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

Archives of Virology

Volumn 157, Issue 8, 2012, Pages 1423-1440

  Clark, David C ^a   Brault, Aaron C ^b   Hunsperger, Elizabeth ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CENTRAL NERVOUS SYSTEM; DISEASE CARRIER; DISEASE MODEL; FLAVIVIRUS; FLAVIVIRUS INFECTION; HAMSTER; HOST PATHOGEN INTERACTION; MOUSE; PATHOGENICITY; REVIEW; RODENT; VIROLOGY; VIRUS ENCEPHALITIS;

ANIMALS; CENTRAL NERVOUS SYSTEM; CRICETINAE; DISEASE MODELS, ANIMAL; ENCEPHALITIS, VIRAL; FLAVIVIRUS; FLAVIVIRUS INFECTIONS; HOST-PATHOGEN INTERACTIONS; INSECT VECTORS; MICE; RODENTIA;

ANIMALIA; FLAVIVIRIDAE; FLAVIVIRUS; RODENTIA;

EID: 84864433330     PISSN: 03048608     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00705-012-1337-4     Document Type: Review

References (195)

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.
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.
3. Anderson SG (1954) Murray Valley encephalitis and Australian X disease. J Hyg 52: 447-468.
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.
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.
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.
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.
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.
10. Balakrishnan A, Mishra AC (2008) Immune response during acute Chandipura viral infection in experimentally infected susceptible mice. Virol J 5: 121.
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.
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.
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.
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.
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.
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.
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.
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.
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.
21. Brinton MA, Perelygin AA (2003) Genetic resistance to flaviviruses. Adv Virus Res 60: 43-85.
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.
23. Campbell GL, Marfin AA, Lanciotti RS, Gubler DJ (2002) West Nile virus. Lancet Infect Dis 2: 519-529.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
40. Dumpis U, Crook D, Oksi J (1999) Tick-borne encephalitis. Clin Infect Dis 28: 882-890.
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.
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.
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.
44. Evans IA, Hueston L, Doggett SL (2009) Murray Valley encephalitis virus. N S W Public Health Bull 20: 195-196.
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.
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.
47. French EL (1952) Murray Valley encephalitis: isolation and characterisation of the aetiological agent. Med J Aust 1: 100-103.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
60. Hollidge BS, González-Scarano F, Soldan SS (2010) Arboviral encephalitides: transmission, emergence, and pathogenesis. J Neuroimmune Pharmacol 5: 428-442.
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.
62. Hunsperger EA, Roehrig JT (2006) Temporal analyses of the neuropathogenesis of a West Nile virus infection in mice. J Neurovirol 12: 129-139.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
84. Lindquist L, Vapalahti O (2008) Tick-borne encephalitis. Lancet 371: 1861-1871.
85. Linton PJ, Dorshkind K (2004) Age-related changes in lymphocyte development and function. Nat Immunol 5: 133-139.
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.
87. Luby JP, Sulkin SE, Sanford JP (1969) The epidemiology of St. Louis encephalitis: a review. Annu Rev Med 20: 329-350.
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.
89. Lumsden LL (1958) St. Louis encephalitis in 1933; observations on epidemiological features. Public Health Rep 73: 340-353.
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.
91. Lynch CJ, Hughes TP (1936) The inheritance of susceptibility to yellow fever encephalitis in mice. Genetics 21: 104-112.
92. Mackenzie JS, Broom AK (1995) Australian X disease, Murray Valley encephalitis and the French connection. [Review] [49 refs]. Vet Microbiol 46: 79-90.
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.
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.
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.
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.
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.
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.
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.
102. Misra UK, Kalita J (2010) Overview: Japanese encephalitis. Prog Neurobiol 91: 108-120.
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.
104. Miyake M (1964) The pathology of Japanese encephalitis a review. Bull World Health Organ 30: 153-160.
105. Monath TP (1980) Epidemiology. In: Monath TP (ed) St Louis encephalitis. American Public Health Association, Washington, DC, pp 239-312.
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.
107. Monath TP, Tsai TF (1987) St. Louis encephalitis: lessons from the last decade. Am J Trop Med Hyg 37: 40S-59S.
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.
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.
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.
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.
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.
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.
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.
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.
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.
118. Nazmi A, Dutta K, Das S, Basu A (2011) Japanese encephalitis virus-infected macrophages induce neuronal death. J Neuroimmune Pharmacol 6: 420-433.
119. Odelola HA, Oduye OO (1977) West Nile virus infection of adult mice by oral route. Arch Virol 54: 251-253.
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.
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.
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.
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.
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.
125. Papa A (2011) Genetic characterization of West Nile Virus lineage 2, Greece, 2010. Emerg Infect Dis 17(5): 920-922.
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.
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 Res23: 47-50.
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.
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.
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.
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.
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.
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.
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.
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.
137. Reisen WK (2003) Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61: 139-183.
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.
139. Reyes MG, Gardner JJ, Poland JD, Monath TP (1981) St Louis encephalitis. Quantitative histologic and immunofluorescent studies. Arch Neurol 38: 329-334.
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.
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.
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.
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.
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.
146. Saunders NR, Habgood MD, Dziegielewska KM (1999) Barrier mechanisms in the brain, II. Immature brain. Clin Exp Pharmacol Physiol 26: 85-91.
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.
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.
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.
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.
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.
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.
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.
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.
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.
156. Shrestha B, Diamond MS (2004) Role of CD8+ T cells in control of West Nile virus infection. J Virol 78: 8312-8321.
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.
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.
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.
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.
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.
162. Smithburn KC (1940) A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med Hyg 20: 471-492.
163. Solomon T, Dung NM, Kneen R, Gainsborough M, Vaughn DW, Khanh VT (2000) Japanese encephalitis. J Neurol Neurosurg Psychiatry 68: 405-415.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
178. Tsai TF (1988) St. Louis encephalitic virus. In: Monath TP (ed) The arboviruses: epidemiology and ecology. CRC Press, Boca Raton, pp 113-141.
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.
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.
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.
182. van den Hurk AF, Ritchie SA, Mackenzie JS (2009) Ecology and geographical expansion of Japanese encephalitis virus. Annu Rev Entomol 54: 17-35.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.