The antiviral effect of baicalin on enterovirus 71 in vitro

Viruses

Volumn 7, Issue 8, 2015, Pages 4756-4771

  Li, X ^d   Liu, Yuanyuan ^b   Wu, Tingting ^c   Jin, Yue ^a   Cheng, Jianpin ^a   Wan, Changbiao ^a   Qian, Weihe ^a   Xing, Fei ^a   Shi, Weifeng ^d  

^a XUZHOU MEDICAL UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

^c Fourth People's Hospital of Huai'an   (China)

^d THE THIRD AFFILIATED HOSPITAL OF SOOCHOW UNIVERSITY   (China)

Author keywords

3D polymerase; Apoptosis; Baicalin; Enterovirus 71

Indexed keywords

BAICALIN; CASPASE 3; FAS LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN VP16; SYNAPTOTAGMIN I; ANTIVIRUS AGENT; DNA DIRECTED RNA POLYMERASE; FLAVONOID;

ANTIVIRAL ACTIVITY; APOPTOSIS; APOPTOSIS ASSAY; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY ASSAY; ENTEROVIRUS 71; ENTEROVIRUS INFECTION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; MTT ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RHABDOMYOSARCOMA CELL; VIRUS REPLICATION; WESTERN BLOTTING; ANTAGONISTS AND INHIBITORS; CELL LINE; CHEMISTRY; DRUG EFFECTS; ENTEROVIRUS A; ISOLATION AND PURIFICATION; MICROBIAL SENSITIVITY TEST; SCUTELLARIA; SIGNAL TRANSDUCTION;

ANTIVIRAL AGENTS; CELL LINE; DNA-DIRECTED RNA POLYMERASES; ENTEROVIRUS A, HUMAN; FAS LIGAND PROTEIN; FLAVONOIDS; HUMANS; MICROBIAL SENSITIVITY TESTS; SCUTELLARIA; SIGNAL TRANSDUCTION;

EID: 84941106240     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7082841     Document Type: Article

References (52)

