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Current Medicinal Chemistry

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ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

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Review Article

Targeting Chikungunya Virus Entry: Alternatives for New Inhibitors in Drug Discovery

Author(s): Leandro Rocha Silva, Érica Erlanny da Silva Rodrigues, Jamile Taniele-Silva, Letícia Anderson, João Xavier de Araújo-Júnior, Ênio José Bassi and Edeildo F. da Silva-Júnior*

Volume 29, Issue 4, 2022

Published on: 23 June, 2021

Page: [612 - 634] Pages: 23

DOI: 10.2174/0929867328666210623165005

Price: $65

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Abstract

Chikungunya virus (CHIKV) is an Alphavirus (Togaviridae) responsible for Chikungunya fever (CHIKF) that is mainly characterized by a severe polyarthralgia, in which it is transmitted by the bite of infected Aedes aegypti and Ae. albopictus mosquitoes. Nowadays, there are no licensed vaccines or approved drugs to specifically treat this viral disease. Structural viral proteins participate in key steps of its replication cycle, such as viral entry, membrane fusion, nucleocapsid assembly, and virus budding. In this context, envelope E3-E2-E1 glycoproteins complex could be targeted for designing new drug candidates. In this review, aspects of the CHIKV entry mechanism are discussed to provide insights into assisting the drug discovery process. Moreover, several naturals, naturebased and synthetic compounds, as well as repurposed drugs and virtual screening are also explored as alternatives for developing CHIKV entry inhibitors. Finally, we provided a complementary analysis of studies involving inhibitors that were not explored by in silico methods. Based on this, Phe118, Val179, and Lys181 were found to be the most frequent residues, being present in 89.6, 82.7, and 93.1% of complexes, respectively. Lastly, some chemical aspects associated with interactions of these inhibitors and mature envelope E3- E2-E1 glycoproteins’ complex were discussed to provide data for scientists worldwide, supporting their search for new inhibitors against this emerging arbovirus.

Keywords: Entry inhibitors, Chikungunya virus, medicinal chemistry, drug design, repurposing, natural products, synthetic, virtual screening, molecular docking, frequency residues.

« Previous Next »
[1]
Weaver, S.C.; Forrester, N.L. Chikungunya: Evolutionary history and recent epidemic spread. Antiviral Res., 2015, 120, 32-39.
[http://dx.doi.org/10.1016/j.antiviral.2015.04.016] [PMID: 25979669]
[2]
van Aalst, M.; Nelen, C.M.; Goorhuis, A.; Stijnis, C.; Grobusch, M.P. Long-term sequelae of Chikungunya virus disease: A systematic review. Travel Med. Infect. Dis., 2017, 15, 8-22.
[http://dx.doi.org/10.1016/j.tmaid.2017.01.004] [PMID: 28163198]
[3]
Thiberville, S.D.; Moyen, N.; Dupuis-Maguiraga, L.; Nougairede, A.; Gould, E.A.; Roques, P.; de Lamballerie, X. Chikungunya fever: Epidemiology, clinical syndrome, pathogenesis and therapy. Antiviral Res., 2013, 99(3), 345-370.
[http://dx.doi.org/10.1016/j.antiviral.2013.06.009] [PMID: 23811281]
[4]
Tanabe, I.S.B.; Tanabe, E.L.L.; Santos, E.C.; Martins, W.V.; Araújo, I.M.T.C.; Cavalcante, M.C.A.; Lima, A.R.V.; Câmara, N.O.S.; Anderson, L.; Yunusov, D.; Bassi, Ê.J. Cellular and molecular immune response to Chikungunya virus infection. Front. Cell. Infect. Microbiol., 2018, 8, 345.
[http://dx.doi.org/10.3389/fcimb.2018.00345] [PMID: 30364124]
[5]
Leta, S.; Beyene, T.J.; De Clercq, E.M.; Amenu, K.; Kraemer, M.U.G.; Revie, C.W. Global risk mapping for major diseases transmitted by Aedes aegypti and Aedes albopictus. Int. J. Infect. Dis., 2018, 67, 25-35.
[http://dx.doi.org/10.1016/j.ijid.2017.11.026] [PMID: 29196275]
[6]
Ross, R.W. The Newala epidemic. III. The virus: Isolation, pathogenic properties and relationship to the epidemic. J. Hyg. (Lond.), 1956, 54(2), 177-191.
[http://dx.doi.org/10.1017/S0022172400044442] [PMID: 13346078]
[7]
Powers, A.M.; Brault, A.C.; Tesh, R.B.; Weaver, S.C. Re-emergence of Chikungunya and O’nyong-nyong viruses: Evidence for distinct geographical lineages and distant evolutionary relationships. J. Gen. Virol., 2000, 81(Pt 2), 471-479.
[PMID: 10644846]
[8]
Pyke, A.T.; Moore, P.R.; McMahon, J. New insights into Chikungunya virus emergence and spread from Southeast Asia. Emerg. Microbes Infect., 2018, 7(1), 26.
[http://dx.doi.org/10.1038/s41426-018-0024-2] [PMID: 29535302]
[9]
Wilson, M.E. Travel and the emergence of infectious diseases. Emerg. Infect. Dis., 1995, 1(2), 39-46.
[http://dx.doi.org/10.3201/eid0102.950201] [PMID: 8903157]
[10]
Yactayo, S.; Staples, J.E.; Millot, V.; Cibrelus, L.; Ramon-Pardo, P. Epidemiology of chikungunya in the americas. J. Infect. Dis., 2016, 214(Suppl. 5), S441-S445.
