Accumulation and Transport of Roxarsone, Arsenobetaine, and Inorganic Arsenic Using the Human Immortalized Caco-2 Cell Line

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 46, 2016, Pages 8902-8908

  Liu, Qingqing ^a   Leslie, Elaine M ^a   Le, X Chris ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

arsenic; arsenobetaine; bioavailability; Caco 2; cellular uptake; organoarsenic; phenylarsenicals; Roxarsone; transepithelial passage; transport

Indexed keywords

ANIMALS; ARSENIC; ARSENIC COMPOUNDS; BIOCHEMISTRY; CELL CULTURE; CYTOLOGY;

ARSENOBETAINE; BIOAVAILABILITY; CACO-2; CELLULAR UPTAKE; ORGANOARSENIC; PHENYLARSENICALS; ROXARSONE; TRANSEPITHELIAL PASSAGE; TRANSPORT;

CELLS;

ARSENOBETAINE; ORGANOARSENIC DERIVATIVE; ROXARSONE;

ANALYSIS; ANIMAL; CACO-2 CELL LINE; CHEMISTRY; CHICKEN; FOOD CONTAMINATION; HUMAN; IMMOBILIZED CELL; KINETICS; MEAT; METABOLISM; PRODUCT SAFETY; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; ARSENICALS; BIOLOGICAL TRANSPORT; CACO-2 CELLS; CELLS, IMMOBILIZED; CHICKENS; CONSUMER PRODUCT SAFETY; FOOD CONTAMINATION; HUMANS; KINETICS; MEAT; ROXARSONE;

EID: 84997785000     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b03341     Document Type: Article

References (38)

