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Published in: European Journal of Medical Research 1/2018

Open Access 01-12-2018 | Review

miRNAs regulate immune response and signaling during hepatitis C virus infection

Authors: Huange Zhu, Yan Geng, Qian He, Miaoxian Li

Published in: European Journal of Medical Research | Issue 1/2018

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Abstract

Hepatitis C is one of the most common types of viral hepatitis that impair human health. At present, there is still no effective specific therapy for hepatitis C virus infection. As host immunity is an important mechanism to defend against or clear infections, the interactions between the virus and the host immune response are crucial to the progress of the disease. Of note, hepatitis C virus infection has been reported to regulate cellular miRNAs, which play significant roles in many processes, including infection and immunity. In this review, we describe how miRNAs regulate the host immune response to hepatitis C virus via complex signaling pathways.
Literature
1.
go back to reference Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol. 2005;5:215–29.CrossRefPubMed Rehermann B, Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat Rev Immunol. 2005;5:215–29.CrossRefPubMed
4.
go back to reference Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, Bzowej NH, et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med. 2011;364:2405–16.CrossRefPubMed Jacobson IM, McHutchison JG, Dusheiko G, Di Bisceglie AM, Reddy KR, Bzowej NH, et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med. 2011;364:2405–16.CrossRefPubMed
5.
8.
go back to reference Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.CrossRefPubMed Lee RC, Feinbaum RL, Ambros V. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell. 1993;75:843–54.CrossRefPubMed
9.
go back to reference Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific microRNAs. Dev Cell. 2003;5:351–8.CrossRefPubMed Houbaviy HB, Murray MF, Sharp PA. Embryonic stem cell-specific microRNAs. Dev Cell. 2003;5:351–8.CrossRefPubMed
10.
11.
12.
go back to reference Verma P, Pandey RK, Prajapati P, Prajapati VK. Circulating microRNAs: potential and emerging biomarkers for diagnosis of human infectious diseases. Front Microbiol. 2016;7:1274.PubMedPubMedCentral Verma P, Pandey RK, Prajapati P, Prajapati VK. Circulating microRNAs: potential and emerging biomarkers for diagnosis of human infectious diseases. Front Microbiol. 2016;7:1274.PubMedPubMedCentral
13.
go back to reference Ura S, Honda M, Yamashita T, Ueda T, Takatori H, Nishino R, et al. Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology. 2009;49:1098–112.CrossRefPubMed Ura S, Honda M, Yamashita T, Ueda T, Takatori H, Nishino R, et al. Differential microRNA expression between hepatitis B and hepatitis C leading disease progression to hepatocellular carcinoma. Hepatology. 2009;49:1098–112.CrossRefPubMed
14.
go back to reference Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science. 2005;309:1577–81.CrossRefPubMed Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science. 2005;309:1577–81.CrossRefPubMed
16.
go back to reference Zhang C, Huys A, Thibault PA, Wilson JA. Requirements for human Dicer and TRBP in microRNA-122 regulation of HCV translation and RNA abundance. Virology. 2012;433:479–88.CrossRefPubMed Zhang C, Huys A, Thibault PA, Wilson JA. Requirements for human Dicer and TRBP in microRNA-122 regulation of HCV translation and RNA abundance. Virology. 2012;433:479–88.CrossRefPubMed
17.
go back to reference Shan Y, Zheng J, Lambrecht RW, Bonkovsky HL. Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes. Gastroenterology. 2007;133:1166–74.CrossRefPubMedPubMedCentral Shan Y, Zheng J, Lambrecht RW, Bonkovsky HL. Reciprocal effects of micro-RNA-122 on expression of heme oxygenase-1 and hepatitis C virus genes in human hepatocytes. Gastroenterology. 2007;133:1166–74.CrossRefPubMedPubMedCentral
18.
