Norovirus immunology: Of mice and mechanisms

European Journal of Immunology

Volumn 45, Issue 10, 2015, Pages 2742-2757

  Newman, Kira L ^a,b   Leon, Juan S ^a  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Animal models; Human; Microbiome; Norovirus; Vaccine

Indexed keywords

VIRUS VACCINE;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; CALF (BOVINE); GNOTOBIOTICS; HUMAN; IMMUNOLOGY; INNATE IMMUNITY; INTESTINE FLORA; MICROBIOME; MOUSE; NONHUMAN; NOROVIRUS; PIG; PRIORITY JOURNAL; SHORT SURVEY; T LYMPHOCYTE; VIRUS MORPHOLOGY; ANIMAL; CALICIVIRUS INFECTION; GASTROENTERITIS; INTESTINE; PATHOLOGY; VIROLOGY;

ANIMALS; B-LYMPHOCYTES; CALICIVIRIDAE INFECTIONS; GASTROENTERITIS; HUMANS; IMMUNITY, INNATE; INTESTINES; MICE; NOROVIRUS; T-LYMPHOCYTES;

EID: 84943199168     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545512     Document Type: Short Survey

References (159)

1. Ahmed, S. M., Hall, A. J., Robinson, A. E., Verhoef, L., Premkumar, P., Parashar, U. D., Koopmans, M. et al., Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect. Dis. 2014. 14: 725-730.
2. Payne, D. C., Vinje, J., Szilagyi, P. G., Edwards, K. M., Staat, M. A., Weinberg, G. A., Hall, C. B. et al., Norovirus and medically attended gastroenteritis in U.S. children. N. Engl. J. Med. 2013. 368: 1121-1130.
3. Verhoef, L., Koopmans, M., VAN Pelt, W., Duizer, E., Haagsma, J., Werber, D., VAN Asten, L. et al., The estimated disease burden of norovirus in The Netherlands. Epidemiol. Infect. 2013. 141: 496-506.
4. Trivedi, T. K., DeSalvo, T., Lee, L., Palumbo, A., Moll, M., Curns, A., Hall, A. J. et al., Hospitalizations and mortality associated with norovirus outbreaks in nursing homes, 2009-2010. J. Am. Med. Assoc. 2012. 308: 1668-1675.
5. Schwartz, S., Vergoulidou, M., Schreier, E., Loddenkemper, C., Reinwald, M., Schmidt-Hieber, M., Flegel, W. A. et al., Norovirus gastroenteritis causes severe and lethal complications after chemotherapy and hematopoietic stem cell transplantation. Blood 2011. 117: 5850-5856.
6. Siebenga, J. J., Beersma, M. F., Vennema, H., van Biezen, P., Hartwig, N. J. and Koopmans, M., High prevalence of prolonged norovirus shedding and illness among hospitalized patients: a model for in vivo molecular evolution. J. Infect. Dis. 2008. 198: 994-1001.
7. Bagci, S., Eis-Hubinger, A. M., Yassin, A. F., Simon, A., Bartmann, P., Franz, A. R. and Mueller, A., Clinical characteristics of viral intestinal infection in preterm and term neonates. Eur. J. Clin. Microbiol. Infect. Dis. 2010. 29: 1079-1084.
8. Murray, C. J., Vos, T., Lozano, R., Naghavi, M., Flaxman, A. D., Michaud, C., Ezzati, M. et al., Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012. 380: 2197-2223.
9. Lozano, R., Naghavi, M., Foreman, K., Lim, S., Shibuya, K., Aboyans, V., Abraham, J. et al., Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2012. 380: 2095-2128.
10. Walker, C. L., Rudan, I., Liu, L., Nair, H., Theodoratou, E., Bhutta, Z. A., O'Brien, K. L. et al., Global burden of childhood pneumonia and diarrhoea. Lancet 2013. 381: 1405-1416.
11. Liu, L., Oza, S., Hogan, D., Perin, J., Rudan, I., Lawn, J. E., Cousens, S. et al., Global, regional, and national causes of child mortality in 2000-13, with projections to inform post-2015 priorities: an updated systematic analysis. Lancet 2015. 385: 430-440.
12. Lanata, C. F., Fischer-Walker, C. L., Olascoaga, A. C., Torres, C. X., Aryee, M. J. and Black, R. E., Child Health Epidemiology Reference Group of the World Health, O. and UNICEF, Global causes of diarrheal disease mortality in children <5 years of age: a systematic review. PLoS One 2013. 8: e72788.
13. Zanini, B., Ricci, C., Bandera, F., Caselani, F., Magni, A., Laronga, A. M., Lanzini, A. et al., Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am. J. Gastroenterol. 2012. 107: 891-899.
14. Khan, R. R., Lawson, A. D., Minnich, L. L., Martin, K., Nasir, A., Emmett, M. K., Welch, C. A. et al., Gastrointestinal norovirus infection associated with exacerbation of inflammatory bowel disease. J. Pediatr. Gastroenterol. Nutr. 2009. 48: 328-333.
15. Gastanaduy, P. A., Hall, A. J., Curns, A. T., Parashar, U. D. and Lopman, B. A., Burden of norovirus gastroenteritis in the ambulatory setting-United States, 2001-2009. J. Infect. Dis. 2013. 207: 1058-1065.
