Benzo[a]pyrene-induced transcriptomic responses in primary hepatocytes and in vivo liver: Toxicokinetics is essential for in vivo-in vitro comparisons

Archives of Toxicology

Volumn 87, Issue 3, 2013, Pages 505-515

  Van Kesteren, P C E ^a,b   Zwart, P E ^a   Schaap, M M ^a,c   Pronk, T E ^a,b   Van Herwijnen, M H M ^b   Kleinjans, J C S ^b   Bokkers, B G H ^a   Godschalk, R W L ^d   Zeilmaker, M J ^a   Van Steeg, H ^a,c   Luijten, M ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Benzo a pyrene; Carcinogenesis; Physiologically based kinetic modeling; Toxicogenomics; Xpa p53 +

Indexed keywords

BENZO[A]PYRENE; PROTEIN P53; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CANCER RISK; COMPARATIVE STUDY; CONTROLLED STUDY; DNA ADDUCT; DNA DAMAGE; DNA REPLICATION; GENE EXPRESSION PROFILING; IN VITRO STUDY; IN VIVO STUDY; LIPID METABOLISM; LIVER CARCINOGENESIS; LIVER CELL; MALE; MOUSE; MUTANT; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RISK ASSESSMENT; TOXICOGENETICS; TOXICOKINETICS; TRANSCRIPTOMICS; TUMOR VASCULARIZATION; WILD TYPE; XENOBIOTIC METABOLISM;

ANIMALS; APOPTOSIS; BENZO(A)PYRENE; CARCINOGENICITY TESTS; CARCINOGENS; CELL TRANSFORMATION, NEOPLASTIC; CELLS, CULTURED; COMPUTER SIMULATION; DNA ADDUCTS; DNA REPLICATION; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTES; HIGH-THROUGHPUT SCREENING ASSAYS; LIVER; LIVER NEOPLASMS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, BIOLOGICAL; PRIMARY CELL CULTURE; RISK ASSESSMENT; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

MUS;

EID: 84878839538     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-012-0949-5     Document Type: Article

References (54)

