Ribavirin inhibits Zika virus (ZIKV) replication in vitro and suppresses viremia in ZIKV-infected STAT1-deficient mice

Antiviral Research

Volumn 146, Issue , 2017, Pages 1-11

  Kamiyama, Naganori ^a   Soma, Ryusuke ^a   Hidano, Shinya ^a   Watanabe, Kei ^a   Umekita, Hiroshi ^a   Fukuda, Chiaki ^a   Noguchi, Kaori ^a   Gendo, Yoshiko ^a   Ozaki, Takashi ^a   Sonoda, Akira ^a   Sachi, Nozomi ^a   Runtuwene, Lucky Ronald ^a   Miura, Yumako ^a   Matsubara, Etsuro ^a   Tajima, Shigeru ^b   Takasaki, Tomohiko ^b   Eshita, Yuki ^a   Kobayashi, Takashi ^a  

^a OITA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

Author keywords

Ribavirin; STAT1 deficient mice; Zika virus

Indexed keywords

COMPLEMENTARY DNA; GANCICLOVIR; RECOMBINANT BETA INTERFERON; RIBAVIRIN; RNA POLYMERASE; STAT1 PROTEIN; VIRUS RNA; ANTIVIRUS AGENT; STAT1 PROTEIN, MOUSE;

AEDES ALBOPICTUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; APOPTOSIS; ARTICLE; BRAZIL; CELL DEATH; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENCY; EPIDEMIC; FRENCH POLYNESIA; GUILLAIN BARRE SYNDROME; HUMAN; HUMAN CELL; IN VITRO STUDY; INCIDENCE; MALE; MICROCEPHALY; MOUSE; NEUROBLASTOMA CELL LINE; NONHUMAN; OUTCOME ASSESSMENT; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL TIME; TREATMENT DURATION; VERO CELL LINE; VIREMIA; VIRUS LOAD; VIRUS REPLICATION; ZIKA FEVER; ZIKA VIRUS; ANIMAL; CHLOROCEBUS AETHIOPS; DEFICIENCY; DNA REPLICATION; DRUG EFFECT; GENETICS; PHYSIOLOGY; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CERCOPITHECUS AETHIOPS; DNA REPLICATION; MICE; RIBAVIRIN; STAT1 TRANSCRIPTION FACTOR; VERO CELLS; VIREMIA; VIRUS REPLICATION; ZIKA VIRUS; ZIKA VIRUS INFECTION;

EID: 85027532703     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2017.08.007     Document Type: Article

References (49)

