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Abstract

Noroviruses (NoVs) are highly prevalent, positive-sense RNA viruses that infect a range of mammals, including humans and mice. Murine noroviruses (MuNoVs) are the most prevalent pathogens in biomedical research colonies, and they have been used extensively as a model system for human noroviruses (HuNoVs). Despite recent successes in culturing HuNoVs in the laboratory and a small animal host, studies of human viruses have inherent limitations. Thus, owing to its versatility, the MuNoV system—with its native host, reverse genetics, and cell culture systems—will continue to provide important insights into NoV and enteric virus biology. In the current review, we summarize recent findings from MuNoVs that increase our understanding of enteric virus pathogenesis and highlight similarities between human and murine NoVs that underscore the value of MuNoVs to inform studies of HuNoV biology. We also discuss the potential of endemic MuNoV infections to impact other disease models.

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2015-11-09
2024-12-07
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Literature Cited

  1. Mumphrey SM, Changotra H, Moore TN, Heimann-Nichols ER, Wobus CE. 1.  et al. 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. 81:3251–63 [Google Scholar]
  2. Karst SM, Wobus CE, Lay M, Davidson J, Virgin HW IV. 2.  2003. STAT1-dependent innate immunity to a Norwalk-like virus. Science 299:1575–78 [Google Scholar]
  3. Hsu CC, Wobus CE, Steffen EK, Riley LK, Livingston RS. 3.  2005. Development of a microsphere-based serologic multiplexed fluorescent immunoassay and a reverse transcriptase PCR assay to detect murine norovirus 1 infection in mice. Clin. Vaccine Immunol. 12:1145–51 [Google Scholar]
  4. Henderson KS. 4.  2008. Murine norovirus, a recently discovered and highly prevalent viral agent of mice. Lab. Anim. 37:314–20 [Google Scholar]
  5. Xiang Z, Tian S, Tong W, Chang H, Su J. 5.  et al. 2014. MNV primarily surveillance by a recombination VP1-derived ELISA in Beijing area in China. J. Immunol. Methods 408:70–77 [Google Scholar]
  6. Mahler M, Kohl W. 6.  2009. A serological survey to evaluate contemporary prevalence of viral agents and Mycoplasma pulmonis in laboratory mice and rats in western Europe. Lab. Anim. 38:161–65 [Google Scholar]
  7. Pritchett-Corning KR, Cosentino J, Clifford CB. 7.  2009. Contemporary prevalence of infectious agents in laboratory mice and rats. Lab. Anim. 43:165–73 [Google Scholar]
  8. Cadwell K. 8.  2015. Expanding the role of the virome: commensalism in the gut. J. Virol. 89:1951–53 [Google Scholar]
  9. Green KY. 9.  2013. Caliciviridae: the noroviruses. Fields Virology DM Knipe, PM Howley 582–608 Philadelphia: Lippincott Williams & Wilkins, 6th ed.. [Google Scholar]
  10. Vongpunsawad S, Venkataram Prasad BV, Estes MK. 10.  2013. Norwalk virus minor capsid protein VP2 associates within the VP1 shell domain. J. Virol. 87:4818–25 [Google Scholar]
  11. Glass PJ, White LJ, Ball JM, Leparc-Goffart I, Hardy ME, Estes MK. 11.  2000. Norwalk virus open reading frame 3 encodes a minor structural protein. J. Virol. 74:6581–91 [Google Scholar]
  12. McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y. 12.  et al. 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 [Google Scholar]
  13. Thackray LB, Wobus CE, Chachu KA, Liu B, Alegre ER. 13.  et al. 2007. Murine noroviruses comprising a single genogroup exhibit biological diversity despite limited sequence divergence. J. Virol. 81:10460–73 [Google Scholar]
  14. Kroneman A, Vega E, Vennema H, Vinje J, White PA. 14.  et al. 2013. Proposal for a unified norovirus nomenclature and genotyping. Arch. Virol. 158:2059–68 [Google Scholar]
  15. Vinje J. 15.  2015. Advances in laboratory methods for detection and typing of norovirus. J. Clin. Microbiol. 53:373–81 [Google Scholar]
