Alternative to Animal Use for Detecting Biologically Active Staphylococcal Enterotoxin Type A
Abstract
:1. Introduction
2. Results
2.1. IL-2 Secretion Assay for Measuring Biologically Active SEA in Food
2.2. Quantitative In Vitro T-cell-Based Assay for Quantifing Biologically Active SEA
2.3. Distinguishing Active from Inactive SEA
2.4. Cross-Reactivity Assay Specificity and Function of CCRF-CEM Cells Elicited by SEA
2.5. Detection of SEA in Whole Milk
3. Discussion
4. Materials and Methods
4.1. Media and Reagents
4.2. Cells and Cell Lines
4.3. Methods of Preparation of Foods for Analysis
4.4. SEA Magnetic Beads Preparation
4.5. Sample Binding and Disassociation of SEA from Beads
4.6. Quantitative Determinations of Active SEA by IL-2 Protein Secretion
4.7. Statistical Analysis
4.8. Ethics Statement
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Scallan, E.; Hoekstra, R.M.; Angulo, F.J.; Tauxe, R.V.; Widdowson, M.A.; Roy, S.L.; Jones, J.L.; Griffin, P.M. Foodborne illness acquired in the United States—Major pathogens. Emerg. Infect. Dis. 2011, 17, 7–15. [Google Scholar] [CrossRef] [PubMed]
- Harris, T.O.; Grossman, D.; Kappler, J.W.; Marrack, P.; Rich, R.R.; Betley, M.J. Lack of complete correlation between emetic and T-cell-stimulatory activities of staphylococcal enterotoxins. Infect. Immun. 1993, 61, 3175–3183. [Google Scholar] [PubMed]
- Hu, D.L.; Omoe, K.; Sashinami, H.; Shinagawa, K.; Nakane, A. Immunization with a nontoxic mutant of staphylococcal enterotoxin A, SEAD227A, protects against enterotoxin-induced emesis in house musk shrews. J. Infect. Dis. 2009, 199, 302–310. [Google Scholar] [CrossRef] [PubMed]
- Hui, J.; Cao, Y.; Xiao, F.; Zhang, J.; Li, H. Staphylococcus aureus enterotoxin C2 mutants: Biological activity assay in vitro. J. Ind. Microbiol. Biotechnol. 2008, 35, 975–980. [Google Scholar] [CrossRef] [PubMed]
- Asao, T.; Kumeda, Y.; Kawai, T.; Shibata, T.; Oda, H.; Haruki, K.; Nakazawa, H.; Kozaki, S. An extensive outbreak of staphylococcal food poisoning due to low-fat milk in Japan: Estimation of enterotoxin A in the incriminated milk and powdered skim milk. Epidemiol. Infect. 2003, 130, 33–40. [Google Scholar] [CrossRef] [PubMed]
- Ikeda, T.; Tamate, N.; Yamaguchi, K.; Makino, S. Mass outbreak of food poisoning disease caused by small amounts of staphylococcal enterotoxins A and H. Appl. Environ. Microbiol. 2005, 71, 2793–2795. [Google Scholar] [CrossRef] [PubMed]
- Wieneke, A.A.; Roberts, D.; Gilbert, R.J. Staphylococcal food poisoning in the United Kingdom, 1969–1990. Epidemiol. Infect. 1993, 110, 519–531. [Google Scholar] [CrossRef]
- Casman, E.P.; Bennett, R.W. Detection of Staphylococcal Enterotoxin in Food. Appl. Microbiol. 1965, 13, 181–189. [Google Scholar]
- Bergdoll, M.S. Monkey feeding test for staphylococcal enterotoxin. Methods Enzymol. 1988, 165, 324–333. [Google Scholar]
- Bennett, R.W. Staphylococcal enterotoxin and its rapid identification in foods by enzyme-linked immunosorbent assay-based methodology. J. Food Prot. 2005, 68, 1264–1270. [Google Scholar] [CrossRef]
- Dupuis, A.; Hennekinne, J.A.; Garin, J.; Brun, V. Protein Standard Absolute Quantification (PSAQ) for improved investigation of staphylococcal food poisoning outbreaks. Proteomics 2008, 8, 4633–4636. [Google Scholar] [CrossRef]
- Fujikawa, H.; Igarashi, H. Rapid latex agglutination test for detection of staphylococcal enterotoxins A to E that uses high-density latex particles. Appl. Environ. Microbiol. 1988, 54, 2345–2348. [Google Scholar] [PubMed]
- Park, C.E.; Akhtar, M.; Rayman, M.K. Nonspecific reactions of a commercial enzyme-linked immunosorbent assay kit (TECRA) for detection of staphylococcal enterotoxins in foods. Appl. Environ. Microbiol. 1992, 58, 2509–2512. [Google Scholar]
- Rasooly, R.; Do, P.; Hernlem, B. Sensitive, Rapid, Quantitative and in Vitro Method for the Detection of Biologically Active Staphylococcal Enterotoxin Type E. Toxins 2016, 8, 150. [Google Scholar] [CrossRef]
