Low doses of the carcinogen furan alter cell cycle and apoptosis gene expression in rat liver independent of DNA methylation

Environmental Health Perspectives

Volumn 118, Issue 11, 2010, Pages 1597-1602

  Chen, Tao ^a   Mally, Angela ^b   Ozden, Sibel ^b,c   Chipman, J Kevin ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c ISTANBUL UNIVERSITY   (Turkey)

Author keywords

Carcinogenicity; DNA methylation; Epigenetic; Furan; Gene expression; Liver; Mirna

Indexed keywords

FURAN; MICRORNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BILE DUCT CARCINOMA; CARCINOGENICITY; CELL CYCLE; CONTROLLED STUDY; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; FEMALE; GENE EXPRESSION; LIVER CARCINOGENESIS; MALE; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; APOPTOSIS; CARCINOGENS, ENVIRONMENTAL; CELL CYCLE; DNA METHYLATION; DOSE-RESPONSE RELATIONSHIP, DRUG; FURANS; GENE EXPRESSION; LIVER; MALE; MICRORNAS; RATS; RATS, INBRED F344; RNA, MESSENGER;

RATTUS; RODENTIA;

EID: 78149345723     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002153     Document Type: Article

References (45)

1. Ambros V. 2004. The functions of animal microRNAs. Nature 431(7006):350-355.
2. Asada K, Kotake Y, Asada R, Saunders D, Broyles RH, Towner RA, et al. 2006. LINE-1 hypomethylation in a choline-deficiency-induced liver cancer in rats: dependence on feeding period. J Biomed Biotechnol 2006(1):17142; doi:10.1155/JBB/2006/17142.
3. Bachman AN, Phillips JM, Goodman JI. 2006. Phenobarbital induces progressive patterns of GC-rich and gene-specific altered DNA methylation in the liver of tumor-prone B6C3F1 mice. Toxicol Sci 91(2):393-405.
4. Barh D, Parida S, Parida BP, Viswanathan G. 2008. Let-7, miR-125, miR-205, and miR-296 are prospective therapeutic agents in breast cancer molecular medicine. Gene Ther Mol Biol 12:189-206.
5. Bartel DP. 2004. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116(2):281-297.
6. Bombail V, Moggs JG, Orphanides G. 2004. Perturbation of epigenetic status by toxicants. Toxicol Lett 149(1-3):51-58.
7. Boyerinas B, Park SM, Hau A, Murmann AE, Peter ME. 2010. The role of let-7 in cell differentiation and cancer. Endocr Relat Cancer 17(1):F19-F36.
8. Burka LT, Washburn KD, Irwin RD. 1991. Disposition of [14C]furan in the male F344 rat. J Toxicol Environ Health 34(2):245-257.
9. Byrns MC, Vu CC, Neidigh JW, Abad JL, Jones RA, Peterson LA. 2006. Detection of DNA adducts derived from the reactive metabolite of furan, cis-2-butene-1,4-dial. Chem Res Toxicol 19(3):414-420.
10. Chen L, Yan HX, Yang W, Hu L, Yu LX, Liu Q, et al. 2009. The role of microRNA expression pattern in human intrahepatic cholangiocarcinoma. J Hepatol 50(2):358-369.
11. Chen XM. 2009. MicroRNA signatures in liver diseases. World J Gastroenterol 15(14):1665-1672.
12. Cheng AM, Byrom MW, Shelton J, Ford LP. 2005. Antisense inhibition of human miRNAs and indications for an involvement of miRNA in cell growth and apoptosis. Nucleic Acids Res 33(4):1290-1297.
13. Corbetta S, Vaira V, Guarnieri V, Scillitani A, Eller-Vainicher C, Ferrero S, et al. 2010. Differential expression of microRNAs in human parathyroid carcinomas compared with normal parathyroid tissue. Endocr Relat Cancer 17(1):135-146.
