Possibility of using microRNA in non-invasive diagnosis of endometriosis

Yarmolinskaya M.I., Cherkashina S.A., Malysheva O.V.

D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology, St. Petersburg, Russia

Due to the high prevalence of endometriosis and its significant negative impact on the reproductive system, quality of life and late diagnosis, there is a clear need to identify new markers for this disease. MicroRNAs are promising biomarkers in non-invasive diagnostis of endometriosis. Their involvement in the pathogenesis of endometriosis has only recently begun to be explored, but microRNAs show promising potential.
This review presents the results of studies on the influence of microRNAs on the occurrence and development of endometriosis, as well as the analysis of their expression in patients with and without this disease. Currently, miR-17-5p, miR-451a and let-7b-5p are the most promising microRNAs for endometriosis diagnosis. The reverse transcription polymerase chain reaction is regarded as the most effective method of detection. Possible biomaterials for non-invasive testing include serum and plasma, saliva and exosomes in the above fluids.
Conclusion: The heterogeneity of the studies presented in this review, variety of test systems used, the differences in methodology, the small number of patients and the lack of a unified research standard, do not allow us to confidently declare any microRNA as a highly specific non-invasive biomarker of endometriosis. It is evident that further research is required to clarify the role of microRNAs in the pathogenesis of endometriosis and their diagnostic capabilities. These findings may contribute to the timely detection and treatment of this disease.

Authors' contributions: Yarmolinskaya M.I., Malysheva O.V., Cherkashina S.A. – developing the concept and design of the study, analysis of data and drawing conclusions; Yarmolinskaya M.I., Cherkashina S.A. – data collection, preparation of the manuscript.
Conflicts of interest: The authors declare no possible conflicts of interest.
Funding: This work was performed within the Basic Scientific Research FGWN-2025-0004 1024032800068-4-3.2.2.
For citation: Yarmolinskaya M.I., Cherkashina S.A., Malysheva O.V. 
Possibility of using microRNA in non-invasive diagnosis of endometriosis.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2025; (4): 12-21 (in Russian)
https://dx.doi.org/10.18565/aig.2025.23

Keywords

microRNA
endometriosis
diagnostics
noninvasive markers
PCR

References

  1. Becker C.M., Bokor A., Heikinheimo O., Horne A., Jansen F., Kiesel L. et al.; ESHRE Endometriosis Guideline Group. ESHRE guideline: endometriosis. Hum Reprod Open. 2022; 2022(2): hoac009. https://dx.doi.org/10.1093/hropen/hoac009
  2. Bernuit D., Ebert A.D., Halis G., Strothmann A., Gerlinger C., Geppert K. et al. Female Perspectives on endometriosis: findings from the uterine bleeding and pain women’s research study. J. Endometr. 2011; 3(2): 73-85. https://dx.doi.org/10.5301/JE.2011.8525
  3. Nnoaham K.E., Hummelshoj L., Webster P., d'Hooghe T., de Cicco Nardone F., de Cicco Nardone C. et al. World Endometriosis Research Foundation Global Study of Women's Health consortium. Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. Fertil. Steril. 2011; 96(2): 366-373.e8. https://dx.doi.org/10.1016/j.fertnstert.2011.05.090.
  4. Министерство здравоохранения Российской Федерации. Клинические рекомендации. Эндометриоз. 2024. [Ministry of Health of the Russian Federation. Clinical guidelines. Endometriosis. 2024. (in Russian)].
  5. Nanda A., K T., Banerjee P., Dutta M., Wangdi T., Sharma P. et al. Cytokines, angiogenesis, and extracellular matrix degradation are augmented by oxidative stress in endometriosis. Ann. Lab. Med. 2020; 40(5): 390-7. https://dx.doi.org/10.3343/alm.2020.40.5.390.