1. Abdel-Hady, M., Bansal, S., Davison, S.M., Brown, M., Tizzard, S.A., Mulla, S., Barnes, E., Davies, P., Mieli-Vergani, G., Kelly, D.A., Treatment of chronic viral hepatitis C in children and adolescents: UK experience. Arch. Dis. Child. 99 (2014), 505–510, 10.1136/archdischild-2013-304601.
2. Bansal, S., Singal, A.K., McGuire, B.M., Anand, B.S., Impact of all oral anti-hepatitis C virus therapy: a meta-analysis. World J. Hepatol. 7 (2015), 806–813, 10.4254/wjh.v7.i5.806.
3. Bausch, D.G., Hadi, C.M., Khan, S.H., Lertora, J.J.L., Review of the literature and proposed guidelines for the use of oral ribavirin as postexposure prophylaxis for Lassa fever. Clin. Infect. Dis. 51 (2010), 1435–1441, 10.1086/657315.
4. Bougie, I., Bisaillon, M., Initial binding of the broad spectrum antiviral nucleoside ribavirin to the hepatitis C Virus RNA polymerase. J. Biol. Chem. 278 (2003), 52471–52478.
5. 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., Calvet, G.A., Neves, E.S., Moreira, M.E., Rodrigues Baião, A.E., Nassar de Carvalho, P.R., Janzen, C., Valderramos, S.G., Cherry, J.D., Bispo de Filippis, A.M., Nielsen-Saines, K., Zika Virus Infection in Pregnant Women in Rio de Janeiro. N. Engl. J. Med. 375 (2016), 2321–2334, 10.1056/NEJMoa1602412.
6. Brochot, E., Castelain, S., Duverlie, G., Capron, D., Nguyen-Khac, E., François, C., Ribavirin monitoring in chronic hepatitis C therapy: anaemia versus efficacy. Antivir. Ther. 15 (2010), 687–695, 10.3851/IMP1609.
7. Bullard-Feibelman, K.M., Govero, J., Zhu, Z., Salazar, V., Veselinovic, M., Diamond, M.S., Geiss, B.J., The FDA-approved drug sofosbuvir inhibits Zika virus infection. Antivir. Res. 137 (2017), 134–140, 10.1016/j.antiviral.2016.11.023.
8. Chang, J., Schul, W., Butters, T.D., Yip, A., Liu, B., Goh, A., Lakshminarayana, S.B., Alonzi, D., Reinkensmeier, G., Pan, X., Qu, X., Weidner, J.M., Wang, L., Yu, W., Borune, N., Kinch, M.A., Rayahin, J.E., Moriarty, R., Xu, X., Shi, P.Y., Guo, J.T., Block, T.M., Combination of α-glucosidase inhibitor and ribavirin for the treatment of dengue virus infection in vitro and in vivo. Antivir. Res. 89 (2011), 26–34, 10.1016/j.antiviral.2010.11.002.
9. Crumpacker, C.S., Ganciclovir. N. Engl. J. Med. 335 (1996), 721–729, 10.1056/NEJM199609053351007.
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., Polonio, C.M., Cunha, I., Freitas, C.L., Brandão, W.N., Rossato, C., Andrade, D.G., Faria, D. de P., Garcez, A.T., Buchpigel, C.A., Braconi, C.T., Mendes, E., Sall, A.A., Zanotto, P.M., Peron, J.P., Muotri, A.R., Beltrão-Braga, P.C., The Brazilian Zika virus strain causes birth defects in experimental models. Nature 534 (2016), 267–271, 10.1038/nature18296.
11. Dick, G.W., Zika Virus (I). Isolations and serological specificity. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 509–520.
12. Dick, G.W., Zika virus (II). Pathogenicity and physical properties. Trans. R. Soc. Trop. Med. Hyg. 46 (1952), 521–534.
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., 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, 10.1056/NEJMoa0805715.
14. Falzarano, D., de Wit, E., Martellaro, C., Callison, J., Munster, V.J., Feldmann, H., Inhibition of novel β coronavirus replication by a combination of interferon-α2b and ribavirin. Sci. Rep., 3, 2013, 1686, 10.1038/srep01686.
15. Falzarano, D., de Wit, E., Rasmussen, A.L., Feldmann, F., Okumura, A., Scott, D.P., Brining, D., Bushmaker, T., Martellaro, C., Baseler, L., Benecke, A.G., Katze, M.G., Munster, V.J., Feldmann, H., Treatment with interferon-α2b and ribavirin improves outcome in MERS-CoV-infected rhesus macaques. Nat. Med. 19 (2013), 1313–1317, 10.1038/nm.3362.
16. Faria, N.R., Azevedo, Rdo, S., Kraemer, M.U., Souza, R., Cunha, M.S., Hill, S.C., Thézé, J., Bonsall, M.B., Bowden, T.A., Rissanen, I., Rocco, I.M., Nogueira, J.S., Maeda, A.Y., Vasami, F.G. da S., Macedo, F.L., Suzuki, A., Rodrigues, S.G., Cruz, A.C., Nunes, B.T., Medeiros, D.B. de A., Rodrigues, D.S., Nunes Queiroz, A.L., da Silva, E.V., Henriques, D.F., Travassos da Rosa, E.S., de Oliveira, C.S., Martins, L.C., Vasconcelos, H.B., Casseb, L.M., Simith, Dde, B., Messina, J.P., Abade, L., Lourenço, J., Alcantara, Carlos Junior, de Lima, M.M., Giovanetti, M., Hay, S.I., de Oliveira, R.S., Lemos, Pda S., de Oliveira, L.F., de Lima, C.P., da Silva, S.P., de Vasconcelos, J.M., Franco, L., Cardoso, J.F., Vianez-Júnior, J.L., Mir, D., Bello, G., Delatorre, E., Khan, K., Creatore, M., Coelho, G.E., de Oliveira, W.K., Tesh, R., Pybus, O.G., Nunes, M.R., Vasconcelos, P.F., Zika virus in the Americas: early epidemiological and genetic findings. Science 352 (2016), 345–349, 10.1126/science.aaf5036.
