Amiodarone exposure during modest inflammation induces idiosyncrasy-like liver injury in rats: Role of tumor necrosis factor-alpha

Toxicological Sciences

Volumn 125, Issue 1, 2012, Pages 126-133

  Lu, Jingtao ^a,b   Jones, A Daniel ^a,b   Harkema, Jack R ^b   Roth, Robert A ^b,c   Ganey, Patricia E ^b,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Amiodarone hepatotoxicity; Drug metabolism; Idiosyncratic adverse drug reactions; Inflammation; Lipopolysaccharide; Tumor necrosis factor alpha

Indexed keywords

ALANINE AMINOTRANSFERASE; AMIODARONE; ASPARTATE AMINOTRANSFERASE; BILE ACID; LIPOPOLYSACCHARIDE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOTOXICITY; DRUG ACCUMULATION; DRUG METABOLISM; ENZYME ACTIVITY; IN VIVO STUDY; INFLAMMATION; LIVER INJURY; LIVER TOXICITY; NONHUMAN; RAT; SIGNAL TRANSDUCTION; TOXICITY TESTING;

ANIMALIA; RATTUS;

EID: 84555195380     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr266     Document Type: Article

References (43)

1. Agoston, M., Orsi, F., Feher, E., Hagymasi, K., Orosz, Z., Blazovics, A., Feher, J., and Vereckei, A.Agoston, M., Orsi, F., Feher, E., Hagymasi, K., Orosz, Z., Blazovics, A., Feher, J., and Vereckei, A. (2003). Silymarin and vitamin E reduce amiodarone-induced lysosomal phospholipidosis in rats. Toxicology 190, 231-241.
2. Babatin, M., Lee, S. S., and Pollak, P. T. (2008). Amiodarone hepatotoxicity. Curr. Vasc. Pharmacol. 6, 228-236.
3. Beutler, B., and Kruys, V. (1995). Lipopolysaccharide signal transduction, regulation of tumor necrosis factor biosynthesis, and signaling by tumor necrosis factor itself. J. Cardiovasc. Pharmacol. 25(Suppl. 2), S1-S8.
4. 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.
5. Deng, X., Stachlewitz, R. F., Liguori, M. J., Blomme, E. A., 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.
6. Dugan, C. M., MacDonald, A. E., Roth, R. A., and Ganey, P. E. (2010). A mouse model of severe halothane hepatitis based on human risk factors. J. Pharmacol. Exp. Ther. 333, 364-372.
7. Elsherbiny, M. E., El-Kadi, A. O., and Brocks, D. R. (2008). The metabolism of amiodarone by various CYP isoenzymes of human and rat, and the inhibitory influence of ketoconazole. J. Pharmacokinet. Pharmacodyn. Sci. 11, 147-159.
8. Fromenty, B., Fisch, C., Berson, A., Letteron, P., Larrey, D., and Pessayre, D. (1990a). Dual effect of amiodarone on mitochondrial respiration. Initial protonophoric uncoupling effect followed by inhibition of the respiratory chain at the levels of complex I and complex II. J. Pharmacol. Exp. Ther. 255, 1377-1384.
9. Fromenty, B., Fisch, C., Labbe, G., Degott, C., Deschamps, D., Berson, A., Letteron, P., and Pessayre, D. (1990b). Amiodarone inhibits the mitochondrial beta-oxidation of fatty acids and produces microvesicular steatosis of the liver in mice. J. Pharmacol. Exp. Ther. 255, 1371-1376.
10. Futamura, Y. (1996). Effect of amiodarone on cytokine release and on enzyme activities of mouse alveolar macrophages, bone marrow macrophages, and blood monocytes. J. Toxicol. Sci. 21, 125-134.
11. 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.
12. Gross, S. A., Bandyopadhyay, S., Klaunig, J. E., and Somani, P. (1989). Amiodarone and desethylamiodarone toxicity in isolated hepatocytes in culture. Proc. Soc. Exp. Biol. Med. 190, 163-169.
