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. 2024 Aug 5;17:160. doi: 10.1186/s13048-024-01480-7

Table 2.

Potential biomarkers found in extracellular vesicles (exosome-like vesicles) of different biological origins from patients with different stages of endometriosis

Types of molecule Potential biomarker(s) Biological origin Comparision EV isolation method EV characterization techniques Detection technique Sample size Endometriosis stage Total number differentially expressed Reference Year of publication Complete reference
miRNAs

↑ miR-342-5p, miR-130b-3p, miR-210-3p

↓ miR-132-5p, miR-335-3p

Uterin cavity fluid Endo vs Control Exosome isolation kit (Echobiotech) TEM, NTA, WB RNASeq 4 endo, 4 ctrl All patients III-IV

7 upregulated

2 downregulated

PMID: 36,551,866 2022 Jiang Y, Chai X, Chen S, Chen Z, Tian H, Liu M, Wu X. Exosomes from the Uterine Cavity Mediate Immune Dysregulation via Inhibiting the JNK Signal Pathway in Endometriosis. Biomedicines. 2022 Dec 2;10(12):3110. https://doi.org/10.3390/biomedicines10123110. PMID: 36,551,866; PMCID: PMC9775046
miRNAs

↑ miR-6795-3p, miR-146b-3p, miR-32-3p

↓ miR-128–1-5p, miR-215-5p, miR-26b-5p

Serum Endo vs Control Exosome binding enhancer and magnetic beads TEM, WB Microarray 4 endo, 4 ctrl 1 patients I-II, 3 patients III-IV

26 upregulated

19 downregulated

PMID: 34,542,679 2022 Wu Y, Yuan W, Ding H, Wu X. Serum exosomal miRNA from endometriosis patients correlates with disease severity. Arch Gynecol Obstet. 2022 Jan;305(1):117–127. https://doi.org/10.1007/s00404-021-06227-z. Epub 2021 Sep 20. PMID: 34,542,679; PMCID: PMC8782809
proteins

↑ RAN, FTH1, UBB

↓ HEL70, MMP2, HEL-S-1

Endometrium and endometriotic lesions Endo vs Control Ultracentrifugation TEM, NTA, WB LS-MS/MS 6 endo, 10 ctrl Not reported

3 upregulated

6 downregulated

PMID: 35,557,941 2022 Abudula M, Fan X, Zhang J, Li J, Zhou X, Chen Y. Ectopic Endometrial Cell-Derived Exosomal Moesin Induces Eutopic Endometrial Cell Migration, Enhances Angiogenesis and Cytosolic Inflammation in Lesions Contributes to Endometriosis Progression. Front Cell Dev Biol. 2022 Apr 26;10:824,075. https://doi.org/10.3389/fcell.2022.824075. PMID: 35,557,941; PMCID: PMC9086167
circRNAs, miRNAs and mRNAs

qRT-PCR:

↑ circ_002612309 (ectopic vs ctrl/eutopic)

↓ miR-15a-5p (eutopic/ectopic vs ctrl)

ATP6V1A (eutopic/ectopic vs ctrl)

Endometrium and endometriotic lesions Overlapping DEGs between Ectopic vs Ctrl, Eutopic vs Ctrl and Ectopic vs Eutopic ExoQuick-TC (System Biosciences) TEM, NTA, WB RNASeq 3 endo (3 eutopic, 3 ectopic samples), 3 ctrl All patients III-IV

circRNAs:

2915 upregulated

640 downregulated

miRNAs:

17 upregulated

9 downregulated

mRNAs:

550 upregulated

136 downregulated

PMID: 33,901,012 2021 Wu J, Fang X, Huang H, Huang W, Wang L, Xia X. Construction and topological analysis of an endometriosis-related exosomal circRNA-miRNA-mRNA regulatory network. Aging (Albany NY). 2021 Apr 26;13(9):12,607–12630. https://doi.org/10.18632/aging.202937. Epub 2021 Apr 26. PMID: 33,901,012; PMCID: PMC8148458
miRNAs

↑ miR-615-3p, miR-6873-3p, miR-3195

↓ miR-1273 h-3p, miR-4262, miR-1269a

Eutopic endometrium from patients with endometriosis and normal endometrium Endometriotic lesions vs Ctrl ExoQuick-TC (System Biosciences) TEM, FC, NTA RNASeq 3 endo, 3 ctrl All patients II-IV

26 upregulated

23 downregulated

PMID: 32,593,507 2020 Zhou W, Lian Y, Jiang J, Wang L, Ren L, Li Y, Yan X, Chen Q. Differential expression of microRNA in exosomes derived from endometrial stromal cells of women with endometriosis-associated infertility. Reprod Biomed Online. 2020 Aug;41(2):170–181. https://doi.org/10.1016/j.rbmo.2020.04.010. Epub 2020 May 3. PMID: 32,593,507
miRNAs

↑ miR-197-5p, miR-22-3p, miR-320a

↓ miR-134-5p, miR-3141, miR-4499

Serum Endo vs Control Differential centrifugation TEM, NTA, WB Microarray 5 endo, 5 ctrl Not reported