1. Adler S, Basketter D, Creton S, Pelkonen O, van Benthem J, Zuang V, Andersen KE, Angers-Loustau A, Aptula A, Bal-Price A, Benfenati E, Bernauer U, Bessems J, Bois FY, Boobis A, Brandon E, Bremer S, Broschard T, Casati S, Coecke S, Corvi R, Cronin M, Daston G, Dekant W, Felter S, Grignard E, Gundert-Remy U, Heinonen T, Kimber I, Kleinjans J, Komulainen H, Kreiling R, Kreysa J, Leite SB, Loizou G, Maxwell G, Mazzatorta P, Munn S, Pfuhler S, Phrakonkham P, Piersma A, Poth A, Prieto P, Repetto G, Rogiers V, Schoeters G, Schwarz M, Serafimova R, Tähti H, Testai E, van Delft J, van Loveren H, Vinken M, Worth A, Zaldivar JM (2011) Alternative (non-animal) methods for cosmetics testing: current status and future prospects - 2010. Arch Toxicol 85 (5):367-485
2. Ames BN, Gold LS (1990) Too many rodent carcinogens: mitogenesis increases mutagenesis. Science 249(4972):970-971
3. Arentson E, Faloon P, Seo J, Moon E, Studts JM, Fremont DH, Choi K (2002) Oncogenic potential of the DNA replication licensing protein CDT1. Oncogene 21(8):1150-1158
4. Auerbach SS, Shah RR, Mav D, Smith CS, Walker NJ, Vallant MK, Boorman GA, Irwin RD (2010) Predicting the hepatocarcinogenic potential of alkenylbenzene flavoring agents using toxicogenomics and machine learning. Toxicol Appl Pharmacol 243(3):300-314
5. Bartosiewicz M, Penn S, Buckpitt A (2001) Applications of gene arrays in environmental toxicology: fingerprints of gene regulation associated with cadmium chloride, benzo(a)pyrene, and trichloroethylene. Environ Health Perspect 109(1):71-74
6. Benigni R (2012) Alternatives to the carcinogenicity bioassay for toxicity prediction: are we there yet? Expert Opin Drug Metab Toxicol 8(4):407-417
7. Blaauboer BJ (2010) Biokinetic modeling and in vitro-in vivo extrapolations. J Toxicol Environ Health B Crit Rev 13(2-4):242-252
8. Blow JJ, Tada S (2000) Cell cycle. A new check on issuing the licence. Nature 404(6778):560-561
9. Boorsma A, Foat BC, Vis D, Klis F, Bussemaker HJ (2005) T-Profiler: scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res 33(Web Server issue):W592-W595
10. Brown RP, Delp MD, Lindstedt SL, Rhomberg LR, Beliles RP (1997) Physiological parameter values for physiologically based pharmacokinetic models. Toxicol Ind Health 13(4):407-484
11. Clewell H Jr, Gentry PR, Covington TR, Gearhart JM (2000) Development of a physiologically based pharmacokinetic model of trichloroethylene and its metabolites for use in risk assessment. Environ Health Perspect 108(Suppl 2):283-305
12. Crowell SR, Amin SG, Anderson KA, Krishnegowda G, Sharma AK, Soelberg JJ, Williams DE, Corley RA (2011) Preliminary physiologically based pharmacokinetic models for benzo[a]pyrene and dibenzo[def, p]chrysene in rodents. Toxicol Appl Pharmacol 257(3):365-376
13. Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, Watson SJ, Meng F (2005) Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res 33(20):e175
14. de Leeuw WC, Rauwerda H, Jonker MJ, Breit TM (2008) Salvaging Affymetrix probes after probe-level re-annotation. BMC Res Notes 1:66
15. de Vries A, van Oostrom CT, Hofhuis FM, Dortant PM, Berg RJ, de Gruijl FR, Wester PW, van Kreijl CF, Capel PJ, van Steeg H (1995) Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377(6545):169-173
16. de Vries A, van Oostrom CT, Dortant PM, Beems RB, van Kreijl CF, Capel PJ, van Steeg H (1997) Spontaneous liver tumors and benzo[a]pyrene-induced lymphomas in XPA -deficient mice. Mol Carcinog 19(1):46-53
17. Ellinger-Ziegelbauer H, Gmuender H, Bandenburg A, Ahr HJ (2008) Prediction of a carcinogenic potential of rat hepatocarcinogens using toxicogenomics analysis of short-term in vivo studies. Mutat Res 637(1-2):23-39
18. Fassett JT, Tobolt D, Nelsen CJ, Albrecht JH, Hansen LK (2003) The role of collagen structure in mitogen stimulation of ERK, cyclin D1 expression, and G1-S progression in rat hepatocytes. J Biol Chem 278(34):31691-31700
19. Fielden MR, Nie A, McMillian M, Elangbam CS, Trela BA, Yang Y, Dunn RT, Dragan Y, Fransson-Stehen R, Bogdanffy M, Adams SP, Foster WR, Chen SJ, Rossi P, Kasper P, Jacobson-Kram D, Tatsuoka KS, Wier PJ, Gollub J, Halbert DN, Roter A, Young JK, Sina JF, Marlowe J, Martus HJ, Aubrecht J, Olaharski AJ, Roome N, Nioi P, Pardo I, Snyder R, Perry R, Lord P, Mattes W, Car BD (2008) Interlaboratory evaluation of genomic signatures for predicting carcinogenicity in the rat. Toxicol Sci 103(1):28-34
20. Flowers L, Ohnishi ST, Penning TM (1997) DNA strand scission by polycyclic aromatic hydrocarbon o-quinones: role of reactive oxygen species, Cu(II)/Cu(I) redox cycling, and o-semiquinone anion radicals. Biochemistry 36(28):8640-8648
21. Foth H, Kahl R, Kahl GF (1988) Pharmacokinetics of low doses of benzo[a]pyrene in the rat. Food Chem Toxicol 26(1):45-51
22. Gelboin HV (1980) Benzo[alpha]pyrene metabolism, activation and carcinogenesis: role and regulation of mixed-function oxidases and related enzymes. Physiol Rev 60(4):1107-1166
23. Godschalk RW, Maas LM, Van Zandwijk N, van 't Veer LJ, Breedijk A, Borm PJ, Verhaert J, Kleinjans JC, van Schooten FJ (1998) Differences in aromatic-DNA adduct levels between alveolar macrophages and subpopulations of white blood cells from smokers. Carcinogenesis 19(5):819-825
24. Hamouchene H, Arlt VM, Giddings I, Phillips DH (2011) Influence of cell cycle on responses of MCF-7 cells to benzo[a]pyrene. BMC Genomics 12:333
