Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
권호 표지
DOI QR코드

DOI QR Code

Expression Analyses of MicroRNAs in Hamster Lung Tissues Infected by SARS-CoV-2

  • Kim, Woo Ryung (Department of Integrated Biological Science, Pusan National University) ;
  • Park, Eun Gyung (Department of Integrated Biological Science, Pusan National University) ;
  • Kang, Kyung-Won (Division of Biotechnology, College of Environmental and Bioresources, Jeonbuk National University) ;
  • Lee, Sang-Myeong (Division of Biotechnology, College of Environmental and Bioresources, Jeonbuk National University) ;
  • Kim, Bumseok (Korea Zoonosis Research Institute and College of Veterinary Medicine, Jeonbuk National University) ;
  • Kim, Heui-Soo (Institute of Systems Biology, Pusan National University)
  • Received : 2020.08.28
  • Accepted : 2020.11.01
  • Published : 2020.11.30
Download PDF
⟨ Previous Next ⟩

Abstract

Coronavirus disease 2019 (COVID-19), caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), is an infectious disease with multiple severe symptoms, such as fever over 37.5℃, cough, dyspnea, and pneumonia. In our research, microRNAs (miRNAs) binding to the genome sequences of severe acute respiratory syndrome coronavirus (SARS-CoV), Middle East respiratory-related coronavirus (MERS-CoV), and SARS-CoV-2 were identified by bioinformatic tools. Five miRNAs (hsa-miR-15a-5p, hsa-miR-15b-5p, hsa-miR-195-5p, hsa-miR-16-5p, and hsa-miR-196a-1-3p) were found to commonly bind to SARS-CoV, MERS-CoV, and SARS-CoV-2. We also identified miRNAs that bind to receptor proteins, such as ACE2, ADAM17, and TMPRSS2, which are important for understanding the infection mechanism of SARS-CoV-2. The expression patterns of those miRNAs were examined in hamster lung samples infected by SARS-CoV-2. Five miRNAs (hsa-miR-15b-5p, hsa-miR-195-5p, hsa-miR-221-3p, hsa-miR-140-3p, and hsa-miR-422a) showed differential expression patterns in lung tissues before and after infection. Especially, hsa-miR-15b-5p and hsa-miR-195-5p showed a large difference in expression, indicating that they may potentially be diagnostic biomarkers for SARS-CoV-2 infection.

Keywords

References

  1. Abdel-Mohsen, M., Deng, X., Danesh, A., Liegler, T., Jacobs, E.S., Rauch, A., Ledergerber, B., Norris, P.J., Gunthard, H.F., Wong, J.K., et al. (2014). Role of microRNA modulation in the interferon-α/ribavirin suppression of HIV-1 in vivo. PLoS One 9, e109220. https://doi.org/10.1371/journal.pone.0109220
  2. Anderson, G. and Reiter, R.J. (2020). Melatonin: roles in influenza, Covid-19, and other viral infections. Rev. Med. Virol. 30, e2109. https://doi.org/10.1002/rmv.2109
  3. Aqeilan, R., Calin, G.A., and Croce, C.M. (2010). miR-15a and miR-16-1 in cancer: discovery, function and future perspectives. Cell Death Differ. 17, 215-220. https://doi.org/10.1038/cdd.2009.69
  4. Ashour, H.M., Elkhatib, W.F., Rahman, M., and Elshabrawy, H.A. (2020). Insights into the recent 2019 novel coronavirus (SARS-CoV-2) in light of past human coronavirus outbreaks. Pathogens 9, 186. https://doi.org/10.3390/pathogens9030186
  5. Bandi, N., Zbinden, S., Gugger, M., Arnold, M., Kocher, V., Hasan, L., Kappeler, A., Brunner, T., and Vassella, E. (2009). miR-15a and miR-16 are implicated in cell cycle regulation in a Rb-dependent manner and are frequently deleted or down-regulated in non-small cell lung cancer. Cancer Res. 69, 5553-5559. https://doi.org/10.1158/0008-5472.CAN-08-4277
