MicroRNA and Pathogenesis of Enterovirus Infection
Abstract
:1. Introduction
2. Host Cellular miRNAs in Enterovirus Pathogenesis
2.1. Host miRNAs Participate in Antiviral Responses and Immune Escape in Enterovirus Infections
2.2. Host miRNAs Are Involved in Enterovirus Infection-Induced Apoptosis
2.3. Enterovirus Regulates Host Signaling Modulators Resulting in Pathogenesis
miRNA | Target | Enterovirus | Expression | Process | Model | Reference |
---|---|---|---|---|---|---|
miR-146a | IRAK1 | EV71 | Upregulation | Immune response | In vitro & In vivo | [58] |
miR-146a | TRAF6 | EV71 | Upregulation | Immune response | In vitro & In vivo | [58] |
miR-526a | CYLD | EV71 | Downregulation | Immune response | In vitro | [70] |
miR-155 | RelA | CVB3 & VMC a | Upregulation | Immune response | In vitro & In vivo | [72] |
miR-148a | RelA | CVB3 & VMC | Upregulation | Immune response | In vitro | [72] |
miR-548 | IFNλ1 | EV71 & HBV-infected subjects b | Downregulation | Immune response | In vitro | [73] |
miR-21 | PDCD4 | CVB3 | Downregulation | Apoptosis | In vitro & In vivo | [78] |
let-7b | CCND1 | EV71 | Upregulation | Cell cycle and Proliferation | In vitro | [79] |
miR-146a | SOS1 | EV71 | Upregulation | Apoptosis | In vitro | [55] |
miR-370 | GADD45b | EV71 | Downregulation | Apoptosis | In vitro | [55] |
miR-21 | YOD1 | CVB3 | Upregulation | Cell-cell interaction | In vitro | [54] |
miR-1 | GPJ1 | CVB3 | Upregulation | Cell-cell interaction | In vitro | [93] |
miR-21 | SPRY1 | VMC & DCM c | Ectopic | MAPK signaling | In vitro | [94] |
miR-126 | LRP | CVB3 | Upregulation | Wnt/β-catenin signaling | In vitro | [96] |
miR-126 | WRCH1 | CVB3 | Upregulation | Wnt/β-catenin signaling | In vitro | [96] |
miR-1246 | DLG3 | EV71 | Upregulation | Cell death signaling | In vitro | [95] |
miR-27a | EGFR | EV71 | Downregulation | EGFR signaling | In vitro | [97] |
miR-141 | eIF4E | EV71 | Upregulation | Protein synthesis | In vitro | [59] |
miR-296-5p | EV71 VP1 | EV71 | Upregulation | Viral replication | In vitro | [56] |
miR-296-5p | EV71 VP3 | EV71 | Upregulation | Viral replication | In vitro | [56] |
miR-23b | EV71 VP1 | EV71 | Downregulation | Viral replication | In vitro | [98] |
miR-342-5p | CVB3 2C | NA d | Ectopic | Viral replication | In vitro | [99] |
miR-373 | EV71 5′ UTR | NA | Ectopic | Viral replication | In vitro | [100] |
miR-542-5p | EV71 5′ UTR | NA | Ectopic | Viral replication | In vitro | [100] |
miR-10a* | CVB3 3D | NA | Ectopic | Viral replication | In vitro | [57] |
2.4. Host miRNAs Are Involved in Enterovirus Infection-Induced Protein Synthesis Shutdown
3. Host miRNAs Are Involved in the Enterovirus Life Cycle
3.1. Cellular miRNAs Target Vial Genome to Suppress Viral Replication
3.2. Cellular miRNAs Target the Viral Genome to Promote Viral Propagation
4. Conclusions and Perspective
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Badran, S.A.; Midgley, S.; Andersen, P.; Bottiger, B. Clinical and virological features of enterovirus 71 infections in Denmark, 2005 to 2008. Scand. J. Infect. Dis. 2011, 43, 642–648. [Google Scholar] [CrossRef] [PubMed]
- Bian, L.; Wang, Y.; Yao, X.; Mao, Q.; Xu, M.; Liang, Z. Coxsackievirus A6: A new emerging pathogen causing hand, foot and mouth disease outbreaks worldwide. Expert Rev. Anti-Infect. Ther. 2015, 13, 1061–1071. [Google Scholar] [CrossRef] [PubMed]
- Chua, K.B.; Kasri, A.R. Hand foot and mouth disease due to enterovirus 71 in Malaysia. Virol. Sin. 2011, 26, 221–228. [Google Scholar] [CrossRef] [PubMed]
- Gaunt, E.; Harvala, H.; Osterback, R.; Sreenu, V.B.; Thomson, E.; Waris, M.; Simmonds, P. Genetic characterization of human coxsackievirus A6 variants associated with atypical hand, foot and mouth disease: A potential role of recombination in emergence and pathogenicity. J. Gen. Virol. 2015, 96, 1067–1079. [Google Scholar] [CrossRef] [PubMed]
