HIGHLIGHTS
- •miRNA cargo of adenomyosis secretory phase EVs promote implantation failure.
- •miRNA cargo of adenomyosis gestational phase EVs promote pregnancy disorders.
- •Adenomyotic-miRNAs modulate mechanisms involved in adenomyosis-related infertility.
- •Adenomyotic-miRNAs may be potential biomarkers of adenomyosis reproductive outcomes.
Abstract
Research question
Do extracellular vesicles secreted by the endometrium of women with adenomyosis contain
miRNAs involved in adenomyosis-related infertility?
Design
A descriptive study using organoids from eutopic endometrium of women with adenomyosis
(n = 4) generated and differentiated to secretory and gestational phases, in which miRNA
cargo from extracellular vesicles secreted by these differentiated organoids in each
phase was analysed by next-generation sequencing. miRNAs in secretory-extracellular
vesicles and gestational-extracellular vesicles were selected based on the counts
per million. miRNAs target genes in each phase were obtained from miRNet and gene
ontology was used for enrichment analysis.
Results
miRNA sequencing identified 80 miRNAs in secretory-phase extracellular vesicles, including
hsa-miR-21-5p, hsa-miR-24-3p, hsa-miR-26a-5p, hsa-miR-92a-3p, hsa-miR-92b-3p, hsa-miR-200c-3p
and hsa-miR-423a-5p, related to adenomyosis pathogenesis and implantation failure.
Further, 60 miRNAs were identified in gestational-phase extracellular vesicles, including
hsa-miR-21-5p, hsa-miR-26a-5p, hsa-miR-30a-5p, hsa-miR-30c-5p, hsa-miR-222-3p and
hsa-miR-423a-5p were associated with preeclampsia and miscarriage. Among the target
genes of these miRNAs, PTEN, MDM4, PLAGL2 and CELF1, whose downregulation (P = 0.0003, P < 0.0001, P = 0.0002 and P = 0.0003, respectively) contributes to adenomyosis pathogenesis, and impaired early
embryo development, leading to implantation failure and miscarriage, are highlihghted.
Further, functional enrichment analyses of the target genes revealed their involvement
in cell differentiation, proliferation, apoptosis, cell cycle regulation and response
to extracellular stimuli.
Conclusions
Eutopic endometrium in secretory and gestational phase from women with adenomyosis
releases extracellular vesicles containing miRNAs involved in adenomyosis progression,
impaired embryo implantation and pregnancy complications.
Graphical abstract
Graphical Abstract
KEYWORDS
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References
- Extracellular vesicles from organoids and 3D culture systems.Biotechnol Bioeng. 2021; 118: 1029-1049https://doi.org/10.1002/bit.27606
- Introduction to Extracellular Vesicles: Biogenesis, RNA Cargo Selection, Content, Release, and Uptake.Cell Mol Neurobiol. 2016; 36: 301-312https://doi.org/10.1007/s10571-016-0366-z
- Expression levels of maternal plasma microRNAs in preeclamptic pregnancies.J Obstet Gynaecol (Lahore). 2021; 41: 910-914https://doi.org/10.1080/01443615.2020.1820465
- Organoid systems to study the human female reproductive tract and pregnancy.Cell Death Differ. 2021; 28: 35-51https://doi.org/10.1038/s41418-020-0565-5
- MicroRNAs in endometriosis: biological function and emerging biomarker candidates†.Biol Reprod. 2019; 100: 1135-1146https://doi.org/10.1093/biolre/ioz014
- MicroRNA-92a Controls Angiogenesis and Functional Recovery of Ischemic Tissues in Mice.Science. 2009; 324: 1710-1713https://doi.org/10.1126/science.1174381
- Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening.Nat Cell Biol. 2019; 21: 1041-1051https://doi.org/10.1038/s41556-019-0360-z
- Analysis of Reciprocally Dysregulated miRNAs in Eutopic Endometrium Is a Promising Approach for Low Invasive Diagnostics of Adenomyosis.Diagnostics. 2020; 10: 782https://doi.org/10.3390/diagnostics10100782
