Drug-induced endoplasmic reticulum and oxidative stress responses independently sensitize toward TNFα-mediated hepatotoxicity

Toxicological Sciences

Volumn 140, Issue 1, 2014, Pages 144-159

  Fredriksson, Lisa ^a   Wink, Steven ^a   Herpers, Bram ^a   Benedetti, Giulia ^a   Hadi, Mackenzie ^b   De Bont, Hans ^a   Groothuis, Geny ^b   Luijten, Mirjam ^c   Danen, Erik ^a   De Graauw, Marjo ^a   Meerman, John ^a   van de Water, Bob ^a  

^a LEIDEN UNIVERSITY   (Netherlands)

^b UNIVERSITY OF GRONINGEN   (Netherlands)

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

Author keywords

Drug induced liver injury; High content microscopy; RNA interference; Transcriptomics

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; KETOCONAZOLE; METHOTREXATE; NEFAZODONE; PROTEIN KINASE R; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA; CARBAMAZEPINE; DICLOFENAC; NFE2L2 PROTEIN, HUMAN; TRANSCRIPTOME;

ARTICLE; CELL KILLING; CELL PROTECTION; CONTROLLED STUDY; CYTOTOXICITY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION; HUMAN; HUMAN CELL; LIVER; LIVER CELL; LIVER TOXICITY; NETHERLANDS; OXIDATIVE STRESS; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSLATION INITIATION; ANIMAL; APOPTOSIS; C57BL MOUSE; DRUG EFFECTS; DRUG POTENTIATION; DRUG-INDUCED LIVER INJURY; GENE EXPRESSION PROFILING; GENETIC ASSOCIATION; GENETICS; HEPG2 CELL LINE; IMMUNOLOGY; METABOLISM; TOXICITY;

ANIMALS; APOPTOSIS; CARBAMAZEPINE; DICLOFENAC; DRUG SYNERGISM; DRUG-INDUCED LIVER INJURY; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION PROFILING; GENOME-WIDE ASSOCIATION STUDY; HEP G2 CELLS; HEPATOCYTES; HUMANS; MICE, INBRED C57BL; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; TRANSCRIPTOME; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84903837546     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfu072     Document Type: Article

References (50)