14. Del Senno L, Maestri I, Piva R, Hanau S, Reggiani A, Romano A, et al. 1989. Differential hypomethylation of the c-myc protooncogene in bladder cancers at different stages and grades. J Urol 142(1):146-149.
15. Durling LJ, Svensson K, Abramsson-Zetterberg L. 2007. Furan is not genotoxic in the micronucleus assay in vivo or in vitro. Toxicol Lett 169(1):43-50.
16. Ellinger-Ziegelbauer H, Stuart B, Wahle B, Bomann W, Ahr HJ. 2005. Comparison of the expression profiles induced by genotoxic and nongenotoxic carcinogens in rat liver. Mutat Res 575(1-2):61-84.
17. European Food Safety Authority. 2004. Report of the Scientific Panel on Contaminants in the Food Chain on provisional findings on furan in food. EFSA J 137:1-20.
18. European Molecular Biology Laboratory, European Bioinformatics Institute. 2010. MicroCosm Targets Version 5. Available: http://www.ebi.ac.uk/enright-srv/microcosm/htdocs/targets/v5/ [accessed 22 September 2010].
19. Food and Drug Administration. 2004. Exploratory Data on Furan in Food. Available: http://www.fda.gov/ohrms/dockets/ac/04/briefing/4045b2_09_furan%20data.p df [accessed 22 September 2010].
20. Fransson-Steen R, Goldsworthy TL, Kedderis GL, Maronpot RR. 1997. Furan-induced liver cell proliferation and apoptosis in female B6C3F1 mice. Toxicology 118(2-3):195-204.
21. Guled M, Lahti L, Lindholm PM, Salmenkivi K, Bagwan I, Nicholson AG, et al. 2009. CDKN2A, NF2, and JUN are dysregulated among other genes by miRNAs in malignant mesothelioma-A miRNA microarray analysis. Genes, Chromosomes Cancer 48(7):615-623.
22. Hamadeh HK, Jayadev S, Gaillard ET, Huang Q, Stoll R, Blanchard K, et al. 2004. Integration of clinical and gene expression endpoints to explore furan-mediated hepatotoxicity. Mutat Res 549(1-2):169-183.
23. Hickling KC, Hitchcock JM, Oreffo V, Mally A, Hammond TG, Evans JG, et al. 2010 Evidence of oxidative stress and associated DNA damage, increased proliferative drive, and altered gene expression in rat liver produced by the cholangiocarcinogenic agent furan. Toxicol Pathol 38(2):230-243.
24. JECFA (Joint Food and Agriculture Organization/World Health Organization Expert Committee on Food Additives). 2010. Joint Fao/Who Expert Committee on Food Additives Seventy-second Meeting, Rome, 16-25 February 2010: Summary and Conclusions. Available: http://www.who.int/foodsafety/chem/summary72_rev.pdf [accessed 18 April 2010].
25. +/- mouse lymphoma cells. Mut Res 657:127-127.
26. Kim HH, Park JH, Jeong KS, Lee S. 2007. Determining the global DNA methylation status of rat according to the identifier repetitive elements. Electrophoresis 28(21):3854-3861.
27. Lee S, Kim WH, Jung HY, Yang MH, Kang GH. 2002. Aberrant CpG island methylation of multiple genes in intrahepatic cholangiocarcinoma. Am J Pathol 161(3):1015-1022.
28. Leopardi P, Cordelli E, Villani P, Cremona TP, Conti L, De Luca G, et al. 2010. Assessment of in vivo genotoxicity of the rodent carcinogen furan: evaluation of DNA damage and induction of micronuclei in mouse splenocytes. Mutagenesis 25(1):57-62.
29. Mally A, Graff C, Schmal O, Moro S, Hamberger C, Schauer UM. 2010. Functional and proliferative effects of repeated low-dose oral administration of furan in rat liver. Mol Nutr Food Res; doi:10.1002/mnfr.201000064 [Online 10 June 2010].
