Hepatitis-C-virus-induced microRNAs dampen interferon-mediated antiviral signaling

Nature Medicine

Volumn 22, Issue 12, 2016, Pages 1475-1481

  Jarret, Abigail ^a   McFarland, Adelle P ^a   Horner, Stacy M ^a,f   Kell, Alison ^a   Schwerk, Johannes ^a   Hong, Meeae ^a   Badil, Samantha ^a   Joslyn, Rochelle C ^a   Baker, Darren P ^a,b,g   Carrington, Mary ^c,d   Hagedorn, Curt H ^e   Gale, Michael ^a   Savan, Ram ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

^b BIOGEN   (United States)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d HARVARD UNIVERSITY   (United States)

^e CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

^f DUKE UNIVERSITY MEDICAL CENTER   (United States)

^g GENZYME CORPORATION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERFERON; INTERFERON RECEPTOR; INTERFERON TYPE 3; MICRORNA; MICRORNA 208B; MICRORNA 499A 5P; UNCLASSIFIED DRUG; ALPHA BETA INTERFERON RECEPTOR; IFNAR1 PROTEIN, HUMAN; IL28A PROTEIN, HUMAN; IL28B PROTEIN, HUMAN; INTERLEUKIN DERIVATIVE; MIRN208 MICRORNA, HUMAN; MIRN499 MICRORNA, HUMAN; MYOSIN;

ANIMAL CELL; ARTICLE; GENE EXPRESSION; HEPATITIS C; HEPATITIS C VIRUS; HEPG2 CELL LINE; HUMAN; HUMAN CELL; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; RECEPTOR DOWN REGULATION; RNA DEGRADATION; SIGNAL TRANSDUCTION; VIRUS IMMUNITY; CHRONIC HEPATITIS C; CRISPR CAS SYSTEM; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENETICS; HEP-G2 CELL LINE; HEPACIVIRUS; IMMUNOLOGY; METABOLISM;

CRISPR-CAS SYSTEMS; DOWN-REGULATION; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HEP G2 CELLS; HEPACIVIRUS; HEPATITIS C; HEPATITIS C, CHRONIC; HEPATOCYTES; HUMANS; INTERFERON TYPE I; INTERLEUKINS; MICRORNAS; MYOSINS; RECEPTOR, INTERFERON ALPHA-BETA;

EID: 84995471895     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.4211     Document Type: Article

References (41)

