Signal transduction in immune cells and extracellular matrix role in viral tick-borne encephalitis
- Authors: Belokrylova J.P.1
-
Affiliations:
- M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)
- Issue: Vol 15, No 5 (2025)
- Pages: 826-836
- Section: REVIEWS
- URL: https://ogarev-online.ru/2220-7619/article/view/380202
- DOI: https://doi.org/10.15789/2220-7619-STI-17940
- ID: 380202
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Full Text
Abstract
Tick-borne encephalitis virus, a member of the genus Orthoflavivirus, consisting of Flaviviridae, is the causative agent of tick-borne encephalitis, a neuroviral disease, the severity of which varies from mild (febrile form) to severe and life-threatening course (meningoencephalitic form or encephalomyelitis). Tick-borne encephalitis virus is widespread in the countries of Eastern, Central, Northern and Eastern Europe, as well as in Northern China, Mongolia and Russia. In endemic areas, about 12 000 cases of tick-borne encephalitis are recorded annually, which affects socio-economic parameters and poses a serious threat to public health. To date, only vaccination is a verified measure for specific prevention of tick-borne encephalitis; no etiotropic approaches for tick-borne encephalitis exist. However, the inactivated vaccines currently available on the market and in use exert a relatively short immunological memory. In recent years, there has been increasingly evident that the susceptibility to tick-borne encephalitis virus and disease severity are determined not only by the pathogen properties but also by the host genetic factors. In this review, we attempted to summarize previous studies and assess the effect of single nucleotide polymorphisms in the genes of innate immunity and the extracellular matrix on susceptibility to tick-borne encephalitis. We have identified the following markers of susceptibility to tick-borne encephalitis: TLR3 rs3775291; DDX58 rs3739674; OAC2 rs1293762; IFIT1 rs304478; CD209 rs2287886; CCR5 CCR5∆32; IL10 rs1800872; ABCB9 rs4148866; COL22A1 rs4909444; MMP9 rs17576. The review presents studies corroborating as significant influence of innate immunity at the time of the emergence of infectious diseases, identified potential single nucleotide polymorphisms in the genes responsible for immune signaling and confirmatory results on overall resistance or resistance to viral invasion. However, further validated studies in larger areas and worldwide association studies (GWAS) are needed for a better understanding. The availability of data on genetic markers that reliably affect tick-borne encephalitis allows to identify patients at risk, individualize vaccination and apply proper therapeutic strategies in the future, as well as provide new data on determining the pathogenesis of tick-borne encephalitis and the host-virus interaction during infection.
About the authors
Jeanne P. Belokrylova
M.P. Chumakov Federal Scientific Center for Research and Development of Immunobiological Drugs of the Russian Academy of Sciences (Polio Institute)
Author for correspondence.
Email: jsanchezpimentel@gmail.com
ORCID iD: 0000-0001-7801-1840
SPIN-code: 7788-7339
Researcher, Laboratory of Tick-borne Encephalitis and Other Viral Encephalitides
Russian Federation, MoscowReferences
- Бархаш А.В., Юрченко А.А., Юдин Н.С., Козлова И.В., Борищук И.А., Смольникова М.В., Зайцева О.И., Позднякова Л.Л., Воевода М.И., Ромащенко А.Г. Связь полиморфизма генов ABCB9 и COL22A1 с предрасположенностью человека к тяжелым формам клещевого энцефалита // Генетика. 2019. Т. 55, № 3. С. 337–347. [Barkhash A.V., Yurchenko A.A., Yudin N.S., Kozlova I.V., Borischuk I.A., Smolnikova M.V., Zaitseva O.I., Pozdnyakova L.L., Voevoda M.I., Romashchenko A.G. Association of ABCB9 and COL22A1 gene polymorphism with human predisposition to severe forms of tick-borne encephalitis. Genetika = Russian Journal of Genetics, 2019, vol. 55, no. 3, pp. 337–347. (In Russ.)] doi: 10.1134/S0016675819030032