- Defective myometrial spiral artery remodelling as a cause of major obstetrical syndromes in endometriosis and adenomyosis.Placenta. 2013; 34: 100-105https://doi.org/10.1016/j.placenta.2012.11.017
- BBMerge – Accurate paired shotgun read merging via overlap.PLoS One. 2017; 12e0185056https://doi.org/10.1371/journal.pone.0185056
- Characterization of the small RNA transcriptomes of cell protrusions and cell bodies of highly metastatic hepatocellular carcinoma cells via RNA sequencing.Oncol Lett. 2021; 22: 568https://doi.org/10.3892/ol.2021.12829
- Infertility and Adenomyosis.Obstet Gynecol Int. 2012; 2012: 1-8https://doi.org/10.1155/2012/786132
- Integrative analysis of the DNA methylome and transcriptome in uterine leiomyoma shows altered regulation of genes involved in metabolism, proliferation, extracellular matrix and vesicles.J Pathol. 2022; (n/a)https://doi.org/10.1002/path.5920
- CELF1 is a central node in post-transcriptional regulatory programmes underlying EMT.Nat Commun. 2016; 7: 13362https://doi.org/10.1038/ncomms13362
- A novel platform for discovery of differentially expressed microRNAs in patients with repeated implantation failure.Fertil Steril. 2021; 116: 181-188https://doi.org/10.1016/j.fertnstert.2021.01.055
- Adenomyosis-derived extracellular vesicles endow endometrial epithelial cells with an invasive phenotype through epithelial-mesenchymal transition.Genes Dis. 2020; 7: 636-648https://doi.org/10.1016/j.gendis.2020.01.011
- MicroRNA expression profiles in placenta with severe preeclampsia using a PNA-based microarray.Placenta. 2013; 34: 799-804https://doi.org/10.1016/j.placenta.2013.06.006
- Biogenesis, Secretion, and Intercellular Interactions of Exosomes and Other Extracellular Vesicles.Annu Rev Cell Dev Biol. 2014; 30: 255-289https://doi.org/10.1146/annurev-cellbio-101512-122326
- Embryo morphokinetic score is associated with biomarkers of developmental competence and implantation.J Assist Reprod Genet. 2021; 38: 1737-1743https://doi.org/10.1007/s10815-021-02162-9
- Extracellular vesicles: Mediators of embryo-maternal crosstalk during pregnancy and a new weapon to fight against infertility.Eur J Cell Biol. 2020; 99151125https://doi.org/10.1016/j.ejcb.2020.151125
- New insights into the mechanisms of epithelial–mesenchymal transition and implications for cancer.Nat Rev Mol Cell Biol. 2019; https://doi.org/10.1038/s41580-018-0080-4
- Proteogenomic Characterization of Endometrial Carcinoma.Cell. 2020; 180 (729-748.e26)https://doi.org/10.1016/j.cell.2020.01.026
- Exosomes as Biomarkers for Female Reproductive Diseases Diagnosis and Therapy.Int J Mol Sci. 2021; 22: 2165https://doi.org/10.3390/ijms22042165
- Human Endometrial Extracellular Vesicles Functionally Prepare Human Trophectoderm Model for Implantation: Understanding Bidirectional Maternal-Embryo Communication.Proteomics. 2019; 191800423https://doi.org/10.1002/pmic.201800423
- MicroRNA-24 Regulates Vascularity After Myocardial Infarction.Circulation. 2011; 124: 720-730https://doi.org/10.1161/CIRCULATIONAHA.111.039008
- Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?.Nat Rev Genet. 2008; 9: 102-114https://doi.org/10.1038/nrg2290
- HOXA10 expression is decreased in endometrium of women with adenomyosis.Fertil Steril. 2011; 95: 1133-1136https://doi.org/10.1016/j.fertnstert.2010.09.060
- Bioengineering trends in female reproduction: a systematic review.Hum Reprod Update. 2022; : dmac025https://doi.org/10.1093/humupd/dmac025
- Exosomes and their cargo are important regulators of cell function in endometriosis.Reprod Biomed Online. 2021; 43: 370-378https://doi.org/10.1016/j.rbmo.2021.05.022
- MicroRNA-26a regulates insulin sensitivity and metabolism of glucose and lipids.Journal of Clinical Investigation. 2015; 125: 2497-2509https://doi.org/10.1172/JCI75438
- ShinyGO: a graphical enrichment tool for ani-mals and plants.bioRxiv. 2018; 36315150https://doi.org/10.1101/082511.Lai
