Role of inflammatory cytokine burst in neuro-invasion of Japanese Encephalitis virus infection: an immunotherapeutic approaches.

Publisher: Springer Country of Publication: United States NLM ID: 9508123 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1538-2443 (Electronic) Linking ISSN: 13550284 NLM ISO Abbreviation: J Neurovirol Subsets: MEDLINE

Publication: 2011- : New York : Springer
Original Publication: Houndmills, Basingstoke, Hampshire ; New York, NY : Stockton Press, c1995-

Encephalitis, Japanese*/immunology ; Encephalitis, Japanese*/virology ; Encephalitis, Japanese*/pathology ; Encephalitis, Japanese*/drug therapy ; Encephalitis, Japanese*/therapy ; Encephalitis Virus, Japanese*/immunology ; Encephalitis Virus, Japanese*/pathogenicity ; Cytokines*/immunology ; Microglia*/immunology ; Microglia*/virology ; Microglia*/pathology; Humans ; Animals ; Antiviral Agents/therapeutic use ; Virus Replication/immunology ; Immunity, Innate ; Immunotherapy/methods ; Brain/virology ; Brain/immunology ; Brain/pathology ; Neuroinflammatory Diseases/immunology ; Neuroinflammatory Diseases/virology ; Neuroinflammatory Diseases/pathology ; Neuroinflammatory Diseases/drug therapy

Japanese Encephalitis remains a significant global health concern, contributing to millions of deaths annually worldwide. Microglial cells, as key innate immune cells within the central nervous system (CNS), exhibit intricate cellular structures and possess molecular phenotypic plasticity, playing pivotal roles in immune responses during CNS viral infections. Particularly under viral inflammatory conditions, microglial cells orchestrate innate and adaptive immune responses to mitigate viral invasion and dampen inflammatory reactions. This review article comprehensively summarizes the pathophysiology of viral invasion into the CNS and the cellular interactions involved, elucidating the roles of various immune mediators, including pro-inflammatory cytokines, in neuroinflammation. Leveraging this knowledge, strategies for modulating inflammatory responses and attenuating hyperactivation of glial cells to mitigate viral replication within the brain are discussed. Furthermore, current chemotherapeutic and antiviral drugs are examined, elucidating their mechanisms of action against viral replication. This review aims to provide insights into therapeutic interventions for Japanese Encephalitis and related viral infections, ultimately contributing to improved outcomes for affected individuals.
(© 2024. The Author(s) under exclusive licence to The Journal of NeuroVirology, Inc.)

Erratum in: J Neurovirol. 2024 Jun;30(3):266. doi: 10.1007/s13365-024-01220-z. (PMID: 38858345)

Al-Obaidi M, Bahadoran A, Har LS, Mui WS, Rajarajeswaran J, Zandi K, Manikam R, Sekaran SD (2017) Japanese encephalitis virus disrupts blood-brain barrier and modulates apoptosis proteins in THBMEC cells. Virus research 233:17–28. https://doi.org/10.1016/j.virusres.2017.02.012. (PMID: 10.1016/j.virusres.2017.02.01228279803)
Anderson CE, Tomlinson GS, Pauly B, Brannan FW, Chiswick A, Brack-Werner R, Simmonds P, Bell JE (2003) Relationship of Nef-positive and GFAP-reactive astrocytes to drug use in early and late HIV infection. Neuropathol Appl Neurobiol 29:378–388. (PMID: 10.1046/j.1365-2990.2003.00475.x12887598)
Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, Marfin AA, Solomon T, Tsai TF, Tsu VD, Ginsburg AS (2011) Estimated global incidence of Japanese encephalitis: a systematic review. Bull World Health Organ 89(10):766-774E. https://doi.org/10.2471/BLT.10.085233. (PMID: 10.2471/BLT.10.085233220845153209971)
Charo IF, Ransohoff RM (2006) The many roles of chemokines and chemokine receptors in inflammation. N Engl J Med 354(6):610–621. https://doi.org/10.1056/NEJMra052723. (PMID: 10.1056/NEJMra05272316467548)
Chauhan A, Mehla R, Vijayakumar TS, Handy I (2014) Endocytosis-mediated HIV-1 entry and its significance in the elusive behavior of the virus in astrocytes. Virology 456–457:1–19. (PMID: 10.1016/j.virol.2014.03.00224889220)
