Mice with different susceptibility to tick-borne encephalitis virus infection show selective neutralizing antibody response and inflammatory reaction in the central nervous system

Journal of Neuroinflammation

Volumn 10, Issue , 2013, Pages

  Palus, Martin ^a,b   Vojtíšková, Jarmila ^a   Salát, Jiří ^a,c   Kopecký, Jan ^a,b   Grubhoffer, Libor ^a,b   Lipoldová, Marie ^a   Demant, Peter ^d   Růžek, Daniel ^a,c  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^c VETERINARY RESEARCH INSTITUTE   (Czech Republic)

^d ROSWELL PARK CANCER INSTITUTE   (United States)

Author keywords

Antibody production; Flavivirus encephalitis; Neuroinflammation; Tick borne encephalitis

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 10; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; NEUTRALIZING ANTIBODY; RANTES; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ARTICLE; BRAIN LEVEL; CELL SURFACE; CENTRAL NERVOUS SYSTEM INFLAMMATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; DISEASE SEVERITY; EXPERIMENTAL MOUSE; FEMALE; FLAVIVIRUS INFECTION; HOST PATHOGEN INTERACTION; IMMUNOCOMPETENT CELL; INFECTION SENSITIVITY; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHOLOGY; NONHUMAN; PROTEIN EXPRESSION; SURVIVAL RATE; TICK BORNE ENCEPHALITIS FLAVIVIRUS; VIREMIA; VIROGENESIS; VIRUS LOAD;

EID: 84879436988     PISSN: None     EISSN: 17422094     Source Type: Journal    
DOI: 10.1186/1742-2094-10-77     Document Type: Article

References (52)

