Cancer Letters
Volume 230, Issue 1 , Pages 57-64 , 8 December 2005

Specific induction of oxidative stress in terminal bronchiolar Clara cells during dimethylarsenic-induced lung tumor promoting process in mice

  • Yan An

      Affiliations

    • Department of Biochemical Toxicology, College of Pharmacy, Nihon University, 7-7-1 Narashinodai, Funabashi, Chiba 274-8555, Japan
    • ,
  • Koichi Kato

      Affiliations

    • Department of Biochemical Toxicology, College of Pharmacy, Nihon University, 7-7-1 Narashinodai, Funabashi, Chiba 274-8555, Japan
    • ,
  • Masayuki Nakano

      Affiliations

    • National Hospital Organization Chiba Medical Center, 4-1-2 Tsubakimori, Chuo-ku, Chiba 260-8606, Japan
    • ,
  • Hiroshi Otsu

      Affiliations

    • National Hospital Organization Chiba Medical Center, 4-1-2 Tsubakimori, Chuo-ku, Chiba 260-8606, Japan
    • ,
  • Shoji Okada

      Affiliations

    • University of Shizuoka, 2-12-7 Mariko, Shizuoka 421-0103, Japan
    • ,
  • Kenzo Yamanaka

      Affiliations

    • Department of Biochemical Toxicology, College of Pharmacy, Nihon University, 7-7-1 Narashinodai, Funabashi, Chiba 274-8555, Japan
    • Corresponding Author InformationCorresponding author. Tel./fax: +81 47 465 6077.

Received 13 December 2004 ,Revised 15 December 2004 ,Accepted 15 December 2004.

