In vitro toxicological characterisation of the S-containing arsenic metabolites thio-dimethylarsinic acid and dimethylarsinic glutathione

Toxicology

Volumn 305, Issue , 2013, Pages 109-119

  Leffers, Larissa ^a   Unterberg, Marlies ^a   Bartel, Marc ^a   Hoppe, Cornelia ^a   Pieper, Imke ^a   Stertmann, Julia ^a   Ebert, Franziska ^a   Humpf, Hans Ulrich ^a   Schwerdtle, Tanja ^a  

^a UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

Boost of existing oxidative stress; Cellular glutathione level; Dimethylarsinic glutathione; S containing arsenic metabolites; Thio dimethylarsinic acid

Indexed keywords

ARSENIC; ARSENIC TRIOXIDE; ARSINIC ACID DERIVATIVE; CACODYLIC ACID; DIMETHYLARSINIC GLUTATHIONE; GLUTATHIONE; ORGANOARSENIC DERIVATIVE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ARSENIC POISONING; ARTICLE; BIOAVAILABILITY; CARCINOGENICITY; CELL CYCLE PROGRESSION; CYTOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG ADENOCARCINOMA; LUNG ALVEOLUS EPITHELIUM; OXIDATIVE STRESS; PRIORITY JOURNAL;

ARSENITES; BIOLOGICAL AVAILABILITY; CACODYLIC ACID; CARCINOGENS; CELL CYCLE; CELL LINE, TUMOR; CELL SURVIVAL; GLUTATHIONE; HUMANS; HYDROGEN PEROXIDE;

EID: 84873976226     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.01.007     Document Type: Article

References (83)

