In vivo infection by a neuroinvasive neurovirulent dengue virus

Journal of NeuroVirology

Volumn 18, Issue 5, 2012, Pages 374-387

  Velandia Romero, Myriam Lucia ^a   Acosta Losada, Orlando ^b   Castellanos, Jaime E ^a  

^a UNIVERSIDAD EL BOSQUE   (Colombia)

^b UNIVERSIDAD NACIONAL DE COLOMBIA   (Colombia)

Author keywords

Dengue virus; Encephalitis; Neuroinfection; Neurosusceptibility; Neurovirulence

Indexed keywords

VIRUS ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BODY POSTURE; BRAIN NERVE CELL; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 4; DISEASE SEVERITY; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; GROUPS BY AGE; IN VIVO STUDY; INFECTION SENSITIVITY; MACROPHAGE ACTIVATION; MEMBRANE DAMAGE; MICROGLIA; MOUSE; NEUROBLASTOMA CELL; NEWBORN; NONHUMAN; OLIGODENDROGLIA; PARALYSIS; PERINATAL PERIOD; PRIORITY JOURNAL; SEROTYPE; SUCKLING; SURVIVAL; VIRUS ENCEPHALITIS; VIRUS ISOLATION; VIRUS REPLICATION; VIRUS TITRATION; VIRUS VIRULENCE;

AGE FACTORS; ANIMALS; ANIMALS, NEWBORN; BLOOD-BRAIN BARRIER; BRAIN; CELL LINE, TUMOR; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; ENCEPHALITIS, VIRAL; ENDOTHELIAL CELLS; HUMANS; MICE; MICROGLIA; NEUROBLASTOMA; NEURONS; SURVIVAL RATE; VIRULENCE;

EID: 84867297575     PISSN: 13550284     EISSN: 15382443     Source Type: Journal    
DOI: 10.1007/s13365-012-0117-y     Document Type: Article

References (67)