References 

  1. Inayama Y. Promoting action of glycerol in pulmonary tumorigenesis model using a single administration of 4-nitroquinoline 1-oxide in mice. Jpn J. Cancer Res. (Gann). 1986;77:345–350
  2. Kanisawa M. Developmental steps of experimentally induced adenocarcinoma of the lung. In:  Shimosato Y,  Melamed MR,  Nettesheim P editor. Morphogenesis of Lung Cancer. vol. II:Florida: CRC Press, Inc.; 1982;p. 181–204
  3. Kitamura H, Inayama Y, Ito T, Yabana M, Piegorsch WW, Kanisawa M. Morphological alteration of mouse Clara cells induced by glycerol: ultrastructural and morphometric studies. Exp. Lung Res. 1987;12:281–302
  4. Yamanaka K, Ohtsubo K, Hasegawa A, Hayashi H, Ohji H, Kanisawa M, et al. Exposure to dimethylarsinic acid, a main metabolite of inorganic arsenics, strongly promotes tumorigenesis initiated by 4-nitroquinoline 1-oxide in the lungs of mice. Carcinogenesis. 1996;17:767–770
  5. Yamanaka K, Katsumata K, Ikuma K, Hasegawa A, Nakano M, Okada S. The role of orally administered dimethylarsinic acid, a main metabolite of inorganic arsenics, in the promotion and progression of UVB-induced skin tumorigenesis in hairless mice. Cancer Lett. 2000;152:79–85
  6. Yamanaka K, Mizoi M, Kato K, Hasegawa A, Nakano M, Okada S. Oral administration of dimethylarsinic acid, a main metabolite of inorganic arsenics, in mice promotes skin tumorigenesis initiated by dimethylbenz(a)anthracene with or without ultraviolet B as a promoter. Bio. Pharm. Bull. 2001;24:510–514
  7. Yamamoto S, Konishi Y, Matsuda T, Murai T, Shibata M, Matsui-Yuasa I, et al. Cancer induction by an organic arsenic compound, dimethylarsinic acid (cacodylic acid), in F344/DuCrj rats after pretreatment with five carcinogens. Cancer Res. 1995;55:1271–1276
  8. Wanibuchi H, Yamamoto S, Chen H, Yoshida K, Endo G, Hori T, et al. Promoting effects of dimethylarsinic acid on N-butyl-N-(4-hydroxybutyl) nitrosamine-induced urinary bladder carcinogenesis in rats. Carcinogenesis. 1996;17:2435–2439
  9. Wei M, Wanibuchi H, Yamamoto S, Li W, Fukushima S. Urinary bladder carcinogenicity of dimethylarsinic acid in F344 rats. Carcinogenesis. 1999;20:1873–1876
  10. Ahmad S, Kitchin KT, Cullen WR. Arsenic species that cause release of iron from ferritin and generation of activated oxygen. Arch. Biochem. Biophys. 2000;382:195–202
  11. Mass MJ, Tennant A, Roop BC, Cullen WR, Styblo M, Thomas DJ, et al. Methylated trivalent arsenics species are genotoxic. Chem. Res. Toxicol. 2001;14:355–361
  12. Yamanaka K, Mizoi M, Tachikawa M, Hasegawa A, Hoshino M, Okada S. Oxidative DNA damage following exposure to dimethylarsinous iodide: the formation of cis-thymine glycol. Toxicol. Lett. 2003;143:145–153
  13. Styblo M, Del Razo LM, Vega L, Germolec DR, LeCluyse EL, Hamilton GA, et al. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rats and human cells. Arch. Toxicol. 2000;74:289–299
  14. Yamanaka K, Hasegawa A, Sawamura R, Okada S. Dimethylated arsenics induced DNA strand breaks in lung via the production of active oxygen in mice. Biochem. Biophys. Res. Commun. 1989;165:43–50
  15. 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
  16. Yamanaka Y, Hasegawa A, Sawamura R, Okada S. Cellular response to oxidative damage in lung induced by the administration of dimethylarsinic acid, a main metabolite of inorganic arsenics, in mice. Toxicol. Appl. Pharmacol. 1991;108:205–213
  17. Kitchin KT, Ahmad S. Oxidative stress as a possible mode of action for arsenic carcinogenesis. Toxicol. Lett. 2003;137:3–13
  18. Yamanaka K, Takabayashi F, Mizoi M, An Y, Hasegawa A, Okada S. Oral exposure of dimethylarsenic acid, a main metabolite of inorganic arsenics, in mice leads to an increase in 8-oxo-2′-deoxyguanosine level, specifically in the target organs for arsenic carcinogenesis. Biochem. Biophys. Res. Commun. 2001;287:66–70
  19. Vijayaraghavan M, Wanibuchi H, Karim R, Yamamoto S, Masuda C, Nakae D, et al. Dimethylarsinic acid induces 8-hydroxy-2′-deoxyguanosine formation in the kidney of NCI-Black Reiter rats. Cancer Lett. 2001;165:11–17
  20. Wanibuchi H, Hori T, Meenakshi V, Ichihara T, Yamamoto S, Yano Y, et al. Promotion of rat hepatocarcinogenesis by dimethylarsinic acid: association with elevated ornithine decarboxylase activity and formation of 8-hydroxydeoxyguanosine in the liver. Jpn J. Cancer Res. 1997;88:1149–1154
  21. International Agency Research on Cancer . IARC monographs on the evaluation of the carcinogenic risk of chemicals to humans. Some Metals and Metallic Compounds. vol. 23. Lyon: IARC; 1980;pp. 39–141
  22. International Agency Research on Cancer . IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans, Overall Evaluations of Carcinogenicity: An Updating of IARC Monographs. Lyon: IARC; 1987;pp. 100–106
  23. Matsui M, Nishigori C, Toyokuni S, Takada J, Akaboshi M, Ishikawa M, et al. The role of oxidative DNA damage in human arsenic carcinogenesis: detection of 8-hydroxy-2′-deoxyguanosine in arsenic-related Bowen's disease. J. Invest. Dermatol. 1999;113:26–31
  24. An Y, Gao ZL, Wang ZW, Yang SH, Liang JF, Feng Y, et al. Immunohistochemical analysis of oxidative DNA damage in arsenic-related human skin samples from arsenic-contaminated area of China. Cancer Lett. 2004;214:11–18
  25. Cattoretti G, Becker MH, Key G, Duchrow M, Schluter C, Galle J, et al. Monoclonal antibodies against recombinant parts of the Ki-67 antigen (MIB 1 and MIB 3) detect proliferating cells in microwave-processed formalin-fixed paraffin sections. J. Pathol. 1992;168:357–363
  26. Muse KE, Oberley TD, Sempf JM, Oberley LW. Immunolocation of antioxidant enzymes in adult hamster kidney. Histochem. J. 1994;26:734–753
  27. Witschi H, Malkinson AM, Peraino C, Russell JJ, Staffeldt EF. Effects of glycerol on lung and liver tumor development. Fundam. Appl. Toxicol. 1989;13:174–180
  28. Cerutti P. Pro-oxidant states and tumor progression. Science. 1985;227:375–381
  29. Binder RL, Aardema MJ, Thompson ED. Benzoyl peroxide: review of experimental carcinogenesis and human safety data. Prog. Clin. Biol. Res. 1995;391:245–294
  30. Gimenez-Conti IB, Binder RL, Johnston D, Slaga TJ. Comparison of the skin tumor-promoting potential of different organic peroxides in SENCAR mice. Toxicol. Appl. Pharmacol. 1998;149:73–79
  31. Swauger JE, Dolan PM, Zweier JL, Kuppusamy P, Kensler TW. Role of the benzoyloxyl radical in DNA damage mediated by benzoyl peroxide. Chem. Res. Toxicol. 1991;4:223–228
  32. Nishikawa T, Wanibuchi H, Ogawa M, Kinoshita A, Morimura K, Hiroi T, et al. Promoting effects of monomethylarsonic acid, dimethylarsenic 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. 2002;100:136–139
  33. Green T, Toghill A, Foster JR. The role of cytochromes P-450 in styrene induced pulmonary toxicity and carcinogenicity. Toxicology. 2001;169:107–117
  34. Nesnow S, Roop BC, Lambert G, Kadiiska M, Mason RP, Cullen WR, et al. DNA damaged induced by methylated trivalent arsenicals is mediated by reactive oxygen species. Chem. Res. Toxicol. 2002;15:1627–1634
  35. Madreiter H, Osieka R, Kaden P, Rombach A, Mittermayer C. Effect of bleomycin on the fine structure of mouse fibroblasts. Z Krebsforsch. 1976;85:63–72
  36. Reynolds ES. Liver parenchymal cell injury. I Initial alterations of the cell following poisoning with carbon tetrachloride. J. Cell Biol. 1963;19:139–157

PII: S0304-3835(04)00991-7

doi: 10.1016/j.canlet.2004.12.029

Cancer Letters
Volume 230, Issue 1 , Pages 57-64 , 8 December 2005

Article Tools

* Image Usage & Resolution