Mechanistic and kinetic characterization of hepatitis C virus NS3 protein interactions with NS4A and protease inhibitors

Journal of Molecular Recognition

Volumn 24, Issue 1, 2011, Pages 60-70

  Geitmann, Matthis ^a,b   Dahl, Göran ^a,c   Danielson, U Helena ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b Beactica   (Sweden)

^c BOEHRINGER INGELHEIM RCV GMBH AND CO KG   (Austria)

Author keywords

biosensor; hepatitis C virus; inhibition; NS3; NS4A; protease; SPR

Indexed keywords

CARBAMIC ACID DERIVATIVE; CILUPREVIR; DANOPREVIR; LACTAM; MACROCYCLIC COMPOUND; NS3 PROTEIN, HEPATITIS C VIRUS; NS4 PROTEIN, HEPATITIS C VIRUS; PROTEINASE INHIBITOR; QUINOLINE DERIVATIVE; SULFONAMIDE; THIAZOLE DERIVATIVE; VIRUS PROTEIN;

ARTICLE; CHEMISTRY; DRUG EFFECT; ENZYME ACTIVATION; ENZYMOLOGY; HEPATITIS C VIRUS; HUMAN; KINETICS; METABOLISM; PROTEIN BINDING;

CARBAMATES; ENZYME ACTIVATION; HEPACIVIRUS; HUMANS; KINETICS; LACTAMS; MACROCYCLIC COMPOUNDS; PROTEASE INHIBITORS; PROTEIN BINDING; QUINOLINES; SULFONAMIDES; THIAZOLES; VIRAL NONSTRUCTURAL PROTEINS;

HEPATITIS C VIRUS; HEPATITIS C VIRUS GENOTYPE 1;

EID: 78650873843     PISSN: 09523499     EISSN: 10991352     Source Type: Journal    
DOI: 10.1002/jmr.1023     Document Type: Article

References (40)