1. Benjamini, Y., and Hochberg, Y. (1995). Controlling FDR. J. R. Stat. Soc., Series B Methodol. 57, 289-300.
2. Boyce, M., Bryant, K. F., Jousse, C., Long, K., Harding, H. P., Scheuner, D., Kaufman, R. J., Ma, D., Coen, D. M., Ron, D., et al. (2005). A selective inhibitor of eIF2alpha dephosphorylation protects cells from ER stress. Science 307, 935-939.
3. Cantoni, L., Valaperta, R., Ponsoda, X., Castell, J. V., Barelli, D., Rizzardini, M., Mangolini, A., Hauri, L., and Villa, P. (2003). Induction of hepatic heme oxygenase-1 by diclofenac in rodents: role of oxidative stress and cytochrome P-450 activity. J. Hepatol. 38, 776-783.
4. Chen, M., Vijay, V., Shi, Q., Liu, Z., Fang, H., and Tong, W. (2011). FDAapproved drug labeling for the study of drug-induced liver injury. Drug Discov. Today 16, 697-703.
5. Choi, S. (2003). Nefazodone (Serzone) withdrawn because of hepatotoxicity. CMAJ 169, 1187.
6. Coldwell, M. J., Mitchell, S. A., Stoneley, M., MacFarlane, M., and Willis, A. E. (2000). Initiation of Apaf-1 translation by internal ribosome entry. Oncogene 19, 899-905.
7. Copple, I. M., Goldring, C. E., Jenkins, R. E., Chia, A. J. L., Randle, L. E., Hayes, J. D., Kitteringham, N. R., and Park, B. K. (2008). The hepatotoxic metabolite of acetaminophen directly activates the Keap1-Nrf2 cell defense system. Hepatology 48, 1292-1301.
8. Cosgrove, B. D., Alexopoulos, L. G., Hang, T.-C., Hendriks, B. S., Sorger, P. K., Griffith, L. G., and Lauffenburger, D. A. (2010). Cytokine-associated drug toxicity in human hepatocytes is associated with signaling network dysregulation. Mol. Biosyst. 6, 1195-1206.
9. Cosgrove, B. D., King, B. M., Hasan, M. A., Alexopoulos, L. G., Farazi, P. A., Hendriks, B. S., Griffith, L. G., Sorger, P. K., Tidor, B., Xu, J. J., et al. (2009). Synergistic drug-cytokine induction of hepatocellular death as an in vitro approach for the study of inflammation-associated idiosyncratic drug hepatotoxicity. Toxicol. Appl. Pharmacol. 237, 317-330.
10. Cui, Y., and Paules, R. S. (2010). Use of transcriptomics in understanding mechanisms of drug-induced toxicity. Pharmacogenomics 11, 573-585.
11. Cullinan, S. B., and Diehl, J. A. (2006). Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 38, 317-332.
12. Dara, L., Ji, C., and Kaplowitz, N. (2011). The contribution of endoplasmic reticulum stress to liver diseases. Hepatology 53, 1752-1763.
13. Deng, X., Liguori, M. J., Sparkenbaugh, E. M., Waring, J. F., Blomme, E. A. G., Ganey, P. E., and Roth, R. A. (2008). Gene expression profiles in livers from diclofenac-treated rats reveal intestinal bacteria-dependent and -independent pathways associated with liver injury. J. Pharmacol. Exp. Ther. 327, 634-644.
14. Deng, X., Stachlewitz, R. F., Liguori, M. J., Blomme, E. A. G., Waring, J. F., Luyendyk, J. P., Maddox, J. F., Ganey, P. E., and Roth, R. A. (2006). Modest inflammation enhances diclofenac hepatotoxicity in rats: role of neutrophils and bacterial translocation. J. Pharmacol. Exp. Ther. 319, 1191-1199.
15. Edgar, R., Domrachev, M., and Lash, A. E. (2002). Gene Expression Omnibus:NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 30, 207-210.
16. Fredriksson, L., Herpers, B., Benedetti, G., Matadin, Q., Puigvert, J. C., de Bont, H., Dragovic, S., Vermeulen, N. P. E., Commandeur, J. N.M., and Danen, E. (2011). Diclofenac inhibits tumor necrosis factor-α-induced nuclear factor-κB activation causing synergistic hepatocyte apoptosis. Hepatology 53, 2027-2041.
17. Gómez-Lechón, M. J., Ponsoda, X., O'Connor, E., Donato, T., Castell, J. V., and Jover, R. (2003). Diclofenac induces apoptosis in hepatocytes by alteration of mitochondrial function and generation of ROS. Biochem. Pharmacol. 66, 2155-2167.
18. Hadi, M., Westra, I. M., Starokozhko, V., Dragovic, S., Merema, M. T., and Groothuis, G. M. M. (2013). Human precision-cut liver slices as an ex vivo model to study idiosyncratic drug-induced liver injury. Chem. Res. Toxicol. 26, 710-720.
19. Harding, H. P., Novoa, I., Zhang, Y., Zeng, H., Wek, R., Schapira, M., and Ron, D. (2000). Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell. 6, 1099-1108.
20. Hendriks, G., Atallah, M., Morolli, B., Calléja, F., Ras-Verloop, N., Huijskens, I., Raamsman, M., van de Water, B., Vrieling, H., et al. (2012). The Tox-Tracker assay: novel GFP reporter systems that provide mechanistic insight into the genotoxic properties of chemicals. Toxicol. Sci. 125, 285-298.
21. Hetz, C. (2012). The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat. Rev. Mol. Cell Biol. 13, 89-102.
22. Holcik, M., Lefebvre, C., Yeh, C., Chow, T., and Korneluk, R. G. (1999). A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat. Cell Biol. 1, 190-192.
23. Huber, W., Heydebreck Von, A., Sültmann, H., Poustka, A., and Vingron, M. (2002). Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics 18, S96-S104.
24. Irizarry, R. A., Hobbs, B., Collin, F., Beazer-Barclay, Y. D., Antonellis, K. J., Scherf, U., and Speed, T. P. (2003). Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264.
25. Jackson, R. J., Hellen, C. U. T., and Pestova, T. V. (2010). The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell. Biol. 11, 113-127.