- Бархаш А.В., Бабенко В.Н., Воевода М.И., Ромащенко А.Г. Полиморфизм генов CD209 и TLR3 в популяциях Северной Евразии // Генетика. 2016. Т. 52, № 6. С. 697–704. [Barkhash A.V., Babenko V.N., Voevoda M.I., Romaschenko A.G. Polymorphism of CD209 and TLR3 genes in populations of North Eurasia. Genetika = Russian Journal of Genetics, 2016, vol. 52, no. 6, pp. 697–704. (In Russ.)] doi: 10.7868/S0016675816040020
- Герасимов С.Г., Погодина В.В., Колясникова Н.М., Карань Л.С., Маленко Г.В., Левина Л.С. Взаимодействие сибирского и дальневосточного подтипов вируса клещевого энцефалита при микст-инфекции в организме млекопитающих. Конкуренция подтипов при острой и инаппарантной инфекции // Вопросы вирусологии. 2011. Т. 56, № 3. C. 41–44. [Gerasimov S.G., Pogodina V.V., Kolyasnikova N.M., Karan’ L.S., Malenko G.V., Levina L.S., Gerasimov S.G., Pogodina V.V., Kolyasnikova N.M., Karan L.S., Malenko G.V., Levina L.S. Interaction of the Siberian and Far Eastern subtypes of tick-borne encephalitis virus in mammals with mixed infection. Competition of the subtypes in acute and inapparent infection. Voprosy virusologii = Problems of Virology, 2011, vol. 56, no. 3, pp. 41–44. (In Russ.)]
- Злобин В.И., Беликов С.И., Джиоев Ю.П., Демина Т.В., Козлова И.В. Молекулярная эпидемиология клещевого энцефалита // Иркутск: РИО ВСНЦ СО РАМН, 2003. 271 с. [Zlobin V.I., Belikov S.I., Dzhioev Yu.P., Demina T.V., Kozlova I.V. Molecular epidemiology of tick-borne encephalitis. Irkutsk: RIO VSRC SB RAMS, 2003. 271 p. (In Russ.)]
- Погодина В.В. Мониторинг популяций вируса клещевого энцефалита и этиологической структуры заболеваемости за 60-летний период // Вопросы вирусологии. 2005. Т. 50, № 3. С. 7–13. [Pogodina V.V. Monitoring of tick-borne encephalitis virus populations and the etiological structure of morbidity over a 60-year period. Voprosy virusologii = Problems of Virology, 2005, vol. 50, no. 3, pp. 7–13. (In Russ.)]
- Погодина В.В., Бочкова Н.Г., Карань Л.С., Трухина А.Г., Левина Л.С., Маленко Г.В., Дружинина Т.А., Лукашенко З.С., Дулькейт О.Ф., Платонов А.Е. Сибирский и дальневосточный подтипы вируса клещевого энцефалита в европейских и азиатских регионах России: генетическая и антигенная характеристика штаммов // Вопросы вирусологии. 2004. Т. 49, № 4. С. 20–25. [Pogodina V.V., Bochkova N.G., Karan L.S., Trukhina A.G., Levina L.S., Malenko G.V., Druzhinina T.A., Lukashenko Z.S., Dulkeit O.F., Platonov A.E. The Siberian and Far-Eastern subtypes of tick-borne encephalitis virus registered in Russia’s Asian regions: genetic and antigen characteristic of the strains. Voprosy virusologii = Problems of Virology, 2004, vol. 49, no. 4, pp. 20–25. (In Russ.)]
- Погодина В.В., Левина Л.С., Скрынник С.М., Травина Н.С., Карань Л.С., Колясникова Н.М., Кармышева В.Я., Герасимов С.Г., Маленко Г.В., Перминов Л.В., Попов М.А., Бочкова Н.Г. Клещевой энцефалит с молниеносным течением и летальным исходом у многократно вакцинированного пациента // Вопросы вирусологии. 2013. № 2. С. 33–37. [Pogodina V.V., Levina L.S., Skrynnik S.M., Travina N.S., Karan L.S., Kolyasnikova N.M., Karmysheva V.Ya., Gerasimov S.G., Malenko G.V., Perminov L.V., Popov M.A., Bochkova N.G. Tick-borne encephalitis with fulminant course and lethal outcome in patients after plural vaccination. Voprosy virusologii = Problems of Virology, 2013, no. 2, pp. 33–37. (In Russ.)]
