Login Register Cart 0
Generic placeholder image

The Natural Products Journal

Editor-in-Chief

ISSN (Print): 2210-3155
ISSN (Online): 2210-3163

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Research Article

Resveratrol Treatment-induced Nuclear HMGB1 Retention is Critical for Inducing Host Interferon Responses Against Zika Virus

Author(s): Kim-Ling Chin, Nurhafiza Zainal, Sing-Sin Sam and Sazaly Abu Bakar*

Volume 13, Issue 6, 2023

Published on: 03 January, 2023

Article ID: e141122210878 Pages: 17

DOI: 10.2174/2210315513666221114112253

Price: $65

Abstract

Background: Zika virus (ZIKV) infection is a public health concern and currently there is no specific therapeutic or approved vaccine. Resveratrol (RESV), a natural antiviral compound, has been shown to possess antiviral properties against ZIKV and other viral infections, but the mechanisms of action against ZIKV remain unknown.

Objective: This study aimed to investigate the role of the high mobility group box 1 protein (HMGB1) in the underlying anti-ZIKV mechanisms of RESV. Methods: HMGB1 protein expression and ZIKV replication in both the RESV-treated wildtype (WT) and HMGB1-knockdown (shHMGB1) Huh7 cells were analyzed using ELISA, immunofluorescence assay, immunoblot assay, focus-forming assay and qRT-PCR. HMGB1’s role was explored by evaluating the changes in the type-1 interferon (IFN) response genes using the qRT-PCR and immunoblot assays.

Results: The treatment of the ZIKV-infected WT Huh7 cells with RESV significantly reduced ZIKV titers by >90% (P < 0.001) at 48 and 72 hr pi in a dose-dependent manner and inhibited ZIKV-induced HMGB1 translocation (P < 0.001), resulting in nuclear HMGB1 accumulation. Compared to the WT Huh7 cells, shHMGB1 Huh7 cells without RESV treatment showed a significant increase in the infectious virus titers and RNA with a maximum rise of 74% (P < 0.001) and 65% (P < 0.01), respectively. RESV treatment of the ZIKV-infected WT Huh7 cells significantly increased the MxA (one of the classical interferon-stimulated genes, ISGs) and IFN-β levels (P < 0.05). The treatment of the infected shHMGB1 Huh7 cells with RESV showed a less effective antiviral response (P > 0.05) and did not cause changes in the expressions of MxA and IFN-β.

Conclusion: RESV possesses therapeutic activity against ZIKV infection and the mechanism of action is mainly attributed to HMGB1 nuclear retention, which could upregulate the type-1 IFN and ISGs.