16. Belliot, G., Lopman, B. A., Ambert-Balay, K. and Pothier, P., The Burden of Norovirus gastroenteritis: an important foodborne and healthcare-related infection. Clin. Microbiol. Infect. 2014. 20: 724-730.
17. Head, M. G., Fitchett, J. R. and Atun, R., Systematic analysis of funding awarded for norovirus research to institutions in the United Kingdom, 1997-2010. J. R. Soc. Med. 2014. 107: 110-115.
18. Vinje, J., Advances in laboratory methods for detection and typing of norovirus. J. Clin. Microbiol. 2014. 53: 373-381.
19. Karst, S. M., Wobus, C. E., Goodfellow, I. G., Green, K. Y. and Virgin, H. W., Advances in norovirus biology. Cell Host Microbe 2014. 15: 668-680.
20. Karst, S. M., Zhu, S. and Goodfellow, I. G., The molecular pathology of noroviruses. J. Pathol. 2015. 235: 206-216.
21. Tan, M. and Jiang, X., Histo-blood group antigens: a common niche for norovirus and rotavirus. Expert Rev. Mol. Med. 2014. 16: e5.
22. Arias, A., Emmott, E., Vashist, S. and Goodfellow, I., Progress towards the prevention and treatment of norovirus infections. Future Microbiol. 2013. 8: 1475-1487.
23. Ramani, S., Atmar, R. L. and Estes, M. K., Epidemiology of human noroviruses and updates on vaccine development. Curr. Opin. Gastroenterol. 2014. 30: 25-33.
24. Rocha-Pereira, J., Neyts, J. and Jochmans, D., Norovirus: targets and tools in antiviral drug discovery. Biochem. Pharmacol. 2014. 91: 1-11.
25. Clarke, I. N. E., Green, M. K., Hansman, K. Y., Knowles, G. S., Koopmans, N. J., Matson, M. K., Meyers, D. O. et al. (Ed.), Virus taxonomy: classification and nomenclature of viruses-ninth report of the International Committee on Taxonomy of Viruses, Elsevier, San Diego, CA 2012, 977-986.
26. Carstens, E. B., Ratification vote on taxonomic proposals to the International Committee on Taxonomy of Viruses (2009). Arch. Virol. 2010. 155: 133-146.
27. Mesquita, J. R., Costantini, V. P., Cannon, J. L., Lin, S. C., Nascimento, M. S. and Vinje, J., Presence of antibodies against genogroup VI norovirus in humans. Virol. J. 2013. 10: 176.
28. McFadden, N., Bailey, D., Carrara, G., Benson, A., Chaudhry, Y., Shortland, A., Heeney, J. et al., Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog. 2011. 7: e1002413.
29. Zheng, D. P., Ando, T., Fankhauser, R. L., Beard, R. S., Glass, R. I. and Monroe, S. S., Norovirus classification and proposed strain nomenclature. Virology 2006. 346: 312-323.
30. Kroneman, A., Vega, E., Vennema, H., Vinje, J., White, P. A., Hansman, G., Green, K. et al., Proposal for a unified norovirus nomenclature and genotyping. Arch. Virol. 2013. 158: 2059-2068.
31. Jones, M. K., Watanabe, M., Zhu, S., Graves, C. L., Keyes, L. R., Grau, K. R., Gonzalez-Hernandez, M. B. et al., Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014. 346: 755-759.
32. Papafragkou, E., Hewitt, J., Park, G. W., Greening, G. and Vinje, J., Challenges of culturing human norovirus in three-dimensional organoid intestinal cell culture models. PLoS One 2013. 8: e63485.
33. Miura, T., Sano, D., Suenaga, A., Yoshimura, T., Fuzawa, M., Nakagomi, T., Nakagomi, O. et al., Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J. Virol. 2013. 87: 9441-9451.
34. Huang, P., Farkas, T., Marionneau, S., Zhong, W., Ruvoen-Clouet, N., Morrow, A. L., Altaye, M. et al., Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strain-specific patterns. J. Infect. Dis. 2003. 188: 19-31.
35. Tan, M. and Jiang, X., Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog. 2010. 6: e1000983.
36. Bok, K., Parra, G. I., Mitra, T., Abente, E., Shaver, C. K., Boon, D., Engle, R. et al., Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc. Natl. Acad. Sci. USA 2011. 108: 325-330.
37. Atmar, R. L., Opekun, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H. and Graham, D. Y., Norwalk virus shedding after experimental human infection. Emerg. Infect. Dis. 2008. 14: 1553-1557.
38. Kirby, A. E., Shi, J., Montes, J., Lichtenstein, M. and Moe, C. L., Disease course and viral shedding in experimental Norwalk virus and Snow Mountain virus infection. J. Med. Virol. 2014. 86: 2055-2064.
39. Souza, M., Azevedo, M. S., Jung, K., Cheetham, S. and Saif, L. J., Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II.4-HS66 strain of human norovirus. J. Virol. 2008. 82: 1777-1786.
40. Souza, M., Cheetham, S. M., Azevedo, M. S., Costantini, V. and Saif, L. J., Cytokine and antibody responses in gnotobiotic pigs after infection with human norovirus genogroup II.4 (HS66 strain). J. Virol. 2007. 81: 9183-9192.
