Молекулярная биология, 2022, T. 56, № 1, стр. 35-54

МикроРНК как потенциальные регуляторы инфицирования SARS-CоV-2 и модификаторы клинической картины COVID-19

А. Н. Кучер a, Ю. А. Королёва a, А. А. Зарубин a, М. С. Назаренко a*

a Научно-исследовательский институт медицинской генетики, Томский национальный исследовательский медицинский центр Российской академии наук
634050 Томск, Россия

* E-mail: maria.nazarenko@medgenetics.ru

Поступила в редакцию 09.03.2021
После доработки 14.05.2021
Принята к публикации 25.05.2021

Аннотация

Пандемия, вызванная вирусом SARS-CoV-2, определила актуальность выявления факторов, способных влиять как на риск инфицирования, так и на тяжесть течения COVID-19. Среди этих факторов особый интерес представляют микроРНК, обладающие широким регуляторным потенциалом. В представленном обзоре обсуждается возможная роль микроРНК человека и генома/микроРНК SARS-CoV-2 в инфицировании и определении клинической картины COVID-19. Обобщена информация о SARS-CoV-2-специфичных микроРНК человека, уровне их экспрессии в различных органах (клетках) в норме и при развитии заболеваний, которые являются факторами риска тяжелого течения COVID-19. Обсуждается возможное участие SARS-CoV-2 в развитии клинической картины COVID-19, в том числе и посредством подавления микроРНК и РНК-связывающих белков человека, изменения уровня экспрессии генов в инфицированных клетках, возможных эпигенетических модификаций генома человека с участием микроРНК коронавирусного происхождения.

Ключевые слова: микроРНК, SARS-CoV-2, COVID-19

Список литературы

  1. Ejaz H., Alsrhani A., Zafar A., Javed H., Junaid K., Abdalla A.E., Abosalif K.O.A., Ahmed Z., Younas S. (2020) COVID-19 and comorbidities: deleterious impact on infected patients. J. Infect. Publ. Hlth. 13(12), 1833–1839.

  2. Fulzele S., Sahay B., Yusufu I., Lee T.J., Sharma A., Kolhe R., Isales C.M. (2020) COVID-19 virulence in aged patients might be impacted by the host cellular microRNAs abundance/profile. Aging Dis. 11(3), 509–522.

  3. Callender L.A., Curran M., Bates S.M., Mairesse M., Weigandt J., Betts C.J. (2020) The impact of pre-existing comorbidities and therapeutic interventions on COVID-19. Front. Immunol. 11, 1991.

  4. Jutzeler C.R., Bourguignon L., Weis C.V., Tong B., Wong C., Rieck B., Pargger H., Tschudin-Sutter S., Egli A., Borgwardt K., Walter M. (2020) Comorbidities, clinical signs and symptoms, laboratory findings, imaging features, treatment strategies, and outcomes in adult and pediatric patients with COVID-19: A systematic review and meta-analysis. Travel. Med. Infect. Dis. 37, 101825.

  5. Murk W., Gierada M., Fralick M., Weckstein A., Klesh R., Rassen J.A. (2021) Diagnosis-wide analysis of COVID-19 complications: an exposure-crossover study. CMAJ. 193(1), E10–E18.

  6. Chang W.T., Toh H.S., Liao C.T., Yu W.L. (2021) Cardiac Involvement of COVID-19: a comprehensive review. Am. J. Med. Sci. 361(1), 14–22.

  7. Avila J., Long B., Holladay D., Gottlieb M. (2021) Thrombotic complications of COVID-19. Am. J. Emerg. Med. 39, 213–218.

  8. Collantes M., Espiritu A.I., Sy M., Anlacan V., Jamora R. (2021). Neurological manifestations in COVID-19 infection: a systematic review and meta-analysis. Can. J. Neurol. Sci. 48(1), 66–76.

  9. Tang H., Gao Y., Li Z., Miao Y., Huang Z., Liu X., Xie L., Li H., Wen W., Zheng Y., Su W. (2020) The noncoding and coding transcriptional landscape of the peripheral immune response in patients with COVID-19. Clin. Transl. Med. 10(6), e200.

  10. Satyam R., Bhardwaj T., Goel S., Jha N.K., Jha S.K., Nand P., Ruokolainen J., Kamal M.A., Kesari K.K. (2021) miRNAs in SARS-CoV-2: a spoke in the wheel of pathogenesis. Curr. Pharm. Des. 27(13), 1628–1641.

