Volume 44 Issue 3
May  2023
Turn off MathJax
Article Contents
Dan Yang, Xiao-Jing Li, De-Zhen Tu, Xiu-Li Li, Bin Wei. Advances in viral encephalitis: Viral transmission, host immunity, and experimental animal models. Zoological Research, 2023, 44(3): 525-542. doi: 10.24272/j.issn.2095-8137.2023.025
Citation: Dan Yang, Xiao-Jing Li, De-Zhen Tu, Xiu-Li Li, Bin Wei. Advances in viral encephalitis: Viral transmission, host immunity, and experimental animal models. Zoological Research, 2023, 44(3): 525-542. doi: 10.24272/j.issn.2095-8137.2023.025

Advances in viral encephalitis: Viral transmission, host immunity, and experimental animal models

doi: 10.24272/j.issn.2095-8137.2023.025
The authors declare that they have no competing interests.
D.Y., X.J.L., and D.Z.T. wrote the original draft and constructed the figures and tables. X.L.L. and B.W. conceptualized, wrote, and edited the manuscript. All authors read and approved the final version of the manuscript.
#Authors contributed equally to this work
Funds:  This work was supported by the National Natural Science Foundation of China (81825011, 81930038, 81961160738), Program of Shanghai Academic/Technology Research Leader (22XD1400800), and Strategic Priority Research Program of the Chinese Academy of Sciences (XDB19030200)
More Information
  • Viral infections have led to many public health crises and pandemics in the last few centuries. Neurotropic virus infection-induced viral encephalitis (VE), especially the symptomatic inflammation of the meninges and brain parenchyma, has attracted growing attention due to its high mortality and disability rates. Understanding the infectious routes of neurotropic viruses and the mechanism underlying the host immune response is critical to reduce viral spread and improve antiviral therapy outcomes. In this review, we summarize the common categories of neurotropic viruses, viral transmission routes in the body, host immune responses, and experimental animal models used for VE study to gain a deeper understanding of recent progress in the pathogenic and immunological mechanisms under neurotropic viral infection. This review should provide valuable resources and perspectives on how to cope with pandemic infections.
  • The authors declare that they have no competing interests.
    D.Y., X.J.L., and D.Z.T. wrote the original draft and constructed the figures and tables. X.L.L. and B.W. conceptualized, wrote, and edited the manuscript. All authors read and approved the final version of the manuscript.
    #Authors contributed equally to this work
  • loading
  • [1]
    Adams Waldorf KM, Nelson BR, Stencel-Baerenwald JE, et al. 2018. Congenital Zika virus infection as a silent pathology with loss of neurogenic output in the fetal brain. Nature Medicine, 24(3): 368−374. doi: 10.1038/nm.4485
    Adams Waldorf KM, Stencel-Baerenwald JE, Kapur RP, et al. 2016. Fetal brain lesions after subcutaneous inoculation of Zika virus in a pregnant nonhuman primate. Nature Medicine, 22(11): 1256−1259. doi: 10.1038/nm.4193
    Agut H, Bonnafous P, Gautheret-Dejean A. 2015. Laboratory and clinical aspects of human herpesvirus 6 infections. Clinical Microbiology Reviews, 28(2): 313−335. doi: 10.1128/CMR.00122-14
    Aguzzi A, Heikenwalder M, Polymenidou M. 2007. Insights into prion strains and neurotoxicity. Nature Reviews Molecular Cell Biology, 8(7): 552−561. doi: 10.1038/nrm2204
    Albe JR, Boyles DA, Walters AW, et al. 2019. Neutrophil and macrophage influx into the central nervous system are inflammatory components of lethal Rift Valley fever encephalitis in rats. PLoS Pathogens, 15(6): e1007833. doi: 10.1371/journal.ppat.1007833
    Alexaki A, Wigdahl B. 2008. HIV-1 infection of bone marrow hematopoietic progenitor cells and their role in trafficking and viral dissemination. PLoS Pathogens, 4(12): e1000215. doi: 10.1371/journal.ppat.1000215
    Aleyas AG, George JA, Han YW, et al. 2009. Functional modulation of dendritic cells and macrophages by Japanese encephalitis virus through MyD88 adaptor molecule-dependent and -independent pathways. The Journal of Immunology, 183(4): 2462−2474. doi: 10.4049/jimmunol.0801952
    Aleyas AG, Han YW, Patil AM, et al. 2012. Impaired cross-presentation of CD8α+CD11c+ dendritic cells by Japanese encephalitis virus in a TLR2/MyD88 signal pathway-dependent manner. European Journal of Immunology, 42(10): 2655−2666. doi: 10.1002/eji.201142052
    Aliota MT, Caine EA, Walker EC, et al. 2016. Characterization of Lethal Zika Virus Infection in AG129 Mice. PLoS Neglected Tropical Diseases, 10(4): e0004682. doi: 10.1371/journal.pntd.0004682
    Al-Obaidi MMJ, Bahadoran A, Har LS, et al. 2017. Japanese encephalitis virus disrupts blood-brain barrier and modulates apoptosis proteins in THBMEC cells. Virus Research, 233: 17−28. doi: 10.1016/j.virusres.2017.02.012
    An J, Kimura-Kuroda J, Hirabayashi Y, et al. 1999. Development of a novel mouse model for dengue virus infection. Virology, 263(1): 70−77. doi: 10.1006/viro.1999.9887
    Ancuta P, Wang JB, Gabuzda D. 2006. CD16+ monocytes produce IL-6, CCL2, and matrix metalloproteinase-9 upon interaction with CX3CL1-expressing endothelial cells. Journal of Leukocyte Biology, 80(5): 1156−1164. doi: 10.1189/jlb.0206125
    Antonucci J, Gehrke L. 2019. Cerebral organoid models for neurotropic viruses. ACS Infectious Diseases, 5(12): 1976−1979. doi: 10.1021/acsinfecdis.9b00339
    Arjona A, Foellmer HG, Town T, et al. 2007. Abrogation of macrophage migration inhibitory factor decreases West Nile virus lethality by limiting viral neuroinvasion. Journal of Clinical Investigation, 117(10): 3059−3066. doi: 10.1172/JCI32218
    Bai FW, Kong KF, Dai JF, et al. 2010. A paradoxical role for neutrophils in the pathogenesis of West Nile virus. The Journal of Infectious Diseases, 202(12): 1804−1812. doi: 10.1086/657416
    Bale JF Jr. 2015. Virus and immune-mediated encephalitides: epidemiology, diagnosis, treatment, and prevention. Pediatric Neurology, 53(1): 3−12. doi: 10.1016/j.pediatrneurol.2015.03.013
    Ballabh P, Braun A, Nedergaard M. 2004. The blood-brain barrier: an overview: structure, regulation, and clinical implications. Neurobiology of Disease, 16(1): 1−13. doi: 10.1016/j.nbd.2003.12.016
    Bao LL, Deng W, Huang BY, et al. 2020. The pathogenicity of SARS-CoV-2 in hACE2 transgenic mice. Nature, 583(7818): 830−833. doi: 10.1038/s41586-020-2312-y
    Beier KT, Saunders A, Oldenburg IA, et al. 2011. Anterograde or retrograde transsynaptic labeling of CNS neurons with vesicular stomatitis virus vectors. Proceedings of the National Academy of Sciences of the United States of America, 108(37): 15414−15419. doi: 10.1073/pnas.1110854108
    Bergmann CC, Altman JD, Hinton D, et al. 1999. Inverted immunodominance and impaired cytolytic function of CD8+ T cells during viral persistence in the central nervous system. The Journal of Immunology, 163(6): 3379−3387. doi: 10.4049/jimmunol.163.6.3379
    Bergmann CC, Lane TE, Stohlman SA. 2006. Coronavirus infection of the central nervous system: host-virus stand-off. Nature Reviews Microbiology, 4(2): 121−132. doi: 10.1038/nrmicro1343
    Bergmann CC, Parra B, Hinton DR, et al. 2003. Perforin-mediated effector function within the central nervous system requires IFN-γ-mediated MHC up-regulation. The Journal of Immunology, 170(6): 3204−3213. doi: 10.4049/jimmunol.170.6.3204
    Bergström T, Svennerholm B, Conradi N, et al. 1991. Discrimination of herpes simplex virus types 1 and 2 cerebral infections in a rat model. Acta Neuropathologica, 82(5): 395−401. doi: 10.1007/BF00296551
    Biswas L, Chen JY, De Angelis J, et al. 2023. Lymphatic vessels in bone support regeneration after injury. Cell, 186(2): 382−397.e24. doi: 10.1016/j.cell.2022.12.031
    Boorman JPT, Porterfield JS. 1956. A simple technique for infection of mosquitoes with viruses transmission of Zika virus. Transactions of the Royal Society of Tropical Medicine and Hygiene, 50(3): 238−242. doi: 10.1016/0035-9203(56)90029-3
    Boutros T, Croze E, Yong VW. 1997. Interferon-beta is a potent promoter of nerve growth factor production by astrocytes. Journal of Neurochemistry, 69(3): 939−946.