17. Faye, O., Faye, O., Dupressoir, A., Weidmann, M., Ndiaye, M., Alpha, Sall, A., One-step RT-PCR for detection of Zika virus. J. Clin. Virol. 43 (2008), 96–101.
18. Feld, J.J., Nanda, S., Huang, Y., Chen, W., Cam, M., Pusek, S.N., Schweigler, L.M., Theodore, D., Zacks, S.L., Liang, T.J., Fried, M.W., Hepatic gene expression during treatment with peginterferon and ribavirin: identifying molecular pathways for treatment response. Hepatology 46 (2007), 1548–1563.
19. Ferm, V.H., Willhite, C., Kilham, L., Teratogenic effects of ribavirin on hamster and rat embryos. Teratology 17 (1978), 93–101.
20. Goswami, B.B., Borek, E., Sharma, O.K., Fujitaki, J., Smith, R.A., The broad spectrum antiviral agent ribavirin inhibits capping of mRNA. Biochem. Biophys. Res. Commun. 89 (1979), 830–836.
21. Hayes, E.B., Zika virus outside Africa. Emerg. Infect. Dis. 15 (2009), 1347–1350, 10.3201/eid1509.090442.
22. Highlights of Prescribing Information. Sovaldi (Sofosbuvir) Tablets, for Oral Use Initial U.S. Approval, 2013.
23. Highlights of Prescribing Information. Harvoni (Ledipasvir and Sofosbuvir) Tablets, for Oral Use Initial U.S. Approval, 2014.
24. Izumi, K., Mine, K., Inoue, Y., Teshima, M., Ogawa, S., Kai, Y., Kurafuji, T., Hirakawa, K., Miyakawa, D., Ikeda, H., Inada, A., Hara, M., Yamada, H., Akashi, K., Niho, Y., Ina, K., Kobayashi, T., Yoshikai, Y., Anzai, K., Yamashita, T., Minagawa, H., Fujimoto, S., Kurisaki, H., Shimoda, K., Katsuta, H., Nagafuchi, S., Reduced Tyk2 gene expression in β-cells due to natural mutation determines susceptibility to virus-induced diabetes. Nat. Commun., 6, 2015, 6748, 10.1038/ncomms7748.
25. Julander, J.G., Siddharthan, V., Evans, J., Taylor, R., Tolbert, K., Apuli, C., Stewart, J., Collins, P., Gebre, M., Neilson, S., Van Wettere, A., Lee, Y.M., Sheridan, W.P., Morrey, J.D., Babu, Y.S., Efficacy of the broad-spectrum antiviral compound BCX4430 against Zika virus in cell culture and in a mouse model. Antivir. Res. 137 (2017), 14–22, 10.1016/j.antiviral.2016.11.003.
26. Koren, G., King, S., Knowles, S., Phillips, E., Ribavirin in the treatment of SARS: a new trick for an old drug?. CMAJ 168 (2003), 1289–1292.
27. Lanciotti, R.S., Kosoy, O.L., Laven, J.J., Velez, J.O., Lambert, A.J., Johnson, A.J., Stanfield, S.M., Duffy, M.R., Genetic and serologic properties of Zika virus associated with an epidemic, Yap State, Micronesia, 2007. Emerg. Infect. Dis. 14 (2008), 1232–1239, 10.3201/eid1408.080287.
28. Lazear, H.M., Diamond, M.S., Zika virus: new clinical syndromes and its emergence in the western hemisphere. J. Virol. 90 (2016), 4864–4875, 10.1128/JVI.00252-16.
29. Lazear, H.M., Govero, J., Smith, A.M., Platt, D.J., Fernandez, E., Miner, J.J., Diamond, M.S., A mouse model of Zika virus pathogenesis. Cell Host Microbe 19 (2016), 720–730, 10.1016/j.chom.2016.03.010.
30. Leming, M.T., Rund, S.S., Behura, S.K., Duffield, G.E., O'Tousa, J.E., A database of circadian and diel rhythmic gene expression in the yellow fever mosquito Aedes aegypti. BMC Genomics, 15, 2014, 1128, 10.1186/1471-2164-15-1128.
31. Li, C., Xu, D., Ye, Q., Hong, S., Jiang, Y., Liu, X., Zhang, N., Shi, L., Qin, C.-F., Xu, Z., Zika virus disrupts neural progenitor development and leads to microcephaly in mice. Cell Stem Cell. 19 (2016), 120–126, 10.1016/j.stem.2016.04.017.
32. Maag, D., Castro, C., Hong, Z., Cameron, C.E., Hepatitis C virus RNA-dependent RNA polymerase (NS5B) as a mediator of the antiviral activity of ribavirin. J. Biol. Chem. 276 (2001), 46094–46098, 10.1074/jbc.C100349200.
33. Matthews, T., Boehme, R., Antiviral activity and mechanism of action of ganciclovir. Rev. Infect. Dis. 10:Suppl. 3 (1988), S490–S494.
