Japanese encephalitis virus-induced DNA methylation contributes to blood-brain barrier permeability by modulating tight junction protein expression.


Journal

Journal of neuroinflammation
ISSN: 1742-2094
Titre abrégé: J Neuroinflammation
Pays: England
ID NLM: 101222974

Informations de publication

Date de publication:
28 Oct 2024
Historique:
received: 21 04 2024
accepted: 18 10 2024
medline: 29 10 2024
pubmed: 29 10 2024
entrez: 29 10 2024
Statut: epublish

Résumé

Japanese encephalitis virus (JEV) is a neurotropic and neuroinvasive flavivirus causing viral encephalitis, which seriously threatens the development of animal husbandry and human health. DNA methylation is a major epigenetic modification involved in viral pathogenesis, yet how DNA methylation affects JEV infection remains unknown. Here, we show genome-wide DNA methylation profiles in the brains of JEV-infected mice compared to mock-infected mice. JEV can significantly increase the overall DNA methylation levels in JEV-infected mouse brains. A total of 14,781 differentially methylated regions associated genes (DMGs) have been identified. Subsequently, KEGG pathway analysis suggested that DNA methylation modulates the tight junction signaling pathway, which can potentially impact the permeability of the blood-brain barrier (BBB). We demonstrate that hypermethylation of the tight junction gene Afdn promoter inhibited AFDN expression and increased monolayer permeability of mouse brain microvascular endothelial (bEnd.3) cells in an in vitro transwell assay. Collectively, this study reveals that DNA methylation is increased in a murine Japanese encephalitis model and that modulation of Afdn expression promotes BBB permeability.

Identifiants

pubmed: 39468601
doi: 10.1186/s12974-024-03266-6
pii: 10.1186/s12974-024-03266-6
doi:

Substances chimiques

Tight Junction Proteins 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

277

Subventions

Organisme : the China Scholarship Council
ID : 202203250067
Organisme : the National Key Research and Development Program of China
ID : 2022YFD1800100

Informations de copyright

© 2024. The Author(s).

