Skip to main content

Advertisement

SpringerLink
Log in

The contribution of rodent models to the pathological assessment of flaviviral infections of the central nervous system

  • Brief Review
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Members of the genus Flavivirus are responsible for a spectrum of important neurological syndromes in humans and animals. Rodent models have been used extensively to model flavivirus neurological disease, to discover host-pathogen interactions that influence disease outcome, and as surrogates to determine the efficacy and safety of vaccines and therapeutics. In this review, we discuss the current understanding of flavivirus neuroinvasive disease and outline the host, viral and experimental factors that influence the outcome and reliability of virus infection of small-animal models.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Agamanolis DP, Leslie MJ, Caveny EA, Guarner J, Shieh WJ, Zaki SR (2003) Neuropathological findings in West Nile virus encephalitis: a case report. Ann Neurol 54:547–551

    Article  PubMed  Google Scholar 

  2. Andersen AA, Hanson RP (1974) Influence of sex and age on natural resistance to St. Louis encephalitis virus infection in mice. Infect Immun 9:1123–1125

    PubMed  CAS  Google Scholar 

  3. Anderson SG (1954) Murray Valley encephalitis and Australian X disease. J Hyg 52:447–468

    Article  CAS  Google Scholar 

  4. Andrews DM, Matthews VB, Sammels LM, Carrello AC, McMinn PC (1999) The severity of Murray valley encephalitis in mice is linked to neutrophil infiltration and inducible nitric oxide synthase activity in the central nervous system. J Virol 73:8781–8790

    PubMed  CAS  Google Scholar 

  5. Anthony D, Dempster R, Fearn S, Clements J, Wells G, Perry VH, Walker K (1998) CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood–brain barrier breakdown. Curr Biol 8:923–926

    Article  PubMed  CAS  Google Scholar 

  6. Armah HB, Wang G, Omalu BI, Tesh RB, Gyure KA, Chute DJ, Smith RD, Dulai P, Vinters HV, Kleinschmidt-DeMasters BK, Wiley CA (2007) Systemic distribution of West Nile virus infection: postmortem immunohistochemical study of six cases. Brain Pathol 17:354–362

    Article  PubMed  Google Scholar 

  7. Avirutnan P, Hauhart RE, Somnuke P, Blom AM, Diamond MS, Atkinson JP (2011) Binding of flavivirus nonstructural protein NS1 to C4b binding protein modulates complement activation. J Immunol

  8. Bai F, Kong KF, Dai J, Qian F, Zhang L, Brown CR, Fikrig E, Montgomery RR (2010) A paradoxical role for neutrophils in the pathogenesis of West Nile virus. J Infect Dis 202:1804–1812

    Article  PubMed  CAS  Google Scholar 

  9. Bakonyi T, Hubalek Z, Rudolf I, Nowotny N (2005) Novel flavivirus or new lineage of West Nile virus, central Europe. Emerg Infect Dis 11:225–231

    Article  PubMed  CAS  Google Scholar 

  10. Balakrishnan A, Mishra AC (2008) Immune response during acute Chandipura viral infection in experimentally infected susceptible mice. Virol J 5:121

    Article  PubMed  CAS  Google Scholar 

  11. Barkhash AV, Perelygin AA, Babenko VN, Myasnikova NG, Pilipenko PI, Romaschenko AG, Voevoda MI, Brinton MA (2010) Variability in the 2’-5’-oligoadenylate synthetase gene cluster is associated with human predisposition to tick-borne encephalitis virus-induced disease. J Infect Dis 202:1813–1818

    Article  PubMed  CAS  Google Scholar 

  12. Beasley DW, Li L, Suderman MT, Barrett AD (2002) Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 296:17–23

    Article  PubMed  CAS  Google Scholar 

  13. Beasley DW, Davis CT, Whiteman M, Granwehr B, Kinney RM, Barrett AD (2004) Molecular determinants of virulence of West Nile virus in North America. Arch Virol Suppl 35–41

  14. Bode AV, Sejvar JJ, Pape WJ, Campbell GL, Marfin AA (2006) West Nile virus disease: a descriptive study of 228 patients hospitalized in a 4-county region of Colorado in 2003. Clin Infect Dis 42:1234–1240

    Article  PubMed  Google Scholar 

  15. Bondre VP, Jadi RS, Mishra AC, Yergolkar PN, Arankalle VA (2007) West Nile virus isolates from India: evidence for a distinct genetic lineage. J Gen Virol 88:875–884

    Article  PubMed  CAS  Google Scholar 

  16. Bosco-Lauth A, Mason G, Bowen R (2011) Pathogenesis of Japanese encephalitis virus infection in a golden hamster model and evaluation of flavivirus cross-protective immunity. Am J Trop Med Hyg 84:727–732

    Article  PubMed  Google Scholar 

  17. Botha EM, Markotter W, Wolfaardt M, Paweska JT, Swanepoel R, Palacios G, Nel LH, Venter M (2008) Genetic determinants of virulence in pathogenic lineage 2 West Nile virus strains. Emerg Infect Dis 14:222–230

    Article  PubMed  Google Scholar 

  18. Brault AC, Huang CY, Langevin SA, Kinney RM, Bowen RA, Ramey WN, Panella NA, Holmes EC, Powers AM, Miller BR (2007) A single positively selected West Nile viral mutation confers increased virogenesis in American crows. Nat Genet 39:1162–1166

    Article  PubMed  CAS  Google Scholar 

  19. Brien JD, Uhrlaub JL, Hirsch A, Wiley CA, Nikolich-Zugich J (2009) Key role of T cell defects in age-related vulnerability to West Nile virus. J Exp Med 206:2735–2745

    Article  PubMed  CAS  Google Scholar 

  20. Brinker KR, Monath TP (1980) The acute disease. In: Monath TP (ed) St Louis encephalitis. American Public Health Association, Washington, DC, pp 503–534

    Google Scholar 

  21. Brinton MA, Perelygin AA (2003) Genetic resistance to flaviviruses. Adv Virus Res 60:43–85

    Article  PubMed  CAS  Google Scholar 

  22. Calisher CH, Karabatsos N, Dalrymple JM, Shope RE, Porterfield JS, Westaway EG, Brandt WE (1989) Antigenic relationships between flaviviruses as determined by cross-neutralization tests with polyclonal antisera. J Gen Virol 70(Pt 1):37–43

    Article  PubMed  Google Scholar 

  23. Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ (2002) West Nile virus. Lancet Infect Dis 2:519–529

