The search for nucleoside/nucleotide analog inhibitors of dengue virus

Antiviral Research

Volumn 122, Issue , 2015, Pages 12-19

  Chen, Yen Liang ^a   Yokokawa, Fumiaki ^a   Shi, Pei Yong ^a  

^a NOVARTIS INSTITUTE FOR TROPICAL DISEASES   (Singapore)

Author keywords

Antiviral therapy; Dengue virus; Monophosphate prodrug; Nucleoside analogs

Indexed keywords

2 METHYLGUANOSINE; 2' METHYLADENOSINE; 3',5' DI O TRITYL 5 FLUORO 2 DEOXYURIDINE; BALAPIRAVIR; INX 08189; MK 0608; NITD 008; NITD 203; NITD 449; NUCLEOSIDE ANALOG; PRODRUG; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; NUCLEOSIDE; NUCLEOTIDE;

ANTIVIRAL ACTIVITY; ANTIVIRAL THERAPY; ARTICLE; CELLS BY BODY ANATOMY; DENGUE; DENGUE VIRUS; DRUG EFFICACY; ENZYME INHIBITION; HUMAN; KINETICS; NONHUMAN; PRIORITY JOURNAL; VIRUS INFECTION; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECTS; METABOLISM; VIROLOGY; VIRUS REPLICATION;

DENGUE VIRUS; FLAVIVIRUS; HEPATITIS C VIRUS; HUMAN IMMUNODEFICIENCY VIRUS;

ANTIVIRAL AGENTS; DENGUE; DENGUE VIRUS; DRUG DISCOVERY; HUMANS; NUCLEOSIDES; NUCLEOTIDES; VIRUS REPLICATION;

EID: 84938847891     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.07.010     Document Type: Review

References (87)

1. S. Abel, D.J. Back, and M. Vourvahis Maraviroc: pharmacokinetics and drug interactions Antivir. Ther. 14 2009 607 618
2. M. Ackermann, and R. Padmanabhan De novo synthesis of RNA by the dengue virus RNA-dependent RNA polymerase exhibits temperature dependence at the initiation but not elongation phase J. Biol. Chem. 276 2001 39926 39937 10.1074/jbc
3. D.E. Amacher Drug-associated mitochondrial toxicity and its detection Curr. Med. Chem. 12 2005 1829 1839
4. J.J. Arnold, S.D. Sharma, J.Y. Feng, A.S. Ray, E.D. Smidansky, M.L. Kireeva, A. Cho, J. Perry, J.E. Vela, Y. Park, Y. Xu, Y. Tian, D. Babusis, O. Barauskus, B.R. Peterson, A. Gnatt, M. Kashlev, W. Zhong, and C.E. Cameron 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
5. S.J. Balsitis, J. Coloma, G. Castro, A. Alava, D. Flores, J.H. McKerrow, P.R. Beatty, and E. Harris Tropism of dengue virus in mice and humans defined by viral nonstructural protein 3-specific immunostaining Am. J. Trop. Med. Hyg. 80 2009 416 424
6. C. Bazzoli, V. Jullien, C. Le Tiec, E. Rey, F. Mentré, and A.-M. Taburet Intracellular pharmacokinetics of antiretroviral drugs in HIV-infected patients, and their correlation with drug action Clin. Pharmacokinet. 49 2010 17 45 10.2165/11318110-000000000-00000
7. P.L. Beaulieu Recent advances in the development of NS5B polymerase inhibitors for the treatment of hepatitis C virus infection Expert Opin. Ther. Pat. 19 2009 145 164
8. F. Becher, R. Landman, S. Mboup, C.N.T. Kane, A. Canestri, F. Liegeois, M. Vray, M.-H. Prevot, G. Leleu, and H. Benech Monitoring of didanosine and stavudine intracellular triphosphorylated anabolite concentrations in HIV-infected patients AIDS 18 2004 181 187
9. J.M. Berke, L. Vijgen, S. Lachau-Durand, M.H. Powdrill, S. Rawe, E. Sjuvarsson, S. Eriksson, M. Götte, E. Fransen, P. Dehertogh, C. Van den Eynde, L. Leclercq, T.H.M. Jonckers, P. Raboisson, M. Nilsson, B. Samuelsson, Å. Rosenquist, G.C. Fanning, and T.-I. Lin Antiviral activity and mode of action of TMC647078, a novel nucleoside inhibitor of the hepatitis C virus NS5B polymerase Antimicrob. Agents Chemother. 55 2011 3812 3820 10.1128/AAC.00214-11
