Hepatitis B virus evades immune recognition via RNA adenosine deaminase ADAR1-mediated viral RNA editing in hepatocytes (original) (raw)

• Seeger C. Control of viral transcripts as a concept for future HBV therapies. Curr Opin Virol. 2018;30:18–23.
  Article CAS PubMed Google Scholar
• Dansako H, Ueda Y, Okumura N, Satoh S, Sugiyama M, Mizokami M, et al. The cyclic GMP-AMP synthetase-STING signaling pathway is required for both the innate immune response against HBV and the suppression of HBV assembly. FEBS J. 2016;283:144–56.
  Article CAS PubMed Google Scholar
• Stacey AR, Norris PJ, Qin L, Haygreen EA, Taylor E, Heitman J, et al. Induction of a striking systemic cytokine cascade prior to peak viremia in acute human immunodeficiency virus type 1 infection, in contrast to more modest and delayed responses in acute hepatitis B and C virus infections. J Virol. 2009;83:3719–33.
  Article CAS PubMed PubMed Central Google Scholar
• Wieland S, Thimme R, Purcell RH, Chisari FV. Genomic analysis of the host response to hepatitis B virus infection. Proc Natl Acad Sci USA. 2004;101:6669–74.
  Article CAS PubMed PubMed Central Google Scholar
• Mutz P, Metz P, Lempp FA, Bender S, Qu B, Schöneweis K, et al. HBV bypasses the innate immune response and does not protect HCV from antiviral activity of interferon. Gastroenterology. 2018;154:1791–804.
  Article PubMed Google Scholar
• Wei C, Ni C, Song T, Liu Y, Yang X, Zheng Z, et al. The hepatitis B virus X protein disrupts innate immunity by downregulating mitochondrial antiviral signaling protein. J Immunol. 2010;185:1158–68.
  Article CAS PubMed Google Scholar
• Luangsay S, Gruffaz M, Isorce N, Testoni B, Michelet M, Faure-Dupuy S, et al. Early inhibition of hepatocyte innate responses by hepatitis B virus. J Hepatol. 2015;63:1314–22.
  Article CAS PubMed Google Scholar
• Sato S, Li K, Kameyama T, Hayashi T, Ishida Y, Murakami S, et al. The RNA sensor RIG-I dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity. 2015;42:123–32.
  Article CAS PubMed Google Scholar
• Thomsen MK, Nandakumar R, Stadler D, Malo A, Valls RM, Wang F, et al. Lack of immunological DNA sensing in hepatocytes facilitates hepatitis B virus infection. Hepatology. 2016;64:746–59.
  Article CAS PubMed Google Scholar
• Cheng X, Xia Y, Serti E, Block PD, Chung M, Chayama K, et al. Hepatitis B virus evades innate immunity of hepatocytes but activates cytokine production by macrophages. Hepatology. 2017;66:1779–93.
  Article CAS PubMed Google Scholar
• Suslov A, Boldanova T, Wang X, Wieland S, Heim MH. Hepatitis B virus does not interfere with innate immune responses in the human liver. Gastroenterology. 2018;154:1778–90.
  Article CAS PubMed Google Scholar
• Li K, Chen Z, Kato N, Gale M Jr., Lemon SM. Distinct poly(I-C) and virus-activated signaling pathways leading to interferon-beta production in hepatocytes. J Biol Chem Iological Chem. 2005;280:16739–47.
  Article CAS Google Scholar
• Yin X, Li X, Ambardekar C, Hu Z, Lhomme S, Feng Z. Hepatitis E virus persists in the presence of a type III interferon response. PLoS Pathog. 2017;13:e1006417.
  Article PubMed PubMed Central CAS Google Scholar
• Sayed IM, Verhoye L, Cocquerel L, Abravanel F, Foquet L, Montpellier C, et al. Study of hepatitis E virus infection of genotype 1 and 3 in mice with humanised liver. Gut. 2017;66:920–9.
  Article CAS PubMed Google Scholar
• Freund I, Eigenbrod T, Helm M, Dalpke AH. RNA modifications modulate activation of innate Toll-like receptors. Genes. 2019;10:92.
  Article CAS PubMed Central Google Scholar
• Mannion NM, Greenwood SM, Young R, Cox S, Brindle J, Read D, et al. The RNA-editing enzyme ADAR1 controls innate immune responses to RNA. Cell Rep. 2014;9:1482–94.
  Article CAS PubMed PubMed Central Google Scholar
• Pestal K, Funk CC, Snyder JM, Price ND, Treuting PM, Stetson DB. Isoforms of RNA-editing enzyme ADAR1 independently control nucleic acid sensor MDA5-driven autoimmunity and multi-organ development. Immunity. 2015;43:933–44.
  Article CAS PubMed PubMed Central Google Scholar
• Liddicoat BJ, Piskol R, Chalk AM, Ramaswami G, Higuchi M, Hartner JC, et al. RNA editing by ADAR1 prevents MDA5 sensing of endogenous dsRNA as nonself. Science. 2015;349:1115–20.
  Article CAS PubMed PubMed Central Google Scholar
• Yang S, Deng P, Zhu Z, Zhu J, Wang G, Zhang L, et al. Adenosine deaminase acting on RNA 1 limits RIG-I RNA detection and suppresses IFN production responding to viral and endogenous RNAs. J Immunol. 2014;193:3436–45.
  Article CAS PubMed Google Scholar
• Pfaller CK, Donohue RC, Nersisyan S, Brodsky L, Cattaneo R. Extensive editing of cellular and viral double-stranded RNA structures accounts for innate immunity suppression and the proviral activity of ADAR1p150. PLoS Biol. 2018;16:e2006577.
  Article PubMed PubMed Central CAS Google Scholar
• Pujantell M, Franco S, Galván-Femenía I, Badia R, Castellví M, Garcia-Vidal E, et al. ADAR1 affects HCV infection by modulating innate immune response. Antivir Res. 2018;156:116–27.
  Article CAS PubMed Google Scholar
• Yang D, Zuo C, Wang X, Meng X, Xue B, Liu N, et al. Complete replication of hepatitis B virus and hepatitis C virus in a newly developed hepatoma cell line. Proc Natl Acad Sci USA. 2014;111:E1264–73.
  Article CAS PubMed PubMed Central Google Scholar
• Duriez M, Mandouri Y, Lekbaby B, Wang H, Schnuriger A, Redelsperger F, et al. Alternative splicing of hepatitis B virus: a novel virus/host interaction altering liver immunity. J Hepatol. 2017;67:687–99.
  Article CAS PubMed PubMed Central Google Scholar
• Thomas JM, Beal PA. How do ADARs bind RNA? New protein-RNA structures illuminate substrate recognition by the RNA editing ADARs. BioEssays. 2017;39:10.
  PubMed Central Google Scholar
• Jeong JK, Yoon GS, Ryu WS. Evidence that the 5’-end cap structure is essential for encapsidation of hepatitis B virus pregenomic RNA. J Virol. 2000;74:5502–8.
  Article CAS PubMed PubMed Central Google Scholar
• Gallo A, Locatelli F. ADARs: allies or enemies? The importance of A-to-I RNA editing in human disease: from cancer to HIV-1. Biol Rev Camb Philos Soc. 2012;87:95–110.
  Article PubMed Google Scholar
• Valente L, Nishikura K. RNA binding-independent dimerization of adenosine deaminases acting on RNA and dominant negative effects of nonfunctional subunits on dimer functions. J Biol Chem. 2007;282:16054–61.
  Article CAS PubMed Google Scholar
• Pujantell M, Riveira-Muñoz E, Badia R, Castellví M, Garcia-Vidal E, Sirera G, et al. RNA editing by ADAR1 regulates innate and antiviral immune functions in primary macrophages. Sci Rep. 2017;7:13339.
  Article PubMed PubMed Central CAS Google Scholar
• Li T, Yang X, Li W, Song J, Li Z, Zhu X, et al. ADAR1 stimulation by IFN-alpha downregulates the expression of MAVS via RNA editing to regulate the anti-HBV response. Mol Ther. 2021;29:1335–48.
  Article PubMed CAS Google Scholar
• Leong CR, Oshiumi H, Suzuki T, Matsumoto M, Seya T. Nucleic acid sensors involved in the recognition of HBV in the liver-specific in vivo transfection mouse models-pattern recognition receptors and sensors for HBV. Med Sci. 2015;3:16–24.
  CAS Google Scholar
• Tomaselli S, Galeano F, Locatelli F, Gallo A. ADARs and the balance game between virus infection and innate immune cell response. Curr Issues Mol Biol. 2015;17:37–51.
  PubMed Google Scholar
• Doria M, Neri F, Gallo A, Farace MG, Michienzi A. Editing of HIV-1 RNA by the double-stranded RNA deaminase ADAR1 stimulates viral infection. Nucleic Acids Res. 2009;37:5848–58.
  Article CAS PubMed PubMed Central Google Scholar
• Yang Y, Zhou X, Jin Y. ADAR-mediated RNA editing in non-coding RNA sequences. Sci China Life Sci. 2013;56:944–52.
  Article CAS PubMed Google Scholar
• Barraud P, Banerjee S, Mohamed W, Jantsch M, Allain F. A bimodular nuclear localization signal assembled via an extended double-stranded RNA-binding domain acts as an RNA-sensing signal for transportin 1. Proc Natl Acad Sci USA. 2014;111:E1852–61.
