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Exosomal microRNAs and long noncoding RNAs: as novel biomarkers for endometriosis

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Abstract

Endometriosis is a gynecological inflammatory disorder characterized by the development of endometrial-like cells outside the uterine cavity. This disease is associated with a wide range of clinical presentations, such as debilitating pelvic pain and infertility issues. Endometriosis diagnosis is not easily discovered by ultrasound or clinical examination. Indeed, difficulties in noninvasive endometriosis diagnosis delay the confirmation and management of the disorder, increase symptoms, and place a significant medical and financial burden on patients. So, identifying specific and sensitive biomarkers for this disease should therefore be a top goal. Exosomes are extracellular vesicles secreted by most cell types. They transport between cells’ bioactive molecules such as noncoding RNAs and proteins. MicroRNAs and long noncoding RNAs which are key molecules transferred by exosomes have recently been identified to have a significant role in endometriosis by modulating different proteins and their related genes. As a result, the current review focuses on exosomal micro-and-long noncoding RNAs that are involved in endometriosis disease. Furthermore, major molecular mechanisms linking corresponding RNA molecules to endometriosis development will be briefly discussed to better clarify the potential functions of exosomal noncoding RNAs in the therapy and diagnosis of endometriosis.

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Data availability

The data that support the findings of this study are available from the corresponding author, Savardashtaki A, upon reasonable request.

Abbreviations

aHIF:

Antisense hypoxia-inducible factor

ALIX:

ALG-2-interacting protein X

BCL9:

B-cell lymphoma 9

bFGF:

Basic fibroblast growth factor

circRNAs:

Circular RNAs

ECSCs:

Endometriotic cyst stromal cells

EECs:

Endometrial epithelial cells

eESCs:

Ectopic endometrial stromal cells

ENCODE:

Encyclopedia of DNA Elements

ERK:

Extracellular signal-regulated kinases

eRNAs:

Enhancer RNAs

ESCs:

Endometrial stromal cells

ESCRT:

Endosomal sorting complexes required for transport

HEK293:

Human embryonic kidney 293

HIF-1a:

Hypoxia-inducible factor 1a

HMGA2:

High-mobility group AT-hook 2

HOTAIR:

Homeobox transcript antisense RNA

HOXA10:

Homeobox A10

HRS:

Hepatocyte growth factor–regulated tyrosine kinase substrate

Hsp70:

Heat shock protein 70

HUVECs:

Human umbilical vein endothelial cells

ILVs:

Intraluminal vesicles

LIF:

Leukemia inhibitory factor

lincRNAs:

Long intergenic ncRNAs

lncRNAs:

Long ncRNAs

miRNAs:

MicroRNAs

MMP2:

Matrix metalloproteinase 2

MMP9:

Matrix metalloproteinase 9

mRNA:

Messenger RNA

MVBs:

Multivesicular bodies

MVs:

Microvesicles

NATs:

Natural antisense transcripts

ncRNAs:

Noncoding RNAs

PI3P:

Phosphatidylinositol 3-phosphate

PKB:

Protein kinase B

pre-miRNA:

Precursor miRNA

pri-miRNA:

Primary miRNA

STAM1/2:

Signal-transducing adaptor molecule 1/2

SCAI:

Suppressor of cancer cell invasion

sncRNAs:

Small ncRNAs

snoRNAs:

Small nucleolar RNAs

SRA1:

Steroid receptor RNA activator 1

TIMP3:

Tissue inhibitor of metalloproteinase 3

TSG101:

Tumor susceptibility gene 101

uaRNA:

UTR-associated RNA

UTR:

Untranslated region

VEGF:

Vascular endothelial growth factor

VPS4:

Vacuolar protein sorting 4

VTA1:

Vesicle trafficking 1

References

  • Agarwal N, Subramanian A (2010) Endometriosis-morphology, clinical presentations and molecular pathology. Journal of Laboratory Physicians 2:001–009

    Article  Google Scholar 

  • Aghajanova L, Giudice LC (2011) Molecular evidence for differences in endometrium in severe versus mild endometriosis. Reprod Sci 18:229–251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ahn SH, Singh V, Tayade C (2017) Biomarkers in endometriosis: challenges and opportunities. Fertil Steril 107:523–532

    Article  CAS  PubMed  Google Scholar 

  • Annese T, Tamma R, De Giorgis M, Ribatti D (2020) microRNAs biogenesis, functions and role in tumor angiogenesis. Front Oncol 10

  • Ardekani AM, Naeini MM (2010) The role of microRNAs in human diseases. Avicenna J Med Biotechnol 2:161–179

    CAS  PubMed  PubMed Central  Google Scholar 

  • Asadi M, Taghizadeh S, Kaviani E, Vakili O, Taheri‐Anganeh M, Tahamtan M, Savardashtaki A (2021) Caspase‐3: structure, function, and biotechnological aspects. Biotechnol Appl Biochem

  • Azmi AS, Bao B, Sarkar FH (2013) Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev 32:623–642

    Article  CAS  PubMed  Google Scholar 

  • Baghaei F, Abdollahi A, Mohammadpour H, Jahanbin M, Naseri Taheri F, Aminishakib P, Emami Razavi A, Kharazifard M (2019) PTEN and miR-26b: promising prognostic biomarkers in initiation and progression of oral squamous cell carcinoma. Journal of Oral Pathology & Medicine: Official Publication of the International Association of Oral Pathologists and the American Academy of Oral Pathology 48:31–35

    Article  CAS  Google Scholar 

  • Bazzan E, Tinè M, Casara A, Biondini D, Semenzato U, Cocconcelli E, Balestro E, Damin M, Radu CM, Turato G, Baraldo S, Simioni P, Spagnolo P, Saetta M, Cosio MG (2021) Critical review of the evolution of extracellular vesicles’ knowledge: from 1946 to today. Int J Mol Sci 22