1. Nachman, K. E.; Baron, P. A.; Raber, G.; Francesconi, K. A.; Navas-Acien, A.; Love, D. C. Roxarsone, inorganic arsenic, and other arsenic species in chicken: a U.S.-based market basket sample Environ. Health Perspect. 2013, 121, 818-824 10.1289/ehp.1206245
2. Jones, F. T. A broad view of arsenic Poult. Sci. 2007, 86, 2-14 10.1093/ps/86.1.2
3. Liu, Q.; Peng, H.; Lu, X.; Zuidhof, M. J.; Li, X.-F.; Le, X. C. Arsenic species in chicken breast: Temporal variations of metabolites, elimination kinetics, and residual concentrations Environ. Health Perspect. 2016, 124, 1174-1181 10.1289/ehp.1510530
4. Peng, H.; Hu, B.; Liu, Q.; Yang, Z.; Lu, X.; Huang, R.; Li, X.-F.; Zuidhof, M. J.; Le, X. C. Liquid chromatography combined with atomic and molecular mass spectrometry for speciation of arsenic in chicken liver J. Chromatogr. A 2014, 1370, 40-49 10.1016/j.chroma.2014.10.012
5. Liu, Q.; Peng, H.; Lu, X.; Le, X. C. Enzyme-assisted extraction and liquid chromatography mass spectrometry for the determination of arsenic species in chicken meat Anal. Chim. Acta 2015, 888, 1-9 10.1016/j.aca.2015.05.001
6. Agriculture and Agri-Food Canada (AAFC). Canada's Poultry and Egg Industry Profile, 2016. http://www.agr.gc.ca/eng/industry-markets-and-trade/statistics-and-market-information/by-product-sector/poultry-and-eggs/poultry-and-egg-market-information-canadian-industry/industry-profile/?id=1384971854389 (accessed July 12, 2016).
7. United States Department of Agriculture, Economic Research Service (ERS). Food Availability (Per Capita) Data System, 2014. http://www.ers.usda.gov/data-products/food-availability-per-capita-data-system (accessed November 4, 2016).
8. National Research Council. Arsenic in Drinking Water, 2001 Update; National Academy Press: Washington, D.C., 2001.
9. Smith, A. H.; Steinmaus, C. M. Health effects of arsenic and chromium in drinking water: Recent human findings Annu. Rev. Public Health 2009, 30, 107-122 10.1146/annurev.publhealth.031308.100143
10. Hughes, M. F.; Beck, B. D.; Chen, Y.; Lewis, A. S.; Thomas, D. J. Arsenic exposure and toxicology: a historical perspective Toxicol. Sci. 2011, 123, 305-332 10.1093/toxsci/kfr184
11. Maull, E. A.; Ahsan, H.; Edwards, J.; Longnecker, M. P.; Navas-Acien, A.; Pi, J.; Silbergeld, E. K.; Styblo, M.; Tseng, C.-H.; Thayer, K. A. et al. Evaluation of the association between arsenic and diabetes: A national toxicology program workshop review Environ. Health Perspect. 2012, 120, 1658 10.1289/ehp.1104579
12. Naujokas, M. F.; Anderson, B.; Ahsan, H.; Aposhian, H. V.; Graziano, J. H.; Thompson, C.; Suk, W. A. The broad scope of health effects from chronic arsenic exposure: Update on a worldwide public health problem Environ. Health Perspect. 2013, 121, 295-302 10.1289/ehp.1205875
13. Yang, Z.; Peng, H.; Lu, X.; Liu, Q.; Huang, R.; Hu, B.; Kachanoski, G.; Zuidhof, M. J.; Le, X. C. Arsenic metabolites, including N-Acetyl-4-hydroxy-m-arsanilic Acid, in chicken litter from a Roxarsone-feeding study involving 1600 Chickens Environ. Sci. Technol. 2016, 50, 6737-6743 10.1021/acs.est.5b05619
14. Calatayud, M.; Barrios, J. A.; Vélez, D.; Devesa, V. In vitro study of transporters involved in intestinal absorption of inorganic arsenic Chem. Res. Toxicol. 2012, 25, 446-453 10.1021/tx200491f
15. Calatayud, M.; Vázquez, M.; Devesa, V.; Vélez, D. In vitro study of intestinal transport of inorganic and methylated arsenic species by Caco-2/HT29-MTX cocultures Chem. Res. Toxicol. 2012, 25, 2654-2662 10.1021/tx300295n
16. Calatayud, M.; Gimeno, J.; Vélez, D.; Devesa, V.; Montoro, R. Characterization of the intestinal absorption of arsenate, monomethylarsonic acid, and dimethylarsinic acid using the caco-2 cell line Chem. Res. Toxicol. 2010, 23, 547-556 10.1021/tx900279e
17. Laparra, J. M.; Vélez, D.; Barberá, R.; Montoro, R.; Farré, R. Bioaccessibility and transport by Caco-2 cells of organoarsenical species present in seafood J. Agric. Food Chem. 2007, 55, 5892-5897 10.1021/jf070490f
18. Leffers, L.; Wehe, C. A.; Hüwel, S.; Bartel, M.; Ebert, F.; Taleshi, M. S.; Galla, H.-J.; Karst, U.; Francesconi, K. A.; Schwerdtle, T. In vitro intestinal bioavailability of arsenosugar metabolites and presystemic metabolism of thio-dimethylarsinic acid in Caco-2 cells Metallomics 2013, 5, 1031 10.1039/c3mt00039g
