Novel broad spectrum inhibitors targeting the flavivirus methyltransferase

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Brecher, Matthew ^a   Chen, Hui ^a   Liu, Binbin ^a   Banavali, Nilesh K ^a,b   Jones, Susan A ^a   Zhang, Jing ^a   Li, Zhong ^a   Kramer, Laura D ^a,b   Li, Hongmin ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHYLTRANSFERASE INHIBITOR; NSC 109268; NSC 115448; NSC 128609; NSC 181486; NSC 21328; NSC 306698; NSC 306711; NSC 35489; NSC 36806; NSC 402959; NSC 51535; NSC 610930; PIBENZIMOL; S ADENOSYLMETHIONINE; UNCLASSIFIED DRUG; ANTIVIRUS AGENT; CAPPED RNA; METHYLTRANSFERASE; NS5 PROTEIN, FLAVIVIRUS; VIRAL PROTEIN; VIRUS RNA;

ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DENGUE VIRUS 2; DENGUE VIRUS 3; DRUG BINDING SITE; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG POTENCY; DRUG SCREENING; DRUG STRUCTURE; DRUG TARGETING; ENZYME INHIBITION; FLAVIVIRUS; IC50; IN VITRO STUDY; NONHUMAN; VIRUS INHIBITION; VIRUS REPLICATION; WEST NILE VIRUS; YELLOW FEVER VIRUS; ANTAGONISTS AND INHIBITORS; BINDING SITE; DRUG EFFECTS; ENZYMOLOGY; FLAVIVIRUS INFECTIONS; GENETICS; METABOLISM; METHYLATION; MICROBIAL SENSITIVITY TEST;

FLAVIVIRUS;

ANTIVIRAL AGENTS; BINDING SITES; FLAVIVIRUS; FLAVIVIRUS INFECTIONS; METHYLATION; METHYLTRANSFERASES; MICROBIAL SENSITIVITY TESTS; RNA CAPS; RNA, VIRAL; VIRAL NONSTRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84939249563     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130062     Document Type: Article

References (46)

1. Lindenbach B, Rice CM. Flaviviridae: The virus and Their Replication,. Fourth ed. Knipe DM, Howley PM, editors: Lippincott William & Wilkins; 2001.
2. Liu L, Dong H, Chen H, Zhang J, Ling H, Li Z, et al. Flavivirus RNA cap methyltransferase: structure, function, and inhibition. Front Biol. 2010; 5(4):286-303. Epub 2011/09/20. PMID:21927615; PubMed Central PMCID:PMC3172701.
3. Schweitzer BK, Chapman NM, Iwen PC. Overview of the Flaviviridae With an Emphasis on the Japanese Encephalitis Group Viruses. LABMEDICINE. 2009; 40:493-9.
4. Turtle L, Griffiths MJ, Solomon T. Encephalitis caused by flaviviruses. QJM: monthly journal of the Association of Physicians. 2012; 105(3):219-23. Epub 2012/03/01. doi:10.1093/qjmed/hcs013 PMID:22367423; PubMed Central PMCID:PMC3285924.
5. Teruel-Lopez E. [Dengue. A review]. Invest Clin. 1991; 32(4):201-17. PMID:1822723
6. Heinz FX, Stiasny K. Flaviviruses and flavivirus vaccines. Vaccine. 2012; 30(29):4301-6. Epub 2012/06/12. doi:10.1016/j.vaccine.2011.09.114 PMID:22682286.
7. Burke DS, Monath TP. Flaviviruses. Fourth ed. Knipe DM, Howley PM, editors: Lippincott William & Wilkins; 2001.
8. Kramer L, Li J, Shi P. West Nile virus. The Lancet Neurology. 2007;In press.
9. Cleaves GR, Dubin DT. Methylation status of intracellular dengue type 2 40 S RNA. Virology. 1979; 96 (1):159-65. PMID:111410
10. Ray D, Shah A, Tilgner M, Guo Y, Zhao Y, Dong H, et al. West nile virus 5'-cap structure is formed by sequential guanine N-7 and ribose 2'-O methylations by nonstructural protein 5. J Virol. 2006; 80 (17):8362-70. PMID:16912287
11. Chambers TJ, Hahn CS, Galler R, Rice CM. Flavivirus genome organization, expression, and replication. Annu Rev Microbiol. 1990; 44:649-88. PMID:2174669
12. Brecher M, Zhang J, Li H. The flavivirus protease as a target for drug discovery. Virol Sin. 2013; 28 (6):326-36. Epub 2013/11/19. doi:10.1007/s12250-013-3390-x PMID:24242363.
13. Noble CG, Chen YL, Dong H, Gu F, Lim SP, Schul W, et al. Strategies for development of Dengue virus inhibitors. Antiviral research. 2010; 85(3):450-62. Epub 2010/01/12. doi:10.1016/j.antiviral.2009.12.011 PMID:20060421.
14. Bollati M, Alvarez K, Assenberg R, Baronti C, Canard B, Cook S, et al. Structure and functionality in flavivirus NS-proteins: perspectives for drug design. Antiviral research. 2010; 87(2):125-48. Epub 2009/12/01. doi:10.1016/j.antiviral.2009.11.009 PMID:19945487.
15. Sampath A, Padmanabhan R. Molecular targets for flavivirus drug discovery. Antiviral research. 2009; 81(1):6-15. Epub 2008/09/18. doi:10.1016/j.antiviral.2008.08.004 PMID:18796313; PubMed Central PMCID:PMC2647018.
16. Lim SP, Wang QY, Noble CG, Chen YL, Dong H, Zou B, et al. Ten years of dengue drug discovery: progress and prospects. Antiviral Res. 2013; 100(2):500-19. Epub 2013/10/01. doi:10.1016/j.antiviral. 2013.09.013 S0166-3542(13)00261-1 [pii]. PMID:24076358.
17. van Cleef KW, Overheul GJ, Thomassen MC, Kaptein SJ, Davidson AD, Jacobs M, et al. Identification of a new dengue virus inhibitor that targets the viral NS4B protein and restricts genomic RNA replication. Antiviral Res. 2013; 99(2):165-71. Epub 2013/06/06. doi:10.1016/j.antiviral.2013.05.011 S0166-3542(13)00142-3 [pii]. PMID:23735301.
18. Byrd CM, Dai D, Grosenbach DW, Berhanu A, Jones KF, Cardwell KB, et al. A novel inhibitor of dengue virus replication that targets the capsid protein. Antimicrob Agents Chemother. 2013; 57(1):15-25. Epub 2012/10/17. doi:10.1128/AAC.01429-12 AAC.01429-12 [pii]. PMID:23070172; PubMed Central PMCID:PMC3535982.
19. Xie X, Wang QY, Xu HY, Qing M, Kramer L, Yuan Z, et al. Inhibition of dengue virus by targeting viral NS4B protein. J Virol. 2011; 85(21):11183-95. Epub 2011/08/26. doi:10.1128/JVI.05468-11 JVI.05468-11 [pii]. PMID:21865382; PubMed Central PMCID:PMC3194949.
20. Chen H, Zhou B, Brecher M, Banavali N, Jones SA, Li Z, et al. S-adenosyl-homocysteine is a weakly bound inhibitor for a flaviviral methyltransferase. PLoS One. 2013; 8(10):e76900. Epub 2013/10/17. doi:10.1371/journal.pone.0076900 PONE-D-13-22207 [pii]. PMID:24130807; PubMed Central PMCID:PMC3793912.
21. Dong H, Ren S, Zhang B, Zhou Y, Puig-Basagoiti F, Li H, et al. West Nile virus methyltransferase catalyzes two methylations of the viral RNA cap through a substrate-repositioning mechanism. Journal of virology. 2008; 82(9):4295-307. Epub 2008/02/29. doi:10.1128/JVI.02202-07 PMID:18305027; PubMed Central PMCID:PMC2293060.
22. Benarroch D, Egloff MP, Mulard L, Guerreiro C, Romette JL, Canard B. A structural basis for the inhibition of the NS5 dengue virus mRNA 2'-O-methyltransferase domain by ribavirin 5'-triphosphate. J Biol Chem. 2004; 279(34):35638-43. PMID:15152003.