  • Beizavi Z, Gheibihayat SM, Moghadasian H, Zare H, Yeganeh BS, Askari H, Vakili S, Tajbakhsh A, Savardashtaki A (2021) The regulation of CD47-SIRPα signaling axis by microRNAs in combination with conventional cytotoxic drugs together with the help of nano-delivery: a choice for therapy? Mol Biol Rep 48:5707–5722

    Article  CAS  PubMed  Google Scholar 

  • Bhan A, Soleimani M, Mandal SS (2017) Long noncoding RNA and cancer: a new paradigm. Can Res 77:3965–3981

    Article  CAS  Google Scholar 

  • Bjorkman S, Taylor HS (2019) MicroRNAs in endometriosis: biological function and emerging biomarker candidates. Biol Reprod 101:1167–1178

    Article  Google Scholar 

  • Bobrie A, Colombo M, Raposo G, Théry C (2011) Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12:1659–1668

    Article  CAS  PubMed  Google Scholar 

  • Boura E, Ivanov V, Carlson LA, Mizuuchi K, Hurley JH (2012) Endosomal sorting complex required for transport (ESCRT) complexes induce phase-separated microdomains in supported lipid bilayers. J Biol Chem 287:28144–28151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ (2010) Exosome release of β-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol 190:1079–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chapron C, Marcellin L, Borghese B, Santulli P (2019) Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol 15:666–682

    Article  PubMed  Google Scholar 

  • Chen C, Zhao Y, Yu Y, Li R, Qiao J (2016) MiR-125b regulates endometrial receptivity by targeting MMP26 in women undergoing IVF-ET with elevated progesterone on HCG priming day. Sci Rep 6:1–12

    Google Scholar 

  • Chen L, Zhang Y-H, Pan X, Liu M, Wang S, Huang T, Cai Y-D (2018) Tissue expression difference between mRNAs and lncRNAs. Int J Mol Sci 19:3416

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen Y, Wang K, Xu Y, Guo P, Hong B, Cao Y, Wei Z, Xue R, Wang C, Jiang H (2019) Alteration of myeloid-derived suppressor cells, chronic inflammatory cytokines, and exosomal miRNA contribute to the peritoneal immune disorder of patients with endometriosis. Reprod Sci 26:1130–1138

    Article  CAS  PubMed  Google Scholar 

  • Cho S, Mutlu L, Grechukhina O, Taylor HS (2015) Circulating microRNAs as potential biomarkers for endometriosis. Fertil Steril 103:1252-1260.e1251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi DS, Kim DK, Kim YK, Gho YS (2013) Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 13:1554–1571

    Article  CAS  PubMed  Google Scholar 

  • Coeman V, Sciot R, Van Breuseghem I (2005) Rectus abdominis endometriosis: a report of two cases. Br J Radiol 78:68–71

    Article  CAS  PubMed  Google Scholar 

  • Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, Théry C, Raposo G (2013) Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 126:5553–5565

    CAS  PubMed  Google Scholar 

  • Conigliaro A, Costa V, Lo Dico A, Saieva L, Buccheri S, Dieli F, Manno M, Raccosta S, Mancone C, Tripodi M (2015) CD90+ liver cancer cells modulate endothelial cell phenotype through the release of exosomes containing H19 lncRNA. Mol Cancer 14:1–11

    Article  Google Scholar 

  • Creinin MD, Meyn LA, Borgatta L, Barnhart K, Jensen J, Burke AE, Westhoff C, Gilliam M, Dutton C, Ballagh SA (2008) Multicenter comparison of the contraceptive ring and patch: a randomized controlled trial. Obstet Gynecol 111:267–277

    Article  PubMed  Google Scholar 

  • Cui S, Sun B, Yin X, Guo X, Chao D, Zhang C, Zhang CY, Chen X, Ma J (2017) Time-course responses of circulating microRNAs to three resistance training protocols in healthy young men. Sci Rep 7:2203

    Article  PubMed  PubMed Central  Google Scholar 

  • Dawson A, Fernandez ML, Anglesio M, Yong PJ, Carey MS (2018) Endometriosis and endometriosis-associated cancers: new insights into the molecular mechanisms of ovarian cancer development. ecancermedicalscience 12:803–803

  • Dilsiz N (2020) Role of exosomes and exosomal microRNAs in cancer. Future Sci OA 6:Fso465

  • Dwivedi S, Purohit P, Sharma P (2019) MicroRNAs and diseases: promising biomarkers for diagnosis and therapeutics. Indian J Clin Biochem 34:243–245

    Article  PubMed  PubMed Central  Google Scholar 

  • Edgar JR (2016) Q&A: What are exosomes, exactly? BMC Biol 14:46

    Article  PubMed  PubMed Central  Google Scholar 

  • Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273:20121–20127

    Article  CAS  PubMed  Google Scholar 

  • Esfandyari S, Elkafas H, Chugh RM, Park H-s, Navarro A, Al-Hendy A (2021) Exosomes as biomarkers for female reproductive diseases diagnosis and therapy. Int J Mol Sci 22:2165

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang Y, Fullwood MJ (2016) Roles, functions, and mechanisms of long non-coding RNAs in cancer. Genomics Proteomics Bioinformatics 14:42–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freger S, Leonardi M, Foster WG (2021) Exosomes and their cargo are important regulators of cell function in endometriosis. Reprod Biomed Online 43:370–378

    Article  CAS  PubMed  Google Scholar 

  • Frischknecht F, Raio L, Fleischmann A, Dreher E, Lüscher K, Mueller M (2004) Umbilical endometriosis. Surg Endosc Other Interv Tech 18:347–347

    Article  CAS  Google Scholar 

  • Geisler S, Coller J (2013) RNA in unexpected places: long non-coding RNA functions in diverse cellular contexts. Nat Rev Mol Cell Biol 14:699–712

