Hepatitis B virus polymerase blocks pattern recognition receptor signaling via interaction with DDX3: Implications for immune evasion

PLoS Pathogens

Volumn 6, Issue 7, 2010, Pages 1-11

  Wang, Haifeng ^a   Ryu, Wang Shick ^a  

^a Yonsei University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; DDX3 PROTEIN; DEAD BOX PROTEIN; I KAPPA B KINASE EPSILON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; TANK BINDING KINASE 1; TOLL LIKE RECEPTOR 3; UNCLASSIFIED DRUG; VIRUS POLYMERASE; VIRUS PROTEIN; DDX3X PROTEIN, HUMAN; I KAPPA B KINASE; INTERFERON REGULATORY FACTOR; P PROTEIN, HEPATITIS B VIRUS; PATTERN RECOGNITION RECEPTOR; POL PROTEIN; PROTEIN SERINE THREONINE KINASE; TBK1 PROTEIN, HUMAN;

ARTICLE; CELL STRAIN HEK293; CELL STRAIN HEPG2; ENZYME INHIBITION; HEPATITIS B VIRUS; INNATE IMMUNITY; INTERFERON PRODUCTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; CELL LINE; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; HUMAN; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY;

HEPATITIS B VIRUS;

CELL LINE; DEAD-BOX RNA HELICASES; GENE PRODUCTS, POL; HEPATITIS B VIRUS; HUMANS; I-KAPPA B KINASE; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERON REGULATORY FACTORS; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, PATTERN RECOGNITION; SIGNAL TRANSDUCTION;

EID: 77955381494     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1000986     Document Type: Article

References (47)

