Antiviral activities of selected antimalarials against dengue virus type 2 and Zika virus

Antiviral Research

Volumn 137, Issue , 2017, Pages 141-150

  Balasubramanian, Anuradha ^a   Teramoto, Tadahisa ^a   Kulkarni, Amol A ^b   Bhattacharjee, Apurba K ^a   Padmanabhan, Radhakrishnan ^a  

^a GEORGETOWN UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HOWARD UNIVERSITY   (United States)

Author keywords

Autophagy; Cathepsin B; In silico modeling; Molecular electrostatic potentials (MEPs); Renilla luciferase reporter replicon; Stereo electronic profiles

Indexed keywords

ANTIVIRUS AGENT; GSK 369796; MEFLOQUINE; MEPACRINE; UNCLASSIFIED DRUG; AMODIAQUINE; ANTIMALARIAL AGENT; N-TERT-BUTYLISOQUINE;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; AUTOPHAGY; COMPUTER MODEL; CONTROLLED STUDY; CYTOTOXICITY ASSAY; DENGUE; DENGUE VIRUS 2; DRUG SCREENING; EC50; MOLECULAR MODEL; NONHUMAN; PHARMACOPHORE; PRIORITY JOURNAL; QUANTITATIVE ASSAY; REAL TIME POLYMERASE CHAIN REACTION; REPLICON; STATIC ELECTRICITY; VIRAL PLAQUE ASSAY; VIRUS REPLICATION; ZIKA FEVER; ZIKA VIRUS; ANALOGS AND DERIVATIVES; CHEMISTRY; COMPUTER SIMULATION; DENGUE VIRUS; DRUG DEVELOPMENT; DRUG EFFECTS; HUMAN; PHYSIOLOGY;

AMODIAQUINE; ANTIMALARIALS; ANTIVIRAL AGENTS; AUTOPHAGY; COMPUTER SIMULATION; DENGUE VIRUS; DRUG DISCOVERY; HUMANS; MEFLOQUINE; QUINACRINE; REPLICON; VIRUS REPLICATION; ZIKA VIRUS;

EID: 84999810252     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.11.015     Document Type: Article

References (55)