[1]
Stawicki, S.P.; Sikka, V.; Chattu, V.K.; Popli, R.K.; Galwankar, S.C.; Kelkar, D.; Sawicki, S.G.; Papadimos, T. The emergence of Zika vi- rus as a global health security threat: A review and a consensus statement of the INDUSEM Joint working Group (JWG). J. Glob. Infect. Dis., 2016, 8(1), 3-15.
[http://dx.doi.org/10.4103/0974-777X.176140] [PMID: 27013839]
[2]
Lanciotti, R.S.; Lambert, A.J.; Holodniy, M.; Saavedra, S. Signor,] L.C.C. Phylogeny of Zika virus in western hemisphere, 2015. Emerg. Infect. Dis., 2016, 22(5), 933-935.
[http://dx.doi.org/10.3201/eid2205.160065] [PMID: 27088323]
[3]
Schuler-Faccini, L.; Ribeiro, E.M.; Feitosa, I.M.L.; Horovitz, D.D.G.; Cavalcanti, D.P.; Pessoa, A.; Doriqui, M.J.R.; Neri, J.I.; Neto, J.M.P.; Wanderley, H.Y.C.; Cernach, M.; El-Husny, A.S.; Pone, M.V.S.; Serao, C.L.C.; Sanseverino, M.T.V. Possible association between Zika virus infection and microcephaly-Brazil, 2015. MMWR Morb. Mortal. Wkly. Rep., 2016, 65(3), 59-62.
[http://dx.doi.org/10.15585/mmwr.mm6503e2] [PMID: 26820244]
[4]
Domínguez-Moreno, R.; Tolosa-Tort, P.; Patiño-Tamez, A.; Quintero-Bauman, A.; Collado-Frías, D.K.; Miranda-Rodríguez, M.G.; Canela-Calderón, O.J.; Hurtado-Valadez, P.; de Gante-Castro, R.; Ortiz-Guillén, K.M.; Estañol-Vidal, B.; Sentíes-Madrid, H. Gar- cía-Ramos, G.; Cantú-Brito, C.; Ruiz-Sandoval, J.L.; Chiquete, E. Mortality associated with a diagnosis of Guillain-Barré syndrome in adults of Mexican health institutions. Rev. Neurol., 2014, 58(1), 4-10.
[PMID: 24343535]
[5]
Schoggins, J.W.; Rice, C.M. Interferon-stimulated genes and their antiviral effector functions. Curr. Opin. Virol., 2011, 1(6), 519-525.
[http://dx.doi.org/10.1016/j.coviro.2011.10.008] [PMID: 22328912]
[6]
Lazear, H.M.; Govero, J.; Smith, A.M.; Platt, D.J.; Fernandez, E.; Miner, J.J.; Diamond, M.S. A mouse model of Zika virus pathogene- sis. Cell Host Microbe, 2016, 19(5), 720-730.
[http://dx.doi.org/10.1016/j.chom.2016.03.010] [PMID: 27066744]
[7]
Krause, K.K.; Azouz, F.; Shin, O.S.; Kumar, M. Understanding the pathogenesis of Zika virus infection using animal models. Immune Netw., 2017, 17(5), 287-297.
[http://dx.doi.org/10.4110/in.2017.17.5.287] [PMID: 29093650]
[8]
Roy, A.; Lim, L.; Song, J. Identification of quercetin from fruits to immediately fight Zika. BioRxiv, 2016, 074559.
[http://dx.doi.org/10.1101/074559]
[9]
Oo, A.; Teoh, B.T.; Sam, S.S.; Bakar, S.A.; Zandi, K. Baicalein and baicalin as Zika virus inhibitors. Arch. Virol., 2019, 164(2), 585-593.
[http://dx.doi.org/10.1007/s00705-018-4083-4] [PMID: 30392049]
[10]
Lee, J.L.; Loe, M.W.C.; Lee, R.C.H.; Chu, J.J.H. Antiviral activity of pinocembrin against Zika virus replication. Antiviral Res., 2019, 167, 13-24.
[http://dx.doi.org/10.1016/j.antiviral.2019.04.003] [PMID: 30959074]
[11]
da Silva, T.F.; Ferraz, A.C.; Almeida, L.T.; Caetano, C.C.S.; Camini, F.C.; Lima, R.L.S.; Andrade, A.C.S.P.; de Oliveira, D.B.; Rocha, K.L.S.; Silva, B.M.; de Magalhães, J.C.; Magalhães, C.L.B. Antiviral effect of silymarin against Zika virus in vitro. Acta Trop., 2020, 211, 105613.
[http://dx.doi.org/10.1016/j.actatropica.2020.105613] [PMID: 32621935]
[12]
Russo, C.A.; Torti, M.F.; Márquez, A.B.; Sepúlveda, C.S.; Alaimo, A.; García, C.C. Antiviral bioactivity of resveratrol against Zika virus infection in human retinal pigment epithelial cells. Mol. Biol. Rep., 2021, 48(7), 5379-5392.
[http://dx.doi.org/10.1007/s11033-021-06490-y]
[13]
Mohd, A.; Zainal, N.; Tan, K.K.; AbuBakar, S. Resveratrol affects Zika virus replication in vitro. Sci. Rep., 2019, 9(1), 14336.
