Immunosorbent analysis of toxin contamination in milk and ground beef using IgY-based ELISAFootnote

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References

• Arimitsu, H., Sasaki, K., Kohda, T., Shimizu, T., & Tsuji, T. (2014) Evaluation of Shiga toxin 2e-specific chicken egg yolk immunoglobulin: Production and neutralization activity. Microbiology and Immunology, 58, 643–648. doi: 10.1111/1348-0421.12197
   PubMed Web of Science ®Google Scholar
• Auld, D. L., Trostle, C. L., Miller, T. D., He, X. & Duncan, R. W. (2014). Risk of ricin from commercial castor production in North America. In J. Cherwonogrodzky (Ed.), Ricin toxin (pp. 86–97). Beijing: Bentham Science.
   Google Scholar
• Brandon, D. L. (2011) Detection of ricin contamination in ground beef by electrochemiluminescence immunosorbent assay. Toxins, 3, 398–408. doi: 10.3390/toxins3040398
   PubMed Web of Science ®Google Scholar
• Brandon, D. L., Adams, L. M., Yang, L. L., & Korn, A. M. (2014) Antibody interactions with Ricinus communis agglutinins studied by biolayer interferometry. Analytical Letters, 47, 1747–1758. doi: 10.1080/00032719.2014.886693
   Web of Science ®Google Scholar
• Brandon, D. L., & Carter, J. M. (2012) Immunoassay. In D.-W. Sun (Ed.), Handbook of food safety engineering (pp. 279–312). London: Blackwell.
   Google Scholar
• Brandon, D. L., & Hernlem, B. J. (2009) Development of monoclonal antibodies specific for Ricinus agglutinins. Food and Agricultural Immunology, 20, 11–22. doi: 10.1080/09540100802626487
   Web of Science ®Google Scholar
• Brandon, D. L., Korn, A. M., & Yang, L. L. (2012) Detection of ricin contamination in liquid egg by electrochemiluminescence immunosorbent assay. Journal of Food Science, 77, T83–T88. doi: 10.1111/j.1750-3841.2012.02627.x
   PubMed Web of Science ®Google Scholar
• Brandon, D. L., Korn, A. M., & Yang, L. L. (2014) Immunosorbent analysis of ricin contamination in milk using colorimetric, chemiluminescent and electrochemiluminescent detection. Food and Agricultural Immunology, 25, 160–172. doi: 10.1080/09540105.2012.753515
   Web of Science ®Google Scholar
• CDC. (2003) Investigation of a ricin-containing envelope at a postal facility – South Carolina, 2003. MMWR. Morbidity and Mortality Weekly Report, 52, 1129–1131.
   PubMedGoogle Scholar
• Chu, P. T., Lin, C. S., Chen, W. J., Chen, C. F., & Wen, H. W. (2012) Detection of gliadin in foods using a quartz crystal microbalance biosensor that incorporates gold nanoparticles. Journal of Agricultural and Food Chemistry, 60, 6483–6492. doi: 10.1021/jf2047866
   PubMed Web of Science ®Google Scholar
• Feng, Y., Liu, W., & Shi, D. (2013) Effectiveness of egg yolk antibody against Shiga toxin ii variant toxicity in vitro and in vivo. Current Microbiology, 67, 448–453. doi: 10.1007/s00284-013-0384-8
   PubMed Web of Science ®Google Scholar
• Fitzgerald, J., Leonard, P., Darcy, E., Danaher, M., & O'Kennedy, R. (2011) Light-chain shuffling from an antigen-biased phage pool allows 185-fold improvement of an anti-halofuginone single-chain variable fragment. Analytical Biochemistry, 410, 27–33. doi: 10.1016/j.ab.2010.11.009
   PubMed Web of Science ®Google Scholar
• Fraser, M. E., Fujinaga, M., Cherney, M. M., Melton-Celsa, A. R., Twiddy, E. M., O'Brien, A. D., & James, M. N. (2004) Structure of Shiga toxin type 2 (Stx2) from Escherichia coli O157:H7. Journal of Biological Chemistry, 279, 27511–27517. doi: 10.1074/jbc.M401939200
   PubMed Web of Science ®Google Scholar
• Garber, E. A. E., & O'Brien, T. W. (2008) Detection of ricin in food using electrochemiluminescence-based technology. Journal of AOAC International, 91, 376–382.
   PubMed Web of Science ®Google Scholar
• Hale, M. L. (2001) Microtiter-based assay for evaluating the biological activity of ribosome-inactivating proteins. Pharmacology Toxicology, 88, 255–260. doi: 10.1111/j.1600-0773.2001.880506.x
   PubMedGoogle Scholar
• Harlow E, Lane D. (1999) Using antibodies: A laboratory manual. Cold Spring Harbor, NY: Cold Spring Harbor Lab. Press.
   Google Scholar
• He, X. (2014) Current technologies for detection of ricin in different matrices. In J. Cherwonogrodzky (Ed.), Ricin toxin (pp. 38–56). Beijing: Bentham Science.
