Low-dose Cd induces hepatic gene hypermethylation, along with the persistent reduction of cell death and increase of cell proliferation in rats and mice

PLoS ONE

Volumn 7, Issue 3, 2012, Pages

  Wang, Bo ^a,b,c   Li, Yang ^a   Tan, Yi ^c   Miao, Xiao ^c,d   Liu, Xu Dong ^e   Shao, Chen ^a   Yang, Xiao Hui ^f   Turdi, Subat ^f   Ma, Li Jie ^e   Ren, Jun ^f   Cai, Lu ^c,g  

^a Basic Medical College   (China)

^b Inner Mongolia Forestry General Hospital   (China)

^c University of Louisville School of Medicine   (United States)

^d THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

^e INNER MONGOLIA MEDICAL COLLEGE   (China)

^f UNIVERSITY OF WYOMING   (United States)

^g UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; CADMIUM; CASPASE 8; CELL DNA; CYTOKERATIN 18; CYTOKERATIN 8; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CASPASE 8 GENE; CELL PROLIFERATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA MICROARRAY; GENE; GENOME ANALYSIS; IMMUNOPRECIPITATION; LIVER CANCER; LIVER INJURY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRECANCER; PROMOTER REGION; PROTEIN EXPRESSION; RAT; TNF GENE; ANIMAL; CELL DIVISION; DOSE RESPONSE; DRUG EFFECT; GENETICS; LIVER; METABOLISM;

MUS; RATTUS;

ANIMALS; APOPTOSIS; CADMIUM; CASPASE 8; CELL DIVISION; CELL PROLIFERATION; CPG ISLANDS; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; LIVER; MICE; PROMOTER REGIONS, GENETIC; RATS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84863338120     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0033853     Document Type: Article

References (39)