41. Bernstein, D. I., Atmar, R. L., Lyon, G. M., Treanor, J. J., Chen, W. H., Jiang, X., Vinje, J. et al., Norovirus vaccine against experimental human GII.4 virus illness: a challenge study in healthy adults. J. Infect. Dis. 2014. 211: 870-878.
42. Frenck, R., Bernstein, D. I., Xia, M., Huang, P., Zhong, W., Parker, S., Dickey, M. et al., Predicting susceptibility to norovirus GII.4 by use of a challenge model involving humans. J. Infect. Dis. 2012. 206: 1386-1393.
43. Cheetham, S., Souza, M., Meulia, T., Grimes, S., Han, M. G. and Saif, L. J., Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J. Virol. 2006. 80: 10372-10381.
44. Taube, S., Kolawole, A. O., Hohne, M., Wilkinson, J. E., Handley, S. A., Perry, J. W., Thackray, L. B. et al., A mouse model for human norovirus. MBio 2013. 4.
45. Atmar, R. L., Opekun, A. R., Gilger, M. A., Estes, M. K., Crawford, S. E., Neill, F. H., Ramani, S. et al., Determination of the 50% human infectious dose for Norwalk virus. J. Infect. Dis. 2014. 209: 1016-1022.
46. Lindesmith, L., Moe, C., Lependu, J., Frelinger, J. A., Treanor, J. and Baric, R. S., Cellular and humoral immunity following Snow Mountain virus challenge. J. Virol. 2005. 79: 2900-2909.
47. Lindesmith, L., Moe, C., Marionneau, S., Ruvoen, N., Jiang, X., Lindblad, L., Stewart, P. et al., Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 2003. 9: 548-553.
48. Leon, J. S., Kingsley, D. H., Montes, J. S., Richards, G. P., Lyon, G. M., Abdulhafid, G. M., Seitz, S. R. et al., Randomized, double-blinded clinical trial for human norovirus inactivation in oysters by high hydrostatic pressure processing. Appl. Environ. Microbiol. 2011. 77: 5476-5482.
49. Seitz, S. R., Leon, J. S., Schwab, K. J., Lyon, G. M., Dowd, M., McDaniels, M., Abdulhafid, G. et al., Norovirus infectivity in humans and persistence in water. Appl. Environ. Microbiol. 2011. 77: 6884-6888.
50. Teunis, P. F., Sukhrie, F. H., Vennema, H., Bogerman, J., Beersma, M. F. and Koopmans, M. P., Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol. Infect. 2014: 1-8.
51. Glass, R. I., Parashar, U. D. and Estes, M. K., Norovirus gastroenteritis. N. Engl. J. Med. 2009. 361: 1776-1785.
52. Ko, G., Jiang, Z. D., Okhuysen, P. C. and DuPont, H. L., Fecal cytokines and markers of intestinal inflammation in international travelers with diarrhea due to Noroviruses. J. Med. Virol. 2006. 78: 825-828.
53. Troeger, H., Loddenkemper, C., Schneider, T., Schreier, E., Epple, H. J., Zeitz, M., Fromm, M. et al., Structural and functional changes of the duodenum in human norovirus infection. Gut 2009. 58: 1070-1077.
54. Schorn, R., Hohne, M., Meerbach, A., Bossart, W., Wuthrich, R. P., Schreier, E., Muller, N. J. et al., Chronic norovirus infection after kidney transplantation: molecular evidence for immune-driven viral evolution. Clin. Infect. Dis. 2010. 51: 307-314.
55. Schreiber, D. S., Blacklow, N. R. and Trier, J. S., The mucosal lesion of the proximal small intestine in acute infectious nonbacterial gastroenteritis. N. Engl. J. Med. 1973. 288: 1318-1323.
56. Schreiber, D. S., Blacklow, N. R. and Trier, J. S., The small intestinal lesion induced by Hawaii agent acute infectious nonbacterial gastroenteritis. J. Infect. Dis. 1974. 129: 705-708.
57. Rocha-Pereira, J., Jochmans, D., Debing, Y., Verbeken, E., Nascimento, M. S. and Neyts, J., 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. 2013. 87: 11798-11805.
58. Jung, K., Wang, Q., Kim, Y., Scheuer, K., Zhang, Z., Shen, Q., Chang, K. O. et al., The effects of simvastatin or interferon-alpha on infectivity of human norovirus using a gnotobiotic pig model for the study of antivirals. PLoS One 2012. 7: e41619.
59. Flynn, W. T., Saif, L. J. and Moorhead, P. D., Pathogenesis of porcine enteric calicivirus-like virus in four-day-old gnotobiotic pigs. Am. J. Vet. Res. 1988. 49: 819-825.
60. Otto, P. H., Clarke, I. N., Lambden, P. R., Salim, O., Reetz, J. and Liebler-Tenorio, E. M., Infection of calves with bovine norovirus GIII.1 strain Jena virus: an experimental model to study the pathogenesis of norovirus infection. J. Virol. 2011. 85: 12013-12021.
61. Sestak, K., Feely, S., Fey, B., Dufour, J., Hargitt, E., Alvarez, X., Pahar, B. et al., Experimental inoculation of juvenile rhesus macaques with primate enteric caliciviruses. PLoS One 2012. 7: e37973.
