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MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis
Open accessAbstract
Endometriosis is a common gynecologic disorder characterized by pain and infertility. In addition to estrogen dependence, progesterone resistance is an emerging feature of this disorder. Specifically, a delayed transition from the proliferative to secretory phase as evidenced by dysregulation of progesterone target genes and maintenance of a proliferative molecular fingerprint in the early secretory endometrium (ESE) has been reported. MicroRNAs (miRNAs) are small noncoding RNAs that collectively represent a novel class of regulators of gene expression. In an effort to investigate further the observed progesterone resistance in the ESE of women with endometriosis, we conducted array-based, global miRNA profiling. We report distinct miRNA expression profiles in the ESE of women with versus without endometriosis in a subset of samples previously used in global gene expression analysis. Specifically, the miR-9 and miR-34 miRNA families evidenced dysregulation. Integration of the miRNA and gene expression profiles provides unique insights into the molecular basis of this enigmatic disorder and, possibly, the regulation of the proliferative phenotype during the early secretory phase of the menstrual cycle in affected women.
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“It is important to emphasize that the endometrium of women with endometriosis has been documented to respond differently to ovarian hormones (83-86), and we can use this fact to discover new potential biomarkers through minimally invasive means (87).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [85]
In the citing paper
“Equally important is the characteristic progesterone resistance of eutopic endometrium in women with moderate to severe endometriosis, where the unresponsiveness to progesterone results in incomplete transition of the endometrium from proliferative to early secretory phase of uterine cycle (85).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [85]
In the citing paper
“However, one limiting factor hindering the exploration of miRNA as biomarkers in clinical trials is the small sample sizes of patients and lack of representation of all stages of endometriosis, which are also stratified by menstrual stage (85, 109, 110).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [85]
In the citing paper
“Burney et al., based on their previous transcriptomics analysis (27) and with the use of computational analysis, discovered a potential functional relationship between decreased expression of miR-9 and miR-34 families in early secretoryphase eutopic endometrium of patients and their role in the delayed transition from proliferative to secretory phase in women with severe endometriosis (85).”
From Biomarkers in endometriosis: Challenges and opportunities (2017) · cites this paper as [85]
In the citing paper
“Though strengthened by the stringency of including only surgically documented presence or absence of advanced stage endometriosis, the study is limited by inclusion of control endometrium from women with coexisting intramural leiomyomata which could confound delineation of endometriosis-specific miRNA differences.”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [125]
In the citing paper
“In a parallel miRNA-mRNA array based comparison of three control early secretory phase endometrium (n = 3) with endometria from four women with moderate-severe endometriosis, six downregulated endometriosis associated miRNA were identified from the miR-9 and miR-34 miRNA families [125].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [125]
In the citing paper
“In contrast to studies comparing miRNA expression in eutopic versus ectopic endometrium, relatively few studies have compared miRNA expression in eutopic endometrium from women with and without surgically confirmed endometriosis [120, 125, 126].”
From Update on biomarkers for the detection of endometriosis (2015) · cites this paper as [125]
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Small RNA molecules in endometriosis: pathogenesis and therapeutic aspects
Yang, L., & Liu, H. Y. (2014) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2014.10.043 · Cited by 13
“endometrium (EUE) [17] miR-9 Early secretory endometrium (ESE) [16], serum [21]”
BackgroundWestern Herbal Medicine, Epigenetics, and Endometriosis
Stephens, L., Whitehouse, J. M., & Polley, M. J. (2013) · The Journal of Alternative and Complementary Medicine · doi:10.1089/acm.2012.0623 · Cited by 14
Preoperative assessment and diagnosis of endometriosis
Hirsch, M., & Davis, C. (2015) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000188 · Cited by 12
Diagnostic Value of Circulating MicroRNAs for Endometriosis: a Meta-analysis
Zhou, L., Chen, Y., Gao, J., Shankar, S., & Zhang, G. (2020) · Reproductive Sciences · doi:10.1007/s43032-019-00024-5 · Cited by 10
“MiR-21-5p was found to be one of the most differentially expressed miRNAs [16].”