- Погодина В.В., Щербинина М.С., Колясникова Н.М., Герасимов С.Г., Слезкина Т.В., Санчес-Пиментель Ж.П., Ишмухаметов А.А. Характеристика случаев клещевого энцефалита у вакцинированных // Эпидемиология и вакцинопрофилактика. 2019. Т. 18, № 6. С. 90–97. [Pogodina V.V., Scherbinina M.S., Kolyasnikova N.M., Gerasimov S.G., Slezkina T.V., Sanchez-Pimentel J.P., Ishmuhametov A.A. Characteristics of Morbidity of the Tick-Borne Encephalitis in Vaccinated. Epidemiologiya i vaktsinoprofilaktika = Epidemiology and Vaccine Prophylaxis, 2019, vol. 18, no. 6, pp. 90–97. (In Russ.)] doi: 10.31631/2073-3046-2019-18-6-90-97
- Abbas Y.M., Pichlmair A., Górna M.W., Superti-Furga G., Nagar B. Structural basis for viral 5’-PPP-RNA recognition by human IFIT proteins. Nature, 2013, vol. 494, no. 7435, pp. 60–64. doi: 10.1038/nature11783
- Afroz S., Giddaluru J., Abbas M.M., Khan N. Transcriptome meta-analysis reveals a dysregulation in extra cellular matrix and cell junction associated gene signatures during Dengue virus infection. Sci. Rep., 2016, vol. 6: 33752. doi: 10.1038/srep33752
- Alagarasu K., Memane R.S., Shah P.S. Polymorphisms in the retinoic acid-1 like-receptor family of genes and their association with clinical outcome of dengue virus infection. Arch. Virol., 2015, vol. 160, no. 6, pp. 1555–1560. doi: 10.1007/s00705-015-2417-z
- Babon J.J., Nicola N.A. The biology and mechanism of action of suppressor of cytokine signaling 3. Growth Factors, 2012, vol. 30, no. 4, pp. 207–219. doi: 10.3109/08977194.2012.687375
- Baños-Lara M.R., Ghosh A., Guerrero-Plata A. Critical role of MDA5 in the interferon response induced by human metapneumovirus infection in dendritic cells and in vivo. J. Virol., 2013, vol. 87, no. 2, pp. 1242–1251. doi: 10.1128/JVI.01213-12
- Barkhash A.V., Kochneva G.V., Chub E.V., Romaschenko A.G. Single nucleotide polymorphism rs1800872 in the promoter region of the IL10 gene is associated with predisposition to chronic hepatitis C in Russian population. Microbes Infect., 2018, vol. 20, no. 3, pp. 212–216. doi: 10.1016/j.micinf.2017.11.012
- Barkhash A.V., Perelygin A.A., Babenko V.N., Brinton M.A., Voevoda M.I. Single nucleotide polymorphism in the promoter region of the CD209 gene is associated with human predisposition to severe forms of tick-borne encephalitis. Antiviral Res., 2012, vol. 93, no. 1, pp. 64–68. doi: 10.1016/j.antiviral.2011.10.017
- Barkhash A.V., Perelygin A.A., Babenko V.N., Myasnikova N.G., Pilipenko P.I., Romaschenko A.G., Voevoda M.I., Brinton M.A. Variability in the 2’-5’-Oligoadenylate Synthetase Gene Cluster Is Associated with Human Predisposition to Tick-Borne Encephalitis Virus-Induced Disease. J. Infect. Dis., 2010, vol. 202, no. 12, pp. 1813–1818. doi: 10.1086/657418
- Barkhash A.V., Yurchenko A.A., Yudin N.S., Ignatieva E.V., Kozlova I.V., Borishchuk I.A., Pozdnyakova L.L., Voevoda M.I., Romaschenko A.G. A matrix metalloproteinase 9 (MMP9) gene single nucleotide polymorphism is associated with predisposition to tick-borne encephalitis virus-induced severe central nervous system disease. Ticks Tick Borne Dis., 2018, vol. 9, no. 4, pp. 763–767. doi: 10.1016/j.ttbdis.2018.02.010
