A model of DENV-3 infection that recapitulates severe disease and highlights the importance of IFN-γ in host resistance to infection

PLoS Neglected Tropical Diseases

Volumn 6, Issue 5, 2012, Pages

  Costa, Vivian V ^a   Fagundes, Caio T ^a   Valadão, Deborah F ^a   Cisalpino, Daniel ^a   Dias, Ana Carolina F ^a   Silveira, Kátia D ^a   Kangussu, Lucas M ^a   Ávila, Thiago V ^a   Bonfim, Maria Rosa Q ^a   Bonaventura, Daniela ^a   Silva, Tarcília A ^a   Sousa, Lirlândia P ^a   Rachid, Milene A ^a   Vieira, Leda Q ^a   Menezes, Gustavo B ^a   de Paula, Ana Maria ^a   Atrasheuskaya, Alena ^b   Ignatyev, George ^c   Teixeira, Mauro M ^a   Souza, Danielle G ^a  

^a FEDERAL UNIVERSITY OF MINAS GERAIS   (Brazil)

^b STATE RESEARCH CENTER OF VIROLOGY AND BIOTECHNOLOGY VECTOR   (Russian Federation)

^c MOSCOW AVIATION INSTITUTE NATIONAL RESEARCH UNIVERSITY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; GAMMA INTERFERON; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 18; INTERLEUKIN 6; MESSENGER RNA; NITRIC OXIDE; NONSTRUCTURAL PROTEIN 1; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; NOS2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; BODY WEIGHT; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENGUE; DENGUE VIRUS 3; DISEASE SEVERITY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE ACTIVATED CELL SORTING; HISTOPATHOLOGY; HOST RESISTANCE; HOST SUSCEPTIBILITY; HYPERALGESIA; IMMUNOCOMPETENCE; IMMUNOHISTOCHEMISTRY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLAQUE FORMING CELL; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SYSTOLIC BLOOD PRESSURE; VIRUS CELL INTERACTION; VIRUS CULTURE; VIRUS LOAD; VIRUS REPLICATION; ADAPTATION; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; DENGUE VIRUS; DISEASE MODEL; IMMUNOLOGY; MORTALITY; MOUSE MUTANT; PATHOGENICITY; PATHOLOGY; SECRETION; SURVIVAL; VIROLOGY;

ADAPTATION, BIOLOGICAL; ANIMALS; CYTOKINES; DENGUE; DENGUE VIRUS; DISEASE MODELS, ANIMAL; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE II; SURVIVAL ANALYSIS;

EID: 84863638729     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001663     Document Type: Article

References (77)