Références

Sharma KB, Vrati S, Kalia M. Pathobiology of Japanese encephalitis virus infection. Mol Aspects Med. 2021;81:100994.
pubmed: 34274157 doi: 10.1016/j.mam.2021.100994
Kumar S, Verma A, Yadav P, Dubey SK, Azhar EI, Maitra SS, Dwivedi VD. Molecular pathogenesis of Japanese encephalitis and possible therapeutic strategies. Arch Virol. 2022;167:1739–62.
pubmed: 35654913 pmcid: 9162114 doi: 10.1007/s00705-022-05481-z
Ghosh D, Basu A. Japanese encephalitis-a pathological and clinical perspective. PLoS Negl Trop Dis. 2009;3:e437.
pubmed: 19787040 pmcid: 2745699 doi: 10.1371/journal.pntd.0000437
Li-Ta Keng L-YC. Japanese encephalitis. Clin IMAGES. 2018;190(21):E657.
Davis EH, Beck AS, Li L, White MM, Greenberg MB, Thompson JK, Widen SG, Barrett ADT, Bourne N. Japanese encephalitis virus live attenuated vaccine strains display altered immunogenicity, virulence and genetic diversity. NPJ Vaccines. 2021;6:112.
pubmed: 34475404 pmcid: 8413339 doi: 10.1038/s41541-021-00371-y
Lee S-IYY-M. Japanese encephalitis:the virus and vaccines. Hum Vaccines Immunotherapeutics. 2014;10(2):263–79.
doi: 10.4161/hv.26902
Mileno MD. Japanese Encephalitis Vaccine. R I Med J (2013) 2020, 103:49–50.
Chen HL, Chang JK, Tang RB. Current recommendations for the Japanese encephalitis vaccine. J Chin Med Assoc. 2015;78:271–5.
pubmed: 25841620 doi: 10.1016/j.jcma.2014.12.009
Sakamoto R, Tanimoto T, Takahashi K, Hamaki T, Kusumi E, Crump A. Flourishing Japanese Encephalitis, Associated with global warming and urbanisation in Asia, demands widespread Integrated Vaccination Programmes. Annals Global Health 2019, 85.
Hameed M, Wahaab A, Nawaz M, Khan S, Nazir J, Liu K, Wei JC, Ma ZY. Potential Role of Birds in Japanese Encephalitis Virus Zoonotic Transmission and Genotype Shift. Viruses-Basel 2021, 13.
Mackenzie JS, Williams DT, van den Hurk AF, Smith DW, Currie BJ. Japanese Encephalitis Virus: the emergence of genotype IV in Australia and its potential endemicity. Viruses 2022, 14.
Guanlun Xu TG, Zhijie Wang J, Zhang B, Cui X, Shen A, Zhou Y, Zhang J, Zhao. Hong Liu: Re-Emerged Genotype IV of Japanese Encephalitis Virus Is the Youngest Virus in Evolution viruses 2023, 15(3):626.
Frank JC, Song BH, Lee YM. Mice as an animal model for Japanese Encephalitis Virus Research: mouse susceptibility, infection Route, and Viral Pathogenesis. Pathogens 2023, 12.
Kumar A, Sharma P, Shukla KK, Misra S, Nyati KK. Japanese encephalitis virus: Associated immune response and recent progress in vaccine development. Microb Pathog 2019, 136.
Filgueira L, Lannes N. Review of emerging Japanese Encephalitis Virus: New aspects and concepts about Entry into the brain and inter-cellular spreading. Pathogens; 2019. p. 8.
Turtle L, Solomon T. Japanese encephalitis - the prospects for new treatments. Nat Reviews Neurol. 2018;14:298–313.
doi: 10.1038/nrneurol.2018.30
Moore LD, Le T, Fan GP. DNA methylation and its basic function. Neuropsychopharmacology. 2013;38:23–38.
pubmed: 22781841 doi: 10.1038/npp.2012.112
Cui D, Xu XR. DNA methyltransferases, DNA methylation, and Age-Associated cognitive function. Int J Mol Sci 2018, 19.
Liu S, Liu L, Xu G, Cao ZY, Wang Q, Li S, Peng NF, Yin JC, Yu HS, Li MQ et al. Epigenetic modification is regulated by the Interaction of Influenza A Virus Nonstructural protein 1 with the De Novo DNA methyltransferase DNMT3B and subsequent transport to the cytoplasm for K48-Linked polyubiquitination. J Virol 2019, 93.