    Bradshaw MJ, Venkatesan A. 2016. Herpes simplex virus-1 encephalitis in adults: pathophysiology, diagnosis, and management. Neurotherapeutics, 13(3): 493−508. doi: 10.1007/s13311-016-0433-7
    Brewoo JN, Kinney RM, Powell TD, et al. 2012. Immunogenicity and efficacy of chimeric dengue vaccine (DENVax) formulations in interferon-deficient AG129 mice. Vaccine, 30(8): 1513−1520. doi: 10.1016/j.vaccine.2011.11.072
    Brioschi S, Wang WL, Peng V, et al. 2021. Heterogeneity of meningeal B cells reveals a lymphopoietic niche at the CNS borders. Science, 373(6553): eabf9277. doi: 10.1126/science.abf9277
    Brownell AD, Reynolds TQ, Livingston B, et al. 2015. Human parechovirus-3 encephalitis in two neonates: acute and follow-up magnetic resonance imaging and evaluation of central nervous system markers of inflammation. Pediatric Neurology, 52(2): 245−249. doi: 10.1016/j.pediatrneurol.2014.09.019
    Buescher EL, Scherer WF, Rosenberg MZ, et al. 1959. Ecologic studies of Japanese encephalitis virus in Japan. II. Mosquito infection. The American Journal of Tropical Medicine and Hygiene, 8(6): 651−664. doi: 10.4269/ajtmh.1959.8.651
    Byrne AB, García AG, Brahamian JM, et al. 2021. A murine model of dengue virus infection in suckling C57BL/6 and BALB/c mice. Animal Models and Experimental Medicine, 4(1): 16−26. doi: 10.1002/ame2.12145
    Byrnes AP, Durbin JE, Griffin DE. 2000. Control of Sindbis virus infection by antibody in interferon-deficient mice. Journal of Virology, 74(8): 3905−3908. doi: 10.1128/JVI.74.8.3905-3908.2000
    Cabre P, Smadja D, Cabié A, et al. 2000. HTLV-1 and HIV infections of the central nervous system in tropical areas. Journal of Neurology, Neurosurgery & Psychiatry, 68(5): 550−557.
    Casiraghi C, Dorovini-Zis K, Horwitz MS. 2011. Epstein-Barr virus infection of human brain microvessel endothelial cells: a novel role in multiple sclerosis. Journal of Neuroimmunology, 230(1–2): 173–177.
    Chan JFW, Zhang AJ, Yuan SF, et al. 2020. Simulation of the clinical and pathological manifestations of coronavirus disease 2019 (COVID-19) in a golden syrian hamster model: implications for disease pathogenesis and transmissibility. Clinical Infectious Diseases, 71(9): 2428−2446.
    Chapagain ML, Nerurkar VR. 2010. Human polyomavirus JC (JCV) infection of human B lymphocytes: a possible mechanism for JCV transmigration across the blood-brain barrier. The Journal of Infectious Diseases, 202(2): 184−191. doi: 10.1086/653823
    Cheeran MCJ, Hu SX, Sheng WS, et al. 2005. Differential responses of human brain cells to West Nile virus infection. Journal of Neurovirology, 11(6): 512−524. doi: 10.1080/13550280500384982
    Cheeran MCJ, Lokensgard JR, Schleiss MR. 2009. Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clinical Microbiology Reviews, 22(1): 99−126. doi: 10.1128/CMR.00023-08
    Chen BP, Kuziel WA, Lane TE. 2001. Lack of CCR2 results in increased mortality and impaired leukocyte activation and trafficking following infection of the central nervous system with a neurotropic coronavirus. The Journal of Immunology, 167(8): 4585−4592. doi: 10.4049/jimmunol.167.8.4585
    Chen JM, Wang LM, Xu H, et al. 2020. Meningeal lymphatics clear erythrocytes that arise from subarachnoid hemorrhage. Nature Communications, 11(1): 3159. doi: 10.1038/s41467-020-16851-z
    Chen SY, Deng Y, Pan DL. 2022. MicroRNA regulation of human herpesvirus latency. Viruses, 14(6): 1215. doi: 10.3390/v14061215
    Chen YL, Li H, Yang JX, et al. 2021. A hSCARB2-transgenic mouse model for Coxsackievirus A16 pathogenesis. Virology Journal, 18(1): 84. doi: 10.1186/s12985-021-01557-5
    Chen ZZ, Zhong D, Li GZ. 2019. The role of microglia in viral encephalitis: a review. Journal of Neuroinflammation, 16(1): 76. doi: 10.1186/s12974-019-1443-2
    Chiou SS, Liu H, Chuang CK, et al. 2005. Fitness of Japanese encephalitis virus to Neuro-2a cells is determined by interactions of the viral envelope protein with highly sulfated glycosaminoglycans on the cell surface. Journal of Medical Virology, 76(4): 583−592. doi: 10.1002/jmv.20406
    Choy MM, Ng DHL, Siriphanitchakorn T, et al. 2020. A non-structural 1 protein G53D substitution attenuates a clinically tested live dengue vaccine. Cell Reports, 31(6): 107617. doi: 10.1016/j.celrep.2020.107617
    Christian KM, Song HJ, Ming GL. 2019. Pathophysiology and mechanisms of Zika virus infection in the nervous system. Annual Review of Neuroscience, 42: 249−269. doi: 10.1146/annurev-neuro-080317-062231
    Clay CC, Rodrigues DS, Ho YS, et al. 2007. Neuroinvasion of fluorescein-positive monocytes in acute simian immunodeficiency virus infection. Journal of Virology, 81(21): 12040−12048. doi: 10.1128/JVI.00133-07
    Constantine DG. 1962. Rabies transmission by nonbite route. Public Health Reports, 77(4): 287−289. doi: 10.2307/4591470
    Cox J, Mota J, Sukupolvi-Petty S, et al. 2012. Mosquito bite delivery of dengue virus enhances immunogenicity and pathogenesis in humanized mice. Journal of Virology, 86(14): 7637−7649. doi: 10.1128/JVI.00534-12
    Cserr HF, Knopf PM. 1992. Cervical lymphatics, the blood-brain barrier and the immunoreactivity of the brain: a new view. Immunology Today, 13(12): 507−512. doi: 10.1016/0167-5699(92)90027-5
    Cugurra A, Mamuladze T, Rustenhoven J, et al. 2021. Skull and vertebral bone marrow are myeloid cell reservoirs for the meninges and CNS parenchyma. Science, 373(6553): eabf7844. doi: 10.1126/science.abf7844
    Cvjetković IH, Cvjetković D, Patić A, et al. 2016. Tick-borne encephalitis virus infection in humans. Medicinski Pregled, 69(3–4): 93–98.
    Da Mesquita S, Louveau A, Vaccari A, et al. 2018. Functional aspects of meningeal lymphatics in ageing and Alzheimer's disease. Nature, 560(7717): 185−191. doi: 10.1038/s41586-018-0368-8
    da Silva SR, Gao SJ. 2016. Zika virus: an update on epidemiology, pathology, molecular biology, and animal model. Journal of Medical Virology, 88(8): 1291−1296. doi: 10.1002/jmv.24563
    Dai JF, Wang PH, Bai FW, et al. 2008. ICAM-1 participates in the entry of West Nile virus into the central nervous system. Journal of Virology, 82(8): 4164−4168. doi: 10.1128/JVI.02621-07
    Daneman R, Prat A. 2015. The blood-brain barrier. Cold Spring Harbor Perspectives in Biology, 7(1): a020412. doi: 10.1101/cshperspect.a020412
    Darai G, Schwaier A, Komitowski D, et al. 1978. Experimental infection of Tupaia belangeri (tree shrews) with herpes simplex virus types 1 and 2. The Journal of Infectious Diseases, 137(3): 221−226. doi: 10.1093/infdis/137.3.221
    Das T, Hoarau JJ, Bandjee MCJ, et al. 2015. Multifaceted innate immune responses engaged by astrocytes, microglia and resident dendritic cells against Chikungunya neuroinfection. Journal of General Virology, 96(Pt 2): 294–310.