[http://dx.doi.org/10.1093/infdis/jiw390] [PMID: 27920170]
[11]
Brito, C.A.A. Alert: Severe cases and deaths associated with chikungunya in Brazil. Rev. Soc. Bras. Med. Trop., 2017, 50(5), 585-589.
[http://dx.doi.org/10.1590/0037-8682-0479-2016] [PMID: 29160503]
[12]
Mehta, R.; Gerardin, P.; de Brito, C.A.A.; Soares, C.N.; Ferreira, M.L.B.; Solomon, T. The neurological complications of Chikungunya virus: A systematic review. Rev. Med. Virol., 2018, 28(3)e1978
[http://dx.doi.org/10.1002/rmv.1978]
[13]
Chen, R.; Mukhopadhyay, S.; Merits, A.; Bolling, B.; Nasar, F.; Coffey, L.L.; Powers, A.; Weaver, S.C. ICTV virus taxonomy profile. Togaviridae. J. Gen. Virol., 2018, 99(6), 761-762.
[http://dx.doi.org/10.1099/jgv.0.001072] [PMID: 29745869]
[14]
Simizu, B.; Yamamoto, K.; Hashimoto, K.; Ogata, T. Structural proteins of Chikungunya virus. J. Virol., 1984, 51(1), 254-258.
[http://dx.doi.org/10.1128/JVI.51.1.254-258.1984] [PMID: 6726893]
[15]
Khan, A.H.; Morita, K.; Parquet, M.D.C.; Hasebe, F.; Mathenge, E.G.M.; Igarashi, A. Complete nucleotide sequence of Chikungunya virus and evidence for an internal polyadenylation site. J. Gen. Virol., 2002, 83(Pt 12), 3075-3084.
[http://dx.doi.org/10.1099/0022-1317-83-12-3075] [PMID: 12466484]
[16]
Rupp, J.C.; Sokoloski, K.J.; Gebhart, N.N.; Hardy, R.W. Alphavirus RNA synthesis and non-structural protein functions. J. Gen. Virol., 2015, 96(9), 2483-2500.
[http://dx.doi.org/10.1099/jgv.0.000249] [PMID: 26219641]
[17]
Metz, S.W.; Pijlman, G.P. Function of Chikungunya virus structural proteins.Chikungunya virus; Okeoma, C.M., Ed.; Springer International Publishing: Cham, 2016, pp. 63-74.
[http://dx.doi.org/10.1007/978-3-319-42958-8_5]
[18]
Subudhi, B.B.; Chattopadhyay, S.; Mishra, P.; Kumar, A. Current strategies for inhibition of chikungunya infection. Viruses, 2018, 10(5), 235.
[http://dx.doi.org/10.3390/v10050235] [PMID: 29751486]
[19]
da Silva-Júnior, E.F.; Leoncini, G.O.; Rodrigues, É.E.S.; Aquino, T.M.; Araújo-Júnior, J.X. The medicinal chemistry of Chikungunya virus. Bioorg. Med. Chem., 2017, 25(16), 4219-4244.
[http://dx.doi.org/10.1016/j.bmc.2017.06.049] [PMID: 28689975]
[20]
Gigante, A.; Gómez-SanJuan, A.; Delang, L.; Li, C.; Bueno, O.; Gamo, A.M.; Priego, E.M.; Camarasa, M.J.; Jochmans, D.; Leyssen, P.; Decroly, E.; Coutard, B.; Querat, G.; Neyts, J.; Pérez-Pérez, M.J. Antiviral activity of [1,2,3]triazolo[4,5-d]pyrimidin-7(6H)-ones against Chikungunya virus targeting the viral capping nsP1. Antiviral Res., 2017, 144, 216-222.
[http://dx.doi.org/10.1016/j.antiviral.2017.06.003] [PMID: 28619679]
[21]
Delang, L.; Li, C.; Tas, A.; Quérat, G.; Albulescu, I.C.; De Burghgraeve, T.; Guerrero, N.A.; Gigante, A.; Piorkowski, G.; Decroly, E.; Jochmans, D.; Canard, B.; Snijder, E.J.; Pérez-Pérez, M.J.; van Hemert, M.J.; Coutard, B.; Leyssen, P.; Neyts, J. The viral capping enzyme nsP1: A novel target for the inhibition of Chikungunya virus infection. Sci. Rep., 2016, 6, 31819.
[http://dx.doi.org/10.1038/srep31819] [PMID: 27545976]
[22]
Das, P.K.; Puusepp, L.; Varghese, F.S.; Utt, A.; Ahola, T.; Kananovich, D.G.; Lopp, M.; Merits, A.; Karelson, M. Design and validation of novel Chikungunya virus protease inhibitors. Antimicrob. Agents Chemother., 2016, 60(12), 7382-7395.
[http://dx.doi.org/10.1128/AAC.01421-16] [PMID: 27736770]
[23]
Kaur, P.; Thiruchelvan, M.; Lee, R.C.H.; Chen, H.; Chen, K.C.; Ng, M.L.; Chu, J.J.H. Inhibition of Chikungunya virus replication by harringtonine, a novel antiviral that suppresses viral protein expression. Antimicrob. Agents Chemother., 2013, 57(1), 155-167.
[http://dx.doi.org/10.1128/AAC.01467-12] [PMID: 23275491]
[24]
Strauss, J.H.; Strauss, E.G. The alphaviruses: Gene expression, replication, and evolution. Microbiol. Rev., 1994, 58(3), 491-562.