Tirado-Magallanes R, Rebbani K, Lim R, Pradhan S, Benoukraf T. Whole genome DNA methylation: beyond genes silencing. Oncotarget. 2017;8:5629–37.
pubmed: 27895318 doi: 10.18632/oncotarget.13562
Mase S, Shinjo K, Totani H, Katsushima K, Arakawa A, Takahashi S, Lai HC, Lin RI, Chan MWY, Sugiura-Ogasawara M, Kondo Y. ZNF671 DNA methylation as a molecular predictor for the early recurrence of serous ovarian cancer. Cancer Sci. 2019;110:1105–16.
pubmed: 30633424 pmcid: 6398878 doi: 10.1111/cas.13936
Blanch M, Mosquera JL, Ansoleaga B, Ferrer I, Barrachina M. Altered mitochondrial DNA methylation pattern in Alzheimer Disease-Related Pathology and in Parkinson Disease. Am J Pathol. 2016;186:385–97.
pubmed: 26776077 doi: 10.1016/j.ajpath.2015.10.004
Zouali M. DNA methylation signatures of autoimmune diseases in human B lymphocytes. Clin Immunol. 2021;222:108622.
pubmed: 33188932 doi: 10.1016/j.clim.2020.108622
De Jager PL, Srivastava G, Lunnon K, Burgess J, Schalkwyk LC, Yu L, Eaton ML, Keenan BT, Ernst J, McCabe C, et al. Alzheimer’s disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci. 2014;17:1156–63.
pubmed: 25129075 pmcid: 4292795 doi: 10.1038/nn.3786
Bennett DA, Yu L, Yang J, Srivastava GP, Aubin C, De Jager PL. Epigenomics of Alzheimer’s disease. Transl Res. 2015;165:200–20.
pubmed: 24905038 doi: 10.1016/j.trsl.2014.05.006
Fang J, Hao Q, Liu L, Li Y, Wu J, Huo X, Zhu Y. Epigenetic changes mediated by microRNA miR29 activate cyclooxygenase 2 and lambda-1 interferon production during viral infection. J Virol. 2012;86:1010–20.
pubmed: 22072783 pmcid: 3255816 doi: 10.1128/JVI.06169-11
Anderson D, Neri JICF, Souza CRM, Valverde JG, De Araujo JMG, Nascimento MDSB, Branco RCC, Arrais NMR, Lassmann T, Blackwell JM, Jeronimo SMB. Zika Virus Changes methylation of genes involved in Immune response and neural development in Brazilian babies born with congenital Microcephaly. J Infect Dis. 2021;223:435–40.
pubmed: 32614431 doi: 10.1093/infdis/jiaa383
Kandilya D, Maskomani S, Shyamasundar S, Tambyah PA, Shiao Yng C, Lee RCH, Hande MP, Mallilankaraman K, Chu JJH, Dheen ST. Zika virus alters DNA methylation status of genes involved in Hippo signaling pathway in human neural progenitor cells. Epigenomics. 2019;11:1143–61.
pubmed: 31234652 doi: 10.2217/epi-2018-0180
Janssens S, Schotsaert M, Karnik R, Balasubramaniam V, Dejosez M, Meissner A, Garcia-Sastre A, Zwaka TP. Zika Virus Alters DNA Methylation of Neural Genes in an Organoid Model of the Developing Human Brain. mSystems 2018, 3.
Gomes AV, de Souza Morais SM, Menezes-Filho SL, de Almeida LG, Rocha RP, Ferreira JM, Dos Santos LL, Malaquias LC, Coelho LF. Demethylation profile of the TNF-alpha promoter gene is associated with high expression of this cytokine in Dengue virus patients. J Med Virol. 2016;88:1297–302.
pubmed: 26792115 doi: 10.1002/jmv.24478
Reed LJ. A simple method of estimating fifty per cent endpoints. Cabidigitallibraryorg. 1938;27:493–7.
Sehgal N, Kumawat KL, Basu A, Ravindranath V. Fenofibrate reduces mortality and precludes neurological deficits in survivors in murine model of Japanese encephalitis viral infection. PLoS ONE. 2012;7:e35427.
pubmed: 22514742 pmcid: 3325984 doi: 10.1371/journal.pone.0035427