1. Ackerman A.H., Creed P.A., Parks A.N., Fricke M.W., Schwegel C.A., Creed J.T., Heitkemper D.T., Velal N.P. Comparison of a chemical and enzymatic extraction of arsenic from rice and an assessment of the arsenic absorption from contaminated water by cooked rice. Environ. Sci. Technol. 2005, 39:5241-5246.
2. Ahmad S., Kitchin K.T., Cullen W.R. Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch. Biochem. Biophys. 2000, 382:195-202.
3. Bartel M., Ebert F., Leffers L., Karst U., Schwerdtle T. Toxicological characterization of the inorganic and organic arsenic metabolite thio-DMA in cultured human lung cells. J. Toxicol. 2011, 2011:373141.
4. Behl C., Moosmann B. Molekulare Mechanismen des Alterns-über das Altern der Zellen und den Einfluss von oxidativem Stress auf den Alternsprozess. Was ist Alter(n)? 2008, Springer Verlag, Heidelberg, 9-32. U.M. Staudinger, H. Häfner (Eds.).
5. Biswas J., Roy S., Mukherjee S., Sinha D., Roy M. Indian spice curcumin may be an effective strategy to combat the genotoxicity of arsenic in Swiss albino mice. Asian Pac. J. Cancer Prev. 2010, 11:239-247.
6. Bornhorst J., Ebert F., Hartwig A., Michalke B., Schwerdtle T. Manganese inhibits poly(ADP-ribosyl)ation in human cells: a possible mechanism behind manganese-induced toxicity?. J. Environ. Monit. 2010, 12:2062-2069.
7. Brodie A.E., Reed D.J. Buthionine sulfoximine inhibition of cystine uptake and glutathione biosynthesis in human lung carcinoma cells. Toxicol. Appl. Pharmacol. 1985, 77:381-387.
8. Bu N., Wang H.Y., Hao W.H., Liu X., Xu S., Wu B., Anan Y., Ogra Y., Lou Y.J., Naranmandura H. Generation of thioarsenicals is dependent on the enterohepatic circulation in rats. Metallomics 2011, 3:1064-1073.
9. 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.
10. Catanzaro I., Schiera G., Sciandrello G., Barbata G., Caradonna F., Proia P., Di Liegro I. Biological effects of inorganic arsenic on primary cultures of rat astrocytes. Int. J. Mol. Med. 2010, 26:457-462.
11. Challenger F. Biological methylation of arsenic. Chem. Rev. 1945, 36:315-361.
12. Chou W.C., Jie C., Kenedy A.A., Jones R.J., Trush M.A., Dang C.V. Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:4578-4583.
13. Chowdhury R., Chatterjee R., Giri A.K., Mandal C., Chaudhuri K. Arsenic-induced cell proliferation is associated with enhanced ROS generation, Erk signaling and CyclinA expression. Toxicol. Lett. 2010, 198:263-271.
14. Clewell H.J., Thomas R.S., Kenyon E.M., Hughes M.F., Adair B.M., Gentry P.R., Yager J.W. Concentration- and time-dependent genomic changes in the mouse urinary bladder following exposure to arsenate in drinking water for up to 12 weeks. Toxicol. Sci. 2011, 123:421-432.
15. Commoner B., Townsend J., Pake G.E. Free radicals in biological materials. Nature 1954, 174:689-691.
16. Cooper K.L., Liu K.J., Hudson L.G. Enhanced ROS production and redox signaling with combined arsenite and UVA exposure: contribution of NADPH oxidase. Free Radic. Biol. Med. 2009, 47:381-388.
17. Cullen B.C.M.B., Reglinski J. The reation of methylarsenical with thiols: some biological implications. J. Inorg. Biochem. 1984, 21:179-193.
18. De Vizcaya-Ruiz A., Barbier O., Ruiz-Ramos R., Cebrian M.E. Biomarkers of oxidative stress and damage in human populations exposed to arsenic. Mutat. Res. 2009, 674:85-92.
19. Ding W., Liu W., Cooper K.L., Qin X.J., de Souza Bergo P.L., Hudson L.G., Liu K.J. Inhibition of poly(ADP-ribose) polymerase-1 by arsenite interferes with repair of oxidative DNA damage. J. Biol. Chem. 2009, 284:6809-6817.
20. Ebert F., Weiss A., Bultemeyer M., Hamann I., Hartwig A., Schwerdtle T. Arsenicals affect base excision repair by several mechanisms. Mutat. Res. 2011, 715:32-41.
