Comparison of genotoxicant-modified transcriptomic responses in conventional and epigenetically stabilized primary rat hepatocytes with in vivo rat liver data

Archives of Toxicology

Volumn 86, Issue 11, 2012, Pages 1703-1715

  Doktorova, Tatyana Y ^a   Ellinger Ziegelbauer, Heidrun ^b   Vinken, Mathieu ^a   Vanhaecke, Tamara ^a   Van Delft, Joost ^c   Kleinjans, Jos ^c   Ahr, Hans Juergen ^b   Rogiers, Vera ^a  

^a VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^b BAYER PHARMA AG   (Germany)

^c MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Genotoxic carcinogens; Global gene expression profiling; In vitro in vivo relevance

Indexed keywords

2 NITROFLUORENE; 4 (METHYLNITROSAMINO) 1 (3 PYRIDYL) 1 BUTANONE; AFLATOXIN B1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DETOXIFICATION; DNA DAMAGE; GENE EXPRESSION PROFILING; GENETIC EPIGENESIS; GENOTOXICITY; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER TOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; TRANSCRIPTOMICS;

AFLATOXIN B1; ANIMALS; CARCINOGENS; CELLS, CULTURED; DNA DAMAGE; EPIGENESIS, GENETIC; FLUORENES; GENE EXPRESSION PROFILING; HEPATOCYTES; MALE; MUTAGENICITY TESTS; MUTAGENS; NITROSAMINES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; RATS; RATS, WISTAR; TOXICOGENETICS;

RATTUS;

EID: 84871257721     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-012-0946-8     Document Type: Article

References (39)