- Charvet B., Guiraud A., Malbouyres M., Zwolanek D., Guillon E., Bretaud S., Monnot C., Schulze J., Bader H.L., Allard B., Koch M., Ruggiero F. Knockdown of col22a1 gene in zebrafish induces a muscular dystrophy by disruption of the myotendinous junction. Development, 2013, vol. 140, no. 22, pp. 4602–4613. doi: 10.1242/dev.096024
- Chen Y., Mehmood K., Chang Y.F., Tang Z., Li Y., Zhang H. The molecular mechanisms of glycosaminoglycan biosynthesis regulating chondrogenesis and endochondral ossification. Life Sci., 2023, vol. 335: 122243. doi: 10.1016/j.lfs.2023.122243
- Chistiakov D.A. Interferon induced with helicase C domain 1 (IFIH1) and virus-induced autoimmunity: a review. Viral Immunol., 2010, vol. 23, no. 1, pp. 3–15. doi: 10.1089/vim.2009.0071
- Choi U.Y., Kang J.-S., Hwang Y.S., Kim Y.-J. Oligoadenylate synthase-like (OASL) proteins: dual functions and associations with diseases. Exp. Mol. Med., 2015, vol. 47, no. 3: e144. doi: 10.1038/emm.2014.110
- De Bruijn M., Van der Lely N., Marcelis J., Roks G. ‘Tick-borne’ encephalitis in an immunocompromised patient. Ned. Tijdschr. Geneeskd., 2015, vol. 159: A8604.
- Erber W., Schmitt H.-J., Vuković Janković T. Chapter 12a: Epidemiology by country an overview. The TBE book (second edition) / Eds. Dobler G., Erber W., Broker M., Schmitt H.-J. Singapore: Global Health Press, 2019, pp. 212–233.
- Fortova A., Barkhash A.V., Pychova M., Krbkova L., Palus M., Salat J., Ruzek D. Genetic polymorphisms in innate immunity genes influence predisposition to tick-borne encephalitis. J. Neurovirol., 2023, vol. 29, no. 6, pp. 699–705. doi: 10.1007/s13365-023-01182-8
- Füzik T., Formanová P., Růžek D., Yoshii K., Niedrig M., Plevka P. Structure of tick-borne encephalitis virus and its neutralization by a monoclonal antibody. Nat. Commun., 2018, vol. 9, no. 1: 436. doi: 10.1038/s41467-018-02882-0
- Gorman J.A., Hundhausen C., Errett J.S., Stone A.E., Allenspach E.J., Ge Y., Arkatkar T., Clough C., Dai X., Khim S., Pestal K., Liggitt D., Cerosaletti K., Stetson D.B., James R.G., Oukka M., Concannon P., Gale M. Jr., Buckner J.H., Rawlings D.J. The A946T variant of the RNA sensor IFIH1 mediates an interferon program that limits viral infection but increases the risk for autoimmunity. Nat. Immunol., 2017, vol. 18, no. 7, pp. 744–752. doi: 10.1038/ni.3766
- Heinz F.X., Mandl C.W. The molecular biology of tick-borne encephalitis virus. APMIS, 1993, vol. 101, no. 10, pp. 735–745. doi: 10.1111/j.1699-0463.1993.tb00174.x
- Heinz F.X., Stiasny K., Holzmann H., Grgic-Vitek M., Kriz B., Essl A., Kundi M. Vaccination and tick-borne encephalitis, central Europe. Emerg. Infect. Dis., 2013, vol. 19, no. 1, pp. 69–76. doi: 10.3201/eid1901.120458
- Herd C.S., Yu X., Cui Y., Franz A.W.E. Identification of the extracellular metallo-endopeptidases ADAM and ADAMTS in the yellow fever mosquito Aedes aegypti. Insect Biochem. Mol. Biol., 2022, vol. 148: 103815. doi: 10.1016/j.ibmb.2022.103815