Ryan Lister MP, Robert H, Dowen RD, Hawkins G, Hon J, Tonti-Filippini JR, Nery L, Lee Z, Ye Q-M, Ngo. Lee Edsall, Jessica Antosiewicz-Bourget, Ron Stewart, Victor Ruotti, a Harvey Millar, James A Thomson, Bing Ren, Joseph R Ecke: human DNA methylomes at base resolution show widespread epigenomic differences. Nature. 2009;462(7271):315–22.
pubmed: 19829295 pmcid: 2857523 doi: 10.1038/nature08514
Wang K, Wang HL, Lou WJ, Ma LH, Li YC, Zhang N, Wang C, Li F, Awais M, Cao SB et al. IP-10 promotes blood-brain barrier damage by Inducing Tumor Necrosis Factor Alpha Production in Japanese encephalitis. Front Immunol 2018, 9.
Tu Y, Fang P, Zhang L, Sun K. Analysis of the Effect of SNAI Family in breast Cancer and Immune Cell. Front Cell Dev Biol. 2022;10:906885.
pubmed: 35898399 pmcid: 9309217 doi: 10.3389/fcell.2022.906885
Tanabe Y, Naito Y, Vasuta C, Lee AK, Soumounou Y, Linhoff MW, Takahashi H. IgSF21 promotes differentiation of inhibitory synapses via binding to neurexin2alpha. Nat Commun. 2017;8:408.
pubmed: 28864826 pmcid: 5581337 doi: 10.1038/s41467-017-00333-w
Juchem KW, Gounder AP, Gao JP, Seccareccia E, Yeddula N, Huffmaster NJ, Cote-Martin A, Fogal SE, Souza D, Wang SS, et al. NFAM1 promotes pro-inflammatory cytokine production in mouse and human monocytes. Front Immunol. 2021;12:773445.
pubmed: 35095847 doi: 10.3389/fimmu.2021.773445
Nakao M, Miyagaki T, Sugaya M, Sato S. Exacerbated Imiquimod-Induced Psoriasis-Like skin inflammation in IRF5-Deficient mice. Int J Mol Sci 2020, 21.
Harada H, Fujita T, Miyamoto M, Kimura Y, Maruyama M, Furia A, Miyata T, Taniguchi T. Structurally similar but functionally distinct factors, IRF-1 and IRF-2, bind to the same regulatory elements of IFN and IFN-inducible genes. Cell. 1989;58:729–39.
pubmed: 2475256 doi: 10.1016/0092-8674(89)90107-4
Zhang XJ, Jiang DS, Li H. The interferon regulatory factors as novel potential targets in the treatment of cardiovascular diseases. Br J Pharmacol. 2015;172:5457–76.
pubmed: 25131895 pmcid: 4667854 doi: 10.1111/bph.12881
Kamath AV, Yip V, Gupta P, Boswell CA, Bumbaca D, Haughney P, Castro J, Tsai SP, Pacheco G, Ross S, et al. Dose dependent pharmacokinetics, tissue distribution, and anti-tumor efficacy of a humanized monoclonal antibody against DLL4 in mice. MAbs. 2014;6:1631–7.
pubmed: 25484068 pmcid: 4622559 doi: 10.4161/mabs.36107
Al-Obaidi MMJ, Bahadoran A, Wang SM, Manikam R, Raju CHS, Sekaran SD. Disruption of the blood brain barrier is vital property of neurotropic viral infection of the central nervous system. Acta Virol. 2018;62:16–27.
pubmed: 29521099 doi: 10.4149/av_2018_102
Chai Q, He WQ, Zhou M, Lu H, Fu ZF. Enhancement of blood-brain barrier permeability and reduction of tight junction protein expression are modulated by chemokines/cytokines induced by Rabies virus infection. J Virol. 2014;88:4698–710.
pubmed: 24522913 pmcid: 3993813 doi: 10.1128/JVI.03149-13
Ohtani H, Orskov AD, Helbo AS, Gillberg L, Liu M, Zhou W, Ungerstedt J, Hellstrom-Lindberg E, Sun W, Liang G, et al. Activation of a subset of evolutionarily young transposable elements and innate immunity are linked to clinical responses to 5-Azacytidine. Cancer Res. 2020;80:2441–50.
pubmed: 32245794 pmcid: 7507765 doi: 10.1158/0008-5472.CAN-19-1696
Choi JY, Kim JH, Hossain FMA, Uyangaa E, Park SO, Kim B, Kim K, Eo SK. Indispensable role of CX(3)CR1(+) dendritic cells in regulation of Virus-Induced Neuroinflammation through Rapid Development of Antiviral Immunity in Peripheral lymphoid tissues. Front Immunol. 2019;10:1467.
pubmed: 31316515 pmcid: 6610490 doi: 10.3389/fimmu.2019.01467
Hsieh JT, St John AL. Japanese encephalitis virus and its mechanisms of neuroinvasion. PLoS Pathog. 2020;16:e1008260.
pubmed: 32240272 pmcid: 7117652 doi: 10.1371/journal.ppat.1008260
Castro-Jorge LA, Pretto CD, Smith AB, Foreman O, Carnahan KE, Spindler KR. A protective role for Interleukin-1 signaling during mouse adenovirus type 1-Induced Encephalitis. J Virol 2017, 91.
Yan Z, Liu YM, Wu WD, Jiang Y, Zhuo LB. Combined exposure of heat stress and ozone enhanced cognitive impairment via neuroinflammation and blood brain barrier disruption in male rats. Sci Total Environ. 2023;857:159599.
pubmed: 36280063 doi: 10.1016/j.scitotenv.2022.159599
Feng SR, Chen ZX, Cen JN, Shen HJ, Wang YY, Yao L. [Critical roles of matrix metalloproteinases secreted by leukemic cells in the pathogenesis of central nervous system leukemia]. Zhonghua Xue Ye Xue Za Zhi. 2016;37:1070–6.
pubmed: 28088972
Huxham J, Tabaries S, Siegel PM. Afadin (AF6) in cancer progression: a multidomain scaffold protein with complex and contradictory roles. BioEssays. 2021;43:e2000221.
pubmed: 33165933 doi: 10.1002/bies.202000221
Yamamoto T, Harada N, Kano K, Taya S, Canaani E, Matsuura Y, Mizoguchi A, Ide C, Kaibuchi K. The ras target AF-6 interacts with ZO-1 and serves as a peripheral component of tight junctions in epithelial cells. J Cell Biol. 1997;139:785–95.
pubmed: 9348294 pmcid: 2141704 doi: 10.1083/jcb.139.3.785
Ooshio T, Kobayash R, Iked W, Miyata M, Fukumoto Y, Matsuzawa N, Ogita H. Involvement of the Interaction of Afadin with ZO-1 in the formation of TJ in MDCK cell. J BIOL CHEM. 2020;285:5003–12.
doi: 10.1074/jbc.M109.043760
Tanaka-Okamoto M, Hori K, Ishizaki H, Itoh Y, Onishi S, Yonemura S, Takai Y, Miyoshi J. Involvement of afadin in barrier function and homeostasis of mouse intestinal epithelia. J Cell Sci. 2011;124:2231–40.
pubmed: 21652626 pmcid: 3115770 doi: 10.1242/jcs.081000
Liu L, Yang C, Lavayen BP, Tishko RJ, Larochelle J, Candelario-Jalil E. Targeted BRD4 protein degradation by dBET1 ameliorates acute ischemic brain injury and improves functional outcomes associated with reduced neuroinflammation and oxidative stress and preservation of blood-brain barrier integrity. J Neuroinflammation. 2022;19:168.
pubmed: 35761277 pmcid: 9237998 doi: 10.1186/s12974-022-02533-8
Yao Y, Chen ZL, Norris EH, Strickland S. Astrocytic laminin regulates pericyte differentiation and maintains blood brain barrier integrity. Nat Commun. 2014;5:3413.
pubmed: 24583950 doi: 10.1038/ncomms4413
Behera J, Kelly KE, Tyagi N. Hydrogen sulfide prevents ethanol-induced ZO-1 CpG promoter hypermethylation-dependent vascular permeability via miR-218/DNMT3a axis. J Cell Physiol. 2021;236:6852–67.
pubmed: 33855696 doi: 10.1002/jcp.30382
Ihezie SA, Mathew IE, McBride DW, Dienel A, Blackburn SL. Thankamani pandit PK: epigenetics in blood-brain barrier disruption. Fluids Barriers CNS. 2021;18:17.
pubmed: 33823899 pmcid: 8025355 doi: 10.1186/s12987-021-00250-7
Ge Y, Zadeh M, Mohamadzadeh M. Vitamin B12 regulates the transcriptional, metabolic, and Epigenetic Programing in Human Ileal epithelial cells. Nutrients 2022, 14.