1. Růžek D, Gritsun TS, Forrester NL, Gould EA, Kopecký J, Golovchenko M, Rudenko N, Grubhoffer L. Mutations in the NS2B and NS3 genes affect mouse neuroinvasiveness of a Western European field strain of tick-borne encephalitis virus. Virology 2008, 374:249-255. 10.1016/j.virol.2008.01.010, 18339416.
2. Růžek D, Salát J, Palus M, Gritsun TS, Gould EA, Dyková I, Skallová A, Jelínek J, Kopecký J, Grubhoffer L. CD8+ T-cells mediate immunopathology in tick-borne encephalitis. Virology 2009, 384:1-6. 10.1016/j.virol.2008.11.023, 19070884.
3. Lipoldová M, Demant P. Genetic susceptibility to infectious disease: lessons from mouse models of leishmaniasis. Nat Rev Genet 2006, 7:294-305. 10.1038/nrg1832, 16543933.
4. Kindberg E, Vene S, Mickiene A, Lundkvist T, 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, 203:523-528. 10.1093/infdis/jiq082, 3071239, 21216866.
5. 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 tickborne encephalitis. J Infect Dis 2008, 197:266-269. 10.1086/524709, 18179389.
6. Barkhash AV, Babenko VN, Kobzev VF, Romashchenko AG, Voevoda MI. Polymorphism in the human 2'-5'-oligoadenylate synthetase genes (OAS), associated with predisposition to severe forms of tick-borne encephalitis, in populations from North Eurasia. Mol Biol (Mosk) 2010, 44:985-993.
7. Barkhash AV, Perelygin AA, Babenko VN, Brinton MA, Voevoda MI. 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, 93:64-68. 10.1016/j.antiviral.2011.10.017, 22061615.
8. Urosevic N, Shellam GR. Host genetic resistance to Japanese encephalitis group viruses. Curr Top Microbiol Immunol 2002, 267:153-170. 10.1007/978-3-642-59403-8_8, 12082988.
9. Brinton MA, Perelygin AA. Genetic resistance to flaviviruses. Adv Virus Res 2003, 60:43-85.
10. Demant P, Hart AA. Recombinant congenic strains-a new tool for analyzing genetic traits determined by more than one gene. Immunogenetics 1986, 24:416-422. 10.1007/BF00377961, 3793154.
11. Banus HA, van Kranen HJ, Mooi FR, Hoebee B, Nagelkerke NJ, Demant P, Kimman TG. Genetic control of Bordetella pertussis infection: identification of susceptibility loci using recombinant congenic strains of mice. Infect Immun 2005, 73:741-747. 10.1128/IAI.73.2.741-747.2005, 547026, 15664912.
12. Demant P, Lipoldova M, Svobodova M. Resistance to Leishmania major in mice. Science 1996, 274:1392. 10.1126/science.274.5291.1392, 8966604.
13. Lipoldová M, Svobodová M, Krulová M, Havelková H, Badalová J, Nohýnková E, Holán V, Hart AA, Volf P, Demant P. Susceptibility to Leishmania major infection in mice: multiple loci and heterogeneity of immunopathological phenotypes. Genes Immun 2000, 1:200-206. 10.1038/sj.gene.6363660, 11196712.
14. Badalová J, Svobodová M, Havelková H, Vladimirov V, Vojtíšková J, Engová J, Pilcík T, Volf P, Demant P, Lipoldová M. Separation and mapping of multiple genes that control IgE level in Leishmania major infected mice. Genes Immun 2002, 3:187-195. 10.1038/sj.gene.6363838, 12058253.
15. Vladimirov V, Badalová J, Svobodová M, Havelková H, Hart AA, Blazková H, Demant P, Lipoldová M. Different genetic control of cutaneous and visceral disease after Leishmania major infection in mice. Infect Immun 2003, 71:2041-2046. 10.1128/IAI.71.4.2041-2046.2003, 152088, 12654824.
16. Havelková H, Badalová J, Svobodová M, Vojtísková J, Kurey I, Vladimirov V, Demant P, Lipoldová M. Genetics of susceptibility to leishmaniasis in mice: four novel loci and functional heterogeneity of gene effects. Genes Immun 2006, 7:220-233. 10.1038/sj.gene.6364290, 16511555.
17. Kurey I, Kobets T, Havelková H, Slapničková M, Quan L, Trtková K, Grekov I, Svobodová M, Stassen AP, Hutson A, Demant P, Lipoldová M. Distinct genetic control of parasite elimination, dissemination, and disease after Leishmania major infection. Immunogenetics 2009, 61:619-633. 10.1007/s00251-009-0392-9, 2744819, 19705113.
18. Kobets T, Havelková H, Grekov I, Volkova V, Vojtíšková J, Slapničková M, Kurey I, Sohrabi Y, Svobodová M, Demant P, Lipoldová M. Genetics of host response to Leishmania tropica in mice-different control of skin pathology, chemokine reaction, and invasion into spleen and liver. PLoS Negl Trop Dis 2012, 6:e1667. 10.1371/journal.pntd.0001667, 3367980, 22679519.
