Sulfamoylbenzamide derivatives inhibit the assembly of hepatitis B virus nucleocapsids

Journal of Virology

Volumn 87, Issue 12, 2013, Pages 6931-6942

  Campagna, Matthew R ^a,b   Liu, Fei ^a   Mao, Richeng ^b   Mills, Courtney ^b   Cai, Dawei ^a   Guo, Fang ^a   Zhao, Xuesen ^a   Ye, Hong ^b   Cuconati, Andrea ^b   Guo, Haitao ^a   Chang, Jinhong ^a   Xu, Xiaodong ^b   Block, Timothy M ^a,b   Guo, Ju Tao ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b BARUCH S BLUMBERG INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; BAY 41 4109; BENZAMIDE DERIVATIVE; CAPSID PROTEIN; DNA POLYMERASE; DVR 01; DVR 0104; DVR 0118; DVR 0119; DVR 0120; DVR 0121; DVR 0122; DVR 0123; DVR 0124; DVR 23; DVR 25; DVR 34; DVR 43; DVR 45; DVR 56; DVR 82; DVR 92; FLUORINE; GENOMIC RNA; LAMIVUDINE; N [1 (ALPHA CHLOROBENZYLIDENE) 2 OXO 2 (1 PIPERIDINYL)ETHYL]BENZAMIDE; SULFAMOYLBENZAMIDE DERIVATIVE; TETRACYCLINE; UNCLASSIFIED DRUG; UNINDEXED DRUG; VIRUS DNA;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL IMMORTALIZATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DNA REPLICATION; DRUG DETERMINATION; DRUG SCREENING; DRUG STRUCTURE; DUCK HEPATITIS B VIRUS; GENETIC COMPLEMENTATION; HEPATITIS B VIRUS; HEPATOMA CELL; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; INHIBITION KINETICS; LIVER CELL CULTURE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS; TRANSCRIPTION INITIATION; VIRUS ASSEMBLY; VIRUS INHIBITION; VIRUS NUCLEOCAPSID; VIRUS REPLICATION; WOODCHUCK HEPATITIS VIRUS;

ANIMALS; ANTIVIRAL AGENTS; BENZAMIDES; CELL LINE, TRANSFORMED; HEP G2 CELLS; HEPATITIS B VIRUS; HEPATITIS B VIRUS, WOODCHUCK; HEPATOCYTES; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MICE; NUCLEOCAPSID; STRUCTURE-ACTIVITY RELATIONSHIP; VIRUS ASSEMBLY; VIRUS REPLICATION;

ANIMALIA; DUCK HEPATITIS B VIRUS; HEPATITIS B VIRUS; MIRIDAE; WOODCHUCK HEPATITIS VIRUS;

EID: 84878588315     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00582-13     Document Type: Article

References (75)

1. McMahon BJ. 2005. Epidemiology and natural history of hepatitis B. Semin. Liver Dis. 25(Suppl 1):3-8.
2. Lee WM. 1997. Hepatitis B virus infection. N. Engl. J. Med. 337:1733-1745.
3. Lok AS. 2004. Prevention of hepatitis B virus-related hepatocellular carcinoma. Gastroenterology 127:S303-309.
4. Keeffe EB, Dieterich DT, Han SH, Jacobson IM, Martin P, Schiff ER, Tobias H. 2008 A treatment algorithm for the management of chronic hepatitis B virus infection in the United States: 2008 update. Clin. Gastroenterol. Hepatol. 6:1315-1341.
5. Zoulim F, Locarnini S. 2009 Hepatitis B virus resistance to nucleos- (t)ide analogues. Gastroenterology 137:1593-1608.e2. doi:10.1053/j .gastro.2009.08.063.
6. Gish R, Jia JD, Locarnini S, Zoulim F. 2012. Selection of chronic hepatitis B therapy with high barrier to resistance. Lancet Infect. Dis. 12:341-353.
