A Screen of FDA-Approved Drugs for Inhibitors of Zika Virus Infection

Cell Host and Microbe

Volumn 20, Issue 2, 2016, Pages 259-270

  Barrows, Nicholas J ^a,b   Campos, Rafael K ^a,b   Powell, Steven T ^a   Prasanth, K Reddisiva ^a   Schott Lerner, Geraldine ^a   Soto Acosta, Ruben ^a   Galarza Muñoz, Gaddiel ^a   McGrath, Erica L ^a   Urrabaz Garza, Rheanna ^a   Gao, Junling ^a   Wu, Ping ^a   Menon, Ramkumar ^a   Saade, George ^a   Fernandez Salas, Ildefonso ^c   Rossi, Shannan L ^a   Vasilakis, Nikos ^a   Routh, Andrew ^a   Bradrick, Shelton S ^a   Garcia Blanco, Mariano A ^a,d  

^a University of Texas Medical Branch School of Medicine   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUTO NACIONAL DE SALUD PÚBLICA   (Mexico)

^d DUKE NUS MEDICAL SCHOOL   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIVIRUS AGENT; AURANOFIN; AZATHIOPRINE; BORTEZOMIB; CLOFAZIMINE; CYCLOSPORIN; CYCLOSPORIN A; DACTINOMYCIN; DAPTOMYCIN; DEFERASIROX; DIGOXIN; FINGOLIMOD; G PROTEIN COUPLED RECEPTOR KINASE 2; GEMCITABINE; IVERMECTIN; MEBENDAZOLE; MEFLOQUINE; METHOXSALEN; MICAFUNGIN; MYCOPHENOLATE MOFETIL; MYCOPHENOLIC ACID; PALONOSETRON; PYRIMETHAMINE; SERTRALINE; SORAFENIB; TIOGUANINE;

AMNION CELL; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; DRUG SCREENING; FLOW CYTOMETRY; FOOD AND DRUG ADMINISTRATION; HUMAN; HUMAN CELL; INFECTION RATE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; VALIDATION STUDY; VIRUS CULTURE; VIRUS REPLICATION; ZIKA FEVER; CELL CULTURE; DRUG EFFECTS; DRUG REPOSITIONING; GROWTH, DEVELOPMENT AND AGING; ISOLATION AND PURIFICATION; PRECLINICAL STUDY; PROCEDURES; ZIKA VIRUS;

ANTIVIRAL AGENTS; CELLS, CULTURED; DRUG EVALUATION, PRECLINICAL; DRUG REPOSITIONING; HUMANS; ZIKA VIRUS;

EID: 84979738780     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.07.004     Document Type: Article

References (73)

