In vitro toxicological characterization of two arsenosugars and their metabolites

Molecular Nutrition and Food Research

Volumn 57, Issue 7, 2013, Pages 1270-1282

  Leffers, Larissa ^a   Ebert, Franziska ^a   Taleshi, Mojtaba S ^b   Francesconi, Kevin A ^b   Schwerdtle, Tanja ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

^b UNIVERSITY OF GRAZ   (Austria)

Author keywords

Arsenosugars; Cellular and intestinal bioavailability; Cellular toxicity; Genotoxicity; Marine food

Indexed keywords

ARSENIC ACID DERIVATIVE; ARSENOSUGAR; ARSENOUS ACID DERIVATIVE; CACODYLIC ACID; DRUG DERIVATIVE; MONOSACCHARIDE; THIO DIMETHYLARSINATE; THIO-DIMETHYLARSINATE;

ARSENOSUGARS; ARTICLE; BIOAVAILABILITY; CELL STRAIN CACO 2; CELLULAR AND INTESTINAL BIOAVAILABILITY; CELLULAR TOXICITY; DNA DAMAGE; DRUG EFFECT; FOOD CONTAMINATION; GENOTOXICITY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; MARINE FOOD; RISK ASSESSMENT; TOXICITY TESTING;

ARSENOSUGARS; CELLULAR AND INTESTINAL BIOAVAILABILITY; CELLULAR TOXICITY; GENOTOXICITY; MARINE FOOD;

ARSENATES; ARSENITES; BIOLOGICAL AVAILABILITY; CACO-2 CELLS; CACODYLIC ACID; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DNA DAMAGE; FOOD CONTAMINATION; HUMANS; MONOSACCHARIDES; RISK ASSESSMENT; TOXICITY TESTS;

EID: 84879793155     PISSN: 16134125     EISSN: 16134133     Source Type: Journal    
DOI: 10.1002/mnfr.201200821     Document Type: Article

References (77)

