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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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Citations
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“In addition, aberrant miRNA expression has been associated with human endometrial disorders such as endometriosis (Burney et al., 2009; Ohlsson Teague et al., 2009), endometrial hyperplasia and carcinoma (Cohn et al.”
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Fassbender, A., Burney, R. O., F. O, D., D’Hooghe, T., & Giudice, L. (2015) · BioMed Research International · doi:10.1155/2015/130854 · Cited by 195
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Wang, W.-T., Zhao, Y.-N., Han, B.-W., Hong, S.-J., & Chen, Y.-Q. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2415 · Cited by 193
“metriosis (27), and 50 miRNAs were confirmed to be dif-”
BackgroundEndometriosis and Ovarian Cancer
Wei, J., William, J., & Bulun, S. E. (2011) · International Journal of Gynecological Pathology · doi:10.1097/pgp.0b013e31821f4b85 · Cited by 176
Molecular and Cellular Pathogenesis of Endometriosis
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Plasma miR-17-5p, miR-20a and miR-22 are down-regulated in women with endometriosis
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“, 2008), progesterone resistance (Burney et al., 2009), cell invasion (Dai et al.”
BackgroundInfluentialEndometrial 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 179
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“In addition, the antiapoptotic protein BCL-2 is overexpressed in the eutopic endometrium of women with endometriosis (Burney et al., 2009; Burney and Giudice, 2012).”
InfluentialRecent insights on the genetics and epigenetics of endometriosis
Borghese, B., Zondervan, K. T., Abrão, M. S., Chapron, C., & Vaiman, D. (2016) · Clinical Genetics · doi:10.1111/cge.12897 · Cited by 167
“Ohlsson Teague (131) Ectopic vs eutopic SUP (N = 7) Array profiling miR-200a, miR-141, miR-200b, miR-142-3p, miR-424, miR-34c, miR-20a and miR-196b miR-145, miR-143, miR-99a, miR-99b, miR-126, miR-100, miR-125b, miR-150, miR-125a, miR-223, miR-194, miR-365, miR-29c and miR-1 Burney (132) Eutopic vs control Endo (N = 4…”
Non-coding RNAs in endometriosis: a narrative review
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“Array studies in the endometrium have demonstrated that aberrant miRNA expression is associated with benign gynaecological conditions, such as endometriosis (Burney et al., 2009; Ha, 2011; Zelenko et al., 2012), gynaecological malignancies (Gilabert-Estelles et al.”
BackgroundSelf-citationProgesterone 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
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“Women with endometriosis have a difference in the expression of two additional miRNA (members of the family miR-9 and miR-34) compared with women without endometriosis in the early secretory phase of the menstrual cycle, suggesting that several microRNA may be involved in endometrial receptivity (24).”
BackgroundYoo, J., Kim, T. H., Fazleabas, A. T., Palomino, W. A., Ahn, S. H., Tayade, C., Schammel, D. P., Young, S. L., Jeong, J., & Lessey, B. A. (2017) · Scientific Reports · doi:10.1038/s41598-017-04577-w · Cited by 140
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“Despite these variables, the following circulating miRNAs were found to be dysregulated in two or more studies: members of the let-7 family (let7a-f), miR-9, miR-20a, miR-122, miR-141, miR145, miR-199a, miR-342, miR-451a, and miR-3613 (Supplemental Table S1, [135]).”
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Progesterone Resistance in Endometriosis: Current Evidence and Putative Mechanisms
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“[71] conducted an array-based miRNA profiling in the early secretory endometrium of women with and without endom triosis and f und that miR-9 was significa tly downregulat d in patients with endometriosis compared with women it out endometriosis.”
BackgroundResultMicroRNA and gynecological reproductive diseases
Santamaría, X., & Taylor, H. S. (2014) · Fertility and Sterility · doi:10.1016/j.fertnstert.2014.04.044 · Cited by 123
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“Aberrant miRNA expression has been observed in the endometria of women with endometriosis (33, 34), and these changes may also be reflected in circulating miRNA levels.”