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghai V, Jan H, Shakir F, Haines P, Kent A (2020) Diagnostic delay for superficial and deep endometriosis in the United Kingdom. Journal of Obstetrics and Gynaecology: the Journal of the Institute of Obstetrics and Gynaecology 40:83–89

    Article  PubMed  Google Scholar 

  • Green SH, Waxman KS, Morris PL, Shadle BD (2007) Case report: Umbilical hernia and endometriosis: a diagnostic consideration. Surgical Rounds 30:380

    Google Scholar 

  • Gruenwald P (1942) Origin of endometriosis from the mesenchyme of the celomic walls. Am J Obstet Gynecol 44:470–474

    Article  Google Scholar 

  • Guo SW (2009) Recurrence of endometriosis and its control. Hum Reprod Update 15:441–461

    Article  PubMed  Google Scholar 

  • Ha M, Kim VN (2014) Regulation of microRNA biogenesis. Nat Rev Mol Cell Biol 15:509–524

    Article  CAS  PubMed  Google Scholar 

  • Hapangama DK, Turner MA, Drury J, Heathcote L, Afshar Y, Mavrogianis PA, Fazleabas AT (2010) Aberrant expression of regulators of cell-fate found in eutopic endometrium is found in matched ectopic endometrium among women and in a baboon model of endometriosis. Human Reproduction (oxford, England) 25:2840–2850

    Article  CAS  PubMed  Google Scholar 

  • Harp D, Driss A, Mehrabi S, Chowdhury I, Xu W, Liu D, Garcia-Barrio M, Taylor RN, Gold B, Jefferson S (2016) Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res 365:187–196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hashemipour M, Boroumand H, Mollazadeh S, Tajiknia V, Nourollahzadeh Z, Rohani Borj M, Pourghadamyari H, Rahimian N, Hamblin MR, Mirzaei H (2021) Exosomal microRNAs and exosomal long non-coding RNAs in gynecologic cancers. Gynecol Oncol 161:314–327

    Article  CAS  PubMed  Google Scholar 

  • Hessvik NP, Llorente A (2018) Current knowledge on exosome biogenesis and release. Cell Mol Life Sci 75:193–208

    Article  CAS  PubMed  Google Scholar 

  • Holopainen JM, Angelova MI, Kinnunen PK (2000) Vectorial budding of vesicles by asymmetrical enzymatic formation of ceramide in giant liposomes. Biophys J 78:830–838

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Homer H, Rice GE, Salomon C (2017) Embryo-and endometrium-derived exosomes and their potential role in assisted reproductive treatments–liquid biopsies for endometrial receptivity. Placenta 54:89–94

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Ni S, Cao Y, Zhang T, Wu T, Yin X, Lang Y, Lu H (2016) The angiogenic effect of microRNA-21 targeting TIMP3 through the regulation of MMP2 and MMP9. PLoS ONE 11:e0149537

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang X, Yuan T, Tschannen M, Sun Z, Jacob H, Du M, Liang M, Dittmar RL, Liu Y, Liang M, Kohli M, Thibodeau SN, Boardman L, Wang L (2013) Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics 14:319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Zhu L, Li H, Ye J, Lin N, Chen M, Pan D, Chen Z (2022) Endometriosis derived exosomal miR-301a-3p mediates macrophage polarization via regulating PTEN-PI3K axis. Biomed Pharmacother 147:112680

    Article  CAS  PubMed  Google Scholar 

  • Hudson QJ, Proestling K, Perricos A, Kuessel L, Husslein H, Wenzl R, Yotova I (2021) The role of long non-coding RNAs in endometriosis. Int J Mol Sci 22:11425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurley JH, Hanson PI (2010) Membrane budding and scission by the ESCRT machinery: it’s all in the neck. Nat Rev Mol Cell Biol 11:556–566

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hurwitz SN, Nkosi D, Conlon MM, York SB, Liu X, Tremblay DC, Meckes DG Jr (2017) CD63 regulates Epstein-Barr virus LMP1 exosomal packaging, enhancement of vesicle production, and noncanonical NF-κB signaling. J Virol 91

  • Ibl V (2019) ESCRTing in cereals: still a long way to go. Science China Life Sciences 62:1144–1152

    Article  PubMed  Google Scholar 

  • Jiang J, Yang X, He X, Ma W, Wang J, Zhou Q, Li M, Yu S (2019) MicroRNA-449b-5p suppresses the growth and invasion of breast cancer cells via inhibiting CREPT-mediated Wnt/β-catenin signaling. Chem Biol Interact 302:74–82

    Article  CAS  PubMed  Google Scholar 

  • Johnson NP, Hummelshoj L, Adamson GD, Keckstein J, Taylor HS, Abrao MS, Bush D, Kiesel L, Tamimi R, Sharpe-Timms KL, Rombauts L, Giudice LC, Consortium WESSP (2017) World Endometriosis Society consensus on the classification of endometriosis. Hum Reprod 32:315–324

    Article  Google Scholar 

  • Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262:9412–9420

    Article  CAS  PubMed  Google Scholar 

  • Khalaj K, Miller JE, Lingegowda H, Fazleabas AT, Young SL, Lessey BA, Koti M, Tayade C (2019) Extracellular vesicles from endometriosis patients are characterized by a unique miRNA-lncRNA signature. JCI Insight 4

  • Koninckx PR, Ussia A, Adamyan L, Wattiez A, Gomel V, Martin DC (2019) Pathogenesis of endometriosis: the genetic/epigenetic theory. Fertil Steril 111:327–340