Chen CJ, Ou YC, Lin SY, Raung SL, Liao SL, Lai CY, Chen SY, Chen JH (2010) Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J Gen Virol 91:1028–1037. https://doi.org/10.1099/vir.0.013565-0. (PMID: 10.1099/vir.0.013565-020007359)
Chen ST, Liu RS, Wu MF, Lin YL, Chen SY, Tan DT, Chou TY, Tsai IS, Li L, Hsieh SL (2012) CLEC5A regulates Japanese encephalitis virus-induced neuroinflammation and lethality. PLoS Pathog 8(4):e1002655. https://doi.org/10.1371/journal.ppat.1002655. (PMID: 10.1371/journal.ppat.1002655225361533334897)
Chen CJ, Ou YC, Li JR, Chang CY, Pan HC, Lai CY, Liao SL, Raung SL, Chang CJ (2014) Infection of pericytes in vitro by Japanese encephalitis virus disrupts the integrity of the endothelial barrier. J Virol 88(2):1150–1161. https://doi.org/10.1128/JVI.02738-13. (PMID: 10.1128/JVI.02738-13241984233911661)
Choi JY, Kim JH, Patil AM, Kim SB, Uyangaa E, Hossain FMA et al (2017) Exacerbation of Japanese Encephalitis by CD11c(hi) Dendritic Cell Ablation Is Associated with an Imbalance in Regulatory Foxp3(+) and IL-17(+)CD4(+) Th17 Cells and in Ly-6C(hi) and Ly-6C(lo) Monocytes. Immune Netw 17(3):192–200. https://doi.org/10.4110/in.2017.17.3.192 . PMID:28680381;PubMedCentralPMCID:PMC5484650. (PMID: 10.4110/in.2017.17.3.192286803815484650)
Chowdhury P, Khan SA (2019) Differential Expression Levels of Inflammatory Chemokines and TLRs in Patients Suffering from Mild and Severe Japanese Encephalitis. Viral Immunol 32(1):68–74. https://doi.org/10.1089/vim.2018.0103. (PMID: 10.1089/vim.2018.010330585774)
Christensen JE, Nansen A, Moos T, Lu B, Gerard C, Christensen JP, Thomsen AR (2004) Efficient T-cell surveillance of the CNS requires expression of the CXC chemokine receptor 3. The Journal of neuroscience : the official journal of the Society for Neuroscience 24(20):4849–4858. https://doi.org/10.1523/JNEUROSCI.0123-04.2004. (PMID: 10.1523/JNEUROSCI.0123-04.200415152045)
Christensen JE, Simonsen S, Fenger C, Sørensen MR, Moos T, Christensen JP, Finsen B, Thomsen AR (2009) Fulminant lymphocytic choriomeningitis virus-induced inflammation of the CNS involves a cytokine-chemokine-cytokine-chemokine cascade. J Immunol 182(2):1079–1087. https://doi.org/10.4049/jimmunol.182.2.1079. (PMID: 10.4049/jimmunol.182.2.107919124751)
Das S, Dutta K, Kumawat KL, Ghoshal A, Adhya D, Basu A (2011) Abrogated inflammatory response promotes neurogenesis in a murine model of Japanese encephalitis. PloS One 6(3):e17225. https://doi.org/10.1371/journal.pone.0017225. (PMID: 10.1371/journal.pone.0017225213902303048396)
Dudvarski Stankovic N, Teodorczyk M, Ploen R, Zipp F, Schmidt MHH (2016) Microglia–blood vessel interactions: a double-edged sword in brain pathologies. Acta Neuropathol 131:347–63. (PMID: 10.1007/s00401-015-1524-y26711460)
Dutta K, Mishra MK, Nazmi A, Kumawat KL, Basu A (2010) Minocycline differentially modulates macrophage mediated peripheral immune response following Japanese encephalitis virus infection. Immunobiology 215(11):884–893. https://doi.org/10.1016/j.imbio.2009.12.003. (PMID: 10.1016/j.imbio.2009.12.00320153075)
Dwibedi B, Mohapatra N, Rathore SK, Panda M, Pati SS, Sabat J, Thakur B, Panda S, Kar SK (2015) An outbreak of Japanese encephalitis after two decades in Odisha, India. Indian J Med Res 142(Suppl 1):S30–S32. https://doi.org/10.4103/0971-5916.176609. (PMID: 10.4103/0971-5916.176609269052394795344)
Endy TP, Nisalak A (2002) Japanese encephalitis virus: ecology and epidemiology. Curr Top Microbiol Immunol 267:11–48. https://doi.org/10.1007/978-3-642-59403-8_2. (PMID: 10.1007/978-3-642-59403-8_212082986)
Fang J, Sun L, Peng G, Xu J, Zhou R, Cao S, Chen H, Song Y (2013) Identification of three antiviral inhibitors against Japanese encephalitis virus from library of pharmacologically active compounds 1280. PloS One 8(11):e78425. https://doi.org/10.1371/journal.pone.0078425. (PMID: 10.1371/journal.pone.0078425243489013857149)