1. Alvarez, D.E., De Lella Ezcurra, A.L., Fucito, S., Gamarnik, A.V., Role of RNA structures present at the 3'UTR of dengue virus on translation, RNA synthesis, and viral replication. Virology 339 (2005), 200–212.
2. Apte-Sengupta, S., Sirohi, D., Kuhn, R.J., Coupling of replication and assembly in flaviviruses. Curr. Opin. Virol. 9 (2014), 134–142.
3. Barrett, A.J., Fluorimetric assays for cathepsin B and cathepsin H with methylcoumarylamide substrates. Biochem. J. 187 (1980), 909–912.
4. Bhatt, S., Gething, P.W., Brady, O.J., Messina, J.P., Farlow, A.W., Moyes, C.L., Drake, J.M., Brownstein, J.S., Hoen, A.G., Sankoh, O., Myers, M.F., George, D.B., Jaenisch, T., Wint, G.R., Simmons, C.P., Scott, T.W., Farrar, J.J., Hay, S.I., The global distribution and burden of dengue. Nature 496 (2013), 504–507.
5. Boonnak, K., Dambach, K.M., Donofrio, G.C., Tassaneetrithep, B., Marovich, M.A., Cell type specificity and host genetic polymorphisms influence antibody-dependent enhancement of dengue virus infection. J. Virol. 85 (2011), 1671–1683.
6. Boonyasuppayakorn, S., Reichert, E.D., Manzano, M., Nagarajan, K., Padmanabhan, R., Amodiaquine, an antimalarial drug, inhibits dengue virus type 2 replication and infectivity. Antivir. Res. 106 (2014), 125–134.
7. Dejnirattisai, W., Jumnainsong, A., Onsirisakul, N., Fitton, P., Vasanawathana, S., Limpitikul, W., Puttikhunt, C., Edwards, C., Duangchinda, T., Supasa, S., Chawansuntati, K., Malasit, P., Mongkolsapaya, J., Screaton, G., Cross-reacting antibodies enhance dengue virus infection in humans. Science 328 (2010), 745–748.
8. Diamond, M.S., Edgil, D., Roberts, T.G., Lu, B., Harris, E., Infection of human cells by dengue virus is modulated by different cell types and viral strains. J. Virol. 74 (2000), 7814–7823.
9. Diamond, M.S., Zachariah, M., Harris, E., Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA. Virology 304 (2002), 211–221.
10. Duffy, M.R., Chen, T.H., Hancock, W.T., Powers, A.M., Kool, J.L., Lanciotti, R.S., Pretrick, M., Marfel, M., Holzbauer, S., Dubray, C., Guillaumot, L., Griggs, A., Bel, M., Lambert, A.J., Laven, J., Kosoy, O., Panella, A., Biggerstaff, B.J., Fischer, M., Hayes, E.B., Zika virus outbreak on Yap island, Federated States of Micronesia. N. Engl. J. Med. 360 (2009), 2536–2543.
11. Durbin, A.P., McArthur, J., Marron, J.A., Blaney, J.E. Jr., Thumar, B., Wanionek, K., Murphy, B.R., Whitehead, S.S., The live attenuated dengue serotype 1 vaccine rDEN1Delta30 is safe and highly immunogenic in healthy adult volunteers. Hum. Vaccin 2 (2006), 167–173.
12. Fink, K., Shi, P.Y., Live attenuated vaccine: the first clinically approved dengue vaccine?. Expert Rev. Vaccines 13 (2014), 185–188.
13. Fischl, W., Bartenschlager, R., Exploitation of cellular pathways by Dengue virus. Curr. Opin. Microbiol. 14 (2011), 470–475.
14. Haddow, A.J., Williams, M.C., Woodall, J.P., Simpson, D.I., Goma, L.K., Twelve isolations of Zika virus from Aedes (stegomyia) africanus (theobald) taken in and above a Uganda forest. Bull. World Health Organ 31 (1964), 57–69.
15. Halstead, S.B., Heinz, F.X., Barrett, A.D., Roehrig, J.T., Dengue virus: molecular basis of cell entry and pathogenesis, 25-27 June 2003, Vienna, Austria. Vaccine 23 (2005), 849–856.
16. Hancock, W.T., Marfel, M., Bel, M., Zika virus, French Polynesia, south Pacific, 2013. Emerg. Infect. Dis., 20, 2014, 1960.
17. Heaton, N.S., Randall, G., Dengue virus and autophagy. Viruses 3 (2011), 1332–1341.
18. Hennessey, M., Fischer, M., Staples, J.E., Zika Virus Spreads to New Areas - Region of the Americas, May 2015-January 2016, vol. 65, 2016, MMWR Morb Mortal Wkly Rep, 55–58.
19. Jackson, W.T., Giddings, T.H. Jr., Taylor, M.P., Mulinyawe, S., Rabinovitch, M., Kopito, R.R., Kirkegaard, K., Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol., 3, 2005, e156.
20. Jounai, N., Takeshita, F., Kobiyama, K., Sawano, A., Miyawaki, A., Xin, K.Q., Ishii, K.J., Kawai, T., Akira, S., Suzuki, K., Okuda, K., The Atg5 Atg12 conjugate associates with innate antiviral immune responses. Proc. Natl. Acad. Sci. U. S. A. 104 (2007), 14050–14055.
21. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., Yoshimori, T., LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19 (2000), 5720–5728.
22. Khakpoor, A., Panyasrivanit, M., Wikan, N., Smith, D.R., A role for autophagolysosomes in dengue virus 3 production in HepG2 cells. J. Gen. Virol. 90 (2009), 1093–1103.
23. Klema, V.J., Padmanabhan, R., Choi, K.H., Flaviviral replication complex: coordination between RNA synthesis and 5’-RNA capping. Viruses 7 (2015), 4640–4656.
24. Lam, S.K., Challenges in reducing dengue burden; diagnostics, control measures and vaccines. Expert Rev. Vaccines 12 (2013), 995–1010.
25. Lazear, H.M., Diamond, M.S., Zika virus: new clinical syndromes and its emergence in the western hemisphere. J. Virol. 90:10 (2016), 4864–4875, 10.1128/JVI.00252-16 Print 2016 May 15.
26. Lee, Y.R., Lei, H.Y., Liu, M.T., Wang, J.R., Chen, S.H., Jiang-Shieh, Y.F., Lin, Y.S., Yeh, T.M., Liu, C.C., Liu, H.S., Autophagic machinery activated by dengue virus enhances virus replication. Virology 374 (2008), 240–248.
27. Lin, C., Amberg, S.M., Chambers, T.J., Rice, C.M., Cleavage at a novel site in the NS4A region by the yellow fever virus NS2B-3 proteinase is a prerequisite for processing at the downstream 4A/4B signalase site. J. Virol. 67 (1993), 2327–2335.
28. Lindenbach, D., Thiel, H.J., Rice, C., Flaviviridae: the viruses and their replication. Knipe, D.M., Howley, P.M., (eds.) Field's Virology, 5 ed., 2007, Lippincott-Raven Publishers, Philadelphia, 1101–1152.
29. Mackenzie, A.H., Pharmacologic actions of 4-aminoquinoline compounds. Am. J. Med. 75 (1983), 5–10.
30. Manzano, M., Reichert, E.D., Polo, S., Falgout, B., Kasprzak, W., Shapiro, B.A., Padmanabhan, R., Identification of cis-acting elements in the 3'-untranslated region of the dengue virus type 2 RNA that modulate translation and replication. J. Biol. Chem. 286 (2011), 22521–22534.
31. Miorin, L., Maiuri, P., Marcello, A., Visual detection of Flavivirus RNA in living cells. Methods 98 (2015), 82–90, 10.1016/j.ymeth.2015.11.002.
32. Mitka, M., Dengue more prevalent than previously thought. JAMA, 309, 2013, 1882.
33. Mizushima, N., Yoshimori, T., Levine, B., Methods in mammalian autophagy research. Cell 140 (2010), 313–326.
34. Nakatogawa, H., Ichimura, Y., Ohsumi, Y., Atg8, a ubiquitin-like protein required for autophagosome formation, mediates membrane tethering and hemifusion. Cell 130 (2007), 165–178.
35. Ng, C.Y., Gu, F., Phong, W.Y., Chen, Y.L., Lim, S.P., Davidson, A., Vasudevan, S.G., Construction and characterization of a stable subgenomic dengue virus type 2 replicon system for antiviral compound and siRNA testing. Antivir. Res. 76 (2007), 222–231.
36. O'Neill, P.M., Barton, V.E., Ward, S.A., Chadwick, J., 4-aminoquinolines: chloroquine, amodiaquine and next-generation analogues. Staines, H.M., Krishna, S., (eds.) Treatment and Prevention of Malaria, 2012, Springer Basel AG, 10.1007/978-3-0346-0480-2_2.
37. O'Neill, P.M., Mukhtar, A., Stocks, P.A., Randle, L.E., Hindley, S., Ward, S.A., Storr, R.C., Bickley, J.F., O'Neil, I.A., Maggs, J.L., Hughes, R.H., Winstanley, P.A., Bray, P.G., Park, B.K., Isoquine and related amodiaquine analogues: a new generation of improved 4-aminoquinoline antimalarials. J. Med. Chem. 46 (2003), 4933–4945.
38. O'Neill, P.M., Park, B.K., Shone, A.E., Maggs, J.L., Roberts, P., Stocks, P.A., Biagini, G.A., Bray, P.G., Gibbons, P., Berry, N., Winstanley, P.A., Mukhtar, A., Bonar-Law, R., Hindley, S., Bambal, R.B., Davis, C.B., Bates, M., Hart, T.K., Gresham, S.L., Lawrence, R.M., Brigandi, R.A., Gomez-delas-Heras, F.M., Gargallo, D.V., Ward, S.A., Candidate selection and preclinical evaluation of N-tert-butyl isoquine (GSK369796), an affordable and effective 4-aminoquinoline antimalarial for the 21st century. J. Med. Chem. 52 (2009), 1408–1415.
39. Oehler, E., Watrin, L., Larre, P., Leparc-Goffart, I., Lastere, S., Valour, F., Baudouin, L., Mallet, H., Musso, D., Ghawche, F., Zika virus infection complicated by Guillain-Barre syndrome–case report. French Polynesia, December 2013. Euro Surveill 19, 2014.
40. Padmanabhan, R., Strongin, A.Y., Translation and processing of the dengue virus polyprotein. Hanley, K.A., Weaver, S.C., (eds.) Frontiers in Dengue Virus Research, 2010, Caister Academic Press, Norfolk, U.K, 14–33.
41. Padmanabhan, R., Takhampunya, R., Teramoto, T., Choi, K.H., Flavivirus RNA synthesis in vitro. Methods 91 (2015), 20–34.
42. Panyasrivanit, M., Khakpoor, A., Wikan, N., Smith, D.R., Co-localization of constituents of the dengue virus translation and replication machinery with amphisomes. J. Gen. Virol. 90 (2009), 448–456.
43. Pungercar, J.R., Caglic, D., Sajid, M., Dolinar, M., Vasiljeva, O., Pozgan, U., Turk, D., Bogyo, M., Turk, V., Turk, B., Autocatalytic processing of procathepsin B is triggered by proenzyme activity. FEBS J. 276 (2009), 660–668.
44. Qiao, S., Tao, S., Rojo de la Vega, M., Park, S.L., Vonderfecht, A.A., Jacobs, S.L., Zhang, D.D., Wondrak, G.T., The antimalarial amodiaquine causes autophagic-lysosomal and proliferative blockade sensitizing human melanoma cells to starvation- and chemotherapy-induced cell death. Autophagy 9 (2013), 2087–2102.
45. Roosendaal, J., Westaway, E.G., Khromykh, A., Mackenzie, J.M., Regulated cleavages at the West Nile virus NS4A-2K-NS4B junctions play a major role in rearranging cytoplasmic membranes and Golgi trafficking of the NS4A protein. J. Virol. 80 (2006), 4623–4632.
46. Rubinsztein, D.C., Codogno, P., Levine, B., Autophagy modulation as a potential therapeutic target for diverse diseases. Nat. Rev. Drug Discov. 11 (2012), 709–730.
47. Samsa, M.M., Mondotte, J.A., Iglesias, N.G., Assuncao-Miranda, I., Barbosa-Lima, G., Da Poian, A.T., Bozza, P.T., Gamarnik, A.V., Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog., 5, 2009, e1000632.
48. Steinman, R.M., Mellman, I.S., Muller, W.A., Cohn, Z.A., Endocytosis and the recycling of plasma membrane. J. Cell Biol. 96 (1983), 1–27.
49. Subramani, S., Farre, J.C., A ubiquitin-like protein involved in membrane fusion. Cell 130 (2007), 18–20.
50. Takhampunya, R., Ubol, S., Houng, H.S., Cameron, C.E., Padmanabhan, R., Inhibition of dengue virus replication by mycophenolic acid and ribavirin. J. Gen. Virol. 87 (2006), 1947–1952.
51. Teramoto, T., Chiang, H.S., Takhampunya, R., Manzano, M., Padmanabhan, R., Maric, M., Gamma interferon-inducible lysosomal thioreductase (GILT) ablation renders mouse fibroblasts sensitive to dengue virus replication. Virology, 2013.
52. Tomasi, J., Mennucci, B., Cammi, R., Quantum mechanical continuum solvation models. Chem. Rev. 105 (2005), 2999–3093.
53. Villar, L., Dayan, G.H., Arredondo-Garcia, J.L., Rivera, D.M., Cunha, R., Deseda, C., Reynales, H., Costa, M.S., Morales-Ramirez, J.O., Carrasquilla, G., Rey, L.C., Dietze, R., Luz, K., Rivas, E., Miranda Montoya, M.C., Cortes Supelano, M., Zambrano, B., Langevin, E., Boaz, M., Tornieporth, N., Saville, M., Noriega, F., Group, C.Y.D.S., Efficacy of a tetravalent dengue vaccine in children in Latin America. N. Engl. J. Med. 372 (2015), 113–123.
54. Villareal, V.A., Rodgers, M.A., Costello, D.A., Yang, P.L., Targeting host lipid synthesis and metabolism to inhibit dengue and hepatitis C viruses. Antivir. Res. 124 (2015), 110–121.
55. Zilbermintz, L., Leonardi, W., Jeong, S.Y., Sjodt, M., McComb, R., Ho, C.L., Retterer, C., Gharaibeh, D., Zamani, R., Soloveva, V., Bavari, S., Levitin, A., West, J., Bradley, K.A., Clubb, R.T., Cohen, S.N., Gupta, V., Martchenko, M., Identification of agents effective against multiple toxins and viruses by host-oriented cell targeting. Sci. Rep., 5, 2015, 13476.