- Järver P., Dondalska A., Poux C., Sandberg A., Bergenstråhle J., Sköld A.E., Dereuddre-Bosquet N., Martinon F., Pålsson S., Zaghloul E., Brodin D., Sander B., Kim A., Lennox K.A., Behlke M.A., El Andaloussi S., Lehtiö J., Lundeberg J., Le Grand R., Spetz A.L. Single-Stranded Nucleic Acids Regulate TLR3/4/7 Activation through Interference with Clathrin-Mediated Endocytosis. Sci. Rep., 2018, vol. 8: 15841. doi: 10.1038/s41598-018-33960-4
- Kemball C.C., Alirezaei M., Whitton J.L. Type B coxsackieviruses and their interactions with the innate and adaptive immune systems. Future Microbiol., 2010, vol. 5, no. 9, pp. 1329–1347. doi: 10.2217/fmb.10.101
- Kindberg E., Mickiene A., Ax C., Akerlind B., Vene S., Lindquist L., Lundkvist A., Svensson L. A deletion in the chemokine receptor 5 (CCR5) gene is associated with tick-borne encephalitis. J. Infect. Dis., 2008, vol. 197, no. 2, pp. 266–269. doi: 10.1086/524709
- Kindberg E., Vene S., Mickiene A., Lundkvist Å., Lindquist L., Svensson L. A functional Toll-like receptor 3 gene (TLR3) may be a risk factor for tick-borne encephalitis virus (TBEV) infection. J. Infect. Dis., 2011, vol. 203, no. 4, pp. 523–528. doi: 10.1093/infdis/jiq082
- King A., Adams M.J., Carstens E.B., Lefkowitz E.J. Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. Amsterdam: Elsevier, 2012, pp. 1003–1020.
- Koch M., Schulze J., Hansen U., Ashwodt T., Keene D.R., Brunken W.J., Burgeson R.E., Bruckner P., Bruckner-Tuderman L. A novel marker of tissue junctions, collagen XXII. J. Biol. Chem., 2004, vol. 279, no. 21, pp. 22514–22521. doi: 10.1074/jbc.M400536200
- Kong K.F., Delroux K., Wang X., Qian F., Arjona A., Malawista S.E., Fikrig E., Montgomery R.R. Dysregulation of TLR3 impairs the innate immune response to West Nile virus in the elderly. J. Virol., 2008, vol. 82, no. 15, pp. 7613–7623. doi: 10.1128/JVI.00618-08
- Kumar H., Kawai T., Akira S. Pathogen Recognition by the Innate Immune System. Int. Rev. Immunol., 2011, vol. 30, no. 1, pp. 16–34. doi: 10.3109/08830185.2010.529976
- Kunze U. The international scientific working group on tick-borne encephalitis (ISW TBE): review of 17 years of activity and commitment. Ticks Tick Borne Dis., 2016, vol. 7, no. 3, pp. 399–404. doi: 10.1016/j.ttbdis.2015.12.018
- Lenhard T., Ott D., Jakob N.J., Pham M., Bäumer P., Martinez-Torres F., Meyding-Lamadé U. Predictors, Neuroimaging Characteristics and Long-Term Outcome of Severe European Tick-Borne Encephalitis: A Prospective Cohort Study. PLoS One, 2016, vol. 11, no. 4: e0154143. doi: 10.1371/journal.pone.0154143
- Lim J.K., Lim J.K., Lisco A., McDermott D.H., Huynh L., Ward J.M., Johnson B., Johnson H., Pape J., Foster G.A., Krysztof D., Follmann D., Stramer S.L., Margolis L.B., Murphy P.M. Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog., 2009, vol. 5, no. 2: e1000321. doi: 10.1371/journal.ppat.1000321
- Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., García-Sastre A., Katze M.G., Gale M. Jr. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol., 2008, vol. 82, no. 1, pp. 335–345. doi: 10.1128/JVI.01080-07
