Binding to histo-blood group antigen-expressing bacteria protects human norovirus from acute heat stress

Frontiers in Microbiology

Volumn 6, Issue JUL, 2015, Pages

  Li, Dan ^a   Breiman, Adrien ^b,c,d,e   le Pendu, Jacques ^b,c,d   Uyttendaele, Mieke ^a  

^a GHENT UNIVERSITY   (Belgium)

^b INSERM   (France)

^c CNRS   (France)

^d UNIVERSITÉ DE NANTES   (France)

^e NANTES UNIVERSITY HOSPITAL   (France)

Author keywords

Bacteria; Heat; Histo blood group antigens (HBGAs); Norovirus; Protection

Indexed keywords

BACTERIAL ANTIGEN; BLOOD GROUP ANTIGEN; HISTO BLOOD GROUP ANTIGEN; UNCLASSIFIED DRUG;

ANTIGEN EXPRESSION; ARTICLE; BIFIDOBACTERIUM ADOLESCENTIS; BIFIDOBACTERIUM LONGUM; BINDING AFFINITY; BINDING ASSAY; CELL PROTECTION; CONTROLLED STUDY; ENTEROBACTER AEROGENES; ENTEROBACTER CLOACAE; ENZYME LINKED IMMUNOSORBENT ASSAY; ESCHERICHIA COLI; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPY; HEAT STRESS; HEAT TREATMENT; NONHUMAN; NOROVIRUS; PEPTOCLOSTRIDIUM DIFFICILE; VIRUS LIKE AGENT; VIRUS TRANSMISSION;

BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM ADOLESCENTIS; CLOSTRIDIUM DIFFICILE; ENTEROBACTER AEROGENES; ENTEROBACTER CLOACAE; ESCHERICHIA COLI; NOROVIRUS; SUS;

EID: 84938820993     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00659     Document Type: Article

References (26)

