Spectrum of disease outcomes in mice infected with YFV-17D

Journal of General Virology

Volumn 96, Issue , 2015, Pages 1328-1339

  Erickson, Andrea K ^a   Pfeiffer, Julie K ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA INTERFERON; BETA INTERFERON RECEPTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; MONOCYTE CHEMOTACTIC PROTEIN; CXCL10 PROTEIN, MOUSE; INTERFERON; MONOCYTE CHEMOTACTIC PROTEIN 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD; BRAIN; ENZYME LINKED IMMUNOSORBENT ASSAY; FLAVIVIRUS INFECTION; HUMAN; IMMUNE RESPONSE; IMMUNOPATHOGENESIS; INTESTINAL BLEEDING; LIVER; MUSCLE; NONHUMAN; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; SCIATIC NERVE; SPLEEN; VIRUS LOAD; VIRUS TITRATION; ANIMAL; C57BL MOUSE; DEFICIENCY; DISEASE MODEL; GASTROINTESTINAL HEMORRHAGE; INTESTINE; KNOCKOUT MOUSE; PATHOLOGY; PHYSIOLOGY; SURVIVAL ANALYSIS; VIROLOGY; YELLOW FEVER; YELLOW FEVER VIRUS;

FLAVIVIRUS; MUS; YELLOW FEVER VIRUS;

ALANINE TRANSAMINASE; ANIMALS; BRAIN; CHEMOKINE CCL2; CHEMOKINE CXCL10; DISEASE MODELS, ANIMAL; GASTROINTESTINAL HEMORRHAGE; INTERFERON TYPE I; INTESTINES; LIVER; MICE, INBRED C57BL; MICE, KNOCKOUT; SPLEEN; SURVIVAL ANALYSIS; VIRAL LOAD; YELLOW FEVER; YELLOW FEVER VIRUS;

EID: 84937611357     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.000075     Document Type: Article

References (66)

