Development of a reverse-genetics system for murine norovirus 3: Long-term persistence occurs in the caecum and colon

Journal of General Virology

Volumn 93, Issue PART 7, 2012, Pages 1432-1441

  Arias, Armando ^a   Bailey, Dalan ^b   Chaudhry, Yasmin ^a   Goodfellow, Ian ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b INSTITUTE FOR ANIMAL HEALTH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CAPSID PROTEIN; ENECADIN; PROTEIN VP2; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CECUM; CELL CULTURE; COLON; CONTROLLED STUDY; FECES; IN VIVO STUDY; MOUSE; NONHUMAN; NOROVIRUS; NOROVIRUS INFECTION; PERSISTENT VIRUS INFECTION; PRIORITY JOURNAL; REVERSE GENETICS;

ADAPTATION, BIOLOGICAL; ANIMALS; CALICIVIRIDAE INFECTIONS; CECUM; CELL LINE; COLON; DISEASE MODELS, ANIMAL; DNA MUTATIONAL ANALYSIS; FECES; GASTROENTERITIS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; NOROVIRUS; REVERSE GENETICS; RNA, VIRAL; SEQUENCE ANALYSIS, DNA; VIRAL PROTEINS;

EID: 84862686191     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.042176-0     Document Type: Article

References (50)