  6. Балан В.Е., Орлова С.А., Титченко Ю.П., Федоров А.А. Неинвазивные маркеры эндометриоза и динамика их уровня на фоне гормональной терапии. Проблемы репродукции. 2018; 24(5): 73-7. [Balan V.E., Orlova S.A., Titchenko Iu.P., Fedorov A.A. Noninvasive markers of endometriosis and their dynamics during hormone therapy. Russian Journal of Human Reproduction. 2018; 24(5): 77-81. (in Russian)]. https://dx.doi.org/10.17116/repro20182405177.
  7. Acimovic M., Vidakovic S., Milic N., Jeremic K., Markovic M., Milosevic-Djeric A. et al. Survivin and VEGF as novel biomarkers in diagnosis of endometriosis. J. Med. Biochem. 2016; 35(1): 63-8. https://dx.doi.org/10.1515/jomb-2015-0005.
  8. Ярмолинская М.И., Андреева Н.Ю., Мишарина Е.В., Ткаченко Н.Н. Патент № 2793841 С1 Российская федерация, СПК A61B 17/42, G01N 33/68. Способ диагностики начальных форм наружного генитального эндометриоза: № 2022127383; заявл. 19.10.2022: опубл. 07.04.2023; заявитель Федеральное государственное бюджетное научное учреждение "Научно-исследовательский институт акушерства, гинекологии и репродуктологии имени Д.О. Отта" [Yarmolinskaya M.I., Andreeva N.Yu., Misharina E.V., Tkachenko N.N. Patent No. 2793841 C1 Russian Federation, SPC A61B 17/42, G01N 33/68. Method for diagnosing initial forms of external genital endometriosis: No. 2022127383; application 19.10.2022: published 07.04.2023; applicant Federal State Budgetary Scientific Institution "D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology" (in Russian)].
  9. Rogers P.A., Adamson G.D., Al-Jefout M., Becker C.M., D'Hooghe T.M., Dunselman G.A. et al. WES/WERF Consortium for Research Priorities in Endometriosis. Research priorities for endometriosis. Reprod. Sci. 2017; 24(2): 202-26. https://dx.doi.org/10.1177/1933719116654991.
  10. Ho P.T.B., Clark I.M., Le L.T.T. MicroRNA-based diagnosis and therapy. Int. J. Mol. Sci. 2022; 23(13): 7167. https://dx.doi.org/10.3390/ijms23137167.
  11. Seyhan A.A. Trials and tribulations of microRNA therapeutics. Int. J. Mol. Sci. 2024; 25(3): 1469. https://dx.doi.org/10.3390/ijms25031469.
  12. Bartel D.P. Metazoan microRNAs. Cell. 2018; 173(1): 20-51. https://dx.doi.org/10.1016/j.cell.2018.03.006.
  13. Запорожченко И.А., Рыкова Е.Ю., Лактионов П.П. Основы биологии микроРНК: строение, биогенез и регуляторные функции. Биоорганическая химия. 2020; 46(1): 3-17. [Zaporozhchenko I.A., Rykova E.Yu., Laktionov P.P. Fundamentals of microRNA biology: structure, biogenesis and regulatory functions. Bioorganic Chemistry. 2020; 46(1): 3-17. (in Russian)]. https://dx.doi.org/10.31857/s0132342320010182.
  14. Marí-Alexandre J., Barceló-Molina M., Olcina-Guillem M., García-Oms J., Braza-Boïls A., Gilabert-Estellés J. MicroRNAs: New players in endometriosis. World J. Obstet. Gynecol. 2016; 5(1): 28-38. https://dx.doi.org/10.5317/wjog.v5.i1.28.
  15. Ширшова А.Н., Кушлинский Д.Н., Филипенко М.Л., Муштенко С.В., Терешкина И.В., Адамян Л.В., Кушлинский Н.Е. Роль микроРНК в биологии и клинике злокачественных опухолей яичников. Проблемы репродукции. 2015; 21(3): 30-7. [Shirshova A.N., Kushlonskiy D.N., Filipenko M.L., Mushtenko S.V., Tereshkina I.V., Adamyan L.V., Kushlinskiy N.E. The role of mRNA in the biology and manifestation of ovarian malignant tumors. Russian Journal of Human Reproduction. 2015; 21(3): 30-7. (in Russian)]. https://dx.doi.org/10.17116/repro201521330-37.