- Guan, H.; Wang, J.; Wang, C.; Yang, M.; Liu, L.; Yang, G.; Ma, X. Etiology of multiple Non-EV71 and non-CVA16 enteroviruses associated with hand, foot and mouth disease in Jinan, China, 2009—June 2013. PLoS ONE 2015, 10, e0142733. [Google Scholar] [CrossRef] [PubMed]
- Honkanen, H.; Oikarinen, S.; Pakkanen, O.; Ruokoranta, T.; Pulkki, M.M.; Laitinen, O.H.; Tauriainen, S.; Korpela, S.; Lappalainen, M.; Vuorinen, T.; et al. Human enterovirus 71 strains in the background population and in hospital patients in Finland. J. Clin. Virol. 2013, 56, 348–353. [Google Scholar] [CrossRef] [PubMed]
- Huang, X.; Wei, H.; Wu, S.; Du, Y.; Liu, L.; Su, J.; Xu, Y.; Wang, H.; Li, X.; Wang, Y.; et al. Epidemiological and etiological characteristics of hand, foot, and mouth disease in Henan, China, 2008–2013. Sci. Rep. 2015, 5. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.; Kang, B.; Hwang, S.; Lee, S.W.; Cheon, D.S.; Kim, K.; Jeong, Y.S.; Hyeon, J.Y. Clinical and enterovirus findings associated with acute flaccid paralysis in the Republic of Korea during the recent decade. J. Med. Virol. 2014, 86, 1584–1589. [Google Scholar] [CrossRef] [PubMed]
- Lee, T.C.; Guo, H.R.; Su, H.J.; Yang, Y.C.; Chang, H.L.; Chen, K.T. Diseases caused by enterovirus 71 infection. Pediatr. Infect. Dis. J. 2009, 28, 904–910. [Google Scholar] [CrossRef] [PubMed]
- Linsuwanon, P.; Puenpa, J.; Huang, S.W.; Wang, Y.F.; Mauleekoonphairoj, J.; Wang, J.R.; Poovorawan, Y. Epidemiology and seroepidemiology of human enterovirus 71 among Thai populations. J. Biomed. Sci. 2014, 21, 1110–1186. [Google Scholar] [CrossRef] [PubMed]
- Singh, S.; Poh, C.L.; Chow, V.T. Complete sequence analyses of enterovirus 71 strains from fatal and non-fatal cases of the hand, foot and mouth disease outbreak in Singapore (2000). Microbiol. Immunol. 2002, 46, 801–808. [Google Scholar] [CrossRef] [PubMed]
- Wu, J.S.; Zhao, N.; Pan, H.; Wang, C.M.; Wu, B.; Zhang, H.M.; He, H.X.; Liu, D.; Amer, S.; Liu, S.L. Patterns of polymorphism and divergence in the VP1 gene of enterovirus 71 circulating in the Asia-Pacific region between 1994 and 2013. J. Virol. Methods 2013, 193, 713–728. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.H.; Kuo, T.C.; Lin, Y.T.; Huang, S.W.; Liu, H.F.; Wang, J.; Chen, Y.M. Molecular epidemiology of enterovirus 71 infection in the central region of Taiwan from 2002 to 2012. PLoS ONE 2013, 8, e83711. [Google Scholar] [CrossRef] [PubMed]
- Fields, B.N.; Knipe, D.M.; Howley, P.M. Fields' Virology; Wolters Kluwer Health/Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007. [Google Scholar]
- Bible, J.M.; Pantelidis, P.; Chan, P.K.; Tong, C.Y. Genetic evolution of enterovirus 71: Epidemiological and pathological implications. Rev. Med. Virol. 2007, 17, 371–379. [Google Scholar] [CrossRef] [PubMed]
- Solomon, T.; Lewthwaite, P.; Perera, D.; Cardosa, M.J.; McMinn, P.; Ooi, M.H. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect. Dis. 2010, 10, 778–790. [Google Scholar] [CrossRef]
- Shimizu, H.; Utama, A.; Yoshii, K.; Yoshida, H.; Yoneyama, T.; Sinniah, M.; Yusof, M.A.; Okuno, Y.; Okabe, N.; Shih, S.R.; et al. Enterovirus 71 from fatal and nonfatal cases of hand, foot and mouth disease epidemics in Malaysia, Japan and Taiwan in 1997–1998. Jpn J. Infect. Dis. 1999, 52, 12–15. [Google Scholar] [PubMed]
- McMinn, P.; Stratov, I.; Nagarajan, L.; Davis, S. Neurological manifestations of enterovirus 71 infection in children during an outbreak of hand, foot, and mouth disease in Western Australia. Clin. Infect. Dis. 2001, 32, 236–242. [Google Scholar] [CrossRef] [PubMed]