  11. Chow J.T., Salmena L. (2020) Prediction and analysis of SARS-CoV2-targeting microRNA in human lung epithelium. Genes. 11(9), 1002.

  12. Jafarinejad-Farsangi S., Jazi M.M., Rostamzadeh F., Hadizadeh M. (2020) High affinity of host human microRNAs to SARS-CoV-2 genome: an in silico analysis. Noncoding RNA Res. 5(4), 222–231.

  13. Guo L., Yu J., Yu H., Zhao Y., Chen S., Xu C., Chen F. (2015) Evolutionary and expression analysis of miR-#-5p and miR-#-3p at the miRNAs/isomiRs levels. Biomed. Res. Int. 2015, 168358.

  14. Guterres A., de Azeredo Lima C.H., Miranda R.L., Gadelha M.R. (2020) What is the potential function of microRNAs as biomarkers and therapeutic targets in COVID-19. Infect. Genet. Evol. 85, 104417.

  15. Saçar Demirci M.D., Adan A. (2020) Computational analysis of microRNA-mediated interactions in SARS-CoV-2 infection. Peer. J. 8, e9369.

  16. Huang Z., Shi J., Gao Y., Cui C., Zhang S., Li J., Zhou Y., Cui Q. (2019). HMDD v3.0: a database for experimentally supported human microRNA-disease associations. Nucl. Acids Res. 47(D1), D1013–D1017.

  17. Zhao X., Wang Y., Sun X. (2020) The functions of microRNA-208 in the heart. Diabetes Res. Clin. Pract. 160, 108004.

  18. Chan A.P., Choi Y., Schork N.J. (2020) Conserved genomic terminals of SARS-CoV-2 as coevolving functional elements and potential therapeutic targets. mSphere. 5(6), e00754-20.

  19. Khan M.A., Sany M., Islam M.S., Islam A. (2020) Epigenetic regulator miRNA pattern differences among SARS-CoV, SARS-CoV-2, and SARS-CoV-2 world-wide isolates delineated the mystery behind the epic pathogenicity and distinct clinical characteristics of pandemic COVID-19. Front. Genet. 11, 765.

  20. Abu-Izneid T., AlHajri N., Mohammed Ibrahim A., Noushad Javed M., Mustafa Salem K., Hyder Pottoo F., Amjad Kamal M. (2021) Micro-RNAs in the regulation of immune response against SARS-CoV-2 and other viral infections. J. Adv. Res. 30, 133–145.

  21. Aydemir M.N., Aydemir H.B., Korkmaz E.M., Budak M., Cekin N., Pinarbasi E. (2021) Computationally predicted SARS-COV-2 encoded microRNAs target NFKB, JAK/STAT and TGFB signaling pathways. Gene Rep. 22, 101012.

  22. Mukherjee M., Goswami S. (2020) Global cataloguing of variations in untranslated regions of viral genome and prediction of key host RNA binding protein-microRNA interactions modulating genome stability in SARS-CoV-2. PLoS One. 15(8), e0237559.

  23. Farshbaf A., Mohtasham N., Zare R., Mohajertehran F., Rezaee S.A. (2021) Potential therapeutic approaches of microRNAs for COVID-19: challenges and opportunities. J. Oral. Biol. Craniofac. Res. 11(2), 132–137.

  24. Girardi E., López P., Pfeffer S. (2018) On the importance of host microRNAs during viral infection. Front. Genet. 9, 439.

  25. Ludwig N., Leidinger P., Becker K., Backes C., Fehlmann T., Pallasch C., Rheinheimer S., Meder B., Stähler C., Meese E., Keller A. (2016) Distribution of miRNA expression across human tissues. Nucl. Acids Res. 44(8), 3865–3877.

