{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,18]],"date-time":"2026-06-18T16:45:48Z","timestamp":1781801148178,"version":"3.54.5"},"reference-count":44,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2022,4,22]],"date-time":"2022-04-22T00:00:00Z","timestamp":1650585600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100005888","name":"Medical University of Lodz","doi-asserted-by":"publisher","award":["570\/1-004-01\/570-01-082"],"award-info":[{"award-number":["570\/1-004-01\/570-01-082"]}],"id":[{"id":"10.13039\/501100005888","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Micro-RNAs expression can vary between different forms of endometriosis, but data on miRNA expression in cesarean scar endometriosis is lacking. The present study is comprised of 30 patients with endometriosis in the cesarean scar (scar endometriosis, SE), 14 patients with deep infiltrating endometriosis (DIE), 47 patients with endometrioma (ovarian endometrial cyst, OE), and 33 patients with healthy ovarian tissue as the control group (CG). In the initial experiment to identify possible dysregulated miRNAs, the levels of 754 miRNAs in formalin-fixed paraffin-embedded tissue (FFPE) samples from OE, high-grade ovarian cancer, endometrioid ovarian cancer, and CG were measured. We identified seven potentially dysregulated miRNAs: miR-1-3p, miR-31-3p, miR-125b-1-3p, miR-200b-3p, miR-548d, miR-502, and miR-503. We then examined the expression profiles of each of these miRNAs individually in the SE, DIE, OE, and CG FFPE samples using RT-qPCR. miR-31-3p had significantly higher levels of expression and miR-125b-1-3p had significantly lower levels of expression in SE compared to the controls. Overall, the higher expression levels of miR-31-3p and the lower expression levels of miR-125b-1-3p are consistent with the benign nature of SE. Importantly, the results of the present study demonstrate the possibility of using miRNA to monitor the risk of malignant transformation of endometriosis tissue.<\/jats:p>","DOI":"10.3390\/ijms23094660","type":"journal-article","created":{"date-parts":[[2022,4,23]],"date-time":"2022-04-23T08:14:06Z","timestamp":1650701646000},"page":"4660","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["miR 31-3p Has the Highest Expression in Cesarean Scar Endometriosis"],"prefix":"10.3390","volume":"23","author":[{"given":"Maria","family":"Szubert","sequence":"first","affiliation":[{"name":"Clinic of Surgical and Oncologic Gynecology, 1st Department of Gynecology and Obstetrics, Medical University of Lodz, M. Pirogow\u2019s Teaching Hospital, Wilenska 37 St., 94-029 Lodz, Poland"},{"name":"Club 35, Polish Society of Gynecologists and Obstetricians, 53-125 Wroc\u0142aw, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna","family":"Nowak-Gl\u00fcck","sequence":"additional","affiliation":[{"name":"Clinic of Surgical and Oncologic Gynecology, 1st Department of Gynecology and Obstetrics, Medical University of Lodz, M. Pirogow\u2019s Teaching Hospital, Wilenska 37 St., 94-029 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daria","family":"Doma\u0144ska-Senderowska","sequence":"additional","affiliation":[{"name":"Department of Molecular Medicine, Medical University of Lodz, Pomorska 251 St., 92-213 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0775-7570","authenticated-orcid":false,"given":"Bo\u017cena","family":"Szyma\u0144ska","sequence":"additional","affiliation":[{"name":"CoreLab, Central Scientific Laboratory of the Medical University of Lodz, Mazowiecka 6\/8 St., 92-215 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Piotr","family":"Sowa","sequence":"additional","affiliation":[{"name":"Department of Pathology, M. Pirogow\u2019s Teaching Hospital, Wilenska 37 St., 94-029 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Aleksander","family":"Rycerz","sequence":"additional","affiliation":[{"name":"Clinic of Surgical and Oncologic Gynecology, 1st Department of Gynecology and Obstetrics, Medical University of Lodz, M. Pirogow\u2019s Teaching Hospital, Wilenska 37 St., 94-029 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2072-6533","authenticated-orcid":false,"given":"Jacek R.","family":"Wilczy\u0144ski","sequence":"additional","affiliation":[{"name":"Clinic of Surgical and Oncologic Gynecology, 1st Department of Gynecology and Obstetrics, Medical University of Lodz, M. Pirogow\u2019s Teaching Hospital, Wilenska 37 St., 94-029 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2022,4,22]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1159\/000358919","article-title":"The History of Endometriosis","volume":"78","author":"Benagiano","year":"2014","journal-title":"Gynecol. Obstet. Investig."