Synergistic drug combination effectively blocks Ebola virus infection

Antiviral Research

Volumn 137, Issue , 2017, Pages 165-172

  Sun, Wei ^a   He, Shihua ^b,c   Martínez Romero, Carles ^d   Kouznetsova, Jennifer ^a   Tawa, Gregory ^a   Xu, Miao ^a   Shinn, Paul ^a   Fisher, Ethan G ^a   Long, Yan ^a   Motabar, Omid ^a   Yang, Shu ^a   Sanderson, Philip E ^a   Williamson, Peter R ^e   García Sastre, Adolfo ^d   Qiu, Xiangguo ^b,c   Zheng, Wei ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b PUBLIC HEALTH AGENCY OF CANADA   (Canada)

^c UNIVERSITY OF MANITOBA   (Canada)

^d MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^e NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

Drug combination; Drug repurposing; Ebola prevention; Ebola treatment; Polypharmacology

Indexed keywords

AZITHROMYCIN; CALCIUM; CATHEPSIN B; CATHEPSIN L; CHLOROQUINE; CLARITHROMYCIN; DIMETHYL SULFOXIDE; MAPROTILINE; MEFLOQUINE; NICOTINIC ACID ADENINE DINUCLEOTIDE PHOSPHATE; POSACONAZOLE; SPHINGOMYELIN PHOSPHODIESTERASE; TETRANDRINE; TOREMIFENE; ACID SPHINGOMYELINASE-1; ANTIVIRUS AGENT; TRIAZOLE DERIVATIVE;

ANIMAL CELL; ANTIVIRAL THERAPY; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MEMBRANE; COMBINATION DRUG THERAPY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; EBOLA HEMORRHAGIC FEVER; ENDOSOME; HIGH THROUGHPUT SCREENING; IC50; INCUBATION TIME; LYSOSOME; NONHUMAN; PRIORITY JOURNAL; VIRUS ENTRY; VIRUS INHIBITION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL LINE; CHLOROCEBUS AETHIOPS; DRUG COMBINATION; DRUG EFFECTS; EBOLAVIRUS; HUMAN; VERO CELL LINE; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CERCOPITHECUS AETHIOPS; CLARITHROMYCIN; DRUG COMBINATIONS; DRUG SYNERGISM; EBOLAVIRUS; HEMORRHAGIC FEVER, EBOLA; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; MEFLOQUINE; SPHINGOMYELIN PHOSPHODIESTERASE; TOREMIFENE; TRIAZOLES; VERO CELLS; VIRUS INTERNALIZATION;

EID: 85001022598     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2016.11.017     Document Type: Article

References (32)