  6. Bartel, D.P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. https://doi.org/10.1016/S0092-8674(04)00045-5
  7. Barwari, T., Joshi, A., and Mayr, M. (2016). MicroRNAs in cardiovascular disease. J. Am. Coll. Cardiol. 68, 2577-2584. https://doi.org/10.1016/j.jacc.2016.09.945
  8. Benvenuto, D., Giovanetti, M., Ciccozzi, A., Spoto, S., Angeletti, S., and Ciccozzi, M. (2020). The 2019-new coronavirus epidemic: evidence for virus evolution. J. Med. Virol. 92, 455-459. https://doi.org/10.1002/jmv.25688
  9. Cao, X., Zhang, G., Li, T., Zhou, C., Bai, L., Zhao, J., and Tursun, T. (2020). LINC00657 knockdown suppresses hepatocellular carcinoma progression by sponging miR-424 to regulate PD-L1 expression. Genes Genomics 42, 1361-1368. https://doi.org/10.1007/s13258-020-01001-y
  10. Casacuberta, E. and Gonzalez, J. (2013). The impact of transposable elements in environmental adaptation. Mol. Ecol. 22, 1503-1517. https://doi.org/10.1111/mec.12170
  11. Chakraborty, C., Doss, C.G.P., Bandyopadhyay, S., and Agoramoorthy, G. (2014). Influence of miRNA in insulin signaling pathway and insulin resistance: micro-molecules with a major role in type-2 diabetes. Wiley Interdiscip. Rev. RNA 5, 697-712. https://doi.org/10.1002/wrna.1240
  12. Chen, J. (2020). Pathogenicity and transmissibility of 2019-nCoV-a quick overview and comparison with other emerging viruses. Microbes Infect. 22, 69-71. https://doi.org/10.1016/j.micinf.2020.01.004
  13. Chen, L., Li, X., Chen, M., Feng, Y., and Xiong, C. (2020a). The ACE2 expression in human heart indicates new potential mechanism of heart injury among patients infected with SARS-CoV-2. Cardiovasc. Res. 116, 1097-1100. https://doi.org/10.1093/cvr/cvaa078
  14. Chen, Y., Chang, G., Chen, X., Li, Y., Li, H., Cheng, D., Tang, Y., and Sang, H. (2020b). IL-6-miR-210 suppresses regulatory T cell function and promotes atrial fibrosis by targeting Foxp3. Mol. Cells 43, 438-447. https://doi.org/10.14348/molcells.2019.2275
  15. Chen, Y., Guo, Y., Pan, Y., and Zhao, Z.J. (2020c). Structure analysis of the receptor binding of 2019-nCoV. Biochem. Biophys. Res. Commun. 525, 135-140. https://doi.org/10.1016/j.bbrc.2020.02.071
  16. Chen, Y., Liu, Q., and Guo, D. (2020d). Emerging coronaviruses: genome structure, replication, and pathogenesis. J. Med. Virol. 92, 418-423. https://doi.org/10.1002/jmv.25681
  17. Cheng, A.M., Byrom, M.W., Shelton, J., and Ford, L.P. (2005). Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res. 33, 1290-1297. https://doi.org/10.1093/nar/gki200
  18. Das, G., Mukherjee, N., and Ghosh, S. (2020). Neurological insights of COVID-19 pandemic. ACS Chem. Neurosci. 11, 1206-1209. https://doi.org/10.1021/acschemneuro.0c00201
  19. Delamater, P.L., Street, E.J., Leslie, T.F., Yang, Y.T., and Jacobsen, K.H. (2019). Complexity of the basic reproduction number (R0). Emerg. Infect. Dis. 25, 1-4. https://doi.org/10.3201/eid2501.171901
  20. Drosten, C., Gunther, S., Preiser, W., Van Der Werf, S., Brodt, H.R., Becker, S., Rabenau, H., Panning, M., Kolesnikova, L., and Fouchier, R.A. (2003). Identification of a novel coronavirus in patients with severe acute respiratory syndrome. N. Engl. J. Med. 348, 1967-1976. https://doi.org/10.1056/NEJMoa030747
  21. Epidemiology Working Group for NCIP Epidemic Response and Chinese Center for Disease Control and Prevention (2020). [The epidemiological characteristics of an outbreak of 2019 novel coronavirus diseases (COVID-19) in China]. Zhonghua Liu Xing Bing Xue Za Zhi 41, 145-151. Chinese.