1. Straif, K., Benbrahim-Tallaa, L., Baan, R., Grosse, Y. et al., A review of human carcinogens-part C: Metals, arsenic, dusts, and fibres. Lancet Oncol. 2009, 10, 453-454.
2. IARC, IARC Monographs on the Evaluation of the Carcinogenic Risks to Humans, Supplement 7, Overall Evaluations of Carcinogenicity: An Updating of IARC Monographs, Volumes 1 to 42, 1987, Lyon, France.
3. IARC, A review of human carcinogens- Part C: Arsenic, metals, fibres and dusts. IARC Monograph, IARC Lyon, 2012, 196-211.
4. EFSA, Opinion of the Panel on Contaminants in the Food Chain (CONTAM), European Food Safety Authority (EFSA), Scientific Opinion on Arsenic in Food. EFSA J. 2009, 7, 1351, 1-198.
5. WHO, WHO Technical Report Series; No. 959, World Health Organization 2011.
6. SCOOP, SCOOP Report of experts participating in Task 3.2.11. March 2004. Assessment of the dietary exposure to arsenic, cadmium, lead and mercury of the population of the (Scientific Cooperation) EU Member States. 2004.
7. Francesconi, K. A., Kuehnelt, D., in: Frankenberger Jr, W.T. (Ed.), Environmental Chemistry of Arsenic. Books in Soils, Plants, and the Environment, Marcel Dekker Inc., New York 2002, pp. 51-94.
8. Francesconi, K. A., Tanggaard, R., McKenzie, C. J., Goessler, W., Arsenic metabolites in human urine after ingestion of an arsenosugar. Clin. Chem. 2002, 48, 92-101.
9. Niegel, C., Matysik, F. M., Analytical methods for the determination of arsenosugars-a review of recent trends and developments. Anal. Chim. Acta 2010, 657, 83-99.
10. Francesconi, K. A., Edmonds, J. S., in: Sykes, A. G. (Ed.), Advances in Inorganic Chemistry, Vol. 44. Academic Press Inc., San Diego, CA 1997, pp. 147-189.
11. Francesconi, K. A., Kuehnelt, D., Determination of arsenic species: a critical review of methods and applications, 2000-2003. Analyst 2004, 129, 373-395.
12. Feldmann, J., Krupp, E. M., Critical review or scientific opinion paper: arsenosugars-a class of benign arsenic species or justification for developing partly speciated arsenic fractionation in foodstuffs? Anal. Bioanal. Chem. 2011, 399, 1735-1741.
13. Thomas, D. J., Molecular processes in cellular arsenic metabolism. Toxicol. Appl. Pharmacol. 2007, 222, 365-373.
14. Styblo, M., Del Razo, L. M., Vega, L., Germolec, D. R. et al., Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch. Toxicol. 2000, 74, 289-299.
15. Petrick, J. S., Ayala-Fierro, F., Cullen, W. R., Carter, D. E. et al., Monomethylarsonous acid (MMA(III)) is more toxic than arsenite in Chang human hepatocytes. Toxicol. Appl. Pharmacol. 2000, 163, 203-207.
16. Mass, M. J., Tennant, A., Roop, B. C., Cullen, W. R. et al., Methylated trivalent arsenic species are genotoxic. Chem. Res. Toxicol. 2001, 14, 355-361.
17. Wang, T. S., Chung, C. H., Wang, A. S., Bau, D. T. et al., Endonuclease III, formamidopyrimidine-DNA glycosylase, and proteinase K additively enhance arsenic-induced DNA strand breaks in human cells. Chem. Res. Toxicol. 2002, 15, 1254-1258.
18. Schwerdtle, T., Walter, I., Mackiw, I., Hartwig, A., Induction of oxidative DNA damage by arsenite and its trivalent and pentavalent methylated metabolites in cultured human cells and isolated DNA. Carcinogenesis 2003, 24, 967-974.
19. Schwerdtle, T., Walter, I., Hartwig, A., Arsenite and its biomethylated metabolites interfere with the formation and repair of stable BPDE-induced DNA adducts in human cells and impair XPAzf and Fpg. DNA Repair 2003, 2, 1449-1463.
20. Nollen, M., Ebert, F., Moser, J., Mullenders, L. H. et al., Impact of arsenic on nucleotide excision repair: XPC function, protein level, and gene expression. Mol. Nutr. Food Res. 2009, 53, 572-582.
