Transport of aflatoxin M1 in human intestinal Caco-2/TC7 cells

Frontiers in Pharmacology

Volumn 3 JUN, Issue , 2012, Pages

  Caloni, Francesca ^a   Cortinovis, Cristina ^a   Pizzo, Fabiola ^a   De Angelis, Isabella ^b  

^a UNIVERSITY OF MILAN   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

Aflatoxin M1; Caco 2 TC7 cells; Intestinal barrier; Tight junctions; Transport

Indexed keywords

AFLATOXIN M1; GLUCURONOSYLTRANSFERASE; OCCLUDIN; PROTEIN ZO1; SUCRASE ISOMALTASE;

ANTIBODY AFFINITY; ARTICLE; CELL DIFFERENTIATION; CHEMICAL ANALYSIS; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EXPOSURE; DRUG TRANSPORT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; INTESTINE ABSORPTION; INTESTINE MUCOSA; PROTEIN LOCALIZATION; TIGHT JUNCTION;

EID: 84866160129     PISSN: None     EISSN: 16639812     Source Type: Journal    
DOI: 10.3389/fphar.2012.00111     Document Type: Article

References (61)

1. Abreu, M. T., Palladino, A. A., Arnold, E. T., Kwon, R. S., and McRoberts, J. A. (2000). Modulation of barrier function during Fasmediated apoptosis in human intestinal epithelial cells. Gastroenterology 119, 1524-1536.
2. Applebaum, R. S., Brackett, R. E., Wiseman, D. W., and Mart, E. H. (1982). Aflatoxin: toxicity to dairy cattle and occurrence in milk and milk products-a review. J. Food Prot. 45, 752-777.
3. Bailey, G. S., Price, R. L., Park, D. L., and Hendricks, J. D. (1994). Effect of ammoniation of aflatoxin B1-contaminated cottonseed feedstock on the aflatoxin M1 content of cows' milk and hepatocarcinogenicity in the trout bioassay. Food Chem. Toxicol. 32, 707-715.
4. Boudra, H., Barnouin, J., Dragacci, S., and Morgavi, D. P. (2007). Aflatoxin M1 and ochratoxin A in raw bulk milk from French dairy herds. J. Dairy Sci. 90, 3197-3201.
5. 1 selectively down-regulates the basal IL-8 expression in pig intestine: in vivo and in vitro studies. Food Chem. Toxicol. 44, 1768-1773.
6. 1 absorption and cytotoxicity on human intestinal in vitro model. Toxicon 47, 409-415.
7. Chantret, I., Rodolosse, A., Barbat, A., Dussaulx, E., Brot-Laroche, E., Zweibaum, A., and Rousset, M. (1994). Differential expression of sucraseisomaltase in clones isolated from early and late passages of the cell line Caco-2: evidence for glucose-dependent negative regulation. J. Cell Sci. 107,213-225.
8. Chin, A. C., Teoh, D. A., Scott, K. G., Meddings, J. B., Macnaughton, W. K., and Buret, A. G. (2002). Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect. Immun. 70, 3673-3680.
9. Coffey, R., Cummins, E., and Ward, S. (2009). Exposure assessment of mycotoxins in dairy milk. Food Control 20,239-249.
10. Commission of the European Communities (CEC). (2004). EC Regulation 683/2004. 13.04.2004. Bruxelles: Official Journal of the EC. L106/3.
11. Commission of the European Communities (CEC). (2006). EC Regulation 1881/2006. 19.12.2006. Bruxelles: Official Journal of the EC L364/5-24.
12. Commission of the European Communities (CEC). (2010). ECRegulation 165/2010. 26.02.2010. Bruxelles: Official Journal of the EC L50/8-12.
13. Creppy, E. E. (2002). Update of survey, regulation and toxic effects of mycotoxins in Europe. Toxicol. Lett. 127, 19-28.
14. De Angelis, I., Friggè, G., Raimondi, F., Stammati, A., Zucco, F., and Caloni, F. (2005). Absorption of Fumonisin B1 and aminopentol on a in vitro model of intestinal epithelium; the role of Pglycoprotein. Toxicon 45, 285-291.
15. FDA. (2005). Sec. 527.400 Whole Milk, Low Fat Milk, Skim Milk-Aflatoxin M1 (CPG71 06. 10).Washington,DC: FDA Compliance Policy Guides, 219.
16. Fukata, T., Sasai, K., Baba, E., and Arakawa, A. (1996). Effect of ochratoxin A on Salmonella typhimurium-challenged layer chickens. Avian Dis. 40, 924-926.
17. Gitter, A. H., Bendfeldt, K., Schulzke, J. D., and Fromm, M. (2000). Leaks in the epithelial barrier caused by spontaneous and TNF-alpha-induced single-cell apoptosis. FASEB J. 14, 1749-1753.
18. Gratz, S., Wu, Q. K., El-Nezami, H., Juvonen, R. O., Mykkänen, H., and Turner, P. C. (2007). Lactobacillus rhamnosus strain GG reduces aflatoxin B1 transport, metabolism, and toxicity in Caco-2 cells. Appl. Environ. Microbiol. 73, 3958-3964.