    Article  CAS  PubMed  Google Scholar 

  • Kung JT, Colognori D, Lee JT (2013) Long noncoding RNAs: past, present, and future. Genetics 193:651–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lang H, Hu G, Chen Y, Liu Y, Tu W, Lu Y, Wu L, Xu G (2017) Glioma cells promote angiogenesis through the release of exosomes containing long non-coding RNA POU3F3. Eur Rev Med Pharmacol Sci 21:959–972

    PubMed  Google Scholar 

  • Larsen H, Muz B, Feldmann M, Paleolog E (2012) Hypoxia and cytokines induce a natural antisense transcript (aHIF) to regulate HIF-1 mediated angiogenesis in rheumatoid arthritis. Vascul Pharmacol 5:321

    Article  Google Scholar 

  • Laschke MW, Menger MD (2007) In vitro and in vivo approaches to study angiogenesis in the pathophysiology and therapy of endometriosis. Hum Reprod Update 13:331–342

    Article  CAS  PubMed  Google Scholar 

  • Lee C, Kikyo N (2012) Strategies to identify long noncoding RNAs involved in gene regulation. Cell Biosci 2:1–6

    Article  Google Scholar 

  • Lee MJ, Park DH, Kang JH (2016) Exosomes as the source of biomarkers of metabolic diseases. Annals of Pediatric Endocrinology & Metabolism 21:119–125

    Article  Google Scholar 

  • Lee RC, Feinbaum RL, Ambros V (1993) The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843–854

    Article  CAS  PubMed  Google Scholar 

  • Lee S-Y, Koo Y-J, Lee D-H (2021) Classification of endometriosis. Yeungnam Univ J Med 38:10–18

    Article  PubMed  Google Scholar 

  • Lessey BA, Kim JJ (2017) Endometrial receptivity in the eutopic endometrium of women with endometriosis: it is affected, and let me show you why. Fertil Steril 108:19–27

    Article  PubMed  PubMed Central  Google Scholar 

  • Li L, Li C, Wang S, Wang Z, Jiang J, Wang W, Li X, Chen J, Liu K, Li C (2016) Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Can Res 76:1770–1780

    Article  CAS  Google Scholar 

  • Li XJ, Ren ZJ, Tang JH, Yu Q (2017) Exosomal microRNA MiR-1246 promotes cell proliferation, invasion and drug resistance by targeting CCNG2 in breast cancer. Cell Physiol Biochem 44:1741–1748

    Article  CAS  PubMed  Google Scholar 

  • Lin H, Zhang R, Wu W, Lei L (2021) miR-4454 promotes hepatic carcinoma progression by targeting Vps4A and Rab27A. Oxid Med Cell Longev 2021:9230435

    Article  PubMed  PubMed Central  Google Scholar 

  • Lin K, Zhan H, Ma J, Xu K, Wu R, Zhou C, Lin J (2017) Silencing of SRA1 regulates ER expression and attenuates the growth of stromal cells in ovarian endometriosis. Reprod Sci 24:836–843

    Article  CAS  PubMed  Google Scholar 

  • Liu L-Z, Li C, Chen Q, Jing Y, Carpenter R, Jiang Y, Kung H-F, Lai L, Jiang B-H (2011) MiR-21 induced angiogenesis through AKT and ERK activation and HIF-1α expression. PLoS ONE 6:e19139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu QW, He Y, Xu WW (2022) Molecular functions and therapeutic applications of exosomal noncoding RNAs in cancer. Exp Mol Med 54:216–225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu T, Liu M, Zheng C, Zhang D, Li M, Zhang L (2021) Exosomal lncRNA CHL1-AS1 derived from peritoneal macrophages promotes the progression of endometriosis via the miR-610/MDM2 axis. Int J Nanomed 16:5451

    Article  Google Scholar 

  • Lv Q, Hu JX, Li YJ, Xie N, Song DD, Zhao W, Yan YF, Li BS, Wang PY, Xie SY (2017) MiR-320a effectively suppresses lung adenocarcinoma cell proliferation and metastasis by regulating STAT3 signals. Cancer Biol Ther 18:142–151

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maas JW, Groothuis PG, Dunselman GA, de Goeij AF, Boudier HAS, Evers JL (2001) Endometrial angiogenesis throughout the human menstrual cycle. Hum Reprod 16:1557–1561

    Article  CAS  PubMed  Google Scholar 

  • Macer ML, Taylor HS (2012) Endometriosis and infertility: a review of the pathogenesis and treatment of endometriosis-associated infertility. Obstetrics and Gynecology Clinics 39:535–549

    PubMed  Google Scholar 

  • Mahutte NG, Arici A (2002) New advances in the understanding of endometriosis related infertility. J Reprod Immunol 55:73–83

    Article  PubMed  Google Scholar 

  • Maier IM, Maier AC (2021) miRNAs and lncRNAs: potential non-invasive biomarkers for endometriosis. Biomedicines 9:1662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Malutan AM, Drugan T, Costin N, Ciortea R, Bucuri C, Rada MP, Mihu D (2015) Pro-inflammatory cytokines for evaluation of inflammatory status in endometriosis. Central-European Journal of Immunology 40:96–102

    Article  PubMed  PubMed Central  Google Scholar 

  • Mashouri L, Yousefi H, Aref AR, Am A, Molaei F, Alahari SK (2019) Exosomes: composition, biogenesis, and mechanisms in cancer metastasis and drug resistance. Mol Cancer 18:75

    Article  PubMed  PubMed Central  Google Scholar 

  • Matsuzaki S, Darcha C (2014) Antifibrotic properties of epigallocatechin-3-gallate in endometriosis. Human Reproduction (oxford, England) 29:1677–1687

    Article  CAS  PubMed  Google Scholar 

  • Mattick JS, Makunin IV (2006) Non-coding RNA. Hum Mol Genet 15 Spec No 1:R17–29

  • Mattick JS, Rinn JL (2015) Discovery and annotation of long noncoding RNAs. Nat Struct Mol Biol 22:5–7