21. Eblin K.E., Bowen M.E., Cromey D.W., Bredfeldt T.G., Mash E.A., Lau S.S., Gandolfi A.J. Arsenite and monomethylarsonous acid generate oxidative stress response in human bladder cell culture. Toxicol. Appl. Pharmacol. 2006, 217:7-14.
22. EFSA Panel on contaminants in the food chain (contam), European food safety authority (EFSA), scientific opinion on arsenic in food. EFSA J. 2009, 7:1198-1351.
23. Flora S.J. Arsenic-induced oxidative stress and its reversibility. Free Radic. Biol. Med. 2011, 51:257-281.
24. Gentry P.R., McDonald T.B., Sullivan D.E., Shipp A.M., Yager J.W., Clewell H.J. Analysis of genomic dose-response information on arsenic to inform key events in a mode of action for carcinogenicity. Environ. Mol. Mutagen. 2010, 51:1-14.
25. Golladay S.A., Park S.H., Aust A.E. Efflux of reduced glutathione after exposure of human lung epithelial cells to crocidolite asbestos. Environ. Health Perspect. 1997, 105(Suppl. 5):1273-1277.
26. Grosse Y., Baan R., Straif K., Secretan B., El Ghissassi F., Bouvard V., Benbrahim-Tallaa L., Guha N., Galichet L., Cogliano V. A review of human carcinogens. Part A: pharmaceuticals. Lancet Oncol. 2009, 10:13-14.
27. Halliwell B., Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean?. Br. J. Pharmacol. 2004, 142:231-255.
28. Hartwig A., Klyszcz-Nasko H., Schlepegrell R., Beyersmann D. Cellular damage by ferric nitrilotriacetate and ferric citrate in V79 cells: interrelationship between lipid peroxidation, DNA strand breaks and sister chromatid exchanges. Carcinogenesis 1993, 14:107-112.
29. Hayakawa T., Kobayashi Y., Cui X., Hirano S. A new metabolic pathway of arsenite: arsenic-glutathione complexes are substrates for human arsenic methyltransferase Cyt19. Arch. Toxicol. 2005, 79:183-191.
30. Huang C., Ke Q., Costa M., Shi X. Molecular mechanisms of arsenic carcinogenesis. Mol. Cell. Biochem. 2004, 255:57-66.
31. IARC IARC monographs on the evaluation of the carcinogenic risks to humans, Suppl. 7. Overall Evaluations of Carcinogenicity: An Updating of IARC Monographs Volumes 1 to 42 1987, IARC (International Agency for Research on Cancer), Lyon, France.
32. IARC A review of human carcinogens. Part C: Arsenic, metals, fibres and dusts, IARC Monographs 2012, IARC, Lyon, France, pp. 196-211.
33. Kala S.V., Neely M.W., Kala G., Prater C.I., Atwood D.W., Rice J.S., Lieberman M.W. The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J. Biol. Chem. 2000, 275:33404-33408.
34. Kanaki K., Pergantis S.A. Development of mass spectrometric methods for detecting arsenic-glutathione complexes. J. Am. Soc. Mass Spectrom. 2008, 19:1559-1567.
35. Kastan M.B., Bartek J. Cell-cycle checkpoints and cancer. Nature 2004, 432:316-323.
36. Korystov Y.N., Shaposhnikova V.V., Korystova A.F., Emel'yanov M.O. Detection of reactive oxygen species induced by radiation in cells using the dichlorofluorescein assay. Radiat. Res. 2007, 168:226-232.
37. Kuroda K., Yoshida K., Yoshimura M., Endo Y., Wanibuchi H., Fukushima S., Endo G. Microbial metabolite of dimethylarsinic acid is highly toxic and genotoxic. Toxicol. Appl. Pharmacol. 2004, 198:345-353.
38. Leslie E.M. Arsenic-glutathione conjugate transport by the human multidrug resistance proteins (MRPs/ABCCs). J. Inorg. Biochem. 2012, 108:141-149.
39. Lii C.K., Lin A.H., Lee S.L., Chen H.W., Wang T.S. Oxidative modifications of proteins by sodium arsenite in human umbilical vein endothelial cells. Environ. Toxicol. 2010, 26:459-471.
40. Liu Z., Sanchez M.A., Jiang X., Boles E., Landfear S.M., Rosen B.P. Mammalian glucose permease GLUT1 facilitates transport of arsenic trioxide and methylarsonous acid. Biochem. Biophys. Res. Commun. 2006, 351:424-430.