10. M. Bollati, M. Milani, E. Mastrangelo, S. Ricagno, G. Tedeschi, S. Nonnis, E. Decroly, B. Selisko, X. de Lamballerie, B. Coutard, B. Canard, and M. Bolognesi Recognition of RNA cap in the Wesselsbron virus NS5 methyltransferase domain: implications for RNA-capping mechanisms in flavivirus J. Mol. Biol. 385 2009 140 152 10.1016/j.jmb.2008.10.028
11. M. Brandl, X. Wu, M. Holper, L. Hong, Z. Jia, R. Birudaraj, M. Reddy, T. Alfredson, T. Tran, S. Larrabee, X. Hadig, K. Sarma, C. Washington, G. Hill, and D.B. Smith Physicochemical properties of the nucleoside prodrug R1626 leading to high oral bioavailability Drug Dev. Ind. Pharm. 34 2008 683 691 10.1080/03639040701836636
12. Y.-L. Chen, N. Abdul Ghafar, R. Karuna, Y. Fu, S.P. Lim, W. Schul, F. Gu, M. Herve, F. Yokohama, G. Wang, D. Cerny, K. Fink, F. Blasco, and P.-Y. Shi Activation of peripheral blood mononuclear cells by dengue virus infection depotentiates balapiravir J. Virol. 88 2014 1740 1747 10.1128/JVI.02841-13
13. Y.-L. Chen, Z. Yin, J. Duraiswamy, W. Schul, C.C. Lim, B. Liu, H.Y. Xu, M. Qing, A. Yip, G. Wang, W.L. Chan, H.P. Tan, M. Lo, S. Liung, R.R. Kondreddi, R. Rao, H. Gu, H. He, T.H. Keller, and P.-Y. Shi Inhibition of dengue virus RNA synthesis by an adenosine nucleoside Antimicrob. Agents Chemother. 54 2010 2932 2939 10.1128/AAC.00140-10
14. Y.L. Chen, Z. Yin, S.B. Lakshminarayana, M. Qing, W. Schul, J. Duraiswamy, R.R. Kondreddi, A. Goh, H.Y. Xu, A. Yip, B. Liu, M. Weaver, V. Dartois, T.H. Keller, and P.Y. Shi Inhibition of dengue virus by an ester prodrug of an adenosine analog Antimicrob. Agents Chemother. 54 2010 3255 3261 10.1128/AAC.00397-10
15. A. Cho, O.L. Saunders, T. Butler, L. Zhang, J. Xu, J.E. Vela, J.Y. Feng, A.S. Ray, and C.U. Kim Synthesis and antiviral activity of a series of 1′-substituted 4-aza-7,9-dideazaadenosine C-nucleosides Bioorg. Med. Chem. Lett. 22 2012 2705 2707 10.1016/j.bmcl.2012.02.105
16. T. Cihlar, G. Laflamme, R. Fisher, A.C. Carey, J.E. Vela, R. Mackman, and A.S. Ray Novel nucleotide human immunodeficiency virus reverse transcriptase inhibitor GS-9148 with a low nephrotoxic potential: characterization of renal transport and accumulation Antimicrob. Agents Chemother. 53 2009 150 156 10.1128/AAC.01183-08
17. E. De Clercq The race for interferon-free HCV therapies: a snapshot by the spring of 2012 Rev. Med. Virol. 22 2012 392 411 10.1002/rmv
18. S.J. Coats, E.C. Garnier-Amblard, F. Amblard, M. Ehteshami, S. Amiralaei, H. Zhang, L. Zhou, S.R.L. Boucle, X. Lu, L. Bondada, J.R. Shelton, H. Li, P. Liu, C. Li, J.H. Cho, S.N. Chavre, S. Zhou, J. Mathew, and R.F. Schinazi Chutes and ladders in hepatitis C nucleoside drug development Antiviral Res. 102 2014 119 147 10.1016/j.antiviral.2013.11.008
19. L. Delang, I. Vliegen, M. Froeyen, and J. Neyts Comparative study of the genetic barriers and pathways towards resistance of selective inhibitors of hepatitis C virus replication Antimicrob. Agents Chemother. 55 2011 4103 4113 10.1128/AAC.00294-11
20. H. Dong, D.C. Chang, M.H.C. Hua, S.P. Lim, Y.H. Chionh, F. Hia, Y.H. Lee, P. Kukkaro, S.M. Lok, P.C. Dedon, and P.Y. Shi 2′-O methylation of internal adenosine by flavivirus NS5 methyltransferase PLoS Pathog. 8 2012 10.1371/journal.ppat.1002642