1. El-Serag, H. B. Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142, 1264-1273. e1 (2012).
2. Lavanchy, D. Evolving epidemiology of hepatitis C virus. Clin. Microbiol. Infect. 17, 107-115 (2011).
3. Shepard, C. W., Finelli, L., Alter, M. J. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5, 558-567 (2005).
4. McFarland, A. P. et al. The favorable IFNL3 genotype escapes mRNA decay mediated by AU-rich elements and hepatitis C virus-induced microRNAs. Nat. Immunol. 15, 72-79 (2014).
5. Liang, T. J., Ghany, M. G. Current and future therapies for hepatitis C virus infection. N. Engl. J. Med. 368, 1907-1917 (2013).
6. Manns, M. P., von Hahn, T. Novel therapies for hepatitis C-one pill fits all Nat. Rev. Drug Discov. 12, 595-610 (2013).
7. Ghany, M. G., Nelson, D. R., Strader, D. B., Thomas, D. L., Seeff, L. B. An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 54, 1433-1444 (2011).
8. Lawitz, E. et al. Sofosbuvir for previously untreated chronic hepatitis C infection. N. Engl. J. Med. 368, 1878-1887 (2013).
9. Afdhal, N. et al. Ledipasvir and sofosbuvir for untreated HCV genotype 1 infection. N. Engl. J. Med. 370, 1889-1898 (2014).
10. Pawlotsky, J. M. New hepatitis C therapies: the toolbox, strategies, challenges. Gastroenterology 146, 1176-1192 (2014).
11. Jayasekera, C. R., Barry, M., Roberts, L. R., Nguyen, M. H. Treating hepatitis C in lower-income countries. N. Engl. J. Med. 370, 1869-1871 (2014).
12. Pearlman, B. L. Protease inhibitors for the treatment of chronic hepatitis C genotype-1 infection: the new standard of care. Lancet Infect. Dis. 12, 717-728 (2012).
13. Schinazi, R., Halfon, P., Marcellin, P., Asselah, T. HCV direct-acting antiviral agents: the best interferon-free combinations. Liver Int. 34 (Suppl. 1), 69-78 (2014).
14. Rauch, A. et al. Genetic variation in IL28B is associated with chronic hepatitis C and treatment failure: a genome-wide association study. Gastroenterology 138, 1338-1345, 1345. e1-1345. e7 (2010).
15. Thomas, D. L. et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 461, 798-801 (2009).
16. Ge, D. et al. Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature 461, 399-401 (2009).
17. Suppiah, V. et al. IL28B is associated with response to chronic hepatitis C interferon-alpha and ribavirin therapy. Nat. Genet. 41, 1100-1104 (2009).
18. Tanaka, Y. et al. Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C. Nat. Genet. 41, 1105-1109 (2009).
19. de Castellarnau, M. et al. Deciphering the interleukin 28B variants that better predict response to pegylated interferon-and ribavirin therapy in HCV/HIV-1 coinfected patients. PLoS One 7, e31016 (2012).
20. di Iulio, J. et al. Estimating the net contribution of interleukin-28B variation to spontaneous hepatitis C virus clearance. Hepatology 53, 1446-1454 (2011).
21. Pedergnana, V. et al. Analysis of IL28B variants in an Egyptian population defines the 20 kilobases minimal region involved in spontaneous clearance of hepatitis C virus. PLoS One 7, e38578 (2012).
22. Prokunina-Olsson, L. et al. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat. Genet. 45, 164-171 (2013).
23. Sheahan, T. et al. Interferon lambda alleles predict innate antiviral immune responses and hepatitis C virus permissiveness. Cell Host Microbe 15, 190-202 (2014).
24. Honda, M. et al. Hepatic ISG expression is associated with genetic variation in interleukin 28B and the outcome of IFN therapy for chronic hepatitis C. Gastroenterology 139, 499-509 (2010).
25. He, X. S. et al. Global transcriptional response to interferon is a determinant of HCV treatment outcome and is modified by race. Hepatology 44, 352-359 (2006).
26. Welzel, T. M. et al. Variants in interferon-alpha pathway genes and response to pegylated interferon-Alpha2a plus ribavirin for treatment of chronic hepatitis C virus infection in the hepatitis C antiviral long-term treatment against cirrhosis trial. Hepatology 49, 1847-1858 (2009).
27. Fukuda, R. et al. Expression of interferon-alpha receptor mRNA in the liver in chronic liver diseases associated with hepatitis C virus: relation to effectiveness of interferon therapy. J. Gastroenterol. 31, 806-811 (1996).
28. Fukuda, R. et al. Effectiveness of interferon-alpha therapy in chronic hepatitis C is associated with the amount of interferon-alpha receptor mRNA in the liver. J. Hepatol. 26, 455-461 (1997).
29. Mathai, J. et al. IFN-alpha receptor mRNA expression in a United States sample with predominantly genotype 1a/I chronic hepatitis C liver biopsies correlates with response to IFN therapy. J. Interferon Cytokine Res. 19, 1011-1018 (1999).
30. Morita, K. et al. Expression of interferon receptor genes in the liver as a predictor of interferon response in patients with chronic hepatitis C. J. Med. Virol. 58, 359-365 (1999).
31. Morita, K. et al. Expression of interferon receptor genes (IFNAR1 and IFNAR2 mRNA) in the liver may predict outcome after interferon therapy in patients with chronic genotype 2a or 2b hepatitis C virus infection. J. Clin. Gastroenterol. 26, 135-140 (1998).
32. Liu, J. et al. Virus-induced unfolded protein response attenuates antiviral defenses via phosphorylation-dependent degradation of the type I interferon receptor. Cell Host Microbe 5, 72-83 (2009).
33. Chandra, P. K. et al. HCV infection selectively impairs type I but not type III IFN signaling. Am. J. Pathos. 184, 214-229 (2014).
34. Schwerk, J., Jarret, A. P., Joslyn, R. C., Savan, R. Landscape of post-transcriptional gene regulation during hepatitis C virus infection. Curr. Opin. Virol. 12, 75-84 (2015).
35. van Rooij, E. et al. A family of microRNAs encoded by myosin genes governs myosin expression and muscle performance. Dev. Cell 17, 662-673 (2009).
36. Liu, S. et al. Measuring antiviral activity of benzimidazole molecules that alter IRES RNA structure with an infectious hepatitis C virus chimera expressing Renilla luciferase. Antiviral Res. 89, 54-63 (2011).
37. Eldrup, A. B. et al. Structure-activity relationship of heterobase-modified 2-C-methyl ribonucleosides as inhibitors of hepatitis C virus RNA replication. J. Med. Chem. 47, 5284-5297 (2004).
38. Ank, N. et al. Lambda interferon (IFN-lambda), a type III IFN, is induced by viruses and IFNs and displays potent antiviral activity against select virus infections in vivo. J. Virol. 80, 4501-4509 (2006).
39. Zeuzem, S. et al. Pegylated Interferon-Lambda (PEGIFN-L) shows superior viral response with improved safety and toleraility versus PEGIFNa-2A in HCV patients (G1/2/3/4): Emerage phase IIB through week 12. J. Hepatol. 54, S538-S539 (2011).
40. Muir, A. J. et al. A randomized phase 2b study of peginterferon lambda-1a for the treatment of chronic HCV infection. J. Hepatol. 61, 1238-1246 (2014).
41. Gonzalez, G., Pfannes, L., Brazas, R., Striker, R. Selection of an optimal RNA transfection reagent and comparison to electroporation for the delivery of viral RNA. J. Virol. Methods 145, 14-21 (2007).