- Docosahexaenoic Acid Modulates the Enterocyte Caco-2 Cell Expression of MicroRNAs Involved in Lipid Metabolism.J Nutr. 2014; 144: 575-585https://doi.org/10.3945/jn.113.189050
- Main actors behind the endometrial receptivity and successful implantation.Tissue Cell. 2021; https://doi.org/10.1016/j.tice.2021.101656
- MicroRNA-423–5p inhibits the progression of trophoblast cells via targeting IGF2BP1.Placenta. 2018; 74: 1-8https://doi.org/10.1016/j.placenta.2018.12.003
- Exosomes and soluble secretome from hormone-treated endometrial epithelial cells direct embryo implantation.Mol Hum Reprod. 2020; 26: 510-520https://doi.org/10.1093/molehr/gaaa034
- Abnormally located SSEA1+/SOX9+ endometrial epithelial cells with a basalis-like phenotype in the eutopic functionalis layer may play a role in the pathogenesis of endometriosis.Human Reproduction. 2019; 34: 56-68https://doi.org/10.1093/humrep/dey336
- Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro.Cell Tissue Res. 2016; 365: 187-196https://doi.org/10.1007/s00441-016-2358-1
- Adenomyosis and adverse perinatal outcomes: increased risk of second trimester miscarriage, preeclampsia, and placental malposition.The Journal of Maternal-Fetal & Neonatal Medicine. 2018; 31: 364-369https://doi.org/10.1080/14767058.2017.1285895
- Regulation of NF-κB by TNF family cytokines.Semin Immunol. 2014; 26: 253-266https://doi.org/10.1016/j.smim.2014.05.004
- Organoid technology in female reproductive biomedicine.Reproductive Biology and Endocrinology. 2020; 18: 64https://doi.org/10.1186/s12958-020-00621-z
- Global Transcriptome Abnormalities of the Eutopic Endometrium From Women With Adenomyosis.Reprod Sci. 2016; 23: 1289-1303https://doi.org/10.1177/1933719116650758
- Diagnostic Potential of MicroRNAs as Biomarkers in the Detection of Preeclampsia.Genet Test Mol Biomarkers. 2020; 24: 321-327https://doi.org/10.1089/gtmb.2019.0264
- MicroRNA expression profiling in placenta and maternal plasma in early pregnancy loss.Mol Med Rep. 2018; 17: 4941-4952https://doi.org/10.3892/mmr.2018.8530
- Association Analysis in Young and Middle-Aged Mothers—Relation between Expression of Cardiovascular Disease Associated MicroRNAs and Abnormal Clinical Findings.J Pers Med. 2021; 11: 39https://doi.org/10.3390/jpm11010039
- Transcriptome sequencing identified the ceRNA network associated with recurrent spontaneous abortion.BMC Med Genomics. 2021; 14: 278https://doi.org/10.1186/s12920-021-01125-4
- NIH Public Access. 2014; 113: 1231-1241https://doi.org/10.1161/CIRCRESAHA.113.301780.MicroRNA-26a
Ioannidis, J., Donadeu, F.X., 2017. Changes in circulating microRNA levels can be identified as early as day 8 of pregnancy in cattle. PLoS One 12, e0174892. https://doi.org/10.1371/journal.pone.0174892.
- Decreased expression of NR4A nuclear receptors in adenomyosis impairs endometrial decidualization.Mol Hum Reprod. 2016; 22: 655-668https://doi.org/10.1093/molehr/gaw042
- Decreased expression of NR4A nuclear receptors in adenomyosis impairs endometrial decidualization.Mol Hum Reprod. 2016; 22: 655-668https://doi.org/10.1093/molehr/gaw042
- Establishment of Adenomyosis Organoids as a Preclinical Model to Study Infertility.J Pers Med. 2022; 12: 219https://doi.org/10.3390/jpm12020219
- Extracellular vesicles in host-pathogen interactions and immune regulation — exosomes as emerging actors in the immunological theater of pregnancy.Heliyon. 2019; 5: e02355https://doi.org/10.1016/j.heliyon.2019.e02355
- Single-nucleotide polymorphisms in the p53 pathway regulate fertility in humans.Proceedings of the National Academy of Sciences. 2009; 106: 9761-9766https://doi.org/10.1073/pnas.0904280106
- Uterotubal transport disorder in adenomyosis and endometriosis—a cause for infertility.BJOG. 2006; 113: 902-908https://doi.org/10.1111/j.1471-0528.2006.00970.x