BackgroundFrisendahl, C., Tang, Y., Boggavarapu, N. R., Peters, M., Lalitkumar, P. G., Piltonen, T., Arffman, R. K., Salumets, A., Götte, M., Korsching, E., et al. (2024) · Biomolecules · doi:10.3390/biom14111400 · Cited by 10
MicroRNAs and the pathogenesis of endometriosis
Neubauer, C., Kiesel, L., & Götte, M. (2012) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/je.2012.9226 · Cited by 10
Clinical markers of endometriosis: Have we been too quick to judge?
Toor, K. K., Wessels, J. M., Agarwal, S. K., Leyland, N. A., & Foster, W. G. (2014) · Medical Hypotheses · doi:10.1016/j.mehy.2014.02.007 · Cited by 10
“In recent years, nerve fiber density in the endometrium [32,33], concentrations of neurotrophins in the endometrium [34] or circulation [35], and measurement of microRNA (miRNA) in endometrial biopsies and endometriotic lesions [36,37] has been proposed as potentially useful diagnostic markers of endometriosis.”
Backgroundde Graaff, A. A., Delvoux, B., de Vijver, K. K. V., Kyama, C. M., D’Hooghe, T., Dunselman, G. A. J., & Romano, A. (2012) · Human Reproduction · doi:10.1093/humrep/des124 · Cited by 10
“Imbalances in the regulation of DNA methylation enzymes, methyl-CpG-binding domains (Borghese et al., 2010; van Kaam et al., 2011) and in the expression of microRNAs (Burney et al., 2009) have been recently shown.”
MicroRNA expression profiles and networks in CXCL12-stimulated human endometrial stromal cells
Mei, J., Li, M., Li, D., & Sun, H. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.5997 · Cited by 10
“Dysregulation of miRNAs leads to alterations in cellular differentiation, proliferation and apoptotic processes involved in the pathogenesis of endometriosis (8).”
Role of repressed microRNAs in endometriosis
Nasu, K., Aoyagi, Y., Zhu, R., Okamoto, M., Yano, M., Kai, K., & Kawano, Y. (2021) · Medical Molecular Morphology · doi:10.1007/s00795-021-00303-8 · Cited by 10
Liu, T., Xiao, L. Y., Pei, T., Luo, B., Tan, J., Long, Y., Huang, X. H., Ouyang, Y., & Huang, W. (2022) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.15526 · Cited by 9
“Previous reports have shown that aberrantly expressed miRNAs may stimulate the development of endometriosis.(27,28) Based on the results of our previous study, miR-297 was chosen as our target miRNA, which is a molecule that has two potential binding sites on the 30-UTR of PR.”
ResultMolecular Biology of Endometriosis
Sengupta, J., Geethadevi, A., Bhat, M. A., & Ghosh, D. (2016) · Human Reproduction · doi:10.1002/9781118849613.ch3 · Cited by 10
Arsalan, H. M., Mumtaz, H., & Laganà, A. S. (2025) · Advances in clinical chemistry · doi:10.1016/bs.acc.2025.01.004 · Cited by 10
Muharam, R., Febri, R. R., Mutia, K., Iffanolida, P. A., Maidarti, M., Wiweko, B., & Hestiantoro, A. (2023) · PubMed Central · doi:10.22074/ijfs.2022.543884.1233 · Cited by 8
“(12) evaluated miR-34c-5p, miR-34c-3p, miR-9 and miR-34b expression levels and found that expression of these miRNAs were downregulated in ectopic endometrium from women with endometriosis, compared to women without endometriosis.”