1. Arias, A., Perales, C., Escarmís, C. & Domingo, E. (2010). Deletion mutants of VPg reveal new cytopathology determinants in a picornavirus. PLoS ONE 5, e10735.
2. Bailey, D., Thackray, L. B. & Goodfellow, I. G. (2008). A single amino acid substitution in the murine norovirus capsid protein is sufficient for attenuation in vivo. J Virol 82, 7725-7728.
3. Bailey, D., Karakasiliotis, I., Vashist, S., Chung, L. M., Rees, J., McFadden, N., Benson, A., Yarovinsky, F., Simmonds, P. & Goodfellow, I. (2010). Functional analysis of RNA structures present at the 39 extremity of the murine norovirus genome: the variable polypyrimidine tract plays a role in viral virulence. J Virol 84, 2859-2870.
4. Barron, E. L., Sosnovtsev, S. V., Bok, K., Prikhodko, V., Sandoval-Jaime, C., Rhodes, C. R., Hasenkrug, K., Carmody, A. B., Ward, J. M. & other authors (2011). Diversity of murine norovirus strains isolated from asymptomatic mice of different genetic backgrounds within a single U.S. research institute. PLoS ONE 6, e21435.
5. Buchholz, U. J., Finke, S. & Conzelmann, K. K. (1999). Generation of bovine respiratory syncytial virus (BRSV) from cDNA: BRSV NS2 is not essential for virus replication in tissue culture, and the human RSV leader region acts as a functional BRSV genome promoter. J Virol 73, 251-259.
6. Byrnes, A. P. & Griffin, D. E. (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.
7. Cadwell, K., Patel, K. K., Maloney, N. S., Liu, T. C., Ng, A. C., Storer, C. E., Head, R. D., Xavier, R., Stappenbeck, T. S. & Virgin, H. W. (2010). Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 141, 1135-1145.
8. Capizzi, T., Makari-Judson, G., Steingart, R. & Mertens, W. C. (2011). Chronic diarrhea associated with persistent norovirus excretion in patients with chronic lymphocytic leukemia: report of two cases. BMC Infect Dis 11, 131.
9. CDC (2002). Outbreak of acute gastroenteritis associated with Norwalk-like viruses among British military personnel - Afghanistan, May 2002. MMWR Morb Mortal Wkly Rep 51, 477-479.
10. Chan, M. C., Lee, N., Ho, W. S., Law, C. O., Lau, T. C., Tsui, S. K. & Sung, J. J. (2012). Covariation of major and minor viral capsid proteins in norovirus genogroup II genotype 4 strains. J Virol 86, 1227-1232.
11. Chaudhry, Y., Nayak, A., Bordeleau, M. E., Tanaka, J., Pelletier, J., Belsham, G. J., Roberts, L. O. & Goodfellow, I. G. (2006). Caliciviruses differ in their functional requirements for eIF4F components. J Biol Chem 281, 25315-25325.
12. Chaudhry, Y., Skinner, M. A. & Goodfellow, I. G. (2007). Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase. J Gen Virol 88, 2091-2100.
13. Chen, S. Y., Tsai, C. N., Lai, M. W., Chen, C. Y., Lin, K. L., Lin, T. Y. & Chiu, C. H. (2009). Norovirus infection as a cause of diarrheaassociated benign infantile seizures. Clin Infect Dis 48, 849-855.
14. Daughenbaugh, K. F., Fraser, C. S., Hershey, J. W. & Hardy, M. E. (2003). The genome-linked protein VPg of the Norwalk virus binds eIF3, suggesting its role in translation initiation complex recruitment. EMBO J 22, 2852-2859.
15. Daughenbaugh, K. F., Wobus, C. E. & Hardy, M. E. (2006). VPg of murine norovirus binds translation initiation factors in infected cells. Virol J 3, 33.
16. Goodfellow, I., Chaudhry, Y., Gioldasi, I., Gerondopoulos, A., Natoni, A., Labrie, L., Laliberté, J. F. & Roberts, L. (2005). Calicivirus translation initiation requires an interaction between VPg and eIF4E. EMBO Rep 6, 968-972.
17. Harris, J. R. & Racaniello, V. R. (2005). Amino acid changes in proteins 2B and 3A mediate rhinovirus type 39 growth in mouse cells. J Virol 79, 5363-5373.
18. Harris, J. P., Edmunds, W. J., Pebody, R., Brown, D. W. & Lopman, B. A. (2008). Deaths from norovirus among the elderly, England and Wales. Emerg Infect Dis 14, 1546-1552.
19. Hsu, C. C., Riley, L. K., Wills, H. M. & Livingston, R. S. (2006). Persistent infection with and serologic cross-reactivity of three novel murine noroviruses. Comp Med 56, 247-251.
20. Hsu, C. C., Riley, L. K. & Livingston, R. S. (2007). Molecular characterization of three novel murine noroviruses. Virus Genes 34, 147-155.
21. Ito, S., Takeshita, S., Nezu, A., Aihara, Y., Usuku, S., Noguchi, Y. & Yokota, S. (2006). Norovirus-associated encephalopathy. Pediatr Infect Dis J 25, 651-652.
22. Kahan, S. M., Liu, G., Reinhard, M. K., Hsu, C. C., Livingston, R. S. & Karst, S. M. (2011). Comparative murine norovirus studies reveal a lack of correlation between intestinal virus titers and enteric pathology. Virology 421, 202-210.
23. Karst, S. M., Wobus, C. E., Lay, M., Davidson, J. & Virgin, H. W., IV (2003). STAT1-dependent innate immunity to a Norwalk-like virus. Science 299, 1575-1578.
24. Khan, R. R., Lawson, A. D., Minnich, L. L., Martin, K., Nasir, A., Emmett, M. K., Welch, C. A. & Udall, J. N., Jr (2009). Gastrointestinal norovirus infection associated with exacerbation of inflammatory bowel disease. J Pediatr Gastroenterol Nutr 48, 328-333.
25. Kitajima, M., Oka, T., Takagi, H., Tohya, Y., Katayama, H., Takeda, N. & Katayama, K. (2010). Development and application of a broadly reactive real-time reverse transcription-PCR assay for detection of murine noroviruses. J Virol Methods 169, 269-273.
26. Koo, H. L., Ajami, N., Atmar, R. L. & DuPont, H. L. (2010). Noroviruses: the leading cause of gastroenteritis worldwide. Discov Med 10, 61-70.
27. Lee, J. H., Alam, I., Han, K. R., Cho, S., Shin, S., Kang, S., Yang, J. M. & Kim, K. H. (2011). Crystal structures of murine norovirus-1 RNAdependent RNA polymerase. J Gen Virol 92, 1607-1616.
28. Lencioni, K. C., Seamons, A., Treuting, P. M., Maggio-Price, L. & Brabb, T. (2008). Murine norovirus: an intercurrent variable in a mouse model of bacteria-induced inflammatory bowel disease. Comp Med 58, 522-533.
29. Lochridge, V. P. & Hardy, M. E. (2007). A single-amino-acid substitution in the P2 domain of VP1 of murine norovirus is sufficient for escape from antibody neutralization. J Virol 81, 12316-12322.
30. Lopman, B. A., Reacher, M. H., Vipond, I. B., Hill, D., Perry, C., Halladay, T., Brown, D. W., Edmunds, W. J. & Sarangi, J. (2004). Epidemiology and cost of nosocomial gastroenteritis, Avon, England, 2002-2003. Emerg Infect Dis 10, 1827-1834.
31. Ludwig, A., Adams, O., Laws, H. J., Schroten, H. & Tenenbaum, T. (2008). Quantitative detection of norovirus excretion in pediatric patients with cancer and prolonged gastroenteritis and shedding of norovirus. J Med Virol 80, 1461-1467.
32. McFadden, N., Bailey, D., Carrara, G., Benson, A., Chaudhry, Y., Shortland, A., Heeney, J., Yarovinsky, F., Simmonds, P. & other authors (2011). Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 7, e1002413.
33. Mead, P. S., Slutsker, L., Dietz, V., McCaig, L. F., Bresee, J. S., Shapiro, C., Griffin, P. M. & Tauxe, R. V. (1999). Food-related illness and death in the United States. Emerg Infect Dis 5, 607-625.
34. Monroe, S. S. (2011). Control and prevention of viral gastroenteritis. Emerg Infect Dis 17, 1347-1348.
35. Mumphrey, S. M., Changotra, H., Moore, T. N., Heimann-Nichols, E. R., Wobus, C. E., Reilly, M. J., Moghadamfalahi, M., Shukla, D. & Karst, S. M. (2007). Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J Virol 81, 3251-3263.
36. Núñez, J. I., Baranowski, E., Molina, N., Ruiz-Jarabo, C. M., Sánchez, C., Domingo, E. & Sobrino, F. (2001). A single amino acid substitution in nonstructural protein 3A can mediate adaptation of foot-and-mouth disease virus to the guinea pig. J Virol 75, 3977-3983.
37. Patel, M. M., Widdowson, M. A., Glass, R. I., Akazawa, K., Vinjé, J. & Parashar, U. D. (2008). Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14, 1224-1231.
38. Phillips, G., Tam, C. C., Rodrigues, L. C. & Lopman, B. (2010). Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiol Infect 138, 1454-1458.
39. Sosnovtsev, S. V., Belliot, G., Chang, K. O., Onwudiwe, O. & Green, K. Y. (2005). Feline calicivirus VP2 is essential for the production of infectious virions. J Virol 79, 4012-4024.
40. Sosnovtsev, S. V., Belliot, G., Chang, K. O., Prikhodko, V. G., Thackray, L. B., Wobus, C. E., Karst, S. M., Virgin, H. W. & Green, K. Y. (2006). Cleavage map and proteolytic processing of the murine norovirus nonstructural polyprotein in infected cells. J Virol 80, 7816-7831.
41. Strong, D. W., Thackray, L. B., Smith, T. J. & Virgin, H. W. (2012). Protruding domain of capsid protein is necessary and sufficient to determine murine norovirus replication and pathogenesis in vivo. J Virol 86, 2950-2958.
42. Taube, S., Rubin, J. R., Katpally, U., Smith, T. J., Kendall, A., Stuckey, J. A. & Wobus, C. E. (2010). High-resolution X-ray structure and functional analysis of the murine norovirus 1 capsid protein protruding domain. J Virol 84, 5695-5705.
43. Thackray, L. B., Wobus, C. E., Chachu, K. A., Liu, B., Alegre, E. R., Henderson, K. S., Kelley, S. T. & Virgin, H. W., IV (2007). Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J Virol 81, 10460-10473.
44. van Asten, L., Siebenga, J., van den Wijngaard, C., Verheij, R., van Vliet, H., Kretzschmar, M., Boshuizen, H., van Pelt, W. & Koopmans, M. (2011). Unspecified gastroenteritis illness and deaths in the elderly associated with norovirus epidemics. Epidemiology 22, 336-343.
45. Vernacchio, L., Vezina, R. M., Mitchell, A. A., Lesko, S. M., Plaut, A. G. & Acheson, D. W. (2006). Characteristics of persistent diarrhea in a community-based cohort of young US children. J Pediatr Gastroenterol Nutr 43, 52-58.
46. Walker, S. C., Avis, J. M. & Conn, G. L. (2003). General plasmids for producing RNA in vitro transcripts with homogeneous ends. Nucleic Acids Res 31, e82.
47. Ward, V. K., McCormick, C. J., Clarke, I. N., Salim, O., Wobus, C. E., Thackray, L. B., Virgin, H. W., IV & Lambden, P. R. (2007). Recovery of infectious murine norovirus using pol II-driven expression of fulllength cDNA. Proc Natl Acad Sci U S A 104, 11050-11055.
48. Wobus, C. E., Karst, S. M., Thackray, L. B., Chang, K. O., Sosnovtsev, S. V., Belliot, G., Krug, A., Mackenzie, J. M., Green, K. Y. & Virgin, H. W. (2004). Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2, e432.
49. Wobus, C. E., Thackray, L. B. & Virgin, H. W., IV (2006). Murine norovirus: a model system to study norovirus biology and pathogenesis. J Virol 80, 5104-5112.
50. Yunus, M. A., Chung, L. M., Chaudhry, Y., Bailey, D. & Goodfellow, I. (2010). Development of an optimized RNA-based murine norovirus reverse genetics system. J Virol Methods 169, 112-118.