Liver is a target of arsenic carcinogenesis

Toxicological Sciences

Volumn 105, Issue 1, 2008, Pages 24-32

  Liu, Jie ^a   Waalkes, Michael P ^a  

^a National Cancer Institute   (United States)

Author keywords

Animal models; Arsenic; Carcinogenesis; Epidemiology; Liver; Mechanisms

Indexed keywords

8 HYDROXYDEOXYGUANOSINE; ARSENIC; CACODYLIC ACID; CYCLIN D1; CYCLINE; DIETHYLNITROSAMINE; DNA; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DRINKING WATER; ESTROGEN; ESTROGEN RECEPTOR ALPHA; GLUTATHIONE TRANSFERASE; HEME OXYGENASE 1; METALLOTHIONEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; ORGANOARSENIC DERIVATIVE; PROTEIN P16; PROTEIN P53; TRIMETHYLARSINE OXIDE; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ANGIOSARCOMA; APOPTOSIS; ARSENIC POISONING; ARTICLE; BIOTRANSFORMATION; CANCER INCIDENCE; CANCER MORTALITY; CARCINOGENICITY; CELL PROLIFERATION; CHEMICAL CARCINOGENESIS; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; ENVIRONMENTAL EXPOSURE; GENOMIC INSTABILITY; HEPATOMEGALY; HUMAN; LIVER ADENOMA; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; LIVER CIRRHOSIS; LIVER DYSFUNCTION; LIVER FIBROSIS; LIVER SARCOMA; LIVER TOXICITY; MALIGNANT TRANSFORMATION; NONHUMAN; OXIDATIVE STRESS; PRENATAL EXPOSURE; PREVALENCE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TARGET ORGAN; TISSUE SPECIFICITY; TOXICOKINETICS; TUMOR PROMOTION; WATER CONTAMINATION;

ANIMALS; APOPTOSIS; ARSENIC; CARCINOMA, HEPATOCELLULAR; DNA DAMAGE; DNA METHYLATION; DNA REPAIR; ESTROGENS; HUMANS; LIVER; LIVER NEOPLASMS; MICE;

ANIMALIA; MUS; MUS MUSCULUS; RATTUS; RODENTIA;

EID: 49249109498     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn120     Document Type: Article

References (71)