  16. Siebenga JJ, Vennema H, Zheng DP, Vinje J, Lee BE. 16.  et al. 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII.4 variants, 2001–2007. J. Infect. Dis. 200:802–12 [Google Scholar]
  17. Vega E, Barclay L, Gregoricus N, Shirley SH, Lee D, Vinje J. 17.  2014. Genotypic and epidemiologic trends of norovirus outbreaks in the United States, 2009 to 2013. J. Clin. Microbiol. 52:147–55 [Google Scholar]
  18. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P. 18.  et al. 2014. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet. Infect. Dis. 14:725–30 [Google Scholar]
  19. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. 19.  2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14:1224–31 [Google Scholar]
  20. Hall AJ, Lopman BA, Payne DC, Patel MM, Gastanaduy PA. 20.  et al. 2013. Norovirus disease in the United States. Emerg. Infect. Dis. 19:1198–205 [Google Scholar]
  21. Becker-Dreps S, Bucardo F, Vilchez S, Zambrana LE, Liu L. 21.  et al. 2014. Etiology of childhood diarrhea after rotavirus vaccine introduction: a prospective, population-based study in Nicaragua. Pediatr. Infect. Dis. J. 33:1156–63 [Google Scholar]
  22. Koo HL, Neill FH, Estes MK, Munoz FM, Cameron A. 22.  et al. 2013. Noroviruses: the most common pediatric viral enteric pathogen at a large university hospital after introduction of rotavirus vaccination. J. Pediatr. Infect. Dis. Soc. 2:57–60 [Google Scholar]
  23. Hemming M, Rasanen S, Huhti L, Paloniemi M, Salminen M, Vesikari T. 23.  2013. Major reduction of rotavirus, but not norovirus, gastroenteritis in children seen in hospital after the introduction of RotaTeq vaccine into the National Immunization Programme in Finland. Eur. J. Pediatr. 172:739–46 [Google Scholar]
  24. Scharff RL. 24.  2010. Health related costs from foodborne illness in the United States Rep., Produce Saf. Proj, Georgetown Univ., Washington, DC [Google Scholar]
  25. Hoffmann S, Batz MB, Morris JG Jr. 25.  2012. Annual cost of illness and quality-adjusted life year losses in the United States due to 14 foodborne pathogens. J. Food Prot. 75:1292–302 [Google Scholar]
  26. Lopman B, Gastanaduy P, Park GW, Hall AJ, Parashar UD, Vinje J. 26.  2012. Environmental transmission of norovirus gastroenteritis. Curr. Opin. Virol. 2:96–102 [Google Scholar]
  27. Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J. 27.  2006. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J. Food Prot. 69:2761–65 [Google Scholar]
  28. Manuel CA, Hsu CC, Riley LK, Livingston RS. 28.  2008. Soiled-bedding sentinel detection of murine norovirus 4. J. Am. Assoc. Lab. Anim. Sci. 47:31–36 [Google Scholar]
  29. Teunis PF, Moe CL, Liu P, Miller SE, Lindesmith L. 29.  et al. 2008. Norwalk virus: How infectious is it?. J. Med. Virol. 80:1468–76 [Google Scholar]
  30. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE. 30.  et al. 2014. Determination of the 50% human infectious dose for Norwalk virus. J. Infect. Dis. 209:1016–22 [Google Scholar]
  31. Teunis PF, Sukhrie FH, Vennema H, Bogerman J, Beersma MF, Koopmans MP. 31.  2015. Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol. Infect. 143:1710–17 [Google Scholar]
  32. Mathijs E, Stals A, Baert L, Botteldoorn N, Denayer S. 32.  et al. 2012. A review of known and hypothetical transmission routes for noroviruses. Food Environ. Virol. 4:131–52 [Google Scholar]
  33. Bitler EJ, Matthews JE, Dickey BW, Eisenberg JN, Leon JS. 33.  2013. Norovirus outbreaks: a systematic review of commonly implicated transmission routes and vehicles. Epidemiol. Infect. 141:1563–71 [Google Scholar]
  34. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR. 34.  et al. 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346:755–59 [Google Scholar]
  35. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV. 35.  et al. 2004. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLOS Biol. 2:e432 [Google Scholar]