- Rasooly, R.; Do, P.; Hernlem, B. Low cost bioluminescence imaging as an alternative to in vivo bioassays for quantifying biologically active staphylococcal enterotoxin type E. Sens. Actuators B Chem. 2018, 259, 387–393. [Google Scholar] [CrossRef]
- Rasooly, R.; Do, P.; Hernlem, B.J. Interleukin 2 Secretion by T Cells for Detection of Biologically Active Staphylococcal Enterotoxin Type E. J. Food Prot. 2017, 80, 1857–1862. [Google Scholar] [CrossRef] [PubMed]
- Rasooly, R.; Hernlem, B. TNF as Biomarker for Rapid Quantification of Active Staphylococcus Enterotoxin A in Food. Sensors 2012, 12, 5978–5985. [Google Scholar] [CrossRef] [Green Version]
- Pinchuk, I.V.; Beswick, E.J.; Reyes, V.E. Staphylococcal Enterotoxins. Toxins 2010, 2, 2177–2197. [Google Scholar] [CrossRef] [Green Version]
- Bayles, K.W.; Iandolo, J.J. Genetic and molecular analyses of the gene encoding staphylococcal enterotoxin D. J. Bacteriol. 1989, 171, 4799–4806. [Google Scholar] [CrossRef]
- Iandolo, J.J. Genetic analysis of extracellular toxins of Staphylococcus aureus. Annu. Rev. Microbiol. 1989, 43, 375–402. [Google Scholar] [CrossRef]
- Bergdoll, M.S.; Borja, C.R.; Robbins, R.N.; Weiss, K.F. Identification of enterotoxin E. Infect. Immun. 1971, 4, 593–595. [Google Scholar] [PubMed]
- Hu, J.Y.; Lin, L.; Chen, M.; Yan, W.L. Modeling for Predicting the Time to Detection of Staphylococcal Enterotoxin A in Cooked Chicken Product. Front. Microbiol. 2018, 9, 1536. [Google Scholar] [CrossRef] [PubMed]
- Rajkovic, A.; Tomasevic, I.; De Meulenaer, B.; Devlieghere, F. The effect of pulsed UV light on Escherichia coli O157:H7, Listeria monocytogenes, Salmonella Typhimurium, Staphylococcus aureus and staphylococcal enterotoxin A on sliced fermented salami and its chemical quality. Food Control 2017, 73, 829–837. [Google Scholar] [CrossRef]
- Bavari, S.; Hunt, R.E.; Ulrich, R.G. Divergence of human and nonhuman primate lymphocyte responses to bacterial superantigens. Clin. Immunol. Immunopathol. 1995, 76, 248–254. [Google Scholar] [CrossRef] [PubMed]
- Hufnagle, W.O.; Tremaine, M.T.; Betley, M.J. The carboxylterminal region of staphylococcal enterotoxin type A is required for a fully active molecule. Infect. Immun. 1991, 59, 2126–2134. [Google Scholar] [PubMed]
- Langley, R.J.; Fraser, J.D.; Proft, T. Bacterial superantigens and superantigen-like toxins. In The Comprehensive Sourcebook of Bacterial Protein Toxins, 4th ed.; Academic Press: Boston, MA, USA, 2015; pp. 911–974. [Google Scholar]
- Rajkovic, A.; El Moualij, B.; Uyttendaele, M.; Brolet, P.; Zorzi, W.; Heinen, E.; Foubert, E.; Debevere, J. Immunoquantitative real-time PCR for detection and quantification of Staphylococcus aureus enterotoxin B in foods. Appl. Environ. Microbiol. 2006, 72, 6593–6599. [Google Scholar] [CrossRef] [PubMed]
- Gill, D.M. Bacterial toxins: A table of lethal amounts. Microbiol. Rev. 1982, 46, 86–94. [Google Scholar]
- Evenson, M.L.; Hinds, M.W.; Bernstein, R.S.; Bergdoll, M.S. Estimation of human dose of staphylococcal enterotoxin A from a large outbreak of staphylococcal food poisoning involving chocolate milk. Int. J. Food Microbiol. 1988, 7, 311–316. [Google Scholar] [CrossRef]
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Rasooly, R.; Do, P.; He, X.; Hernlem, B. Alternative to Animal Use for Detecting Biologically Active Staphylococcal Enterotoxin Type A. Toxins 2018, 10, 540. https://doi.org/10.3390/toxins10120540
Rasooly R, Do P, He X, Hernlem B. Alternative to Animal Use for Detecting Biologically Active Staphylococcal Enterotoxin Type A. Toxins. 2018; 10(12):540. https://doi.org/10.3390/toxins10120540
Chicago/Turabian StyleRasooly, Reuven, Paula Do, Xiaohua He, and Bradley Hernlem. 2018. "Alternative to Animal Use for Detecting Biologically Active Staphylococcal Enterotoxin Type A" Toxins 10, no. 12: 540. https://doi.org/10.3390/toxins10120540