- Mackenzie J.S., Gubler D.J., Petersen L.R. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med., 2004, vol. 10, no. 12, pp. 98–109. doi: 10.1038/nm1144
- Melik W., Ellencrona K., Wigerius M., Hedström C., Elväng A., Johansson M. Two PDZ binding motifs within NS5 have roles in tick-borne encephalitis virus replication. Virus Res., 2012, vol. 169, no. 1, pp. 54–62. doi: 10.1016/j.virusres.2012.07.001
- Mickienė A., Pakalnienė J., Nordgren J., Carlsson B., Hagbom M., Svensson L., Lindquist L. Polymorphisms in chemokine receptor 5 and Toll-like receptor 3 genes are risk factors for clinical tick-borne encephalitis in the Lithuanian population. PLoS One, 2014, vol. 9, no. 9: e0106798. doi: 10.1371/journal.pone.0106798
- Mielcarska M.B., Bossowska-Nowicka M., Toka F.N. Functional failure of TLR3 and its signaling components contribute to herpes simplex encephalitis. J. Neuroimmunol., 2018, vol. 316, no. 15, pp. 65–73. doi: 10.1016/j.jneuroim.2017.12.011
- Morozova O.V., Bakhvalova V.N., Potapova O.F., Grishechkina A.E., Isaeva E.I., Aldarov K.V., Klinov D.V., Vorovich M.F. Evaluation of immune response and protective effect of four vaccines against the tick-borne encephalitis virus. Vaccine, 2014, vol. 32, no. 25, pp. 3101–3106. doi: 10.1016/j.vaccine.2014.02.046
- Pabalan N., Chaisri S., Tabunhan S., Phumyen A., Jarjanazi H., Steiner T.S. Associations of DC-SIGN (CD209) promoter –336G/A polymorphism (rs4804803) with dengue infection: A systematic review and meta-analysis. Acta Trop., 2018, vol. 177, pp. 186–193. doi: 10.1016/j.actatropica.2017.10.017
- Radzišauskienė D., Žagminas K., Ašoklienė L., Jasionis A., Mameniškienė R., Ambrozaitis A., Jančorienė L., Jatužis D., Petraitytė I., Mockienė E. Epidemiological patterns of tick-borne encephalitis in Lithuania and clinical features in adults in the light of the high incidence in recent years: a retrospective study. Eur. J. Neurol., 2018, vol. 25, no. 2, pp. 268–274. doi: 10.1111/ene.13486
- Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol., 2008, vol. 89, no. 1, pp. 1–47. doi: 10.1099/vir.0.83391-0
- Ruzek D., Avšič Županc T., Borde J., Chrdle A., Eyer L., Karganova G., Kholodilov I., Knap N., Kozlovskaya L., Matveev A., Miller A.D., Osolodkin D.I., Överby A.K., Tikunova N., Tkachev S., Zajkowska J. Tick-borne encephalitis in Europe and Russia: Review of pathogenesis, clinical features, therapy, and vaccines. Antiviral Res., 2019, vol. 164, pp. 23–51. doi: 10.1016/j.antiviral.2019.01.014
- Saito T., Owen D.M., Jiang F., Marcotrigiano J., Gale M. Jr. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature, 2008, vol. 454, no. 7203, pp. 523–527. doi: 10.1038/nature07106
- Selinger M., Věchtová P., Tykalová H., Ošlejšková P., Rumlová M., Štěrba J., Grubhoffer L. Integrative RNA profiling of TBEV-infected neurons and astrocytes reveals potential pathogenic effectors. Comput. Struct. Biotechnol. J., 2022, vol. 20, pp. 2759–2777. doi: 10.1016/j.csbj.2022.05.052
- Schindler C., Levy D.E., Decker T. JAK-STAT Signaling: From Interferons to Cytokines. J. Biol. Chem., 2007, vol. 282, no. 28, pp. 20059–20063. doi: 10.1074/jbc.R700016200