    Article  CAS  PubMed  Google Scholar 

  • McAndrews KM, Kalluri R (2019) Mechanisms associated with biogenesis of exosomes in cancer. Mol Cancer 18:52

    Article  PubMed  PubMed Central  Google Scholar 

  • McLeod BS, Retzloff MG (2010) Epidemiology of endometriosis: an assessment of risk factors. Clin Obstet Gynecol 53:389–396

    Article  PubMed  Google Scholar 

  • Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10:155–159

    Article  CAS  PubMed  Google Scholar 

  • Minciacchi VR, Freeman MR, Di Vizio D (2015) Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol 40:41–51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mineo M, Ricklefs F, Rooj AK, Lyons SM, Ivanov P, Ansari KI, Nakano I, Chiocca EA, Godlewski J, Bronisz A (2016) The long non-coding RNA HIF1A-AS2 facilitates the maintenance of mesenchymal glioblastoma stem-like cells in hypoxic niches. Cell Rep 15:2500–2509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohamed OA, Jonnaert M, Labelle-Dumais C, Kuroda K, Clarke HJ, Dufort D (2005) Uterine Wnt/β-catenin signaling is required for implantation. Proc Natl Acad Sci 102:8579–8584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monnaka VU, Hernandes C, Heller D, Podgaec S (2021) Overview of miRNAs for the non-invasive diagnosis of endometriosis: evidence, challenges and strategies. A systematic review. Einstein (Sao Paulo, Brazil) 19:eRW5704

  • Moradi Y, Shams-Beyranvand M, Khateri S, Gharahjeh S, Tehrani S, Varse F, Tiyuri A, Najmi Z (2021) A systematic review on the prevalence of endometriosis in women. Indian J Med Res 154:446–454

    Article  PubMed  PubMed Central  Google Scholar 

  • Moustafa S, Burn M, Mamillapalli R, Nematian S, Flores V, Taylor HS (2020) Accurate diagnosis of endometriosis using serum microRNAs. Am J Obstet Gynecol 223:557. e551–557. e511

  • Movahedpour A, Khatami SH, Khorsand M, Salehi M, Savardashtaki A, Mirmajidi SH, Negahdari B, Khanjani N, Naeli P, Vakili O (2021) Exosomal noncoding RNAs: key players in glioblastoma drug resistance. Mol Cell Biochem 476:4081–4092

    Article  CAS  PubMed  Google Scholar 

  • Muhaidat N, Saleh S, Fram K, Nabhan M, Almahallawi N, Alryalat SA, Elfalah M, Elfalah M (2021) Prevalence of endometriosis in women undergoing laparoscopic surgery for various gynaecological indications at a Jordanian referral centre: gaining insight into the epidemiology of an important women’s health problem. BMC Women’s Health 21:381

    Article  PubMed  PubMed Central  Google Scholar 

  • Murphy AA, Palinski W, Rankin S, Morales AJ, Parthasarathy S (1998) Evidence for oxidatively modified lipid-protein complexes in endometrium and endometriosis. Fertil Steril 69:1092–1094

    Article  CAS  PubMed  Google Scholar 

  • Ng YH, Rome S, Jalabert A, Forterre A, Singh H, Hincks CL, Salamonsen LA (2013) Endometrial exosomes/microvesicles in the uterine microenvironment: a new paradigm for embryo-endometrial cross talk at implantation. PLoS ONE 8:e58502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Brien J, Hayder H, Zayed Y, Peng C (2018) Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front Endocrinol (lausanne) 9:402–402

    Article  CAS  PubMed  Google Scholar 

  • O’Brien K, Breyne K, Ughetto S, Laurent LC, Breakefield XO (2020) RNA delivery by extracellular vesicles in mammalian cells and its applications. Nat Rev Mol Cell Biol 21:585–606

    Article  PubMed  PubMed Central  Google Scholar 

  • Ohlsson Teague EMC, Print CG, Hull ML (2009) The role of microRNAs in endometriosis and associated reproductive conditions. Hum Reprod Update 16:142–165

    Article  Google Scholar 

  • Olive DL, Schwartz LB (1993) Endometriosis. N Engl J Med 328:1759–1769

    Article  CAS  PubMed  Google Scholar 

  • Panir K, Schjenken JE, Robertson SA, Hull ML (2018) Non-coding RNAs in endometriosis: a narrative review. Hum Reprod Update 24:497–515

    Article  CAS  PubMed  Google Scholar 

  • Parente Barbosa C, Bentes De Souza AM, Bianco B, Christofolini DM (2011) The effect of hormones on endometriosis development. Minerva Ginecol 63:375–386

    CAS  PubMed  Google Scholar 

  • Parlatan U, Inanc MT, Ozgor BY, Oral E, Bastu E, Unlu MB, Basar G (2019) Raman spectroscopy as a non-invasive diagnostic technique for endometriosis. Sci Rep 9:19795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pegtel DM, Gould SJ (2019) Exosomes. Annu Rev Biochem 88:487–514

    Article  CAS  PubMed  Google Scholar 

  • Peters BA, Xue X, Sheira LA, Qi Q, Sharma A, Santoro N, Alcaide ML, Ofotokun I, Adimora AA, McKay HS, Tien PC, Michel KG, Gustafson D, Turan B, Landay AL, Kaplan RC, Weiser SD (2021) Menopause is associated with immune activation in women with HIV. J Infect Dis

  • Pina Carvalho LF, Hui CY, Agarwal A (2013) Endometriosis and infertility: biomarkers affecting implantation rate. Expert Review of Obstetrics & Gynecology 8:467–473

    Article  Google Scholar 

  • Poliakov A, Spilman M, Dokland T, Amling CL, Mobley JA (2009) Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 69:159–167