    Article  PubMed  Google Scholar 

  24. Cavrini F GP, Longo G, Pierro AM, Rossini G, Bonilauri P, Pasetto A, Girardis M, Dottori M, Landini M P, Sambri V (2009) Usutu virus infection in a patient who underwent orthotropic live transplantation, Italy, August–September 2009. Eurosurveillance 14

  25. Cerna F, Mehrad B, Luby JP, Burns D, Fleckenstein JL (1999) St. Louis encephalitis and the substantia nigra: MR imaging evaluation. AJNR Am J Neuroradiol 20:1281–1283

    PubMed  CAS  Google Scholar 

  26. Chandler LJ, Parsons R, Randle Y (2001) Multiple genotypes of St. Louis encephalitis virus (Flaviviridae: Flavivirus) circulate in Harris County, Texas. Am J Trop Med Hyg 64:12–19

    PubMed  CAS  Google Scholar 

  27. Chen CJ, Ou YC, Lin SY, Raung SL, Liao SL, Lai CY, Chen SY, Chen JH (2010) Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J Gen Virol 91:1028–1037

    Article  PubMed  CAS  Google Scholar 

  28. Chen WH, Kao YF, Liu JS (2005) An increase of blood anti-beta2-glycoprotein I antibody in Japanese encephalitis associated with cerebral ischemia. Blood Coagul Fibrinolysis Int J Haemost Thromb 16:55–59

    Article  CAS  Google Scholar 

  29. Cho HJ, Kim S, Kwak SE, Kang TC, Kim HS, Kwon HJ, Kim YW, Kim YS, Choi EK, Song MJ (2009) Age-dependent pathogenesis of murine gammaherpesvirus 68 infection of the central nervous system. Mol Cells 27:105–111

    Article  PubMed  CAS  Google Scholar 

  30. Daffis S, Samuel MA, Suthar MS, Gale M Jr, Diamond MS (2008) Toll-like receptor 3 has a protective role against West Nile virus infection. J Virol 82:10349–10358

    Article  PubMed  CAS  Google Scholar 

  31. Davis CW, Nguyen HY, Hanna SL, Sanchez MD, Doms RW, Pierson TC (2006) West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J Virol 80:1290–1301

    Article  PubMed  CAS  Google Scholar 

  32. Davis LE, DeBiasi R, Goade DE, Haaland KY, Harrington JA, Harnar JB, Pergam SA, King MK, DeMasters BK, Tyler KL (2006) West Nile virus neuroinvasive disease. Ann Neurol 60:286–300

    Article  PubMed  Google Scholar 

  33. Day JF, Curtis GA (1989) Influence of rainfall on Culex nigripalpus (Diptera: Culicidae) blood-feeding behavior in Indian River Country, Florida. Ann Entomol Soc Am 82:32–37

    Google Scholar 

  34. De Groot AS, Saint-Aubin C, Bosma A, Sbai H, Rayner J, Martin W (2001) Rapid determination of HLA B*07 ligands from the West Nile virus NY99 genome. Emerg Infect Dis 7:706–713

    PubMed  Google Scholar 

  35. Depoortere E, Kavle J, Keus K, Zeller H, Murri S, Legros D (2004) Outbreak of West Nile virus causing severe neurological involvement in children, Nuba Mountains, Sudan, 2002. Trop Med Int Health 9:730–736

    Article  PubMed  Google Scholar 

  36. Desai A, Ravi V, Guru SC, Shankar SK, Kaliaperumal VG, Chandramuki A, Gourie-Devi M (1994) Detection of autoantibodies to neural antigens in the CSF of Japanese encephalitis patients and correlation of findings with the outcome. J Neurol Sci 122:109–116

    Article  PubMed  CAS  Google Scholar 

  37. Desai A, Shankar SK, Ravi V, Chandramuki A, Gourie-Devi M (1995) Japanese encephalitis virus antigen in the human brain and its topographic distribution. Acta Neuropathol 89:368–373

    Article  PubMed  CAS  Google Scholar 

  38. Dickerson RB, Newton JR, Hansen JE (1952) Diagnosis and immediate prognosis of Japanese B encephalitis; observations based on more than 200 patients with detailed analysis of 65 serologically confirmed cases. Am J Med 12:277–288

    Article  PubMed  CAS  Google Scholar 

  39. Dropulic B, Masters CL (1990) Entry of neurotropic arboviruses into the central nervous system: an in vitro study using mouse brain endothelium. J Infect Dis 161:685–691

    Article  PubMed  CAS  Google Scholar 

  40. Dumpis U, Crook D, Oksi J (1999) Tick-borne encephalitis. Clin Infect Dis 28:882–890

    Article  PubMed  CAS  Google Scholar 

  41. Ek CJ, Dziegielewska KM, Stolp H, Saunders NR (2006) Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 496:13–26

    Article  PubMed  CAS  Google Scholar 

  42. Eldadah AH, Nathanson N, Sarsitis R (1967) Pathogenesis of West Nile Virus encephalitis in mice and rats. 1. Influence of age and species on mortality and infection. Am J Epidemiol 86:765–775

    PubMed  CAS  Google Scholar 

  43. Engle MJ, Diamond MS (2003) Antibody prophylaxis and therapy against West Nile virus infection in wild-type and immunodeficient mice. J Virol 77:12941–12949

    Article  PubMed  CAS  Google Scholar 

  44. Evans IA, Hueston L, Doggett SL (2009) Murray Valley encephalitis virus. N S W Public Health Bull 20:195–196

    Article  PubMed  Google Scholar 

  45. Firth AE, Atkins JF (2009) A conserved predicted pseudoknot in the NS2A-encoding sequence of West Nile and Japanese encephalitis flaviviruses suggests NS1’ may derive from ribosomal frameshifting. Virol J 6:14

    Article  PubMed  CAS  Google Scholar 

  46. Firth AE, Blitvich BJ, Wills NM, Miller CL, Atkins JF (2010) Evidence for ribosomal frameshifting and a novel overlapping gene in the genomes of insect-specific flaviviruses. Virology 399:153–166

    Article  PubMed  CAS  Google Scholar 

  47. French EL (1952) Murray Valley encephalitis: isolation and characterisation of the aetiological agent. Med J Aust 1:100–103

    PubMed  CAS  Google Scholar 

  48. French EL, Anderson SG, Price AVG, Rhodes FA (1957) Murray Valley encephalitis in New Guinea I. Isolation of Murray Valley encephalitis virus from the brain of a fatal case of encephalitis occurring in a Papuan native. Am J Trop Med Hyg 6

  49. Gardner JJ, Reyes MG (1980) Pathology. In: Monath TP (ed) St Louis encephalitis. American Public Health Association, Washington, DC, pp 551–569

