Identification of 2′-deoxy-2′-fluorocytidine as a potent inhibitor of Crimean-Congo hemorrhagic fever virus replication using a recombinant fluorescent reporter virus

Antiviral Research

Volumn 147, Issue , 2017, Pages 91-99

  Welch, Stephen R ^a   Scholte, Florine E M ^a   Flint, Mike ^a   Chatterjee, Payel ^a   Nichol, Stuart T ^a   Bergeron, Éric ^a   Spiropoulou, Christina F ^a  

^a NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2' DEOXY 2' FLUOROCYTIDINE; FAVIPIRAVIR; GREEN FLUORESCENT PROTEIN; MYCOPHENOLATE MOFETIL; MYCOPHENOLIC ACID; NUCLEOSIDE ANALOG; RECOMBINANT PROTEIN; RIBAVIRIN; UNCLASSIFIED DRUG; 2'-FLUORO-2'-DEOXYCYTIDINE; AMIDE; ANTIVIRUS AGENT; DEOXYCYTIDINE; PYRAZINE DERIVATIVE; VIRAL PROTEIN;

AMINO ACID SUBSTITUTION; ANTIVIRAL ACTIVITY; ARTICLE; CC50; CELL VIABILITY; CONTROLLED STUDY; CRIMEAN CONGO HEMORRHAGIC FEVER; CRIMEAN-CONGO HEMORRHAGIC FEVER VIRUS; DRUG IDENTIFICATION; DRUG POTENCY; DRUG POTENTIATION; EC50; GENETIC STABILITY; HIGH THROUGHPUT SCREENING; HUH-7 CELL LINE; HUMAN; HUMAN CELL; LIMIT OF DETECTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCREENING; SW13 CELL LINE; VERO C1008 CELL LINE; VIRUS RECOMBINANT; VIRUS REPLICATION; WESTERN BLOTTING; ANALOGS AND DERIVATIVES; CELL SURVIVAL; DOSE RESPONSE; DRUG DEVELOPMENT; DRUG EFFECT; GENETICS; LD50; PROCEDURES; REPORTER GENE; TUMOR CELL LINE; VIROLOGY;

AMIDES; ANTIVIRAL AGENTS; CELL LINE, TUMOR; CELL SURVIVAL; DEOXYCYTIDINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG DISCOVERY; DRUG SYNERGISM; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HEMORRHAGIC FEVER VIRUS, CRIMEAN-CONGO; HEMORRHAGIC FEVER, CRIMEAN; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LETHAL DOSE 50; PYRAZINES; RIBAVIRIN; VIRAL PROTEINS; VIRUS REPLICATION;

EID: 85031277646     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2017.10.008     Document Type: Article

References (46)

