Various miRNAs compensate the role of miR-122 on HCV replication

English version

Autoři: Chikako Ono ^aff001; Takasuke Fukuhara ^aff001; Songling Li ^aff002; Jian Wang ^aff003; Asuka Sato ^aff001; Takuma Izumi ^aff001; Yuzy Fauzyah ^aff001; Takuya Yamamoto ^aff001; Yuhei Morioka ^aff001; Nikolay V. Dokholyan ^aff003; Daron M. Standley ^aff002; Yoshiharu Matsuura ^aff001
Působiště autorů: Department of Molecular Virology, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan ^aff001; Department of Genome Informatics, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan ^aff002; Department of Pharmacology, Penn State University College of Medicine, Hershey, Pennsylvania, United States of America ^aff003; Department of Biochemistry & Molecular Biology, Penn State University College of Medicine, Hershey, Pennsylvania, United States of America ^aff004
Vyšlo v časopise: Various miRNAs compensate the role of miR-122 on HCV replication. PLoS Pathog 16(6): e32767. doi:10.1371/journal.ppat.1008308
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.ppat.1008308

Souhrn

One of the determinants for tissue tropism of hepatitis C virus (HCV) is miR-122, a liver-specific microRNA. Recently, it has been reported that interaction of miR-122 to HCV RNA induces a conformational change of the 5’UTR internal ribosome entry site (IRES) structure to form stem-loop II structure (SLII) and hijack of translating 80S ribosome through the binding of SLIII to 40S subunit, which leads to efficient translation. On the other hand, low levels of HCV-RNA replication have also been detected in some non-hepatic cells; however, the details of extrahepatic replication remain unknown. These observations suggest the possibility that miRNAs other than miR-122 can support efficient replication of HCV-RNA in non-hepatic cells. Here, we identified a number of such miRNAs and show that they could be divided into two groups: those that bind HCV-RNA at two locations (miR-122 binding sites I and II), in a manner similar to miR-122 (miR-122-like), and those that target a single site that bridges sites I and II and masking both G28 and C29 in the 5’UTR (non-miR-122-like). Although the enhancing activity of these non-hepatic miRNAs were lower than those of miR-122, substantial expression was detected in various normal tissues. Furthermore, structural modeling indicated that both miR-122-like and non-miR-122-like miRNAs not only can facilitate the formation of an HCV IRES SLII but also can stabilize IRES 3D structure in order to facilitate binding of SLIII to the ribosome. Together, these results suggest that HCV facilitates miR-122-independent replication in non-hepatic cells through recruitment of miRNAs other than miR-122. And our findings can provide a more detailed mechanism of miR-122-dependent enhancement of HCV-RNA translation by focusing on IRES tertiary structure.

Klíčová slova:

Hepatitis C virus – Internal ribosome entry site – Luciferase – MicroRNAs – Protein translation – RNA structure – Sequence motif analysis – Viral replication

Zdroje

1. WHO | Global hepatitis report, 2017. WHO. 2017. http://entity/hepatitis/publications/global-hepatitis-report2017/en/index.html.

2. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science. 2005;309(5740):1577–81. doi: 10.1126/science.1113329 16141076.

3. Galossi A, Guarisco R, Bellis L, Puoti C. Extrahepatic manifestations of chronic HCV infection. J Gastrointestin Liver Dis. 2007;16(1):65–73. 17410291.

4. Castillo I, Rodríguez-Iñigo E, Bartolomé J, de Lucas S, Ortíz-Movilla N, López-Alcorocho JM, et al. Hepatitis C virus replicates in peripheral blood mononuclear cells of patients with occult hepatitis C virus infection. Gut. 2005;54(5):682–5. doi: 10.1136/gut.2004.057281 15831916; PubMed Central PMCID: PMC1774478.

5. Wilkinson J, Radkowski M, Laskus T. Hepatitis C virus neuroinvasion: identification of infected cells. J Virol. 2009;83(3):1312–9. doi: 10.1128/JVI.01890-08 19019968; PubMed Central PMCID: PMC2620915.

6. Maciocia N, O'Brien A, Ardeshna K. Remission of Follicular Lymphoma after Treatment for Hepatitis C Virus Infection. N Engl J Med. 2016;375(17):1699–701. doi: 10.1056/NEJMc1513288 27783921.