    Google Scholar 

  50. Gelpi E, Preusser M, Laggner U, Garzuly F, Holzmann H, Heinz FX, Budka H (2006) Inflammatory response in human tick-borne encephalitis: analysis of postmortem brain tissue. J Neurovirol 12:322–327

    Article  PubMed  CAS  Google Scholar 

  51. German AC, Myint KS, Mai NT, Pomeroy I, Phu NH, Tzartos J, Winter P, Collett J, Farrar J, Barrett A, Kipar A, Esiri MM, Solomon T (2006) A preliminary neuropathological study of Japanese encephalitis in humans and a mouse model. Trans R Soc Trop Med Hyg 100:1135–1145

    Article  PubMed  Google Scholar 

  52. Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM (2005) Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 202:1087–1098

    Article  PubMed  CAS  Google Scholar 

  53. Glass WG, McDermott DH, Lim JK, Lekhong S, Yu SF, Frank WA, Pape J, Cheshier RC, Murphy PM (2006) CCR5 deficiency increases risk of symptomatic West Nile virus infection. J Exp Med 203:35–40

    Article  PubMed  CAS  Google Scholar 

  54. Granwehr BP, Lillibridge KM, Higgs S, Mason PW, Aronson JF, Campbell GA, Barrett AD (2004) West Nile virus: where are we now? Lancet Infect Dis 4:547–556

    Article  PubMed  Google Scholar 

  55. 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. Proc Soc Exp Biol Med 123:118–124

    PubMed  CAS  Google Scholar 

  56. Guarner J, Shieh WJ, Hunter S, Paddock CD, Morken T, Campbell GL, Marfin AA, Zaki SR (2004) Clinicopathologic study and laboratory diagnosis of 23 cases with West Nile virus encephalomyelitis. Hum Pathol 35:983–990

    Article  PubMed  Google Scholar 

  57. Hase T, Dubois DR, Summers PL (1990) Comparative study of mouse brains infected with Japanese encephalitis virus by intracerebral or intraperitoneal inoculation. Int J Exp Pathol 71:857–869

    PubMed  CAS  Google Scholar 

  58. Heinz FX, Stiasny K, Allison SL (2004) The entry machinery of flaviviruses. Arch Virol Suppl 133–137

  59. Hirsch MS, Zisman B, Allison AC (1970) Macrophages and age-dependent resistance to Herpes simplex virus in mice. J Immunol 104:1160–1165

    PubMed  CAS  Google Scholar 

  60. Hollidge BS, González-Scarano F, Soldan SS (2010) Arboviral encephalitides: transmission, emergence, and pathogenesis. J Neuroimmune Pharmacol 5:428–442

    Article  PubMed  Google Scholar 

  61. Hovanessian AG, Justesen J (2007) The human 2’-5’oligoadenylate synthetase family: unique interferon-inducible enzymes catalyzing 2’-5’ instead of 3’-5’ phosphodiester bond formation. Biochimie 89:779–788

    Article  PubMed  CAS  Google Scholar 

  62. Hunsperger EA, Roehrig JT (2006) Temporal analyses of the neuropathogenesis of a West Nile virus infection in mice. J Neurovirol 12:129–139

    Article  PubMed  CAS  Google Scholar 

  63. Johnson RT, Burke DS, Elwell M, Leake CJ, Nisalak A, Hoke CH, Lorsomrudee W (1985) Japanese encephalitis: immunocytochemical studies of viral antigen and inflammatory cells in fatal cases. Ann Neurol 18:567–573

    Article  PubMed  CAS  Google Scholar 

  64. Jones SC, Morris J, Hill G, Alderman M, Ratard RC (2002) St. Louis encephalitis outbreak in Louisiana in 2001. J La State Med Soc 154:303–306

    PubMed  Google Scholar 

  65. Justesen J, Hartmann R, Kjeldgaard NO (2000) Gene structure and function of the 2’-5’-oligoadenylate synthetase family. Cell Mol Life Sci 57:1593–1612

    Article  PubMed  CAS  Google Scholar 

  66. Kim S, Li L, McMurtrey CP, Hildebrand WH, Weidanz JA, Gillanders WE, Diamond MS, Hansen TH (2010) Single-chain HLA-A2 MHC trimers that incorporate an immundominant peptide elicit protective T cell immunity against lethal West Nile virus infection. J Immunol 184:4423–4430

    Article  PubMed  CAS  Google Scholar 

  67. Kimoto T, Yamada T, Ueba N, Kunita N, Kawai A (1968) Laboratory diagnosis of Japanese encephalitis. Comparison of the fluorescent antibody technique with virus isolation and serologic tests. Biken J 11:157–168

    PubMed  CAS  Google Scholar 

  68. Kindberg E, Mickiene A, Ax C, Akerlind B, Vene S, Lindquist L, Lundkvist A, Svensson L (2008) A deletion in the chemokine receptor 5 (CCR5) gene is associated with tickborne encephalitis. J Infect Dis 197:266–269

    Article  PubMed  CAS  Google Scholar 

  69. Kindberg E, Vene S, Mickiene A, Lundkvist A, Lindquist L, Svensson L (2011) A functional Toll-like receptor 3 gene (TLR3) may be a risk factor for tick-borne encephalitis virus (TBEV) infection. J Infect Dis 203:523–528

    Article  PubMed  CAS  Google Scholar 

  70. Kleinschmidt-DeMasters BK, Marder BA, Levi ME, Laird SP, McNutt JT, Escott EJ, Everson GT, Tyler KL (2004) Naturally acquired West Nile virus encephalomyelitis in transplant recipients: clinical, laboratory, diagnostic, and neuropathological features. Arch Neurol 61:1210–1220

    Article  PubMed  CAS  Google Scholar 

  71. Kong KF, Delroux K, Wang X, Qian F, Arjona A, Malawista SE, Fikrig E, Montgomery RR (2008) Dysregulation of TLR3 Impairs the Innate Immune Response to West Nile Virus in the Elderly. J Virol 82:7613–7623

    Article  PubMed  CAS  Google Scholar 

  72. Kreil TR, Eibl MM (1996) 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 219:304–306

    Article  PubMed  CAS  Google Scholar 

  73. Krisztalovics K, Ferenczi E, Molnar Z, Csohan A, Ban E, Zoldi V, Kaszas K (2008) West Nile virus infections in Hungary, August-September 2008. Eurosurveillance 13:pii: 19030