  36. Ward VK, McCormick CJ, Clarke IN, Salim O, Wobus CE. 36.  et al. 2007. Recovery of infectious murine norovirus using pol II-driven expression of full-length cDNA. PNAS 104:11050–55 [Google Scholar]
  37. Arias A, Urena L, Thorne L, Yunus MA, Goodfellow I. 37.  2012. Reverse genetics mediated recovery of infectious murine norovirus. J. Vis. Exp. 2012:e4145 [Google Scholar]
  38. Chaudhry Y, Skinner MA, Goodfellow IG. 38.  2007. Recovery of genetically defined murine norovirus in tissue culture by using a fowlpox virus expressing T7 RNA polymerase. J. Gen. Virol. 88:2091–100 [Google Scholar]
  39. Wobus CE, Thackray LB, Virgin HW IV. 39.  2006. Murine norovirus: a model system to study norovirus biology and pathogenesis. J. Virol. 80:5104–12 [Google Scholar]
  40. Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW. 40.  2014. Advances in norovirus biology. Cell Host Microbe 15:668–80 [Google Scholar]
  41. Thorne LG, Goodfellow IG. 41.  2014. Norovirus gene expression and replication. J. Gen. Virol. 95:278–91 [Google Scholar]
  42. Lay MK, Atmar RL, Guix S, Bharadwaj U, He H. 42.  et al. 2010. Norwalk virus does not replicate in human macrophages or dendritic cells derived from the peripheral blood of susceptible humans. Virology 406:1–11 [Google Scholar]
  43. Papafragkou E, Hewitt J, Park GW, Greening G, Vinje J. 43.  2013. Challenges of culturing human norovirus in three-dimensional organoid intestinal cell culture models. PLOS ONE 8:e63485 [Google Scholar]
  44. Duizer E, Schwab KJ, Neill FH, Atmar RL, Koopmans MP, Estes MK. 44.  2004. Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85:79–87 [Google Scholar]
  45. Herbst-Kralovetz MM, Radtke AL, Lay MK, Hjelm BE, Bolick AN. 45.  et al. 2013. Lack of norovirus replication and histo-blood group antigen expression in 3-dimensional intestinal epithelial cells. Emerg. Infect. Dis. 19:431–38 [Google Scholar]
  46. Takanashi S, Saif LJ, Hughes JH, Meulia T, Jung K. 46.  et al. 2014. Failure of propagation of human norovirus in intestinal epithelial cells with microvilli grown in three-dimensional cultures. Arch. Virol. 159:257–66 [Google Scholar]
  47. Ward JM, Wobus CE, Thackray LB, Erexson CR, Faucette LJ. 47.  et al. 2006. Pathology of immunodeficient mice with naturally occurring murine norovirus infection. Toxicol. Pathol. 34:708–15 [Google Scholar]
  48. Bok K, Prikhodko VG, Green KY, Sosnovtsev SV. 48.  2009. Apoptosis in murine norovirus-infected RAW264.7 cells is associated with downregulation of survivin. J. Virol. 83:3647–56 [Google Scholar]
  49. Bok K, Parra GI, Mitra T, Abente E, Shaver CK. 49.  et al. 2011. Chimpanzees as an animal model for human norovirus infection and vaccine development. PNAS 108:325–30 [Google Scholar]
  50. Chan MC, Ho WS, Sung JJ. 50.  2011. In vitro whole-virus binding of a norovirus genogroup II genotype 4 strain to cells of the lamina propria and Brunner's glands in the human duodenum. J. Virol. 85:8427–30 [Google Scholar]
  51. Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA. 51.  et al. 2013. A mouse model for human norovirus. mBio 4:e00450–13 [Google Scholar]
  52. Gonzalez-Hernandez MB, Liu T, Blanco LP, Auble H, Payne HC, Wobus CE. 52.  2013. Murine norovirus transcytosis across an in vitro polarized murine intestinal epithelial monolayer is mediated by M-like cells. J. Virol. 87:12685–93 [Google Scholar]
  53. Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M. 53.  et al. 2014. Efficient norovirus and reovirus replication in the mouse intestine requires microfold (M) cells. J. Virol. 88:6934–43 [Google Scholar]
  54. Miller H, Zhang J, Kuolee R, Patel GB, Chen W. 54.  2007. Intestinal M cells: the fallible sentinels?. World J. Gastroenterol. 13:1477–86 [Google Scholar]
  55. Neutra MR, Frey A, Kraehenbuhl JP. 55.  1996. Epithelial M cells: gateways for mucosal infection and immunization. Cell 86:345–48 [Google Scholar]