Farina C, Aloisi F, Meinl E (2007) Astrocytes are active players in cerebral innate immunity. Trends Immunol 28:138–145. (PMID: 10.1016/j.it.2007.01.00517276138)
Fekete R, Cserép C, Lénárt N, Tóth K, Orsolits B, Martinecz B et al (2018) Microglia control the spread of neurotropic virus infection via P2Y12 signalling and recruit monocytes through P2Y12-independent mechanisms. Acta Neuropathol 136:461–482. (PMID: 10.1007/s00401-018-1885-0300274506096730)
German AC, Myint KS, Mai NT, Pomeroy I, Phu NH, Tzartos J et al (2006) A preliminary neuropathological study of Japanese encephalitis in humans and a mouse model. Trans R Soc Trop Med Hyg 100(12):1135–45. https://doi.org/10.1016/j.trstmh.2006.02.008 . PMID: 16814333. (PMID: 10.1016/j.trstmh.2006.02.00816814333)
Ghosh J, Swarup V, Saxena A, Das S, Hazra A, Paira P, Banerjee S, Mondal NB, Basu A (2008) Therapeutic effect of a novel anilidoquinoline derivative, 2-[2-methyl-quinoline-4ylamino]-N-[2-chlorophenyl]-acetamide, in Japanese encephalitis: correlation with in vitro neuroprotection. Int J Antimicrob Agents 32(4):349–354. https://doi.org/10.1016/j.ijantimicag.2008.05.001. (PMID: 10.1016/j.ijantimicag.2008.05.00118674886)
Ghoshal A, Das S, Ghosh S, Mishra MK, Sharma V, Koli P, Sen E, Basu A (2007) Proinflammatory mediators released by activated microglia induces neuronal death in Japanese encephalitis. Glia 55(5):483–496. https://doi.org/10.1002/glia.20474. (PMID: 10.1002/glia.2047417203475)
Glasner DR, Ratnasiri K, Puerta-Guardo H et al (2017) Dengue virus NS1 cytokine-independent vascular leak is dependent on endothelial glycocalyx components. PLoS Pathog 13:e1006673. (PMID: 10.1371/journal.ppat.1006673291210995679539)
Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM (2005) Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 202(8):1087–1098. https://doi.org/10.1084/jem.20042530. (PMID: 10.1084/jem.20042530162304762213214)
Glass WG, Hickey MJ, Hardison JL, Liu MT, Manning JE, Lane TE (2004) Antibody targeting of the CC chemokine ligand 5 results in diminished leukocyte infiltration into the central nervous system and reduced neurologic disease in a viral model of multiple sclerosis. J Immunol [Baltimore, Md. : 1950] 172(7):4018–4025. https://doi.org/10.4049/jimmunol.172.7.4018. (PMID: 10.4049/jimmunol.172.7.401815034013)
Gough DJ, Messina NL, Clarke CJ, Johnstone RW, Levy DE (2012) Constitutive type I interferon modulates homeostatic balance through tonic signaling. Immunity 36:166–174. (PMID: 10.1016/j.immuni.2012.01.011223656633294371)
Halstead SB, Thomas SJ (2011) New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10(3):355–364. https://doi.org/10.1586/erv.11.7. (PMID: 10.1586/erv.11.721434803)
Hasegawa H, Satake Y, Kobayashi Y (1990) Effect of cytokines on Japanese encephalitis virus production by human monocytes. J Microbiol Immunol 34(5):459–466. https://doi.org/10.1111/j.1348-0421.1990.tb01028.x. (PMID: 10.1111/j.1348-0421.1990.tb01028.x)
Hickman SE, Kingery ND, Ohsumi TK, Borowsky ML, Wang LC, Means TK, El Khoury J (2013) The microglial sensome revealed by direct RNA sequencing. Nat Neurosci 16(12):1896–1905. https://doi.org/10.1038/nn.3554. (PMID: 10.1038/nn.3554241626523840123)
Hoke CH Jr, Vaughn DW, Nisalak A, Intralawan P, Poolsuppasit S, Jongsawas V, Titsyakorn U, Johnson RT (1992) Effect of high-dose dexamethasone on the outcome of acute encephalitis due to Japanese encephalitis virus. J Infect Dis 165(4):631–637. https://doi.org/10.1093/infdis/165.4.631. (PMID: 10.1093/infdis/165.4.6311313068)
Hsieh JT, St John AL, Evans MJ (2020) Japanese encephalitis virus and its mechanisms of neuroinvasion. PLoS Pathog 16(4):e1008260. (PMID: 10.1371/journal.ppat.1008260322402727117652)
Huang HN, Rajanbabu V, Pan CY, Chan YL, Hui CF, Chen JY, Wu CJ (2011) Modulation of the immune-related gene responses to protect mice against Japanese encephalitis virus using the antimicrobial peptide, tilapia hepcidin 1–5. Biomaterials 32(116).