21. Ebert, F., Weiss, A., Bultemeyer, M., Hamann, I. et al., Arsenicals affect base excision repair by several mechanisms. Mutat. Res. 2011, 715, 32-41.
22. Naranmandura, H., Ibata, K., Suzuki, K. T., Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem. Res. Toxicol. 2007, 20, 1120-1125.
23. Bartel, M., Ebert, F., Leffers, L., Karst, U. et al., Toxicological characterization of the inorganic and organic arsenic metabolite thio-DMA in cultured human lung cells. J. Toxicol. 2011, DOI: 10.1155/2011/373141.
24. Cohen, S. M., Ohnishi, T., Arnold, L. L., Le, X. C., Arsenic-induced bladder cancer in an animal model. Toxicol. Appl. Pharmacol. 2007, 222, 258-263.
25. Cohen, S. M., Arnold, L. L., Eldan, M., Lewis, A. S. et al., Methylated arsenicals: the implications of metabolism and carcinogenicity studies in rodents to human risk assessment. Crit. Rev. Toxicol. 2006, 36, 99-133.
26. Ahsan, H., Chen, Y., Kibriya, M. G., Slavkovich, V. et al., Arsenic metabolism, genetic susceptibility, and risk of premalignant skin lesions in Bangladesh. Cancer Epidemiol. Biomarkers Prev. 2007, 16, 1270-1278.
27. McCarty, K. M., Chen, Y. C., Quamruzzaman, Q., Rahman, M. et al., Arsenic methylation, GSTT1, GSTM1, GSTP1 polymorphisms, and skin lesions. Environ. Health Perspect. 2007, 115, 341-345.
28. Lindberg, A. L., Rahman, M., Persson, L. A., Vahter, M., The risk of arsenic induced skin lesions in Bangladeshi men and women is affected by arsenic metabolism and the age at first exposure. Toxicol. Appl. Pharmacol. 2008, 230, 9-16.
29. Brown, R. M., Newton, D., Pickford, C. J., Sherlock, J. C., Human metabolism of arsenobetaine ingested with fish. Hum. Exp. Toxicol. 1990, 9, 41-46.
30. Cannon, J. R., Edmonds, J. S., Francesconi, K. A., Raston, C. L. et al., Isolation, crystal structure and synthesis of arsenobetaine, a constituent of the western rock lobster, Panulirus cygnus, the dusky shark, Carcharhinus obscurus, and some samples of human urine. Aust. J. Chem. 1981, 34, 787-798.
31. Francesconi, K. A., Arsenic species in seafood: origin and human health implications. Pure Appl. Chem. 2010, 82, 373-381.
32. 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.
33. Ma, M., Le, X. C., Effect of arsenosugar ingestion on urinary arsenic speciation. Clin. Chem. 1998, 44, 539-550.
34. Raml, R., Goessler, W., Traar, P., Ochi, T. et al., Novel thioarsenic metabolites in human urine after ingestion of an arsenosugar, 2', 3'-dihydroxypropyl 5-deoxy-5-dimethylarsinoyl-beta-D-riboside. Chem. Res. Toxicol. 2005, 18, 1444-1450.
35. Raml, R., Raber, G., Rumpler, A., Bauernhofer, T. et al., Individual variability in the human metabolism of an arsenic-containing carbohydrate, 2', 3'-dihydroxypropyl 5-deoxy-5-dimethylarsinoyl-beta-D-riboside, a naturally occurring arsenical in seafood. Chem. Res. Toxicol. 2009, 22, 1534-1540.
36. Hansen, H. R., Jaspars, M., Feldmann, J., Arsinothioyl-sugars produced by in vitro incubation of seaweed extract with liver cytosol analysed by HPLC coupled simultaneously to ES-MS and ICP-MS. Analyst 2004, 129, 1058-1064.
37. Bin Sayeed, M. S., Ratan, M., Hossen, F., Hassan, F. et al., Arsenosugar induced blood and brain oxidative stress, DNA damage and neurobehavioral impairments. Neurochem. Res. 2013, 38, 405-412.
38. Oya-Ohta, Y., Kaise, T., Ochi, T., Induction of chromosomal aberrations in cultured human fibroblasts by inorganic and organic arsenic compounds and the different roles of glutathione in such induction. Mutat. Res. 1996, 357, 123-129.
39. Sakurai, T., Kaise, T., Ochi, T., Saitoh, T. et al., Study of in vitro cytotoxicity of a water soluble organic arsenic compound, arsenosugar, in seaweed. Toxicology 1997, 122, 205-212.