  74. Kunz C (2003) TBE vaccination and the Austrian experience. Vaccine 21(Suppl 1):S50–S55

    Article  PubMed  Google Scholar 

  75. Kutasi O, Bakonyi T, Lecollinet S, Biksi I, Ferenczi E, Bahuon C, Sardi S, Zientara S, Szenci O (2011) Equine encephalomyelitis outbreak caused by a genetic lineage 2 West Nile Virus in Hungary. J Vet Intern Med 25(3):586–591

    Google Scholar 

  76. Lanteri MC, Kaidarova Z, Peterson T, Cate S, Custer B, Wu S, Agapova M, Law JP, Bielawny T, Plummer F, Tobler LH, Loeb M, Busch MP, Bramson J, Luo M, Norris PJ (2011) Association between HLA Class I and Class II alleles and the outcome of West Nile virus infection: an exploratory study. PLoS One 6:e22948

    Article  PubMed  CAS  Google Scholar 

  77. Latham PS, Sepelak SB, Pifat DY, Smith JF (1991) Role of hepatocytes and Kupffer cells in age-dependent murine hepatitis caused by a phlebovirus, Punta Toro. J Med Virol 33:10–18

    Article  PubMed  CAS  Google Scholar 

  78. Liao CL, Lin YL, Wang JJ, Huang YL, Yeh CT, Ma SH, Chen LK (1997) Effect of enforced expression of human bcl-2 on Japanese encephalitis virus-induced apoptosis in cultured cells. J Virol 71:5963–5971

    PubMed  CAS  Google Scholar 

  79. Licon Luna RM, Lee E, Mullbacher A, Blanden RV, Langman R, Lobigs M (2002) Lack of both Fas ligand and perforin protects from flavivirus-mediated encephalitis in mice. J Virol 76:3202–3211

    Article  PubMed  CAS  Google Scholar 

  80. Lim JK, Lisco A, McDermott DH, Huynh L, Ward JM, Johnson B, Johnson H, Pape J, Foster GA, Krysztof D, Follmann D, Stramer SL, Margolis LB, Murphy PM (2009) Genetic variation in OAS1 is a risk factor for initial infection with West Nile virus in man. PLoS Pathog 5:e1000321

    Article  PubMed  CAS  Google Scholar 

  81. Lim JK, McDermott DH, Lisco A, Foster GA, Krysztof D, Follmann D, Stramer SL, Murphy PM (2009) CCR5 deficiency is a risk factor for early clinical manifestations of West Nile virus infection but not for viral transmission. J Infect Dis 201:178–185

    Article  CAS  Google Scholar 

  82. Lim JK, McDermott DH, Lisco A, Foster GA, Krysztof D, Follmann D, Stramer SL, Murphy PM (2010) CCR5 deficiency is a risk factor for early clinical manifestations of West Nile virus infection but not for viral transmission. J Infect Dis 201:178–185

    Article  PubMed  CAS  Google Scholar 

  83. Lim JK, Obara CJ, Rivollier A, Pletnev AG, Kelsall BL, Murphy PM (2011) Chemokine receptor Ccr2 is critical for monocyte accumulation and survival in West Nile virus encephalitis. J Immunol 186:471–478

    Article  PubMed  CAS  Google Scholar 

  84. Lindquist L, Vapalahti O (2008) Tick-borne encephalitis. Lancet 371:1861–1871

    Article  PubMed  Google Scholar 

  85. Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5:133–139

    Article  PubMed  CAS  Google Scholar 

  86. Liou ML, Hsu CY (1998) Japanese encephalitis virus is transported across the cerebral blood vessels by endocytosis in mouse brain. Cell Tissue Res 293:389–394

    Article  PubMed  CAS  Google Scholar 

  87. Luby JP, Sulkin SE, Sanford JP (1969) The epidemiology of St. Louis encephalitis: a review. Annu Rev Med 20:329–350

    Article  PubMed  CAS  Google Scholar 

  88. Lucas M, Mashimo T, Frenkiel MP, Simon-Chazottes D, Montagutelli X, Ceccaldi PE, Guenet JL, Despres P (2003) Infection of mouse neurones by West Nile virus is modulated by the interferon-inducible 2’-5’ oligoadenylate synthetase 1b protein. Immunol Cell Biol 81:230–236

    Article  PubMed  CAS  Google Scholar 

  89. Lumsden LL (1958) St. Louis encephalitis in 1933; observations on epidemiological features. Public Health Rep 73:340–353

    Article  PubMed  CAS  Google Scholar 

  90. Lustig S, Jackson AC, Hahn CS, Griffin DE, Strauss EG, Strauss JH (1988) Molecular basis of Sindbis virus neurovirulence in mice. J Virol 62:2329–2336

    PubMed  CAS  Google Scholar 

  91. Lynch CJ, Hughes TP (1936) The inheritance of susceptibility to yellow fever encephalitis in mice. Genetics 21:104–112

    PubMed  CAS  Google Scholar 

  92. Mackenzie JS, Broom AK (1995) Australian X disease, Murray Valley encephalitis and the French connection. [Review] [49 refs]. Vet Microbiol 46:79–90

    Article  PubMed  CAS  Google Scholar 

  93. Mackenzie JS, Williams DT (2009) The zoonotic flaviviruses of Southern, South-Eastern and Eastern Asia, and Australasia: the potential for emergent viruses. Zoonoses Public Health 56:338–356

    Article  PubMed  CAS  Google Scholar 

  94. Martina BE, Koraka P, van den Doel P, Rimmelzwaan GF, Haagmans BL, Osterhaus AD (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-alpha and TNF-alpha. Virus Res

  95. Mateo R, Xiao SY, Guzman H, Lei H, Da Rosa AP, Tesh RB (2006) Effects of immunosuppression on West Nile virus infection in hamsters. Am J Trop Med Hyg 75:356–362

    PubMed  Google Scholar 

  96. Matsuo S, Morita K, Bundo-Morita K, Igarashi A (1994) Differences in susceptibility to peripheral infection with Japanese encephalitis virus among inbred strains of mouse. Uirusu 44:205–215

    Article  PubMed  CAS  Google Scholar 

  97. May FJ, Davis CT, Tesh RB, Barrett AD (2010) Phylogeography of West Nile virus: from the cradle of evolution in Africa to Eurasia, Australia and the Americas. J Virol

  98. McMinn PC, Dalgarno L, Weir RC (1996) A comparison of the spread of Murray Valley encephalitis viruses of high or low neuroinvasiveness in the tissues of Swiss mice after peripheral inoculation. Virology 220:414–423

