Downregulation of cellular c-Jun N-terminal protein kinase and NF-κB activation by berberine may result in inhibition of herpes simplex virus replication

Antimicrobial Agents and Chemotherapy

Volumn 58, Issue 9, 2014, Pages 5068-5078

  Song, Siwei ^a   Qiu, Min ^a   Chu, Ying ^a   Chen, Deyan ^a   Wang, Xiaohui ^a   Su, Airong ^a   Wu, Zhiwei ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACICLOVIR; BERBERINE; GENOMIC DNA; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PROTEIN P63; STRESS ACTIVATED PROTEIN KINASE; VIRUS RNA; I KAPPA B; NF-KAPPAB INHIBITOR ALPHA;

ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA REPLICATION; DOWN REGULATION; GENE EXPRESSION; HERPES SIMPLEX VIRUS 1; HERPES SIMPLEX VIRUS 2; HERPES VIRUS INFECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; RNA TRANSCRIPTION; VIRUS ATTACHMENT; VIRUS ENTRY; VIRUS INHIBITION; VIRUS REPLICATION; CELL LINE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; HUMAN; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SIMPLEXVIRUS;

BERBERINE; CELL LINE; DNA REPLICATION; DOWN-REGULATION; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; I-KAPPA B PROTEINS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SIMPLEXVIRUS; VIRUS REPLICATION;

EID: 84906081424     PISSN: 00664804     EISSN: 10986596     Source Type: Journal    
DOI: 10.1128/AAC.02427-14     Document Type: Article

References (62)

1. Lafferty WE, Downey L, Celum C, Wald A. 2000. Herpes simplex virus type 1 as a cause of genital herpes: impact on surveillance and prevention. J. Infect. Dis. 181:1454-1457. http://dx.doi.org/10.1086/315395.
2. Whitley RJ, Roizman B. 2001. Herpes simplex virus infections. Lancet 357:1513-1518. http://dx.doi.org/10.1016/S0140-6736(00)04638-9.
3. Corey L, Wald A, Celum CL, Quinn TC. 2004. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlapping epidemics. J. Acquir. Immune Defic. Syndr. 35:435-445. http://dx.doi.org/10. 1097/00126334-200404150-00001.
4. Freeman EE, Weiss HA, Glynn JR, Cross PL, Whitworth JA, Hayes RJ. 2006. Herpes simplex virus 2 infection increases HIV acquisition in men and women: systematic review and meta-analysis of longitudinal studies. AIDS 20:73-83. http://dx.doi.org/10.1097/01.aids.0000198081.09337.a7.
5. Mbopi-Kéou F-X, Grésenguet G, Mayaud P, Weiss HA, Gopal R, Matta M, Paul J-L, Brown DW, Hayes RJ, Mabey DC. 2000. Interactions between herpes simplex virus type 2 and human immunodeficiency virus type 1 infection in African women: opportunities for intervention. J. Infect. Dis. 182:1090-1096. http://dx.doi.org/10.1086/315836.
6. Wald A, Link K. 2002. Risk of human immunodeficiency virus infection in herpes simplex virus type 2-seropositive persons: a meta-analysis. J. Infect. Dis. 185:45-52. http://dx.doi.org/10.1086/338231.
7. Roberts CM, Pfister JR, Spear SJ. 2003. Increasing proportion of herpes simplex virus type 1 as a cause of genital herpes infection in college students. Sex. Transm. Dis. 30:797-800. http://dx.doi.org/10.1097/01.OLQ.0000092387. 58746.C7.
8. De Clercq E, Field HJ. 2006. Antiviral prodrugs-the development of successful prodrug strategies for antiviral chemotherapy. Br. J. Pharmacol. 147:1-11. http://dx.doi.org/10.1038/sj.bjp.0706446.
9. Earnshaw D, Bacon T, Darlison S, Edmonds K, Perkins R, Hodge RV. 1992. Mode of antiviral action of penciclovir in MRC-5 cells infected with herpes simplex virus type 1 (HSV-1), HSV-2, and varicella-zoster virus. Antimicrob. Agents Chemother. 36:2747-2757. http://dx.doi.org/10.1128/AAC.36.12.2747.
