A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads

Journal of Virology

Volumn 82, Issue 17, 2008, Pages 8411-8421

  Prestwood, Tyler R ^a   Prigozhin, Daniil M ^a   Sharar, Kristin L ^a   Zellweger, Raphaël M ^a   Shresta, Sujan ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ENVELOPE PROTEIN; HEPARAN SULFATE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DENGUE VIRUS; MOUSE; NONHUMAN; PARALYSIS; PLASMA HALF LIFE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; VIRION; VIRUS LOAD; VIRUS MUTATION; VIRUS RECOMBINANT; VIRUS STRAIN;

ANIMALS; DENGUE HEMORRHAGIC FEVER; DENGUE VIRUS; HEPARITIN SULFATE; MICE; MUTATION; SEROTYPING; SEVERITY OF ILLNESS INDEX; SPECIFIC PATHOGEN-FREE ORGANISMS; TUMOR NECROSIS FACTOR-ALPHA; VIRAL LOAD; VIRAL PROTEINS;

ANIMALIA; DENGUE VIRUS; MUS;

EID: 50149086295     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.00611-08     Document Type: Article

References (58)

1. An, J., J. Kimura-Kuroda, Y. Hirabayashi, and K. Yasui. 1999. Development of a novel mouse model for dengue virus infection. Virology 263:70-77.
2. Bente, D. A., M. W. Melkus, J. V. Garcia, and R. Rico-Hesse. 2005. Dengue fever in humanized NOD/SCID mice. J. Virol. 79:13797-13799.
3. Bernard, K. A., W. B. Klimstra, and R. E. Johnston. 2000. Mutations in the E2 glycoprotein of Venezuelan equine encephalitis virus confer heparan sulfate interaction, low morbidity, and rapid clearance from blood of mice. Virology 276:93-103.
4. Blaney, J. E., Jr., A. P. Durbin, B. R. Murphy, and S. S. Whitehead. 2006. Development of a live attenuated dengue virus vaccine using reverse genetics. Viral Immunol. 19:10-32.
5. Burke, D., and T. Monath. 2001. Flaviviruses, p. 1043-1126. In D. Knipe and P. Howley (ed.), Field's virology. Lippincott/The Williams & Wilkins Co., Philadelphia, PA.
6. Byrnes, A. P., and D. E. Griffin. 1998. Binding of Sindbis virus to cell surface heparan sulfate. J. Virol. 72:7349-7356.
7. Byrnes, A. P., and D. E. Griffin. 2000. Large-plaque mutants of Sindbis virus show reduced binding to heparan sulfate, heightened viremia, and slower clearance from the circulation. J. Virol. 74:644-651.
8. Couvelard, A., P. Marianneau, C. Bedel, M. Drouet, F. Vachon, D. Henin, and V. Deubel. 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.
9. Dasaneyavaja, A., and U. Charansri. 1961. First known isolation of a dengue virus from other human source than blood, p. 61. SEATO Medical Research Monograph No. 2: Proceedings of the Symposium on Thai Hemorrhagic Fever, Bangkok, Thailand.
10. Davis, C. W., H. Y. Nguyen, S. L. Hanna, M. D. Sanchez, R. W. Doms, and T. C. Pierson. 2006. West Nile virus discriminates between DC-SIGN and DC-SIGNR for cellular attachment and infection. J. Virol. 80:1290-1301.
11. dos Santos, F. B., M. P. Miagostovich, R. M. Nogueira, H. G. Schatzmayr, L. W. Riley, and E. Harris. 2004. Analysis of recombinant dengue virus polypeptides for dengue diagnosis and evaluation of the humoral immune response. Am. J. Trop. Med. Hyg. 71:144-152.
12. Falgout, B., M. Bray, J. J. Schlesinger, and C. J. Lai. 1990. Immunization of mice with recombinant vaccinia virus expressing authentic dengue virus nonstructural protein NS1 protects against lethal dengue virus encephalitis. J. Virol. 64:4356-4363.
