Design of inhibitors of influenza virus membrane fusion: Synthesis, structure-activity relationship and in vitro antiviral activity of a novel indole series

Antiviral Research

Volumn 99, Issue 2, 2013, Pages 125-135

  Brancato, Virginia ^a,c,d   Peduto, Antonella ^b   Wharton, Stephen ^a   Martin, Stephen ^a   More, Vijaykumar ^b   Di Mola, Antonia ^b   Massa, Antonio ^b   Perfetto, Brunella ^c   Donnarumma, Giovanna ^c   Schiraldi, Chiara ^c   Tufano, Maria Antonietta ^c   de Rosa, Mario ^c   Filosa, Rosanna ^b   Hay, Alan ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b UNIVERSITY OF SALERNO   (Italy)

^c SECOND UNIVERSITY OF NAPLES   (Italy)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Antiviral action; Arbidol derivatives; Differential binding to haemagglutinin; Fluorescence binding assay; Influenza haemagglutinin; PH stabilization

Indexed keywords

ANTIVIRUS AGENT; ARBIDOL; ETHYL 5 (HYDROXYMETHYL) 1 METHYL 2 (PHENYSULPHANYLMETHYL) 1H INDOLE 3 CARBOXYLATE; HEMAGGLUTININ; INDOLE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; CYTOTOXICITY TEST; DRUG CYTOTOXICITY; DRUG SYNTHESIS; IN VITRO STUDY; INFLUENZA VIRUS A; MEMBRANE FUSION; NONHUMAN; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION; VIRUS INHIBITION; VIRUS REPLICATION;

ANTIVIRAL ACTION; ARBIDOL DERIVATIVES; DIFFERENTIAL BINDING TO HAEMAGGLUTININ; FLUORESCENCE BINDING ASSAY; INFLUENZA HAEMAGGLUTININ; PH STABILIZATION;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CHO CELLS; CRICETINAE; CRICETULUS; DOGS; DRUG DESIGN; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INDOLES; INFLUENZA A VIRUS; INFLUENZA, HUMAN; MADIN DARBY CANINE KIDNEY CELLS; MEMBRANE FUSION; STRUCTURE-ACTIVITY RELATIONSHIP; VIRUS INTERNALIZATION;

EID: 84880637794     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2013.05.005     Document Type: Article

References (48)

