Unique gene expression and hepatocellular injury in the lipopolysaccharide-ranitidine drug idiosyncrasy rat model: Comparison with famotidine

Toxicological Sciences

Volumn 90, Issue 2, 2006, Pages 569-585

  Luyendyk, James P ^a   Lehman McKeeman, Lois D ^b   Nelson, David M ^b   Bhaskaran, Vasanthi M ^a   Reilly, Timothy P ^c   Car, Bruce D ^b   Cantor, Glenn H ^b   Maddox, Jane F ^a   Ganey, Patricia E ^a   Roth, Robert A ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

^c BRISTOL MYERS SQUIBB COMPANY   (United States)

Author keywords

Drug idiosyncrasy; Gene array; Hepatotoxicity; Inflammation; Lipopolysaccharide

Indexed keywords

CYCLOOXYGENASE 2; DRUG VEHICLE; EARLY GROWTH RESPONSE FACTOR 1; FAMOTIDINE; GAMMA INTERFERON; GENE PRODUCT; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE ACTIVATED PROTEIN KINASE 2; PLASMINOGEN ACTIVATOR INHIBITOR 1; PROTEIN BNIP3; PROTEIN EGLN3; RANITIDINE; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORRELATION ANALYSIS; DOSE RESPONSE; GENE EXPRESSION; GENE PROBE; GENE TARGETING; HEMOSTASIS; HYPOXIA; LIVER CELL DAMAGE; LIVER TOXICITY; MALE; NEUTROPHIL; NONHUMAN; NUCLEOTIDE SEQUENCE; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ANIMALS; DRUG INTERACTIONS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FAMOTIDINE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HISTAMINE H2 ANTAGONISTS; LIPOPOLYSACCHARIDES; LIVER; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; POLYMERASE CHAIN REACTION; RANITIDINE; RATS; RATS, SPRAGUE-DAWLEY;

ANIMALIA;

EID: 33645111748     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfj103     Document Type: Article

References (53)