19. Cullen, W. R.; Liu, Q.; Lu, X.; McKnight-Whitford, A.; Peng, H.; Popowich, A.; Yan, X.; Zhang, Q.; Fricke, M.; Sun, H.; Le, X. C. Methylated and thiolated arsenic species for environmental and health research: A review of synthesis and characterization. J. Environ. Sci. 2016, 49, in press.
20. Chen, B.; Lu, X.; Shen, S.; Arnold, L. L.; Cohen, S. M.; Le, X. C. Arsenic speciation in the blood of arsenite-treated F344 rats Chem. Res. Toxicol. 2013, 26, 952-962 10.1021/tx400123q
21. Hubatsch, I.; Ragnarsson, E. G. E.; Artursson, P. Determination of drug permeability and prediction of drug absorption in Caco-2 monolayers Nat. Protoc. 2007, 2, 2111-2119 10.1038/nprot.2007.303
22. Ménez, C.; Buyse, M.; Dugave, C.; Farinotti, R.; Barratt, G. Intestinal absorption of miltefosine: contribution of passive paracellular transport Pharm. Res. 2007, 24, 546-554 10.1007/s11095-006-9170-7
23. Laparra, J. M.; Vélez, D.; Barberá, R.; Montoro, R.; Farré, R. An approach to As(III) and As(V) bioavailability studies with Caco-2 cells Toxicol. In Vitro 2005, 19, 1071-1078 10.1016/j.tiv.2005.05.007
24. Calatayud, M.; Devesa, V.; Montoro, R.; Vélez, D. In vitro study of intestinal transport of arsenite, monomethylarsonous acid, and dimethylarsinous acid by Caco-2 cell line Toxicol. Lett. 2011, 204, 127-133 10.1016/j.toxlet.2011.04.023
25. Roggenbeck, B. A.; Banerjee, M.; Leslie, E. M. Cellular arsenic transport pathways in mammals. J. Environ. Sci. 2016, 49, DOI: 10.1016/j.jes.2016.10.001.
26. Mathieu, F.; Galmier, M.-J.; Pognat, J.-F.; Petit, J.; Lartigue, C. Transepithelial transport of bepridil in the human intestinal cell line, Caco-2, using two media, DMEMc and HBSS Int. J. Pharm. 1999, 181, 203-217 10.1016/S0378-5173(99)00027-7
27. Yee, S. In vitro permeability across Caco-2 cells (colonic) can predict in vivo (small intestinal) absorption in man-fact or myth Pharm. Res. 1997, 14, 763-766 10.1023/A:1012102522787
28. Edmonds, J. S.; Francesconi, K. A. Methylated arsenic from marine fauna Nature 1977, 265, 436 10.1038/265436a0
29. Crecelius, E. A. Changes in the chemical speciation of arsenic following ingestion by man Environ. Health Perspect. 1977, 19, 147-150 10.1289/ehp.7719147
30. Freeman, H. C.; Uthe, J. F.; Fleming, R. B.; Odense, P. H.; Ackman, R. G.; Landry, G.; Musial, C. J. Clearance of arsenic ingested by man from arsenic contaminated fish Bull. Environ. Contam. Toxicol. 1979, 22, 224-229 10.1007/BF02026934
31. Vahter, M.; Marafante, E.; Dencker, L. Metabolism of arsenobetame in mice, rats and rabbits Sci. Total Environ. 1983, 30, 197-211 10.1016/0048-9697(83)90012-8
32. Le, X. C.; Cullen, W. R.; Reimer, K. J. Determination of urinary arsenic and impact of dietary arsenic intake Talanta 1993, 40, 185-193 10.1016/0039-9140(93)80320-Q
33. Le, X. C.; Cullen, W. R.; Reimer, K. J. Human urinary arsenic excretion after one-time ingestion of seaweed, crab, and shrimp Clin. Chem. 1994, 40, 617-624
34. Sugano, K.; Kansy, M.; Artursson, P.; Avdeef, A.; Bendels, S.; Di, L.; Ecker, G. F.; Faller, B.; Fischer, H.; Gerebtzoff, G. et al. Coexistence of passive and carrier-mediated processes in drug transport Nat. Rev. Drug Discovery 2010, 9, 597-614 10.1038/nrd3187
35. Chávez-Capilla, T.; Maher, W.; Kelly, T.; Foster, S. Evaluation of the ability of arsenic species to traverse cell membranes by simple diffusion using octanol-water and liposome-water partition coefficients. J. Environ. Sci. 2016, 49. DOI: 10.1016/j.jes.2016.08.007.
36. Ward, P. D.; Tippin, T. K.; Thakker, D. R. Enhancing paracellular permeability by modulating epithelial tight junctions Pharm. Sci. Technol. Today 2000, 3, 346-358 10.1016/S1461-5347(00)00302-3
37. Rothen-Rutishauser, B.; Riesen, F. K.; Braun, A.; Günthert, M.; Wunderli-Allenspach, H. Dynamics of tight and adherens junctions under EGTA treatment J. Membr. Biol. 2002, 188, 151-162 10.1007/s00232-001-0182-2
38. Laparra, J. M.; Vélez, D.; Barberá, R.; Farré, R.; Montoro, R. Bioavailability of inorganic arsenic in cooked rice: practical aspects for human health risk assessments J. Agric. Food Chem. 2005, 53, 8829-8833 10.1021/jf051365b