13. Ha, H. R., Bigler, L., Wendt, B., Maggiorini, M., and Follath, F. (2005). Identification and quantitation of novel metabolites of amiodarone in plasma of treated patients. Eur. J. Pharm. Sci. 24, 271-279.
14. Lewis, J. H., Ranard, R. C., Caruso, A., Jackson, L. K., Mullick, F., Ishak, K. G., Seeff, L. B., and Zimmerman, H. J. (1989). Amiodarone hepatotoxicity: Prevalence and clinicopathologic correlations among 104 patients. Hepatology 9, 679-685.
15. 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.
16. Luyendyk, J. P., Shaw, P. J., Green, C. D., Maddox, J. F., Ganey, P. E., and Roth, R. A. (2005). Coagulation-mediated hypoxia and neutrophil-dependent hepatic injury in rats given lipopolysaccharide and ranitidine. J. Pharmacol. Exp. Ther. 314, 1023-1031.
17. O'Sullivan, J. J., McCarthy, P. T., and Wren, C. (1995). Differences in amiodarone, digoxin, flecainide and sotalol concentrations between antemortem serum and femoral postmortem blood. Hum. Exp. Toxicol. 14, 605-608.
18. Pollak, P. T., Bouillon, T., and Shafer, S. L. (2000). Population pharmacokinetics of long-term oral amiodarone therapy. Clin. Pharmacol. Ther. 67, 642-652.
19. Pollak, P. T., and You, Y. D. (2003). Monitoring of hepatic function during amiodarone therapy. Am. J. Cardiol. 91, 613-616.
20. Punithavathi, D., Venkatesan, N., and Babu, M. (2003). Protective effects of curcumin against amiodarone-induced pulmonary fibrosis in rats. Br. J. Pharmacol. 139, 1342-1350.
21. Rätz Bravo, A. E., Drewe, J., Schlienger, R. G., Krähenbühl, S., Pargger, H., and Ummenhofer, W. (2005). Hepatotoxicity during rapid intravenous loading with amiodarone: Description of three cases and review of the literature. Crit. Care Med. 33, 128-134.
22. Reinhart, P. G., and Gairola, C. G. (1997). Amiodarone-induced pulmonary toxicity in Fischer rats: Release of tumor necrosis factor alpha and transforming growth factor beta by pulmonary alveolar macrophages. J. Toxicol. Environ. Health 52, 353-365.
23. 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.
24. Rotmensch, H. H., Belhassen, B., Swanson, B. N., Shoshani, D., Spielman, S. R., Greenspon, A. J., Greenspan, A. M., Vlasses, P. H., and Horowitz, L. N. (1984). Steady-state serum amiodarone concentrations: Relationships with antiarrhythmic efficacy and toxicity. Ann. Intern. Med. 101, 462-469.
25. Sewer, M. B., Koop, D. R., and Morgan, E. T. (1997). Differential inductive and suppressive effects of endotoxin and particulate irritants on hepatic and renal cytochrome P-450 expression. J. Pharmacol. Exp. Ther. 280, 1445-1454.
26. Shaw, P. J., Fullerton, A. M., Scott, M. A., Ganey, P. E., and Roth, R. A. (2009a). The role of the hemostatic system in murine liver injury induced by coexposure to lipopolysaccharide and trovafloxacin, a drug with idiosyncratic liability. Toxicol. Appl. Pharmacol. 236, 293-300.
27. Shaw, P. J., Ganey, P. E., and Roth, R. A. (2009b). Tumor necrosis factor alpha is a proximal mediator of synergistic hepatotoxicity from trovafloxacin/ lipopolysaccharide coexposure. J. Pharmacol. Exp. Ther. 328, 62-68.
28. 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.