19. Fijneman RJ, de Vries SS, Jansen RC, Demant P. Complex interactions of new quantitative trait loci, Sluc1, Sluc2, Sluc3, and Sluc4, that influence the susceptibility to lung cancer in the mouse. Nat Genet 1996, 14:465-467. 10.1038/ng1296-465, 8944028.
20. van Wezel T, Stassen AP, Moen CJ, Hart AA, van der Valk MA, Demant P. Gene interaction and single gene effects in colon tumour susceptibility in mice. Nat Genet 1996, 14:468-470.
21. Ruivenkamp CA, van Wezel T, Zanon C, Stassen AP, Vlcek C, Csikós T, Klous AM, Tripodis N, Perrakis A, Boerrigter L, Groot PC, Lindeman J, Mooi WJ, Meijjer GA, Scholten G, Dauwerse H, Paces V, van Zandwijk N, van Ommen GJ, Demant P. Ptprj is a candidate for the mouse colon-cancer susceptibility locus Scc1 and is frequently deleted in human cancers. Nat Genet 2002, 31:295-300. 10.1038/ng903, 12089527.
22. Lipoldová M, Havelková H, Badalová J, Demant P. Novel loci controlling lymphocyte proliferative response to cytokines and their clustering with loci controlling autoimmune reactions, macrophage function and lung tumor susceptibility. Int J Cancer 2005, 114:394-399. 10.1002/ijc.20731, 15551356.
23. Lipoldová M, Havelková H, Badalova J, Vojtísková J, Quan L, Krulova M, Sohrabi Y, Stassen AP, Demant P. Loci controlling lymphocyte production of interferon γ after alloantigen stimulation in vitro and their co-localization with genes controlling lymphocyte infiltration of tumors and tumor susceptibility. Cancer Immunol Immunother 2010, 59:203-213. 10.1007/s00262-009-0739-y, 2776939, 19655140.
24. Rey FA, Heinz FX, Mandl C, Kunz C, Harrison SC. The envelope glycoprotein from tick-borne encephalitis virus at 2 A resolution. Nature 1995, 375:291-298. 10.1038/375291a0, 7753193.
25. De Madrid AT, Porterfield JS. A simple micro-culture method for the study of group B arboviruses. Bull World Health Organ 1969, 40:113-121. 2554446, 4183812.
26. Růžek D, Salát J, Singh SK, Kopecký J. Breakdown of the blood-brain barrier during tick-borne encephalitis in mice is not dependent on CD8+ T-cells. PLoS One 2011, 6:e20472. 10.1371/journal.pone.0020472, 3100324, 21629771.
27. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408. 10.1006/meth.2001.1262, 11846609.
28. Bárdoš V, Sixl W, Wisidagama CL, Halouzka J, Stünzner D, Hubálek Z, Withalm H. Prevalence of arbovirus antibodies in sera of animals in Sri Lanka. Bull World Health Organ 1983, 61:987-990. 2536247, 6609014.
29. Clark DC, Brault AC, Hunsperger E. The contribution of rodent models to the pathological assessment of flaviviral infections of the central nervous system. Arch Virol 2012, 157:1423-1440. 10.1007/s00705-012-1337-4, 22592957.
30. Kyuwa S, Yamaguchi K, Toyoda Y, Fujiwara K, Hilgers J. Acute and late disease induced by murine coronavirus, strain JHM, in a series of recombinant inbred strains between BALB/cHeA and STS/A mice. Microb Pathog 1992, 12:95-104. 10.1016/0882-4010(92)90112-2, 1316530.
31. Šíma M, Havelková H, Quan L, Svobodová M, Jarosíková T, Vojtíšková J, Stassen AP, Demant P, Lipoldová M. Genetic control of resistance to Trypanosoma brucei brucei infection in mice. PLoS Negl Trop Dis 2011, 5:e1173. 10.1371/journal.pntd.0001173, 3110168, 21666791.
32. Lipoldová M, Svobodová M, Havelková H, Krulová M, Badalová J, Nohýnková E, Hart AA, Schlegel D, Volf P, Demant P. Mouse genetic model for clinical and immunological heterogeneity of leishmaniasis. Immunogenetics 2002, 54:174-183. 10.1007/s00251-002-0439-7, 12073146.
33. Brown AN, Kent KA, Bennett CJ, Bernard KA. Tissue tropism and neuroinvasion of West Nile virus do not differ for two mouse strains with different survival rates. Virology 2007, 368:422-430. 10.1016/j.virol.2007.06.033, 2814419, 17675128.
34. Bréhin AC, Mouriès J, Frenkiel MP, Dadaglio G, Desprès P, Lafon M, Couderc T. Dynamics of immune cell recruitment during West Nile encephalitis and identification of a new CD19 + B220-BST-2+ leukocyte population. J Immunol 2008, 180:6760-6767.