1. Adamson, G. M., and Billings, R. E. (1993). Cytokine toxicity and induction of NO synthase activity in cultured mouse hepatocytes. Toxicol Appl. Pharmacol. 119, 100-107.
2. Balabanian, K., Lagane, B., Infantino, S., Chow, K. Y., Harriague, J., Moepps, B., Arenzana-Seisdedos, F., Thelen, M., and Bachelerie, F. (2005). The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J. Biol. Chem. 280, 35760-35766.
3. Bertini, R., Allegretti, M., Bizzarri, C., Moriconi, A., Locati, M., Zampella, G., Cervellera, M. N., Di, C. V., Cesta, M. C., Galliera, et al. (2004). Noncompetitive allosteric inhibitors of the inflammatory chemokine receptors CXCR1 and CXCR2: Prevention of reperfusion injury. Proc. Natl. Acad. Sci. U.S.A. 101, 11791-11796.
4. Bruick, R. K. (2000). Expression of the gene encoding the proapoptotic Nip3 protein is induced by hypoxia. Proc. Natl. Acad. Sci. U.S.A. 97, 9082-9087.
5. Buchweitz, J. P., Ganey, P. E., Bursian, S. J., and Roth, R. A. (2002). Underlying endotoxemia augments toxic responses to chlorpromazine: Is there a relationship to drug idiosyncrasy? J. Pharmacol. Exp. Ther. 300, 460-467.
6. Car, B. D., Eng, V. M., Schnyder, B., Ozmen, L., Huang, S., Gallay, P., Heumann, D., Aguet, M., and Ryffel, B. (1994). Interferon gamma receptor deficient mice are resistant to endotoxic shock. J. Exp. Med. 179, 1437-1444.
7. Clauss, M., Weich, H., Breier, G., Knies, U., Rockl, W., Waltenberger, J., and Risau, W. (1996). The vascular endothelial growth factor receptor Flt-1 mediates biological activities. Implications for a functional role of placenta growth factor in monocyte activation and chemotaxis. J. Biol. Chem. 271, 17629-17634.
8. Cheng, P. Y., Wang, M., and Morgan, E. T. (2003). Rapid transcriptional suppression of rat cytochrome P450 genes by endotoxin treatment and its inhibition by curcumin. J. Pharmacol. Exp. Ther. 307, 1205-1212.
9. Dean, J. L., Sully, G., Clark, A. R., and Saklatvala, J. (2004). The involvement of AU-rich element-binding proteins in p38 mitogen-activated protein kinase pathway-mediated mRNA stabilisation. Cell Signal. 16, 1113-1121.
10. Dorman, R. B., Gujral, J. S., Bajt, M. L., Farhood, A., and Jaeschke, H. (2005). Generation and functional significance of CXC chemokines for neutrophil-induced liver injury during endotoxemia. Am. J. Physiol. Gastrointest. Liver Physiol. 288, G880-G886.
11. Freeman, R. S., Hasbani, D. M., Lipscomb, E. A., Straub, J. A., and Xie, L. (2003). SM-20, EGL-9, and the EGLN family of hypoxia-inducible factor prolyl hydroxylases. Mol. Cells 16, 1-12.
12. Ganey, P. E., Barton, Y. W., Kinser, S., Sneed, R. A., Barton, C. C., and Roth, R. A. (2001). Involvement of cyclooxygenase-2 in the potentiation of allyl alcohol-induced liver injury by bacterial lipopolysaccharide. Toxicol. Appl. Pharmacol. 174, 113-121.
13. Ganey, P. E., Luyendyk, J. P., Maddox, J. F., and Roth, R. A. (2004). Adverse hepatic drug reactions: Inflammatory episodes as consequence and contributor. Chem. Biol. Interact. 150, 35-51.
14. Ganey, P. E., and Roth, R. A. (2001). Concurrent inflammation as a determinant of susceptibility to toxicity from xenobiotic agents. Toxicology 169, 195-208.
15. Hayhurst, G. P., Lee, Y. H., Lambert, G., Ward, J. M., and Gonzalez, F. J. (2001). Hepatocyte nuclear factor 4alpha (nuclear receptor 2A1) is essential for maintenance of hepatic gene expression and lipid homeostasis. Mol. Cell Biol. 21, 1393-1403.
16. Ishida, Y., Kondo, T., Ohshima, T., Fujiwara, H., Iwakura, Y., and Mukaida, N. (2002). A pivotal involvement of IFN-gamma in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J. 16, 1227-1236.
17. Ju, C., and Uetrecht, J. P. (2002). Mechanism of idiosyncratic drug reactions: Reactive metabolite formation, protein binding and the regulation of the immune system. Curr. Drug Metab. 3, 367-377.