[http://dx.doi.org/10.1038/s41598-019-50674-3] [PMID: 31586088]
[14]
Creasy, L.L.; Coffee, M. Phytoalexin production potential of grape berries. J. Am. Soc. Hortic. Sci., 1988, 113(2), 230-234.
[http://dx.doi.org/10.21273/JASHS.113.2.230]
[15]
Burns, J.; Yokota, T.; Ashihara, H.; Lean, M.E.J.; Crozier, A. Plant foods and herbal sources of resveratrol. J. Agric. Food Chem., 2002, 50(11), 3337-3340.
[http://dx.doi.org/10.1021/jf0112973] [PMID: 12010007]
[16]
Abba, Y.; Hassim, H.; Hamzah, H.; Noordin, M.M. Antiviral activity of resveratrol against human and animal viruses. Adv. Virol., 2015, 2015, 1-7.
[http://dx.doi.org/10.1155/2015/184241] [PMID: 26693226]
[17]
Zhang, L.; Li, Y.; Gu, Z.; Wang, Y.; Shi, M.; Ji, Y.; Sun, J.; Xu, X.; Zhang, L.; Jiang, J.; Shi, W. Resveratrol inhibits enterovirus 71 repli- cation and pro-inflammatory cytokine secretion in rhabdosarcoma cells through blocking IKKs/NF-κB signaling pathway. PLoS One, 2015, 10(2), e0116879.
[http://dx.doi.org/10.1371/journal.pone.0116879] [PMID: 25692777]
[18]
Palamara, A.T.; Nencioni, L.; Aquilano, K.; De Chiara, G. Hernan- dez, L.; Cozzolino, F.; Ciriolo, M.R.; Garaci, E. Inhibition of influen- za A virus replication by resveratrol. J. Infect. Dis., 2005, 191(10), 1719-1729.
[http://dx.doi.org/10.1086/429694] [PMID: 15838800]
[19]
Yiu, C.Y.; Chen, S.Y.; Chang, L.K.; Chiu, Y.F.; Lin, T.P. Inhibitory effects of resveratrol on the Epstein-Barr virus lytic cycle. Molecules, 2010, 15(10), 7115-7124.
[http://dx.doi.org/10.3390/molecules15107115] [PMID: 20948499]
[20]
Kapadia, G.J.; Azuine, M.A.; Tokuda, H.; Takasaki, M.; Mukainaka, T.; Konoshima, T.; Nishino, H. Chemopreventive effect of resvera- trol, sesamol, sesame oil and sunflower oil in the epstein–barr virus early antigen activation assay and the mouse skin two-stage carcino- genesis. Pharmacol. Res., 2002, 45(6), 499-505.
[http://dx.doi.org/10.1006/phrs.2002.0992] [PMID: 12162952]
[21]
Zhang, H.S.; Zhou, Y.; Wu, M.R.; Zhou, H.S.; Xu, F. Resveratrol inhibited Tat-induced HIV-1 LTR transactivation via NAD+- dependent SIRT1 activity. Life Sci., 2009, 85(13-14), 484-489.
[http://dx.doi.org/10.1016/j.lfs.2009.07.014] [PMID: 19664641]
[22]
Clouser, C.L.; Chauhan, J.; Bess, M.A.; Oploo, J.L.; Zhou, D.; Dimick-Gray, S.; Mansky, L.M.; Patterson, S.E. Anti-HIV-1 activity of resveratrol derivatives and synergistic inhibition of HIV-1 by the combination of resveratrol and decitabine. Bioorg. Med. Chem. Lett., 2012, 22(21), 6642-6646.
[http://dx.doi.org/10.1016/j.bmcl.2012.08.108] [PMID: 23010273]
[23]
Faith, S.A.; Sweet, T.J.; Bailey, E.; Booth, T.; Docherty, J.J. Resvera- trol suppresses nuclear factor-κB in herpes simplex virus infected cells. Antiviral Res., 2006, 72(3), 242-251.
[http://dx.doi.org/10.1016/j.antiviral.2006.06.011] [PMID: 16876885]
[24]
Docherty, J.J.; Fu, M.M.H.; Stiffler, B.S.; Limperos, R.J.; Pokabla, C.M.; DeLucia, A.L. Resveratrol inhibition of herpes simplex virus replication. Antiviral Res., 1999, 43(3), 145-155.
[http://dx.doi.org/10.1016/S0166-3542(99)00042-X] [PMID: 10551373]
[25]
Xie, X.; Zang, N.; Li, S.; Wang, L.; Deng, Y.; He, Y.; Yang, X. Liu,] E. Resveratrol Inhibits respiratory syncytial virus-induced IL-6 pro- duction, decreases viral replication, and downregulates TRIF expres- sion in airway epithelial cells. Inflammation, 2012, 35(4), 1392-1401.
[http://dx.doi.org/10.1007/s10753-012-9452-7] [PMID: 22391746]
[26]