   Google Scholar
• He, X., McMahon, S., McKeon, T. A., & Brandon, D. L. (2010) Development of a novel immuno-PCR assay for detection of ricin in ground beef, liquid chicken egg and milk. Journal of Food Protection, 73, 695–700.
   PubMed Web of Science ®Google Scholar
• He, X., McMahon, S. A., Skinner, C. B., Merrill, P. A., Scotcher, M. C., & Stanker, L. H. (2013) Development and characterization of monoclonal antibodies against Shiga toxin 2 and their application for toxin detection in milk. Journal of Immunological Methods, 389, 18–28. doi: 10.1016/j.jim.2012.12.005
   PubMed Web of Science ®Google Scholar
• He, X., Patfield, S., Hnasko, R., Rasooly, R., & Mandrell, R. E. (2013) A polyclonal antibody based immunoassay detects seven subtypes of Shiga toxin 2 produced by Escherichia coli in human and environmental samples. PLoS One, 8, e76368. doi:10.1371/journal.pone.0076368.
   Web of Science ®Google Scholar
• He, X., Qi, W., Quinones, B., McMahon, S., Cooley, M., & Mandrell, R. E. (2011) Sensitive detection of Shiga toxin 2 and some of its variants in environmental samples by a novel immuno-PCR assay. Applied and Environmental Microbiology, 77, 3558–3564. doi: 10.1128/AEM.02205-10
   PubMed Web of Science ®Google Scholar
• He, X., Quiñones, B., Carter, J. M., & Mandrell, R. E. (2009) Validation of a cell-free translation assay for detecting Shiga toxin 2 in bacterial culture. Journal of Agricultural & Food Chemistry, 57, 5084–5088. doi: 10.1021/jf9002285
   PubMed Web of Science ®Google Scholar
• Jackson, M. P., Neill, R. J., O'Brien, A. D., Holmes, R. K., & Newland, J. W. (1987) Nucleotide sequence analysis and comparison of the structural genes for Shiga-like toxin I and Shiga-like toxin II encoded by bacteriophages from Escherichia coli 933. FEMS Microbiology Letters, 44, 109–114. doi: 10.1111/j.1574-6968.1987.tb02252.x
   Web of Science ®Google Scholar
• Jin, W., Yamada, K., Ikami, M., Kaji, N., Tokeshi, M., Atsumi, … Ohta, M. (2013) Application of IgY to sandwich enzyme-linked immunosorbent assays, lateral flow devices, and immunopillar chips for detecting staphylococcal enterotoxins in milk and dairy products. Journal of Microbiological Methods, 92, 323–331. doi: 10.1016/j.mimet.2013.01.001
   PubMed Web of Science ®Google Scholar
• Keithlin, J., Sargeant, J., Thomas, M. K., & Fazil, A. (2014) Chronic sequelae of E. coli O157: Systematic review and meta-analysis of the proportion of E. coli O157 cases that develop chronic sequelae. Foodborne Pathogens and Disease, 11, 79–95. doi: 10.1089/fpd.2013.1572
   PubMed Web of Science ®Google Scholar
• Losch, U., Schranner, I., Wanke, R., & Jurgens, L. (1986). Kapnographie – eine Methode zur Beurteilung der Ventilationslage während der Allgemeinanästhesie beim Pferd. Journal of Veterinary Medicine Series A, 33, 609–616. doi: 10.1111/j.1439-0450.1986.tb00076.x
   Google Scholar
• Machaiah, M. I., & Krishnan, M. H. (2014) Immunodetection of Bacillus cereus haemolytic enterotoxin (HBL) in food samples. Analytical Methods, 6, 1841–1847. doi: 10.1039/c3ay41737a
   Web of Science ®Google Scholar
• McKeon, T. A., Auld, D., Brandon, D. L., Leviatov, S., & He, X. (2014) Toxin content of commercial castor cultivars. Journal of the American Oil Chemists' Society, 91, 1515–1519. doi: 10.1007/s11746-014-2505-3
   Web of Science ®Google Scholar
• Mi, T., Wang, Z., Eremin, S. A., Shen, J., & Zhang, S. (2013) Simultaneous determination of multiple (fluoro)quinolone antibiotics in food samples by a one-step fluorescence polarization immunoassay. Journal of Agricultural and Food Chemistry, 61, 9347–9355. doi: 10.1021/jf403972r
   PubMed Web of Science ®Google Scholar
• Nakao, H., Kataoka, C., Kiyokawa, N., Fujimoto, J., Yamasaki, S., & Takeda, T. (1999) Monoclonal antibody to Shiga toxin 2 which blocks receptor binding and neutralizes cytotoxicity. Infection and Immunity, 67, 5717–5722.
   Google Scholar
• Neri, P., Tokoro, S., Kobayashi, R., Sugiyama, T., Umeda, K., Shimizu, T., … Mori, H. (2011) Specific egg yolk immunoglobulin as a new preventive approach for shiga-toxin-mediated diseases. PLoS One, 6, e26526. doi:10.1371/journal.pone.0026526.
   PubMed Web of Science ®Google Scholar
• O'Brien, A. D., LaVeck, G. D., Griffin, D. E., & Thompson, M. R. (1980) Characterization of Shigella dysenteriae 1 (Shiga) toxin purified by anti-Shiga toxin affinity chromatography. Infection and Immunity, 30, 170–179.