  56. Basic M, Keubler LM, Buettner M, Achard M, Breves G. 56.  et al. 2014. Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm. Bowel Dis. 20:431–43 [Google Scholar]
  57. Makino A, Shimojima M, Miyazawa T, Kato K, Tohya Y, Akashi H. 57.  2006. Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J. Virol. 80:4482–90 [Google Scholar]
  58. Taube S, Jiang M, Wobus CE. 58.  2010. Glycosphingolipids as receptors for non-enveloped viruses. Viruses 2:1011–49 [Google Scholar]
  59. Ruvoen-Clouet N, Belliot G, Le Pendu J. 59.  2013. Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. Rev. Med. Virol. 23:355–66 [Google Scholar]
  60. Tan M, Jiang X. 60.  2011. Norovirus-host interaction: multi-selections by human histo-blood group antigens. Trends Microbiol. 19:382–88 [Google Scholar]
  61. Zakhour M, Ruvoen-Clouet N, Charpilienne A, Langpap B, Poncet D. 61.  et al. 2009. The αGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. PLOS Pathog. 5:e1000504 [Google Scholar]
  62. Caddy S, Breiman A, Le Pendu J, Goodfellow I. 62.  2014. Genogroup IV and VI canine noroviruses interact with histo-blood group antigens. J. Virol. 88:10377–91 [Google Scholar]
  63. Singh BK, Glatt S, Ferrer JL, Koromyslova AD, Leuthold MM. 63.  et al. 2014. Structural analysis of a feline norovirus protruding domain. Virology 474:181–85 [Google Scholar]
  64. Tamura M, Natori K, Kobayashi M, Miyamura T, Takeda N. 64.  2004. Genogroup II noroviruses efficiently bind to heparan sulfate proteoglycan associated with the cellular membrane. J. Virol. 78:3817–26 [Google Scholar]
  65. Rydell GE, Nilsson J, Rodriguez-Diaz J, Ruvoen-Clouet N, Svensson L. 65.  et al. 2009. Human noroviruses recognize sialyl Lewis x neoglycoprotein. Glycobiology 19:309–20 [Google Scholar]
  66. Bally M, Rydell GE, Zahn R, Nasir W, Eggeling C. 66.  et al. 2012. Norovirus GII.4 virus-like particles recognize galactosylceramides in domains of planar supported lipid bilayers. Angew. Chem. Int. Ed. Engl. 51:12020–24 [Google Scholar]
  67. Taube S, Perry JW, McGreevy E, Yetming K, Perkins C. 67.  et al. 2012. Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. J. Virol. 86:5584–93 [Google Scholar]
  68. Taube S, Perry JW, Yetming K, Patel SP, Auble H. 68.  et al. 2009. Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J. Virol. 83:4092–101 [Google Scholar]
  69. Tan M, Jiang X. 69.  2014. Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev. Mol. Med. 16:e5 [Google Scholar]
  70. Taube S, Rubin JR, Katpally U, Smith TJ, Kendall A. 70.  et al. 2010. High-resolution X-ray structure and functional analysis of the murine norovirus 1 capsid protein protruding domain. J. Virol. 84:5695–705 [Google Scholar]
  71. Kolawole AO, Li M, Xia C, Fischer AE, Giacobbi NS. 71.  et al. 2014. Flexibility in surface-exposed loops in a virus capsid mediates escape from antibody neutralization. J. Virol. 88:4543–57 [Google Scholar]
  72. Chen Z, Sosnovtsev SV, Bok K, Parra GI, Makiya M. 72.  et al. 2013. Development of Norwalk virus-specific monoclonal antibodies with therapeutic potential for the treatment of Norwalk virus gastroenteritis. J. Virol. 87:9547–57 [Google Scholar]
  73. Le Pendu J. 73.  2004. Histo-blood group antigen and human milk oligosaccharides: genetic polymorphism and risk of infectious diseases. Adv. Exp. Med. Biol. 554:135–43 [Google Scholar]
  74. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH. 74.  et al. 2007. Norwalk virus RNA is infectious in mammalian cells. J. Virol. 81:12238–48 [Google Scholar]
  75. Rydell GE, Dahlin AB, Hook F, Larson G. 75.  2009. QCM-D studies of human norovirus VLPs binding to glycosphingolipids in supported lipid bilayers reveal strain-specific characteristics. Glycobiology 19:1176–84 [Google Scholar]