    Article  PubMed  CAS  Google Scholar 

  99. Meehan PJ, Wells DL, Paul W, Buff E, Lewis A, Muth D, Hopkins R, Karabatsos N, Tsai TF (2000) Epidemiological features of and public health response to a St. Louis encephalitis epidemic in Florida, 1990-1. Epidemiol Infect 125:181–188

    Article  PubMed  CAS  Google Scholar 

  100. Mehlhop E, Whitby K, Oliphant T, Marri A, Engle M, Diamond MS (2005) Complement activation is required for induction of a protective antibody response against West Nile virus infection. J Virol 79:7466–7477

    Article  PubMed  CAS  Google Scholar 

  101. Melian EB, Hinzman E, Nagasaki T, Firth AE, Wills NM, Nouwens AS, Blitvich BJ, Leung J, Funk A, Atkins JF, Hall R, Khromykh AA (2010) NS1’ of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J Virol 84:1641–1647

    Article  PubMed  CAS  Google Scholar 

  102. Misra UK, Kalita J (2010) Overview: Japanese encephalitis. Prog Neurobiol 91:108–120

    Article  PubMed  CAS  Google Scholar 

  103. Miura K, Goto N, Suzuki H, Fujisaki Y (1988) Strain difference of mouse in susceptibility to Japanese encephalitis virus infection. Jikken Dobutsu Exp Anim 37:365–373

    CAS  Google Scholar 

  104. Miyake M (1964) The pathology of Japanese encephalitis. a review. Bull World Health Organ 30:153–160

    PubMed  CAS  Google Scholar 

  105. Monath TP (1980) Epidemiology. In: Monath TP (ed) St Louis encephalitis. American Public Health Association, Washington, DC, pp 239–312

    Google Scholar 

  106. Monath TP, Cropp CB, Harrison AK (1983) Mode of entry of a neurotropic arbovirus into the central nervous system. Reinvestigation of an old controversy. Lab Invest J Tech Methods Pathol 48:399–410

    CAS  Google Scholar 

  107. Monath TP, Tsai TF (1987) St. Louis encephalitis: lessons from the last decade. Am J Trop Med Hyg 37:40S–59S

    PubMed  CAS  Google Scholar 

  108. Moos T, Mollgard K (1993) Cerebrovascular permeability to azo dyes and plasma proteins in rodents of different ages. Neuropathol Appl Neurobiol 19:120–127

    Article  PubMed  CAS  Google Scholar 

  109. Morahan G, Balmer L, Monley D (2008) Establishment of “The Gene Mine”: a resource for rapid identification of complex trait genes. Mamm Genome 19:390–393

    Article  PubMed  Google Scholar 

  110. Morrey JD, Day CW, Julander JG, Olsen AL, Sidwell RW, Cheney CD, Blatt LM (2004) Modeling hamsters for evaluating West Nile virus therapies. Antiviral Res 63:41–50

    Article  PubMed  CAS  Google Scholar 

  111. Morrey JD, Olsen AL, Siddharthan V, Motter NE, Wang H, Taro BS, Chen D, Ruffner D, Hall JO (2008) Increased blood brain barrier permeability is not a primary determinant for lethality of West Nile virus infection in rodents. J Gen Virol 89:467–473

    Article  PubMed  CAS  Google Scholar 

  112. Morrey JD, Siddharthan V, Wang H, Hall JO, Motter NE, Skinner RD, Skirpstunas RT (2010) Neurological suppression of diaphragm electromyographs in hamsters infected with West Nile virus. J Neurovirol

  113. Mukherji AK, Biswas SK (1976) Histopathological studies of brains (and other viscera) from cases of JE virus encephalitis during 1973 epidemic at Bankura. Indian J Med Res 64:1143–1149

    PubMed  CAS  Google Scholar 

  114. Mullbacher A, Regner M, Wang Y, Lee E, Lobigs M, Simon M (2004) Can we really learn from model pathogens? Trends Immunol 25:524–528

    Article  PubMed  CAS  Google Scholar 

  115. Murata R, Eshita Y, Maeda A, Maeda J, Akita S, Tanaka T, Yoshii K, Kariwa H, Umemura T, Takashima I (2010) Glycosylation of the West Nile virus envelope protein increases in vivo and in vitro viral multiplication in birds. Am J Trop Med Hyg 82:696–704

    Article  PubMed  CAS  Google Scholar 

  116. Murray K, Baraniuk S, Resnick M, Arafat R, Kilborn C, Cain K, Shallenberger R, York TL, Martinez D, Hellums JS, Hellums D, Malkoff M, Elgawley N, McNeely W, Khuwaja SA, Tesh RB (2006) Risk factors for encephalitis and death from West Nile virus infection. Epidemiol Infect 134:1325–1332

    Article  PubMed  CAS  Google Scholar 

  117. Myint KS, Raengsakulrach B, Young GD, Gettayacamin M, Ferguson LM, Innis BL, Hoke CH Jr, Vaughn DW (1999) Production of lethal infection that resembles fatal human disease by intranasal inoculation of macaques with Japanese encephalitis virus. Am J Trop Med Hyg 60:338–342

    PubMed  CAS  Google Scholar 

  118. Nazmi A, Dutta K, Das S, Basu A (2011) Japanese encephalitis virus-infected macrophages induce neuronal death. J Neuroimmune Pharmacol 6:420–433

    Article  PubMed  Google Scholar 

  119. Odelola HA, Oduye OO (1977) West Nile virus infection of adult mice by oral route. Arch Virol 54:251–253

    Article  PubMed  CAS  Google Scholar 

  120. Ogata A, Nagashima K, Hall WW, Ichikawa M, Kimura-Kuroda J, Yasui K (1991) Japanese encephalitis virus neurotropism is dependent on the degree of neuronal maturity. J Virol 65:880–886

    PubMed  CAS  Google Scholar 

  121. Paddock CD, Nicholson WL, Bhatnagar J, Goldsmith CS, Greer PW, Hayes EB, Risko JA, Henderson C, Blackmore CG, Lanciotti RS, Campbell GL, Zaki SR (2006) Fatal hemorrhagic fever caused by West Nile virus in the United States. Clin Infect Dis 42:1527–1535

    Article  PubMed  Google Scholar 

  122. Palmer RJ, Finley KH (1956) Sequelae of encephalitis: report of a study of a clinical follow-up in California. Calif Med 84:98–100

    PubMed  CAS  Google Scholar 

  123. Panda A, Arjona A, Sapey E, Bai F, Fikrig E, Montgomery RR, Lord JM, Shaw AC (2009) Human innate immunosenescence: causes and consequences for immunity in old age. Trends Immunol 30:325–333