18. Kietzmann, T., Jungermann, K., and Gorlach, A. (2003). Regulation of the hypoxia-dependent plasminogen activator inhibitor 1 expression by MAP kinases. Thromb. Haemost. 89, 666-673.
19. Kotlyarov, A., and Gaestel, M. (2002). Is MK2 (mitogen-activated protein kinase-activated protein kinase 2) the key for understanding post-transcriptional regulation of gene expression? Biochem. Soc. Trans. 30, 959-963.
20. Kotlyarov, A., Neininger, A., Schubert, C., Eckert, R, Birchmeier, C., Volk, H. D., and Gaestel, M. (1999). MAPKAP kinase 2 is essential for LPS-induced TNF-alpha biosynthesis. Nat. Cell Biol. 1, 94-97.
21. Labib, R., Turkall, R., and bdel-Rahman, M. S. (2002). Endotoxin potentiates the hepatotoxicity of cocaine in male mice. J. Toxicol. Environ. Health A 65, 977-993.
22. Lasa, M., Mahtani, K. R., Finch, A., Brewer, G., Saklatvala, J., and Clark, A. R. (2000). Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell Biol. 20, 4265-4274.
23. Lin, B., Kolluri, S. K., Lin, F., Liu, W., Han, Y. H., Cao, X., Dawson, M. I., Reed, J. C., and Zhang, X. K. (2004). Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/ TR3. Cell 116, 527-540.
24. Lin, J. H. (1991). Pharmacokinetic and pharmacodynamic properties of histamine H2-receptor antagonists. Relationship between intrinsic potency and effective plasma concentrations. Clin. Pharmacokinet. 20, 218-236.
25. Lind, R. C., Gandolfi, A. J., Sipes, I. G., and Brown, B. R. J. (1984). The involvement of endotoxin in halothane-associated liver injury. Anesthesiology 61, 544-550.
26. Liu, L., Tsai, J. C., and Aird, W. C. (2000). Egr-1 gene is induced by the systemic administration of the vascular endothelial growth factor and the epidermal growth factor. Blood 96, 1772-1781.
27. Liu, Z. X., Govindarajan, S., and Kaplowitz, N. (2004). Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 127, 1760-1774.
28. Luyendyk, J. P., Lehman-McKeeman, L. D., Nelson, D. M., Bhaskaran, V., Car, B. D., Cantor, G. H., North, C. M., Newport, S. W., Maddox, J. F., Ganey, P. E., et al. (2005a). Augmentation of lipopolysaccharide-induced gene expression and liver injury by ranitidine, but not famotidine. Toxicol. Sci. 84(S-1), 1930 (Abstract).
29. Luyendyk, J. P., Maddox, J. F., Green, C. D., Ganey, P. E., and Roth, R. A. (2004a). Role of hepatic fibrin in idiosyncrasy-like liver injury from lipopolysaccharide-ranitidine coexposure in rats. Hepatology 40, 1342-1351.
30. Luyendyk, J. P., Maddox, J. F., Cosma, G. N., Ganey, P. E., Cockerell, G. L., and Roth, R. A. (2003). Ranitidine treatment during a modest inflammatory response precipitates idiosyncrasy-like liver injury in rats. J. Pharmacol. Exp. Ther. 307, 9-16.
31. Luyendyk, J. P., Mattes, W. B., Burgoon, L. D., Zacharewski, T. R., Maddox, J. F., Cosma, G. N., Ganey, P. E., and Roth, R. A. (2004b). Gene expression analysis points to hemostasis in livers of rats cotreated with lipopolysaccharide and ranitidine. Toxicol. Sci. 80, 203-213.
32. Luyendyk, J. P., Shaw, P. J., Green, C. D., Maddox, J. F., Ganey, P. E., and Roth, R. A. (2005b). Coagulation-mediated hypoxia and neutrophil-dependent hepatic injury in rats given lipopolysaccharide and ranitidine. J. Pharmacol. Exp. Ther. 314, 1023-1031.
33. Mavropoulos, A., Sully, G., Cope, A. P., and Clark, A. R. (2005). Stabilization of IFN-gamma mRNA by MAPK p38 in IL-12- and IL-18-stimulated human NK cells. Blood 105, 282-288.
34. Mechtcheriakova, D., Wlachos, A., Holzmuller, H., Binder, B. R., and Hofer, E. (1999). Vascular endothelial cell growth factor-induced tissue factor expression in endothelial cells is mediated by EGR-1. Blood 93, 3811-3823.
