Sting agonists induce an innate antiviral immune response against hepatitis B virus

Antimicrobial Agents and Chemotherapy

Volumn 59, Issue 2, 2015, Pages 1273-1281

  Guo, Fang ^a   Han, Yanxing ^b,c   Zhao, Xuesen ^a,d   Wang, Jianghua ^e   Liu, Fei ^a   Xu, Chunxiao ^a   Wei, Lai ^e   Jiang, Jian Dong ^b,c   Block, Timothy M ^a,d   Guo, Ju Tao ^a   Chang, Jinhong ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b INSTITUTE OF MEDICINAL BIOTECHNOLOGY   (China)

^c INSTITUTE OF MATERIA MEDICA   (China)

^d BARUCH S BLUMBERG INSTITUTE   (United States)

^e PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; BETA INTERFERON; PATTERN RECOGNITION RECEPTOR; STIMULATOR OF INTERFERON GENE; TETRACYCLINE; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG; VADIMEZAN; ANTIVIRUS AGENT; MEMBRANE PROTEIN; MPYS PROTEIN, MOUSE; XANTHONE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL THERAPY; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DRUG EFFICACY; FEMALE; HEPATITIS B; HEPATITIS B VIRUS; HYDRODYNAMICS; IMMUNE RESPONSE; IMMUNOTHERAPY; IN VIVO STUDY; INNATE IMMUNITY; LIVER CELL; LIVER CELL CULTURE; MACROPHAGE ACTIVATION; MACROPHAGE CULTURE; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; AGONISTS; ANIMAL; CELL LINE; DRUG EFFECTS; HEPATITIS B, CHRONIC; PHYSIOLOGY;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; HEPATITIS B VIRUS; HEPATITIS B, CHRONIC; IMMUNITY, INNATE; MEMBRANE PROTEINS; MICE; VIRUS REPLICATION; XANTHONES;

EID: 84921914245     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.04321-14     Document Type: Article

References (55)