1. Albarino, C.G., Wiggleton Guerrero, L., Lo, M.K., Nichol, S.T., Towner, J.S., Development of a reverse genetics system to generate a recombinant Ebola virus Makona expressing a green fluorescent protein. Virology 484 (2015), 259–264, 10.1016/j.virol.2015.06.013.
2. Albariño, C.G., Wiggleton Guerrero, L., Lo, M.K., Nichol, S.T., Towner, J.S., Development of a reverse genetics system to generate a recombinant Ebola virus Makona expressing a green fluorescent protein. Virology 484 (2015), 259–264, 10.1016/j.virol.2015.06.013.
3. Arnold, J.J., Sharma, S.D., Feng, J.Y., Ray, A.S., Smidansky, E.D., Kireeva, M.L., Cho, A., Perry, J., Vela, J.E., Park, Y., Xu, Y., Tian, Y., Babusis, D., Barauskus, O., Peterson, B.R., Gnatt, A., Kashlev, M., Zhong, W., Cameron, C.E., Sensitivity of mitochondrial transcription and resistance of RNA polymerase II dependent nuclear transcription to antiviral ribonucleosides. PLoS Pathog., 8, 2012, e1003030, 10.1371/journal.ppat.1003030.
4. Ascioglu, S., Leblebicioglu, H., Vahaboglu, H., Chan, K.A., Ribavirin for patients with Crimean-Congo haemorrhagic fever: a systematic review and meta-analysis. J. Antimicrob. Chemother. 66 (2011), 1215–1222, 10.1093/jac/dkr136.
5. Barrows, N.J., Campos, R.K., Powell, S.T., Prasanth, K.R., Schott-Lerner, G., Soto-Acosta, R., Galarza-Muñoz, G., McGrath, E.L., Urrabaz-Garza, R., Gao, J., Wu, P., Menon, R., Saade, G., Fernandez-Salas, I., Rossi, S.L., Vasilakis, N., Routh, A., Bradrick, S.S., Garcia-Blanco, M.A., A screen of FDA-approved drugs for inhibitors of Zika virus infection. Cell Host Microbe 20 (2016), 259–270, 10.1016/j.chom.2016.07.004.
6. Bente, D.A., Alimonti, J.B., Shieh, W.-J., Camus, G., Ströher, U., Zaki, S., Jones, S.M., Pathogenesis and immune response of Crimean-Congo hemorrhagic fever virus in a STAT-1 knockout mouse model. J. Virol. 84 (2010), 11089–11100, 10.1128/JVI.01383-10.
7. Bente, D.A., Forrester, N.L., Watts, D.M., McAuley, A.J., Whitehouse, C.A., Bray, M., Crimean-Congo hemorrhagic fever: history, epidemiology, pathogenesis, clinical syndrome and genetic diversity. Antivir. Res. 100 (2013), 159–189, 10.1016/j.antiviral.2013.07.006.
8. Bergeron, É., Albariño, C.G., Khristova, M.L., Nichol, S.T., Crimean-Congo hemorrhagic fever virus-encoded ovarian tumor protease activity is dispensable for virus RNA polymerase function. J. Virol. 84 (2010), 216–226, 10.1128/JVI.01859-09.
9. Bergeron, É., Zivcec, M., Chakrabarti, A.K., Nichol, S.T., Albariño, C.G., Spiropoulou, C.F., Recovery of recombinant crimean Congo hemorrhagic fever virus reveals a function for non-structural glycoproteins cleavage by furin. PLoS Pathog., 11, 2015, e1004879, 10.1371/journal.ppat.1004879.
10. Carette, J.E., Raaben, M., Wong, A.C., Herbert, A.S., Obernosterer, G., Mulherkar, N., Kuehne, A.I., Kranzusch, P.J., Griffin, A.M., Ruthel, G., Dal Cin, P., Dye, J.M., Whelan, S.P., Chandran, K., Brummelkamp, T.R., Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 477 (2011), 340–343, 10.1038/nature10348.
11. Di Veroli, G.Y., Fornari, C., Wang, D., Mollard, S., Bramhall, J.L., Richards, F.M., Jodrell, D.I., Combenefit: an interactive platform for the analysis and visualization of drug combinations. Bioinformatics 32 (2016), 2866–2868, 10.1093/bioinformatics/btw230.
