Cited by 168Endometriosis Research and TreatmentEndometrial and Cervical Cancer TreatmentsEctopic Pregnancy Diagnosis and Management

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Molecular Classification of Endometriosis and Disease Stage Using High-Dimensional Genomic Data

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Tamaresis, John S., Irwin, Juan C., Goldfien, Gabriel A., Rabban, Joseph T., Burney, Richard O., Nezhat, Camran, DePaolo, Louis V., Giudice, Linda C.·2014·Endocrinology

DOI 10.1210/en.2014-1490PMC PMC4239429

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Abstract

Endometriosis (E), an estrogen-dependent, progesterone-resistant, inflammatory disorder, affects 10% of reproductive-age women. It is diagnosed and staged at surgery, resulting in an 11-year latency from symptom onset to diagnosis, underscoring the need for less invasive, less expensive approaches. Because the uterine lining (endometrium) in women with E has altered molecular profiles, we tested whether molecular classification of this tissue can distinguish and stage disease. We developed classifiers using genomic data from n = 148 archived endometrial samples from women with E or without E (normal controls or with other common uterine/pelvic pathologies) across the menstrual cycle and evaluated their performance on independent sample sets. Classifiers were trained separately on samples in specific hormonal milieu, using margin tree classification, and accuracies were scored on independent validation samples. Classification of samples from women with E or no E involved 2 binary decisions, each based on expression of specific genes. These first distinguished presence or absence of uterine/pelvic pathology and then no E from E, with the latter further classified according to severity (minimal/mild or moderate/severe). Best performing classifiers identified E with 90%-100% accuracy, were cycle phase-specific or independent, and used relatively few genes to determine disease and severity. Differential gene expression and pathway analyses revealed immune activation, altered steroid and thyroid hormone signaling/metabolism, and growth factor signaling in endometrium of women with E. Similar findings were observed with other disorders vs controls. Thus, classifier analysis of genomic data from endometrium can detect and stage pelvic E with high accuracy, dependent or independent of hormonal milieu. We propose that limited classifier candidate genes are of high value in developing diagnostics and identifying therapeutic targets. Discovery of endometrial molecular differences in the presence of E and other uterine/pelvic pathologies raises the broader biological question of their impact on the steroid hormone response and normal functions of this tissue.

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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
Retracted
Analyzing real-time PCR data by the comparative CT method
Schmittgen, T. D., & Livak, K. J. (2008) · Nature Protocols · doi:10.1038/nprot.2008.73 · Cited by 26,190
Linear Models and Empirical Bayes Methods for Assessing Differential Expression in Microarray Experiments
Smyth, G. K. (2004) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1027 · Cited by 11,829
Immunobiology: the immune system in health and disease
(1995) · Choice Reviews Online · doi:10.5860/choice.32-3876 · Cited by 4,111
Endometriosis
Giudice, L. C., & Kao, L. C. (2004) · The Lancet · doi:10.1016/s0140-6736(04)17403-5 · Cited by 3,166
Revised American Society for Reproductive Medicine classification of endometriosis: 1996
American Society for Reproductive Medicine (1997) · Fertility and Sterility · doi:10.1016/s0015-0282(97)81391-x · Cited by 3,018
Peritoneal endometriosis due to the menstrual dissemination of endometrial tissue into the peritoneal cavity
Sampson, J. A. (1927) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(15)30003-x · Cited by 2,334
Endometriosis
Giudice, L. C. (2010) · New England Journal of Medicine · doi:10.1056/nejmcp1000274 · Cited by 1,924
Endometriosis
Bulun, S. E. (2009) · New England Journal of Medicine · doi:10.1056/nejmra0804690 · Cited by 1,772
A Model-Based Background Adjustment for Oligonucleotide Expression Arrays
Wu, Z. J., Irizarry, R. A., Gentleman, R. C., Martínez-Murillo, F., & Spencer, F. A. (2004) · Journal of the American Statistical Association · doi:10.1198/016214504000000683 · Cited by 1,717