  Article CAS PubMed PubMed Central Google Scholar
• Guo X, Chen P, Hou X, Xu W, Wang D, Wang TY, et al. The recombined cccDNA produced using minicircle technology mimicked HBV genome in structure and function closely. Sci Rep. 2016;6:25552.
  Article CAS PubMed PubMed Central Google Scholar
• Zipeto MA, Court AC, Sadarangani A, Delos Santos NP, Balaian L, Chun HJ, et al. ADAR1 activation drives leukemia stem cell self-renewal by impairing let-7 biogenesis. Cell Stem Cell. 2016;19:177–91.
  Article CAS PubMed PubMed Central Google Scholar
• Xu L, Wu Z, Tan S, Wang Z, Lin Q, Li X, et al. Tumor suppressor ZHX2 restricts hepatitis B virus replication via epigenetic and non-epigenetic manners. Antivir Res. 2018;153:114–23.
  Article CAS PubMed Google Scholar
• Liu Y, Li J, Chen J, Li Y, Wang W, Du X, et al. Hepatitis B virus polymerase disrupts K63-linked ubiquitination of STING to block innate cytosolic DNA-sensing pathways. J Virol. 2015;89:2287–300.
  Article PubMed CAS Google Scholar
• Jiang J, Tang H. Mechanism of inhibiting type I interferon induction by hepatitis B virus X protein. Protein Cell. 2010;1:1106–17.
  Article CAS PubMed Google Scholar
• Wang G, Wang H, Singh S, Zhou P, Yang S, Wang Y, et al. ADAR1 prevents liver injury from inflammation and suppresses interferon production in hepatocytes. Am J Pathol. 2015;185:3224–37.
  Article CAS PubMed PubMed Central Google Scholar
• Wang H, Wang G, Zhang L, Zhang J, Zhang J, Wang Q, et al. ADAR1 suppresses the activation of cytosolic RNA-sensing signaling pathways to protect the liver from ischemia/reperfusion injury. Sci Rep. 2016;6:20248.
  Article CAS PubMed PubMed Central Google Scholar
• Lu HL, Liao F. Melanoma differentiation-associated gene 5 senses hepatitis B virus and activates innate immune signaling to suppress virus replication. J Immunol. 2013;191:3264–76.
  Article CAS PubMed Google Scholar
• Chung H, Calis JJA, Wu X, Sun T, Yu Y, Sarbanes SL, et al. Human ADAR1 prevents endogenous RNA from triggering translational shutdown. Cell. 2018;172:811–24.
  Article CAS PubMed PubMed Central Google Scholar
• Liu G, Ma X, Wang Z, Wakae K, Yuan Y, He Z, et al. Adenosine deaminase acting on RNA-1 (ADAR1) inhibits hepatitis B virus (HBV) replication by enhancing microRNA-122 processing. J Biol Chem. 2019;294:14043–54.
  Article CAS PubMed PubMed Central Google Scholar
• Yuan L, Jia Q, Yang S, Idris N, Li Y, Wang Y, et al. ADAR1 promotes HBV replication through its deaminase domain. Front Biosci. 2020;25:710–21.
  Article CAS Google Scholar
• Sung WK, Lu Y, Lee C, Zhang D, Ronaghi M, Lee C. Deregulated direct targets of the hepatitis B virus (HBV) protein, HBx, identified through chromatin immunoprecipitation and expression microarray profiling. J Biol Chem. 2009;284:21941–54.
  Article CAS PubMed PubMed Central Google Scholar
• Shen C, Feng X, Mao T, Yang D, Zou J, Zao X, et al. Yin-Yang 1 and HBx protein activate HBV transcription by mediating the spatial interaction of cccDNA minichromosome with cellular chromosome 19p13.11. Emerg Microbes Infect. 2020;9:2455–64.
  Article CAS PubMed PubMed Central Google Scholar
• Shan X, Ren M, Chen K, Huang A, Tang H. Regulation of the microRNA processor DGCR8 by hepatitis B virus proteins via the transcription factor YY1-803. Arch Virol. 2015;160:795–803.
  Article CAS PubMed Google Scholar
• Zhang L, Cai X, Chen K, Wang Z, Wang L, Ren M, et al. Hepatitis B virus protein up-regulated HLJ1 expression via the transcription factor YY1 in human hepatocarcinoma cells. Virus Res. 2011;157:76–81.
  Article CAS PubMed Google Scholar
• Ishizuka JJ, Manguso RT, Cheruiyot CK, Bi K, Panda A, Iracheta-Vellve A, et al. Loss of ADAR1 in tumours overcomes resistance to immune checkpoint blockade. Nature. 2019;565:43–8.
  Article CAS PubMed Google Scholar
• Dorhoi A, Du Plessis N. Monocytic myeloid-derived suppressor cells in chronic infections. Front Immunol. 2017;8:1895.
  Article PubMed CAS Google Scholar