go back to reference Marquez RT, Bandyopadhyay S, Wendlandt EB, Keck K, Hoffer BA, Icardi MS, et al. Correlation between microRNA expression levels and clinical parameters associated with chronic hepatitis C viral infection in humans. Lab Invest. 2010;90:1727–36.CrossRefPubMed Marquez RT, Bandyopadhyay S, Wendlandt EB, Keck K, Hoffer BA, Icardi MS, et al. Correlation between microRNA expression levels and clinical parameters associated with chronic hepatitis C viral infection in humans. Lab Invest. 2010;90:1727–36.CrossRefPubMed
19.
go back to reference Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. Decreased levels of microRNA miR–122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med. 2009;15:31–3.CrossRefPubMed Sarasin-Filipowicz M, Krol J, Markiewicz I, Heim MH, Filipowicz W. Decreased levels of microRNA miR–122 in individuals with hepatitis C responding poorly to interferon therapy. Nat Med. 2009;15:31–3.CrossRefPubMed
20.
go back to reference Sendi H, Mehrab-Mohseni M, Foureau DM, Ghosh S, Walling TL, Steuerwald N, et al. miR-122 decreases HCV entry into hepatocytes through binding to the 3′ UTR of OCLN mRNA. Liver Int. 2015;35:1315–23.CrossRefPubMed Sendi H, Mehrab-Mohseni M, Foureau DM, Ghosh S, Walling TL, Steuerwald N, et al. miR-122 decreases HCV entry into hepatocytes through binding to the 3′ UTR of OCLN mRNA. Liver Int. 2015;35:1315–23.CrossRefPubMed
21.
go back to reference Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, et al. microRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology. 2008;47:1223–32.CrossRefPubMed Varnholt H, Drebber U, Schulze F, Wedemeyer I, Schirmacher P, Dienes HP, et al. microRNA gene expression profile of hepatitis C virus-associated hepatocellular carcinoma. Hepatology. 2008;47:1223–32.CrossRefPubMed
22.
go back to reference Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, et al. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem. 2006;99:671–8.CrossRefPubMedPubMedCentral Kutay H, Bai S, Datta J, Motiwala T, Pogribny I, Frankel W, et al. Downregulation of miR-122 in the rodent and human hepatocellular carcinomas. J Cell Biochem. 2006;99:671–8.CrossRefPubMedPubMedCentral
23.
go back to reference O’Connell RM, Kahn D, Gibson WS, Round JL, Scholz RL, Chaudhuri AA, et al. microRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity. 2010;33:607–19.CrossRefPubMedPubMedCentral O’Connell RM, Kahn D, Gibson WS, Round JL, Scholz RL, Chaudhuri AA, et al. microRNA-155 promotes autoimmune inflammation by enhancing inflammatory T cell development. Immunity. 2010;33:607–19.CrossRefPubMedPubMedCentral
24.
go back to reference Jiang M, Broering R, Trippler M, Wu J, Zhang E, Zhang X, et al. microRNA-155 controls Toll-like receptor 3- and hepatitis C virus-induced immune responses in the liver. J Viral Hepat. 2014;21:99–110.CrossRefPubMed Jiang M, Broering R, Trippler M, Wu J, Zhang E, Zhang X, et al. microRNA-155 controls Toll-like receptor 3- and hepatitis C virus-induced immune responses in the liver. J Viral Hepat. 2014;21:99–110.CrossRefPubMed
25.
go back to reference Zhang Y, Wei W, Cheng N, Wang K, Li B, Jiang X, et al. Hepatitis C virus-induced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology. 2012;56:1631–40.CrossRefPubMed Zhang Y, Wei W, Cheng N, Wang K, Li B, Jiang X, et al. Hepatitis C virus-induced up-regulation of microRNA-155 promotes hepatocarcinogenesis by activating Wnt signaling. Hepatology. 2012;56:1631–40.CrossRefPubMed
26.
go back to reference Bala S, Tilahun Y, Taha O, Alao H, Kodys K, Catalano D, et al. Increased microRNA-155 expression in the serum and peripheral monocytes in chronic HCV infection. J Transl Med. 2012;10:151.CrossRefPubMedPubMedCentral Bala S, Tilahun Y, Taha O, Alao H, Kodys K, Catalano D, et al. Increased microRNA-155 expression in the serum and peripheral monocytes in chronic HCV infection. J Transl Med. 2012;10:151.CrossRefPubMedPubMedCentral
27.