  26. de Rie D., Abugessaisa I., Alam T., Arner E., Arner P., Ashoor H., Åström G., Babina M., Bertin N., Burroughs A.M., Carlisle A.J., Daub C.O., Detmar M., Deviatiiarov R., Fort A., Gebhard C., Goldowitz D., Guhl S., Ha T.J., Harshbarger J., Hasegawa A., Hashimoto K., Herlyn M., Heutink P., Hitchens K.J., Hon C.C., Huang E., Ishizu Y., Kai C., Kasukawa T., Klinken P., Lassmann T., Lecellier C.H., Lee W., Lizio M., Makeev V., Mathelier A., Medvedeva Y.A., Mejhert N., Mungall C.J., Noma S., Ohshima M., Okada-Hatakeyama M., Persson H., Rizzu P., Roudnicky F., Sætrom P., Sato H., Severin J., Shin J.W., Swoboda R.K., Tarui H., Toyoda H., Vitting-Seerup K., Winteringham L., Yamaguchi Y., Yasuzawa K., Yoneda M., Yumoto N., Zabierowski S., Zhang P.G., Wells C.A., Summers K.M., Kawaji H., Sandelin A., Rehli M., FANTOM Consortium, Hayashizaki Y., Carninci P., Forrest A.R.R., de Hoon M.J.L. (2017). An integrated expression atlas of miRNAs and their promoters in human and mouse. Nat. Biotechnol. 35(9), 872–878.

  27. Sardar R., Satish D., Birla S., Gupta, D. (2020) Integrative analyses of SARS-CoV-2 genomes from different geographical locations reveal unique features potentially consequential to host-virus interaction, pathogenesis and clues for novel therapies. Heliyon. 6(9), e04658.

  28. Pierce J.B., Simion V., Icli B., Pérez-Cremades D., Cheng H.S., Feinberg M.W. (2020) Computational analysis of targeting SARS-CoV-2, viral entry proteins ACE2 and TMPRSS2, and interferon genes by host microRNAs. Genes. 11(11), 1354.

  29. Bartoszewski R., Dabrowski M., Jakiela B., Matalon S., Harrod K.S., Sanak M., Collawn J.F. (2020) SARS-CoV-2 may regulate cellular responses through depletion of specific host miRNAs. Am. J. Physiol. Lung Cell Mol. Physiol. 319(3), L444–L455.

  30. Hosseini Rad Sm A., McLellan A.D. (2020) Implications of SARS-CoV-2 mutations for genomic RNA structure and host microRNA targeting. Int. J. Mol. Sci. 21(13), 4807.

  31. Arisan E.D., Dart A., Grant G.H., Arisan S., Cuhadaroglu S., Lange S., Uysal-Onganer P. (2020) The prediction of miRNAs in SARS-CoV-2 genomes: hsa-miR databases identify 7 key miRs linked to host responses and virus pathogenicity-related KEGG pathways significant for comorbidities. Viruses. 12(6), 614.

  32. Balmeh N., Mahmoudi S., Mohammadi N., Karabedianhajiabadi A. (2020) Predicted therapeutic targets for COVID-19 disease by inhibiting SARS-CoV-2 and its related receptors. Inform. Med. Unlocked. 20, 100407.

  33. Kozomara A., Birgaoanu M., Griffiths-Jones S. (2019) miRBase: from microRNA sequences to function. Nucl. Acids Res. 47(D1), D155–D162.

  34. Nersisyan S., Engibaryan N., Gorbonos A., Kirdey K., Makhonin A., Tonevitsky A. (2020) Potential role of cellular miRNAs in coronavirus-host interplay. Peer J. 8, e9994.

  35. Naqvi A., Fatima K., Mohammad T., Fatima U., Singh I.K., Singh A., Atif S.M., Hariprasad G., Hasan G.M., Hassan M.I. (2020). Insights into SARS-CoV-2 genome, structure, evolution, pathogenesis and therapies: structural genomics approach. Biochim. Biophys. Acta Mol. Basis Dis. 1866(10), 165878.

  36. Li J., Huang D.Q., Zou B., Yang H., Hui W.Z., Rui F., Yee N., Liu C., Nerurkar S.N., Kai J., Teng M., Li X., Zeng H., Borghi J.A., Henry L., Cheung R., Nguyen M.H. (2021). Epidemiology of COVID-19: a systematic review and meta-analysis of clinical characteristics, risk factors, and outcomes. J. Med. Virol. 93(3), 1449–1458.

  37. Musri M.M., Coll-Bonfill N., Maron B.A., Peinado V.I., Wang R.S., Altirriba J., Blanco I., Oldham W.M., Tura-Ceide O., García-Lucio J., de la Cruz-Thea B., Meister G., Loscalzo J., Barberà J.A. (2018) MicroRNA dysregulation in pulmonary arteries from chronic obstructive pulmonary disease. relationships with vascular remodeling. Am. J. Respir. Cell Mol. Biol. 59(4), 490–499.

  38. Sundar I.K., Li D., Rahman I. (2019) Small RNA-sequence analysis of plasma-derived extracellular vesicle miRNAs in smokers and patients with chronic obstructive pulmonary disease as circulating biomarkers. J. Extracell. Vesicles. 8(1), 1684816.

  39. Cazorla-Rivero S., Mura-Escorche G., Gonzalvo-Hernández F., Mayato D., Córdoba-Lanús E., Casanova C. (2020) Circulating miR-1246 in the progression of chronic obstructive pulmonary disease (COPD) in patients from the BODE cohort. Int. J. Chron. Obstruct. Pulmon. Dis. 15, 2727–2737.

  40. Shi L., Xin Q., Chai R., Liu L., Ma Z. (2015) Ectopic expressed miR-203 contributes to chronic obstructive pulmonary disease via targeting TAK1 and PIK3CA. Int. J. Clin. Exp. Pathol. 8(9), 10662–10670.

  41. Wei C., Henderson H., Spradley C., Li L., Kim I.K., Kumar S., Hong N., Arroliga A.C., Gupta S. (2013) Circulating miRNAs as potential marker for pulmonary hypertension. PLoS One. 8(5), e64396.

  42. Huber L.C., Ulrich S., Leuenberger C., Gassmann M., Vogel J., von Blotzheim L.G., Speich R., Kohler M., Brock M. (2015) Featured article: microRNA-125a in pulmonary hypertension: regulator of a proliferative phenotype of endothelial cells. Ex. Biol. Med. (Maywood). 240(12), 1580–1589.

  43. Jardim M.J., Dailey L., Silbajoris R., Diaz-Sanchez D. (2012) Distinct microRNA expression in human airway cells of asthmatic donors identifies a novel asthma-associated gene. Am. J. Respir. Cell. Mol. Biol. 47(4), 536–542.

  44. Ke X.F., Fang J., Wu X.N., Yu C.H. (2014) MicroRNA-203 accelerates apoptosis in LPS-stimulated alveolar epithelial cells by targeting PIK3CA. Biochem. Biophys. Res. Commun. 450(4), 1297–1303.

  45. Marketou M.E., Kontaraki J.E., Maragkoudakis S., Patrianakos A., Konstantinou J., Nakou H., Vougia D., Logakis J., Chlouverakis G., Vardas P.E., Parthenakis F.I. (2018) MicroRNAs in peripheral mononuclear cells as potential biomarkers in hypertensive patients with heart failure with preserved ejection fraction. Am. J. Hypertens. 31(6), 651–657.

  46. Huang X., Li Z., Bai B., Li X., Li Z. (2015) High expression of microRNA-208 is associated with cardiac hypertrophy via the negative regulation of the sex-determining region Y-box 6 protein. Exp., Ther. Med. 10(3), 921–926.

  47. Kontaraki J.E., Marketou M.E., Parthenakis F.I., Maragkoudakis S., Zacharis E.A., Petousis S., Kochiadakis G.E., Vardas P.E. (2015) Hypertrophic and antihypertrophic microRNA levels in peripheral blood mononuclear cells and their relationship to left ventricular hypertrophy in patients with essential hypertension. J. Am. Soc. Hypertens. 9(10), 802–810.

  48. Wang G., Kwan B.C., Lai F.M., Choi P.C., Chow K.M., Li P.K., Szeto C.C. (2010) Intrarenal expression of miRNAs in patients with hypertensive nephrosclerosis. Am. J. Hypertens. 23(1), 78–84.

  49. Liu W., Zheng J., Dong J., Bai R., Song D., Ma X., Zhao L., Yao Y., Zhang H., Liu T. (2018) Association of miR-197-5p, a circulating biomarker for heart failure, with myocardial fibrosis and adverse cardiovascular events among patients with stage C or D heart failure. Cardiology. 141(4), 212–225.