62. Rydell, G. E., Kindberg, E., Larson, G. and Svensson, L., Susceptibility to winter vomiting disease: a sweet matter. Rev. Med. Virol. 2011. 21: 370-382.
63. Thorven, M., Grahn, A., Hedlund, K. O., Johansson, H., Wahlfrid, C., Larson, G. and Svensson, L., A homozygous nonsense mutation (428G→A) in the human secretor (FUT2) gene provides resistance to symptomatic norovirus (GGII) infections. J. Virol. 2005. 79: 15351-15355.
64. Hutson, A. M., Airaud, F., LePendu, J., Estes, M. K. and Atmar, R. L., Norwalk virus infection associates with secretor status genotyped from sera. J. Med. Virol. 2005. 77: 116-120.
65. Ferrer-Admetlla, A., Sikora, M., Laayouni, H., Esteve, A., Roubinet, F., Blancher, A., Calafell, F. et al., A natural history of FUT2 polymorphism in humans. Mol. Biol. Evol. 2009. 26: 1993-2003.
66. Currier, R. L., Payne, D. C., Staat, M. A., Selvarangan, R., Shirley, S. H., Halasa, N., Boom, J. A. et al., Innate susceptibility to norovirus infections influenced by FUT2 genotype in a United States pediatric population. Clin. Infect. Dis. 2015. 60: 1631-1638.
67. Reeck, A., Kavanagh, O., Estes, M. K., Opekun, A. R., Gilger, M. A., Graham, D. Y. and Atmar, R. L., Serological correlate of protection against norovirus-induced gastroenteritis. J. Infect. Dis. 2010. 202: 1212-1218.
68. Blacklow, N. R., Cukor, G., Bedigian, M. K., Echeverria, P., Greenberg, H. B., Schreiber, D. S. and Trier, J. S., Immune response and prevalence of antibody to Norwalk enteritis virus as determined by radioimmunoassay. J. Clin. Microbiol. 1979. 10: 903-909.
69. Johnson, P. C., Mathewson, J. J., DuPont, H. L. and Greenberg, H. B., Multiple-challenge study of host susceptibility to Norwalk gastroenteritis in US adults. J. Infect. Dis. 1990. 161: 18-21.
70. Larsson, M. M., Rydell, G. E., Grahn, A., Rodriguez-Diaz, J., Akerlind, B., Hutson, A. M., Estes, M. K. et al., Antibody prevalence and titer to norovirus (genogroup II) correlate with secretor (FUT2) but not with ABO phenotype or Lewis (FUT3) genotype. J. Infect. Dis. 2006. 194: 1422-1427.
71. Malm, M., Uusi-Kerttula, H., Vesikari, T. and Blazevic, V., High serum levels of norovirus genotype-specific blocking antibodies correlate with protection from infection in children. J. Infect. Dis. 2014. 210: 1755-1762.
72. Nurminen, K., Blazevic, V., Huhti, L., Rasanen, S., Koho, T., Hytonen, V. P. and Vesikari, T., Prevalence of norovirus GII-4 antibodies in Finnish children. J. Med. Virol. 2011. 83: 525-531.
73. Ryder, R. W., Singh, N., Reeves, W. C., Kapikian, A. Z., Greenberg, H. B. and Sack, R. B., Evidence of immunity induced by naturally acquired rotavirus and Norwalk virus infection on two remote Panamanian islands. J. Infect. Dis. 1985. 151: 99-105.
74. Ramani, S., Neill, F. H., Opekun, A. R., Gilger, M. A., Graham, D. Y., Estes, M. K. and Atmar, R. L., Mucosal and cellular immune responses to Norwalk virus. J. Infect. Dis. 2015. 212: 397-405.
75. Czako, R., Atmar, R. L., Opekun, A. R., Gilger, M. A., Graham, D. Y. and Estes, M. K., Serum hemagglutination inhibition activity correlates with protection from gastroenteritis in persons infected with Norwalk virus. Clin. Vaccine Immunol. 2012. 19: 284-287.
76. Harrington, P. R., Lindesmith, L., Yount, B., Moe, C. L. and Baric, R. S., Binding of Norwalk virus-like particles to ABH histo-blood group antigens is blocked by antisera from infected human volunteers or experimentally vaccinated mice. J. Virol. 2002. 76: 12335-12343.
77. Wobus, C. E., Karst, S. M., Thackray, L. B., Chang, K. O., Sosnovtsev, S. V., Belliot, G., Krug, A. et al., Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol. 2004. 2: e432.
78. Gonzalez-Hernandez, M. B., Liu, T., Payne, H. C., Stencel-Baerenwald, J. E., Ikizler, M., Yagita, H., Williams, I. R., et al., Efficient Norovirus and Reovirus Replication in the Mouse Intestine Requires Microfold (M) Cells. J Virol 2014. 88: 6934-6943.
79. McCartney, S. A., Thackray, L. B., Gitlin, L., Gilfillan, S., Virgin, H. W. and Colonna, M., MDA-5 recognition of a murine norovirus. PLoS Pathog. 2008. 4: e1000108.
80. Karst, S. M., Wobus, C. E., Lay, M., Davidson, J. and Virgin, H. W. t., STAT1-dependent innate immunity to a Norwalk-like virus. Science 2003. 299: 1575-1578.