25. Hansen LK, Wilhelm J, Fassett JT (2006) Regulation of hepatocyte cell cycle progression and differentiation by type I collagen structure. Curr Top Dev Biol 72:205-236
26. Hecht SS, Grabowski W, Groth K (1979) Analysis of faeces for benzo[a]pyrene after consumption of charcoal-broiled beef by rats and humans. Food Cosmet Toxicol 17(3):223-227
27. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4(2):249-264
28. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA (1994) Tumor spectrum analysis in p53-mutant mice. Curr Biol 4(1):1-7
29. Jacobson-Kram D, Sistare FD, Jacobs AC (2004) Use of transgenic mice in carcinogenicity hazard assessment. Toxicol Pathol 32(Suppl 1):49-52
30. Klaassen R, Olling M, Lusthof KJ (1996) The influence of the use of animal cages with wire floor or macrolon cages with middle size saw on the kinetics of benzo(a)pyrene in the rat. RIVM Report 658603 006
31. Malik AI, Williams A, Lemieux CL, White PA, Yauk CL (2012) Hepatic mRNA, microRNA, and miR-34a-target responses in mice after 28 days exposure to doses of benzo(a)pyrene that elicit DNA damage and mutation. Environ Mol Mutagen 53(1):10-21
32. Mielke H, Anger LT, Schug M, Hengstler JG, Stahlmann R, Gundert-Remy U (2011) A physiologically based toxicokinetic modelling approach to predict relevant concentrations for in vitro testing. Arch Toxicol 85(6):555-563
33. Nishitani H, Lygerou Z, Nishimoto T, Nurse P (2000) The Cdt1 protein is required to license DNA for replication in fission yeast. Nature 404(6778):625-628
34. Park HJ, Oh JH, Park SM, Cho JW, Yum YN, Park SN, Yoon DY, Yoon S (2011) Identification of biomarkers of chemically induced hepatocarcinogenesis in rasH2 mice by toxicogenomic analysis. Arch Toxicol 85(12):1627-1640
35. Pery AR, Brochot C, Desmots S, Boize M, Sparfel L, Fardel O (2011) Predicting in vivo gene expression in macrophages after exposure to benzo(a)pyrene based on in vitro assays and toxicokinetic/toxicodynamic models. Toxicol Lett 201(1):8-14
36. Pritchard JB, French JE, Davis BJ, Haseman JK (2003) The role of transgenic mouse models in carcinogen identification. Environ Health Perspect 111(4):444-454
37. Ramesh A, Inyang F, Hood DB, Archibong AE, Knuckles ME, Nyanda AM (2001) Metabolism, bioavailability, and toxicokinetics of benzo(alpha)pyrene in F-344 rats following oral administration. Exp Toxicol Pathol 53(4):275-290
38. Reddy MV, Randerath K (1986) Nuclease P1-mediated enhancement of sensitivity of 32P-postlabeling test for structurally diverse DNA adducts. Carcinogenesis 7(9):1543-1551
39. Rohrbeck A, Salinas G, Maaser K, Linge J, Salovaara S, Corvi R, Borlak J (2010) Toxicogenomics applied to in vitro carcinogenicity testing with Balb/c 3T3 cells revealed a gene signature predictive of chemical carcinogens. Toxicol Sci 118(1):31-41
40. Seo J, Chung YS, Sharma GG, Moon E, Burack WR, Pandita TK, Choi K (2005) Cdt1 transgenic mice develop lymphoblastic lymphoma in the absence of p53. Oncogene 24(55):8176-8186
41. Tada S, Li A, Maiorano D, Mechali M, Blow JJ (2001) Repression of origin assembly in metaphase depends on inhibition of RLF-B/Cdt1 by geminin. Nat Cell Biol 3(2):107-113
42. Tatsumi Y, Sugimoto N, Yugawa T, Narisawa-Saito M, Kiyono T, Fujita M (2006) Deregulation of Cdt1 induces chromosomal damage without rereplication and leads to chromosomal instability. J Cell Sci 119(Pt 15):3128-3140
43. 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
44. Uehara T, Minowa Y, Morikawa Y, Kondo C, Maruyama T, Kato I, Nakatsu N, Igarashi Y, Ono A, Hayashi H, Mitsumori K, Yamada H, Ohno Y, Urushidani T (2011) Prediction model of potential hepatocarcinogenicity of rat hepatocarcinogens using a large-scale toxicogenomics database. Toxicol Appl Pharmacol 255(3):297-306
45. Uno S, Dalton TP, Derkenne S, Curran CP, Miller ML, Shertzer HG, Nebert DW (2004) Oral exposure to benzo[a]pyrene in the mouse: detoxication by inducible cytochrome P450 is more important than metabolic activation. Mol Pharmacol 65(5):1225-1237
46. van Delft JH, van Agen E, van Breda SG, Herwijnen MH, Staal YC, Kleinjans JC (2004) Discrimination of genotoxic from non-genotoxic carcinogens by gene expression profiling. Carcinogenesis 25(7):1265-1276
47. +/- mice upon exposure to benzo[a]pyrene. Toxicol Sci 123(1):123-132
48. +/- knockout mice: overview of available data. Toxicol Pathol 29(Suppl):117-127
49. +/- knock-out mice: nature of the models. ToxicolPathol 29(Suppl):109-116
50. Verwei M, van Burgsteden JA, Krul CA, van de Sandt JJ, Freidig AP (2006) Prediction of in vivo embryotoxic effect levels with a combination of in vitro studies and PBPK modelling. Toxicol Lett 165(1):79-87
51. Waters MD, Jackson M, Lea I (2010) Characterizing and predicting carcinogenicity and mode of action using conventional and toxicogenomics methods. Mutat Res 705(3):184-200
52. Wohlschlegel JA, Dwyer BT, Dhar SK, Cvetic C, Walter JC, Dutta A (2000) Inhibition of eukaryotic DNA replication by geminin binding to Cdt1. Science 290(5500):2309-2312
53. Yauk CL, Jackson K, Malowany M, Williams A (2011) Lack of change in microRNA expression in adult mouse liver following treatment with benzo(a)pyrene despite robust mRNA transcriptional response. Mutat Res 722(2):131-139
54. Zeilmaker MJ, van Eijkeren JCH, Olling M (1999) A PBPK-model for B(a)P in the rat relating dose and liver DNA-adduct level. RIVM Report 658603 008