    Article  PubMed  Google Scholar 

  • Poller W, Dimmeler S, Heymans S, Zeller T, Haas J, Karakas M, Leistner D-M, Jakob P, Nakagawa S, Blankenberg S (2018) Non-coding RNAs in cardiovascular diseases: diagnostic and therapeutic perspectives. Eur Heart J 39:2704–2716

    Article  CAS  PubMed  Google Scholar 

  • Qiu J, Hua K (2019) Exosomal long noncoding RNA-NONHAT076754 faciliates endometriosis invasion and predicts endometriosis recurrence. J Minim Invasive Gynecol 26:S12

    Article  Google Scholar 

  • Qiu J-J, Lin X-J, Zheng T-T, Tang X-Y, Zhang Y, Hua K-Q (2019) The exosomal long noncoding RNA aHIF is upregulated in serum from patients with endometriosis and promotes angiogenesis in endometriosis. Reprod Sci 26:1590–1602

    Article  CAS  PubMed  Google Scholar 

  • Qiu J-J, Lin Y-Y, Ding J-X, Feng W-W, Jin H-Y, Hua K-Q (2015a) Long non-coding RNA ANRIL predicts poor prognosis and promotes invasion/metastasis in serous ovarian cancer. Int J Oncol 46:2497–2505

    Article  CAS  PubMed  Google Scholar 

  • Qiu J-J, Lin Y-Y, Tang X-Y, Ding Y, Yi X-F, Hua K-Q (2020) Extracellular vesicle-mediated transfer of the lncRNA-TC0101441 promotes endometriosis migration/invasion. Exp Cell Res 388:111815

    Article  CAS  PubMed  Google Scholar 

  • Qiu J-J, Wang Y, Ding J-X, Jin H-Y, Yang G, Hua K-Q (2015) The long non-coding RNA HOTAIR promotes the proliferation of serous ovarian cancer cells through the regulation of cell cycle arrest and apoptosis. Exp Cell Res 333:238–248

    Article  CAS  PubMed  Google Scholar 

  • Rana S, Zöller M (2011) Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem Soc Trans 39:559–562

    Article  CAS  PubMed  Google Scholar 

  • Record M, Carayon K, Poirot M, Silvente-Poirot S (2014) Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochem Biophys Acta 1841:108–120

    CAS  PubMed  Google Scholar 

  • Rivandi M, Pasdar A, Hamzezadeh L, Tajbakhsh A, Seifi S, Moetamani-Ahmadi M, Ferns GA, Avan A (2019) The prognostic and therapeutic values of long noncoding RNA PANDAR in colorectal cancer. J Cell Physiol 234:1230–1236

    Article  CAS  PubMed  Google Scholar 

  • Rocchi A, Chiti E, Maiese A, Turillazzi E, Spinetti I (2021) MicroRNAs: an update of applications in forensic science. Diagnostics 11:32

    Article  CAS  Google Scholar 

  • Rogers PA, Adamson GD, Al-Jefout M, Becker CM, D’Hooghe TM, Dunselman GA, Fazleabas A, Giudice LC, Horne AW, Hull ML, Hummelshoj L, Missmer SA, Montgomery GW, Stratton P, Taylor RN, Rombauts L, Saunders PT, Vincent K, Zondervan KT (2017) Research priorities for endometriosis. Reproductive Sciences (thousand Oaks, Calif) 24:202–226

    Article  PubMed  Google Scholar 

  • Salehi M, Vafadar A, Khatami SH, Taheri-Anganeh M, Vakili O, Savardashtaki A, Negahdari B, Naeli P, Behrouj H, Ghasemi H (2021) Gastrointestinal cancer drug resistance: the role of exosomal miRNAs. Mol Biol Rep 1–12

  • Sansone P, Savini C, Kurelac I, Chang Q, Amato LB, Strillacci A, Stepanova A, Iommarini L, Mastroleo C, Daly L, Galkin A, Thakur BK, Soplop N, Uryu K, Hoshino A, Norton L, Bonafé M, Cricca M, Gasparre G, Lyden D, Bromberg J (2017) Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci USA 114:E9066-e9075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Santanam N, Kavtaradze N, Murphy A, Dominguez C, Parthasarathy S (2013) Antioxidant supplementation reduces endometriosis-related pelvic pain in humans. Transl Res 161:189–195

    Article  CAS  PubMed  Google Scholar 

  • Sato-Kuwabara Y, Melo SA, Soares FA, Calin GA (2015) The fusion of two worlds: non-coding RNAs and extracellular vesicles–diagnostic and therapeutic implications (review). Int J Oncol 46:17–27

    Article  CAS  PubMed  Google Scholar 

  • Savardashtaki A, Shabaninejad Z, Movahedpour A, Sahebnasagh R, Mirzaei H, Hamblin MR (2019) miRNAs derived from cancer-associated fibroblasts in colorectal cancer. Epigenomics 11:1627–1645

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schjenken J, Panir K, Robertson S, Hull M (2019) Exosome-mediated intracellular signalling impacts the development of endometriosis—new avenues for endometriosis research. MHR: Basic Science of Reproductive Medicine 25:2–4

  • Schmidt O, Teis D (2012) The ESCRT Machinery Current Biology: CB 22:R116-120

    Article  CAS  PubMed  Google Scholar 

  • Schmitz SU, Grote P, Herrmann BG (2016) Mechanisms of long noncoding RNA function in development and disease. Cell Mol Life Sci 73:2491–2509

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seli E, Berkkanoglu M, Arici A (2003) Pathogenesis of endometriosis. Obstetrics and Gynecology Clinics 30:41–61

    PubMed  Google Scholar 

  • Shan S, Yang Y, Jiang J, Yang B, Yang Y, Sun F, Zhang J, Lin Y, Xu H (2022) Extracellular vesicle-derived long non-coding RNA as circulating biomarkers for endometriosis. Reprod Biomed Online 44:923–933