  16. Алиева А.М., Резник Е.В., Теплова Н.В., Меликулов А.А., Ахмедова М.Ф., Котикова И.А., Никитин И.Г. МикроРНК-34а при сердечно-сосудистых заболеваниях: взгляд в будущее. Кардиологический вестник. 2023; 18(1): 14-22. [Alieva A.M., Reznik E.V., Teplova N.V., Melikulov A.A., Akhmedova M.F., Kotikova I.A., Nikitin I.G. MicroRNA-34a in cardiovascular disease: a glimpse into the future. Russian Cardiology Bulletin. 2023; 18(1): 14-22. (in Russian)]. https://dx.doi.org/10.17116/Cardiobulletin20231801114.
  17. McDaneld T.G. MicroRNA: mechanism of gene regulation and application to livestock. J. Anim. Sci. 2009; 87(14 Suppl): E21-8. https://dx.doi.org/10.2527/jas.2008-1303.
  18. Коробкина Е.А., Князева М.С., Киль Ю.В., Титов С.Е., Малек А.В. Сравнительный анализ методов детекции микроРНК с помощью метода обратной транскрипции и количественной полимеразной цепной реакции (ОТ-ПЦР). Клиническая лабораторная диагностика. 2018; 63(11): 722-8. [Korobkina E.A., Knyazeva M.S., Kil Yu.V., Titov S.E., Malek A.V. Comparative analysis of microRNA detection methods using reverse transcription and quantitative polymerase chain reaction (RT-PCR). Clinical Laboratory Diagnostics. 2018; 63(11): 722-8. (in Russian)]. https://dx.doi.org/10.18821/0869-2084-2018-63-11-722-728.
  19. Mestdagh P., Van Vlierberghe P., De Weer A., Muth D., Westermann F., Speleman F. et al. A novel and universal method for microRNA RT-qPCR data normalization. Genome Biol. 2009; 10(6): R64. https://dx.doi.org/10.1186/gb-2009-10-6-r64.
  20. Hawkins S.M., Creighton C.J., Han D.Y., Zariff A., Anderson M.L., Gunaratne P.H. et al. Functional microRNA involved in endometriosis. Mol. Endocrinol. 2011; 25(5): 821-32. https://dx.doi.org/10.1210/me.2010-0371.
  21. Hon J.X., Wahab N.A., Karim A.K.A., Mokhtar N.M., Mokhtar M.H. MicroRNAs in endometriosis: insights into inflammation and progesterone resistance. Int. J. Mol. Sci. 2023; 24(19):15001. https://dx.doi.org/10.3390/ijms241915001.
  22. Pei T., Liu C., Liu T., Xiao L., Luo B., Tan J. et al. miR-194-3p Represses the progesterone receptor and decidualization in eutopic endometrium from women with endometriosis. Endocrinology. 2018; 159(7): 2554-62. https://dx.doi.org/10.1210/en.2018-00374.
  23. Liu T., Xiao L., Pei T., Luo B., Tan J., Long Y. et al. miR-297 inhibits expression of progesterone receptor and decidualization in eutopic endometria of endometriosis. J. Obstet. Gynaecol. Res. 2023; 49(3): 956-65. https://dx.doi.org/10.1111/jog.15526.
  24. Lin S.C., Li W.N., Lin S.C., Hou H.T., Tsai Y.C., Lin T.C. et al. Targeting YAP1 ameliorates progesterone resistance in endometriosis. Hum. Reprod. 2023; 38(6): 1124-34. https://dx.doi.org/10.1093/humrep/dead071.