    Article  PubMed  CAS  Google Scholar 

  124. Papa A, Danis K, Baka A, Bakas A, Dougas G, Lytras T, Theocharopoulos G, Chrysagis D, Vassiliadou E, Kamaria F, Liona A, Mellou K, Saroglou G, Panagiotopoulos T (2010) Ongoing outbreak of West Nile virus infections in humans in Greece, July-August 2010. Eurosurveillance 15(34)pii: 19644

    Google Scholar 

  125. Papa A (2011) Genetic characterization of West Nile Virus lineage 2, Greece, 2010. Emerg Infect Dis 17(5):920–922

    Google Scholar 

  126. Pecorari M LG, Gennari W, Grottola A, Sabbatini AM, Tagliazucchi S, Savini G, Monaco F, Simone M L, Lelli R, Rumpianesi F (2009) First human case of Usutu virus neuroinvasive infection, Italy, August–September 2009. Eurosurveillance 14

  127. Perelygin AA, Scherbik SV, Zhulin IB, Stockman BM, Li Y, Brinton MA (2002) Positional cloning of the murine flavivirus resistance gene. Proc Nat Acad Sci USA 99:9322–9327

    Article  PubMed  CAS  Google Scholar 

  128. Phillpotts RJ, Jones LD, Lukaszewski RA, Lawrie C, Brooks TJ (2003) Antibody and interleukin-12 treatment in murine models of encephalitogenic flavivirus (St. Louis encephalitis, tick-borne encephalitis) and alphavirus (Venezuelan equine encephalitis) infection. J Interf Cytokine Res 23:47–50

    Article  CAS  Google Scholar 

  129. Piazza P, McMurtrey CP, Lelic A, Cook RL, Hess R, Yablonsky E, Borowski L, Loeb MB, Bramson JL, Hildebrand WH, Rinaldo CR (2010) Surface phenotype and functionality of WNV specific T cells differ with age and disease severity. PLoS One 5:e15343

    Article  PubMed  CAS  Google Scholar 

  130. Pijlman GP, Funk A, Kondratieva N, Leung J, Torres S, van der Aa L, Liu WJ, Palmenberg AC, Shi PY, Hall RA, Khromykh AA (2008) A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579–591

    Article  PubMed  CAS  Google Scholar 

  131. Pradhan S, Gupta RK, Singh MB, Mathur A (2001) Biphasic illness pattern due to early relapse in Japanese-B virus encephalitis. J Neurol Sci 183:13–18

    Article  PubMed  CAS  Google Scholar 

  132. Prandovszky E, Horvath S, Gellert L, Kovacs SK, Janka Z, Toldi J, Shukla D, Valyi-Nagy T (2008) Nectin-1 (HveC) is expressed at high levels in neural subtypes that regulate radial migration of cortical and cerebellar neurons of the developing human and murine brain. J Neurovirol 14:164–172

    Article  PubMed  CAS  Google Scholar 

  133. Qian F, Wang X, Zhang L, Lin A, Zhao H, Fikrig E, Montgomery RR (2011) Impaired interferon signaling in dendritic cells from older donors infected in vitro with West Nile virus. J Infect Dis 203:1415–1424

    Article  PubMed  CAS  Google Scholar 

  134. Reisen WK, Milby MM, Presser SB, Hardy JL (1992) Ecology of mosquitoes and St. Louis encephalitis virus in the Los Angeles Basin of California, 1987–1990. J Med Entomol 29:582–598

    PubMed  CAS  Google Scholar 

  135. Reisen WK, Meyer RP, Presser SB, Hardy JL (1993) Effect of temperature on the transmission of western equine encephalomyelitis and St. Louis encephalitis viruses by Culex tarsalis (Diptera: Culicidae). J Med Entomol 30:151–160

    PubMed  CAS  Google Scholar 

  136. Reisen WK, Hardy JL, Lothrop HD (1995) Landscape ecology of arboviruses in southern California: patterns in the epizootic dissemination of western equine encephalomyelitis and St. Louis encephalitis viruses in Coachella Valley, 1991–1992. J Med Entomol 32:267–275

    PubMed  CAS  Google Scholar 

  137. Reisen WK (2003) Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61:139–183

    Article  PubMed  Google Scholar 

  138. Reisen WK, Thiemann T, Barker CM, Lu H, Carroll B, Fang Y, Lothrop HD (2010) Effects of warm winter temperature on the abundance and gonotrophic activity of Culex (Diptera: Culicidae) in California. J Med Entomol 47:230–237

    Article  PubMed  Google Scholar 

  139. Reyes MG, Gardner JJ, Poland JD, Monath TP (1981) St Louis encephalitis. Quantitative histologic and immunofluorescent studies. Arch Neurol 38:329–334

    Article  PubMed  CAS  Google Scholar 

  140. Ruzek D, Salat J, Palus M, Gritsun TS, Gould EA, Dykova I, Skallova A, Jelinek J, Kopecky J, Grubhoffer L (2009) CD8+ T-cells mediate immunopathology in tick-borne encephalitis. Virology 384:1–6

    Article  PubMed  CAS  Google Scholar 

  141. Samuel MA, Diamond MS (2005) Alpha/beta interferon protects against lethal West Nile virus infection by restricting cellular tropism and enhancing neuronal survival. J Virol 79:13350–13361

    Article  PubMed  CAS  Google Scholar 

  142. Samuel MA, Wang H, Siddharthan V, Morrey JD, Diamond MS (2007) Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc Nat Acad Sci USA 104:17140–17145

    Article  PubMed  CAS  Google Scholar 

  143. Samuel MA, Wang H, Siddharthan V, Morrey JD, Diamond MS (2007) Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc Natl Acad Sci USA

  144. Sangster MY, Heliams DB, MacKenzie JS, Shellam GR (1993) Genetic studies of flavivirus resistance in inbred strains derived from wild mice: evidence for a new resistance allele at the flavivirus resistance locus (Flv). J Virol 67:340–347

    PubMed  CAS  Google Scholar 

  145. Sangster MY, Urosevic N, Mansfield JP, Mackenzie JS, Shellam GR (1994) Mapping the Flv locus controlling resistance to flaviviruses on mouse chromosome 5. J Virol 68:448–452

    PubMed  CAS  Google Scholar 

  146. Saunders NR, Habgood MD, Dziegielewska KM (1999) Barrier mechanisms in the brain, II. Immature brain. Clin Exp Pharmacol Physiol 26:85–91

    Article  PubMed  CAS  Google Scholar 

  147. Sbrana E, Tonry JH, Xiao SY, da Rosa AP, Higgs S, Tesh RB (2005) Oral transmission of West Nile virus in a hamster model. Am J Trop Med Hyg 72:325–329