  76. Rydell GE, Svensson L, Larson G, Johannes L, Romer W. 76.  2013. Human GII.4 norovirus VLP induces membrane invaginations on giant unilamellar vesicles containing secretor gene dependent α1,2-fucosylated glycosphingolipids. Biochim. Biophys. Acta 1828:1840–45 [Google Scholar]
  77. Oriol R, Le Pendu J, Sparkes RS, Sparkes MC, Crist M. 77.  et al. 1981. Insights into the expression of ABH and Lewis antigens through human bone marrow transplantation. Am. J. Hum. Genet. 33:551–60 [Google Scholar]
  78. Wilks J, Golovkina T. 78.  2012. Influence of microbiota on viral infections. PLOS Pathog. 8e1002681 [Google Scholar]
  79. Robinson CM, Pfeiffer JK. 79.  2014. Viruses and the microbiota. Annu. Rev. Virol. 1:55–69 [Google Scholar]
  80. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM. 80.  et al. 2011. Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334:249–52 [Google Scholar]
  81. Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C. 81.  et al. 2011. Successful transmission of a retrovirus depends on the commensal microbiota. Science 334:245–49 [Google Scholar]
  82. Uchiyama R, Chassaing B, Zhang B, Gewirtz AT. 82.  2014. Antibiotic treatment suppresses rotavirus infection and enhances specific humoral immunity. J. Infect. Dis. 210:171–82 [Google Scholar]
  83. Robinson CM, Jesudhasan PR, Pfeiffer JK. 83.  2014. Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15:36–46 [Google Scholar]
  84. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A. 84.  et al. 2015. Commensal microbes and interferon-λ determine persistence of enteric murine norovirus infection. Science 347:266–69 [Google Scholar]
  85. Kernbauer E, Ding Y, Cadwell K. 85.  2014. An enteric virus can replace the beneficial function of commensal bacteria. Nature 516:94–98 [Google Scholar]
  86. Miura T, Sano D, Suenaga A, Yoshimura T, Fuzawa M. 86.  et al. 2013. Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J. Virol. 87:9441–51 [Google Scholar]
  87. Karst SM, Wobus CE. 87.  2015. A working model of how noroviruses infect the intestine. PLOS Pathog. 11:e1004626 [Google Scholar]
  88. Atmar RL, Opekun AR, Gilger MA, Estes MK, Crawford SE. 88.  et al. 2008. Norwalk virus shedding after experimental human infection. Emerg. Infect. Dis. 14:1553–57 [Google Scholar]
  89. Murata T, Katsushima N, Mizuta K, Muraki Y, Hongo S, Matsuzaki Y. 89.  2007. Prolonged norovirus shedding in infants ≤6 months of age with gastroenteritis. Pediatr. Infect. Dis. J. 26:46–49 [Google Scholar]
  90. Bok K, Green KY. 90.  2012. Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 367:2126–32 [Google Scholar]
  91. Siebenga JJ, Beersma MF, Vennema H, van Biezen P, Hartwig NJ, Koopmans M. 91.  2008. High prevalence of prolonged norovirus shedding and illness among hospitalized patients: a model for in vivo molecular evolution. J. Infect. Dis. 198:994–1001 [Google Scholar]
  92. Bull RA, Eden JS, Luciani F, McElroy K, Rawlinson WD, White PA. 92.  2012. Contribution of intra- and interhost dynamics to norovirus evolution. J. Virol. 86:3219–29 [Google Scholar]
  93. Arias A, Bailey D, Chaudhry Y, Goodfellow I. 93.  2012. Development of a reverse-genetics system for murine norovirus 3: Long-term persistence occurs in the caecum and colon. J. Gen. Virol. 93:1432–41 [Google Scholar]
  94. Nice TJ, Strong DW, McCune BT, Pohl CS, Virgin HW. 94.  2013. A single-amino-acid change in murine norovirus NS1/2 is sufficient for colonic tropism and persistence. J. Virol. 87:327–34 [Google Scholar]
  95. Tomov VT, Osborne LC, Dolfi DV, Sonnenberg GF, Monticelli LA. 95.  et al. 2013. Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J. Virol. 87:7015–31 [Google Scholar]
  96. Nice TJ, Baldridge MT, McCune BT, Norman JM, Lazear HM. 96.  et al. 2014. Interferon-λ cures persistent murine norovirus infection in the absence of adaptive immunity. Science 347:269–73 [Google Scholar]
