Parallelogram approach using rat-human In vitro and rat in vivo toxicogenomics predicts acetaminophen-induced hepatotoxicity in humans

Toxicological Sciences

Volumn 107, Issue 2, 2009, Pages 544-552

  Kienhuis, Anne S ^a,b   Van de Poll, Marcel C G ^c   Wortelboer, Heleen ^b   Van Herwijnen, Marcel ^a   Gottschalk, Ralph ^a   Dejong, Cornelis H C ^c   Boorsma, André ^b   Paules, Richard S ^d   Kleinjans, Jos C S ^a   Stierum, Rob H ^b   Van Delft, Joost H M ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b TNO   (Netherlands)

^c MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Acetaminophen; Gene expression profiling; Hepatocyte based in vitro models; Interspecies extrapolation; Liver injury; T profiler

Indexed keywords

OXIDOREDUCTASE; PARACETAMOL;

ADULT; AGED; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CELL FUNCTION; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENERGY CONSUMPTION; ENZYME ACTIVITY; FEMALE; GENE EXPRESSION PROFILING; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; HUMAN VERSUS ANIMAL COMPARISON; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; LIVER METABOLISM; LIVER MITOCHONDRION; LIVER TOXICITY; MALE; NONHUMAN; RAT; SPECIES COMPARISON; TOXICOGENETICS;

ACETAMINOPHEN; ADULT; AGED; ANALGESICS, NON-NARCOTIC; ANIMALS; CELL SURVIVAL; CELLS, CULTURED; FEMALE; HEPATITIS, TOXIC; HEPATOCYTES; HUMANS; IN SITU HYBRIDIZATION; MALE; PREDICTIVE VALUE OF TESTS; RATS; RATS, INBRED F344; RATS, WISTAR; RNA; SPECIES SPECIFICITY; TOXICOGENETICS;

RATTUS; RODENTIA;

EID: 59149103386     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfn237     Document Type: Article

References (37)

1. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000). Gene ontology: Tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25, 25-29.
2. Beken, S., Vanhaecke, T., De Smet, K., Pauwels, M., Vercruysse, A., and Rogiers, V. (2004). Collagen-gel cultures of rat hepatocytes: Collagen-gel sandwich and immobilization cultures. In Cytochrome P450 Protocols (I. R. Phillips, and E. A. Shephard, Eds.). Humana Press Inc., Totowa, NJ.
3. Bessems, J. G., ahd Vermeulen, N. P. (2001). Paracetamol (acetaminophen)- induced toxicity: Molecular and biochemical mechanisms, analogues and protective approaches. Crit. Rev. Toxicol. 31, 55-138.
4. Beyer, R. P., Fry, R. C., Lasarev, M. R., McConnachie, L. A., Meira, L. B., Palmer, V. S., Powell, C. L., Ross, P. K., Bamurtler, T. K., Bradford, B. U., et al. (2007). Multicenter study of acetaminophen hepatotoxicity reveals the importance of biological endpoints in genomic analyses. Toxicol. Sci. 99, 326-337.
5. Boorsma, A., Foat, B. C., Vis, D., Klis, F., and Bussemaker, H. J. (2005). T-profiler: Scoring the activity of predefined groups of genes using gene expression data. Nucleic Acids Res. 33, W592-W595.
6. Burcham, P. C., and Harman, A. W. (1991). Acetaminophen toxicity results in site-specific mitochondrial damage in isolated mouse hepatocytes. J. Biol. Chem. 266, 5049-5054.
7. Bushel, P. R., Heinloth, A. N., Li, J., Huang, L., Chou, J. W., Boorman, G. A., Malarkey, D. E., Houle, C. D., Ward, S. M., Wilson, R. E., et al. (2007). Blood gene expression signatures predict exposure levels. Proc. Natl. Acad. Sci. U.S.A. 104, 18211-18216.
8. Currie, R. A., Orphanides, G., and Moggs, J. G. (2005). Mapping molecular responses to xenoestrogens through gene ontology and pathway analysis of toxicogenomic data. Reprod. Toxicol. 20, 433-440.
9. Dambach, D. M., Andrews, B. A., and Moulin, F. (2005). New technologies and screening strategies for hepatotoxicity: Use of in vitro models. Toxicol. Pathol. 33, 17-26.
10. Dejong, C. H. C., and Garden, O. J. (2003). Neoplasms in the liver. In Advanced Surgical Practice (A. A. Majid and A. Kingsnorth, Eds.), pp. 146-156. Greenwich Medical Media, London.
11. de Longueville, F., Atienzar, F. A., Marcq, L., Dufrane, S., Evrard, S., Wouters, L., Leroux, F., Bertholet, V., Gerin, B., Whomsley, R., et al. (2003). Use of a low-density microarray for studying gene expression patterns induced by hepatotoxicants on primary cultures of rat hepatocytes. Toxicol. Sci. 75, 378-392.
12. Guillouzo, A. (1998). Liver cell models in in vitro toxicology. Environ, Health Perspect. 106(Suppl. 2), 511-532.
13. Guo, L., Lobenhofer, E. K., Wang, C., Shippy, R., Harris, S. C., Zhang, L., Mei, N., Chen, T., Herman, D., Goodsaid, F. M., et al. (2006). Rat toxicogenomic study reveals analytical consistency across microarray platforms. Nat. Biotechnol. 24, 1162-1169.
14. Hamilton, G. A., Jolley, S. L., Gilbert, D., Coon, D. J., Barros, S., and LeCluyse, E. L. (2001). Regulation of cell morphology and cytochrome P450 expression in human hepatocytes by extracellular matrix and ceti-cell interactions. Cell Tissue Res. 306, 85-99.
15. Harris, A. J., Dial, S. L., and Casciano, D. A. (2004). Comparison of basal gene exprrssion profile's and effects of hepatocarcinogens on gene expression in cultured primary human hepatocytes and HepG2 cells. Mutat. Res. 549, 79-99.
16. Heinloth, A. N., Boorman, G. A., Foley, J. F., Flagler, N. D., and Paules, R. S. (2007). Gene expression analysis offers unique advantages to histopathology in liver biopsy evaluations. Toxicol. Pathol. 35, 276-283.
17. Heinloth, A. N., Irwin, R. D., Boorman, G. A., Nettesheim, P., Fannin, R. D., Sieber, S. O., Snell, M. L., Tucker, C. J., Li, L., Travlos, G. S., et al. (2004). Gene expression profiling of rat livers reveals indicators of potential adverse effects. Toxicol. Sci. 80, 193-201.
18. Jaeschke, H., and Bajt, M. L. (2006). Intracellular signaling mechanisms of acetaminophen-induced liver cell death. Toxicol. Sci. 99, 31-41.