26. Jaiswal, A. K. (2004). Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic. Biol. Med. 36, 1199-1207.
27. Kobayashi, A., Kang, M.-I., Okawa, H., Ohtsuji, M., Zenke, Y., Chiba, T., Igarashi, K., and Yamamoto, M. (2004). Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell Biol. 24, 7130-7139.
28. Leeder, J. S. (1998). Mechanisms of idiosyncratic hypersensitivity reactions to antiepileptic drugs. Epilepsia 39(Suppl. 7), S8-S16.
29. Lu, J., Jones, A. D., Harkema, J. R., Roth, R. A., and Ganey, P. E. (2012). Amiodarone exposure during modest inflammation induces idiosyncrasy-like liver injury in rats: role of tumor necrosis factor-alpha. Toxicol. Sci. 125, 126-133.
30. Okawa, H., Motohashi, H., Kobayashi, A., Aburatani, H., Kensler, T. W., and Yamamoto, M. (2006). Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity. Biochem. Biophys. Res. Commun. 339, 79-88.
31. O'Brien, P. J., Irwin, W., Diaz, D., Howard-Cofield, E., Krejsa, C. M., Slaughter, M. R., Gao, B., Kaludercic, N., Angeline, A., Bernardi, P., et al. (2006). High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Arch. Toxicol. 80, 580-604.
32. Parsyan, A., Svitkin, Y., Shahbazian, D., Gkogkas, C., Lasko, P., Merrick, W. C., and Sonenberg, N. (2011). mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell Biol. 12, 235-245.
33. Poser, I., Sarov, M., Hutchins, J. R. A., Hériché, J.-K., Toyoda, Y., Pozniakovsky, A., Weigl, D., Nitzsche, A., Hegemann, B., Bird, A. W., et al. (2008). BAC TransgeneOmics: a high-throughput method for exploration of protein function in mammals. Nat. Methods 5, 409-415.
34. Puigvert, J. C., de Bont, H., van de Water, B., and Danen, E. H.J. (2010). High-throughput live cell imaging of apoptosis. Curr. Protoc. Cell Biol. 47, 18.10.1-13.
35. Puthalakath, H., O'Reilly, L. A., Gunn, P., Lee, L., Kelly, P. N., Huntington, N. D., Hughes, P. D., Michalak, E. M., McKimm-Breschkin, J., Motoyama, N., et al. (2007). ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129, 1337-1349.
36. Roberts, R. A., Ganey, P. E., Ju, C., Kamendulis, L. M., Rusyn, I., and Klaunig, J. E. (2007). Role of the Kupffer cell in mediating hepatic toxicity and carcinogenesis. Toxicol. Sci. 96, 2-15.
37. Roth, R. A., and Ganey, P. E. (2011). Animal models of idiosyncratic druginduced liver injury-current status. Crit. Rev. Toxicol. 41, 723-739.
38. Saeed, A., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T., Thiagarajan, M., et al. (2003). TM4: a free, opensource system for microarray data management and analysis. Biotechniques 34, 374-378.
39. Santos, N. A. G., Medina, W. S. G., Martins, N. M., Rodrigues, M. A. C., Curti, C., and Santos, A. C. (2008). Involvement of oxidative stress in the hepatotoxicity induced by aromatic antiepileptic drug. Toxicol. in Vitro 22, 1820-1824,
40. Shaw, P. J., Hopfensperger, M. J., Ganey, P. E., and Roth, R. A. (2007). Lipopolysaccharide and trovafloxacin coexposure in mice causes idiosyncrasy-like liver injury dependent on tumor necrosis factor-alpha. Toxicol. Sci. 100, 259-266.
41. Smyth, G. K. (2004). Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol. 3, 3.
42. Soriano, F. X., Baxter, P., Murray, L. M., Sporn, M. B., Gillingwater, T. H., and Hardingham, G. E. (2009). Transcriptional regulation of the AP-1 and Nrf2 target gene sulfiredoxin. Mol. Cells. 27, 279-282.
43. Stricker, B. H., Blok, A. P., Bronkhorst, F. B., Van Parys, G. E., and Desmet, V. J. (1986). Ketoconazole-associated hepatic injury. A clinicopathological study of 55 cases. J. Hepatol. 3, 399-406.
44. van de Water, B., Wang, Y., Asmellash, S., Liu, H., Zhan, Y., Miller, E., and Stevens, J. L. (1999). Distinct endoplasmic reticulum signaling pathways regulate apoptotic and necrotic cell death following iodoacetamide treatment. Chem. Res. Toxicol. 12, 943-951.
45. van Kesteren, P. C. E., Zwart, P. E., Pennings, J. L. A., Gottschalk, W. H. R., Kleinjans, J. C. S., van Delft, J. H., van Steeg, H., and Luijten, M. (2011). Deregulation of cancer-related pathways in primary hepatocytes derived from DNA repair-deficient Xpa-/-p53+/- mice upon exposure to benzo[a]pyrene. Toxicol. Sci. 123, 123-132.
46. West, S. G. (1997). Methotrexate hepatotoxicity. Rheum. Dis. Clin. North Am. 23, 883-915.
47. Woehlbier, U., and Hetz, C. (2011). Modulating stress responses by the UPRosome:a matter of life and death. Trends Biochem. Sci. 36, 329-337.
48. Wolfinger, R. D., Gibson, G., Wolfinger, E. D., Bennett, L., Hamadeh, H., Bushel, P., Afshari, C., and Paules, R. S. (2001). Assessing gene significance from cDNA microarray expression data via mixed models. J. Comput. Biol. 8, 625-637.
49. Xu, J. J., Henstock, P. V., Dunn, M. C., Smith, A. R., Chabot, J. R., and de Graaf, D. (2008). Cellular imaging predictions of clinical drug-induced liver injury. Toxicol. Sci. 105, 97-105.
50. Zou, W., Beggs, K.M., Sparkenbaugh, E. M., Jones, A. D., Younis, H. S., Roth, R. A., and Ganey, P. E. (2009). Sulindac metabolism and synergy with tumor necrosis factor-alpha in a drug-inflammation interaction model of idiosyncratic liver injury. J. Pharmacol. Exp. Ther. 331, 114-121.