1. Gubler DJ, (1998) Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11: 480-496.
2. Kurane I, (2007) Dengue hemorrhagic fever with special emphasis on immunopathogenesis. Comp Immunol Microbiol Infect Dis 30: 329-340.
3. Kyle JL, Harris E, (2008) Global spread and persistence of dengue. Annu Rev Microbiol 62: 71-92.
4. Guzman MG, Kouri G, (2002) Dengue: an update. Lancet Infect Dis 2: 33-42.
5. Deen JL, Harris E, Wills B, Balmaseda A, Hammond SN, et al. (2006) The WHO dengue classification and case definitions: time for a reassessment. Lancet 368: 170-173.
6. Green S, Rothman A, (2006) Immunopathological mechanisms in dengue and dengue hemorrhagic fever. Curr Opin Infect Dis 19: 429-436.
7. Fagundes CT, Costa VV, Cisalpino D, Souza DG, Teixeira MM, (2011) Therapeutic opportunities in dengue infection. Drug Development Res 72: 480-500.
8. Parkash O, Almas A, Jafri SM, Hamid S, Akhtar J, et al. (2010) Severity of acute hepatitis and its outcome in patients with dengue fever in a tertiary care hospital Karachi, Pakistan (South Asia). BMC Gastroenterol 10: 43.
9. Nguyen TL, Nguyen TH, Tieu NT, (1997) The impact of dengue haemorrhagic fever on liver function. Res Virol 148: 273-277.
10. Narvaez F, Gutierrez G, Perez MA, Elizondo D, Nunez A, et al. (2011) Evaluation of the traditional and revised WHO classifications of Dengue disease severity. PLoS Negl Trop Dis 5: e1397.
11. Murphy BR, Whitehead SS, (2011) Immune response to dengue virus and prospects for a vaccine. Annu Rev Immunol 29: 587-619.
12. Guzman MG, Kouri G, Bravo J, Valdes L, Vazquez S, et al. (2002) Effect of age on outcome of secondary dengue 2 infections. Int J Infect Dis 6: 118-124.
13. Shresta S, Sharar KL, Prigozhin DM, Beatty PR, Harris E, (2006) Murine model for dengue virus-induced lethal disease with increased vascular permeability. J Virol 80: 10208-10217.
14. Noisakran S, Dechtawewat T, Rinkaewkan P, Puttikhunt C, Kanjanahaluethai A, et al. (2007) Characterization of dengue virus NS1 stably expressed in 293T cell lines. J Virol Methods 142: 67-80.
15. Martina BE, Koraka P, Osterhaus AD, (2009) Dengue virus pathogenesis: an integrated view. Clin Microbiol Rev 22: 564-581.
16. Yauch LE, Shresta S, (2008) Mouse models of dengue virus infection and disease. Antiviral Res 80: 87-93.
17. Schul W, Liu W, Xu HY, Flamand M, Vasudevan SG, (2007) A dengue fever viremia model in mice shows reduction in viral replication and suppression of the inflammatory response after treatment with antiviral drugs. J Infect Dis 195: 665-674.
18. Avirutnan P, Punyadee N, Noisakran S, Komoltri C, Thiemmeca S, et al. (2006) Vascular leakage in severe dengue virus infections: a potential role for the nonstructural viral protein NS1 and complement. J Infect Dis 193: 1078-1088.
19. Libraty DH, Endy TP, Houng HS, Green S, Kalayanarooj S, et al. (2002) Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J Infect Dis 185: 1213-1221.
20. Murgue B, Roche C, Chungue E, Deparis X, (2000) Prospective study of the duration and magnitude of viraemia in children hospitalised during the 1996-1997 dengue-2 outbreak in French Polynesia. J Med Virol 60: 432-438.
21. Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, et al. (2000) Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181: 2-9.
22. Atrasheuskaya A, Petzelbauer P, Fredeking TM, Ignatyev G, (2003) Anti-TNF antibody treatment reduces mortality in experimental dengue virus infection. FEMS Immunol Med Microbiol 35: 33-42.
23. Chen ST, Lin YL, Huang MT, Wu MF, Cheng SC, et al. (2008) CLEC5A is critical for dengue-virus-induced lethal disease. Nature 453: 672-676.
24. Souza DG, Fagundes CT, Sousa LP, Amaral FA, Souza RS, et al. (2009) Essential role of platelet-activating factor receptor in the pathogenesis of Dengue virus infection. Proc Natl Acad Sci U S A 106: 14138-14143.
25. Assuncao-Miranda I, Amaral FA, Bozza FA, Fagundes CT, Sousa LP, et al. (2010) Contribution of macrophage migration inhibitory factor to the pathogenesis of dengue virus infection. FASEB J 24: 218-228.
26. Groger M, Pasteiner W, Ignatyev G, Matt U, Knapp S, et al. (2009) Peptide Bbeta(15-42) preserves endothelial barrier function in shock. PLoS One 4: e5391.
27. Guabiraba R, Marques RE, Besnard AG, Fagundes CT, Souza DG, et al. (2010) Role of the chemokine receptors CCR1, CCR2 and CCR4 in the pathogenesis of experimental dengue infection in mice. PLoS One 5: e15680.
28. Renneson J, Guabiraba R, Maillet I, Marques RE, Ivanov S, et al. (2011) A detrimental role for invariant natural killer T cells in the pathogenesis of experimental dengue virus infection. Am J Pathol 179: 1872-1883.