35. Neininger, A., Kontoyiannis, D., Kotlyarov, A., Winzen, R., Eckert, R., Volk, H. D., Holtmann, H., Kollias, G., and Gaestel, M. (2002). MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J. Biol. Chem. 277, 3065-3068.
36. Okada, M., Fujita, T., Sakaguchi, T., Olson, K. E., Collins, T., Stern, D. M., Yan, S. F., and Pinsky, D. J. (2001). Extinguishing Egr-1-dependent inflammatory and thrombotic cascades after lung transplantation. FASEB J. 15, 2757-2759.
37. Pawlinski, R., Pedersen, B., Kehrle, B., Aird, W. C., Frank, R. D., Guha, M., and Mackman, N. (2003). Regulation of tissue factor and inflammatory mediators by Egr-1 in a mouse endotoxemia model. Blood 101, 3940-3947.
38. Pawlinski, R., Pedersen, B., Schabbauer, G., Tencati, M., Holscher, T., Boisvert, W., Andrade-Gordon, P., Frank, R. D., and Mackman, N. (2004). Role of tissue factor and protease-activated receptors in a mouse model of endotoxemia. Blood 103, 1342-1347.
39. Pirmohamed, M., Madden, S., and Park, B. K. (1996). Idiosyncratic drug reactions. Metabolic bioactivation as a pathogenic mechanism. Clin. Pharmacokinet. 31, 215-230.
40. Roth, R. A., Luyendyk, J. P., Maddox, J. F., and Ganey, P. E. (2003). Inflammation and drug idiosyncrasy-is there a connection? J. Pharmacol. Exp. Ther. 307, 1-8.
41. Rousseau, S., Morrice, N., Peggie, M., Campbell, D. G., Gaestel, M., and Cohen, P. (2002). Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J. 21, 6505-6514.
42. Scarpignato, C., Tramacere, R., and Zappia, L. (1987). Antisecretory and antiulcer effect of the H2-receptor antagonist famotidine in the rat: Comparison with ranitidine. Br. J. Pharmacol. 92, 153-159.
43. Shoshani, T., Faerman, A., Mett, I., Zelin, E., Tenne, T., Gorodin, S., Moshel, Y., Elbaz, S., Budanov, A., Chajut, A., et al. (2002). Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol. Cell Biol. 22, 2283-2293.
44. Straub, J. A., Lipscomb, E. A., Yoshida, E. S., and Freeman, R. S. (2003). Induction of SM-20 in PC12 cells leads to increased cytochrome c levels, accumulation of cytochrome c in the cytosol, and caspase-dependent cell death. J. Neurochem. 85, 318-328.
45. Struyf, S., Gouwy, M., Dillen, C., Proost, P., Opdenakker, G., and Van, D. J. (2005). Chemokines synergize in the recruitment of circulating neutrophils into inflamed tissue. Eur. J. Immunol. 35, 1583-1591.
46. Suratt, B. T., Petty, J. M., Young, S. K., Malcolm, K. C., Lieber, J. G., Nick, J. A., Gonzalo, J. A., Henson, P. M., and Worthen, G. S. (2004). Role of the CXCR4/SDF-1 chemokine axis in circulating neutrophil homeostasis. Blood 104, 565-571.
47. Tafazoli, S., Spehar, D. D., and O'Brien, P. J. (2005). Oxidative stress mediated idiosyncratic drug toxicity. Drug Metab Rev. 37, 311-325.
48. Vial, T., Goubier, C., Bergeret, A., Cabrera, F., Evreux, J. C., and Descotes, J. (1991). Side effects of ranitidine. Drug Saf. 6, 94-117.
49. Watt, A. J., Garrison, W. D., and Duncan, S. A. (2003). HNF4: A central regulator of hepatocyte differentiation and function. Hepatology 37, 1249-1253.
50. Winzen, R., Kracht, M., Ritter, B., Wilhelm, A., Chen, C. Y., Shyu, A. B., Muller, M., Gaestel, M., Resch, K., and Holtmann, H. (1999). The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 18, 4969-4980.
51. Xiong, M., Elson, G., Legarda, D., and Leibovich, S. J. (1998). Production of vascular endothelial growth factor by murine macrophages: Regulation by hypoxia, lactate, and the inducible nitric oxide synthase pathway. Am. J. Pathol. 153, 587-598.
52. Yan, S. F., Fujita, T., Lu, J., Okada, K., Shan, Z. Y., Mackman, N., Pinsky, D. J., and Stern, D. M. (2000). Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat. Med. 6, 1355-1361.
53. Yoo, Y. G., Yeo, M. G., Kim, D. K., Park, H., and Lee, M. O. (2004). Novel function of orphan nuclear receptor Nur77 in stabilizing hypoxia-inducible factor-1alpha. J. Biol. Chem. 279, 53365-53373.