10. Wald A, Zeh J, Barnum G, Davis L, Corey L. 1996. Suppression of subclinical shedding of herpes simplex virus type 2 with acyclovir. Ann. Intern. Med. 124:8-15. http://dx.doi.org/10.7326/0003-4819-124-1-Part-1-199601010- 00002.
11. Reyes M, Shaik NS, Graber JM, Nisenbaum R, Wetherall NT, Fukuda K, Reeves WC. 2003. Acyclovir-resistant genital herpes among persons attending sexually transmitted disease and human immunodeficiency virus clinics. Arch. Intern. Med. 163:76-80. http://dx.doi.org/10.1001/archinte.163.1.76.
12. Shin YK, Weinberg A, Spruance S, Bernard M, Bacon TH, Boon RJ, Levin MJ. 2003. Susceptibility of herpes simplex virus isolates to nucleoside analogues and the proportion of nucleoside-resistant variants after repeated topical application of penciclovir to recurrent herpes labialis. J. Infect. Dis. 187:1241-1245. http://dx.doi.org/10.1086/373993.
13. Stránská R, Schuurman R, Nienhuis E, Goedegebuure IW, Polman M, Weel JF, Wertheim-Van Dillen PM, Berkhout RJ, van Loon AM. 2005. Survey of acyclovir-resistant herpes simplex virus in the Netherlands: prevalence and characterization. J. Clin. Virol. 32:7-18. http://dx.doi.org/10. 1016/j.jcv.2004.04.002.
14. Hsu W-H, Hsieh Y-S, Kuo H-C, Teng C-Y, Huang H-I, Wang C-J, Yang S-F, Liou Y-S, Kuo W-H. 2007. Berberine induces apoptosis in SW620 human colonic carcinoma cells through generation of reactive oxygen species and activation of JNK/p38 MAPK and FasL. Arch. Toxicol. 81:719-728. http://dx.doi.org/10.1007/ s00204-006-0169-y.
15. Choi MS, Yuk DY, Oh JH, Jung HY, Han SB, Moon DC, Hong JT. 2008. Berberine inhibits human neuroblastoma cell growth through induction of p53-dependent apoptosis. Anticancer Res. 28:3777-3784.
16. Tang J, Feng YB, Tsao S, Wang N, Curtain R, Wang YW. 2009. Berberine and Coptidis Rhizoma as novel antineoplastic agents: a review of traditional use and biomedical investigations. J. Ethnopharmacol. 126:5-17. http://dx.doi.org/10. 1016/j.jep.2009.08.009.
17. Pandey MK, Sung B, Kunnumakkara AB, Sethi G, Chaturvedi MM, Aggarwal BB. 2008. Berberine modifies cysteine 179 of IκBα kinase, suppresses nuclear factor-κB-regulated antiapoptotic gene products, and potentiates apoptosis. Cancer Res. 68:5370-5379. http://dx.doi.org/10.1158/0008-5472.CAN-08- 0511.
18. Cui G, Qin X, Zhang Y, Gong Z, Ge B, Zang YQ. 2009. Berberine differentially modulates the activities of ERK, p38 MAPK, and JNK to suppress Th17 and Th1 T cell differentiation in type 1 diabetic mice. J. Biol. Chem. 284:28420-28429. http://dx.doi.org/10.1074/jbc.M109.012674.
19. McLean C, Erturk M, Jennings R, Challanain DN, Minson A, Duncan I, Boursnell M, Inglis S. 1994. Protective vaccination against primary and recurrent disease caused by herpes simplex virus (HSV) type 2 using a genetically disabled HSV-1. J. Infect. Dis. 170:1100-1109. http://dx.doi.org/10. 1093/infdis/170.5.1100.
20. Qiu M, Chen Y, Chu Y, Song S, Yang N, Gao J, Wu Z. 2013. Zinc ionophores pyrithione inhibits herpes simplex virus replication through interfering with proteasome function and NF-κB activation. Antiviral Res. 100:44-53. http://dx.doi.org/10.1016/j.antiviral.2013.07.001.