Huppert J, Closhen D, Croxford A, White R, Kulig P, Pietrowski E, Bechmann I, Becher B, Luhmann HJ, Waisman A, Kuhlmann CR (2010) Cellular mechanisms of IL-17-induced blood-brain barrier disruption. FASEB J 24:1023–1034. https://doi.org/10.1096/fj.09-141978. (PMID: 10.1096/fj.09-14197819940258)
Ireland DDC, Manangeeswaran M, Lewkowicz AP, Engel K, Clark SM, Laniyan A, Sykes J, Lee HN, McWilliams IL, Kelley-Baker L et al (2020) Long-term persistence of infectious Zika virus: Inflammation and behavioral sequela in mice. PLoS Pathog 16:e1008689. (PMID: 10.1371/journal.ppat.1008689333015277728251)
Jakhmola S, Jha HC (2021) Glial cell response to Epstein-Barr Virus infection: A plausible contribution to virus-associated inflammatory reactions in the brain. Virology 559:182–195. (PMID: 10.1016/j.virol.2021.04.00533964684)
Johari J, Kianmehr A, Mustafa MR, Abubakar S, Zandi K (2012) Antiviral activity of baicalein and quercetin against the Japanese encephalitis virus. Int J Mol Sci 13(12):16785–16795. https://doi.org/10.3390/ijms131216785. (PMID: 10.3390/ijms131216785232226833546721)
Jorgačevski J, Korva M, Potokar M, Lisjak M, Avšič-Županc T, Zorec R (2019) ZIKV Strains Differentially Affect Survival of Human Fetal Astrocytes versus Neurons and Traffic of ZIKV-Laden Endocytotic Compartments. Sci Rep 9:8069. (PMID: 10.1038/s41598-019-44559-8311476296542792)
Kalita J, Srivastava R, Mishra MK, Basu A, Misra UK (2010) Cytokines and chemokines in viral encephalitis: a clinicoradiological correlation. Neurosci Lett 473(1):48–51. https://doi.org/10.1016/j.neulet.2010.02.017. (PMID: 10.1016/j.neulet.2010.02.01720153811)
Keaney J, Campbell M (2015) The dynamic blood-brain barrier. Febs J 282(21):4067–4079. (PMID: 10.1111/febs.1341226277326)
Kim JH, Choi JY, Kim SB, Uyangaa E, Patil AM, Han YW et al (2015) CD11c(hi) Dendritic Cells Regulate Ly-6C(hi) Monocyte Differentiation to Preserve Immune-privileged CNS in Lethal Neuroinflammation. Sci Rep 5:17548. https://doi.org/10.1038/srep17548 . PMID:26626303;PubMedCentralPMCID:PMC4667186. (PMID: 10.1038/srep17548266263034667186)
Kim JH, Hossain FM, Patil AM, Choi JY, Kim SB, Uyangaa E, Park SY, Lee JH, Kim B, Kim K, Eo SK (2016a) Ablation of CD11c[hi] dendritic cells exacerbates Japanese encephalitis by regulating blood-brain barrier permeability and altering tight junction/adhesion molecules. Comparative immunology, microbiology and infectious diseases 48:22–32. https://doi.org/10.1016/j.cimid.2016.07.007. (PMID: 10.1016/j.cimid.2016.07.00727638116)
Kim JH, Patil AM, Choi JY, Kim SB, Uyangaa E, Hossain FM, Park SY, Lee JH, Kim K, Eo SK (2016b) CCL2, but not its receptor, is essential to restrict immune privileged central nervous system-invasion of Japanese encephalitis virus via regulating accumulation of CD11b[+] Ly-6C[hi] monocytes. Immunology 149(2):186–203. https://doi.org/10.1111/imm.12626. (PMID: 10.1111/imm.12626272601365011677)
Klein RS, Lin E, Zhang B, Luster AD, Tollett J, Samuel MA, Engle M, Diamond MS (2005) Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol 79(17):11457–11466. https://doi.org/10.1128/JVI.79.17.11457-11466.2005. (PMID: 10.1128/JVI.79.17.11457-11466.2005161031961193600)
Knap N, Korva M, Dolinšek V, Sekirnik M, Trilar T, Avšič-Županc T (2012) Patterns of tick-borne encephalitis virus infection in rodents in Slovenia. Vector Borne Zoonotic Dis 12:236–242. (PMID: 10.1089/vbz.2011.072822022821)
Kumar R, Tripathi P, Baranwal M, Singh S, Tripathi S, Banerjee G (2009) Randomized, controlled trial of oral ribavirin for Japanese encephalitis in children in Uttar Pradesh, India. Clinical infectious diseases : an official publication of the Infectious Diseases Society of America 48(4):400–406. https://doi.org/10.1086/596309. (PMID: 10.1086/59630919143532)
Lai CY, Ou YC, Chang CY, Pan HC, Chang CJ, Liao SL, Su HL, Chen CJ (2012) Endothelial Japanese encephalitis virus infection enhances migration and adhesion of leukocytes to brain microvascular endothelia via MEK-dependent expression of ICAM1 and the CINC and RANTES chemokines. J Neurochem 123(2):250–261. https://doi.org/10.1111/j.1471-4159.2012.07889.x. (PMID: 10.1111/j.1471-4159.2012.07889.x22845610)
Lannes N, Summerfield A, Filgueira L (2017a) Regulation of inflammation in Japanese encephalitis. J Neuroinflammation 14(1):158-. https://doi.org/10.1186/s12974-017-0931-5 . PMID: 28807053. (PMID: 10.1186/s12974-017-0931-5288070535557552)
Lannes N, Neuhaus V, Scolari B, Kharoubi-Hess S, Walch M, Summerfield A, Filgueira L (2017b) Interactions of human microglia cells with Japanese encephalitis virus. Virol J 14(1):8. https://doi.org/10.1186/s12985-016-0675-3. (PMID: 10.1186/s12985-016-0675-3280882495237516)
Larena M, Regner M, Lobigs M (2013) Cytolytic effector pathways and IFN-gamma help protect against Japanese encephalitis. Eur J Immunol 43(7):1789–1798. https://doi.org/10.1002/eji.201243152 . Epub 2013/04/10. PMID: 23568450. (PMID: 10.1002/eji.20124315223568450)
Lau EK, Allen S, Hsu AR, Handel TM (2004) Chemokine-receptor interactions: GPCRs, glycosaminoglycans and viral chemokine binding proteins. Adv Protein Chem 68:351–391. https://doi.org/10.1016/S0065-3233[04]68010-7. (PMID: 10.1016/S0065-3233[04]68010-715500866)
Li GH, Henderson L, Nath A (2016) Astrocytes as an HIV Reservoir: Mechanism of HIV Infection. Curr HIV Res 14:373–381. (PMID: 10.2174/1570162X146661610061214552771966311345863)
Li W, Hofer MJ, Songkhunawej P, Jung SR, Hancock D, Denyer G, Campbell IL (2017) Type I interferon-regulated gene expression and signaling in murine mixed glial cells lacking signal transducers and activators of transcription 1 or 2 or interferon regulatory factor 9. J Biol Chem 292:5845–5859. (PMID: 10.1074/jbc.M116.756510282135225392577)
Li L, Acioglu C, Heary RF, Elkabes S (2021) Role of astroglial toll-like receptors (TLRs) in central nervous system infections, injury and neurodegenerative diseases. Brain Behav Immun 91(740–755):53.