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"381","DOI":"10.23736\/S0026-4784.17.04054-0","article-title":"Sexual Pain in Women: Quality of Sex Life and Marital Relations","volume":"69","author":"Ghizzani","year":"2017","journal-title":"Minerva Obstet. Gynecol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1080\/01443610701497660","article-title":"Rectovaginal Endometriosis\u2014A Frequently Missed Diagnosis","volume":"27","author":"Griffiths","year":"2007","journal-title":"J. Obstet. Gynaecol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1055\/s-0032-1333476","article-title":"Eutopic Endometrium in Women with Endometriosis: Ground Zero for the Study of Implantation Defects","volume":"31","author":"Lessey","year":"2013","journal-title":"Semin. Reprod. Med."},{"key":"ref_5","doi-asserted-by":"crossref","unstructured":"Kolanska, K., Bendifallah, S., Canlorbe, G., Mekinian, A., Touboul, C., Aractingi, S., Chabbert-Buffet, N., and Dara\u00ef, E. (2021). Role of miRNAs in Normal Endometrium and in Endometrial Disorders: Comprehensive Review. J. Clin. Med., 10.","DOI":"10.3390\/jcm10163457"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1097\/01.JAA.0000750940.47126.58","article-title":"Recognizing and Treating Endometriosis","volume":"34","author":"Blamble","year":"2021","journal-title":"J. Am. Acad. Physician Assist."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"O\u2019Brien, J., Hayder, H., Zayed, Y., and Peng, C. (2018). Overview of MicroRNA Biogenesis, Mechanisms of Actions, and Circulation. Front. Endocrinol. (Lausanne), 402.","DOI":"10.3389\/fendo.2018.00402"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1038\/ncb1722","article-title":"The MiR-200 Family and MiR-205 Regulate Epithelial to Mesenchymal Transition by Targeting ZEB1 and SIP1","volume":"10","author":"Gregory","year":"2008","journal-title":"Nat. Cell Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"760698","DOI":"10.1155\/2015\/760698","article-title":"Profiling of Selected MicroRNAs in Proliferative Eutopic Endometrium of Women with Ovarian Endometriosis","volume":"2015","author":"Laudanski","year":"2015","journal-title":"BioMed Res. Int."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Choi, P.-W., and Ng, S.-W. (2017). The Functions of MicroRNA-200 Family in Ovarian Cancer: Beyond Epithelial-Mesenchymal Transition. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18061207"},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Vilming, E.B., Olstad, O.K., Haug, K.B., Brusletto, B., Sandvik, L., Staff, A.C., Gautvik, K.M., and Davidson, B. (2014). Global miRNA expression analysis of serous and clear cell ovarian carcinomas identifies differentially expressed miRNAs including miR-200c-3p as a prognostic marker. BMC Cancer, 14.","DOI":"10.1186\/1471-2407-14-80"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"243","DOI":"10.3892\/etm.2021.9674","article-title":"Ovarian endometriosis, a precursor of ovarian cancer: Histological aspects, gene expression and microRNA alterations (Review)","volume":"21","author":"Braicu","year":"2021","journal-title":"Exp. Ther. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"805","DOI":"10.3892\/ol.2021.13066","article-title":"miR-148a, miR-152 and miR-200b promote prostate cancer metastasis by targeting DNMT1 and PTEN expression","volume":"22","author":"Gurbuz","year":"2021","journal-title":"Oncol. Lett."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1007\/978-1-61779-055-3_16","article-title":"MicroRNA Isolation from Formalin-Fixed, Paraffin-Embedded Tissues","volume":"724","author":"Liu","year":"2011","journal-title":"Methods Mol. Biol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"478","DOI":"10.3389\/fgene.2019.00478","article-title":"The Potential for microRNA Therapeutics and Clinical Research","volume":"10","author":"Hanna","year":"2019","journal-title":"Front. Genet."