  97. Haque R, Snider C, Liu Y, Ma JZ, Liu L. 97.  et al. 2014. Oral polio vaccine response in breast fed infants with malnutrition and diarrhea. Vaccine 32:478–82 [Google Scholar]
  98. Qadri F, Bhuiyan TR, Sack DA, Svennerholm AM. 98.  2013. Immune responses and protection in children in developing countries induced by oral vaccines. Vaccine 31:452–60 [Google Scholar]
  99. von Bubnoff A. 99.  2011. A gut response to vaccines. IAVI Rep. 15:12–14 [Google Scholar]
  100. Beck MA, Handy J, Levander OA. 100.  2004. Host nutritional status: the neglected virulence factor. Trends Microbiol. 12:417–23 [Google Scholar]
  101. Hickman D, Jones MK, Zhu S, Kirkpatrick E, Ostrov DA. 101.  et al. 2014. The effect of malnutrition on norovirus infection. mBio 5:e01032–13 [Google Scholar]
  102. Osborne LC, Monticelli LA, Nice TJ, Sutherland TE, Siracusa MC. 102.  et al. 2014. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 345:578–82 [Google Scholar]
  103. Chang KO, Sosnovtsev SV, Belliot G, King AD, Green KY. 103.  2006. Stable expression of a Norwalk virus RNA replicon in a human hepatoma cell line. Virology 353:463–73 [Google Scholar]
  104. Arias A, Emmott E, Vashist S, Goodfellow I. 104.  2013. Progress towards the prevention and treatment of norovirus infections. Future Microbiol. 8:1475–87 [Google Scholar]
  105. Rocha-Pereira J, Neyts J, Jochmans D. 105.  2014. Norovirus: targets and tools in antiviral drug discovery. Biochem. Pharmacol. 91:1–11 [Google Scholar]
  106. Zeitler CE, Estes MK, Venkataram Prasad BV. 106.  2006. X-ray crystallographic structure of the Norwalk virus protease at 1.5-Å resolution. J. Virol. 80:5050–58 [Google Scholar]
  107. Ng KK, Pendas-Franco N, Rojo J, Boga JA, Machin A. 107.  et al. 2004. Crystal structure of Norwalk virus polymerase reveals the carboxyl terminus in the active site cleft. J. Biol. Chem. 279:16638–45 [Google Scholar]
  108. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Cunha R. 108.  et al. 2012. Inhibition of norovirus replication by the nucleoside analogue 2′-C-methylcytidine. Biochem. Biophys. Res. Commun. 427:796–800 [Google Scholar]
  109. Costantini VP, Whitaker T, Barclay L, Lee D, McBrayer TR. 109.  et al. 2012. Antiviral activity of nucleoside analogues against norovirus. Antivir. Ther. 17:981–91 [Google Scholar]
  110. Rocha-Pereira J, Jochmans D, Debing Y, Verbeken E, Nascimento MS, Neyts J. 110.  2013. The viral polymerase inhibitor 2′-C-methylcytidine inhibits Norwalk virus replication and protects against norovirus-induced diarrhea and mortality in a mouse model. J. Virol. 87:11798–805 [Google Scholar]
  111. Rocha-Pereira J, Jochmans D, Neyts J. 111.  2015. Prophylactic treatment with the nucleoside analogue 2′-C-methylcytidine completely prevents transmission of norovirus. J. Antimicrob. Chemother. 70:190–97 [Google Scholar]
  112. Toniutto P, Fabris C, Bitetto D, Fornasiere E, Rapetti R, Pirisi M. 112.  2007. Valopicitabine dihydrochloride: a specific polymerase inhibitor of hepatitis C virus. Curr. Opin. Investig. Drugs 8:150–58 [Google Scholar]
  113. Lopatto E, Zimm A. 113.  2007. Novartis, Idenix suspend tests on hepatitis C drug NM283 Hepat. C Artic. 3630, Nat. AIDS Treat. Advocacy Proj. (NATAP), New York, NY. http://www.natap.org/2007/HCV/071607_03.htm [Google Scholar]
  114. Sidwell RW, Barnard DL, Day CW, Smee DF, Bailey KW. 114.  et al. 2007. Efficacy of orally administered T-705 on lethal avian influenza A (H5N1) virus infections in mice. Antimicrob. Agents Chemother. 51:845–51 [Google Scholar]
  115. Gowen BB, Wong MH, Jung KH, Sanders AB, Mendenhall M. 115.  et al. 2007. In vitro and in vivo activities of T-705 against arenavirus and bunyavirus infections. Antimicrob. Agents Chemother. 51:3168–76 [Google Scholar]
  116. Morrey JD, Taro BS, Siddharthan V, Wang H, Smee DF. 116.  et al. 2008. Efficacy of orally administered T-705 pyrazine analog on lethal West Nile virus infection in rodents. Antivir. Res. 80:377–79 [Google Scholar]
