Travel Medicine and Infectious Disease
Volume 8, Issue 4 , Pages 213-222 , July 2010

Tick-borne encephalitis virus and the immune response of the mammalian host

  • Bastian Dörrbecker

      Affiliations

    • University Medical Center, Department of Virology, Kreuzbergring 57, 37075 Göttingen, Germany
    • Corresponding Author InformationCorresponding authors. Tel.: +49 551 3910551; fax: +49 551 3910552.
    • ,
  • Gerhard Dobler

      Affiliations

    • Institute of Microbiology of the Armed Forces, Neuherbergstrasse 11, 80937 München, Germany
    • ,
  • Martin Spiegel

      Affiliations

    • University Medical Center, Department of Virology, Kreuzbergring 57, 37075 Göttingen, Germany
    • Corresponding Author InformationCorresponding authors. Tel.: +49 551 3910551; fax: +49 551 3910552.
    • ,
  • Frank T. Hufert

      Affiliations

    • University Medical Center, Department of Virology, Kreuzbergring 57, 37075 Göttingen, Germany

Received 14 May 2010 ,Accepted 25 May 2010.

References 

  1. Grard G, Moureau G, Charrel RN, Lemasson JJ, Gonzalez JP, Gallian P, et al. Genetic characterization of tick-borne flaviviruses: new insights into evolution, pathogenetic determinants and taxonomy. Virology. 2007;361(1):80–92
  2. Ecker M, Allison SL, Meixner T, Heinz FX. Sequence analysis and genetic classification of tick-borne encephalitis viruses from Europe and Asia. J Gen Virol. 1999;80(Pt 1):179–185
  3. Burke DS, Monath TP. Flaviviruses. In:  Knipe DM,  Howley PM editor. 4th ed.. Fields Virology. vol. 1:Philadelphia: Lippincott, Williams & Wilkins; 2001;p. 1043–1125
  4. Pavlidou V, Gerou S, Diza E, Antoniadis A. Genetic study of the distribution of Greek goat encephalitis virus in Greece. Vector Borne Zoonotic Dis. 2008;8(3):351–354
  5. Süss J. Tick-borne encephalitis in Europe and beyond–the epidemiological situation as of 2007. Euro Surveill. 2008;13(26):
  6. Mansfield KL, Johnson N, Phipps LP, Stephenson JR, Fooks AR, Solomon T. Tick-borne encephalitis virus - a review of an emerging zoonosis. J Gen Virol. 2009;90:1781–1794
  7. Gustafson R, Svenungsson B, Gardulf A, Stiernstedt G, Forsgren M. Prevalence of tick-borne encephalitis and Lyme borreliosis in a defined Swedish population. Scand J Infect Dis. 1990;22(3):297–306
  8. Kaiser R. The clinical and epidemiological profile of tick-borne encephalitis in southern Germany 1994–98: a prospective study of 656 patients. Brain. 1999;122(Pt 11):2067–2078
  9. Lindquist L, Vapalahti O. Tick-borne encephalitis. Lancet. 2008;371(9627):1861–1871
  10. Dumpis U, Crook D, Oksi J. Tick-borne encephalitis. Clin Infect Dis. 1999;28(4):882–890
  11. Holzmann H. Diagnosis of tick-borne encephalitis. Vaccine. 2003;21:S36–S40
  12. Logar M, Arnez M, Kolbl J, Avsic-Zupanc T, Strle F. Comparison of the epidemiological and clinical features of tick-borne encephalitis in children and adults. Infection. 2000;28(2):74–77
  13. Kunz C. TBE vaccination and the Austrian experience. Vaccine. 2003;21:S50–S55
  14. Bender A, Jager G, Scheuerer W, Feddersen B, Kaiser R, Pfister HW. Two severe cases of tick-borne encephalitis despite complete active vaccination–the significance of neutralizing antibodies. J Neurol. 2004;251(3):353–354
  15. Schneider H. Über epidemische akute meningitis serosa. vol. 44. Wien. Klin. Wochenschr; 1931;pp. 350–352
  16. Zilber L. Spring-summer tick-borne encephalitis (in Russian). vol. 56. Arkhiv Biol Nauk; 1939;pp. 255–261
  17. Robertson SJ, Mitzel DN, Taylor RT, Best SM, Bloom ME. Tick-borne flaviviruses: dissecting host immune responses and virus countermeasures. Immunol Res. 2009;43(1–3):172–186