13. Green, S., D. W. Vaughn, S. Kalayanarooj, S. Nimmannitya, S. Suntayakorn, A. Nisalak, R. Lew, B. L. Innis, I. Kurane, A. L. Rothman, and F. A. Ennis. 1999. Early immune activation in acute dengue illness is related to development of plasma leakage and disease severity. J. Infect. Dis. 179:755-762.
14. Gubler, D. J. 1998. Dengue and dengue hemorrhagic fever. Clin. Microbiol. Rev. 11:480-496.
15. Hall, W., T. Crowell, D. Watts, V. Barros, H. Kruger, F. Pinheiro, and C. Peters. 1991. Demonstration of yellow fever and dengue antigens in formalin-fixed paraffin-embedded human liver by immunohistochemical analysis. Am. J. Trop. Med. Hyg. 45:408-417.
16. Halstead, S. B. 2007. Dengue. Lancet 370:1644-1652.
17. Helt, A. M., and E. Harris. 2005. S-phase-dependent enhancement of dengue virus 2 replication in mosquito cells, but not in human cells. J. Virol. 79:13218-13230.
18. Hober, D., L. Poli, B. Roblin, P. Gestas, E. Chungue, G. Granic, P. Imbert, J. L. Pecarere, R. Vergez-Pascal, P. Wattre, et al. 1993. Serum levels of tumor necrosis factor-α(TNF-α), interleukin-6 (IL-6), and interleukin-1β (IL-1β) in dengue-infected patients. Am. J. Trop. Med. Hyg. 48:324-331.
19. Houng, H. H., D. Hritz, and N. Kanesa-thasan. 2000. Quantitative detection of dengue 2 virus using fluorogenic RT-PCR based on 3′-noncoding sequence. J. Virol. Methods 86:1-11.
20. Huang, K.-J., S.-Y. J. Li, S.-C. Chen, H.-S. Liu, Y.-S. Lin, T.-M. Yeh, C.-C. Liu, and H.-Y. Lei. 2000. Manifestation of thrombocytopenia in dengue-2-virus-infected mice. J. Gen. Virol. 81:2177-2182.
21. Huerre, M., T. Nguyen, P. Marianneau, B. Nguyen, K. Huot, T. Nguyen, T. Nguyen, M. Drouet, T. Vu, Q. Do, Y. Buisson, and V. Deubel. 2001. Liver histopathology and biological correlates in five cases of fatal dengue fever in Vietnamese children. Virchows Arch. 438:107-115.
22. Hung, S. L., P. L. Lee, H. W. Chen, L. K. Chen, C. L. Kao, and C. C. King. 1999. Analysis of the steps involved in Dengue virus entry into host cells. Virology 257:156-167.
23. Jahrling, P. B., and L. Gorelkin. 1975. Selective clearance of a benign clone of Venezuelan equine encephalitis virus from hamster plasma by hepatic reticuloendothelial cells. J. Infect. Dis. 132:667-676.
24. Jessie, K., M. Fong, S. Devi, S. Lam, and K. Wong. 2004. Localization of dengue virus in naturally infected human tissues, by immunohistochemistry and in situ hybridization. J. Infect. Dis. 189:1411-1418.
25. Jinno-Oue, A., M. Oue, and S. K. Ruscetti. 2001. A unique heparin-binding domain in the envelope protein of the neuropathogenic PVC-211 murine leukemia virus may contribute to its brain capillary endothelial cell tropism. J. Virol. 75:12439-12445.
26. Johnson, A. J., and J. T. Roehrig. 1999. New mouse model for dengue virus vaccine testing. J. Virol. 73:783-786.
27. Kinney, R. M., S. Butrapet, G. J. Chang, K. R. Tsuchiya, J. T. Roehrig, N. Bhamarapravati, and D. J. Gubler. 1997. Construction of infectious cDNA clones for dengue 2 virus strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230:300-308.