30. Manoharan H, Babcock K, Pitot HC. 2004. Changes in the DNA methylation profile of the rat H19 gene upstream region during development and transgenic hepatocarcinogenesis and its role in the imprinted transcriptional regulation of the H19 gene. Mol Carcinog 41(1):1-16.
31. Maronpot RR, Giles HD, Dykes DJ, Irwin RD. 1991. Furan-induced hepatic cholangiocarcinomas in Fischer 344 rats. Toxicol Pathol 19(4 Pt 2):561-570.
32. Megraw M, Sethupathy P, Corda B, Hatzigeorgiou AG. 2007. MiRGen: a database for the study of animal microRNA genomic organization and function. Nucleic Acids Res 35(suppl 1):D149-D155.
33. Mortelmans K, Haworth S, Lawlor T, Speck W, Tainer B, Zeiger E. 1986. Salmonella mutagenicity tests: II. Results from the testing of 270 chemicals. Environ Mutagen 8(suppl 7):1-119.
34. Mugford CA, Carfagna MA, Kedderis GL. 1997. Furan-mediated uncoupling of hepatic oxidative phosphorylation in Fischer-344 rats: an early event in cell death. Toxicol Appl Pharmacol 144(1):1-11.
35. NTP (National Toxicology Program). 1993. Toxicology and Carcinogenesis Studies of Furan (CAS No. 110-00-9) in F344 Rats and B6C3F1 Mice (Gavage Studies). Technical Report 402. Research Triangle Park, NC:National Toxicology Program. Available: http://ntp.niehs.nih.gov/ntp/htdocs/LT_rpts/tr402.pdf [accessed 23 September 2010].
36. NTP (National Toxicology Program). 2008. NTP Research Concept: Furan. Available: http://ntp.niehs.nih.gov/ntp/Noms/Final_ResConcept/furan.pdf [accessed 23 September 2010].
37. Özden S, Chen T, Dekant W, Chipman K, Mally A. 2008. Alteration in global DNA methylation as an early event in non-genotoxic carcinogenesis [Abstract]. Toxicol Lett 180(suppl 1):S55.
38. Phillips JM, Goodman JI. 2009. Multiple genes exhibit phenobarbital-induced constitutive active/androstane receptor-mediated DNA methylation changes during liver tumorigenesis and in liver tumors. Toxicol Sci 108(2):273-289.
39. Sandhu DS, Shire AM, Roberts LR. 2008. Epigenetic DNA hypermethylation in cholangiocarcinoma: potential roles in pathogenesis, diagnosis and identification of treatment targets. Liver Int 28(1):12-27.
40. Szyf M. 2007. The dynamic epigenome and its implications in toxicology. Toxicol Sci 100:7-23.
41. Tao L, Li Y, Wang W, Kramer PM, Gunning WT, Lubet RA, et al. 2002. Effect of budesonide on the methylation and mRNA expression of the insulin-like growth factor 2 and c-myc genes in mouse lung tumors. Mol Carcinog 35(2):93-102.
42. Tsujiuchi T, Tsutsumi M, Sasaki Y, Takahama M, Konishi Y. 1999. Hypomethylation of CpG sites and c-myc gene overexpression in hepatocellular carcinomas, but not hyperplastic nodules, induced by a choline-deficient l-amino acid-defined diet in rats. Jpn J Cancer Res 90(9):909-913.
43. Umemura T, Kai S, Hasegawa R, Sai K, Kurokawa Y, Williams GM. 1999. Pentachlorophenol (PCP) produces liver oxidative stress and promotes but does not initiate hepatocarcinogenesis in B6C3F1 mice. Carcinogenesis 20(6):1115-1120.
44. Wilson DM, Goldsworthy TL, Popp JA, Butterworth BE. 1992. Evaluation of genotoxicity, pathological lesions, and cell proliferation in livers of rats and mice treated with furan. Environ Mol Mutagen 19(3):209-222.
45. Yang B, House MG, Guo M, Herman JG, Clark DP. 2005. Promoter methylation profiles of tumor suppressor genes in intrahepatic and extrahepatic cholangiocarcinoma. Mod Pathol 18(3):412-420.