BackgroundmicroRNAs expression in endometriosis and their relation to angiogenic factors
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“…their significant regulatory influence on the expression of target genes involved in both physiologic and pathologic conditions (Ambros, 2004; Burney et al., 2009; Ohlsson-Teague et al., 2009, 2010; Kuokkanen et al., 2010). miRNA expression is cell-type-specific, with each miRNA…”
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“An earlier study demonstrated dysregulation of miR-9 and miR-34 miRNA families in eutopic, early secretory endometrial tissue from women with endometriosis.(33) The Table 5.”
BackgroundThe endocrine and paracrine control of menstruation
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Non-Coding RNAs in Endometrial Physiopathology
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“Burney et collaborators were among the first authors to publish the difference in expression profiles of miRNAs between eutopic endometrial tissues of woman with and without endometriosis [164].”
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miRNA Signature and Dicer Requirement during Human Endometrial Stromal Decidualization In Vitro
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“In a recent work [178], the same authors reported distinct miRNA expression profiles in the early secretory endometrium (ESE) of women with versus without endometriosis in a subset of samples previously used in global gene expression analysis.”
BackgroundAnalysis of Serum microRNA Profile by Solexa Sequencing in Women With Endometriosis
Wang, L., Huang, W., Ren, C., Zhao, M., Jiang, X., Fang, X., & Xia, X. (2016) · Reproductive Sciences · doi:10.1177/1933719116641761 · Cited by 89
“As for endometriosis, the significant roles of miRNAs in pathological processes have been revealed by several studies.(7) Currently, there are only a few reports that evaluate the clinical significance of circulating miRNAs in patients with endometriosis.”
BackgroundMüllerianosis: Four Developmental (Embryonic) Müllerian Diseases
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Joshi, N. R., Miyadahira, E. H., Afshar, Y., Jeong, J.-W., Young, S. L., Lessey, B. A., Serafini, P. C., & Fazleabas, A. T. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-2076 · Cited by 87
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“in the eutopic endometrium compared with normal endometrium [17].”
BackgroundHuman 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 81
“18 (Continued) 1126 Houshdaran et al Human Endometrial Methylome Mol Endocrinol, July 2014, 28(7):1118–1135”
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The role of micro-RNAs in the female reproductive tract
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Challenges in endometriosis miRNA studies — From tissue heterogeneity to disease specific miRNAs
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Diagnostic accuracy of serum miR‐122 and miR‐199a in women with endometriosis
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Genetics and Epigenetics of Infertility and Treatments on Outcomes
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Androgens, oestrogens and endometrium: a fine balance between perfection and pathology
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miRNAs Regulation and Its Role as Biomarkers in Endometriosis
Marí‐Alexandre, J., Sánchez-Izquierdo, D., Gilabert–Estellés, J., Barceló‐Molina, M., Braza‐Boïls, A., & Sandoval, J. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17010093 · Cited by 71
“As Figure 3 details, cell survival, matrix remodeling, proliferation, and angiogenesis are essential systems in the pathophysiology of this disease and all of them are potentially regulated by miRNAs [21,22,25,28,62].”
BackgroundLaudanski, P., Charkiewicz, R., Kuzmicki, M., Szamatowicz, J., Charkiewicz, A., & Niklinski, J. (2013) · Reproductive Biology and Endocrinology · doi:10.1186/1477-7827-11-78 · Cited by 70
“Although the miRNA expression profiles in the eutopic and ectopic endometrium from women with endometriosis have previously been revealed in a few independent studies [9,11], and it has been shown that these differences exist between the eutopic secretory endometrium of patients with and without endometriosis [12,13],…”
BackgroundTissue and circulating microRNA influence reproductive function in endometrial disease
Louise Hull, M., & Nisenblat, V. (2013) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2013.07.012 · Cited by 69
“In a comparison of three control mid-secretory-phase endometrium (n = 3) with endometria from four women with severe endometriosis (Burney et al., 2009), six down-regulated endometriosisassociated miRNA were identified from the miR-9 and miR-34 miRNA families.”