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Lin, K., Ma, J., Peng, Y., Sun, M., Xu, K., Wu, R., & Lin, J. (2019) · Scientific Reports · doi:10.1038/s41598-019-52741-1 · Cited by 18
Effects of noncavity-distorting fibroids on endometrial gene expression and function†
Aghajanova, L., Houshdaran, S., Irwin, J. C., & Giudice, L. C. (2017) · Biology of Reproduction · doi:10.1093/biolre/iox107 · Cited by 17
DNA methylation alterations—potential cause of endometriosis pathogenesis or a reflection of tissue heterogeneity?†
Saare, M., Krigul, K. L., Laisk, T., Ponandai‐Srinivasan, S., Rahmioğlu, N., Kumar, P. G. L., Zondervan, K. T., Salumets, A., & Peters, M. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy067 · Cited by 17
Aberrant reactive aldehyde detoxification by aldehyde dehydrogenase-2 influences endometriosis development and pain-associated behaviors
McAllister, S. L., Sinharoy, P., Vasu, M., & Gross, E. R. (2020) · Pain · doi:10.1097/j.pain.0000000000001949 · Cited by 17
Endometrial DNA damage response is modulated in endometriosis
Bane, K., Desouza, J., Shetty, D., Choudhary, P., Kadam, S., Katkam, R. R., Fernandes, G., Sawant, R., Dudhedia, U., Warty, N. R., et al. (2020) · Human Reproduction · doi:10.1093/humrep/deaa255 · Cited by 15
Histone H3K4me3 breadth in hypoxia reveals endometrial core functions and stress adaptation linked to endometriosis
Rytkönen, K. T., Faux, T., Mahmoudian, M., Heinosalo, T., Nnamani, M. C., Perheentupa, A. H., POUTANEN, M. H., Elo, L. L., & Wagner, G. P. (2022) · iScience · doi:10.1016/j.isci.2022.104235 · Cited by 14
Identification of key modules and candidate genes associated with endometriosis based on transcriptome data via bioinformatics analysis
Zheng, W., Xiang, D., Wen, D., Luo, M., Liang, X., & Cao, L. (2023) · Pathology - Research and Practice · doi:10.1016/j.prp.2023.154404 · Cited by 14
Puzzling Out the Genetic Architecture of Endometriosis: Whole-Exome Sequencing and Novel Candidate Gene Identification in a Deeply Clinically Characterised Cohort
Santin, A., Spedicati, B., Morgan, A., Lenarduzzi, S., Tesolin, P., Nardone, G. G., Mazzà, D., Lorenzo, G. D., Romano, F., Buonomo, F., et al. (2023) · Biomedicines · doi:10.3390/biomedicines11082122 · Cited by 14
In search for an ideal marker of endometrial receptivity: from histology to comprehensive molecular genetics-based approaches
Kibanov, M. V., Makhmudova, G. M., & Gokhberg, Y. A. (2019) · Almanac of Clinical Medicine · doi:10.18786/2072-0505-2019-47-005 · Cited by 14
Changes in Healthcare Spending After Diagnosis of Comorbidities Among Endometriosis Patients: A Difference-in-Differences Analysis
Epstein, A. J., Soliman, A. M., Davis, M. R., Johnson, S. J., Snabes, M. C., & Surrey, E. S. (2017) · Advances in Therapy · doi:10.1007/s12325-017-0630-8 · Cited by 13
Big Data: Challenge and Opportunity for Translational and Industrial Research in Healthcare
Rossi, R. L., & Grifantini, R. (2018) · Frontiers in Digital Humanities · doi:10.3389/fdigh.2018.00013 · Cited by 16
Circulating Endometrial Cells in Women with Spontaneous Pneumothorax
Kiss, I., Pospisilova, E., Kolostova, K., Maly, V., Stanek, I., Lischke, R., Schutzner, J., Pawlak, I., & Bobek, V. (2020) · Chest · doi:10.1016/j.chest.2019.09.008 · Cited by 12
Eutopic endometrium from women with endometriosis and chlamydial endometritis share immunological cell types and DNA repair imbalance: A transcriptome meta-analytical perspective
Poli‐Neto, O. B., Carlos, D., Favaretto, A. L., Silva, J. C. R. E., Meola, J., & Tiezzi, D. G. (2021) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2021.103307 · Cited by 13
SULFATION PATHWAYS: Contribution of intracrine oestrogens to the aetiology of endometriosis
Piccinato, C. D. A., Malvezzi, H., Gibson, D. A., & Saunders, P. T. K. (2018) · Journal of Molecular Endocrinology · doi:10.1530/jme-17-0297 · Cited by 12
Aberrant expression of epithelial leucine-rich repeat containing G protein–coupled receptor 5–positive cells in the eutopic endometrium in endometriosis and implications in deep-infiltrating endometriosis
Vallvé-Juanico, J., Suárez-Salvador, E., Castellví, J., Ballesteros, A., Taylor, H. S., Gil‐Moreno, A., & Santamaría, X. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.018 · Cited by 11
