{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T00:15:10Z","timestamp":1790727310689,"version":"4.1.0"},"reference-count":98,"publisher":"MDPI AG","issue":"7","license":[{"start":{"date-parts":[[2023,4,2]],"date-time":"2023-04-02T00:00:00Z","timestamp":1680393600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Medical University of Lodz","award":["503\/1-013-02\/503-11-001-19-00"],"award-info":[{"award-number":["503\/1-013-02\/503-11-001-19-00"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Alterations in the expression of numerous genes and the miRNAs that are recognized as their regulators in the endometrial cells of women with endometriosis may disrupt the intracellular signaling pathways associated with epithelial\u2013mesenchymal transition (EMT). So far, the functional role of BMP7 in endometrial physiology has been confirmed, especially in the context of fertility, but the role of the activation of a specific mechanism operating through the BMP\u2013SMAD\u2013CDH1 axis in the formation of endometrial lesions remains unexplored. The aim of this study was to evaluate the expression profile of miR-542-3p and the EMT markers (BMP7, SMAD4, CDH1) in matched eutopic endometrium (EUE) and ectopic endometrium (ECE) samples from women with endometriosis in relation to healthy women. The levels of expression of the studied genes and miRNA in peripheral blood mononuclear cells (PBMCs) obtained from women diagnosed with endometriosis and those without the disease were also evaluated. Fifty-four patients (n = 54: with endometriosis\u2014n = 29 and without endometriosis\u2014n = 25) were included in the study. A comparative analysis of the relative mean expression values (RQ) of the studied mRNA and miRNA assessed by RT-qPCR demonstrated downregulation of BMP7, SMAD4, and CDH1 expression in ectopic lesions and upregulation in the eutopic endometrium compared with the control group. In the eutopic tissue of women with endometriosis, miR-542-3p expression was similar to that of the control but significantly lower than in endometrial lesions. We also confirmed a trend towards a negative correlation between miR-542-3p and BMP7 in ectopic tissue, and in PBMC, a significant negative correlation of miR-542-3p with further BMP signaling genes, i.e., SMAD4 and CDH1, was observed. These results indicate that the miRNA selected by us may be a potential negative regulator of BMP7-SMAD4-CDH1 signaling associated with EMT. The different patterns of BMP7, SMAD4, and CDH1 gene expression in ECE, EUE, and the control endometrium observed by us suggests the loss of the endometrial epithelium phenotype in women with endometriosis and demonstrates their involvement in the pathogenesis and pathomechanism of this disease.<\/jats:p>","DOI":"10.3390\/ijms24076637","type":"journal-article","created":{"date-parts":[[2023,4,3]],"date-time":"2023-04-03T03:32:59Z","timestamp":1680492779000},"page":"6637","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":14,"title":["Assessment of BMP7, SMAD4, and CDH1 Expression Profile and Regulatory miRNA-542-3p in Eutopic and Ectopic Endometrium of Women with Endometriosis"],"prefix":"10.3390","volume":"24","author":[{"given":"Anna","family":"Zubrzycka","sequence":"first","affiliation":[{"name":"Department of Biomedicine and Genetics, Medical University of Lodz, St. Pomorska 251, C-5, 92-213 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9856-0764","authenticated-orcid":false,"given":"Monika","family":"Migdalska-S\u0119k","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Genetics, Medical University of Lodz, St. Pomorska 251, C-5, 92-213 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8166-3444","authenticated-orcid":false,"given":"S\u0142awomir","family":"J\u0119drzejczyk","sequence":"additional","affiliation":[{"name":"Institute of Medical Expertises, St. Aleksandrowska 67\/93, 91-205 Lodz, Poland"},{"name":"Operative and Conservative Gynecology Ward, Dr. K. Jonscher Municipal Medical Centre, St. Milionowa 14, 93-113 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0882-1458","authenticated-orcid":false,"given":"Ewa","family":"Brzezia\u0144ska-Lasota","sequence":"additional","affiliation":[{"name":"Department of Biomedicine and Genetics, Medical University of Lodz, St. Pomorska 251, C-5, 92-213 Lodz, Poland"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,2]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2389","DOI":"10.1056\/NEJMcp1000274","article-title":"Endometriosis","volume":"362","author":"Giudice","year":"2010","journal-title":"N. Engl. J. Med."