[http://dx.doi.org/10.1128/MR.58.3.491-562.1994] [PMID: 7968923]
[25]
Lampio, A.; Kilpeläinen, I.; Pesonen, S.; Karhi, K.; Auvinen, P.; Somerharju, P.; Kääriäinen, L. Membrane binding mechanism of an RNA virus-capping enzyme. J. Biol. Chem., 2000, 275(48), 37853-37859.
[http://dx.doi.org/10.1074/jbc.M004865200] [PMID: 10984480]
[26]
Cross, R.K. Identification of a unique guanine-7-methyltransferase in Semliki Forest virus (SFV) infected cell extracts. Virology, 1983, 130(2), 452-463.
[http://dx.doi.org/10.1016/0042-6822(83)90099-5] [PMID: 6649413]
[27]
Ahola, T.; Kääriäinen, L. Reaction in alphavirus mRNA capping: Formation of a covalent complex of nonstructural protein nsP1 with 7-methyl-GMP. Proc. Natl. Acad. Sci. USA, 1995, 92(2), 507-511.
[http://dx.doi.org/10.1073/pnas.92.2.507] [PMID: 7831320]
[28]
Abraham, R.; Hauer, D.; McPherson, R.L.; Utt, A.; Kirby, I.T.; Cohen, M.S.; Merits, A.; Leung, A.K.L.; Griffin, D.E. ADP-ribosyl-binding and hydrolase activities of the alphavirus nsP3 macrodomain are critical for initiation of virus replication. Proc. Natl. Acad. Sci. USA, 2018, 115(44), E10457-E10466.
[http://dx.doi.org/10.1073/pnas.1812130115] [PMID: 30322911]
[29]
Rubach, J.K.; Wasik, B.R.; Rupp, J.C.; Kuhn, R.J.; Hardy, R.W.; Smith, J.L. Characterization of purified Sindbis virus nsP4 RNA-dependent RNA polymerase activity in vitro. Virology, 2009, 384(1), 201-208.
[http://dx.doi.org/10.1016/j.virol.2008.10.030] [PMID: 19036396]
[30]
Tomar, S.; Hardy, R.W.; Smith, J.L.; Kuhn, R.J. Catalytic core of alphavirus nonstructural protein nsP4 possesses terminal adenylyltransferase activity. J. Virol., 2006, 80(20), 9962-9969.
[http://dx.doi.org/10.1128/JVI.01067-06] [PMID: 17005674]
[31]
Sun, S.; Xiang, Y.; Akahata, W.; Holdaway, H.; Pal, P.; Zhang, X.; Diamond, M.S.; Nabel, G.J.; Rossmann, M.G. Structural analyses at pseudo atomic resolution of Chikungunya virus and antibodies show mechanisms of neutralization. eLife, 2013, 2e00435
[http://dx.doi.org/10.7554/eLife.00435] [PMID: 23577234]
[32]
Lescar, J.; Roussel, A.; Wien, M.W.; Navaza, J.; Fuller, S.D.; Wengler, G.; Wengler, G.; Rey, F.A. The fusion glycoprotein shell of Semliki Forest virus: An icosahedral assembly primed for fusogenic activation at endosomal pH. Cell, 2001, 105(1), 137-148.
[http://dx.doi.org/10.1016/S0092-8674(01)00303-8] [PMID: 11301009]
[33]
Voss, J.E.; Vaney, M-C.; Duquerroy, S.; Vonrhein, C.; Girard-Blanc, C.; Crublet, E.; Thompson, A.; Bricogne, G.; Rey, F.A. Glycoprotein organization of Chikungunya virus particles revealed by X-ray crystallography. Nature, 2010, 468(7324), 709-712.
[http://dx.doi.org/10.1038/nature09555] [PMID: 21124458]
[34]
Li, L.; Jose, J.; Xiang, Y.; Kuhn, R.J.; Rossmann, M.G. Structural changes of envelope proteins during alphavirus fusion. Nature, 2010, 468(7324), 705-708.
[http://dx.doi.org/10.1038/nature09546] [PMID: 21124457]
[35]
Lee, S.; Owen, K.E.; Choi, H.K.; Lee, H.; Lu, G.; Wengler, G.; Brown, D.T.; Rossmann, M.G.; Kuhn, R.J. Identification of a protein binding site on the surface of the alphavirus nucleocapsid and its implication in virus assembly. Structure, 1996, 4(5), 531-541.
[http://dx.doi.org/10.1016/S0969-2126(96)00059-7] [PMID: 8736552]
[36]
Sjöberg, M.; Garoff, H. Interactions between the transmembrane segments of the alphavirus E1 and E2 proteins play a role in virus budding and fusion. J. Virol., 2003, 77(6), 3441-3450.
[http://dx.doi.org/10.1128/JVI.77.6.3441-3450.2003] [PMID: 12610119]
[37]
Uchime, O.; Fields, W.; Kielian, M. The role of E3 in pH protection during alphavirus assembly and exit. J. Virol., 2013, 87(18), 10255-10262.
[http://dx.doi.org/10.1128/JVI.01507-13] [PMID: 23864626]
[38]
Linger, B.R.; Kunovska, L.; Kuhn, R.J.; Golden, B.L. Sindbis virus nucleocapsid assembly: RNA folding promotes capsid protein dimerization. RNA, 2004, 10(1), 128-138.