  25. Joshi N.R., Miyadahira E.H., Afshar Y., Jeong J.W., Young S.L., Lessey B.A. et al. Progesterone resistance in endometriosis is modulated by the altered expression of microRNA-29c and FKBP4. J. Clin. Endocrinol. Metab. 2017; 102(1):141-9. https://dx.doi.org/10.1210/jc.2016-2076.
  26. Joshi N.R., Su R.W., Chandramouli G.V., Khoo S.K., Jeong J.W., Young S.L. et al. Altered expression of microRNA-451 in eutopic endometrium of baboons (Papio anubis) with endometriosis. Hum. Reprod. 2015; 30(12): 2881-91. https://dx.doi.org/10.1093/humrep/dev229.
  27. Kai K., Joshi N.R., Burns G.W., Hrbek S.M., Vegter E.L., Ochoa-Bernal M.A. et al. MicroRNA-210-3p regulates endometriotic lesion development by targeting IGFBP3 in baboons and women with endometriosis. Reprod. Sci. 2023; 30(10): 2932-44. https://dx.doi.org/10.1007/s43032-023-01253-5.
  28. Yang R.Q., Teng H., Xu X.H., Liu S.Y., Wang Y.H., Guo F.J. et al. Microarray analysis of microRNA deregulation and angiogenesis-related proteins in endometriosis. Genet. Mol. Res. 2016; 15(2). https://dx.doi.org/10.4238/gmr.15027826.
  29. Бобров М.Ю., Балашов И.С., Филиппова Е.С., Альмова И.К., Тимофеева А.В., Гусар В.А., Боровиков П.И., Хилькевич Е.Г., Чупрынин В.Д., Павлович С.В. Оценка экспрессии микроРНК в очагах ретроцервикального эндометриоза. Акушерство и гинекология. 2018; 6: 55-61. [Bobrov M.Yu., Balashov I.S., Filippova E.S., Almova I.K., Timofeeva A.V., Gusar V.A., Borovikov P.I., Khilkevich E.G., Chuprynin V.D., Pavlovich S.V. Assessment of microRNA expression in retrocervical endometriotic lesions. Obstetrics and Gynecology. 2018; (6): 55-61. (in Russian)]. https://dx.doi.org/10.18565/aig.2018.6.55-61.
  30. Фархат К.Н., Савилова А.М., Макиян З.Н., Адамян Л.В. Эндометриоз: роль стволовых клеток в развитии заболевания (обзор литературы). Проблемы репродукции. 2016; 22(1): 20 7. [Farkhat KN, Savilova AM, Makiian ZN, Adamyan LV. The role of stem cells in the pathogenesis of endometriosis (а review). Russian Journal of Human Reproduction. 2016; 22(1): 20-7. (in Russian)]. https://dx.doi.org/10.17116/repro201622120-27.
  31. Bahramy A., Zafari N., Izadi P., Soleymani F., Kavousi S., Noruzinia M. The role of miRNAs 340-5p, 92a-3p, and 381-3p in patients with endometriosis: a plasma and mesenchymal stem-like cell study. Biomed. Res. Int. 2021; 2021: 5298006. https://dx.doi.org/10.1155/2021/5298006.
  32. Filip L., Duică F., Prădatu A., Crețoiu D., Suciu N., Crețoiu S.M. et al. Endometriosis associated infertility: a critical review and analysis on etiopathogenesis and therapeutic approaches. Medicina (Kaunas). 2020; 56(9): 460. https://dx.doi.org/10.3390/medicina56090460.
  33. Gilabert-Estelles J., Braza-Boils A., Ramon L.A., Zorio E., Medina P., Espana F. et al. Role of microRNAs in gynecological pathology. Curr. Med. Chem. 2012; 19(15): 2406-13. https://dx.doi.org/10.2174/092986712800269362
  34. Blondal T., Jensby Nielsen S., Baker A., Andreasen D., Mouritzen P., Wrang Teilum M. et al. Assessing sample and miRNA profile quality in serum and plasma or other biofluids. Methods. 2013; 59(1): S1-6. https://dx.doi.org/10.1016/j.ymeth.2012.09.015.