1. Anonymous (1966). Fatal viral encephalitis following 17D yellow fever vaccine inoculation. Report of a case in a 3-year-old child. JAMA 198, 671-672.
2. Bae, H.-G., Domingo, C., Tenorio, A., de Ory, F., Muñoz, J., Weber, P., Teuwen, D. E. & Niedrig, M. (2008). Immune response during adverse events after 17D-derived yellow fever vaccination in Europe. J Infect Dis 197, 1577-1584.
3. Barrett, A. D. & Gould, E. A. (1986). Comparison of neurovirulence of different strains of yellow fever virus in mice. J Gen Virol 67, 631-637.
4. Beck, A., Tesh, R. B., Wood, T. G., Widen, S. G., Ryman, K. D. & Barrett, A. D. (2014). Comparison of the live attenuated yellow fever vaccine 17D-204 strain to its virulent parental strain Asibi by deep sequencing. J Infect Dis 209, 334-344.
5. Belsher, J. L., Gay, P., Brinton, M., DellaValla, J., Ridenour, R., Lanciotti, R., Perelygin, A., Zaki, S., Paddock, C. & other authors (2007). Fatal multiorgan failure due to yellow fever vaccineassociated viscerotropic disease. Vaccine 25, 8480-8485.
6. Brown, A. N., Kent, K. A., Bennett, C. J. & Bernard, K. A. (2007). Tissue tropism and neuroinvasion of West Nile virus do not differ for two mouse strains with different survival rates. Virology 368, 422-430.
7. Card, J. P., Whealy, M. E., Robbins, A. K., Moore, R. Y. & Enquist, L. W. (1991). Two alpha-herpesvirus strains are transported differentially in the rodent visual system. Neuron 6, 957-969.
8. Centers for Disease Control and Prevention (2002). Adverse events associated with 17D-derived yellow fever vaccination-United States, 2001-2002. MMWR Morb Mortal Wkly Rep 51, 989-993.
9. Cetron, M. S., Marfin, A. A., Julian, K. G., Gubler, D. J., Sharp, D. J., Barwick, R. S., Weld, L. H., Chen, R., Clover, R. D. & other authors (2002). Yellow fever vaccine. Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2002. MMWR Recomm Rep 51 (RR-17), 1-11.
10. Chan, R. C., Penney, D. J., Little, D., Carter, I. W., Roberts, J. A. & Rawlinson, W. D. (2001). Hepatitis and death following vaccination with 17D-204 yellow fever vaccine. Lancet 358, 121-122.
11. Chen, H. W., King, K., Tu, J., Sanchez, M., Luster, A. D. & Shresta, S. (2013). The roles of IRF-3 and IRF-7 in innate antiviral immunity against dengue virus. J Immunol 191, 4194-4201.
12. Dominguez, A. & Baruch, E. (1963). Histopathology of the central nervous system in Swiss mice intracerebrally inoculated with 17-D strain of yellow fever virus. Am J Trop Med Hyg 12, 815-819.
13. Erickson, A. K. & Pfeiffer, J. K. (2013). Dynamic viral dissemination in mice infected with yellow fever virus strain 17D. J Virol 87, 12392-12397.
14. Fink, J., Gu, F., Ling, L., Tolfvenstam, T., Olfat, F., Chin, K. C., Aw, P., George, J., Kuznetsov, V. A. & other authors (2007). Host gene expression profiling of dengue virus infection in cell lines and patients. PLoS Negl Trop Dis 1, e86.
15. Fitzgeorge, R. & Bradish, C. J. (1980). The in vivo differentiation of strains of yellow fever virus in mice. J Gen Virol 46, 1-13.
16. Fox, J. P. (1943). Immunity to yellow fever encephalitis of monkeys and mice immunized by neural and extraneural routes. J Exp Med 77, 487-506.
17. Gerasimon, G. & Lowry, K. (2005). Rare case of fatal yellow fever vaccine-associated viscerotropic disease. South Med J 98, 653-656.
18. Goodman, G. T. & Koprowski, H. (1962). Macrophages as a cellular expression of inherited natural resistance. Proc Natl Acad Sci U S A 48, 160-165.
19. Guirakhoo, F., Kitchener, S., Morrison, D., Forrat, R., McCarthy, K., Nichols, R., Yoksan, S., Duan, X., Ermak, T. H. & other authors (2006). Live attenuated chimeric yellow fever dengue type 2 (ChimeriVax-DEN2) vaccine: Phase I clinical trial for safety and immunogenicity: effect of yellow fever pre-immunity in induction of cross neutralizing antibody responses to all 4 dengue serotypes. Hum Vaccin 2, 60-67.
20. Guy, B., Guirakhoo, F., Barban, V., Higgs, S., Monath, T. P. & Lang, J. (2010). Preclinical and clinical development of YFV 17D-based chimeric vaccines against dengue, West Nile and Japanese encephalitis viruses. Vaccine 28, 632-649.
21. Hahn, C. S., Dalrymple, J. M., Strauss, J. H. & Rice, C. M. (1987). Comparison of the virulent Asibi strain of yellow fever virus with the 17D vaccine strain derived from it. Proc Natl Acad Sci U S A 84, 2019-2023.
22. Hase, T., Dubois, D. R. & Summers, P. L. (1990). Comparative study of mouse brains infected with Japanese encephalitis virus by intracerebral or intraperitoneal inoculation. Int J Exp Pathol 71, 857-869.
23. Horsfall, F. L. & Tam, I. (editors) (1965). Viral and Rickettsial Infections of Man, 4th edn. Philadelphia, PA: Lippincott.
