Молекулярная биология, 2022, T. 56, № 3, стр. 418-427

МикроРНК miR-375 как многофункциональный регулятор сердечно-сосудистой системы

Н. А. Матвеева ab, Н. М. Баулина ab, И. С. Киселев ab, Б. В. Титов ab, О. О. Фаворова ab*

a Национальный медицинский исследовательский центр кардиологии Министерства здравоохранения Российской Федерации
121552 Москва, Россия

b Российский национальный исследовательский медицинский университет им. Н.И. Пирогова Министерства здравоохранения Российской Федерации
117997 Москва, Россия

* E-mail: olga_favorova@mail.ru

Поступила в редакцию 21.09.2021
После доработки 12.10.2021
Принята к публикации 12.10.2021

Аннотация

МикроРНК miR-375 действует как многофункциональный регулятор активности многих физиологических и патологических клеточных процессов путем взаимодействия с большим числом генов-мишеней. Эта микроРНК вовлечена в регуляцию дифференцировки и функционирования клеток нервной и иммунной систем, костной и жировой ткани и даже жизненного цикла ряда вирусов. Изменения экспрессии miR-375 обнаружены при канцерогенезе, воспалении, аутоиммунных и сердечно-сосудистых заболеваниях. С каждым годом появляются новые исследования, расширяющие наше представление о круге процессов, регулируемых этой микроРНК. Согласно последним данным, miR-375 может быть использована в качестве биомаркера и терапевтической мишени при некоторых заболеваниях. В этом обзоре обсуждается роль miR-375 в функционировании сердечно-сосудистой системы в норме и при патологических состояниях.

Ключевые слова: микроРНК, miR-375, сердечно-сосудистая система, сердечно-сосудистые заболевания, экспрессия генов

Список литературы

  1. Jonas S., Izaurralde E. (2015) Towards a molecular understanding of microRNA-mediated gene silencing. Nat. Rev. Genet. 16, 421–433.

  2. Kamanu T.K.K., Radovanovic A., Archer J.A.C., Bajic V.B. (2013) Exploration of miRNA families for hypotheses generation. Sci. Rep. 3, 2940.

  3. Kozomara A., Birgaoanu M., Griffiths-Jones S. (2019) miRBase: from microRNA sequences to function. Nucl. Acids Res. 47, D155–162.

  4. Bartel D.P. (2009) MicroRNAs: target recognition and regulatory functions. Cell. 136, 215–233.

  5. Lim L.P., Lau N.C., Weinstein E.G., Abdelhakim A., Yekta S., Rhoades M.W., Burge C.B., Bartel D.P. (2003) The microRNAs of Caenorhabditis elegans. Genes Dev. 17, 991–1008.

  6. Landgraf P., Rusu M., Sheridan R., Sewer A., Iovino N., Aravin A., Pfeffer S., Rice A., Kamphorst A.O., Landthaler M., Lin C., Socci N.D., Hermida L., Fulci V., Chiaretti S., Foà R., Schliwka J., Fuchs U., Novosel A., Müller R.U., Schermer B., Bissels U., Inman J., Phan Q., Chien M., Weir D.B., Choksi R., De Vita G., Frezzetti D., Trompeter H.I., Hornung V., Teng G., Hartmann G., Palkovits M., Di Lauro R., Wernet P., Macino G., Rogler C.E., Nagle J.W., Ju J., Papavasiliou F.N., Benzing T., Lichter P., Tam W., Brownstein M.J., Bosio A., Borkhardt A., Russo J.J., Sander C., Zavolan M., Tuschl T. (2007) A mammalian microRNA expression atlas based on small RNA library sequencing. Cell. 129, 1401–1414.

  7. Baulina N.M., Kulakova O.G., Favorova O.O. (2016) MicroRNAs: the role in autoimmune inflammation. Acta Naturae. 8, 21–33.

  8. Ivey K.N., Srivastava D. (2015) microRNAs as developmental regulators. Cold Spring Harb. Perspect. Biol. 7, a008144.

  9. Smith-Vikos T., Slack F.J. (2012) MicroRNAs and their roles in aging. J. Cell Sci. 125, 7–17.

  10. Hwang H.-W., Mendell J.T. (2006) MicroRNAs in cell proliferation, cell death, and tumorigenesis. Br. J. Cancer. 94, 776–780.

