Hepatitis B virus nucleocapsid uncoating: biological consequences and regulation by cellular nucleases

References

• Seeger C, Mason WS. Molecular biology of hepatitis B virus infection. Virology. 2015 May;479–480:672–686.
   PubMed Web of Science ®Google Scholar
• Tuttleman JS, Pourcel C, Summers J. Formation of the pool of covalently closed circular viral DNA in hepadnavirus-infected cells. Cell. 1986;47:451–460.
   PubMed Web of Science ®Google Scholar
• Guo JT, Guo H. Metabolism and function of hepatitis B virus cccDNA: implications for the development of cccDNA-targeting antiviral therapeutics. Antiviral Res. 2015 Oct;122:91–100.
   PubMed Web of Science ®Google Scholar
• Liang TJ, Block TM, McMahon BJ, et al. Present and future therapies of hepatitis B: from discovery to cure. Hepatology. 2015 Dec;62(6):1893–1908.
   PubMed Web of Science ®Google Scholar
• Alter H, Block T, Brown N, et al. A research agenda for curing chronic hepatitis B virus infection. Hepatology. 2018 Mar;67(3):1127–1131.
   Web of Science ®Google Scholar
• Hu J, Cheng J, Tang L, et al. Virological basis for the cure of chronic hepatitis B. ACS Infect Dis. 2019 May 10;5(5):659–674.
   PubMed Web of Science ®Google Scholar
• Gallucci L, Kann M. Nuclear import of hepatitis B virus capsids and genome. Viruses. 2017 Jan 21;9(1):21.
   Web of Science ®Google Scholar
• Guo F, Tang L, Shu S, et al. Activation of STING in hepatocytes suppresses the replication of hepatitis B virus. Antimicrob Agents Chemother. 2017 Jul 17;61(10):e00771-17.
   Web of Science ®Google Scholar
• Cai X, Chiu YH, Chen ZJ. The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling. Mol Cell. 2014 Apr 24;54(2):289–296.
   PubMed Web of Science ®Google Scholar
• Verrier ER, Yim SA, Heydmann L, et al. Hepatitis B virus evasion from cyclic guanosine monophosphate-adenosine monophosphate synthase sensing in human hepatocytes. Hepatology. 2018 Nov;68(5):1695–1709.
   Web of Science ®Google Scholar
• Cui X, Luckenbaugh L, Bruss V, et al. Alteration of mature nucleocapsid and enhancement of covalently closed circular DNA formation by hepatitis B virus core mutants defective in complete-virion formation. J Virol. 2015 Oct;89(19):10064–10072.
   Web of Science ®Google Scholar
• Guo F, Zhao Q, Sheraz M, et al. HBV core protein allosteric modulators differentially alter cccDNA biosynthesis from de novo infection and intracellular amplification pathways. PLoS Pathog. 2017 Sep 25;13(9):e1006658.
   PubMed Web of Science ®Google Scholar
• Cui X, Guo JT, Hu J. Hepatitis B virus covalently closed circular DNA formation in immortalized mouse hepatocytes associated with nucleocapsid destabilization. J Virol. 2015 Sep;89(17):9021–9028.
   Web of Science ®Google Scholar
• Ladner SK, Otto MJ, Barker CS, et al. Inducible expression of human hepatitis B virus (HBV) in stably transfected hepatoblastoma cells: a novel system for screening potential inhibitors of HBV replication. Antimicrob Agents Chemother. 1997;41(8):1715–1720.
   PubMed Web of Science ®Google Scholar
• Liu B, Tang L, Zhang X, et al. A cell-based high throughput screening assay for the discovery of cGAS-STING pathway agonists. Antiviral Res. 2017 Nov;147:37–46.
   PubMed Web of Science ®Google Scholar
• Guo H, Jiang D, Zhou T, et al. Characterization of the intracellular deproteinized relaxed circular DNA of hepatitis B virus: an intermediate of covalently closed circular DNA formation. J Virol. 2007 Nov;81(22):12472–12484.
   PubMed Web of Science ®Google Scholar
• Guo H, Xu C, Zhou T, et al. Characterization of the host factors required for hepadnavirus covalently closed circular (ccc) DNA formation. PLoS One. 2012;7(8):e43270.
   Web of Science ®Google Scholar
• Wu S, Zhao Q, Zhang P, et al. Discovery and mechanistic study of benzamide derivatives that modulate hepatitis B virus capsid assembly. J Virol. 2017 May 31;91(16):e0051917.
   Web of Science ®Google Scholar
• Sheraz M, Cheng J, Tang L, et al. Cellular DNA topoisomerases are required for the synthesis of hepatitis B virus covalently closed circular DNA. J Virol. 2019 Mar 15;93(11):e02230–18.
   PubMed Web of Science ®Google Scholar
• Chang J, Block TM, Guo JT. The innate immune response to hepatitis B virus infection: implications for pathogenesis and therapy. Antiviral Res. 2012 Dec;96(3):405–413.