Lim JK, Louie CY, Glaser C, Jean C, Johnson B, Johnson H, McDermott DH, Murphy PM (2008) Genetic deficiency of chemokine receptor CCR5 is a strong risk factor for symptomatic West Nile virus infection: a meta-analysis of 4 cohorts in the US epidemic. The Journal of infectious diseases 197(2):262–265. https://doi.org/10.1086/524691. (PMID: 10.1086/52469118179388)
Limonta D, Jovel J, Kumar A, Airo AM, Hou S, Saito L, Branton W, Ka-Shu Wong G, Mason A, Power C et al (2018) Human Fetal Astrocytes Infected with Zika Virus Exhibit Delayed Apoptosis and Resistance to Interferon: Implications for Persistence. Viruses 10:646. (PMID: 10.3390/v10110646304536216266559)
Lindqvist R, Mundt F, Gilthorpe JD, Wölfel S, Gekara NO, Kröger A, Överby AK (2016a) Fast type I interferon response protects astrocytes from flavivirus infection and virus-induced cytopathic effects. J. Neuroinflammation 13:277. (PMID: 10.1186/s12974-016-0748-7277765485078952)
Lindqvist R, Mundt F, Gilthorpe JD, Wolfel S, Gekara NO, Kroger A et al (2016b) Fast type I interferon response protects astrocytes from flavivirus infection and virus-induced cytopathic effects. J Neuroinflammation 13(1):277. https://doi.org/10.1186/s12974-016-0748-7 . Epub 2016/10/26. PMID:27776548; PubMed Central PMCID: PMC5078952. (PMID: 10.1186/s12974-016-0748-7277765485078952)
Linnerbauer M, Wheeler MA, Quintana FJ (2020) Astrocyte Crosstalk in CNS Inflammation. Neuron 108:608–622. (PMID: 10.1016/j.neuron.2020.08.012328984757704785)
Liu H, Nakayama EE, Theodorou I, Nagai Y, Likanonsakul S, Wasi C, Debre P, Iwamoto A, Shioda T (2007) Polymorphisms in CCR5 chemokine receptor gene in Japan. Int J Immunogenet 34(5):325–335. https://doi.org/10.1111/j.1744-313X.2007.00694.x. (PMID: 10.1111/j.1744-313X.2007.00694.x17845302)
Liu TH, Liang LC, Wang CC, Liu HC, Chen WJ (2008) The blood-brain barrier in the cerebrum is the initial site for the Japanese encephalitis virus entering the central nervous system. J Neurovirol 14(6):514–521. https://doi.org/10.1080/13550280802339643. (PMID: 10.1080/1355028080233964319023687)
Liu K, Xiao C, Wang F, Xiang X, Ou A, Wei J, Li B, Shao D, Miao D, Zhao F, Long G, Qiu Y, Zhu H, Ma Z (2018) Chemokine receptor antagonist block inflammation and therapy Japanese encephalitis virus infection in mouse model. Cytokine 110:70–77. https://doi.org/10.1016/j.cyto.2018.04.022. (PMID: 10.1016/j.cyto.2018.04.02229704821)
Liu MT, Chen BP, Oertel P, Buchmeier MJ, Armstrong D, Hamilton TA, Lane TE (2000) The T cell chemoattractant IFN-inducible protein 10 is essential in host defense against viral-induced neurologic disease [Baltimore, Md. : 1950]. J Immunol 165(5):2327–2330. https://doi.org/10.4049/jimmunol.165.5.2327. (PMID: 10.4049/jimmunol.165.5.232710946253)
Liu MT, Keirstead HS, Lane TE (2001) Neutralization of the chemokine CXCL10 reduces inflammatory cell invasion and demyelination and improves neurological function in a viral model of multiple sclerosis. J Immunol [Baltimore, Md. : 1950] 167(7):4091–4097. https://doi.org/10.4049/jimmunol.167.7.4091. (PMID: 10.4049/jimmunol.167.7.409111564831)
Ludlow M, Kortekaas J, Herden C, Hoffmann B, Tappe D, Trebst C, Griffin DE, Brindle HE, Solomon T, Brown AS et al (2016) Neurotropic virus infections as the cause of immediate and delayed neuropathology. Acta Neuropathol 131:159–184. (PMID: 10.1007/s00401-015-1511-326659576)
Mameli G, Poddighe L, Mei A, Uleri E, Sotgiu S, Serra C, Manetti R, Dolei A (2012) Expression and activation by Epstein Barr virus of human endogenous retroviruses-W in blood cells and astrocytes: Inference for multiple sclerosis. PLoS ONE 7:e44991. (PMID: 10.1371/journal.pone.0044991230287273459916)
Man S, Ubogu EE, Ransohoff RM (2007) Inflammatory cell migration into the central nervous system: a few new twists on an old tale. Brain Pathol 17:243–250. https://doi.org/10.1111/j.1750-3639.2007.00067.x. (PMID: 10.1111/j.1750-3639.2007.00067.x173889558095646)
