A Working Model of How Noroviruses Infect the Intestine

1. Payne DC, Vinje J, Szilagyi PG, Edwards KM, Staat MA, et al. (2013) Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med 368: 1121–1130. doi: 10.1056/NEJMsa1206589 23514289

2. Green KY (2013) Caliciviridae: The Noroviruses. In: Knipe DM, Howley P.M., Cohen J.I., Griffin D.I., Lamb R.A., Martin M.A., Racaniello V.R., and Roizman B., editor. Fields Virology. Philadelphia: Lippincott Williams & Wilkins, a Wolters Kluwer Business. pp. 582–608.

3. Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, et al. (2008) Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg Infect Dis 14: 1224–1231. doi: 10.3201/eid1408.071114 18680645

4. Gonzalez-Hernandez MB, Liu T, Blanco LP, Auble H, Payne HC, et al. (2013) Murine norovirus transcytosis across an in vitro polarized murine intestinal epithelial monolayer is mediated by M-like cells. J Virol 87: 12685–12693. doi: 10.1128/JVI.02378-13 24049163

5. Marionneau S, Ruvoen N, Le Moullac-Vaidye B, Clement M, Cailleau-Thomas A, et al. (2002) Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122: 1967–1977. 12055602

6. Karst SM, Wobus CE, Goodfellow IG, Green KY, Virgin HW (2014) Advances in norovirus biology. Cell Host Microbe 15: 668–680. doi: 10.1016/j.chom.2014.05.015 24922570

7. Mabbott NA, Donaldson DS, Ohno H, Williams IR, Mahajan A (2013) Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 6: 666–677. doi: 10.1038/mi.2013.30 23695511

8. Gonzalez-Hernandez MB, Liu T, Payne HC, Stencel-Baerenwald JE, Ikizler M, et al. (2014) Efficient Norovirus and Reovirus Replication in the Mouse Intestine Requires Microfold (M) Cells. J Virol 88: 6934–6943. doi: 10.1128/JVI.00204-14 24696493

9. Miller H, Zhang J, Kuolee R, Patel GB, Chen W (2007) Intestinal M cells: the fallible sentinels? World J Gastroenterol 13: 1477–1486. 17461437

10. Otto PH, Clarke IN, Lambden PR, Salim O, Reetz J, et al. (2011) Infection of calves with bovine norovirus GIII.1 strain Jena virus: an experimental model to study the pathogenesis of norovirus infection. J Virol 85: 12013–12021. doi: 10.1128/JVI.05342-11 21880760

11. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV, et al. (2004) Replication of Norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2: e432. 15562321

12. Ward JM, Wobus CE, Thackray LB, Erexson CR, Faucette LJ, et al. (2006) Pathology of immunodeficient mice with naturally occurring murine norovirus infection. Toxicol Pathol 34: 708–715. 17074739

13. Lay MK, Atmar RL, Guix S, Bharadwaj U, He H, 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. doi: 10.1016/j.virol.2010.07.001 20667573

14. Chan MC, Ho WS, Sung JJ (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: 8427–8430. doi: 10.1128/JVI.05016-11 21680503

15. Taube S, Kolawole AO, Hohne M, Wilkinson JE, Handley SA, et al. (2013) A mouse model for human norovirus. MBio 4: e00450–13. doi: 10.1128/mBio.00450-13 23860770

16. Bok K, Parra GI, Mitra T, Abente E, Shaver CK, et al. (2011) Chimpanzees as an animal model for human norovirus infection and vaccine development. Proc Natl Acad Sci U S A 108: 325–330. doi: 10.1073/pnas.1014577107 21173246

17. Sestak K, Feely S, Fey B, Dufour J, Hargitt E, et al. (2012) Experimental inoculation of juvenile rhesus macaques with primate enteric caliciviruses. PLoS ONE 7: e37973. doi: 10.1371/journal.pone.0037973 22666426

18. Zhu S, Regev D, Watanabe M, Hickman D, Moussatche N, et al. (2013) Identification of immune and viral correlates of norovirus protective immunity through comparative study of intra-cluster norovirus strains. PLoS Pathog 9: e1003592. doi: 10.1371/journal.ppat.1003592 24039576

19. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR, et al. (2014) Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346: 755–759. doi: 10.1126/science.1257147 25378626

20. Narvaez CF, Franco MA, Angel J, Morton JM, Greenberg HB (2010) Rotavirus differentially infects and polyclonally stimulates human B cells depending on their differentiation state and tissue of origin. J Virol 84: 4543–4555. doi: 10.1128/JVI.02550-09 20164228

21. Feng Z, Hensley L, McKnight KL, Hu F, Madden V, et al. (2013) A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496: 367–371. doi: 10.1038/nature12029 23542590

22. Basic M, Keubler LM, Buettner M, Achard M, Breves G, et al. (2014) Norovirus triggered microbiota-driven mucosal inflammation in interleukin 10-deficient mice. Inflamm Bowel Dis 20: 431–443. doi: 10.1097/01.MIB.0000441346.86827.ed 24487272

23. Mumphrey SM, Changotra H, Moore TN, Heimann-Nichols ER, Wobus CE, 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: 3251–3263. 17229692

24. Wilks J, Golovkina T (2012) Influence of microbiota on viral infections. PLoS Pathog 8: e1002681. doi: 10.1371/journal.ppat.1002681 22615558