19. 2. Tetrahedron Lett. 25, 2799-2803.
20. Hussein, S. H., and Brasel, J. M. (2001). Toxicity, metabolism and impact of mycotoxins on humans and animals. Toxicology 167, 101-134.
21. International Agency for Research on Cancer (IARC). (1993). "Some naturally occurring substances: food items and constituents, heterocyclic aromatic amines and mycotoxins," in IARC Monographs on the Evaluation of Carcinogenic Risk to Humans, Vol. 56, (Lyon: IARC Scientific publications), 245-395.
22. Joint FAO/WHO Expert Committee on Food Additives (JECFA). (2001). "Safety evaluation of certain mycotoxins in food," in 56th Meeting of the JECFA-FAO Food and Nutrition Paper 74/WHO Foods Additives Series 47, Geneva.
23. Kuiper-Goodman, T. (1990). Uncertainties in the risk assessment of three mycotoxins: aflatoxin, ochratoxin and zearalenone. Can. J. Physiol. Pharmacol. 68,1017-1024.
24. Lambert, D., Padfield, P. J., McLaughlin, J., Cannell, S., and O'Neill, C. A. (2007). Ochratoxin A displaces claudins from detergent resistant membrane microdomains. Biochem. Biophys. Res. Commun. 358, 632-636.
25. Li, M., Cuff, C. F., and Pestka, J. J. (2005). Modulation of murine host response to enteric reovirus infection by the trichothecene deoxynivalenol. Toxicol. Sci. 87, 134-145.
26. Li, M., Cuff, C. F., and Pestka, J. J. (2006). T-2 toxin impairment of enteric reovirus clearance in the mouse associated with suppressed immunoglobulin and IFN-gamma responses. Toxicol. Appl. Pharmacol. 214,318-325.
27. Madara, J. L. (1998). Regulation of the movement of solutes across tight junctions. Annu. Rev. Physiol. 60, 143-159.
28. Maresca, M., and Fantini, J. (2010). Some food-associated mycotoxins as a potential risk factors in human predisposed to chronic intestinal inflammatory diseases. Toxicon 56, 282-294.
29. Maresca, M., Yahi, N., Younès-Sakr, L., Boyron, M., Caporiccio, B., and Fantini, J. (2008). Both direct and indirect effects account for the proinflammatory activity of enteropathogenic mycotoxins on the human intestinal epithelium: stimulation of interleukin-8 secretion, potentiation of interleukin1beta effect and increase in the transepithelial passage of commensal bacteria. Toxicol. Appl. Pharmacol. 228, 84-92.
30. McLaughlin, J., Lambert, D., Padfield, P. J., Burt, J. P., and O'Neill, C. A. (2009). The mycotoxin patulin, modulates tight junctions in caco-2 cells. Toxicol. In vitro 23, 83-89.
31. McLaughlin, J., Padfield, P. J., Burt, J. P., and O'Neill, C. A. (2004). Ochratoxin A increases permeability through tight junctions by removal of specific claudin isoforms. Am. J. Physiol. Cell Physiol. 287, C1412-C1417.
32. 1 in human-derived in vitro system. Toxicol. Appl. Pharmacol. 151, 152-158.
33. Obremski, K., Zielonka, L., Gajecka, M., Jakimiuk, E., Bakula, T., Baranowski, M., and Gajecki, M. (2008). Histological estimation of the small intestine wall after administration of feed containing deoxynivalenol, T-2 toxin and zearalenone in the pig. Pol. J. Vet. Sci. 11,339-345.
34. Oswald, I. P., Desautels, C., Laffitte, J., Fournout, S., Peres, S. Y., Odin, M., Le Bars, P., Le Bars, J., and Fairbrother, J. M. (2003). Mycotoxin fumonisin B1 increases intestinal colonization by pathogenic Escherichia coli in pigs. Appl. Environ. Microbiol. 69, 5870-5874.
35. Pietri, A., Bertuzzi, T., Bertuzzi, P., and Piva, G. (1997). Aflatoxin M1 occurrence in samples of Grana Padano cheese. Food Addit. Contam. 14, 341-344.
36. Pinton, P., Nougayrède, J. P., Del Rio, J. C., Moreno, C., Marin, D. E., Ferrier, L., Bracarense, A. P., KolfClauw, M., and Oswald, I. P. (2009). The food contaminant deoxynivalenol, decreases intestinal barrier permeability and reduces Claudin expression. Toxicol. Appl. Pharmacol. 237, 41-48.
37. 1 in rat liver. J. Natl. Cancer Inst. 47, 585-590.
38. Prandini, A., Tansini, G., Sigolo, S., Filippi, L., Laporta, M., and Piva, G. (2009). On the occurrence of aflatoxinM1 inmilkanddairyproducts. Food Chem. Toxicol. 47, 984-991.