29. Shayeganpour, A., Hamdy, D. A., and Brocks, D. R. (2008). Pharmacokinetics of desethylamiodarone in the rat after its administration as the preformed metabolite, and after administration of amiodarone. Biopharm. Drug Dispos. 29(3), 159-166.
30. Singh, B. N. (1996). Antiarrhythmic actions of amiodarone: A profile of a paradoxical agent. Am. J. Cardiol. 78, 41-53.
31. Spaniol, M., Bracher, R., Ha, H. R., Follath, F., and Krähenbühl, S. (2001). Toxicity of amiodarone and amiodarone analogues on isolated rat liver mitochondria. J. Hepatol. 35, 628-636.
32. Stadler, K., Ha, H. R., Ciminale, V., Spirli, C., Saletti, G., Schiavon, M., Bruttomesso, D., Bigler, L., Follath, F., Pettenazzo, A., and Baritussio, A. (2008). Amiodarone alters late endosomes and inhibits SARS coronavirus infection at a post-endosomal level. Am. J. Respir. Cell Mol. Biol. 39, 142-149.
33. Talajic, M., DeRoode, M. R., and Nattel, S. (1987). Comparative electrophysiologic effects of intravenous amiodarone and desethylamiodarone in dogs: Evidence for clinically relevant activity of the metabolite. Circulation 75, 265-271.
34. Teoh, N., Field, J., Sutton, J., and Farrell, G. (2004). Dual role of tumor necrosis factor-alpha in hepatic ischemia-reperfusion injury: Studies in tumor necrosis factor-alpha gene knockout mice. Hepatology 39, 412-421.
35. Tukov, F. F., Luyendyk, J. P., Ganey, P. E., and Roth, R. A. (2007). The role of tumor necrosis factor alpha in lipopolysaccharide/ranitidine-induced inflammatory liver injury. Toxicol. Sci. 100, 267-280.
36. Uetrecht, J. (2007). Idiosyncratic drug reactions: Current understanding. Annu. Rev. Pharmacol. Toxicol. 47, 513-539.
37. Waldhauser, K. M., Török, M., Ha, H. R., Thomet, U., Konrad, D., Brecht, K., Follath, F., and Krähenbühl, S. (2006). Hepatocellular toxicity and pharmacological effect of amiodarone and amiodarone derivatives. J. Pharmacol. Exp. Ther. 319, 1413-1423.
38. Waring, J. F., Liguori, M. J., Luyendyk, J. P., Maddox, J. F., Ganey, P. E., Stachlewitz, R. F., North, C., Blomme, E. A., and Roth, R. A. (2006). Microarray analysis of lipopolysaccharide potentiation of trovafloxacininduced liver injury in rats suggests a role for proinflammatory chemokines and neutrophils. J. Pharmacol. Exp. Ther. 316, 1080-1087.
39. Wullaert, A., van Loo, G., Heyninck, K., and Beyaert, R. (2007). Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: Effects on liver homeostasis and beyond. Endocr. Rev. 28, 365-386.
40. Yin, M., Wheeler, M. D., Kono, H., Bradford, B. U., Gallucci, R. M., Luster, M. I., and Thurman, R. G. (1999). Essential role of tumor necrosis factor alpha in alcohol-induced liver injury in mice. Gastroenterology 117, 942-952.
41. Young, R. A., and Mehendale, H. M. (1989). Effects of short-term and longterm administration of amiodarone on hepatobiliary function in male rats. J. Appl. Toxicol. 9, 407-412.
42. Zou, W., Beggs, K. M., Sparkenbaugh, E. M., Jones, A. D., Younis, H. S., Roth, R. A., and Ganey, P. E. (2009a). 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.
43. Zou, W., Devi, S. S., Sparkenbaugh, E., Younis, H. S., Roth, R. A., and Ganey, P. E. (2009b). Hepatotoxic interaction of sulindac with lipopolysaccharide: Role of the hemostatic system. Toxicol. Sci. 108, 184-193.