  35. Bashti O., Noruzinia M., Garshasbi M., Abtahi M. miR-31 and miR-145 as potential non-invasive regulatory biomarkers in patients with endometriosis. Cell J. 2018; 20(2): 293. https://dx.doi.org/10.22074/cellj.2018.5850.
  36. Zafari N., Tarafdari A.M., Izadi P., Noruzinia M., Yekaninejad M.S., Bahramy A. et al. A panel of plasma miRNAs 199b-3p, 224-5p and Let-7d-3p as non-invasive diagnostic biomarkers for endometriosis. Reprod. Sci. 2021; 28(4): 991-9. https://dx.doi.org/10.1007/s43032-020-00415-z.
  37. Pateisky P., Pils D., Szabo L., Kuessel L., Husslein H., Schmitz A. et al. hsa-miRNA-154-5p expression in plasma of endometriosis patients is a potential diagnostic marker for the disease. Reprod.. Biomed. Online. 2018; 37(4): 449-66. https://dx.doi.org/10.1016/j.rbmo.2018.05.007.
  38. Nothnick W.B., Falcone T., Joshi N., Fazleabas A.T., Graham A. Serum miR-451a levels are significantly elevated in women with endometriosis and recapitulated in baboons (Papio anubis) with experimentally-induced disease. Reprod. Sci. 2017; 24(8): 1195-202. https://dx.doi.org/10.1177/1933719116681519.
  39. Moustafa S., Burn M., Mamillapalli R., Nematian S., Flores V., Taylor H.S. Accurate diagnosis of endometriosis using serum microRNAs. Am. J. Obstet. Gynecol. 2020; 223(4): 557.e1-557.e11. https://dx.doi.org/10.1016/j.ajog.2020.02.050.
  40. Chico-Sordo L., Ruiz-Martínez T., Toribio M., González-Martín R., Spagnolo E., Domínguez F. et al. Identification of miR-30c-5p microRNA in serum as a candidate biomarker to diagnose endometriosis. Int. J. Mol. Sci. 2024; 25(3): 1853. https://dx.doi.org/10.3390/ijms25031853.
  41. Maged A.M., Deeb W.S., El Amir A., Zaki S.S., El Sawah H., Al Mohamady M. et al. Diagnostic accuracy of serum miR-122 and miR-199a in women with endometriosis. Int. J. Gynaecol. Obstet. 2018; 141(1): 14-9. https://dx.doi.org/10.1002/ijgo.12392.
  42. Papari E., Noruzinia M., Kashani L., Foster W.G. Identification of candidate microRNA markers of endometriosis with the use of next-generation sequencing and quantitative real-time polymerase chain reaction. Fertil. Steril. 2020; 113(6): 1232-41. https://dx.doi.org/10.1016/j.fertnstert.2020.01.026.
  43. Cosar E., Mamillapalli R., Ersoy G.S., Cho S., Seifer B., Taylor H.S. Serum microRNAs as diagnostic markers of endometriosis: a comprehensive array-based analysis. Fertil. Steril. 2016; 106(2): 402-9. https://dx.doi.org/10.1016/j.fertnstert.2016.04.013.
  44. Cho S., Mutlu L., Grechukhina O., Taylor H.S. Circulating microRNAs as potential biomarkers for endometriosis. Fertil. Steril. 2015; 103(5): 1252-60.e1. https://dx.doi.org/10.1016/j.fertnstert.2015.02.013.
  45. Vanhie A., Caron E., Vermeersch E., O D., Tomassetti C., Meuleman C., Mestdagh P. et al. Circulating microRNAs as non-invasive biomarkers in endometriosis diagnosis-a systematic review. Biomedicines. 2024; 12(4): 888. https://dx.doi.org/10.3390/biomedicines12040888.