    de Alcantara BN, Imbeloni AA, de Brito Simith Durans D, et al. 2021. Histopathological lesions of congenital Zika syndrome in newborn squirrel monkeys. Scientific Reports, 11(1): 6099. doi: 10.1038/s41598-021-85571-1
    de Lima KA, Rustenhoven J, Kipnis J. 2020. Meningeal immunity and its function in maintenance of the central nervous system in health and disease. Annual Review of Immunology, 38: 597−620. doi: 10.1146/annurev-immunol-102319-103410
    Delhaye S, Paul S, Blakqori G, et al. 2006. Neurons produce type I interferon during viral encephalitis. Proceedings of the National Academy of Sciences of the United States of America, 103(20): 7835−7840. doi: 10.1073/pnas.0602460103
    Depla JA, Mulder LA, de Sá RV, et al. 2022. Human brain organoids as models for central nervous system viral infection. Viruses, 14(3): 634. doi: 10.3390/v14030634
    Diagne CT, Diallo D, Faye O, et al. 2015. Potential of selected senegalese Aedes spp. mosquitoes (Diptera: Culicidae) to transmit Zika virus. BMC Infectious Diseases, 15: 492. doi: 10.1186/s12879-015-1231-2
    Diamond MS, Shrestha B, Marri A, et al. 2003a. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. Journal of Virology, 77(4): 2578−2586. doi: 10.1128/JVI.77.4.2578-2586.2003
    Diamond MS, Sitati EM, Friend LD, et al. 2003b. A critical role for induced IgM in the protection against West Nile virus infection. Journal of Experimental Medicine, 198(12): 1853−1862. doi: 10.1084/jem.20031223
    Dietzschold B, Kao M, Zheng YM, et al. 1992. Delineation of putative mechanisms involved in antibody-mediated clearance of rabies virus from the central nervous system. Proceedings of the National Academy of Sciences of the United States of America, 89(15): 7252−7256. doi: 10.1073/pnas.89.15.7252
    Ding SW. 2010. RNA-based antiviral immunity. Nature Reviews Immunology, 10(9): 632−644. doi: 10.1038/nri2824
    Duchemin JB, Mee PT, Lynch SE, et al. 2017. Zika vector transmission risk in temperate Australia: a vector competence study. Virology Journal, 14(1): 108. doi: 10.1186/s12985-017-0772-y
    Dudley DM, Aliota MT, Mohr EL, et al. 2016. A rhesus macaque model of Asian-lineage Zika virus infection. Nature Communications, 7: 12204. doi: 10.1038/ncomms12204
    Dudley DM, Van Rompay KK, Coffey LL, et al. 2018. Miscarriage and stillbirth following maternal Zika virus infection in nonhuman primates. Nature Medicine, 24(8): 1104−1107. doi: 10.1038/s41591-018-0088-5
    Erickson MA, Rhea EM, Knopp RC, et al. 2021. Interactions of SARS-CoV-2 with the Blood-Brain barrier. International Journal of Molecular Sciences, 22(5): 2681. doi: 10.3390/ijms22052681
    Falasco RF, Robinson E, Faja BW. 1990. Problems encountered by recent graduates in establishing dental practices. The Journal of the Michigan Dental Association, 72(1): 15−19.
    Fan Y, Yu DD, Yao YG. 2014. Tree shrew database (TreeshrewDB): a genomic knowledge base for the Chinese tree shrew. Scientific Reports, 4: 7145. doi: 10.1038/srep07145
    Fan YC, Liang JJ, Chen JM, et al. 2019. NS2B/NS3 mutations enhance the infectivity of genotype I Japanese encephalitis virus in amplifying hosts. PLoS Pathogens, 15(8): e1007992. doi: 10.1371/journal.ppat.1007992
    Fang Y, Liu ZZ, Qiu Y, et al. 2021. Inhibition of viral suppressor of RNAi proteins by designer peptides protects from enteroviral infection in vivo. Immunity, 54(10): 2231–2244. e6.
    Fekadu M, Shaddock JH, Baer GM. 1982. Excretion of rabies virus in the saliva of dogs. The Journal of Infectious Diseases, 145(5): 715−719. doi: 10.1093/infdis/145.2.715
    Fekete R, Cserép C, Lénárt N, et al. 2018. Microglia control the spread of neurotropic virus infection via P2Y12 signalling and recruit monocytes through P2Y12-independent mechanisms. Acta Neuropathologica, 136(3): 461−482. doi: 10.1007/s00401-018-1885-0
    Ferenczy MW, Marshall LJ, Nelson CDS, et al. 2012. Molecular biology, epidemiology, and pathogenesis of progressive multifocal leukoencephalopathy, the JC virus-induced demyelinating disease of the human brain. Clinical Microbiology Reviews, 25(3): 471−506. doi: 10.1128/CMR.05031-11
    Fiette L, Aubert C, Müller U, et al. 1995. Theiler's virus infection of 129Sv mice that lack the interferon α/β or interferon γ receptors. Journal of Experimental Medicine, 181(6): 2069−2076. doi: 10.1084/jem.181.6.2069
    Fillatre P, Crabol Y, Morand P, et al. 2017. Infectious encephalitis: management without etiological diagnosis 48 hours after onset. Médecine et Maladies Infectieuses, 47(3): 236−251.
    Fisher DL, Defres S, Solomon T. 2015. Measles-induced encephalitis. QJM:An International Journal of Medicine, 108(3): 177−182. doi: 10.1093/qjmed/hcu113
    Fuchs J, Chu HY, O'Day P, et al. 2014. Investigating the efficacy of monovalent and tetravalent dengue vaccine formulations against DENV-4 challenge in AG129 mice. Vaccine, 32(48): 6537−6543. doi: 10.1016/j.vaccine.2014.08.087
    Gao Q, Bao LL, Mao HY, et al. 2020. Development of an inactivated vaccine candidate for SARS-CoV-2. Science, 369(6499): 77−81. doi: 10.1126/science.abc1932
    Garber C, Soung A, Vollmer LL, et al. 2019. T cells promote microglia-mediated synaptic elimination and cognitive dysfunction during recovery from neuropathogenic flaviviruses. Nature Neuroscience, 22(8): 1276−1288. doi: 10.1038/s41593-019-0427-y
    García-Nicolás O, Braun RO, Milona P, et al. 2018. Targeting of the nasal mucosa by Japanese encephalitis virus for non-vector-borne transmission. Journal of Virology, 92(24): e01091−18.
    Gilden DH, Dueland AN, Cohrs R, et al. 1991. Preherpetic neuralgia. Neurology, 41(8): 1215−1218. doi: 10.1212/WNL.41.8.1215
    Glass WG, Lane TE. 2003. Functional expression of chemokine receptor CCR5 on CD4+ T cells during virus-induced central nervous system disease. Journal of Virology, 77(1): 191−198. doi: 10.1128/JVI.77.1.191-198.2003
    Glass WG, Lim JK, Cholera R, et al. 2005. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. Journal of Experimental Medicine, 202(8): 1087−1098. doi: 10.1084/jem.20042530
    González JM, Bergmann CC, Ramakrishna C, et al. 2006. Inhibition of interferon-γ signaling in oligodendroglia delays coronavirus clearance without altering demyelination. The American Journal of Pathology, 168(3): 796−804. doi: 10.2353/ajpath.2006.050496
    González-Scarano F, Martín-García J. 2005. The neuropathogenesis of AIDS. Nature Reviews Immunology, 5(1): 69−81. doi: 10.1038/nri1527
    Gori Savellini G, Anichini G, Gandolfo C, et al. 2019. Toscana virus non-structural protein NSs acts as E3 ubiquitin ligase promoting RIG-I degradation. PLoS Pathogens, 15(12): e1008186. doi: 10.1371/journal.ppat.1008186
    Griffin DE, Metcalf T. 2011. Clearance of virus infection from the CNS. Current Opinion in Virology, 1(3): 216−221. doi: 10.1016/j.coviro.2011.05.021
    Grossberg SE, Scherer WF. 1966. The effect of host age, virus dose and route of inoculation on inapparent infection in mice with Japanese encephalitis virus. Experimental Biology and Medicine, 123(1): 118−124. doi: 10.3181/00379727-123-31418
    Guo XX, Li CX, Deng YQ, et al. 2016. Culex pipiens quinquefasciatus: a potential vector to transmit Zika virus. Emerging Microbes & Infections, 5(9): e102.