   PubMed Web of Science ®Google Scholar
• Mutz P, Metz P, Lempp FA, et al. HBV bypasses the innate immune response and does not protect HCV from antiviral activity of interferon. Gastroenterology. 2018 May;154(6):1791–1804.e22.
   PubMed Web of Science ®Google Scholar
• Thomsen MK, Nandakumar R, Stadler D, et al. Lack of immunological DNA sensing in hepatocytes facilitates hepatitis B virus infection. Hepatology. 2016 Sep;64(3):746–759.
   PubMed Web of Science ®Google Scholar
• Lauterbach-Riviere L, Bergez M, Monch S, et al. Hepatitis B virus DNA is a substrate for the cGAS/STING pathway but is not sensed in infected hepatocytes. Viruses. 2020 May 29;12(6):592.
   Web of Science ®Google Scholar
• Viswanathan U, Mani N, Hu Z, et al. Targeting the multifunctional HBV core protein as a potential cure for chronic hepatitis B. Antiviral Res. 2020 Aug 17;182:104917.
   PubMed Web of Science ®Google Scholar
• Guo H, Mao R, Block TM, et al. Production and function of the cytoplasmic deproteinized relaxed circular DNA of hepadnaviruses. J Virol. 2010 Jan;84(1):387–396.
   PubMed Web of Science ®Google Scholar
• Dezhbord M, Lee S, Kim W, et al. Characterization of the molecular events of covalently closed circular DNA synthesis in de novo hepatitis B virus infection of human hepatoma cells. Antiviral Res. 2019 Mar;163:11–18.
   PubMed Web of Science ®Google Scholar
• Yan N, Regalado-Magdos AD, Stiggelbout B, et al. The cytosolic exonuclease TREX1 inhibits the innate immune response to human immunodeficiency virus type 1. Nat Immunol. 2010 Nov;11(11):1005–1013.
   PubMed Web of Science ®Google Scholar
• Wheeler LA, Trifonova RT, Vrbanac V, et al. TREX1 knockdown induces an Interferon response to HIV that delays viral infection in humanized mice. Cell Rep. 2016 May 24;15(8):1715–1727.
   Web of Science ®Google Scholar
• Sironi M, Biasin M, Forni D, et al. Genetic variability at the TREX1 locus is not associated with natural resistance to HIV-1 infection. AIDS. 2012 Jul 17;26(11):1443–1445.
   Web of Science ®Google Scholar
• Pontillo A, Girardelli M, Catamo E, et al. Polymorphisms in TREX1 and susceptibility to HIV-1 infection. Int J Immunogenet. 2013 Dec;40(6):492–494.
   Web of Science ®Google Scholar
• Kumar S, Morrison JH, Dingli D, et al. HIV-1 Activation of innate immunity depends strongly on the intracellular level of TREX1 and sensing of incomplete reverse transcription products. J Virol. 2018 Jul 31;92(16):e00001–18.
   Web of Science ®Google Scholar
• Geijtenbeek TB. Host DNase TREX1 hides HIV from DNA sensors. Nat Immunol. 2010 Nov;11(11):979–980.
   Web of Science ®Google Scholar
• Fye JM, Orebaugh CD, Coffin SR, et al. Dominant mutation of the TREX1 exonuclease gene in lupus and aicardi-goutieres syndrome. J Biol Chem. 2011 Sep 16;286(37):32373–32382.
   Web of Science ®Google Scholar
• Lehtinen DA, Harvey S, Mulcahy MJ, et al. The TREX1 double-stranded DNA degradation activity is defective in dominant mutations associated with autoimmune disease. J Biol Chem. 2008 Nov 14;283(46):31649–31656.
   PubMed Web of Science ®Google Scholar
• Petersen J, Dandri M, Mier W, et al. Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat Biotechnol. 2008 Mar;26(3):335–341.
   PubMed Web of Science ®Google Scholar
• Summers J, Smith PM, Horwich AL. Hepadnavirus envelope proteins regulate covalently closed circular DNA amplification. J Virol. 1990;64(6):2819–2824.
   PubMed Web of Science ®Google Scholar
• Ambrose Z, Aiken C. HIV-1 uncoating: connection to nuclear entry and regulation by host proteins. Virology. 2014 Apr;454-455:371–379.
   PubMed Web of Science ®Google Scholar
• Qi Y, Gao Z, Xu G, et al. DNA polymerase kappa is a key cellular factor for the formation of covalently closed circular DNA of hepatitis B virus. PLoS Pathog. 2016 Oct;12(10):e1005893.
   PubMed Web of Science ®Google Scholar
• Tang L, Sheraz M, McGrane M, et al. DNA polymerase alpha is essential for intracellular amplification of hepatitis B virus covalently closed circular DNA. PLoS Pathog. 2019 Apr;15(4):e1007742.
   PubMed Web of Science ®Google Scholar