  46. Bendifallah S., Dabi Y., Suisse S., Delbos L., Spiers A., Poilblanc M. et al. Validation of a salivary miRNA signature of endometriosis - interim data. NEJM Evid. 2023; 2(7): EVIDoa2200282. https://dx.doi.org/10.1056/EVIDoa2200282.
  47. Bendifallah S., Dabi Y., Suisse S., Ilic J., Delbos L., Poilblanc M. et al. Saliva-based microRNA diagnostic signature for the superficial peritoneal endometriosis phenotype. Eur. J. Obstet. Gynecol. Reprod. Biol. 2024; 297: 187-96. https://dx.doi.org/10.1016/j.ejogrb.2024.04.020.
  48. Dabi Y., Suisse S., Puchar A., Delbos L., Poilblanc M., Descamps P. et al. Endometriosis-associated infertility diagnosis based on saliva microRNA signatures. Reprod. Biomed. Online. 2023; 46(1): 138-49. https://dx.doi.org/10.1016/j.rbmo.2022.09.019.
  49. Yáñez-Mó M., Siljander P.R., Andreu Z., Zavec A.B., Borràs F.E., Buzas E.I. et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles. 2015; 4: 27066. https://dx.doi.org/10.3402/jev.v4.27066.
  50. Gallo A., Tandon M., Alevizos I., Illei G.G. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One. 2012; 7(3): e30679. https://dx.doi.org/10.1371/journal.pone.0030679.
  51. Zhang L., Li H., Yuan M., Li D., Sun C., Wang G. Serum exosomal microRNAs as potential circulating biomarkers for endometriosis. Dis. Markers. 2020; 2020: 2456340. https://dx.doi.org/10.1155/2020/2456340.
  52. Jia S.Z., Yang Y., Lang J., Sun P., Leng J. Plasma miR-17-5p, miR-20a and miR-22 are down-regulated in women with endometriosis. Hum. Reprod. 2013; 28(2): 322-30. https://dx.doi.org/10.1093/humrep/des413.
  53. Rekker K., Saare M., Roost A.M., Kaart T., Sõritsa D., Karro H. et al. Circulating miR-200-family micro-RNAs have altered plasma levels in patients with endometriosis and vary with blood collection time. Fertil. Steril. 2015; 104(4): 938-946.e2. https://dx.doi.org/10.1016/j.fertnstert.2015.06.029.
  54. Wang F., Wang H., Jin D., Zhang Y. Serum miR-17, IL-4, and IL-6 levels for diagnosis of endometriosis. Medicine (Baltimore). 2018; 97(24): e10853. https://dx.doi.org/10.1097/MD.0000000000010853.
  55. Nisenblat V., Sharkey D.J., Wang Z., Evans S.F., Healey M., Ohlsson Teague E.M.C. et al. Plasma miRNAs display limited potential as diagnostic tools for endometriosis. J. Clin. Endocrinol. Metab. 2019; 104(6): 1999-2022. https://dx.doi.org/10.1210/jc.2018-01464.
  56. Hossein Razi M., Eftekhar M., Ghasemi N., Hasan Sheikhha M., Dehghani Firoozabadi A. Expression levels of circulatory mir-185-5p, vascular endothelial growth factor, and platelet-derived growth factor target genes in endometriosis. Int. J. Reprod. Biomed. 2020; 18(5): 347-58. https://dx.doi.org/10.18502/ijrm.v13i5.7155.
  57. Gu C.L., Zhang Z., Fan W.S., Li L.A., Ye M.X., Zhang Q. et al. Identification of microRNAs as potential biomarkers in ovarian endometriosis. Reprod. Sci. 2020; 27(9): 1715-23. https://dx.doi.org/10.1007/s43032-020-00148-z.