BackgroundTherapeutic Implication of miRNAs as an Active Regulatory Player in the Management of Pain: A Review
Hassan, M., Shahzadi, S., Yasir, M., Chun, W., & Kloczkowski, A. (2024) · Genes · doi:10.3390/genes15081003 · Cited by 9
Kiba, A., Banno, K., Yanokura, M., Asada, M., Nakayama, Y., Aoki, D., & Watanabe, T. (2016) · Journal of obstetrics and gynaecology research · doi:10.1111/jog.13137 · Cited by 9
Mariani, L. L., Mancarella, M., Fuso, L., Baino, S., Biglia, N., & Menato, G. (2020) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-020-05794-x · Cited by 9
Jaafar, S. O., Jaffar, J. O., Ibrahim, S. A., & Jarjees, K. K. (2022) · British Journal of Biomedical Science · doi:10.3389/bjbs.2021.10207 · Cited by 8
“Similarly, Burney and coworkers showed that in endometriosis cases different miRNAs including miR-34c-5p, miR-9, miR-34b are down regulated in comparison to healthy cases (21).”
BackgroundOMICs 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
Endometriosis: A new perspective on epigenetics and oxidative stress
Guan, Y., Chen, Y., Lin, R., Mo, T., Li, S., Cao, Y., Yin, T., Diao, L., & Li, Y. (2025) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2025.104462 · Cited by 7
Arosh, J. A., Sivakumar, K. K., Lee, J., & Banu, S. K. (2022) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2022.111728 · Cited by 7
Mezhlumova, N. A., Bobrov, М. Y., & Adamyan, L. V. (2018) · Russian Journal of Human Reproduction · doi:10.17116/repro201824061139 · Cited by 9
Abnormal Pathways in Endometriosis in Relation to Progesterone Resistance: A Review
Lode, L., Sveen, M. O., & Rudnicki, M. (2017) · Journal of Endometriosis and Pelvic Pain Disorders · doi:10.5301/jeppd.5000302 · Cited by 7
“This up-regulation was observed in the mid-secretory endometrium, which is the cycle phase displaying the peak circulating and endometrial tissue levels of P4, suggesting © 2017 Wichtig Publishing tAbLE I - Quality assessment of included studies (The Newcastle-Ottawa Scale) Selection comparability Exposure total score…”
BackgroundResultInfluentialThe Structure, Function, and Evaluation of the Female Reproductive Tract
Lessey, B. A., & Young, S. L. (2013) · Elsevier eBooks · doi:10.1016/b978-1-4557-2758-2.00010-x · Cited by 8
Promising therapeutic targets of endometriosis obtained from microRNA studies
Nasu, K., Aoyagi, Y., Zhu, R., Okamoto, M., Kai, K., & Kawano, Y. (2021) · Medical Molecular Morphology · doi:10.1007/s00795-021-00308-3 · Cited by 6
Viganò, P., Casalechi, M., Vercellini, P., & Somigliana, E. (2023) · Biomolecules · doi:10.3390/biom13040651 · Cited by 7
Testing the endometrium: is there enough evidence to justify clinical use?
Rahmati, M., & Macklon, N. (2020) · Current Opinion in Obstetrics & Gynecology · doi:10.1097/gco.0000000000000627 · Cited by 6
Diagnostic Value and Molecular Function of MicroRNAs in Endometrial Diseases: A Systematic Review
Kluz, N., Kowalczyk, E., Wasilewska, M., & Gil-Kulik, P. (2024) · Cancers · doi:10.3390/cancers16132416 · Cited by 6
“One of the regulatory targets of miR-9 is FOXP1, a gene that contains information about an anti-apoptotic protein known to be overexpressed in the endometrium of patients with the disease described in this chapter [29].”