   PubMed Web of Science ®Google Scholar
• Parma, Y. R., Chacana, P. A., Rogé, A., Kahl, A., Cangelosi, A., Geoghegan, P., … Fernandez-Miyakawa, M. E. (2011) Antibodies anti-Shiga toxin 2 B subunit from chicken egg yolk: Isolation, purification and neutralization efficacy. Toxicon, 58, 380–388. doi: 10.1016/j.toxicon.2011.07.009
   PubMed Web of Science ®Google Scholar
• Paton, A. W., Bourne, A. J., Manning, P. A., & Paton, J. C. (1995) Comparative toxicity and virulence of Escherichia coli clones expressing variant and chimeric Shiga-like toxin type II operons. Infection and Immunity, 63, 2450–2458.
   Google Scholar
• Pauly, D., Chacana, P. A., Calzado, E. G., Brembs, B., & Schade, R. (2011) IgY technology: Extraction of chicken antibodies from egg yolk by polyethylene glycol (PEG) precipitation. Journal of Visualized Experiments. doi:10.3791/3084.
   PubMed Web of Science ®Google Scholar
• Pauly, D., Dorner, M., Zhang, X., Hlinak, A., Dorner, B., & Schade, R. (2009) Monitoring of laying capacity, immunoglobulin Y concentration, and antibody titer development in chickens immunized with ricin and botulinum toxins over a two-year period. Poultry Science, 88, 281–290. doi: 10.3382/ps.2008-00323
   PubMed Web of Science ®Google Scholar
• Poli, M. A., Rivera, V. R., Hewetson, J. F., & Merrill, G. A. (1994) Detection of ricin by colorimetric and chemiluminescence ELISA. Toxicon, 32, 1371–1377. doi: 10.1016/0041-0101(94)90409-X
   PubMed Web of Science ®Google Scholar
• Polson, A., von Wechmar, M. B., & Fazakerley, G. (1980) Antibodies to proteins from yolk of immunized hens. Immunology Communications, 9, 495–514. doi: 10.3109/08820138009066011
   PubMed Web of Science ®Google Scholar
• Rasooly, R., & He, X. (2012) Sensitive bioassay for detection of biologically active ricin in food. Journal of Food Protection, 75, 951–954. doi: 10.4315/0362-028X.JFP-11-448
   PubMed Web of Science ®Google Scholar
• Severino, L. S., Auld, D. L., Baldanzi, M., Candido, M. J. D., Chen, G., Crosby, W., … Zieler, H. (2012) A review on the challenges for increased production of castor. Journal of Visualized Experiments, 104, 853–880.
   Google Scholar
• Shimizu, M., Nagashima, H., Hashimoto, K. & Suzuki, T. (1994) Egg yolk antibody (Ig Y) stability in aqueous solution with high sugar concentrations. Journal of Food Science, 59, 763–765.
   Google Scholar
• Shimizu, M., Nakai, S., & Fitzsimmons, R. C. (1988) Anti-E. coli immunoglobulin Y isolated from egg yolk of immunized chickens as a potential food ingredient. Journal of Food Science, 53, 1360–1368. doi: 10.1111/j.1365-2621.1988.tb09277.x
   Web of Science ®Google Scholar
• Skinner, C., Patfield, S., Stanker, L. H., Fratamico, P., & He, X. (2014) New high-affinity monoclonal antibodies against Shiga toxin 1 facilitate the detection of hybrid Stx1/Stx2 in vivo. PLoS One, 9, e9985. doi:10.1371/journal.pone.0099854.
   Google Scholar
• Smith, J. L., Fratamico, P. M., & Gunther, N. W. (2014) Shiga toxin-producing Escherichia coli. Advances in Applied Microbiology, 86, 145–197. doi: 10.1016/B978-0-12-800262-9.00003-2
   PubMed Web of Science ®Google Scholar
• Stirpe, F. (2004) Ribosome-inactivating proteins. Toxicon, 44, 371–383. doi: 10.1016/j.toxicon.2004.05.004
   PubMed Web of Science ®Google Scholar
• Strockbine, N. A., Marques, L. R., Holmes, R. K., & O'Brien, A. D. (1985) Characterization of monoclonal antibodies against Shiga-like toxin from Escherichia coli. Infection and Immunity, 50, 695–700.
   PubMed Web of Science ®Google Scholar
• Tonegawa, S. (1983) Somatic generation of antibody diversity. Nature, 302, 575–581. doi: 10.1038/302575a0
   PubMed Web of Science ®Google Scholar
• Vinayaka, A. C., Muthukumar, S. P., & Thakur, M. S. (2013) Avian antibodies for staphylococcal enterotoxin B as an efficient tool for FRET-based fluoroimmunosensor. BioNanoScience, 3, 232–240. doi: 10.1007/s12668-013-0101-x
   Google Scholar
• Warr, G. W., Magor, K. E., & Higgins, D. A. (1995) IgY: Clues to the origins of modern antibodies. Immunology Today, p. 16, 392–398.
   Google Scholar