  11. Song L., Tuan R.S. (2006) MicroRNAs and cell differentiation in mammalian development. Birth Defects Res. Part C Embryo Today Rev. 78, 140–149.

  12. Subramanian S., Steer C.J. (2010) MicroRNAs as gatekeepers of apoptosis. J. Cell. Physiol. 223, 289–298.

  13. Momen-Heravi F., Bala S. (2018) miRNA regulation of innate immunity. J. Leukoc. Biol. 103, 1205–1217.

  14. Inui M., Martello G., Piccolo S. (2010) MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 252–263.

  15. Vienberg S., Geiger J., Madsen S., Dalgaard L.T. (2017) MicroRNAs in metabolism. Acta Physiol. Oxf. Engl. 219, 346–361.

  16. Peng Y., Croce C.M. (2016) The role of microRNAs in human cancer. Signal Transduct. Target. Ther. 1, 15004.

  17. Viswambharan V., Thanseem I., Vasu M.M., Poovathinal S.A., Anitha A. (2017) miRNAs as biomarkers of neurodegenerative disorders. Biomark. Med. 11, 151–167.

  18. Zhou S.S., Jin J.P., Wang J.Q., Zhang Z.G., Freedman J.H., Zheng Y., Cai L. (2018) miRNAS in cardiovascular diseases: potential biomarkers, therapeutic targets and challenges. Acta Pharmacol. Sin. 39, 1073–1084.

  19. Khudiakov A.A., Panshin D.D., Fomicheva Y.V., Knyazeva A.A., Simonova K.A., Lebedev D.S., Mik-haylov E.N., Kostareva A.A. (2021) Different expressions of pericardial fluid microRNAs in patients with arrhythmogenic right ventricular cardiomyopathy and ischemic heart disease undergoing ventricular tachycardia ablation. Front. Cardiovasc. Med. 8, 647812.

  20. Poy M.N. Eliasson L., Krutzfeldt J., Kuwajima S., Ma X., Macdonald P.E., Pfeffer S., Tuschl T., Rajewsky N., Rorsman P., Stoffel M. (2004) A pancreatic islet-specific microRNA regulates insulin secretion. Nature. 432, 226–230.

  21. Liu Y., Wang Q., Wen J., Wu Y., Man C. (2021) MiR-375: a novel multifunctional regulator. Life Sci. 275, 119323.

  22. Baroukh N.N., Van Obberghen E. (2009) Function of microRNA-375 and microRNA-124a in pancreas and brain. FEBS J. 276, 6509–6521.

  23. Yan J.-W., Lin J.-S., He X.-X. (2014) The emerging role of miR-375 in cancer: the emerging role of miR-375 in cancer. Int. J. Cancer. 135, 1011–1018.

  24. Avnit-Sagi T., Kantorovich L., Kredo-Russo S., Hornstein E., Walker M.D. (2009) The promoter of the pri-miR-375 gene directs expression selectively to the endocrine pancreas. PLoS One. 4, e5033.

  25. de Souza Rocha Simonini P., Breiling A., Gupta N., Malekpour M., Youns M., Omranipour R., Malekpour F., Volinia S., Croce C.M., Najmabadi H., Diederichs S., Sahin O., Mayer D., Lyko F., Hoheisel J.D., Riazalhosseini Y. (2010) Epigenetically deregulated microRNA-375 is involved in a positive feedback loop with estrogen receptor alpha in breast cancer cells. Cancer Res. 70, 9175–9184.

  26. Yan M., Liu Q., Jiang Y., Wang B., Ji Y., Liu H., Xie Y. (2020) Long noncoding RNA LNC_000898 alleviates cardiomyocyte apoptosis and promotes cardiac repair after myocardial infarction through modulating the miR-375/PDK1 axis. J. Cardiovasc. Pharmacol. 76, 77–85.

  27. Cao L., Kong L.P., Yu Z.B., Han S.P., Bai Y.F., Zhu J., Hu X., Zhu C., Zhu S., Guo X.R. (2012) microRNA expression profiling of the developing mouse heart. Int. J. Mol. Med. 30, 1095–1104.

  28. Wang L., Song G., Liu M., Chen B., Chen Y., Shen Y., Zhu J., Zhou X. (2016) MicroRNA-375 overexpression influences P19 cell proliferation, apoptosis and differentiation through the Notch signaling pathway. Int. J. Mol. Med. 37, 47–55.

  29. Zhuang S., Fu Y., Li J., Li M., Hu X., Zhu J., Tong M. (2020) MicroRNA-375 overexpression disrupts cardiac development of zebrafish (Danio rerio) by targeting Notch2. Protoplasma. 257, 1309–1318.

  30. Zhu S., Cao L., Zhu J., Kong L., Jin J., Qian L., Zhu C., Hu X., Li M., Guo X., Han S., Yu Z. (2013) Identification of maternal serum microRNAs as novel non-invasive biomarkers for prenatal detection of fetal congenital heart defects. Clin. Chim. Acta Int. J. Clin. Chem. 424, 66–72.

  31. Li Y., Li X., Wang L., Han N., Yin G. (2021) miR-375-3p contributes to hypoxia-induced apoptosis by targeting forkhead box P1 (FOXP1) and Bcl2 like protein 2 (Bcl2l2) in rat cardiomyocyte h9c2 cells. Biotechnol. Lett. 43, 353–367.

  32. Ali Sheikh M.S. (2020) Overexpression of miR-375 protects cardiomyocyte injury following hypoxic-reoxygenation injury. Oxid. Med. Cell. Longev. 2020, 7164069.

  33. Libby P. (2002) Inflammation in atherosclerosis. Nature. 420, 868–874.

  34. Qiu Y., Xu J., Yang L., Zhao G., Ding J., Chen Q., Zhang N., Yang R., Wang J., Li S., Zhang L. (2021) MiR-375 silencing attenuates pro-inflammatory macrophage response and foam cell formation by targeting KLF4. Exp. Cell Res. 400, 112507.

  35. D’Alessandra Y., Devanna P., Limana F., Straino S., Di Carlo A., Brambilla P.G., Rubino M., Carena M.C., Spazzafumo L., De Simone M., Micheli B., Biglioli P., Achilli F., Martelli F., Maggiolini S., Marenzi G., Pompilio G., Capogrossi M.C. (2010) Circulating microRNAs are new and sensitive biomarkers of myocardial infarction. Eur. Heart J. 31, 2765–2773.

  36. Baulina N., Osmak G., Kiselev I., Matveeva N., Kukava N., Shakhnovich R., Kulakova O., Favorova O. (2018) NGS-identified circulating miR-375 as a potential regulating component of myocardial infarction associated network. J. Mol. Cell. Cardiol. 121, 173–179.

  37. Valadi H., Ekström K., Bossios A., Sjöstrand M., Lee J.J., Lötvall J.O. (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654–659.

  38. Xu D., Tahara H. (2013) The role of exosomes and microRNAs in senescence and aging. Adv. Drug Deliv. Rev. 65, 368–375.

  39. Kay S.D., Carlsen A.L., Voss A., Burton M., Diederichsen A., Poulsen M.K., Heegaard N. (2019) Associations of circulating cell-free microRNA with vasculopathy and vascular events in systemic lupus erythematosus patients. Scand. J. Rheumatol. 48, 32–41.

  40. Gacoń J., Kabłak-Ziembicka A., Stępień E., Enguita F.J., Karch I., Derlaga B., Żmudka K., Przewłocki T. (2016) Decision-making microRNAs (miR-124, -133a/b, -34a and -134) in patients with occluded target vessel in acute coronary syndrome. Kardiol. Pol. 74, 280–288.

  41. Garikipati V.N.S., Verma S.K., Jolardarashi D., Cheng Z., Ibetti J., Cimini M., Tang Y., Khan M., Yue Y., Benedict C., Nickoloff E., Truongcao M.M., Gao E., Krishnamurthy P., Goukassian D.A., Koch W.J., Kishore R. (2017) Therapeutic inhibition of miR-375 attenuates post-myocardial infarction inflammatory response and left ventricular dysfunction via PDK-1-AKT signalling axis. Cardiovasc. Res. 113, 938–949.

  42. Garikipati V.N.S., Krishnamurthy P., Verma S.K., Khan M., Abramova T., Mackie A.R., Qin G., Benedict C., Nickoloff E., Johnson J., Gao E., Losordo D.W., Houser S.R., Koch W.J., Kishore R. (2015) Negative regulation of miR-375 by interleukin-10 enhances bone marrow-derived progenitor cell-mediated myocardial repair and function after myocardial infarction. Stem Cells Dayt. Ohio. 33, 3519–3529.

