Identification and biochemical characterization of halisulfate 3 and suvanine as novel inhibitors of hepatitis C virus NS3 helicase from a marine sponge

Marine Drugs

Volumn 12, Issue 1, 2014, Pages 462-476

  Furuta, Atsushi ^a,b   Salam, Kazi Abdus ^c   Hermawan, Idam ^d   Akimitsu, Nobuyoshi ^c   Tanaka, Junichi ^d   Tani, Hidenori ^b   Yamashita, Atsuya ^e   Moriishi, Kohji ^e   Nakakoshi, Masamichi ^f   Tsubuki, Masayoshi ^f   Peng, Poh Wee ^g   Suzuki, Youichi ^g   Yamamoto, Naoki ^g   Sekiguchi, Yuji ^b   Tsuneda, Satoshi ^a   Noda, Naohiro ^a,b  

^a WASEDA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d UNIVERSITY OF THE RYUKYUS   (Japan)

^e UNIVERSITY OF YAMANASHI   (Japan)

^f HOSHI UNIVERSITY   (Japan)

^g NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Dengue virus; Halisulfate 3; Hepatitis C virus; Marine organism; NS3 helicase; Suvanine

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ENZYME INHIBITOR; HALISULFATE 3; HELICASE; NONSTRUCTURAL PROTEIN 3; RNA; SERINE PROTEINASE; SUVANINE; UNCLASSIFIED DRUG;

ANTIINFLAMMATORY ACTIVITY; ANTIMICROBIAL ACTIVITY; ARTICLE; BINDING SITE; CATALYSIS; CONFORMATIONAL TRANSITION; DENGUE VIRUS; DRUG STRUCTURE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME INHIBITION; HEPATITIS C VIRUS; IC 50; NONHUMAN; RNA BINDING;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; ELECTRONS; HEPACIVIRUS; NAPHTHALENES; PORIFERA; RNA, VIRAL; SERINE PROTEASES; SERINE PROTEINASE INHIBITORS; SESTERTERPENES; SULFURIC ACID ESTERS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84892853290     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md12010462     Document Type: Article

References (47)

1. Ghany, M.G.; Nelson, D.R.; Strader, D.B.; Thomas, D.L.; Seeff, L.B. An update on treatment of genotype 1 chronic hepatitis C virus infection: 2011 practice guideline by the American Association for the Study of Liver Diseases. Hepatology 2011, 54, 1433-1444.
2. Liang, T.J.; Ghany, M.G. Current and future therapies for hepatitis C virus infection. N. Engl. J. Med. 2013, 368, 1907-1917.
3. Sarrazin, C.; Hézode, C.; Zeuzem, S.; Pawlotsky, J.-M. Antiviral strategies in hepatitis C virus infection. J. Hepatol. 2012, 56, S88-S100.
4. Scheel, T.K.H.; Rice, C.M. Understanding the hepatitis C virus life cycle paves the way for highly effective therapies. Nat. Med. 2013, 19, 837-849.
5. Lam, A.M.I.; Frick, D.N. Hepatitis C virus subgenomic replicon requires an active NS3 RNA helicase. J. Virol. 2006, 80, 404-411.
6. Kwong, A.D.; Rao, B.G.; Jeang, K.-T. Viral and cellular RNA helicases as antiviral targets. Nat. Rev. Drug Discov. 2005, 4, 845-853.
7. Bartenschlager, R.; Penin, F.; Lohmann, V.; André, P. Assembly of infectious hepatitis C virus particles. Trends Microbiol. 2011, 19, 95-103.
8. Bartenschlager, R.; Lohmann, V.; Penin, F. The molecular and structural basis of advanced antiviral therapy for hepatitis C virus infection. Nat. Rev. Microbiol. 2013, 11, 482-496.
9. Lohmann, V.; Körner, F.; Koch, J.-O.; Herian, U.; Theilmann, L.; Bartenschlager, R. Replication of subgenomic hepatitis C virus RNAs in a hepatoma cell line. Science 1999, 285, 110-113.
10. Gallinari, P.; Brennan, D.; Nardi, C.; Brunetti, M.; Tomei, L.; Steinkühler, C.; de Francesco, R. Multiple enzymatic activities associated with recombinant NS3 protein of hepatitis C virus. J. Virol. 1998, 72, 6758-6769.
11. Kim, D.W.; Gwack, Y.; Han, J.H.; Choe, J. C-terminal domain of the hepatitis C virus NS3 protein contains an RNA helicase activity. Biochem. Biophys. Res. Commun. 1995, 215, 160-166.
12. Tai, C.-L.; Chi, W.-K.; Chen, D.-S.; Hwang, L.-H. The helicase activity associated with hepatitis C virus nonstructural protein 3 (NS3). J. Virol. 1996, 70, 8477-8484.
13. Gwack, Y.; Kim, D.W.; Han, J.H.; Choe, J. Characterization of RNA binding activity and RNA helicase activity of the hepatitis C virus NS3 protein. Biochem. Biophys. Res. Commun. 1996, 225, 654-659.
14. Gwack, Y.; Kim, D.W.; Han, J.H.; Choe, J. DNA helicase activity of the hepatitis C virus nonstructural protein 3. Eur. J. Biochem. 1997, 250, 47-54.
15. Kolykhalov, A.A.; Mihalik, K.; Feinstone, S.M.; Rice, C.M. Hepatitis C virus-encoded enzymatic activities and conserved RNA elements in the 3′ nontranslated region are essential for virus replication in vivo. J. Virol. 2000, 74, 2046-2051.
16. Hall, M.C.; Matson, S.W. Helicase motifs: The engine that powers DNA unwinding. Mol. Microbiol. 1999, 34, 867-877.
17. Gorbalenya, A.E.; Koonin, E.V. Helicases: Amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 1993, 3, 419-429.
18. Jankowsky, E. RNA Helicases; Royal Society of Chemistry: London, UK, 2010; pp. 168-188.
19. Frick, D.N.; Lam, A.M.I. Understanding helicases as a means of virus control. Curr. Pharm. Des. 2006, 12, 1315-1338.
20. Borowski, P.; Deinert, J.; Schalinski, S.; Bretner, M.; Ginalski, K.; Kulikowski, T.; Shugar, D. Halogenated benzimidazoles and benzotriazoles as inhibitors of the NTPase/helicase activities of hepatitis C and related viruses. Eur. J. Biochem. 2003, 270, 1645-1653.
21. Zhang, N.; Chen, H.-M.; Koch, V.; Schmitz, H.; Liao, C.-L.; Bretner, M.; Bhadti, V.S.; Fattom, A.I.; Naso, R.B.; Hosmane, R.S.; et al. Ring-expanded ("fat") nucleoside and nucleotide analogues exhibit potent in vitro activity against Flaviviridae NTPases/helicases, including those of the West Nile virus, hepatitis C virus, and Japanese encephalitis virus. J. Med. Chem. 2003, 46, 4149-4164.
22. Borowski, P.; Heising, M.V.; Miranda, I.B.; Liao, C.-L.; Choe, J.; Baier, A. Viral NS3 helicase activity is inhibited by peptides reproducing the Arg-rich conserved motif of the enzyme (motif VI). Biochem. Pharmacol. 2008, 76, 28-38.
23. Frick, D.N.; Ginzburg, O.; Lam, A.M.I. A method to simultaneously monitor hepatitis C virus NS3 helicase and protease activities. Methods Mol. Biol. 2010, 587, 223-233.
24. Dahl, G.; Sandström, A.; Akerblom, E.; Danielson, U.H. Effects on protease inhibition by modifying of helicase residues in hepatitis C virus nonstructural protein 3. FEBS J. 2007, 274, 5979-5986.
25. Frick, D.N. The hepatitis C virus NS3 protein: A model RNA helicase and potential drug target. Curr. Issues Mol. Biol. 2007, 9, 1-20.
26. Belon, C.A.; Frick, D.N. Helicase inhibitors as specifically targeted antiviral therapy for hepatitis C. Future Virol. 2009, 4, 277-293.
27. Mayer, A.M.S.; Glaser, K.B.; Cuevas, C.; Jacobs, R.S.; Kem, W.; Little, R.D.; McIntosh, J.M.; Newman, D.J.; Potts, B.C.; Shuster, D.E. The odyssey of marine pharmaceuticals: A current pipeline perspective. Trends Pharmacol. Sci. 2010, 31, 255-265.
28. Gerwick, W.H.; Moore, B.S. Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem. Biol. 2012, 19, 85-98.
29. Newman, D.J.; Cragg, G.M. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J. Nat. Prod. 2012, 75, 311-335.
30. Furuta, A.; Salam, K.A.; Akimitsu, N.; Tanaka, J.; Tani, H.; Yamashita, A.; Moriishi, K.; Nakakoshi, M.; Tsubuki, M.; Sekiguchi, Y.; et al. Cholesterol sulfate as a potential inhibitor of hepatitis C virus NS3 helicase. J. Enzym. Inhib. Med. Chem. 2013, doi:10.3109/14756366.2013.766607.
31. Müller, E.L.; Faulkner, D.J. Absolute configuration of halisulfate 3 from the sponge Ircinia sp. Tetrahedron 1997, 53, 5373-5378.
32. Manes, L.V.; Crews, P.; Kernan, M.R.; Faulkner, D.J.; Fronczek, F.R.; Gandour, R.D. Chemistry and revised structure of suvanine. J. Org. Chem. 1988, 53, 570-575.
33. Kernan, M.R.; Faulkner, D.J. Sesterterpene sulfates from a sponge of the family Halichondriidae. J. Org. Chem. 1988, 53, 4574-4578.
34. Manes, L.V.; Naylor, S.; Crews, P.; Bakus, G.J. Suvanine, a novel sesterterpene from an Ircinia marine sponge. J. Org. Chem. 1985, 50, 284-286.
35. Kimura, J.; Ishizuka, E.; Nakao, Y.; Yoshida, W.Y.; Scheuer, P.J.; Kelly-Borges, M. Isolation of 1-methylherbipoline salts of halisulfate-1 and of suvanine as serine protease inhibitors from a marine sponge, Coscinoderma mathewsi. J. Nat. Prod. 1998, 61, 248-250.
36. Di Leva, F.S.; Festa, C.; D'Amore, C.; de Marino, S.; Renga, B.; D'Auria, M.V.; Novellino, E.; Limongelli, V.; Zampella, A.; Fiorucci, S. Binding mechanism of the farnesoid X receptor marine antagonist suvanine reveals a strategy to forestall drug modulation on nuclear receptors. Design, synthesis, and biological evaluation of novel ligands. J. Med. Chem. 2013, 56, 4701-4717.
37. Cassiano, C.; Monti, M.C.; Festa, C.; Zampella, A.; Riccio, R.; Casapullo, A. Chemical proteomics reveals heat shock protein 60 to be the main cellular target of the marine bioactive sesterterpene suvanine. ChemBioChem 2012, 13, 1953-1958.
38. Singleton, M.R.; Dillingham, M.S.; Wigley, D.B. Structure and mechanism of helicases and nucleic acid translocases. Annu. Rev. Biochem. 2007, 76, 23-50.
39. Wang, C.-C.; Huang, Z.-S.; Chiang, P.-L.; Chen, C.-T.; Wu, H.-N. Analysis of the nucleoside triphosphatase, RNA triphosphatase, and unwinding activities of the helicase domain of dengue virus NS3 protein. FEBS Lett. 2009, 583, 691-696.
40. Ndjomou, J.; Kolli, R.; Mukherjee, S.; Shadrick, W.R.; Hanson, A.M.; Sweeney, N.L.; Bartczak, D.; Li, K.; Frankowski, K.J.; Schoenen, F.J.; et al. Fluorescent primuline derivatives inhibit hepatitis C virus NS3-catalyzed RNA unwinding, peptide hydrolysis and viral replicase formation. Antivir. Res. 2012, 96, 245-255.
41. Saalau-Bethell, S.M.; Woodhead, A.J.; Chessari, G.; Carr, M.G.; Coyle, J.; Graham, B.; Hiscock, S.D.; Murray, C.W.; Pathuri, P.; Rich, S.J.; et al. Discovery of an allosteric mechanism for the regulation of HCV NS3 protein function. Nat. Chem. Biol. 2012, 8, 920-925.
42. Ding, S.C.; Kohlway, A.S.; Pyle, A.M. Unmasking the active helicase conformation of nonstructural protein 3 from hepatitis C virus. J. Virol. 2011, 85, 4343-4353.
43. Tani, H.; Akimitsu, N.; Fujita, O.; Matsuda, Y.; Miyata, R.; Tsuneda, S.; Igarashi, M.; Sekiguchi, Y.; Noda, N. High-throughput screening assay of hepatitis C virus helicase inhibitors using fluorescence-quenching phenomenon. Biochem. Biophys. Res. Commun. 2009, 379, 1054-1059.
44. Copeland, R.A. Evaluation of Enzyme Inhibitors in Drug Discovery; John Wiley & Sons: New York, NY, USA, 2005; pp. 111-140.
45. Salam, K.A.; Furuta, A.; Noda, N.; Tsuneda, S.; Sekiguchi, Y.; Yamashita, A.; Moriishi, K.; Nakakoshi, M.; Tsubuki, M.; Tani, H.; et al. Inhibition of hepatitis C virus NS3 helicase by manoalide. J. Nat. Prod. 2012, 75, 650-654.
46. Salam, K.A.; Furuta, A.; Noda, N.; Tsuneda, S.; Sekiguchi, Y.; Yamashita, A.; Moriishi, K.; Nakakoshi, M.; Tsubuki, M.; Tani, H.; et al. Psammaplin A inhibits hepatitis C virus NS3 helicase. J. Nat. Med. 2013, 67, 765-772.
47. Takahashi, H.; Takahashi, C.; Moreland, N.J.; Chang, Y.-T.; Sawasaki, T.; Ryo, A.; Vasudevan, S.G.; Suzuki, Y.; Yamamoto, N. Establishment of a robust dengue virus NS3-NS5 binding assay for identification of protein-protein interaction inhibitors. Antivir. Res. 2012, 96, 305-314.