35. 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, 57:973-989. 10.1369/jhc.2009.954180, 2746730, 19581627.
36. King NJC, Van Vreden C, Terry RL, Getts DR, Yeung AWS, Teague Getts M, Davison AM, Deffrasnes C, Munoz Erazo L. The immunopathogenesis of neurotropic flavivirus infection. Flavivirus Encephalitis 2011, 25-52. Rijeka: Intech, Růžek D, 1.
37. Bardina SV, Lim JK. The role of chemokines in the pathogenesis of neurotropic flaviviruses. Immunol Res 2012, 54:121-132. 10.1007/s12026-012-8333-3, 22547394.
38. Diamond MS, Shrestha B, Marri A, Mahan D, Engle M. B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol 2003, 77:2578-2586. 10.1128/JVI.77.4.2578-2586.2003, 141119, 12551996.
39. Biswas SM, Kar S, Singh R, Chakraborty D, Vipat V, Raut CG, Mishra AC, Gore MM, Ghosh D. Immunomodulatory cytokines determine the outcome of Japanese encephalitis virus infection in mice. J Med Virol 2010, 82:304-310. 10.1002/jmv.21688, 20029807.
40. Wang K, Deubel V. Mice with different susceptibility to Japanese encephalitis virus infection show selective neutralizing antibody response and myeloid cell infectivity. PLoS One 2011, 6:e24744. 10.1371/journal.pone.0024744, 3174963, 21949747.
41. Shirato K, Kimura T, Mizutani T, Kariwa H, Takashima I. Different chemokine expression in lethal and non-lethal murine West Nile virus infection. J Med Virol 2004, 74:507-513. 10.1002/jmv.20205, 15368509.
42. Tigabu B, Juelich T, Holbrook MR. Comparative analysis of immune responses to Russian spring-summer encephalitis and Omsk hemorrhagic fever viruses in mouse models. Virology 2010, 408:57-63. 10.1016/j.virol.2010.08.021, 2966520, 20875909.
43. Ng LF, Chow A, Sun YJ, Kwek DJ, Lim PL, Dimatatac F, Ng LC, Ooi EE, Choo KH, Her Z, Kourilsky P, Leo YS. IL-1beta, IL-6, and RANTES as biomarkers of Chikungunya severity. PLoS One 2009, 4:e4261. 10.1371/journal.pone.0004261, 2625438, 19156204.
44. Getts DR, Terry RL, Getts MT, Müller M, Rana S, Shrestha B, Radford J, Van Rooijen N, Campbell IL, King NJ. Ly6c + "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J Exp Med 2008, 205:2319-2337. 10.1084/jem.20080421, 2556789, 18779347.
45. Sui Y, Stehno-Bittel L, Li S, Loganathan R, Dhillon NK, Pinson D, Nath A, Kolson D, Narayan O, Buch S. CXCL10-induced cell death in neurons: role of calcium dysregulation. Eur J Neurosci 2006, 23:957-964. 10.1111/j.1460-9568.2006.04631.x, 16519660.
46. Zajkowska J, Moniuszko-Malinowska A, Pancewicz SA, Muszyńska-Mazur A, Kondrusik M, Grygorczuk S, Swierzbińska-Pijanowska R, Dunaj J, Czupryna P. Evaluation of CXCL10, CXCL11, CXCL12 and CXCL13 chemokines in serum and cerebrospinal fluid in patients with tick borne encephalitis (TBE). Adv Med Sci 2011, 56:311-317.
47. Lepej SZ, Misić-Majerus L, Jeren T, Rode OD, Remenar A, Sporec V, Vince A. Chemokines CXCL10 and CXCL11 in the cerebrospinal fluid of patients with tick-borne encephalitis. Acta Neurol Scand 2007, 115:109-114. 10.1111/j.1600-0404.2006.00726.x, 17212614.
48. Klein RS, Lin E, Zhang B, Luster AD, Tollett J, Samuel MA, Engle M, Diamond MS. Neuronal CXCL10 directs CD8+ T-cell recruitment and control of West Nile virus encephalitis. J Virol 2005, 79:11457-11466. 10.1128/JVI.79.17.11457-11466.2005, 1193600, 16103196.
49. Sasseville VG, Smith MM, Mackay CR, Pauley DR, Mansfield KG, Ringler DJ, Lackner AA. Chemokine expression in simian immunodeficiency virus-induced AIDS encephalitis. Am J Pathol 1996, 149:1459-1467. 1865261, 8909235.
50. Westmoreland SV, Rottman JB, Williams KC, Lackner AA, Sasseville VG. Chemokine receptor expression on resident and inflammatory cells in the brain of macaques with simian immunodeficiency virus encephalitis. Am J Pathol 1998, 152:659-665. 1858400, 9502406.
51. Sui Y, Potula R, Dhillon N, Pinson D, Li S, Nath A, Anderson C, Turchan J, Kolson D, Narayan O, Buch S. Neuronal apoptosis is mediated by CXCL10 overexpression in simian human immunodeficiency virus encephalitis. Am J Pathol 2004, 164:1557-1566. 10.1016/S0002-9440(10)63714-5, 1615658, 15111302.
52. Bender A, Jäger 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, 251:353-354. 10.1007/s00415-004-0329-z, 15015020.