    Article  CAS  PubMed  Google Scholar 

  • Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P (2002) High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Human Reproduction (oxford, England) 17:2715–2724

    Article  CAS  PubMed  Google Scholar 

  • Skotland T, Hessvik NP, Sandvig K, Llorente A (2019) Exosomal lipid composition and the role of ether lipids and phosphoinositides in exosome biology. J Lipid Res 60:9–18

    Article  CAS  PubMed  Google Scholar 

  • Smolarz B, Szyłło K, Romanowicz H (2021) Endometriosis: epidemiology, classification, pathogenesis, treatment and genetics (review of literature). Int J Mol Sci 22:

  • Soltani-Fard E, Taghvimi S, Abedi Kichi Z, Weber C, Shabaninejad Z, Taheri-Anganeh M, Hossein Khatami S, Mousavi P, Movahedpour A, Natarelli L (2021) Insights into the function of regulatory RNAs in bacteria and archaea. Int J Transl Med 1:403–423

    Article  Google Scholar 

  • Sourial S, Tempest N, Hapangama DK (2014) Theories on the pathogenesis of endometriosis. International J Rep Med 2014:179515

    Article  PubMed  PubMed Central  Google Scholar 

  • Span P, Rao J, Ophuis SO, Lenders J, Sweep F, Wesseling P, Kusters B, van Nederveen F, de Krijger R, Hermus A (2011) Overexpression of the natural antisense hypoxia-inducible factor-1α transcript is associated with malignant pheochromocytoma/paraganglioma. Endocr Relat Cancer 18:323–331

    Article  CAS  PubMed  Google Scholar 

  • Statello L, Guo C-J, Chen L-L, Huarte M (2021) Gene regulation by long non-coding RNAs and its biological functions. Nat Rev Mol Cell Biol 22:96–118

    Article  CAS  PubMed  Google Scholar 

  • Taghvimi S, Vakili O, Soltani Fard E, Khatami SH, Karami N, Taheri-Anganeh M, Salehi M, Negahdari B, Ghasemi H, Movahedpour A (2022) Exosomal microRNAs and long noncoding RNAs: novel mediators of drug resistance in lung cancer. J Cell Physiol 237:2095–2106

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Mao L, Huang C, Yang W, Guo J, Chen Z, Chen Z (2021) Comprehensive analysis of lncRNA-miRNA-mRNA regulatory networks for microbiota-mediated colorectal cancer associated with immune cell infiltration. Bioengineered 12:3410–3425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tschuschke M, Kocherova I, Bryja A, Mozdziak P, Angelova Volponi A, Janowicz K, Sibiak R, Piotrowska-Kempisty H, Iżycki D, Bukowska D, Antosik P, Shibli JA, Dyszkiewicz-Konwińska M, Kempisty B (2020) Inclusion biogenesis, methods of isolation and clinical application of human cellular exosomes. J Clin Med 9:

  • Vassilopoulou L, Matalliotakis M, Zervou MI, Matalliotaki C, Krithinakis K, Matalliotakis I, Spandidos DA, Goulielmos GN (2019) Defining the genetic profile of endometriosis (review). Exp Ther Med 17:3267–3281

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vercellini P, Barbara G, Somigliana E, Bianchi S, Abbiati A, Fedele L (2010) Comparison of contraceptive ring and patch for the treatment of symptomatic endometriosis. Fertil Steril 93:2150–2161

    Article  CAS  PubMed  Google Scholar 

  • Viereck J, Thum T (2017) Circulating noncoding RNAs as biomarkers of cardiovascular disease and injury. Circ Res 120:381–399

    Article  CAS  PubMed  Google Scholar 

  • Vilella F, Moreno-Moya JM, Balaguer N, Grasso A, Herrero M, Martínez S, Marcilla A, Simón C (2015) Hsa-miR-30d, secreted by the human endometrium, is taken up by the pre-implantation embryo and might modify its transcriptome. Development 142:3210–3221

    Article  CAS  PubMed  Google Scholar 

  • Vlassov AV, Magdaleno S, Setterquist R, Conrad R (2012) Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochimica et Biophysica Acta (BBA)-General Subjects 1820:940–948

  • Wang X, Parodi L, Hawkins SM (2021) Translational applications of linear and circular long noncoding RNAs in endometriosis. Int J Mol Sci 22:10626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei Z, Lyu B, Hou D, Liu X (2021) Mir-5100 mediates proliferation, migration and invasion of oral squamous cell carcinoma cells via targeting SCAI. Journal of Investigative Surgery: the Official Journal of the Academy of Surgical Research 34:834–841

    Article  PubMed  Google Scholar 

  • Wightman B, Ha I, Ruvkun G (1993) Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855–862

    Article  CAS  PubMed  Google Scholar 

  • Wilusz JE, Sunwoo H, Spector DL (2009) Long noncoding RNAs: functional surprises from the RNA world. Genes Dev 23:1494–1504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Woodward PJ, Sohaey R, Mezzetti TP Jr (2001) Endometriosis: radiologic-pathologic correlation. Radiographics 21:193–216

    Article  CAS  PubMed  Google Scholar 

  • Wu D, Lu P, Mi X, Miao J (2018) Exosomal miR-214 from endometrial stromal cells inhibits endometriosis fibrosis. MHR: Basic Science of Reproductive Medicine 24:357–365

  • Wu J, Huang H, Huang W, Wang L, Xia X, Fang X (2020) Analysis of exosomal lncRNA, miRNA and mRNA expression profiles and ceRNA network construction in endometriosis. Epigenomics 12:1193–1213

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Yuan W, Ding H, Wu X (2022) Serum exosomal miRNA from endometriosis patients correlates with disease severity. Arch Gynecol Obstet 305:117–127