  50. Wong L.L., Armugam A., Sepramaniam S., Karolina D.S., Lim K.Y., Lim J.Y., Chong J.P., Ng J.Y., Chen Y.T., Chan M.M., Chen Z., Yeo P.S., Ng T.P., Ling L.H., Sim D., Leong K.T., Ong H.Y., Jaufeerally F., Wong R., Chai P., Low A.F., Lam C.S., Jeyaseelan K., Richards A.M. (2015) Circulating microRNAs in heart failure with reduced and preserved left ventricular ejection fraction. Eur. J. Heart Fail. 17(4), 393–404.

  51. Hu Q., Luo W., Huang L., Huang R., Chen R. (2016) Apoptosis-related microRNA changes in the right atrium induced by remote ischemic perconditioning during valve replacement surgery. Sci. Rep. 6, 18959.

  52. He X., Ji J., Wang T., Wang M.B., Chen X.L. (2017) Upregulation of circulating miR-195-3p in heart failure. Cardiology. 138(2), 107–114.

  53. Liu H., Yang N., Fei Z., Qiu J., Ma D., Liu X., Cai G., Li S. (2016) Analysis of plasma miR-208a and miR-370 expression levels for early diagnosis of coronary artery disease. Biomed. Rep. 5(3), 332–336.

  54. Liu W., Ling S., Sun W., Liu T., Li Y., Zhong G., Zhao D., Zhang P., Song J., Jin X., Xu Z., Song H., Li Q., Liu S., Chai M., Dai Q., He Y., Fan Z., Zhou Y.J., Li Y. (2015) Circulating microRNAs correlated with the level of coronary artery calcification in symptomatic patients. Sci. Rep. 5, 16099.

  55. van Rooij E., Sutherland L.B., Liu N., Williams A.H., McAnally J., Gerard R.D., Richardson J.A., Olson E.N. (2006) A signature pattern of stress-responsive microRNAs that can evoke cardiac hypertrophy and heart failure. Proc. Natl. Acad. Sci. USA. 103(48), 18255–18260.

  56. Zhang X., Ji R., Liao X., Castillero E., Kennel P.J., Brunjes D.L., Franz M., Möbius-Winkler S., Drosatos K., George I., Chen E.I., Colombo P.C., Schulze P.C. (2018) MicroRNA-195 regulates metabolism in failing myocardium via alterations in sirtuin 3 expression and mitochondrial protein acetylation. Circulation. 137(19), 2052–2067.

  57. Weber K., Rostert N., Bauersachs S., Wess G. (2015) Serum microRNA profiles in cats with hypertrophic cardiomyopathy. Mol. Cell. Biochem. 402(1–2), 171–180.

  58. Slagsvold K.H., Johnsen A.B., Rognmo O., Høydal M.A., Wisløff U., Wahba A. (2014) Mitochondrial respiration and microRNA expression in right and left atrium of patients with atrial fibrillation. Physiol. Genomics. 46(14), 505–511.

  59. Cañón S., Caballero R., Herraiz-Martínez A., Pérez-Hernández M., López B., Atienza F., Jalife J., Hove-Madsen L., Delpón E., Bernad A. (2016) miR-208b upregulation interferes with calcium handling in HL-1 atrial myocytes: Implications in human chronic atrial fibrillation. J. Mol. Cell. Cardiol. 99, 162–173.

  60. Long G., Wang F., Duan Q., Yang S., Chen F., Gong W., Yang X., Wang Y., Chen C., Wang D.W. (2012) Circulating miR-30a, miR-195 and let-7b associated with acute myocardial infarction. PLoS One. 7(12), e50926.

  61. Boštjančič E., Brandner T., Zidar N., Glavač D., Štajer D. (2018) Down-regulation of miR-133a/b in patients with myocardial infarction correlates with the presence of ventricular fibrillation. Biomed. Pharmacother. 99, 65–71.

  62. Li C., Fang Z., Jiang T., Zhang Q., Liu C., Zhang C., Xiang Y. (2013) Serum microRNAs profile from genome-wide serves as a fingerprint for diagnosis of acute myocardial infarction and angina pectoris. BMC Med. Genomics. 6, 16.

  63. Nair N., Kumar S., Gongora E., Gupta S. (2013) Circulating miRNA as novel markers for diastolic dysfunction. Mol. Cell. Biochem. 376(1–2), 33–40.

  64. Wang Y.F., Lian X.L., Zhong J.Y., Su S.X., Xu Y.F., Xie X.F., Wang Z.P., Li W., Zhang L., Che D., Yu L., Huang P., Jia H.L., Gu X.Q. (2019) Serum exosomal microRNA let-7i-3p as candidate diagnostic biomarker for Kawasaki disease patients with coronary artery aneurysm. IUBMB Life. 71(7), 891–900.