12. Diamond, M.S., Zachariah, M., Harris, E., Mycophenolic acid inhibits dengue virus infection by preventing replication of viral RNA. Virology 304 (2002), 211–221.
13. Dokuzoguz, B., Celikbas, A.K., Gök, Ş.E., Baykam, N., Eroglu, M.N., Ergönül, O., Severity scoring index for Crimean-Congo hemorrhagic fever and the impact of ribavirin and corticosteroids on fatality. Clin. Infect. Dis. 57 (2013), 1270–1274, 10.1093/cid/cit527.
14. Hoogstraal, H., The epidemiology of tick-borne Crimean-Congo hemorrhagic fever in Asia, Europe, and Africa. J. Med. Entomol. 15 (1979), 307–417.
15. Humolli, I., Dedushaj, I., Zupanac, T.A., Muçaj, S., Epidemiological, serological and herd immunity of Crimean-Congo haemorrhagic fever in Kosovo. Med. Arh. 64 (2010), 91–93.
16. Jae, L.T., Raaben, M., Riemersma, M., van Beusekom, E., Blomen, V.A., Velds, A., Kerkhoven, R.M., Carette, J.E., Topaloglu, H., Meinecke, P., Wessels, M.W., Lefeber, D.J., Whelan, S.P., van Bokhoven, H., Brummelkamp, T.R., Deciphering the glycosylome of dystroglycanopathies using haploid screens for lassa virus entry. Science 340 (2013), 479–483, 10.1126/science.1233675.
17. Kim, J.H., Lee, S.-R., Li, L.-H., Park, H.-J., Park, J.-H., Lee, K.Y., Kim, M.-K., Shin, B.A., Choi, S.-Y., High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. PLoS One, 6, 2011, e18556, 10.1371/journal.pone.0018556.
18. Köksal, I., Yilmaz, G., Aksoy, F., Aydin, H., Yavuz, I., Iskender, S., Akcay, K., Erensoy, S., Caylan, R., Aydin, K., The efficacy of ribavirin in the treatment of Crimean-Congo hemorrhagic fever in Eastern Black Sea region in Turkey. J. Clin. Virol. 47 (2010), 65–68, 10.1016/j.jcv.2009.11.007.
19. Kuhn, J.H., Wiley, M.R., Rodriguez, S.E., Bào, Y., Prieto, K., Travassos da Rosa, A.P.A., Guzman, H., Savji, N., Ladner, J.T., Tesh, R.B., Wada, J., Jahrling, P.B., Bente, D.A., Palacios, G., Genomic characterization of the genus nairovirus (family bunyaviridae). Viruses, 8, 2016, 164, 10.3390/v8060164.
20. Kumaki, Y., Day, C.W., Smee, D.F., Morrey, J.D., Barnard, D.L., In vitro and in vivo efficacy of fluorodeoxycytidine analogs against highly pathogenic avian influenza H5N1, seasonal, and pandemic H1N1 virus infections. Antivir. Res. 92 (2011), 329–340, 10.1016/j.antiviral.2011.09.001.
21. Leblebicioglu, H., Ozaras, R., Irmak, H., Sencan, I., Crimean-Congo hemorrhagic fever in Turkey: current status and future challenges. Antivir. Res. 126 (2016), 21–34, 10.1016/j.antiviral.2015.12.003.
22. Lee, H., Hanes, J., Johnson, K.A., Toxicity of nucleoside analogues used to treat AIDS and the selectivity of the mitochondrial DNA polymerase. Biochemistry 42 (2003), 14711–14719, 10.1021/bi035596s.
23. Mishra, A.C., Mehta, M., Mourya, D.T., Gandhi, S., Crimean-Congo haemorrhagic fever in India. Lancet, 378, 2011, 372, 10.1016/S0140-6736(11)60680-6.
24. Mohr, E.L., McMullan, L.K., Lo, M.K., Spengler, J.R., Bergeron, É., Albariño, C.G., Shrivastava-Ranjan, P., Chiang, C.-F., Nichol, S.T., Spiropoulou, C.F., Flint, M., Inhibitors of cellular kinases with broad-spectrum antiviral activity for hemorrhagic fever viruses. Antivir. Res. 120 (2015), 40–47, 10.1016/j.antiviral.2015.05.003.
25. Oestereich, L., Rieger, T., Ludtke, A., Ruibal, P., Wurr, S., Pallasch, E., Bockholt, S., Krasemann, S., Munoz-Fontela, C., Gunther, S., Efficacy of favipiravir alone and in combination with ribavirin in a lethal, immunocompetent mouse model of lassa fever. J. Infect. Dis. 213 (2016), 934–938, 10.1093/infdis/jiv522.
26. Oestereich, L., Rieger, T., Neumann, M., Bernreuther, C., Lehmann, M., Krasemann, S., Wurr, S., Emmerich, P., de Lamballerie, X., Ölschläger, S., Günther, S., Evaluation of antiviral efficacy of ribavirin, arbidol, and T-705 (favipiravir) in a mouse model for Crimean-Congo hemorrhagic fever. PLoS Negl. Trop. Dis., 8, 2014, e2804, 10.1371/journal.pntd.0002804.
27. Ozbey, S.B., Kader, Ç., Erbay, A., Ergönül, O., Early use of ribavirin is beneficial in Crimean-Congo hemorrhagic fever. Vector Borne Zoonotic Dis. 14 (2014), 300–302, 10.1089/vbz.2013.1421.
28. Park, A., Yun, T., Hill, T.E., Ikegami, T., Juelich, T.L., Smith, J.K., Zhang, L., Freiberg, A.N., Lee, B., Optimized P2A for reporter gene insertion into Nipah virus results in efficient ribosomal skipping and wild-type lethality. J. Gen. Virol. 97 (2016), 839–843, 10.1099/jgv.0.000405.
29. Pierra, C., Amador, A., Benzaria, S., Cretton-Scott, E., D'Amours, M., Mao, J., Mathieu, S., Moussa, A., Bridges, E.G., Standring, D.N., Sommadossi, J.-P., Storer, R., Gosselin, G., Synthesis and pharmacokinetics of valopicitabine (NM283), an efficient prodrug of the potent anti-HCV agent 2'-C-methylcytidine. J. Med. Chem. 49 (2006), 6614–6620, 10.1021/jm0603623.
30. Pockros, P.J., Jensen, D., Tsai, N., Taylor, R., Ramji, A., Cooper, C., Dickson, R., Tice, A., Kulkarni, R., Vierling, J.M., Lou Munson, M., Chen, Y.-C., Najera, I., Thommes, J., JUMP-C Investigators, JUMP-C: a randomized trial of mericitabine plus pegylated interferon alpha-2a/ribavirin for 24 weeks in treatment-naïve HCV genotype 1/4 patients. Hepatology 58 (2013), 514–523, 10.1002/hep.26275.
31. Reed, L.J., Muench, H., A simple method of estimating fifty per cent endpoints., 27, 1938, 493–497.
32. Reuther, P., Göpfert, K., Dudek, A.H., Heiner, M., Herold, S., Schwemmle, M., Generation of a variety of stable Influenza A reporter viruses by genetic engineering of the NS gene segment. Sci. Rep., 5, 2015, 11346, 10.1038/srep11346.
33. Richardson, F.C., Tennant, B.C., Meyer, D.J., Richardson, K.A., Mann, P.C., McGinty, G.R., Wolf, J.L., Zack, P.M., Bendele, R.A., An evaluation of the toxicities of 2“-fluorouridine and 2-”fluorocytidine-HCl in F344 rats and woodchucks (Marmota monax). Toxicol. Pathol. 27 (1999), 607–617, 10.1177/019262339902700601.
34. Soares-Weiser, K., Thomas, S., Thomson, G., Garner, P., Ribavirin for Crimean-Congo hemorrhagic fever: systematic review and meta-analysis. BMC Infect. Dis., 10, 2010, 207, 10.1186/1471-2334-10-207.
35. Spengler, J.R., Keating, M.K., McElroy, A.K., Zivcec, M., Coleman-McCray, J.D., Harmon, J.R., Bollweg, B.C., Goldsmith, C.S., Bergeron, É., Keck, J.G., Zaki, S.R., Nichol, S.T., Spiropoulou, C.F., Crimean-Congo hemorrhagic fever in humanized mice reveals glial cells as primary targets of neurological infection. J. Infect. Dis., 2017, 10.1093/infdis/jix215.
36. Stuyver, L.J., McBrayer, T.R., Whitaker, T., Tharnish, P.M., Ramesh, M., Lostia, S., Cartee, L., Shi, J., Hobbs, A., Schinazi, R.F., Watanabe, K.A., Otto, M.J., Inhibition of the subgenomic hepatitis C virus replicon in huh-7 cells by 2“-deoxy-2-”fluorocytidine. Antimicrob. Agents Chemother. 48 (2004), 651–654, 10.1128/AAC.48.2.651-654.2004.
37. Sun, Y., Chung, D.-H., Chu, Y.-K., Jonsson, C.B., Parker, W.B., Activity of ribavirin against Hantaan virus correlates with production of ribavirin-5'-triphosphate, not with inhibition of IMP dehydrogenase. Antimicrob. Agents Chemother. 51 (2007), 84–88, 10.1128/AAC.00790-06.
38. Tasdelen Fisgin, N., Ergonul, O., Doganci, L., Tulek, N., The role of ribavirin in the therapy of Crimean-Congo hemorrhagic fever: early use is promising. Eur. J. Clin. Microbiol. Infect. Dis. 28 (2009), 929–933, 10.1007/s10096-009-0728-2.
39. To, K.K.W., Mok, K.-Y., Chan, A.S.F., Cheung, N.N., Wang, P., Lui, Y.-M., Chan, J.F.W., Chen, H., Chan, K.-H., Kao, R.Y.T., Yuen, K.-Y., Mycophenolic acid, an immunomodulator, has potent and broad-spectrum in vitro antiviral activity against pandemic, seasonal and avian influenza viruses affecting humans. J. Gen. Virol. 97 (2016), 1807–1817, 10.1099/jgv.0.000512.
40. Wedemeyer, H., Jensen, D., Herring, R., Ferenci, P., Ma, M.-M., Zeuzem, S., Rodriguez-Torres, M., Bzowej, N., Pockros, P., Vierling, J., Ipe, D., Munson, M.L., Chen, Y.-C., Najera, I., Thommes, J., Investigators, P.R.O.P.E.L., PROPEL: a randomized trial of mericitabine plus peginterferon alpha-2a/ribavirin therapy in treatment-naïve HCV genotype 1/4 patients. Hepatology 58 (2013), 524–537, 10.1002/hep.26274.
41. Welch, S.R., Guerrero, L.W., Chakrabarti, A.K., McMullan, L.K., Flint, M., Bluemling, G.R., Painter, G.R., Nichol, S.T., Spiropoulou, C.F., Albariño, C.G., Lassa and Ebola virus inhibitors identified using minigenome and recombinant virus reporter systems. Antivir. Res. 136 (2016), 9–18, 10.1016/j.antiviral.2016.10.007.
42. WHO, Blueprint for R&D Preparedness and Response to Public Health Emergencies Due to Highly Infectious Pathogens. 2016.
43. Yin, Y., Wang, Y., Dang, W., Xu, L., Su, J., Zhou, X., Wang, W., Felczak, K., van der Laan, L.J.W., Pankiewicz, K.W., van der Eijk, A.A., Bijvelds, M., Sprengers, D., de Jonge, H., Koopmans, M.P.G., Metselaar, H.J., Peppelenbosch, M.P., Pan, Q., Mycophenolic acid potently inhibits rotavirus infection with a high barrier to resistance development. Antivir. Res. 133 (2016), 41–49, 10.1016/j.antiviral.2016.07.017.
44. 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.
45. Zivcec, M., Safronetz, D., Scott, D., Robertson, S., Ebihara, H., Feldmann, H., Lethal Crimean-Congo hemorrhagic fever virus infection in interferon α/β receptor knockout mice is associated with high viral loads, proinflammatory responses, and coagulopathy. J. Infect. Dis. 207 (2013), 1909–1921, 10.1093/infdis/jit061.
46. Zivcec, M., Scholte, F., Spiropoulou, C., Spengler, J., Bergeron, É., Molecular insights into Crimean-Congo hemorrhagic fever virus. Viruses, 8, 2016, 106, 10.3390/v8040106.