    PubMed  Google Scholar 

  148. Scherbik SV, Kluetzman K, Perelygin AA, Brinton MA (2007) Knock-in of the Oas1b(r) allele into a flavivirus-induced disease susceptible mouse generates the resistant phenotype. Virology 368:232–237

    Article  PubMed  CAS  Google Scholar 

  149. Schneider BS, McGee CE, Jordan JM, Stevenson HL, Soong L, Higgs S (2007) Prior exposure to uninfected mosquitoes enhances mortality in naturally-transmitted West Nile virus infection. PLoS One 2:e1171

    Article  PubMed  Google Scholar 

  150. Schneider BS, Higgs S (2008) The enhancement of arbovirus transmission and disease by mosquito saliva is associated with modulation of the host immune response. Trans R Soc Trop Med Hyg 102:400–408

    Article  PubMed  Google Scholar 

  151. Schuh AJ, Tesh RB, Barrett AD (2010) Genetic characterization of Japanese encephalitis virus genotype II strains isolated from 1951 to 1978. J Gen Virol 92:516–527

    Article  PubMed  CAS  Google Scholar 

  152. Sejvar JJ, Haddad MB, Tierney BC, Campbell GL, Marfin AA, Van Gerpen JA, Fleischauer A, Leis AA, Stokic DS, Petersen LR (2003) Neurologic manifestations and outcome of West Nile virus infection. J Am Med Assoc (JAMA) 290:511–515

    Article  Google Scholar 

  153. Sejvar JJ, Bode AV, Marfin AA, Campbell GL, Ewing D, Mazowiecki M, Pavot PV, Schmitt J, Pape J, Biggerstaff BJ, Petersen LR (2005) West Nile virus-associated flaccid paralysis. Emerg Infect Dis 11:1021–1027

    Article  PubMed  Google Scholar 

  154. Shankar SK, Rao TV, Mruthyunjayanna BP, Gourie Devi M, Deshpande DH (1983) Autopsy study of brains during an epidemic of Japanese encephalitis in Karnataka. Indian J Med Res 78:431–440

    PubMed  CAS  Google Scholar 

  155. Shirato K, Miyoshi H, Goto A, Ako Y, Ueki T, Kariwa H, Takashima I (2004) Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J Gen Virol 85:3637–3645

    Article  PubMed  CAS  Google Scholar 

  156. Shrestha B, Diamond MS (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78:8312–8321

    Article  PubMed  CAS  Google Scholar 

  157. Shrestha B, Wang T, Samuel MA, Whitby K, Craft J, Fikrig E, Diamond MS (2006) Gamma interferon plays a crucial early antiviral role in protection against West Nile virus infection. J Virol 80:5338–5348

    Article  PubMed  CAS  Google Scholar 

  158. Shrestha B, Zhang B, Purtha WE, Klein RS, Diamond MS (2008) Tumor necrosis factor alpha protects against lethal West Nile virus infection by promoting trafficking of mononuclear leukocytes into the central nervous system. J Virol 82:8956–8964

    Article  PubMed  CAS  Google Scholar 

  159. Siddharthan V, Wang H, Motter NE, Hall JO, Skinner RD, Skirpstunas RT, Morrey JD (2009) Persistent West Nile virus associated with a neurological sequela in hamsters identified by motor unit number estimation. J Virol 83:4251–4261

    Article  PubMed  CAS  Google Scholar 

  160. Sirbu A, Ceianu C, Panculescu-Gatej R, Vazquez A, Tenorio A, Rebreanu R, Niedrig M, Nicolescu G, Pistol A (2011) Outbreak of West Nile virus infection in humans, Romania, July to October 2010. Eurosurveillance 16(2)pii: 19762

    Google Scholar 

  161. Sitati EM, Diamond MS (2006) CD4+ T-cell responses are required for clearance of West Nile virus from the central nervous system. J Virol 80:12060–12069

    Article  PubMed  CAS  Google Scholar 

  162. Smithburn KC (1940) A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 20:471–492

    Google Scholar 

  163. Solomon T, Dung NM, Kneen R, Gainsborough M, Vaughn DW, Khanh VT (2000) Japanese encephalitis. J Neurol Neurosurg Psychiatry 68:405–415

    Article  PubMed  CAS  Google Scholar 

  164. Solomon T, Vaughn DW (2002) Pathogenesis and clinical features of Japanese encephalitis and West Nile virus infections. Curr Top Microbiol Immunol 267:171–194

    Article  PubMed  CAS  Google Scholar 

  165. Solomon T, Winter PM (2004) Neurovirulence and host factors in flavivirus encephalitis—evidence from clinical epidemiology. Arch Virol Suppl 161–170

  166. Styer LM, Bernard KA, Kramer LD (2006) Enhanced early West Nile virus infection in young chickens infected by mosquito bite: effect of viral dose. Am J Trop Med Hyg 75:337–345

    PubMed  Google Scholar 

  167. Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA (2010) Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol

  168. Styer LM, Lim PY, Louie KL, Albright RG, Kramer LD, Bernard KA (2011) Mosquito saliva causes enhancement of West Nile virus infection in mice. J Virol 85:1517–1527

    Article  PubMed  CAS  Google Scholar 

  169. Suss J (2008) Tick-borne encephalitis in Europe and beyond–the epidemiological situation as of 2007. Eurosurveillance 13

  170. Swarup V, Das S, Ghosh S, Basu A (2007) Tumor necrosis factor receptor-1-induced neuronal death by TRADD contributes to the pathogenesis of Japanese encephalitis. J Neurochem 103:771–783

    Article  PubMed  CAS  Google Scholar 

  171. Swarup V, Ghosh J, Das S, Basu A (2008) Tumor necrosis factor receptor-associated death domain mediated neuronal death contributes to the glial activation and subsequent neuroinflammation in Japanese encephalitis. Neurochem Int 52:1310–1321

    Article  PubMed  CAS  Google Scholar 

  172. Tesh RB, Arroyo J, Travassos da Rosa AP, Guzman H, Xiao SY, Monath TP (2002) Efficacy of killed virus vaccine, live attenuated chimeric virus vaccine, and passive immunization for prevention of West Nile virus encephalitis in hamster model. Emerg Infect Dis 8:1392–1397

    Article  PubMed  Google Scholar 

  173. Tesh RB, Siirin M, Guzman H, Travassos da Rosa AP, Wu X, Duan T, Lei H, Nunes MR, Xiao SY (2005) Persistent West Nile virus infection in the golden hamster: studies on its mechanism and possible implications for other flavivirus infections. J Infect Dis 192:287–295