    Gurung S, Reuter N, Preno A, et al. 2019. Zika virus infection at mid-gestation results in fetal cerebral cortical injury and fetal death in the olive baboon. PLoS Pathogens, 15(1): e1007507. doi: 10.1371/journal.ppat.1007507
    Haese NN, Roberts VHJ, Chen A, et al. 2021. Nonhuman primate models of Zika virus infection and disease during pregnancy. Viruses, 13(10): 2088. doi: 10.3390/v13102088
    Hameed M, Liu K, Anwar MN, et al. 2019. The emerged genotype I of Japanese encephalitis virus shows an infectivity similar to genotype III in Culex pipiens mosquitoes from China. PLoS Neglected Tropical Diseases, 13(9): e0007716. doi: 10.1371/journal.pntd.0007716
    Hameed M, Wahaab A, Nawaz M, et al. 2021. Potential role of birds in Japanese encephalitis virus zoonotic transmission and genotype shift. Viruses, 13(3): 357. doi: 10.3390/v13030357
    Harling-Berg CJ, Park TJ, Knopf PM. 1999. Role of the cervical lymphatics in the Th2-type hierarchy of CNS immune regulation. Journal of Neuroimmunology, 101(2): 111−127. doi: 10.1016/S0165-5728(99)00130-7
    Heininger U, Seward JF. 2006. Varicella. The Lancet, 368(9544): 1365−1376. doi: 10.1016/S0140-6736(06)69561-5
    Hemachudha T, Ugolini G, Wacharapluesadee S, et al. 2013. Human rabies: neuropathogenesis, diagnosis, and management. The Lancet Neurology, 12(5): 498−513. doi: 10.1016/S1474-4422(13)70038-3
    Hirsch AJ, Smith JL, Haese NN, et al. 2017. Zika Virus infection of rhesus macaques leads to viral persistence in multiple tissues. PLoS Pathogens, 13(3): e1006219. doi: 10.1371/journal.ppat.1006219
    Hirsch JM, Johansson SL, Vahlne A. 1984. Effect of snuff and herpes simplex virus-1 on rat oral mucosa: possible associations with the development of squamous cell carcinoma. Journal of Oral Pathology & Medicine, 13(1): 52−62.
    Hooi YT, Ong KC, Tan SH, et al. 2020. Coxsackievirus A16 in a 1-day-old mouse model of central nervous system infection shows lower neurovirulence than enterovirus A71. Journal of Comparative Pathology, 176: 19−32. doi: 10.1016/j.jcpa.2020.02.001
    Houen G, Trier NH, Frederiksen JL. 2020. Epstein-barr virus and multiple sclerosis. Frontiers in Immunology, 11: 587078. doi: 10.3389/fimmu.2020.587078
    Hsu M, Rayasam A, Kijak JA, et al. 2019. Neuroinflammation-induced lymphangiogenesis near the cribriform plate contributes to drainage of CNS-derived antigens and immune cells. Nature Communications, 10(1): 229. doi: 10.1038/s41467-018-08163-0
    Hu XT, Deng QP, Ma L, et al. 2020. Meningeal lymphatic vessels regulate brain tumor drainage and immunity. Cell Research, 30(3): 229−243. doi: 10.1038/s41422-020-0287-8
    Jiang RD, Liu MQ, Chen Y, et al. 2020. Pathogenesis of SARS-CoV-2 in transgenic mice expressing human angiotensin-converting enzyme 2. Cell, 182(1): 50−58.e8. doi: 10.1016/j.cell.2020.05.027
    Joe S, Salam AAA, Neogi U, et al. 2022. Antiviral drug research for Japanese encephalitis: an updated review. Pharmacological Reports, 74(2): 273−296. doi: 10.1007/s43440-022-00355-2
    Johnson RT, Burke DS, Elwell M, et al. 1985. Japanese encephalitis: immunocytochemical studies of viral antigen and inflammatory cells in fatal cases. Annals of Neurology, 18(5): 567−573. doi: 10.1002/ana.410180510
    Jordan I, Ian Lipkin W. 2001. Borna disease virus. Reviews in Medical Virology, 11(1): 37−57. doi: 10.1002/rmv.300
    Jung S, Aliberti J, Graemmel P, et al. 2000. Analysis of fractalkine receptor CX3CR1 function by targeted deletion and green fluorescent protein reporter gene insertion. Molecular and Cellular Biology, 20(11): 4106−4114. doi: 10.1128/MCB.20.11.4106-4114.2000
    Kennedy PGE. 2005. Viral encephalitis. Journal of Neurology, 252(3): 268−272. doi: 10.1007/s00415-005-0770-7
    Kenyon RH, Rippy MK, McKee KT Jr, et al. 1992. Infection of Macaca radiata with viruses of the tick-borne encephalitis group. Microbial Pathogenesis, 13(5): 399−409. doi: 10.1016/0882-4010(92)90083-Z
    Kim JH, Choi JY, Kim SB, et al. 2015. CD11chi dendritic cells regulate Ly-6Chi monocyte differentiation to preserve immune-privileged CNS in lethal neuroinflammation. Scientific Reports, 5: 17548. doi: 10.1038/srep17548
    Kimberlin DW, Whitley RJ. 1998. Human herpesvirus-6: neurologic implications of a newly-described viral pathogen. Journal of Neurovirology, 4(5): 474−485. doi: 10.3109/13550289809113492
    Kimura T, Sasaki M, Okumura M, et al. 2010. Flavivirus encephalitis: pathological aspects of mouse and other animal models. Veterinary Pathology, 47(5): 806−818. doi: 10.1177/0300985810372507
    Kjeldsen L, Sengelov H, Lollike K, et al. 1994. Isolation and characterization of gelatinase granules from human neutrophils. Blood, 83(6): 1640−1649. doi: 10.1182/blood.V83.6.1640.1640
    Klein RS. 2021. Encephalitic arboviruses of africa: emergence, clinical presentation and neuropathogenesis. Frontiers in Immunology, 12: 769942. doi: 10.3389/fimmu.2021.769942
    Klein RS, Lin E, Zhang B, et al. 2005. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. Journal of Virology, 79(17): 11457−11466. doi: 10.1128/JVI.79.17.11457-11466.2005
    Koyuncu OO, Hogue IB, Enquist LW. 2013. Virus infections in the nervous system. Cell Host & Microbe, 13(4): 379−393.
    Kubinski M, Beicht J, Gerlach T, et al. 2020. Tick-borne encephalitis virus: a quest for better vaccines against a virus on the rise. Vaccines (Basel), 8(3): 451.
    Lam JH, Smith FL, Baumgarth N. 2020. B cell activation and response regulation during viral infections. Viral Immunology, 33(4): 294−306. doi: 10.1089/vim.2019.0207
    Lane TE, Hardison JL, Walsh KB. 2006. Functional diversity of chemokines and chemokine receptors in response to viral infection of the central nervous system. In: Lane TE. Chemokines and Viral Infection. Berlin, Heidelberg: Springer, 1–27.
    Laulund ASB, Trøstrup H, Lerche CJ, et al. 2020. Synergistic effect of immunomodulatory S100A8/A9 and ciprofloxacin against Pseudomonas aeruginosa biofilm in a murine chronic wound model. Pathogens and Disease, 78(5): ftz027. doi: 10.1093/femspd/ftz027
    Lazear HM, Govero J, Smith AM, et al. 2016. A mouse model of Zika virus pathogenesis. Cell Host & Microbe, 19(5): 720−730.
    Lee BJ, Weiss ML, Mosier D, et al. 1999. Spread of bovine herpesvirus type 5 (BHV-5) in the rabbit brain after intranasal inoculation. Journal of Neurovirology, 5(5): 474−484. doi: 10.3109/13550289909045376
    Li CH, Yan LZ, Ban WZ, et al. 2017. Long-term propagation of tree shrew spermatogonial stem cells in culture and successful generation of transgenic offspring. Cell Research, 27(2): 241−252. doi: 10.1038/cr.2016.156
    Li HD, Saucedo-Cuevas L, Regla-Nava JA, et al. 2016a. Zika virus infects neural progenitors in the adult mouse brain and alters proliferation. Cell Stem Cell, 19(5): 593−598. doi: 10.1016/j.stem.2016.08.005
    Li J, Loeb JA, Shy ME, et al. 2003. Asymmetric flaccid paralysis: a neuromuscular presentation of West Nile virus infection. Annals of Neurology, 53(6): 703−710. doi: 10.1002/ana.10575
    Li JP, Liao Y, Zhang Y, et al. 2014. Experimental infection of tree shrews (Tupaia belangeri) with Coxsackie virus A16. Zoological Research, 35(6): 485−491.