81. Mumphrey, S. M., Changotra, H., Moore, T. N., Heimann-Nichols, E. R., Wobus, C. E., Reilly, M. J., Moghadamfalahi, M. et al., Murine norovirus 1 infection is associated with histopathological changes in immunocompetent hosts, but clinical disease is prevented by STAT1-dependent interferon responses. J. Virol. 2007. 81: 3251-3263.
82. Thackray, L. B., Duan, E., Lazear, H. M., Kambal, A., Schreiber, R. D., Diamond, M. S. and Virgin, H. W., Critical role for interferon regulatory factor 3 (IRF-3) and IRF-7 in type I interferon-mediated control of murine norovirus replication. J. Virol. 2012. 86: 13515-13523.
83. Changotra, H., Jia, Y., Moore, T. N., Liu, G., Kahan, S. M., Sosnovtsev, S. V. and Karst, S. M., Type I and type II interferons inhibit the translation of murine norovirus proteins. J. Virol. 2009. 83: 5683-5692.
84. Hwang, S., Maloney, N. S., Bruinsma, M. W., Goel, G., Duan, E., Zhang, L., Shrestha, B. et al., Nondegradative role of Atg5-Atg12/ Atg16L1 autophagy protein complex in antiviral activity of interferon gamma. Cell Host Microbe 2012. 11: 397-409.
85. Rodriguez, M. R., Monte, K., Thackray, L. B. and Lenschow, D. J., ISG15 functions as an interferon-mediated antiviral effector early in the murine norovirus life cycle. J. Virol. 2014. 88: 9277-9286.
86. Nice, T. J., Baldridge, M. T., McCune, B. T., Norman, J. M., Lazear, H. M., Artyomov, M., Diamond, M. S. et al., Interferon lambda cures persistent murine norovirus infection in the absence of adaptive immunity. Science 2014. 347: 269-273.
87. Baldridge, M. T., Nice, T. J., McCune, B. T., Yokoyama, C. C., Kambal, A., Wheadon, M., Diamond, M. S. et al., Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science 2015. 347: 266-269.
88. Bui, T., Kocher, J., Li, Y., Wen, K., Li, G., Liu, F., Yang, X. et al., Median infectious dose of human norovirus GII.4 in gnotobiotic pigs is decreased by simvastatin treatment and increased by age. J. Gen. Virol. 2013. 94: 2005-2016.
89. Meurens, F., Summerfield, A., Nauwynck, H., Saif, L. and Gerdts, V., The pig: a model for human infectious diseases. Trends Microbiol. 2012. 20: 50-57.
90. Pabst, R. and Rothkotter, H. J., Postnatal development of lymphocyte subsets in different compartments of the small intestine of piglets. Vet. Immunol. Immunopathol. 1999. 72: 167-173.
91. Pabst, R., Geist, M., Rothkotter, H. J. and Fritz, F. J., Postnatal development and lymphocyte production of jejunal and ileal Peyer's patches in normal and gnotobiotic pigs. Immunology 1988. 64: 539-544.
92. Dolin, R., Levy, A. G., Wyatt, R. G., Thornhill, T. S. and Gardner, J. D., Viral gastroenteritis induced by the Hawaii agent. Jejunal histopathology and serologic response. Am. J. Med. 1975. 59: 761-768.
93. Chachu, K. A., Strong, D. W., LoBue, A. D., Wobus, C. E., Baric, R. S. and Virgin, H. W., Antibody is critical for the clearance of murine norovirus infection. J. Virol. 2008. 82: 6610-6617.
94. Chachu, K. A., LoBue, A. D., Strong, D. W., Baric, R. S. and Virgin, H. W., Immune mechanisms responsible for vaccination against and clearance of mucosal and lymphatic norovirus infection. PLoS Pathog. 2008. 4: e1000236.
95. Park, K., Cha, K. E. and Myung, H., Observation of inflammatory responses in mice orally fed with bacteriophage T7. J. Appl. Microbiol. 2014. 117: 627-633.
96. Tomov, V. T., Osborne, L. C., Dolfi, D. V., Sonnenberg, G. F., Monticelli, L. A., Mansfield, K., Virgin, H. W. et al., Persistent enteric murine norovirus infection is associated with functionally suboptimal virus-specific CD8 T cell responses. J. Virol. 2013. 87: 7015-7031.
97. Zhu, S., Regev, D., Watanabe, M., Hickman, D., Moussatche, N., Jesus, D. M., Kahan, S. M. et al., Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLoS Pathog. 2013. 9: e1003592.
98. Chagla, Z., Quirt, J., Woodward, K., Neary, J. and Rutherford, C., Chronic norovirus infection in a transplant patient successfully treated with enterally administered immune globulin. J. Clin. Virol. 2013. 58: 306-308.
99. Ronchetti, A. M., Henry, B., Ambert-Balay, K., Pothier, P., Decroocq, J., Leblond, V. and Roos-Weil, D., Norovirus-related chronic diarrhea in a patient treated with alemtuzumab for chronic lymphocytic leukemia. BMC Infect. Dis. 2014. 14: 239.
100. Saif, M. A., Bonney, D. K., Bigger, B., Forsythe, L., Williams, N., Page, J., Babiker, Z. O. et al., Chronic norovirus infection in pediatric hematopoietic stem cell transplant recipients: a cause of prolonged intestinal failure requiring intensive nutritional support. Pediatr. Transplant. 2011. 15: 505-509.
