2140 · Cited by 44 · see citing works
Inhibition of type 1 17β-hydroxysteroid dehydrogenase impairs the synthesis of 17β-estradiol in endometriosis lesions
Delvoux, B., D'Hooghe, T., Kyama, C., Koskimies, P., Hermans, R. J. J., Dunselman, G. A., & Romano, A. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2851 · Cited by 59 · see citing works
Influence of AKT on Progesterone Action in Endometrial Diseases
Lee, I. I., & Kim, J. J. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.119255 · Cited by 45 · see citing works
Pathogenesis of Endometriosis: Roles of Retinoids and Inflammatory Pathways
Kane, M. A., Sidell, N., & Taylor, R. N. (2015) · Seminars in Reproductive Medicine · doi:10.1055/s-0035-1554920 · Cited by 47 · see citing works
Regulation of androgen action during establishment of pregnancy
Gibson, D. A., Simitsidellis, I., & Saunders, P. T. K. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0027 · Cited by 42 · see citing works
Physiological and pathological implications of retinoid action in the endometrium
Jiang, Y., Chen, L., Taylor, R. N., Li, C., & Zhou, X. (2018) · Journal of Endocrinology · doi:10.1530/joe-17-0544 · Cited by 51 · see citing works
The Endometrial Response to Chorionic Gonadotropin Is Blunted in a Baboon Model of Endometriosis
Sherwin, J. R. A., Hastings, J. M., Jackson, K. S., Mavrogianis, P. A., Sharkey, A., & Fazleabas, A. T. (2010) · Endocrinology · doi:10.1210/en.2010-0275 · Cited by 43 · see citing works
Menstrual Effluent Provides a Novel Diagnostic Window on the Pathogenesis of Endometriosis
Nayyar, A., Saleem, M. I., Yilmaz, M., DeFranco, M., Klein, G., Elmaliki, K., Kowalsky, E., Chatterjee, P. K., Xue, X., Viswanathan, R., et al. (2020) · Frontiers in Reproductive Health · doi:10.3389/frph.2020.00003 · Cited by 42 · see citing works
Roles of Estrogen Receptor-α and the Coactivator MED1 During Human Endometrial Decidualization
Kaya-Okur, H. S., Das, A., Taylor, R. N., Bagchi, I. C., & Bagchi, M. K. (2016) · Molecular Endocrinology · doi:10.1210/me.2015-1274 · Cited by 42 · see citing works
Seminal plasma promotes decidualization of endometrial stromal fibroblasts in vitro from women with and without inflammatory disorders in a manner dependent on interleukin-11 signaling
George, A. F., Jang, K. S., Nyegaard, M., Neidleman, J. A., Spitzer, T., Xie, G., Chen, J. C., Herzig, E., Laustsen, A., de Menezes, E. G. M., et al. (2020) · Human Reproduction · doi:10.1093/humrep/deaa015 · Cited by 42 · see citing works
Self-citation
Metformin inhibits estradiol and progesterone-induced decidualization of endometrial stromal cells by regulating expression of progesterone receptor, cytokines and matrix metalloproteinases
Xiong, F., Xiao, J., Bai, Y., Zhang, Y., Li, Q., & Lishuang, X. (2018) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2018.10.128 · Cited by 41 · see citing works
Role of hydroxysteroid (17beta) dehydrogenase type 1 in reproductive tissues and hormone-dependent diseases
Heinosalo, T., Saarinen, N., & POUTANEN, M. H. (2018) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2018.08.004 · Cited by 40 · see citing works
Impaired CRH and Urocortin Expression and Function in Eutopic Endometrium of Women with Endometriosis
Novembri, R., Borges, L. E., Carrarelli, P., Rocha, A. L. L., De Pascalis, F., Florio, P., & Petraglia, F. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2263 · Cited by 38 · see citing works
Three-Dimensional Biofabrication Models of Endometriosis and the Endometriotic Microenvironment
Wendel, J. R. H., Wang, X., Smith, L. J., & Hawkins, S. M. (2020) · Biomedicines · doi:10.3390/biomedicines8110525 · Cited by 35 · see citing works
Archimetrosis: the evolution of a disease and its extant presentation
LEYENDECKER, G., Wildt, L., Laschke, M. W., & Mall, G. (2022) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-022-06597-y · Cited by 37 · see citing works
Expression Patterns of Progesterone Receptor Membrane Components 1 and 2 in Endometria From Women With and Without Endometriosis
Bunch, K. P., Tinnemore, D., Huff, S., Hoffer, Z. S., Burney, R. O., & Stallings, J. D. (2013) · Reproductive Sciences · doi:10.1177/1933719113492208 · Cited by 36 · 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
Cannabidiol (CBD) but not tetrahydrocannabinol (THC) dysregulate in vitro decidualization of human endometrial stromal cells by disruption of estrogen signaling
Almada, M., Amaral, C., de Oliveira, A. L. N., Fernandes, P. A., Ramos, M. J., Fonseca, B. M., Correia‐da‐Silva, G., & Teixeira, N. A. A. (2020) · Reproductive Toxicology · doi:10.1016/j.reprotox.2020.01.003 · Cited by 32 · see citing works
The human oviduct transcriptome reveals an anti-inflammatory, anti-angiogenic, secretory and matrix-stable environment during embryo transit
Hess, A. P., Talbi, S., Hamilton, A. E., Baston-Buest, D. M., Nyegaard, M., Irwin, J. C., Barragan, F., Krüssel, J.-S., Germeyer, A., & Giudice, L. C. (2013) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2013.06.013 · Cited by 31 · see citing works
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Altered differentiation of endometrial mesenchymal stromal fibroblasts is associated with endometriosis susceptibility
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Authors: Aghajanova, L., Hamilton, A., Kwintkiewicz, J., Vo, K. C., & Giudice, L. C.
Affiliations: University of California, San Francisco (US)
Corresponding author: Giudice, L.C.
ORCID: Aghajanova, L.
Vo, K.C.
Giudice, L.C.
Venue: Biology of Reproduction
Publisher: Oxford University Press (OUP)
Published: 2009-01-01
Volume: 80
Issue: 1
Pages: 105-114
ISSN: 0006-3363 (ISSN-L)
1529-7268
DOI: 10.1095/biolreprod.108.070300
PMC: PMC2704986
OpenAlex: W2103654313
Cited by: 168
References: 78
Citations by year: 2026: 5 · 2025: 7 · 2024: 3 · 2023: 5 · 2022: 9 · 2021: 6 · 2020: 11 · 2019: 8 · 2018: 13 · 2017: 11 · 2016: 10 · 2015: 7 · 2014: 8 · 2013: 12 · 2012: 11
FWCI: 16.27
Type: journal article
Language: en
Open access: green
europepmc.org
Locations: Biology of Reproduction (publishedVersion)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
BioOne Complete (BioOne) (submittedVersion)
Funders: Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD055764)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
Keywords: endometriosis, endometrial stromal fibroblasts, decidualization, steroidogenic enzymes, aromatase, estradiol, progesterone, 8-bromo-cAMP, protein kinase A, HSD3B1, HSD17B1, HSD17B2, IGFBP-1, prolactin, implantation failure, eutopic endometrium
MeSH terms: Adult, Aromatase, Decidua, Endometriosis, Endometrium, Enzyme-Linked Immunosorbent Assay, Estradiol, Estradiol Dehydrogenases, Female, Humans, Immunohistochemistry, Middle Aged, Progesterone, Prolactin, RNA, Messenger, 8-Bromo Cyclic Adenosine Monophosphate, Stromal Cells, Insulin-Like Growth Factor Binding Protein 1, Reverse Transcriptase Polymerase Chain Reaction, Young Adult

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Steroidogenic Enzyme and Key Decidualization Marker Dysregulation in Endometrial Stromal Cells from Women with Versus Without Endometriosis1

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