23. Dong H, Zhang B, Shi PY. Flavivirus methyltransferase: a novel antiviral target. Antiviral research. 2008; 80(1):1-10. Epub 2008/06/24. doi:10.1016/j.antiviral.2008.05.003 PMID:18571739; PubMed Central PMCID:PMC3214650.
24. Lim SP, Wen D, Yap TL, Yan CK, Lescar J, Vasudevan SG. A scintillation proximity assay for dengue virus NS5 2'-O-methyltransferase-kinetic and inhibition analyses. Antiviral research. 2008; 80(3):360-9. Epub 2008/09/24. doi:10.1016/j.antiviral.2008.08.005 PMID:18809436.
25. Luzhkov V, Selisko B, Nordqvist A, Peyrane F, Decroly E, Alvarez K, et al. Virtual screening and bioassay study of novel inhibitors for dengue virus mRNA cap (nucleoside-2'O)-methyltransferase. Bioorg Med Chem. 2007; 15(24):7795-802. PMID:17888664
26. Milani M, Mastrangelo E, Bollati M, Selisko B, Decroly E, Bouvet M, et al. Flaviviral methyltransferase/RNA interaction: structural basis for enzyme inhibition. Antiviral research. 2009; 83(1):28-34. Epub 2009/06/09. doi:10.1016/j.antiviral.2009.03.001 PMID:19501254.
27. Podvinec M, Lim SP, Schmidt T, Scarsi M, Wen D, Sonntag LS, et al. Novel inhibitors of dengue virus methyltransferase: discovery by in vitro-driven virtual screening on a desktop computer grid. Journal of medicinal chemistry. 2010; 53(4):1483-95. Epub 2010/01/30. doi:10.1021/jm900776m PMID:20108931.
28. Puig-Basagoiti F, Qing M, Dong H, Zhang B, Zou G, Yuan Z, et al. Identification and characterization of inhibitors of West Nile virus. Antiviral research. 2009; 83(1):71-9. Epub 2009/06/09. doi:10.1016/j. antiviral.2009.03.005 PMID:19501258; PubMed Central PMCID:PMC3214651.
29. Selisko B, Peyrane FF, Canard B, Alvarez K, Decroly E. Biochemical characterization of the (nucleoside- 2'O)-methyltransferase activity of dengue virus protein NS5 using purified capped RNA oligonucleotides (7Me)GpppAC(n) and GpppAC(n). The Journal of general virology. 2010; 91(Pt 1):112-21. Epub 2009/09/25. doi:10.1099/vir.0.015511-0 PMID:19776234.
30. Chen H, Liu L, Jones SA, Banavali N, Kass J, Li Z, et al. Selective inhibition of the West Nile virus methyltransferase by nucleoside analogs. Antiviral Res. 2013; 97(3):232-9. Epub 2012/12/27. doi:10. 1016/j.antiviral.2012.12.012 S0166-3542(12)00292-6 [pii]. PMID:23267828; PubMed Central PMCID:PMC3608738.
31. Egloff MP, Benarroch D, Selisko B, Romette JL, Canard B. An RNA cap (nucleoside-2'-O-)-methyltransferase in the flavivirus RNA polymerase NS5: crystal structure and functional characterization. EMBO J. 2002; 21(11):2757-68. PMID:12032088
32. Dong H, Chang DC, Hua MH, Lim SP, Chionh YH, Hia F, et al. 2'-O methylation of internal adenosine by flavivirus NS5 methyltransferase. PLoS Pathog. 2012; 8(4):e1002642. Epub 2012/04/13. doi:10. 1371/journal.ppat.1002642 PMID:22496660; PubMed Central PMCID:PMC3320599.
33. Zhou Y, Ray D, Zhao Y, Dong H, Ren S, Li Z, et al. Structure and function of flavivirus NS5 methyltransferase. J Virol. 2007; 81(8):3891-903. PMID:17267492.