1. Lin, T.Y.; Liu, Y.C.; Jheng, J.R.; Tsai, H.P.; Jan, J.T.; Wong, W.R.; Horng, J.T. Anti-enterovirus 71 activity screening of Chinese herbs with anti-infection and inflammation activities. Am. J. Chin. Med. 2009, 37, 143-158. [CrossRef] [PubMed]
2. Han, J.F.; Cao, R.Y.; Tian, X.; Yu, M.; Qin, E.D.; Qin, C.F. Producing infectious enterovirus type 71 in a rapid strategy. Virol. J. 2010, 7, e116. [CrossRef] [PubMed]
3. Kiener, T.K.; Jia, Q.; Lim, X.F.; He, F.; Meng, T.; Chow, V.T.; Kwang, J. Characterization and specificity of the linear epitope of the enterovirus 71 VP2 protein. Virol. J. 2012, 9, e55. [CrossRef] [PubMed]
4. Lu, G.; Qi, J.; Chen, Z.; Xu, X.; Gao, F.; Lin, D.; Qian, W.; Liu, H.; Jiang, H.; Yan, J.; et al. Enterovirus 71 and coxsackievirus A16 3C proteases: Binding to rupintrivir and their substrates and anti-hand, foot, and mouth disease virus drug design. J. Virol. 2011, 85, 10319-10331. [PubMed]
5. Wei, Y.; Shi, L.; Wang, K.; Liu, M.; Yang, Q.; Yang, Z.; Ke, S. Discovery of Gramine Derivatives That Inhibit the Early Stage of EV71 Replication in Vitro. Molecules 2014, 19, 8949-8964. [CrossRef] [PubMed]
6. Zu, M.; Yang, F.; Zhou, W.; Liu, A.; Du, G.; Zheng, L. In vitro anti-influenza virus and anti-inflammatory activities of theaflavin derivatives. Antivir. Res. 2012, 94, 217-224. [CrossRef] [PubMed]
7. Huang, X.; Lu, Z.; Lv, Z.; Yu, T.; Yang, P.; Shen, Y.; Ding, Y.; Fu, D.; Zhang, X.; Fu, Q.; et al. The Fas/Fas ligand death receptor pathway contributes to phenylalanine-induced apoptosis in cortical neurons. PLoS ONE 2013, 8, e71553. [PubMed]
8. Shi, W.; Li, X.; Hou, X.; Peng, H.; Jiang, Q.; Shi, M.; Ji, Y.; Liu, X.; Liu, J.; et al. Differential apoptosis gene expressions of rhabdomyosarcoma cells in response to enterovirus 71 infection. BMC Infect. Dis. 2012, 12, e327.
9. Zhu, G.; Zheng, Y.; Zhang, L.; Shi, Y.; Li, W.; Liu, Z.; Peng, B.; Yin, J.; Liu, W.; He, X. Coxsackievirus A16 infection triggers apoptosis in RD cells by inducing ER stress. Biochem. Biophys. Res. Commun. 2013, 441, 856-861. [CrossRef] [PubMed]
10. Zhang, X.; Tang, Q.; Xu, L. Herpes simplex virus 2 infects human endothelial ECV304 cells and induces cell apoptosis synergistically with ox-LDL. J. Toxicol. Sci. 2014, 39, 909-917. [CrossRef] [PubMed]
11. Boonnak, K.; Vogel, L.; Feldmann, F.; Feldmann, H.; Legge, K.L.; Subbarao, K. Lymphopenia Associated with Highly Virulent H5N1 Virus Infection Due to Plasmacytoid Dendritic Cell-Mediated Apoptosis of T Cells. J. Immunol. 2014, 192, 5906-5912. [CrossRef] [PubMed]
12. Vachirayonstien, T.; Promkhatkaew, D.; Bunjob, M.; Chueyprom, A.; Chavalittumrong, P.; Sawanpanyalert, P. Molecular evaluation of extracellular activity of medicinal herb Clinacanthus nutans against herpes simplex virus type-2. Natl. Prod. Res. 2010, 24, 236-245. [CrossRef] [PubMed]
13. Zhou, W.; Zhang, X.Y. Research progress of Chinese herbal medicine Radix isatidis (banlangen). Am. J. Chin. Med. 2013, 41, 743-764. [CrossRef] [PubMed]
14. Xu, X.F.; Cai, B.L.; Guan, S.M.; Li, Y.; Wu, J.Z.; Wang, Y.; Liu, B. Baicalin induces human mucoepidermoid carcinoma Mc3 cells apoptosis in vitro and in vivo. Investig. New Drugs 2011, 29, 637-645. [CrossRef] [PubMed]
15. Hour, M.J.; Huang, S.H.; Chang, C.Y.; Lin, Y.K.; Wang, C.Y.; Chang, Y.S.; Lin, C.W. Baicalein, ethyl acetate, and chloroform extracts of Scutellaria baicalensis inhibit the neuraminidase activity of pandemic 2009 H1N1 and seasonal influenza A viruses. Evid. Based Complement. Altern. Med. 2013, 2013. [CrossRef] [PubMed]
16. Li, B.Q.; Fu, T.; Dongyan, Y.; Mikovits, J.A.; Ruscetti, F.W.; Wang, J.M. Flavonoid baicalin inhibits HIV-1 infection at the level of viral entry. Biochem. Biophys. Res. Commun. 2000, 276, 534-538. [CrossRef] [PubMed]