1. Zoulim F (2006) Antiviral therapy of chronic hepatitis B. Antiviral Res 71:206-215.
2. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
3. Pichlmair A, Reis e Sousa C (2007) Innate recognition of viruses. Immunity 27:370-383.
4. Honda K, Taniguchi T (2006) IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658.
5. Wieland S, Thimme R, Purcell RH, Chisari FV (2004) Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci U S A 101: 6669-6674.
6. Wieland SF, Chisari FV (2005) Stealth and cunning: hepatitis B and hepatitis C viruses. J Virol 79: 9369-9380.
7. Fisicaro P, Valdatta C, Boni C, Massari M, Mori C, et al. (2009) Early kinetics of innate and adaptive immune responses during hepatitis B virus infection. Gut 58: 974-982.
8. Lucifora J, Durantel D, Testoni B, Hantz O, Levrero M, et al. (2010) Control of hepatitis B virus replication by innate response of HepaRG cells. Hepatology 51: 63-72.
9. Schroder M, Baran M, Bowie AG (2008) Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J 27:2147-2157.
10. Soulat D, Burckstummer T, Westermayer S, Goncalves A, Bauch A, et al. (2008) The DEAD-box helicase DDX3X is a critical component of the TANK-binding kinase 1-dependent innate immune response. EMBO J 27:2135-2146.
11. Wang H, Kim S, Ryu WS (2009) DDX3 DEAD-Box RNA helicase inhibits hepatitis B virus reverse transcription by incorporation into nucleocapsids. J Virol 83: 5815-5824.
12. Alexopoulou L, Holt AC, Medzhitov R, Flavell RA (2001) Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 413: 732-738.
13. Li K, Chen Z, Kato N, Gale M, Jr., Lemon SM (2005) Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem 280: 16739-16747.
14. Cha MY, Ryu DK, Jung HS, Chang HE, Ryu WS (2009) Stimulation of hepatitis B virus genome replication by HBx is linked to both nuclear and cytoplasmic HBx expression. J Gen Virol 90: 978-986.
15. Nassal M (2008) Hepatitis B viruses: reverse transcription a different way. Virus Res 134: 235-249.
16. Saito T, Gale M, Jr. (2008) Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J Exp Med 205: 1523-1527.
17. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
18. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, et al. (2004) The RNA helicase RIG-I has an essential function in double-stranded RNAinduced innate antiviral responses. Nat Immunol 5: 730-737.
19. Sells MA, Chen ML, Acs G (1987) Production of hepatitis B virus particles in Hep G2 cells transfected with cloned hepatitis B virus DNA. Proc Natl Acad Sci U S A 84: 1005-1009.
20. Mibayashi M, Martinez-Sobrido L, Loo YM, Cardenas WB, Gale M, Jr., et al. (2007) Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J Virol 81: 514-524.
21. Wu J, Meng Z, Jiang M, Pei R, Trippler M, et al. (2009) Hepatitis B virus suppresses toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells. Hepatology 49: 1132-1140.
22. Preiss S, Thompson A, Chen X, Rodgers S, Markovska V, et al. (2008) Characterization of the innate immune signalling pathways in hepatocyte cell lines. J Viral Hepat 15: 888-900.
23. Wang N, Liang Y, Devaraj S, Wang J, Lemon SM, et al. (2009) Toll-like Receptor 3 Mediates Establishment of an Antiviral State Against Hepatitis C Virus in Hepatoma Cells. J Virol.
24. Yao E, Gong Y, Chen N, Tavis JE (2000) The Majority of Duck Hepatitis B Virus Reverse Transcriptase in Cells Is Nonencapsidated and Is Bound to a Cytoplasmic Structure. J Virol 74: 8648-8657.
25. Cao F, Tavis JE (2004) Detection and characterization of cytoplasmic hepatitis B virus reverse transcriptase. J Gen Virol 85: 3353-3360.
26. Foster GR, Ackrill AM, Goldin RD, Kerr IM, Thomas HC, et al. (1991) Expression of the terminal protein region of hepatitis B virus inhibits cellular responses to interferons alpha and gamma and double-stranded RNA [published erratum appears in Proc Natl Acad Sci U S A 1995 Apr 11;92(8):3632]. Proc Natl Acad Sci U S A 88: 2888-2892.
27. Wu M, Xu Y, Lin S, Zhang X, Xiang L, et al. (2007) Hepatitis B virus polymerase inhibits the interferon-inducible MyD88 promoter by blocking nuclear translocation of Stat1. J Gen Virol 88: 3260-3269.
28. Linder P (2006) Dead-box proteins: a family affair-active and passive players in RNP-remodeling. Nucleic Acids Res 34: 4168-4180.
29. Rocak S, Linder P (2004) DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 5: 232-241.
30. Chao CH, Chen CM, Cheng PL, Shih JW, Tsou AP, et al. (2006) DDX3, a DEAD box RNA helicase with tumor growth-suppressive property and transcriptional regulation activity of the p21waf1/cip1 promoter, is a candidate tumor suppressor. Cancer Res 66: 6579-6588.
31. Shih JW, Tsai TY, Chao CH, Wu Lee YH (2008) Candidate tumor suppressor DDX3 RNA helicase specifically represses cap-dependent translation by acting as an eIF4E inhibitory protein. Oncogene 27: 700-714.
32. Yedavalli VS, Neuveut C, Chi YH, Kleiman L, Jeang KT (2004) Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 119: 381-392.
33. Ariumi Y, Kuroki M, Abe K, Dansako H, Ikeda M, et al. (2007) DDX3 DEADbox RNA helicase is required for hepatitis C virus RNA replication. J Virol 81: 13922-13926.
34. Owsianka AM, Patel AH (1999) Hepatitis C virus core protein interacts with a human DEAD box protein DDX3. Virology 257: 330-340.
35. Botlagunta M, Vesuna F, Mironchik Y, Raman A, Lisok A, et al. (2008) Oncogenic role of DDX3 in breast cancer biogenesis. Oncogene 27: 3912-3922.
36. Bowie AG, Unterholzner L (2008) Viral evasion and subversion of patternrecognition receptor signalling. Nat Rev Immunol 8: 911-922.
37. Isogawa M, Robek MD, Furuichi Y, Chisari FV (2005) Toll-like receptor signaling inhibits hepatitis B virus replication in vivo. J Virol 79: 7269-7272.
38. Guo H, Jiang D, Ma D, Chang J, Dougherty AM, et al. (2009) Activation of pattern recognition receptor-mediated innate immunity inhibits the replication of hepatitis B virus in human hepatocyte-derived cells. J Virol 83: 847-858.
39. Wu J, Lu M, Meng Z, Trippler M, Broering R, et al. (2007) Toll-like receptormediated control of HBV replication by nonparenchymal liver cells in mice. Hepatology 46: 1769-1778.
40. Wang H, Ryu W.-S (2009) HBV Polymerase inhibits pattern recognition receptor-mediated innate immune response via its interaction with DDX3 DEAD-BOX RNA helicase. 2009 International meeting The Molecular Biology of Hepatitis B Viruses. pp 109.
41. Yu S, Chen J, Wu M, Chen H, Kato N, et al. (2010) Hepatitis B virus polymerase inhibits RIG-I- and Toll-like receptor 3-mediated beta interferon induction in human hepatocytes through interference with interferon regulatory factor 3 activation and dampening of the interaction between TBK1/IKK and DDX3. J Gen Virol 91(8): 2080-2090.
42. Ryu DK, Kim S, Ryu WS (2008) Hepatitis B virus polymerase suppresses translation of pregenomic RNA via a mechanism involving its interaction with 59 stem-loop structure. Virology 373: 112-123.
43. Lee J, Lee H-J, Shin M-K, Ryu W-S (2004) Versatile PCR-mediated insertion or deletion mutagenesis. BioTechniques 36: 398-400.
44. Radziwill G, Tucker W, Schaller H (1990) Mutational analysis of the hepatitis B virus P gene product: domain structure and RNase H activity. J Virol 64: 613-620.
45. Stack J, Haga IR, Schroder M, Bartlett NW, Maloney G, et al. (2005) Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J Exp Med 201: 1007-1018.
46. Shin M-K, Lee J, Ryu W-S (2004) A novel cis-acting element facilitates minusstrand DNA synthesis during reverse transcription of the hepatitis B viruses genome. J Virol 78: 6252-6262.
47. Pyronnet S, Imataka H, Gingras AC, Fukunaga R, Hunter T, et al. (1999) Human eukaryotic translation initiation factor 4G (eIF4G) recruits mnk1 to phosphorylate eIF4E. Embo J 18: 270-279.