  22. Finnerty, J.R., Wang, W.X., Hebert, S.S., Wilfred, B.R., Mao, G., and Nelson, P.T. (2010). The miR-15/107 group of microRNA genes: evolutionary biology, cellular functions, and roles in human diseases. J. Mol. Biol. 402, 491-509. https://doi.org/10.1016/j.jmb.2010.07.051
  23. Fulzele, S., Sahay, B., Yusufu, I., Lee, T.J., Sharma, A., Kolhe, R., and Isales, C.M. (2020). COVID-19 virulence in aged patients might be impacted by the host cellular MicroRNAs abundance/profile. Aging Dis. 11, 509. https://doi.org/10.14336/ad.2020.0428
  24. Gambardella, J., Sardu, C., Morelli, M.B., Messina, V., Castellanos, V., Marfella, R., Maggi, P., Paolisso, G., Wang, X., and Santulli, G. (2020). Exosomal microRNAs drive thrombosis in COVID-19. medRxiv.
  25. Gao, Y., Yan, L., Huang, Y., Liu, F., Zhao, Y., Cao, L., Wang, T., Sun, Q., Ming, Z., and Zhang, L. (2020). Structure of the RNA-dependent RNA polymerase from COVID-19 virus. Science 368, 779-782. https://doi.org/10.1126/science.abb7498
  26. Gross, S., Jahn, C., Cushman, S., Bar, C., and Thum, T. (2020). SARS-CoV-2 receptor ACE2-dependent implications on the cardiovascular system: from basic science to clinical implications. J. Mol. Cell. Cardiol. 144, 47-53. https://doi.org/10.1016/j.yjmcc.2020.04.031
  27. Guterres, A., de Azeredo Lima, C.H., Miranda, R.L., and Gadelha, M.R. (2020). What is the potential function of microRNAs as biomarkers and therapeutic targets in COVID-19? Infect. Genet. Evol. 85, 104417. https://doi.org/10.1016/j.meegid.2020.104417
  28. Haga, S., Yamamoto, N., Nakai-Murakami, C., Osawa, Y., Tokunaga, K., Sata, T., Yamamoto, N., Sasazuki, T., and Ishizaka, Y. (2008). Modulation of TNF-α-converting enzyme by the spike protein of SARS-CoV and ACE2 induces TNF-α production and facilitates viral entry. Proc. Natl. Acad. Sci. U. S. A. 105, 7809-7814. https://doi.org/10.1073/pnas.0711241105
  29. Heurich, A., Hofmann-Winkler, H., Gierer, S., Liepold, T., Jahn, O., and Pohlmann, S. (2014). TMPRSS2 and ADAM17 cleave ACE2 differentially and only proteolysis by TMPRSS2 augments entry driven by the severe acute respiratory syndrome coronavirus spike protein. J. Virol. 88, 1293-1307. https://doi.org/10.1128/JVI.02202-13
  30. Ho, B.C., Yang, P.C., and Yu, S.L. (2016). MicroRNA and pathogenesis of enterovirus infection. Viruses 8, 11. https://doi.org/10.3390/v8010011
  31. Hoffmann, M., Kleine-Weber, H., Schroeder, S., Kruger, N., Herrler, T., Erichsen, S., Schiergens, T.S., Herrler, G., Wu, N.H., Nitsche, A., et al. (2020). SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181, 271-280.e8. https://doi.org/10.1016/j.cell.2020.02.052
  32. Hooykaas, M.J., Kruse, E., Wiertz, E.J., and Lebbink, R.J. (2016). Comprehensive profiling of functional Epstein-Barr virus miRNA expression in human cell lines. BMC Genom. 17, 1-13. https://doi.org/10.1186/s12864-015-2294-6
  33. Imai, Y., Kuba, K., Ohto-Nakanishi, T., and Penninger, J.M. (2010). Angiotensin-converting enzyme 2 (ACE2) in disease pathogenesis. Circ. J. 74, 405-410. https://doi.org/10.1253/circj.CJ-10-0045
  34. Ivashchenko, A., Rakhmetullina, A., and Aisina, D. (2020). How miRNAs can protect humans from coronaviruses COVID-19, SARS-CoV, and MERS-CoV. Research Square https://doi.org/10.21203/rs.3.rs-16264/v1
  35. Jin, D. and Lee, H. (2016). Prioritizing cancer-related microRNAs by integrating microRNA and mRNA datasets. Sci. Rep. 6, 35350. https://doi.org/10.1038/srep35350
  36. Jopling, C.L., Yi, M., Lancaster, A.M., Lemon, S.M., and Sarnow, P. (2005). Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309, 1577-1581. https://doi.org/10.1126/science.1113329
  37. Lee, H.E., Huh, J.W., and Kim, H.S. (2020). Bioinformatics analysis of evolution and human disease related transposable element-derived microRNAs. Life 10, 95. https://doi.org/10.3390/life10060095
  38. Lee, H.E., Jo, A., Im, J., Cha, H.J., Kim, W.J., Kim, H.H., Kim, D.S., Kim, W., Yang, T.J., and Kim, H.S. (2019). Characterization of the long terminal repeat of the endogenous retrovirus-derived microRNAs in the olive flounder. Sci. Rep. 9, 1-10.