- Ryu, W.S.; Kang, B.; Hong, J.; Hwang, S.; Kim, A.; Kim, J.; Cheon, D.S. Enterovirus 71 infection with central nervous system involvement, South Korea. Emerg. Infect. Dis. 2010, 16, 1764–1766. [Google Scholar] [CrossRef] [PubMed]
- Pons-Salort, M.; Parker, E.P.; Grassly, N.C. The epidemiology of non-polio enteroviruses: Recent advances and outstanding questions. Curr. Opin. Infect. Dis. 2015, 28, 479–487. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.Y.; Huang, L.M.; Gau, S.S.; Wu, Y.Y.; Hsia, S.H.; Fan, T.Y.; Lin, K.L.; Huang, Y.C.; Lu, C.Y.; Lin, T.Y. Neurodevelopment and cognition in children after enterovirus 71 infection. N. Engl. J. Med. 2007, 356, 1226–1234. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.F.; Chou, C.T.; Lei, H.Y.; Liu, C.C.; Wang, S.M.; Yan, J.J.; Su, I.J.; Wang, J.R.; Yeh, T.M.; Chen, S.H.; et al. A mouse-adapted enterovirus 71 strain causes neurological disease in mice after oral infection. J. Virol. 2004, 78, 7916–7924. [Google Scholar] [CrossRef] [PubMed]
- Chang, L.Y.; Huang, Y.C.; Lin, T.Y. Fulminant neurogenic pulmonary oedema with hand, foot, and mouth disease. Lancet 1998, 352, 36736–36738. [Google Scholar]
- Huang, C.C.; Liu, C.C.; Chang, Y.C.; Chen, C.Y.; Wang, S.T.; Yeh, T.F. Neurologic complications in children with enterovirus 71 infection. N. Engl. J. Med. 1999, 341, 936–942. [Google Scholar] [CrossRef] [PubMed]
- Lin, Y.W.; Wang, S.W.; Tung, Y.Y.; Chen, S.H. Enterovirus 71 infection of human dendritic cells. Exp. Biol. Med. 2009, 234, 1166–1173. [Google Scholar] [CrossRef] [PubMed]
- Whitton, J.L.; Cornell, C.T.; Feuer, R. Host and virus determinants of picornavirus pathogenesis and tropism. Nat. Rev. Microbiol. 2005, 3, 765–776. [Google Scholar] [CrossRef] [PubMed]
- Hammond, S.M. MicroRNAs as oncogenes. Curr. Opin. Genet. Dev. 2006, 16, 4–9. [Google Scholar] [CrossRef] [PubMed]
- Bartel, D.P. MicroRNAs: Target recognition and regulatory functions. Cell 2009, 136, 215–233. [Google Scholar] [CrossRef] [PubMed]
- Ha, M.; Kim, V.N. Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 2014, 15, 509–524. [Google Scholar] [CrossRef] [PubMed]
- Park, J.H.; Shin, C. MicroRNA-directed cleavage of targets: Mechanism and experimental approaches. BMB Rep. 2014, 47, 417–423. [Google Scholar] [CrossRef] [PubMed]
- Hammond, S.M. An overview of microRNAs. Adv. Drug Deliv. Rev. 2015, 87, 3–14. [Google Scholar] [CrossRef] [PubMed]
- Lin, S.; Gregory, R.I. MicroRNA biogenesis pathways in cancer. Nat. Rev. Cancer 2015, 15, 321–333. [Google Scholar] [CrossRef] [PubMed]
- Lewis, B.P.; Burge, C.B.; Bartel, D.P. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120, 15–20. [Google Scholar] [CrossRef] [PubMed]
- Cullen, B.R. Transcription and processing of human microRNA precursors. Mol. Cell 2004, 16, 861–865. [Google Scholar] [CrossRef] [PubMed]
- Borchert, G.M.; Lanier, W.; Davidson, B.L. RNA polymerase III transcribes human microRNAs. Nat. Struct. Mol. Biol. 2006, 13, 1097–1101. [Google Scholar] [CrossRef] [PubMed]
- Hutvagner, G.; McLachlan, J.; Pasquinelli, A.E.; Balint, E.; Tuschl, T.; Zamore, P.D. A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 2001, 293, 834–838. [Google Scholar] [CrossRef] [PubMed]
- Bernstein, E.; Caudy, A.A.; Hammond, S.M.; Hannon, G.J. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 2001, 409, 363–366. [Google Scholar] [CrossRef] [PubMed]
- Grishok, A.; Pasquinelli, A.E.; Conte, D.; Li, N.; Parrish, S.; Ha, I.; Baillie, D.L.; Fire, A.; Ruvkun, G.; Mello, C.C. Genes and mechanisms related to RNA interference regulate expression of the small temporal RNAs that control C. elegans developmental timing. Cell 2001, 106, 23–34. [Google Scholar] [CrossRef]