    Article  PubMed  Google Scholar 

  174. Thangamani S, Higgs S, Ziegler S, Vanlandingham D, Tesh R, Wikel S (2010) Host immune response to mosquito-transmitted chikungunya virus differs from that elicited by needle inoculated virus. PLoS One 5(8):e12137

    Google Scholar 

  175. Tohmi M, Tsuda N, Zheng Y, Mizuno M, Sotoyama H, Shibuya M, Kawamura M, Kakita A, Takahashi H, Nawa H (2007) The cellular and behavioral consequences of interleukin-1 alpha penetration through the blood-brain barrier of neonatal rats: a critical period for efficacy. Neuroscience 150:234–250

    Article  PubMed  CAS  Google Scholar 

  176. Tonry JH, Xiao SY, Siirin M, Chen H, da Rosa AP, Tesh RB (2005) Persistent shedding of West Nile virus in urine of experimentally infected hamsters. Am J Trop Med Hyg 72:320–324

    PubMed  Google Scholar 

  177. Trgovcich J, Aronson JF, Eldridge JC, Johnston RE (1999) TNFalpha, interferon, and stress response induction as a function of age-related susceptibility to fatal Sindbis virus infection of mice. Virology 263:339–348

    Article  PubMed  CAS  Google Scholar 

  178. Tsai TF (1988) St. Louis encephalitic virus. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, pp 113–141

    Google Scholar 

  179. Tsai TF (2000) New initiatives for the control of Japanese encephalitis by vaccination: minutes of a WHO/CVI meeting, Bangkok, Thailand, 13-15 October 1998. Vaccine 18(Suppl 2):1–25

    Article  PubMed  Google Scholar 

  180. Uno M, Takano T, Yamano T, Shimada M (1997) Age-dependent susceptibility in mumps-associated hydrocephalus: neuropathologic features and brain barriers. Acta Neuropathol 94:207–215

    Article  PubMed  CAS  Google Scholar 

  181. Urosevic N, Mansfield JP, Mackenzie JS, Shellam GR (1995) Low resolution mapping around the flavivirus resistance locus (Flv) on mouse chromosome 5. Mamm Genome 6:454–458

    Article  PubMed  CAS  Google Scholar 

  182. van den Hurk AF, Ritchie SA, Mackenzie JS (2009) Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54:17–35

    Article  PubMed  CAS  Google Scholar 

  183. Vernon PS, Griffin DE (2005) Characterization of an in vitro model of alphavirus infection of immature and mature neurons. J Virol 79:3438–3447

    Article  PubMed  CAS  Google Scholar 

  184. Wang H, Siddharthan V, Hall JO, Morrey JD (2009) West Nile virus preferentially transports along motor neuron axons after sciatic nerve injection of hamsters. J Neuroviro 1–7

  185. Wang H, Siddharthan V, Hall JO, Morrey JD (2011) Autonomic nervous dysfunction in hamsters infected with West Nile virus. PLoS One 6:e19575

    Article  PubMed  CAS  Google Scholar 

  186. Wang L, Fu S, Zhang H, Ye X, Yu D, Deng Z, Yuan J, Zhai Y, Li M, Lv Z, Chen W, Jiang H, Gao X, Cao Y, Wang H, Tang Q, Liang G (2010) Identification and isolation of Genotype-I Japanese encephalitis virus from encephalitis patients. Virol J 7:345

    Article  PubMed  Google Scholar 

  187. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA (2004) Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10:1366–1373

    Article  PubMed  CAS  Google Scholar 

  188. Wasay M, Diaz-Arrastia R, Suss RA, Kojan S, Haq A, Burns D, Van Ness P (2000) St Louis encephalitis: a review of 11 cases in a 1995 Dallas, Tex, epidemic. Arch Neurol 57:114–118

    Article  PubMed  CAS  Google Scholar 

  189. Watson JT, Pertel PE, Jones RC, Siston AM, Paul WS, Austin CC, Gerber SI (2004) Clinical characteristics and functional outcomes of West Nile Fever. Ann Intern Med 141:360–365

    PubMed  Google Scholar 

  190. Weissenbock H, Kolodziejek J, Url A, Lussy H, Rebel-Bauder B, Nowotny N (2002) Emergence of Usutu virus, an African mosquito-borne flavivirus of the Japanese encephalitis virus group, central Europe. Emerg Infect Dis 8:652–656

    Article  PubMed  Google Scholar 

  191. Weissenbock H, Bakonyi T, Chvala S, Nowotny N (2004) Experimental Usutu virus infection of suckling mice causes neuronal and glial cell apoptosis and demyelination. Acta Neuropathol (Berl) 108:453–460

    Article  Google Scholar 

  192. Wilson JR, de Sessions PF, Leon MA, Scholle F (2008) West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J Virol 82:8262–8271

    Article  PubMed  CAS  Google Scholar 

  193. Xiao SY, Guzman H, Zhang H, Travassos da Rosa AP, Tesh RB (2001) West Nile virus infection in the golden hamster (Mesocricetus auratus): a model for West Nile encephalitis. Emerg Infect Dis 7:714–721

    PubMed  CAS  Google Scholar 

  194. Zeller HG, Schuffenecker I (2004) West Nile virus: an overview of its spread in Europe and the Mediterranean basin in contrast to its spread in the Americas. Eur J Clin Microbiol Infect Dis 23:147–156

    Article  PubMed  CAS  Google Scholar 

  195. Zijlstra M, Li E, Sajjadi F, Subramani S, Jaenisch R (1989) Germ-line transmission of a disrupted beta 2-microglobulin gene produced by homologous recombination in embryonic stem cells. Nature 342:435–438

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Vectorborne Diseases and Department of Pathology, Microbiology and Immunology, School of Veterinary Medicine, University of California, Davis, 95616, USA

    David C. Clark

  2. Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, Fort Collins, CO, 80521, USA

    Aaron C. Brault

  3. Division of Vector-Borne Diseases, Centers for Disease Control and Prevention, San Juan, PR, 00920, USA

    Elizabeth Hunsperger

Authors
  1. David C. Clark
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aaron C. Brault
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elizabeth Hunsperger
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to David C. Clark.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Clark, D.C., Brault, A.C. & Hunsperger, E. The contribution of rodent models to the pathological assessment of flaviviral infections of the central nervous system. Arch Virol 157, 1423–1440 (2012). https://doi.org/10.1007/s00705-012-1337-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-012-1337-4

Keywords

Search

Navigation