29. Rothman AL, (2011) Immunity to dengue virus: a tale of original antigenic sin and tropical cytokine storms. Nat Rev Immunol 11: 532-543.
30. Fagundes CT, Costa VV, Cisalpino D, Amaral FA, Souza PR, et al. (2011) IFN-gamma Production Depends on IL-12 and IL-18 Combined Action and Mediates Host Resistance to Dengue Virus Infection in a Nitric Oxide-Dependent Manner. PLoS Negl Trop Dis 5: e1449.
31. Whitehead SS, Blaney JE, Durbin AP, Murphy BR, (2007) Prospects for a dengue virus vaccine. Nat Rev Microbiol 5: 518-528.
32. Wei XQ, Leung BP, Arthur HM, McInnes IB, Liew FY, (2001) Reduced incidence and severity of collagen-induced arthritis in mice lacking IL-18. J Immunol 166: 517-521.
33. Plitz T, Saint-Mezard P, Satho M, Herren S, Waltzinger C, et al. (2003) IL-18 binding protein protects against contact hypersensitivity. J Immunol 171: 1164-1171.
34. Freire MS, Marchevsky RS, Almeida LFC, Yamamura AMY, Caride EC, et al. (2007) Wild dengue virus types 1, 2 and 3 viremia in rhesus monkeys. Mem Inst Oswaldo Cruz 102 (2): 203-208.
35. Lutz MB, Kukutsch N, Ogilvie AL, Rossner S, Koch F, et al. (1999) An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods 223: 77-92.
36. Green LC, Ruiz de Luzuriaga K, Wagner DA, Rand W, Istfan N, et al. (1981) Nitrate biosynthesis in man. Proc Natl Acad Sci U S A 78: 7764-7768.
37. Chang SF, Su CL, Shu PY, Yang CF, Liao TL, et al. (2010) Concurrent isolation of chikungunya virus and dengue virus from a patient with coinfection resulting from a trip to Singapore. J Clin Microbiol 48: 4586-4589.
38. Saria A, Lundberg JM, (1983) Evans blue fluorescence: quantitative and morphological evaluation of vascular permeability in animal tissues. J Neurosci Methods 8: 41-49.
39. Krege JH, Hodgin JB, Hagaman JR, Smithies O, (1995) A noninvasive computerized tail-cuff system for measuring blood pressure in mice. Hypertension 25: 1111-1115.
40. Sachs D, Coelho FM, Costa VV, Lopes F, Pinho V, et al. Cooperative role of tumour necrosis factor-alpha, interleukin-1beta and neutrophils in a novel behavioural model that concomitantly demonstrates articular inflammation and hypernociception in mice. Br J Pharmacol 162: 72-83.
41. Cunha TM, Verri WA Jr, Vivancos GG, Moreira IF, Reis S, et al. (2004) An electronic pressure-meter nociception paw test for mice. Braz J Med Biol Res 37: 401-407.
42. Lanciotti RS, Calisher CH, Gubler DJ, Chang GJ, Vorndam AV, (1992) Rapid detection and typing of dengue viruses from clinical samples by using reverse transcriptase-polymerase chain reaction. J Clin Microbiol 30: 545-551.
43. Paes MV, Lenzi HL, Nogueira AC, Nuovo GJ, Pinhao AT, et al. (2009) Hepatic damage associated with dengue-2 virus replication in liver cells of BALB/c mice. Lab Invest 89: 1140-1151.
44. McDonald B, Pittman K, Menezes GB, Hirota SA, Slaba I, et al. (2010) Intravascular danger signals guide neutrophils to sites of sterile inflammation. Science 330: 362-366.
45. Balsitis SJ, Williams KL, Lachica R, Flores D, Kyle JL, et al. (2010) Lethal antibody enhancement of dengue disease in mice is prevented by Fc modification. PLoS Pathog 6: e1000790.
46. Zellweger RM, Prestwood TR, Shresta S, (2010) Enhanced infection of liver sinusoidal endothelial cells in a mouse model of antibody-induced severe dengue disease. Cell Host Microbe 7: 128-139.
47. Mota J, Rico-Hesse R, (2011) Dengue virus tropism in humanized mice recapitulates human dengue fever. PLoS One 6: e20762.
48. Balsitis SJ, Harris E, (2010) Animal models of dengue virus infection and disease: Applications, insights and frontiers. In: Hanley KA, Weaver SC, editors. Frontiers in dengue virus research Norfolk, UK pp. 103-120.
49. Amaral DC, Rachid MA, Vilela MC, Campos RD, Ferreira GP, et al. (2011) Intracerebral infection with dengue-3 virus induces meningoencephalitis and behavioral changes that precede lethality in mice. J Neuroinflammation 8: 23.
50. Tesh RB, Guzman H, da Rosa AP, Vasconcelos PF, Dias LB, et al. (2001) Experimental yellow fever virus infection in the Golden Hamster (Mesocricetus auratus). I. Virologic, biochemical, and immunologic studies. J Infect Dis 183: 1431-1436.
51. Shresta S, Kyle JL, Snider HM, Basavapatna M, Beatty PR, et al. (2004) Interferon-dependent immunity is essential for resistance to primary dengue virus infection in mice, whereas T- and B-cell-dependent immunity are less critical. J Virol 78: 2701-2710.
52. Rothman AL, (2003) Immunology and immunopathogenesis of dengue disease. Adv Virus Res 60: 397-419.