24. Hsieh, M. F., Lai, S. L., Chen, J. P., Sung, J. M., Lin, Y. L., Wu-Hsieh, B. A., Gerard, C., Luster, A. & Liao, F. (2006). Both CXCR3 and CXCL10/IFN-inducible protein 10 are required for resistance to primary infection by dengue virus. J Immunol 177, 1855-1863.
25. Ida-Hosonuma, M., Iwasaki, T., Yoshikawa, T., Nagata, N., Sato, Y., Sata, T., Yoneyama, M., Fujita, T., Taya, C. & other authors (2005). The alpha/beta interferon response controls tissue tropism and pathogenicity of poliovirus. J Virol 79, 4460-4469.
26. Kengsakul, K., Sathirapongsasuti, K. & Punyagupta, S. (2002). Fatal myeloencephalitis following yellow fever vaccination in a case with HIV infection. J Med Assoc Thai 85, 131-134.
27. Khaiboullina, S. F., Rizvanov, A. A., Holbrook, M. R. & St Jeor, S. (2005). Yellow fever virus strains Asibi and 17D-204 infect human umbilical cord endothelial cells and induce novel changes in gene expression. Virology 342, 167-176.
28. Klein, R. S., Lin, E., Zhang, B., Luster, A. D., Tollett, J., Samuel, M. A., Engle, M. & Diamond, M. S. (2005). Neuronal CXCL10 directs CD8+T-cell recruitment and control of West Nile virus encephalitis. J Virol 79, 11457-11466.
29. Kumar, M., Roe, K., Orillo, B., Muruve, D. A., Nerurkar, V. R., Gale, M., Jr & Verma, S. (2013). Inflammasome adaptor protein Apoptosisassociated speck-like protein containing CARD (ASC) is critical for the immune response and survival in West Nile virus encephalitis. J Virol 87, 3655-3667.
30. Lee, E. & Lobigs,M. (2008). E protein domain III determinants of yellow fever virus 17D vaccine strain enhance binding to glycosaminoglycans, impede virus spread, and attenuate virulence. J Virol 82, 6024-6033.
31. Lee, E., Wright, P. J., Davidson, A. & Lobigs, M. (2006a). Virulence attenuation of Dengue virus due to augmented glycosaminoglycanbinding affinity and restriction in extraneural dissemination. J Gen Virol 87, 2791-2801.
32. Lee, Y. R., Liu, M. T., Lei, H. Y., Liu, C. C., Wu, J. M., Tung, Y. C., Lin, Y. S., Yeh, T. M., Chen, S. H. & Liu, H. S. (2006b). MCP-1, a highly expressed chemokine in dengue haemorrhagic fever/dengue shock syndrome patients, may cause permeability change, possibly through reduced tight junctions of vascular endothelium cells. J Gen Virol 87, 3623-3630.
33. Liprandi, F. & Walder, R. (1983). Replication of virulent and attenuated strains of yellow fever virus in human monocytes and macrophage-like cells (U937). Arch Virol 76, 51-61.
34. Liu, T. & Chambers, T. J. (2001). Yellow fever virus encephalitis: properties of the brain-associated T-cell response during virus clearance in normal and gamma interferon-deficient mice and requirement for CD4+lymphocytes. J Virol 75, 2107-2118.
35. Liu, M., Guo, S., Hibbert, J. M., Jain, V., Singh, N., Wilson, N. O. & Stiles, J. K. (2011). CXCL10/IP-10 in infectious diseases pathogenesis and potential therapeutic implications. Cytokine Growth Factor Rev 22, 121-130.
36. Martin, M., Tsai, T. F., Cropp, B., Chang, G. J., Holmes, D. A., Tseng, J., Shieh, W., Zaki, S. R., Al-Sanouri, I. & other authors (2001). Fever and multisystem organ failure associated with 17D-204 yellow fever vaccination: a report of four cases. Lancet 358, 98-104.
37. Mateo, R. I., Xiao, S. Y., Travassos da Rosa, A. P., Lei, H., Guzman, H., Lu, L. & Tesh, R. B. (2007). Yellow fever 17-D vaccine is neurotropic and produces encephalitis in immunosuppressed hamsters. Am J Trop Med Hyg 77, 919-924.
38. Meier, K. C., Gardner, C. L., Khoretonenko, M. V., Klimstra, W. B. & Ryman, K. D. (2009). A mouse model for studying viscerotropic disease caused by yellow fever virus infection. PLoS Pathog 5, e1000614.
39. Monath, T. P. (2008). Treatment of yellow fever. Antiviral Res 78, 116-124.
40. Monath, T. P. & Barrett, A. D. (2003). Pathogenesis and pathophysiology of yellow fever. Adv Virus Res 60, 343-395.
41. Monath, T. P., Guirakhoo, F., Nichols, R., Yoksan, S., Schrader, R., Murphy, C., Blum, P., Woodward, S., McCarthy, K. & other authors (2003). Chimeric live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J Infect Dis 188, 1213-1230.
42. Monath, T. P., Liu, J., Kanesa-Thasan, N., Myers, G. A., Nichols, R., Deary, A., McCarthy, K., Johnson, C., Ermak, T. & other authors (2006). A live, attenuated recombinant West Nile virus vaccine. Proc Natl Acad Sci U S A 103, 6694-6699.
43. Monath, T. P., Gershman, M., Staples, J. E. & Barrett, A. D. (2013). Yellow fever vaccine. In Vaccines, 6th edn, pp. 870-968. Edited by S. A. Plotkin, W. Orenstein & P. A. Offit. London: Saunders.