- An Essential Role for NF-κB in IL-18-Induced IFN-γ Expression in KG-1 Cells.The Journal of Immunology. 1999; 162: 5063
- Bovine serum miR-21 expression affected by mastitis.Res Vet Sci. 2021; 135: 290-292https://doi.org/10.1016/j.rvsc.2020.10.001
- Isolation and Characterization of RNA-Containing Exosomes.Journal of Visualized Experiments. 2012; : 1-6https://doi.org/10.3791/3037
- Association of miR-34a-3p/5p, miR-141-3p/5p, and miR-24 in Decidual Natural Killer Cells with Unexplained Recurrent Spontaneous Abortion.Medical Science Monitor. 2016; 22: 922-929https://doi.org/10.12659/MSM.895459
- Follistatin dysregulation impaired trophoblast biological functions by GDF11-Smad2/3 axis in preeclampsia placentas.Placenta. 2022; 121: 145-154https://doi.org/10.1016/j.placenta.2022.03.015
- Lin28B/miR-92b Promote the Proliferation, Migration, and Invasion in the Pathogenesis of Preeclampsia via the DKK1/Wnt/β-Catenin Pathway.Reproductive Sciences. 2020; 27: 815-822https://doi.org/10.1007/s43032-019-00083-8
- Role of microRNAs in embryo implantation.Reproductive Biology and Endocrinology. 2017; 15: 1-11https://doi.org/10.1186/s12958-017-0309-7
- The Subread aligner: fast, accurate and scalable read mapping by seed-and-vote.Nucleic Acids Res. 2013; 41 (e108–e108)https://doi.org/10.1093/nar/gkt214
- Tet1 Deficiency Leads to Premature Ovarian Failure.Front Cell Dev Biol. 2021; 9644135https://doi.org/10.3389/fcell.2021.644135
- ZEB1 induced miR-99b/let-7e/miR-125a cluster promotes invasion and metastasis in esophageal squamous cell carcinoma.Cancer Lett. 2017; 398: 37-45https://doi.org/10.1016/j.canlet.2017.04.006
- Window of implantation is significantly displaced in patients with adenomyosis with previous implantation failure as determined by endometrial receptivity assay.J Hum Reprod Sci. 2018; 11: 353https://doi.org/10.4103/jhrs.JHRS_52_18
- Cyclooxygenase 2-derived prostaglandin E2 production by corticotropin-releasing hormone contributes to the activated cAMP response element binding protein content in rheumatoid arthritis synovial tissue.Arthritis Rheum. 2004; 50: 1132-1145https://doi.org/10.1002/art.20157
- MDM4 downregulates p53 transcriptional activity and response to stress during differentiation.Cell Cycle. 2011; 10: 1100-1108https://doi.org/10.4161/cc.10.7.15090
- Apoptosis is increased and cell proliferation is decreased in out-of-phase endometria from infertile and recurrent abortion patients.Reproductive Biology and Endocrinology. 2010; 8: 126https://doi.org/10.1186/1477-7827-8-126
- 基因的改变NIH Public Access.Gerontology. 2015; 61: 515-525https://doi.org/10.4049/jimmunol.1000917.IL-23
- Uterine polyps, adenomyosis, leiomyomas, and endometrial receptivity.Fertil Steril. 2019; 111: 629-640https://doi.org/10.1016/j.fertnstert.2019.02.008
- Inhibition of miR-92a Enhances Fracture Healing via Promoting Angiogenesis in a Model of Stabilized Fracture in Young Mice.Journal of Bone and Mineral Research. 2014; 29: 316-326https://doi.org/10.1002/jbmr.2040
- Differential expression of plasma microRNA in preeclamptic patients at delivery and 1 year postpartum.Am J Obstet Gynecol. 2015; 213 (367.e1-367.e9)https://doi.org/10.1016/j.ajog.2015.05.013
- Characterization of exosomes in peritoneal fluid of endometriosis patients.Fertil Steril. 2020; 113 (364-373.e2)https://doi.org/10.1016/j.fertnstert.2019.09.032
- Investigation of infertility using endometrial organoids.Reproduction. 2021; 161: R113-R127https://doi.org/10.1530/REP-20-0428
- Coupling miR/isomiR and mRNA Expression Signatures Unveils New Molecular Layers of Endometrial Receptivity.Life. 2021; 11: 1391https://doi.org/10.3390/life11121391
Ota, H., 1998. Is adenomyosis an immune disease? Hum Reprod Update 4, 360-367. https://doi.org/10.1093/humupd/4.4.360.