101. Bok, K. and Green, K. Y., Norovirus gastroenteritis in immunocompromised patients. N. Engl. J. Med. 2012. 367: 2126-2132.
102. Waugh, E., Chen, A., Baird, M. A., Brown, C. M. and Ward, V. K., Characterization of the chemokine response of RAW264.7 cells to infection by murine norovirus. Virus Res. 2014. 181: 27-34.
103. Groom, J. R. and Luster, A. D., CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol. Cell Biol. 2011. 89: 207-215.
104. Strong, D. W., Thackray, L. B., Smith, T. J. and Virgin, H. W., Protruding domain of capsid protein is necessary and sufficient to determine murine norovirus replication and pathogenesis in vivo. J. Virol. 2012. 86: 2950-2958.
105. Ponterio, E., Petrizzo, A., Di Bartolo, I., Buonaguro, F. M., Buonaguro, L. and Ruggeri, F. M., Pattern of activation of human antigen presenting cells by genotype GII.4 norovirus virus-like particles. J. Transl. Med. 2013. 11: 127.
106. Lindesmith, L. C., Donaldson, E., Leon, J., Moe, C. L., Frelinger, J. A., Johnston, R. E., Weber, D. J. et al., Heterotypic humoral and cellular immune responses following Norwalk virus infection. J. Virol. 2010. 84: 1800-1815.
107. Chen, S. M., Lin, C. P., Tsai, J. D., Chao, Y. H. and Sheu, J. N., The significance of serum and fecal levels of interleukin-6 and interleukin-8 in hospitalized children with acute rotavirus and norovirus gastroenteritis. Pediatr. Neonatol. 2014. 55: 120-126.
108. Long, K. Z., Garcia, C., Ko, G., Santos, J. I., Al Mamun, A., Rosado, J. L., DuPont, H. L. et al., Vitamin A modifies the intestinal chemokine and cytokine responses to norovirus infection in Mexican children. J. Nutr. 2011. 141: 957-963.
109. Hinkula, J., Ball, J. M., Lofgren, S., Estes, M. K. and Svensson, L., Antibody prevalence and immunoglobulin IgG subclass pattern to Norwalk virus in Sweden. J. Med. Virol. 1995. 47: 52-57.
110. Wingfield, T., Gallimore, C. I., Xerry, J., Gray, J. J., Klapper, P., Guiver, M. and Blanchard, T. J., Chronic norovirus infection in an HIV-positive patient with persistent diarrhoea: a novel cause. J. Clin. Virol. 2010. 49: 219-222.
111. Nilsson, M., Hedlund, K. O., Thorhagen, M., Larson, G., Johansen, K., Ekspong, A. and Svensson, L., Evolution of human calicivirus RNA in vivo: accumulation of mutations in the protruding P2 domain of the capsid leads to structural changes and possibly a new phenotype. J. Virol. 2003. 77: 13117-13124.
112. Iritani, N., Seto, T., Hattori, H., Natori, K., Takeda, N., Kubo, H., Yamano, T. et al., Humoral immune responses against norovirus infections of children. J. Med. Virol. 2007. 79: 1187-1193.
113. Rockx, B., Baric, R. S., deGrijs, I., Duizer, E. and Koopmans, M. P., Characterization of the homo- and heterotypic immune responses after natural norovirus infection. J. Med. Virol. 2005. 77: 439-446.
114. Cukor, G., Nowak, N. A. and Blacklow, N. R., Immunoglobulin M responses to the Norwalk virus of gastroenteritis. Infect. Immun. 1982. 37: 463-468.
115. Leon, J., Souza, M., Qiuhong, W., Smith, E., Saif, L. and Moe, C., Immunology of norovirus infection. In Michael, V. (Ed.) Immunity against mucosal pathogens, Springer, New York, 2008, 219-262.
116. Treanor, J. J., Jiang, X., Madore, H. P. and Estes, M. K., Subclass-specific serum antibody responses to recombinant Norwalk virus capsid antigen (rNV) in adults infected with Norwalk, Snow Mountain, or Hawaii virus. J. Clin. Microbiol. 1993. 31: 1630-1634.
117. Wyatt, R. G., Dolin, R., Blacklow, N. R., DuPont, H. L., Buscho, R. F., Thornhill, T. S., Kapikian, A. Z. et al., Comparison of three agents of acute infectious nonbacterial gastroenteritis by cross-challenge in volunteers. J. Infect. Dis. 1974. 129: 709-714.
118. Parra, G. I. and Green, K. Y., Sequential gastroenteritis episodes caused by 2 norovirus genotypes. Emerg. Infect. Dis. 2014. 20: 1016-1018.
119. Saito, M., Goel-Apaza, S., Espetia, S., Velasquez, D., Cabrera, L., Loli, S., Crabtree, J. E. et al., Multiple norovirus infections in a birth cohort in a Peruvian Periurban community. Clin. Infect. Dis. 2014. 58: 483-491.
120. Simmons, K., Gambhir, M., Leon, J. and Lopman, B., Duration of immunity to norovirus gastroenteritis. Emerg. Infect. Dis. 2013. 19: 1260-1267.