17. Cheng, Y.; Ping, J.; Xu, H.D.; Fu, H.J.; Zhou, Z.H. Synergistic effect of a novel oxymatrine-baicalin combination against hepatitis B virus replication, alpha smooth muscle actin expression and type I collagen synthesis in vitro. World J. Gastroenterol. 2006, 12, 5153-5159. [PubMed]
18. Wan, Q.; Wang, H.; Han, X.; Lin, Y.; Yang, Y.; Gu, L.; Zhao, J.; Wang, L.; Huang, L.; Li, Y.; et al. Baicalin inhibits TLR7/MYD88 signaling pathway activation to suppress lung inflammation in mice infected with influenza A virus. Biomed. Rep. 2014, 2, 437-441. [PubMed]
19. Liu, J.; Yang, Y.; Xu, Y.; Ma, C.; Qin, C.; Zhang, L. Lycorine reduces mortality of human enterovirus 71-infected mice by inhibiting virus replication. Virol. J. 2011, 8, e483. [CrossRef] [PubMed]
20. Hung, H.C.; Chen, T.C.; Fang, M.Y.; Yen, K.J.; Shih, S.R.; Hsu, J.T.A.; Tseng, C.P. Inhibition of enterovirus 71 replication and the viral 3D polymerase by aurintricarboxylic acid. J. Antimicrob. Chemother. 2010, 65, 676-683. [CrossRef] [PubMed]
21. Lin, C.W.; Wu, C.F.; Hsiao, N.W.; Chang, C.Y.; Li, S.W.; Wan, L.; Lin, Y.J.; Lin, W.Y. Aloe-emodin is an interferon-inducing agent with antiviral activity against Japanese encephalitis virus and enterovirus 71. Int. J. Antimicrob. Agents 2008, 32, 355-359. [CrossRef] [PubMed]
22. Schnellrath, L.C.; Damaso, C.R. Potent antiviral activity of brequinar against the emerging Cantagalo virus in cell culture. Int. J. Antimicrob. Agents 2011, 38, 435-441. [CrossRef] [PubMed]
23. Zhu, W.; Chiu, L.; Ooi, V.; Chan, P.; Ang, P. Antiviral property and mode of action of a sulphated polysaccharide from Sargassum patens against herpes simplex virus type 2. Int. J. Antimicrob. Agents 2004, 24, 279-283. [CrossRef] [PubMed]
24. Song, X.; Yin, Z.; Li, L.; Cheng, A.; Jia, R.; Xu, J.; Wang, Y.; Yao, X.; Lv, C.; Zhao, X.; et al. Antiviral activity of sulfated Chuanminshen violaceum polysaccharide against duck enteritis virus in vitro. Antivir. Res. 2013, 98, 344-351. [PubMed]
25. Shin, H.B.; Choi, M.S.; Ryu, B.; Lee, N.R.; Kim, H.I.; Choi, H.E.; Chang, J.; Lee, K.T.; Jang, D.S.; Inn, K.S.; et al. Antiviral activity of carnosic acid against respiratory syncytial virus. Virol. J. 2013, 10, e303.
26. Choi, Y.H.; Kim, G.Y.; Lee, H.H. Anti-inflammatory effects of cordycepin in lipopolysaccharide-stimulated raW 264.7 macrophages through Toll-like receptor 4-mediated suppression of mitogen-activated protein kinases and NF-κB signaling pathways. Drug Des. Dev. Ther. 2014, 8, 1941-1953.
27. Jung, Y.C.; Kim, M.E.; Yoon, J.H.; Park, P.R.; Youn, H.Y.; Lee, H.W.; Lee, J.S. Anti-inflammatory effects of galangin on lipopolysaccharide-activated macrophages via ERK and NF-κB pathway regulation. Immunopharmacol. Immunotoxicol. 2014, 36, 426-432. [CrossRef] [PubMed]
28. Zhang, W.; Qiao, H.; Lv, Y.; Wang, J.; Chen, X.; Hou, Y.; Tan, R.; Li, E. Apigenin inhibits enterovirus-71 infection by disrupting viral RNA association with trans-acting factors. PLoS ONE 2014, 9, e110429. [CrossRef] [PubMed]
29. Xu, L.; Su, W.; Jin, J.; Chen, J.; Li, X.; Zhang, X.; Sun, M.; Sun, S.; Fan, P.; An, D.; et al. Identification of luteolin as enterovirus 71 and coxsackievirus A16 inhibitors through reporter viruses and cell viability-based screening. Viruses 2014, 6, 2778-2795. [PubMed]
30. Burnett, B.; Jia, Q.; Zhao, Y.; Levy, R. A medicinal extract of Scutellaria baicalensis and Acacia catechu acts as a dual inhibitor of cyclooxygenase and 5-lipoxygenase to reduce inflammation. J. Med. Food 2007, 10, 442-451. [CrossRef] [PubMed]
31. Tseng, Y.; Wu, Y.; Leu, Y.; Yeh, S.; Chou, C. Scutellariae radix suppresses hepatitis B virus production in human hepatoma cells. Front. Biosci. (Elite Ed.) 2009, 2, 1538-1547. [CrossRef]
32. Nayak, M.K.; Agrawal, A.S.; Bose, S.; Naskar, S.; Bhowmick, R.; Chakrabarti, S.; Sarkar, S.; Chawla-Sarkar, M. Antiviral activity of baicalin against influenza virus H1N1-pdm09 is due to modulation of NS1-mediated cellular innate immune responses. J. Antimicrob. Chemother. 2014, 69, 1298-1310.
