Chronic arsenic-exposed human prostate epithelial cells exhibit stable arsenic tolerance: Mechanistic implications of altered cellular glutathione and glutathione S-transferase

Toxicology and Applied Pharmacology

Volumn 183, Issue 2, 2002, Pages 99-107

  Brambila, Eduardo M ^a   Achanzar, William E ^a   Qu, Wei ^a   Webber, Mukta M ^b   Waalkes, Michael P ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Arsenic resistance; Human; Prostate

Indexed keywords

ARSENIC TRIOXIDE; ARSENITE SODIUM; BUTHIONINE SULFOXIMINE; ETACRYNIC ACID; GLUTATHIONE; GLUTATHIONE TRANSFERASE; PROBENECID; RECEPTOR PROTEIN; VALSPODAR;

ACUTE TOXICITY; ARSENIC POISONING; ARTICLE; BIOACCUMULATION; CELL GROWTH; CHRONIC TOXICITY; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; DRUG EFFECT; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; HUMAN; HUMAN CELL; LC 50; LONG TERM EXPOSURE; PHENOTYPE; PROSTATE EPITHELIUM;

EID: 0036407708     PISSN: 0041008X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0041-008X(02)99468-8     Document Type: Article

References (44)

1. Abernathy, C. O., Liu, Y.-P., Longfellow, D., Aposhian, H. V., Beck, B., Fowler, B., Goyer, R., Menzer, R., Rossman, T., Thompson, C., and Waalkes, M. P. (1999). Arsenic: Health effects, mechanisms of actions, and research issues. Environ. Health Perspect. 107, 593-597.
2. Achanzar, W. E., Diwan, B. A., Liu, J., Quader, S., Webber, M. M., and Waalkes, M. P. (2001). Cadmium-induced malignant transformation of human prostate epithelial cells. Cancer Res. 61, 455-458.
3. Achanzar, W. E., Webber, M. M., and Waalkes, M. P. (2002). Altered apoptotic gene expression and acquired apoptotic resistance in cadmium-transformed human prostate epithelial cells. Prostate 52, 236-244.
4. ATSDR (1999). Toxicological Profiles for Arsenic. Agency for Toxic Substances and Disease Registry, Atlanta.
5. Aposhian, H. V. (1997). Enzymatic methylation of arsenic species and other new approaches to arsenic toxicity. Annu. Rev. Pharmacol. Toxicol. 37, 397-419.
6. Bello, D., Webber, M. M., Kleinman, H. K., Wartinger, D. D., and Rhim, J. S. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis 18, 1215-1223.
7. Borst, P., Evers, R., Kool, M., and Wijnholds, J. (2000). A family of drug transporters: The multidrug resistance-associated proteins. J. Natl. Cancer Inst. 92, 1295-1302.
8. Chen, C.-J., and Wang, C.-J. (1990). Ecological correlation between arsenic level in well water and age-adjusted mortality from malignant neoplasms. Cancer Res. 50, 5470-5474.
9. Chen, Z.-S., Mutoh, M., Sumizawa, T., Furukawa, T., Haraguchi, M., Tani, A., and Akiyama, S.-I. (1997). Reversal of heavy metal resistance in multidrug-resistant human KB carcinoma cells. Biochem. Biophys. Res. Commun. 236, 586-590.
10. Cohen, M. H., Hirschfeld, S., Flamm Honig, S., Ibrahim, A., Johnson, J. R., O'Leary, J. J., White, R. M., Williams, G. A., and Pazdur, R. (2001). Drug approval summaries: Arsenic trioxide, tamoxifen citrate, anastrazole, paclitaxel, bexarotene. Oncologist 6, 4-11.
11. Delnomdedieu, M., Basti, M. M., Otvos, J. D., and Thomas, D. J. (1994). Reduction and binding of arsenate and dimethylarsinate by glutathione: A magnetic resonance study. Chem. Biol. Interact. 90, 139-155.