  117. Smither SJ, Eastaugh LS, Steward JA, Nelson M, Lenk RP, Lever MS. 117.  2014. Post-exposure efficacy of oral T-705 (favipiravir) against inhalational Ebola virus infection in a mouse model. Antivir. Res. 104:153–55 [Google Scholar]
  118. Rocha-Pereira J, Jochmans D, Dallmeier K, Leyssen P, Nascimento MS, Neyts J. 118.  2012. Favipiravir (T-705) inhibits in vitro norovirus replication. Biochem. Biophys. Res. Commun. 424:777–80 [Google Scholar]
  119. Arias A, Thorne L, Goodfellow I. 119.  2014. Favipiravir elicits antiviral mutagenesis during virus replication in vivo. eLife 3:e03679 [Google Scholar]
  120. Jin Z, Smith LK, Rajwanshi VK, Kim B, Deval J. 120.  2013. The ambiguous base-pairing and high substrate efficiency of T-705 (favipiravir) ribofuranosyl 5′-triphosphate towards influenza A virus polymerase. PLOS ONE 8:e68347 [Google Scholar]
  121. Furuta Y, Gowen BB, Takahashi K, Shiraki K, Smee DF, Barnard DL. 121.  2013. Favipiravir (T-705), a novel viral RNA polymerase inhibitor. Antivir. Res. 100:446–54 [Google Scholar]
  122. Kapuria V, Peterson LF, Fang D, Bornmann WG, Talpaz M, Donato NJ. 122.  2010. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res. 70:9265–76 [Google Scholar]
  123. Perry JW, Ahmed M, Chang KO, Donato NJ, Showalter HD, Wobus CE. 123.  2012. Antiviral activity of a small molecule deubiquitinase inhibitor occurs via induction of the unfolded protein response. PLOS Pathog. 8:e1002783 [Google Scholar]
  124. Hayashimoto N, Morita H, Ishida T, Uchida R, Tanaka M. 124.  et al. 2015. Microbiological survey of mice (Mus musculus) purchased from commercial pet shops in Kanagawa and Tokyo, Japan. Exp. Anim. 64:155–60 [Google Scholar]
  125. Kastenmayer RJ, Perdue KA, Elkins WR. 125.  2008. Eradication of murine norovirus from a mouse barrier facility. J. Am. Assoc. Lab. Anim. Sci. 47:26–30 [Google Scholar]
  126. Larsson E, Tremaroli V, Lee YS, Koren O, Nookaew I. 126.  et al. 2012. Analysis of gut microbial regulation of host gene expression along the length of the gut and regulation of gut microbial ecology through MyD88. Gut 61:1124–31 [Google Scholar]
  127. Paik J, Fierce Y, Mai PO, Phelps SR, McDonald T. 127.  et al. 2011. Murine norovirus increases atherosclerotic lesion size and macrophages in Ldlr−/− mice. Comp. Med. 61:330–38 [Google Scholar]
  128. Paik J, Fierce Y, Drivdahl R, Treuting PM, Seamons A. 128.  et al. 2010. Effects of murine norovirus infection on a mouse model of diet-induced obesity and insulin resistance. Comp. Med. 60:189–95 [Google Scholar]
  129. Lencioni KC, Drivdahl R, Seamons A, Treuting PM, Brabb T, Maggio-Price L. 129.  2011. Lack of effect of murine norovirus infection on a mouse model of bacteria-induced colon cancer. Comp. Med. 61:219–26 [Google Scholar]
  130. Compton SR, Paturzo FX, Macy JD. 130.  2010. Effect of murine norovirus infection on mouse parvovirus infection. J. Am. Assoc. Lab. Anim. Sci. 49:11–21 [Google Scholar]
  131. Hensley SE, Pinto AK, Hickman HD, Kastenmayer RJ, Bennink JR. 131.  et al. 2009. Murine norovirus infection has no significant effect on adaptive immunity to vaccinia virus or influenza A virus. J. Virol. 83:7357–60 [Google Scholar]
  132. Doom CM, Turula HM, Hill AB. 132.  2009. Investigation of the impact of the common animal facility contaminant murine norovirus on experimental murine cytomegalovirus infection. Virology 392:153–61 [Google Scholar]
  133. Ammann CG, Messer RJ, Varvel K, Debuysscher BL, Lacasse RA. 133.  et al. 2009. Effects of acute and chronic murine norovirus infections on immune responses and recovery from Friend retrovirus infection. J. Virol. 83:13037–41 [Google Scholar]
  134. Hampe J, Franke A, Rosenstiel P, Till A, Teuber M. 134.  et al. 2007. A genome-wide association scan of nonsynonymous SNPs identifies a susceptibility variant for Crohn disease in ATG16L1. Nat. Genet. 39:207–11 [Google Scholar]