21. A.P. Durbin, M.J. Vargas, K. Wanionek, S.N. Hammond, A. Gordon, C. Rocha, A. Balmaseda, and E. Harris Phenotyping of peripheral blood mononuclear cells during acute dengue illness demonstrates infection and increased activation of monocytes in severe cases compared to classic dengue fever Virology 376 2008 429 435 10.1016/j.virol.2008.03.028
22. M.P. Egloff, D. Benarroch, B. Selisko, J.L. Romette, and B. Canard An RNA cap (nucleoside-2′-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization EMBO J. 21 2002 2757 2768
23. M.P. Egloff, E. Decroly, H. Malet, B. Selisko, D. Benarroch, F. Ferron, and B. Canard Structural and functional analysis of methylation and 5′-RNA sequence requirements of short capped RNAs by the methyltransferase domain of dengue virus NS5 J. Mol. Biol. 372 2007 723 736 10.1016/j.jmb.2007.07.005
24. A.B. Eldrup, M. Prhavc, J. Brooks, B. Bhat, T.P. Prakash, Q. Song, S. Bera, N. Bhat, P. Dande, P.D. Cook, C.F. Bennett, S.S. Carroll, R.G. Ball, M. Bosserman, C. Burlein, L.F. Colwell, J.F. Fay, O.A. Flores, K. Getty, R.L. LaFemina, J. Leone, M. MacCoss, D.R. McMasters, J.E. Tomassini, D. Von Langen, B. Wolanski, and D.B. Olsen Structure-activity relationship of heterobase-modified 2′-C-methyl ribonucleosides as inhibitors of hepatitis C virus RNA replication J. Med. Chem. 47 2004 5284 5297 10.1021/jm040068f
25. J.Y. Feng, G. Cheng, J. Perry, O. Barauskas, Y. Xu, M. Fenaux, S. Eng, N. Tirunagari, B. Peng, M. Yu, Y. Tian, Y.-J. Lee, G. Stepan, L.L. Lagpacan, D. Jin, M. Hung, K.S. Ku, B. Han, K. Kitrinos, M. Perron, G. Birkus, K.A. Wong, W. Zhong, C.U. Kim, A. Carey, A. Cho, and A.S. Ray Inhibition of hepatitis C virus replication by GS-6620, a potent C-nucleoside monophosphate prodrug Antimicrob. Agents Chemother. 58 2014 1930 1942 10.1128/AAC.02351-13
26. C.V. Fletcher, S.P. Kawle, T.N. Kakuda, P.L. Anderson, D. Weller, L.R. Bushman, R.C. Brundage, and R.P. Remmel Zidovudine triphosphate and lamivudine triphosphate concentration-response relationships in HIV-infected persons AIDS 14 2000 2137 2144
27. J.E. Fraser, S. Watanabe, C. Wang, W.K.K. Chan, B. Maher, A. Lopez-Denman, C. Hick, K.M. Wagstaff, J.M. Mackenzie, P.M. Sexton, S.G. Vasudevan, and D.A. Jans A nuclear transport inhibitor that modulates the unfolded protein response and provides in vivo protection against lethal dengue virus infection J. Infect. Dis. 210 2014 1780 1791 10.1093/infdis/jiu319
28. Y. Furuta, B.B. Gowen, K. Takahashi, K. Shiraki, D.F. Smee, and D.L. Barnard Favipiravir (T-705), a novel viral RNA polymerase inhibitor Antiviral Res. 100 2013 446 454 10.1016/j.antiviral.2013.09.015
29. W.Y. Gao, D.G. Johns, and H. Mitsuya Potentiation of the anti-HIV activity of zalcitabine and lamivudine by a CTP synthase inhibitor, 3-deazauridine Nucleosides, Nucleotides Nucleic Acids 19 2000 371 377 10.1080/15257770008033015
30. W.-Y. Gao, T. Shirasaka, D.G. Johns, S. Broder, and H. Mitsuya Differential phosphorylation of azidothymidine, dideoxycytidine, and dideoxyinosine in resting and activated periphoeal blood mononuclear cells J. Clin. Invest. 91 1993 2326 2333
31. J.G. García-Lerma, W. Aung, M. Cong, Q. Zheng, A.S. Youngpairoj, J. Mitchell, A. Holder, A. Martin, S. Kuklenyik, W. Luo, C.Y.-C. Lin, D.L. Hanson, E. Kersh, C.-P. Pau, A.S. Ray, J.F. Rooney, W.A. Lee, and W Heneine Natural substrate concentrations can modulate the prophylactic efficacy of nucleotide HIV reverse transcriptase inhibitors J. Virol. 85 2011 6610 6617 10.1128/JVI.00311-11