- The role of mesenchymal–epithelial transition in endometrial function.Hum Reprod Update. 2019; 25: 114-133https://doi.org/10.1093/humupd/dmy035
- Chapter 19.The Crucible. Rutgers University Press, 2019: 186-195https://doi.org/10.36019/9780813548203-024
- An Anti-inflammatory microRNA Signature Distinguishes Group 3 Innate Lymphoid Cells From Natural Killer Cells in Human Decidua.Front Immunol. 2020; 11: 1-15https://doi.org/10.3389/fimmu.2020.00133
- The symptomatology of adenomyosis.Best Pract Res Clin Obstet Gynaecol. 2006; 20: 547-555https://doi.org/10.1016/j.bpobgyn.2006.01.006
- Non-coding RNAs as direct and indirect modulators of epigenetic regulation.Epigenetics. 2014; 9: 3-12https://doi.org/10.4161/epi.27473
- Endometrial causes of recurrent pregnancy losses: endometriosis, adenomyosis, and chronic endometritis.Fertil Steril. 2021; 115: 546-560https://doi.org/10.1016/j.fertnstert.2020.12.010
- Adenomyosis in infertile women: prevalence and the role of 3D ultrasound as a marker of severity of the disease.Reproductive Biology and Endocrinology. 2016; 14: 60https://doi.org/10.1186/s12958-016-0185-6
- Upregulated miR-222 targets BCL2L11 and promotes apoptosis of mesenchymal stem cells in preeclampsia patients in response to severe hypoxia.Int J Clin Exp Pathol. 2018; 11: 110-119
- Genome-wide analysis reveals miR-3184-5p and miR-181c-3p as a critical regulator for adipocytes-associated breast cancer.J Cell Physiol. 2019; 234: 17959-17974https://doi.org/10.1002/jcp.28428
- Extracellular vesicles: Exosomes, microvesicles, and friends.Journal of Cell Biology. 2013; 200: 373-383https://doi.org/10.1083/jcb.201211138
- Organoids to model the endometrium: implantation and beyond.Reproduction & fertility. 2021; 2: R85-R101https://doi.org/10.1530/RAF-21-0023
- A scaling normalization method for differential expression analysis of RNA-seq data.Genome Biol. 2010; 11: R25https://doi.org/10.1186/gb-2010-11-3-r25
- Identification of Mammalian microRNA Host Genes and Transcription Units.Genome Res. 2004; 14: 1902-1910https://doi.org/10.1101/gr.2722704
- Identification of MicroRNAs in Human Follicular Fluid: Characterization of MicroRNAs That Govern Steroidogenesis in Vitro and Are Associated With Polycystic Ovary Syndrome in Vivo.J Clin Endocrinol Metab. 2013; 98: 3068-3079https://doi.org/10.1210/jc.2013-1715
- Proteomic analysis of extracellular vesicles secreted by primary human epithelial endometrial cells reveals key proteins related to embryo implantation.Reproductive Biology and Endocrinology. 2022; 20: 3https://doi.org/10.1186/s12958-021-00879-x
- Exosomes: Emerging biomarkers and targets in folliculogenesis and endometriosis.J Reprod Immunol. 2020; 142103181https://doi.org/10.1016/j.jri.2020.103181
- MicroRNA Therapeutics: the Next Magic Bullet?.Mini-Reviews in Medicinal Chemistry. 2015; 15: 467-474https://doi.org/10.2174/1389557515666150324123208
- The evaluation of pinopode formation in patients with adenomyosis.Fertil Steril. 2002; 77: S27https://doi.org/10.1016/S0015-0282(01)03092-8
- Clinical outcomes of infertility treatment for women with adenomyosis in Japan.Reprod Med Biol. 2017; 16: 276-282https://doi.org/10.1002/rmb2.12036
- APEX1/miR-24 axis: a promising therapeutic target in endometriosis.Arch Gynecol Obstet. 2021; 304: 131-141https://doi.org/10.1007/s00404-021-05963-6
Tech, V., Pathology, P., 2007. r Fo Pe er Re vi ew r Fo Pe er Re vi.