BackgroundMoga, M., Bălan, A., Dimienescu, O. G., Burtea, V., Dragomir, R. M., & Anastasiu, C. V. (2019) · Journal of Clinical Medicine · doi:10.3390/jcm8050735 · Cited by 67
“Burney, 2009 [107] Serum 4 cases of endometriosis and 3 controls Array profiling Down-regulated: miR-34c-3p, miR-9*, miR-34b*, miR-34c-5p, miR-9”
BackgroundMethodProgestin regulated miRNAs that mediate progesterone receptor action in breast cancer
Cochrane, D. R., Jacobsen, B. M., Connaghan, K. D., Howe, E. N., Bain, D. L., & Richer, J. K. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.12.020 · Cited by 68
“, 2010), as well as in disease states such as leiomyoma and endometriosis (Aghajanova and Giudice, 2011; Burney et al., 2009; Ohlsson Teague et al., 2009; Pan et al., 2008; Pan et al., 2007).”
BackgroundInside the Endometrial Cell Signaling Subway: Mind the Gap(s)
Makieva, S., Giacomini, E., Ottolina, J., Sanchez, A. M., Papaleo, E., & Viganò, P. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19092477 · Cited by 65
“Since their discovery in the physiological and pathological endometrium, miRNAs have been mostly investigated in luteal phase [57,58].”
BackgroundPateisky, P., Pils, D., Szabo, L., Kuessel, L., Husslein, H., Schmitz, A. A. P., Wenzl, R. J., & Yotova, I. (2018) · Reproductive BioMedicine Online · doi:10.1016/j.rbmo.2018.05.007 · Cited by 61
Forte, A., Cipollaro, M., & Galderisi, U. (2013) · Clinical Science · doi:10.1042/cs20130099 · Cited by 63
Ponsuksili, S., Tesfaye, D., Schellander, K., Hoelker, M., Hadlich, F., Schwerin, M., & Wimmers, K. (2014) · Biology of Reproduction · doi:10.1095/biolreprod.114.121392 · Cited by 64
“In addition, aberrant miRNA expression is associated with human endometrial disorders, such as endometriosis [15, 16], endometrial hyperplasia, and carcinoma [17], and previous studies have reported miRNA-regulated molecular pathways that are likely to contribute to defects in endometrial receptivity in humans [18].”
BackgroundThe known, the unknown and the future of the pathophysiology of endometriosis
Ochoa Bernal, M. A., & Fazleabas, A. T. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115815 · Cited by 59
“Abnormal expression of different miRNAs has been observed in several reproductive tract diseases, including preeclampsia, endometrioid endometrial adenocarcinoma and endometriosis [147,148].”
BackgroundEndometriosis and ovarian cancer: links, risks, and challenges faced
Pavone, M. E., & Lyttle, B. (2015) · International Journal of Women s Health · doi:10.2147/ijwh.s66824 · Cited by 60
“miRNA profiling in the plasma of healthy individuals compared to that of individuals with endometriosis and ovarian cancer found that novel miRNA markers could distinguish between these groups with good sensitivity and specificity.(15,23) However, subsequent studies comparing expression of high, low, or stable microsa…”
InfluentialEstrogen Induces Distinct Patterns of MicroRNA Expression Within the Mouse Uterus
Nothnick, W. B., & Healy, C. (2010) · Reproductive Sciences · doi:10.1177/1933719110377472 · Cited by 61
“Furthermore, studies in rodents have identified specific miRNAs within the uterus, which are proposed to participate in the preparation of the uterus for embryo implantation.(19-21) Although there is limited information on the role of miRNAs in normal uterine physiology, there has been a greater emphasis”
BackgroundBraza‐Boïls, A., Salloum‐Asfar, S., Marí‐Alexandre, J., Arroyo, A. B., Gónzález‐Conejero, R., Barceló‐Molina, M., García-Oms, J., Vicente, V., Estellés, A., Gilabert–Estellés, J., et al. (2015) · Human Reproduction · doi:10.1093/humrep/dev204 · Cited by 58
“In relation to gynecological diseases, it has been suggested that altered expression of miRNAs may be involved in the development of endometriosis (Pan et al., 2007, 2008; Toloubeydokhti et al., 2008; Burney et al., 2009; Guo, 2009; Ohlsson-Teague et al., 2009, 2010; Hawkins et al., 2011; Ramón et al., 2011; GilabertE…”
BackgroundLam, E. W. ‐., Shah, K., & Brosens, J. J. (2011) · Journal of Endocrinology · doi:10.1530/joe-10-0480 · Cited by 56
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
González-Ramos, R., Rocco, J., Rojas, C., Hugo Sovino, S., Poch, A., Kohen, P., Alvarado-Díaz, C. P., & Devoto, L. (2011) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.12.006 · Cited by 56
Marí‐Alexandre, J., Barceló‐Molina, M., Belmonte-López, E., García-Oms, J., Estellés, A., Braza‐Boïls, A., & Gilabert–Estellés, J. (2018) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.11.036 · Cited by 58
MicroRNAs as new players in the pain game
Niederberger, E., Kynast, K. L., Lötsch, J., & Geißlinger, G. (2011) · Pain · doi:10.1016/j.pain.2011.01.042 · Cited by 53
“Differences in miRNA expression profiles have also been shown between the endometrium of women with and of those without painful endometriosis in the early secretory phase [7].”