19. James, L. P., Mayeux, P. R., and Hinson, J. A. (2003). Acetaminophen-induced hepatotoxicity. Drug Metab. Dispos. 31 1499-1506.
20. Kern, A., Bader, A., Pichlmayr, R., and Sewing, K. F. (1997). Drug metabolism in hepatocyte sandwich cultures of rats and humans. Biochem. Pharmacol. 54, 761-772.
21. Kienhuis, A. S., Wortelboer, H. M., Hoflack, J. C., Moonen, E. J., Kleinjans, J. C, van Ommen, B., van Delt J. H., and Stierum, R. H. (2006). Comparison of coumarin-induced toxicity between sandwich-cultured primary rat hepatocytes and rats in vivo: A toxicogenomics approach. Drug Metab. Dispos. 34, 2083-2090.
22. Kienhuis, A. S., Wortelboer, H. M., Maas, W. J., van Herwijnen, M., Kleinjans, J. C., van Delft, J. H., and Stierum, R. H. (2007). A sandwich-cultured rat hepatocyte system with increased metabolic competence evaluated by gene expression profiling. Toxicol. In Vitro 21, 892-901.
23. Kikkawa, R., Fujikawa, M., Yamamoto, T., Hamada, Y., Yamada, H., and Horii, I. (2006). In vivo hepatotoxicity study of rats in comparison with in vitro hepatotoxicity screening system. J. Toxicol. Sci. 31, 23-34.
24. Larson, A. M. (2007). Acetaminophen hepatotoxicity. Clin. Liver Dis. 11, 525-548; vi.
25. Larson, A. M., Polson, J., Fontana, R. J., Daverb, T. J., Lalani, E., Hynan, L. S., Reisch, J. S., Schiodt, F. V., Ostapowicz, G., Shakil, A. O., et al. (2005). Acetaminophen-induced acute liver failure: Results of a United States multicenter, prospective study. Hepatology 42, 1364-1372.
26. LeCluyse, E. L. (2001). Human hepatocyte culture systems for the in vitro evaluation of cytochrome P450 expression and regulation. Eur. J. Pharm. Sci. 13, 343-368.
27. LeCluyse, E. L., Alexandre, E., Hamilton, G. A., Viollon-Abadie, C., Coon, D. J., Jolley, S., and Richert, L. (2005). Isolation and culture of primary human hepatocytes. Methods Mol. Biol. 290, 207-229.
28. Maurel, P. (1996). The use of adult human hepatocytes in primary culture and other in vitro systems to investigate drug metabolism in man. Adv. Drug Delivery Rev. 22, 105-132.
29. Richert, L., Alexandre, E., Lloyd, T., Orr, S., Viollon-Abadie, C., Patel, R., Kingston, S., Berry, D., Dennison. A., Heyd, B., et al. (2004). Tissue collection, transport and isolation procedures required to optimize human hepatocyte isolation ftorn waste liver surgical resections. A multilaboratory study. Liver Int. 24, 371-378.
30. Ruepp, S. U., Tonge, R. P., Shaw, J., Wallis, N., and Pognan, F. (2002). Genomics and proteomics analysis of acetaminophen toxicity in mouse liver. Toxicol. Sci. 65, 135-150.
31. Seglen, P. O. (1976). Preparation of isolated rat liver cells. Methods Cell Biol. 13, 29-83.
32. Slikker, W., Jr, Andersen, M. E., Bogdanffy, M. S., Bus, J. S., Cohen, S. D., Conolly, R. B., David, R. M., Doerrer, N. G., Dorman, D. C., Gaylor, D. W., et al. (2004). Dose-dependent transitions in mechanisms of toxicity: Case studies. Toxicol. Appl. Pharmacol. 201, 226-294.
33. Sobels, F. H. (1977). Some problems associated with the testing for environmental mutagens and a perspective for studies in "comparative mutagenesis". Mutat. Res. 46, 245-260.
34. Sobels, F. H. (1984). Problems and perspectives in genetic toxicology. In Mutations in Man (G. Obe, Ed.), pp. 1-19. Springer, Berlin.
35. Sobels, F. H. (1989). Models and assumptions underlying genetic risk assessment. Mutat. Res. 212, 77-89.
36. Wolf, K. K., Wood, S. G., Allard, J. L., Hunt, J. A., Gorman, N., Walton-Strong, B. W., Szakacs, J. G., Duan, S. X., Hao, Q., Court, M. H., et al. (2007). Role of CYP3A ind CYP2El in alcohol-mediated increases in acetaminophen hepatotoxicity: Comparison of wild-type and Cyp2el(-/-) mice. Drug Metab. Dispos. 35, 1223-1231.
37. Yang, Y. H., Dudoit, S., Luu, P., Lin, D. M., Peng, V., Ngai, J., and Speed, T. P. (2002). Normalization for cDNA microarray data: A robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30, e15.