53. Halstead SB, (2007) Dengue. Lancet 370: 1644-1652.
54. Balmaseda A, Hammond SN, Pérez L, Tellez Y, Sabório SI, et al. (2006) Serotype-specific differences in clinical manifestations of dengue. Am J Trop Med Hyg 74 (3): 449-456.
55. Clyde K, Kyle JL, Harris E, (2006) Recent advances in Deciphering Viral and Host Determinants of Dengue Virus Replication and Pathogenesis. Journal of Virology 80: 11418-11431.
56. Halstead SB, (1970) Observations related to pathogenesis of dengue hemorrhagic fever. VI. Hypotheses and discussion. Yale J Biol Med 42: 350-62.
57. Sangkawibha N, Rojanasuphot S, Ahandrik S, Viriyaponqse S, Jatanasen S, et al. (1984) Risk Factors in Dengue shock syndrome: a prospective epidemiologic study in Rayong, Thailand. I. The 1980 outbreak. Am J Epidemiol 120: 653-69.
58. Thein S, Aung MM, Shwe TN, Aye M, Zaw A, et al. (1997) Risk factors in dengue shock syndrome. Am J Trop Med Hyg 56: 566-72.
59. Nishiura H, Halstead SB, (2007) Natural history of dengue virus (DENV)-1 and DENV-4 infections: reanalysis of classic studies. J Infect Dis 195: 1007-13.
60. Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, et al. (2010) Cross-reacting antibodies enhance dengue virus infection in humans. Science 7: 745-8.
61. Rosen L, Drouet MT, Deubel V, (1999) Detection of dengue virus RNA by reverse transcription-polymerase chain reaction in the liver and lymphoid organs but not in the brain in fatal human infection. Am J Trop Med Hyg 61: 720-724.
62. Seneviratne SL, Malavige GN, de Silva HJ, (2006) Pathogenesis of liver involvement during dengue viral infections. Trans R Soc Trop Med Hyg 100: 608-614.
63. Ling LM, Wilder-Smith A, Leo YS, (2007) Fulminant hepatitis in dengue haemorrhagic fever. J Clin Virol 38: 265-268.
64. Potts JA, Rothman AL, (2008) Clinical and laboratory features that distinguish dengue from other febrile illnesses in endemic populations. Trop Med Int Health 13: 1328-1340.
65. Paes MV, Pinhao AT, Barreto DF, Costa SM, Oliveira MP, et al. (2005) Liver injury and viremia in mice infected with dengue-2 virus. Virology 338: 236-246.
66. Couvelard A, Marianneau P, Bedel C, Drouet MT, Vachon F, et al. (1999) Report of a fatal case of dengue infection with hepatitis: demonstration of dengue antigens in hepatocytes and liver apoptosis. Hum Pathol 30: 1106-1110.
67. Huerre MR, Lan NT, Marianneau P, Hue NB, Khun H, et al. (2001) Liver histopathology and biological correlates in five cases of fatal dengue fever in Vietnamese children. Virchows Arch 438: 107-115.
68. Basilio-de-Oliveira CA, Aguiar GR, Baldanza MS, Barth OM, Eyer-Silva WA, et al. (2005) Pathologic study of a fatal case of dengue-3 virus infection in Rio de Janeiro, Brazil. Braz J Infect Dis 9: 341-347.
69. Bozza FA, Cruz OG, Zagne SM, Azeredo EL, Nogueira RM, et al. (2008) Multiplex cytokine profile from dengue patients: MIP-1beta and IFN-gamma as predictive factors for severity. BMC Infect Dis 8: 86.
70. Chen LC, Lei HY, Liu CC, Shiesh SC, Chen SH, et al. (2006) Correlation of serum levels of macrophage migration inhibitory factor with disease severity and clinical outcome in dengue patients. Am J Trop Med Hyg 74: 142-147.
71. Gunther VJ, Putnak R, Eckels KH, Mammen MP, Scherer JM, et al. (2011) A human challenge model for dengue infection reveals a possible protective role for sustained interferon gamma levels during the acute phase of illness. Vaccine 29: 3895-3904.
72. Horras CJ, Lamb CL, Mitchell KA, (2011) Regulation of hepatocyte fate by interferon-gamma. Cytokine Growth Factor Rev 22: 35-43.
73. Akdis M, Burgler S, Crameri R, Eiwegger T, Fujita H, et al. (2011) Interleukins, from 1 to 37, and interferon-gamma: receptors, functions, and roles in diseases. J Allergy Clin Immunol 127: 701-721 e701-770.
74. Neves-Souza PC, Azeredo EL, Zagne SM, Valls-de-Souza R, Reis SR, et al. (2005) Inducible nitric oxide synthase (iNOS) expression in monocytes during acute Dengue Fever in patients and during in vitro infection. BMC Infect Dis 5: 64.
75. Valero N, Espina LM, Anez G, Torres E, Mosquera JA, (2002) Short report: increased level of serum nitric oxide in patients with dengue. Am J Trop Med Hyg 66: 762-764.
76. Charnsilpa W, Takhampunya R, Endy TP, Mammen MP Jr, Libraty DH, et al. (2005) Nitric oxide radical suppresses replication of wild-type dengue 2 viruses in vitro. J Med Virol 77: 89-95.
77. Takhampunya R, Padmanabhan R, Ubol S, (2006) Antiviral action of nitric oxide on dengue virus type 2 replication. J Gen Virol 87: 3003-3011.