Logan, P. C., Yango, P., & Tran, N. D. (2017) · Reproductive Sciences · doi:10.1177/1933719117704905 · Cited by 54
“Since endometrium from patients was shown to share similar defects to ectopic endometrium (although there are some differences), the studies of isolated stromal and epithelial cells from the eutopic endometrium could minimize the heterogeneity seen among current studies.(23,51) Endometrial stromal and epithelial cells…”
ResultThe Systemic Effects of Endometriosis
Alderman, M. H., Yoder, N. D., & Taylor, H. S. (2017) · Seminars in Reproductive Medicine · doi:10.1055/s-0037-1603582 · Cited by 52
Endometriosis research in the -omics era
Goulielmos, G. N., Matalliotakis, M., Matalliotaki, C., Eliopoulos, E., Matalliotakis, I., & Zervou, M. I. (2020) · Gene · doi:10.1016/j.gene.2020.144545 · Cited by 50
Exosomes: Emerging biomarkers and targets in folliculogenesis and endometriosis
Shomali, N., Hemmatzadeh, M., Yousefzadeh, Y., Soltani‐Zangbar, M. S., Hamdi, K., Mehdizadeh, A., & yousefi, M. (2020) · Journal of Reproductive Immunology · doi:10.1016/j.jri.2020.103181 · Cited by 55
Saare, M., Rekker, K., Laisk, T., Sõritsa, D., Roost, A. M., Simm, J., Velthut‐Meikas, A., Samuel, K., Metsalu, T., Karro, H., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112630 · Cited by 50
“[9] the results of this study showed no significant differences.”
ResultApoptotic functions of microRNAs in pathogenesis, diagnosis, and treatment of endometriosis
Taghavipour, M., Sadoughi, F., Mirzaei, H., Yousefi, B., Moazzami, B., Chaichian, S., Mansournia, M. A., & Asemi, Z. (2020) · Cell & Bioscience · doi:10.1186/s13578-020-0381-0 · Cited by 54
Liu, S., Gao, S., Wang, X. Y., & Wang, D. B. (2012) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-011-2112-6 · Cited by 49
“Therefore, the different miRNA expression profiles of patients with EMs may be a primary reason for and control the development of EMs [24].”
BackgroundLaudanski, P., Charkiewicz, R., Tolwinska, A., Szamatowicz, J., Charkiewicz, A., & Niklinski, J. (2015) · BioMed Research International · doi:10.1155/2015/760698 · Cited by 48
“5 in the ESE from women with versus without endometriosis [12].”
BackgroundMethodSigurgeirsson, B., Åmark, H., Jemt, A., Ujvári, D., Westgren, M., Lundeberg, J., & Gidlöf, S. B. (2016) · Biology of Reproduction · doi:10.1095/biolreprod.116.142547 · Cited by 50
“Altered miRNA in the human endometrium expression has been described in endometrial carcinoma, and associated with infertility and endometriosis [3,19,20].”
