Возможности применения микроРНК для неинвазивной диагностики эндометриоза

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.
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.
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"
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.
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.
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.
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.
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.
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.
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.

Поступила 05.02.2025

Принята в печать 23.04.2025