21. Chou T, Hayball M. 1991. CalcuSyn: Windows software for dose effect analysis. CalcuSyn, Ferguson, MO.
22. Chou T-C, Talalay P. 1984. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv. Enzyme Regul. 22:27-55. http://dx.doi.org/10.1016/0065-2571(84)90007-4.
23. Dicker IB, Seetharam S. 1995. Herpes simplex type 1: lacZ recombinant viruses. I. Characterization and application to defining the mechanisms of action of known antiherpes agents. Antiviral Res. 28:191-212.
24. Zhu Q-C, Wang Y, Peng T. 2010. Herpes simplex virus (HSV) immediate-early (IE) promoter-directed reporter system for the screening of antiherpetics targeting the early stage of HSV infection. J. Biomol. Screening 15:1016-1020. http://dx.doi.org/10.1177/1087057110372804.
25. Boehmer PE, Lehman I. 1993. Herpes simplex virus type 1 ICP8: helix-destabilizing properties. J. Virol. 67:711-715. (Pubitemid 23032047)
26. Goodkin ML, Ting AT, Blaho JA. 2003. NF-κB is required for apoptosis prevention during herpes simplex virus type 1 infection. J. Virol. 77:7261-7280. http://dx.doi.org/10.1128/JVI.77.13.7261-7280.2003.
27. Gregory D, Hargett D, Holmes D, Money E, Bachenheimer S. 2004. Efficient replication by herpes simplex virus type 1 involves activation of the IκB kinase-IκB-p65 pathway. J. Virol. 78:13582-13590. http://dx.doi.org/10. 1128/JVI.78.24.13582-13590.2004.
28. Li H, Li X, Wei Y, Tan Y, Liu X, Wu X. 2009. HSV-2 induces TLRs and NF-κB-dependent cytokines in cervical epithelial cells. Biochem. Biophys. Res. Commun. 379:686-690. http://dx.doi.org/10.1016/j.bbrc.2008.12.150.
29. Yedowitz JC, Blaho JA. 2005. Herpes simplex virus 2 modulates apoptosis and stimulates NF-κB nuclear translocation during infection in human epithelial HEp-2 cells. Virology 342:297-310. http://dx.doi.org/10.1016/j.virol. 2005.07.036.
30. Gillis PA, Okagaki LH, Rice SA. 2009. Herpes simplex virus type 1 ICP27 induces p38 mitogen-activated protein kinase signaling and apoptosis in HeLa cells. J. Virol. 83: 1767-1777. http://dx.doi.org/10.1128/JVI.01944-08.
31. McLean T, Bachenheimer S. 1999. Activation of c-Jun N-terminal kinase by herpes simplex virus type 1 enhances viral replication. J. Virol. 73:8415-8426. (Pubitemid 29441704)
32. Li H, Zhang J, Kumar A, Zheng M, Atherton SS, Yu FSX. 2006. Herpes simplex virus 1 infection induces the expression of proinflammatory cytokines, interferons and TLR7 in human corneal epithelial cells. Immunology 117:167-176. http://dx.doi.org/10.1111/j.1365-2567.2005.02275.x.
33. Melchjorsen J, Sirén J, Julkunen I, Paludan SR, Matikainen S. 2006. Induction of cytokine expression by herpes simplex virus in human monocyte-derived macrophages and dendritic cells is dependent on virus replication and is counteracted by ICP27 targeting NF-κB and IRF-3. J. Gen. Virol. 87:1099-1108. http://dx.doi.org/10.1099/vir.0.81541-0.
34. Birdsall TC, Kelly GS. 1997. Berberine therapeutic potential of an alkaloid found in several medicinal plants. Alternative Med. Rev. 2:94-103. (Pubitemid 127735667)
35. Mahata S, Bharti AC, Shukla S, Tyagi A, Husain SA, Das BC. 2011. Berberine modulates AP-1 activity to suppress HPV transcription and downstream signaling to induce growth arrest and apoptosis in cervical cancer cells. Mol. Cancer 10:39. http://dx.doi.org/10.1186/1476-4598-10-39.