1. Andrew, A. S., Burgess, J. L., Meza, M. M., Demidenko, E., Waugh, M. G., Hamilton, J. W., and Karagas, M. R. (2006). Arsenic exposure is associated with decreased DNA repair in vitro and in individuals exposed to drinking water arsenic. Environ. Health Perspect. 114, 1193-1198.
2. Buchet, J. P., Geubel, A., Pauwels, S., Mahieu, P., and Lauwerys, R. (1984). The influence of liver disease on the methylation of arsenite in humans. Arch. Toxicol. 55, 151-154.
3. Centeno, J A., Mullick, F. G., Martinez, L., Page, N. P., Gibb, H., Longfellow, D., Thompson, C., and Ladich, E. R. (2002). Pathology related to chronic arsenic exposure. Environ. Health Perspect. 110(Suppl. 5), 883-880.
4. Chen, C. J., Chen, C. W., Wu, M. M., and Kuo, T. L. (1992). Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br. J. Cancer 66, 888-892.
5. Chen, C. J., Chuang, Y. C., Lin, T. M., and Wu, H. Y. (1985). Malignant neoplasms among residents of a blackfoot disease-endemic area in Taiwan: High-arsenic artesian well water and cancers. Cancer Res. 45 5895-5899.
6. Chen, C. J., Chuang, Y. C., You, S. L., Lin, T. M., and Wu, H. Y. (1986). A retrospective study on malignant neoplasms of bladder, lung and liver in blackfoot disease endemic area in Taiwan. Br. J. Cancer 53, 399-405.
7. Chen, C. J., Kuo, T. L., and Wu, M. M. (1988). Arsenic and cancers. Lancet 8582, 414-415.
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, H., Li, S., Liu, J., Diwan, B. A., Barrett, J. C., and Waalkes, M. P. (2004). Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: Implications for arsenic hepatocarcinogenesis. Carcinogenesis 25, 1779-1786.
10. Cher, H., Liu, J., Merrick, B. A., and Waalkes, M. P. (2001a). Genetic events associated with arsenic-induced malignant transformation: Applications of cDNA microarray technology. Mol. Carcinog. 30 79-87.
11. Chen, H., Liu, J., Zhao, C. Q., Diwan, B. A., Merrick, B. A., and Waalkes, M. P. (2001b). Association of c-myc overexpression and hyperproliferation with arsenite-induced malignant transformation. Toxicol. Appl. Pharmacol. 175, 260-268.
12. Chen, J. G., Chen, Y. G., Zhou, Y. S., Lin, G. F., Li, X. J., Jia, C. G., Guo, W. C., Du, H., Lu, H. C., Meng, H., et al. (2007). A follow-up study of mortality among the arseniasis patients exposed to indoor combustion of high arsenic coal in Southwest Guizhou Autonomous Prefecture, China. Int. Arch. Occup. Environ. Health 81, 9-17.
13. Chen, Y., and Ahsan, H. (2004). Cancer burden from arsenic in drinking water in Bangladesh. Am. J. Public Health 94, 741-744.
14. Chiu, H. F., Ho, S. C., Wang, L. Y., Wu, T. N, and Yang, C. Y. (2004). Does arsenic exposure increase the risk for liver cancer? J. Toxicol. Environ. Health A 67, 1491-1500.
15. Datta, D. V., Mitra, S. K., Chhuttani, P. N., and Chakravarti, R. N. (1979). Chronic oral arsenic intoxication as a possible aetiological factor in idiopathic portal hypertension (non-cirrhotic portal fibrosis) in India. Gut 20, 378-384.
16. Dhawan, D., Narang, A. P., and Darta, D. V. (1983). Levels of arsenic in liver cirrhosis. Toxicol. Lett. 15, 105-108.
17. Dickson, R. B., and Stancel, G. M. (2000). Estrogen receptor-mediated processes in normal and cancer cells. J. Natl. Cancer Inst. Monogr. 27, 135-145.
18. Geubel, A. P., Mairlot, M. C., Buchet, J. P., Dive, C., and Lauwerys, R. (1988). Abnormal methylation capacity in human liver cirrhosis. Int. J. Clin. Pharmacol. Res. 8, 117-122.
19. Gregus, Z., and Nemeti, B. (2002). Purine nucleoside phosphorylase as a cytosolic arsenate reductase. Toxicol. Sci. 70, 13-19.
20. Guo, H. R. (2003). The lack of a specific association between arsenic in drinking water and hepatocellular carcinoma. J. Hepatol. 39, 383-388.
21. Hartwig, A., Blessing, H., Schwerdtle, T., and Walter, I. (2003). Modulation of DNA repair processes by arsenic and selenium compounds. Toxicology 193, 161-169.