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"659","DOI":"10.1111\/aogs.13082","article-title":"Endometriosis-associated infertility: Aspects of pathophysiological mechanisms and treatment options","volume":"96","author":"Tanbo","year":"2017","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Lagan\u00e0, A.S., Garzon, S., G\u00f6tte, M., Vigan\u00f2, P., Franchi, M., Ghezzi, F., and Martin, D.C. (2019). The Pathogenesis of Endometriosis: Molecular and Cell Biology Insights. Int. J. Mol. Sci., 20.","DOI":"10.3390\/ijms20225615"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"590823","DOI":"10.3389\/fncel.2020.590823","article-title":"Pain and endometriosis","volume":"14","author":"Maddern","year":"2020","journal-title":"Front. Cell Neurosci."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"327","DOI":"10.1016\/j.fertnstert.2018.10.013","article-title":"Pathogenesis of endometriosis: The genetic\/epigenetic theory","volume":"111","author":"Koninckx","year":"2019","journal-title":"Fertil. Steril."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1146\/annurev-pathmechdis-012419-032654","article-title":"The Origin and Pathogenesis of Endometriosis","volume":"15","author":"Wang","year":"2020","journal-title":"Annu. Rev. Pathol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1180","DOI":"10.1016\/j.fertnstert.2006.07.1550","article-title":"Molecular profling of experimental endometriosis identifed gene expression patterns in common with human disease","volume":"87","author":"Flores","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/j.bpobgyn.2003.03.001","article-title":"Endometriosis and the development of malignant tumours of the pelvis. A review of literature","volume":"18","author":"Amant","year":"2004","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"406","DOI":"10.1093\/humupd\/dmt010","article-title":"Endometriosis: Hormone regulation and clinical consequences of chemotaxis and apoptosis","volume":"19","author":"Reis","year":"2013","journal-title":"Hum. Reprod. Update"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"707","DOI":"10.1007\/s00404-019-05429-w","article-title":"microRNA-141 inhibits TGF-beta1-induced epithelial-to-mesenchymal transition through inhibition of the TGF-beta1\/SMAD2 signalling pathway in endometriosis","volume":"301","author":"Wang","year":"2020","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/S0140-6736(21)00389-5","article-title":"Endometriosis is a chronic systemic disease: Clinical challenges and novel innovations","volume":"10276","author":"Taylor","year":"2021","journal-title":"Lancet"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"178","DOI":"10.1038\/nrm3758","article-title":"Molecular mechanisms of epithelial\/mesenchymal transition","volume":"15","author":"Lamouille","year":"2014","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e108","DOI":"10.1038\/emm.2014.44","article-title":"Role of the epithelial-mesenchymal transition and its effects on embryonic stem cells","volume":"46","author":"Kim","year":"2014","journal-title":"Exp. Mol. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"41679","DOI":"10.18632\/oncotarget.16472","article-title":"Epithelial-to-mesenchymal transition in the development of endometriosis","volume":"8","author":"Yang","year":"2017","journal-title":"Oncotarget"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"8035","DOI":"10.1111\/jcmm.14668","article-title":"E2-mediated EMT by activation of \u03b2-catenin\/Snail signalling during the development of ovarian endometriosis","volume":"23","author":"Xiong","year":"2019","journal-title":"J. Cell Mol. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1038\/s41556-018-0195-z","article-title":"Mesenchymal\u2013epithelial transition in development and reprogramming","volume":"21","author":"Pei","year":"2019","journal-title":"Nat. Cell Biol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1091","DOI":"10.1080\/09513590.2018.1498477","article-title":"ILK enhances migration and invasion abilities of human endometrial stromal cells by facilitating the epithelial-mesenchymal transition","volume":"34","author":"Zheng","year":"2018","journal-title":"Gynecol. Endocrinol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"277","DOI":"10.1016\/j.cell.2004.07.011","article-title":"Epithelial-mesenchymal transitions: Twist in development and metastasis","volume":"118","author":"Kang","year":"2004","journal-title":"Cell"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1016\/j.cell.2009.11.007","article-title":"Epithelial-mesenchymal