Changes in Eutopic Endometrial Gene Expression During the Progression of Experimental Endometriosis in the Baboon, Papio Anubis1
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Endometriosis is associated with aberrant gene expression in the eutopic endometrium of women with disease. To determine if the development of endometriotic lesions directly impacts eutopic endometrial gene expression, we sequentially analyzed the eutopic endometrium across the time course of disease progression in a baboon model of induced disease. Endometriosis was induced in baboons (n = 4) by intraperitoneal inoculation of autologous menstrual endometrium. Eutopic endometria were collected during the midsecretory phase (Days 9-11 postovulation) at 1, 3, 6-7, 10-12, and 15-16 mo after disease induction and compared with tissue from disease-free baboons. RNA was hybridized to Human Genome U133 Plus 2.0 Arrays, and data were extracted using Gene-Chip Operating Software. Subsequently, both Gene Set Enrichment Analysis and Ingenuity Pathways Analysis were used to find biological states that have a statistically significant enrichment concomitant with pairwise comparison of human endometriosis arrays. Within 1 mo of induction of the disease, 4331 genes were differentially expressed (P < 0.05). Hierarchical clustering revealed self-segregation into two groups-a) 1, 3, and 10-12 mo and b) 6-7 and 15-16 mo-together with controls. Clustering analysis at each stage of disease validated dysregulation of several signaling pathways, including Nodal-like receptor, EGF, ERK/MAPK, and PI3/AKT. Sequential analysis of the same animals during disease progression demonstrated an early disease insult and a transitory dominance of an estrogenic phenotype; however, as the disease progressed, a progesterone-resistant phenotype became evident. Furthermore, we demonstrate a 38.6% differential gene expression overlap with endometrial samples in the midsecretory phase from women with endometriosis, concomitant with similar dysregulation in human disease candidate genes Fos, Nodal, Suclg2, and Kras, among others. Molecular changes in the eutopic endometrium, associated with endometriosis, are directly impacted by endometriotic lesions, providing strong evidence that it is the disease rather than inherent defective endometrium that results in aberrant gene expression in the eutopic endometrium. Furthermore, this baboon model provides a powerful means whereby the early events associated with the pathology of disease and the resulting infertility may be elucidated.
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Using nonhuman primate models, it has been demonstrated that the presence of menstrual fragments in the peritoneal cavity directly influences gene expression pattern of the eutopic endometrium.
“Using nonhuman primate models of endometriosis, it has been demonstrated that it is the presence of the menstrual fragments in the peritoneal cavity that directly influences gene expression pattern of the eutopic endometrium (97,98).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [98]
The presence of endometriosis likely programs hyperestrogen responsiveness and progesterone resistance into the eutopic endometrium as disease progresses.
“Those studies hint at the ''cross-talk'' between the ectopic endometriotic foci and the eutopic endometrium, wherein the presence of endometriosis likely programs hyperestrogen responsiveness and progesterone resistance into the eutopic endometrium as disease progresses (98) (Fig. 1).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [98]
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- Authors
- Afshar, Y., Hastings, J., Roqueiro, D., Jeong, J.-W., Giudice, L. C., & Fazleabas, A. T.
- Affiliations
- Cedars-Sinai Medical Center (US)
- The Queen's Medical Research Institute (GB)
- University of Illinois Chicago (US)
- Michigan State University (US)
- University of California, San Francisco (US)
- Corresponding author
- Fazleabas, Asgerally T.
- ORCID
- Venue
- Biology of Reproduction
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-02-01
- Volume
- 88
- Issue
- 2
- Pages
- 44-44
- ISSN
- 0006-3363 (ISSN-L)
- 1529-7268
- PMC
- PMC3589234
- OpenAlex
- W2141020709
- Cited by
- 77
- References
- 68
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 5 · 2023: 6 · 2022: 4 · 2021: 2 · 2020: 4 · 2019: 6 · 2018: 7 · 2017: 8 · 2016: 10 · 2015: 9 · 2014: 7 · 2013: 4
- FWCI
- 12.12
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Biology of Reproduction (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- BioOne Complete (BioOne) (submittedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Institute of Child Health and Human Development (U54 HD 40093)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54 HD55764, U54HD055764, U54HD040093, U54-HD40093)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- endometriosis, eutopic endometrium, gene expression, disease progression, baboon model, Papio anubis, Nodal signaling, EGF signaling, ERK signaling, PI3K/Akt signaling, estrogen resistance, progesterone resistance, FOS, SUCLG2, KRAS
- MeSH terms
- Animals, Disease Models, Animal, Endometriosis, Endometrium, Epidermal Growth Factor, Female, Gene Expression Regulation, Humans, Time Factors, Signal Transduction, Disease Progression, Phosphatidylinositol 3-Kinases, Mitogen-Activated Protein Kinase Kinases, Extracellular Signal-Regulated MAP Kinases, Papio anubis, Oncogene Protein v-akt
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