1. Ampofo W.K., Baylor N., Cobey S., Cox N.J., Daves S., Edwards S., Ferguson N., Grohmann G., Hay A., Katz J., Kullabutr K., Lambert L., Levandowski R., Mishra A.C., Monto A., Siqueira M., Tashiro M., Waddell A.L., Wairagkar N., Wood J., Zambon M., Zhang W. Improving influenza vaccine virus selection: report of a WHO informal consultation held at WHO headquarters, Geneva, Switzerland, 14-16 June 2010. Influenza Other Respir. Viruses 2012, 6:142-152.
2. Bautista E., Chotpitayasunondh T., Gao Z., Harper S.A., Shaw M., Uyeki T.M., Zaki S.R., Hayden F.G., Hui D.S., Kettner J.D., Kumar A., Lim M., Shindo N., Penn C., Nicholson K.G. Writing committee of the WHO consultation on the clinical aspects of pandemic (H1N1) 2009 Influenza. Clinical aspects of pandemic 2009 influenza A (H1N1) virus infection. N. Engl. J. Med. 2010, 362:1708-1719.
3. Bodian D.L., Yamasaki R.B., Buswell R.L., Stearns J.F., White J.M., Kuntz I.D. Inhibition of the fusion-inducing conformational change of influenza hemagglutinin by benzoquinones and hydroquinones. Biochemistry 1993, 32:2967-2978.
4. Boriskin Y.S., Leneva I.A., Pécheur E.I., Polyak S.J. Arbidol: a broad spectrum antiviral compound that blocks viral fusion. Curr. Med. Chem. 2008, 15:997-1005.
5. Brooks M.J., Sasadeusz J.J., Tannock G.A. Antiviral chemotherapeutic agents against respiratory viruses: where are we now and what's in the pipeline?. Curr. Opin. Pulm. Med. 2004, 10:197-203.
6. Cao R., Chen H., Peng W., Ma Y., Hou X., Guan H., Liu X., Xu A. Design, synthesis and in vitro and in vivo antitumor activities of novel beta-carboline derivatives. Eur. J. Med. Chem. 2005, 3:991-1001.
7. Chai H., Zhao Y., Zhao C., Gong P. Synthesis and in vitro anti-hepatitis B virus activities of some ethyl 6-bromo-5-hydroxy-1H-indole-3-carboxylates. Bioorg. Med. Chem. 2006, 14:911-917.
8. Collins P.J., Haire L.F., Lin Y.P., Liu J., Russell R.J., Walker P.A., Martin S.R., Daniels R.S., Gregory V., Skehel J.J., Gamblin S.J., Hay A.J. Structural basis for oseltamivir resistance of influenza viruses. Vaccine 2009, 27:6317-6323.
9. Corey E.J., Brunelle J., Nicolaou K.C. A translactonization route to macrocyclic lactones. J. Am. Chem. Soc. 1977, 99:7359-7360.
10. Daniels R.S., Downie J.C., Hay A.J., Knossow M., Skehel J.J., Wang M.L., Wiley D.C. Fusion mutants of the influenza virus hemagglutinin glycoprotein. Cell 1985, 40:431-439.
11. Daniels P.S., Jeffries S., Yates P., Schild G.C., Rogers G.N., Paulson J.C., Wharton S.A., Douglas A.R., Skehel J.J., Wiley D.C. Receptor-binding and membrane-fusion properties of influenza virus variants selected using anti-haemagglutinin monoclonal antibodies. EMBO J. 1987, 5:1459-1465.
12. Das K., Aramini J.M., Ma L.C., Krug R.M., Arnold E. Structures of influenza A proteins and insights into antiviral drug targets. Nat. Struct. Mol. Biol. 2010, 17:530-538.
13. Deyde V.M., Xu X., Bright R.A., Shaw M., Smith C.B., Zhang Y., Shu Y., Gubareva L.V., Cox N.J., Klimov A.I. Surveillance of resistance to adamantanes among influenza A (H3N2) and A (H1N1) viruses isolated worldwide. J. Infect. Dis. 2007, 196:249-257.
14. Di Trani L., Savarino A., Campitelli L., Norelli S., Puzelli S., D'Ostilio D., Vignolo E., Donatelli I., Cassone A. Different pH requirements are associated with divergent inhibitory effects of chloroquine on human and avian influenza A viruses. Virol. J. 2007, 4:39.
15. Godley L., Pfeifer J., Steinhauer D., Ely B., Shaw G., Kaufmann R., Suchanek E., Pabo C., Skehel J.J., Wiley D.C., Wharton S. Introduction of intersubunit disulfide bonds in the membrane-distal region of the influenza hemagglutinin abolishes membrane fusion activity. Cell 1992, 68:635-645.