- Hammond, S.M.; Bernstein, E.; Beach, D.; Hannon, G.J. An RNA-directed nuclease mediates post-transcriptional gene silencing in Drosophila cells. Nature 2000, 404, 293–296. [Google Scholar] [PubMed]
- Wu, L.; Fan, J.; Belasco, J.G. MicroRNAs direct rapid deadenylation of mRNA. Proc. Natl. Acad. Sci. USA 2006, 103, 4034–4039. [Google Scholar] [CrossRef] [PubMed]
- Standart, N.; Jackson, R.J. MicroRNAs repress translation of m7Gppp-capped target mRNAs in vitro by inhibiting initiation and promoting deadenylation. Genes Dev. 2007, 21, 1975–1982. [Google Scholar] [CrossRef] [PubMed]
- Duursma, A.M.; Kedde, M.; Schrier, M.; le Sage, C.; Agami, R. miR-148 targets human DNMT3b protein coding region. RNA 2008, 14, 872–877. [Google Scholar] [CrossRef] [PubMed]
- Rigoutsos, I. New tricks for animal microRNAS: Targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res. 2009, 69, 3245–3248. [Google Scholar] [CrossRef] [PubMed]
- Lee, I.; Ajay, S.S.; Yook, J.I.; Kim, H.S.; Hong, S.H.; Kim, N.H.; Dhanasekaran, S.M.; Chinnaiyan, A.M.; Athey, B.D. New class of microRNA targets containing simultaneous 5′-UTR and 3′-UTR interaction sites. Genom. Res. 2009, 19, 1175–1183. [Google Scholar] [CrossRef] [PubMed]
- Grey, F.; Tirabassi, R.; Meyers, H.; Wu, G.; McWeeney, S.; Hook, L.; Nelson, J.A. A viral microRNA down-regulates multiple cell cycle genes through mRNA 5′AUTRs. PLoS Pathog. 2010, 6, e1000967. [Google Scholar] [CrossRef] [PubMed]
- Croce, C.M. Causes and consequences of microRNA dysregulation in cancer. Nat. Rev. Genet. 2009, 10, 704–714. [Google Scholar] [CrossRef] [PubMed]
- Umbach, J.L.; Cullen, B.R. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 2009, 23, 1151–1164. [Google Scholar] [CrossRef] [PubMed]
- Winter, J.; Jung, S.; Keller, S.; Gregory, R.I.; Diederichs, S. Many roads to maturity: MicroRNA biogenesis pathways and their regulation. Nat. Cell Biol. 2009, 11, 228–234. [Google Scholar] [CrossRef] [PubMed]
- Umbach, J.L.; Kramer, M.F.; Jurak, I.; Karnowski, H.W.; Coen, D.M.; Cullen, B.R. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 2008, 454, 780–783. [Google Scholar] [CrossRef] [PubMed]
- Pfeffer, S.; Zavolan, M.; Grasser, F.A.; Chien, M.; Russo, J.J.; Ju, J.; John, B.; Enright, A.J.; Marks, D.; Sander, C.; et al. Identification of virus-encoded microRNAs. Science 2004, 304, 734–736. [Google Scholar] [CrossRef] [PubMed]
- Gottwein, E.; Mukherjee, N.; Sachse, C.; Frenzel, C.; Majoros, W.H.; Chi, J.T.; Braich, R.; Manoharan, M.; Soutschek, J.; Ohler, U.; et al. A viral microRNA functions as an orthologue of cellular miR-155. Nature 2007, 450, 1096–1099. [Google Scholar] [CrossRef] [PubMed]
- Triboulet, R.; Mari, B.; Lin, Y.L.; Chable-Bessia, C.; Bennasser, Y.; Lebrigand, K.; Cardinaud, B.; Maurin, T.; Barbry, P.; Baillat, V.; et al. Suppression of microRNA-silencing pathway by HIV-1 during virus replication. Science 2007, 315, 1579–1582. [Google Scholar] [CrossRef] [PubMed]
- Jopling, C.L.; Yi, M.; Lancaster, A.M.; Lemon, S.M.; Sarnow, P. Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 2005, 309, 1577–1581. [Google Scholar] [CrossRef] [PubMed]
- Ye, X.; Zhang, H.M.; Qiu, Y.; Hanson, P.J.; Hemida, M.G.; Wei, W.; Hoodless, P.A.; Chu, F.; Yang, D. Coxsackievirus-induced miR-21 disrupts cardiomyocyte interactions via the downregulation of intercalated disk components. PLoS Pathog. 2014, 10, e1004070. [Google Scholar] [CrossRef] [PubMed]
- Chang, Y.L.; Ho, B.C.; Sher, S.; Yu, S.L.; Yang, P.C. miR-146a and miR-370 coordinate enterovirus 71-induced cell apoptosis through targeting SOS1 and GADD45β. Cell Microbiol. 2015, 17, 802–818. [Google Scholar] [CrossRef] [PubMed]
