Binding of human GII.4 norovirus virus-like particles to carbohydrates of romaine lettuce leaf cell wall materials

Applied and Environmental Microbiology

Volumn 78, Issue 3, 2012, Pages 786-794

  Esseili, Malak A ^a   Wang, Qiuhong ^a   Saif, Linda J ^a  

^a OHIO STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL WALLS; CUT EDGE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOFLUORESCENCE ANALYSIS; LEAF CELLS; LEAF SURFACES; PORCINE GASTRIC MUCINS; SIALIC ACIDS; VIRUS-LIKE PARTICLES;

CARBOXYLIC ACIDS; VIRUSES;

CARBOHYDRATES;

CARBOHYDRATE; LECTIN; VIROSOME; VIRUS PROTEIN;

ANTIGEN; CARBOHYDRATE; CELL ORGANELLE; GENOTYPE; IMMUNOASSAY; INHIBITION; LEAF; LEAFY VEGETABLE; PERSISTENCE; STOMATA; VIRUS;

ARTICLE; CARBOHYDRATE METABOLISM; CELL WALL; CHEMISTRY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; ISOLATION AND PURIFICATION; LETTUCE; METABOLISM; NOROVIRUS; PHYSIOLOGY; PLANT LEAF; VIROLOGY; VIRUS ATTACHMENT;

CARBOHYDRATE METABOLISM; CARBOHYDRATES; CELL WALL; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; LECTINS; LETTUCE; NOROVIRUS; PLANT LEAVES; VIRAL PROTEINS; VIROSOMES; VIRUS ATTACHMENT;

LACTUCA; NOROVIRUS; SUS;

EID: 84862965497     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.07081-11     Document Type: Article

References (51)

