Identification of luteolin as enterovirus 71 and coxsackievirus A16 inhibitors through reporter viruses and cell viability-based screening

Viruses

Volumn 6, Issue 7, 2014, Pages 2778-2795

  Xu, Lin ^a   Su, Weiheng ^a   Jin, Jun ^a   Chen, Jiawen ^a   Li, Xiaojun ^a   Zhang, Xuyuan ^a   Sun, Meiyan ^a,b   Sun, Shiyang ^a   Fan, Peihu ^a   An, Dong ^a   Zhang, Huafei ^a   Zhang, Xiguang ^a   Kong, Wei ^a   Ma, Tonghui ^b   Jiang, Chunlai ^a  

^a JILIN UNIVERSITY   (China)

^b DALIAN MEDICAL UNIVERSITY   (China)

Author keywords

Antiviral drug discovery; Coxsackievirus A16; Enterovirus 71; High throughput assay; Luteolin; Reporter virus

Indexed keywords

ANTIVIRUS AGENT; ENHANCED GREEN FLUORESCENT PROTEIN; LUTEOLIN; VIRUS RNA; BIOLOGICAL PRODUCT; CAPSID PROTEIN; FLAVONOID; GALANGIN; GREEN FLUORESCENT PROTEIN; LUCIFERASE; QUERCETIN;

ARTICLE; BIOLOGICAL ACTIVITY; CELL VIABILITY ASSAY; CONTROLLED STUDY; COXSACKIE VIRUS; COXSACKIEVIRUS A16; ENTEROVIRUS 71; GENETIC ANALYSIS; HAND FOOT AND MOUTH DISEASE; HUMAN; HUMAN CELL; IN VITRO STUDY; INFECTION CONTROL; NONHUMAN; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA EXTRACTION; RNA REPLICATION; VIRUS INFECTION; VIRUS ISOLATION; VIRUS STRAIN; VIRUS TITRATION; ANIMAL; CELL SURVIVAL; CHLOROCEBUS AETHIOPS; DRUG EFFECTS; ENTEROVIRUS; GENE EXPRESSION REGULATION; GENETICS; HIGH THROUGHPUT SCREENING; IC50; METABOLISM; PHYSIOLOGY; REPLICON; REPORTER GENE; TUMOR CELL LINE; VERO CELL LINE; VIRUS REPLICATION;

ANIMALS; ANTIVIRAL AGENTS; BIOLOGICAL PRODUCTS; CAPSID PROTEINS; CELL LINE, TUMOR; CELL SURVIVAL; CERCOPITHECUS AETHIOPS; ENTEROVIRUS; ENTEROVIRUS A, HUMAN; FLAVONOIDS; GENE EXPRESSION REGULATION, VIRAL; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INHIBITORY CONCENTRATION 50; LUCIFERASES; LUTEOLIN; QUERCETIN; REPLICON; VERO CELLS; VIRUS REPLICATION;

EID: 84904562610     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v6072778     Document Type: Article

References (53)

1. Qiu, J. Enterovirus 71 infection: A new threat to global public health? Lancet Neurol. 2008, 7, 868-869.
2. Fujimoto, T.; Chikahira, M.; Yoshida, S.; Ebira, H.; Hasegawa, A.; Totsuka, A.; Nishio, O. Outbreak of central nervous system disease associated with hand, foot, and mouth disease in japan during the summer of 2000: Detection and molecular epidemiology of enterovirus 71. Microbiol. Immunol. 2002, 46, 621-627.
3. Chan, L.G.; Parashar, U.D.; Lye, M.S.; Ong, F.G.; Zaki, S.R.; Alexander, J.P.; Ho, K.K.; Han, L.L.; Pallansch, M.A.; Suleiman, A.B.; et al. Deaths of children during an outbreak of hand, foot, and mouth disease in sarawak, malaysia: Clinical and pathological characteristics of the disease. For the outbreak study group. Clin. Infect. Dis. 2000, 31, 678-683.
4. Ahmad, K. Hand, foot, and mouth disease outbreak reported in singapore. Lancet 2000, 356, 1338.
5. WHO. Wpro hand, foot and mouth disease situation update, 15 January 2014. Available online: http://www.wpro.who.int/emerging_diseases/HFMD.Biweekly.15Jan2014.pdf?ua=1 (accessed on 17 May 2014).
6. Ang, L.W.; Koh, B.K.; Chan, K.P.; Chua, L.T.; James, L.; Goh, K.T. Epidemiology and control of hand, foot and mouth disease in singapore, 2001-2007. Ann. Acad. Med. Singapore 2009, 38, 106-112.
7. Solomon, T.; Lewthwaite, P.; Perera, D.; Cardosa, M.J.; McMinn, P.; Ooi, M.H. Virology, epidemiology, pathogenesis, and control of enterovirus 71. Lancet Infect. Dis. 2010, 10, 778-790.
8. Rabenau, H.F.; Richter, M.; Doerr, H.W. Hand, foot and mouth disease: Seroprevalence of coxsackie a16 and enterovirus 71 in germany. Med. Microbiol. Immunol. 2010, 199, 45-51.
9. Li, W.; Yi, L.; Su, J.; Lu, J.; Zeng, H.; Guan, D.; Ma, C.; Zhang, W.; Xiao, H.; Li, H.; et al. Seroepidemiology of human enterovirus71 and coxsackievirusa16 among children in guangdong province, china. BMC Infect. Dis. 2013, 13, 322.
10. Yip, C.C.; Lau, S.K.; Zhou, B.; Zhang, M.X.; Tsoi, H.W.; Chan, K.H.; Chen, X.C.; Woo, P.C.; Yuen, K.Y. Emergence of enterovirus 71 "double-recombinant" strains belonging to a novel genotype d originating from southern china: First evidence for combination of intratypic and intertypic recombination events in ev71. Arch. Virol. 2010, 155, 1413-1424.
11. Zhang, Y.; Zhu, Z.; Yang, W.; Ren, J.; Tan, X.; Wang, Y.; Mao, N.; Xu, S.; Zhu, S.; Cui, A.; et al. An emerging recombinant human enterovirus 71 responsible for the 2008 outbreak of hand foot and mouth disease in fuyang city of china. Virol. J. 2010, 7, 94.
12. Shang, L.; Xu, M.; Yin, Z. Antiviral drug discovery for the treatment of enterovirus 71 infections. Antivir. Res. 2013, 97, 183-194.
13. Liang, Z.-L.; Mao, Q.-Y.; Wang, Y.-P.; Zhu, F.-C.; Li, J.-X.; Yao, X.; Gao, F.; Wu, X.; Xu, M.; Wang, J. Progress on the research and development of inactivated ev71 whole-virus vaccines. Hum. Vaccin. Immunother. 2013, 9, 1701-1705.
14. Zhu, Q.C.; Wang, Y.; Liu, Y.P.; Zhang, R.Q.; Li, X.; Su, W.H.; Long, F.; Luo, X.D.; Peng, T. Inhibition of enterovirus 71 replication by chrysosplenetin and penduletin. Eur. J. Pharm. Sci. 2011, 44, 392-398.
15. Wang, J.; Chen, X.; Wang, W.; Zhang, Y.; Yang, Z.; Jin, Y.; Ge, H.M.; Li, E.; Yang, G. Glycyrrhizic acid as the antiviral component of glycyrrhiza uralensis fisch. Against coxsackievirus a16 and enterovirus 71 of hand foot and mouth disease. J. Ethnopharmacol. 2013, 147, 114-121.
16. Yang, Y.; Xiu, J.; Zhang, X.; Zhang, L.; Yan, K.; Qin, C.; Liu, J. Antiviral effect of matrine against human enterovirus 71. Molecules 2012, 17, 10370-10376.
17. Chen, T.C.; Chang, H.Y.; Lin, P.F.; Chern, J.H.; Hsu, J.T.; Chang, C.Y.; Shih, S.R. Novel antiviral agent dtrip-22 targets rna-dependent rna polymerase of enterovirus 71. Antimicrob. Agents Chemother. 2009, 53, 2740-2747.