Evers, D.L.; Wang, X.; Huong, S.M.; Huang, D.Y.; Huang, E.S. 3,4′5-Trihydroxy-trans-stilbene (resveratrol) inhibits human cyto- megalovirus replication and virus-induced cellular signaling. Antiviral Res., 2004, 63(2), 85-95.
[http://dx.doi.org/10.1016/j.antiviral.2004.03.002] [PMID: 15302137]
[27]
Yang, M.; Wei, J.; Huang, T.; Lei, L.; Shen, C.; Lai, J.; Yang, M.; Liu, L.; Yang, Y.; Liu, G. Resveratrol inhibits the replication of se- vere acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in cul- tured Vero cells. Phytother. Res., 2020.
[PMID: 33222316]
[28]
Zainal, N.; Chang, C.P.; Cheng, Y.L.; Wu, Y.W.; Anderson, R.; Wan, S.W.; Chen, C.L.; Ho, T.S.; AbuBakar, S.; Lin, Y.S. Resveratrol treatment reveals a novel role for HMGB1 in regulation of the type 1 interferon response in dengue virus infection. Sci. Rep., 2017, 7(1), 42998.
[http://dx.doi.org/10.1038/srep42998] [PMID: 28216632]
[29]
Yang, H.; Wang, H.; Czura, C.J.; Tracey, K.J. The cytokine activity of HMGB1. J. Leukoc. Biol., 2005, 78(1), 1-8.
[http://dx.doi.org/10.1189/jlb.1104648] [PMID: 15734795]
[30]
Kamau, E.; Takhampunya, R.; Li, T.; Kelly, E.; Peachman, K.K.; Lynch, J.A.; Sun, P.; Palmer, D.R. Dengue virus infection promotes translocation of high mobility group box 1 protein from the nucleus to the cytosol in dendritic cells, upregulates cytokine production and modulates virus replication. J. Gen. Virol., 2009, 90(8), 1827-1835.
[http://dx.doi.org/10.1099/vir.0.009027-0] [PMID: 19369409]
[31]
Qu, Y.; Zhan, Y.; Yang, S.; Ren, S.; Qiu, X.; Rehamn, Z.U.; Tan, L.; Sun, Y.; Meng, C.; Song, C.; Yu, S.; Ding, C. Newcastle disease vi- rus infection triggers HMGB1 release to promote the inflammatory response. Virology, 2018, 525, 19-31.
[http://dx.doi.org/10.1016/j.virol.2018.09.001] [PMID: 30216776]
[32]
Jung, J.H.; Park, J.H.; Jee, M.H.; Keum, S.J.; Cho, M.S.; Yoon, S.K.; Jang, S.K. Hepatitis C virus infection is blocked by HMGB1 released from virus-infected cells. J. Virol., 2011, 85(18), 9359-9368.
[http://dx.doi.org/10.1128/JVI.00682-11] [PMID: 21752923]
[33]
Yu, R.; Yang, D.; Lei, S.; Wang, X.; Meng, X.; Xue, B.; Zhu, H. HMGB1 promotes hepatitis C virus replication by interaction with stem-loop 4 in the viral 5′ untranslated region. J. Virol., 2016, 90(5), 2332-2344.
[http://dx.doi.org/10.1128/JVI.02795-15] [PMID: 26656705]
[34]
Moisy, D.; Avilov, S.V.; Jacob, Y.; Laoide, B.M.; Ge, X.; Baudin, F.; Naffakh, N.; Jestin, J.L. HMGB1 protein binds to influenza virus nu-] cleoprotein and promotes viral replication. J. Virol., 2012, 86(17), 9122-9133.
[http://dx.doi.org/10.1128/JVI.00789-12] [PMID: 22696656]
[35]
Hou, X.; Liu, G.; Zhang, H.; Hu, X.; Zhang, X.; Han, F.; Cui, H.; Luo, J.; Guo, R.; Li, R.; Li, N.; Wei, L. High-mobility group box 1 protein (HMGB1) from cherry valley duck mediates signaling path- ways and antiviral activity. Vet. Res., 2020, 51(1), 12.
[http://dx.doi.org/10.1186/s13567-020-00742-8] [PMID: 32070432]
[36]
Chin, K.L.; Zainal, N.; Sam, S.S.; Hassandarvish, P.; Lani, R. Abu- Bakar, S. Intracellular translocation of HMGB1 is important for Zika virus replication in Huh7 cells. Sci. Rep., 2022, 12(1), 1054.
[http://dx.doi.org/10.1038/s41598-022-04955-z] [PMID: 35058496]
[37]
Hashemi, M.; Zali, A.; Hashemi, J.; Oraee-Yazdani, S.; Akbari, A. Down-regulation of 14-3-3 zeta sensitizes human glioblastoma cells to apoptosis induction. Apoptosis, 2018, 23(11-12), 616-625.
[http://dx.doi.org/10.1007/s10495-018-1476-5] [PMID: 30101359]
[38]