1. Backman D, Monod M, Danielson UH, 2006. Biosensor-based screening and characterization of HIV-1 inhibitor interactions with Sap 1, Sap 2, and Sap 3 from Candida albicans. J. Biomol. Screen. 11: 165-175.
2. Barbato G, Cicero DO, Cordier F, Narjes F, Gerlach B, Sambucini S, Grzesiek S, Matassa VG, De Francesco R, Bazzo R, 2000. Inhibitor binding induces active site stabilization of the HCV NS3 protein serine protease domain. EMBO J. 19: 1195-1206.
3. Barbato G, Cicero DO, Nardi MC, Steinkühler C, Cortese R, De Francesco R, Bazzo R, 1999. The solution structure of the N-terminal proteinase domain of the hepatitis C virus (HCV) NS3 protein provides new insights into its activation and catalytic mechanism. J. Mol. Biol. 289: 371-384.
4. Beran RK, Lindenbach BD, Pyle AM, 2009. The NS4A protein of hepatitis C virus promotes RNA-coupled ATP hydrolysis by the NS3 helicase. J. Virol. 83: 3268-3275.
5. Beran RK, Pyle AM, 2008. Hepatitis C viral NS3-4A protease activity is enhanced by the NS3 helicase. J. Biol. Chem. 283: 29929-29937.
6. Bianchi E, Urbani A, Biasiol G, Brunetti M, Pessi A, De Francesco R, Steinkühler C, 1997. Complex formation between the hepatitis C virus serine protease and a synthetic NS4A cofactor peptide. Biochemistry 36: 7890-7897.
7. Brass V, Berke JM, Montserret R, Blum HE, Penin F, Moradpour D, 2008. Structural determinants for membrane association and dynamic organization of the hepatitis C virus NS3-4A complex. Proc. Natl Acad. Sci. USA 105: 14545-14550.
8. Dahl G, Gutierrez Arenas O, Danielson UH, Hepatitis C virus NS3 protease is activated by low concentrations of protease inhibitors. Biochemistry 8: 11592-11602.
9. Dahl G, Sandström A, Åkerblom E, Danielson UH, 2007a. Resistance profiling of hepatitis C virus protease inhibitors using full-length NS3. Antivir. Ther. 12: 733-740.
10. Dahl G, Sandström A, Åkerblom E, Danielson UH, 2007b. Effects on protease inhibition by modifying of helicase residues in hepatitis C virus nonstructural protein 3. FEBS J. 274: 5979-5986.
11. Eckart MR, Selby M, Masiarz F, Lee C, Berger K, Crawford K, Kuo C, Kuo G, Houghton M, Choo QL, 1993. The Hepatitis C virus encodes a serine protease involved in processing of the putative nonstructural proteins from the viral polyprotein precursor. Biochem. Biophys. Res. Commun. 192: 399-406.
12. Failla C, Tomei L, De Francesco R, 1994. Both NS3 and NS4A are required for proteolytic processing of hepatitis C virus nonstructural proteins. J. Virol. 68: 3753-3760.
13. Feld JJ, Hoofnagle JH, 2005. Mechanism of action of interferon and ribavirin in treatment of hepatitis C. Nature 436: 967-972.
14. Flores MV, Strawbridge J, Ciaramella G, Corbau R, 2009. HCV-NS3 inhibitors: Determination of their kinetic parameters and mechanism. Biochim. Biophys. Acta 1794: 1441-1448.
15. Gallo M, Pennestri M, Bottomley MJ, Barbato G, Eliseo T, Paci M, Narjes F, De Francesco R, Summa V, Koch U, Bazzo R, Cicero DO, 2009. Binding of a noncovalent inhibitor exploiting the S' region stabilizes the hepatitis C virus NS3 protease conformation in the absence of cofactor. J. Mol. Biol. 385: 1142-1155.
16. Geitmann M, Danielson UH, 2004. Studies of substrate-induced conformational changes in human cytomegalovirus protease using optical biosensor technology. Anal. Biochem. 332: 203-214.
17. Geitmann M, Unge T, Danielson UH, 2006. Interaction kinetic characterization of HIV-1 reverse transcriptase non-nucleoside inhibitor resistance. J. Med. Chem. 49: 2375-2387.
18. Huber W, Mueller F, 2006. Biomolecular interaction analysis in drug discovery using surface plasmon resonance technology. Curr. Pharm. Des. 12: 3999-4021.
19. Kim DW, Gwack Y, Han JH, Choe J, 1995. C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem. Biophys. Res. Commun. 215: 160-166.
20. Kim JL, Morgenstern KA, Lin C, Fox T, Dwyer MD, Landro JA, Chambers SP, Markland W, Lepre CA, O'Malley ET, Harbeson SL, Rice CM, Murcko MA, Caron PR, Thomson JA, 1996. Crystal structure of the hepatitis C virus NS3 protease domain complexed with a synthetic NS4A cofactor peptide. Cell 87: 343-355.
21. Landro JA, Raybuck SA, Luong YP, O'Malley ET, Harbeson SL, Morgenstern KA, Rao G, Livingston DJ, 1997. Mechanistic role of an NS4A peptide cofactor with the truncated NS3 protease of hepatitis C virus: elucidation of the NS4A stimulatory effect via kinetic analysis and inhibitor mapping. Biochemistry 36: 9340-9348.
