{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,20]],"date-time":"2026-09-20T16:45:13Z","timestamp":1789922713047,"version":"4.0.1"},"reference-count":105,"publisher":"MDPI AG","issue":"22","license":[{"start":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T00:00:00Z","timestamp":1699315200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Eunice Kennedy Shriver NICHD\/NIH","award":["R01 HD090066"],"award-info":[{"award-number":["R01 HD090066"]}]},{"name":"Eunice Kennedy Shriver NICHD\/NIH","award":["R21 HD109726"],"award-info":[{"award-number":["R21 HD109726"]}]},{"name":"Eunice Kennedy Shriver NICHD\/NIH","award":["T32 ES007326"],"award-info":[{"award-number":["T32 ES007326"]}]},{"name":"NIEHS training","award":["R01 HD090066"],"award-info":[{"award-number":["R01 HD090066"]}]},{"name":"NIEHS training","award":["R21 HD109726"],"award-info":[{"award-number":["R21 HD109726"]}]},{"name":"NIEHS training","award":["T32 ES007326"],"award-info":[{"award-number":["T32 ES007326"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>There are several critical events that occur in the uterus during early pregnancy which are necessary for the establishment and maintenance of pregnancy. These events include blastocyst implantation, uterine decidualization, uterine neoangiogenesis, differentiation of trophoblast stem cells into different trophoblast cell lineages, and formation of a placenta. These processes involve several different cell types within the pregnant uterus. Communication between these cell types must be intricately coordinated for successful embryo implantation and the formation of a functional maternal\u2013fetal interface in the placenta. Understanding how this intricate coordination transpires has been a focus of researchers in the field for many years. It has long been understood that maternal endometrial tissue plays a key role in intercellular signaling during early pregnancy, sending signals to nearby tissues in a paracrine manner. Recently, insights have been obtained into the mechanisms by which these signaling events occur. Notably, the endometrium has been shown to secrete extracellular vesicles (EVs) that contain crucial cargo (proteins, lipids, RNA, miRNA) that are taken up by recipient cells to initiate a response leading to the occurrence of critical events during implantation and placentation. In this review, we aim to summarize the role that endometrium-derived EVs play in mediating cell-to-cell communications within the pregnant uterus to orchestrate the events that must occur to establish and maintain pregnancy. We will also discuss how aberrant endometrial EV signaling may lead to pathophysiological conditions, such as endometriosis and infertility.<\/jats:p>","DOI":"10.3390\/cells12222584","type":"journal-article","created":{"date-parts":[[2023,11,7]],"date-time":"2023-11-07T00:44:18Z","timestamp":1699317858000},"page":"2584","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":40,"title":["Role of Endometrial Extracellular Vesicles in Mediating Cell-to-Cell Communication in the Uterus: A Review"],"prefix":"10.3390","volume":"12","author":[{"given":"Jacob R.","family":"Beal","sequence":"first","affiliation":[{"name":"Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2955-8206","authenticated-orcid":false,"given":"Qiuyan","family":"Ma","sequence":"additional","affiliation":[{"name":"Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Indrani C.","family":"Bagchi","sequence":"additional","affiliation":[{"name":"Department of Comparative Biosciences, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0371-2463","authenticated-orcid":false,"given":"Milan K.","family":"Bagchi","sequence":"additional","affiliation":[{"name":"Department of Molecular and Integrative Physiology, University of Illinois at Urbana-Champaign, Urbana, IL 61801, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,11,7]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"10159","DOI":"10.1073\/pnas.90.21.10159","article-title":"Blastocyst\u2019s State of Activity Determines the \u201cWindow\u201d of Implantation in the Receptive Mouse Uterus","volume":"90","author":"Paria","year":"1993","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"351","DOI":"10.12717\/DR.2017.21.4.351","article-title":"A Review of Mechanisms of Implantation","volume":"21","author":"Kim","year":"2017","journal-title":"Dev. Reprod."