Aberrant DNA methylation and gene expression in livers of newborn mice transplacentally exposed to a hepatocarcinogenic dose of inorganic arsenic

Toxicology

Volumn 236, Issue 1-2, 2007, Pages 7-15

  Xie, Yaxiong ^a   Liu, Jie ^a   Benbrahim Tallaa, Lamia ^a   Ward, Jerry M ^b   Logsdon, Daniel ^c   Diwan, Bhalchandra A ^d   Waalkes, Michael P ^a  

^a National Cancer Institute   (United States)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

^d SAIC FREDERICK INC   (United States)

Author keywords

Arsenic; DNA methylation; Gene expression; Newborn mouse liver; Transplacental exposure

Indexed keywords

ARSENIC; BETAINE HOMOCYSTEINE METHYLTRANSFERASE; CYCLIN DEPENDENT KINASE INHIBITOR; CYTOCHROME P450; GLUTATHIONE; HEAT SHOCK PROTEIN; METALLOTHIONEIN I; METHYLTRANSFERASE; SOMATOMEDIN; THIOETHER METHYLTRANSFERASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA METHYLATION; GENE EXPRESSION; GESTATION PERIOD; LIVER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; MALE; MICROARRAY ANALYSIS; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; PLACENTAL TRANSFER; PRENATAL EXPOSURE; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; ARSENIC; CARCINOGENS; DNA METHYLATION; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; LIVER; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C3H; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PREGNANCY;

MUS;

EID: 34248658848     PISSN: 0300483X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tox.2007.03.021     Document Type: Article

References (39)