1. Chisari FV, Ferrari C. 1995. Hepatitis B virus immunopathogenesis. Annu Rev Immunol 13:29-60. http://dx.doi.org/10.1146/annurev.iy.13 .040195.000333.
2. Lee WM. 1997. Hepatitis B virus infection. N Engl J Med 337:1733-1745. http://dx.doi.org/10.1056/NEJM199712113372406.
3. Liang TJ. 2009. Hepatitis B: the virus and disease. Hepatology 49:S13-S21. http://dx.doi.org/10.1002/hep.22881.
4. Dienstag JL. 2009. Benefits and risks of nucleoside analog therapy for hepatitis B. Hepatology 49: S112-S121. http://dx.doi.org/10.1002/hep .22920.
5. Perrillo R. 2009. Benefits and risks of interferon therapy for hepatitis B. Hepatology 49:S103-S111. http://dx.doi.org/10.1002/hep.22956.
6. Rehermann B, Ferrari C, Pasquinelli C, Chisari FV. 1996. The hepatitis B virus persists for decades after patients' recovery from acute viral hepatitis despite active maintenance of a cytotoxic T-lymphocyte response. Nat Med 2:1104-1108. http://dx.doi.org/10.1038/nm1096-1104.
7. Block TM, Gish R, Guo H, Mehta A, Cuconati A, Thomas London W, Guo JT. 2013. Chronic hepatitis B: what should be the goal for new therapies? Antiviral Res 98:27-34. http://dx.doi.org/10.1016/j.antiviral.2013.01.006.
8. Chang J, Block TM, Guo JT. 2012. The innate immune response to hepatitis B virus infection: implications for pathogenesis and therapy. Antiviral Res 96:405-413. http://dx.doi.org/10.1016/j.antiviral.2012.10.001.
9. Publicover J, Goodsell A, Nishimura S, Vilarinho S, Wang ZE, Avanesyan L, Spolski R, Leonard WJ, Cooper S, Baron JL. 2011. IL-21 is pivotal in determining age-dependent effectiveness of immune responses in a mouse model of human hepatitis B. J Clin Invest 121:1154-1162. http://dx.doi.org/10.1172/JCI44198.
10. Publicover J, Gaggar A, Nishimura S, Van Horn CM, Goodsell A, Muench MO, Reinhardt RL, van Rooijen N, Wakil AE, Peters M, Cyster JG, Erle DJ, Rosenthal P, Cooper S, Baron JL. 2013. Age-dependent hepatic lymphoid organization directs successful immunity to hepatitis B. J Clin Invest 123:3728-3739. http://dx.doi.org/10.1172/JCI68182.
11. Lanford RE, Guerra B, Chavez D, Giavedoni L, Hodara VL, Brasky KM, Fosdick A, Frey CR, Zheng J, Wolfgang G, Halcomb RL, Tumas DB. 2013. GS-9620, an oral agonist of Toll-like receptor-7, induces prolonged suppression of hepatitis B virus in chronically infected chimpanzees. Gastroenterology 144:1508-1517, 1517 e1501-1510. http://dx.doi.org/10 .1053/j.gastro.2013.02.003.
12. Kimura K, Moriwaki H, Nagaki M, Saio M, Nakamoto Y, Naito M, Kuwata K, Chisari FV. 2006. Pathogenic role of B cells in anti-CD40-induced necroinflammatory liver disease. Am J Pathol 168:786-795. http: //dx.doi.org/10.2353/ajpath.2006.050314.
13. Kimura K, Kakimi K, Wieland S, Guidotti LG, Chisari FV. 2002. Activated intrahepatic antigen-presenting cells inhibit hepatitis B virus replication in the liver of transgenic mice. J Immunol 169:5188-5195. http://dx.doi.org/10.4049/jimmunol.169.9.5188.
14. Isogawa M, Chung J, Murata Y, Kakimi K, Chisari FV. 2013. CD40 activation rescues antiviral CD8(+) T cells from PD-1-mediated exhaustion. PLoS Pathog 9: e1003490. http://dx.doi.org/10.1371/journal .ppat.1003490.
15. Burdette DL, Vance RE. 2013. STING and the innate immune response to nucleic acids in the cytosol. Nat Immunol 14:19-26. http://dx.doi.org/10 .1038/ni.2491.
16. 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. http://dx.doi.org/10.1126 /science.1240933.
17. Ishikawa H, Barber GN. 2008. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 455:674-678. http: //dx.doi.org/10.1038/nature07317.
18. Conlon J, Burdette DL, Sharma S, Bhat N, Thompson M, Jiang Z, Rathinam VA, Monks B, Jin T, Xiao TS, Vogel SN, Vance RE, Fitzgerald KA. 2013. Mouse, but not human STING, binds and signals in response to the vascular disrupting agent 5,6-dimethylxanthenone-4-acetic acid. J Immunol 190:5216-5225. http://dx.doi.org/10.4049/jimmunol.1300097.
19. Cavlar T, Deimling T, Ablasser A, Hopfner KP, Hornung V. 2013. Species-specific detection of the antiviral small-molecule compound CMA by STING. EMBO J 32:1440-1450. http://dx.doi.org/10.1038 /emboj.2013.86.
20. Campagna MR, Liu F, Mao R, Mills C, Cai D, Guo F, Zhao X, Ye H, Cuconati A, Guo H, Chang J, Xu X, Block TM, Guo JT. 2013. Sulfamoylbenzamide derivatives inhibit the assembly of hepatitis B virus nucleocapsids. J Virol 87:6931-6942. http://dx.doi.org/10.1128/JVI.00582-13.