  39. Li, W., Moore, M.J., Vasilieva, N., Sui, J., Wong, S.K., Berne, M.A., Somasundaran, M., Sullivan, J.L., Luzuriaga, K., and Greenough, T.C. (2003). Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature 426, 450-454. https://doi.org/10.1038/nature02145
  40. Liang, H.X. and Li, Y.H. (2020). MiR-873, as a suppressor in cervical cancer, inhibits cells proliferation, invasion and migration via negatively regulating ULBP2. Genes Genomics 42, 371-382. https://doi.org/10.1007/s13258-019-00905-8
  41. Linsley, P.S., Schelter, J., Burchard, J., Kibukawa, M., Martin, M.M., Bartz, S.R., Johnson, J.M., Cummins, J.M., Raymond, C.K., and Dai, H. (2007). Transcripts targeted by the microRNA-16 family cooperatively regulate cell cycle progression. Mol. Cell. Biol. 27, 2240-2252. https://doi.org/10.1128/MCB.02005-06
  42. Liu, M., Wang, T., Zhou, Y., Zhao, Y., Zhang, Y., and Li, J. (2020). Potential role of ACE2 in coronavirus disease 2019 (COVID-19) prevention and management. J. Transl. Int. Med. 8, 9-19. https://doi.org/10.2478/jtim-2020-0003
  43. Liu, Q., Fu, H., Sun, F., Zhang, H., Tie, Y., Zhu, J., Xing, R., Sun, Z., and Zheng, X. (2008). miR-16 family induces cell cycle arrest by regulating multiple cell cycle genes. Nucleic Acids Res. 36, 5391-5404. https://doi.org/10.1093/nar/gkn522
  44. Lu, R., Zhao, X., Li, J., Niu, P., Yang, B., Wu, H., Wang, W., Song, H., Huang, B., Zhu, N., et al. (2020). Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet 395, 565-574. https://doi.org/10.1016/s0140-6736(20)30251-8
  45. Luo, H., Li, Y., Liu, B., Yang, Y., and Xu, Z.Q.D. (2017). MicroRNA-15b-5p targets ERK1 to regulate proliferation and apoptosis in rat PC12 cells. Biomed. Pharmacother. 92, 1023-1029. https://doi.org/10.1016/j.biopha.2017.05.140
  46. Malik, Y.S., Sircar, S., Bhat, S., Sharun, K., Dhama, K., Dadar, M., Tiwari, R., and Chaicumpa, W. (2020). Emerging novel coronavirus (2019-nCoV)-current scenario, evolutionary perspective based on genome analysis and recent developments. Vet. Q. 40, 68-76. https://doi.org/10.1080/01652176.2020.1727993
  47. McCue, A.D., Nuthikattu, S., Reeder, S.H., and Slotkin, R.K. (2012). Gene expression and stress response mediated by the epigenetic regulation of a transposable element small RNA. PLoS Genet. 8, e1002474. https://doi.org/10.1371/journal.pgen.1002474
  48. Mousavizadeh, L. and Ghasemi, S. (2020). Genotype and phenotype of COVID-19: their roles in pathogenesis. J. Microbiol. Immunol. Infect. https://doi.org/10.1016/j.jmii.2020.03.022
  49. Munster, V.J., Koopmans, M., van Doremalen, N., van Riel, D., and de Wit, E. (2020). A novel coronavirus emerging in China-key questions for impact assessment. N. Engl. J. Med. 382, 692-694. https://doi.org/10.1056/nejmp2000929
  50. Murakami, Y., Yasuda, T., Saigo, K., Urashima, T., Toyoda, H., Okanoue, T., and Shimotohno, K. (2006). Comprehensive analysis of microRNA expression patterns in hepatocellular carcinoma and non-tumorous tissues. Oncogene 25, 2537-2545. https://doi.org/10.1038/sj.onc.1209283
  51. Pedersen, S.F. and Ho, Y.C. (2020). SARS-CoV-2: a storm is raging. J. Clin. Invest. 130, 2202-2205. https://doi.org/10.1172/jci137647
  52. Piedade, D. and Azevedo-Pereira, J.M. (2016). The role of microRNAs in the pathogenesis of herpesvirus infection. Viruses 8, 156. https://doi.org/10.3390/v8060156