41. Liu Z., Shen J., Carbrey J.M., Mukhopadhyay R., Agre P., Rosen B.P. Arsenite transport by mammalian aquaglyceroporins AQP7 and AQP9. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6053-6058.
42. Liu Z., Styblo M., Rosen B.P. Methylarsonous acid transport by aquaglyceroporins. Environ. Health Perspect. 2006, 114:527-531.
43. Lu W.J., Tamai I., Nezu J., Lai M.L., Huang J.D. Organic anion transporting polypeptide-C mediates arsenic uptake in HEK-293 cells. J. Biomed. Sci. 2006, 13:525-533.
44. Lynn S., Gurr J.R., Lai H.T., Jan K.Y. NADH oxidase activation is involved in arsenite-induced oxidative DNA damage in human vascular smooth muscle cells. Circ. Res. 2000, 86:514-519.
45. Mann K.K., Wallner B., Lossos I.S., Miller W.H. Darinaparsin: a novel organic arsenical with promising anticancer activity. Expert Opin. Investig. Drugs 2009, 18:1727-1734.
46. Marchiset-Ferlay N., Savanovitch C., Sauvant-Rochat M.P. What is the best biomarker to assess arsenic exposure via drinking water?. Environ. Int. 2012, 39:150-171.
47. McDermott J.R., Jiang X., Beene L.C., Rosen B.P., Liu Z. Pentavalent methylated arsenicals are substrates of human AQP9. Biometals 2010, 23:119-127.
48. Mishra D., Flora S.J. Differential oxidative stress and DNA damage in rat brain regions and blood following chronic arsenic exposure. Toxicol. Ind. Health 2008, 24:247-256.
49. Naranmandura H., Carew M.W., Xu S., Lee J., Leslie E.M., Weinfeld M., Le X.C. Comparative toxicity of arsenic metabolites in human bladder cancer EJ-1 cells. Chem. Res. Toxicol. 2011, 24:1586-1596.
50. Naranmandura H., Ibata K., Suzuki K.T. Toxicity of dimethylmonothioarsinic acid toward human epidermoid carcinoma A431 cells. Chem. Res. Toxicol. 2007, 20:1120-1125.
51. Naranmandura H., Ogra Y., Iwata K., Lee J., Suzuki K.T., Weinfeld M., Le X.C. Evidence for toxicity differences between inorganic arsenite and thioarsenicals in human bladder cancer cells. Toxicol. Appl. Pharmacol. 2009, 238:133-140.
52. Naranmandura H., Suzuki N., Suzuki K.T. Trivalent arsenicals are bound to proteins during reductive methylation. Chem. Res. Toxicol. 2006, 19:1010-1018.
53. Naranmandura H., Xu S., Sawata T., Hao W.H., Liu H., Bu N., Ogra Y., Lou Y.J., Suzuki N. Mitochondria are the main target organelle for trivalent monomethylarsonous acid (MMA(III))-induced cytotoxicity. Chem. Res. Toxicol. 2011, 24:1094-1103.
54. Ochi T., Kita K., Suzuki T., Rumpler A., Goessler W., Francesconi K.A. 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.
55. Pinyayev T.S., Kohan M.J., Herbin-Davis K., Creed J.T., Thomas D.J. 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.
56. Raab A., Meharg A.A., Jaspars M., Genney D., Feldmann J. Arsenic-glutathione complexes-their stability in solution and during separation by differnt HPLC modes. J. Anal. At. Spectrom. 2004, 19:183-190.
57. Rahman I., Kode A., Biswas S.K. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat. Protoc. 2006, 1:3159-3165.
58. Rahman I., Li X.Y., Donaldson K., Harrison D.J., MacNee W. Glutathione homeostasis in alveolar epithelial cells in vitro and lung in vivo under oxidative stress. Am. J. Physiol. 1995, 269:L285-L292.
59. Raml R., Goessler W., Traar P., Ochi T., Francesconi K.A. 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.
60. Raml R., Raber G., Rumpler A., Bauernhofer T., Goessler W., Francesconi K.A. 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.
61. Raml R., Rumpler A., Goessler W., Vahter M., Li L., Ochi T., Francesconi K.A. Thio-dimethylarsinate is a common metabolite in urine samples from arsenic-exposed women in Bangladesh. Toxicol. Appl. Pharmacol. 2007, 222:374-380.
62. Rossman T.G., Klein C.B. Genetic and epigenetic effects of environmental arsenicals. Metallomics 2011.