1. Barton CJ, et al. 2006. Enzymatic fingerprinting of Arabidopsis pectic polysaccharides using polysaccharide analysis by carbohydrate gel electrophoresis (PACE). Planta 224:163-174.
2. Berger CN, et al. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ. Microbiol. 12:2385-2397.
3. Blancard D, Lot H, Maisonneuve B. 2006. A color atlas of diseases of lettuce and related salad crops: observation, biology and control. Elsevier/Academic Press, Boston, MA.
4. Bull RA, Tu ET, McIver CJ, Rawlinson WD, White PA. 2006. Emergence of a new norovirus genotype II.4 variant associated with global outbreaks of gastroenteritis. J. Clin. Microbiol. 44:327-333.
5. Caffall KH, Mohnen D. 2009. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 344:1879-1900.
6. Carter MJ. 2005. Enterically infecting viruses: pathogenicity, transmission and significance for food and waterborne infection. J. Appl. Microbiol. 98:1354-1380.
7. Cheetham S, et al. 2007. Binding patterns of human norovirus-like particles to buccal and intestinal tissues of gnotobiotic pigs in relation to A/H histo-blood group antigen expression. J. Virol. 81:3535-3544.
8. Cheetham S, et al. 2006. Pathogenesis of a genogroup II human norovirus in gnotobiotic pigs. J. Virol. 80:10372-10381.
9. Cheng PK, Wong DK, Chung TW, Lim WW. 2005. Norovirus contamination found in oysters worldwide. J. Med. Virol. 76:593-597.
10. Delaquis P, Stewart S, Toivonen P, Moyls A. 1999. Effect of warm, chlorinated water on the microbial flora of shredded iceberg lettuce. Food Res. Int. 32:7-14.
11. Ethelberg S, et al. 2010. Outbreaks of gastroenteritis linked to lettuce, Denmark, January 2010. Euro Surveill. 15:pii=19484.
12. Fligger JM, Gibson CA, Sordillo LM, Baumrucker CR. 1997. Arginine supplementation increases weight gain, depresses antibody production, and alters circulating leukocyte profiles in preruminant calves without affecting plasma growth hormone concentrations. J. Anim. Sci. 75:3019-3025.
13. Fry SC. 2000. The growing plant cell wall: chemical and metabolic analysis, reprint of 1st ed. Blackburn Press, Caldwell, NJ.
14. Gandhi KM, Mandrell RE, Tian P. 2010. Binding of virus-like particles of Norwalk virus to romaine lettuce veins. Appl. Environ. Microbiol. 76:7997-8003.
15. Glass RI, Parashar UD, Estes MK. 2009. Norovirus gastroenteritis. N. Engl. J. Med. 361:1776-1785.
16. Goyal SM. 2006. Viruses in foods. Springer, New York, NY.
17. Hoffman M, et al. 2005. Structural analysis of xyloglucans in the primary cell walls of plants in the subclass Asteridae. Carbohydr. Res. 340:1826-1840.
18. Huang P, et al. 2003. Noroviruses bind to human ABO, Lewis, and secretor histo-blood group antigens: identification of 4 distinct strainspecific patterns. J. Infect. Dis. 188:19-31.
19. Huang P, Morrow AL, Jiang X. 2009. The carbohydrate moiety and high molecular weight carrier of histo-blood group antigens are both required for norovirus-receptor recognition. Glycoconj. J. 26:1085-1096.
20. Kerstetter RA, Poethig RS. 1998. The specification of leaf identity during shoot development. Annu. Rev. Cell Dev. Biol. 14:373-398.
21. Koch JL, Nevins DJ. 1989. Tomato fruit cell wall. I. Use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental changes in pectins. Plant Physiol. 91:816-822.
22. Kondo N, Murata M, Isshiki K. 2006. Efficiency of sodium hypochlorite, fumaric acid, and mild heat in killing native microflora and Escherichia coli O157:H7, Salmonella typhimurium DT104, and Staphylococcus aureus attached to fresh-cut lettuce. J. Food Prot. 69:323-329.
23. Kristiansen KA, Potthast A, Christensen BE. 2010. Periodate oxidation of polysaccharides for modification of chemical and physical properties. Carbohydr Res. 345:1264-1271.
24. Kroupitski Y, Pinto R, Belausov E, Sela S. 2011. Distribution of Salmonella typhimurium in romaine lettuce leaves. Food Microbiol. 28:990-997.
25. Le Guyader F, et al. 2006. Norwalk virus-specific binding to oyster digestive tissues. Emerg. Infect. Dis. 12:931-936.
26. Lowther JA, Henshilwood K, Lees DN. 2008. Determination of norovirus contamination in oysters from two commercial harvesting areas over an extended period, using semiquantitative real-time reverse transcription PCR. J. Food Prot. 71:1427-1433.
27. Marionneau S, et al. 2002. Norwalk virus binds to histo-blood group antigens present on gastroduodenal epithelial cells of secretor individuals. Gastroenterology 122:1967-1977.
28. Matsui T, Hamako J, Ozeki Y, Titani K. 2001. Comparative study of blood group-recognizing lectins toward ABO blood group antigens on neoglycoproteins, glycoproteins and complex-type oligosaccharides. Biochim. Biophys. Acta 1525:50-57.
29. Mead PS, et al. 1999. Food-related illness and death in the United States. Emerg. Infect. Dis. 5:607-625.
30. Mesquita JR, Nascimento MS. 2009. A foodborne outbreak of norovirus gastroenteritis associated with a Christmas dinner in Porto, Portugal, December 2008. Euro Surveill. 14:19355.
31. Nevins DJ, English PD, Albersheim P. 1967. The specific nature of plant cell wall polysaccharides. Plant Physiol. 42:900-906.
32. Nyachuba, D. G. 2010. Foodborne illness: is it on the rise? Nutr. Rev. 68:257-269.
33. Rose JKC. 2003. The plant cell wall. Blackwell, Oxford, United Kingdom.
34. Scallan E, et al. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 17:7-15.
35. Schmid D, et al. 2007. A foodborne norovirus outbreak due to manually prepared salad, Austria 2006. Infection 35:232-239.
36. Shirato H, et al. 2008. Noroviruses distinguish between type 1 and type 2 histo-blood group antigens for binding. J. Virol. 82:10756-10767.
37. Sussich F, Cesaro A. 2000. The kinetics of periodate oxidation of carbohydrates: a calorimetric approach. Carbohydr. Res. 329:87-95.
38. Teunis PF, et al. 2008. Norwalk virus: how infectious is it? J. Med. Virol. 80:1468-1476.
39. Thiellement H. 2007. Plant proteomics methods and protocols, p 79-91. Humana Press, Totowa, NJ.
40. Tian P, Bates AH, Jensen HM, Mandrell RE. 2006. Norovirus binds to blood group A-like antigens in oyster gastrointestinal cells. Lett. Appl. Microbiol. 43:645-651.
41. Tian P, Brandl M, Mandrell R. 2005. Porcine gastric mucin binds to recombinant norovirus particles and competitively inhibits their binding to histo-blood group antigens and Caco-2 cells. Lett. Appl. Microbiol. 41:315-320.
42. Tian P, Engelbrektson A, 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.
43. Tian P, et al. 2007. Binding of recombinant norovirus like particle to histo-blood group antigen on cells in the lumen of pig duodenum. Res. Vet. Sci. 83:410-418.
44. Tian P, et al. 2010. Specificity and kinetics of norovirus binding to magnetic bead-conjugated histo-blood group antigens. J. Appl. Microbiol. 109:1753-1762.
45. Tuan Zainazor C, et al. 2010. The scenario of norovirus contamination in food and food handlers. J. Microbiol. Biotechnol. 20:229-237.
46. Urbanucci A, Myrmel M, Berg I, von Bonsdorff CH, Maunula L. 2009. Potential internalisation of caliciviruses in lettuce. Int. J. Food Microbiol. 135:175-178.
47. Van Damme EJM, Peumans WJ, Pusztai A, Bardocz S. 1998. Handbook of plant lectins: properties and biomedical applications. John Wiley, Chichester, United Kingdom.
48. Vega E, Garland J, Pillai SD. 2008. Electrostatic forces control nonspecific virus attachment to lettuce. J. Food Prot. 71:522-529.
49. Vega E, Smith J, Garland J, Matos A, Pillaii SD. 2005. Variability of virus attachment patterns to butterhead lettuce. J. Food Prot. 68:2112-2117.
50. Wei J, Jin Y, Sims T, Kniel KE. 2010. Manure-and biosolids-resident murine norovirus 1 attachment to and internalization by Romaine lettuce. Appl. Environ. Microbiol. 76:578-583.
51. Zakhour M, et al. 2009. 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. 5:e1000504.