    Li LH, Li ZR, Wang EL, et al. 2016b. Herpes simplex virus 1 infection of tree shrews differs from that of mice in the severity of acute infection and viral transcription in the peripheral nervous system. Journal of Virology, 90(2): 790−804. doi: 10.1128/JVI.02258-15
    Li LL, Xu CC, Zhang WJ, et al. 2019. Cargo-compatible encapsulation in virus-based nanoparticles. Nano Letters, 19(4): 2700−2706. doi: 10.1021/acs.nanolett.9b00679
    Li XF, Deng YQ, Yang HQ, et al. 2013. A chimeric dengue virus vaccine using Japanese encephalitis virus vaccine strain SA14–14-2 as backbone is immunogenic and protective against either parental virus in mice and nonhuman primates. Journal of Virology, 87(24): 13694−13705. doi: 10.1128/JVI.00931-13
    Li XF, Dong HL, Huang XY, et al. 2016c. Characterization of a 2016 clinical isolate of Zika virus in non-human primates. eBioMedicine, 12: 170−177. doi: 10.1016/j.ebiom.2016.09.022
    Li XJ, Qi LL, Yang D, et al. 2022. Meningeal lymphatic vessels mediate neurotropic viral drainage from the central nervous system. Nature Neuroscience, 25(5): 577−587. doi: 10.1038/s41593-022-01063-z
    Li YM, Ye J, Yang XH, et al. 2011. Infection of mouse bone marrow-derived dendritic cells by live attenuated Japanese encephalitis virus induces cells maturation and triggers T cells activation. Vaccine, 29(4): 855−862. doi: 10.1016/j.vaccine.2010.09.108
    Lin MT, Stohlman SA, Hinton DR. 1997. Mouse hepatitis virus is cleared from the central nervous systems of mice lacking perforin-mediated cytolysis. Journal of Virology, 71(1): 383−391. doi: 10.1128/jvi.71.1.383-391.1997
    Lindquist L, Vapalahti O. 2008. Tick-borne encephalitis. The Lancet, 371(9627): 1861−1871. doi: 10.1016/S0140-6736(08)60800-4
    Linterman MA, Beaton L, Yu D, et al. 2010. IL-21 acts directly on B cells to regulate Bcl-6 expression and germinal center responses. Journal of Experimental Medicine, 207(2): 353−363. doi: 10.1084/jem.20091738
    Liou ML, Hsu CY. 1998. Japanese encephalitis virus is transported across the cerebral blood vessels by endocytosis in mouse brain. Cell and Tissue Research, 293(3): 389−394. doi: 10.1007/s004410051130
    Liu QY, Wang XJ, Xie CH, et al. 2021. A novel human acute encephalitis caused by pseudorabies virus variant strain. Clinical Infectious Diseases, 73(11): e3690−e3700. doi: 10.1093/cid/ciaa987
    Louveau A. 2018. Meningeal immunity, drainage, and tertiary lymphoid structure formation. In: Dieu-Nosjean MC. Tertiary Lymphoid Structures. New York: Humana Press, 31–45.
    Louveau A, Herz J, Alme MN, et al. 2018. CNS lymphatic drainage and neuroinflammation are regulated by meningeal lymphatic vasculature. Nature Neuroscience, 21(10): 1380−1391. doi: 10.1038/s41593-018-0227-9
    Louveau A, Smirnov I, Keyes TJ, et al. 2015. Structural and functional features of central nervous system lymphatic vessels. Nature, 523(7560): 337−341. doi: 10.1038/nature14432
    Ludlow M, Kortekaas J, Herden C, et al. 2016. Neurotropic virus infections as the cause of immediate and delayed neuropathology. Acta Neuropathologica, 131(2): 159−184. doi: 10.1007/s00401-015-1511-3
    Lundin KE, Good L, Strömberg R, et al. 2006. Biological activity and biotechnological aspects of peptide nucleic acid. Advanceds in Genetics, 56: 1−51.
    Luo Z, Su R, Wang WB, et al. 2019. EV71 infection induces neurodegeneration via activating TLR7 signaling and IL-6 production. PLoS Pathogens, 15(11): e1008142. doi: 10.1371/journal.ppat.1008142
    Maciejewski-Lenoir D, Chen SZ, Feng LL, et al. 1999. Characterization of fractalkine in rat brain cells: migratory and activation signals for CX3CR-1-expressing microglia. The Journal of Immunology, 163(3): 1628−1635. doi: 10.4049/jimmunol.163.3.1628
    Marques RE, Del Sarto JL, Rocha RPF, et al. 2017. Development of a model of Saint Louis encephalitis infection and disease in mice. Journal of Neuroinflammation, 14(1): 61. doi: 10.1186/s12974-017-0837-2
    Martina BEE, Koraka P, van den Doel P, et al. 2008. DC-SIGN enhances infection of cells with glycosylated West Nile virus in vitro and virus replication in human dendritic cells induces production of IFN-α and TNF-α. Virus Research, 135(1): 64−71. doi: 10.1016/j.virusres.2008.02.008
    Martinot AJ, Abbink P, Afacan O, et al. 2018. Fetal neuropathology in Zika virus-infected pregnant female rhesus monkeys. Cell, 173(5): 1111−1122.e10. doi: 10.1016/j.cell.2018.03.019
    Maury A, Lyoubi A, Peiffer-Smadja N, et al. 2021. Neurological manifestations associated with SARS-CoV-2 and other coronaviruses: a narrative review for clinicians. Revue Neurologique, 177(1–2): 51–64.
    Mavigner M, Raper J, Kovacs-Balint Z, et al. 2018. Postnatal Zika virus infection is associated with persistent abnormalities in brain structure, function, and behavior in infant macaques. Science Translational Medicine, 10(435): eaao6975. doi: 10.1126/scitranslmed.aao6975
    McJunkin JE, de los Reyes EC, Irazuzta JE, et al. 2001. La Crosse encephalitis in children. New England Journal of Medicine, 344(11): 801−807. doi: 10.1056/NEJM200103153441103
    McMenamin PG. 1999. Distribution and phenotype of dendritic cells and resident tissue macrophages in the dura mater, leptomeninges, and choroid plexus of the rat brain as demonstrated in wholemount preparations. Journal of Comparative Neurology, 405(4): 553−562. doi: 10.1002/(SICI)1096-9861(19990322)405:4<553::AID-CNE8>3.0.CO;2-6
    Medigeshi GR, Hirsch AJ, Brien JD, et al. 2009. West nile virus capsid degradation of claudin proteins disrupts epithelial barrier function. Journal of Virology, 83(12): 6125−6134. doi: 10.1128/JVI.02617-08
    Meertens L, Bertaux C, Cukierman L, et al. 2008. The tight junction proteins claudin-1, -6, and -9 are entry cofactors for hepatitis C virus. Journal of Virology, 82(7): 3555−3560. doi: 10.1128/JVI.01977-07
    Meinhardt J, Radke J, Dittmayer C, et al. 2021. Olfactory transmucosal SARS-CoV-2 invasion as a port of central nervous system entry in individuals with COVID-19. Nature Neuroscience, 24(2): 168−175. doi: 10.1038/s41593-020-00758-5
    Metcalf TU, Griffin DE. 2011. Alphavirus-induced encephalomyelitis: antibody-secreting cells and viral clearance from the nervous system. Journal of Virology, 85(21): 11490−11501. doi: 10.1128/JVI.05379-11
    Meyer KF, Haring CM, Howitt B. 1931. The etiology of epizootic encephalomyelitis of horses in the san joaquin valley, 1930. Science, 74(1913): 227−228.