121. Parrino, T. A., Schreiber, D. S., Trier, J. S., Kapikian, A. Z. and Blacklow, N. R., Clinical immunity in acute gastroenteritis caused by Norwalk agent. N. Engl. J. Med. 1977. 297: 86-89.
122. Atmar, R. L., Bernstein, D. I., Harro, C. D., Al-Ibrahim, M. S., Chen, W. H., Ferreira, J., Estes, M. K. et al., Norovirus vaccine against experimental human Norwalk virus illness. N. Engl. J. Med. 2011. 365: 2178-2187.
123. Ball, J. M., Graham, D. Y., Opekun, A. R., Gilger, M. A., Guerrero, R. A. and Estes, M. K., Recombinant Norwalk virus-like particles given orally to volunteers: phase I study. Gastroenterology 1999. 117: 40-48.
124. El-Kamary, S. S., Pasetti, M. F., Mendelman, P. M., Frey, S. E., Bernstein, D. I., Treanor, J. J., Ferreira, J. et al., Adjuvanted intranasal Norwalk virus-like particle vaccine elicits antibodies and antibody-secreting cells that express homing receptors for mucosal and peripheral lymphoid tissues. J. Infect. Dis. 2010. 202: 1649-1658.
125. Tacket, C. O., Sztein, M. B., Losonsky, G. A., Wasserman, S. S. and Estes, M. K., Humoral, mucosal, and cellular immune responses to oral Norwalk virus-like particles in volunteers. Clin. Immunol. 2003. 108: 241-247.
126. Treanor, J. J., Atmar, R. L., Frey, S. E., Gormley, R., Chen, W. H., Ferreira, J., Goodwin, R. et al., A novel intramuscular bivalent norovirus virus-like particle vaccine candidate-reactogenicity, safety, and immunogenicity in a phase 1 trial in healthy adults. J. Infect. Dis. 2014. 210: 1763-1771.
127. Atmar, R. L. and Estes, M. K., Norovirus vaccine development: next steps. Expert Rev. Vaccines 2012. 11: 1023-1025.
128. Hickman, D., Jones, M. K., Zhu, S., Kirkpatrick, E., Ostrov, D. A., Wang, X., Ukhanova, M. et al., The effect of malnutrition on norovirus infection. MBio 2014. 5: e01032-01013.
129. Nelson, A. M., Elftman, M. D., Pinto, A. K., Baldridge, M., Hooper, P., Kuczynski, J., Petrosino, J. F. et al., Murine norovirus infection does not cause major disruptions in the murine intestinal microbiota. Microbiome 2013. 1: 7.
130. Nelson, A. M., Walk, S. T., Taube, S., Taniuchi, M., Houpt, E. R., Wobus, C. E. and Young, V. B., Disruption of the human gut microbiota following Norovirus infection. PLoS One 2012. 7: e48224.
131. Cadwell, K., Patel, K. K., Maloney, N. S., Liu, T. C., Ng, A. C., Storer, C. E., Head, R. D. et al., Virus-plus-susceptibility gene interaction determines Crohn's disease gene Atg16L1 phenotypes in intestine. Cell 2010. 141: 1135-1145.
132. Basic, M., Keubler, L. M., Buettner, M., Achard, M., Breves, G., Schroder, B., Smoczek, A. et al., Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm. Bowel Dis. 2014. 20: 431-443.
133. Kernbauer, E., Ding, Y. and Cadwell, K., An enteric virus can replace the beneficial function of commensal bacteria. Nature 2014. 516: 94-98.
134. Tamura, M., Natori, K., Kobayashi, M., Miyamura, T. and Takeda, N., Genogroup II noroviruses efficiently bind to heparan sulfate proteoglycan associated with the cellular membrane. J. Virol. 2004. 78: 3817-3826.
135. Murakami, K., Kurihara, C., Oka, T., Shimoike, T., Fujii, Y., Takai-Todaka, R., Park, Y. et al., Norovirus binding to intestinal epithelial cells is independent of histo-blood group antigens. PLoS One 2013. 8: e66534.
136. Makino, A., Shimojima, M., Miyazawa, T., Kato, K., Tohya, Y. and Akashi, H., Junctional adhesion molecule 1 is a functional receptor for feline calicivirus. J. Virol. 2006. 80: 4482-4490.
137. Stuart, A. D. and Brown, T. D., Alpha2, 6-linked sialic acid acts as a receptor for Feline calicivirus. J. Gen. Virol. 2007. 88: 177-186.
138. Monne Rodriguez, J. M., Soare, T., Malbon, A., Blundell, R., Papoula-Pereira, R., Leeming, G., Kohler, K. et al., Alveolar macrophages are the main target cells in feline calicivirus-associated pneumonia. Vet. J. 2014. 201: 156-165.
139. Kreutz, L. C., Seal, B. S. and Mengeling, W. L., Early interaction of feline calicivirus with cells in culture. Arch. Virol. 1994. 136: 19-34.
140. Taube, S., Perry, J. W., Yetming, K., Patel, S. P., Auble, H., Shu, L., Nawar, H. F. et al., Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J. Virol. 2009. 83: 4092-4101.