32. N.L. Golitsina, F.T. Danehy, R. Fellows, E. Cretton-Scott, and D.N. Standring Evaluation of the role of three candidate human kinases in the conversion of the hepatitis C virus inhibitor 2′-C-methyl-cytidine to its 5′-monophosphate metabolite Antiviral Res. 85 2010 470 481 10.1016/j.antiviral.2009.10.020
33. S. Green, and A. Rothman Immunopathological mechanisms in dengue and dengue hemorrhagic fever Curr. Opin. Infect. Dis. 19 2006 429 436 10.1097/01.qco.0000244047.31135.fa
34. J. Guedj, P.S. Pang, J. Denning, M. Rodriguez-Torres, E. Lawitz, W. Symonds, and A.S. Perelson Analysis of hepatitis C viral kinetics during administration of two nucleotide analogues: sofosbuvir (GS-7977) and GS-0938 Antivir. Ther. 19 2014 211 220 10.3851/IMP2733
35. R. Haudecoeur, M. Peuchmaur, A. Ahmed-belkacem, and J. Pawlotsky Structure-activity relationships in the development of allosteric hepatitis C virus RNA-dependent RNA polymerase inhibitors: ten years of research Med. Res. Rev. 33 2013 934 984 10.1002/med
36. M. Issur, B.J. Geiss, I. Bougie, F. Picard-Jean, S. Despins, J. Mayette, S.E. Hobdey, and M. Bisaillon The flavivirus NS5 protein is a true RNA guanylyltransferase that catalyzes a two-step reaction to form the RNA cap structure RNA 15 2009 2340 2350 10.1261/rna.1609709
37. R.S. Jansen, H. Rosing, W. Kromdijk, R. ter Heine, J.H. Schellens, and J.H. Beijnen Simultaneous quantification of emtricitabine and tenofovir nucleotides in peripheral blood mononuclear cells using weak anion-exchange liquid chromatography coupled with tandem mass spectrometry J. Chromatogr., B: Anal. Technol. Biomed. Life Sci. 878 7-8 2010 621 627 10.1016/j.jchromb.2010.01.002
38. K. Jessie, M.Y. Fong, S. Devi, S.K. Lam, and K.T. Wong Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization J. Infect. Dis. 189 2004 1411 1418 10.1086/383043
39. L.P. Jordheim, D. Durantel, F. Zoulim, and C. Dumontet Advances in the development of nucleoside and nucleotide analogues for cancer and viral diseases Nat. Rev. Drug Discov. 12 2013 447 464 10.1038/nrd4010
40. S. Kewn, G.J. Veal, P.G. Hoggard, M.G. Barry, and D.J. Back Lamivudine (3TC) phosphorylation and drug interactions in vitro Biochem. Pharmacol. 54 1997 589 595 10.1016/S0006-2952(97)00189-5
41. V. Khungar, and S.-H. Han A systematic review of side effects of nucleoside and nucleotide drugs used for treatment of chronic hepatitis B Curr. Hepat. Rep. 9 2010 75 90 10.1007/s11901-010-0039-1
42. K. Klumpp, V. Lévêque, S. Le Pogam, H. Ma, W.-R. Jiang, H. Kang, C. Granycome, M. Singer, C. Laxton, J.Q. Hang, K. Sarma, D.B. Smith, D. Heindl, C.J. Hobbs, J.H. Merrett, J. Symons, N. Cammack, J.A. Martin, R. Devos, and I. Nájera The novel nucleoside analog R1479 (4′-azidocytidine) is a potent inhibitor of NS5B-dependent RNA synthesis and hepatitis C virus replication in cell culture J. Biol. Chem. 281 2006 3793 3799 10.1074/jbc.M510195200
43. A. Lavie, I. Schlichting, I.R. Vetter, M. Konrad, J. Reinstein, and R.S. Goody The bottleneck in AZT activation Nat. Med. 3 1997 922 924 10.1038/nm0897-922
44. Lawitz, E., Denning, J., Cornpropst, M., Albanis, E., Symonds, W.T., Berrey, M.M., 2011. PSI-352938, A Novel Purine Nucleotide Analog, Exhibits Potent Antiviral Activity and No Evidence of Resistance in Patients with HCV Genotype 1 Over 7 Days. 46th Annual meetings of EASL.