Xu XF, Hu QY, Liang LF, Wu L, Gu WZ, Tang LL, Fu LC, Du LZ. Epigenetics of hyper-responsiveness to allergen challenge following intrauterine growth retardation rat. Respir Res. 2014;15:137.
pubmed: 25391516 pmcid: 4233040 doi: 10.1186/s12931-014-0137-7
Smith J, Sen S, Weeks RJ, Eccles MR, Chatterjee A. Promoter DNA hypermethylation and paradoxical gene activation. Trends Cancer. 2020;6:392–406.
pubmed: 32348735 doi: 10.1016/j.trecan.2020.02.007
de Mendoza A, Nguyen TV, Ford E, Poppe D, Buckberry S, Pflueger J, Grimmer MR, Stolzenburg S, Bogdanovic O, Oshlack A, et al. Large-scale manipulation of promoter DNA methylation reveals context-specific transcriptional responses and stability. Genome Biol. 2022;23:163.
pubmed: 35883107 pmcid: 9316731 doi: 10.1186/s13059-022-02728-5
Lin Y, Wozniak JM, Grimsey NJ, Girada S, Patwardhan A, Molinar-Inglis O, Smith TH, Lapek JD, Gonzalez DJ, Trejo J. Phosphoproteomic analysis of protease-activated receptor-1 biased signaling reveals unique modulators of endothelial barrier function. Proc Natl Acad Sci U S A. 2020;117:5039–48.
pubmed: 32071217 pmcid: 7060683 doi: 10.1073/pnas.1917295117
Faralla C, Bastounis EE, Ortega FE, Light SH, Rizzuto G, Gao L, Marciano DK, Nocadello S, Anderson WF, Robbins JR, et al. Listeria monocytogenes InlP interacts with afadin and facilitates basement membrane crossing. PLoS Pathog. 2018;14:e1007094.
pubmed: 29847585 pmcid: 6044554 doi: 10.1371/journal.ppat.1007094
Kim KA, Kim D, Kim JH, Shin YJ, Kim ES, Akram M, Kim EH, Majid A, Baek SH, Bae ON. Autophagy-mediated occludin degradation contributes to blood-brain barrier disruption during ischemia in bEnd.3 brain endothelial cells and rat ischemic stroke models. Fluids Barriers CNS. 2020;17:21.
pubmed: 32169114 pmcid: 7071658 doi: 10.1186/s12987-020-00182-8
Hao W, Cui Y, Fan Y, Chen M, Yang G, Wang Y, Yang M, Li Z, Gong W, Yang Y, Gao C. Hybrid membrane-coated nanosuspensions for multi-modal anti-glioma therapy via drug and antigen delivery. J Nanobiotechnol. 2021;19:378.
doi: 10.1186/s12951-021-01110-0

Auteurs

Xiao Xiang (X)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.
Laboratory of Virology, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Du Yu (D)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Zhuangzhuang Li (Z)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Jelke J Fros (JJ)

Laboratory of Virology, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Jianchao Wei (J)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Ke Liu (K)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Zongjie Li (Z)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Donghua Shao (D)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Beibei Li (B)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Jeroen Kortekaas (J)

Laboratory of Virology, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Monique M van Oers (MM)

Laboratory of Virology, Wageningen University & Research, Wageningen, 6708PB, The Netherlands.

Zhiyong Ma (Z)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China.

Gorben P Pijlman (GP)

Laboratory of Virology, Wageningen University & Research, Wageningen, 6708PB, The Netherlands. gorben.pijlman@wur.nl.

Yafeng Qiu (Y)

Shanghai Veterinary Research Institute, Chinese Academy of Agricultural Sciences, CAAS, 518 Ziyue Road, Shanghai, 200241, China. yafengq@shvri.ac.cn.

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