Mandl C (2005) Steps of the tick-borne encephalitis virus replication cycle that affect neuropathogenesis. Virus Res 111:161–174. (PMID: 10.1016/j.virusres.2005.04.00715871909)
Mathur A, Khanna N, Chaturvedi UC (1992) Breakdown of blood-brain barrier by virus-induced cytokine during Japanese encephalitis virus infection. Int J Exp Pathol 73:603–611. (PMID: 13299142002010)
Miner JJ, Diamond MS (2016) Mechanisms of restriction of viral neuroinvasion at the blood-brain barrier. Curr Opin Immunol 38:18–23. (PMID: 10.1016/j.coi.2015.10.00826590675)
Mishra MK, Kumawat KL, Basu A (2008) Japanese encephalitis virus differentially modulates the induction of multiple proinflammatory mediators in human astrocytoma and astroglioma cell-lines. Cell Biol Int 32:1506–1513. https://doi.org/10.1016/j.cellbi.2008.08.020. (PMID: 10.1016/j.cellbi.2008.08.02018801452)
Mishra MK, Dutta K, Saheb SK, Basu A (2009) Understanding the molecular mechanism of blood-brain barrier damage in an experimental model of Japanese encephalitis: correlation with minocycline administration as a therapeutic agent. Neurochem Int 55(8):717–723. https://doi.org/10.1016/j.neuint.2009.07.006. (PMID: 10.1016/j.neuint.2009.07.00619628016)
Misra UK, Kalita J (1997) Movement disorders in Japanese encephalitis. J Neurol 244(5):299–303. https://doi.org/10.1007/s004150050090. (PMID: 10.1007/s0041500500909178154)
Misra UK, Kalita J (2010) Overview: Japanese encephalitis. Prog Neurobiol 91(2):108–120. https://doi.org/10.1016/j.pneurobio.2010.01.008. (PMID: 10.1016/j.pneurobio.2010.01.00820132860)
Murayama T, Yamaguchi N, Iwamoto K, Eizuru Y (2006) Inhibition of ganciclovir-resistant human cytomegalovirus replication by Kampo [Japanese herbal medicine]. Antivir Chem Chemother 17(1):11–16. https://doi.org/10.1177/095632020601700102. (PMID: 10.1177/09563202060170010216542001)
Murdoch C, Finn A (2000) Chemokine receptors and their role in inflammation and infectious diseases. Blood 95(10):3032–3043. (PMID: 10.1182/blood.V95.10.303210807766)
Muse M, Kane JA, Carr DJ, Farber JM, Lane TE (2008) Insertion of the CXC chemokine ligand 9 [CXCL9] into the mouse hepatitis virus genome results in protection from viral-induced encephalitis and hepatitis. Virology 382(2):132–44. https://doi.org/10.1016/j.virol.2008.09.032. (PMID: 10.1016/j.virol.2008.09.03218973912)
Nazmi A, Dutta K, Basu A (2010) Antiviral and neuroprotective role of octaguanidinium dendrimer-conjugated morpholino oligomers in Japanese encephalitis. PLOS Negl Trop Dis 4(11):e892. https://doi.org/10.1371/journal.pntd.000089. (PMID: 10.1371/journal.pntd.0000892211248822990691)
Negishi H, Taniguchi T, Yanai H (2018) The Interferon (IFN) Class of Cytokines and the IFN Regulatory Factor (IRF) Transcription Factor Family. Cold Spring Harb Perspect Biol 10:a028423. (PMID: 10.1101/cshperspect.a028423289631096211389)
Palus M, Bílý T, Elsterová J, Langhansová H, Salát J, Vancová M, Růžek D (2014) Infection and injury of human astrocytes by tick-borne encephalitis virus. J Gen Virol 95:2411–2426. (PMID: 10.1099/vir.0.068411-025000960)
Parida M, Dash PK, Tripathi NK, Sannarangaiah Ambuj S, Saxena P, Agarwal S, Sahni AK, Singh SP, Rathi AK, Bhargava R, Abhyankar A, Verma SK, Rao PV, Sekhar K (2006) Japanese Encephalitis Outbreak, India, 2005. Emerg Infect Dis 12(9):1427–1430. https://doi.org/10.3201/eid1209.060200. (PMID: 10.3201/eid1209.060200170730953294746)
Pfeffer M, Dobler G (2010) Emergence of zoonotic arboviruses by animal trade and migration. Parasites Vectors 3(1):35. https://doi.org/10.1186/1756-3305-3-35. (PMID: 10.1186/1756-3305-3-35203778732868497)
Plesner AM, Arlien-Soborg P, Herning M (1998) Neurological complications to vaccination against Japanese encephalitis. Eur J Neurol  5(5):479–485. https://doi.org/10.1046/j.1468-1331.1998.550479.x. (PMID: 10.1046/j.1468-1331.1998.550479.x10210877)
Potokar M, Korva M, Jorgačevski J, Avšič-Županc T, Zorec R (2014) Tick-borne encephalitis virus infects rat astrocytes but does not affect their viability. PLoS ONE 9:e86219. (PMID: 10.1371/journal.pone.0086219244659693896472)
Potokar M, Jorgacevski J, Zorec R (2019) Astrocytes in Flavivirus Infections. Int J Mol Sci 20:691. (PMID: 10.3390/ijms20030691307362736386967)
Puerta-Guardo H, Glasner DR, Espinosa DA et al (2019) Flavivirus NS1 triggers tissue-specific vascular endothelial dysfunction reflecting disease tropism. Cell Rep 26:1598–1613. (PMID: 10.1016/j.celrep.2019.01.036307267416934102)
Ray NB, Power C, Lynch WP, Ewalt LC, Lodmell DL (1997) Rabies viruses infect primary cultures of murine, feline, and human microglia and astrocytes. Arch Virol 142:1011–1019. (PMID: 10.1007/s00705005013691918657086959)
Richards DM, Carmine AA, Brogden RN, Heel RC, Speight TM, Avery GS (1983) Acyclovir. A review of its pharmacodynamic properties and therapeutic efficacy. Drugs 26(5):378–438. https://doi.org/10.2165/00003495-198326050-00002. (PMID: 10.2165/00003495-198326050-000026315332)
Sebastian L, Desai A, Madhusudana SN, Ravi V (2009) Pentoxifylline inhibits replication of Japanese encephalitis virus: a comparative study with ribavirin. Int J Antimicrob Agents 33(2):168–173. https://doi.org/10.1016/j.ijantimicag.2008.07.013. (PMID: 10.1016/j.ijantimicag.2008.07.01318804347)
Sehgal N, Kumawat KL, Basu A, Ravindranath V (2012) Fenofibrate reduces mortality and precludes neurological deficits in survivors in murine model of Japanese encephalitis viral infection. PloS one 7(4):e35427. https://doi.org/10.1371/journal.pone.0035427. (PMID: 10.1371/journal.pone.0035427225147423325984)
Shi Z, Wei J, Deng X, Li S, Qiu Y, Shao D, Li B, Zhang K, Xue F, Wang X, Ma Z (2014) Nitazoxanide inhibits the replication of Japanese encephalitis virus in cultured cells and in a mouse model. Virol J 11:10. https://doi.org/10.1186/1743-422X-11-10. (PMID: 10.1186/1743-422X-11-10244568153927656)
Singh A, Kulshreshtha R, Mathur A (2000) Secretion of the chemokine interleukin-8 during Japanese encephalitis virus infection. J Med Microbiol 49(7):607–612. https://doi.org/10.1099/0022-1317-49-7-607. (PMID: 10.1099/0022-1317-49-7-60710882085)
Singh S, Singh G, Tiwari S, Kumar A (2020) CCR2 Inhibition Reduces Neurotoxic Microglia Activation Phenotype After Japanese Encephalitis Viral Infection. Front Cell Neurosci 14:230. https://doi.org/10.3389/fncel.2020.00230. (PMID: 10.3389/fncel.2020.00230329037997439097)
Sooryanarain H, Sapkal GN, Gore MM (2012) Pathogenic and vaccine strains of Japanese encephalitis virus elicit different levels of human macrophage effector functions. Arch Virol 157(10):1905–1918. https://doi.org/10.1007/s00705-012-1386-8. (PMID: 10.1007/s00705-012-1386-822729616)
Sorce S, Bonnefont J, Julien S, Marq-Lin N, Rodriguez I, Dubois-Dauphin M, Krause KH (2010) Increased brain damage after ischaemic stroke in mice lacking the chemokine receptor CCR5. Br J Pharmacol 160(2):311–321. https://doi.org/10.1111/j.1476-5381.2010.00697.x. (PMID: 10.1111/j.1476-5381.2010.00697.x204233422874853)
Spengler JR, Kelly Keating M, McElroy AK, Zivcec M, Coleman-McCray JD, Harmon JR, Bollweg BC, Goldsmith CS, Bergeron É, Keck JG et al (2017) Crimean-Congo Hemorrhagic Fever in Humanized Mice Reveals Glial Cells as Primary Targets of Neurological Infection. J Infect Dis 216:1386–1397. (PMID: 10.1093/infdis/jix21528482001)
Srivastava R, Kalita J, Khan MY, Misra UK (2012) Status of proinflammatory and anti-inflammatory cytokines in different brain regions of a rat model of Japanese encephalitis. Inflamm Res : Official Journal of the European Histamine Research Society … [et al.] 61(4):381–389. https://doi.org/10.1007/s00011-011-0423-5. (PMID: 10.1007/s00011-011-0423-5)