7. Perrillo R. 2009. Benefits and risks of interferon therapy for hepatitis B. Hepatology 49:S103-111.
8. Janssen HL, van Zonneveld M, Senturk H, Zeuzem S, Akarca US, Cakaloglu Y, Simon C, So TM, Gerken G, de Man RA, Niesters HG, Zondervan P, Hansen B, Schalm SW. 2005. Pegylated interferon alfa-2b alone or in combination with lamivudine for HBeAg-positive chronic hepatitis B: a randomised trial. Lancet 365:123-129.
9. Lau GK, Piratvisuth T, Luo KX, Marcellin P, Thongsawat S, Cooksley G, Gane E, Fried MW, Chow WC, Paik SW, Chang WY, Berg T, Flisiak R, McCloud P, Pluck N. 2005. Peginterferon Alfa-2a, lamivudine, and the combination for HBeAg-positive chronic hepatitis B. N. Engl. J. Med. 352:2682-2695.
10. Dienstag JL. 2009. Benefits and risks of nucleoside analog therapy for hepatitis B. Hepatology 49:S112-421.
11. Wiegand J, van Bommel F, Berg T. 2010. Management of chronic hepatitis B: status and challenges beyond treatment guidelines. Semin. Liver Dis. 30:361-377.
12. Akbar SM, Hiasa Y, Mishiro S, Onji M. 2009. Treatment of hepatitis B virus-infected patients: utility of therapeutic recommendations in developing countries. Expert Opin. Pharmacother. 10:1605-1614.
13. Liaw YF. 2009. Antiviral therapy of chronic hepatitis B: opportunities and challenges in Asia. J. Hepatol. 51:403-410.
14. Peters MG. 2009. Special populations with hepatitis B virus infection. Hepatology 49:S146 -S155.
15. Este JA, Cihlar T. 2010. Current status and challenges of antiretroviral research and therapy. Antiviral Res. 85:25-33.
16. Billioud G, Pichoud C, Puerstinger G, Neyts J, Zoulim F. 2011. The main Hepatitis B virus (HBV) mutants resistant to nucleoside analogs are susceptible in vitro to non-nucleoside inhibitors of HBV replication. Antiviral Res. 92:271-276.
17. Summers J, O'Connell A, Millman I. 1975. Genome of hepatitis B virus: restriction enzyme cleavage and structure of DNA extracted from Dane particles. Proc. Natl. Acad. Sci. U. S. A. 72:4597- 4601.
18. Gerlich WH, Feitelson MA, Marion PL, Robinson WS. 1980. Structural relationships between the surface antigens of ground squirrel hepatitis virus and human hepatitis B virus. J. Virol. 36:787-795.
19. Molnar-Kimber KL, Summers J, Taylor JM, Mason WS. 1983. Protein covalently bound to minus-strand DNA intermediates of duck hepatitis B virus. J. Virol. 45:165-172.
20. Newbold JE, Xin H, Tencza M, Sherman G, Dean J, Bowden S, Locarnini S. 1995. The covalently closed duplex form of the hepadnavirus genome exists in situ as a heterogeneous population of viral minichromosomes. J. Virol. 69:3350 -3357.
21. Summers J, Mason WS. 1982. Replication of the genome of a hepatitis B-like virus by reverse transcription of an RNA intermediate. Cell 29:403-415.
22. Wang GH, Seeger C. 1993. Novel mechanism for reverse transcription in hepatitis B viruses. J. Virol. 67:6507-6512.
23. Wang GH, Seeger C. 1992. The reverse transcriptase of hepatitis B virus acts as a protein primer for viral DNA synthesis. Cell 71:663-670.
24. Seeger C, Mason WS. 2000. Hepatitis B virus biology. Microbiol. Mol. Biol. Rev. 64:51-68.
25. Ganem D, Varmus HE. 1987. The molecular biology of the hepatitis B viruses. Annu. Rev. Biochem. 56:651-693.
26. Wu TT, Coates L, Aldrich CE, Summers J, Mason WS. 1990. In hepatocytes infected with duck hepatitis B virus, the template for viral RNA synthesis is amplified by an intracellular pathway. Virology 175:255-261.
27. 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.
28. Guo H, Jiang D, Zhou T, Cuconati A, Block TM, Guo JT. 2007. Characterization of the intracellular deproteinized relaxed circular DNA of hepatitis B virus: an intermediate of covalently closed circular DNA formation. J. Virol. 81:12472-12484.
29. Mao R, Zhang J, Jiang D, Cai D, Levy JM, Cuconati A, Block TM, Guo JT, Guo H. 2011. Indoleamine 2,3-dioxygenase mediates the antiviral effect of gamma interferon against hepatitis B virus in human hepatocytederived cells. J. Virol. 85:1048-1057.
30. Summers J, Smith PM, Horwich AL. 1990. Hepadnavirus envelope proteins regulate covalently closed circular DNA amplification. J. Virol. 64:2819-2824.
31. Zoulim F, Saputelli J, Seeger C. 1994. Woodchuck hepatitis virus X protein is required for viral infection in vivo. J. Virol. 68:2026-2030.
32. Yu W, Goddard C, Clearfield E, Mills C, Xiao T, Guo H, Morrey JD, Motter NE, Zhao K, Block TM, Cuconati A, Xu X. 2011. Design, synthesis, and biological evaluation of triazolo-pyrimidine derivatives as novel inhibitors of hepatitis B virus surface antigen (HBsAg) secretion. J. Med. Chem. 54:5660-5670.
33. Dougherty AM, Guo H, Westby G, Liu Y, Simsek E, Guo JT, Mehta A, Norton P, Gu B, Block T, Cuconati A. 2007. A substituted tetrahydrotetrazolo- pyrimidine is a specific and novel inhibitor of hepatitis B virus surface antigen secretion. Antimicrob. Agents Chemother. 51:4427-4437.
34. Guo JT, Pryce M, Wang X, Barrasa MI, Hu J, Seeger C. 2003. Conditional replication of duck hepatitis B virus in hepatoma cells. J. Virol. 77:1885-1893.
35. Korba BE, Gerin JL. 1992. Use of a standardized cell culture assay to assess activities of nucleoside analogs against hepatitis B virus replication. Antiviral Res. 19:55-70.
36. Ladner SK, Otto MJ, Barker CS, Zaifert K, Wang GH, Guo JT, Seeger C, King RW. 1997. 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. 41:1715-1720.
37. Korba B.E., Milman G. 1991. A cell culture assay for compounds which inhibit hepatitis B virus replication. Antiviral Res. 15:217-228.
38. Stuyver LJ, Lostia S, Adams M, Mathew JS, Pai BS, Grier J, Tharnish PM, Choi Y, Chong Y, Choo H, Chu CK, Otto MJ, Schinazi RF. 2002. Antiviral activities and cellular toxicities of modified 2=,3=-dideoxy-2=,3=- didehydrocytidine analogues. Antimicrob. Agents Chemother. 46:3854-3860.
39. King RW, Ladner SK, Miller TJ, Zaifert K, Perni RB, Conway SC, Otto MJ. 1998. Inhibition of human hepatitis B virus replication by AT-61, a phenylpropenamide derivative, alone and in combination with (-)beta-L- 2=,3=-dideoxy-3=-thiacytidine. Antimicrob. Agents Chemother. 42:3179-3186. (Erratum, 43:726, 1999.)
40. Deres K, Schroder CH, Paessens A, Goldmann S, Hacker HJ, Weber O, Kramer T, Niewohner U, Pleiss U, Stoltefuss J, Graef E, Koletzki D, Masantschek RN, Reimann A, Jaeger R, Gross R, Beckermann B, Schlemmer KH, Haebich D, Rubsamen-Waigmann H. 2003. Inhibition of hepatitis B virus replication by drug-induced depletion of nucleocapsids. Science 299:893-896.
41. Zhou T, Guo JT, Nunes FA, Molnar-Kimber KL, Wilson JM, Aldrich CE, Saputelli J, Litwin S, Condreay LD, Seeger C, Mason WS. 2000. Combination therapy with lamivudine and adenovirus causes transient suppression of chronic woodchuck hepatitis virus infections. J. Virol. 74: 11754-11763.
42. Stray SJ, Zlotnick A. 2006. BAY 41-4109 has multiple effects on Hepatitis B virus capsid assembly. J. Mol. Recognit. 19:542-548.
43. Feld JJ, Colledge D, Sozzi V, Edwards R, Littlejohn M, Locarnini SA. 2007. The phenylpropenamide derivative AT-130 blocks HBV replication at the level of viral RNA packaging. Antiviral Res. 76:168-177.
44. Katen SP, Chirapu SR, Finn MG, Zlotnick A. 2010. Trapping of hepatitis B virus capsid assembly intermediates by phenylpropenamide assembly accelerators. ACS Chem. Biol. 5:1125-1136.
45. Nassal M. 2008. Hepatitis B viruses: reverse transcription a different way. Virus Res. 134:235-249.
46. Wang GH, Zoulim F, Leber EH, Kitson J, Seeger C. 1994. Role of RNA in enzymatic activity of the reverse transcriptase of hepatitis B viruses. J. Virol. 68:8437-8442.
47. Hu J, Seeger C. 1996. Hsp90 is required for the activity of a hepatitis B virus reverse transcriptase. Proc. Natl. Acad. Sci. U. S. A. 93:1060-1064.
48. Hu J, Toft DO, Seeger C. 1997. Hepadnavirus assembly and reverse transcription require a multi-component chaperone complex which is incorporated into nucleocapsids. EMBO J. 16:59-68.
49. Chen Y, Robinson WS, Marion PL. 1994. Selected mutations of the duckhepatitis B virus P gene RNase H domain affect both RNA packaging and priming of minus-strand DNA synthesis. J. Virol. 68:5232-5238.
50. Bartenschlager R, Schaller H. 1992. Hepadnaviral assembly is initiated by polymerase binding to the encapsidation signal in the viral RNA genome. EMBO J. 11:3413-3420.
51. Hu J, Boyer M. 2006. Hepatitis B virus reverse transcriptase and epsilon RNAsequences required for specific interaction in vitro. J. Virol. 80:2141-2150.
52. Hu J, Flores D, Toft D, Wang X, Nguyen D. 2004. Requirement of heat shock protein 90 for human hepatitis B virus reverse transcriptase function. J. Virol. 78:13122-13131.
53. Hu J, Toft D, Anselmo D, Wang X. 2002. In vitro reconstitution of functional hepadnavirus reverse transcriptase with cellular chaperone proteins. J. Virol. 76:269-279.
54. Jones SA, Boregowda R, Spratt TE, Hu J. 2012. In vitro epsilon RNAdependent protein priming activity of human hepatitis B virus polymerase. J. Virol. 86:5134-5150.
55. Ziermann R, Ganem D. 1996. Homologous and heterologous complementation of HBV and WHV capsid and polymerase functions in RNA encapsidation. Virology 219:350-356.
56. Okamoto H, Omi S, Wang Y, Imai M, Mayumi M. 1990 Transcomplementation of the C gene of human and the P gene of woodchuck hepadnaviruses. J. Gen. Virol. 71:959-963.
57. Delaney WE, IV, Yang H, Miller MD, Gibbs CS, and Xiong S. 2004. Combinations of adefovir with nucleoside analogs produce additive antiviral effects against hepatitis B virus in vitro. Antimicrob. Agents Chemother. 48:3702-3710.
58. Tenney DJ, Levine SM, Rose RE, Walsh AW, Weinheimer SP, Discotto L, Plym M, Pokornowski K, Yu CF, Angus P, Ayres A, Bartholomeusz A, Sievert W, Thompson G, Warner N, Locarnini S, Colonno RJ. 2004. Clinical emergence of entecavir-resistant hepatitis B virus requires additional substitutions in virus already resistant to Lamivudine. Antimicrob. Agents Chemother. 48:3498-3507.
59. Levine S, Hernandez D, Yamanaka G, Zhang S, Rose R, Weinheimer S, Colonno RJ. 2002. Efficacies of entecavir against lamivudine-resistant hepatitis B virus replication and recombinant polymerases in vitro. Antimicrob. Agents Chemother. 46:2525-2532.
60. Lampertico P, Liaw YF. 2012. New perspectives in the therapy of chronic hepatitis B. Gut 61(Suppl 1):i18-i24.
61. Cai D, Mills C, Yu W, Yan R, Aldrich CE, Saputelli JR, Mason WS, Xu X, Guo JT, Block TM, Cuconati A, Guo H. 2012. Identification of disubstituted sulfonamide compounds as specific inhibitors of hepatitis B virus covalently closed circular DNA formation. Antimicrob. Agents Chemother. 56:4277-4288.
62. Zhou T, Guo H, Guo JT, Cuconati A, Mehta A, Block TM. 2006. Hepatitis B virus e antigen production is dependent upon covalently closed circular (ccc) DNA in HepAD38 cell cultures and may serve as a cccDNA surrogate in antiviral screening assays. Antiviral Res. 72:116-124.
63. Lipinski CA, Lombardo F, Dominy BW, Feeney PJ. 2001. Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Adv. Drug Deliv. Rev. 46:3-26.
64. Delaney WEt., Edwards R, Colledge D, Shaw T, Furman P, Painter G, Locarnini S. 2002. Phenylpropenamide derivatives AT-61 and AT-130 inhibit replication of wild-type and lamivudine-resistant strains of hepatitis B virus in vitro. Antimicrob. Agents Chemother. 46:3057-3060.
65. Wang P, Naduthambi D, Mosley RT, Niu C, Furman PA, Otto MJ, Sofia MJ. 2011. Phenylpropenamide derivatives: anti-hepatitis B virus activity of the Z isomer, SAR and the search for novel analogs. Bioorg. Med. Chem. Lett. 21:4642-4647.
66. Stray SJ, Bourne CR, Punna S, Lewis WG, Finn MG, Zlotnick A. 2005. A heteroaryldihydropyrimidine activates and can misdirect hepatitis B virus capsid assembly. Proc. Natl. Acad. Sci. U. S. A. 102:8138-8143.
67. Nassal M. 1992. The arginine-rich domain of the hepatitis B virus core protein is required for pregenome encapsidation and productive viral positive- strand DNA synthesis but not for virus assembly. J. Virol. 66:4107-4116.
68. Kock J, Nassal M, Deres K, Blum HE, von Weizsacker F. 2004. Hepatitis B virus nucleocapsids formed by carboxy-terminally mutated core proteins contain spliced viral genomes but lack full-size DNA. J. Virol. 78: 13812-13818.
69. Lewellyn EB, Loeb DD. 2011. The arginine clusters of the carboxyterminal domain of the core protein of hepatitis B virus make pleiotropic contributions to genome replication. J. Virol. 85:1298-1309.
70. Pugh J, Zweidler A, Summers J. 1989. Characterization of the major duck hepatitis B virus core particle protein. J. Virol. 63:1371-1376.
71. Perlman DH, Berg EA, O'Connor P, Costello BCE, Hu J. 2005. Reverse transcription-associated dephosphorylation of hepadnavirus nucleocapsids. Proc. Natl. Acad. Sci. U. S. A. 102:9020-9025.
72. Lan YT, Li J, Liao W, Ou J. 1999. Roles of the three major phosphorylation sites of hepatitis B virus core protein in viral replication. Virology 259:342-348.
73. Liao W, Ou JH. 1995. Phosphorylation and nuclear localization of the hepatitis B virus core protein: significance of serine in the three repeated SPRRR motifs. J. Virol. 69:1025-1029.
74. Lewellyn EB, Loeb DD. 2011. Serine phosphoacceptor sites within the core protein of hepatitis B virus contribute to genome replication pleiotropically. PLoS One 6:e17202.
75. Lee SM, Park SG, Park E, Lee JY, Jung G. 2003. The 113th and 117th charged amino acids in the 5th alpha-helix of the HBV core protein are necessary for pgRNA encapsidation. Virus Genes 27:227-235.