45. S.P. Lim, C.G. Noble, and P.-Y. Shi The dengue virus NS5 protein as a target for drug discovery Antiviral Res. 119 2015 57 67 10.1016/j.antiviral.2015.04.010
46. J.G. Low, C. Sung, L. Wijaya, Y. Wei, A.P.S. Rathore, S. Watanabe, B.H. Tan, L. Toh, L.T. Chua, Y. Hou, A. Chow, S. Howe, W.K. Chan, K.H. Tan, J.S. Chung, B.P. Cherng, D.C. Lye, P.A. Tambayah, L.C. Ng, J. Connolly, M.L. Hibberd, Y.S. Leo, Y.B. Cheung, E.E. Ooi, and S.G. Vasudevan Efficacy and safety of celgosivir in patients with dengue fever (CELADEN): a phase 1b, randomised, double-blind, placebo-controlled, proof-of-concept trial Lancet Infect. Dis. 14 2014 706 715 10.1016/S1473-3099(14)70730-3
47. F. Malinoski, and V. Stollar Inhibitors of IMP dehydrogenase prevent sindbis virus replication and reduce GTP levels in Aedes albopictus cells Virology 110 1981 281 289
48. B.E.E. Martina, P. Koraka, and A.D.M.E. Osterhaus Dengue virus pathogenesis: an integrated view Clin. Microbiol. Rev. 22 2009 564 581 10.1128/CMR.00035-09
49. M.F. McCown, S. Rajyaguru, S. Le Pogam, S. Ali, W.-R. Jiang, H. Kang, J. Symons, N. Cammack, and I. Najera The hepatitis C virus replicon presents a higher barrier to resistance to nucleoside analogs than to nonnucleoside polymerase or protease inhibitors Antimicrob. Agents Chemother. 52 2008 1604 1612 10.1128/AAC.01317-07
50. C. McGuigan, S.A. Harris, S.M. Daluge, K.S. Gudmundsson, E.W. McLean, T.C. Burnette, H. Marr, R. Hazen, L.D. Condreay, L. Johnson, E. De Clercq, and J. Balzarini Application of phosphoramidate pronucleotide technology to abacavir leads to a significant enhancement of antiviral potency J. Med. Chem. 48 2005 3504 3515 10.1021/jm0491400
51. C. McGuigan, M.R. Kelleher, P. Perrone, S. Mulready, G. Luoni, F. Daverio, S. Rajyaguru, S. Le Pogam, I. Najera, J.A. Martin, K. Klumpp, and D.B. Smith The application of phosphoramidate ProTide technology to the potent anti-HCV compound 4′-azidocytidine (R1479) Bioorg. Med. Chem. Lett. 19 2009 4250 4254 10.1016/j.bmcl.2009.05.099
52. C. McGuigan, P. Perrone, K. Madela, and J. Neyts The phosphoramidate ProTide approach greatly enhances the activity of beta-2′-C-methylguanosine against hepatitis C virus Bioorg. Med. Chem. Lett. 19 2009 4316 4320 10.1016/j.bmcl.2009.05.122
53. G. Migliaccio, J.E. Tomassini, S.S. Carroll, L. Tomei, S. Altamura, B. Bhat, L. Bartholomew, M.R. Bosserman, A. Ceccacci, L.F. Colwell, R. Cortese, R. De Francesco, A.B. Eldrup, K.L. Getty, X.S. Hou, R.L. LaFemina, S.W. Ludmerer, M. MacCoss, D.R. McMasters, M.W. Stahlhut, D.B. Olsen, D.J. Hazuda, and O.A. Flores Characterization of resistance to non-obligate chain-terminating ribonucleoside analogs that inhibit hepatitis C virus replication in vitro J. Biol. Chem. 278 2003 49164 49170 10.1074/jbc.M305041200
54. E. Mukherji, J.L. Au, and L.E. Mathes Differential antiviral activities and intracellular metabolism of 3′-azido-3′-deoxythymidine and 2′,3′-dideoxyinosine in human cells Antimicrob. Agents Chemother. 38 1994 1573 1579 10.1128/AAC.38.7.1573.Updated