16. Gubareva L., Okomo-Adhiambo M., Deyde V., Fry A.M., Sheu T.G., Garten R., Smith D.C., Barnes J., Myrick A., Hillman M., Shaw M., Bridges C., Klimov A., Cox N. Centers for Disease Control and Prevention (CDC). Update: drug susceptibility of swine origin influenza A (H1N1) viruses. MMWR Morb. Mortal. Wkly Rep. 2009, 58:433-435.
17. Ha Y., Stevens D.J., Skehel J.J., Wiley D.C. H5 avian and H9 swine influenza virus haemagglutinin structures: possible origin of influenza subtypes. EMBO J. 2002, 21:865-875.
18. Hay, A., Collins, P.J., Russell, R.J., 2008. Antivirals and resistance. In: Klenk, H-D., Matrosovich, M. (Ed.), Avian Influenza. Stech J. Monogr. Virol. 27, 252-270.
19. Hayden F.G., Pavia A.T. Antiviral management of seasonal and pandemic influenza. J. Infect. Dis. 2006, 2:119-126.
20. Hübner H., Kraxner J., Gmeiner P. Cyanoindole derivatives as highly selective dopamine D(4) receptor partial agonists: solid-phase synthesis, binding assays, and functional experiments. J. Med. Chem. 2000, 43:4563-4569.
21. Hurt A.C., Selleck P., Komadina N., Shaw R., Brown L., Barr I.G. Susceptibility of highly pathogenic A (H5N1) avian influenza viruses to the neuraminidase inhibitors and adamantanes. Antiviral Res. 2007, 73:228-231.
22. Hurt A.C., Hardie K., Wilson N.J., Deng Y.M., Osbourn M., Gehrig N., Kelso A. Community transmission of oseltamivir-resistant A(H1N1)pdm09 influenza. N. Engl. J. Med. 2011, 365:2541-2542.
23. Leneva I.A., Russell R.J., Boriskin Y.S., Hay A.J. Characteristics of arbidol-resistant mutants of influenza virus: implications for the mechanism of anti-influenza action of arbidol. Antiviral Res. 2009, 81:132-140.
24. Ling L.M., Chow A.L., Lye D.C., Tan A.S., Krishnan P., Cui L., Win N.N., Chan M., Lim P.L., Lee C.C., Leo Y.S. Effects of early oseltamivir therapy on viral shedding in 2009 pandemic influenza A (H1N1) virus infection. Clin. Infect. Dis. 2010, 50:963-969.
25. Luo M. Influenza virus entry. Adv. Exp. Med. Biol. 2012, 726:201-221.
26. Luo G., Torri A., Harte W.E., Danetz S., Cianci C., Tiley L., Day S., Mullaney D., Yu K.L., Ouellet C., Dextraze P., Meanwell N., Colonna R., Krystal M. Molecular mechanism underlying the action of a novel fusion inhibitor of influenza A virus. J. Virol. 1997, 71:4062-4070.
27. Matrosovich M., Matrosovich T., Garten W., Klenk H.D. New low-viscosity overlay medium for viral plaque assays. Virol. J. 2006, 31:3-63.
28. Moscona A. Neuraminidase inhibitors for influenza. N. Eng. J. Med. 2005, 353:1363-1373.
29. Niesen F.H., Berglund H., Vedadi M. The use of differential scanning fluorimetry to detect ligand interactions that promote protein stability. Nat. Protoc. 2007, 2:2212-2221.
30. Palese P., Shaw M.L. Orthomyxoviridae: the viruses and their replication in Fields Virology. Fields Virology 2007, 1647-1689. Lippincott-Williams and Wilkins, Philadelphia. fifth ed. D.M. Knipe, D.E. Griffin, R.A. Lamb, S.E. Straus, P.M. Howley, M.A. Martin, B. Roizman (Eds.).
31. Pécheur E.I., Lavillette D., Alcaras F., Molle J., Boriskin Y.S., Roberts M., Cosset F.L., Polyak S.J. Biochemical mechanism of hepatitis C virus inhibition by the broad-spectrum antiviral arbidol. Biochemistry 2007, 46:6050-6059.
32. Peduto A., Massa A., Di Mola A., de Caprariis P., La Colla P., Loddo R., Altamura S., Maga G., Filosa R. 2,3-dihydro-1,2-diphenyl-substituted 4HPyridinone derivatives as new anti flaviviridae inhibitors. Chem. Biol. Drug. Des. 2011, 77:441-449.
33. Plotch S.J., O'Hara B.O., Morin J., Palant O., LaRocque J., Bloom J.D., Lang S.A., Di Grandi M.J., Bradley M., Nilakantan R., Gluzman Y. Inhibiton of influenza A virus replication by compounds interfering with the fusogenic function of the viral hemagglutinin. J. Virol. 1999, 73:140-151.
34. Roubini E., Laufer R., Gilon C., Selinger Z., Roques B.P., Chorev M. Pseudopeptide analogues of substance P and leucine enkephalinamide containing the psi (CH2O) modification: synthesis and biological activity. J. Med. Chem. 1991, 34:2430-2438.
35. Russell R.J., Kerry P.S., Stevens D.J., Steinhauer D.A., Martin S.R., Gamblin S.J., Skehel J.J. Structure of influenza hemagglutinin in complex with an inhibitor of membrane fusion. Proc. Natl. Acad. Sci. USA 2008, 105:17736-17741.
36. Sellitto G., Faruolo A., de Caprariis P., Altamura S., Paonessa G., Ciliberto G. Synthesis and anti-hepatitis C virus activity of novel ethyl 1H-indole-3-carboxylates in vitro. Bioorg. Med. Chem. 2010, 18:6143-6148.
37. Skehel J.J., Wiley D.C. Influenza haemagglutinin. Vaccine 2002, 20(Suppl. 2):51-54.
38. Steinhauer D.A., Wharton S.A., Skehel J.J., Wiley D.C. Studies of the membrane fusion activities of fusion peptide mutants of influenza virus hemagglutinin. J. Virol. 1995, 69:6643-6651.
39. Sullivan K., Kloess J., Qian C., Bell D., Hay A., Lin Y.P., Gu Y. High throughput virus plaque quantitation using a flatbed scanner. J. Virol. Methods 2012, 179:81-89.
40. Tanimori S., Ura H., Kirihata M. Copper-catalyzed synthesis of 2,3-disubstituted indoles. Eur. J. Org. Chem. 2007, 2007:3977-3980.
41. Teissier E., Zandomeneghi G., Loquet A., Lavillette D., Lavergne J.P., Montserret R., Cosset F.L., Böckmann A., Meier B.H., Penin F., Pécheur E.I. Mechanism of inhibition of enveloped virus membrane fusion by the antiviral drug arbidol. PLoS ONE 2011, 25. (e15874, 1-13).
42. Trofimov, F.A., Tsyshkova, N.G., Bogdanova, N.S., Nikolaeva, I.S., Zotova, S.A., Sakhaschik, Z.M., Padeyskaya, E.N., Fomina, A.N., Svirina, E.H., Zlydnikov, D.M., Kubar, O.I., Shvetsova, E.G., Kutchak, S.N., Peters, V.V., Bryantseva, E.A., Konoplyannikov, A.G., Surinov, B.P., Yadrovskaya, V.A., Satonova, L.S., Karpova, N.A., Savina, E.P., Savinova, E.A., Grinev, A.N., Pershin, G.N.1993 Patent number 5, 198, 552.
43. Vanderlinden E., Göktas F., Cesur Z., Froeyen M., Reed M.L., Russell C.J., Cesur N., Naesens L. Novel inhibitors of influenza virus fusion: structure-activity relationship and interaction with the viral hemagglutinin. J. Virol. 2010, 844:277-288.
44. Weinstain R., Sagi A., Karton N., Shabat D. Self-immolative comb-polymers: multiple-release of side-reporters by a single stimulus event. Chem. Eur. J. 2008, 14:6857-6961.
45. Wharton S.A., Ruigrok R.W., Martin S.R., Skehel J.J., Bayley P.M., Weis W., Wiley D.C. Conformational aspects of the acid-induced fusion mechanism of influenza virus hemagglutinin. Circular dichroism and fluorescence studies. J. Biol. Chem. 1988, 263:4474-4480.
46. Wharton S.A., Belshe R.B., Skehel J.J., Hay A.J. Role of virion M2 protein in influenza virus uncoating: specific reduction in the rate of membrane fusion between virus and liposomes by amantadine. J. Gen. Virol. 1994, 75:945-948.
47. Wright P.F., Neumann G., Kawaoka Y. Orthomyxoviruses in fields virology. Fields virology 2007, 1691-1740. Lippincott-Williams & Wilkins, Philadelphia. D.M. Knipe, D.E. Griffin, R.A. Lamb, S.E. Straus, P.M. Howley, M.A. Martin, B. Roizman (Eds.).
48. Zhan P., Wang L., Liu H., Chen X., Li X., Jiang X., Zhang Q., Liu X., Pannecouque C., Naesens L., De Clercq E., Liu A., Du G. Arylazolyl(azinyl)thioacetanilide. Part 9: synthesis and biological investigation of thiazolylthioacetamides derivatives as a novel class of potential antiviral agents. Arch. Pharm. Res. 2012, 359:75-86.