36. Remppis A, Bea F, Greten HJ, Buttler A, Wang H, Zhou Q, Preusch MR, Enk R, Ehehalt R, Katus H. 2010. Rhizoma Coptidis inhibits LPS-induced MCP-1/CCL2 production in murine macrophages via an AP-1 and NF-κB-dependent pathway. Mediators Inflamm. 2010:194896. http://dx.doi.org/10.1155/2010/194896.
37. Kuo CL, Chi CW, Liu TY. 2004. The anti-inflammatory potential of berberine in vitro and in vivo. Cancer Lett. 203:127-137. http://dx.doi.org/10. 1016/j.canlet.2003.09.002.
38. Lee C-H, Chen J-C, Hsiang C-Y, Wu S-L, Wu H-C, Ho T-Y. 2007. Berberine suppresses inflammatory agents-induced interleukin-1β and tumor necrosis factor-α productions via the inhibition of IκB degradation in human lung cells. Pharmacol. Res. 56:193-201. http://dx.doi.org/10.1016/j.phrs.2007. 06.003.
39. Cecil CE, Davis JM, Cech NB, Laster SM. 2011. Inhibition of H1N1 influenza A virus growth and induction of inflammatory mediators by the isoquinoline alkaloid berberine and extracts of goldenseal (Hydrastis canadensis). Int. Immunopharmacol. 11:1706-1714. http://dx.doi.org/10.1016/j. intimp.2011.06.002.
40. Hayashi K, Minoda K, Nagaoka Y, Hayashi T, Uesato S. 2007. Antiviral activity of berberine and related compounds against human cytomegalovirus. Bioorg. Med. Chem. Lett. 17:1562-1564. http://dx.doi.org/10.1016/j.bmcl.2006.12. 085.
41. Chin LW, Cheng Y-W, Lin S-S, Lai Y-Y, Lin L-Y, Chou M-Y, Chou M-C, Yang C-C. 2010. Anti-herpes simplex virus effects of berberine from Coptidis rhizoma, a major component of a Chinese herbal medicine, Ching-Wei-San. Arch. Virol. 155:1933-1941. http://dx.doi.org/10.1007/s00705-010-0779-9.
42. Andersen JH, Jenssen H, Gutteberg TJ. 2003. Lactoferrin and lactoferricin inhibit Herpes simplex 1 and 2 infection and exhibit synergy when combined with acyclovir. Antiviral Res. 58:209-215. http://dx.doi.org/10.1016/S0166-3542(02) 00214-0.
43. Schinazi R, Peters J, Williams C, Chance D, Nahmias A. 1982. Effect of combinations of acyclovir with vidarabine or its 5′-monophosphate on herpes simplex viruses in cell culture and in mice. Antimicrob. Agents Chemother. 22:499-507. http://dx.doi.org/10.1128/AAC.22.3.499.
44. Stanwick TL, Schinazi RF, Campbell DE, Nahmias AJ. 1981. Combined antiviral effect of interferon and acyclovir on herpes simplex virus types 1 and 2. Antimicrob. Agents Chemother. 19:672-674. http://dx.doi.org/10.1128/AAC.19. 4.672.
45. Yoosook C, Bunyapraphatsara N, Boonyakiat Y, Kantasuk C. 2000. Anti-herpes simplex virus activities of crude water extracts of Thai medicinal plants. Phytomedicine 6:411-419. http://dx.doi.org/10.1016/S0944-7113(00)80068- 9.
46. DeLuca NA, Schaffer PA. 1985. Activation of immediate-early, early, and late promoters by temperature-sensitive and wild-type forms of herpes simplex virus type 1 protein ICP4. Mol. Cell. Biol. 5:1997-2008. (Pubitemid 15049160)
47. McGregor F, Phelan A, Dunlop J, Clements J. 1996. Regulation of herpes simplex virus poly(A) site usage and the action of immediate-early protein IE63 in the early-late switch. J. Virol. 70:1931-1940. (Pubitemid 26062958)
48. Patel A, Hanson J, McLean TI, Olgiate J, Hilton M, Miller WE, Bachenheimer SL. 1998. Herpes simplex virus type 1 induction of persistent NF-κB nuclear translocation increases the efficiency of virus replication. Virology 247:212-222. http://dx.doi.org/10.1006/viro.1998.9243.