transitions in development and disease","volume":"139","author":"Thiery","year":"2009","journal-title":"Cell"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.critrevonc.2017.11.010","article-title":"E-cadherin: Its dysregulation in carcinogenesis and clinical implications","volume":"121","author":"Wong","year":"2018","journal-title":"Crit. Rev. Oncol. Hematol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1093\/humrep\/der442","article-title":"Epithelial to mesenchymal transition-like and mesenchymal to epithelial transition-like processes might be involved in the pathogenesis of pelvic endometriosis","volume":"27","author":"Matsuzaki","year":"2012","journal-title":"Hum. Reprod."},{"key":"ref_22","first-page":"1","article-title":"Regulation of epithelial-mesenchymal transition through epigenetic and post-translational modifications","volume":"15","author":"Maziveyi","year":"2016","journal-title":"Mol. Cancer"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"145","DOI":"10.3389\/fonc.2017.00145","article-title":"Epithelial-to-Mesenchymal Transition in the Female Reproductive Tract: From Normal Functioning to Disease Pathology","volume":"7","author":"Bilyk","year":"2017","journal-title":"Front. Oncol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"352616","DOI":"10.1155\/2011\/352616","article-title":"Loss of function of e-cadherin in embryonic stem cells and the relevance to models of tumorigenesis","volume":"2011","author":"Mohamet","year":"2011","journal-title":"J. Oncol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1032","DOI":"10.1097\/01.MP.0000028573.34289.04","article-title":"Beta-catenin and E-cadherin expression patterns in high-grade endometrial carcinoma are associated with histological subtype","volume":"15","author":"Schlosshauer","year":"2002","journal-title":"Mod. Pathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1016\/j.jgeb.2017.10.006","article-title":"Differentially expressed genes: OCT-4, SOX 2, STAT 3, CDH 1 and CDH 2, in cultured mesenchymal stem cells challenged with serum of women with endometriosis","volume":"16","author":"Salama","year":"2018","journal-title":"J. Genet. Eng. Biotechnol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1186\/s12958-015-0063-7","article-title":"Enhanced epithelial to mesenchymal transition (EMT) and upregulated MYC in ectopic lesions contribute independently to endometriosis","volume":"13","author":"Proestling","year":"2015","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1488","DOI":"10.1111\/jog.14001","article-title":"Roles of cell migration and invasion mediated by Twist in endometriosis","volume":"45","author":"Li","year":"2019","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"0300060520971993","DOI":"10.1177\/0300060520971993","article-title":"Expression of cellular adherent and invasive molecules in recurrent ovarian endometriosis","volume":"48","author":"Wu","year":"2020","journal-title":"J. Int. Med. Res."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"485","DOI":"10.1159\/000499625","article-title":"Silencing of Forkhead Box M1 Reverses Transforming Growth Factor-\u03b21-Induced Invasion and Epithelial-Mesenchymal Transition of Endometriotic Epithelial Cells","volume":"84","author":"Zhang","year":"2019","journal-title":"Gynecol. Obstet. Investig."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"116","DOI":"10.1186\/s12958-020-00673-1","article-title":"Differential expression of Oct-4, CD44, and E-cadherin in eutopic and ectopic endometrium in ovarian endometriomas and their correlations with clinicopathological variables","volume":"18","author":"Usta","year":"2020","journal-title":"Reprod. Biol. Endocrinol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1034\/j.1600-0412.2002.810302.x","article-title":"Expression of cadherins and CD44 isoforms in human endometrium and peritoneal endometriosis","volume":"81","author":"Poncelet","year":"2002","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"871","DOI":"10.1007\/s00404-013-3040-4","article-title":"Epithelial to mesenchymal transition (EMT) seems to be regulated differently in endometriosis and the endometrium","volume":"289","author":"Bartley","year":"2014","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.ejogrb.2008.01.004","article-title":"Matrix metalloproteinases 2 and 9, E-cadherin and betacatenin expression in endometriosis, low-grade endometrial carcinoma and non-neoplastic eutopic