[http://dx.doi.org/10.1261/rna.5127104] [PMID: 14681591]
[39]
Aliperti, G.; Schlesinger, M.J. Evidence for an autoprotease activity of sindbis virus capsid protein. Virology, 1978, 90(2), 366-369.
[http://dx.doi.org/10.1016/0042-6822(78)90321-5] [PMID: 726255]
[40]
Hahn, C.S.; Strauss, J.H. Site-directed mutagenesis of the proposed catalytic amino acids of the Sindbis virus capsid protein autoprotease. J. Virol., 1990, 64(6), 3069-3073.
[http://dx.doi.org/10.1128/JVI.64.6.3069-3073.1990] [PMID: 2335827]
[41]
Liljeström, P.; Garoff, H. Internally located cleavable signal sequences direct the formation of Semliki Forest virus membrane proteins from a polyprotein precursor. J. Virol., 1991, 65(1), 147-154.
[http://dx.doi.org/10.1128/JVI.65.1.147-154.1991] [PMID: 1985194]
[42]
Gaedigk-Nitschko, K.; Ding, M.X.; Levy, M.A.; Schlesinger, M.J. Site-directed mutations in the Sindbis virus 6K protein reveal sites for fatty acylation and the underacylated protein affects virus release and virion structure. Virology, 1990, 175(1), 282-291.
[http://dx.doi.org/10.1016/0042-6822(90)90210-I] [PMID: 2309447]
[43]
Yao, J.S.; Strauss, E.G.; Strauss, J.H. Interactions between PE2, E1, and 6K required for assembly of alphaviruses studied with chimeric viruses. J. Virol., 1996, 70(11), 7910-7920.
[http://dx.doi.org/10.1128/JVI.70.11.7910-7920.1996] [PMID: 8892914]
[44]
Loewy, A.; Smyth, J.; von Bonsdorff, C.H.; Liljeström, P.; Schlesinger, M.J. The 6-kilodalton membrane protein of Semliki Forest virus is involved in the budding process. J. Virol., 1995, 69(1), 469-475.
[http://dx.doi.org/10.1128/JVI.69.1.469-475.1995] [PMID: 7983743]
[45]
Long, K.M.; Whitmore, A.C.; Ferris, M.T.; Sempowski, G.D.; McGee, C.; Trollinger, B.; Gunn, B.; Heise, M.T. Dendritic cell immunoreceptor regulates Chikungunya virus pathogenesis in mice. J. Virol., 2013, 87(10), 5697-5706.
[http://dx.doi.org/10.1128/JVI.01611-12] [PMID: 23487448]
[46]
Klimstra, W.B.; Nangle, E.M.; Smith, M.S.; Yurochko, A.D.; Ryman, K.D. DC-SIGN and L-SIGN can act as attachment receptors for alphaviruses and distinguish between mosquito cell- and mammalian cell-derived viruses. J. Virol., 2003, 77(22), 12022-12032.
[http://dx.doi.org/10.1128/JVI.77.22.12022-12032.2003] [PMID: 14581539]
[47]
Moller-Tank, S.; Kondratowicz, A.S.; Davey, R.A.; Rennert, P.D.; Maury, W. Role of the phosphatidylserine receptor TIM-1 in enveloped-virus entry. J. Virol., 2013, 87(15), 8327-8341.
[http://dx.doi.org/10.1128/JVI.01025-13] [PMID: 23698310]
[48]
McAllister, N.; Liu, Y.; Silva, L.M.; Lentscher, A.J.; Chai, W.; Wu, N.; Griswold, K.A.; Raghunathan, K.; Vang, L.; Alexander, J.; Warfield, K.L.; Diamond, M.S.; Feizi, T.; Silva, L.A.; Dermody, T.S. Chikungunya virus strains from each genetic clade bind sulfated glycosaminoglycans as attachment factors. J. Virol., 2020, 94(24), e01500-e01520.
[http://dx.doi.org/10.1128/JVI.01500-20] [PMID: 32999033]
[49]
Holmes, A.C.; Basore, K.; Fremont, D.H.; Diamond, M.S. A molecular understanding of alphavirus entry. PLoS Pathog., 2020, 16(10)e1008876
[http://dx.doi.org/10.1371/journal.ppat.1008876] [PMID: 33091085]
[50]
Schnierle, B.S. Cellular attachment and entry factors for Chikungunya virus. Viruses, 2019, 11(11)E1078
[http://dx.doi.org/10.3390/v11111078] [PMID: 31752346]
[51]
Sahoo, B.; Chowdary, T.K. Conformational changes in Chikungunya virus E2 protein upon heparan sulfate receptor binding explain mechanism of E2-E1 dissociation during viral entry. Biosci. Rep., 2019, 39(6), 39.
[http://dx.doi.org/10.1042/BSR20191077] [PMID: 31167876]
[52]
Pirtle, E.C.; Beran, G.W. Virus survival in the environment. Rev. Sci. Tech., 1991, 10(3), 733-748.
[http://dx.doi.org/10.20506/rst.10.3.570]
[53]
Smith, T.J.; Cheng, R.H.; Olson, N.H.; Peterson, P.; Chase, E.; Kuhn, R.J.; Baker, T.S. Putative receptor binding sites on alphaviruses as visualized by cryoelectron microscopy. Proc. Natl. Acad. Sci. USA, 1995, 92(23), 10648-10652.