- Simon-Loriere E., Lin R.J., Kalayanarooj S.M., Chuansumrit A., Casademont I., Lin S.Y., Yu H.P., Lert-Itthiporn W., Chaiyaratana W., Tangthawornchaikul N., Tangnararatchakit K., Vasanawathana S., Chang B.L., Suriyaphol P., Yoksan S., Malasit P., Despres P., Paul R., Lin Y.L., Sakuntabhai A. High Anti-Dengue Virus Activity of the OAS Gene Family Is Associated With Increased Severity of Dengue. J. Infect. Dis., 2015, vol. 212, no. 12, pp. 2011–2020. doi: 10.1093/infdis/jiv321
- Slater L., Bartlett N.W., Haas J.J., Zhu J., Message S.D., Walton R.P., Sykes A., Dahdaleh S., Clarke D.L., Belvski M.G., Kon O.M., Fujita T., Jeffery P.K., Johnston S.L., Edwards M.R. Co-ordinated role of TLR3, RIG-I and MDA5 in the innate response to rhinovirus in bronchial epithelium. PLoS Pathog., 2010, vol. 6, no. 11: e1001178. doi: 10.1371/journal.ppat.1001178
- Sui L., Zhao Y., Wang W., Chi H., Tian T., Wu P., Zhang J., Zhao Y., Wei Z.K., Hou Z., Zhou G., Wang G., Wang Z., Liu Q. Flavivirus prM interacts with MDA5 and MAVS to inhibit RLR antiviral signaling. Cell Biosci., 2023, vol. 13, no. 1: 9. doi: 10.1186/s13578-023-00957-0
- Tang D., Kang R., Coyne C.B., Zeh H.J., Lotze M.T. PAMPs and DAMPs: signal 0s that spur autophagy and immunity. Immunol. Rev., 2012, vol. 249, no. 1, pp. 158–175. doi: 10.1111/j.1600-065X.2012.01146.x
- Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med., 2004, vol. 10, no. 12, pp. 1366–1373. doi: 10.1038/nm1140
- Werme K., Wigerius M., Johansson M. Tick-borne encephalitis virus NS5 associates with membrane protein scribble and impairs interferon-stimulated JAKSTAT signalling. Cell Microbiol., 2008, vol. 10, no. 3, pp. 696–712. doi: 10.1111/j.1462-5822.2007.01076.x
- Wilhelm S.M., Collier I.E., Marmer B.L., Eisen A.Z., Grant G.A., Goldberg G.I. SV40-transformed human lung fibroblasts secrete a 92-kDa type IV collagenase which is identical to that secreted by normal human macrophages. J. Biol. Chem., 1989, vol. 264, no. 29, pp. 17213–17221. doi: 10.1016/S0021-9258(18)71480-4
- Wolf H.M., Thon V., Litzman J., Eibl M.M. Detection of impaired IgG antibody formation facilitates the decision on early immunoglobulin replacement in hypogammaglobulinemic patients. Front. Immunol., 2015, vol. 6: 32. doi: 10.3389/fimmu.2015.00032
- Xu J., Dai X., Shang G., Lu S., Yang J. A new subtype of eastern tick-borne encephalitis virus discovered in Qinghai-Tibet Plateau, China. Emerg. Microbes Infect., 2018, vol. 7, no. 1: 74. doi: 10.1038/s41426-018-0081-6
- Zaitsev B.N., Benedetti F., Mikhaylov A.G., Korneev D.V., Sekatskii S.K., Karakouz T., Belav P.A., Netesova N.A., Protopopova E.V., Konovalova S.N., Dietler G., Loktev V. Force-induced globule-coil transition in laminin binding protein and its role for viral-cell membrane fusion. J. Mol. Recognit., 2014, vol. 27, no. 12, pp. 727–738. doi: 10.1002/jmr.2345
- Zhang D., Zheng N., Liu X. The role and mechanism of NF-κB in viral encephalitis of children. Exp. Ther. Med., 2017, vol. 13, no. 6, pp. 3489–3493. doi: 10.3892/etm.2017.4396
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