endometrium","volume":"139","author":"Charabi","year":"2008","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Janusz, J., Janusz, A., Kondera-Anasz, Z., Sikora, S., Smycz-Kuba\u0144ska, M., Englisz, A., Wendlocha, D., and Mielczarek-Palacz, A. (2021). Participation of Selected Soluble BMP-2 and BMP-7 Bone Morphogenetic Proteins and Their Soluble Type I ALK-1 and Type II BMPR2 Receptors in Formation and Development of Endometriosis. Biomedicines, 9.","DOI":"10.3390\/biomedicines9101292"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1177\/1933719116671218","article-title":"Abnormal uterine bleeding is associated with increased BMP7 expression in human endometrium","volume":"24","author":"Richards","year":"2017","journal-title":"Reprod. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1210\/en.2016-1629","article-title":"BMP7 Induces Uterine Receptivity and Blastocyst Attachment","volume":"158","author":"Monsivais","year":"2017","journal-title":"Endocrinology"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Large, M.J., Wetendorf, M., Lanz, R.B., Hartig, S.M., Creighton, C.J., Mancini, M.A., Kovanci, E., Lee, K.F., Threadgill, D.W., and Lydon, J.P. (2014). The epidermal growth factor receptor critically regulates endometrial function during early pregnancy. PLoS Genet., 10.","DOI":"10.1371\/journal.pgen.1004451"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2783","DOI":"10.1101\/gad.1350705","article-title":"Smad transcription factors","volume":"19","author":"Seoane","year":"2005","journal-title":"Genes Dev."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"797","DOI":"10.1007\/s00404-015-3875-y","article-title":"Molecular mechanisms underlying endometriosis pathogenesis revealed by bioinformatics analysis of microarray data","volume":"293","author":"Ping","year":"2016","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"868","DOI":"10.1111\/aogs.13931","article-title":"BMP-6 and SMAD4 gene expression is altered in cumulus cells from women with endometriosis-associated infertility","volume":"100","author":"Matte","year":"2021","journal-title":"Acta Obstet. Gynecol. Scand."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1095\/biolreprod.116.139477","article-title":"SMAD Signaling Is Required for Structural Integrity of the Female Reproductive Tract and Uterine Function During Early Pregnancy in Mice","volume":"95","author":"Rodriguez","year":"2016","journal-title":"Biol. Reprod."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"4573","DOI":"10.1002\/jcb.27746","article-title":"MiR-542-3p controls hepatic stellate cell activation and fibrosis via targeting BMP-7","volume":"120","author":"Feihong","year":"2019","journal-title":"J. Cell Biochem."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"27945","DOI":"10.3390\/ijms161126075","article-title":"MiR542-3p regulates the Epithelial-Mesenchymal Transition by directly targeting BMP7 in NRK52e","volume":"16","author":"Liu","year":"2015","journal-title":"Int. J. Mol. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"40001","DOI":"10.1038\/srep40001","article-title":"Loss of Mir-542-3P enhances Igfp-1 expression in decidualizing human endometrial stromal cells","volume":"7","author":"Tochigi","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1359","DOI":"10.1177\/1933719116641761","article-title":"Analysis of Serum MicroRNA Profile by Solexa Sequencing in Women with Endometriosis","volume":"23","author":"Wang","year":"2016","journal-title":"Reprod. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/j.biopha.2018.01.131","article-title":"MicroRNA-542-3P functions as a tumor suppressor via directly targeting survivin in hepatocellular carcinoma","volume":"99","author":"Wang","year":"2018","journal-title":"Biomed. Pharmacother."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"e1050","DOI":"10.1038\/cddis.2014.4","article-title":"Mir-542-3P suppresses osteoblast cell proliferation and diferentiation, targets Bmp-7 signaling and inhibits bone formation","volume":"5","author":"Kureel","year":"2014","journal-title":"Cell Death. Dis."},{"key":"ref_49","first-page":"3545","article-title":"Upregulation of Mir-542-3P inhibits the growth and invasion of human colon cancer cells through Pi3K\/Akt\/survivin signaling","volume":"38","author":"Yang","year":"2017","journal-title":"Oncol. Rep."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"Rev-529","DOI":"10.12688\/f1000research.14817.1","article-title":"Endometriosis: Advances and Controversies in Classification, Pathogenesis, Diagnosis, and Treatment","volume":"8","author":"Rolla","year":"2019","journal-title":"F1000Research"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"4051","DOI":"10.1038\/s41598-022-07771-7","article-title":"MicroRNome analysis generates a blood-based signature for endometriosis","volume":"12","author":"Bendifallah","year":"2022","journal-title":"Sci. Rep."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"557.e1","DOI":"10.1016\/j.ajog.2020.02.050","article-title":"Accurate diagnosis of endometriosis using serum microRNAs","volume":"223","author":"Moustafa","year":"2020","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Mar\u00ed-Alexandre, J., Sanchez-Izquierdo, D., Gilabert-Estelles, J., Barcelo-molina, M., Braza-Boils, A., and Sandoval, J. (2016). miRNAs regulation and its role as biomarkers in endometriosis. Int. J. Mol. Sci., 17.","DOI":"10.3390\/ijms17010093"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"eRW5704","DOI":"10.31744\/einstein_journal\/2021RW5704","article-title":"Overview of miRNAs for the non-invasive diagnosis of endometriosis: Evidence, challenges and strategies. A systematic review","volume":"19","author":"Monnaka","year":"2021","journal-title":"Einstein"},{"key":"ref_55","first-page":"1135","article-title":"MicroRNAs in Endometriosis: Biological Function and Emerging Biomarker Candidates","volume":"100","author":"Bjorkman","year":"2019","journal-title":"Biol. Reprod."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Agrawal, S., Tapmeier, T., Rahmioglu, N., Kirtley, S., Zondervan, K., and Becker, C. (2018). The MiRNA Mirage: How Close Are We to Finding a Non-Invasive Diagnostic Biomarker in Endometriosis? A Systematic Review. Int. J. Mol. Sci., 19.","DOI":"10.3390\/ijms19020599"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"4225","DOI":"10.2147\/OTT.S137107","article-title":"miRNA expression profiling in formalin-fixed paraffin-embedded endometriosis and ovarian cancer samples","volume":"10","author":"Braicu","year":"2017","journal-title":"Onco. Targets Ther."},{"key":"ref_58","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_59","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1093\/humupd\/dmt052","article-title":"Structural and Molecular Features of the Endomyometrium in Endometriosis and Adenomyosis","volume":"20","author":"Benagiano","year":"2014","journal-title":"Hum. Reprod. Update"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"1505","DOI":"10.1016\/j.fertnstert.2007.01.056","article-title":"Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium","volume":"88","author":"Eyster","year":"2007","journal-title":"Fertil. Steril."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"bqac043","DOI":"10.1210\/endocr\/bqac043","article-title":"BMP\/SMAD1\/5 Signaling in the Endometrial Epithelium Is Essential for Receptivity and Early Pregnancy","volume":"163","author":"Tang","year":"2022","journal-title":"Endocrinology"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"3386","DOI":"10.1038\/s41467-021-23571-5","article-title":"Endometrial receptivity and implantation require uterine BMP signaling through an ACVR2A-SMAD1\/SMAD5 axis","volume":"12","author":"Monsivais","year":"2021","journal-title":"Nat. Commun."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"2282","DOI":"10.1016\/j.bbadis.2017.06.018","article-title":"Challenges in endometriosis miRNA studies from tissue heterogeneity to disease specific miRNAs","volume":"1863","author":"Saare","year":"2017","journal-title":"Biochim. Biophys. Acta Mol. Basis Dis."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1055\/s-0037-1599089","article-title":"MicroRNAs and endometriosis: Distinguishing drivers from passengers in disease pathogenesis","volume":"35","author":"Nothnick","year":"2017","journal-title":"Semin. Reprod. Med."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1623","DOI":"10.1038\/onc.2011.367","article-title":"MicroRNA-mediated upregulation of integrin-linked kinase promotes Src-induced tumor progression","volume":"31","author":"Oneyama","year":"2012","journal-title":"Oncogene"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"4048","DOI":"10.1016\/j.febslet.2010.08.025","article-title":"Induction of growth arrest by miR-542-3p that targets survivin","volume":"584","author":"Yoon","year":"2010","journal-title":"FEBS Lett."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"885","DOI":"10.1080\/01443615.2017.1404014","article-title":"Highly elevated human epididymis protein 4 (HE4) following endometrioma rupture: A case report","volume":"38","author":"Taskin","year":"2018","journal-title":"J. Obstet. Gynaecol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1315","DOI":"10.1038\/sj.bjc.6605011","article-title":"Serum HE4 concentration differentiates malignant ovarian tumours from ovarian endometriotic cysts","volume":"100","author":"Huhtinen","year":"2009","journal-title":"Br. J. Cancer"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"450","DOI":"10.5603\/GP.a2021.0127","article-title":"Plasma microRNAs can be a potential diagnostic biomarker for endometriosis","volume":"93","author":"Zhuo","year":"2022","journal-title":"Ginekol. Pol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1210\/jc.2012-2415","article-title":"Circulating MicroRNAs Identified in a Genome-Wide Serum MicroRNA Expression Analysis as Noninvasive Biomarkers for Endometriosis","volume":"98","author":"Wang","year":"2013","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"993","DOI":"10.1177\/1933719108324132","article-title":"The expression and ovarian steroid regulation of endometrial micro-RNAs","volume":"15","author":"Toloubeydokhti","year":"2008","journal-title":"Reprod. Sci."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1002\/rmb2.12028","article-title":"Overexpression of microRNA-542-3p attenuates the differentiating capacity of endometriotic stromal cells","volume":"16","author":"Sultana","year":"2017","journal-title":"Reprod. Med. Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"564","DOI":"10.1016\/j.fertnstert.2005.08.046","article-title":"Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity","volume":"85","author":"Klemmt","year":"2006","journal-title":"Fertil. Steril."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2516","DOI":"10.1210\/jc.2009-0207","article-title":"Decidualization attenuates the contractility of eutopic and ectopic endometrial stromal cells: Implications for hormone therapy of endometriosis","volume":"94","author":"Tsuno","year":"2009","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"7186","DOI":"10.1038\/s41598-021-85295-2","article-title":"Micro-RNA miR-542-3p suppresses decidualization by targeting ILK pathways in human endometrial stromal cells","volume":"11","author":"Qu","year":"2021","journal-title":"Sci. Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1839","DOI":"10.1016\/S0002-9440(10)63030-1","article-title":"Identification of an invasive, N-cadherin-expressing epithelial cell type in endometriosis using a new cell culture model","volume":"159","author":"Zeitvogel","year":"2001","journal-title":"Am. J. Pathol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"850","DOI":"10.1016\/j.biopha.2018.11.104","article-title":"MiR-542-3p, a microRNA targeting CDK14, suppresses cell proliferation, invasiveness, and tumorigenesis of epithelial ovarian cancer","volume":"110","author":"Li","year":"2019","journal-title":"Biomed. Pharmacother."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"1233","DOI":"10.21037\/atm-21-2980","article-title":"Hyperoside suppresses BMP-7-dependent PI3K\/AKT pathway in human hepatocellular carcinoma cells","volume":"9","author":"Wei","year":"2021","journal-title":"Ann. Transl. Med."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1016\/j.bbrc.2011.12.064","article-title":"Bone morphogenetic protein (BMP)-4 and BMP-7 suppress granulosa cell apoptos is via different pathways: BMP-4 via PI3K\/PDK-1\/Akt and BMP-7 via PI3K\/PDK-1\/PKC","volume":"417","author":"Shimizu","year":"2012","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1006\/bbrc.1997.6624","article-title":"Osteogenic protein-1 mRNA in the uterine endometrium","volume":"234","author":"Ozkaynak","year":"1997","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1073\/pnas.98.3.1047","article-title":"Cellular and molecular responses of the uterus to embryo implantation can be elicited by locally applied growth factors","volume":"98","author":"Paria","year":"2001","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1447","DOI":"10.1093\/humrep\/den110","article-title":"A distinct cohort of the TGFbeta superfamily members expressed in human endometrium regulate decidualization","volume":"23","author":"Stoikos","year":"2008","journal-title":"Hum. Reprod."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"751","DOI":"10.1093\/humrep\/dep455","article-title":"Progesterone decreases bone morphogenetic protein (BMP) 7 expression and BMP7 inhibits decidualization and proliferation in endometrial stromal cells","volume":"25","author":"Kodama","year":"2010","journal-title":"Hum. Reprod."