[http://dx.doi.org/10.1073/pnas.92.23.10648] [PMID: 7479858]
[54]
Duijl-richter, M.K.S. Van, ; Hoornweg, T.E.; Rodenhuiszybert, I.A.; Smit, J.M. Early events in Chikungunya virus infection—from virus cell binding to membrane fusion. 2015, 3647-3674.
[55]
Wintachai, P.; Wikan, N.; Kuadkitkan, A.; Jaimipuk, T.; Ubol, S.; Pulmanausahakul, R.; Auewarakul, P.; Kasinrerk, W.; Weng, W.Y.; Panyasrivanit, M.; Paemanee, A.; Kittisenachai, S.; Roytrakul, S.; Smith, D.R. Identification of prohibitin as a Chikungunya virus receptor protein. J. Med. Virol., 2012, 84(11), 1757-1770.
[http://dx.doi.org/10.1002/jmv.23403] [PMID: 22997079]
[56]
Zhang, R.; Kim, A.S.; Fox, J.M.; Nair, S.; Basore, K.; Klimstra, W.B.; Rimkunas, R.; Fong, R.H.; Lin, H.; Poddar, S.; Crowe, J.E., Jr; Doranz, B.J.; Fremont, D.H.; Diamond, M.S. Mxra8 is a receptor for multiple arthritogenic alphaviruses. Nature, 2018, 557(7706), 570-574.
[http://dx.doi.org/10.1038/s41586-018-0121-3] [PMID: 29769725]
[57]
Hoornweg, T.E.; van Duijl-Richter, M.K.S.; Ayala Nuñez, N.V.; Albulescu, I.C.; van Hemert, M.J.; Smit, J.M. Dynamics of Chikungunya virus cell entry unraveled by single-virus tracking in living cells. J. Virol., 2016, 90(9), 4745-4756.
[http://dx.doi.org/10.1128/JVI.03184-15] [PMID: 26912616]
[58]
Bernard, E.; Solignat, M.; Gay, B.; Chazal, N.; Higgs, S.; Devaux, C.; Briant, L. Endocytosis of Chikungunya virus into mammalian cells: Role of clathrin and early endosomal compartments. PLoS One, 2010, 5(7)e11479
[http://dx.doi.org/10.1371/journal.pone.0011479] [PMID: 20628602]
[59]
Lee, C.H.R.; Mohamed Hussain, K.; Chu, J.J.H. Macropinocytosis dependent entry of Chikungunya virus into human muscle cells. PLoS Negl. Trop. Dis., 2019, 13(8)e0007610
[http://dx.doi.org/10.1371/journal.pntd.0007610] [PMID: 31449523]
[60]
Meyer, W.J.; Johnston, R.E. Structural rearrangement of infecting sindbis virions at the cell surface: Mapping of newly accessible epitopes. J. Virol., 1993, 67(9), 5117-5125.
[http://dx.doi.org/10.1128/JVI.67.9.5117-5125.1993] [PMID: 7688818]
[61]
Meyer, W.J.; Gidwitz, S.; Ayers, V.K.; Schoepp, R.J.; Johnston, R.E. Conformational alteration of Sindbis virion glycoproteins induced by heat, reducing agents, or low pH. J. Virol., 1992, 66(6), 3504-3513.
[http://dx.doi.org/10.1128/JVI.66.6.3504-3513.1992] [PMID: 1374808]
[62]
Wahlberg, J.M.; Garoff, H. Membrane fusion process of Semliki Forest virus. I: Low pH-induced rearrangement in spike protein quaternary structure precedes virus penetration into cells. J. Cell Biol., 1992, 116(2), 339-348.
[http://dx.doi.org/10.1083/jcb.116.2.339] [PMID: 1370493]
[63]
Fuller, S.D.; Berriman, J.A.; Butcher, S.J.; Gowen, B.E.; Low, P.H. Low pH induces swiveling of the glycoprotein heterodimers in the Semliki Forest virus spike complex. Cell, 1995, 81(5), 715-725.
[http://dx.doi.org/10.1016/0092-8674(95)90533-2] [PMID: 7774013]
[64]
Gibbons, D.L.; Erk, I.; Reilly, B.; Navaza, J.; Kielian, M.; Rey, F.A.; Lepault, J. Visualization of the target-membrane-inserted fusion protein of Semliki Forest virus by combined electron microscopy and crystallography. Cell, 2003, 114(5), 573-583.
[http://dx.doi.org/10.1016/S0092-8674(03)00683-4] [PMID: 13678581]
[65]
Kielian, M.; Rey, F.A. Virus membrane-fusion proteins: More than one way to make a hairpin. Nat. Rev. Microbiol., 2006, 4(1), 67-76.
[http://dx.doi.org/10.1038/nrmicro1326] [PMID: 16357862]
[66]
Marsh, M.; Helenius, A. Virus entry: Open sesame. Cell, 2006, 124(4), 729-740.
[http://dx.doi.org/10.1016/j.cell.2006.02.007] [PMID: 16497584]
[67]
Raghavendhar, S.; Tripati, P.K.; Ray, P.; Patel, A.K. Evaluation of medicinal herbs for anti-chikv activity. Virology, 2019, 533, 45-49.
[http://dx.doi.org/10.1016/j.virol.2019.04.007] [PMID: 31082733]
[68]
K, S.; Purushothaman, I.; S, R. Spectral characterisation, antiviral activities, in silico ADMET and molecular docking of the compounds isolated from Tectona grandis to Chikungunya virus. Biomed. Pharmacother., 2017, 87, 302-310.