55. N.M. Nguyen, C.N.B. Tran, L.K. Phung, K.T.H. Duong, H.L.A. Huynh, J. Farrar, Q.T.H. Nguyen, H.T. Tran, C.V.V. Nguyen, L. Merson, L.T. Hoang, M.L. Hibberd, P.P.K. Aw, A. Wilm, N. Nagarajan, D.T. Nguyen, M.P. Pham, T.T. Nguyen, H. Javanbakht, K. Klumpp, J. Hammond, R. Petric, M. Wolbers, C.T. Nguyen, and C.P. Simmons A randomized, double-blind placebo controlled trial of balapiravir, a polymerase inhibitor, in adult dengue patients J. Infect. Dis. 207 2013 1442 1450 10.1093/infdis/jis470
56. P. Niyomrattanakit, Y.-L. Chen, H. Dong, Z. Yin, M. Qing, J.F. Glickman, K. Lin, D. Mueller, H. Voshol, J.Y.H. Lim, S. Nilar, T.H. Keller, and P.-Y. Shi Inhibition of dengue virus polymerase by blocking of the RNA tunnel J. Virol. 84 11 2010 5678 5686 10.1128/JVI.02451-09
57. L. Oestereich, A. Lüdtke, S. Wurr, T. Rieger, C. Muñoz-Fontela, and S. Günther Successful treatment of advanced Ebola virus infection with T-705 (favipiravir) in a small animal model Antiviral Res. 105 2014 17 21 10.1016/j.antiviral.2014.02.014
58. H. Okuda, K. Ogura, A. Kato, H. Takubo, and T. Watabe A possible mechanism of eighteen patient deaths caused by interactions of sorivudine, a new antiviral drug, with oral 5-fluorouracil prodrugs J. Pharmacol. Exp. Ther. 287 1998 791 799
59. D.B. Olsen, A.B. Eldrup, L. Bartholomew, B. Bhat, M.R. Bosserman, A. Ceccacci, L.F. Colwell, J.F. Fay, O.A. Flores, K.L. Getty, J.A. Grobler, R.L. Lafemina, E.J. Markel, G. Migliaccio, M. Prhavc, M.W. Stahlhut, J.E. Tomassini, M. Maccoss, D.J. Hazuda, and S.S. Carroll A 7-deaza-adenosine analog is a potent and selective inhibitor of hepatitis C virus replication with excellent pharmacokinetic properties Antimicrob. Agents Chemother. 48 2004 3944 3953 10.1128/AAC.48.10.3944
60. A.S. Perelson, and J. Guedj Modelling hepatitis C therapy-predicting effects of treatment Nat. Rev. Gastroenterol. Hepatol. 2015 1 9 10.1038/nrgastro.2015.97
61. P. Perrone, F. Daverio, R. Valente, S. Rajyaguru, J.A. Martin, V. Lévêque, S. LePogam, I. Najera, K. Klumpp, D.B. Smith, and C. McGuigan First example of phosphoramidate approach applied to a 4′-substituted purine nucleoside (4′-azidoadenosine): conversion of an inactive nucleoside to a submicromolar compound versus hepatitis C virus J. Med. Chem. 50 2007 5463 5470 10.1021/jm070362i
62. A.S. Ray, and K.Y. Hostetler Application of kinase bypass strategies to nucleoside antivirals Antiviral Res. 92 2011 277 291 10.1016/j.antiviral.2011.08.015
63. D. Ray, A. Shah, M. Tilgner, Y. Guo, Y. Zhao, H. Dong, T.S. Deas, Y. Zhou, H. Li, and P.-Y. Shi West Nile virus 5′-cap structure is formed by sequential guanine N-7 and ribose 2′-O methylations by nonstructural protein 5 J. Virol. 80 2006 8362 8370 10.1128/JVI.00814-06
64. B.L. Robbins, J. Rodman, C. Mcdonald, R.V. Srinivas, P.M. Flynn, and A. Fridland Enzymatic assay for measurement of zidovudine triphosphate in peripheral blood mononuclear cells Antimicrob. Agents Chemother. 38 1994 115 121
65. S.K. Roberts, G. Cooksley, G.J. Dore, R. Robson, D. Shaw, H. Berns, G. Hill, K. Klumpp, I. Najera, and C. Washington Robust antiviral activity of R1626, a novel nucleoside analog: a randomized, placebo-controlled study in patients with chronic hepatitis C Hepatology 48 2008 398 406 10.1002/hep.22321