1. Andersen ME, Krewski D (2010) The vision of toxicity testing in the 21st century: moving from discussion to action. Toxicol Sci 117(1):17-24.
2. Balls M, Amcoff P, Bremer S, Casati S, Coecke S, Clothier R, Combes R, Corvi R, Curren R, Eskes C, Fentem J, Gribaldo L, Halder M, Hartung T, Hoffmann S, Schectman L, Scott L, Spielmann H, Stokes W, Tice R, Wagner D, Zuang V (2006) The principles of weight of evidence validation of test methods and testing strategies. The report and recommendations of ECVAM workshop 58. Altern Lab Anim 34(6):603-620.
3. Boess F, Kamber M, Romer S, Gasser R, Muller D, Albertini S, Suter L (2003) Gene expression in two hepatic cell lines, cultured primary hepatocytes, and liver slices compared to the in vivo liver gene expression in rats: possible implications for toxicogenomics use of in vitro systems. Toxicol Sci 73(2):386-402.
4. Ceelen L, De Spiegelaere W, David M, De Craene J, Vinken M, Vanhaecke T, Rogiers V (2011) Critical selection of reliable reference genes for gene expression study in the HepaRG cell line. Biochem Pharmacol 81(10):1255-1261.
5. Diaz GJ, Murcia HW, Cepeda SM, Boermans HJ (2010) The role of selected cytochrome P450 enzymes on the bioactivation of aflatoxin B1 by duck liver microsomes. Avian Pathol 39(4): 279-285.
6. Elaut G, Henkens T, Papeleu P, Snykers S, Vinken M, Vanhaecke T, Rogiers V (2006) Molecular mechanism underlying the dedifferentiation process of isolated hepatocytes and their cultures. Curr Drug Metab 7:629-660.
7. Elaut G, Laus G, Alexandre E, Richert L, Bachellier P, Tourwe D, Rogiers V, Vanhaecke T (2007) A metabolic screening study of trichostatin A (TSA) and TSA-like histone deacetylase inhibitors in rat and human primary hepatocyte cultures. J Pharmacol Exp Ther 321(1):400-408.
8. Ellinger-Ziegelbauer H, Stuart B, Wahle B, Bomann W, Ahr HJ (2004) Characteristic expression profiles induced by genotoxic carcinogens in rat liver. Toxicol Sci 77(1):19-34.
9. 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.
10. EU (2003) Directive 2003/15/EC of the European parliament and of the council of 27 February 2003 amending Council directive76/768/EEC on the approximation of the laws of the member states relating to cosmetic products. L066:26-35
11. EU (2006) Regulation (EC) No 1907/2006 of the European Parliament and of the Council of 18 December 2006 concerning the Registration, Evaluation, Authorization and Restriction of Chemicals (REACH), establishing a European Chemicals Agency, amending Directive 1999/45/EC and repealing Council Regulation (EEC) No 793/93 and Commission Regulation (EC) No 1488/94 as well as Council Directive 76/769/EEC and Commission Directives 91/155/EEC, 93/67/EEC, 93/105/EC and 2000/21/EC. Off J L396:1-849.
12. Gao A, Zuo X, Song S, Guo W, Tian L (2011) Epigenetic modification involved in benzene-induced apoptosis through regulating apoptosis-related genes expression. Cell Biol Int 35(4):391-396.
13. Goldin BR (1990) Intestinal microflora: metabolism of drugs and carcinogens. Ann Med 22(1):43-48.
14. Henkens T, Papeleu P, Elaut G, Vinken M, Rogiers V, Vanhaecke T (2007) Trichostatin A, a critical factor in maintaining the functional differentiation of primary cultured rat hepatocytes. Toxicol Appl Pharmacol 218(1):64-71.
15. Jalas JR, Ding X, Murphy SE (2003) Comparative metabolism of the tobacco-specific nitrosamines 4-(methylnitrosamino)-1-(3-pyridyl)- 1-butanone and 4-(methylnitrosamino)-1-(3-pyridyl)-1- butanol by rat cytochrome P450 2A3 and human cytochrome P450 2A13. Drug Metab Dispos Biol Fate Chem 31(10): 1199-1202.
16. Jennen DG, Magkoufopoulou C, Ketelslegers HB, van Herwijnen MH, Kleinjans JC, van Delft JH (2010) Comparison of HepG2 and HepaRG by whole-genome gene expression analysis for the purpose of chemical hazard identification. Toxicol Sci 115(1):66-79.
17. Kirkland D, Aardema M, Henderson L, Muller L (2005) Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens I. Sensitivity, specificity and relative predictivity. Mutat Res 584(1-2): 1-256.
18. Lee JH, Choy ML, Ngo L, Foster SS, Marks PA (2010) Histone deacetylase inhibitor induces DNA damage, which normal but not transformed cells can repair. Proc Nat Acad Sci USA 107(33):14639-14644.
19. Matsumoto H, Yakabe Y, Saito K, Sumida K, Sekijima M, Nakayama K, Miyaura H, Saito F, Otsuka M, Shirai T (2009) Discrimination of carcinogens by hepatic transcript profiling in rats following 28-day administration. Cancer inform 7:253-269.
20. Moller L (1994) In vivo metabolism and genotoxic effects of nitrated polycyclic aromatic hydrocarbons. Environ Health Perspect 102(Suppl 4):139-146.
21. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65(1-2):55-63.
22. Nakayama K, Kawano Y, Kawakami Y, Moriwaki N, Sekijima M, Otsuka M, Yakabe Y, Miyaura H, Saito K, Sumida K, Shirai T (2006) Differences in gene expression profiles in the liver between carcinogenic and non-carcinogenic isomers of compounds given to rats in a 28-day repeat-dose toxicity study. Toxicol Appl Pharmacol 217(3):299-307.
23. Papeleu P, Loyer P, Vanhaecke T, Elaut G, Geerts A, Guguen- Guillouzo C, Rogiers V (2003) Trichostatin A induces differential cell cycle arrests but does not induce apoptosis in primary cultures of mitogen-stimulated rat hepatocytes. J Hepatol 39(3):374-382.
24. Papeleu P, Vanhaecke T, Henkens T, Elaut G, Vinken M, Snykers S, Rogiers V (2006) Isolation of rat hepatocytes. Methods Mol Biol 320:229-237.
25. Poirier MC (2004) Chemical-induced DNA damage and human cancer risk. Nat Rev 4(8):630-637.
26. Roth A, Boess F, Landes C, Steiner G, Freichel C, Plancher JM, Raab S, de Vera Mudry C, Weiser T, Suter L (2011) Gene expressionbased in vivo and in vitro prediction of liver toxicity allows compound selection at an early stage of drug development. J Biochem Mol Toxicol 25(3):183-194.
27. Russell WMS, Burch RL (1959) The principle of humane experimental technique. Methuen and Co Ltd., London.
28. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3(6):1101-1108.
29. Schug M, Heise T, Bauer A, Storm D, Blaszkewicz M, Bedawy E, Brulport M, Geppert B, Hermes M, Follmann W, Rapp K, Maccoux L, Schormann W, Appel KE, Oberemm A, Gundert- Remy U, Hengstler JG (2008) Primary rat hepatocytes as in vitro system for gene expression studies: comparison of sandwich, Matrigel and 2D cultures. Arch Toxicol 82(12):923-931.
30. Thomas RS, Pluta L, Yang L, Halsey TA (2007) Application of genomic biomarkers to predict increased lung tumor incidence in 2-year rodent cancer bioassays. Toxicol Sci 97(1):55-64.
31. Tsujimura K, Asamoto M, Suzuki S, Hokaiwado N, Ogawa K, Shirai T (2006) Prediction of carcinogenic potential by a toxicogenomic approach using rat hepatoma cells. Cancer Sci 97(10): 1002-1010.
32. Ueda O, Kitamura S, Kubo R, Yano Y, Kanzaki Y, Fujimoto T, Tatsumi K, Ohta S (2001) Metabolism of 2-nitrofluorene, 2-aminofluorene and 2-acylaminofluorenes in rat and dog and the role of intestinal bacteria. Xenobiotica Fate Foreign Compd Biol Syst 31(1):33-49.
33. van Delft JH, Mathijs K, Staal YC, van Herwijnen MH, Brauers KJ, Boorsma A, Kleinjans JC (2010) Time series analysis of benzo[A]pyrene-induced transcriptome changes suggests that a network of transcription factors regulates the effects on functional gene sets. Toxicol Sci 117(2):381-392.
34. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of realtime quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7):34.
35. Vanhaecke T, Henkens T, Kass GE, Rogiers V (2004a) Effect of the histone deacetylase inhibitor trichostatin A on spontaneous apoptosis in various types of adult rat hepatocyte cultures. Biochem Pharmacol 68(4):753-760.
36. Vanhaecke T, Papeleu P, Elaut G, Rogiers V (2004b) Trichostatin A-like hydroxamate histone deacetylase inhibitors as therapeutic agents: toxicological point of view. Curr Med Chem 11(12): 1629-1643.
37. Vinken M, Henkens T, Vanhaecke T, Papeleu P, Geerts A, Van Rossen E, Chipman JK, Meda P, Rogiers V (2006) Trichostatin a enhances gap junctional intercellular communication in primary cultures of adult rat hepatocytes. Toxicol Sci 91(2):484-492.
38. Yoshikawa M, Hishikawa K, Idei M, Fujita T (2010) Trichostatin a prevents TGF-beta1-induced apoptosis by inhibiting ERK activation in human renal tubular epithelial cells. Eur J Pharmacol 642(1-3):28-36.
39. Zhang Y, Yu G, Wang D, Hu Y, Lei W (2011) ERK1/2 activation plays important roles in the opposite effects of Trichostatin A in non-cancer and cancer cells. Toxicon 57(6):932-937.