},{"key":"ref_84","first-page":"2547","article-title":"BMP7 coordinates endometrial epithelial cell receptivity for blastocyst implantation through the endoglin pathway in cell lines and a mouse model","volume":"17","author":"Yuan","year":"2019","journal-title":"Exp. Ther. Med."},{"key":"ref_85","first-page":"103","article-title":"Osteogenic protein-1 is produced by human fetal trophoblasts in vivo and regulates the synthesis of chorionic gonadotropin and progesterone by trophoblasts in vitro","volume":"34","author":"Martinovic","year":"1996","journal-title":"Eur. J. Clin. Chem. Clin. Biochem."},{"key":"ref_86","first-page":"4726","article-title":"Smad signaling coincides with epithelial-mesenchymal transition in a rat model of intrauterine adhesion","volume":"11","author":"Guo","year":"2019","journal-title":"Am. J. Transl. Res."},{"key":"ref_87","first-page":"17","article-title":"Immunohistochemical localization of inhibin and activin subunits, activin receptors and Smads in ovarian endometriosis","volume":"25","author":"Mabuchi","year":"2010","journal-title":"Int. J. Mol. Med."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1177\/1933719114549855","article-title":"Expression of Nodal, Cripto, SMAD3, Phosphorylated SMAD3, and SMAD4 in the Proliferative Endometrium of Women with Endometriosis","volume":"22","author":"Cruz","year":"2015","journal-title":"Reprod. Sci."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"111","DOI":"10.7150\/ijbs.23230","article-title":"The role of TGF-\u03b2\/SMAD4 signaling in cancer","volume":"14","author":"Zhao","year":"2018","journal-title":"Int. J. Biol. Sci."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"9624","DOI":"10.1073\/pnas.97.17.9624","article-title":"Smad4\/DPC4-mediated tumor suppression through suppression of angiogenesis","volume":"97","author":"Volpert","year":"2000","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1007\/s10735-018-9763-6","article-title":"Smad4 and epithelial-mesenchymal transition proteins in colorectal carcinoma: An immunohistochemical study","volume":"49","author":"Ioannou","year":"2018","journal-title":"J. Mol. Histol."},{"key":"ref_92","first-page":"461","article-title":"Nonmalignant epithelial cells, potentially invasive in human endometriosis, lack the tumor suppressor molecule E-cadherin","volume":"150","author":"Gaetje","year":"1997","journal-title":"Am. J. Pathol."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"117","DOI":"10.1007\/s00404-017-4560-0","article-title":"Knockdown of E-cadherin expression of endometrial epithelial cells may activate Wnt\/\u03b2-catenin pathway in vitro","volume":"297","author":"Zhu","year":"2018","journal-title":"Arch. Gynecol. Obstem."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/0301-2115(96)02432-3","article-title":"Expression of E-cadherin, alpha- and beta-catenin mRNAs in ovarian endometriosis","volume":"67","author":"Fujimoto","year":"1996","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_95","first-page":"251","article-title":"Gene expression profiling of peripheral blood mononuclear leukocytes from psoriasis patients identifies new immune regulatory molecules","volume":"15","author":"Koczan","year":"2005","journal-title":"Eur. J. Dermatol."},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"817","DOI":"10.1016\/S0015-0282(97)81391-X","article-title":"Revised American Society for Reproductive Medicine Classification of Endometriosis: 1996","volume":"67","author":"Canis","year":"1997","journal-title":"Fertil. Steril."},{"key":"ref_97","doi-asserted-by":"crossref","unstructured":"Zubrzycka, A., Migdalska-S\u0119k, M., J\u0119drzejczyk, S., and Brzezia\u0144ska-Lasota, E. (2023). The Expression of TGF-\u03b21, SMAD3, ILK and miRNA-21 in the Ectopic and Eutopic Endometrium of Women with Endometriosis. Int. J. Mol. Sci., 24.","DOI":"10.3390\/ijms24032453"},{"key":"ref_98","first-page":"614","article-title":"Biostatistics 104: Correlational analysis","volume":"44","author":"Chan","year":"2003","journal-title":"Singap. Med. J."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/7\/6637\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:08:32Z","timestamp":1760123312000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/7\/6637"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,2]]},"references-count":98,"journal-issue":{"issue":"7","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["ijms24076637"],"URL":"https:\/\/doi.org\/10.3390\/ijms24076637","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,2]]}}}