1. An J, Kimura-Kuroda J, Hirabayashi Y, Yasui K (1999) Development of a novel mouse model for dengue virus infection. Virology 263:70-77. doi:10.1006/viro.1999.9887
2. Añez G, Men R, Eckles K, Lai C (2009) Passage of dengue virus type 4 vaccine candidates in fatal rhesus lung cells selects heparin sensitive variants that result in loss of infectivity and immunogenicity in rhesus macaques. J Virol 83:10384-10394. doi:10.1128/JVI.01083-09
3. Atrasheuskaya A, Petzelbauer P, Fredeking T, Ignatyev G (2003) Anti-TNF antibody treatment reduces mortality in experimental dengue virus infection. FEMS Immunol Med Microbiol 35:33-42. doi:10.1111/j.1574-695X.2003.tb00646.x
4. Avirutnan P, Malasit P, Seliger B, Bhakdi S, Husmann M (1998) Dengue virus infection of human endothelial cell leads to chemokine production, complement activation and apoptosis. J Immunol 161:6338-6346. doi:10.4049/jimmunol.1190090
5. Bacsal K, Chee S, Cheng C, Flores J (2007) Dengue-associated maculopathy. Arch Ophthalmol 125:501-510. doi:10.1001/archopht.125.4.501
6. Barreto D, Takiya C, Schatzmayr H, Ribeiro R, Farias J (2007) Barth O (2007) Histological and ultrastructural aspects of mice lungs experimentally infected with dengue virus serotipe 2. Mem Inst Oswaldo Cruz 102:175-182. doi:10.1590/S0074-02762007 005000007
7. Barth O, Barreto D, Paes M, Takiya C, Pinhão A (2006) Schatzmayr H (2006) Morphological studies in a model for dengue-2 virus infection in mice. Mem Inst Oswaldo Cruz 101:905-915. doi:10.1590/S0074-02762006000800014
8. Basu A, Chaturvedi UC (2008) Vascular endothelium: the battlefield of dengue viruses. FEMS Immunol Med Microbiol 53:287-299. doi:10.1111/j.1574-695X. 2008.00420.x
9. Bente D, Melkus M, Garcia J, Rico-Hesse R (2005) Dengue fever in humanized NOD/SCID mice. J Virol 79:13797-13799. doi:10.1128/JVI.79.21.13797- 13799.2005
10. Bielefeldt-Ohmann H, Mayer M, Fitzpatrick D, Mackenzie J (2001) Dengue virus binding to human leucocyte cell lines: receptor usage differs between types and virus strains. Virus Res 73:81-89
11. Bordignon J, Strottmann D, Mosimann A, Probst C, Stella V, Noronha L, Zanata S, Duarte dos Santos C (2007) Dengue neurovirulence in mice: identification of molecular signatures in the E and NS3 helicase domains. J Med Virol 79:1506-1517. doi:10.1002/jmv. 20958
12. Chaturvedi U, Dhawan R, Khanna M, Mathur A (1991) Breakdown of the blood-brain barrier during dengue virus infection of mice. J Gen Virol 72:859-866. doi:10.1371/journal.pone.0020472
13. Chen W, Wu H, Chiou S (2003) E/NS1 modifications of dengue 2 virus after serial passages in mammalian and/or mosquito cells. Intervirology 46:289-295. doi:10.1128/JVI.02575-06
14. Chen H, Hofman F, Kung J, Lin Y, Wu-Hsieh B (2007) Both virus and tumor necrosis factor alpha are critical for endothelium damage in a mouse model of dengue virus-induced hemorrhage. J Virol 81:5518-5526. doi:10.1128/JVI.02575-06
15. Chen C, Ou Y, Lins Y, Raung S, Liao S, Lai C, Chen S, Chen J (2009) Glial activation involvement in neuronal death by Japanese encephalitis virus infection. J Gen Virol 91:1028-1037. doi:10. 1099/vir.0.013565-0
16. Chien J, Ong A, Low SY (2008) An unusual complication of dengue infection. Singapore Med J 49:e340-e341. doi:10.4103/0028-3886.68654
17. Chingsuwanrote P, Suksanpaisan L, Smith D (2004) Adaptation of the plaque assay methodology for dengue virus infected HepG2 cells. J Virol Methods 116:119-121. doi:10.1016/j.jviromet.2003. 11.002
18. Cole G, Wisseman C (1969) Pathogenesis of type1 dengue virus infection in sckling, weanling and adult mice. 1. The relation of virus replication to interferon and antibody formation. Am J Epidemiol 89:669-680
19. Després P, Flamand M, Ceccaldi PE, Deubel V (1996) Human isolates of dengue type 1 virus induce apoptosis in mouse neuroblastoma cells. J Virol 70:4090-4096
20. Després P, Frenkiel M, Ceccaldi PE, Duarte dos Santos C, Deubel V (1998) Apoptosis in the mouse central nervous system in response to infection with mouse-neurovirulent dengue viruses. J Virol 72:823-829
21. Domingues R, Kuster G, Onuki-Castro F, Souza V, Levi J, Pannuti C (2008) Involvement of the central nervous system in patients with dengue virus infection. J Neurol Sci 267:36-40. doi:10.1016/j.jns.2007.09.040