[http://dx.doi.org/10.1016/j.biopha.2016.12.069] [PMID: 28063412]
[69]
Ciesek, S.; von Hahn, T.; Colpitts, C.C.; Schang, L.M.; Friesland, M.; Steinmann, J.; Manns, M.P.; Ott, M.; Wedemeyer, H.; Meuleman, P.; Pietschmann, T.; Steinmann, E. The green tea polyphenol, epigallocatechin-3-gallate, inhibits hepatitis C virus entry. Hepatology, 2011, 54(6), 1947-1955.
[http://dx.doi.org/10.1002/hep.24610] [PMID: 21837753]
[70]
Carneiro, B.M.; Batista, M.N.; Braga, A.C.S.; Nogueira, M.L.; Rahal, P. The green tea molecule EGCG inhibits Zika virus entry. Virology, 2016, 496, 215-218.
[http://dx.doi.org/10.1016/j.virol.2016.06.012] [PMID: 27344138]
[71]
Weber, C.; Sliva, K.; von Rhein, C.; Kümmerer, B.M.; Schnierle, B.S. The green tea catechin, epigallocatechin gallate inhibits Chikungunya virus infection. Antiviral Res., 2015, 113, 1-3.
[http://dx.doi.org/10.1016/j.antiviral.2014.11.001] [PMID: 25446334]
[72]
Lu, J.W.; Hsieh, P.S.; Lin, C.C.; Hu, M.K.; Huang, S.M.; Wang, Y.M.; Liang, C.Y.; Gong, Z.; Ho, Y.J. Synergistic effects of combination treatment using EGCG and suramin against the Chikungunya virus. Biochem. Biophys. Res. Commun., 2017, 491(3), 595-602.
[http://dx.doi.org/10.1016/j.bbrc.2017.07.157] [PMID: 28760340]
[73]
von Rhein, C.; Weidner, T.; Henß, L.; Martin, J.; Weber, C.; Sliva, K.; Schnierle, B.S. Curcumin and Boswellia serrata gum resin extract inhibit chikungunya and vesicular stomatitis virus infections in vitro. Antiviral Res., 2016, 125, 51-57.
[http://dx.doi.org/10.1016/j.antiviral.2015.11.007] [PMID: 26611396]
[74]
Mounce, B.C.; Cesaro, T.; Carrau, L.; Vallet, T.; Vignuzzi, M. Curcumin inhibits Zika and Chikungunya virus infection by inhibiting cell binding. Antiviral Res., 2017, 142, 148-157.
[http://dx.doi.org/10.1016/j.antiviral.2017.03.014] [PMID: 28343845]
[75]
Lani, R.; Hassandarvish, P.; Shu, M.H.; Phoon, W.H.; Chu, J.J.H.; Higgs, S.; Vanlandingham, D.; Abu Bakar, S.; Zandi, K. Antiviral activity of selected flavonoids against Chikungunya virus. Antiviral Res., 2016, 133, 50-61.
[http://dx.doi.org/10.1016/j.antiviral.2016.07.009] [PMID: 27460167]
[76]
Oo, A.; Rausalu, K.; Merits, A.; Higgs, S.; Vanlandingham, D.; Bakar, S.A.; Zandi, K. Deciphering the potential of baicalin as an antiviral agent for Chikungunya virus infection. Antiviral Res., 2018, 150, 101-111.
[http://dx.doi.org/10.1016/j.antiviral.2017.12.012] [PMID: 29269135]
[77]
Wintachai, P.; Thuaud, F.; Basmadjian, C.; Roytrakul, S.; Ubol, S.; Désaubry, L.; Smith, D.R. Assessment of flavaglines as potential Chikungunya virus entry inhibitors. Microbiol. Immunol., 2015, 59(3), 129-141.
[http://dx.doi.org/10.1111/1348-0421.12230] [PMID: 25643977]
[78]
Kaur, R. Neetu; Mudgal, R.; Jose, J.; Kumar, P.; Tomar, S. Glycan-dependent chikungunya viral infection divulged by antiviral activity of NAG specific chi-like lectin. Virology, 2019, 526, 91-98.
[http://dx.doi.org/10.1016/j.virol.2018.10.009] [PMID: 30388630]
[79]
Albulescu, I.C.; van Hoolwerff, M.; Wolters, L.A.; Bottaro, E.; Nastruzzi, C.; Yang, S.C.; Tsay, S.C.; Hwu, J.R.; Snijder, E.J.; van Hemert, M.J. Suramin inhibits Chikungunya virus replication through multiple mechanisms. Antiviral Res., 2015, 121, 39-46.
[http://dx.doi.org/10.1016/j.antiviral.2015.06.013] [PMID: 26112648]
[80]
Kuo, S.C.; Wang, Y.M.; Ho, Y.J.; Chang, T.Y.; Lai, Z.Z.; Tsui, P.Y.; Wu, T.Y.; Lin, C.C. Suramin treatment reduces chikungunya pathogenesis in mice. Antiviral Res., 2016, 134, 89-96.
[http://dx.doi.org/10.1016/j.antiviral.2016.07.025] [PMID: 27577529]
[81]
D’hooghe, M.; Mollet, K.; De Vreese, R.; Jonckers, T.H.M.; Dams, G.; De Kimpe, N. Design, synthesis, and antiviral evaluation of purine-β-lactam and purine-aminopropanol hybrids. J. Med. Chem., 2012, 55(11), 5637-5641.