BackgroundExploring the Role of MicroRNAs in Progesterone and Estrogen Receptor Expression in Endometriosis
Hon, J.-X., Wahab, N. A., Karim, A. K. A., Mokhtar, N. M., & Mokhtar, M. H. (2024) · Biomedicines · doi:10.3390/biomedicines12102218 · Cited by 7
Diagnostic accuracy of plasma microRNA as a potential biomarker for detection of endometriosis
Mohammadi, S. D., Moeini, A., Rastegar, T., Amidi, F., Saffari, M., Zhaeentan, S., Akhavan, S., Moradi, B., Heydarikhah, F., & Takzare, N. (2025) · Systems Biology in Reproductive Medicine · doi:10.1080/19396368.2025.2465268 · Cited by 6
“…show that circadian rhythms affect physiological processes (Rekker et al. 2015), as well as changes in the composition of the control group and the timing of sample collection in relation to the phases of a woman’s menstrual cycle (Burney et al. 2009; Teague et al. 2010; Petracco et al. 2019).”
mRNA and miRNA Biomarkers for Endometriosis
Aghajanova, L., Burney, R. O., Tran, N. D., & Giudice, L. C. (2017) · Springer eBooks · doi:10.1007/978-3-319-59856-7_9 · Cited by 7
Do MicroRNAs Modulate Visceral Pain?
Tao, Z.-Y., Yang, X. W., Li, J., Traub, R. J., & Cao, D. (2018) · BioMed Research International · doi:10.1155/2018/5406973 · Cited by 6
“An early clinical study showed that miR-9 and miR-34 families were downregulated in endometrial tissues of women with painful endometriosis, but the downstream genes of the miRNAs regulation were not determined [66].”
BackgroundHow Benign is Endometriosis: Multi-Scale Interrogation of Documented Evidence
Ghosh, D., Geethadevi, A., Bhat, M. A., Bharti, J. N., Mridha, A., Jb, S., Kk, R., & Sengupta, J. (2019) · Current Opinion in Gynecology and Obstetrics · doi:10.18314/cogo.v2i1.1840 · Cited by 6
“• miR-34 family: Dysregulated miR-34 has reportedly been associated with EE, ET and EAC, presumably due to its targets on transcript subnetworks toward regulation of cell proliferation, migration and invasion [181,182,184,185].”
BackgroundGeoffron, S., Legendre, G., Daraï, É., & Chabbert‐Buffet, N. (2017) · La Presse Médicale · doi:10.1016/j.lpm.2017.10.005 · Cited by 6
Muharam, R., Bowolaksono, A., Maidarti, M., Febri, R. R., Mutia, K., Iffanolida, P. A., Ikhsan, M., Sumapraja, K., Pratama, G., Harzif, A. K., et al. (2024) · International Journal of Women s Health · doi:10.2147/ijwh.s469864 · Cited by 5
“5 Several miRNAs are also involved in angiogenesis, cell adhesion, cell proliferation, and invasion.”
Background
Metadata
- Authors
- Burney, R. O., Hamilton, A. E., Aghajanova, L., Vo, K. C., Nezhat, C. N., Lessey, B. A., & Giudice, L. C.
- Affiliations
- Madigan Army Medical Center (US)
- University of California, San Francisco (US)
- Venue
- MHR: Basic science of reproductive medicine
- Publisher
- Oxford University Press (OUP)
- Published
- 2009-08-19
- Volume
- 15
- Issue
- 10
- Pages
- 625-631
- ISSN
- 1360-9947 (ISSN-L)
- 1460-2407
- PMC
- PMC2744474
- OpenAlex
- W2163150283
- Cited by
- 254
- References
- 27
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 11 · 2023: 12 · 2022: 13 · 2021: 15 · 2020: 22 · 2019: 15 · 2018: 21 · 2017: 19 · 2016: 20 · 2015: 18 · 2014: 15 · 2013: 20 · 2012: 12
- FWCI
- 17.27
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Molecular Human Reproduction (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (U54HD055764, U54HD035041, HD-35041-12)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › MicroRNA in disease regulation
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Keywords
- endometriosis, secretory endometrium, miRNA expression profiling, progesterone resistance, miR-9, miR-34, menstrual cycle, endometrial gene expression
- MeSH terms
- Adult, Endometriosis, Endometrium, Female, Humans, Middle Aged, Reverse Transcriptase Polymerase Chain Reaction, Oligonucleotide Array Sequence Analysis, MicroRNAs, Young Adult
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