Fink, S.L.; Vojtech, L.; Wagoner, J.; Slivinski, N.S.J.; Jackson, K.J.; Wang, R.; Khadka, S.; Luthra, P.; Basler, C.F.; Polyak, S.J. The anti- viral drug arbidol inhibits Zika virus. Sci. Rep., 2018, 8(1), 8989.
[http://dx.doi.org/10.1038/s41598-018-27224-4] [PMID: 29895962]
[39]
Teoh, B.T.; Sam, S.S.; Tan, K.K.; Johari, J.; Shu, M.H.; Danlami, M.B.; Abd-Jamil, J. MatRahim, N.A.; Mahadi, N.M.; AbuBakar, S. Dengue virus type 1 clade replacement in recurring homotypic out- breaks. BMC Evol. Biol., 2013, 13(1), 213.
[http://dx.doi.org/10.1186/1471-2148-13-213]
[40]
Chan, J.F.W.; Yip, C.C.Y.; Tsang, J.O.L.; Tee, K.M.; Cai, J.P.; Chik, K.K.H.; Zhu, Z.; Chan, C.C.S.; Choi, G.K.Y.; Sridhar, S.; Zhang, A.J.; Lu, G.; Chiu, K.; Lo, A.C.Y.; Tsao, S.W.; Kok, K.H.; Jin, D.Y.; Chan, K.H.; Yuen, K.Y. Differential cell line susceptibility to the emerging Zika virus: implications for disease pathogenesis, non- vector-borne human transmission and animal reservoirs. Emerg. Microbes Infect., 2016, 5(1), 1-12.
[http://dx.doi.org/10.1038/emi.2016.99] [PMID: 27553173]
[41]
Luangsay, S.; Ait-Goughoulte, M.; Michelet, M.; Floriot, O.; Bonnin, M.; Gruffaz, M.; Rivoire, M.; Fletcher, S.; Javanbakht, H.; Lucifora, J.; Zoulim, F.; Durantel, D. Expression and functionality of Toll- and RIG-like receptors in HepaRG cells. J. Hepatol., 2015, 63(5), 1077-1085.
[http://dx.doi.org/10.1016/j.jhep.2015.06.022] [PMID: 26144659]
[42]
Preiss, S.; Thompson, A.; Chen, X.; Rodgers, S.; Markovska, V.; Desmond, P.; Visvanathan, K.; Li, K.; Locarnini, S.; Revill, P. Char- acterization of the innate immune signalling pathways in hepatocyte cell lines. J. Viral Hepat., 2008, 15(12), 888-900.
[http://dx.doi.org/10.1111/j.1365-2893.2008.01001.x] [PMID: 18673429]
[43]
Sherman, K.E.; Rouster, S.D.; Kong, L.X.; Aliota, M.T.; Blackard, J.T.; Dean, G.E. Zika virus replication and cytopathic effects in liver cells. PLoS One, 2019, 14(3), e0214016.
[http://dx.doi.org/10.1371/journal.pone.0214016] [PMID: 30893357]
[44]
MacNamara, F.N. Zika virus: A report on three cases of human infection during an epidemic of jaundice in Nigeria. Trans. R. Soc. Trop. Med. Hyg., 1954, 48(2), 139-145.
[http://dx.doi.org/10.1016/0035-9203(54)90006-1] [PMID: 13157159]
[45]
Wu, Y.; Cui, X.; Wu, N.; Song, R.; Yang, W.; Zhang, W.; Fan, D.; Chen, Z.; An, J. A unique case of human Zika virus infection in asso- ciation with severe liver injury and coagulation disorders. Sci. Rep., 2017, 7(1), 11393.
[http://dx.doi.org/10.1038/s41598-017-11568-4] [PMID: 28900143]
[46]
Chong, Z.X.; Yeap, S.K.; Ho, W.Y. Transfection types, methods and strategies: a technical review. PeerJ, 2021, 9, e11165.
[http://dx.doi.org/10.7717/peerj.11165] [PMID: 33976969]
[47]
Condreay, J.P.; Witherspoon, S.M.; Clay, W.C.; Kost, T.A. Transient and stable gene expression in mammalian cells transduced with a re- combinant baculovirus vector. Proc. Natl. Acad. Sci. USA, 1999, 96(1), 127-132.
[http://dx.doi.org/10.1073/pnas.96.1.127] [PMID: 9874783]
[48]
Campagna, M.; Rivas, C. Antiviral activity of resveratrol. Biochem. Soc. Trans., 2010, 38(1), 50-53.
[http://dx.doi.org/10.1042/BST0380050] [PMID: 20074034]
[49]
Yang, T.; Li, S.; Zhang, X.; Pang, X.; Lin, Q.; Cao, J. Resveratrol, sirtuins, and viruses. Rev. Med. Virol., 2015, 25(6), 431-445.
[http://dx.doi.org/10.1002/rmv.1858] [PMID: 26479742]
[50]
Yang, H.; Wang, H.; Chavan, S.S.; Andersson, U. High mobility group box protein 1 (HMGB1): the prototypical endogenous danger molecule. Mol. Med., 2015, 21(S1)(Suppl. 1), S6-S12.
[http://dx.doi.org/10.2119/molmed.2015.00087] [PMID: 26605648]
[51]