18 upregulated

6 downregulated

PMID: 32,076,458 2020 Zhang L, Li H, Yuan M, Li D, Sun C, Wang G. Serum Exosomal MicroRNAs as Potential Circulating Biomarkers for Endometriosis. Dis Markers. 2020 Jan 23;2020:2,456,340. https://doi.org/10.1155/2020/2456340. PMID: 32,076,458; PMCID: PMC7008302
proteins PRDX1, H2A type 2-C, ANXA2, ITIH4 and tubulin a-chain Peritoneal fluid Endo I/II vs Endo III/IV vs Ctrl Exo-spin size-exclusion chromatography columns (Cell Guidance Systems) TEM, NTA, WB LC–MS/MS 16 endo I/II, 6 endo III/IV and 6 ctrl Patients split I/II and III/IV 5 proteins exclusively found in endo PMID: 32,106,990 2020 Nazri HM, Imran M, Fischer R, Heilig R, Manek S, Dragovic RA, Kessler BM, Zondervan KT, Tapmeier TT, Becker CM. Characterization of exosomes in peritoneal fluid of endometriosis patients. Fertil Steril. 2020 Feb;113(2):364–373.e2. https://doi.org/10.1016/j.fertnstert.2019.09.032. PMID: 32,106,990; PMCID: PMC7057257
miRNAs

↑ miR-1908-5p, miR-130b-5p, miR-4488

↓ miR-6508-3p, miR-145-5p, miR-365b-3p

Peritoneal fluid Early endo, late endo vs Ctrl Ultracentrifugation None RNASeq 3 early stage endo, 3 advanced stage endo and 3 ctrl Patients I-IV

early vs ctrl:

130 upregulated

43 downregulated

late vs ctrl:

87 upregulated

63 downregulated

PMID: 30,453,861 2019 Chen Y, Wang K, Xu Y, Guo P, Hong B, Cao Y, Wei Z, Xue R, Wang C, Jiang H. Alteration of Myeloid-Derived Suppressor Cells, Chronic Inflammatory Cytokines, and Exosomal miRNA Contribute to the Peritoneal Immune Disorder of Patients With Endometriosis. Reprod Sci. 2019 Aug;26(8):1130–1138. https://doi.org/10.1177/1933719118808923. Epub 2018 Nov 19. PMID: 30,453,861
miRNAs

↑ miR-27a-3p

↓ miR-375, miR-30d-5p

(endometrium, lesions and plasma)

Endometrium, endometriotic lesions and plasma Eutopic vs Ectopic, Ectopic vs Ctrl and Eutopic vs Ctrl miRCURY exosome isolation kit (Qiagen) TEM, WB RNASeq 6 endometrium, 6 endometriotic lesions and 6 plasma All patients III-IV

Plasma: 21 DE

Ectopic/Eutopic samples: 14 DE

PMID: 31,534,048 2019 Khalaj K, Miller JE, Lingegowda H, Fazleabas AT, Young SL, Lessey BA, Koti M, Tayade C. Extracellular vesicles from endometriosis patients are characterized by a unique miRNA-lncRNA signature. JCI Insight. 2019 Sep 19;4(18):e128846. https://doi.org/10.1172/jci.insight.128846. PMID: 31,534,048; PMCID: PMC6795291
lncRNA ↑ circulating exosomal aHIF and exosomal ectopic endometrium Endometrium, endometriotic lesions and plasma Eutopic vs Ectopic, Ectopic vs Ctrl and Eutopic vs Ctrl Total Exosome Isolation kit (Invitrogen) for cell culture and ExoQuick exosome precipitation solution kit for serum TEM, WB qRT-PCR 30 endo and 16 ctrl All patients III-IV Single gene assessment PMID: 30,808,247 2019 Qiu JJ, Lin XJ, Zheng TT, Tang XY, Zhang Y, Hua KQ. The Exosomal Long Noncoding RNA aHIF is Upregulated in Serum From Patients With Endometriosis and Promotes Angiogenesis in Endometriosis. Reprod Sci. 2019 Dec;26(12):1590–1602. https://doi.org/10.1177/1933719119831775. Epub 2019 Feb 26. PMID: 30,808,247
miRNAs

qRT-PCR:

↑ miR-21-5p

Endometrium and endometriotic lesions Endometriotic lesions vs Ctrl Total Exosome Isolation kit (Invitrogen) TEM, NTA Targeted qRT-PCR 5 endo (5 eutopic, 5 ectopic samples), 5 ctrl Not reported Non applicable PMID: 26,841,879 2016 Harp D, Driss A, Mehrabi S, Chowdhury I, Xu W, Liu D, Garcia-Barrio M, Taylor RN, Gold B, Jefferson S, Sidell N, Thompson W. Exosomes derived from endometriotic stromal cells have enhanced angiogenic effects in vitro. Cell Tissue Res. 2016 Jul;365(1):187–96. https://doi.org/10.1007/s00441-016-2358-1. Epub 2016 Feb 3. PMID: 26,841,879; PMCID: PMC4917586