39. Prieto, P., Hoffmann, S., Tirelli, V., Tancredi, F., González, I., Bermelo, M., and De Angelis, I. (2010). An exploratory study of two Caco-2 cell models for oral absorption: a report on their within-laboratory and between-laboratory variability, and their predictive capacity. Altern. Lab. Anim. 38, 367-386.
40. 1 in raw milk of five dairy species in Ahvaz, Iran. Food Chem. Toxicol. 48,129-131.
41. 1 on haematopoietic progenitors (BFU-E, CFU-E, and CFU-GM): species-related susceptibility. Toxicol. In vitro 24,217-223.
42. Sambuy, Y. (2009). "Cellular tight junctions as mediators of adverse effects," in General and Applied Toxicology, eds B. Ballantyne, T. Marrs, and T. Syversen (London: Wiley), 1-21.
43. 1 in raw milk in the North of Paraná state. Food Chem. Toxicol. 43, 981-984.
44. Schneeberger, E. E., and Lynch, R. D. (2004). The tight junction: a multifunctional complex. Am. J. Physiol. Cell Physiol. 286, C1213-C1228.
45. 1 in cheese. J. Chromatogr. 474,457-461.
46. 1 in somatic cells in vivo of Drosophila melanogaster. Mutagenesis 10, 161-164.
47. 1 a potent carcinogen for rainbowtrout. Fed. Proc. 29, 568-579.
48. Sun, H., Chow, E. C., Liu, S., Du, Y., and Pang, K. S. (2008). The Caco-2 cell monolayer: usefulness and limitations. Expert Opin. Drug Metab. Toxicol. 4,395-411.
49. Sun, Z., Wang, X., Wallen, R., Deng, X., Du, X., Hallberg, E., and Andersson, R. (1998). The influence of apoptosis on intestinal barrier integrity in rats. Scand. J. Gastroenterol. 33, 415-422.
50. Tenk, I., Fodor, E., and Szathmáry, C. (1982). The effect of pure Fusarium toxins (T-2, F-2, DAS) on the microflora of the gut and on plasma glucocorticoid levels in rat and swine. Zentralbl. Bakteriol. Mikrobiol. Hyg. A 252, 384-393.
51. Turco, L., Catone, T., Caloni, F., Consiglio, E. D., Testai, E., and Stammati, A. (2011). Caco-2/TC7 cell line characterization for intestinal absorption: how reliable is this in vitro model for the prediction of the oral dose fraction absorbed in human? Toxicol. In vitro 25, 13-20.
52. Turconi, G., Guarcello, M., Livieri, C., Comizzoli, S., Maccarini, L., Castellazzi, A. M., Pietri, A., Piva, G., and Roggi, C. (2004). Evaluation of xenobiotics in human milk and ingestion by the newbornan epidemiological survey in Lombardy (Northern Italy). Eur. J. Nutr. 43, 191-197.
53. 1 in UHT milk in Turkey. Food Chem. Toxicol. 44, 1897-1900.
54. Van De Walle, J., Sergent, T., Piront, N., Toussaint, O., Schneider, Y. J., and Larondelle, Y. (2010). Deoxynivalenol affects in vitro intestinal epithelial cell barrier integrity through inhibition of protein synthesis. Toxicol. Appl. Pharmacol. 245, 291-298.
55. Van Egmond, H. P. (1989). Mycotoxins in Dairy Products. London: Elsevier.
56. Videmann, B., Mazallon, M., Tep, J., and Lecoeur, S. (2008). Metabolism and transfer of the mycotoxin zearalenone in human intestinal Caco-2 cells. Food Chem. Toxicol. 46, 3279-3286.
57. Vismara, C., Di Muzio, A., Tarca, S., Lucchino, M., Foti, I., and Caloni, E (2006). Aflatoxin M1 effects on Xenopus laevis development. Birth Defects Res. B Dev. Reprod. Toxicol. 77,234-237.
58. Waché, Y. J., Valat, C., Postollec, G., Bougeard, S., Burel, C., Oswald, I. P., and Fravalo, P. (2009). Impact of deoxynivalenol on the intestinal microflora of pigs. Int. J. Mol. Sci. 10,1-17.
59. 1," in Mycotoxins and Phytoalexins, eds R. P. Sharma and D. K. Salunkhe (Boca Raton, FL: CRC Press), 145-164.
60. Zhang, L., Balimane, P. V., Johnson, S. R., and Chong, S. (2007). Development of an in silico model for predicting efflux substrates in Caco-2 cells. Int. J. Pharm. 343, 98-105.
61. Zucco, F., Batto, A. F., Bises, G., Chambaz, J., Chiusolo, A., Consalvo, R., Cross, H., Dal Negro, G., De Angelis, I., Fabre, G., Guillou, F., Hoffman, S., Laplanche, L., Morel, E., Pinçon-Raymond, M., Prieto, P., Turco, L., Ranaldi, G., Rousset, M., Sambuy, Y., Scarino, M. L., Torreilles, F., and Stammati, A. (2005). An inter-laboratory study to evaluate the effects of medium composition on the differentiation and barrier function of Caco-2 cell lines. Altern. Lab. Anim. 33, 603-618.