22. Hopenhayn-Rich, C., Biggs, M. L., and Smith, A. H. (1998). Lung and kidney cancer mortality associated with arsenic in drinking water in Cordoba, Argentina. Int. J. Epidemiol. 27, 561-569.
23. IARC (International Agency for Research on Cancer) (1980). Monographs on the evaluation of carcinogenic risk of chemicals to humans. In Some Metals and Metallic Compounds, Vol. 23, pp. 39-141. IARC Press, Lyon.
24. IARC (International Agency for Research on Cancer) (2004). Monographs on evaluation of carcinogenic risk to humans. In Some Drinking Water Disinfectants and Contaminants, including Arsenic, Vol. 84, pp. 269-477. IARC Press, Lyon.
25. Kinoshita, A., Wanibuchi, H., Wei, M., Yunoki, T., and Fukushima, S. (2007). Elevation of 8-hydroxydeoxyguanosine and cell proliferation via generation of oxidative stress by organic arsenicals contributes to their carcinogenicity in the rat liver and bladder. Toxicol. Appl. Pharmacol. 221, 295-305.
26. 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.
27. Liu, D. N., Lu, X. Z., Li, B. L., Zhou, D. X., Li, F. X., Zheng, D. H., and Wang, K. H. (1992). Clinical analysis of 535 cases of chronic arsenic poisoning from coal burning. Chin. J. Med. 31, 560-562.
28. Liu, J., Benbrahim-Tallaa, L., Qian, X., Yu, L., Xie, Y., Boos, J., Qu, W., and Waalkes, M. P. (2006a). Further studies on aberrant gene expression associated with arsenic-induced malignant transformation in rat liver TRL1215. Toxicol. Appl. Pharmacol. 216, 407-415.
29. Liu, J., Chen, H., Miller, D. S., Saavedra, J. E., Keefer, L. K., Johnson, D. R., Klaassen, C. D., and Waalkes, M. P. (2001a). Overexpression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol. Pharmacol. 60, 302-309.
30. Liu, J., Kadiiska, M. B., Liu, Y., Lu, T., Qu, W., and Waalkes, M. P. (2001b). Stress-related gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 61, 314-320.
31. Liu, J., Xie, Y., Cooper, R., Ducharme, D. N. K., Tennant, R., Diwan, B. A., and Waalkes, M. P. (2007). Transplacental exposure to inorganic arsenic at a hepatocarcinogenic dose induces fetal gene expression changes in mice indicative of aberrant estrogen signaling and disrupted steroid metabolism. Toxicol. Appl. Pharmacol. 220, 284-291.
32. Liu, J., Xie, Y., Ducharme, D. M. K., Shen, J., Diwan, B. A., Merrick, A. B., Grissom, S. F., Tucker, C. J., Paules, R. S., Tennant, R., et al. (2006b). Global gene expression associated with hepatocarcinogenesis in adult male mice induced by in utero arsenic exposure. Environ. Health Perspect. 114, 404-411.
33. Liu, J., Xie, Y., Ward, J. M., Diwan, B. A., and Waalkes, M. P. (2004). Toxicogenomic analysis of aberrant gene expression in liver tumors and nontumorous livers of adult mice exposed in utero to inorganic arsenic. Toxicol. Sci. 77, 249-257.
34. Liu, J., Zheng, B., Aposhian, H. V., Zhou, Y., Cheng, M.-L., Zhang, A. H., and Waalkes, M. P. (2002). Chronic arsenic poisoning from burning high-arsenic-containing coal in Guizhou, China. Environ. Health Perspect. 110, 119-122.
35. Lu, T., Liu, J., LeCluyse, E. L., Zhou, Y.-S., Cheng, M.-L., and Waalkes, M. P. (2001). Application of cDNA microarray to the study of arsenic-induced liver diseases in the population of Guizhou, China. Toxicol. Sci. 59, 185-192.
36. Luo, F. J., Luo, Z. D., and Ma, L. (1995). A study on the relationship between drinking water with high arsenic content and incidence of malignant tumour in Heihe Village, western part of Huhehot, Inner Mongolia. Zhonghua Liu Xing Bing Xue Za Zhi 16, 289-291.
37. Mass, M. J., and Wang, L. (1997). Arsenic alters cytosine methylation patterns of the promoter of the tumor suppressor gene p53 in human lung cells: A model for a mechanism of carcinogenesis. Mutat. Res. 386, 263-277.