25. Kuss SK, Best GT, Etheredge CA, Pruijssers AJ, Frierson JM, et al. (2011) Intestinal microbiota promote enteric virus replication and systemic pathogenesis. Science 334: 249–252. doi: 10.1126/science.1211057 21998395

26. Kane M, Case LK, Kopaskie K, Kozlova A, MacDearmid C, et al. (2011) Successful transmission of a retrovirus depends on the commensal microbiota. Science 334: 245–249. doi: 10.1126/science.1210718 21998394

27. Robinson CM, Jesudhasan PR, Pfeiffer JK (2014) Bacterial lipopolysaccharide binding enhances virion stability and promotes environmental fitness of an enteric virus. Cell Host Microbe 15: 36–46. doi: 10.1016/j.chom.2013.12.004 24439896

28. Tan M, Jiang X (2011) Norovirus-host interaction: multi-selections by human histo-blood group antigens. Trends Microbiol 19: 382–388. doi: 10.1016/j.tim.2011.05.007 21705222

29. Guix S, Asanaka M, Katayama K, Crawford SE, Neill FH, et al. (2007) Norwalk virus RNA is infectious in mammalian cells. J Virol 81: 12238–12248. 17855551

30. Andersson M, Carlin N, Leontein K, Lindquist U, Slettengren K (1989) Structural studies of the O-antigenic polysaccharide of Escherichia coli O86, which possesses blood-group B activity. Carbohydr Res 185: 211–223. 2471591

31. Aspinall GO, Monteiro MA (1996) Lipopolysaccharides of Helicobacter pylori strains P466 and MO19: structures of the O antigen and core oligosaccharide regions. Biochemistry 35: 2498–2504. 8652594

32. Rasko DA, Wang G, Monteiro MA, Palcic MM, Taylor DE (2000) Synthesis of mono- and di-fucosylated type I Lewis blood group antigens by Helicobacter pylori. Eur J Biochem 267: 6059–6066. 10998067

33. Springer GF, Williamson P, Brandes WC (1961) Blood Group Activity of Gram-Negative Bacteria. J Exp Med 113: 1077–1093. 19867191

34. Yi W, Shao J, Zhu L, Li M, Singh M, et al. (2005) Escherichia coli O86 O-antigen biosynthetic gene cluster and stepwise enzymatic synthesis of human blood group B antigen tetrasaccharide. J Am Chem Soc 127: 2040–2041. 15713070

35. Miura T, Sano D, Suenaga A, Yoshimura T, Fuzawa M, et al. (2013) Histo-blood group antigen-like substances of human enteric bacteria as specific adsorbents for human noroviruses. J Virol 87: 9441–9451. doi: 10.1128/JVI.01060-13 23804639

36. Taube S, Perry JW, Yetming K, Patel SP, Auble H, et al. (2009) Ganglioside-linked terminal sialic acid moieties on murine macrophages function as attachment receptors for murine noroviruses. J Virol 83: 4092–4101. doi: 10.1128/JVI.02245-08 19244326

37. Vimr ER, Kalivoda KA, Deszo EL, Steenbergen SM (2004) Diversity of microbial sialic acid metabolism. Microbiol Mol Biol Rev 68: 132–153. 15007099

38. Bansil R, Celli JP, Hardcastle JM, Turner BS (2013) The Influence of Mucus Microstructure and Rheology in Helicobacter pylori Infection. Front Immunol 4: 310. doi: 10.3389/fimmu.2013.00310 24133493

39. Rol N, Favre L, Benyacoub J, Corthesy B (2012) The role of secretory immunoglobulin A in the natural sensing of commensal bacteria by mouse Peyer’s patch dendritic cells. J Biol Chem 287: 40074–40082. doi: 10.1074/jbc.M112.405001 23027876

40. Mkaddem SB, Christou I, Rossato E, Berthelot L, Lehuen A, et al. (2014) IgA, IgA receptors, and their anti-inflammatory properties. Curr Top Microbiol Immunol 382: 221–235. doi: 10.1007/978-3-319-07911-0_10 25116102

41. Teunis PF, Sukhrie FH, Vennema H, Bogerman J, Beersma MF, et al. (2014) Shedding of norovirus in symptomatic and asymptomatic infections. Epidemiol Infect: 1–8. 25544572

42. Ball JM, Mitchell DM, Gibbons TF, Parr RD (2005) Rotavirus NSP4: a multifunctional viral enterotoxin. Viral Immunol 18: 27–40. 15802952

43. Muller PA, Koscso B, Rajani GM, Stevanovic K, Berres ML, et al. (2014) Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158: 300–313. doi: 10.1016/j.cell.2014.04.050 25036630

44. Wouters MM, Boeckxstaens GE (2011) Neuroimmune mechanisms in functional bowel disorders. Neth J Med 69: 55–61. 21411840

45. Wehner S, Behrendt FF, Lyutenski BN, Lysson M, Bauer AJ, et al. (2007) Inhibition of macrophage function prevents intestinal inflammation and postoperative ileus in rodents. Gut 56: 176–185. 16809419

46. Kernbauer E, Ding Y, Cadwell K (2014) An enteric virus can replace the beneficial function of commensal bacteria. Nature 516: 94–98. doi: 10.1038/nature13960 25409145

47. Baldridge MT, Nice TJ, McCune BT, Yokoyama CC, Kambal A, et al. (2014) Commensal microbes and interferon-lambda determine persistence of enteric murine norovirus infection. Science 347: 266–269. doi: 10.1126/science.1258025 25431490