34. Dong H, Liu L, Zou G, Zhao Y, Li Z, Lim SP, et al. Structural and functional analyses of a conserved hydrophobic pocket of flavivirus methyltransferase. The Journal of biological chemistry. 2010; 285 (42):32586-95. Epub 2010/08/06. doi:10.1074/jbc.M110.129197 PMID:20685660; PubMed Central PMCID:PMC2952261.
35. Dong H, Ren S, Li H, Shi PY. Separate molecules of West Nile virus methyltransferase can independently catalyze the N7 and 2'-O methylations of viral RNA cap. Virology. 2008; 377(1):1-6. Epub 2008/05/27. doi:10.1016/j.virol.2008.04.026 PMID:18501946; PubMed Central PMCID:PMC2494700.
36. Bhattacharya D, Hoover S, Falk SP, Weisblum B, Vestling M, Striker R. Phosphorylation of yellow fever virus NS5 alters methyltransferase activity. Virology. 2008; 380(2):276-84. PMID:18757072. doi:10. 1016/j.virol.2008.07.013
37. Kroschewski H, Lim SP, Butcher RE, Yap TL, Lescar J, Wright PJ, et al. Mutagenesis of the dengue virus type 2 NS5 methyltransferase domain. The Journal of biological chemistry. 2008; 283(28):19410-21. Epub 2008/05/13. doi:10.1074/jbc.M800613200 PMID:18469001.
38. Khromykh AA, Kenney MT, Westaway EG. trans-Complementation of flavivirus RNA polymerase gene NS5 by using Kunjin virus replicon-expressing BHK cells. J Virol. 1998; 72(9):7270-9. PMID:9696822
39. Lim SP, Sonntag LS, Noble C, Nilar SH, Ng RH, Zou G, et al. Small molecule inhibitors that selectively block dengue virus methyltransferase. The Journal of biological chemistry. 2011; 286(8):6233-40. Epub 2010/12/15. doi:10.1074/jbc.M110.179184 PMID:21147775; PubMed Central PMCID:PMC3057852.
40. Feng BY, Shelat A, Doman TN, Guy RK, Shoichet BK. High-throughput assays for promiscuous inhibitors. Nat Chem Biol. 2005; 1(3):146-8. Epub 2006/01/13. doi:10.1038/nchembio718 PMID:16408018.
41. Feng BY, Shoichet BK. A detergent-based assay for the detection of promiscuous inhibitors. Nat Protoc. 2006; 1(2):550-3. Epub 2006/12/28. doi:10.1038/nprot.2006.77 PMID:17191086; PubMed Central PMCID:PMC1544377.
42. Li SH, Dong H, Li XF, Xie X, Zhao H, Deng YQ, et al. Rational design of a flavivirus vaccine by abolishing viral RNA 2'-O methylation. J Virol. 2013; 87(10):5812-9. Epub 2013/03/15. doi:10.1128/JVI. 02806-12 JVI.02806-12 [pii]. PMID:23487465; PubMed Central PMCID:PMC3648161.
43. Dong H, Ray D, Ren S, Zhang B, Puig-Basagoiti F, Takagi Y, et al. Distinct RNA elements confer specificity to flavivirus RNA cap methylation events. J Virol. 2007; 81(9):4412-21. PMID:17301144.
44. Dong H, Fink K, Zust R, Lim SP, Qin CF, Shi PY. Flavivirus RNA methylation. J Gen Virol. 2014; 95(Pt 4):763-78. Epub 2014/02/04. doi:10.1099/vir.0.062208-0 vir.0.062208-0 [pii]. PMID:24486628.
45. Trott O, Olson AJ. AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem. 2010; 31(2):455-61. Epub 2009/06/06. doi:10.1002/jcc.21334 PMID:19499576; PubMed Central PMCID:PMC3041641.
46. O'Boyle NM, Banck M, James CA, Morley C, Vandermeersch T, Hutchison GR. Open Babel: An open chemical toolbox. J Cheminform. 2011; 3:33. Epub 2011/10/11. doi:10.1186/1758-2946-3-33 1758-2946-3-33 [pii]. PMID:21982300; PubMed Central PMCID:PMC3198950.