1. Adams, J., Palombella, V.J., Sausville, E.A., Johnson, J., Destree, A., Lazarus, D.D., Maas, J., Pien, C.S., Prakash, S., Elliott, P.J., Proteasome inhibitors: a novel class of potent and effective antitumor agents. Cancer Res. 59 (1999), 2615–2622.
2. Araújo, H.R., Carvalho, D.O., Ioshino, R.S., Costa-da-Silva, A.L., Capurro, M.L., Aedes aegypti Control Strategies in Brazil: Incorporation of New Technologies to Overcome the Persistence of Dengue Epidemics. Insects 6 (2015), 576–594.
3. Arzuza-Ortega, L., Polo, A., Pérez-Tatis, G., López-García, H., Parra, E., Pardo-Herrera, L.C., Rico-Turca, A.M., Villamil-Gómez, W., Rodríguez-Morales, A.J., Fatal Sickle Cell Disease and Zika Virus Infection in Girl from Colombia. Emerg. Infect. Dis. 22 (2016), 925–927.
4. Baltz, R.H., Daptomycin: mechanisms of action and resistance, and biosynthetic engineering. Curr. Opin. Chem. Biol. 13 (2009), 144–151.
5. Benelli, G., Plant-borne ovicides in the fight against mosquito vectors of medical and veterinary importance: a systematic review. Parasitol. Res. 114 (2015), 3201–3212.
6. Benvenuto, M., Benziger, D.P., Yankelev, S., Vigliani, G., Pharmacokinetics and tolerability of daptomycin at doses up to 12 milligrams per kilogram of body weight once daily in healthy volunteers. Antimicrob. Agents Chemother. 50 (2006), 3245–3249.
7. Brasil, P., Pereira, J.P. Jr., Raja Gabaglia, C., Damasceno, L., Wakimoto, M., Ribeiro Nogueira, R.M., Carvalho de Sequeira, P., Machado Siqueira, A., Abreu de Carvalho, L.M., Cotrim da Cunha, D., et al. Zika Virus Infection in Pregnant Women in Rio de Janeiro - Preliminary Report. N. Engl. J. Med., 2016 Published online March 4, 2016.
8. Bullingham, R.E., Nicholls, A.J., Kamm, B.R., Clinical pharmacokinetics of mycophenolate mofetil. Clin. Pharmacokinet. 34 (1998), 429–455.
9. Choy, M.M., Zhang, S.L., Costa, V.V., Tan, H.C., Horrevorts, S., Ooi, E.E., Proteasome Inhibition Suppresses Dengue Virus Egress in Antibody Dependent Infection. PLoS Negl. Trop. Dis., 9, 2015, e0004058.
10. Cugola, F.R., Fernandes, I.R., Russo, F.B., Freitas, B.C., Dias, J.L.M., Guimarães, K.P., Benazzato, C., Almeida, N., Pignatari, G.C., Romero, S., et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534 (2016), 267–271.
11. Diamond, M.S., Zachariah, M., Harris, E., Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA. Virology 304 (2002), 211–221.
12. Dick, G.W., Kitchen, S.F., Haddow, A.J., Zika virus. I. Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 509–520.
13. 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., et al. Zika virus outbreak on Yap Island, Federated States of Micronesia. N. Engl. J. Med. 360 (2009), 2536–2543.
14. Dupont-Rouzeyrol, M., O'Connor, O., Calvez, E., Daurès, M., John, M., Grangeon, J.P., Gourinat, A.C., Co-infection with Zika and dengue viruses in 2 patients, New Caledonia, 2014. Emerg. Infect. Dis. 21 (2015), 381–382.
15. Ekins, S., Mietchen, D., Coffee, M., Stratton, T.P., Freundlich, J.S., Freitas-Junior, L., Muratov, E., Siqueira-Neto, J., Williams, A.J., Andrade, C., Open drug discovery for the Zika virus. F1000Res., 5, 2016, 150.
16. Fauci, A.S., Morens, D.M., Zika Virus in the Americas—Yet Another Arbovirus Threat. N. Engl. J. Med. 374 (2016), 601–604.
17. Faye, O., Freire, C.C., Iamarino, A., Faye, O., de Oliveira, J.V., Diallo, M., Zanotto, P.M., Sall, A.A., Molecular evolution of Zika virus during its emergence in the 20(th) century. PLoS Negl. Trop. Dis., 8, 2014, e2636.
18. Fontes, C.A., Dos Santos, A.A., Marchiori, E., Magnetic resonance imaging findings in Guillain-Barré syndrome caused by Zika virus infection. Neuroradiology, 2016 Published online April 11, 2016.
19. Foy, B.D., Kobylinski, K.C., Chilson Foy, J.L., Blitvich, B.J., Travassos da Rosa, A., Haddow, A.D., Lanciotti, R.S., Tesh, R.B., Probable non-vector-borne transmission of Zika virus, Colorado, USA. Emerg. Infect. Dis. 17 (2011), 880–882.