44. Ohka, S., Yang, W. X., Terada, E., Iwasaki, K. & Nomoto, A. (1998). Retrograde transport of intact poliovirus through the axon via the fast transport system. Virology 250, 67-75.
45. Paessler, S. & Walker, D. H. (2013). Pathogenesis of the viral hemorrhagic fevers. Annu Rev Pathol 8, 411-440.
46. Prestwood, T. R., Prigozhin, D. M., Sharar, K. L., Zellweger, R. M. & Shresta, S. (2008). A mouse-passaged dengue virus strain with reduced affinity for heparan sulfate causes severe disease in mice by establishing increased systemic viral loads. J Virol 82, 8411-8421.
47. Pugachev, K. V., Guirakhoo, F. & Monath, T. P. (2005). New developments in flavivirus vaccines with special attention to yellow fever. Curr Opin Infect Dis 18, 387-394.
48. Querec, T. D., Akondy, R. S., Lee, E. K., Cao, W., Nakaya, H. I., Teuwen, D., Pirani, A., Gernert, K., Deng, J. & other authors (2009). Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol 10, 116-125.
49. Rathakrishnan, A., Wang, S. M., Hu, Y., Khan, A. M., Ponnampalavanar, S., Lum, L. C., Manikam, R. & Sekaran, S. D. (2012). Cytokine expression profile of dengue patients at different phases of illness. PLoS One 7, e52215.
50. Samuel, M. A., Wang, H., Siddharthan, V., Morrey, J. D. & Diamond, M. S. (2007). Axonal transport mediates West Nile virus entry into the central nervous system and induces acute flaccid paralysis. Proc Natl Acad Sci U S A 104, 17140-17145.
51. Schlesinger, J. J. & Brandriss, M. W. (1981). Antibody-mediated infection of macrophages and macrophage-like cell lines with 17Dyellow fever virus. J Med Virol 8, 103-117.
52. Sellards, A. W. (1931). The behavior of the virus of yellow fever in monkeys and mice. Proc Natl Acad Sci U S A 17, 339-343.
53. Shehan, D. C. H. & Barbara, B. (1980). Theory and Practice of Histotechnology, 2nd edn. Columbus, OH: Battelle Press.
54. Shirato, K., Kimura, T., Mizutani, T., Kariwa, H. & Takashima, I. (2004). Different chemokine expression in lethal and non-lethal murine West Nile virus infection. J Med Virol 74, 507-513.
55. Silva, M. L., Espírito-Santo, L. R., Martins, M. A., Silveira-Lemos, D., Peruhype-Magalhães, V., Caminha, R. C., de Andrade Maranhão-Filho, P., Auxiliadora-Martins, M., de Menezes Martins, R. & other authors (2010). Clinical and immunological insights on severe, adverse neurotropic and viscerotropic disease following 17D yellow fever vaccination. Clin Vaccine Immunol 17, 118-126.
56. Sung, J. M., Lee, C. K. & Wu-Hsieh, B. A. (2012). Intrahepatic infiltrating NK and CD8 T cells cause liver cell death in different phases of dengue virus infection. PLoS One 7, e46292.
57. ter Meulen, J., Sakho, M., Koulemou, K., Magassouba, N., Bah, A., Preiser, W., Daffis, S., Klewitz, C., Bae, H. G. & other authors (2004). Activation of the cytokine network and unfavorable outcome in patients with yellow fever. J Infect Dis 190, 1821-1827.
58. Theiler, M. (1930). Susceptibility of white mice to the virus of yellow fever. Science 71, 367.
59. Thibodeaux, B. A., Garbino, N. C., Liss, N. M., Piper, J., Blair, C. D. & Roehrig, J. T. (2012). A small animal peripheral challenge model of yellow fever using interferon-receptor deficient mice and the 17D-204 vaccine strain. Vaccine 30, 3180-3187.
60. Tyler, K. L., McPhee, D. A. & Fields, B. N. (1986). Distinct pathways of viral spread in the host determined by reovirus S1 gene segment. Science 233, 770-774.
61. Vasconcelos, P. F., Luna, E. J., Galler, R., Silva, L. J., Coimbra, T. L., Barros, V. L., Monath, T. P., Rodigues, S. G., Laval, C. & other authors (2001). Serious adverse events associated with yellow fever 17DD vaccine in Brazil: a report of two cases. Lancet 358, 91-97.
62. Wang, T., Town, T., Alexopoulou, L., Anderson, J. F., Fikrig, E. & Flavell, R. A. (2004). Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10, 1366-1373.
63. Wang, P. Z., Li, Z. D., Yu, H. T., Zhang, Y., Wang, W., Jiang, W. & Bai, X. F. (2012). Elevated serum concentrations of inflammatory cytokines and chemokines in patients with haemorrhagic fever with renal syndrome. J Int Med Res 40, 648-656.
64. Wauquier, N., Becquart, P., Padilla, C., Baize, S. & Leroy, E. M. (2010). Human fatal Zaire ebola virus infection is associated with an aberrant innate immunity and with massive lymphocyte apoptosis. PLoS Negl Trop Dis 4, e837.
65. Woods, A.E. & Roy, C. (1996). Laboratory Histopathology: A Complete Reference. London: Churchill Livingston.
66. Zisman, B., Wheelock, E. F. & Allison, A. C. (1971). Role of macrophages and antibody in resistance of mice against yellow fever virus. J Immunol 107, 236-243.