1. Atmar, R. L., and Estes, M. K. (2006). The epidemiologic and clinical importance of norovirus infection. Gastroenterol. Clin. North Am. 35, 275-290. doi: 10.1016/j.gtc.2006.03.001.
2. Bertrand, I., Schijven, J., Sanchez, G., Wyn-Jones, P., Ottoson, J., Morin, T., et al. (2012). The impact of temperature on the inactivation of enteric viruses in food and water: a review. J. Appl. Microbiol. 112, 1059-1074. doi: 10.1111/j.1365-2672.2012.05267.x.
3. Caddy, S., Breiman, A., le Pendu, J., and Goodfellow, I. (2014). Genogroup IV and VI canine noroviruses interact with histo-blood group antigens. J. Virol. 88, 10377-10391. doi: 10.1128/JVI.01008-14.
4. da Silva, A. K., Le Saux, J.-C., Parnaudeau, S., Pommepuy, M., Elimelech, M., and Le Guyader, F. S. (2007). Evaluation of removal of noroviruses during wastewater treatment, using real-time reverse transcription-PCR: different behaviors of genogroups I and II. Appl. Environ. Microbiol. 73, 7891-7897. doi: 10.1128/AEM.01428-07.
5. Donaldson, E. F., Lindesmith, L. C., Lobue, A. D., and Baric, R. S. (2010). Viral shape-shifting: norovirus evasion of the human immune system. Nat. Rev. Microbiol. 8, 231-241. doi: 10.1038/nrmicro2296.
6. Duizer, E., Schwab, K. J., Neill, F. H., Atmar, R. L., Koopmans, M. P., and Estes, M. K. (2004). Laboratory efforts to cultivate noroviruses. J. Gen. Virol. 85, 79-87. doi: 10.1099/vir.0.19478-0.
7. Hirneisen, K. A., Black, E. P., Cascarino, J. L., Fino, V. R., Hoover, D. G., and Kniel, K. E. (2010). Viral inactivation in foods: a review of traditional and novel food-processing technologies. Compr. Rev. Food Sci. Food Saf. 9, 3-20. doi: 10.1111/j.1541-4337.2009.00092.x.
8. Hirneisen, K. A., and Kniel, K. E. (2013). Norovirus attachment: implications for food safety. Food Prot. Trends 33, 290-299.
9. Huang, P., Farkas, T., Zhong, W., Tan, M., Thornton, S., Morrow, A. L., et al. (2005). Norovirus and histo-blood group antigens: demonstration of a wide spectrum of strain specificities and classification of two major binding groups among multiple binding patterns. J. Virol. 79, 6714-6722. doi: 10.1128/JVI.79.11.6714-6722.2005.
10. Jones, M. K., Watanabe, M., Zhu, S., Graves, C. L., Keyes, L. R., Grau, K. R., et al. (2014). Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346, 755-759. doi: 10.1126/science.1257147.
11. Le Guyader, S., Atmar, R., Maalouf, H., and Le Pendu, J. (2013). Shellfish contamination by norovirus: strain selection based on ligand expression? Rinsho to uirusu. Clin. Virol. 41, 3-18.
12. Le Pendu, J., Le Cabellec, M., and Bara, J. (1997). Immunohistological analysis of antibodies against ABH and other glycoconjugates in normal human pyloric and duodenal mucosae. Transfus. Clin. Biol. 4, 41-46. doi: 10.1016/S1246-7820(97)80009-2.
13. Marionneau, S., Cailleau-Thomas, A., Rocher, J., Le Moullac-Vaidye, B., Ruvoen, N., Clement, M., et al. (2001). ABH and Lewis histo-blood group antigens, a model for the meaning of oligosaccharide diversity in the face of a changing world. Biochimie 83, 565-573. doi: 10.1016/S0300-9084(01)01321-9.
14. Marionneau, S., Ruvoën, N., Le Moullac-Vaidye, B., Clement, M., Cailleau-Thomas, A., Ruiz-Palacois, G., et al. (2002). Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122, 1967-1977. doi: 10.1053/gast.2002.33661.
15. Miura, T., Sano, D., Suenaga, A., Yoshimura, T., Fuzawa, M., Nakagomi, T., 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.
16. Papafragkou, E., Hewitt, J., Park, G. W., Greening, G., and Vinje, J. (2013). Challenges of culturing human norovirus in three-dimensional organoid intestinal cell culture models. PLoS ONE 8:e63485. doi: 10.1371/journal.pone.0063485.
17. Patel, M. M., Hall, A. J., Vinjé, J., and Parashar, U. D. (2009). Noroviruses: a comprehensive review. J. Clin. Virol. 44, 1-8. doi: 10.1016/j.jcv.2008.10.009.
18. Pettit, N., Styslinger, T., Mei, Z., Han, W., Zhao, G., and Wang, P. G. (2010). Characterization of WbiQ: an α1,2-fucosyltransferase from Escherichia coli O127:K63(B8), and synthesis of H-type 3 blood group antigen. Biochem. Biophys. Res. Commun. 402, 190-195. doi: 10.1016/j.bbrc.2010.08.087.
19. Prasad, B. V., Shanker, S., Hu, L., Cho, J.-M., Crawford, S. E., Ramani, S., et al. (2014). Structural basis of glycan interaction in gastroenteric viral pathogens. Curr. Opin. Virol. 7, 119-127. doi: 10.1016/j.coviro.2014.05.008.
20. Rahman, S. (2007). Handbook of Food Preservation, 2 Edn. Boca Raton: CRC Press, 71-634. doi: 10.1201/9781420017373.
21. Ruvoën-Clouet, N., Belliot, G., and Le Pendu, J. (2013). Noroviruses and histo-blood groups: the impact of common host genetic polymorphisms on virus transmission and evolution. J. Rev. Med. Virol. 23, 355-366. doi: 10.1002/rmv.1757.
22. Springer, G. F., Williamson, P., and Brandes, W. C. (1961). Blood group activity of gram-negative bacteria. J. Exp. Med. 113, 1077-1093. doi: 10.1084/jem.113.6.1077.
23. Tan, M., and Jiang, X. (2010). Norovirus gastroenteritis, carbohydrate receptors, and animal models. PLoS Pathog. 6:e1000983. doi: 10.1371/journal.ppat.1000983.
24. Tian, P., Engelbrektson, A., and Mandrell, R. (2008). Two-log increase in sensitivity for detection of norovirus in complex samples by concentration with porcine gastric mucin conjugated to magnetic beads. Appl. Environ. Microbiol. 74, 4271-4276. doi: 10.1128/AEM.00539-08.
25. Van Beek, J., Ambert-Balay, K., Botteldoorn, N., Eden, J., Fonager, J., Hewitt, J., et al. (2013). Indications for worldwide increased norovirus activity associated with emergence of a new variant of genotype II. 4, late 2012. Euro Surveill. 18, 8-9.
26. Yi, W., Shao, J., Zhu, L., Li, M., Singh, M., Lu, Y., 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. doi: 10.1021/ja045021y.