28. Kittigul, L., W. Temprom, D. Sujirarat, and C. Kittigul. 2000. Determination of tumor necrosis factor-alpha levels in dengue virus-infected patients by sensitive biotin-streptavidin enzyme-linked immunosorbent assay. J. Virol. Methods 90:51-57.
29. Klimstra, W. B., K. D. Ryman, K. A. Bernard, K. B. Nguyen, C. A. Biron, and R. E. Johnston. 1999. Infection of neonatal mice with Sindbis virus results in a systemic inflammatory response syndrome. J. Virol. 73:10387-10398.
30. Klimstra, W. B., K. D. Ryman, and R. E. Johnston. 1998. Adaptation of Sindbis virus to BHK cells selects for use of heparan sulfate as an attachment receptor. J. Virol. 72:7357-7366.
31. -/- (RAG-hu) mice. Virology 369:143-152.
32. Lee, E., R. A. Hall, and M. Lobigs. 2004. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J. Virol. 78:8271-8280.
33. Lee, E., and M. Lobigs. 2002. Mechanism of virulence attenuation of glycosaminoglycan-binding variants of Japanese encephalitis virus and Murray Valley encephalitis virus. J. Virol. 76:4901-4911.
34. Lee, E., P. J. Wright, A. Davidson, and M. Lobigs. 2006. Virulence attenuation of Dengue virus due to augmented glycosaminoglycan-binding affinity and restriction in extraneural dissemination. J. Gen. Virol. 87:2791-2801.
35. Libraty, D. H., T. P. Endy, H. S. Houng, S. Green, S. Kalayanarooj, S. Suntayakorn, W. Chansiriwongs, D. W. Vaughn, A. Nisalak, F. A. Ennis, and A. L. Rothman. 2002. Differing influences of virus burden and immune activation on disease severity in secondary dengue-3 virus infections. J. Infect. Dis. 185:1213-1221.
36. Lin, Y. L., C. L. Liao, L. K. Chen, C. T. Yeh, C. I. Liu, S. H. Ma, Y. Y. Huang, Y. L. Huang, C. L. Kao, and C. C. King. 1998. Study of Dengue virus infection in SCID mice engrafted with human K562 cells. J. Virol. 72:9729-9737.
37. Lyon, M., J. A. Deakin, and J. T. Gallagher. 1994. Liver heparan sulfate structure: a novel molecular design. J. Biol. Chem. 269:11208- 11215.
38. Miagostovich, M., R. Ramos, A. Nicol, R. Nogueira, T. Cuzzi-Maya, A. Oliveira, R. Marchevsky, R. Mesquita, and H. Schatzmayr. 1997. Retrospective study on dengue fatal cases. Clin. Neuropathol. 16:204-208.
39. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2003. A ligand-binding pocket in the dengue virus envelope glycoprotein. Proc. Natl. Acad. Sci. USA 100:6986-6991.
40. Modis, Y., S. Ogata, D. Clements, and S. C. Harrison. 2005. Variable surface epitopes in the crystal structure of dengue virus type 3 envelope glycoprotein. J. Virol. 79:1223-1231.
41. Mukhopadhyay, S., R. J. Kuhn, and M. G. Rossmann. 2005. A structural perspective of the flavivirus life cycle. Nat. Rev. Microbiol. 3:13-22.
42. Navarro-Sanchez, E., R. Altmeyer, A. Amara, O. Schwartz, F. Fieschi, J. L. Virelizier, F. Arenzana-Seisdedos, and P. Despres. 2003. Dendritic-cell-specific ICAM3-grabbing non-integrin is essential for the productive infection of human dendritic cells by mosquito-cell-derived dengue viruses. EMBO Rep. 4:1-6.
43. Nisalak, A., S. Halstead, P. Singharaj, S. Udomsakdi, S. Nye, and K. Vinijchaikul. 1970. Observations related to pathogenesis of dengue hemorrhagic fever. III. Virologie studies of fatal disease. Yale J. Biol. Med. 42:293-310.