  65. He L.P., Zhao X.S., He L.P. (2018) Abnormally expressed miR-23b in Chinese Mongolian at high cardiovascular risk may contribute to monocyte/macrophage inflammatory reaction in atherosclerosis. Biosci. Rep. 38(6), BSR20180673.

  66. Zampetaki A., Kiechl S., Drozdov I., Willeit P., Mayr U., Prokopi M., Mayr A., Weger S., Oberhollenzer F., Bonora E., Shah A., Willeit J., Mayr M. (2010) Plasma microRNA profiling reveals loss of endothelial miR-126 and other microRNAs in type 2 diabetes. Circ. Res. 107(6), 810–817.

  67. Zhao B., Li H., Liu J., Han P., Zhang C., Bai H., Yuan X., Wang X., Li L., Ma H., Jin X., Chu Y. (2016) MicroRNA-23b targets Ras GTPase-activating protein SH3 domain-binding protein 2 to alleviate fibrosis and albuminuria in diabetic nephropathy. J. Am. Soc. Nephrol. 27(9), 2597–2608.

  68. Párrizas M., Brugnara L., Esteban Y., González-Franquesa A., Canivell S., Murillo S., Gordillo-Bastidas E., Cussó R., Cadefau J.A., García-Roves P.M., Servitja J.M., Novials A. (2015) Circulating miR-192 and miR-193b are markers of prediabetes and are modulated by an exercise intervention. J. Clin. Endocrinol. Metab. 100(3), E407–E415.

  69. Kim H., Bae Y.U., Jeon J.S., Noh H., Park H.K., Byun D.W., Han D.C., Ryu S., Kwon S.H. (2019) The circulating exosomal microRNAs related to albuminuria in patients with diabetic nephropathy. J. Transl. Med. 17(1), 236.

  70. Torella D., Ellison G.M., Torella M., Vicinanza C., Aquila I., Iaconetti C., Scalise M., Marino F., Henning B.J., Lewis F.C., Gareri C., Lascar N., Cuda G., Salvatore T., Nappi G., Indolfi C., Torella R., Cozzolino D., Sasso F.C. (2014) Carbonic anhydrase activation is associated with worsened pathological remodeling in human ischemic diabetic cardiomyopathy. J. Am. Heart Assoc. 3(2), e000434.

  71. Friedrich J., Steel D.H.W., Schlingemann R.O., Koss M.J., Hammes H.P., Krenning G., Klaassen I. (2020) microRNA expression profile in the vitreous of proliferative diabetic retinopathy patients and differences from patients treated with anti-VEGF therapy. Transl. Vis. Sci. Technol. 9(6), 16.

  72. Dubois-Camacho K., Diaz-Jimenez D., De la Fuente M., Quera R., Simian D., Martínez M., Landskron G., Olivares-Morales M., Cidlowski J.A., Xu X., Gao G., Xie J., Chnaiderman J., Soto-Rifo R., González M.J., Calixto A., Hermoso M.A. (2019) Inhibition of miR-378a-3p by inflammation enhances IL-33 levels: a novel mechanism of alarmin modulation in ulcerative colitis. Front. Immunol. 10, 2449.

  73. Zhu S., Pan W., Song X., Liu Y., Shao X., Tang Y., Liang D., He D., Wang H., Liu W., Shi Y., Harley J.B., Shen N., Qian Y. (2012) The microRNA miR-23b suppresses IL-17-associated autoimmune inflammation by targeting TAB2, TAB3 and IKK-α. Nat. Med. 18(7), 1077–1086.

  74. Krissansen G.W., Yang Y., McQueen F.M., Leung E., Peek D., Chan Y.C., Print C., Dalbeth N., Williams M., Fraser A.G. (2015) Overexpression of miR-595 and miR-1246 in the sera of patients with active forms of inflammatory bowel disease. Inflamm. Bowel Dis. 21(3), 520–530.

  75. Méndez-Flores S., Furuzawa-Carballeda J., Hernández-Molina G., Ramírez-Martinez G., Regino-Zamarripa N.E., Ortiz-Quintero B., Jiménez-Alvarez L., Cruz-Lagunas A., Zúñiga J. (2019) MicroRNA expression in cutaneous lupus: a new window to understand its pathogenesis. Mediators Inflamm. 2019, 5049245.

  76. Hiratsuka I., Yamada H., Munetsuna E., Hashi-moto S., Itoh M. (2016) Circulating microRNAs in Graves’ disease in relation to clinical activity. Thyroid. 26(10), 1431–1440.

  77. Tsigaris P., Teixeira da Silva J.A. (2020) Smoking prevalence and COVID-19 in Europe. Nicotine Tob. Res. 22(9), 1646–1649.

  78. Liu S., Cao Y., Du T., Zhi Y. (2020) Prevalence of comorbid asthma and related outcomes in COVID-19: a systematic review and meta-analysis. J. Allergy Clin. Immunol. Pract. 9(2), 693–701.

  79. Wakabayashi M., Pawankar R., Narazaki H., Ueda T., Itabashi T. (2021) Coronavirus disease 2019 and asthma, allergic rhinitis: molecular mechanisms and host-environmental interactions. Curr. Opin. Allergy Clin. Immunol. 21(1), 1–7.

  80. Inchley C.S., Sonerud T., Fjærli H.O., Nakstad B. (2015) Nasal mucosal microRNA expression in children with respiratory syncytial virus infection. BMC Infect. Dis. 15, 150.

  81. Zhu X., Ge Y., Wu T., Zhao K., Chen Y., Wu B., Zhu F., Zhu B., Cui L. (2020) Co-infection with respiratory pathogens among COVID-2019 cases. Virus Res. 285, 198005.

  82. Zhang H., Rostami M.R., Leopold P.L., Mezey J.G., O’Beirne S.L., Strulovici-Barel Y., Crystal R.G. (2020) Expression of the SARS-CoV-2 ACE2 receptor in the human airway epithelium. Am. J. Respir. Crit. Care Med. 202(2), 219–229.

  83. Azevedo R.B., Botelho B.G., Hollanda J., Ferreira L., Junqueira de Andrade L.Z., Oei S., Mello T.S., Muxfeldt E.S. (2021) COVID-19 and the cardiovascular system: a comprehensive review. J. Hum. Hypertens. 35(1), 4–11.

  84. Sabbatinelli J., Giuliani A., Matacchione G., Latini S., Laprovitera N., Pomponio G., Ferrarini A., Baroni S.S., Pavani M., Moretti M., Gabrielli A., Procopio A.D., Ferracin M., Bonafè M., Olivieri F. (2020) Decreased serum levels of the inflammaging marker miR-146a are associated with clinical response to tocilizumab in COVID-19 patients. Mech. Ageing Dev. 193, 111413.

  85. Kabeerdoss J., Pilania R.K., Karkhele R., Kumar T.S., Danda D., Singh S. (2021) Severe COVID-19, multisystem inflammatory syndrome in children, and Kawasaki disease: immunological mechanisms, clinical manifestations and management. Rheumatol. Int. 41(1), 19–32.

  86. Sokolovsky S., Soni P., Hoffman T., Kahn P., Scheers-Masters J. (2021) COVID-19 associated Kawasaki-like multisystem inflammatory disease in an adult. Am. J. Emerg. Med. 39, 253.e1–253.e2.

  87. Alsaied T., Tremoulet A.H., Burns J.C., Saidi A., Dionne A., Lang S.M., Newburger J.W., de Ferranti S., Friedman K.G. (2021) Review of cardiac involvement in multisystem inflammatory syndrome in children. Circulation. 143(1), 78–88.

  88. Galeotti C., Bayry J. (2020) Autoimmune and inflammatory diseases following COVID-19. Nat. Rev. Rheumatol. 16(8), 413–414.

  89. Wolff D., Nee S., Hickey N.S., Marschollek M. (2021) Risk factors for Covid-19 severity and fatality: a structured literature review. Infection. 49 (1), 15–28.

  90. Zhou Y., Chi J., Lv W., Wang Y. (2021) Obesity and diabetes as high-risk factors for severe coronavirus disease 2019 (COVID-19). Diabetes Metab. Res. Rev. 37(2), e3377.

  91. Monteleone G., Ardizzone S. (2020) Are patients with inflammatory bowel disease at increased risk for COVID-19 infection? J. Crohns Colitis. 14(9), 1334–1336.