Swarup V, Ghosh J, Ghosh S, Saxena A, Basu A (2007) Antiviral and anti-inflammatory effects of rosmarinic acid in an experimental murine model of Japanese encephalitis. Antimicrob Agents Chemother 51(9):3367–3370. https://doi.org/10.1128/AAC.00041-07. (PMID: 10.1128/AAC.00041-07175768302043228)
Swarup V, Ghosh J, Mishra MK, Basu A (2008) Novel strategy for treatment of Japanese encephalitis using arctigenin, a plant lignan. J Antimicrob Chemother 61(3):679–688. https://doi.org/10.1093/jac/dkm503. (PMID: 10.1093/jac/dkm50318230688)
Takeuchi T, Miyasaka N, Kawai S, Sugiyama N, Yuasa H, Yamashita N, Sugiyama N, Wagerle LC, Vlahos B, Wajdula J (2015) Pharmacokinetics, efficacy and safety profiles of etanercept monotherapy in Japanese patients with rheumatoid arthritis: review of seven clinical trials. Mod Rheumatol 25(2):173–186. https://doi.org/10.3109/14397595.2014.914014. (PMID: 10.3109/14397595.2014.91401424842477)
Trifilo MJ, Montalto-Morrison C, Stiles LN, Hurst KR, Hardison JL, Manning JE, Masters PS, Lane TE (2004) CXC chemokine ligand 10 controls viral infection in the central nervous system: evidence for a role in innate immune response through recruitment and activation of natural killer cells. J Virol 78(2):585–594. https://doi.org/10.1128/jvi.78.2.585-594.2004. (PMID: 10.1128/jvi.78.2.585-594.200414694090368822)
van den Hurk AF, Ritchie SA, Mackenzie JS (2009) Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54:17–35. https://doi.org/10.1146/annurev.ento.54.110807.090510. (PMID: 10.1146/annurev.ento.54.110807.09051019067628)
Villabona-Rueda A, Erice C, Pardo CA et al (2019) The evolving concept of the Blood Brain Barrier (BBB): From a single static barrier to a heterogeneous and dynamic relay center. Front Cell Neurosci 13:405. (PMID: 10.3389/fncel.2019.00405316162516763697)
Vonderstein K, Nilsson E, Hubel P, Nygård Skalman L, Upadhyay A, Pasto J, Pichlmair A, Lundmark R, Överby A.K. Viperin (2018) Targets Flavivirus Virulence by Inducing Assembly of Noninfectious Capsid Particles. J Virol 92.
Wang X, Zhang K, Yang F, Ren Z, Xu M, Frank JA, Ke ZJ, Luo J (2018) Minocycline protects developing brain against ethanol-induced damage. Neuropharmacology 129:84–99. https://doi.org/10.1016/j.neuropharm.2017.11.019. (PMID: 10.1016/j.neuropharm.2017.11.01929146504)
Winter PM, Dung NM, Loan HT, Kneen R, Wills B, Thu I, House D, White NJ, Farrar JJ, Hart CA, Solomon T (2004) Proinflammatory cytokines and chemokines in humans with Japanese encephalitis. J Infect Dis 190(9):1618–1626. https://doi.org/10.1086/423328. (PMID: 10.1086/42332815478067)
Ye J, Jiang R, Cui M, Zhu B, Sun L, Wang Y, Zohaib A, Dong Q, Ruan X, Song Y, He W, Chen H, Cao S (2014) Etanercept reduces neuroinflammation and lethality in mouse model of Japanese encephalitis. J Infect Dis 210(6):875–889. https://doi.org/10.1093/infdis/jiu179. (PMID: 10.1093/infdis/jiu17924652493)
Zhang B, Chan YK, Lu B, Diamond MS, Klein RS (2008) CXCR3 mediates region-specific antiviral T cell trafficking within the central nervous system during West Nile virus encephalitis. J Immunol [Baltimore, Md 1950] 180(4):2641–2649. https://doi.org/10.4049/jimmunol.180.4.2641. (PMID: 10.4049/jimmunol.180.4.264118250476)
Zhang F, Qi L, Li T, Li X, Yang D, Cao S, Ye J, Wei B (2019) PD1+CCR2+CD8+ T Cells Infiltrate the Central Nervous System during Acute Japanese Encephalitis Virus Infection. Virol Sin 34(5):538–548. https://doi.org/10.1007/s12250-019-00134-z. (PMID: 10.1007/s12250-019-00134-z312150006814683)

Keywords: Blood brain barrier; Cytokine; Microglia; Neuroinflammation

0 (Cytokines)
0 (Antiviral Agents)

Date Created: 20240606 Date Completed: 20240906 Latest Revision: 20240906

20240906

10.1007/s13365-024-01212-z

38842651