  43. Gacoń J., Badacz R., Stępień E., Karch I., Enguita F.J., Żmudka K., Przewłocki T., Kabłak-Ziembicka A. (2018) Diagnostic and prognostic micro-RNAs in ischaemic stroke due to carotid artery stenosis and in acute coronary syndrome: a four-year prospective study. Kardiol. Pol. 76, 362–369.

  44. Badacz R., Przewłocki T., Gacoń J., Stępień E., Enguita F.J., Karch I., Żmudka K., Kabłak-Ziembicka A. (2018) Circulating miRNA levels differ with respect to carotid plaque characteristics and symptom occurrence in patients with carotid artery stenosis and provide information on future cardiovascular events. Postepy W Kardiologii Interwencyjnej Adv. Interv. Cardiol. 14, 75–84.

  45. Charrier H., Cuvelliez M., Dubois-Deruy E., Mulder P., Richard V., Bauters C., Pinet F. (2019) Integrative system biology analyses identify seven microRNAs to predict heart failure. Non-Coding RNA. 5, E22.

  46. Watson C.J., Gupta S.K., O’Connell E., Thum S., Glezeva N., Fendrich J., Gallagher J., Ledwidge M., Grote-Levi L., McDonald K., Thum T. (2015) MicroRNA signatures differentiate preserved from reduced ejection fraction heart failure. Eur. J. Heart Fail. 17, 405–415.

  47. Zhang H., Tian Y., Liang D., Fu Q., Jia L., Wu D., Zhu X. (2020) The effects of inhibition of microRNA-375 in a mouse model of doxorubicin-induced cardiac toxicity. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 26, e920557.

  48. Zhelankin A.V., Vasiliev S.V., Stonogina D.A., Babalyan K.A., Sharova E.I., Doludin Y.V., Shchekochi-khin D.Y., Generozov E.V., Akselrod A.S. (2020) Elevated plasma levels of circulating extracellular miR-320a-3p in patients with paroxysmal atrial fibrillation. Int. J. Mol. Sci. 21, E3485.

  49. Hong X., Wang J., Li S., Zhao Z., Feng Z. (2021) MicroRNA-375-3p in endothelial progenitor cells-derived extracellular vesicles relieves myocardial injury in septic rats via BRD4-mediated PI3K/AKT signaling pathway. Int. Immunopharmacol. 96, 107740.

  50. Feng H., Wu J., Chen P., Wang J., Deng Y., Zhu G., Xian J., Huang L., Ouyang W. (2019) MicroRNA-375-3p inhibitor suppresses angiotensin II-induced cardiomyocyte hypertrophy by promoting lactate dehydrogenase B expression. J. Cell. Physiol. 234, 14198–14209.

  51. Ro W.-B., Kang M.-H., Song D.-W., Lee S.-H., Park H.-M. (2021) Expression profile of circulating MicroRNAs in dogs with cardiac hypertrophy: a pilot study. Front. Vet. Sci. 8, 652224.

  52. http://mirtarbase.cuhk.edu.cn/

  53. Ou J., Kou L., Liang L., Tang C. (2017) MiR-375 attenuates injury of cerebral ischemia/reperfusion via targetting Ctgf. Biosci. Rep. 37, BSR20171242.

  54. https://www.disgenet.org/

  55. https://www.proteinatlas.org/

  56. https://string-db.org/

  57. Osmak G., Kiselev I., Baulina N., Favorova O. (2020) From miRNA target gene network to miRNA function: miR-375 might regulate apoptosis and actin dynamics in the heart muscle via Rho-GTPases-dependent pathways. Int. J. Mol. Sci. 21, E9670.

  58. An Y., Liu Z., Ding H., Lv Q., Fan H., Hou S., Cai W., Liu S. (2020) MiR-375-3p regulates rat pulmonary microvascular endothelial cell activity by targeting Notch1 during hypoxia. J. Int. Med. Res. 48, 030006052092685.

  59. Ghanbari M., Franco O.H., de Looper H.W.J., Hofman A., Erkeland S.J., Dehghan A. (2015). Genetic variations in microRNA-binding sites affect microRNA-mediated regulation of several genes associated with cardio-metabolic phenotypes. Circ. Cardiovasc. Genet. 8, 473–486.

Дополнительные материалы отсутствуют.