66. P.T. Ronaldson, and R. Bendayan Renal drug transport and drug-drug interactions J. Pharm. Pract. 15 2002 490 503 10.1177/089719002237667
67. L. Rosen, M.T. Drouet, and V. Deubel Detection of dengue virus RNA by reverse transcription-polymerase chain reaction in the liver and lymphoid organs but not in the brain in fatal human infection Am. J. Trop. Med. Hyg. 61 1999 720 724
68. H. Sangawa, T. Komeno, H. Nishikawa, A. Yoshida, K. Takahashi, N. Nomura, and Y. Furuta Mechanism of action of T-705 ribosyl triphosphate against influenza virus RNA polymerase Antimicrob. Agents Chemother. 57 2013 5202 5208 10.1128/AAC.00649-13
69. M. Saudi, J. Zmurko, S. Kaptein, J. Rozenski, J. Neyts, and A. Van Aerschot In search of Flavivirus inhibitors part 2: Tritylated, diphenylmethylated and other alkylated nucleoside analogues Eur. J. Med. Chem. 76 2014 98 109 10.1016/j.ejmech.2014.02.011
70. S. Selvaraj, M. Ghebremichael, M. Li, Y. Foli, A. Langs-Barlow, A. Ogbuagu, L. Barakat, E. Tubridy, R. Edifor, W. Lam, Y.-C. Cheng, and E. Paintsil Antiretroviral therapy-induced mitochondrial toxicity: potential mechanisms beyond polymerase-γ inhibition Clin. Pharmacol. Ther. 96 2014 110 120 10.1038/clpt.2014.64
71. C.P. Simmons, J.J. Farrar, N. Van Vinh Chau, and B. Wills Dengue N. Engl. J. Med. 366 2012 1423 1432
72. Sofia, M.J., 2013. Nucleotide prodrugs for the treatment of HCV infection, first ed., In: Advances in pharmacology, Copyright© 2013 Elsevier Inc., All rights reserved, San Diego, Calif. doi: 10.1016/B978-0-12-405880-4.00002-0.
73. M.J. Sofia, D. Bao, W. Chang, J. Du, D. Nagarathnam, S. Rachakonda, P.G. Reddy, B.S. Ross, P. Wang, H.-R. Zhang, S. Bansal, C. Espiritu, M. Keilman, A.M. Lam, H.M.M. Steuer, C. Niu, M.J. Otto, and P.A. Furman Discovery of a β-d-2′-deoxy-2′-α-fluoro-2′-β-C-methyluridine nucleotide prodrug (PSI-7977) for the treatment of hepatitis C virus J. Med. Chem. 53 2010 7202 7218 10.1021/jm100863x
74. D.S. Stein, and K.H.P. Moore Phosphorylation of nucleoside analog antiretrovirals: a review for clinicians Pharmacotherapy 21 2001 11 34
75. L.J. Stuyver, T.R. Mcbrayer, P.M. Tharnish, J. Clark, L. Hollecker, S. Lostia, T. Nachman, J. Grier, M.A. Bennett, M. Xie, F. Raymond, J.D. Morrey, J.L. Julander, P.A. Furman, and M.J. Otto Inhibition of hepatitis C replicon RNA synthesis by β-d-2′-deoxy-2′-fluoro-2′-C-methylcytidine: a specific inhibitor of hepatitis C virus replication Antivir. Chem. Chemother. 17 2006 79 87
76. E.S. Svarovskaia, R. Martin, J.G. McHutchison, M.D. Miller, and H. Mo Abundant drug-resistant NS3 mutants detected by deep sequencing in hepatitis C virus-infected patients undergoing NS3 protease inhibitor monotherapy J. Clin. Microbiol. 50 2012 3267 3274 10.1128/JCM.00838-12
77. D.T.H. Tam, T.V. Ngoc, N.T.H. Tien, N.T.T. Kieu, T.T.T. Thuy, L.T.C. Thanh, C.T. Tam, N.T. Truong, N.T. Dung, P.T. Qui, T.T. Hien, J.J. Farrar, C.P. Simmons, M. Wolbers, and B.A. Wills Effects of short-course oral corticosteroid therapy in early dengue infection in vietnamese patients: a randomized, placebo-controlled trial Clin. Infect. Dis. 55 2012 1216 1224 10.1093/cid/cis655