44. Ramos, C., G. Sanchez, R. Pando, J. Baquera, D. Hernandez, J. Mota, J. Ramos, A. Flores, and E. Llausas. 1998. Dengue virus in the brain of a fatal case of hemorrhagic dengue fever. J. Neurovirol. 4:465-468.
45. Reddi, H. V., and H. L. Lipton. 2002. Heparan sulfate mediates infection of high-neurovirulence Theiler's viruses. J. Virol. 76:8400-8407.
46. Rosen, L., M. Drouet, and V. Deubel. 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.
47. Ryman, K. D., C. L. Gardner, C. W. Burke, K. C. Meier, J. M. Thompson, and W. B. Klimstra. 2007. Heparan sulfate binding can contribute to the neurovirulence of neuroadapted and nonneuroadapted Sindbis viruses. J. Virol. 81:3563-3573.
48. Ryman, K. D., W. B. Klimstra, K. B. Nguyen, C. A. Biron, and R. E. Johnston. 2000. Alpha/beta interferon protects adult mice from fatal Sindbis virus infection and is an important determinant of cell and tissue tropism. J. Virol. 74:3366-3378.
49. Sa-Carvalho, D., E. Rieder, B. Baxt, R. Rodarte, A. Tanuri, and P. W. Mason. 1997. Tissue culture adaptation of foot-and-mouth disease virus selects viruses that bind to heparin and are attenuated in cattle. J. Virol. 71:5115-5123.
50. Scherer, W. F., R. W. Dickerman, and J. V. Ordonez. 1977. Serologic surveys for antibodies to Western, Eastern, California, and St. Louis encephalitis and Dengue 3 arboviruses in Middle America, 1961-1975. Bull. Pan Am. Health Org. 11:212-223.
51. Shresta, S., J. L. Kyle, P. Robert Beatty, and E. Harris. 2004. Early activation of natural killer and B cells in response to primary dengue virus infection in A/J. mice. Virology 319:262-273.
52. Shresta, S., J. L. Kyle, H. M. Snider, M. Basavapatna, P. R. Beatty, and E. Harris. 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.
53. Shresta, S., K. L. Sharar, D. M. Prigozhin, P. R. Beatty, and E. Harris. 2006. Murine model for dengue virus-induced lethal disease with increased vascular permeability. J. Virol. 80:10208-10217.
54. Tassaneetrithep, B., T. H. Burgess, A. Granelli-Piperno, C. Trumpfheller, J. Finke, W. Sun, M. A. Eller, K. Pattanapanyasat, S. Sarasombath, D. L. Birx, R. M. Steinman, S. Schlesinger, and M. A. Marovich. 2003. DC-SIGN (CD209) mediates dengue virus infection of human dendritic cells. J. Exp. Med. 197:823-829.
55. Van Gennip, H. G., A. C. Vlot, M. M. Hulst, A. J. De Smit, and R. J. Moormann. 2004. Determinants of virulence of classical swine fever virus strain Brescia. J. Virol. 78:8812-8823.
56. Vaughn, D. W., S. Green, S. Kalayanarooj, B. L. Innis, S. Nimmannitya, S. Suntayakorn, T. Endy, B. Raengsakulrach, A. L. Rothman, F. A. Ennis, and A. Nisalak. 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J. Infect. Dis. 181:2-9.
57. Wang, W. K., D. Y. Chao, C. L. Kao, H. C. Wu, Y. C. Liu, C. M. Li, S. C. Lin, S. T. Ho, J. H. Huang, and C. C. King. 2003. High levels of plasma dengue viral load during defervescence in patients with dengue hemorrhagic fever: implications for pathogenesis. Virology 305:330-338.
58. Wu, S. J., C. G. Hayes, D. R. Dubois, M. G. Windheuser, Y. H. Kang, D. M. Watts, and D. G. Sieckmann. 1995. Evaluation of the severe combined immunodeficient (SCID) mouse as an animal model for dengue viral infection. Am. J. Trop. Med. Hyg. 52:468-476.