  92. Favalli E.G., Ingegnoli F., De Lucia O., Cincinelli G., Cimaz R., Caporali R. (2020) COVID-19 infection and rheumatoid arthritis: faraway, so close! Autoimmun. Rev. 19(5), 102523.

  93. Liu Y., Sawalha A.H., Lu Q. (2021) COVID-19 and autoimmune diseases. Curr. Opin. Rheumatol. 33(2), 155–162.

  94. Xu L.J., Jiang T., Zhao W., Han J.F., Liu J., Deng Y.Q., Zhu S.Y., Li Y.X., Nian Q.G., Zhang Y., Wu X.Y., Qin E.D., Qin C.F. (2014) Parallel mRNA and microRNA profiling of HEV71-infected human neuroblastoma cells reveal the up-regulation of miR-1246 in association with DLG3 repression. PLoS One. 9(4), e95272.

  95. Morales L., Oliveros J.C., Fernandez-Delgado R., tenOever B.R., Enjuanes L., Sola I. (2017) SARS-CoV-encoded small RNAs contribute to infection-associated lung pathology. Cell Host Microbe. 21, 344–355.

  96. El-Hefny M., Fouad S., Hussein T., Abdel-Hameed R., Effat H., Mohamed H., Abdel Wahab A.H. (2019) Circulating microRNAs as predictive biomarkers for liver disease progression of chronic hepatitis C (genotype-4) Egyptian patients. J. Med. Virol. 91(1), 93–101.

  97. Bastian F.B., Roux J., Niknejad A., Comte A., Fonseca Costa S.S., de Farias T.M., Moretti S., Parmentier G., de Laval V.R., Rosikiewicz M., Wollbrett J., Echchiki A., Escoriza A., Gharib W.H., Gonzales-Porta M., Jarosz Y., Laurenczy B., Moret P., Person E., Roelli P., Sanjeev K., Seppey M., Robinson-Rechavi M. (2021) The Bgee suite: integrated curated expression atlas and comparative transcriptomics in animals. Nucl. Acids Res. 49(D1), D831–D847.

  98. UniProt Consortium (2021) UniProt: the universal protein knowledgebase in 2021. Nucl. Acids Res. 49(D1), D480–D489.

  99. Ahmad I., Rathore F.A. (2020) Neurological manifestations and complications of COVID-19: a literature review. J. Clin. Neurosci. 77, 8–12.

  100. Srivastava R., Daulatabad S.V., Srivastava M., Janga S.C. (2020) Role of SARS-CoV-2 in altering the RNA-binding protein and miRNA-directed post-transcriptional regulatory networks in humans. Int. J. Mol. Sci. 21(19), 7090.

  101. Jang Y., Seo S.H. (2020) Gene expression pattern differences in primary human pulmonary epithelial cells infected with MERS-CoV or SARS-CoV-2. Arch. Virol. 165(10), 2205–2211.

  102. Blanco-Melo D., Nilsson-Payant B.E., Liu W.C., Uhl S., Hoagland D., Møller R., Jordan T.X., Oishi K., Panis M., Sachs D., Wang T.T., Schwartz R.E., Lim J.K., Albrecht R.A., tenOever B.R. (2020) Imbalanced host response to SARS-CoV-2 drives development of COVID-19. Cell. 181(5), 1036–1045.e9.

  103. Bertolazzi G., Cipollina C., Benos P.V., Tumminello M., Coronnello C. (2020) miR-1207-5p can contribute to dysregulation of inflammatory response in COVID-19 via targeting SARS-CoV-2 RNA. Front Cell Infect. Microbiol. 10, 586592.

  104. Mishra R., Kumar A., Ingle H., Kumar H. (2020) The interplay between viral-derived miRNAs and host immunity during infection. Front. Immunol. 10, 3079.

  105. Merino G.A., Raad J., Bugnon L.A., Yones C., Kamenetzky L., Claus J., Ariel F., Milone D.H., Stegmayer G. (2021) Novel SARS-CoV-2 encoded small RNAs in the passage to humans. Bioinformatics. 36(24), 5571–5581.

Дополнительные материалы

скачать ESM.docx
Таблица S1. Методические подходы, использованные в исследованиях, посвященных поиску микроРНК, потенциально способных связываться с геномами SARS-CoV-2 и других коронавирусов
 
Список литературы.