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1387\/ijdb.130348mb","article-title":"Role of Uterine Stromal-Epithelial Crosstalk in Embryo Implantation","volume":"58","author":"Hantak","year":"2014","journal-title":"Int. J. Dev. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Massimiani, M., Lacconi, V., La Civita, F., Ticconi, C., Rago, R., and Campagnolo, L. (2019). Molecular Signaling Regulating Endometrium-Blastocyst Crosstalk. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21010023"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1006\/dbio.2000.9767","article-title":"Embryo Implantation","volume":"223","author":"Carson","year":"2000","journal-title":"Dev. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1055\/s-0029-1242989","article-title":"Endometrial Decidualization: Of Mice and Men","volume":"28","author":"Ramathal","year":"2010","journal-title":"Semin. Reprod. Med."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1038\/nm.3012","article-title":"Mechanisms of Implantation: Strategies for Successful Pregnancy","volume":"18","author":"Cha","year":"2012","journal-title":"Nat. Med."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1002\/rmb2.12088","article-title":"Decidualization of the Human Endometrium","volume":"17","author":"Okada","year":"2018","journal-title":"Reprod. Med. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"336","DOI":"10.1177\/1933719108317975","article-title":"Review Article: Steroid Hormones and Uterine Vascular Adaptation to Pregnancy","volume":"15","author":"Chang","year":"2008","journal-title":"Reprod. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"e13333","DOI":"10.1111\/asj.13333","article-title":"The Potential Function of Endometrial-Secreted Factors for Endometrium Remodeling during the Estrous Cycle","volume":"91","author":"Billhaq","year":"2020","journal-title":"Anim. Sci. J."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"S10","DOI":"10.1016\/S0301-2115(03)00168-4","article-title":"Angiogenesis and Vasculogenesis in Pregnancy","volume":"110","author":"Zygmunt","year":"2003","journal-title":"Eur. J. Obstet. Gynecol. Reprod. Biol."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Massri, N., Loia, R., Sones, J.L., Arora, R., and Douglas, N.C. (2023). Vascular Changes in the Cycling and Early Pregnant Uterus. JCI Insight, 8.","DOI":"10.1172\/jci.insight.163422"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1016\/S1043-2760(01)00379-4","article-title":"Regulation of Angiogenesis in the Endometrium","volume":"12","author":"Smith","year":"2001","journal-title":"Trends Endocrinol. Metab."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"413","DOI":"10.1016\/0143-4004(95)90100-0","article-title":"Characteristic\u2019s of Trophoblast Cells Migrating from First Trimester Chorionic Villus Explants and Propagated in Culture","volume":"16","author":"Irving","year":"1995","journal-title":"Placenta"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"a023010","DOI":"10.1101\/cshperspect.a023010","article-title":"Molecular Cross-Talk at the Feto-Maternal Interface","volume":"5","author":"Lash","year":"2015","journal-title":"Cold Spring Harb. Perspect. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"369","DOI":"10.1007\/BF00049525","article-title":"Mechanisms of Trophoblast Invasiveness and Their Control: The Role of Proteases and Protease Inhibitors","volume":"9","author":"Lala","year":"1990","journal-title":"Cancer Metastasis Rev."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1093\/humupd\/2.4.307","article-title":"Trophoblast Migration during Human Placental Implantation","volume":"2","author":"Burrows","year":"1996","journal-title":"Hum. Reprod. Update"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/aji.12466","article-title":"Decidual Control of Trophoblast Invasion","volume":"75","author":"Sharma","year":"2016","journal-title":"Am. J. Reprod. Immunol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1093\/humrep\/der019","article-title":"Decidual HtrA3 Negatively Regulates Trophoblast Invasion during Human Placentation","volume":"26","author":"Singh","year":"2011","journal-title":"Hum. Reprod."