- Zheng, Z.; Ke, X.; Wang, M.; He, S.; Li, Q.; Zheng, C.; Zhang, Z.; Liu, Y.; Wang, H. Human microRNA hsa-miR-296-5p suppresses enterovirus 71 replication by targeting the viral genome. J. Virol. 2013, 87, 5645–5656. [Google Scholar] [CrossRef] [PubMed]
- Tong, L.; Lin, L.; Wu, S.; Guo, Z.; Wang, T.; Qin, Y.; Wang, R.; Zhong, X.; Wu, X.; Wang, Y.; et al. MiR-10a* up-regulates coxsackievirus B3 biosynthesis by targeting the 3D-coding sequence. Nucleic Acids Res. 2013, 41, 3760–3771. [Google Scholar] [CrossRef] [PubMed]
- Ho, B.C.; Yu, I.S.; Lu, L.F.; Rudensky, A.; Chen, H.Y.; Tsai, C.W.; Chang, Y.L.; Wu, C.T.; Chang, L.Y.; Shih, S.R.; et al. Inhibition of miR-146a prevents enterovirus-induced death by restoring the production of type I interferon. Nat. Commun. 2014, 5. [Google Scholar] [CrossRef] [PubMed]
- Ho, B.C.; Yu, S.L.; Chen, J.J.; Chang, S.Y.; Yan, B.S.; Hong, Q.S.; Singh, S.; Kao, C.L.; Chen, H.Y.; Su, K.Y.; et al. Enterovirus-induced miR-141 contributes to shutoff of host protein translation by targeting the translation initiation factor eIF4E. Cell Host Microbe 2011, 9, 58–69. [Google Scholar] [CrossRef] [PubMed]
- Klotman, M.E.; Chang, T.L. Defensins in innate antiviral immunity. Nat. Rev. Immunol. 2006, 6, 447–456. [Google Scholar] [CrossRef] [PubMed]
- Wilson, S.S.; Wiens, M.E.; Smith, J.G. Antiviral mechanisms of human defensins. J. Mol. Biol. 2013, 425, 4965–4980. [Google Scholar] [CrossRef] [PubMed]
- Kawai, T.; Akira, S. Innate immune recognition of viral infection. Nat. Immunol. 2006, 7, 131–137. [Google Scholar] [CrossRef] [PubMed]
- Thompson, M.R.; Kaminski, J.J.; Kurt-Jones, E.A.; Fitzgerald, K.A. Pattern recognition receptors and the innate immune response to viral infection. Viruses 2011, 3, 920–940. [Google Scholar] [CrossRef] [PubMed]
- Biron, C.A.; Nguyen, K.B.; Pien, G.C.; Cousens, L.P.; Salazar-Mather, T.P. Natural killer cells in antiviral defense: Function and regulation by innate cytokines. Annu. Rev. Immunol. 1999, 17, 189–220. [Google Scholar] [CrossRef] [PubMed]
- Le Bon, A.; Schiavoni, G.; D’Agostino, G.; Gresser, I.; Belardelli, F.; Tough, D.F. Type I interferons potently enhance humoral immunity and can promote isotype switching by stimulating dendritic cells in vivo. Immunity 2001, 14, 461–470. [Google Scholar] [CrossRef]
- Nguyen, K.B.; Watford, W.T.; Salomon, R.; Hofmann, S.R.; Pien, G.C.; Morinobu, A.; Gadina, M.; O’Shea, J.J.; Biron, C.A. Critical role for STAT4 activation by type 1 interferons in the interferon-γ response to viral infection. Science 2002, 297, 2063–2066. [Google Scholar] [CrossRef] [PubMed]
- Tough, D.F.; Sun, S.; Zhang, X.; Sprent, J. Stimulation of naive and memory T cells by cytokines. Immunol. Rev. 1999, 170, 39–47. [Google Scholar] [CrossRef] [PubMed]
- Ichimura, H.; Shimase, K.; Tamura, I.; Kaneto, E.; Kurimura, O.; Aramitsu, Y.; Kurimura, T. Neutralizing antibody and interferon-α in cerebrospinal fluids and sera of acute aseptic meningitis. J. Med. Virol. 1985, 15, 231–237. [Google Scholar] [CrossRef] [PubMed]
- Liu, M.L.; Lee, Y.P.; Wang, Y.F.; Lei, H.Y.; Liu, C.C.; Wang, S.M.; Su, I.J.; Wang, J.R.; Yeh, T.M.; Chen, S.H.; et al. Type I interferons protect mice against enterovirus 71 infection. J. Gen. Virol. 2005, 86Pt 12, 3263–3269. [Google Scholar] [CrossRef] [PubMed]
- Xu, C.; He, X.; Zheng, Z.; Zhang, Z.; Wei, C.; Guan, K.; Hou, L.; Zhang, B.; Zhu, L.; Cao, Y.; et al. Downregulation of microRNA miR-526a by enterovirus inhibits RIG-I-dependent innate immune response. J. Virol. 2014, 88, 11356–11368. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Q.; Xiao, Z.; He, F.; Zou, J.; Wu, S.; Liu, Z. MicroRNAs regulate the pathogenesis of CVB3-induced viral myocarditis. Intervirology 2013, 56, 104–113. [Google Scholar] [CrossRef] [PubMed]
- Bao, J.L.; Lin, L. MiR-155 and miR-148a reduce cardiac injury by inhibiting NF-κB pathway during acute viral myocarditis. Eur. Rev. Med. Pharmacol. Sci. 2014, 18, 2349–2356. [Google Scholar] [PubMed]
- Li, Y.; Xie, J.; Xu, X.; Wang, J.; Ao, F.; Wan, Y.; Zhu, Y. MicroRNA-548 down-regulates host antiviral response via direct targeting of IFN-lambda1. Protein Cell 2013, 4, 130–141. [Google Scholar] [CrossRef] [PubMed]
- Shauer, A.; Gotsman, I.; Keren, A.; Zwas, D.R.; Hellman, Y.; Durst, R.; Admon, D. Acute viral myocarditis: Current concepts in diagnosis and treatment. Isr. Med. Assoc. J. IMAJ 2013, 15, 180–185. [Google Scholar] [PubMed]
- Khong, W.X.; Foo, D.G.; Trasti, S.L.; Tan, E.L.; Alonso, S. Sustained high levels of interleukin-6 contribute to the pathogenesis of enterovirus 71 in a neonate mouse model. J. Virol. 2011, 85, 3067–3076. [Google Scholar] [CrossRef] [PubMed]
- Ch’ng, W.C.; Stanbridge, E.J.; Ong, K.C.; Wong, K.T.; Yusoff, K.; Shafee, N. Partial protection against enterovirus 71 (EV71) infection in a mouse model immunized with recombinant Newcastle disease virus capsids displaying the EV71 VP1 fragment. J. Med. Virol. 2011, 83, 1783–1791. [Google Scholar] [CrossRef] [PubMed]
- Aubert, M.; Jerome, K.R. Apoptosis prevention as a mechanism of immune evasion. Int. Rev. Immunol. 2003, 22, 361–371. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Yue, Y.; Dong, C.; Xiong, S. MiR-21 confers resistance against CVB3-induced myocarditis by inhibiting PDCD4-mediated apoptosis. Clin. Investig. Med. Med. Clin. Exp. 2013, 36, E103–E111. [Google Scholar]
- Du, X.; Wang, H.; Xu, F.; Huang, Y.; Liu, Z.; Liu, T. Enterovirus 71 induces apoptosis of SHSY5Y human neuroblastoma cells through stimulation of endogenous microRNA let-7b expression. Mol. Med. Rep. 2015, 12, 953–959. [Google Scholar] [PubMed]
- Cheng, Y.; Liu, X.; Zhang, S.; Lin, Y.; Yang, J.; Zhang, C. MicroRNA-21 protects against the H2O2-induced injury on cardiac myocytes via its target gene PDCD4. J. Mol. Cell Cardiol. 2009, 47, 5–14. [Google Scholar] [CrossRef] [PubMed]
- Lu, P.; Sun, H.; Zhang, L.; Hou, H.; Zhang, L.; Zhao, F.; Ge, C.; Yao, M.; Wang, T.; Li, J. Isocorydine targets the drug-resistant cellular side population through PDCD4-related apoptosis in hepatocellular carcinoma. Mol. Med. 2012, 18, 1136–1146. [Google Scholar] [CrossRef] [PubMed]
- Frankel, L.B.; Christoffersen, N.R.; Jacobsen, A.; Lindow, M.; Krogh, A.; Lund, A.H. Programmed cell death 4 (PDCD4) is an important functional target of the microRNA miR-21 in breast cancer cells. J. Biol. Chem. 2008, 283, 1026–1033. [Google Scholar] [CrossRef] [PubMed]
- Xiang, Z.; Li, L.; Lei, X.; Zhou, H.; Zhou, Z.; He, B.; Wang, J. Enterovirus 68 3C protease cleaves TRIF to attenuate antiviral responses mediated by Toll-like receptor 3. J. Virol. 2014, 88, 6650–6659. [Google Scholar] [CrossRef] [PubMed]
- Lei, X.; Han, N.; Xiao, X.; Jin, Q.; He, B.; Wang, J. Enterovirus 71 3C inhibits cytokine expression through cleavage of the TAK1/TAB1/TAB2/TAB3 complex. J. Virol. 2014, 88, 9830–9841. [Google Scholar] [CrossRef] [PubMed]
- Kuyumcu-Martinez, N.M.; van Eden, M.E.; Younan, P.; Lloyd, R.E. Cleavage of poly(A)-binding protein by poliovirus 3C protease inhibits host cell translation: A novel mechanism for host translation shutoff. Mol. Cell Biol. 2004, 24, 1779–1790. [Google Scholar] [CrossRef] [PubMed]
- Kuo, R.L.; Kung, S.H.; Hsu, Y.Y.; Liu, W.T. Infection with enterovirus 71 or expression of its 2A protease induces apoptotic cell death. J. Gen. Virol. 2002, 83, 1367–1376. [Google Scholar] [CrossRef] [PubMed]
- Graham, K.L.; Gustin, K.E.; Rivera, C.; Kuyumcu-Martinez, N.M.; Choe, S.S.; Lloyd, R.E.; Sarnow, P.; Utz, P.J. Proteolytic cleavage of the catalytic subunit of DNA-dependent protein kinase during poliovirus infection. J. Virol. 2004, 78, 6313–6321. [Google Scholar] [CrossRef] [PubMed]
- Feng, Q.; Langereis, M.A.; Lork, M.; Nguyen, M.; Hato, S.V.; Lanke, K.; Emdad, L.; Bhoopathi, P.; Fisher, P.B.; Lloyd, R.E.; et al. Enterovirus 2Apro targets MDA5 and MAVS in infected cells. J. Virol. 2014, 88, 3369–3378. [Google Scholar] [CrossRef] [PubMed]
- Barnabei, M.S.; Sjaastad, F.V.; Townsend, D.; Bedada, F.B.; Metzger, J.M. Severe dystrophic cardiomyopathy caused by the enteroviral protease 2A-mediated C-terminal dystrophin cleavage fragment. Sci. Transl. Med. 2015, 7. [Google Scholar] [CrossRef] [PubMed]
- Goldstaub, D.; Gradi, A.; Bercovitch, Z.; Grosmann, Z.; Nophar, Y.; Luria, S.; Sonenberg, N.; Kahana, C. Poliovirus 2A protease induces apoptotic cell death. Mol. Cell Biol. 2000, 20, 1271–1277. [Google Scholar] [CrossRef] [PubMed]
- Corsten, M.F.; Papageorgiou, A.; Verhesen, W.; Carai, P.; Lindow, M.; Obad, S.; Summer, G.; Coort, S.L.; Hazebroek, M.; van Leeuwen, R.; et al. MicroRNA profiling identifies microRNA-155 as an adverse mediator of cardiac injury and dysfunction during acute viral myocarditis. Circ. Res. 2012, 111, 415–425. [Google Scholar] [CrossRef] [PubMed]
- Lam, W.Y.; Cheung, A.C.; Tung, C.K.; Yeung, A.C.; Ngai, K.L.; Lui, V.W.; Chan, P.K.; Tsui, S.K. miR-466 is putative negative regulator of Coxsackie virus and Adenovirus Receptor. FEBS Lett. 2015, 589, 246–254. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.F.; Ding, Y.J.; Shen, Y.W.; Xue, A.M.; Xu, H.M.; Luo, C.L.; Li, B.X.; Liu, Y.L.; Zhao, Z.Q. MicroRNA-1 represses Cx43 expression in viral myocarditis. Mol. Cell Biochem. 2012, 362, 141–148. [Google Scholar] [CrossRef] [PubMed]
- Xu, H.F.; Ding, Y.J.; Zhang, Z.X.; Wang, Z.F.; Luo, C.L.; Li, B.X.; Shen, Y.W.; Tao, L.Y.; Zhao, Z.Q. MicroRNA21 regulation of the progression of viral myocarditis to dilated cardiomyopathy. Mol. Med. Rep. 2014, 10, 161–168. [Google Scholar] [PubMed]
- 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.; et al. 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 2014, 9, e95272. [Google Scholar] [CrossRef] [PubMed]
- Ye, X.; Hemida, M.G.; Qiu, Y.; Hanson, P.J.; Zhang, H.M.; Yang, D. MiR-126 promotes coxsackievirus replication by mediating cross-talk of ERK1/2 and Wnt/β-catenin signal pathways. Cell Mol. Life Sci. CMLS 2013, 70, 4631–444. [Google Scholar] [CrossRef] [PubMed]
- Zhang, L.; Chen, X.; Shi, Y.; Zhou, B.; Du, C.; Liu, Y.; Han, S.; Yin, J.; Peng, B.; He, X.; et al. miR-27a suppresses EV71 replication by directly targeting EGFR. Virus Genes 2014, 49, 373–382. [Google Scholar] [CrossRef] [PubMed]
- Wen, B.P.; Dai, H.J.; Yang, Y.H.; Zhuang, Y.; Sheng, R. MicroRNA-23b inhibits enterovirus 71 replication through downregulation of EV71 VPl protein. Intervirology 2013, 56, 195–200. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Qin, Y.; Tong, L.; Wu, S.; Wang, Q.; Jiao, Q.; Guo, Z.; Lin, L.; Wang, R.; Zhao, W.; et al. MiR-342-5p suppresses coxsackievirus B3 biosynthesis by targeting the 2C-coding region. Antivir. Res. 2012, 93, 270–279. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Tien, P. MiR373 and miR542-5p regulate the replication of enterovirus 71 in rhabdomyosarcoma cells. Chin. J. Biotechnol. 2014, 30, 943–953. (in Chinese). [Google Scholar]
- Piralla, A.; Mariani, B.; Stronati, M.; Marone, P.; Baldanti, F. Human enterovirus and parechovirus infections in newborns with sepsis-like illness and neurological disorders. Early Hum. Dev. 2014, 90 (Suppl. 1), S75–S77. [Google Scholar] [CrossRef]
- Britton, P.N.; Khandaker, G.; Booy, R.; Jones, C.A. The causes and consequences of childhood encephalitis in Asia. Infect. Disord. Drug Targets 2014, 14. [Google Scholar] [CrossRef]
- Tung, W.H.; Hsieh, H.L.; Lee, I.T.; Yang, C.M. Enterovirus 71 induces integrin β1/EGFR-Rac1-dependent oxidative stress in SK-N-SH cells: Role of HO-1/CO in viral replication. J. Cell Physiol. 2011, 226, 3316–3329. [Google Scholar] [CrossRef] [PubMed]
- Tung, W.H.; Hsieh, H.L.; Lee, I.T.; Yang, C.M. Enterovirus 71 modulates a COX-2/PGE2/cAMP-dependent viral replication in human neuroblastoma cells: Role of the c-Src/EGFR/p42/p44 MAPK/CREB signaling pathway. J. Cell Biochem. 2011, 112, 559–570. [Google Scholar] [CrossRef] [PubMed]
- Tung, W.H.; Hsieh, H.L.; Yang, C.M. Enterovirus 71 induces COX-2 expression via MAPKs, NF-κB, and AP-1 in SK-N-SH cells: Role of PGE(2) in viral replication. Cell Signal. 2010, 22, 234–246. [Google Scholar] [CrossRef] [PubMed]
- Belsham, G.J.; Sonenberg, N. Picornavirus RNA translation: Roles for cellular proteins. Trends Microbiol. 2000, 8, 330–335. [Google Scholar] [CrossRef]
- Schneider, R.J.; Mohr, I. Translation initiation and viral tricks. Trends Biochem. Sci. 2003, 28, 130–136. [Google Scholar] [CrossRef]
- Hemida, M.G.; Ye, X.; Zhang, H.M.; Hanson, P.J.; Liu, Z.; McManus, B.M.; Yang, D. MicroRNA-203 enhances coxsackievirus B3 replication through targeting zinc finger protein-148. Cell Mol. Life Sci. CMLS 2013, 70, 277–291. [Google Scholar] [CrossRef] [PubMed]
- Abraham, T.M.; Sarnow, P. RNA virus harnesses microRNAs to seize host translation control. Cell Host Microbe 2011, 9, 5–7. [Google Scholar] [CrossRef] [PubMed]
- Orom, U.A.; Nielsen, F.C.; Lund, A.H. MicroRNA-10a binds the 5′MUTR of ribosomal protein mRNAs and enhances their translation. Mol. Cell 2008, 30, 460–471. [Google Scholar] [CrossRef] [PubMed]
- Roberts, A.P.; Lewis, A.P.; Jopling, C.L. miR-122 activates hepatitis C virus translation by a specialized mechanism requiring particular RNA components. Nucleic Acids Res. 2011, 39, 7716–7729. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Liu, L.; Mo, Z.; Wang, X.; Xia, J.; Liang, Z.; Zhang, Y.; Li, Y.; Mao, Q.; Wang, J.; et al. An inactivated enterovirus 71 vaccine in healthy children. N. Engl. J. Med. 2014, 370, 829–837. [Google Scholar] [CrossRef] [PubMed]
- Zhu, F.; Xu, W.; Xia, J.; Liang, Z.; Liu, Y.; Zhang, X.; Tan, X.; Wang, L.; Mao, Q.; Wu, J.; et al. Efficacy, safety, and immunogenicity of an enterovirus 71 vaccine in China. N. Engl. J. Med. 2014, 370, 818–828. [Google Scholar] [CrossRef] [PubMed]
- Farooqi, A.A.; Fayyaz, S.; Shatynska-Mytsyk, I.; Javed, Z.; Jabeen, S.; Yaylim, I.; Gasparri, M.L.; Panici, P.B. Is miR-34a a well equipped swordsman to conquer temple of molecular oncology? Chem. Biol. Drug Des. 2015, 86. [Google Scholar] [CrossRef] [PubMed]
- Janssen, H.L.; Reesink, H.W.; Lawitz, E.J.; Zeuzem, S.; Rodriguez-Torres, M.; Patel, K.; van der Meer, A.J.; Patick, A.K.; Chen, A.; Zhou, Y.; et al. Treatment of HCV infection by targeting microRNA. N. Engl. J. Med. 2013, 368, 1685–1694. [Google Scholar] [CrossRef] [PubMed]
© 2016 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons by Attribution (CC-BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Ho, B.-C.; Yang, P.-C.; Yu, S.-L. MicroRNA and Pathogenesis of Enterovirus Infection. Viruses 2016, 8, 11. https://doi.org/10.3390/v8010011
Ho B-C, Yang P-C, Yu S-L. MicroRNA and Pathogenesis of Enterovirus Infection. Viruses. 2016; 8(1):11. https://doi.org/10.3390/v8010011
Chicago/Turabian StyleHo, Bing-Ching, Pan-Chyr Yang, and Sung-Liang Yu. 2016. "MicroRNA and Pathogenesis of Enterovirus Infection" Viruses 8, no. 1: 11. https://doi.org/10.3390/v8010011