    Article  CAS  PubMed  Google Scholar 

  • Xue M, Zhuo Y, Shan B (2017) MicroRNAs, long noncoding RNAs, and their functions in human disease. Methods in Molecular Biology (clifton, NJ) 1617:1–25

    Article  CAS  Google Scholar 

  • Yang X, Su W, Li Y, Zhou Z, Zhou Y, Shan H, Han X, Zhang M, Zhang Q, Bai Y, Guo C, Yang S, Beer DG, Chen G (2021) MiR-22-3p suppresses cell growth via MET/STAT3 signaling in lung cancer. Am J Transl Res 13:1221–1232

    CAS  PubMed  PubMed Central  Google Scholar 

  • Yousefi H, Maheronnaghsh M, Molaei F, Mashouri L, Reza Aref A, Momeny M, Alahari SK (2020) Long noncoding RNAs and exosomal lncRNAs: classification, and mechanisms in breast cancer metastasis and drug resistance. Oncogene 39:953–974

    Article  CAS  PubMed  Google Scholar 

  • Zaborowski MP, Balaj L, Breakefield XO, Lai CP (2015) Extracellular vesicles: composition, biological relevance, and methods of study. Bioscience 65:783–797

    Article  PubMed  PubMed Central  Google Scholar 

  • Zanatta A, Rocha AM, Carvalho FM, Pereira R, Taylor HS, Motta EL, Baracat EC, Serafini PC (2010) The role of the Hoxa10/HOXA10 gene in the etiology of endometriosis and its related infertility: a review. J Assist Reprod Genet 27:701–710

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang A, Wang G, Jia L, Su T, Zhang L (2019a) Exosome-mediated microRNA-138 and vascular endothelial growth factor in endometriosis through inflammation and apoptosis via the nuclear factor-κB signaling pathway. Int J Mol Med 43:358–370

    PubMed  Google Scholar 

  • Zhang J, Li S, Li L, Li M, Guo C, Yao J, Mi S (2015) Exosome and exosomal microRNA: trafficking, sorting, and function. Genomics Proteomics Bioinformatics 13:17–24

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang L, Li H, Yuan M, Li D, Sun C, Wang G (2020a) Serum exosomal microRNAs as potential circulating biomarkers for endometriosis. Dis Markers 2020a

  • Zhang L, Li H, Yuan M, Li D, Wang G (2020b) Exosomal miR-22-3p derived from peritoneal macrophages enhances proliferation, migration, and invasion of ectopic endometrial stromal cells through regulation of the SIRT1/NF-κB signaling pathway. Eur Rev Med Pharmacol Sci 24:571–580

    CAS  PubMed  Google Scholar 

  • Zhang L, Liu H, Zhu L-T, Luo H-J, Chen X-L, Yu G-Y, Li Q-X, Jin P (2020c) Exosomal miRNAs as novel potential biomarkers for endometriosis

  • Zhang L, Yu Z, Qu Q, Li X, Lu X, Zhang H (2022a) Exosomal lncRNA HOTAIR promotes the progression and angiogenesis of endometriosis via the miR-761/HDAC1 axis and activation of STAT3-mediated inflammation. Int J Nanomed 17:1155

    Article  CAS  Google Scholar 

  • Zhang M, Wang X, Xia X, Fang X, Zhang T, Huang F (2022b) Endometrial epithelial cells-derived exosomes deliver microRNA-30c to block the BCL9/Wnt/CD44 signaling and inhibit cell invasion and migration in ovarian endometriosis. Cell Death Discovery 8:1–10

    Google Scholar 

  • Zhang Y, Chang X, Wu D, Deng M, Miao J, Jin Z (2021) Down-regulation of exosomal miR-214-3p targeting CCN2 contributes to endometriosis fibrosis and the role of exosomes in the horizontal transfer of miR-214-3p. Reprod Sci 28:715–727

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Liu Y, Liu H, Tang WH (2019b) Exosomes: biogenesis, biologic function and clinical potential. Cell Biosci 9:19

    Article  PubMed  PubMed Central  Google Scholar 

  • Zheng H, Bi F-r, Yang Y, Hong Y-g, Ni J-s, Ma L, Liu M-h, Hao L-q, Zhou W-p, Song L-h, Yan H-L (2019) Downregulation of miR-196-5p induced by hypoxia drives tumorigenesis and metastasis in hepatocellular carcinoma. Hormones and Cancer 10:177–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou W, Lian Y, Jiang J, Wang L, Ren L, Li Y, Yan X, Chen Q (2020) Differential expression of microRNA in exosomes derived from endometrial stromal cells of women with endometriosis-associated infertility. Reprod Biomed Online 41:170–181

    Article  PubMed  Google Scholar 

  • Zhu Q, Heon M, Zhao Z, He M (2018) Microfluidic engineering of exosomes: editing cellular messages for precision therapeutics. Lab Chip 18:1690–1703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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This study was financially supported by the Shiraz University of Medical Sciences, Shiraz, Iran.

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The authors confirm contribution to the paper as follows: study conception and design: Elahe Soltani-Fard, Sina Taghvimi, and Marzieh Asadi; data collection: Elahe Soltani-Fard, Marzieh Asadi, Sina Taghvimi, Asma Vafadar, and Parisa Vosough; analysis and interpretation of the results: Amir Tajbakhsh and Amir Savardashtaki; draft manuscript preparation: Elahe Soltani-Fard, Marzieh Asadi, and Amir Tajbakhsh.

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Correspondence to Amir Savardashtaki.

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Soltani-Fard, E., Asadi, M., Taghvimi, S. et al. Exosomal microRNAs and long noncoding RNAs: as novel biomarkers for endometriosis. Cell Tissue Res 394, 55–74 (2023). https://doi.org/10.1007/s00441-023-03802-5

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