1. Abramowicz, M., Zuccotti, G., Pflomm, J.M., A 4-Drug combination (viekira pak) for hepatitis C. Jama-J Am. Med. Assoc. 313 (2015), 1857–1858.
2. Amini, H., Ahmadiani, A., Sensitive determination of clarithromycin in human plasma by high-performance liquid chromatography with spectrophotometric detection. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 817 (2005), 193–197.
3. Andersson, D.I., Hughes, D., Antibiotic resistance and its cost: is it possible to reverse resistance?. Nat. Rev. Microbiol. 8 (2010), 260–271.
4. 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–U115.
5. Chandran, K., Sullivan, N.J., Felbor, U., Whelan, S.P., Cunningham, J.M., Endosomal proteolysis of the Ebola virus glycoprotein is necessary for infection. Science 308 (2005), 1643–1645.
6. Cote, M., Misasi, J., Ren, T., Bruchez, A., Lee, K., Filone, C.M., Hensley, L., Li, Q., Ory, D., Chandran, K., Cunningham, J., Small molecule inhibitors reveal Niemann-Pick C1 is essential for Ebola virus infection. Nature, 477, 2011 344–U122.
7. DeGregorio, M.W., Wurz, G.T., Taras, T.L., Erkkola, R.U., Halonen, K.H., Huupponen, R.K., Pharmacokinetics of (deaminohydroxy)toremifene in humans: a new, selective estrogen-receptor modulator. Eur. J. Clin. Pharmacol. 56 (2000), 469–475.
8. Garcia, M., Cooper, A., Shi, W., Bornmann, W., Carrion, R., Kalman, D., Nabel, G.J., Productive replication of Ebola virus is regulated by the c-abl1 tyrosine kinase. Sci. Transl. Med., 4, 2012.
9. Herbert, A.S., Davidson, C., Kuehne, A.I., Bakken, R., Braigen, S.Z., Gunn, K.E., Whelan, S.P., Brummelkamp, T.R., Twenhafel, N.A., Chandran, K., Walkley, S.U., Dye, J.M., Niemann-pick C1 Is Essential for Ebolavirus Replication and Pathogenesis in Vivo. 2015 Mbio 6.
10. Ho, D.D., Time to hit HIV, early and hard. N. Engl. J. Med. 333 (1995), 450–451.
11. Jae, L.T., Brummelkamp, T.R., Emerging intracellular receptors for hemorrhagic fever viruses. Trends Microbiol. 23 (2015), 392–400.
12. Johansen, L.M., Brannan, J.M., Delos, S.E., Shoemaker, C.J., Stossel, A., Lear, C., Hoffstrom, B.G., Dewald, L.E., Schornberg, K.L., Scully, C., Lehar, J., Hensley, L.E., White, J.M., Olinger, G.G., FDA-approved selective estrogen receptor modulators inhibit Ebola virus infection. Sci. Transl. Med., 5, 2013 190ra179.
13. Karbwang, J., Na Bangchang, K., Thanavibul, A., Back, D.J., Bunnag, D., Harinasuta, T., Pharmacokinetics of mefloquine alone or in combination with artesunate. Bull. World Health Organ 72 (1994), 83–87.
14. Kersemaekers, W.M., van Iersel, T., Nassander, U., O'Mara, E., Waskin, H., Caceres, M., van Iersel, M.L., Pharmacokinetics and safety study of posaconazole intravenous solution administered peripherally to healthy subjects. Antimicrob. Agents Chemother. 59 (2015), 1246–1251.
15. Kouznetsova, J., Sun, W., Martinez-Romero, C., Tawa, G., Shinn, P., Chen, C.Z., Schimmer, A., Sanderson, P., McKew, J.C., Zheng, W., Garcia-Sastre, A., Identification of 53 compounds that block Ebola virus-like particle entry via a repurposing screen of approved drugs. Emerg. Microbes Infect., 3, 2014, e84.
16. Madrid, P.B., Chopra, S., Manger, I.D., Gilfillan, L., Keepers, T.R., Shurtleff, A.C., Green, C.E., Iyer, L.V., Dilks, H.H., Davey, R.A., Kolokoltsov, A.A., Carrion, R. Jr., Patterson, J.L., Bavari, S., Panchal, R.G., Warren, T.K., Wells, J.B., Moos, W.H., Burke, R.L., Tanga, M.J., A systematic screen of FDA-approved drugs for inhibitors of biological threat agents. PLoS One, 8, 2013, e60579.