go back to reference Cheng YQ, Ren JP, Zhao J, Wang JM, Zhou Y, Li GY, et al. microRNA-155 regulates interferon-gamma production in natural killer cells via Tim-3 signalling in chronic hepatitis C virus infection. Immunology. 2015;145:485–97.CrossRefPubMedPubMedCentral Cheng YQ, Ren JP, Zhao J, Wang JM, Zhou Y, Li GY, et al. microRNA-155 regulates interferon-gamma production in natural killer cells via Tim-3 signalling in chronic hepatitis C virus infection. Immunology. 2015;145:485–97.CrossRefPubMedPubMedCentral
28.
go back to reference Sidorkiewicz M, Grek M, Jozwiak B, Krol A, Piekarska A. The impact of chronic hepatitis C infection on cholesterol metabolism in PBMCs is associated with microRNA-146a expression. Eur J Clin Microbiol Infect Dis. 2017;36:697–702.CrossRefPubMed Sidorkiewicz M, Grek M, Jozwiak B, Krol A, Piekarska A. The impact of chronic hepatitis C infection on cholesterol metabolism in PBMCs is associated with microRNA-146a expression. Eur J Clin Microbiol Infect Dis. 2017;36:697–702.CrossRefPubMed
29.
go back to reference Bhanja Chowdhury J, Shrivastava S, Steele R, Di Bisceglie AM, Ray R, Ray RB. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J Virol. 2012;86:10221–5.CrossRefPubMedPubMedCentral Bhanja Chowdhury J, Shrivastava S, Steele R, Di Bisceglie AM, Ray R, Ray RB. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J Virol. 2012;86:10221–5.CrossRefPubMedPubMedCentral
30.
go back to reference Li S, Duan X, Li Y, Liu B, McGilvray I, Chen L. microRNA-130a inhibits HCV replication by restoring the innate immune response. J Viral Hepat. 2014;21:121–8.CrossRefPubMed Li S, Duan X, Li Y, Liu B, McGilvray I, Chen L. microRNA-130a inhibits HCV replication by restoring the innate immune response. J Viral Hepat. 2014;21:121–8.CrossRefPubMed
31.
go back to reference Chen Y, Chen J, Wang H, Shi J, Wu K, Liu S, et al. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 2013;9:e1003248.CrossRefPubMedPubMedCentral Chen Y, Chen J, Wang H, Shi J, Wu K, Liu S, et al. HCV-induced miR-21 contributes to evasion of host immune system by targeting MyD88 and IRAK1. PLoS Pathog. 2013;9:e1003248.CrossRefPubMedPubMedCentral
32.
go back to reference Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, et al. microRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology. 2008;47:1955–63.CrossRefPubMed Ladeiro Y, Couchy G, Balabaud C, Bioulac-Sage P, Pelletier L, Rebouissou S, et al. microRNA profiling in hepatocellular tumors is associated with clinical features and oncogene/tumor suppressor gene mutations. Hepatology. 2008;47:1955–63.CrossRefPubMed
33.
go back to reference Li G, Yu M, Lee WW, Tsang M, Krishnan E, Weyand CM, et al. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat Med. 2012;18:1518–24.CrossRefPubMedPubMedCentral Li G, Yu M, Lee WW, Tsang M, Krishnan E, Weyand CM, et al. Decline in miR-181a expression with age impairs T cell receptor sensitivity by increasing DUSP6 activity. Nat Med. 2012;18:1518–24.CrossRefPubMedPubMedCentral
34.
go back to reference Li GY, Zhou Y, Ying RS, Shi L, Cheng YQ, Ren JP, et al. Hepatitis C virus-induced reduction in miR-181a impairs CD4(+) T-cell responses through overexpression of DUSP6. Hepatology. 2015;61:1163–73.CrossRefPubMedPubMedCentral Li GY, Zhou Y, Ying RS, Shi L, Cheng YQ, Ren JP, et al. Hepatitis C virus-induced reduction in miR-181a impairs CD4(+) T-cell responses through overexpression of DUSP6. Hepatology. 2015;61:1163–73.CrossRefPubMedPubMedCentral
35.
go back to reference Shirasaki T, Honda M, Shimakami T, Horii R, Yamashita T, Sakai Y, et al. microRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells. J Virol. 2013;87:5270–86.CrossRefPubMedPubMedCentral Shirasaki T, Honda M, Shimakami T, Horii R, Yamashita T, Sakai Y, et al. microRNA-27a regulates lipid metabolism and inhibits hepatitis C virus replication in human hepatoma cells. J Virol. 2013;87:5270–86.CrossRefPubMedPubMedCentral
36.
go back to reference Hou W, Tian Q, Zheng J, Bonkovsky HL. microRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology. 2010;51:1494–504.CrossRefPubMedPubMedCentral Hou W, Tian Q, Zheng J, Bonkovsky HL. microRNA-196 represses Bach1 protein and hepatitis C virus gene expression in human hepatoma cells expressing hepatitis C viral proteins. Hepatology. 2010;51:1494–504.CrossRefPubMedPubMedCentral
37.
38.
go back to reference Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007;449:919–22.CrossRefPubMedPubMedCentral Pedersen IM, Cheng G, Wieland S, Volinia S, Croce CM, Chisari FV, et al. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature. 2007;449:919–22.CrossRefPubMedPubMedCentral
39.
go back to reference Peng C, Wang H, Zhang WJ, Jie SH, Tong QX, Lu MJ, et al. Inhibitory effect of miR-125b on hepatitis C virus core protein-induced TLR2/MyD88 signaling in THP-1 cells. World J Gastroenterol. 2016;22:4354–61.CrossRefPubMedPubMedCentral Peng C, Wang H, Zhang WJ, Jie SH, Tong QX, Lu MJ, et al. Inhibitory effect of miR-125b on hepatitis C virus core protein-induced TLR2/MyD88 signaling in THP-1 cells. World J Gastroenterol. 2016;22:4354–61.CrossRefPubMedPubMedCentral
40.
go back to reference Yoshikawa T, Takata A, Otsuka M, Kishikawa T, Kojima K, Yoshida H, et al. Silencing of microRNA-122 enhances interferon-α signaling in the liver through regulating SOCS3 promoter methylation. Sci Rep. 2012;2:637.CrossRefPubMedPubMedCentral Yoshikawa T, Takata A, Otsuka M, Kishikawa T, Kojima K, Yoshida H, et al. Silencing of microRNA-122 enhances interferon-α signaling in the liver through regulating SOCS3 promoter methylation. Sci Rep. 2012;2:637.CrossRefPubMedPubMedCentral
41.
go back to reference Yang X, Marcucci K, Anguela X, Couto LB. Preclinical evaluation of an anti-HCV miRNA cluster for treatment of HCV infection. Mol Ther. 2013;21:588–601.CrossRefPubMedPubMedCentral Yang X, Marcucci K, Anguela X, Couto LB. Preclinical evaluation of an anti-HCV miRNA cluster for treatment of HCV infection. Mol Ther. 2013;21:588–601.CrossRefPubMedPubMedCentral
42.
go back to reference Collins AS, McCoy CE, Lloyd AT, O’Farrelly C, Stevenson NJ. miR-19a: an effective regulator of SOCS3 and enhancer of JAK-STAT signalling. PLoS ONE. 2013;8:e69090.CrossRefPubMedPubMedCentral Collins AS, McCoy CE, Lloyd AT, O’Farrelly C, Stevenson NJ. miR-19a: an effective regulator of SOCS3 and enhancer of JAK-STAT signalling. PLoS ONE. 2013;8:e69090.CrossRefPubMedPubMedCentral
43.
go back to reference Mukherjee A, Di Bisceglie AM, Ray RB. Hepatitis C virus-mediated enhancement of microRNA miR-373 impairs the JAK/STAT signaling pathway. J Virol. 2015;89:3356–65.CrossRefPubMedPubMedCentral Mukherjee A, Di Bisceglie AM, Ray RB. Hepatitis C virus-mediated enhancement of microRNA miR-373 impairs the JAK/STAT signaling pathway. J Virol. 2015;89:3356–65.CrossRefPubMedPubMedCentral
44.
go back to reference Kim JH, Lee CH, Lee SW. Hepatitis C virus infection stimulates transforming growth factor-β1 expression through up-regulating miR-192. J Microbiol. 2016;54:520–6.CrossRefPubMed Kim JH, Lee CH, Lee SW. Hepatitis C virus infection stimulates transforming growth factor-β1 expression through up-regulating miR-192. J Microbiol. 2016;54:520–6.CrossRefPubMed
45.
go back to reference Huang S, Xie Y, Yang P, Chen P, Zhang L. HCV core protein-induced down-regulation of microRNA-152 promoted aberrant proliferation by regulating Wnt1 in HepG2 cells. PLoS ONE. 2014;9:e81730.CrossRefPubMedPubMedCentral Huang S, Xie Y, Yang P, Chen P, Zhang L. HCV core protein-induced down-regulation of microRNA-152 promoted aberrant proliferation by regulating Wnt1 in HepG2 cells. PLoS ONE. 2014;9:e81730.CrossRefPubMedPubMedCentral
46.
go back to reference Ishida H, Tatsumi T, Hosui A, Nawa T, Kodama T, Shimizu S, et al. Alterations in microRNA expression profile in HCV-infected hepatoma cells: involvement of miR-491 in regulation of HCV replication via the PI3 kinase/Akt pathway. Biochem Biophys Res Commun. 2011;412:92–7.CrossRefPubMed Ishida H, Tatsumi T, Hosui A, Nawa T, Kodama T, Shimizu S, et al. Alterations in microRNA expression profile in HCV-infected hepatoma cells: involvement of miR-491 in regulation of HCV replication via the PI3 kinase/Akt pathway. Biochem Biophys Res Commun. 2011;412:92–7.CrossRefPubMed
47.
go back to reference Singaravelu R, Chen R, Lyn RK, Jones DM, O’Hara S, Rouleau Y, et al. Hepatitis C virus induced up-regulation of microRNA-27: a novel mechanism for hepatic steatosis. Hepatology. 2014;59:98–108.CrossRefPubMed Singaravelu R, Chen R, Lyn RK, Jones DM, O’Hara S, Rouleau Y, et al. Hepatitis C virus induced up-regulation of microRNA-27: a novel mechanism for hepatic steatosis. Hepatology. 2014;59:98–108.CrossRefPubMed
48.
go back to reference Xie Z, Xiao Z, Wang F. Hepatitis C virus nonstructural 5A protein (HCV-NS5A) inhibits hepatocyte apoptosis through the NF-κb/miR-503/bcl-2 pathway. Mol Cells. 2017;40:202–10.PubMedPubMedCentral Xie Z, Xiao Z, Wang F. Hepatitis C virus nonstructural 5A protein (HCV-NS5A) inhibits hepatocyte apoptosis through the NF-κb/miR-503/bcl-2 pathway. Mol Cells. 2017;40:202–10.PubMedPubMedCentral
49.
go back to reference Sarma NJ, Tiriveedhi V, Subramanian V, Shenoy S, Crippin JS, Chapman WC, et al. Hepatitis C virus mediated changes in miRNA-449a modulates inflammatory biomarker YKL40 through components of the NOTCH signaling pathway. PLoS ONE. 2012;7:e50826.CrossRefPubMedPubMedCentral Sarma NJ, Tiriveedhi V, Subramanian V, Shenoy S, Crippin JS, Chapman WC, et al. Hepatitis C virus mediated changes in miRNA-449a modulates inflammatory biomarker YKL40 through components of the NOTCH signaling pathway. PLoS ONE. 2012;7:e50826.CrossRefPubMedPubMedCentral
Metadata
Title
miRNAs regulate immune response and signaling during hepatitis C virus infection
Authors
Huange Zhu
Yan Geng
Qian He
Miaoxian Li
Publication date
01-12-2018
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2018
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-018-0317-x

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