78. V. Tricou, N.N. Minh, T.P. Van, S.J. Lee, J. Farrar, B. Wills, H.T. Tran, and C.P. Simmons A randomized controlled trial of chloroquine for the treatment of dengue in Vietnamese adults PLoS Negl. Trop. Dis. 4 2010 e785 10.1371/journal.pntd.0000785
79. K.W.R. Van Cleef, G.J. Overheul, M.C. Thomassen, S.J.F. Kaptein, A.D. Davidson, M. Jacobs, J. Neyts, F.J.M. van Kuppeveld, and R.P. van Rij Identification of a new dengue virus inhibitor that targets the viral NS4B protein and restricts genomic RNA replication Antiviral Res. 99 2013 165 171 10.1016/j.antiviral.2013.05.011
80. G. Wang, J. Deval, J. Hong, N. Dyatkina, M. Prhavc, J. Taylor, A. Fung, Z. Jin, S.K. Stevens, V. Serebryany, J. Liu, Q. Zhang, Y. Tam, S.M. Chanda, D.B. Smith, J.A. Symons, L.M. Blatt, and L. Beigelman Discovery of 4′-chloromethyl-2′-deoxy-3′,5′-di-O-isobutyryl-2′-fluorocytidine (ALS-8176), a first-in-class rsv polymerase inhibitor for treatment of human respiratory syncytial virus infection J. Med. Chem. 2015 10.1021/jm5017279 150210141202008
81. L.H. Wang, J. Begley, R.L.S.T. Claire, J. Harris, C. Wakeford, F.S. Rousseau, and W.E.T. Al Pharmacokinetic and pharmacodynamic characteristics of emtricitabine support its once daily dosing for the treatment of HIV infection AIDS 20 2004 1173 1182
82. G. Wang, J. Deval, J. Hong, N. Dyatkina, M. Prhavc, J. Taylor, A. Fung, Z. Jin, S.K. Stevens, V. Serebryany, J. Liu, Q. Zhang, Y. Tam, S.M. Chanda, D.B. Smith, J.A. Symons, L.M. Blatt, and L. Beigelman Discovery of 4′-chloromethyl-2′-deoxy-3′,5′-di- O-isobutyryl-2′-fluorocytidine (ALS-8176), a first-in-class RSV polymerase inhibitor for treatment of human respiratory syncytial virus infection J. Med. Chem. 150210141202008 2015 10.1021/jm5017279
83. X. Xie, J. Zou, Q.-Y. Wang, and P.-Y. Shi Targeting dengue virus NS4B protein for drug discovery Antiviral Res. 2015 10.1016/j.antiviral.2015.03.007
84. K.L. Yeo, Y.-L. Chen, H.Y. Xu, H. Dong, Q.-Y. Wang, F. Yokokawa, and P.-Y. Shi Synergistic suppression of dengue virus replication using a combination of nucleoside analogs and nucleoside synthesis inhibitors Antimicrob. Agents Chemother. 59 2015 2086 2093 10.1128/AAC.04779-14
85. Z. Yin, Y.-L. Chen, W. Schul, Q.-Y. Wang, F. Gu, J. Duraiswamy, R.R. Kondreddi, P. Niyomrattanakit, S.B. Lakshminarayana, A. Goh, H.Y. Xu, W. Liu, B. Liu, J.Y.H. Lim, C.Y. Ng, M. Qing, C.C. Lim, A. Yip, G. Wang, W.L. Chan, H.P. Tan, K. Lin, B. Zhang, G. Zou, K.A. Bernard, C. Garrett, K. Beltz, M. Dong, M. Weaver, H. He, A. Pichota, V. Dartois, T.H. Keller, and P.-Y. Shi An adenosine nucleoside inhibitor of dengue virus Proc. Natl. Acad. Sci. U.S.A. 106 2009 20435 20439 10.1073/pnas.0907010106
86. Y. Zhao, T.S. Soh, J. Zheng, K.W.K. Chan, W.W. Phoo, C.C. Lee, M.Y.F. Tay, K. Swaminathan, T.C. Cornvik, S.P. Lim, P.-Y. Shi, J. Lescar, S.G. Vasudevan, and D. Luo A crystal structure of the dengue virus NS5 protein reveals a novel inter-domain interface essential for protein flexibility and virus replication PLoS Pathog. 11 2015 e1004682 10.1371/journal.ppat.1004682
87. Y. Zhou, D. Ray, Y. Zhao, H. Dong, S. Ren, Z. Li, Y. Guo, K.A. Bernard, P.-Y. Shi, and H. Li Structure and function of flavivirus NS5 methyltransferase J. Virol. 81 2007 3891 3903 10.1128/JVI.02704-06