  53. Pineau, P., Volinia, S., McJunkin, K., Marchio, A., Battiston, C., Terris, B., Mazzaferro, V., Lowe, S.W., Croce, C.M., and Dejean, A. (2010). miR-221 overexpression contributes to liver tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 107, 264-269. https://doi.org/10.1073/pnas.0907904107
  54. Pinto, Y., Buchumenski, I., Levanon, E.Y., and Eisenberg, E. (2018). Human cancer tissues exhibit reduced A-to-I editing of miRNAs coupled with elevated editing of their targets. Nucleic Acids Res. 46, 71-82. https://doi.org/10.1093/nar/gkx1176
  55. Piriyapongsa, J., Marino-Ramirez, L., and Jordan, I.K. (2007). Origin and evolution of human microRNAs from transposable elements. Genetics 176, 1323-1337. https://doi.org/10.1534/genetics.107.072553
  56. Reddy, K.B. (2015). MicroRNA (miRNA) in cancer. Cancer Cell Int. 15, 1-6. https://doi.org/10.1186/s12935-015-0156-6
  57. Roberts, J.T., Cooper, E.A., Favreau, C.J., Howell, J.S., Lane, L.G., Mills, J.E., Newman, D.C., Perry, T.J., Russell, M.E., Wallace, B.M., et al. (2013). Continuing analysis of microRNA origins: formation from transposable element insertions and noncoding RNA mutations. Mob. Genet. Elements 3, e27755. https://doi.org/10.4161/mge.27755
  58. Scheel, T.K., Luna, J.M., Liniger, M., Nishiuchi, E., Rozen-Gagnon, K., Shlomai, A., Auray, G., Gerber, M., Fak, J., Keller, I., et al. (2016). A broad RNA virus survey reveals both miRNA dependence and functional sequestration. Cell Host Microbe 19, 409-423. https://doi.org/10.1016/j.chom.2016.02.007
  59. Singh, A.K., Rooge, S.B., Varshney, A., Vasudevan, M., Bhardwaj, A., Venugopal, S.K., Trehanpati, N., Kumar, M., Geffers, R., Kumar, V., et al. (2018). Global microRNA expression profiling in the liver biopsies of hepatitis B virus-infected patients suggests specific microRNA signatures for viral persistence and hepatocellular injury. Hepatology 67, 1695-1709. https://doi.org/10.1002/hep.29690
  60. Slotkin, R.K. and Martienssen, R. (2007). Transposable elements and the epigenetic regulation of the genome. Nat. Rev. Genet. 8, 272-285. https://doi.org/10.1038/nrg2072
  61. Smalheiser, N.R. and Torvik, V.I. (2005). Mammalian microRNAs derived from genomic repeats. Trends Genet. 21, 322-326. https://doi.org/10.1016/j.tig.2005.04.008
  62. Small, E.M., Frost, R.J., and Olson, E.N. (2010). MicroRNAs add a new dimension to cardiovascular disease. Circulation 121, 1022-1032. https://doi.org/10.1161/CIRCULATIONAHA.109.889048
  63. Song, L., Liu, H., Gao, S., Jiang, W., and Huang, W. (2010). Cellular microRNAs inhibit replication of the H1N1 influenza A virus in infected cells. J. Virol. 84, 8849-8860. https://doi.org/10.1128/JVI.00456-10
  64. Trobaugh, D.W. and Klimstra, W.B. (2017). MicroRNA regulation of RNA virus replication and pathogenesis. Trends Mol. Med. 23, 80-93. https://doi.org/10.1016/j.molmed.2016.11.003
  65. ul Qamar, M.T., Alqahtani, S.M., Alamri, M.A., and Chen, L.L. (2020). Structural basis of SARS-CoV-2 3CLpro and anti-COVID-19 drug discovery from medicinal plants. J. Pharm. Anal. 10, 313-319. https://doi.org/10.1016/j.jpha.2020.03.009
  66. Wan, Y., Shang, J., Graham, R., Baric, R.S., and Li, F. (2020). Receptor recognition by the novel coronavirus from Wuhan: an analysis based on decade-long structural studies of SARS coronavirus. J. Virol. 94, e00127-20.