- 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.J Extracell Vesicles. 2018; 71535750https://doi.org/10.1080/20013078.2018.1535750
- Identification of potential early biomarkers of preeclampsia.Placenta. 2018; 61: 61-71https://doi.org/10.1016/j.placenta.2017.11.011
- Influence of gestational diabetes mellitus on human umbilical vein endothelial cell miRNA.Clin Sci. 2016; 130: 1955-1967https://doi.org/10.1042/CS20160305
- Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium.Nat Cell Biol. 2017; 19: 568-577https://doi.org/10.1038/ncb3516
- Shedding light on the cell biology of extracellular vesicles.Nat Rev Mol Cell Biol. 2018; 19: 213-228https://doi.org/10.1038/nrm.2017.125
- Adenomyosis and infertility: is there a causal link?.Expert Rev Endocrinol Metab. 2019; 14: 365-367https://doi.org/10.1080/17446651.2019.1697675
- Uterine adenomyosis and in vitro fertilization outcome: a systematic review and meta-analysis.Human Reproduction. 2014; 29: 964-977https://doi.org/10.1093/humrep/deu041
- Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome.Development. 2015; 142: 3210-3221https://doi.org/10.1242/dev.124289
- Uterine fluid microRNAs are dysregulated in women with recurrent implantation failure.Human Reproduction. 2022; 37: 734-746https://doi.org/10.1093/humrep/deac019
- FastQ Screen: A tool for multi-genome mapping and quality control.F1000Res. 2018; 7: 1338https://doi.org/10.12688/f1000research.15931.2
- Circulating microRNAs are elevated in plasma from severe preeclamptic pregnancies.REPRODUCTION. 2012; 143: 389-397https://doi.org/10.1530/REP-11-0304
- PLAGL2 promotes epithelial–mesenchymal transition and mediates colorectal cancer metastasis via β-catenin-dependent regulation of ZEB1.Br J Cancer. 2020; 122: 578-589https://doi.org/10.1038/s41416-019-0679-z
- miRNA–miRNA crosstalk: from genomics to phenomics.Brief Bioinform. 2017; 18: 1002-1011https://doi.org/10.1093/bib/bbw073
- miR-99b promotes metastasis of hepatocellular carcinoma through inhibition of claudin 11 expression and may serve as a prognostic marker.Oncol Rep. 2015; 34: 1415-1423https://doi.org/10.3892/or.2015.4104
- Regulation of interleukin-1 and interleukin-1 inhibitor release by human airway epithelial cells.European Respiratory Journal. 2004; 24: 360-366https://doi.org/10.1183/09031936.04.00089703
- Effects of adenomyosis on in vitro fertilization treatment outcomes: a meta-analysis.Fertil Steril. 2017; 108 (483-490.e3)https://doi.org/10.1016/j.fertnstert.2017.06.025
- Adenomyosis: Mechanisms and Pathogenesis.Semin Reprod Med. 2020; 38https://doi.org/10.1055/s-0040-1716687
- MiR-30c-5p Directly Targets MAPK1 to Regulate the Proliferation, Migration and Invasion of Adenomyotic Epithelial Cells in Adenomyosis.Twin Research and Human Genetics. 2021; 24: 22-28https://doi.org/10.1017/thg.2021.11
- Loss of PP2A and PTEN immunoexpression coexists with survivin overexpression in adenomyosis.Reprod Biol. 2014; 14: 200-205https://doi.org/10.1016/J.REPBIO.2014.04.004
- Long Non-coding RNA Gas5 Is Associated With Preeclampsia and Regulates Biological Behaviors of Trophoblast via MicroRNA-21.Front Genet. 2020; 11https://doi.org/10.3389/fgene.2020.00188
- Circular RNA PUM1 (CircPUM1) attenuates trophoblast cell dysfunction and inflammation in recurrent spontaneous abortion via the MicroRNA-30a-5p (miR-30a-5p)/JUNB axis.Bioengineered. 2021; 12: 6878-6890https://doi.org/10.1080/21655979.2021.1973207
- MicroRNA Regulation of Endothelial Junction Proteins and Clinical Consequence.Mediators Inflamm. 2016; 2016: 1-6https://doi.org/10.1155/2016/5078627
Biography
Elena Juárez-Barber graduated with a master's degree in biotechnology of assisted human reproduction from the University of Valencia. She is pursuing a PhD in biomedicine and biotechnology at IIS-LaFe with PFIS Grant (FI19/00110) from the Institute of Health Carlos III. Her research focuses on new therapeutic targets to treat adenomyosis.
Article info
Publication history
Published online: December 17, 2022
Accepted:
December 13,
2022
Received in revised form:
December 2,
2022
Received:
October 6,
2022
Declaration: The authors report no financial or commercial conflicts of interest.Identification
Copyright
© 2022 Reproductive Healthcare Ltd. Published by Elsevier Ltd. All rights reserved.