20. Garcez, P.P., Loiola, E.C., Madeiro da Costa, R., Higa, L.M., Trindade, P., Delvecchio, R., Nascimento, J.M., Brindeiro, R., Tanuri, A., Rehen, S.K., Zika virus impairs growth in human neurospheres and brain organoids. Science 352 (2016), 816–818.
21. Geng, Y., Kohli, L., Klocke, B.J., Roth, K.A., Chloroquine-induced autophagic vacuole accumulation and cell death in glioma cells is p53 independent. Neuro-oncol. 12 (2010), 473–481.
22. Guerbois, M., Fernandez-Salas, I., Azar, S.R., Danis-Lozano, R., Alpuche-Aranda, M.C., Lela, G., Garcia-Malo, I.R., Diaz-Gonzalez, E.E., Casas-Martinez, M., Rossi, S.L., et al. Outbreak of Zika virus infection, Chiapas State, Mexico, 2015, and first confirmed transmission by Aedes aegypti mosquitoes in the Americas. J. Infect. Dis., 2016 Published online July 19, 2016.
23. Guzzo, C.A., Furtek, C.I., Porras, A.G., Chen, C., Tipping, R., Clineschmidt, C.M., Sciberras, D.G., Hsieh, J.Y., Lasseter, K.C., Safety, tolerability, and pharmacokinetics of escalating high doses of ivermectin in healthy adult subjects. J. Clin. Pharmacol. 42 (2002), 1122–1133.
24. Hanners, N.W., Eitson, J.L., Usui, N., Richardson, R.B., Wexler, E.M., Konopka, G., Schoggins, J.W., Western Zika Virus in Human Fetal Neural Progenitors Persists Long Term with Partial Cytopathic and Limited Immunogenic Effects. Cell Rep. 15 (2016), 2315–2322.
25. Harris, A.F., McKemey, A.R., Nimmo, D., Curtis, Z., Black, I., Morgan, S.A., Oviedo, M.N., Lacroix, R., Naish, N., Morrison, N.I., et al. Successful suppression of a field mosquito population by sustained release of engineered male mosquitoes. Nat. Biotechnol. 30 (2012), 828–830.
26. Henchal, E.A., Gentry, M.K., McCown, J.M., Brandt, W.E., Dengue virus-specific and flavivirus group determinants identified with monoclonal antibodies by indirect immunofluorescence. Am. J. Trop. Med. Hyg. 31 (1982), 830–836.
27. Hertel, L.W., Boder, G.B., Kroin, J.S., Rinzel, S.M., Poore, G.A., Todd, G.C., Grindey, G.B., Evaluation of the antitumor activity of gemcitabine (2′,2′-difluoro-2′-deoxycytidine). Cancer Res. 50 (1990), 4417–4422.
28. Kang, S., Shields, A.R., Jupatanakul, N., Dimopoulos, G., Suppressing dengue-2 infection by chemical inhibition of Aedes aegypti host factors. PLoS Negl. Trop. Dis., 8, 2014, e3084.
29. Karbwang, J., White, N.J., Clinical pharmacokinetics of mefloquine. Clin. Pharmacokinet. 19 (1990), 264–279.
30. Kleber de Oliveira, W., Cortez-Escalante, J., De Oliveira, W.T., do Carmo, G.M., Henriques, C.M., Coelho, G.E., Araújo de França, G.V., Increase in Reported Prevalence of Microcephaly in Infants Born to Women Living in Areas with Confirmed Zika Virus Transmission During the First Trimester of Pregnancy - Brazil, 2015. MMWR Morb. Mortal. Wkly. Rep. 65 (2016), 242–247.
31. Koe, B.K., Weissman, A., Welch, W.M., Browne, R.G., Sertraline, 1S,4S-N-methyl-4-(3,4-dichlorophenyl)-1,2,3,4-tetrahydro-1-naphthylamine, a new uptake inhibitor with selectivity for serotonin. J. Pharmacol. Exp. Ther. 226 (1983), 686–700.
32. Kok, W.M., New developments in flavivirus drug discovery. Expert Opin. Drug Discov. 11 (2016), 433–445.
33. Krishnan, M.N., Ng, A., Sukumaran, B., Gilfoy, F.D., Uchil, P.D., Sultana, H., Brass, A.L., Adametz, R., Tsui, M., Qian, F., et al. RNA interference screen for human genes associated with West Nile virus infection. Nature 455 (2008), 242–245.
34. Ladner, J.T., Wiley, M.R., Prieto, K., Yasuda, C.Y., Nagle, E., Kasper, M.R., Reyes, D., Vasilakis, N., Heang, V., Weaver, S.C., et al. Complete Genome Sequences of Five Zika Virus Isolates. Genome Announc., 4, 2016, 4.
35. Lennard, L., The clinical pharmacology of 6-mercaptopurine. Eur. J. Clin. Pharmacol. 43 (1992), 329–339.
36. Le Sommer, C., Barrows, N.J., Bradrick, S.S., Pearson, J.L., Garcia-Blanco, M.A., G protein-coupled receptor kinase 2 promotes flaviviridae entry and replication. PLoS Negl. Trop. Dis., 6, 2012, 10.1371/journal.pntd.0001820.
37. Lednicky, J., Beau De Rochars, V.M., El Badry, M., Loeb, J., Telisma, T., Chavannes, S., Anilis, G., Cella, E., Ciccozzi, M., Rashid, M., et al. Zika Virus Outbreak in Haiti in 2014: Molecular and Clinical Data. PLoS Negl. Trop. Dis., 10, 2016, e0004687.
38. Lundberg, L., Pinkham, C., Baer, A., Amaya, M., Narayanan, A., Wagstaff, K.M., Jans, D.A., Kehn-Hall, K., Nuclear import and export inhibitors alter capsid protein distribution in mammalian cells and reduce Venezuelan Equine Encephalitis Virus replication. Antiviral Res. 100 (2013), 662–672.
39. Madeira, J.M., Gibson, D.L., Kean, W.F., Klegeris, A., The biological activity of auranofin: implications for novel treatment of diseases. Inflammopharmacology 20 (2012), 297–306.
40. Mansuy, J.M., Dutertre, M., Mengelle, C., Fourcade, C., Marchou, B., Delobel, P., Izopet, J., Martin-Blondel, G., Zika virus: high infectious viral load in semen, a new sexually transmitted pathogen?. Lancet Infect. Dis., 16, 2016, 405.
41. Mastrangelo, E., Pezzullo, M., De Burghgraeve, T., Kaptein, S., Pastorino, B., Dallmeier, K., de Lamballerie, X., Neyts, J., Hanson, A.M., Frick, D.N., et al. Ivermectin is a potent inhibitor of flavivirus replication specifically targeting NS3 helicase activity: new prospects for an old drug. J. Antimicrob. Chemother. 67 (2012), 1884–1894.
42. Menéndez-Arias, L., Richman, D.D., Editorial overview: antivirals and resistance: advances and challenges ahead. Curr. Opin. Virol. 8 (2014), iv–vii.
43. Miner, J.J., Cao, B., Govero, J., Smith, A.M., Fernandez, E., Cabrera, O.H., Garber, C., Noll, M., Klein, R.S., Noguchi, K.K., et al. Zika Virus Infection during Pregnancy in Mice Causes Placental Damage and Fetal Demise. Cell 165 (2016), 1081–1091.
44. Mlakar, J., Korva, M., Tul, N., Popović, M., Poljšak-Prijatelj, M., Mraz, J., Kolenc, M., Resman Rus, K., Vesnaver Vipotnik, T., Fabjan Vodušek, V., et al. Zika Virus Associated with Microcephaly. N. Engl. J. Med. 374 (2016), 951–958.
45. Moreira, L.A., Iturbe-Ormaetxe, I., Jeffery, J.A., Lu, G., Pyke, A.T., Hedges, L.M., Rocha, B.C., Hall-Mendelin, S., Day, A., Riegler, M., et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, Chikungunya, and Plasmodium. Cell 139 (2009), 1268–1278.
46. Navari, R.M., 5-HT3 receptors as important mediators of nausea and vomiting due to chemotherapy. Biochim. Biophys. Acta 1848:10 Pt B (2015), 2738–2746.
47. 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. Antiviral Res. 76 (2007), 222–231.
48. Noronha, Ld., Zanluca, C., Azevedo, M.L., Luz, K.G., Santos, C.N., Zika virus damages the human placental barrier and presents marked fetal neurotropism. Mem. Inst. Oswaldo Cruz 111 (2016), 287–293.
49. Parrish, J.A., Fitzpatrick, T.B., Tanenbaum, L., Pathak, M.A., Photochemotherapy of psoriasis with oral methoxsalen and longwave ultraviolet light. N. Engl. J. Med. 291 (1974), 1207–1211.
50. Petersen, L.R., Jamieson, D.J., Powers, A.M., Honein, M.A., Zika Virus. N. Engl. J. Med. 374 (2016), 1552–1563.
51. Poole, B., Ohkuma, S., Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J. Cell Biol. 90 (1981), 665–669.
52. Prassas, I., Diamandis, E.P., Novel therapeutic applications of cardiac glycosides. Nat. Rev. Drug Discov. 7 (2008), 926–935.
53. Qian, X., Nguyen, H.N., Song, M.M., Hadiono, C., Ogden, S.C., Hammack, C., Yao, B., Hamersky, G.R., Jacob, F., Zhong, C., et al. Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure. Cell 165 (2016), 1238–1254.
54. Qing, M., Yang, F., Zhang, B., Zou, G., Robida, J.M., Yuan, Z., Tang, H., Shi, P.Y., Cyclosporine inhibits flavivirus replication through blocking the interaction between host cyclophilins and viral NS5 protein. Antimicrob. Agents Chemother. 53 (2009), 3226–3235.