7. Hsu SH, Wang B, Kota J, Yu J, Costinean S, Kutay H, et al. Essential metabolic, anti-inflammatory, and anti-tumorigenic functions of miR-122 in liver. J Clin Invest. 2012;122(8):2871–83. doi: 10.1172/JCI63539 22820288; PubMed Central PMCID: PMC3408748.

8. Tsai WC, Hsu SD, Hsu CS, Lai TC, Chen SJ, Shen R, et al. MicroRNA-122 plays a critical role in liver homeostasis and hepatocarcinogenesis. J Clin Invest. 2012;122(8):2884–97. doi: 10.1172/JCI63455 22820290; PubMed Central PMCID: PMC3408747.

9. Shimakami T, Yamane D, Jangra RK, Kempf BJ, Spaniel C, Barton DJ, et al. Stabilization of hepatitis C virus RNA by an Ago2-miR-122 complex. Proc Natl Acad Sci U S A. 2012;109(3):941–6. doi: 10.1073/pnas.1112263109 22215596; PubMed Central PMCID: PMC3271899.

10. Henke JI, Goergen D, Zheng J, Song Y, Schüttler CG, Fehr C, et al. microRNA-122 stimulates translation of hepatitis C virus RNA. EMBO J. 2008;27(24):3300–10. doi: 10.1038/emboj.2008.244 19020517; PubMed Central PMCID: PMC2586803.

11. Roberts AP, Lewis AP, Jopling CL. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res. 2011;39(17):7716–29. doi: 10.1093/nar/gkr426 21653556; PubMed Central PMCID: PMC3177192.

12. Masaki T, Arend KC, Li Y, Yamane D, McGivern DR, Kato T, et al. miR-122 Stimulates Hepatitis C Virus RNA Synthesis by Altering the Balance of Viral RNAs Engaged in Replication versus Translation. Cell Host Microbe. 2015;17(2):217–28. doi: 10.1016/j.chom.2014.12.014 25662750; PubMed Central PMCID: PMC4326553.

13. Jopling CL, Schütz S, Sarnow P. Position-dependent function for a tandem microRNA miR-122-binding site located in the hepatitis C virus RNA genome. Cell Host Microbe. 2008;4(1):77–85. doi: 10.1016/j.chom.2008.05.013 18621012; PubMed Central PMCID: PMC3519368.

14. Machlin ES, Sarnow P, Sagan SM. Masking the 5' terminal nucleotides of the hepatitis C virus genome by an unconventional microRNA-target RNA complex. Proc Natl Acad Sci U S A. 2011;108(8):3193–8. doi: 10.1073/pnas.1012464108 21220300; PubMed Central PMCID: PMC3044371.

15. Jopling CL. Regulation of hepatitis C virus by microRNA-122. Biochem Soc Trans. 2008;36(Pt 6):1220–3. doi: 10.1042/BST0361220 19021529.

16. Li Y, Masaki T, Yamane D, McGivern DR, Lemon SM. Competing and noncompeting activities of miR-122 and the 5' exonuclease Xrn1 in regulation of hepatitis C virus replication. Proc Natl Acad Sci U S A. 2013;110(5):1881–6. doi: 10.1073/pnas.1213515110 23248316; PubMed Central PMCID: PMC3562843.

17. Sedano CD, Sarnow P. Hepatitis C virus subverts liver-specific miR-122 to protect the viral genome from exoribonuclease Xrn2. Cell Host Microbe. 2014;16(2):257–64. doi: 10.1016/j.chom.2014.07.006 25121753; PubMed Central PMCID: PMC4227615.

18. Li Y, Yamane D, Lemon SM. Dissecting the roles of the 5' exoribonucleases Xrn1 and Xrn2 in restricting hepatitis C virus replication. J Virol. 2015;89(9):4857–65. doi: 10.1128/JVI.03692-14 25673723; PubMed Central PMCID: PMC4403451.

19. Luna JM, Scheel TK, Danino T, Shaw KS, Mele A, Fak JJ, et al. Hepatitis C Virus RNA Functionally Sequesters miR-122. Cell. 2015;160(6):1099–110. doi: 10.1016/j.cell.2015.02.025 25768906.