  135. Rioux JD, Xavier RJ, Taylor KD, Silverberg MS, Goyette P. 135.  et al. 2007. Genome-wide association study identifies new susceptibility loci for Crohn disease and implicates autophagy in disease pathogenesis. Nat. Genet. 39:596–604 [Google Scholar]
  136. Cadwell K, Patel KK, Komatsu M, Virgin HW IV, Stappenbeck TS. 136.  2009. A common role for Atg16L1, Atg5 and Atg7 in small intestinal Paneth cells and Crohn disease. Autophagy 5:250–52 [Google Scholar]
  137. Cadwell K, Liu JY, Brown SL, Miyoshi H, Loh J. 137.  et al. 2008. A key role for autophagy and the autophagy gene Atg16L1 in mouse and human intestinal Paneth cells. Nature 456:259–63 [Google Scholar]
  138. Cadwell K. 138.  2010. Crohn's disease susceptibility gene interactions, a NOD to the newcomer ATG16L1. Gastroenterology 139:1448–50 [Google Scholar]
  139. Cadwell K, Stappenbeck TS, Virgin HW. 139.  2009. Role of autophagy and autophagy genes in inflammatory bowel disease. Curr. Top. Microbiol. Immunol. 335:141–67 [Google Scholar]
  140. Lencioni KC, Seamons A, Treuting PM, Maggio-Price L, Brabb T. 140.  2008. Murine norovirus: an intercurrent variable in a mouse model of bacteria-induced inflammatory bowel disease. Comp. Med. 58:522–33 [Google Scholar]
  141. Hsu CC, Paik J, Treuting PM, Seamons A, Meeker SM. 141.  et al. 2014. Infection with murine norovirus 4 does not alter Helicobacter-induced inflammatory bowel disease in Il10−/−mice. Comp. Med. 64:256–63 [Google Scholar]
  142. Higgins PD, Johnson LA, Sauder K, Moons D, Blanco L. 142.  et al. 2011. Transient or persistent norovirus infection does not alter the pathology of Salmonella typhimurium induced intestinal inflammation and fibrosis in mice. Comp. Immunol. Microbiol. Infect. Dis. 34:247–57 [Google Scholar]
  143. Abt MC, Artis D. 143.  2009. The intestinal microbiota in health and disease: the influence of microbial products on immune cell homeostasis. Curr. Opin. Gastroenterol. 25:496–502 [Google Scholar]
  144. Brestoff JR, Artis D. 144.  2013. Commensal bacteria at the interface of host metabolism and the immune system. Nat. Immunol. 14:676–84 [Google Scholar]
  145. Kau AL, Ahern PP, Griffin NW, Goodman AL, Gordon JI. 145.  2011. Human nutrition, the gut microbiome and the immune system. Nature 474:327–36 [Google Scholar]
  146. Nelson AM, Elftman MD, Pinto AK, Baldridge M, Hooper P. 146.  et al. 2013. Murine norovirus infection does not cause major disruptions in the murine intestinal microbiota. Microbiome 1:7 [Google Scholar]
  147. Nelson AM, Walk ST, Taube S, Taniuchi M, Houpt ER. 147.  et al. 2012. Disruption of the human gut microbiota following norovirus infection. PLOS ONE 7:e48224 [Google Scholar]
  148. Power SE, O'Toole PW, Stanton C, Ross RP, Fitzgerald GF. 148.  2014. Intestinal microbiota, diet and health. Br. J. Nutr. 111:387–402 [Google Scholar]
  149. Schippa S, Conte MP. 149.  2014. Dysbiotic events in gut microbiota: impact on human health. Nutrients 6:5786–805 [Google Scholar]
  150. Cao S, Lou Z, Tan M, Chen Y, Liu Y. 150.  et al. 2007. Structural basis for the recognition of blood group trisaccharides by norovirus. J. Virol. 81:5949–57 [Google Scholar]
  151. Hao N, Chen Y, Xia M, Tan M, Liu W. 151.  et al. 2015. Crystal structures of GI.8 Boxer virus P dimers in complex with HBGAs, a novel evolutionary path selected by the Lewis epitope. Protein Cell 6:101–16 [Google Scholar]
  152. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K. 152.  et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7:539 [Google Scholar]
  153. Shanker S, Czako R, Sankaran B, Atmar RL, Estes MK, Prasad BV. 153.  2014. Structural analysis of determinants of histo-blood group antigen binding specificity in genogroup I noroviruses. J. Virol. 88:6168–80 [Google Scholar]
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