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"17728","DOI":"10.1038\/s41598-020-74685-7","article-title":"The Crucial Choice of Reference Genes: Identification of MiR-191-5p for Normalization of MiRNAs Expression in Bone Marrow Mesenchymal Stromal Cell and HS27a\/HS5 Cell Lines","volume":"10","year":"2020","journal-title":"Sci. Rep."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"828","DOI":"10.1093\/carcin\/bgs030","article-title":"Serum microRNA profiling and breast cancer risk: The use of miR-484\/191 as endogenous controls","volume":"33","author":"Hu","year":"2012","journal-title":"Carcinogenesis"},{"key":"ref_18","first-page":"258","article-title":"Comparative Analysis of Differentially Expressed miRNAs and their Downstream mRNAs in Ovarian Cancer and its Associated Endometriosis","volume":"7","author":"Wu","year":"2015","journal-title":"J. Cancer Sci. Ther."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1093\/biolre\/ioy019","article-title":"MicroRNA Expression Pattern Differs Depending on Endometriosis Lesion Type","volume":"98","author":"Haikalis","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_20","first-page":"853","article-title":"Identification of novel genes coding for small expressed RNAs","volume":"26","author":"Rauhut","year":"2001","journal-title":"Science"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"D756","DOI":"10.1093\/nar\/gku956","article-title":"Xenbase, the Xenopus Model Organism Database; New Virtualized System, Data Types and Genomes","volume":"43","author":"Karpinka","year":"2015","journal-title":"Nucleic Acids Res."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"1625","DOI":"10.7754\/Clin.Lab.2015.150404","article-title":"MiR-31 Reduces Cell Growth of Papillary Thyroid Carcinoma by RNA-Binding Protein HuR","volume":"61","author":"Wu","year":"2015","journal-title":"Clin. Lab."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"5741","DOI":"10.21037\/jtd-21-555","article-title":"BRCA-Associated Protein 1 (BAP1) and MiR-31 Combination Predicts Outcomes in Epithelioid Malignant Pleural Mesothelioma","volume":"13","author":"Murrone","year":"2021","journal-title":"J. Thorac. Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"42371","DOI":"10.1074\/jbc.M111.261065","article-title":"MicroRNA-31 Regulated by the Extracellular Regulated Kinase Is Involved in Vascular Smooth Muscle Cell Growth via Large Tumor Suppressor Homolog 2","volume":"286","author":"Liu","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1162","DOI":"10.1016\/j.biopha.2018.09.132","article-title":"Functions and mechanisms of microRNA-31 in human cancers","volume":"108","author":"Yu","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.canlet.2013.09.034","article-title":"MicroRNA-31 Inhibits Cisplatin-Induced Apoptosis in Non-Small Cell Lung Cancer Cells by Regulating the Drug Transporter ABCB9","volume":"343","author":"Dong","year":"2014","journal-title":"Cancer Lett."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"e15698","DOI":"10.1097\/MD.0000000000015698","article-title":"ATP binding cassette subfamily B member 9 (ABCB9) is a prognostic indicator of overall survival in ovarian cancer","volume":"98","author":"Hou","year":"2019","journal-title":"Medicine (Baltimore)"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"252","DOI":"10.1016\/j.yexcr.2015.09.015","article-title":"Progress on the Relationship between MiR-125 Family and Tumorigenesis","volume":"339","author":"Yin","year":"2015","journal-title":"Exp. Cell Res."},{"key":"ref_29","first-page":"e2021028","article-title":"Circulating microRNAs as Potential Non-invasive Biomarkers for Breast Cancer Detection","volume":"92","author":"Canatan","year":"2021","journal-title":"Acta Bio-Medica Atenei Parmensis"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1758","DOI":"10.1002\/ijc.25509","article-title":"MicroRNA-125b Suppresses the Development of Bladder Cancer by Targeting E2F3","volume":"128","author":"Huang","year":"2011","journal-title":"Int. J. Cancer"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"e556","DOI":"10.1038\/cddis.2013.79","article-title":"Functional Cooperation of MiR-125a, MiR-125b, and MiR-205 in Entinostat-Induced Downregulation of ErbB2\/ErbB3 and Apoptosis in Breast Cancer Cells","volume":"4","author":"Wang","year":"2013","journal-title":"Cell Death Dis."