12. Gebel, T. W., Leister, M., Schumann, W., and Hirsch-Ernst, K. (2002). Low-level self-tolerance to arsenite in human HepG2 cells is associated with a depressed induction of micronuclei. Mutat. Res. 514, 245-255.
13. Gregus, Z., and Gyurasics, A. (2000). Role of glutathione in the biliary excretion of arsenical drugs trimelarsan and melarsoprol. Biochem. Pharmacol. 59, 1375-1385.
14. Habig, W. H., Pabst, M. J., and Jakoby, W. B. (1974). Glutathione S-transferases: The first enzymatic step in mercapturic acid formation. J. Biol. Chem. 249, 7130-7139.
15. Hissin, P. J., and Hilf, R. (1976). A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal. Biochem. 74, 214-226.
16. Huang, H., Huang, C. F., Wu, D. R., Jinn, C. M., and Yan, K. Y. (1993). Glutathione as a cellular defense against arsenite toxicity in cultured Chinese hamster ovary cells. Toxicology 79, 195-204.
17. IARC (1980). Some metals and metallic compounds. In IARC Monograph on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Vol. 23. pp. 39-142. IARC, Lyon.
18. IARC (1987). Some metals and metallic compounds. In IARC Monograph on the Evaluation of the Carcinogenic Risk to Humans - Overall Evaluations of Carcinogenicity: An Update of IARC Monographs 1 to 42, Suppl. 7, pp. 100-103. IARC, Lyon
19. Ishikawa, T. (1992). The ATP-dependent glutathione S-conjugate export pump. Trends Biochem. Sci. 17, 463-468.
20. Kala, S. V., Neely, M. W., Kala, G., Prater, C. I., Atwood, D. W., Rice, J. S., and Lieberman, M. W. (2000). The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J. Biol. Chem. 275, 33404-33408.
21. Klaassen, C. D. (1996). Heavy metals and heavy-metal antagonists. In Good-man and Gilman's The Pharmacological Basis of Therapeutics, 9th ed., pp. 1649-1671. McGraw-Hill, New York.
22. Kitchin, K. T. (2001). Recent advances in arsenic carcinogenesis: Modes of action, animal model systems, and methylated arsenic metabolites. Toxicol. Appl. Pharmacol. 172, 249-261.
23. Lee, T. C., Wei, M. L., Chang, W. J., Ho, I. C., Lo, J. F., Jan, K. Y., and Huang, H. (1989a). Elevation of glutathione levels and glutathione S-transferase activity in arsenic-resistant Chinese hamster ovary cells. In Vitro Cell. Dev. Biol. 25, 442-448.
24. Lee, T.-C., Ko, J.-L., and Jan, K. Y. (1989b). Differential cytotoxicity of sodium arsenite in human fibroblasts and Chinese hamster ovary cells. Toxicology 56, 289-299.
25. Lewis, D. R., Southwick, J. W., Ouellet-Hellstrom, R., Rench, J., and Calderon, R. L. (1999). Drinking water arsenic in Utah: A cohort mortality study. Environ. Health Perspect. 107, 359-365.
26. Lo, J.-F., Wang, H.-F., Tam, M. F., and Lee, T.-C. (1992). Glutathione S-transferase π in an arsenic-resistant Chinese hamster ovary cell line. Biochem. J. 288, 977-981.
27. Liu, J., Chen, H., Miller, D. S., Saavedra, J. E., Keefer, L. K., Johnson, D. R., Klaassen, C. D., and Waalkes, M. P. (2001). Overexpression of glutathione S-transferase π and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol. Pharmacol. 60, 302-309.
28. Murgo, A. J. (2001). Clinical trials of arsenic trioxide in hematologic and solid tumors: Overview of the National Cancer Institute Cooperative Research and Development Studies. Oncologist 6(Suppl. 2), 22-28.
29. Ovelgonne, H. H., Wiegant, F. A. C., Souren, J. E. M., Van Rijn, H., and Van Wijk, R. (1995). Enhancement of the stress response by low concentrations of arsenite in arsenite-pretreated Reuber H35 hepatoma cells. Toxicol. Appl. Pharmacol. 132, 146-155.
30. Romach, E. H., Zhao, C. Q., Del Razo, L. M., Cebrian, M. E., and Waalkes, M. P. (2000). Studies on the mechanisms of arsenic-induced self tolerance developed in liver epithelial cells through continuous low-level arsenite exposure. Toxicol. Sci. 54, 500-508.
31. Rossman, T. G., Goncharova, E. I., Rajah, T., and Wang, Z. (1997). Human cells lack the inducible tolerance to arsenite seen in hamster cells. Mutat. Res. 386, 307-314.
32. Sakurai, T., Qu, W., Sakurai, M. H., and Waalkes, M. P. (2002). A major human arsenic metabolite, dimethylarsinic acid, requires reduced glutathione to induce apoptosis. Chem. Res. Toxicol. 15, 629-637.
33. Scott, N., Hatlelid, K. M., MacKenzie, N. E., and Carter, D. E. (1993). Reactions of arsenic (III) and arsenic (V) species with glutathione. Chem. Res. Toxicol. 6, 102-106.
34. 3 in the treatment of acute promyelocytic leukemia (APL). II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 89, 3354-3360.
35. Soignet, S. L., Maslak, P., Wang, Z.-G., Jhanwar, S., Calleja, E., Dardashti, L. J., Corso, D., DeBlasio, A., Gabrilove, J., Scheinberg, D. A., Pandolfi, P. P., and Warrell, R. P. (1998). Complete remission after treatment of acute promyelocytic leukemia with arsenic trioxide. N. Engl. J. Med. 339, 1341-1348.
36. Thomas, D. J., Styblo, M., and Lin, S. (2001). The cellular metabolism and systemic toxicity of arsenic. Toxicol. Appl. Pharmacol. 176, 127-144.
37. Wang, H.-F., and Lee, T.-C. (1993). Glutathione S-transferase π facilitates the excretion of arsenic from arsenic-resistant Chinese hamster ovary cells. Biochem. Biophys. Res. Commun. 192, 1093-1099.
38. Wang, Z., Dey, S., Rosen, B. P., and Rossman, T. G. (1996). Efflux-mediated resistance to arsenicals in arsenic-resistant and -hypersensitive Chinese hamster cells. Toxicol. Appl. Pharmacol. 137, 112-119.
39. Wang, Z., Hou, G., and Rossman, T. G. (1994). Induction of arsenite tolerance and thermotolerance by arsenite occur by different mechanisms. Environ. Health Perspect. 102(Suppl. 3), 97-100.
40. Wang, Z., and Rossman, T. G. (1993). Stable and inducible arsenite resistance in Chinese hamster cells. Toxicol. Appl. Pharmacol. 118, 80-86.
41. Waxman, S., and Anderson, K. C. (2001). History of the development of arsenic derivatives in cancer therapy. Oncologist 6 (Suppl. 2), 3-10.
42. Wu, M.-M., Kuo, T.-L., Hwang, Y.-H., and Chen, C.-J. (1989). Dose-response relation between arsenic concentration in well water and mortality from cancers and vascular diseases. Am. J. Epidemiol. 130, 1123-1132.
43. Zaman, G. J. R., Lankelma, J., van Tellingen, O., Beijnen, J., Dekker, H., Paulusma, C., Elferink, P. J. O., Baas, F., and Borst, P. (1995). Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl. Acad. Sci. USA 92, 7690-7694.
44. Zhao, C. Q., Young, M. R., Diwan, B. A., Coogan, T. P., and Waalkes, M. P. (1997). Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc. Natl. Acad. Sci. USA 94, 10907-10912.