63. Sakurai T., Kojima C., Kobayashi Y., Hirano S., Sakurai M.H., Waalkes M.P., Himeno S. Toxicity of a trivalent organic arsenic compound, dimethylarsinous glutathione in a rat liver cell line (TRL 1215). Br. J. Pharmacol. 2006, 149:888-897.
64. Samikkannu T., Chen C.H., Yih L.H., Wang A.S., Lin S.Y., Chen T.C., Jan K.Y. Reactive oxygen species are involved in arsenic trioxide inhibition of pyruvate dehydrogenase activity. Chem. Res. Toxicol. 2003, 16:409-414.
65. Schuliga M., Chouchane S., Snow E.T. Upregulation of glutathione-related genes and enzyme activities in cultured human cells by sublethal concentrations of inorganic arsenic. Toxicol. Sci. 2002, 70:183-192.
66. 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.
67. Shi H., Shi X., Liu K.J. Oxidative mechanism of arsenic toxicity and carcinogenesis. Mol. Cell. Biochem. 2004, 255:67-78.
68. Shi Y., Wei Y., Qu S., Wang Y., Li Y., Li R. Arsenic induces apoptosis of human umbilical vein endothelial cells through mitochondrial pathways. Cardiovasc. Toxicol. 2010, 10:153-160.
69. Sies H., Mehlhorn R. Mutagenicity of nitroxide-free radicals. Arch. Biochem. Biophys. 1986, 251:393-396.
70. Suzuki S., Arnold L.L., Pennington K.L., Chen B., Naranmandura H., Le X.C., Cohen S.M. Dietary administration of sodium arsenite to rats: relations between dose and urinary concentrations of methylated and thio-metabolites and effects on the rat urinary bladder epithelium. Toxicol. Appl. Pharmacol. 2010, 244:99-105.
71. Tezuka M., Hanioka K., Yamanaka K., Okada S. Gene damage induced in human alveolar type II (L-132) cells by exposure to dimethylarsinic acid. Biochem. Biophys. Res. Commun. 1993, 191:1178-1183.
72. Thomas D.J. Molecular processes in cellular arsenic metabolism. Toxicol. Appl. Pharmacol. 2007, 222:365-373.
73. Thomas D.J. Unraveling arsenic-glutathione connections. Toxicol. Sci. 2009, 107:309-311.
74. Tian J., Zhao H., Nolley R., Reese S.W., Young S.R., Li X., Peehl D.M., Knox S.J. Darinaparsin: solid tumor hypoxic cytotoxin and radiosensitizer. Clin. Cancer Res. 2012.
75. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal. Biochem. 1969, 27:502-522.
76. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Curr. Med. Chem. 2005, 12:1161-1208.
77. Walter I., Schwerdtle T., Thuy C., Parsons J.L., Dianov G.L., Hartwig A. Impact of arsenite and its methylated metabolites on PARP-1 activity, PARP-1 gene expression and poly(ADP-ribosyl)ation in cultured human cells. DNA Repair (Amst.) 2007, 6:61-70.
78. Wang T.S., Chung C.H., Wang A.S., Bau D.T., Samikkannu T., Jan K.Y., Cheng Y.M., Lee T.C. 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.
79. Watanabe T., Hirano S. Metabolism of arsenic and its toxicological relevance. Arch. Toxicol. 2012.
80. WHO, 2011. Evaluation of certain food additives: Seventy-second Report of the Joint FAO/WHO Expert Committee on Food Additives WHO Technical Report Series No. 959, World Health Organization.
81. Wnek S.M., Kuhlman C.L., Camarillo J.M., Medeiros M.K., Liu K.J., Lau S.S., Gandolfi A.J. Interdependent genotoxic mechanisms of monomethylarsonous acid: role of ROS-induced DNA damage and poly(ADP-ribose) polymerase-1 inhibition in the malignant transformation of urothelial cells. Toxicol. Appl. Pharmacol. 2011, 257:1-13.
82. Yamanaka K., Hoshino M., Okamoto M., Sawamura R., Hasegawa A., Okada S. Induction of DNA damage by dimethylarsine, a metabolite of inorganic arsenics, is for the major part likely due to its peroxyl radical. Biochem. Biophys. Res. Commun. 1990, 168:58-64.
83. Yoshida K., Kuroda K., Zhou X., Inoue Y., Date Y., Wanibuchi H., Fukushima S., Endo G. Urinary sulfur-containing metabolite produced by intestinal bacteria following oral administration of dimethylarsinic acid to rats. Chem. Res. Toxicol. 2003, 16:1124-1129.