17. Miller, M.E., Adhikary, S., Kolokoltsov, A.A., Davey, R.A., Ebolavirus requires acid sphingomyelinase activity and plasma membrane sphingomyelin for infection. J. Virol. 86 (2012), 7473–7483.
18. Mitui, M., Khokhar, S.K., Leos, N.K., Doern, C.D., Park, J.Y., Helicobacter pylori 23S rRNA gene sequencing for the identification of mutations associated with clarithromycin resistance in FFPE samples. Lab. Invest, 93, 2013 373a-373a.
19. Moller-Tank, S., Maury, W., Ebola virus entry: a curious and complex series of events. PLoS Pathog., 11, 2015, e1004731.
20. Munayyer, H.K., Mann, P.A., Chau, A.S., Yarosh-Tomaine, T., Greene, J.R., Hare, R.S., Heimark, L., Palermo, R.E., Loebenberg, D., McNicholas, P.M., Posaconazole is a potent inhibitor of sterol 14 alpha-demethylation in yeasts and molds. Antimicrob. Agents Chemother. 48 (2004), 3690–3696.
21. Munkhjargal, T., AbouLaila, M., Terkawi, M.A., Sivakumar, T., Ichikawa, M., Davaasuren, B., Nyamjargal, T., Yokoyama, N., Igarashi, I., Inhibitory effects of pepstatin a and mefloquine on the growth of babesia parasites. Am. J. Trop. Med. Hyg. 87 (2012), 681–688.
22. Sakurai, Y., Kolokoltsov, A.A., Chen, C.C., Tidwell, M.W., Bauta, W.E., Klugbauer, N., Grimm, C., Wahl-Schott, C., Biel, M., Davey, R.A., Ebola virus. Two-pore channels control Ebola virus host cell entry and are drug targets for disease treatment. Science 347 (2015), 995–998.
23. Schlagenhauf, P., Adamcova, M., Regep, L., Schaerer, M.T., Rhein, H.G., The Position of Mefloquine as a 21(st) Century Malaria Chemoprophylaxis. 2010 Malaria J 9.
24. Sun, W., Sanderson, P., Zheng, W., Drug Combination Therapy Increases Successful Drug Repositioning. 2016, Drug Discov Today.
25. Tscherne, D.M., Manicassamy, B., Garcia-Sastre, A., An enzymatic virus-like particle assay for sensitive detection of virus entry. J. Virol. Methods 163 (2010), 336–343.
26. Clarithromycin. Tuberc. (Edinb) 88 (2008), 92–95.
27. Vogel, C.L., Johnston, M.A., Capers, C., Braccia, D., Toremifene for breast Cancer: a review of 20 Years of data. Clin. Breast Cancer 14 (2014), 1–9.
28. Walsh, T.J., Raad, I., Patterson, T.F., Chandrasekar, P., Donowitz, G.R., Graybill, R., Greene, R.E., Hachem, R., Hadley, S., Herbrecht, R., Langston, A., Louie, A., Ribaud, P., Segal, B.H., Stevens, D.A., van Burik, J.A., White, C.S., Corcoran, G., Gogate, J., Krishna, G., Pedicone, L., Hardalo, C., Perfect, J.R., Treatment of invasive aspergillosis with posaconazole in patients who are refractory to or intolerant of conventional therapy: an externally controlled trial. Clin. Infect. Dis. 44 (2007), 2–12.
29. Wang, Y., Jadhav, A., Southal, N., Huang, R., Nguyen, D.T., A grid algorithm for high throughput fitting of dose-response curve data. Curr. Chem. Genomics 4 (2010), 57–66.
30. Xu, M., Liu, K., Southall, N., Marugan, J.J., Remaley, A.T., Zheng, W., A high-throughput sphingomyelinase assay using natural substrate. Anal. Bioanal. Chem. 404 (2012), 407–414.
31. Xu, M., Liu, K., Swaroop, M., Porter, F.D., Sidhu, R., Firnkes, S., Ory, D.S., Marugan, J.J., Xiao, J., Southall, N., Pavan, W.J., Davidson, C., Walkley, S.U., Remaley, A.T., Baxa, U., Sun, W., McKew, J.C., Austin, C.P., Zheng, W., delta-Tocopherol reduces lipid accumulation in Niemann-Pick type C1 and Wolman cholesterol storage disorders. J. Biol. Chem. 287 (2012), 39349–39360.
32. Zhao, Y., Ren, J., Harlos, K., Jones, D.M., Zeltina, A., Bowden, T.A., Padilla-Parra, S., Fry, E.E., Stuart, D.I., Toremifene interacts with and destabilizes the Ebola virus glycoprotein. Nature 535 (2016), 169–172.