    Mifune K, Shichijo A, Makino Y, et al. 1980. A mouse model for the pathogenesis and postexposure prophylaxis of rabies. Microbiology and Immunology, 24(9): 835−845. doi: 10.1111/j.1348-0421.1980.tb02888.x
    Miller KN, Victorelli SG, Salmonowicz H, et al. 2021. Cytoplasmic DNA: sources, sensing, and role in aging and disease. Cell, 184(22): 5506−5526. doi: 10.1016/j.cell.2021.09.034
    Mitchell MJ, Billingsley MM, Haley RM, et al. 2021. Engineering precision nanoparticles for drug delivery. Nature Reviews Drug Discovery, 20(2): 101−124. doi: 10.1038/s41573-020-0090-8
    Miura K, Goto N, Suzuki H, et al. 1988. Strain difference of mouse in susceptibility to Japanese encephalitis virus infection. Experimental Animals, 37(4): 365−373. doi: 10.1538/expanim1978.37.4_365
    Mockus TE, Ren HM, Shwetank, et al. 2019. To go or stay: the development, benefit, and detriment of tissue-resident memory CD8 T cells during central nervous system viral infections. Viruses, 11(9): 842. doi: 10.3390/v11090842
    Møllgård K, Beinlich FRM, Kusk P, et al. 2023. A mesothelium divides the subarachnoid space into functional compartments. Science, 379(6627): 84−88. doi: 10.1126/science.adc8810
    Mori I, Nishiyama Y, Yokochi T, et al. 2005. Olfactory transmission of neurotropic viruses. Journal of Neurovirology, 11(2): 129−137. doi: 10.1080/13550280590922793
    Mostashari F, Bunning ML, Kitsutani PT, et al. 2001. Epidemic West Nile encephalitis, New York, 1999: results of a household-based seroepidemiological survey. The Lancet, 358(9278): 261−264. doi: 10.1016/S0140-6736(01)05480-0
    Müller U, Steinhoff U, Reis LF, et al. 1994. Functional role of type I and type II interferons in antiviral defense. Science, 264(5167): 1918−1921. doi: 10.1126/science.8009221
    Munster VJ, Feldmann F, Williamson BN, et al. 2020. Respiratory disease in rhesus macaques inoculated with SARS-CoV-2. Nature, 585(7824): 268−272. doi: 10.1038/s41586-020-2324-7
    Munster VJ, Prescott JB, Bushmaker T, et al. 2012. Rapid Nipah virus entry into the central nervous system of hamsters via the olfactory route. Scientific Reports, 2: 736. doi: 10.1038/srep00736
    Mustafá YM, Meuren LM, Coelho SVA, et al. 2019. Pathways exploited by flaviviruses to counteract the blood-brain barrier and invade the central nervous system. Frontiers in Microbiology, 10: 525. doi: 10.3389/fmicb.2019.00525
    Nagel MA, Niemeyer CS, Bubak AN. 2020. Central nervous system infections produced by varicella zoster virus. Current Opinion in Infectious Diseases, 33(3): 273−278. doi: 10.1097/QCO.0000000000000647
    Narita M, Uchimura A, Kawanabe M, et al. 2001. Invasion and spread of equine herpesvirus 9 in the olfactory pathway of pigs after intranasal inoculation. Journal of Comparative Pathology, 124(4): 265−272. doi: 10.1053/jcpa.2000.0461
    Nemeth N, Bosco-Lauth A, Oesterle P, et al. 2012. North American birds as potential amplifying hosts of Japanese encephalitis virus. The American Journal of Tropical Medicine and Hygiene, 87(4): 760−767. doi: 10.4269/ajtmh.2012.12-0141
    Niu CX, Yu JJ, Zou T, et al. 2022. Identification of hematopoietic stem cells residing in the meninges of adult mice at steady state. Cell Reports, 41(6): 111592. doi: 10.1016/j.celrep.2022.111592
    Ohka S, Nihei CI, Yamazaki M, et al. 2012. Poliovirus trafficking toward central nervous system via human poliovirus receptor-dependent and -independent pathway. Frontiers in Microbiology, 3: 147.
    O'Neal JT, Upadhyay AA, Wolabaugh A, et al. 2019. West nile virus-inclusive single-cell RNA sequencing reveals heterogeneity in the type i interferon response within single cells. Journal of Virology, 93(6): e01778−18.
    Overall JC Jr. 1994. Herpes simplex virus infection of the fetus and newborn. Pediatric Annals, 23(3): 131−136. doi: 10.3928/0090-4481-19940301-06
    Papa MP, Meuren LM, Coelho SVA, et al. 2017. Zika virus infects, activates, and crosses brain microvascular endothelial cells, without barrier disruption. Frontiers in Microbiology, 8: 2557. doi: 10.3389/fmicb.2017.02557
    Parameswaran P, Sklan E, Wilkins C, et al. 2010. Six RNA viruses and forty-one hosts: viral small RNAs and modulation of small RNA repertoires in vertebrate and invertebrate systems. PLoS Pathogens, 6(2): e1000764. doi: 10.1371/journal.ppat.1000764
    Parra B, Hinton DR, Marten NW, et al. 1999. IFN-γ is required for viral clearance from central nervous system oligodendroglia. The Journal of Immunology, 162(3): 1641−1647. doi: 10.4049/jimmunol.162.3.1641
    Pfeffer S, Zavolan M, Grasser FA, et al. 2004. Identification of virus-encoded microRNAs. Science, 304(5671): 734−736. doi: 10.1126/science.1096781
    Phares TW, Marques CP, Stohlman SA, et al. 2011. Factors supporting intrathecal humoral responses following viral encephalomyelitis. Journal of Virology, 85(6): 2589−2598. doi: 10.1128/JVI.02260-10
    Pilotto A, Masciocchi S, Volonghi I, et al. 2021. Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) encephalitis is a cytokine release syndrome: evidences from cerebrospinal fluid analyses. Clinical Infectious Diseases, 73(9): e3019−e3026. doi: 10.1093/cid/ciaa1933
    Pompon J, Manuel M, Ng GK, et al. 2017. Dengue subgenomic flaviviral RNA disrupts immunity in mosquito salivary glands to increase virus transmission. PLoS Pathogens, 13(7): e1006535. doi: 10.1371/journal.ppat.1006535
    Puntambekar SS, Bergmann CC, Savarin C, et al. 2011. Shifting hierarchies of interleukin-10-producing T cell populations in the central nervous system during acute and persistent viral encephalomyelitis. Journal of Virology, 85(13): 6702−6713. doi: 10.1128/JVI.00200-11
    Racaniello VR. 2006. One hundred years of poliovirus pathogenesis. Virology, 344(1): 9−16. doi: 10.1016/j.virol.2005.09.015
    Ramakrishna C, Stohlman SA, Atkinson RA, et al. 2004. Differential regulation of primary and secondary CD8+ T cells in the central nervous system. The Journal of Immunology, 173(10): 6265−6273. doi: 10.4049/jimmunol.173.10.6265
    Ransohoff RM, Kivisäkk P, Kidd G. 2003. Three or more routes for leukocyte migration into the central nervous system. Nature Reviews Immunology, 3(7): 569−581. doi: 10.1038/nri1130
    Reagin KL, Funk KE. 2022. The role of antiviral CD8+ T cells in cognitive impairment. Current Opinion in Neurobiology, 76: 102603. doi: 10.1016/j.conb.2022.102603
    Rebejac J, Eme-Scolan E, Arnaud Paroutaud L, et al. 2022. Meningeal macrophages protect against viral neuroinfection. Immunity, 55(11): 2103−2117.e10. doi: 10.1016/j.immuni.2022.10.005
    Redant V, Favoreel HW, Dallmeier K, et al. 2020. Efficient control of Japanese encephalitis virus in the central nervous system of infected pigs occurs in the absence of a pronounced inflammatory immune response. Journal of Neuroinflammation, 17(1): 315. doi: 10.1186/s12974-020-01974-3
    Ren MS, Mei H, Zhou JJ, et al. 2021. Early diagnosis of rabies virus infection by RPA-CRISPR techniques in a rat model. Archives of Virology, 166(4): 1083−1092. doi: 10.1007/s00705-021-04970-x
    Ricklin ME, García-Nicolás O, Brechbühl D, et al. 2016. Vector-free transmission and persistence of Japanese encephalitis virus in pigs. Nature Communications, 7: 10832. doi: 10.1038/ncomms10832
    Roberts TK, Buckner CM, Berman JW. 2010. Leukocyte transmigration across the blood-brain barrier: perspectives on neuroAIDS. Frontiers in Bioscience, 15(2): 478−536.
    Roe K, Kumar M, Lum S, et al. 2012. West Nile virus-induced disruption of the blood-brain barrier in mice is characterized by the degradation of the junctional complex proteins and increase in multiple matrix metalloproteinases. Journal of General Virology, 93(6): 1193−1203. doi: 10.1099/vir.0.040899-0
    Rossi SL, Tesh RB, Azar SR, et al. 2016. Characterization of a Novel Murine Model to Study Zika Virus. The American Journal of Tropical Medicine and Hygiene, 94(6): 1362−1369. doi: 10.4269/ajtmh.16-0111
    Rua R, McGavern DB. 2018. Advances in meningeal immunity. Trends in Molecular Medicine, 24(6): 542−559. doi: 10.1016/j.molmed.2018.04.003
    Rubin SA, Pletnikov M, Carbone KM. 1998. Comparison of the neurovirulence of a vaccine and a wild-type mumps virus strain in the developing rat brain. Journal of Virology, 72(10): 8037−8042. doi: 10.1128/JVI.72.10.8037-8042.1998
    Sabin AB, Olitsky PK. 1937. Influence of host factors on neuroinvasiveness of vesicular stomatitis virus: II. Effect of age on the invasion of the peripheral and central nervous systems by virus injected into the leg muscles or the eye. Journal of Experimental Medicine, 66(1): 35−57. doi: 10.1084/jem.66.1.35
    Salimi H, Cain MD, Klein RS. 2016. Encephalitic arboviruses: emergence, clinical presentation, and neuropathogenesis. Neurotherapeutics, 13(3): 514−534. doi: 10.1007/s13311-016-0443-5
    Samuel MA, Wang H, Siddharthan V, et al. 2007. Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proceedings of the National Academy of Sciences of the United States of America, 104(43): 17140−17145. doi: 10.1073/pnas.0705837104
    Sasseville VG, Newman W, Brodie SJ, et al. 1994. Monocyte adhesion to endothelium in simian immunodeficiency virus-induced AIDS encephalitis is mediated by vascular cell adhesion molecule-1/α4β1 integrin interactions. American Journal of Pathology, 144(1): 27−40.