  58. Bendifallah S., Dabi Y., Suisse S., Jornea L., Bouteiller D., Touboul C. et al. MicroRNome analysis generates a blood-based signature for endometriosis. Sci Rep. 2022; 12(1): 4051. https://dx.doi.org/10.1038/s41598-022-07771-7.
  59. Perricos A., Proestling K., Husslein H., Kuessel L., Hudson Q.J., Wenzl R. et al. Hsa-mir-135a shows potential as a putative diagnostic biomarker in saliva and plasma for endometriosis. Biomolecules. 2022; 12(8): 1144. https://dx.doi.org/10.3390/biom12081144.
  60. Walasik I., Klicka K., Grzywa T.M., Szymusik I., Włodarski P., Wielgoś M. et al. Circulating miR-3613-5p but not miR-125b-5p, miR-199a-3p, and miR-451a are biomarkers of endometriosis. Reprod. Biol. 2023; 23(4): 100796. https://dx.doi.org/10.1016/j.repbio.2023.100796.
  61. Tahermanesh K., Hakimpour S., Govahi A., Rokhgireh S., Mehdizadeh M., Minaeian S. et al. Evaluation of expression of biomarkers of PLAGL1 (ZAC1), microRNA, and their non-coding RNAs in patients with endometriosis. J. Gynecol. Obstet. Hum. Reprod. 2023; 52(4): 102568. https://dx.doi.org/10.1016/j.jogoh.2023.102568.
  62. Hsu C.Y., Hsieh T.H., Tsai C.F., Tsai H.P., Chen H.S., Chang Y. et al. miRNA-199a-5p regulates VEGFA in endometrial mesenchymal stem cells and contributes to the pathogenesis of endometriosis. J. Pathol. 2014; 232(3):330-43. https://dx.doi.org/10.1002/path.4295.
  63. Wang W.T., Zhao Y.N., Han B.W., Hong S.J., Chen Y.Q. Circulating microRNAs identified in a genome-wide serum microRNA expression analysis as noninvasive biomarkers for endometriosis. J. Clin. Endocrinol. Metab. 2013; 98(1): 281-9. https://dx.doi.org/10.1210/jc.2012-2415.
  64. Hu Z., Mamillapalli R., Taylor H.S. Increased circulating miR-370-3p regulates steroidogenic factor 1 in endometriosis. Am. J. Physiol. Endocrinol. Metab. 2019; 316(3): E373-E382. doi: 10.1152/ajpendo.00244.2018.
  65. Pang Q.X., Liu Z. miR-17-5p mitigates endometriosis by directly regulating VEGFA. J. Biosci. 2020; 45: 78.
  66. Misir S., Hepokur C., Oksasoglu B., Yildiz C., Yanik A., Aliyazicioglu Y. Circulating serum miR-200c and miR-34a-5p as diagnostic biomarkers for endometriosis. J. Gynecol. Obstet. Hum. Reprod. 2021; 50(4): 102092. https://dx.doi.org/10.1016/j.jogoh.2021.102092.
  67. He S., Li J., Ma D., Liu Z., Lv N. MicroRNA-148a targets ADAMTS5 to inhibit proliferation of endometriosis cells. Pak. J. Pharm. Sci. 2022; 35(1(Special)): 335-41.
  68. Neuhausser W.M., Faure-Kumar E., Mahurkar-Joshi S., Iliopoulos D., Sakkas D. Identification of miR-34-3p as a candidate follicular phase serum marker for endometriosis: a pilot study. F. S. Sci. 2022; 3(3): 269-78. https://dx.doi.org/10.1016/j.xfss.2022.02.005.
  69. Kumari P., Sharma I., Saha S.C., Srinivasan R., Bhardwaj P. Role of serum microRNAs as biomarkers for endometriosis, endometrioid carcinoma of ovary & endometrioid endometrial cancer. Indian J. Med. Res. 2022; 156(3): 516-23. https://dx.doi.org/10.4103/ijmr.IJMR_288_20.
  70. Lin C., Zeng S., Li M. miR-424-5p combined with miR-17-5p has high diagnostic efficacy for endometriosis. Arch. Gynecol. Obstet. 2023; 307(1):169-77. https://dx.doi.org/10.1007/s00404-022-06492-6.
  71. Yang X., Tao Y., Jin O., Lai J., Yang X. MiR-17-5p promoter methylation regulated by DNA methyltransferase 3 beta (DNMT3B) expedites endometriosis via the Krüppel-like factor 12 (KLF12)/Wnt/β-catenin axis. J. Reprod. Immunol. 2023; 158: 103974. https://dx.doi.org/10.1016/j.jri.2023.103974.
  72. Wang L., Huang W., Ren C., Zhao M., Jiang X., Fang X. et al. Analysis of serum microRNA profile by Solexa sequencing in women with endometriosis. Reprod. Sci. 2016; 23(10): 1359-70. https://dx.doi.org/10.1177/1933719116641761.
  73. Wang W.T., Zhao Y.N., Han B.W., Hong S.J., Chen Y.Q. Circulating microRNAs identified in a genome-wide serum microRNA expression analysis as noninvasive biomarkers for endometriosis. J. Clin. Endocrinol. Metab. 2013; 98(1): 281-9. https://dx.doi.org/10.1210/jc.2012-2415.
  74. Dai L., Gu L., Di W. MiR-199a attenuates endometrial stromal cell invasiveness through suppression of the IKKβ/NF-κB pathway and reduced interleukin-8 expression. Mol. Hum. Reprod. 2012; 18(3): 136-45. https://dx.doi.org/10.1093/molehr/gar066.
  75. Vitonis A.F., Vincent K., Rahmioglu N., Fassbender A., Buck Louis G.M., Hummelshoj L. et al.; WERF EPHect Working Group. World Endometriosis Research Foundation Endometriosis Phenome and Biobanking Harmonization Project: II. Clinical and covariate phenotype data collection in endometriosis research. Fertil. Steril. 2014; 102(5): 1223-32. https://dx.doi.org/10.1016/j.fertnstert.2014.07.1244.
  76. Rahmioglu N., Fassbender A., Vitonis A.F., Tworoger S.S., Hummelshoj L., D'Hooghe T.M. et al.; WERF EPHect Working Group. World Endometriosis Research Foundation Endometriosis Phenome and Biobanking Harmonization Project: III. Fluid biospecimen collection, processing, and storage in endometriosis research. Fertil. Steril. 2014; 102(5): 1233-43. https://dx.doi.org/10.1016/j.fertnstert.2014.07.1208.

Received 05.02.2025

Accepted 23.04.2025

About the Authors

Maria I. Yarmolinskaya, Dr. Med. Sci., Professor of the Russian Academy of Sciences, Head of the Department of Gynecology and Endocrinology, Head of the Center of Diagnostics and Treatment of Endometriosis, D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology,
199034, Russia, St. Petersburg, Mendeleevskaya line, 3, m.yarmolinskaya@gmail.com, SPIN-код: 3686-3605, Researcher ID: P-2183-2014, Scopus Author ID: 7801562649, https://orcid.org/0000-0002-6551-4147
Sofya A. Cherkashina, doctor at the Consultative and Diagnostic Department II, D.O. Ott Research institute of Obstetrics, Gynecology and Reproductology,
199034, Russia, St. Petersburg, Mendeleevskaya line, 3, sonyach@list.ru, https://orcid.org/0009-0005-7208-3575
Olga V. Malysheva, PhD (Bio), Senior Researcher at the Laboratory of Genomics, D.O. Ott Research Institute of Obstetrics, Gynecology and Reproductology,
199034, Russia, St. Petersburg, Mendeleevskaya line, 3, omal99@mail.ru, https://orcid.org/0000-0002-8626-5071
Corresponding author: Maria I. Yarmolinskaya, m.yarmolinskaya@gmail.com

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