[http://dx.doi.org/10.1021/jm300383k] [PMID: 22519297]
[82]
Ching, K.C.; Kam, Y.W.; Merits, A.; Ng, L.F.P.; Chai, C.L.L. Trisubstituted thieno[3,2-b]pyrrole 5-carboxamides as potent inhibitors of alphaviruses. J. Med. Chem., 2015, 58(23), 9196-9213.
[http://dx.doi.org/10.1021/acs.jmedchem.5b01047] [PMID: 26540338]
[83]
Passos, G.F.S.; Gomes, M.G.M.; Aquino, T.M.; Araújo-Júnior, J.X.; Souza, S.J.M.; Cavalcante, J.P.M.; Santos, E.C.D.; Bassi, Ê.J.; Silva-Júnior, E.F.D. Computer-aided design, synthesis, and antiviral evaluation of novel acrylamides as potential inhibitors of e3-e2-e1 glycoproteins complex from Chikungunya virus. Pharmaceuticals (Basel), 2020, 13(7), 141.
[http://dx.doi.org/10.3390/ph13070141] [PMID: 32629969]
[84]
Wang, Y.M.; Lu, J.W.; Lin, C.C.; Chin, Y.F.; Wu, T.Y.; Lin, L.I.; Lai, Z.Z.; Kuo, S.C.; Ho, Y.J. Antiviral activities of niclosamide and nitazoxanide against Chikungunya virus entry and transmission. Antiviral Res., 2016, 135, 81-90.
[http://dx.doi.org/10.1016/j.antiviral.2016.10.003] [PMID: 27742486]
[85]
Delogu, I.; Pastorino, B.; Baronti, C.; Nougairède, A.; Bonnet, E.; de Lamballerie, X. in vitro antiviral activity of arbidol against Chikungunya virus and characteristics of a selected resistant mutant. Antiviral Res., 2011, 90(3), 99-107.
[http://dx.doi.org/10.1016/j.antiviral.2011.03.182] [PMID: 21440006]
[86]
Khan, M.; Santhosh, S.R.; Tiwari, M.; Lakshmana Rao, P.V.; Parida, M. Assessment of in vitro prophylactic and therapeutic efficacy of chloroquine against Chikungunya virus in vero cells. J. Med. Virol., 2010, 82(5), 817-824.
[http://dx.doi.org/10.1002/jmv.21663] [PMID: 20336760]
[87]
Rothan, H.A.; Bahrani, H.; Abdulrahman, A.Y.; Mohamed, Z.; Teoh, T.C.; Othman, S.; Rashid, N.N.; Rahman, N.A.; Yusof, R. Mefenamic acid in combination with ribavirin shows significant effects in reducing Chikungunya virus infection in vitro and in vivo. Antiviral Res., 2016, 127, 50-56.
[http://dx.doi.org/10.1016/j.antiviral.2016.01.006] [PMID: 26794398]
[88]
Varghese, F.S.; Rausalu, K.; Hakanen, M.; Saul, S.; Kümmerer, B.M.; Susi, P.; Merits, A.; Ahola, T. Obatoclax inhibits alphavirus membrane fusion by neutralizing the acidic environment of endocytic compartments. Antimicrob. Agents Chemother., 2017, 61(3), 61.
[http://dx.doi.org/10.1128/AAC.02227-16] [PMID: 27993855]
[89]
Rashad, A.A.; Keller, P.A. Structure based design towards the identification of novel binding sites and inhibitors for the Chikungunya virus envelope proteins. J. Mol. Graph. Model., 2013, 44, 241-252.
[http://dx.doi.org/10.1016/j.jmgm.2013.07.001] [PMID: 23911992]
[90]
Millies, B.; von Hammerstein, F.; Gellert, A.; Hammerschmidt, S.; Barthels, F.; Göppel, U.; Immerheiser, M.; Elgner, F.; Jung, N.; Basic, M.; Kersten, C.; Kiefer, W.; Bodem, J.; Hildt, E.; Windbergs, M.; Hellmich, U.A.; Schirmeister, T. Proline-based allosteric inhibitors of zika and dengue virus ns2b/ns3 proteases. J. Med. Chem., 2019, 62(24), 11359-11382.
[http://dx.doi.org/10.1021/acs.jmedchem.9b01697] [PMID: 31769670]
[91]
Kovacikova, K.; van Hemert, M.J. Small-molecule inhibitors of Chikungunya virus: Mechanisms of action and antiviral drug resistance. Antimicrob. Agents Chemother., 2020, 64(12), 64.
[http://dx.doi.org/10.1128/AAC.01788-20] [PMID: 32928738]
[92]
Agarwal, G.; Gupta, S.; Gabrani, R.; Gupta, A.; Chaudhary, V.K.; Gupta, V. Virtual screening of inhibitors against envelope glycoprotein of Chikungunya virus: A drug repositioning approach. Bioinformation, 2019, 15(6), 439-447.
[http://dx.doi.org/10.6026/97320630015439] [PMID: 31312082]
[93]
Vora, J.; Patel, S.; Sinha, S.; Sharma, S.; Srivastava, A.; Chhabria, M.; Shrivastava, N. Structure based virtual screening, 3d-qsar, molecular dynamics and admet studies for selection of natural inhibitors against structural and non-structural targets of chikungunya. J. Biomol. Struct. Dyn., 2019, 37(12), 3150-3161.