34. McCormick, J.B., King, I.J., Webb, P.A., Scribner, C.L., Craven, R.B., Johnson, K.M., Elliott, L.H., Belmont-Williams, R., Lassa fever: effective therapy with ribavirin. N. Engl. J. Med. 314 (1986), 20–26, 10.1056/NEJM198601023140104.
35. Meraz, M.A., White, J.M., Sheehan, K.C., Bach, E.A., Rodig, S.J., Dighe, A.S., Kaplan, D.H., Riley, J.K., Greenlund, A.C., Campbell, D., Carver-Moore, K., DuBois, R.N., Clark, R., Aguet, M., Schreiber, R.D., Targeted disruption of the Stat1 gene in mice reveals unexpected physiologic specificity in the JAK-STAT signaling pathway. Cell 84 (1996), 431–442.
36. 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., Mysorekar, I.U., Diamond, M.S., Zika virus infection during pregnancy in mice causes placental damage and fetal demise. Cell 165 (2016), 1081–1091, 10.1016/j.cell.2016.05.008.
37. Petersen, E.E., Staples, J.E., Meaney-delman, D., Fischer, M., Ellington, S.R., Callaghan, W.M., Jamieson, D.J., Interim guidelines for pregnant women during a Zika virus outbreak - United States, 2016. MMWR. Morb. Mortal. Wkly. Rep. 65 (2016), 30–33, 10.15585/mmwr.mm6502e1.
38. Poynard, T., Marcellin, P., Lee, S.S., Niederau, C., Minuk, G.S., Ideo, G., Bain, V., Heathcote, J., Zeuzem, S., Trepo, C., Albrecht, J., Randomised trial of interferon alpha2b plus ribavirin for 48 weeks or for 24 weeks versus interferon alpha2b plus placebo for 48 weeks for treatment of chronic infection with hepatitis C virus. International Hepatitis Interventional Therapy Group (IHIT). Lancet 352 (1998), 1426–1432.
39. Rattanaburee, T., Junking, M., Panya, A., Sawasdee, N., Songprakhon, P., Suttitheptumrong, A., Limjindaporn, T., Haegeman, G., Yenchitsomanus, P., Inhibition of dengue virus production and cytokine/chemokine expression by ribavirin and compound A. Antivir. Res. 124 (2015), 83–92, 10.1016/j.antiviral.2015.10.005.
40. Russmann, S., Grattagliano, I., Portincasa, P., Palmieri, V.O., Palasciano, G., Ribavirin-induced anemia: mechanisms, risk factors and related targets for future research. Curr. Med. Chem. 13 (2006), 3351–3357.
41. Sarno, M., Sacramento, G.A., Khouri, R., do Rosário, M.S., Costa, F., Archanjo, G., Santos, L.A., Nery, N., Vasilakis, N., Ko, A.I., de Almeida, A.R., Zika virus infection and stillbirths: a case of hydrops fetalis, hydranencephaly and fetal demise. PLoS Negl. Trop. Dis., 10, 2016, e0004517, 10.1371/journal.pntd.0004517.
42. Schul, W., Liu, W., Xu, H.Y., Flamand, M., Vasudevan, S.G., A dengue fever viremia model in mice shows reduction in viral replication and suppression of the inflammatory response after treatment with antiviral drugs. J. Infect. Dis. 195 (2007), 665–674.
43. Slavov, S.N., Otaguiri, K.K., Kashima, S., Covas, D.T., Overview of Zika virus (ZIKV) infection in regards to the Brazilian epidemic. Braz. J. Med. Biol. Res., 49, 2016, e5420, 10.1590/1414-431X20165420.
44. Solomon, T., Flavivirus encephalitis and other neurological syndromes (Japanese encephalitis, WNV, Tick borne encephalits, Dengue, Zika virus). Int. J. Infect. Dis., 45, 2016, 24.
45. Tanaka, M., Kodaira, H., Nishiyama, Y., Sata, T., Kawaguchi, Y., Construction of recombinant herpes simplex virus type I expressing green fluorescent protein without loss of any viral genes. Microbes Infect. 6 (2004), 485–493.
46. Tang, H., Hammack, C., Ogden, S.C., Jin, P., Wen, Z., Qian, X., Li, Y., Yao, B., Shin, J., Zhang, F., Lee, E.M., Christian, K.M., Didier, R.A., Song, H., Ming, G.L., Zika virus infects human cortical neural progenitors and attenuates their growth. Cell Stem Cell. 18 (2016), 587–590, 10.1016/j.stem.2016.02.016.
47. Toltzis, P., O'Connell, K., Patterson, J.L., Effect of phosphorylated ribavirin on vesicular stomatitis virus transcription. Antimicrob. Agents Chemother. 32 (1988), 492–497.
48. Ventura, C.V., Maia, M., Bravo-Filho, V., Góis, A.L., Belfort, R., Zika virus in Brazil and macular atrophy in a child with microcephaly. Lancet, 387, 2016, 228, 10.1016/S0140-6736(16)00006-4.
49. Zhang, Y., Jamaluddin, M., Wang, S., Tian, B., Garofalo, R.P., Casola, A., Brasier, A.R., Ribavirin treatment up-regulates antiviral gene expression via the interferon-stimulated response element in respiratory syncytial virus-infected epithelial cells. J. Virol. 77 (2003), 5933–5947.