1. Waisberg M, Joseph P, Hale B, Beyersmann D, (2003) Molecular and cellular mechanisms of cadmium carcinogenesis. Toxicology 192: 95-117.
2. Takiguchi M, Achanzar WE, Qu W, Li G, Waalkes MP, (2003) Effects of cadmium on DNA-(Cytosine-5) methyltransferase activity and DNA methylation status during cadmium-induced cellular transformation. Exp Cell Res 286: 355-365.
3. Baylin SB, Herman JG, (2000) DNA hypermethylation in tumorigenesis: epigenetics joins genetics. Trends Genet 16: 168-174.
4. Yu J, Ni M, Xu J, Zhang H, Gao B, et al. (2002) Methylation profiling of twenty promoter-CpG islands of genes which may contribute to hepatocellular carcinogenesis. BMC Cancer 2: 29.
5. Lehmann U, Berg-Ribbe I, Wingen LU, Brakensiek K, Becker T, et al. (2005) Distinct methylation patterns of benign and malignant liver tumors revealed by quantitative methylation profiling. Clin Cancer Res 11: 3654-3660.
6. Teitz T, Wei T, Valentine MB, Vanin EF, Grenet J, et al. (2000) Caspase 8 is deleted or silenced preferentially in childhood neuroblastomas with amplification of MYCN. Nat Med 6: 529-535.
7. Achanzar WE, Diwan BA, Liu J, Quader ST, Webber MM, et al. (2001) Cadmium-induced malignant transformation of human prostate epithelial cells. Cancer Res 61: 455-458.
8. Qu W, Diwan BA, Reece JM, Bortner CD, Pi J, et al. (2005) Cadmium-induced malignant transformation in rat liver cells: role of aberrant oncogene expression and minimal role of oxidative stress. Int J Cancer 114: 346-355.
9. Huang D, Zhang Y, Qi Y, Chen C, Ji W, (2008) Global DNA hypomethylation, rather than reactive oxygen species (ROS), a potential facilitator of cadmium-stimulated K562 cell proliferation. Toxicol Lett 179: 43-47.
10. Wang B, Wang S, Shao C, Wang G, Li Y, et al. (2011) Proteomic characterization of the late and persistent effects of cadmium at low doses on the rat liver. Journal of Applied Toxicology Inpress.
11. Kakehashi A, Kato A, Inoue M, Ishii N, Okazaki E, et al. (2010) Cytokeratin 8/18 as a new marker of mouse liver preneoplastic lesions. Toxicol Appl Pharmacol 242: 47-55.
12. Kuo LJ, Yang LX, (2008) Gamma-H2AX- a novel biomarker for DNA double-strand breaks. In Vivo 22: 305-309.
13. Brama M, Gnessi L, Basciani S, Cerulli N, Politi L, et al. (2007) Cadmium induces mitogenic signaling in breast cancer cell by an ERalpha-dependent mechanism. Mol Cell Endocrinol 264: 102-108.
14. Feinberg AP, Ohlsson R, Henikoff S, (2006) The epigenetic progenitor origin of human cancer. Nat Rev Genet 7: 21-33.
15. Larson J, Yasmin T, Sens DA, Zhou XD, Sens MA, et al. (2010) SPARC gene expression is repressed in human urothelial cells (UROtsa) exposed to or malignantly transformed by cadmium or arsenite. Toxicol Lett 199: 166-172.
16. Jiang G, Xu L, Song S, Zhu C, Wu Q, et al. (2008) Effects of long-term low-dose cadmium exposure on genomic DNA methylation in human embryo lung fibroblast cells. Toxicology 244: 49-55.
17. Misra UK, Gawdi G, Akabani G, Pizzo SV, (2002) Cadmium-induced DNA synthesis and cell proliferation in macrophages: the role of intracellular calcium and signal transduction mechanisms. Cell Signal 14: 327-340.
18. Martinez R, Setien F, Voelter C, Casado S, Quesada MP, et al. (2007) CpG island promoter hypermethylation of the pro-apoptotic gene caspase-8 is a common hallmark of relapsed glioblastoma multiforme. Carcinogenesis 28: 1264-1268.
19. Gunawardana CG, Martinez RE, Xiao W, Templeton DM, (2006) Cadmium inhibits both intrinsic and extrinsic apoptotic pathways in renal mesangial cells. Am J Physiol Renal Physiol 290: F1074-1082.
20. Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, et al. (2002) Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology 170: 111-117.
21. Oh SH, Choi JE, Lim SC, (2006) Protection of betulin against cadmium-induced apoptosis in hepatoma cells. Toxicology 220: 1-12.
22. Shimada H, Shiao YH, Shibata M, Waalkes MP, (1998) Cadmium suppresses apoptosis induced by chromium. J Toxicol Environ Health A 54: 159-168.
23. Yuan C, Kadiiska M, Achanzar WE, Mason RP, Waalkes MP, (2000) Possible role of caspase-3 inhibition in cadmium-induced blockage of apoptosis. Toxicol Appl Pharmacol 164: 321-329.
24. Stresemann C, Brueckner B, Musch T, Stopper H, Lyko F, (2006) Functional diversity of DNA methyltransferase inhibitors in human cancer cell lines. Cancer Res 66: 2794-2800.
25. Hashimoto E, Tokushige K, (2012) Hepatocellular carcinoma in non-alcoholic steatohepatitis: Growing evidence of an epidemic? Hepatol Res 42: 1-14.
26. Denda A, Kitayama W, Kishida H, Murata N, Tsutsumi M, et al. (2002) Development of hepatocellular adenomas and carcinomas associated with fibrosis in C57BL/6J male mice given a choline-deficient, L-amino acid-defined diet. Jpn J Cancer Res 93: 125-132.
27. Wang B, Majumder S, Nuovo G, Kutay H, Volinia S, et al. (2009) Role of microRNA-155 at early stages of hepatocarcinogenesis induced by choline-deficient and amino acid-defined diet in C57BL/6 mice. Hepatology 50: 1152-1161.
28. Hill-Baskin AE, Markiewski MM, Buchner DA, Shao H, DeSantis D, et al. (2009) Diet-induced hepatocellular carcinoma in genetically predisposed mice. Hum Mol Genet 18: 2975-2988.
29. Matsuzaki K, Murata M, Yoshida K, Sekimoto G, Uemura Y, et al. (2007) Chronic inflammation associated with hepatitis C virus infection perturbs hepatic transforming growth factor beta signaling, promoting cirrhosis and hepatocellular carcinoma. Hepatology 46: 48-57.
30. Inman GJ, (2011) Switching TGFbeta from a tumor suppressor to a tumor promoter. Curr Opin Genet Dev 21: 93-99.
31. Kakehashi A, Inoue M, Wei M, Fukushima S, Wanibuchi H, (2009) Cytokeratin 8/18 overexpression and complex formation as an indicator of GST-P positive foci transformation into hepatocellular carcinomas. Toxicol Appl Pharmacol 238: 71-79.
32. Kawai M, Saegusa Y, Kemmochi S, Harada T, Shimamoto K, et al. (2010) Cytokeratin 8/18 is a useful immunohistochemical marker for hepatocellular proliferative lesions in mice. J Vet Med Sci 72: 263-269.
33. Kawai M, Saegusa Y, Dewa Y, Nishimura J, Kemmochi S, et al. (2010) Elevation of cell proliferation via generation of reactive oxygen species by piperonyl butoxide contributes to its liver tumor-promoting effects in mice. Arch Toxicol 84: 155-164.
34. Yamashiro Y, Takei K, Umikawa M, Asato T, Oshiro M, et al. (2010) Ectopic coexpression of keratin 8 and 18 promotes invasion of transformed keratinocytes and is induced in patients with cutaneous squamous cell carcinoma. Biochem Biophys Res Commun 399: 365-372.
35. Kabukcuoglu S, Ozalp SS, Yalcin OT, Colak E, Abubakar AA, (2010) Comparison of histopathologic classification and surgical stage by cytokeratin 8 and cytokeratin 18 in endometrial cancer. Eur J Gynaecol Oncol 31: 641-644.
36. Waalkes MP, Rehm S, Riggs CW, Bare RM, Devor DE, et al. (1988) Cadmium carcinogenesis in male Wistar [Crl:(WI)BR] rats: dose-response analysis of tumor induction in the prostate and testes and at the injection site. Cancer Res 48: 4656-4663.
37. Maitani T, Suzuki KT, (1986) Effect of cadmium on essential metal concentrations in testis, liver and kidney of five inbred strains of mice. Toxicology 42: 121-130.
38. Hanigan MH, Winkler ML, Drinkwater NR, (1990) Partial hepatectomy is a promoter of hepatocarcinogenesis in C57BL/6J male mice but not in C3H/HeJ male mice. Carcinogenesis 11: 589-594.
39. Pelizzola M, Koga Y, Urban AE, Krauthammer M, Weissman S, et al. (2008) MEDME: an experimental and analytical methodology for the estimation of DNA methylation levels based on microarray derived MeDIP-enrichment. Genome Res 18: 1652-1659.