1. Anderson L.M., Diwan B.A., Fear N.T., and Roman E. Critical windows of exposure for children's health: cancer in human epidemiological studies and neoplasms in experimental animal models. Environ. Health Perspect. 108 Suppl. 3 (2000) 573-594
2. Aposhian H.V., and Aposhian M.M. Arsenic toxicology: five questions. Chem. Res. Toxicol. 19 (2006) 1-15
3. Baylin S.B., Herman J.G., Graff J.R., Vertino P.M., and Issa J.P. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 72 (1998) 141-196
4. Centeno J.A., Mullick F.G., Martinez L., Page N.P., Gibb H., Longfellow D., Thompson C., and Ladich E.R. Pathology related to chronic arsenic exposure. Environ. Health Perspect. 110 Suppl. 5 (2002) 883-886
5. Chanda S., Dasgupta U.B., Guhamazumder D., Gupta M., Chaudhuri U., Lahiri S., Das S., Ghosh N., and Chatterjee D. DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy. Toxicol. Sci. 89 (2006) 431-437
6. Chen C.J., Yu M.W., and Liaw Y.F. Epidemiological characteristics and risk factors of hepatocellular carcinoma. J. Gastroenterol. Hepatol. 12 (1997) S294-S308
7. Chen H., Li S., Liu J., Diwan B.A., Barrett J.C., and Waalkes M.P. Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: implications for arsenic hepatocarcinogenesis. Carcinogenesis 25 (2004) 1779-1786
8. Chiou H.Y., Hsueh Y.M., Hsieh L.L., Hsu L.I., Hsu Y.H., Hsieh F.I., et al. Arsenic methylation capacity, body retention, and null genotypes of glutathione S-transferase M1 and T1 among current arsenic-exposed residents in Taiwan. Mutat. Res. 386 (1997) 197-207
9. Cook J.D., Davis B.J., Cai S.L., Barrett J.C., Conti C.J., and Walker C.L. Interaction between genetic susceptibility and early life environmental exposure determines tumor suppressor gene penetrance. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 8644-8649
10. Counts J.L., McClain R.M., and Goodman J.I. Comparison of effect of tumor promoter treatments on DNA methylation status and gene expression in B6C3F1 and C57BL/6 mouse liver and in B6C3F1 mouse liver tumors. Mol. Carcinog. 18 (1997) 97-106
11. Devesa V., Adair B.M., Liu J., Waalkes M.P., Diwan B.A., Styblo M., and Thomas D.J. Speciation of arsenic in the maternal and fetal mouse tissues following gestational exposure to arsenite. Toxicology 224 (2006) 147-155
12. Gielen S.C., Hanekamp E.E., Blok L.J., Huikeshoven F.J., and Burger C.W. Steroid-modulated proliferation of human endometrial carcinoma cell lines: any role for insulin-like growth factor signaling?. J. Soc. Gynecol. Investig. 12 (2005) 58-64
13. Goodman J.I., and Watson R.E. Altered DNA methylation: a secondary mechanism involved in carcinogenesis. Annu. Rev. Pharmacol. Toxicol. 42 (2002) 501-525
14. IARC (International Agency for Research on Cancer). IARC monographs on the evaluation of carcinogenic risks to humans, vol. 84: arsenic in drinking water. Some Drinking Water Disinfectants and Contaminants, Including Arsenic (2004), IARC, Lyon, France pp. 269-477
15. Leslie E.M., Haimeur A., and Waalkes M.P. Arsenic transport by the human multidrug resistance protein 1 (MRP1/ABCC1). Evidence that a tri-glutathione conjugate is required. J. Biol. Chem. 279 (2004) 32700-32708
16. Liu J., Chen H., Miller D.S., Saavedra J.E., Keefer L.K., Johnson D.R., Klaassen C.D., and Waalkes M.P. Overexpression of glutathione S-transferase II and multidrug resistance transport proteins is associated with acquired tolerance to inorganic arsenic. Mol. Pharmacol. 60 (2001) 302-309
17. Liu J., Xie Y., Ward J.M., Diwan B.A., and Waalkes M.P. Toxicogenomic analysis of aberrant gene expression in liver tumors and nontumorous livers of adult mice exposed in utero to inorganic arsenic. Toxicol. Sci. 77 (2004) 249-257
18. Liu J., Xie Y., Ducharme D.M.K., Shen J., Diwan B.A., Merrick B.A., Grissom S.F., Tucker C.J., Paules P.S., Tennant R., and Waalkes M.P. Global gene expression associated with hepatocarcinogenesis in adult male mice induced by in utero arsenic exposure. Environ. Health Perspect. 114 (2006) 404-411
19. Liu, J., Xie, Y., Cooper, R., Ducharme, D.M.K., Tennant, R., Diwan, B.A., 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., in press.
20. Lu T., Liu J., LeCluyse E.L., Zhou Y.S., Cheng M.L., and Waalkes M.P. Application of cDNA microarray to the study of arsenic-induced liver diseases in the population of Guizhou, China. Toxicol. Sci. 59 (2001) 185-192
21. Marnell L.L., Garcia-Vargas G.G., Chowdhury U.K., Zakharyan R.A., Walsh B., Avram M.D., Kopplin M.J., Cebrian M.E., Silbergeld E.K., and Aposhian H.V. Polymorphisms in the human monomethylarsonic acid (MMA(V)) reductase/hGSTO1 gene and changes in urinary arsenic profiles. Chem. Res. Toxicol. 16 (2003) 1507-1513
22. Mazumder D.N. Effect of chronic intake of arsenic-contaminated water on liver. Toxicol. Appl. Pharmacol. 206 (2005) 169-175
23. NRC (National Research Council). Arsenic in the Drinking Water (Update) (2001), NRC, National Academy, Washington, DC pp. 1-225
24. Okoji R.S., Yu R.C., Maronpot R.R., and Froines J.R. Sodium arsenite administration via drinking water increases genome-wide and Ha-ras DNA hypomethylation in methyl-deficient C57BL/6J mice. Carcinogenesis 23 (2002) 777-785
25. Pi J., Yamauchi H., Kumagai Y., Sun G., Yoshida T., Aikawa H., Hopenhayn-Rich C., and Shimojo N. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environ. Health Perspect. 110 (2002) 331-336
26. Shen J., Liu J., Xie Y., Diwan B.A., and Waalkes M.P. Fetal onset of aberrant gene expression relevant to pulmonary carcinogenesis in lung adenocarcinoma development induced by in utero arsenic exposure. Toxicol. Sci. 95 (2007) 313-320
27. Smith A.H., Marshall G., Yuan Y., Ferreccio C., Liaw J., von Ehrenstein O., Steinmaus C., Bates M.N., and Selvin S. Increased mortality from lung cancer and bronchiectasis in young adults after exposure to arsenic in utero and in early childhood. Environ. Health Perspect. 114 (2006) 1293-1296
28. Steele W., Allegrucci C., Singh R., Lucas E., Priddle H., Denning C., Sinclair K., and Young L. Human embryonic stem cell methyl cycle enzyme expression: modelling epigenetic programming in assisted reproduction?. Reprod. Biomed. Online 10 (2005) 755-766
29. Thomas, D.J., Li, J., Waters, S.B., Styblo, M., 2007. Arsenic (+3 oxidation state) methyltransferase and the methylation of arsenicals. Exp. Biol. Med., in press.
30. Waalkes M.P., Ward J.M., Liu J., and Diwan B.A. Transplacental carcinogenicity of inorganic arsenic in the drinking water: induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol. Appl. Pharmacol. 186 (2003) 7-17
31. Waalkes M.P., Ward J.M., and Diwan B.A. 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 (2004) 133-141
32. Waalkes M.P., Liu J., Chen H., Xie Y., Achanzar W.E., Zhou Y.S., Cheng M.L., and Diwan B.A. Estrogen signaling in livers of male mice with hepatocellular carcinoma induced by exposure to arsenic in utero. J. Natl. Cancer Inst. 96 (2004) 466-474
33. Waalkes M.P., Liu J., Ward J.M., Powell D.A., and Diwan B.A. Urogenital system cancers in female CD1 mice induced by in utero arsenic exposure are exacerbated by postnatal diethylstilbestrol treatment. Cancer Res. 66 (2006) 1337-1445
34. Waalkes M.P., Liu J., Ward J.M., and Diwan B.A. Enhanced urinary bladder and liver carcinogenesis in male CD1 mice exposed to transplacental inorganic arsenic and postnatal diethylstilbestrol or tamoxifen. Toxicol. Appl. Pharmacol. 215 (2006) 295-305
35. Waalkes, M.P., Liu, J., Diwan, B.A., 2007. Transplacental arsenic carcinogenesis in mice. Toxicol. Appl. Pharmacol. January 12, 2007 [Epub ahead of print].
36. Watson R.E., Curtin G.M., Doolittle D.J., and Goodman J.I. Progressive alterations in global and GC-rich DNA methylation during tumorigenesis. Toxicol. Sci. 75 (2003) 289-299
37. Xie Y., Trouba K.J., Liu J., Waalkes M.P., and Germolec D.R. 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 (2004) 1255-1263
38. Zhao C.Q., Young M.R., Diwan B.A., Coogan T.P., and Waalkes M.P. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 10907-10912
39. Zhou Y.S., Du H., Cheng M.-L., Liu J., Zhang X.J., and Xu L. The investigation of death from diseases caused by coal-burning type of arsenic poisoning. Chin. J. Endemiol. 21 (2002) 448-484