141. Taube, S., Perry, J. W., McGreevy, E., Yetming, K., Perkins, C., Henderson, K. and Wobus, C. E., Murine noroviruses bind glycolipid and glycoprotein attachment receptors in a strain-dependent manner. J. Virol. 2012. 86: 5584-5593.
142. Zakhour, M., Ruvoen-Clouet, N., Charpilienne, A., Langpap, B., Poncet, D., Peters, T., Bovin, N. et al., The alphaGal epitope of the histo-blood group antigen family is a ligand for bovine norovirus Newbury2 expected to prevent cross-species transmission. PLoS Pathog. 2009. 5: e1000504.
143. Jung, K., Scheuer, K. A., Zhang, Z., Wang, Q. and Saif, L. J., Pathogenesis of GIII.2 bovine norovirus, CV186-OH/00/US strain in gnotobiotic calves. Vet. Microbiol. 2014. 168: 202-207.
144. Kim, D. S., Hosmillo, M., Alfajaro, M. M., Kim, J. Y., Park, J. G., Son, K. Y., Ryu, E. H. et al., Both alpha2, 3- and alpha2, 6-linked sialic acids on o-linked glycoproteins act as functional receptors for porcine sapovirus. PLoS Pathog. 2014. 10: e1004172.
145. Chang, K. O., Sosnovtsev, S. V., Belliot, G., Kim, Y., Saif, L. J. and Green, K. Y., Bile acids are essential for porcine enteric calicivirus replication in association with down-regulation of signal transducer and activator of transcription 1. Proc. Natl. Acad. Sci. USA 2004. 101: 8733-8738.
146. Parwani, A. V., Flynn, W. T., Gadfield, K. L. and Saif, L. J., Serial propagation of porcine enteric calicivirus in a continuous cell line. Effect of medium supplementation with intestinal contents or enzymes. Arch. Virol. 1991. 120: 115-122.
147. Farkas, T., Cross, R. W., Hargitt, E., 3rd, Lerche, N. W., Morrow, A. L. and Sestak, K., Genetic diversity and histo-blood group antigen interactions of rhesus enteric caliciviruses. J. Virol. 2010. 84: 8617-8625.
148. Farkas, T., Sestak, K., Wei, C. and Jiang, X., Characterization of a rhesus monkey calicivirus representing a new genus of Caliciviridae. J. Virol. 2008. 82: 5408-5416.
149. Smiley, J. R., Chang, K. O., Hayes, J., Vinje, J. and Saif, L. J., Characterization of an enteropathogenic bovine calicivirus representing a potentially new calicivirus genus. J. Virol. 2002. 76: 10089-10098.
150. Dolin, R., Blacklow, N. R., DuPont, H., Formal, S., Buscho, R. F., Kasel, J. A., Chames, R. P. et al., Transmission of acute infectious nonbacterial gastroenteritis to volunteers by oral administration of stool filtrates. J. Infect. Dis. 1971. 123: 307-312.
151. Kapikian, A. Z., Wyatt, R. G., Dolin, R., Thornhill, T. S., Kalica, A. R. and Chanock, R. M., Visualization by immune electron microscopy of a 27-nm particle associated with acute infectious nonbacterial gastroenteritis. J. Virol. 1972. 10: 1075-1081.
152. Dolin, R., Blacklow, N. R., DuPont, H., Buscho, R. F., Wyatt, R. G., Kasel, J. A., Hornick, R. et al., Biological properties of Norwalk agent of acute infectious nonbacterial gastroenteritis. Proc. Soc. Exp. Biol. Med. 1972. 140: 578-583.
153. Agus, S. G., Dolin, R., Wyatt, R. G., Tousimis, A. J. and Northrup, R. S., Acute infectious nonbacterial gastroenteritis: intestinal histopathology. Histologic and enzymatic alterations during illness produced by the Norwalk agent in man. Ann. Intern. Med. 1973. 79: 18-25.
154. Widerlite, L., Trier, J. S., Blacklow, N. R. and Schreiber, D. S., Structure of the gastric mucosa in acute infectious bacterial gastroenteritis. Gastroenterology 1975. 68: 425-430.
155. Dolin, R., Reichman, R. C., Roessner, K. D., Tralka, T. S., Schooley, R. T., Gary, W. and Morens, D., Detection by immune electron microscopy of the Snow Mountain agent of acute viral gastroenteritis. J. Infect. Dis. 1982. 146: 184-189.
156. Keswick, B. H., Satterwhite, T. K., Johnson, P. C., DuPont, H. L., Secor, S. L., Bitsura, J. A., Gary, G. W. et al., Inactivation of Norwalk virus in drinking water by chlorine. Appl. Environ. Microbiol. 1985. 50: 261-264.
157. Treanor, J. J., Madore, H. P. and Dolin, R., Development of an enzyme immunoassay for the Hawaii agent of viral gastroenteritis. J. Virol. Methods 1988. 22: 207-214.
158. Graham, D. Y., Jiang, X., Tanaka, T., Opekun, A. R., Madore, H. P. and Estes, M. K., Norwalk virus infection of volunteers: new insights based on improved assays. J. Infect. Dis. 1994. 170: 34-43.
159. Teunis, P. F., Moe, C. L., Liu, P., Miller, S. E., Lindesmith, L., Baric, R. S., LePendu, J. et al., Norwalk virus: how infectious is it? J. Med. Virol. 2008. 80: 1468-1476.