22. Lin C, Lin K, Luong YP, Rao BG, Wei YY, Brennan DL, Fulghum JR, Hsiao HM, Ma S, Maxwell JP, Cottrell KM, Perni RB, Gates CA, Kwong AD, 2004. In vitro resistance studies of hepatitis C virus serine protease inhibitors, VX-950 and BILN 2061: structural analysis indicates different resistance mechanisms. J. Biol. Chem. 279: 17508-17514.
23. Llinás-Brunet M, Bailey M, Déziel R, Fazal G, Gorys V, Goulet S, Halmos T, Maurice R, Poirier M, Poupart M, Rancourt J, Thibeault D, Wernic D, Lamarre D, 1998. Studies on the C-terminal of hexapeptide inhibitors of the hepatitis C virus serine protease. Bioorg. Med. Chem. Lett. 8: 2719-2724.
24. Lohmann V, Körner F, Koch J, Herian U, Theilmann L, Bartenschlager R, 1999. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 285: 110-113.
25. Markgren PO, Schaal W, Hämäläinen M, Karlén A, Hallberg A, Samuelsson B, Danielson UH, 2002. Relationships between structure and interaction kinetics for HIV-1 protease inhibitors. J. Med. Chem. 45: 5430-5439.
26. Nordström H, Gossas T, Hämäläinen M, Källblad P, Nyström S, Wallberg H, Danielson UH, 2008. Identification of MMP-12 inhibitors by using biosensor-based screening of a fragment library. J. Med. Chem. 51: 3449-3459.
27. Poliakov A, Hubatsch I, Shuman CF, Stenberg G, Danielson UH, 2002. Expression and purification of recombinant full-length NS3 protease-helicase from a new variant of Hepatitis C virus. Protein Expr. Purif. 25: 363-371.
28. Poliakov A, Sandström A, Åkerblom E, Danielson UH, 2007. Mechanistic studies of electrophilic protease inhibitors of full length hepatic C virus (HCV) NS3. J. Enz. Inhib. Med. Chem. 22: 191-199.
29. Rajagopalan R, Misialek S, Stevens S, Myszka D, Brandhuber B, Ballard J, Andrews S, Seiwert S, Kossen K, 2009. Inhibition and binding kinetics of the hepatitis C virus NS3 protease inhibitor ITMN-191 reveals tight binding and slow dissociative behavior. Biochemistry 48: 2559-2568.
30. Rönn R, Gossas T, Sabnis YA, Daoud H, Åkerblom E, Danielson UH, Sandström A, 2007. Evaluation of a diverse set of potential P1 carboxylic acid bioisosteres in hepatitis C virus NS3 protease inhibitors. Bioorg. Med. Chem. 15: 4057-4068.
31. Rönn R, Sabnis YA, Gossas T, Åkerblom E, Danielson UH, Hallberg A, Johansson A, 2006. Exploration of acyl sulfonamides as carboxylic acid replacements in protease inhibitors of the hepatitis C virus full-length NS3. Bioorg. Med. Chem. 14: 544-559.
32. Rönn R, Sandström A, 2008. New developments in the discovery of agents to treat hepatitis C. Curr. Top. Med. Chem. 8: 533-562.
33. Seiwert SD, Andrews SW, Jiang Y, Serebryany V, Tan H, Kossen K, Rajagopalan PT, Misialek S, Stevens SK, Stoycheva A, Hong J, Lim SR, Qin X, Rieger R, Condroski KR, Zhang H, Do MG, Lemieux C, Hingorani GP, Hartley DP, Josey JA, Pan L, Beigelman L, Blatt LM, 2008. Preclinical characteristics of the hepatitis C virus NS3/4A protease inhibitor ITMN-191 (R7227). Antimicrob. Agents Chemother. 52: 4432-4441.
34. Shepard CW, Finelli L, Alter MJ, 2005. Global epidemiology of hepatitis C virus infection. Lancet Infect. Dis. 5: 558-567.
35. Shuman CF, Hämäläinen MD, Danielson UH, 2004a. Kinetic and thermodynamic characterization of HIV-1 protease inhibitors. J. Mol. Recognit. 17: 106-119.
36. Shuman CF, Vrang L, Danielson UH, 2004b. Improved structure-activity relationship analysis of HIV-1 protease inhibitors using interaction kinetic data. J. Med. Chem. 47: 5953-5961.
37. Summa V, 2005. VX-950 (Vertex/Mitsubishi). Curr. Opin. Investig. Drugs 6: 831-837.
38. Tomei L, Failla C, Vitale RL, Bianchi E, De Francesco R, 1996. A central hydrophobic domain of the hepatitis C virus NS4A protein is necessary and sufficient for the activation of the NS3 protease. J. Gen. Virol. 77: 1065-1070.
39. Urbani A, Biasiol G, Brunetti M, Volpari C, Di Marco S, Sollazzo M, Orru S, Piaz FD, Casbarra A, Pucci P, Nardi C, Gallinari P, De Francesco R, Steinkuhler C, 1999. Multiple determinants influence complex formation of the hepatitis C virus NS3 protease domain with its NS4A cofactor peptide. Biochemistry 38: 5206-5215.
40. Yao N, Reichert P, Taremi SS, Prosise WW, Weber PC, 1999. Molecular views of viral polyprotein processing revealed by the crystal structure of the hepatitis C virus bifunctional protease-helicase. Structure 7: 1353-1363.