22. Duarte dos Santos C, Frenkiel M, Courageot M, Rocha C, Vazeille M, Wien M, Rey F, Deubel V, Després P (2000) Determinants in the envelope E protein and viral RNA helicase NS3 that influence the induction of apoptosis in response to infection with dengue type 1 virus. Virology 2000;274:292-08. DOI: 10.1006/viro.2000.0457
23. Esack A, Teelucksingh S, Singh N (1999) The Guillain-Barre syndrome following dengue fever. West Indian Med J 48:36-37. doi:10.1016/j.annemergmed. 2007.02.026
24. Gera C, George U (2010) Acute disseminating encephalomyelitis with hemorrhage following dengue. Neurol India 58:595-596. doi:10.4103/0028-3886. 68661
25. Gulati S, Maheshwari A (2007) Atypical manifestations of dengue. Tropl Med Int Health 12:1087-1095. doi:10.1111/j.1365-3156. 2007.01891.x
26. Guzman M, Kouri G, Valdes L, Bravo J, Vazquez S, Halstead S (2002) Effect of age on outcome of secondary dengue 2 infections. Int J Infect Dis 6:118-124. doi:10.1016/S1201-9712 (02) 90072-X
27. Halstead S (2002) Dengue. Curr Opin Infect Dis 15:471-476
28. Huang K, Li S, Chen S, Liu H, Lin Y, Yeh T, Liu C, Lei H (2000) Manifestation of thrombocytopenia in dengue 2 virus infected mice. J Gen Virol 81:2177-2182
29. Imbert J, Guevara P, Castañeda J, Ramos C, Sotelo J (1994) Dengue virus infects mouse cultured neurons but not astrocitos. J Med Virol 42:228-233. doi:10.1002/jmv. 1890420304
30. Ip P, Liao F (2010) Resistance to dengue virus infection in mice is potentiated by CXCL10 and is independent of CXCL10-mediated leukocyte recruitment. J Immunol 184:5705-5714. doi:10.4049/jimmunol.0903484
31. Jackson ST, Mullings A, Bennett F, Khan C, Gordon-Strachan G, Rhoden T (2008) Dengue infection in patients presenting with neurological manifestations in a dengue endemic population. West Indian Med J 57:373-376
32. Johnson A, Roehring J (1999) New model for dengue virus vaccine testing. J Virol 73:783-786
33. Kawano H, Rostapshov V, Rosen L, Lai C (1993) Genetic determinants of dengue type 4 virus neurovirulence for mice. J Virol 67:6567-6575
34. Kumar J, Kumar A, Gupta S, Jain D (2007) Dengue hemorrhagic fever: an unusual cause of intracranial hemorrhage. J Neurol Neurosurg Psychiatry 78:253. doi:10.1136/jnnp. 2006.100909
35. Kumar R, Tripathi S, Tambe J, Arora V, Srivastava A, Nag V (2008) Dengue encephalopathy in children in Northern India: clinical factures and comparison with non dengue. J Neurol Sci 269:41-4846. doi:10.1016/j.jns.2007.12.018
36. Kunishige M, Mitsui T, Tan B, Leong H, Takasaki T, Kurane I, Mihara A, Matsumoto T (2004) Preferential gray matter involvement in dengue myelitis. Neurology 63:1980-1981. doi:10.1212/01. WNL.0000 144194.29643. D0
37. Kyle J, Harris E (2008) Global spread and persistence of dengue. Annual Rev Microbiol 62:71-92. doi:10.1146/annurev. micro.62.081307.163005
38. Leyo R, Oikawa T, Rosa E, Yamaki J, Rodriguez S, Vasconcelos H, Sousa M, Tsukimata J, Azevedo R, Vasconcelos P (2002) Isolation of dengue 2 virus from a patient with central nervous system involvement (transverse myelitis). Rev Soc Bras Med Trop 35:401-404. doi:10.1590/S0037-86822002000400018
39. Lin YL, Liao CL, Chen LK, Yeh CT, Liu CI, Ma SH, Huang YY, Huang YL, Kao CL, King CC (1998) Study of dengue virus infection in SCID mice engrafted with human K562 cells. J Virol 72:9729-9737
40. Lin C, Wan S, Chen M, Lin S, Cheng C, Chiu S, Hsiao Y, Lei H, Liu H, Yeh T, Lin Y (2008) Liver injury caused by antibodies against dengue virus nonstructural protein 1 in a murine model. Lab Invest 88:1079-1089. doi:10.1038/labinvest.2008.70
41. Lindenbach B, Rice C (2001a) Flaviviridae: the viruses and their replication. In: Knipe DM, Howley PM; associate editors, Diane E. Griffin [et al.] Fields virology. 4th ed. Lippincott Williams and Wilkins. PA Vol 1:991-1041
42. Lindenbach B, Rice C (2001b) In: Knipe DM, Howley PM; associate editors, Diane E. Griffin [et al.] Fields virology. 4th ed. Lippincott Williams and Wilkins, PA Vol. 1:1:1043-1090
43. Lum LC, Lam SK, Choy YS, George R, Harun F (1996) Dengue encephalitis: a true entity? Am J Trop Med Hyg 54:256-259
44. Malavige G, Ranatunga P, Jayaratne S, Wijesiriwardana B, Seneviratne S, Karunatilaka D (2007) Dengue viral infections as a cause of encephalopathy. Indian J Med Micro 25:143-145. doi:10.4103/0255-0857.32722