40. Andrewes, P., Demarini, D. M., Funasaka, K., Wallace, K. et al., Do arsenosugars pose a risk to human health? The comparative toxicities of a trivalent and pentavalent arsenosugar. Environ. Sci. Technol. 2004, 38, 4140-4148.
41. Traar, P., Rumpler, A., Madl, T., Saischek, G. et al., Synthesis of naturally-occurring arsenic-containing carbohydrates. Australian J. Chem. 2009, 62, 538-545.
42. Francesconi, K. A., Edmonds, J. S., Stick, R. V., Accumulation of arsenic in yelloweye mullet (Aldrichetta forsteri) following oral administration of organoarsenic compounds and arsenate. Sci. Total Environ. 1989, 79, 59-67.
43. Edmonds, J. S., Francesconi, K. A., Hansen, J. A., Dimethyloxarsylethanol from anaerobic decomposition of brown kelp (Ecklonia radiata)-a likely precursor of arsenobetaine in marine fauna. Experientia 1982, 38, 643-644.
44. Bornhorst, J., Wehe, C. A., Huwel, S., Karst, U. et al., Impact of manganese on and transfer across blood-brain and blood-cerebrospinal fluid barrier in vitro. J. Biol. Chem. 2012, 287, 17140-17151.
45. Sambuy, Y., De Angelis, I., Ranaldi, G., Scarino, M. L. et al., The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol. Toxicol. 2005, 21, 1-26.
46. Volpe, D. A., Variability in Caco-2 and MDCK cell-based intestinal permeability assays. J. Pharm. Sci. 2008, 97, 712-725.
47. Laparra, J. M., Velez, D., Barbera, R., Montoro, R. et al., Bioaccessibility and transport by Caco-2 cells of organoarsenical species present in seafood. J. Agric Food Chem. 2007, 55, 5892-5897.
48. Laparra, J. M., Velez, D., Barbera, R., Montoro, R. et al., An approach to As(III) and As(V) bioavailability studies with Caco-2 cells. Toxicol. In Vitro 2005, 19, 1071-1078.
49. Laparra, J. M., Velez, D., Barbera, R., Granero, L. et al., Cytotoxic effect of As(III) in Caco-2 cells and evaluation of its human intestinal permeability. Toxicol. In Vitro 2006, 20, 658-663.
50. Calatayud, M., Barrios, J. A., Velez, D., Devesa, V., In vitro study of transporters involved in intestinal absorption of inorganic arsenic. Chem. Res. Toxicol. 2012, 25, 446-453.
51. Calatayud, M., Devesa, V., Montoro, R., Velez, 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.
52. Calatayud, M., Velez, D., Devesa, V., Metabolism of inorganic arsenic in intestinal epithelial cell lines. Chem. Res. Toxicol. 2012, 25, 2402-2411.
53. Calatayud, M., Vazquez, M., Devesa, V., Velez, D., In vitro study of intestinal transport of inorganic and methylated arsenic species by Caco-2/HT29-MTX co-cultures. Chem. Res. Toxicol. 2012, 25, 2654-2662.
54. Calatayud, M., Gimeno, J., Velez, D., Devesa, V. et al., 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.
55. Raml, R., Rumpler, A., Goessler, W., Vahter, M. et al., Thio-dimethylarsinate is a common metabolite in urine samples from arsenic-exposed women in Bangladesh. Toxicol. Appl. Pharmacol. 2007, 222, 374-380.
56. Wang, T. S., Huang, H., Active oxygen species are involved in the induction of micronuclei by arsenite in XRS-5 cells. Mutagenesis 1994, 9, 253-257.
57. Gebel, T. W., Genotoxicity of arsenical compounds. Int. J. Hyg. Environ. Health 2001, 203, 249-262.
58. Naranmandura, H., Carew, M. W., Xu, S., Lee, J. et al., Comparative toxicity of arsenic metabolites in human bladder cancer EJ-1 cells. Chem. Res. Toxicol. 2011, 24, 1586-1596.
59. Rossman, T. G., Klein, C. B., Genetic and epigenetic effects of environmental arsenicals. Metallomics 2011, 3, 1135-1141.
60. Kligerman, A. D., Tennant, A. H., Insights into the carcinogenic mode of action of arsenic. Toxicol. Appl. Pharmacol. 2007, 222, 281-288.
