Discovery of berberine, abamectin and ivermectin as antivirals against chikungunya and other alphaviruses

Antiviral Research

Volumn 126, Issue , 2016, Pages 117-124

  Varghese, Finny S ^a   Kaukinen, Pasi ^a   Gläsker, Sabine ^b   Bespalov, Maxim ^a   Hanski, Leena ^a   Wennerberg, Krister ^a   Kümmerer, Beate M ^b   Ahola, Tero ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF BONN   (Germany)

Author keywords

Alphavirus; Antiviral screening; Chikungunya virus; RNA replication; Yellow fever virus

Indexed keywords

ABAMECTIN; AMPHOTERICIN B; ANTIVIRUS AGENT; AZAURIDINE; BERBERINE; BROMOCRIPTINE; CERIVASTATIN; DIMETHYL SULFOXIDE; FENRETINIDE; ISOQUINOLINE ALKALOID; IVERMECTIN; RENILLA LUCIFERIN 2 MONOOXYGENASE; VIRUS PROTEIN; VIRUS RNA; VIRAL PROTEIN; VIRUS DNA;

ALPHAVIRUS INFECTION; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; BHK CELL LINE; CHIKUNGUNYA; CONCENTRATION RESPONSE; CONTROLLED STUDY; DOWN REGULATION; EC50; FERMENTATION; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; LUCIFERASE ASSAY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON CELL; RNA SYNTHESIS; SEMLIKI FOREST VIRUS; SINDBIS VIRUS; STREPTOMYCES AVERMITILIS; VIRUS REPLICATION; WILD TYPE; YELLOW FEVER; ALPHAVIRUS; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; CELL LINE; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; DRUG EFFECTS; FLAVIVIRUS; GENETICS; HAMSTER; PHYSIOLOGY; REPLICON; TUMOR CELL LINE; VIROLOGY; YELLOW FEVER VIRUS;

ALPHAVIRUS; ANIMALS; ANTIVIRAL AGENTS; BERBERINE; CELL LINE; CELL LINE, TUMOR; CHIKUNGUNYA FEVER; CHIKUNGUNYA VIRUS; CRICETINAE; DNA, VIRAL; FLAVIVIRUS; HUMANS; IVERMECTIN; REPLICON; RNA, VIRAL; VIRAL PROTEINS; VIRUS REPLICATION; YELLOW FEVER VIRUS;

EID: 84953738119     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.12.012     Document Type: Article

References (36)

1. R. Abdelnabi, J. Neyts, and L. Delang Towards antivirals against chikungunya virus Antivir. Res. 121 2015 59 68
2. T. Ahola, T. Courderc, L.F. Ng, D. Hallengard, A. Powers, M. Lecuit, M. Esteban, A. Merits, P. Roques, and P. Liljestrom Therapeutics and vaccines against chikungunya virus Vector Borne Zoonotic Dis. 15 2015 250 257
3. A. Awasthi, M. Razzak, R. Al-Kassas, J. Harvey, and S. Garg An overview on chemical dervatization and stability aspects of selected avermectin derivatives Chem. Pharm. Bull. 60 2012 931 944
4. P.J. Bredenbeek A stable full-length yellow fever virus cDNA clone and the role of conserved RNA elements in flavivirus replication J. General Virol. 84 2003 1261 1268
5. A.C. Brehin, L. Rubrecht, M.E. Navarro-Sanchez, V. Marechal, M.P. Frenkiel, P. Lapalud, D. Laune, A.A. Sall, and P. Despres Production and characterization of mouse monoclonal antibodies reactive to chikungunya envelope E2 glycoprotein Virology 371 2008 185 195
6. S. Briolant, D. Garin, N. Scaramozzino, A. Jouan, and J.M. Crance In vitro inhibition of chikungunya and Semliki Forest viruses replication by antiviral compounds: synergistic effect of interferon-α and ribavirin combination Antivir. Res. 61 2004 111 117
7. F.J. Burt, M.S. Rolph, N.E. Rulli, S. Mahalingam, and M.T. Heise Chikungunya: a re-emerging virus Lancet 379 2012 662 671
8. W.C. Campbell History of avermectin and ivermectin, with notes on the history of other macrocyclic lactone antiparasitic agents Curr. Pharm. Biotechnol. 13 2012 853 865
9. M. Carocci, S.M. Hinshaw, M.A. Rodgers, V.A. Villareal, D.J. Burri, R. Pilankatta, N.P. Maharaj, M.U. Gack, E.J. Stavale, K.L. Warfield, and P.L. Yang The bioactive lipid 4-hydroxyphenyl retinamide inhibits flavivirus replication Antimicrob. Agents Chemother. 59 2015 85 95
10. L.W. Chin, Y.W. Cheng, S.S. Lin, Y.Y. Lai, L.Y. Lin, M.Y. Chou, M.C. Chou, and C.C. Yang Anti-herpes simplex virus effects of berberine from Coptidis rhizoma, a major component of a Chinese herbal medicine, Ching-Wei-San Arch. Virol. 155 2010 1933 1941
11. A. Chopra, M. Saluja, and A. Venugopalan Effectiveness of chloroquine and inflammatory Cytokine response in patients with early persistent musculoskeletal pain and arthritis following chikungunya virus infection Arthritis Rheumatol. 66 2014 319 326
12. M. Fischer, J.E. Staples Arboviral Diseases Branch N.C.f.E. Zoonotic Infectious Diseases C.D.C Notes from the field: chikungunya virus spreads in the americas - Caribbean and South america, 2013-2014 MMWR. Morb. Mortal. Wkly. Rep. 63 2014 500 501
13. J.E. Fraser, S. Watanabe, C. Wang, W.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
14. K. Hayashi, K. Minoda, Y. Nagaoka, T. Hayashi, and S. Uesato Antiviral activity of berberine and related compounds against human cytomegalovirus Bioorg. Med. Chem. Lett. 17 2007 1562 1564
15. Y.C. Hsu, N.C. Chen, P.C. Chen, C.C. Wang, W.C. Cheng, and H.N. Wu Identification of a small-molecule inhibitor of dengue virus using a replicon system Arch. Virol. 157 2012 681 688
16. K. Kallio, K. Hellstrom, G. Balistreri, P. Spuul, E. Jokitalo, and T. Ahola Template RNA length determines the size of replication complex spherules for Semliki Forest virus J. Virol. 87 2013 9125 9134
17. P. Kaur, and J.J. Chu Chikungunya virus: an update on antiviral development and challenges Drug Discov. Today 18 2013 969 983
18. H.Y. Kim, X. Li, C.T. Jones, C.M. Rice, J.M. Garcia, A. Genovesio, M.A. Hansen, and M.P. Windisch Development of a multiplex phenotypic cell-based high throughput screening assay to identify novel hepatitis C virus antivirals Antivir. Res. 99 2013 6 11
19. W. Kong, J. Wei, P. Abidi, M. Lin, S. Inaba, C. Li, Y. Wang, Z. Wang, S. Si, H. Pan, S. Wang, J. Wu, Y. Wang, Z. Li, J. Liu, and J.D. Jiang Berberine is a novel cholesterol-lowering drug working through a unique mechanism distinct from statins Nat. Med. 10 2004 1344 1351
20. L. Kääriäinen, and T. Ahola Functions of alphavirus nonstructural proteins in RNA replication Prog. Nucleic Acid. Res. 71 2002 187 222
21. I. Leparc-Goffart, A. Nougairede, S. Cassadou, C. Prat, and X. de Lamballerie Chikungunya in the Americas Lancet 383 2014 514
22. P. Liljeström, S. Lusa, D. Huylebroeck, and H. Garoff In vitro mutagenesis of a full-length cDNA clone of Semliki Forest virus: the small 6,000-molecular-weight membrane protein modulates virus release J. Virol. 65 1991 4107 4113
23. T. Lynagh, and J.W. Lynch Ivermectin binding sites in human and invertebrate Cys-loop receptors Trends Pharmacol. Sci. 33 2012 432 441
24. E. Mastrangelo, M. Pezzullo, T. De Burghgraeve, S. Kaptein, B. Pastorino, K. Dallmeier, X. de Lamballerie, J. Neyts, A.M. Hanson, D.N. Frick, M. Bolognesi, and M. Milani Ivermectin is a potent inhibitor of flavivirus replication specifically targeting NS3 helicase activity: new prospects for an old drug J. Antimicrob. Chemother. 67 2012 1884 1894
25. S. Omura Ivermectin: 25 years and still going strong Int. J. Antimicrob. Agents 31 2008 91 98
26. W. Peng, D.C. Peltier, M.J. Larsen, P.D. Kirchhoff, S.D. Larsen, R.R. Neubig, and D.J. Miller Identification of thieno[3,2-b]pyrrole derivatives as novel small molecule inhibitors of neurotropic alphaviruses J. Infect. Dis. 199 2009 950 957
27. L. Pohjala, A. Utt, M. Varjak, A. Lulla, A. Merits, T. Ahola, and P. Tammela Inhibitors of alphavirus entry and replication identified with a stable chikungunya replicon cell line and virus-based assays PLoS One 6 2011 e28923
28. B. Rada, and M. Dragúň Antiviral action and selectivity of 6-azauridine Ann. N. Y. Acad. Sci. 284 1977 410 417
29. C.M. Rice, R. Levis, J.H. Strauss, and H.V. Huang Production of infectious RNA transcripts from Sindbis virus cDNA clones: mapping of lethal mutations, rescue of a temperature-sensitive marker, and in vitro mutagenesis to generate defined mutants J. Virol. 61 1987 3809 3819
30. H.B. Shin, M.S. Choi, C.M. Yi, J. Lee, N.J. Kim, and K.S. Inn Inhibition of respiratory syncytial virus replication and virus-induced p38 kinase activity by berberine Int. Immunopharmacol. 27 2015 65 68
31. S. Song, M. Qiu, Y. Chu, D. Chen, X. Wang, A. Su, and Z. Wu Downregulation of cellular c-Jun N-terminal protein kinase and NF-kappaB activation by berberine may result in inhibition of herpes simplex virus replication Antimicrob. Agents Chemother. 58 2014 5068 5078
32. S.D. Thiberville, N. Moyen, L. Dupuis-Maguiraga, A. Nougairede, E.A. Gould, P. Roques, and X. de Lamballerie Chikungunya fever: epidemiology, clinical syndrome, pathogenesis and therapy Antivir. Res. 99 2013 345 370
33. M. Tillhon, L.M. Guaman Ortiz, P. Lombardi, and A.I. Scovassi Berberine: new perspectives for old remedies Biochem. Pharmacol. 84 2012 1260 1267
34. S.C. Weaver, and N.L. Forrester Chikungunya: evolutionary history and recent epidemic spread Antivir. Res. 120 2015 32 39
35. Y. Wu, J.Q. Li, Y.J. Kim, J. Wu, Q. Wang, and Y. Hao In vivo and in vitro antiviral effects of berberine on influenza virus Chin. J. Integr. Med. 17 2011 444 452
36. J. Yao, W. Kong, and J. Jiang Learning from berberine: treating chronic diseases through multiple targets Sci. China. Life Sci. 58 9 2015 854 859 Epub 2013 Oct 30