  67. Wang, D., Hu, B., Hu, C., Zhu, F., Liu, X., Zhang, J., Wang, B., Xiang, H., Cheng, Z., Xiong, Y., et al. (2020). Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus-infected pneumonia in Wuhan, China. JAMA 323, 1061-1069. https://doi.org/10.1001/jama.2020.1585
  68. Wang, H., Yang, P., Liu, K., Guo, F., Zhang, Y., Zhang, G., and Jiang, C. (2008). SARS coronavirus entry into host cells through a novel clathrin-and caveolae-independent endocytic pathway. Cell Res. 18, 290-301. https://doi.org/10.1038/cr.2008.15
  69. Wang, L., Qin, Y., Tong, L., Wu, S., Wang, Q., Jiao, Q., Guo, Z., Lin, L., Wang, R., Zhao, W., et al. (2012). MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antiviral Res. 93, 270-279. https://doi.org/10.1016/j.antiviral.2011.12.004
  70. World Health Organization (2020a). Coronavirus disease (COVID-19) Situation Report - 80. Available from: https://www.who.int/docs/default-source/coronaviruse/situation-reports/20200409-sitrep-80-covid-19.pdf?sfvrsn=1b685d64_6 (accessed April 9, 2020)
  71. World Health Organization (2020b). Report of the WHO-China Joint Mission on Coronavirus Disease 2019 (COVID-19). Available from: https://www.who.int/docs/default-source/coronaviruse/who-china-joint-mission-on-covid-19-final-report.pdf (accessed March 9, 2020)
  72. Wortzel, I. and Seger, R. (2011). The ERK cascade: distinct functions within various subcellular organelles. Genes Cancer 2, 195-209. https://doi.org/10.1177/1947601911407328
  73. Wu, A., Peng, Y., Huang, B., Ding, X., Wang, X., Niu, P., Meng, J., Zhu, Z., Zhang, Z., Wang, J., et al. (2020a). Genome composition and divergence of the novel coronavirus (2019-nCoV) originating in China. Cell Host Microbe 27, 325-328. https://doi.org/10.1016/j.chom.2020.02.001
  74. Wu, J.T., Leung, K., and Leung, G.M. (2020b). Nowcasting and forecasting the potential domestic and international spread of the 2019-nCoV outbreak originating in Wuhan, China: a modelling study. Lancet 395, 689-697. https://doi.org/10.1016/s0140-6736(20)30260-9
  75. Xu, X., Yu, C., Qu, J., Zhang, L., Jiang, S., Huang, D., Chen, B., Zhang, Z., Guan, W., Ling, Z.J., et al. (2020). Imaging and clinical features of patients with 2019 novel coronavirus SARS-CoV-2. Eur. J. Nucl. Med. Mol. Imaging 47, 1275-1280. https://doi.org/10.1007/s00259-020-04735-9
  76. Yanamadala, S. and Ljungman, M. (2003). Potential role of MLH1 in the induction of p53 and apoptosis by blocking transcription on damaged DNA templates1 1 NIH grant CA82376, a grant from the Gastrointestinal Oncology Program Fund of the University of Michigan Comprehensive Cancer Center, and a grant from the Biomedical Research Council at the University of Michigan Medical School. Mol. Cancer Res. 1, 747-754.