33. Garcia, C.C.; Acosta, E.G.; Carro, A.C.; Fernandez Belmonte, M.C.; Bomben, R.; Duschatzky, C.B.; Perotti, M.; Schuff, C.; Damonte, E.B. Virucidal activity and chemical composition of essential oils from aromatic plants of central west Argentina. Nat. Prod. Commun. 2010, 5, 1307-1310. [PubMed]
34. Schnitzler, P.; Reichling, J. Efficacy of plant products against herpetic infections. HNO 2011, 59, 1176-1184. [CrossRef] [PubMed]
35. Faral-Tello, P.; Mirazo, S.; Dutra, C.; Pérez, A.; Geis-Asteggiante, L.; Frabasile, S.; Koncke, E.; Davyt, D.; Cavallaro, L.; Heinzen, H.; et al. Cytotoxic, virucidal, and antiviral activity of South American plant and algae extracts. Sci. World J. 2012, 2012. [CrossRef] [PubMed]
36. Lu, J.; He, Y.Q.; Yi, L.N.; Zan, H.; Kung, H.F.; He, M.L. Viral kinetics of enterovirus 71 in human abdomyosarcoma cells. World J. Gastroenterol. 2011, 17, 4135-4142. [CrossRef] [PubMed]
37. Lin, J.Y.; Chen, T.C.; Weng, K.F.; Chang, S.C.; Chen, L.L.; Shih, S.R. Viral and host proteins involved in picornavirus life cycle. J. Biomed. Sci. 2009, 16, e103. [CrossRef] [PubMed]
38. Shang, L.; Xu, M.; Yin, Z. Antiviral drug discovery for the treatment of enterovirus 71 infections. Antivir. Res. 2013, 97, 183-194. [CrossRef] [PubMed]
39. Wang, B.; Xi, X.; Lei, X.; Zhang, X.; Cui, S.; Wang, J.; Jin, Q.; Zhao, Z. Enterovirus 71 protease 2A pro targets MAVS to inhibit anti-viral type I interferon responses. PLoS Pathog. 2013, 9, e1003231. [CrossRef] [PubMed]
40. Jiang, H.; Weng, L.; Zhang, N.; Arita, M.; Li, R.; Chen, L.; Toyoda, T. Biochemical characterization of enterovirus 71 3D RNA polymerase. Biochim. Biophys. Acta Gene Regul. Mech. 2011, 1809, 211-219. [CrossRef] [PubMed]
41. Chen, T.C.; Weng, K.F.; Chang, S.C.; Lin, J.Y.; Huang, P.N.; Shih, S.R. Development of antiviral agents for enteroviruses. J. Antimicrob. Chemother. 2008, 62, 1169-1173. [CrossRef] [PubMed]
42. Liu, Y.; Wimmer, E.; Paul, A.V. Cis-acting RNA elements in human and animal plus-strand RNA viruses. Biochim. Biophys. Acta Gene Regul. Mech. 2009, 1789, 495-517. [CrossRef] [PubMed]
43. Nguyen, M.; Haenni, A.L. Expression strategies of ambisense viruses. Virus Res. 2003, 93, 141-150. [CrossRef]
44. Kaiser, W.J.; Upton, J.W.; Mocarski, E.S. Viral modulation of programmed necrosis. Curr. Opin. Virol. 2013, 3, 296-306. [CrossRef] [PubMed]
45. Iwai, A.; Shiozaki, T.; Miyazaki, T. Relevance of signaling molecules for apoptosis induction on influenza A virus replication. Biochem. Biophys. Res. Commun. 2013, 441, 531-537. [CrossRef] [PubMed]
46. Pruijssers, A.J.; Hengel, H.; Abel, T.W.; Dermody, T.S. Apoptosis induction influences reovirus replication and virulence in newborn mice. J. Virol. 2013, 87, 12980-12989. [CrossRef] [PubMed]
47. Holloway, G.; Truong, T.T.; Coulson, B.S. Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-κB. J. Virol. 2009, 83, 4942-4951. [CrossRef] [PubMed]
48. Liu, Y.; Liu, H.; Zou, J.; Zhang, B.; Yuan, Z. Dengue virus subgenomic RNA induces apoptosis through the Bcl-2-mediated PI3k/Akt signaling pathway. Virology 2014, 448, 15-25. [CrossRef] [PubMed]
49. Mankan, A.K.; Lawless, M.W.; Gray, S.G.; Kelleher, D.; McManus, R. NF-κB regulation: The nuclear response. J. Cell. Mol. Med. 2009, 13, 631-643. [CrossRef] [PubMed]
50. Tung, W.H.; Hsieh, H.L.; Lee, I.T.; Yang, C.M. Enterovirus 71 modulates a COX-2/PGE2/cAMP-dependent viral replication in human neuroblastoma cells: Role of the c-Src/EGFR/p42/p44 MAPK/CREB signaling pathway. J. Cell. Biochem. 2011, 112, 559-570. [CrossRef] [PubMed]
51. Kumar, N.; Xin, Z.Y.; Liang, Y.; Ly, H. NF-κB signaling differentially regulates influenza virus RNA synthesis. J. Virol. 2008, 82, 9880-9889. [CrossRef] [PubMed]
52. La Frazia, S.; Amici, C.; Santoro, M.G. Antiviral activity of proteasome inhibitors in herpes simplex virus-1 infection: Role of nuclear factor-κB. Antivir. Ther. 2006, 11, 995-1004. [PubMed]