Tang, D.; Kang, R.; Cheh, C-W.; Livesey, K.M.; Liang, X.; Schapiro, N.E.; Benschop, R.; Sparvero, L.J.; Amoscato, A.A.; Tracey, K.J.; Zeh, H.J.; Lotze, M.T. HMGB1 release and redox regulates autopha- gy and apoptosis in cancer cells. Oncogene, 2010, 29(38), 5299-5310.
[http://dx.doi.org/10.1038/onc.2010.261] [PMID: 20622903]
[52]
Ito, I.; Fukazawa, J.; Yoshida, M. Post-translational methylation of high mobility group box 1 (HMGB1) causes its cytoplasmic localiza- tion in neutrophils. J. Biol. Chem., 2007, 282(22), 16336-16344.
[http://dx.doi.org/10.1074/jbc.M608467200] [PMID: 17403684]
[53]
Barqasho, B.; Nowak, P.; Abdurahman, S.; Walther-Jallow, L. Sön- nerborg, A. Implications of the release of high-mobility group box 1 protein from dying cells during human immunodeficiency virus type 1 infection in vitro. J. Gen. Virol., 2010, 91(7), 1800-1809.
[http://dx.doi.org/10.1099/vir.0.016915-0] [PMID: 20200191]
[54]
Gougeon, M-L.; Melki, M-T.; Saïdi, H. HMGB1, an alarmin promot- ing HIV dissemination and latency in dendritic cells. Cell Death Differ., 2012, 19(1), 96-106.
[http://dx.doi.org/10.1038/cdd.2011.134] [PMID: 22033335]
[55]
Lotze, M.T.; Tracey, K.J. High-mobility group box 1 protein (HMGB1): Nuclear weapon in the immune arsenal. Nat. Rev. Immunol., 2005, 5(4), 331-342.
[http://dx.doi.org/10.1038/nri1594] [PMID: 15803152]
[56]
Ong, S.P.; Lee, L.M.; Leong, Y.F.I.; Ng, M.L.; Chu, J.J.H. Dengue virus infection mediates HMGB1 release from monocytes involving PCAF acetylase complex and induces vascular leakage in endothelial cells. PLoS One, 2012, 7(7), e41932.
[http://dx.doi.org/10.1371/journal.pone.0041932] [PMID: 22860034]
[57]
de Carvalho, G.C.; Borget, M.Y.; Bernier, S.; Garneau, D.; da Silva Duarte, A.J.; Dumais, N. RAGE and CCR7 mediate the transmigra- tion of Zika-infected monocytes through the blood-brain barrier. Immunobiology, 2019, 224(6), 792-803.
[http://dx.doi.org/10.1016/j.imbio.2019.08.007] [PMID: 31493920]
[58]
Zou, S-S.; Zou, Q-C.; Xiong, W-J.; Cui, N-Y.; Wang, K.; Liu, H-X.; Lou, W-J.; Higazy, D.; Chen, H-W.; Zhang, Y-G. Brain micro- vascular endothelial cells-derived HMGB1 facilitates monocyte tran- sendothelial migration favoring JEV neuroinvasion. Front. Cell. Infect. Microbiol., 2021, 11, 701820.
[http://dx.doi.org/10.21203/rs.3.rs-108411/v1]
[59]
Chen, S.; Dong, Z.; Yang, P.; Wang, X.; Jin, G.; Yu, H.; Chen, L.; Li, L.; Tang, L.; Bai, S.; Yan, H.; Shen, F.; Cong, W.; Wen, W. Wang,] H. Hepatitis B virus X protein stimulates high mobility group box 1 secretion and enhances hepatocellular carcinoma metastasis. Cancer Lett., 2017, 394, 22-32.
[http://dx.doi.org/10.1016/j.canlet.2017.02.011] [PMID: 28216372]
[60]
Xu, W.; Lu, Y.; Yao, J.; Li, Z.; Chen, Z.; Wang, G.; Jing, H.; Zhang, X.; Li, M.; Peng, J.; Tian, X. Novel role of resveratrol: suppression of high-mobility group protein box 1 nucleocytoplasmic translocation by the upregulation of sirtuin 1 in sepsis-induced liver injury. Shock, 2014, 42(5), 440-447.
[http://dx.doi.org/10.1097/SHK.0000000000000225] [PMID: 25004063]
[61]
Hwang, J.S.; Choi, H.S.; Ham, S.A.; Yoo, T.; Lee, W.J.; Paek, K.S.; Seo, H.G. Deacetylation-mediated interaction of SIRT1-HMGB1 im- proves survival in a mouse model of endotoxemia. Sci. Rep., 2015, 5(1), 15971.
[http://dx.doi.org/10.1038/srep15971] [PMID: 26522327]
[62]
Naghavi, M.H.; Nowak, P.; Andersson, J.; Sönnerborg, A.; Yang, H.; Tracey, K.J.; Vahlne, A. Intracellular high mobility group B1 protein (HMGB1) represses HIV-1 LTR-directed transcription in a promoter- and cell-specific manner. Virology, 2003, 314(1), 179-189.
[http://dx.doi.org/10.1016/S0042-6822(03)00453-7] [PMID: 14517071]
[63]
Bowen, J.R.; Quicke, K.M.; Maddur, M.S.; O’Neal, J.T.; McDonald, C.E.; Fedorova, N.B.; Puri, V.; Shabman, R.S.; Pulendran, B. Suthar,] M.S. Zika virus antagonizes type I interferon responses during infec- tion of human dendritic cells. PLoS Pathog., 2017, 13(2), e1006164.
[http://dx.doi.org/10.1371/journal.ppat.1006164] [PMID: 28152048]
[64]
Hamel, R.; Dejarnac, O.; Wichit, S.; Ekchariyawat, P.; Neyret, A.; Luplertlop, N.; Perera-Lecoin, M.; Surasombatpattana, P.; Talignani, L.; Thomas, F.; Cao-Lormeau, V.M.; Choumet, V.; Briant, L.; Desprès, P.; Amara, A.; Yssel, H.; Missé, D. Biology of Zika virus infection in human skin cells. J. Virol., 2015, 89(17), 8880-8896.
[http://dx.doi.org/10.1128/JVI.00354-15] [PMID: 26085147]
[65]
Frumence, E.; Roche, M.; Krejbich-Trotot, P.; El-Kalamouni, C.; Nativel, B.; Rondeau, P.; Missé, D.; Gadea, G.; Viranaicken, W.; Desprès, P. The South Pacific epidemic strain of Zika virus replicates efficiently in human epithelial A549 cells leading to IFN-β produc- tion and apoptosis induction. Virology, 2016, 493, 217-226.
[http://dx.doi.org/10.1016/j.virol.2016.03.006] [PMID: 27060565]
[66]
Nazerai, L.; Schøller, A.S.; Rasmussen, P.O.S.; Buus, S.; Stryhn, A.; Christensen, J.P.; Thomsen, A.R. A new in vivo model to study pro- tective immunity to Zika virus infection in mice with intact type I in- terferon signaling. Front. Immunol., 2018, 9, 593.
[http://dx.doi.org/10.3389/fimmu.2018.00593] [PMID: 29623081]
[67]
Ren, K.; Sun, H.; Chen, L.; Chen, N.; Yu, L. Myxovirus resistance protein A activates type I IFN signaling pathway to inhibit Zika virus replication. Virus Res., 2021, 306, 198534.
[http://dx.doi.org/10.1016/j.virusres.2021.198534] [PMID: 34537259]
[68]
Van der Hoek, K.H.; Eyre, N.S.; Shue, B.; Khantisitthiporn, O. Glab- Ampi, K.; Carr, J.M.; Gartner, M.J.; Jolly, L.A.; Thomas, P.Q.; Adikusuma, F.; Jankovic-Karasoulos, T.; Roberts, C.T.; Helbig, K.J.; Beard, M.R. Viperin is an important host restriction factor in control of Zika virus infection. Sci. Rep., 2017, 7(1), 4475.
[http://dx.doi.org/10.1038/s41598-017-04138-1] [PMID: 28667332]
[69]
Liao, X.; Xie, H.; Li, S.; Ye, H.; Li, S.; Ren, K.; Li, Y.; Xu, M.; Lin, W.; Duan, X.; Yang, C.; Chen, L. 2′, 5′-Oligoadenylate Synthetase 2 (OAS2) inhibits Zika virus replication through activation of type Ι IFN signaling pathway. Viruses, 2020, 12(4), 418.
[http://dx.doi.org/10.3390/v12040418] [PMID: 32276512]
[70]
Imaizumi, T.; Yoshida, H.; Hayakari, R.; Xing, F.; Wang, L. Matsu- miya, T.; Tanji, K.; Kawaguchi, S.; Murakami, M.; Tanaka, H. Inter- feron-stimulated gene (ISG) 60, as well as ISG56 and ISG54, posi- tively regulates TLR3/IFN-β/STAT1 axis in U373MG human astro- cytoma cells. Neurosci. Res., 2016, 105, 35-41.
[http://dx.doi.org/10.1016/j.neures.2015.09.002] [PMID: 26423178]
[71]
Ma, F.; Li, B.; Yu, Y.; Iyer, S.S.; Sun, M.; Cheng, G. Positive feed- back regulation of type I interferon by the interferon-stimulated gene STING. EMBO Rep., 2015, 16(2), 202-212.
[http://dx.doi.org/10.15252/embr.201439366] [PMID: 25572843]
[72]
Chan, J.F.W.; Zhang, A.J.; Chan, C.C.S.; Yip, C.C.Y.; Mak, W.W.N.; Zhu, H.; Poon, V.K.M.; Tee, K.M.; Zhu, Z.; Cai, J.P.; Tsang, J.O.L.; Chik, K.K.H.; Yin, F.; Chan, K.H.; Kok, K.H.; Jin, D.Y.; Au-Yeung, R.K.H.; Yuen, K.Y. Zika virus infection in dexamethasone- immunosuppressed mice demonstrating disseminated infection with multi-organ involvement including orchitis effectively treated by re- combinant type I interferons. EBioMedicine, 2016, 14, 112-122.