20. Schult P, Roth H, Adams RL, Mas C, Imbert L, Orlik C, et al. microRNA-122 amplifies hepatitis C virus translation by shaping the structure of the internal ribosomal entry site. Nat Commun. 2018;9(1):2613. Epub 2018/07/06. doi: 10.1038/s41467-018-05053-3 29973597; PubMed Central PMCID: PMC6031695.

21. Amador-Canizares Y, Panigrahi M, Huys A, Kunden RD, Adams HM, Schinold MJ, et al. miR-122, small RNA annealing and sequence mutations alter the predicted structure of the Hepatitis C virus 5' UTR RNA to stabilize and promote viral RNA accumulation. Nucleic Acids Res. 2018. Epub 2018/07/28. doi: 10.1093/nar/gky662 30053137.

22. Yokoyama T, Machida K, Iwasaki W, Shigeta T, Nishimoto M, Takahashi M, et al. HCV IRES Captures an Actively Translating 80S Ribosome. Mol Cell. 2019;74(6):1205–14.e8. Epub 2019/05/09. doi: 10.1016/j.molcel.2019.04.022 31080011.

23. Ono C, Fukuhara T, Motooka D, Nakamura S, Okuzaki D, Yamamoto S, et al. Characterization of miR-122-independent propagation of HCV. PLoS Pathog. 2017;13(5):e1006374. Epub 2017/05/12. doi: 10.1371/journal.ppat.1006374 28494029; PubMed Central PMCID: PMC5441651.

24. Israelow B, Mullokandov G, Agudo J, Sourisseau M, Bashir A, Maldonado AY, et al. Hepatitis C virus genetics affects miR-122 requirements and response to miR-122 inhibitors. Nat Commun. 2014;5:5408. doi: 10.1038/ncomms6408 25403145; PubMed Central PMCID: PMC4236719.

25. Zhang W, Thevapriya S, Kim PJ, Yu WP, Je HS, Tan EK, et al. Amyloid precursor protein regulates neurogenesis by antagonizing miR-574-5p in the developing cerebral cortex. Nat Commun. 2014;5:3330. Epub 2014/03/04. doi: 10.1038/ncomms4330 24584353.

26. Ludwig N, Leidinger P, Becker K, Backes C, Fehlmann T, Pallasch C, et al. Distribution of miRNA expression across human tissues. Nucleic Acids Res. 2016;44(8):3865–77. Epub 2016/02/28. doi: 10.1093/nar/gkw116 26921406; PubMed Central PMCID: PMC4856985.

27. Fukuhara T, Kambara H, Shiokawa M, Ono C, Katoh H, Morita E, et al. Expression of microRNA miR-122 facilitates an efficient replication in nonhepatic cells upon infection with hepatitis C virus. J Virol. 2012;86(15):7918–33. doi: 10.1128/JVI.00567-12 22593164; PubMed Central PMCID: PMC3421686.

28. Chahal J, Gebert LFR, Gan HH, Camacho E, Gunsalus KC, MacRae IJ, et al. miR-122 and Ago interactions with the HCV genome alter the structure of the viral 5' terminus. Nucleic Acids Res. 2019;47(10):5307–24. doi: 10.1093/nar/gkz194 30941417; PubMed Central PMCID: PMC6547439.

29. Bogerd HP, Kennedy EM, Whisnant AW, Cullen BR. Induced Packaging of Cellular MicroRNAs into HIV-1 Virions Can Inhibit Infectivity. MBio. 2017;8(1). Epub 2017/01/18. doi: 10.1128/mBio.02125-16 28096489; PubMed Central PMCID: PMC5241401.

30. Huang J, Wang F, Argyris E, Chen K, Liang Z, Tian H, et al. Cellular microRNAs contribute to HIV-1 latency in resting primary CD4+ T lymphocytes. Nat Med. 2007;13(10):1241–7. Epub 2007/10/02. doi: 10.1038/nm1639 17906637.

31. Shi G, Ando T, Suzuki R, Matsuda M, Nakashima K, Ito M, et al. Involvement of the 3' Untranslated Region in Encapsidation of the Hepatitis C Virus. PLoS Pathog. 2016;12(2):e1005441. Epub 2016/02/13. doi: 10.1371/journal.ppat.1005441 26867128; PubMed Central PMCID: PMC4750987.