  18. Labuda M, Jones LD, Williams T, Danielova V, Nuttall PA. Efficient transmission of tick-borne encephalitis virus between cofeeding ticks. J Med Entomol. 1993;30(1):295–299
  19. Gritsun TS, Lashkevich VA, Gould EA. Tick-borne encephalitis. Antivir Res. 2003;57(1–2):129–146
  20. Sumilo D, Bormane A, Asokliene L, Vasilenko V, Golovljova I, Avsic-Zupanc T, et al. Socio-economic factors in the differential upsurge of tick-borne encephalitis in Central and Eastern Europe. Rev Med Virol. 2008;18(2):81–95
  21. Nuttall PA, Labuda M. Tick-Borne encephalitis. In:  Goodman JL,  Dennis DT,  Sonenshine DE editor. Tick-borne diseases of humans. Herndon USA: American Society of Microbiology (ASM) PressHerndon USA; 2005;p. 150–163
  22. Moshkin MP, Novikov EA, Tkachev SE, Vlasov VV. Epidemiology of a tick-borne viral infection: theoretical insights and practical implications for public health. Bioessays. 2009;31(6):620–628
  23. Alekseev AN, Chunikhin SP. The experimental transmission of the tick-borne encephalitis virus by ixodid ticks (the mechanisms, time periods, species and sex differences). Parazitologiia. 1990;24(3):177–185
  24. Labuda M, Austyn JM, Zuffova E, Kozuch O, Fuchsberger N, Lysy J, et al. Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology. 1996;219(2):357–366
  25. Takeuchi O, Akira S. Innate immunity to virus infection. Immunol Rev. 2009;227(1):75–86
  26. de Veer MJ, Holko M, Frevel M, Walker E, Der S, Paranjape JM, et al. Functional classification of interferon-stimulated genes identified using microarrays. J Leukoc Biol. 2001;69(6):912–920
  27. Haller O, Kochs G, Weber F. The interferon response circuit: induction and suppression by pathogenic viruses. Virology. 2006;344(1):119–130
  28. Best SM, Morris KL, Shannon JG, Robertson SJ, Mitzel DN, Park GS, et al. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J Virol. 2005;79(20):12828–12839
  29. Ashour J, Laurent-Rolle M, Shi PY, Garcia-Sastre A. NS5 of dengue virus mediates STAT2 binding and degradation. J Virol. 2009;83(11):5408–5418
  30. Guo JT, Hayashi J, Seeger C. West Nile virus inhibits the signal transduction pathway of alpha interferon. J Virol. 2005;79(3):1343–1350
  31. Lin RJ, Chang BL, Yu HP, Liao CL, Lin YL. Blocking of interferon-induced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J Virol. 2006;80(12):5908–5918
  32. Mazzon M, Jones M, Davidson A, Chain B, Jacobs M. Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation. J Infect Dis. 2009;200(8):1261–1270
  33. Werme K, Wigerius M, Johansson M. Tick-borne encephalitis virus NS5 associates with membrane protein scribble and impairs interferon-stimulated JAK-STAT signalling. Cell Microbiol. 2008;10(3):696–712
  34. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature. 1998;392(6673):245–252
  35. Segura E, Villadangos JA. Antigen presentation by dendritic cells in vivo. Curr Opin Immunol. 2009;21(1):105–110
  36. Ueno H, Schmitt N, Palucka AK, Banchereau J. Dendritic cells and humoral immunity in humans. Immunol Cell Biol. 2010;88(4):376–380
  37. Mutyambizi K, Berger CL, Edelson RL. The balance between immunity and tolerance: the role of Langerhans cells. Cell Mol Life Sci. 2009;66(5):831–840
  38. Cerovic V, McDonald V, Nassar MA, Paulin SM, Macpherson GG, Milling SW. New insights into the roles of dendritic cells in intestinal immunity and tolerance. Int Rev Cell Mol Biol. 2009;272:33–105
  39. Kenyon RH, Rippy MK, McKee KT, Zack PM, Peters CJ. Infection of Macaca radiata with viruses of the tick-borne encephalitis group. Microb Pathog. 1992;13(5):399–409