[http://dx.doi.org/10.1016/j.ebiom.2016.11.017] [PMID: 27884655]
[73]
Chan, J.F.W.; Choi, G.K.Y.; Yip, C.C.Y.; Cheng, V.C.C.; Yuen, K.Y. Zika fever and congenital Zika syndrome: An unexpected emerging arboviral disease. J. Infect., 2016, 72(5), 507-524.
[http://dx.doi.org/10.1016/j.jinf.2016.02.011] [PMID: 26940504]
[74]
Sarmiento-Ospina, A.; Vásquez-Serna, H.; Jimenez-Canizales, C.E.; Villamil-Gómez, W.E.; Rodriguez-Morales, A.J. Zika virus associat- ed deaths in Colombia. Lancet Infect. Dis., 2016, 16(5), 523-524.
[http://dx.doi.org/10.1016/S1473-3099(16)30006-8] [PMID: 27068488]
[75]
Quicke, K.M.; Bowen, J.R.; Johnson, E.L.; McDonald, C.E.; Ma, H.; O’Neal, J.T.; Rajakumar, A.; Wrammert, J.; Rimawi, B.H. Pulen- dran, B.; Schinazi, R.F.; Chakraborty, R.; Suthar, M.S. Zika virus in- fects human placental macrophages. Cell Host Microbe, 2016, 20(1), 83-90.
[http://dx.doi.org/10.1016/j.chom.2016.05.015] [PMID: 27247001]
[76]
Tappe, D.; Pérez-Girón, J.V.; Zammarchi, L.; Rissland, J.; Ferreira, D.F.; Jaenisch, T.; Gómez-Medina, S.; Günther, S.; Bartoloni, A.; Muñoz-Fontela, C.; Schmidt-Chanasit, J. Cytokine kinetics of Zika virus-infected patients from acute to reconvalescent phase. Med. Microbiol. Immunol. (Berl.), 2016, 205(3), 269-273.
[http://dx.doi.org/10.1007/s00430-015-0445-7] [PMID: 26702627]
[77]
Zhang, F.; Liu, J.; Shi, J.S. Anti-inflammatory activities of resveratrol in the brain: Role of resveratrol in microglial activation. Eur. J. Pharmacol., 2010, 636(1-3), 1-7.
[http://dx.doi.org/10.1016/j.ejphar.2010.03.043] [PMID: 20361959]
[78]
Zhou, Z.X.; Mou, S.F.; Chen, X.Q.; Gong, L.L.; Ge, W.S. Anti- inflammatory activity of resveratrol prevents inflammation by inhibit- ing NF-κB in animal models of acute pharyngitis. Mol. Med. Rep., 2018, 17(1), 1269-1274.
[PMID: 29115472]
[79]
Ma, C.; Wang, Y.; Dong, L.; Li, M.; Cai, W. Anti-inflammatory effect of resveratrol through the suppression of NF-κB and JAK/STAT signaling pathways. Acta Biochim. Biophys. Sin. (Shanghai),, 2015, 47(3), 207-213.
[http://dx.doi.org/ 10.1093/abbs/gmu135] [PMID: 25651848]
[80]
Goldberg, D.M.; Yan, J.; Soleas, G.J. Absorption of three wine- related polyphenols in three different matrices by healthy subjects. Clin. Biochem., 2003, 36(1), 79-87.
[http://dx.doi.org/10.1016/S0009-9120(02)00397-1] [PMID: 12554065]
[81]
de Vries, K.; Strydom, M.; Steenkamp, V. Bioavailability of resvera- trol: Possibilities for enhancement. J. Herb. Med., 2018, 11, 71-77.
[http://dx.doi.org/10.1016/j.hermed.2017.09.002]
[82]
Cottart, C.H.; Nivet-Antoine, V.; Laguillier-Morizot, C. Beaudeux,] J.L. Resveratrol bioavailability and toxicity in humans. Mol. Nutr. Food Res., 2010, 54(1), 7-16.
[http://dx.doi.org/10.1002/mnfr.200900437] [PMID: 20013887]
[83]
Penalva, R.; Esparza, I.; Larraneta, E.; González-Navarro, C.J.; Gamazo, C.; Irache, J.M. Zein-based nanoparticles improve the oral bioavailability of resveratrol and its anti-inflammatory effects in a mouse model of endotoxic shock. J. Agric. Food Chem., 2015, 63(23), 5603-5611.
[http://dx.doi.org/10.1021/jf505694e] [PMID: 26027429]
[84]
Neves, A.R.; Lúcio, M.; Martins, S.; Lima, J.L.C.; Reis, S. Novel resveratrol nanodelivery systems based on lipid nanoparticles to en- hance its oral bioavailability. Int. J. Nanomedicine, 2013, 8, 177-187.
[PMID: 23326193]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy