Cited by 209Endometriosis Research and TreatmentEctopic Pregnancy Diagnosis and ManagementEndometrial and Cervical Cancer Treatments

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Transcriptional Characterizations of Differences between Eutopic and Ectopic Endometrium

Wu, Yan, Kajdacsy-Balla, André, Strawn, Estil, Basir, Zainab, Halverson, Gloria, Jailwala, Parthav, Wang, Yuedong, Wang, Xujing, Ghosh, Soumitra, Guo, Sun-Wei·2006·Endocrinology

DOI 10.1210/en.2005-0426

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Abstract

Endometriosis, defined as the presence of endometrial glandular and stromal cells outside the uterine cavity, is a common gynecological disease with poorly understood pathogenesis. Using laser capture microdissection and a cDNA microarray with 9600 genes/expressed sequence tags (ESTs), we have conducted a comprehensive profiling of gene expression differences between the ectopic and eutopic endometrium taken from 12 women with endometriosis adjusted for menstrual phase and the location of the lesions. With dye-swapping and replicated arrays, we found 904 genes/ESTs that are differentially expressed. We validated the gene expression using real-time RT-PCR. We found that the expression patterns of these genes/ESTs correctly classified the 12 patients into ovarian and nonovarian endometriosis. We identified gene clusters that are location-specific. In addition, we identified several biological themes using Expression Analysis Systematic Explorer. Finally, we identified 79 pathways with over 100 genes with known functions, which include oxidative stress, focal adhesion, Wnt signaling, and MAPK signaling. The identification of these genes and their associated pathways provides new insight. Our findings will stimulate future investigations on molecular genetic mechanisms underlying the pathogenesis of endometriosis.

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Background
Priorities for Endometriosis Research: Recommendations From an International Consensus Workshop
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“…that many genes are deregulated in endometriosis (Carson et al., 2002; Arimoto et al., 2003; Kao et al., 2003; Matsuzaki et al., 2005; Wu et al., 2006a; Burney et al., 2007; Chand et al., 2007; Eyster et al., 2007; Flores et al., 2007; Hever et al., 2007; Konno et al., 2007; Mettler…”
Background
Endometrial receptivity in the eutopic endometrium of women with endometriosis: it is affected, and let me show you why
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The expression profile of micro-RNA in endometrium and endometriosis and the influence of ovarian steroids on their expression
Pan, Q., Luo, X., Toloubeydokhti, T., & Chegini, N. (2007) · Molecular Human Reproduction · doi:10.1093/molehr/gam063 · Cited by 261
“Conventional and recent large-scale gene expression studies have provided further evidence reflecting the molecular environments that differentiate normal endometrium from disorders affecting this tissue, including endometrial cancer, adenomyosis and endometriosis (Eyster et al., 2002; Kao et al., 2002; Riesewijk et a…”
Influential
Retracted
Role of oxidative stress in endometriosis
Gupta, S., Agarwal, A., Krajcir, N., & Alvarez, J. G. (2006) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)62026-3 · Cited by 240
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Self-citation
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“(52) profiled gene expression differences between Ahn et al.”
Background
Mechanisms of endometrial progesterone resistance
Al-Sabbagh, M., Lam, E. W.-F., & Brosens, J. J. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.035 · Cited by 183
“Progesterone resistance is also a hallmark of ectopic implants and probably plays a role in ovarian and tubal dysfunction associated with the endometriosis (Bulun, 2009; Wu et al., 2006a,b).”
Endometriosis and Ovarian Cancer
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“from the gene profiles can differentiate ectopic from eutopic endometria and classify different subtypes of endometrioses from the peritoneum and ovary (72).”
Background
Endometrial-Peritoneal Interactions during Endometriotic Lesion Establishment
Hull, M. L., Rangel‐Escareño, C., Godsland, J. M., Doig, J. R., Johnson, C. M., Phillips, S. C., Smith, S. K., Tavaré, S., Print, C. G., & Jones, D. S. (2008) · American Journal Of Pathology · doi:10.2353/ajpath.2008.071128 · Cited by 179
“In addition, laser capture microdissection of glandular epithelial cells from eutopic and ectopic sites identified differentially expressed transcripts associated with several biological processes in epithelial cells.(13) Taken together, these studies have identified large numbers of endometriosisassociated RNA transc…”
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“together with microarray data [64] advocate involvement of”
Background
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“Moreover, in the last few years, several papers based on microarray methods have shown differences in gene expression of MMP components, between normal and eutopic endometrium from women with endo- metriosis (Wu et al., 2006).”
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Background
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“Recent studies showed that the oxidative stress may be associated with the development of endometriosis: (1) women with endometriosis had increased levels of low-density lipoprotein (LDL) and HSP70b0 as well as decreased levels of paraoxonase-1 (PON-1) compared with controls [23]; (2) the concentrations of receptor fo…”
Background
Is it time for a paradigm shift in drug research and development in endometriosis/adenomyosis?
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“…Al‐Abed, Naccache, & Akoum, 2009; Carvalho, Podgaec, Bellodi‐Privato, Falcone, & Abrão, 2011; Dai, Leng, Lang, Li, & Zhang, 2012; Eyster, Klinkova, Kennedy, & Hansen, 2007; Honda, Barrueto, Gogusev, Im, &Morin, 2008; Hu, Tay, & Zhao, 2006; Hull et al., 2008; Mihalyi et al., 2010; Wu et al., 2006).”
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BackgroundInfluential
Transcriptional profiling of endometriosis tissues identifies genes related to organogenesis defects
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“To the best of our knowledge, very few studies compared ectopic and eutopic lesions analyzing only some of the different cell type contained in the lesion (Matsuzaki et al., 2006; Wu et al., 2006).”
Background
Dienogest inhibits BrdU uptake with G0/G1 arrest in cultured endometriotic stromal cells
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“Gene expression profiling has provided considerable evidence in support of altered expression of a number of genes in various endometrial disorders, including EN as compared to normal endometrium.(20-25) Accumulated evidence also suggests that miRNAs play a key regulatory function in gene expression stability through…”
Background
Retracted
Interaction between sex hormones and WNT/β-catenin signal transduction in endometrial physiology and disease
van der Horst, P. H., Wang, Y., van der Zee, M., Burger, C. W., & Blok, L. J. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.06.010 · Cited by 82
Obstetrical Complications in Women with Endometriosis: A Cohort Study in Japan
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Inhibition of METTL3/m6A/miR126 promotes the migration and invasion of endometrial stromal cells in endometriosis
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New concepts on the etiology of endometriosis
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Genome-wide expressions in autologous eutopic and ectopic endometrium of fertile women with endometriosis
Khan, M. A., Sengupta, J., Mittal, S., & Ghosh, D. (2012) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-10-84 · Cited by 68
“More over, it is notable that two types of endometriosis, namely ovarian endometriosis and peritoneal endometriosis reportedly show differential characteristics [4,9].”
Background
P-selectin as a potential therapeutic target for endometriosis
Guo, S., Ding, D., Geng, J.-G., Wang, L., & Liu, X. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.01.001 · Cited by 68
Hypoxia‐inhibited dual‐specificity phosphatase‐2 expression in endometriotic cells regulates cyclooxygenase‐2 expression
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“Elevation of activated ERK and MAPK signaling pathway were observed in endometriotic tissues of women with endometriosis [17, 18].”
Background
Aberrant gene expression profile in a mouse model of endometriosis mirrors that observed in women
Pelch, K. E., Schroder, A. L., Kimball, P. A., Sharpe-Timms, K. L., Davis, J., & Nagel, S. C. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.03.086 · Cited by 64
Genome-wide profiling of long noncoding ribonucleic acid expression patterns in ovarian endometriosis by microarray
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Adverse obstetrical outcomes for women with endometriosis and adenomyosis: A large cohort of the Japan Environment and Children’s Study
Harada, T., Taniguchi, F., Amano, H., Kurozawa, Y., Ideno, Y., Hayashi, K., Harada, T., & Japan Environment and Children’s Study Group (2019) · PLoS ONE · doi:10.1371/journal.pone.0220256 · Cited by 61
Cancer driver mutations in endometriosis: Variations on the major theme of fibrogenesis
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Genomic Alterations in Ectopic and Eutopic Endometria of Women with Endometriosis
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Differentially expressed genes in human endometrial endothelial cells derived from eutopic endometrium of patients with endometriosis compared with those from patients without endometriosis
Sha, G., Wu, D. T., Zhang, L., Chen, X., Lei, M., Sun, H., Lin, S., & Lang, J.-H. (2007) · Human Reproduction · doi:10.1093/humrep/dem266 · Cited by 58
“They have paid attention to epithelial and/or stromal compartments through laser capture microdissection or have used entire endometrial tissue without discriminating between the cellular compartments (Wu et al., 2006).”
Background
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 60
Bentamapimod (JNK Inhibitor AS602801) Induces Regression of Endometriotic Lesions in Animal Models
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Comparison of c-DNA microarray analysis of gene expression between eutopic endometrium and ectopic endometrium (endometriosis)
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COUP-TFII Regulates Human Endometrial Stromal Genes Involved in Inflammation
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A system-wide analysis of differentially expressed genes in ectopic and eutopic endometrium
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“…2003; Kao et al., 2003; Matsuzaki et al., 2004; Smith, 2004; Fan et al., 2005; Matsuzaki et al., 2005a; Matsuzaki et al., 2005b; Kato et al., 2006; Wu et al., 2006a), differing by focus, study design, microarray platform , quality control measure, data analysis, cell type used for RNA extraction,…”
BackgroundInfluential
Extracellularly Signal-Regulated Kinase Activity in the Human Endometrium: Possible Roles in the Pathogenesis of Endometriosis
Murk, W. K., Atabekoğlu, C. S., Çakmak, H., Heper, A. O., Ensarı, A., Kayisli, U. A., & Arici, A. M. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-2051 · Cited by 49
“This is consistent with microarray analyses reporting that genes activating the ERK1/2 MAPK signalingcascadeareup-regulatedinpatientswithendometriosis (21, 22 ).”
Result
Intracellular Wnt/Beta-Catenin Signaling Underlying 17beta-Estradiol-Induced Matrix Metalloproteinase 9 Expression in Human Endometriosis1
Zhang, L., Xiong, W., Xiong, Y., Liu, H., Li, N., Du, Y., & Liu, Y. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.115.135574 · Cited by 49
“Several studies have found that the aberrant activation of Wnt/β-catenin signaling may be involved in the pathophysiology of endometriosis [26-28].”
Background
Two unsuccessful clinical trials on endometriosis and a few lessons learned
Guo, S.-W., & Olive, D. L. (2007) · Gynecologic and Obstetric Investigation · doi:10.1159/000098413 · Cited by 49
Self-citation
Endometriotic stromal cells lose the ability to regulate cell-survival signaling in endometrial epithelial cells in vitro
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Laser capture microdissection and cDNA array analysis of endometrium identify CCL16 and CCL21 as epithelial-derived inflammatory mediators associated with endometriosis
Chand, A. L., Murray, A. S., Jones, R. L., Hannan, N. J., Salamonsen, L. A., & Rombauts, L. J. F. (2007) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-5-18 · Cited by 49
Potential mechanisms of postmenopausal endometriosis
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miR-29c is downregulated in the ectopic endometrium and exerts its effects on endometrial cell proliferation, apoptosis and invasion by targeting c-Jun
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Immunoreactivity of progesterone receptor isoform B and nuclear factor kappa-B as biomarkers for recurrence of ovarian endometriomas
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Background
Targeting the Wnt/β-catenin pathway in endometriosis: a potentially effective approach for treatment and prevention
Matsuzaki, S., Botchorishvili, R., Pouly, J. L., & Canis, M. J. (2014) · Molecular and Cellular Therapies · doi:10.1186/s40591-014-0036-9 · Cited by 43
“Several studies, including those from our laboratory, have suggested that aberrant activation of the Wnt/β-catenin pathway may be involved in the pathophysiology of endometriosis [2-9].”
Background
Laser-assisted microdissection for real-time PCR sample preparation
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Transcriptional expression of type-I interferon response genes and stability of housekeeping genes in the human endometrium and endometriosis
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“Previous studies of transcriptional levels in Eu versus Ec endometrium have used a single reference gene, such as GAPDH (Matsuzaki et al., 2006; Colette et al., 2009; Watanabe et al., 2009) and 18S (Wu et al., 2006; Lee et al., 2010).”
Novel estrogen-related genes and potential biomarkers of ovarian endometriosis identified by differential expression analysis.
Vouk, K., Šmuc, T., Guggenberger, C., Ribič-pucelj, M., Šinkovec, J., Husen, B., Thole, H., Houba, P. H. J., Thaete, C., Adamski, J., et al. (2011) · Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2011.03.010 · Cited by 40
Evolving Spectrum:
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Activated Platelets Induce Estrogen Receptor β Expression in Endometriotic Stromal Cells
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Identification of Susceptibility Genes for Peritoneal, Ovarian, and Deep Infiltrating Endometriosis Using a Pooled Sample-Based Genome-Wide Association Study
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“SUP, OMA, and DIE have different responsiveness to progesterone [18], differential gene expressions [19, 20], and specific putative variants that may influence one form and not the others [21– 23].”
Macrophages infiltrating endometriosis-like lesions exhibit progressive phenotype changes in a heterologous mouse model
Johan, M. Z., Ingman, W. V., Robertson, S. A., & Hull, M. L. (2019) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2019.01.002 · Cited by 35
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“There is now a wealth of data studying both individual genes and using microarray methods that show differences in gene expression between normal and eutopic endometrium from women with endometriosis (reviewed in Wu et al. 2006).”
Background
The Targeted Delivery of Interleukin 4 Inhibits Development of Endometriotic Lesions in a Mouse Model
Quattrone, F., Sanchez, A. M., Pannese, M., Hemmerle, T., Viganò, P., Candiani, M., Petraglia, F., Neri, D., & Panina‐Bordignon, P. (2015) · Reproductive Sciences · doi:10.1177/1933719115578930 · Cited by 34
Secreted frizzled-related protein 2 (SFRP2) expression promotes lesion proliferation via canonical WNT signaling and indicates lesion borders in extraovarian endometriosis
Heinosalo, T., Gabriel, M., Kallio, L., Adhikari, P. R., Huhtinen, K., Laajala, T. D., Kaikkonen, E., Mehmood, A., Suvitie, P. A., Kujari, H. P., et al. (2018) · Human Reproduction · doi:10.1093/humrep/dey026 · Cited by 36
“…tissues (Anastas and Moon, 2013), and there is evidence that WNT signaling also plays a role in the endometrium and endometrial diseases (Talbi et al., 2006; Wu et al., 2006; Eyster et al., 2007; Aghajanova et al., 2010; Matsuzaki et al., 2010; Matsuzaki and Darcha, 2013; Zhang et al., 2016a).”
Background
Glycemic Index, Glycemic Load, Fiber, and Gluten Intake and Risk of Laparoscopically Confirmed Endometriosis in Premenopausal Women
Schwartz, N. R. M., Afeiche, M. C., Terry, K. L., Farland, L. V., Chavarro, J. E., Missmer, S. A., & Harris, H. R. (2022) · Journal of Nutrition · doi:10.1093/jn/nxac107 · Cited by 39
Altered glycosylation in peri-implantation phase endometrium in women with stages III and IV endometriosis
Miller, D. L., Jones, C. J. P., Aplin, J., & Nardo, L. G. (2009) · Human Reproduction · doi:10.1093/humrep/dep401 · Cited by 34
“Differences in the methylation status of the progesterone receptor B-isoform (PR-B) promoter have been seen between eutopic endometrium and controls (Wu et al., 2006b) but these also did not reach statistical significance.”
Background
High-throughput mRNA sequencing of stromal cells from endometriomas and endometrium
Rekker, K., Saare, M., Eriste, E., Tasa, T., Kukuškina, V., Roost, A. M., Anderson, K. B., Samuel, K., Karro, H., Salumets, A., et al. (2017) · Reproduction · doi:10.1530/rep-17-0092 · Cited by 33
Differential Proteome Profiling of Eutopic Endometrium from Women with Endometriosis To Understand Etiology of Endometriosis
Rai, P., Kota, V., Deendayal, M., & Shivaji, S. (2010) · Journal of Proteome Research · doi:10.1021/pr100657s · Cited by 33
Role of Wnt signalling in early pregnancy
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The Endometriotic Tissue Lining the Internal Surface of Endometrioma: Hormonal, Genetic, Epigenetic Status, and Gene Expression Profile
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“Based on the statistical analysis that took into account lesion location and menstrual cycle, the genes identified include some ILs and their receptors (ie, IL-8, IL-15, and IL-15R), growth factors (platelet-derived growth factor b), and a member of the transforming growth factor (TGF) family (TGF-b3).(33)”
BackgroundMethodInfluential
Knockdown of prohibitin expression promotes glucose metabolism in eutopic endometrial stromal cells from women with endometriosis
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Background
Assessment of the proliferative status of epithelial cell types in the endometrium of young and menopausal transition women
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Method
Epithelial Cells of Deep Infiltrating Endometriosis Harbor Mutations in Cancer Driver Genes
Koppolu, A. A., Maksym, R., Paskal, W., Machnicki, M. M., Rak, B., Pępek, M., Garbicz, F., Pełka, K., Kuśmierczyk, Z., Jacko, J., et al. (2021) · Cells · doi:10.3390/cells10040749 · Cited by 28
“They suggested the importance of over seventy pathways with over one hundred genes involved in the disease pathogenesis [32].”
Background
A Functional Promoter Polymorphism in NFKB1 Increases Susceptibility to Endometriosis
Zhou, B., Rao, L., Peng, Y., Wang, Y., Qie, M., Zhang, Z., Song, Y., & Zhang, L. (2010) · DNA and Cell Biology · doi:10.1089/dna.2009.0992 · Cited by 27
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Metformin regulates stromal-epithelial cells communication via Wnt2/β-catenin signaling in endometriosis
Zhang, H., Xue, J., Li, M., Ζhao, X., Wei, D., & Li, C. (2015) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2015.06.011 · Cited by 27
“Aberrant Wnt2 expression (Wu et al., 2006) and abnormal activation of Wnt/b-catenin signaling (Matsuzaki et al.”

Authors: Wu, Y., Kajdacsy-Balla, A., Strawn, E., Basir, Z., Halverson, G., Jailwala, P., Wang, Y., Wang, X., Ghosh, S., & Guo, S.-W.
Affiliations: Medical College of Wisconsin (US)
Department of Pathology (A.K.-B.), University of Illinois, Chicago, Illinois 60612
University of California, Santa Barbara (US)
Corresponding author: Guo, Sun-Wei
ORCID: Wu, Yan
Jailwala, Parthav
Wang, Yuedong
Wang, Xujing
Ghosh, Soumitra
Guo, Sun-Wei
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2006-01-01
Volume: 147
Issue: 1
Pages: 232-246
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2005-0426
OpenAlex: W2032547793
Cited by: 208
References: 120
Citations by year: 2025: 4 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 4 · 2020: 7 · 2019: 12 · 2018: 14 · 2017: 11 · 2016: 8 · 2015: 11 · 2014: 13 · 2013: 11 · 2012: 12
FWCI: 13.72
Type: journal article
Language: en
Open access: closed
Locations: Endocrinology (publishedVersion)
PubMed (publishedVersion)
Funders: Medical College of Wisconsin
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Obstetrics and Gynecology › Ectopic Pregnancy Diagnosis and Management
Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
Keywords: endometriosis, ectopic endometrium, eutopic endometrium, gene expression profiling, differentially expressed genes, endometrioma, gene clusters, oxidative stress, focal adhesions, Wnt signaling, MAPK signaling, endometriosis pathogenesis
MeSH terms: Base Sequence, Endometrium, Female, Humans, Menstrual Cycle, Ovarian Diseases, Pregnancy, Pregnancy, Ectopic, Reference Values, Transcription, Genetic, DNA Primers, Reverse Transcriptase Polymerase Chain Reaction, Expressed Sequence Tags, Oligonucleotide Array Sequence Analysis

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Transcriptional Characterizations of Differences between Eutopic and Ectopic Endometrium

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