[http://dx.doi.org/10.1080/07391102.2018.1509732] [PMID: 30114965]
[94]
Montes-Grajales, D.; Puerta-Guardo, H.; Espinosa, D.A.; Harris, E.; Caicedo-Torres, W.; Olivero-Verbel, J.; Martínez-Romero, E. in silico drug repurposing for the identification of potential candidate molecules against arboviruses infection. Antiviral Res., 2020, 173104668
[http://dx.doi.org/10.1016/j.antiviral.2019.104668] [PMID: 31786251]
[95]
Silva-Junior, E.F.; Barcellos Franca, P.H.; Quintans-Junior, L.J.; Mendonca-Junior, F.J.B.; Scotti, L.; Scotti, M.T.; de Aquino, T.M.; de Araujo-Junior, J.X. Dynamic simulation, docking and dft studies applied to a set of anti-acetylcholinesterase inhibitors in the enzyme β-secretase (BACE-1): An important therapeutic target in alzheimer’s disease. Curr. Comput. Aided. Drug Des, 2017, 13(4), 266-274.
[http://dx.doi.org/10.2174/1573409913666170406150905] [PMID: 28382866]
[96]
Santana, C.C.; Silva-Júnior, E.F.; Santos, J.C.N.; Rodrigues, É.E.D.S.; da Silva, I.M.; Araújo-Júnior, J.X.; do Nascimento, T.G.; Oliveira Barbosa, L.A.; Dornelas, C.B.; Figueiredo, I.M.; Santos, J.C.C.; Grillo, L.A.M. Evaluation of guanylhydrazone derivatives as inhibitors of Candida rugosa digestive lipase: Biological, biophysical, theoretical studies and biotechnological application. Bioorg. Chem., 2019, 87, 169-180.
[http://dx.doi.org/10.1016/j.bioorg.2019.03.030] [PMID: 30889500]
[97]
Silva, M.M.; Savariz, F.C.; Silva, E.F.; De Aquino, T.M.; Sarragiotto, M.H.; Santos, J.C.C.; Figueiredo, I.M.; Silva-Júnior, E.F.; de Aquino, T.M.; Sarragiotto, M.H.; Santos, J.C.C.; Figueiredo, I.M. Interaction of β-carbolines with DNA: Spectroscopic studies, correlation with biological activity and molecular docking. J. Braz. Chem. Soc., 2016, 27, 1558-1568.
[http://dx.doi.org/10.5935/0103-5053.20160035]
[98]
Dantas, N.; de Aquino, T.M.T.M.; de Araújo-Júnior, J.X.J.X.; da Silva-Júnior, E.; Gomes, E.A.E.A.; Gomes, A.A.S.; Siqueira-Júnior, J.P.J.P.; Mendonça, Junior F.J.B. Aminoguanidine hydrazones (AGH’s) as modulators of norfloxacin resistance in Staphylococcus aureus that overexpress NorA efflux pump. Chem. Biol. Interact., 2018, 280, 8-14.
[http://dx.doi.org/10.1016/j.cbi.2017.12.009] [PMID: 29208359]
[99]
Marques, R.A.; Gomes, A.O.C.V.; de Brito, M.V.; dos Santos, A.L.P.; da Silva, G.S.; de Lima, L.B.; Nunes, F.M.; de Mattos, M.C.; de Oliveira, F.C.E.; do Ó Pessoa, C.; de Moraes, M.O.; de Fátima, Â.; Franco, L.L.; Silva, M.D.M.; Dantas, M.D.D.A.; Santos, J.C.C.; Figueiredo, I.M.; da Silva-Júnior, E.F.; de Aquino, T.M.; de Araújo-Júnior, J.X.; de Oliveira, M.C.F.; Leslie Gunatilaka, A.A. Annonalide and derivatives: Semisynthesis, cytotoxic activities and studies on interaction of annonalide with dna. J. Photochem. Photobiol. Bol. Biol., 2018, 179, 156-166.
[http://dx.doi.org/10.1016/j.jphotobiol.2018.01.016] [PMID: 29413989]
[100]
de M. Silva, M.; Macedo, T.S.; Teixeira, H.M.P.; Moreira, D.R.M.; Soares, M.B.P.; da C. Pereira, A.L.; de L. Serafim, V.; Mendonça-Júnior, F.J.B.; do Carmo A. de Lima, M.; de Moura, E.F.; de Araújo-Júnior, J.X.; de A. Dantas, M.D.; de O. O. Nascimento, E.; Maciel, T.M.S.; de Aquino, T.M.; Figueiredo, I.M.; Santos, J.C.C. Correlation between DNA/HSA-interactions and antimalarial activity of acridine derivatives: Proposing a possible mechanism of action. J. Photochem. Photobiol. Bol. Biol., 2018, 189, 165-175.
[http://dx.doi.org/10.1016/j.jphotobiol.2018.10.016] [PMID: 30366283]
[101]
Roque Marques, K.M.; do Desterro, M.R.; de Arruda, S.M.; de Araújo Neto, L.N.; do Carmo Alves de Lima, M.; de Almeida, S.M.V.; da Silva, E.C.D.; de Aquino, T.M.; da Silva-Júnior, E.F.; de Araújo-Júnior, J.X. de M Silva, M.; de A Dantas, M.D.; Santos, J.C.C.; Figueiredo, I.M.; Bazin, M.A.; Marchand, P.; da Silva, T.G.; Mendonça Junior, F.J.B. 5-nitro-thiophene-thiosemicarbazone derivatives present antitumor activity mediated by apoptosis and dna intercalation. Curr. Top. Med. Chem., 2019, 19(13), 1075-1091.
[http://dx.doi.org/10.2174/1568026619666190621120304] [PMID: 31223089]

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