45. Malheiros S, Oliveira A, Schmidt B, Lima J, Gabbai A (1993) Dengue: muscle biopsy findings in 15 patients. Arq Neuropsiquiatr 51:159-164. doi:10.1590/S0004-282X1993000200001
46. McMinn P (1997) The molecular basis of virulence of the encephalitogenic flavivirus. J Gen Virol 78:2711-2722
47. Méndez A, González G (2003) Dengue hemorrágico en niños: diez años de experiencia clínica. Biomedica 23:180-193
48. Méndez A, González G (2006) Manifestaciones clínicas inusuales del dengue hemorrágico en niños. Biomedica 26:61-70
49. Miagostovich M, Ramos R, Nicol A, Nogueira R, Cuzzi-Maya T, Oliveira A, Marchevsky R, Mesquita R, Schatzmayr H (1997) Retrospective study on dengue fatal cases. Clin Neuropathol 16:204-208
50. Miranda A, Puccioni M, Dias A, Fernández L, Papais M, Papais R (2007) Post-dengue neuromyelitis optica: case report of a Japanese-descendent Brazilian child. J Infect Chemother 19:396-398. doi:10.1007/s10156-006-0475-6
51. Mishra M, Dutta K, Saheb S, Basu A (2009) Understanding the molecular mechanism of blood-brain barrier damage in an experimental model of Japanese encephalitis: correlation with minocycline administration as a therapeutic agent. Neurochem Int 55:717-723. doi:10.1016/j.neuint.2009.07.006
52. Mota J, Rico-Hesse R (2009) Humanized mice show clinical signs of dengue fever according to infecting virus genotype. J Virol 83:8638-8645. doi:10.1128/JVI.00581-09
53. Murthy J (2010) Neurological complications of dengue infection. Neurol India 58:581-584. doi:10.4103/0028-3886.68654
54. Ogata A, Nagashima K, Hall W, 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
55. Prestwood T, Prigozhin D, Sharar K, Zellweger R, Shresta S (2008) A mouse passaged dengue virus strain with reduce affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 82:8411-8421. doi:10. 1128/JVI.00611-08
56. Ramos C, Sánchez G, Hernández R, Baquero J, Hernández D, Mota J, Ramos J, Flores A, Llausas E (1998) Dengue virus in the brain of a fatal case of hemorrhagic dengue fever. J Neurovirol 4:465-468
57. Sánchez I, Ruiz B (1996) A single nucleotide change in the E protein gene of dengue virus 2 Mexican strain affects neurovirulence in mice. J Gen Virol 77:2541-2545. doi:10.1099/0022-1317-77-10-2541
58. Sánchez-Burgos G, Hernández R, Campbell I, Castañeda J, Ramos C (2004) Cytokine production in brain of mice experimentally infected with dengue virus. NeuroReport 15:37-42
59. Shresta S, Kyle J, Beatty P, Harris E (2004) Early activation of natural killer and B cells in responses to primary dengue virus infection in A/J mice. Virology 319:262-273. doi:10.1016/j.virol.2003.09.048
60. Souza D, Fagundes C, Sousa L, Amaral F, Souza R, Sousa A, Kroon E, Sachs D, Cunha F, Bukin E, Atrasheuskaya A, Ignatyev G, Texeira M (2009) Essential role of platelet activating factor receptor in the pathogenesis of dengue virus infection. PNAS 106:14138-14143. doi:10.1073/pnas.0906467106
61. Tan G, Ng J, Trasti S, Schul W, Yip G, Alonso S (2010) A non mouse adapted dengue virus strain as a new modelo of severe dengue infection in AG129 mice. PLoS Negl Trop Dis 4:e672. doi:10.1371/journal.pntd.0000672
62. Thisyakorn U, Thisyakorn C, Limpitikul W, Nisalak A (1999) Dengue infection with central nervous system manifestations. Southeast Asian J Trop Med Public Health 30:504-506
63. Wang T, Town T, Alexopoulou L, Anderson J, Fikring E, Flavell R (2003) Toll like receptor 3 mediates West Nile Virus entry into de brain causing lethal encephalitis. Nat Med 10:1366-1373. doi:10.1038/nm1140
64. Williams K, Zompi S, Beatty P, Harris E (2009) A mouse model for studying dengue virus pathogenesis and immune response. Immunology and pathogenesis of viral hemorrhagic fevers. Ann NY Acad Sci 1171:E12-E23. doi:10.1111/j.1749-6632. 2009.05057.x
65. World Health Organization (2009) Dengue guidelines for diagnosis, treatment, prevention and control. New Edition
66. Wu-Hsieh B, Yen Y, Chen H (2009) Dengue hemorrhage in a mouse model. Immunology and pathogenesis of viral hemorrhagic fevers. Ann NY Acad Sci 1171:E42-E47. doi:10.1111/j.1749-6632. 2009.05053.x
67. Yauch L, Shresta S (2008) Mouse models of dengue virus infection and disease. Antiviral Res 80:87-93. doi:10.1371/journal.pntd. 0000672.g001