Five immune-related genes as diagnostic markers for endometriosis and their correlation with immune infiltration
Huang, Y., Li, Q., Hu, R. M., Li, R., & Yang, Y. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1011742 · Cited by 11
Characterizing the Extracellular Matrix Transcriptome of Endometriosis
Cook, C. J., Wiggin, N., & Fogg, K. C. (2023) · Reproductive Sciences · doi:10.1007/s43032-023-01359-w · Cited by 13
Type 2 17-β Hydroxysteroid Dehydrogenase as a Novel Target for the Treatment of Osteoporosis
Soubhye, J., Alard, I. C., Antwerpen, P. V., & Dufrasne, F. (2015) · Future Medicinal Chemistry · doi:10.4155/fmc.15.74 · Cited by 11
Increased FOXL2 expression alters uterine structures and functions†
Li, R., Wu, S., Zhou, L., Nicol, B., Lydon, J. P., Yao, H. H., & DeMayo, F. J. (2020) · Biology of Reproduction · doi:10.1093/biolre/ioaa143 · Cited by 11
Identification of a Novel Cuproptosis-Related Gene Signature in Eutopic Endometrium of Women with Endometriosis
Wei, J., Huang, B., Nong, Y., Zhang, Q., Liu, W., Xie, Y., Peng, T., Wang, W., Liang, X., Li, Q., et al. (2022) · Reproductive Sciences · doi:10.1007/s43032-022-01130-7 · Cited by 12
A review on menstrual health in adolescent girls emphasizing multi-omics and machine learning strategies for preventing reproductive tract infections
Ganguly, M., Ganguly, A., Chattaraj, S., & Midya, D. K. (2025) · Discover Public Health · doi:10.1186/s12982-025-00485-x · Cited by 16
Correlation Between the Clinical Parameters and Tissue Phenotype in Patients Affected by Deep-Infiltrating Endometriosis
VINCI, G., Arkwright, S., Audebourg, A., Radenen, B., Chapron, C., Borghese, B., Dousset, B. E., Méhats, C., Vaiman, D., Vacher‐Lavenu, M., et al. (2016) · Reproductive Sciences · doi:10.1177/1933719116638188 · Cited by 10
Hypersensitive intercellular responses of endometrial stromal cells drive invasion in endometriosis
Chen, C.-W., Chavez, J. B., Lin, L.-L., Wang, C., Hsu, Y., Hart, M. J., Ruan, J., Gillette, L., Burney, R. O., Schenken, R. S., et al. (2024) · eLife · doi:10.7554/elife.94778 · Cited by 8
Analysis of Gene Expression in the Endocervical Epithelium of Wonnen With Deep Endometriosis
Kopelman, A., Girão, M. J. B. C., Bonetti, T. C., de Carvalho, C. V., da Silva, I. D. C. G., & Schor, E. (2016) · Reproductive Sciences · doi:10.1177/1933719116638179 · Cited by 9
Genetic association study in a three-generation family with seven members with endometriosis
Matalliotakis, M., Zervou, M. I., Matalliotaki, C., Arici, A. M., Spandidos, D. A., Matalliotakis, I., & Goulielmos, G. N. (2017) · Molecular Medicine Reports · doi:10.3892/mmr.2017.7337 · Cited by 9
Molecular Biology of Endometriosis
Sengupta, J., Geethadevi, A., Bhat, M. A., & Ghosh, D. (2016) · Human Reproduction · doi:10.1002/9781118849613.ch3 · Cited by 10
Impaired pathogen-induced autophagy and increased IL-1β and TNFα release in response to pathogenic triggers in secretory phase endometrial stromal cells of endometriosis patients
Matsuzaki, S., Grémeau, A., & Pouly, J. L. (2020) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2020.06.011 · Cited by 10
OMICs Studies and Endometriosis Biomarker Identification
Saare, M., Peters, M., Aints, A., Laisk, T., Salumets, A., & Altmäe, S. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_12 · Cited by 8
Bioinformatics-based analysis of the roles of sex hormone receptors in endometriosis development
Zhao, X., Kong, W., Zhou, C., Deng, B., Zhang, H., Guo, H., Chen, S., & Pan, Z. (2023) · International Journal of Medical Sciences · doi:10.7150/ijms.79516 · Cited by 7
Transcriptomic changes in eutopic endometrium and ectopic lesions during endometriosis progression in a mouse model
Li, R., Tran, D. N., Lessey, B. A., Young, S. L., Kim, T. H., & Jeong, J. (2024) · F&S Science · doi:10.1016/j.xfss.2024.02.001 · Cited by 7
Are matrix metalloproteinases and their inhibitors reliable diagnosis biomarkers and attractive therapeutic targets in endometriosis?
Henriet, P., Mon, K. S., & Marbaix, É. (2016) · Metalloproteinases In Medicine · doi:10.2147/mnm.s102209 · Cited by 7

Authors: Tamaresis, J. S., Irwin, J. C., Goldfien, G. A., Rabban, J. T., Burney, R. O., Nezhat, C., DePaolo, L. V., & Giudice, L. C.
Affiliations: University of California, San Francisco (US)
Madigan Army Medical Center (US)
Stanford Medicine (US)
National Institutes of Health (US)
Corresponding author: Giudice, Linda C.
ORCID: Tamaresis, John S.
Irwin, Juan C.
Rabban, Joseph T.
Burney, Richard O.
Nezhat, Camran
Giudice, Linda C.
Venue: Endocrinology
Publisher: The Endocrine Society
Published: 2014-12-01
Volume: 155
Issue: 12
Pages: 4986-4999
ISSN: 0013-7227 (ISSN-L)
1945-7170
DOI: 10.1210/en.2014-1490
PMC: PMC4239429
OpenAlex: W2007347214
Cited by: 168
References: 58
Citations by year: 2026: 8 · 2025: 16 · 2024: 17 · 2023: 13 · 2022: 14 · 2021: 9 · 2020: 28 · 2019: 13 · 2018: 15 · 2017: 13 · 2016: 13 · 2015: 9
FWCI: 14.17
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Endocrinology (publishedVersion, cc-by-nc)
Europe PMC (PubMed Central) (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: University of Virginia
Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD055764, P50HD055764)
Topics: Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
Health Sciences › Medicine › Obstetrics and Gynecology › Endometrial and Cervical Cancer Treatments
Health Sciences › Medicine › Obstetrics and Gynecology › Ectopic Pregnancy Diagnosis and Management
Keywords: endometriosis, endometriosis staging, endometrium, molecular classification, gene expression classifier, menstrual cycle, immune activation, steroid hormone signaling, thyroid hormone signaling, growth factor signaling, uterine pathology, non-invasive diagnosis, differential gene expression
MeSH terms: Adult, Artificial Intelligence, Decision Trees, Endometriosis, Endometrium, Female, Humans, Menstrual Cycle, Middle Aged, Severity of Illness Index, Case-Control Studies, Gene Expression Profiling, Genomics, Molecular Diagnostic Techniques, Transcriptome

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Molecular Classification of Endometriosis and Disease Stage Using High-Dimensional Genomic Data

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