61. Kligerman, A. D., Doerr, C. L., Tennant, A. H., Harrington-Brock, K. et al., Methylated trivalent arsenicals as candidate ultimate genotoxic forms of arsenic: induction of chromosomal mutations but not gene mutations. Environ. Mol. Mutagen 2003, 42, 192-205.
62. Ochi, T., Kita, K., Suzuki, T., Rumpler, A. et al., Cytotoxic, genotoxic and cell-cycle disruptive effects of thio-dimethylarsinate in cultured human cells and the role of glutathione. Toxicol. Appl. Pharmacol. 2008, 228, 59-67.
63. Van Hulle, M., Zhang, C., Schotte, B., Mees, L. et al., Identification of some arsenic species in human urine and blood after ingestion of Chinese seaweed Laminaria. J. Anal. At. Spectrom 2004, 19, 58-64.
64. Lai, V. W., Sun, Y., Ting, E., Cullen, W. R. et al., Arsenic speciation in human urine: are we all the same? Toxicol. Appl. Pharmacol. 2004, 198, 297-306.
65. Gamble, B. M., Gallagher, P. A., Shoemaker, J. A., Wei, X. et al., An investigation of the chemical stability of arsenosugars in simulated gastric juice and acidic environments using IC-ICP-MS and IC-ESI-MS/MS. Analyst 2002, 127, 781-785.
66. Almela, C., Laparra, J. M., Velez, D., Barbera, R. et al., Arsenosugars in raw and cooked edible seaweed: characterization and bioaccessibility. J. Agric. Food Chem. 2005, 53, 7344-7351.
67. Le Ferrec, E., Chesne, C., Artusson, P., Brayden, D. et al., In vitro models of the intestinal barrier. The report and recommendations of ECVAM Workshop 46. European Centre for the Validation of Alternative Methods. Altern. Lab Anim. 2001, 29, 649-668.
68. Artursson, P., Palm, K., Luthman, K., Caco-2 monolayers in experimental and theoretical predictions of drug transport. Adv. Drug Deliv. Rev. 2001, 46, 27-43.
69. Shah, P., Jogani, V., Bagchi, T., Misra, A., Role of Caco-2 cell monolayers in prediction of intestinal drug absorption. Biotechnol. Prog. 2006, 22, 186-198.
70. Conklin, S. D., Ackerman, A. H., Fricke, M. W., Creed, P. A. et al., In vitro biotransformation of an arsenosugar by mouse anaerobic cecal microflora and cecal tissue as examined using IC-ICP-MS and LC-ESI-MS/MS. Analyst 2006, 131, 648-655.
71. Van de Wiele, T., Gallawa, C. M., Kubachka, K. M., Creed, J. T. et al., Arsenic metabolism by human gut microbiota upon in vitro digestion of contaminated soils. Environ. Health Perspect. 2010, 118, 1004-1009.
72. Pinyayev, T. S., Kohan, M. J., Herbin-Davis, K., Creed, J. T. et al., Preabsorptive metabolism of sodium arsenate by anaerobic microbiota of mouse cecum forms a variety of methylated and thiolated arsenicals. Chem. Res. Toxicol. 2011, 24, 475-477.
73. Kubachka, K. M., Kohan, M. C., Herbin-Davis, K., Creed, J. T. et al., Exploring the in vitro formation of trimethylarsine sulfide from dimethylthioarsinic acid in anaerobic microflora of mouse cecum using HPLC-ICP-MS and HPLC-ESI-MS. Toxicol. Appl. Pharmacol. 2009, 239, 137-143.
74. Shimbo, S., Hayase, A., Murakami, M., Hatai, I. et al., Use of a food composition database to estimate daily dietary intake of nutrient or trace elements in Japan, with reference to its limitation. Food Addit. Contam. 1996, 13, 775-786.
75. Hansen, H. R., Raab, A., Francesconi, K. A., Feldmann, I., Metabolism of arsenic by sheep chronically exposed to arsenosugars as a normal part of their diet. 1. Quantitative intake, uptake, and excretion. Environ. Sci. Technol. 2003, 37, 845-851.
76. Erickson, B. E., Field kits fail to provide accurate measure of arsenic in groundwater. Environ. Sci. Technol. 2003, 37, 35A-38A.
77. Leffers, L., Unterberg, M., Bartel, M., Hoppe, C. et al., In vitro toxicological characterisation of the S-containing arsenic metabolites thio-dimethylarsinic acid and dimethylarsinic glutathione. Toxicology 2013, 305, 109-119.