  40. Daneman R, Rescigno M. The gut immune barrier and the blood-brain barrier: are they so different?. Immunity. 2009;31(5):722–735
  41. Cox K, North M, Burke M, Singhal H, Renton S, Aqel N, et al. Plasmacytoid dendritic cells (PDC) are the major DC subset innately producing cytokines in human lymph nodes. J Leukoc Biol. 2005;78(5):1142–1152
  42. Takeda K, Akira S. Toll-like receptors in innate immunity. Int Immunol. 2005;17(1):1–14
  43. Ito T, Wang YH, Liu YJ. Plasmacytoid dendritic cell precursors/type I interferon-producing cells sense viral infection by Toll-like receptor (TLR) 7 and TLR9. Springer Semin Immunopathology. 2005;26(3):221–229
  44. Fredericksen BL, Gale M. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J Virol. 2006;80(6):2913–2923
  45. Ortaldo JR, Mantovani A, Hobbs D, Rubinstein M, Pestka S, Herberman RB. Effects of several species of human-leukocyte interferon on Cyto-Toxic activity of Nk-cells and monocytes. Int J Cancer. 1983;31(3):285–289
  46. Kadowaki N, Liu YJ. Natural type I interferon-producing cells as a link between innate and adaptive immunity. Hum Immunol. 2002;63(12):1126–1132
  47. Hellman P, Eriksson H. Early activation markers of human peripheral dendritic cells. Hum Immunol. 2007;68(5):324–333
  48. Atrasheuskaya AV, Fredeking TM, Ignatyev GM. Changes in immune parameters and their correction in human cases of tick-borne encephalitis. Clin Exp Immunol. 2003;131(1):148–154
  49. Toporkova MG, Aleshin SE, Ozherelkov SV, Nadezhdina MV, Stephenson JR, Timofeev AV. Serum levels of interleukin 6 in recently hospitalized tick-borne encephalitis patients correlate with age, but not with disease outcome. Clin Exp Immunol. 2008;152(3):517–521
  50. Skallova A, Iezzi G, Ampenberger F, Kopf M, Kopecky J. Tick saliva inhibits dendritic cell migration, maturation, and function while promoting development of Th2 responses. J Immunol. 2008;180(9):6186–6192
  51. Fialova A, Cimburek Z, Iezzi G, Kopecky J. Ixodes ricinus tick saliva modulates tick-borne encephalitis virus infection of dendritic cells. Microbes Infect. 2010;
  52. Mackenzie JS, Gubler DJ, Petersen LR. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med. 2004;10(Suppl. 12):S98–S109
  53. Plekhova NG, Somova LM, Zavorueva DV, Krylova NV, Leonova GN. NO-producing activity of macrophages infected with tick-borne encephalitis virus. Bull Exp Biol Med. 2008;145(3):344–347
  54. Kreil TR, Eibl MM. Nitric oxide and viral infection: NO antiviral activity against a flavivirus in vitro, and evidence for contribution to pathogenesis in experimental infection in vivo. Virology. 1996;219(1):304–306
  55. Lin YL, Huang YL, Ma SH, Yeh CT, Chiou SY, Chen LK, et al. Inhibition of Japanese encephalitis virus infection by nitric oxide: antiviral effect of nitric oxide on RNA virus replication. J Virol. 1997;71(7):5227–5235
  56. Kreil TR, Burger I, Bachmann M, Fraiss S, Eibl MM. Antibodies protect mice against challenge with tick-borne encephalitis virus (TBEV)-infected macrophages. Clin Exp Immunol. 1997;110(3):358–361
  57. Ahantarig A, Ruzek D, Vancova M, Janowitz A, St'astna H, Tesarova M, et al. Tick-borne encephalitis virus infection of cultured mouse macrophages. Intervirology. 2009;52(5):283–290
  58. Nathan C. Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol. 2006;6(3):173–182
  59. Vargin VV, Semenov BF. Changes of natural killer cell activity in different mouse lines by acute and asymptomatic flavivirus infections. Acta Virol. 1986;30(4):303–308
  60. Pirogova NP, Novitskii VV, Mikhailova OV, Khlusova MY, Babaeva LV, Voronkova OV, et al. Cytogenetic disorders in peripheral blood lymphocytes of patients with febrile form of tick-borne encephalitis. Bull Exp Biol Med. 2004;137(1):61–63