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"397","DOI":"10.1016\/j.thromres.2004.06.038","article-title":"Growth and Function of the Normal Human Placenta","volume":"114","author":"Gude","year":"2004","journal-title":"Thromb. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1067\/mob.2001.108075","article-title":"Placental Glucose Transport in Gestational Diabetes Mellitus","volume":"184","author":"Jansson","year":"2001","journal-title":"Am. J. Obstet. Gynecol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1016\/S1521-6934(02)00130-X","article-title":"The Endometrium as a Cause of Implantation Failure","volume":"17","author":"Sharkey","year":"2003","journal-title":"Best Pract. Res. Clin. Obstet. Gynaecol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1053\/plac.1999.0448","article-title":"Current Topic: Glucose Transporters in the Human Placenta","volume":"21","author":"Illsley","year":"2000","journal-title":"Placenta"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Apicella, C., Ruano, C.S.M., Thilaganathan, B., Khalil, A., Giorgione, V., Gascoin, G., Marcellin, L., Gaspar, C., Jacques, S., and Murdoch, C.E. (2023). Pan-Genomic Regulation of Gene Expression in Normal and Pathological Human Placentas. Cells, 12.","DOI":"10.3390\/cells12040578"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"479","DOI":"10.1038\/s41574-020-0372-6","article-title":"Tracking Placental Development in Health and Disease","volume":"16","author":"Aplin","year":"2020","journal-title":"Nat. Rev. Endocrinol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1038\/s41556-018-0250-9","article-title":"Specificities of Secretion and Uptake of Exosomes and Other Extracellular Vesicles for Cell-to-Cell Communication","volume":"21","author":"Mathieu","year":"2019","journal-title":"Nat. Cell Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"20304","DOI":"10.3402\/jev.v2i0.20304","article-title":"Emerging Roles of Extracellular Vesicles in the Adaptive Response of Tumour Cells to Microenvironmental Stress","volume":"2","author":"Kucharzewska","year":"2013","journal-title":"J. Extracell. Vesicles"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"5210","DOI":"10.1038\/s41598-017-05549-w","article-title":"Secretome of in Vitro Cultured Human Embryos Contains Extracellular Vesicles That Are Uptaken by the Maternal Side","volume":"7","author":"Giacomini","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"340","DOI":"10.4049\/jimmunol.0803477","article-title":"Human Placenta Expresses and Secretes NKG2D Ligands via Exosomes That Down-Modulate the Cognate Receptor Expression: Evidence for Immunosuppressive Function 1","volume":"183","author":"Hedlund","year":"2009","journal-title":"J. Immunol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e2200252119","DOI":"10.1073\/pnas.2200252119","article-title":"Extracellular Vesicles Secreted by Human Uterine Stromal Cells Regulate Decidualization, Angiogenesis, and Trophoblast Differentiation","volume":"119","author":"Ma","year":"2022","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_31","doi-asserted-by":"crossref","unstructured":"Segura-Ben\u00edtez, M., Carbajo-Garc\u00eda, M.C., Corach\u00e1n, A., Faus, A., Pellicer, A., and Ferrero, H. (2022). Proteomic Analysis of Extracellular Vesicles Secreted by Primary Human Epithelial Endometrial Cells Reveals Key Proteins Related to Embryo Implantation. Reprod. Biol. Endocrinol., 20.","DOI":"10.1186\/s12958-021-00879-x"},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Harris, E.A., Stephens, K.K., and Winuthayanon, W. (2020). Extracellular Vesicles and the Oviduct Function. Int. J. Mol. Sci., 21.","DOI":"10.20944\/preprints202010.0638.v1"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1038\/nrm.2017.125","article-title":"Shedding Light on the Cell Biology of Extracellular Vesicles","volume":"19","author":"Raposo","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1535750","DOI":"10.1080\/20013078.2018.1535750","article-title":"Minimal Information for Studies of Extracellular Vesicles 2018 (MISEV2018): A Position Statement