21. Xu C, Guo H, Pan XB, Mao R, Yu W, Xu X, Wei L, Chang J, Block TM, Guo JT. 2010. Interferons accelerate decay of replication-competent nucleocapsids of hepatitis B virus. J Virol 84:9332-9340. http://dx.doi.org/10 .1128/JVI.00918-10.
22. Zhao X, Guo F, Liu F, Cuconati A, Chang J, Block TM, Guo JT. 2014. Interferon induction of IFITM proteins promotes infection by human coronavirus OC43. Proc Natl Acad Sci U S A 111:6756-6761. http://dx .doi.org/10.1073/pnas.1320856111.
23. Chang J, Sigal LJ, Lerro A, Taylor J. 2001. Replication of the human hepatitis delta virus genome is initiated in mouse hepatocytes following intravenous injection of naked DNA or RNA sequences. J Virol 75:3469-3473. http://dx.doi.org/10.1128/JVI.75.7.3469-3473.2001.
24. Yang PL, Althage A, Chung J, Chisari FV. 2002. Hydrodynamic injection of viral DNA: a mouse model of acute hepatitis B virus infection. Proc Natl Acad Sci U S A 99:13825-13830. http://dx.doi.org/10 .1073/pnas.202398599.
25. Wu J, Lu M, Meng Z, Trippler M, Broering R, Szczeponek A, Krux F, Dittmer U, Roggendorf M, Gerken G, Schlaak JF. 2007. Toll-like recep-tor-mediated control of HBV replication by nonparenchymal liver cells in mice. Hepatology 46:1769-1778. http://dx.doi.org/10.1002/hep.21897.
26. 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. http://dx.doi.org/10.1128/JVI.79.11.7269-7272.2005.
27. Guidotti LG, Ishikawa T, Hobbs MV, Matzke B, Schreiber R, Chisari FV. 1996. Intracellular inactivation of the hepatitis B virus by cytotoxic T lymphocytes. Immunity 4:25-36. http://dx.doi.org/10.1016/S1074-7613 (00)80295-2.
28. Guidotti LG, Rochford R, Chung J, Shapiro M, Purcell R, Chisari FV. 1999. Viral clearance without destruction of infected cells during acute HBV infection. Science 284:825-829. http://dx.doi.org/10.1126/science .284.5415.825.
29. Wu J, Meng Z, Jiang M, Pei R, Trippler M, Broering R, Bucchi A, Sowa JP, Dittmer U, Yang D, Roggendorf M, Gerken G, Lu M, Schlaak JF. 2009. Hepatitis B virus suppresses Toll-like receptor-mediated innate immune responses in murine parenchymal and nonparenchymal liver cells. Hepatology 49:1132-1140. http://dx.doi.org/10.1002/hep.22751.
30. Stringfellow DA. 1977. Comparation interferon-inducing and antiviral properties of 2-amino-5-bromo-6-methyl-4-pyrimidinol (U-25,166), tilorone hydrochloride, and polyinosinic-polycytidylic acid. Antimicrob Agents Chemother 11:984-992. http://dx.doi.org/10.1128/AAC.11.6.984.
31. Ching LM, Young HA, Eberly K, Yu CR. 1999. Induction of STAT and NFkappaB activation by the antitumor agents 5,6-dimethylxanthenone-4-acetic acid and flavone acetic acid in a murine macrophage cell line. Biochem Pharmacol 58: 1173-1181. http://dx.doi .org/10.1016/S0006-2952(99)00194-X.
32. Baguley BC. 2001. Small-molecule cytokine inducers causing tumor necrosis. Curr Opin Investig Drugs 2:967-975.
33. Kim S, Li L, Maliga Z, Yin Q, Wu H, Mitchison TJ. 2013. Anticancer flavonoids are mouse-selective STING agonists. ACS Chem Biol 8:1396-1401. http://dx.doi.org/10.1021/cb400264n.
34. Viganò M, Degasperi E, Aghemo A, Lampertico P, Colombo M. 2012. Anti-TNF drugs in patients with hepatitis B orCvirus infection: safety and clinical management. Expert Opin Biol Ther 12:193-207. http://dx.doi .org/10.1517/14712598.2012.646986.
35. Seeger C, Mason WS. 2000. Hepatitis B virus biology. Microbiol Mol Biol Rev 64:51-68. http://dx.doi.org/10.1128/MMBR.64.1.51-68.2000.
36. Knolle PA, Thimme R. 2014. Hepatic immune regulation and its involvement in viral hepatitis infection. Gastroenterology 146:1193-1207. http: //dx.doi.org/10.1053/j.gastro.2013.12.036.
37. Summers J, Jilbert AR, Yang W, Aldrich CE, Saputelli J, Litwin S, Toll E, Mason WS. 2003. Hepatocyte turnover during resolution of a transient hepadnaviral infection. Proc Natl Acad Sci U S A 100:11652-11659. http: //dx.doi.org/10.1073/pnas.1635109100.
38. Kajino K, Jilbert AR, Saputelli J, Aldrich CE, Cullen J, Mason WS. 1994. Woodchuck hepatitis virus infections: very rapid recovery after a prolonged viremia and infection of virtually every hepatocyte. J Virol 68: 5792-5803.
39. Rehermann B, Lau D, Hoofnagle JH, Chisari FV. 1996. Cytotoxic T lymphocyte responsiveness after resolution of chronic hepatitis B virus infection. J Clin Invest 97: 1655-1665. http://dx.doi.org/10.1172 /JCI118592.
40. Guo JT, Zhou H, Liu C, Aldrich C, Saputelli J, Whitaker T, Barrasa MI, Mason WS, Seeger C. 2000. Apoptosis and regeneration of hepatocytes during recovery from transient hepadnavirus infections. J Virol 74:1495-1505. http://dx.doi.org/10.1128/JVI.74.3.1495-1505.2000.
41. Zeissig S, Murata K, Sweet L, Publicover J, Hu Z, Kaser A, Bosse E, Iqbal J, Hussain MM, Balschun K, Rocken C, Arlt A, Gunther R, Hampe J, Schreiber S, Baron JL, Moody DB, Liang TJ, Blumberg RS. Hepatitis B virus-induced lipid alterations contribute to natural killer T cell-dependent protective immunity. Nat Med 18:1060-1068. http://dx.doi.org/10.1038/nm.2811.
42. Baron JL, Gardiner L, Nishimura S, Shinkai K, Locksley R, Ganem D. 2002. Activation of a nonclassical NKT cell subset in a transgenic mouse model of hepatitis B virus infection. Immunity 16:583-594. http://dx.doi .org/10.1016/S1074-7613(02)00305-9.
43. Edlich B, Ahlenstiel G, Zabaleta Azpiroz A, Stoltzfus J, Noureddin M, Serti E, Feld JJ, Liang TJ, Rotman Y, Rehermann B. 2012. Early changes in interferon signaling define natural killer cell response and refractoriness to interferon-based therapy of hepatitis C patients. Hepatology 55:39-48. http://dx.doi.org/10.1002/hep.24628.
44. Verrier ER, Gack MU, Baumert TF. 2014. Cyclic guanosine monophosphate/ adenosine monophosphate synthase (cGAS), innate immune responses, and viral hepatitis. Hepatology 60:1098-1100. http://dx.doi.org /10.1002/hep.27187.
45. Schoggins JW, MacDuff DA, Imanaka N, Gainey MD, Shrestha B, Eitson JL, Mar KB, Richardson RB, Ratushny AV, Litvak V, Dabelic R, Manicassamy B, Aitchison JD, Aderem A, Elliott RM, Garcia-Sastre A, Racaniello V, Snijder EJ, Yokoyama WM, Diamond MS, Virgin HW, Rice CM. 2014. Pan-viral specificity of IFN-induced genes reveals new roles for cGAS in innate immunity. Nature 505:691-695. http://dx.doi .org/10.1038/nature12862.
46. Liu F, Campagna M, Qi Y, Zhao X, Guo F, Xu C, Li S, Li W, Block TM, Chang J, Guo JT. 2013. Alpha-interferon suppresses hepadnavirus transcription by altering epigenetic modification of cccDNA minichromosomes. PLoS Pathog 9:e1003613. http://dx.doi.org/10.1371/journal.ppat .1003613.
47. Lucifora J, Xia Y, Reisinger F, Zhang K, Stadler D, Cheng X, Sprinzl MF, Koppensteiner H, Makowska Z, Volz T, Remouchamps C, Chou WM, Thasler WE, Huser N, Durantel D, Liang TJ, Munk C, Heim MH, Browning JL, Dejardin E, Dandri M, Schindler M, Heikenwalder M, Protzer U. 2014. Specific and nonhepatotoxic degradation of nuclear hepatitis B virus cccDNA. Science 343:1221-1228. http://dx.doi.org/10 .1126/science.1243462.
48. Ding S, Robek MD. 2014. Cytidine deamination and cccDNA degradation: a new approach for curing HBV? Hepatology 60:2118-2121. http: //dx.doi.org/10.1002/hep.27386.
49. Yang D, Liu L, Zhu D, Peng H, Su L, Fu YX, Zhang L. 2014. A mouse model for HBV immunotolerance and immunotherapy. Cell Mol Immunol 11:71-78. http://dx.doi.org/10.1038/cmi.2013.43.
50. Bility MT, Cheng L, Zhang Z, Luan Y, Li F, Chi L, Zhang L, Tu Z, Gao Y, Fu Y, Niu J, Wang F, Su L. 2014. Hepatitis B virus infection and immunopathogenesis in a humanized mouse model: induction of humanspecific liver fibrosis and M2-like macrophages. PLoS Pathog 10: e1004032. http://dx.doi.org/10.1371/journal.ppat.1004032.
51. Guidotti LG, Matzke B, Schaller H, Chisari FV. 1995. High-level hepatitis B virus replication in transgenic mice. J Virol 69:6158-6169.
52. Li XD, Wu J, Gao D, Wang H, Sun L, Chen ZJ. 2013. Pivotal roles of cGAS-cGAMP signaling in antiviral defense and immune adjuvant effects. Science 341:1390-1394. http://dx.doi.org/10.1126/science.1244040.
53. Kanzler H, Barrat FJ, Hessel EM, Coffman RL. 2007. Therapeutic targeting of innate immunity with Toll-like receptor agonists and antagonists. Nat Med 13:552-559. http://dx.doi.org/10.1038/nm1589.
54. Horsmans Y, Berg T, Desager JP, Mueller T, Schott E, Fletcher SP, Steffy KR, Bauman LA, Kerr BM, Averett DR. 2005. Isatoribine, an agonist of TLR7, reduces plasma virus concentration in chronic hepatitis C infection. Hepatology 42:724-731. http://dx.doi.org/10.1002/hep .20839.
55. Ponnappa BC, Israel Y. 2002. Targeting Kupffer cells with antisense oligonucleotides. Front Biosci 7:e223-233. http://dx.doi.org/10.2741 /ponnappa.