Inhibition of hepatitis B virus replication by activation of the cGAS-STING pathway

Journal of General Virology

Volumn 97, Issue 12, 2016, Pages 3368-3378

  He, Jing ^a   Hao, Ruidong ^a   Liu, Dan ^a   Liu, Xing ^a   Wu, Shaoshuai ^a   Guo, Shuting ^b   Wang, Yuan ^a   Tien, Po ^a   Guo, Deyin ^a  

^a WUHAN UNIVERSITY   (China)

^b Wuhan University of Bioengineering   (China)

Author keywords

CGAMP; CGAS; HBV replication

Indexed keywords

ALPHA INTERFERON; BETA INTERFERON; CYCLIC AMP; CYCLIC GMP; DNA; MB21D1 PROTEIN, HUMAN; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; NUCLEOTIDYLTRANSFERASE;

ANIMAL EXPERIMENT; ARTICLE; BLOOD; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION; HEPATITIS B; HEPATITIS B VIRUS; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROMOTER REGION; SECOND MESSENGER; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; VIRUS REPLICATION; ANIMAL; BAGG ALBINO MOUSE; FEMALE; GENETICS; HOST PATHOGEN INTERACTION; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; VIROLOGY; VIRUS ASSEMBLY;

ANIMALS; FEMALE; HEPATITIS B; HEPATITIS B VIRUS; HOST-PATHOGEN INTERACTIONS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; NUCLEOTIDYLTRANSFERASES; SIGNAL TRANSDUCTION; VIRUS ASSEMBLY; VIRUS REPLICATION;

EID: 85007228578     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000647     Document Type: Article

References (38)

1. Ablasser, A., Goldeck, M., Cavlar, T., Deimling, T., Witte, G., Röhl, I., Hopfner, K. P., Ludwig, J. & Hornung, V. (2013). cGAS produces a 2’-5’linked cyclic dinucleotide second messenger that activates STING. Nature 498, 380-384
2. Atianand, M. K. & Fitzgerald, K. A. (2013). Molecular basis of DNA recognition in the immune system. J Immunol 190, 1911-1918
3. Beck, J. & Nassal, M. (2007). Hepatitis B virus replication. World J Gastroenterol 13, 48-64
4. Cabrerizo, M., Bartolomé, J., De Sequera, P., Caramelo, C. & Carreño, V. (1997). Hepatitis B virus DNA in serum and blood cells of Hepatitis B surface antigen-negative hemodialysis patients and staff. J Am Soc Nephrol 8, 1443-1447
5. Cai, X., Chiu, Y. H. & Chen, Z. J. (2014). The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell 54, 289-296
6. Cavlar, T., Ablasser, A. & Hornung, V. (2012). Induction of type I IFNs by intracellular DNA-sensing pathways. Immunol Cell Biol 90, 474-482
7. Civril, F., Deimling, T., De Oliveira Mann, C. C., Ablasser, A., Moldt, M., Witte, G., Hornung, V. & Hopfner, K. P. (2013). Structural mechanism of cytosolic DNA sensing by cGAS. Nature 498, 332-337
8. Dansako, H., Ueda, Y., Okumura, N., Satoh, S., Sugiyama, M., Mizokami, M., Ikeda, M. & Kato, N. (2015). 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 283, 144-156
9. Diamond, M. S. & Farzan, M. (2013). The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat Rev Immunol 13, 46-57
10. Gao, D., Wu, J., Wu, Y. T., Du, F., Aroh, C., Yan, N., Sun, L. & Chen, Z. J. (2013a). Cyclic GMP-AMP synthase is an innate immune sensor of HIV and other retroviruses. Science 341, 903-906
11. Gao, P., Ascano, M., Wu, Y., Barchet, W., Gaffney, B. L., Zillinger, T., Serganov, A. A., Liu, Y., Jones, R. A. & other authors (2013b). Cyclic [G (2¢,5¢)pA(3¢,5¢)p] is the metazoan second messenger produced by DNAactivated cyclic GMP-AMP synthase. Cell 153, 1094-1107
12. Grimm, D., Thimme, R. & Blum, H. E. (2011). Hbv life cycle and novel drug targets. Hepatol Int 5, 644-653
13. Guidotti, L. G. & Chisari, F. V. (2006). Immunobiology and pathogenesis of viral hepatitis. Annu Rev Pathol 1, 23-61
14. Guo, H., Jiang, D., Ma, D., Chang, J., Dougherty, A. M., Cuconati, A., Block, T. M. & Guo, J. T. (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
15. Hao, R., He, J., Liu, X., Gao, G., Liu, D., Cui, L., Yu, G., Yu, W., Chen, Y. & Guo, D. (2015). Inhibition of Hepatitis B virus gene expression and replication by hepatocyte nuclear factor 6. J Virol 89, 4345-4355
16. Hösel, M., Quasdorff, M., Wiegmann, K., Webb, D., Zedler, U., Broxtermann, M., Tedjokusumo, R., Esser, K., Arzberger, S. & other authors (2009). Not interferon, but interleukin-6 controls early gene expression in Hepatitis B virus infection. Hepatology 50, 1773-1782
17. Ishii, K. J., Coban, C., Kato, H., Takahashi, K., Torii, Y., Takeshita, F., Ludwig, H., Sutter, G., Suzuki, K. & other authors (2006). A Toll-like receptor-independent antiviral response induced by double-stranded Bform DNA. Nat Immunol 7, 40-48
18. Ishikawa, H. & Barber, G. N. (2008). STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455, 674-678
19. Ishikawa, H., Ma, Z. & Barber, G. N. (2009). STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461, 788-792
20. Kranzusch, P. J., Lee, A. S., Berger, J. M. & Doudna, J. A. (2013). Structure of human cGAS reveals a conserved family of second-messenger enzymes in innate immunity. Cell Rep 3, 1362-1368
21. Kristiansen, H., Gad, H. H., Eskildsen-Larsen, S., Despres, P. & Hartmann, R. (2011). The oligoadenylate synthetase family: an ancient protein family with multiple antiviral activities. J Interferon Cytokine Res 31, 41-47
22. Li, X., Shu, C., Yi, G., Chaton, C. T., Shelton, C. L., Diao, J., Zuo, X., Kao, C. C., Herr, A. B. & Li, P. (2013). Cyclic GMP-AMP synthase is activated by double-stranded DNA-induced oligomerization. Immunity 39, 1019-1031
23. Michalak, T. I., Pasquinelli, C., Guilhot, S. & Chisari, F. V. (1994). Hepatitis B virus persistence after recovery from acute viral hepatitis. J Clin Invest 94, 907
24. Morales, D. J. & Lenschow, D. J. (2013). The antiviral activities of ISG15. J Mol Biol 425, 4995-5008
25. Römling, U. (2008). Great times for small molecules: c-di-AMP, a second messenger candidate in Bacteria and Archaea. Sci Signal 1, p e39
26. Saitoh, T., Fujita, N., Hayashi, T., Takahara, K., Satoh, T., Lee, H., Matsunaga, K., Kageyama, S., Omori, H. & other authors (2009). Atg9a controls dsDNA-driven dynamic translocation of STING and the innate immune response. Proc Natl Acad Sci U S A 106, 20842-20846
27. Schneider, W. M., Chevillotte, M. D. & Rice, C. M. (2014). Interferonstimulated genes: a complex web of host defenses. Annu Rev Immunol 32, 513-545
28. Seeger, C. & Mason, W. S. (2000). Hepatitis B virus biology. Microbiol Mol Biol Rev 64, 51-68
29. Stark, G. R., Kerr, I. M., Williams, B. R., Silverman, R. H. & Schreiber, R. D. (1998). How cells respond to interferons. Annu Rev Biochem 67, 227-264
30. Sun, W., Li, Y., Chen, L., Chen, H., You, F., Zhou, X., Zhou, Y., Zhai, Z., Chen, D. & Jiang, Z. (2009). ERIS, an endoplasmic reticulum IFN stimulator, activates innate immune signaling through dimerization. Proc Natl Acad Sci U S A 106, 8653-8658
31. Sun, L., Wu, J., Du, F., Chen, X. & Chen, Z. J. (2013). Cyclic GMP-AMP synthase is a cytosolic DNA sensor that activates the type I interferon pathway. Science 339, 786-791
32. Tamayo, R., Pratt, J. T. & Camilli, A. (2007). Roles of cyclic diguanylate in the regulation of bacterial pathogenesis. Annu Rev Microbiol 61, 131-148
33. Tanaka, Y. & Chen, Z. J. (2012). STING specifies IRF3 phosphorylation by TBK1 in the cytosolic DNA signaling pathway. Sci Signal 5, ra20
34. Trippler, M., Meyer zum Büschenfelde, K. H. & Gerken, G. (1999). HBV viral load within subpopulations of peripheral blood mononuclear cells in HBV infection using limiting dilution PCR. J Virol Methods 78, 129-147
35. Wu, J., Sun, L., Chen, X., Du, F., Shi, H., Chen, C. & Chen, Z. J. (2013). Cyclic GMP-AMP is an endogenous second messenger in innate immune signaling by cytosolic DNA. Science 339, 826-830
36. Zhang, E. & Lu, M. (2015). Toll-like receptor (TLR)-mediated innate immune responses in the control of Hepatitis B virus (HBV) infection. Med Microbiol Immunol 204, 11-20
37. Zhang, X., Shi, H., Wu, J., Zhang, X., Sun, L., Chen, C. & Chen, Z. J. (2013). Cyclic GMP-AMP containing mixed phosphodiester linkages is an endogenous high-affinity ligand for STING. Mol Cell 51, 226-235
38. Zhang, X., Wu, J., Du, F., Xu, H., Sun, L., Chen, Z., Brautigam, C. A., Zhang, X. & Chen, Z. J. (2014). The cytosolic DNA sensor cGAS forms an oligomeric complex with DNA and undergoes switch-like conformational changes in the activation loop. Cell Rep 6, 421-430