18. Zhang, X.; Song, Z.; Qin, B.; Zhang, X.; Chen, L.; Hu, Y.; Yuan, Z. Rupintrivir is a promising candidate for treating severe cases of enterovirus-71 infection: Evaluation of antiviral efficacy in a murine infection model. Antivir. Res. 2013, 97, 264-269.
19. Chen, T.C.; Liu, S.C.; Huang, P.N.; Chang, H.Y.; Chern, J.H.; Shih, S.R. Antiviral activity of pyridyl imidazolidinones against enterovirus 71 variants. J. Biomed. Sci. 2008, 15, 291-300.
20. Arita, M.; Wakita, T.; Shimizu, H. Characterization of pharmacologically active compounds that inhibit poliovirus and enterovirus 71 infectivity. J. Gen. Virol. 2008, 89, 2518-2530.
21. Noble, C.G.; Chen, Y.L.; Dong, H.; Gu, F.; Lim, S.P.; Schul, W.; Wang, Q.Y.; Shi, P.Y. Strategies for development of dengue virus inhibitors. Antivir. Res. 2010, 85, 450-462.
22. Gudmundsdottir, H.S.; Olafsdottir, K.; Franzdottir, S.R.; Andresdottir, V. Construction and characterization of an infectious molecular clone of maedi-visna virus that expresses green fluorescent protein. J. Virol. Meth. 2010, 168, 98-102.
23. Marriott, A.C.; Hornsey, C.A. Reverse genetics system for chandipura virus: Tagging the viral matrix protein with green fluorescent protein. Virus Res. 2011, 160, 166-172.
24. Kim, C.S.; Keum, S.J.; Jang, S.K. Generation of a cell culture-adapted hepatitis c virus with longer half life at physiological temperature. PLoS One 2011, 6, e22808.
25. Tsueng, G.; Tabor-Godwin, J.M.; Gopal, A.; Ruller, C.M.; Deline, S.; An, N.; Frausto, R.F.; Milner, R.; Crocker, S.J.; Whitton, J.L.; et al. Coxsackievirus preferentially replicates and induces cytopathic effects in undifferentiated neural progenitor cells. J. Virol. 2011, 85, 5718-5732.
26. Shang, B.; Deng, C.; Ye, H.; Xu, W.; Yuan, Z.; Shi, P.Y.; Zhang, B. Development and characterization of a stable egfp enterovirus 71 for antiviral screening. Antivir. Res. 2013, 97, 198-205.
27. Yamayoshi, S.; Yamashita, Y.; Li, J.; Hanagata, N.; Minowa, T.; Takemura, T.; Koike, S. Scavenger receptor b2 is a cellular receptor for enterovirus 71. Nat. Med. 2009, 15, 798-801.
28. Li, X.; Fan, P.; Jin, J.; Su, W.; An, D.; Xu, L.; Sun, S.; Zhang, Y.; Meng, X.; Gao, F.; et al. Establishment of cell lines with increased susceptibility to ev71/ca16 by stable overexpression of scarb2. Virol. J. 2013, 10, 250.
29. Jin, J.; Ma, H.; Xu, L.; An, D.; Sun, S.; Huang, X.; Kong, W.; Jiang, C. Development of a coxsackievirus a16 neutralization assay based on pseudoviruses for measurement of neutralizing antibody titer in human serum. J. Virol. Meth. 2013, 187, 362-367.
30. Jin, J.; Xu, L.; Guo, S.; Sun, S.; Zhang, S.; Zhu, C.; Kong, W.; Jiang, C. Safe and objective assay of enterovirus 71 neutralizing antibodies via pseudovirus. Chem. Res. Chin. Univ. 2012, 28, 91-95.
31. Troupin, C.; Dehee, A.; Schnuriger, A.; Vende, P.; Poncet, D.; Garbarg-Chenon, A. Rearranged genomic rna segments offer a new approach to the reverse genetics of rotaviruses. J. Virol. 2010, 84, 6711-6719.
32. Lu, J.; Yi, L.; Zhao, J.; Yu, J.; Chen, Y.; Lin, M.C.; Kung, H.F.; He, M.L. Enterovirus 71 disrupts interferon signaling by reducing the level of interferon receptor 1. J. Virol. 2012, 86, 3767-3776.
33. Reed, L.J.; Muench, H. A simple method of estimating fifty percent endpoints. Am. J. Hyg. 1938, 27, 493-497.
34. Marschall, M.; Freitag, M.; Weiler, S.; Sorg, G.; Stamminger, T. Recombinant green fluorescent protein-expressing human cytomegalovirus as a tool for screening antiviral agents. Antimicrob. Agents Chemother. 2000, 44, 1588-1597.
35. Zuo, J.; Quinn, K.K.; Kye, S.; Cooper, P.; Damoiseaux, R.; Krogstad, P. Fluoxetine is a potent inhibitor of coxsackievirus replication. Antimicrob. Agents Chemother. 2012, 56, 4838-4844.
