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 Journal

Volumn 283, Issue 1, 2016, Pages 144-156

  Dansako, Hiromichi ^a   Ueda, Youki ^a   Okumura, Nobuaki ^a   Satoh, Shinya ^a   Sugiyama, Masaya ^b   Mizokami, Masashi ^b   Ikeda, Masanori ^a,c   Kato, Nobuyuki ^a  

^a OKAYAMA UNIVERSITY   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c KAGOSHIMA UNIVERSITY   (Japan)

Author keywords

antiviral response; cGAS STING signaling pathway; hepatitis B virus; innate immune response; viral assembly

Indexed keywords

ADAPTOR PROTEIN; ADAPTOR PROTEIN STING; ADENOSINE PHOSPHATE; GUANOSINE PHOSPHATE; UNCLASSIFIED DRUG; VIRUS DNA; ADENYLATE CYCLASE; CYCLIC GMP; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN;

ARTICLE; CONTROLLED STUDY; HEPATITIS B; HEPATITIS B VIRUS; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SOUTHERN BLOTTING; VIRUS ASSEMBLY; VIRUS REPLICATION; IMMUNOLOGY; METABOLISM; TUMOR CELL CULTURE;

ADENYLYL CYCLASES; CYCLIC GMP; HEPATITIS B; HEPATITIS B VIRUS; HUMANS; IMMUNITY, INNATE; MEMBRANE PROTEINS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED; VIRUS ASSEMBLY;

EID: 84961286262     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.13563     Document Type: Article

References (37)

1. Chen DS, (1993) From hepatitis to hepatoma: lessons from type B viral hepatitis. Science 262, 369-370.
2. Kao JH, &, Chen DS, (2002) Global control of hepatitis B virus infection. Lancet Infect Dis 2, 395-403.
3. Bertoletti A, &, Ferrari C, (2012) Innate and adaptive immune responses in chronic hepatitis B virus infections: towards restoration of immune control of viral infection. Gut 61, 1754-1764.
4. Busca A, &, Kumar A, (2014) Innate immune response in hepatitis B virus (HBV) infection. Virol J 11, 22.
5. Seeger C, Ganem D, &, Varmus HE, (1986) Biochemical and genetic evidence for the hepatitis B virus replication strategy. Science 232, 477-484.
6. Orito E, &, Mizokami M, (2003) Hepatitis B virus genotypes and hepatocellular carcinoma in Japan. Intervirology 46, 408-412.
7. Okumura N, Ikeda M, Satoh S, Dansako H, Sugiyama M, Mizokami M, &, Kato N, (2015) Negative regulation of hepatitis B virus replication by forkhead box protein A in human hepatoma cells. FEBS Lett 589, 1112-1118.
8. Quasdorff M, &, Protzer U, (2010) Control of hepatitis B virus at the level of transcription. J Viral Hepat 17, 527-536.
9. Sato S, Li K, Kameyama T, Hayashi T, Ishida Y, Murakami S, Watanabe T, Iijima S, Sakurai Y, Watashi K, et al,. (2015) The RNA sensor dually functions as an innate sensor and direct antiviral factor for hepatitis B virus. Immunity 42, 123-132.
10. Sun L, Wu J, Du F, Chen X, &, Chen ZJ, (2013) Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791.
11. Wu J, Sun L, Chen X, Du F, Shi H, Chen C, &, Chen ZJ, (2013) Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826-830.
12. Gao D, Wu J, Wu YT, Du F, Aroh C, Yan N, Sun L, &, Chen ZJ, (2013) Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903-906.
13. Kato N, Mori K, Abe K, Dansako H, Kuroki M, Ariumi Y, Wakita T, &, Ikeda M, (2009) Efficient replication systems for hepatitis C virus using a new human hepatoma cell line. Virus Res 146, 41-50.
14. 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 USA 84, 1005-1009.
15. Diamond MS, &, Farzan M, (2013) The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13, 46-57.
16. Mori K, Ikeda M, Ariumi Y, &, Kato N, (2010) Gene expression profile of Li23, a new human hepatoma cell line that enables robust hepatitis C virus replication: comparison with HuH-7 and other hepatic cell lines. Hepatol Res 40, 1248-1253.
17. Sejima H, Mori K, Ariumi Y, Ikeda M, &, Kato N, (2012) Identification of host genes showing differential expression profiles with cell-based long-term replication of hepatitis C virus RNA. Virus Res 167, 74-85.
18. Mori K, Hiraoka O, Ikeda M, Ariumi Y, Hiramoto A, Wataya Y, &, Kato N, (2013) Adenosine kinase is a key determinant for the anti-HCV activity of ribavirin. Hepatology 58, 1236-1244.
19. Dansako H, Ikeda M, &, Kato N, (2007) Limited suppression of the interferon-beta production by hepatitis C virus serine protease in cultured human hepatocytes. FEBS J 274, 4161-4176.
20. Maylan E, Curran J, Hofman K, Moradpour D, Binder M, Bartenschlager R, &, Tschopp J, (2005) Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437, 1167-1172.
21. Yan H, Zhong G, Xu G, He W, Jing Z, Gao Z, Huang Y, Qi Y, Peng B, Wang H, et al,. (2012) Sodium taurocholate cotransporting polypeptide is a functional receptor for human hepatitis B and D virus. eLife 1, e00049.
22. Zhang Z, Yuan B, Bao M, Lu N, Kim T, &, Liu YJ, (2011) The helicase DDX41 senses intracellular DNA mediated by the adaptor STING in dendritic cells. Nat Immunol 12, 959-965.
23. Nordhelm A, Lafer EM, Peck LJ, Wang JC, Stollar BD, &, Rich A, (1982) Negatively supercoiled plasmids contain left-handed Z-DNA segments as detected by specific antibody binding. Cell 31, 309-318.
24. n DNA sequences from right- to left-handed helical structure by salt, Co(III), or negative supercoiling. Proc Natl Acad Sci USA 79, 4560-4564.
25. Thomas R, Beck S, &, Pohl FM, (1983) Isolation of Z-DNA-containing plasmids. Proc Natl Acad Sci USA 80, 5550-5553.
26. Lafer EM, Valle RP, Moller A, Nordheim A, Schur PH, Rich A, &, Stollar BD, (1983) Z-DNA-specific antibodies in human systemic lupus erythematosus. J Clin Invest 71, 314-321.
27. Jeong JK, Yoon GS, &, Ryu WS, (2000) Evidence that the 5′-end cap structure is essential for encapsidation of hepatitis B virus pregenomic RNA. J Virol 74, 5502-5508.
28. Yang D, Zuo C, Wang X, Meng X, Xue B, Liu N, Yu R, Qin Y, Gao Y, Wang Q, et al,. (2014) Complete replication of hepatitis B virus and hepatitis C virus in a newly developed hepatoma cell line. Proc Natl Acad Sci USA 111, E1264-E1273.
29. Dansako H, Hiramoto H, Ikeda M, Wakita T, &, Kato N, (2014) Rab18 is required for viral assembly of hepatitis C virus through trafficking of the core protein to lipid droplets. Virology 462-463C, 166-174.
30. Ikeda M, Sugiyama K, Mizutani T, Tanaka T, Tanaka K, Sekihara H, Shimotohno K, &, Kato N, (1998) Human hepatocyte clonal cell lines that support persistent replication of hepatitis C virus. Virus Res 56, 157-167.
31. Kobayashi N, Fujiwara T, Westerman KA, Inoue Y, Sakaguchi M, Noguchi H, Miyazaki M, Cai J, Tanaka N, Fox IJ, et al,. (2000) Prevention of acute liver failure in rats with reversibly immortalized human hepatocytes. Science 287, 1258-1262.
32. Kobayashi N, Miyazaki M, Fukaya K, Inoue Y, Sakaguchi M, Uemura T, Noguchi H, Kondo A, Tanaka N, &, Namba M, (2000) Transplantation of highly differentiated immortalized human hepatocytes to treat acute liver failure. Transplantation 69, 202-207.
33. Dansako H, Ikeda M, Ariumi Y, Wakita T, &, Kato N, (2009) Double-stranded RNA-induced interferon-beta and inflammatory cytokine production modulated by hepatitis C virus serine proteases derived from patients with hepatic diseases. Arch Virol 154, 801-810.
34. Dansako H, Yamane D, Welsch C, McGivern DR, Hu F, Kato N, &, Lemon SM, (2013) Class A scavenger receptor 1 (MSR1) restricts hepatitis C virus replication by mediating Toll-like receptor 3 recognition of viral RNAs produced in neighboring cells. PLoS Pathog 9, e1003345.
35. Dansako H, Ikeda M, Abe K, Mori K, Takemoto K, Ariumi Y, &, Kato N, (2008) A new living cell-based assay system for monitoring genome-length hepatitis C virus RNA replication. Virus Res 137, 72-79.
36. Sugiyama M, Tanaka Y, Kato T, Orito E, Ito K, Acharya SK, Gish RG, Kramvis A, Shimada T, Izumi N, et al,. (2006) Influence of hepatitis B virus genotypes on the intra- and extracellular expression of viral DNA and antigens. Hepatology 44, 915-924.
37. Dansako H, Naganuma A, Nakamura T, Ikeda F, Nozaki A, &, Kato N, (2003) Differential activation of interferon-inducible genes by hepatitis C virus core protein mediated by the interferon stimulated response element. Virus Res 97, 17-30.