    Saxena V, Mathur A, Krishnani N, et al. 2008. Kinetics of cytokine profile during intraperitoneal inoculation of Japanese encephalitis virus in BALB/c mice model. Microbes and Infection, 10(10–11): 1210–1217.
    Seferovic M, Martín CSS, Tardif SD, et al. 2018. Experimental zika virus infection in the pregnant common marmoset induces spontaneous fetal loss and neurodevelopmental abnormalities. Scientific Reports, 8(1): 6851. doi: 10.1038/s41598-018-25205-1
    Sejvar JJ, Haddad MB, Tierney BC, et al. 2003. Neurologic manifestations and outcome of West Nile virus infection. JAMA, 290(4): 511−515. doi: 10.1001/jama.290.4.511
    Shan C, Yao YF, Yang XL, et al. 2020. Infection with novel coronavirus (SARS-CoV-2) causes pneumonia in Rhesus macaques. Cell Research, 30(8): 670–677.
    Shrestha B, Diamond MS. 2007. Fas ligand interactions contribute to CD8+ T-cell-mediated control of West Nile virus infection in the central nervous system. Journal of Virology, 81(21): 11749−11757. doi: 10.1128/JVI.01136-07
    Shrestha B, Pinto AK, Green S, et al. 2012. CD8+ T cells use TRAIL to restrict West Nile virus pathogenesis by controlling infection in neurons. Journal of Virology, 86(17): 8937−8948. doi: 10.1128/JVI.00673-12
    Shrestha B, Zhang B, Purtha WE, et al. 2008. Tumor necrosis factor alpha protects against lethal West Nile virus infection by promoting trafficking of mononuclear leukocytes into the central nervous system. Journal of Virology, 82(18): 8956−8964. doi: 10.1128/JVI.01118-08
    Silva MC, Guerrero-Plata A, Gilfoy FD, et al. 2007. Differential activation of human monocyte-derived and plasmacytoid dendritic cells by West Nile virus generated in different host cells. Journal of Virology, 81(24): 13640−13648. doi: 10.1128/JVI.00857-07
    Silva MTT. 2013. Viral encephalitis. Arquivos de Neuro-Psiquiatria, 71(9B): 703−709. doi: 10.1590/0004-282X20130155
    Sips GJ, Wilschut J, Smit JM. 2012. Neuroinvasive flavivirus infections. Reviews in Medical Virology, 22(2): 69−87. doi: 10.1002/rmv.712
    Smith JS. 1981. Mouse model for abortive rabies infection of the central nervous system. Infection and Immunity, 31(1): 297−308. doi: 10.1128/iai.31.1.297-308.1981
    Solomon T, Lewthwaite P, Perera D, et al. 2010. Virology, epidemiology, pathogenesis, and control of enterovirus 71. The Lancet Infectious Diseases, 10(11): 778−790. doi: 10.1016/S1473-3099(10)70194-8
    Song E, Mao TY, Dong HP, et al. 2020. VEGF-C-driven lymphatic drainage enables immunosurveillance of brain tumours. Nature, 577(7792): 689−694. doi: 10.1038/s41586-019-1912-x
    Sooryanarain H, Ayachit V, Gore M. 2012. Activated CD56+ lymphocytes (NK+NKT) mediate immunomodulatory and anti-viral effects during Japanese encephalitis virus infection of dendritic cells in-vitro. Virology, 432(2): 250–260.
    Spudich S, Nath A. 2022. Nervous system consequences of COVID-19. Science, 375(6578): 267−269. doi: 10.1126/science.abm2052
    Steinbach K, Vincenti I, Kreutzfeldt M, et al. 2016. Brain-resident memory T cells represent an autonomous cytotoxic barrier to viral infection. Journal of Experimental Medicine, 213(8): 1571−1587. doi: 10.1084/jem.20151916
    Stiles LN, Hosking MP, Edwards RA, et al. 2006. Differential roles for CXCR3 in CD4+ and CD8+ T cell trafficking following viral infection of the CNS. European Journal of Immunology, 36(3): 613−622. doi: 10.1002/eji.200535509
    Sumathy K, Kulkarni B, Gondu RK, et al. 2017. Protective efficacy of Zika vaccine in AG129 mouse model. Scientific Reports, 7: 46375. doi: 10.1038/srep46375
    Sun SH, Chen Q, Gu HJ, et al. 2020. A mouse model of SARS-CoV-2 infection and pathogenesis. Cell Host & Microbe, 28(1): 124−133.e4.
    Süss J, Gelpi E, Klaus C, et al. 2007. Tickborne encephalitis in naturally exposed monkey (Macaca sylvanus). Emerging Infectious Diseases, 13(6): 905−907. doi: 10.3201/eid1306.061173
    Suthar MS, Diamond MS, Gale M Jr. 2013. West Nile virus infection and immunity. Nature Reviews Microbiology, 11(2): 115−128. doi: 10.1038/nrmicro2950
    Takahashi M, Yamada T, Nakajima S, et al. 1995. The substantia nigra is a major target for neurovirulent influenza A virus. Journal of Experimental Medicine, 181(6): 2161−2169. doi: 10.1084/jem.181.6.2161
    Tan SH, Ong KC, Wong KT. 2014. Enterovirus 71 can directly infect the brainstem via cranial nerves and infection can be ameliorated by passive immunization. Journal of Neuropathology & Experimental Neurology, 73(11): 999−1008.
    Tarantal AF, Salamat MS, Britt WJ, et al. 1998. Neuropathogenesis induced by rhesus cytomegalovirus in fetal rhesus monkeys (Macaca mulatta). The Journal of Infectious Diseases, 177(2): 446−450. doi: 10.1086/514206
    Templeton SP, Kim TS, O'Malley K, et al. 2008. Maturation and localization of macrophages and microglia during infection with a neurotropic murine coronavirus. Brain Pathology, 18(1): 40−51. doi: 10.1111/j.1750-3639.2007.00098.x
    Throsby M, Geuijen C, Goudsmit J, et al. 2006. Isolation and characterization of human monoclonal antibodies from individuals infected with West Nile Virus. Journal of Virology, 80(14): 6982−6992. doi: 10.1128/JVI.00551-06
    Trifilo MJ, Lane TE. 2004. The CC chemokine ligand 3 regulates CD11c+CD11b+CD8α- dendritic cell maturation and activation following viral infection of the central nervous system: implications for a role in T cell activation. Virology, 327(1): 8−15. doi: 10.1016/j.virol.2004.06.027
    Trivedi S, Chakravarty A. 2022. Neurological complications of dengue fever. Current Neurology and Neuroscience Reports, 22(8): 515−529. doi: 10.1007/s11910-022-01213-7
    Tselis AC. 2014. Epstein-Barr virus infections of the nervous system. Handbook of Clinical Neurology, 123: 285−305.
    Tuite MF, Serio TR. 2010. The prion hypothesis: from biological anomaly to basic regulatory mechanism. Nature Reviews Molecular Cell Biology, 11(12): 823−833. doi: 10.1038/nrm3007
    Turell MJ, Sardelis MR, Dohm DJ, et al. 2001. Potential North American vectors of West Nile virus. Annals of the New York Academy of Sciences, 951(1): 317−324.
    Turtle L, Bali T, Buxton G, et al. 2016. Human T cell responses to Japanese encephalitis virus in health and disease. Journal of Experimental Medicine, 213(7): 1331−1352. doi: 10.1084/jem.20151517
    Ugolini G. 2011. Rabies virus as a transneuronal tracer of neuronal connections. Advances in Virus Research, 79: 165−202.