  77. Yang, X., Yu, Y., Xu, J., Shu, H., Liu, H., Wu, Y., Zhang, L., Yu, Z., Fang, M., Yu, T., et al. (2020). Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study. Lancet Respir. Med. 8, 475-481. https://doi.org/10.1016/s2213-2600(20)30079-5
  78. Zaki, A.M., Van Boheemen, S., Bestebroer, T.M., Osterhaus, A.D., and Fouchier, R.A. (2012). Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia. N. Engl. J. Med. 367, 1814-1820. https://doi.org/10.1056/NEJMoa1211721
  79. Zeng, P., Wagoner, H.A., Pescovitz, O.H., and Steinmetz, R. (2005). RNA interference (RNAi) for extracellular signal-regulated kinase 1 (ERK1) alone is sufficient to suppress cell viability in ovarian cancer cells. Cancer Biol. Ther. 4, 961-967. https://doi.org/10.4161/cbt.4.9.1912
  80. Zhang, B., Pan, X., Cobb, G.P., and Anderson, T.A. (2007). microRNAs as oncogenes and tumor suppressors. Dev. Biol. 302, 1-12. https://doi.org/10.1016/j.ydbio.2006.08.028
  81. Zhang, H., Richards, B., Wilson, T., Lloyd, M., Cranston, A., Thorburn, A., Fishel, R., and Meuth, M. (1999). Apoptosis induced by overexpression of hMSH2 or hMLH1. Cancer Res. 59, 3021-3027.
  82. Zhao, W. (2013). Negative regulation of TBK1-mediated antiviral immunity. FEBS Lett. 587, 542-548. https://doi.org/10.1016/j.febslet.2013.01.052
  83. Zheng, Y.Y., Ma, Y.T., Zhang, J.Y., and Xie, X. (2020). COVID-19 and the cardiovascular system. Nat. Rev. Cardiol. 17, 259-260. https://doi.org/10.1038/s41569-020-0360-5
  84. Zhu, Z.R., He, Q., Wu, W.B., Chang, G.Q., Yao, C., Zhao, Y., Wang, M., and Wang, S.M. (2018). MiR-140-3p is involved in in-stent restenosis by targeting C-Myb and BCL-2 in peripheral artery disease. J. Atheroscler. Thromb. 25, 1168-1181. https://doi.org/10.5551/jat.44024

Cited by

  1. Human microRNA hsa-miR-15b-5p targets the RNA template component of the RNA-dependent RNA polymerase structure in severe acute respiratory syndrome coronavirus 2 vol.40, pp.8, 2021, https://doi.org/10.1080/15257770.2021.1950759
  2. miRNAs; a novel strategy for the treatment of COVID‐19 vol.45, pp.10, 2020, https://doi.org/10.1002/cbin.11653
  3. Natural and Experimental SARS-CoV-2 Infection in Domestic and Wild Animals vol.13, pp.10, 2020, https://doi.org/10.3390/v13101993
  4. Insights into the SARS-CoV-2-Mediated Alteration in the Stress Granule Protein Regulatory Networks in Humans vol.10, pp.11, 2021, https://doi.org/10.3390/pathogens10111459
  5. Role of microRNAs in COVID-19 with implications for therapeutics vol.144, 2020, https://doi.org/10.1016/j.biopha.2021.112247
  6. Drug repurposing for coronavirus (SARS-CoV-2) based on gene co-expression network analysis vol.11, pp.1, 2021, https://doi.org/10.1038/s41598-021-01410-3
  7. Expression of plasma IFN signaling-related miRNAs during acute SARS-CoV-2 infection and its association with RBD-IgG antibody response vol.18, pp.1, 2020, https://doi.org/10.1186/s12985-021-01717-7
  8. Role of miRNAs as biomarkers of COVID-19: a scoping review of the status and future directions for research in this field vol.15, pp.18, 2021, https://doi.org/10.2217/bmm-2021-0348