  61. Kubes M, Fuchsberger N, Labuda M, Zuffova E, Nuttall PA. Salivary gland extracts of partially fed Dermacentor reticulatus ticks decrease natural killer cell activity in vitro. Immunology. 1994;82(1):113–116
  62. Johnston LJ, Halliday GM, King NJ. Langerhans cells migrate to local lymph nodes following cutaneous infection with an arbovirus. J Invest Dermatol. 2000;114(3):560–568
  63. Haglund M, Gunther G. Tick-borne encephalitis–pathogenesis, clinical course and long-term follow-up. Vaccine. 2003;21(Suppl. 1):S11–S18
  64. Shilov YI, Ryzhaenkov VG. Alterations in the proliferative response of peripheral lymphocytes in tick-borne encephalitis. Dokl Biol Sci. 2000;375:553–555
  65. Erman BA, Tulakina LG, Konev VP, Poleshchuk TI. Ultrastructural pathology of the lymph nodes in tick-borne encephalitis. Arkh Patol. 1996;58(2):37–41
  66. Timofeev AV, Kondrat'eva I, Orlovskii VG, Kurzhukov GP, Loktev VB, Karganova GG. Connection between severity of the course of tick-borne encephalitis with the concentration of interleukin-2 and interleukin-6 in blood. Ter Arkh. 2002;74(11):22–23
  67. Günther G, Haglund M, Lindquist L, Skoldenberg B, Forsgren M. Intrathecal IgM, IgA and IgG antibody response in tick-borne encephalitis. Long-term follow-up related to clinical course and outcome. Clin Diagn Virol. 1997;8(1):17–29
  68. Heinz FX. Molecular aspects of TBE virus research. Vaccine. 2003;21:S3–S10
  69. Melik W, Nilsson AS, Johansson M. Detection strategies of tick-borne encephalitis virus in Swedish Ixodes ricinus reveal evolutionary characteristics of emerging tick-borne flaviviruses. Arch Virol. 2007;152(5):1027–1034
  70. Kaiser R, Holzmann H. Laboratory findings in tick-borne encephalitis–correlation with clinical outcome. Infection. 2000;28(2):78–84
  71. Kock T, Stunzner D, Freidl W, Pierer K. On the clinical course of tick-borne encephalitis (Tbe) in Styria. Nervenarzt. 1992;63(4):205–208
  72. McMinn PC. The molecular basis of virulence of the encephalitogenic flaviviruses. J Gen Virol. 1997;78:2711–2722
  73. Correale J, Villa A. Cellular Elements of the blood-brain barrier. Neurochem Res. 2009;34(12):2067–2077
  74. Banks WA, Lynch JL, Price TO. Cytokines and the blood–brain barrier. In:  Siegel A,  Zalcman SS editor. The neuroimmunological basis of behavior and mental disorders. 2009;p. 3–18
  75. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med. 2004;10(12):1366–1373
  76. Banks WA, Erickson MA. The blood-brain barrier and immune function and dysfunction. Neurobiol Dis. 2010;37(1):26–32
  77. Brett FM, Mizisin AP, Powell HC, Campbell IL. Evolution of neuropathologic abnormalities associated with blood-brain barrier breakdown in transgenic mice expressing interleukin-6 in astrocytes. J Neuropathol Exp Neurol. 1995;54(6):766–775
  78. Campbell IL, Abraham CR, Masliah E, Kemper P, Inglis JD, Oldstone MB, et al. Neurologic disease induced in transgenic mice by cerebral overexpression of interleukin 6. Proc Natl Acad Sci U S A. 1993;90(21):10061–10065
  79. Brunello AG, Weissenberger J, Kappeler A, Vallan C, Peters M, Rose-John S, et al. Astrocytic alterations in interleukin-6/Soluble interleukin-6 receptor alpha double-transgenic mice. Am J Pathol. 2000;157(5):1485–1493
  80. Schnoor M, Parkos CA. Disassembly of endothelial and epithelial junctions during leukocyte transmigration. Front Biosci. 2008;13:6638–6652
  81. Gelpi E, Preusser M, Garzuly F, Holzmann H, Heinz FX, Budka H. Visualization of Central European tick-borne encephalitis infection in fatal human cases. J Neuropathol Exp Neurol. 2005;64(6):506–512
  82. Kindberg E, Mickiene A, Ax C, Akerlind B, Vene S, Lindquist L, et al. A deletion in the chemokine receptor 5 (CCR5) gene is associated with tickborne encephalitis. J Infect Dis. 2008;197(2):266–269
  83. Glass WG, McDermott DH, Lim JK, Lekhong S, Yu SF, Frank WA, et al. CCR5 deficiency increases risk of symptomatic West Nile virus infection. J Exp Med. 2006;203(1):35–40
  84. Monath TP, Cropp CB, Harrison AK. Mode of entry of a neurotropic arbovirus into the central nervous system. Reinvestigation of an old controversy. Lab Invest. 1983;48(4):399–410
  85. Zlotnik I, Grant DP. Further observations on subacute sclerosing encephalitis in adult hamsters: the effects of intranasal infections with Langat virus, measles virus and SSPE-measles virus. Br J Exp Pathol. 1976;57(1):49–66
  86. Avsic-Zupanc T, Poljak M, Maticic M, Radselmedvescek A, Leduc JW, Stiasny K, et al. Laboratory acquired tick-borne meningoencephalitis - characterization of virus-strains. Clin Diagn Virol. 1995;4(1):51–59
  87. Marjelund S, Tikkakoski T, Tuisku S, Raisanen S. Magnetic resonance imaging findings and outcome in severe tick-borne encephalitis. Report of four cases and review of the literature. Acta Radiol. 2004;45(1):88–94
  88. Lorenzl S, Pfister HW, Padovan C, Yousry T. MRI abnormalities in tick-borne encephalitis. Lancet. 1996;347(9002):698–699
  89. Ruzek D, Vancova M, Tesarova M, Ahantarig A, Kopecky J, Grubhoffer L. Morphological changes in human neural cells following tick-borne encephalitis virus infection. J Gen Virol. 2009;90(Pt 7):1649–1658
  90. Ruzek D, Salat J, Palus M, Gritsun TS, Gould EA, Dykova I, et al. CD8 + T-cells mediate immunopathology in tick-borne encephalitis. Virology. 2009;384(1):1–6
  91. Gelpi E, Preusser M, Laggner U, Garzuly F, Holzmann H, Heinz FX, et al. Inflammatory response in human tick-borne encephalitis: analysis of postmortem brain tissue. J Neurovirol. 2006;12(4):322–327
  92. Maximova OA, Faucette LJ, Ward JM, Murphy BR, Pletnev AG. Cellular inflammatory response to flaviviruses in the central nervous system of a primate host. J Histochem Cytochem. 2009;57(10):973–989
  93. Günther G, Haglund M, Lindquist L, Skoldenberg B, Forsgren M. Intrathecal production of neopterin and beta 2 microglobulin in tick-borne encephalitis (TBE) compared to meningoencephalitis of other etiology. Scand J Infect Dis. 1996;28(2):131–138
  94. Lepej SZ, Misic-Majerus L, Jeren T, Rode OD, Remenar A, Sporec V, et al. Chemokines CXCL10 and CXCL11 in the cerebrospinal fluid of patients with tick-borne encephalitis. Acta Neurol Scand. 2007;115(2):109–114
  95. Sui Y, Stehno-Bittel L, Li S, Loganathan R, Dhillon NK, Pinson D, et al. CXCL10-induced cell death in neurons: role of calcium dysregulation. Eur J Neurosci. 2006;23(4):957–964
  96. van Marle G, Antony J, Ostermann H, Dunham C, Hunt T, Halliday W, et al. West Nile virus-induced neuroinflammation: glial infection and capsid protein-mediated neurovirulence. J Virol. 2007;81(20):10933–10949
  97. Tomazic J, Ihan A. Flow cytometric analysis of lymphocytes in cerebrospinal fluid in patients with tick-borne encephalitis. Acta Neurol Scand. 1997;95(1):29–33
  98. Maximova OA, Ward JM, Asher DM, St Claire M, Finneyfrock BW, Speicher JM, et al. Comparative neuropathogenesis and neurovirulence of attenuated flaviviruses in nonhuman primates. J Virol. 2008;82(11):5255–5268

PII: S1477-8939(10)00096-7

doi: 10.1016/j.tmaid.2010.05.010

Travel Medicine and Infectious Disease
Volume 8, Issue 4 , Pages 213-222 , July 2010

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