55. Rasmussen, S.A., Jamieson, D.J., Honein, M.A., Petersen, L.R., Zika Virus and Birth Defects—Reviewing the Evidence for Causality. N. Engl. J. Med. 374 (2016), 1981–1987.
56. Roth, A., Mercier, A., Lepers, C., Hoy, D., Duituturaga, S., Benyon, E., Guillaumot, L., Souares, Y., Concurrent outbreaks of dengue, chikungunya and Zika virus infections - an unprecedented epidemic wave of mosquito-borne viruses in the Pacific 2012-2014. Euro. Surveill., 19, 2014 Publihsed online October 16, 2014.
57. Schweitzer, B.I., Dicker, A.P., Bertino, J.R., Dihydrofolate reductase as a therapeutic target. FASEB J. 4 (1990), 2441–2452.
58. Sessions, O.M., Barrows, N.J., Souza-Neto, J.A., Robinson, T.J., Hershey, C.L., Rodgers, M.A., Ramirez, J.L., Dimopoulos, G., Yang, P.L., Pearson, J.L., Garcia-Blanco, M.A., Discovery of insect and human dengue virus host factors. Nature 458 (2009), 1047–1050.
59. Sobell, H.M., Actinomycin and DNA transcription. Proc. Natl. Acad. Sci. USA 82 (1985), 5328–5331.
60. Spiegel, S., Milstien, S., The outs and the ins of sphingosine-1-phosphate in immunity. Nat. Rev. Immunol. 11 (2011), 403–415.
61. Svendsen, C.N., ter Borg, M.G., Armstrong, R.J., Rosser, A.E., Chandran, S., Ostenfeld, T., Caldwell, M.A., A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 85 (1998), 141–152.
62. 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.
63. Tang, H., Hammack, C., Ogden, S.C., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E.M., et al. Zika Virus Infects Human Cortical Neural Progenitors and Attenuates Their Growth. Cell Stem Cell 18 (2016), 587–590.
64. Tognarelli, J., Ulloa, S., Villagra, E., Lagos, J., Aguayo, C., Fasce, R., Parra, B., Mora, J., Becerra, N., Lagos, N., et al. A report on the outbreak of Zika virus on Easter Island, South Pacific, 2014. Arch. Virol. 161 (2016), 665–668.
65. Torti, S.V., Torti, F.M., Iron and cancer: more ore to be mined. Nat. Rev. Cancer 13 (2013), 342–355.
66. Varghese, F.S., Kaukinen, P., Gläsker, S., Bespalov, M., Hanski, L., Wennerberg, K., Kümmerer, B.M., Ahola, T., Discovery of berberine, abamectin and ivermectin as antivirals against chikungunya and other alphaviruses. Antiviral Res. 126 (2016), 117–124.
67. Wagstaff, K.M., Sivakumaran, H., Heaton, S.M., Harrich, D., Jans, D.A., Ivermectin is a specific inhibitor of importin α/β-mediated nuclear import able to inhibit replication of HIV-1 and dengue virus. Biochem. J. 443 (2012), 851–856.
68. Weaver, S.C., Costa, F., Garcia-Blanco, M.A., Ko, A.I., Ribeiro, G.S., Saade, G., Shi, P.Y., Vasilakis, N., Zika virus: History, emergence, biology, and prospects for control. Antiviral Res. 130 (2016), 69–80.
69. Wilhelm, S., Carter, C., Lynch, M., Lowinger, T., Dumas, J., Smith, R.A., Schwartz, B., Simantov, R., Kelley, S., Discovery and development of sorafenib: a multikinase inhibitor for treating cancer. Nat. Rev. Drug Discov. 5 (2006), 835–844.
70. Wu, P., Tarasenko, Y.I., Gu, Y., Huang, L.Y., Coggeshall, R.E., Yu, Y., Region-specific generation of cholinergic neurons from fetal human neural stem cells grafted in adult rat. Nature Neuroscience 5 (2002), 1271–1278.
71. Yin, Z., Chen, Y.L., Schul, W., Wang, Q.Y., Gu, F., Duraiswamy, J., Kondreddi, R.R., Niyomrattanakit, P., Lakshminarayana, S.B., Goh, A., et al. An adenosine nucleoside inhibitor of dengue virus. Proc. Natl. Acad. Sci. USA 106 (2009), 20435–20439.
72. Zaitseva, E., Yang, S.T., Melikov, K., Pourmal, S., Chernomordik, L.V., Dengue virus ensures its fusion in late endosomes using compartment-specific lipids. PLoS Pathog., 6, 2010, e1001131.
73. Zhang, J.H., Chung, T.D., Oldenburg, K.R., A Simple Statistical Parameter for Use in Evaluation and Validation of High Throughput Screening Assays. J. Biomol. Screen. 4 (1999), 67–73.