36. Pirrone, V.; Passic, S.; Wigdahl, B.; Rando, R.F.; Labib, M.; Krebs, F.C. A styrene-alt-maleic acid copolymer is an effective inhibitor of r5 and x4 human immunodeficiency virus type 1 infection. J. Biomed. Biotechnol. 2010, 2010, 1-11.
37. Nijhuis, M.; van Maarseveen, N.; Schuurman, R.; Verkuijlen, S.; de Vos, M.; Hendriksen, K.; van Loon, A.M. Rapid and sensitive routine detection of all members of the genus enterovirus in different clinical specimens by real-time pcr. J. Clin. Microbiol. 2002, 40, 3666-3670.
38. Zhang, J.H. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J. Biomol. Screen. 1999, 4, 67-73.
39. Hung, H.C.; Chen, T.C.; Fang, M.Y.; Yen, K.J.; Shih, S.R.; Hsu, J.T.; Tseng, C.P. Inhibition of enterovirus 71 replication and the viral 3d polymerase by aurintricarboxylic acid. J. Antimicrob. Chemother 2010, 65, 676-683.
40. Chang, J.S.; Wang, K.C.; Chiang, L.C. Sheng-ma-ge-gen-tang inhibited enterovirus 71 infection in human foreskin fibroblast cell line. J. Ethnopharmacol. 2008, 119, 104-108.
41. Ho, H.Y.; Cheng, M.L.; Weng, S.F.; Leu, Y.L.; Chiu, D.T. Antiviral effect of epigallocatechin gallate on enterovirus 71. J. Agr. Food Chem. 2009, 57, 6140-6147.
42. Wang, C.Y.; Huang, S.C.; Zhang, Y.; Lai, Z.R.; Kung, S.H.; Chang, Y.S.; Lin, C.W. Antiviral ability of kalanchoe gracilis leaf extract against enterovirus 71 and coxsackievirus a16. Evid. base. Compl. Alternative Med. 2012, 2012, 503165.
43. Yang, Y.; Xiu, J.; Liu, J.; Zhang, L.; Li, X.; Xu, Y.; Qin, C.; Zhang, L. Chebulagic acid, a hydrolyzable tannin, exhibited antiviral activity in vitro and in vivo against human enterovirus 71. Int. J. Mol. Sci. 2013, 14, 9618-9627.
44. Campagnola, G.; Gong, P.; Peersen, O.B. High-throughput screening identification of poliovirus rna-dependent rna polymerase inhibitors. Antivir. Res. 2011, 91, 241-251.
45. Falah, N.; Violot, S.; Decimo, D.; Berri, F.; Foucault-Grunenwald, M.L.; Ohlmann, T.; Schuffenecker, I.; Morfin, F.; Lina, B.; Riteau, B.; et al. Ex vivo and in vivo inhibition of human rhinovirus replication by a new pseudosubstrate of viral 2a protease. J. Virol. 2012, 86, 691-704.
46. Lee, J.C.; Shih, S.R.; Chang, T.Y.; Tseng, H.Y.; Shih, Y.F.; Yen, K.J.; Chen, W.C.; Shie, J.J.; Fang, J.M.; Liang, P.H.; et al. A mammalian cell-based reverse two-hybrid system for functional analysis of 3c viral protease of human enterovirus 71. Anal. Biochem. 2008, 375, 115-123.
47. Puig-Basagoiti, F.; Deas, T.S.; Ren, P.; Tilgner, M.; Ferguson, D.M.; Shi, P.Y. High-throughput assays using a luciferase-expressing replicon, virus-like particles, and full-length virus for west nile virus drug discovery. Antimicrob. Agents Chemother. 2005, 49, 4980-4988.
48. Phillips, T.; Jenkinson, L.; McCrae, C.; Thong, B.; Unitt, J. Development of a high-throughput human rhinovirus infectivity cell-based assay for identifying antiviral compounds. J. Virol. Meth. 2011, 173, 182-188.
49. Tsuchiya, Y.; Shimizu, M.; Hiyama, Y.; Itoh, K.; Hashimoto, Y.; Nakayama, M.; Horie, T.; Morita, N. Antiviral activity of natural occurring flavonoids in vitro. Chem. Pharm. Bull. (Tokyo) 1985, 33, 3881-3886.
50. Vrijsen, R.; Everaert, L.; Boeye, A. Antiviral activity of flavones and potentiation by ascorbate. J. Gen. Virol. 1988, 69, 1749-1751.
51. Mehla, R.; Bivalkar-Mehla, S.; Chauhan, A. A flavonoid, luteolin, cripples hiv-1 by abrogation of tat function. PLoS One 2011, 6, e27915.
52. Manvar, D.; Mishra, M.; Kumar, S.; Pandey, V.N. Identification and evaluation of anti hepatitis c virus phytochemicals from eclipta alba. J. Ethnopharmacol. 2012, 144, 545-554.
53. Seelinger, G.; Merfort, I.; Schempp, C.M. Anti-oxidant, anti-inflammatory and anti-allergic activities of luteolin. Planta Medica 2008, 74, 1667-1677.