32. Friebe P, Bartenschlager R. Role of RNA structures in genome terminal sequences of the hepatitis C virus for replication and assembly. J Virol. 2009;83(22):11989–95. Epub 2009/09/11. doi: 10.1128/JVI.01508-09 19740989; PubMed Central PMCID: PMC2772684.

33. Preciado MV, Valva P, Escobar-Gutierrez A, Rahal P, Ruiz-Tovar K, Yamasaki L, et al. Hepatitis C virus molecular evolution: transmission, disease progression and antiviral therapy. World J Gastroenterol. 2014;20(43):15992–6013. doi: 10.3748/wjg.v20.i43.15992 25473152; PubMed Central PMCID: PMC4239486.

34. Lavanchy D. Evolving epidemiology of hepatitis C virus. Clin Microbiol Infect. 2011;17(2):107–15. doi: 10.1111/j.1469-0691.2010.03432.x 21091831.

35. Zhou R, Zhou X, Yin Z, Guo J, Hu T, Jiang S, et al. MicroRNA-574-5p promotes metastasis of non-small cell lung cancer by targeting PTPRU. Sci Rep. 2016;6:35714. Epub 2016/10/21. doi: 10.1038/srep35714 27761023; PubMed Central PMCID: PMC5071770.

36. Zhou R, Zhou X, Yin Z, Guo J, Hu T, Jiang S, et al. Tumor invasion and metastasis regulated by microRNA-184 and microRNA-574-5p in small-cell lung cancer. Oncotarget. 2015;6(42):44609–22. Epub 2015/11/21. doi: 10.18632/oncotarget.6338 26587830; PubMed Central PMCID: PMC4792579.

37. Li Q, Li X, Guo Z, Xu F, Xia J, Liu Z, et al. MicroRNA-574-5p was pivotal for TLR9 signaling enhanced tumor progression via down-regulating checkpoint suppressor 1 in human lung cancer. PLoS One. 2012;7(11):e48278. Epub 2012/11/08. doi: 10.1371/journal.pone.0048278 23133627; PubMed Central PMCID: PMC3487732.

38. Zhang S, Zhang Y, Cheng Q, Ma Z, Gong G, Deng Z, et al. Silencing protein kinase C zeta by microRNA-25-5p activates AMPK signaling and inhibits colorectal cancer cell proliferation. Oncotarget. 2017;8(39):65329–38. Epub 2017/10/17. doi: 10.18632/oncotarget.18649 29029434; PubMed Central PMCID: PMC5630334.

39. Zhang BB, Zhou G, Li C. AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab. 2009;9(5):407–16. Epub 2009/05/07. doi: 10.1016/j.cmet.2009.03.012 19416711.

40. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, Zhao Z, et al. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med. 2005;11(7):791–6. doi: 10.1038/nm1268 15951748; PubMed Central PMCID: PMC2918402.

41. Das MK, Andreassen R, Haugen TB, Furu K. Identification of Endogenous Controls for Use in miRNA Quantification in Human Cancer Cell Lines. Cancer Genomics Proteomics. 2016;13(1):63–8. Epub 2015/12/29. 26708600.

42. Sharma S, Ding F, Dokholyan NV. iFoldRNA: three-dimensional RNA structure prediction and folding. Bioinformatics. 2008;24(17):1951–2. Epub 2008/06/25. doi: 10.1093/bioinformatics/btn328 18579566; PubMed Central PMCID: PMC2559968.

43. Krokhotin A, Houlihan K, Dokholyan NV. iFoldRNA v2: folding RNA with constraints. Bioinformatics. 2015;31(17):2891–3. Epub 2015/04/24. doi: 10.1093/bioinformatics/btv221 25910700; PubMed Central PMCID: PMC4547609.

44. Ding F, Tsao D, Nie H, Dokholyan NV. Ab initio folding of proteins with all-atom discrete molecular dynamics. Structure. 2008;16(7):1010–8. doi: 10.1016/j.str.2008.03.013 18611374; PubMed Central PMCID: PMC2533517.

45. Proctor E, Ding F, Dokholyan N. Discrete molecular dynamics. Wiley Interdisciplinary Reviews-Computational Molecular Science. 2011;1(1):80–92. doi: 10.1002/wcms.4 WOS:000295991000008.

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