38. Mazumder, D. N. (2005). Effect of chronic intake of arsenic-contaminated water on liver. Toxicol. Appl. Pharmacol. 206, 169-175.
39. Morales, K. H., Ryan, L., Kuo, T. L., Wu, M. M., and Chen, C. J. (2000). Risk of internal cancers from arsenic in drinking water. Environ. Health Perspect. 108, 655-661.
40. Nevens, F., Fevery, J., Van Steenbergen, W., Sciot, R., Desmet, V., and De Groote, J. (1990). Arsenic and non-cirrhotic portal hypertension. A report of eight cases. J. Hepatol. 11, 80-85.
41. Nishikawa, T., Wanibuchi, H., Ogawa, M., Kinoshita, A., Morimura, K., Hiroi, T., Funae, Y., Kishida, H., Nakae, D., and Fukushima, S. (2002). Promoting effects of monomethylarsonic acid, dimethylarsinic acid and trimethylarsine oxide on induction of rat liver preneoplastic glutathione S-transferase placental form positive foci: A possible reactive oxygen species mechanism. Int. J. Cancer 100, 136-139.
42. NRC. (1999). Arsenic in the Drinking Water. National Research Council, National Academy, Washington, DC.
43. Okoji, R. S., Yu, R. C., Maronpot, R. R., and Froines, J. R. (2002). Sodium arsenite administration via drinking water increases genome-wide and Ha-ras DNA hypomethylation in methyl-deficient C57BL/6J mice. Carcinogenesis 23, 777-785.
44. Qu, W., Bortner, C. D., Sakurai, T., Hobson, M. J., and Waalkes, M. P. (2002). Acquisition of apoptotic resistance in arsenic-induced malignant transformation: Role of the JNK signal transduction pathway. Carcinogenesis 23, 151-159.
45. Reichard, J. F., Schnekenburger, M., and Puga, A. (2007). Long term low-dose arsenic exposure induces loss of DNA methylation. Biochem. Biophys. Res. Commun. 352, 188-192.
46. Rossman, T. G. (2003). Mechanism of arsenic carcinogenesis: An integrated approach. Mutat. Res. 533, 37-65.
47. Santra, A., Das Gupta, J., De, B. K., Roy, B., and Guha Mazumder, D. N. (1999). Hepatic manifestations in chronic arsenic toxicity. Indian J. Gastroenterol. 18, 152-155.
48. Sciandrello, G., Caradonna, F., Mauro, M., and Barbata, G. (2004). Arsenic-induced DNA hypomethylation affects chromosomal instability in mammalian cells. Carcinogenesis 25, 413-417.
49. Shen, J., Wanibuchi, H., Salim, E. I., Wei, M., Kinoshita, A., Yoshida, K., Endo, G., and Fukushima, S. (2003). Liver tumorigenicity of trimethylarsine oxide in male Fischer 344 rats - Association with oxidative DNA damage and enhanced cell proliferation. Carcinogenesis 24, 1827-1835.
50. Smith, A. H., Goycolea, M., Haque, R., and Biggs, M. L. (1998). Marked increase in bladder and lung cancer mortality in a region of Northern Chile due to arsenic in drinking water. Am. J. Epidemiol. 147 660-669.
51. Smith, A. H., Hopenhayn-Rich, C., Bates, M. N., Goeden, H. M., Hertz-Picciotto, I., Duggan, H. M., Wood, R., Kosnett, M. J., and Smith, M. T. (1992). Cancer risks from arsenic in drinking water. Environ. Health Perspect. 97, 259-267.
52. Smith, A. H., Marshall, G., Yuan, Y., Ferreccio, C., Liaw, J., von Ehrenstein, O., Steinmaus, C., Bates, M. N., and Selvin, S. (2006). Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ. Health Perspect. 114, 1293-1296.
53. Straub, A. C., Stolz, D. B., Ross, M. A., Hernandez-Zavala, A., Soucy, N. V., Klei, L. R., and Barchowsky, A. (2007). Arsenic stimulates sinusoidal endothelial cell capillarization and vessel remodeling in mouse liver. Hepatology 45, 205-212.
54. Thomas, D. J. (2007). Molecular processes in cellular arsenic metabolism. Toxicol. Appl. Pharmacol. 222, 365-373.
55. Tsai, S. M., Wang, T. N., and Ko, Y. C. (1999). Mortality for certain diseases in areas with high levels of arsenic in drinking water. Arch. Environ. Health 54, 186-193.
56. Tsuda, T., Babazono, A., Yamamoto, E., Kurumatani, N., Mino, Y., Ogawa, T., Kishi, Y., and Aoyama, H. (1995). Ingested arsenic and internal cancer: A historical cohort study followed for 33 years. Am. J. Epidemiol. 141, 198-209.
57. Waalkes, M. P., Keefer, L. K., and Diwan, B. A. (2000). Induction of proliferative lesions of the uterus, testes, and liver in swiss mice given repealed injections of sodium arsenate: Possible estrogenic mode of action. Toxicol. Appl. Pharmacol. 166, 24-35.
58. Waalkes, M. P., Liu, J., Chen, H., Xie, Y., Achanzar, W. E., Zhou, Y. S., Cheng, M. L., and Diwan, B. A. (2004a). Estrogen signaling in livers of male mice with hepatocellular carcinoma induced by exposure to arsenic in utero. J. Natl. Cancer Inst. 96, 466-474.
59. Waalkes, M. P., Liu, J., and Diwan, B. A. (2007). Transplacental arsenic carcinogenesis in mice. Toxicol. Appl. Pharmacol. 222, 271-280.
60. Waalkes, M. P., Liu, J., Ward, J. M., and Diwan, B. A. (2006a). Enhanced urinary bladder and liver carcinogenesis in male CD1 mice exposed to transplacental inorganic arsenic and postnatal diethylstilbestrol or tamoxifen. Toxicol. Appl. Pharmacol. 215, 295-305.
61. Waalkes, M. P., Liu, J., Ward, J. M., Powell, D. A., and Diwan, B. A. (2006b). Urogenital carcinogenesis in female CD1 mice induced by in utero arsenic exposure is exacerbated by postnatal diethylstilbestrol treatment. Cancer Res. 66, 1337-1345.
62. Waalkes, M. P., Ward, J. M., and Diwan, B. A. (2004b). Induction of tumors of the liver, lung, ovary and adrenal in adult mice after brief maternal gestational exposure to inorganic arsenic: Promotional effects of postnatal phorbol ester exposure on hepatic and pulmonary, but not dermal cancers. Carcinogenesis 25, 133-141.
63. Waalkes, M. P., Ward, J. M., Liu, J., and Diwan, B. A. (2003). Transplacental carcinogenicity of inorganic arsenic in the drinking water: Induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol. Appl. Pharmacol. 186, 7-17.
64. Wanibuchi, H., Salim, E. I., Kinoshita, A., Shen, J., Wei, M., Morimura, K., Yoshida, K., Kuroda, K., Endo, G., and Fukushima, S. (2004). Understanding arsenic carcinogenicity by the use of animal models. Toxicol. Appl. Pharmacol. 198, 366-376.
65. Wu, M. M., Kuo, T. L., Hwang, Y. H., and Chen, C. J. (1999). Dose-response relation between arsenic concentration in well water and mortality from cancers and vascular diseases. Am. J. Epidemiol. 130, 1123-1132.
66. Xie, Y., Liu, J., Benbrahim-Tallaa, L., Ward, J. M., Logsdon, D., Diwan, B. A., and Waalkes, M. P. (2007). Aberrant DNA methylation and gene expression in livers of newborn mice transplacentally exposed to a hepatocarcinogenic dose of inorganic arsenic. Toxicology 236 7-15.
67. Xie, Y., Trouba, K. J., Liu, J., Waalkes, M. P., and Germolec, D. R. (2004). Biokinetics and subchronic toxic effects of oral arsenite, arsenate, monomethylarsonic acid, and dimethylarsinic acid in v-Ha-ras transgenic (Tg.AC) mice. Environ. Health Perspect. 112, 1255-1263.
68. Yamamoto, S., Konishi, Y., Matsuda, T., Murai, T., Shibata, M. A., Matsui-Yuasa, I., Otani, S., Kuroda, K., Endo, G., and Fukushima, S. (1995). Cancer induction by an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in F344/DuCrj rats after pretreatment with five carcinogens. Cancer Res. 55, 1271-1276.
69. Zhang, A. H., Huang, X. X., Jiang, X. Y., Luo, P., Guo, Y. C., and Xue, S. Z. (2000). The progress of study on endemic arsenism due to burning arsenic containing coal in Guizhou province. In Metal Ions in Biology and Medicine (J. A. Centeno, P. Collery, G. Vernet, R. O. Finkelman, H. Gibb, and J.-C. Etienne, Eds.), Vol. 6, pp. 53-55. John Libbey Eurotext, Ltd., France.
70. 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. U. S. A. 94, 10907-10912.
71. Zhou, Y.-S., Du, H., Cheng, M.-L., Liu, J., Zhang, X.-J., and Xu, L. (2002). The investigation of death from diseases caused by coal-burning type of arsenic poisoning. Chin. J. Endemiol. 21, 484-486.