    Uyar O, Dominguez JM, Bordeleau M, et al. 2022. Single-cell transcriptomics of the ventral posterolateral nucleus-enriched thalamic regions from HSV-1-infected mice reveal a novel microglia/microglia-like transcriptional response. Journal of Neuroinflammation, 19(1): 81. doi: 10.1186/s12974-022-02437-7
    van den Pol AN, Mocarski E, Saederup N, et al. 1999. Cytomegalovirus cell tropism, replication, and gene transfer in brain. Journal of Neuroscience, 19(24): 10948−10965. doi: 10.1523/JNEUROSCI.19-24-10948.1999
    van Riel D, Verdijk R, Kuiken T. 2015. The olfactory nerve: a shortcut for influenza and other viral diseases into the central nervous system. The Journal of Pathology, 235(2): 277−287. doi: 10.1002/path.4461
    Venkatesan A, Tunkel AR, Bloch KC, et al. 2013. Case definitions, diagnostic algorithms, and priorities in encephalitis: consensus statement of the international encephalitis consortium. Clinical Infectious Diseases, 57(8): 1114−1128. doi: 10.1093/cid/cit458
    Verboon-Maciolek MA, Groenendaal F, Hahn CD, et al. 2008. Human parechovirus causes encephalitis with white matter injury in neonates. Annals of Neurology, 64(3): 266−273. doi: 10.1002/ana.21445
    Verma R, Sharma P, Garg RK, et al. 2011. Neurological complications of dengue fever: experience from a tertiary center of north India. Annals of Indian Academy of Neurology, 14(4): 272−278. doi: 10.4103/0972-2327.91946
    Verstrepen BE, Fagrouch Z, van Heteren M, et al. 2014. Experimental infection of rhesus macaques and common marmosets with a European strain of West Nile virus. PLoS Neglected Tropical Diseases, 8(4): e2797. doi: 10.1371/journal.pntd.0002797
    Walsh KB, Edwards RA, Romero KM, et al. 2007. Expression of CXC chemokine ligand 10 from the mouse hepatitis virus genome results in protection from viral-induced neurological and liver disease. The Journal of Immunology, 179(2): 1155−1165. doi: 10.4049/jimmunol.179.2.1155
    Wang ML, Cao RY, Zhang LK, et al. 2020. Remdesivir and chloroquine effectively inhibit the recently emerged novel coronavirus (2019-nCoV) in vitro. Cell Research, 30(3): 269−271. doi: 10.1038/s41422-020-0282-0
    Wang Y, Chen DY, Xu D, et al. 2021. Early developing B cells undergo negative selection by central nervous system-specific antigens in the meninges. Immunity, 54(12): 2784−2794.e6. doi: 10.1016/j.immuni.2021.09.016
    Watson JT, Pertel PE, Jones RC, et al. 2004. Clinical characteristics and functional outcomes of West Nile Fever. Annals of Internal Medicine, 141(5): 360−365. doi: 10.7326/0003-4819-141-5-200409070-00010
    Weinger JG, Marro BS, Hosking MP, et al. 2013. The chemokine receptor CXCR2 and coronavirus-induced neurologic disease. Virology, 435(1): 110−117. doi: 10.1016/j.virol.2012.08.049
    White MK, Wollebo HS, David Beckham J, et al. 2016. Zika virus: an emergent neuropathological agent. Annals of Neurology, 80(4): 479−489. doi: 10.1002/ana.24748
    Whitley RJ. 2015. Herpes simplex virus infections of the central nervous system. Continuum (Minneap Minn), 21(6): 1704–1713.
    Wilkins C, Gale M Jr. 2010. Recognition of viruses by cytoplasmic sensors. Current Opinion in Immunology, 22(1): 41−47. doi: 10.1016/j.coi.2009.12.003
    Winkler ES, Bailey AL, Kafai NM, et al. 2020. SARS-CoV-2 infection of human ACE2-transgenic mice causes severe lung inflammation and impaired function. Nature Immunology, 21(11): 1327−1335. doi: 10.1038/s41590-020-0778-2
    Wong P, Pamer EG. 2003. CD8 T cell responses to infectious pathogens. Annual Review of Immunology, 21: 29−70. doi: 10.1146/annurev.immunol.21.120601.141114
    Wong PSJ, Li MZI, Chong CS, et al. 2013. Aedes (Stegomyia) albopictus (Skuse): a potential vector of Zika virus in Singapore. PLoS Neglected Tropical Diseases, 7(8): e2348. doi: 10.1371/journal.pntd.0002348
    Wu SJL, Grouard-Vogel G, Sun W, et al. 2000. Human skin Langerhans cells are targets of dengue virus infection. Nature Medicine, 6(7): 816−820. doi: 10.1038/77553
    Xiao CG, Wang X, Cui GH, et al. 2018. Possible pathogenicity of Japanese encephalitis virus in newly hatched domestic ducklings. Veterinary Microbiology, 227: 8−11. doi: 10.1016/j.vetmic.2018.10.016
    Xiao SY, Guzman H, Zhang H, et al. 2001. West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis. Emerging Infectious Diseases, 7(4): 714−721. doi: 10.3201/eid0704.017420
    Xie XP, Wang QY, Xu HY, et al. 2011. Inhibition of dengue virus by targeting viral NS4B protein. Journal of Virology, 85(21): 11183−11195. doi: 10.1128/JVI.05468-11
    Xu L, Yu DD, Ma YH, et al. 2020. COVID-19-like symptoms observed in Chinese tree shrews infected with SARS-CoV-2. Zoological Research, 41(5): 517−526. doi: 10.24272/j.issn.2095-8137.2020.053
    Xu RF, Feng XY, Xie X, et al. 2012a. HIV-1 Tat protein increases the permeability of brain endothelial cells by both inhibiting occludin expression and cleaving occludin via matrix metalloproteinase-9. Brain Research, 1436: 13−19. doi: 10.1016/j.brainres.2011.11.052
    Xu ZK, Waeckerlin R, Urbanowski MD, et al. 2012b. West nile virus infection causes endocytosis of a specific subset of tight junction membrane proteins. PLoS One, 7(5): e37886. doi: 10.1371/journal.pone.0037886
    Yan Q, Zheng WJ, Jiang Y, et al. 2023. Transcriptomic reveals the ferroptosis features of host response in a mouse model of Zika virus infection. Journal of Medical Virology, 95(1): e28386.
    Yang ZF, Zhao J, Zhu YT, et al. 2013. The tree shrew provides a useful alternative model for the study of influenza H1N1 virus. Virology Journal, 10: 111. doi: 10.1186/1743-422X-10-111
    Yao YG. 2017. Creating animal models, why not use the Chinese tree shrew (Tupaia belangeri chinensis)?. Zoological Research, 38(3): 118−126. doi: 10.24272/j.issn.2095-8137.2017.032
    Yshii L, Gebauer C, Bernard-Valnet R, et al. 2015. Neurons and T cells: understanding this interaction for inflammatory neurological diseases. European Journal of Immunology, 45(10): 2712−2720. doi: 10.1002/eji.201545759
    Yu JH, Liu XL, Ke CW, et al. 2017. Effective suckling C57BL/6, kunming, and BALB/c mouse models with remarkable neurological manifestation for Zika virus infection. Viruses, 9(7): 165. doi: 10.3390/v9070165
    Zhang F, Qi LL, Li T, et al. 2019a. PD1+CCR2+CD8+ T cells infiltrate the central nervous system during acute japanese encephalitis virus infection. Virologica Sinica, 34(5): 538−548. doi: 10.1007/s12250-019-00134-z
    Zhang NN, Zhang L, Deng YQ, et al. 2019b. Zika virus infection in tupaia belangeri causes dermatological manifestations and confers protection against secondary infection. Journal of Virology, 93(8): e01982−18.
    Zhang RY, Sun C, Chen XM, et al. 2022a. COVID-19-related brain injury: the potential role of ferroptosis. Journal of Inflammation Research, 15: 2181−2198. doi: 10.2147/JIR.S353467
    Zhang Y, Zhang SF, Li LT, et al. 2016. Ineffectiveness of rabies vaccination alone for post-exposure protection against rabies infection in animal models. Antiviral Research, 135: 56−61. doi: 10.1016/j.antiviral.2016.10.002
    Zhang YY, Bailey JT, Xu E, et al. 2022b. Mucosal-associated invariant T cells restrict reactive oxidative damage and preserve meningeal barrier integrity and cognitive function. Nature Immunology, 23(12): 1714−1725. doi: 10.1038/s41590-022-01349-1
    Zuo J, Stohlman SA, Hoskin JB, et al. 2006. Mouse hepatitis virus pathogenesis in the central nervous system is independent of IL-15 and natural killer cells. Virology, 350(1): 206−215. doi: 10.1016/j.virol.2006.01.027
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Figures(2)  / Tables(3)

    Article Metrics

    Article views (617) PDF downloads(114) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint