Direct binding of a hepatitis C virus inhibitor to the viral capsid protein

PLoS ONE

Volumn 7, Issue 2, 2012, Pages

  Kota, Smitha ^a   Takahashi, Virginia ^a   Ni, Feng ^c   Snyder, John K ^c   Strosberg, A Donny ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c USA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; BIOTIN; CAPSID PROTEIN; DIMETHYL 8 (5 AMINOPHENYL) 4 BENZYL 3 OXO 1,2,3,4,7A,8 HEXAHYDROINDOLO[2,3 D][1,8]NAPHTHYRIDINE 6,7 DICARBOXYLIC ACID; SL 209; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

ANTIVIRAL ACTIVITY; ARTICLE; BIOTINYLATION; CELL LYSATE; CONTROLLED STUDY; DIMERIZATION; DRUG PENETRATION; DRUG PROTEIN BINDING; DRUG STRUCTURE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; INHIBITION KINETICS; PROTEIN ASSEMBLY; VIRUS CAPSID; VIRUS PARTICLE; VIRUS VIRULENCE; CHEMISTRY; DRUG EFFECT; FLUORESCENCE MICROSCOPY; GENETICS; IMMUNOBLOTTING; METABOLISM; PROTEIN MULTIMERIZATION; REAL TIME POLYMERASE CHAIN REACTION; TUMOR CELL LINE;

HEPATITIS B VIRUS; HEPATITIS C VIRUS; MIRIDAE;

ANTIVIRAL AGENTS; CAPSID PROTEINS; CELL LINE, TUMOR; HEPACIVIRUS; HUMANS; IMMUNOBLOTTING; MICROSCOPY, FLUORESCENCE; PROTEIN MULTIMERIZATION; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84857586532     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0032207     Document Type: Article

References (46)

1. Lavanchy D, (2011) Evolving epidemiology of hepatitis C virus. Clinical Microbiol Infect 17: 107-115.
2. Alter MJ, (2007) Epidemiology of Hepatitis C infection. World J Gastroenterol 13: 2436-2441.
3. Cristina J, Moreno-del Pilar M, Moratorio G, (2007) Hepatitis C virus genetic variability in patients undergoing antiviral therapy. Virus Research 127: 185-194.
4. Meurs EF, Breiman A, (2007) The interferon inducing pathways and the hepatitis C virus. World J Gastroenterol 13: 2446-2454.
5. Gentile I, Carleo MA, Borgia F, Castaldo G, Borgia G, (2010) The efficacy and safety of telaprevir- a new protease inhibitor against hepatitis C virus. Expert Opi Invest Drugs 19: 151-159.
6. Chen KX, Njoroge FG, (2009) A review of HCV protease inhibitors. Curr Opin Investig Drugs 10: 821-837.
7. Lamarre D, Anderson PC, Bailey M, Beaulieu P, Bolger G, Bonneau P, et al. (2003) An NS3 protease inhibitor with antiviral effects in humans infected with hepatitis C virus. Nature 426: 186-189.
8. Wang P, Chun BK, Rachakonda S, Du J, Khan N, et al. (2009) An efficient and diastereoselective synthesis of PSI-6130: a clinically efficacious inhibitor of HCV NS5B polymerase. J Org Chem 74: 6819-6824.
9. Lalezari J, Asmuth D, Vargas H, Dubuc Patrick G, Liu W, et al. (2010) The IDX-08C-003 investigator group, Antiviral Activity, Pharmacokinetics and Safety of IDX184 in Combination with Pegylated Interferon (pegIFN) and Ribavirin (RBV) in Treatment-Naive HCV Genotype 1-infected Subjects. EasL 2010. 4.15.10.
10. Ruebsam F, Tran CV, Li LS, Kim SH, Xiang AX, et al. (2009) 5,6-Dihydro-1H-pyridin-2-ones as potent inhibitors of HCV NS5B polymerase. BMCL 19: 451-458.
11. Gao M, Nettles RE, Belema M, Snyder LB, Nguyen VN, et al. (2010) Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 465: 96-100.
12. Lemm JA, O'Boyle D 2nd, Liu M, Nower PT, Colonno R, et al. (2010) Identification of hepatitis C virus NS5A inhibitors. J Virol 84: 482-491.
13. Courcambeck J, Bouzidi M, Perbost R, Jouirou B, Amrani N, et al. (2006) Resistance of hepatitis C virus to NS3-4A protease inhibitors: mechanisms of drug resistance induced by R155Q, A156T, D168A and D168V mutations. Antivir Ther 11: 847-855.
14. De Francesco R, Carfi A, (2007) Advances in the development of new therapeutic agents targeting the NS3-4A serine protease or the NS5B RNA-dependent RNA polymerase of the hepatitis C virus. Adv Drug Del Rev 59: 1242-1262.
15. Strosberg AD, Kota S, Takahashi V, Snyder JK, Mousseau G, (2010) Core as a novel viral target for Hepatitis C drugs. Viruses 2: 1734-1751.
16. Lindenbach BD, Rice CM, (2005) Unravelling hepatitis C virus replication from genome to function. Nature 436: 933-938.
17. Mousseau G, Kota S, Takahashi V, Frick DN, Strosberg AD, (2011) Dimerization-driven interaction of Hepatitis C Virus core protein with NS3 helicase. J Gen Virol 92: 101-111.
18. Boulant S, Montserret R, Hope RG, Ratinier M, Targett-Adams P, et al. (2006) Structural determinants that target the hepatitis C virus core protein to lipid droplets. J Biol Chem 281: 22236-22247.
19. Penin F, Dubuisson J, Rey FA, Moradpour D, Pawlotsky JM, (2004) Structural biology of hepatitis C virus. Hepatology 39: 5-19.
20. Blair WS, Pickford C, Irving SL, Brown DG, Anderson M, et al. (2010) HIV capsid is a tractable target for small molecule therapeutic intervention. PloSpathogens 6: e1001220 doi:10.1371/journal.ppat.1001220.
21. Kota S, Coito C, Mousseau G, Lavergne J-P, Strosberg AD, (2009) Peptide inhibitors of Hepatitis C Virus core oligomerization and virus production. J Genl Virol 90: 1319-1328.
22. Kota S, Scampavia L, Spicer T, Beeler AB, Takahashi V, et al. (2010) A homogeneous time resolved fluorescence assay for identifying inhibitors of Hepatitis C virus dimerization. Assay Drug Dev Tech 8: 96-105.
23. Ni F, Kota S, Takahashi V, Strosberg AD, Snyder JK, (2011) Potent inhibitors of hepatitis C core dimerization as new leads for anti-hepatitis C agents. BMCL 21: 2198-2202.
24. Wei W, Cai C, Kota S, Takahashi V, Strosberg AD, et al. (2009) New Small Molecule Inhibitors of Hepatitis C Virus. BMCL 19: 6926-6930.
25. Tellinghuisen TL, Marcotrigiano J, Rice CM, (2005) Structure of the zinc-binding domain of an essential component of the hepatitis C virus replicase. Nature 435: 374-379.
26. Peppard J, Glickman F, He Y, Hu SI, Doughty J, et al. (2003) Development of a high-throughput screening assay for inhibitors of aggrecan cleavage using luminescent oxygen channeling (AlphaScreen). J Biomol Screen 8: 149-156.
27. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
28. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M, et al. (2005) Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11: 791-796.
29. Zhong J, Gastaminza P, Cheng G, Kapadia S, Kato T, et al. (2005) Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 102: 9294-9299.
30. Pietschmann T, Lohmann V, Kaul A, Krieger N, Rinck G, et al. (2002) Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J Virol 76: 4008-4021.
31. Pietschmann T, Kaul A, Koutsoudakis G, Shavinskaya A, Kallis S, et al. (2006) Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci USA 103: 7408-7413.
32. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL, et al. (2005) Complete replication of hepatitis C virus in cell culture. Science 309: 623-626.
33. Miyanari Y, Atsuzawa K, Usuda N, Watashi K, Hishiki T, et al. (2007) The lipid droplet is an important organelle for hepatitis C virus production. Nature Cell Biol 9: 1089-1097.
34. Scudiero DA, Shoemaker RH, Paull KD, Monks A, Tierney S, et al. (1988) Evaluation of a Soluble Tetrazolium/Formazan Assay for Cell Growth and Drug Sensitivity in Culture Using Human and Other Tumor Cell Lines. Cancer Research 48: 4827-4833.
35. Ma Y, Yates J, Liang Y, Lemon SM, Yi M, (2008) NS3 helicase domains involved in infectious intracellular hepatitis C virus particle assembly. J Virol 82: 7624-7639.
36. Boulant S, Vanabelle C, Ebel C, Penin F, Lavergne JP, (2005) Hepatitis C virus core protein is a dimeric alpha-helical protein exhibiting membrane protein features. J Virol 79: 11353-11365.
37. Klein KC, Dellos SR, Lingappa JR, (2005) Identification of residues in the hepatitis C virus core protein that are critical for capsid assembly in a cell-free system. J Virol 79: 6814-6826.
38. Cheng G, Montero A, Gastaminza P, Whitten-Bauer C, Wieland SF, et al. (2008) A virocidal amphipathic {alpha}-helical peptide that inhibits hepatitis C virus infection in vitro. Proc Natl Acad Sci USA 105: 3088-3093.
39. Prevelige PE Jr, (2011) New approaches for antiviral targeting of HIV assembly. J Mol Biol 410: 634-640.
40. Boson B, Granio O, Bartenschlager R, Cosset F-C, (2011) A Concerted Action of Hepatitis C Virus P7 and Nonstructural Protein 2 Regulates Core Localization at the Endoplasmic Reticulum and Virus Assembly. PLoS Pathogens 7: e1002144 doi:10.1371/journal.ppat.1002144.
41. Boulant S, Targett-Adams P, McLauchlan J, (2007) Disrupting the association of hepatitis C virus core protein with lipid droplets correlates with a loss in production of infectious virus. J Gen Virol 88: 2204-2213.
42. Barba G, Harper F, Harada T, Kohara M, Goulinet S, et al. (1997) Hepatitis C virus core protein shows a cytoplasmic localization and associates to cellular lipid storage droplets. Proc Natl Acad Sci USA 94: 1200-1205.
43. Curreli F, Zhang H, Zhang X, Pyatkin I, Zagorodnikov V, et al. (2011) Virtual screening based identification of novel small-molecule inhibitors targeted to the HIV-1 capsid. BMC 19: 77-90.
44. Zlotnick A, Ceres P, Singh S, Johnson JM, (2002) A small molecule inhibits and misdirects assembly of Hepatitis B virus capsids. J Virol 76: 4848-4854.
45. Zhang H, Curreli F, Zhang X, Shattacharya S, Waheed A, et al. (2011) Antiviral activity of alpha helical stapled peptides designed from the HIV-1 capsid dimerization. Retrovirology 8: 28.
46. Fader LD, Bethell R, Bonneau P, Bos M, Bosquet Y, et al. (2011) Discovery of a 1,5 dihydrobenzo (b)(1) diazepine-2,4-dione series of inhibitors of HIV-1 capsid assembly. BMC 21: 398-404.