49. Baldwin AS, Jr. 1996. The NF-κB and IκB proteins: new discoveries and insights. Annu. Rev. Immunol. 14:649-681. http://dx.doi.org/10. 1146/annurev.immunol.14.1.649.
50. Amici C, Belardo G, Rossi A, Santoro MG. 2001. Activation of IκB kinase by herpes simplex virus type 1 a novel target for anti-herpetic therapy. J. Biol. Chem. 276:28759-28766. http://dx.doi.org/10.1074/jbc.M103408200.
51. Zachos G, Clements B, Conner J. 1999. Herpes simplex virus type 1 infection stimulates p38/c-Jun N-terminal mitogen-activated protein kinase pathways and activates transcription factor AP-1. J. Biol. Chem. 274:5097-5103. http://dx.doi.org/10.1074/jbc.274.8.5097.
52. Kyriakis JM, Avruch J. 2001. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:807-869. (Pubitemid 32267078)
53. Andrade A, Silva P, Pereira A, De Sousa L, Ferreira P, Gazzinelli R, Kroon E, Ropert C, Bonjardim C. 2004. The vaccinia virus-stimulated mitogen-activated protein kinase(MAPK)pathway is required for virus multiplication. Biochem. J. 381:437-446. http://dx.doi.org/10.1042/BJ20031375.
54. Holloway G, Coulson BS. 2006. Rotavirus activates JNK and p38 signaling pathways in intestinal cells, leading to AP-1-driven transcriptional responses and enhanced virus replication. J. Virol. 80:10624-10633. http://dx.doi.org/10. 1128/JVI.00390-06.
55. Rahaus M, Desloges N, Wolff MH. 2004. Replication of varicella-zoster virus is influenced by the levels of JNK/SAPK and p38/MAPK activation. J. Gen. Virol. 85:3529-3540. http://dx.doi.org/10.1099/vir.0.80347-0.
56. Jacqué JM, Mann A, Enslen H, Sharova N, Brichacek B, Davis RJ, Stevenson M. 1998. Modulation of HIV-1 infectivity by MAPK, a virion-associated kinase. EMBO J. 17:2607-2618. http://dx.doi.org/10.1093/emboj/17.9.2607.
57. Si X, Luo H, Morgan A, Zhang J, Wong J, Yuan J, Esfandiarei M, Gao G, Cheung C, McManus BM. 2005. Stress-activated protein kinases are involved in coxsackievirus B3 viral progeny release. J. Virol. 79:13875-13881. http://dx.doi.org/10.1128/JVI.79.22.13875-13881.2005.
58. Pleschka S, Wolff T, Ehrhardt C, Hobom G, Planz O, Rapp UR, Ludwig S. 2001. Influenza virus propagation is impaired by inhibition of the Raf/MEK/ERK signaling cascade. Nat. Cell Biol. 3:301-305. http://dx.doi.org/10.1038/ 35060098.
59. Panteva M, Korkaya H, Jameel S. 2003. Hepatitis viruses and the MAPK pathway: is this a survival strategy? Virus Res. 92:131-140. http://dx.doi.org/10.1016/S0168-1702(02)00356-8.
60. Hoffmann E, Dittrich-Breiholz O, Holtmann H, Kracht M. 2002. Multiple control of interleukin-8 gene expression. J. Leukoc. Biol. 72:847-855. (Pubitemid 35365158)
61. Kunsch C, Rosen CA. 1993. NF-κB subunit-specific regulation of the interleukin-8 promoter. Mol. Cell. Biol. 13:6137-6146. (Pubitemid 23292608)
62. Bazzoni F, Kruys V, Shakhov A, Jongeneel C, Beutler B. 1994. Analysis of tumor necrosis factor promoter responses to ultraviolet light. J. Clin. Invest. 93:56. http://dx.doi.org/10.1172/JCI116984.