of the International Society for Extracellular Vesicles and Update of the MISEV2014 Guidelines","volume":"7","author":"Witwer","year":"2018","journal-title":"J. Extracell. Vesicles"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"bqac165","DOI":"10.1210\/endocr\/bqac165","article-title":"Extracellular Vesicles Secreted by Mouse Decidual Cells Carry Critical Information for the Establishment of Pregnancy","volume":"163","author":"Ma","year":"2022","journal-title":"Endocrinology"},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"14532","DOI":"10.1073\/pnas.2000810117","article-title":"A Hypoxia-Induced Rab Pathway Regulates Embryo Implantation by Controlled Trafficking of Secretory Granules","volume":"117","author":"Bhurke","year":"2020","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"354","DOI":"10.1177\/1933719112472738","article-title":"The Mesenchymal\u2014Epithelial Transition During In Vitro Decidualization","volume":"20","author":"Zhang","year":"2013","journal-title":"Reprod. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Ng, Y.H., Rome, S., Jalabert, A., Forterre, A., Singh, H., Hincks, C.L., and Salamonsen, L.A. (2013). Endometrial Exosomes\/Microvesicles in the Uterine Microenvironment: A New Paradigm for Embryo-Endometrial Cross Talk at Implantation. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0058502"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3210","DOI":"10.1242\/dev.124289","article-title":"Hsa-MiR-30d, Secreted by the Human Endometrium, Is Taken up by the Pre-Implantation Embryo and Might Modify Its Transcriptome","volume":"142","author":"Vilella","year":"2015","journal-title":"Development"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1530\/REP-14-0538","article-title":"Exosomes, Endogenous Retroviruses and Toll-like Receptors: Pregnancy Recognition in Ewes","volume":"149","author":"Xu","year":"2015","journal-title":"Reproduction"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1007\/s00441-016-2358-1","article-title":"Exosomes Derived from Endometriotic Stromal Cells Have Enhanced Angiogenic Effects in Vitro","volume":"365","author":"Harp","year":"2016","journal-title":"Cell Tissue Res."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"146337","DOI":"10.1016\/j.gene.2022.146337","article-title":"Transcriptome Regulation of Extracellular Vesicles Derived from Porcine Uterine Flushing Fluids during Peri-Implantation on Endometrial Epithelial Cells and Embryonic Trophoblast Cells","volume":"822","author":"Hua","year":"2022","journal-title":"Gene"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1516","DOI":"10.1210\/clinem\/dgab045","article-title":"Characterization and Proteomic Analysis of Endometrial Stromal Cell\u2013Derived Small Extracellular Vesicles","volume":"106","author":"Hsu","year":"2021","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"2000211","DOI":"10.1002\/pmic.202000211","article-title":"Proteomic Profiling of Human Uterine Extracellular Vesicles Reveal Dynamic Regulation of Key Players of Embryo Implantation and Fertility during Menstrual Cycle","volume":"21","author":"Rai","year":"2021","journal-title":"Proteomics"},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Marinaro, F., G\u00f3mez-Serrano, M., Jorge, I., Silla-Castro, J.C., V\u00e1zquez, J., S\u00e1nchez-Margallo, F.M., Bl\u00e1zquez, R., L\u00f3pez, E., \u00c1lvarez, V., and Casado, J.G. (2019). Unraveling the Molecular Signature of Extracellular Vesicles from Endometrial-Derived Mesenchymal Stem Cells: Potential Modulatory Effects and Therapeutic Applications. Front. Bioeng. Biotechnol., 7.","DOI":"10.3389\/fbioe.2019.00431"},{"key":"ref_46","doi-asserted-by":"crossref","unstructured":"Burns, G.W., Brooks, K.E., and Spencer, T.E. (2016). Extracellular Vesicles Originate from the Conceptus and Uterus During Early Pregnancy in Sheep 1. Biol. Reprod., 94.","DOI":"10.1095\/biolreprod.115.134973"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"8","DOI":"10.1016\/j.theriogenology.2021.10.021","article-title":"Porcine Uterine Luminal Fluid-Derived Extracellular Vesicles Improve Conceptus-Endometrial Interaction during Implantation","volume":"178","author":"Hu","year":"2022","journal-title":"Theriogenology"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"145117","DOI":"10.1016\/j.gene.2020.145117","article-title":"Small RNA-Seq Analysis of Extracellular Vesicles from Porcine Uterine Flushing Fluids during Peri-Implantation","volume":"766","author":"Hua","year":"2021","journal-title":"Gene"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1164","DOI":"10.1007\/s43032-019-00115-3","article-title":"Mir-Let-7a\/g Enhances Uterine Receptivity via Suppressing Wnt\/\u03b2-Catenin Under the Modulation of Ovarian Hormones","volume":"27","author":"Li","year":"2020","journal-title":"Reprod. Sci."},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Greening, D.W., Nguyen, H.P.T., Elgass, K., Simpson, R.J., and Salamonsen, L.A. (2016). Human Endometrial Exosomes Contain Hormone-Specific Cargo Modulating Trophoblast Adhesive Capacity: Insights into Endometrial-Embryo Interactions 1. Biol. Reprod., 94.","DOI":"10.1095\/biolreprod.115.134890"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"612","DOI":"10.1093\/biolre\/ioy011","article-title":"Progesterone Effects on Extracellular Vesicles in the Sheep Uterus \u2020","volume":"98","author":"Burns","year":"2018","journal-title":"Biol. Reprod."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1530\/REP-18-0616","article-title":"Decidual Small Extracellular Vesicles Induce Trophoblast Invasion by Upregulating N-Cadherin","volume":"159","author":"Liu","year":"2020","journal-title":"Reproduction"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1016\/j.diff.2013.11.005","article-title":"Pig Blastocyst\u2013Uterine Interactions","volume":"87","author":"Bazer","year":"2014","journal-title":"Differentiation"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Burns, G., Brooks, K., Wildung, M., Navakanitworakul, R., Christenson, L.K., and Spencer, T.E. (2014). Extracellular Vesicles in Luminal Fluid of the Ovine Uterus. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0090913"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"F33","DOI":"10.1530\/REP-17-0432","article-title":"Interferon-Tau and Fertility in Ruminants","volume":"154","author":"Forde","year":"2017","journal-title":"Reproduction"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1007\/s10456-023-09876-7","article-title":"Pathological Angiogenesis: Mechanisms and Therapeutic Strategies","volume":"26","author":"Dudley","year":"2023","journal-title":"Angiogenesis"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"1603","DOI":"10.1242\/jcs.064386","article-title":"Microvesicles: Mediators of Extracellular Communication during Cancer Progression","volume":"123","author":"Clancy","year":"2010","journal-title":"J. Cell Sci."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.jphotobiol.2018.03.010","article-title":"Stereological and Molecular Studies on the Combined Effects of Photobiomodulation and Human Bone Marrow Mesenchymal Stem Cell Conditioned Medium on Wound Healing in Diabetic Rats","volume":"182","author":"Amini","year":"2018","journal-title":"J. Photochem. Photobiol. B"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1131","DOI":"10.5966\/sctm.2015-0078","article-title":"Extracellular Vesicles Improve Post-Stroke Neuroregeneration and Prevent Postischemic Immunosuppression","volume":"4","author":"Doeppner","year":"2015","journal-title":"Stem Cells Transl. Med."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"804","DOI":"10.1111\/j.1447-0756.2011.01800.x","article-title":"Effect of Menstrual Blood-Derived Stromal Stem Cells on Proliferative Capacity of Peripheral Blood Mononuclear Cells in Allogeneic Mixed Lymphocyte Reaction","volume":"38","author":"Nikoo","year":"2012","journal-title":"J. Obstet. Gynaecol. Res."},{"key":"ref_61","doi-asserted-by":"crossref","unstructured":"Aldhamen, Y.A., Seregin, S.S., Rastall, D.P.W., Aylsworth, C.F., Pepelyayeva, Y., Busuito, C.J., Godbehere-Roosa, S., Kim, S., and Amalfitano, A. (2013). Endoplasmic Reticulum Aminopeptidase-1 Functions Regulate Key Aspects of the Innate Immune Response. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0069539"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.placenta.2017.02.025","article-title":"Tumour and Placenta Establishment: The Importance of Antigen Processing and Presentation","volume":"56","author":"Reeves","year":"2017","journal-title":"Placenta"},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Nooshabadi, V.T., Verdi, J., Ebrahimi-Barough, S., Mowla, J., Atlasi, M.A., Mazoochi, T., Valipour, E., Shafiei, S., Ai, J., and Banafshe, H.R. (2019). Endometrial Mesenchymal Stem Cell-Derived Exosome Promote Endothelial Cell Angiogenesis in a Dose Dependent Manner: A New Perspective on Regenerative Medicine and Cell-Free Therapy. Arch. Neurosci., 6.","DOI":"10.5812\/ans.94041"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"60","DOI":"10.1016\/j.semcdb.2015.02.008","article-title":"Emerging Roles of Exosomes during Epithelial\u2013Mesenchymal Transition and Cancer Progression","volume":"40","author":"Greening","year":"2015","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.semcancer.2020.11.022","article-title":"Diverse Roles of EV-RNA in Cancer Progression","volume":"75","author":"Cocks","year":"2021","journal-title":"Semin. Cancer Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"3719","DOI":"10.1111\/jcmm.13676","article-title":"Emerging Role of Exosome Signalling in Maintaining Cancer Stem Cell Dynamic Equilibrium","volume":"22","author":"Sun","year":"2018","journal-title":"J. Cell. Mol. Med."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"1061076","DOI":"10.3389\/fnmol.2022.1061076","article-title":"Extracellular Vesicles in Neurodegenerative Diseases: A Systematic Review","volume":"15","author":"Raghav","year":"2022","journal-title":"Front. Mol. Neurosci."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"1625677","DOI":"10.1080\/20013078.2019.1625677","article-title":"Extracellular Vesicles in Type 2 Diabetes Mellitus: Key Roles in Pathogenesis, Complications, and Therapy","volume":"8","author":"Xiao","year":"2019","journal-title":"J. Extracell. Vesicles"},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.molimm.2017.11.016","article-title":"Role of Extracellular Vesicles in Rheumatoid Arthritis","volume":"93","author":"Fu","year":"2018","journal-title":"Mol. Immunol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1056\/NEJMra0804690","article-title":"Endometriosis","volume":"360","author":"Bulun","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_71","first-page":"93","article-title":"Metastatic or Embolic Endometriosis, Due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation","volume":"3","author":"Sampson","year":"1927","journal-title":"Am. J. Pathol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"649","DOI":"10.1093\/biolre\/ioy212","article-title":"Eutopic Stromal Cells of Endometriosis Promote Neuroangiogenesis via Exosome Pathway \u2020","volume":"100","author":"Sun","year":"2019","journal-title":"Biol. Reprod."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"e128846","DOI":"10.1172\/jci.insight.128846","article-title":"Extracellular Vesicles from Endometriosis Patients Are Characterized by a Unique MiRNA-LncRNA Signature","volume":"4","author":"Khalaj","year":"2019","journal-title":"JCI Insight"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1093\/humupd\/dmz018","article-title":"The Endometrial Immune Environment of Women with Endometriosis","volume":"25","author":"Houshdaran","year":"2019","journal-title":"Hum. Reprod. Update"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1093\/molehr\/gay049","article-title":"Macrophages Alternatively Activated by Endometriosis-Exosomes Contribute to the Development of Lesions in Mice","volume":"25","author":"Sun","year":"2019","journal-title":"MHR Basic Sci. Reprod. Med."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"547","DOI":"10.2353\/ajpath.2009.081011","article-title":"Macrophages Are Alternatively Activated in Patients with Endometriosis and Required for Growth and Vascularization of Lesions in a Mouse Model of Disease","volume":"175","author":"Bacci","year":"2009","journal-title":"Am. J. Pathol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1155","DOI":"10.2147\/IJN.S354314","article-title":"Exosomal LncRNA HOTAIR Promotes the Progression and Angiogenesis of Endometriosis via the MiR-761\/HDAC1 Axis and Activation of STAT3-Mediated Inflammation","volume":"17","author":"Zhang","year":"2022","journal-title":"Int. J. Nanomed."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1055\/s-0040-1716687","article-title":"Adenomyosis: Mechanisms and Pathogenesis","volume":"38","author":"Zhai","year":"2020","journal-title":"Semin. Reprod. Med."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1093\/humupd\/dmg010","article-title":"Uterine Adenomyosis in the Infertility Clinic","volume":"9","author":"Devlieger","year":"2003","journal-title":"Hum. Reprod. Update"},{"key":"ref_80","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_81","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1042\/BCJ20160006","article-title":"Extracellular Vesicles: Their Role in Cancer Biology and Epithelial\u2013Mesenchymal Transition","volume":"474","author":"Gopal","year":"2017","journal-title":"Biochem. J."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"643","DOI":"10.1016\/j.bbrc.2016.07.124","article-title":"Exosome Cargo Reflects TGF-\u03921-Mediated Epithelial-to-Mesenchymal Transition (EMT) Status in A549 Human Lung Adenocarcinoma Cells","volume":"478","author":"Kim","year":"2016","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"636","DOI":"10.1016\/j.gendis.2020.01.011","article-title":"Adenomyosis-Derived Extracellular Vesicles Endow Endometrial Epithelial Cells with an Invasive Phenotype through Epithelial-Mesenchymal Transition","volume":"7","author":"Chen","year":"2020","journal-title":"Genes Dis."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"58","DOI":"10.1016\/j.jri.2011.12.001","article-title":"The Distribution of Immune Cells and Macrophages in the Endometrium of Women with Recurrent Reproductive Failure. II: Adenomyosis and Macrophages","volume":"93","author":"Tremellen","year":"2012","journal-title":"J. Reprod. Immunol."},{"key":"ref_85","first-page":"46","article-title":"Interaction of Macrophages and Endometrial Cells Induces Epithelial\u2013Mesenchymal Transition-like Processes in Adenomyosis","volume":"96","author":"An","year":"2017","journal-title":"Biol. Reprod."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"584","DOI":"10.1093\/biolre\/ioad015","article-title":"Extracellular Vesicles Contribute to EMT in Adenomyosis by Inducing Macrophage Polarization \u2020","volume":"108","author":"Hu","year":"2023","journal-title":"Biol. Reprod."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"470","DOI":"10.1016\/j.rbmo.2022.12.008","article-title":"Extracellular Vesicles Secreted by Adenomyosis Endometrial Organoids Contain MiRNAs Involved in Embryo Implantation and Pregnancy","volume":"46","author":"Faus","year":"2023","journal-title":"Reprod. Biomed. Online"},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Practice Committee for the American Society for Reproductive Medicine (2015). Diagnostic Evaluation of the Infertile Female: A Committee Opinion. Fertil. Steril., 103, e44\u2013e50.","DOI":"10.1016\/j.fertnstert.2015.03.019"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"2249","DOI":"10.1093\/humrep\/deab123","article-title":"Global Transcriptomic Changes Occur in Uterine Fluid-Derived Extracellular Vesicles during the Endometrial Window for Embryo Implantation","volume":"36","author":"Giacomini","year":"2021","journal-title":"Hum. Reprod."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"1327","DOI":"10.1016\/j.fertnstert.2020.10.046","article-title":"Cargo Small Non-Coding RNAs of Extracellular Vesicles Isolated from Uterine Fluid Associate with Endometrial Receptivity and Implantation Success","volume":"115","author":"Li","year":"2021","journal-title":"Fertil. Steril."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"427","DOI":"10.1016\/j.juro.2013.08.083","article-title":"Out-of-Pocket Fertility Patient Expense: Data from a Multicenter Prospective Infertility Cohort","volume":"191","author":"Wu","year":"2014","journal-title":"J. Urol."},{"key":"ref_92","doi-asserted-by":"crossref","unstructured":"Rubin, S.C., Abdulkadir, M., Lewis, J., Harutyunyan, A., Hirani, R., and Grimes, C.L. (2023). Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications. J. Pers. Med., 13.","DOI":"10.3390\/jpm13050749"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/j.fertnstert.2010.04.063","article-title":"A Genomic Diagnostic Tool for Human Endometrial Receptivity Based on the Transcriptomic Signature","volume":"95","author":"Horcajadas","year":"2011","journal-title":"Fertil. Steril."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"618","DOI":"10.1016\/j.fertnstert.2019.02.011","article-title":"Clinical Approach to Recurrent Implantation Failure: Evidence-Based Evaluation of the Endometrium","volume":"111","author":"Kliman","year":"2019","journal-title":"Fertil. Steril."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"394","DOI":"10.3322\/caac.21492","article-title":"Global Cancer Statistics 2018: GLOBOCAN Estimates of Incidence and Mortality Worldwide for 36 Cancers in 185 Countries","volume":"68","author":"Bray","year":"2018","journal-title":"CA Cancer J. Clin."},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Roman-Canal, B., Moiola, C.P., Gatius, S., Bonnin, S., Ruiz-Mir\u00f3, M., Gonz\u00e1lez, E., Gonz\u00e1lez-Tallada, X., Llordella, I., Hern\u00e1ndez, I., and Porcel, J.M. (2019). EV-Associated MiRNAs from Peritoneal Lavage Are a Source of Biomarkers in Endometrial Cancer. Cancers, 11.","DOI":"10.3390\/cancers11060839"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"187","DOI":"10.2217\/epi-2017-0109","article-title":"Circular RNA Expression in Extracellular Vesicles Isolated from Serum of Patients with Endometrial Cancer","volume":"10","author":"Xu","year":"2018","journal-title":"Epigenomics"},{"key":"ref_98","doi-asserted-by":"crossref","unstructured":"Sykaras, A.G., Christofidis, K., Politi, E., and Theocharis, S. (2022). Exosomes on Endometrial Cancer: A Biomarkers Treasure Trove?. Cancers, 14.","DOI":"10.3390\/cancers14071733"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1007\/s40572-022-00357-5","article-title":"Environmental Exposures and Extracellular Vesicles: Indicators of Systemic Effects and Human Disease","volume":"9","author":"Eckhardt","year":"2022","journal-title":"Curr. Environ. Health Rep."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1186\/s12964-021-00782-3","article-title":"Extracellular Vesicles from Maternal Uterine Cells Exposed to Risk Factors Cause Fetal Inflammatory Response","volume":"19","author":"Shepherd","year":"2021","journal-title":"Cell Commun. Signal."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"608","DOI":"10.1038\/s41598-018-37002-x","article-title":"Exosomes Cause Preterm Birth in Mice: Evidence for Paracrine Signaling in Pregnancy","volume":"9","author":"Trivedi","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"582","DOI":"10.1016\/j.envint.2018.09.052","article-title":"Urinary Trace Metals Individually and in Mixtures in Association with Preterm Birth","volume":"121","author":"Kim","year":"2018","journal-title":"Environ. Int."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"105370","DOI":"10.1016\/j.envint.2019.105370","article-title":"Exposure to Multiple Metals in Early Pregnancy and Gestational Diabetes Mellitus: A Prospective Cohort Study","volume":"135","author":"Wang","year":"2020","journal-title":"Environ. Int."},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"110388","DOI":"10.1016\/j.envres.2020.110388","article-title":"Prenatal Metal Mixtures and Fetal Size in Mid-Pregnancy in the MADRES Study","volume":"196","author":"Howe","year":"2021","journal-title":"Environ. Res."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1128","DOI":"10.1080\/15592294.2021.1994189","article-title":"Urinary Metals and Maternal Circulating Extracellular Vesicle MicroRNA in the MADRES Pregnancy Cohort","volume":"17","author":"Howe","year":"2022","journal-title":"Epigenetics"}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/22\/2584\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T21:18:32Z","timestamp":1760131112000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/12\/22\/2584"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,11,7]]},"references-count":105,"journal-issue":{"issue":"22","published-online":{"date-parts":[[2023,11]]}},"alternative-id":["cells12222584"],"URL":"https:\/\/doi.org\/10.3390\/cells12222584","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,11,7]]}}}