},{"key":"ref_32","first-page":"190","article-title":"MicroRNAS in endometrial cancer: Recent advances and potential clinical applications","volume":"14","author":"Yanokura","year":"2015","journal-title":"EXCLI J."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"BR149","DOI":"10.12659\/MSM.882617","article-title":"MicroRNA-125b down-regulation mediates endometrial cancer invasion by targeting ERBB2","volume":"18","author":"Shang","year":"2012","journal-title":"Med. Sci. Monit."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Jiang, F., Liu, T., He, Y., Yan, Q., Hen, X., Wang, H., and Wan, X. (2011). MiR-125b promotes proliferation and migration of type II endometrial carcinoma cells through targeting TP53INP1 tumor suppressor in vitro and in vivo. BMC Cancer, 11.","DOI":"10.1186\/1471-2407-11-425"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s12253-016-0184-0","article-title":"Entangling Relation of Micro RNA-Let7, MiRNA-200 and MiRNA-125 with Various Cancers","volume":"23","author":"Masood","year":"2017","journal-title":"Pathol. Oncol. Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1016\/j.cell.2011.02.013","article-title":"Hallmarks of Cancer: The Next Generation","volume":"144","author":"Hanahan","year":"2011","journal-title":"Cell"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"96","DOI":"10.3892\/or.2022.8307","article-title":"Regulatory functions of miR-200b-3p in tumor development (Review)","volume":"47","author":"Chen","year":"2022","journal-title":"Oncol. Rep."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/j.apjtm.2017.05.007","article-title":"MiR-200a and miR-200b target PTEN to regulate the endometrial cancer cell growth in vitro","volume":"10","author":"Wu","year":"2017","journal-title":"Asian Pac. J. Trop. Med."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"66629","DOI":"10.18632\/oncotarget.18343","article-title":"The MiR-200 Family in Ovarian Cancer","volume":"8","author":"Koutsaki","year":"2017","journal-title":"Oncotarget"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"587","DOI":"10.1097\/OGX.0000000000000218","article-title":"Evidence for the Relationship Between Endometriosis and Epithelial Ovarian Cancer","volume":"70","year":"2015","journal-title":"Obstet. Gynecol. Surv."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"102092","DOI":"10.1016\/j.jogoh.2021.102092","article-title":"Circulating Serum MiR-200c and MiR-34a-5p as Diagnostic Biomarkers for Endometriosis","volume":"50","author":"Misir","year":"2021","journal-title":"J. Gynecol. Obstet. Hum. Reprod."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"938","DOI":"10.1016\/j.fertnstert.2015.06.029","article-title":"Circulating MiR-200\u2013Family Micro-RNAs Have Altered Plasma Levels in Patients with Endometriosis and Vary with Blood Collection Time","volume":"104","author":"Rekker","year":"2015","journal-title":"Fertil. Steril."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1007\/s43032-022-00860-y","article-title":"Overexpression of miR-200b-3p in Menstrual Blood-Derived Mesenchymal Stem Cells from Endometriosis Women","volume":"29","author":"Cressoni","year":"2022","journal-title":"Reprod. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"3865","DOI":"10.1093\/nar\/gkw116","article-title":"Distribution of miRNA expression across human tissues","volume":"5","author":"Ludwig","year":"2016","journal-title":"Nucleic Acids Res."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/9\/4660\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T22:59:16Z","timestamp":1760137156000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/23\/9\/4660"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,4,22]]},"references-count":44,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2022,5]]}},"alternative-id":["ijms23094660"],"URL":"https:\/\/doi.org\/10.3390\/ijms23094660","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,4,22]]}}}