BackgroundRole of miRNAs in Normal Endometrium and in Endometrial Disorders: Comprehensive Review
Kolańska, K., Bendifallah, S., Canlorbe, G., MEKINIAN, A., Touboul, C., Aractingi, S., Chabbert‐Buffet, N., & Daraï, É. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10163457 · Cited by 47
“miR-200c Up-regulated in secretory phase [24] Regulation of EMT via ZEB1, ZEB2 and MALAT1 [64] Down-regulated in ectopic endometrium [64]”
BackgroundSchneider, C., Kässens, N., Greve, B., Hassan, H., Schüring, A. N., Starzinski‐Powitz, A., Kiesel, L., Seidler, D. G., & Götte, M. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2012.10.051 · Cited by 46
Rahmioğlu, N., Drong, A., Lockstone, H. E., Tapmeier, T. T., Hellner, K., Saare, M., Laisk, T., Dew, C., Tough, E., Nicholson, G., et al. (2017) · Epigenetics · doi:10.1080/15592294.2017.1367475 · Cited by 47
Yang, P., Wu, Z., Ma, C., Pan, N., Wang, Y., & Yan, L. (2018) · Reproductive Sciences · doi:10.1177/1933719118799199 · Cited by 45
Altered expression of miRNAs in the uterus from a letrozole-induced rat PCOS model
Li, C., Chen, L., Zhao, Y., Chen, S., Fu, L., Jiang, Y., Gao, S., Liu, Z., Wang, F., Zhu, X., et al. (2016) · Gene · doi:10.1016/j.gene.2016.10.033 · Cited by 43
Joshi, N., Su, R., Chandramouli, G. V. R., Khoo, S. K., Jeong, J., Young, S. L., Lessey, B. A., & Fazleabas, A. T. (2015) · Human Reproduction · doi:10.1093/humrep/dev229 · Cited by 46
miR-20a contributes to endometriosis by regulating NTN4 expression
Zhao, M., Tang, Q., Wu, W., Xia, Y., Chen, D., & Wang, X. (2014) · Molecular Biology Reports · doi:10.1007/s11033-014-3452-7 · Cited by 43
“In addition, a large numbers of differentially expressed miRNAs have been identified in the eutopic endometrium of women with and without endometriosis [27, 28] and between ectopic and eutopic endometrial samples from the same women [29, 30].”
microRNAs and angiogenesis in endometriosis
Marí‐Alexandre, J., García-Oms, J., Barceló‐Molina, M., Gilabert-Aguilar, J., Estellés, A., Braza‐Boïls, A., & Gilabert–Estellés, J. (2015) · Thrombosis Research · doi:10.1016/s0049-3848(15)50439-8 · Cited by 42
“On the other hand, the overexpression of Bcl-2 found in the eutopic endometrium of women with endometriosis [34,35] could be modulated by miR-202-3p by regulating the expression of the GLI1 transcription factor.”
BackgroundShan, J., Li, D., & Wang, X.-Q. (2023) · Biomolecules · doi:10.3390/biom13030430 · Cited by 50
“[13] n = 7: moderate-severe EMS (n = 4); Controls (n = 3) miRNA microarray analysis Differentially expressed mRNA genes associated with the biological processes of cell death, cell cycle, and cellular assembly and organization.”
BackgroundMicroRNA expression pattern differs depending on endometriosis lesion type†
Haikalis, M. E., Wessels, J. M., Leyland, N. A., Agarwal, S. K., & Foster, W. G. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy019 · Cited by 41
The Pathological Role of miRNAs in Endometriosis
Begum, M. I. A., Lin, C., Hong, S., & Chae, H. (2023) · Biomedicines · doi:10.3390/biomedicines11113087 · Cited by 40
Risk Factors for Endometriosis in a German Case–Control Study
Burghaus, S., Klingsiek, P., Fasching, P. A., Engel, A., Häberle, L., Strissel, P. L., Schmidt, M., Jonas, K., Strehl, J. D., Hartmann, A., et al. (2011) · Geburtshilfe und Frauenheilkunde · doi:10.1055/s-0031-1280436 · Cited by 40
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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