Development of a novel mouse model of amodiaquine-induced liver injury with a delayed onset

Journal of Immunotoxicology

Volumn 12, Issue 3, 2015, Pages 247-260

  Metushi, Imir G ^a   Cai, Ping ^b   Dervovic, Dzana ^b   Liu, Feng ^b   Lobach, Alexandra ^b   Nakagawa, Tetsuya ^b   Uetrecht, Jack ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Covalent binding; Drug induced liver injury; Immune tolerance; Immune mediated; Reactive metabolite

Indexed keywords

ALANINE AMINOTRANSFERASE; AMODIAQUINE; CD11B ANTIGEN; CD4 ANTIGEN; CD69 ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; GRANULOCYTE COLONY STIMULATING FACTOR; HERMES ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1ALPHA; INTERLEUKIN 3; INTERLEUKIN 5; L SELECTIN; PROGRAMMED DEATH 1 RECEPTOR; RAG1 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; HOMEODOMAIN PROTEIN; RAG-1 PROTEIN;

ADAPTIVE IMMUNITY; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL PROLIFERATION; CONTROLLED STUDY; COVALENT BOND; DOWN REGULATION; FEMALE; IDIOSYNCRATIC DRUG INDUCED LIVER INJURY; IMMUNOLOGICAL TOLERANCE; INTESTINE; KIDNEY; LIVER; LIVER HISTOLOGY; LYMPHOCYTIC INFILTRATION; MALE; MONONUCLEAR CELL; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN; T LYMPHOCYTE ACTIVATION; TOXIC HEPATITIS; UPREGULATION; AGRANULOCYTOSIS; ANIMAL; C57BL MOUSE; DISEASE COURSE; DRUG EFFECTS; GENETICS; HUMAN; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; METABOLISM; MUTANT MOUSE STRAIN; PATHOLOGY;

ANIMALIA; MUS;

ADAPTIVE IMMUNITY; AGRANULOCYTOSIS; ALANINE TRANSAMINASE; AMODIAQUINE; ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DISEASE PROGRESSION; DRUG-INDUCED LIVER INJURY; FEMALE; HOMEODOMAIN PROTEINS; HUMANS; IMMUNE TOLERANCE; KILLER CELLS, NATURAL; LIVER; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; MALE; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; MODELS, ANIMAL;

EID: 84928604507     PISSN: 1547691X     EISSN: 15476901     Source Type: Journal    
DOI: 10.3109/1547691X.2014.934977     Document Type: Article

References (42)

1. Bjorkdahl, O., Barber, K. A., Brett, S. J., et al. 2003. Characterization of CC-chemokine receptor 7 expression on murine T-cells in lymphoid tissues. Immunology 110:170-179.
2. Bjornsson, E. 2010. Review article: Drug-induced liver injury in clinical practice. Aliment Pharmacol. Ther. 32:3-13.
3. Bowen, D. G., Mccaughan, G. W., and Bertolino, P. 2005. Intrahepatic immunity: A tale of two sites? Trends Immunol. 26:512-517.
4. Chao, C. C., Jensen, R., and Dailey, M. O. 1997. Mechanisms of L-selectin regulation by activated T-cells. J. Immunol. 159: 1686-1694.
5. Clarke, J. B., Maggs, J. L., Kitteringham, N. R., and Park, B. K. 1990. Immunogenicity of amodiaquine in the rat. Int. Arch. Allergy Appl. Immunol. 91:335-342.
6. Clarke, J. B., Neftel, K., Kitteringham, N. R., and Park, B. K. 1991. Detection of antidrug IgG antibodies in patients with adverse drug reactions to amodiaquine. Int. Arch. Allergy Appl. Immunol. 95: 369-375.
7. De Valle, M. B., Av Klinteberg, V., Alem, N., et al. 2006. Drug-induced liver injury in a Swedish University hospital out-patient hepatology clinic. Aliment Pharmacol. Ther. 24:1187-1195.
8. Foureau, D. M., Walling, T. L., Kleiner, D. E., et al. 2012. Profiles of leukocytes infiltrating livers of subjects with drug-induced liver injury (DILI). Hepatology 56:596A (Abstract #827).
9. Hatton, C. S., Peto, T. E., Bunch, C., et al. 1986. Frequency of severe neutropenia associated with amodiaquine prophylaxis against malaria. Lancet 1:411-414.
10. Johnson, P., and Ruffell, B. 2009. CD44 and its role in inflammation and inflammatory diseases. Inflamm. Allergy Drug Targets 8: 208-220.
11. Koo, G. C., Dumont, F. J., Tutt, M., et al. 1986. The NK-1.1 mouse: A model to study differentiation of murine NK cells. J. Immunol. 137: 3742-3747.
12. Lang, P. A., Lang, K. S., Xu, H. C., et al. 2012. Natural killer cell activation enhances immune pathology and promotes chronic infection by limiting CD8+ T-cell immunity. Proc. Natl. Acad. Sci. USA 109: 1210-1215.
13. Larrey, D., Castot, A., Pessayre, D., et al. 1986. Amodiaquineinduced hepatitis. A report of seven cases. Ann. Int. Med. 104: 801-803.
14. Li, X. Q., Bjorkman, A., Andersson, T. B., et al. 2002. Amodiaquine clearance and its metabolism to N-desethylamodiaquine is mediated by CYP2C8: A new high affinity and turnover enzyme-specific probe substrate. J. Pharmacol. Exp. Ther. 300: 399-407.
15. Lobach, A., and Uetrecht, J. 2014. Involvement of myeloperoxidase and NADPH oxidase in the covalent binding of amodiaquine and clozapine to neutrophils: Implications for drug-induced agranulocytosis. Chem. Res. Toxicol. 27:699-709.
16. Lucena, M. I., Andrade, R. J., Kaplowitz, N., et al. 2009. Phenotypic characterization of idiosyncratic drug-induced liver injury: Influence of age and sex. Hepatology 49:2001-2009.
17. Maggs, J. L., Kitteringham, N. R., Breckenridge, A. M., and Park, B. K. 1987. Autoxidative formation of a chemically-reactive intermediate from amodiaquine, a myelotoxin and hepato-toxin in man. Biochem. Pharmacol. 36:2061-2062.
18. Maggs, J. L., Tingle, M. D., Kitteringham, N. R., and Park, B. K. 1988. Drug-protein conjugates-XIV. Mechanisms of formation of proteinarylating intermediates from amodiaquine, a myelotoxin and hepatotoxin in man. Biochem. Pharmacol. 37:303-311.
19. Masson, M. J., Carpenter, L. D., Graf, M. L., and Pohl, L. R. 2008. Pathogenic role of natural killer T-and natural killer cells in acetaminophen-induced liver injury in mice is dependent on the presence of dimethyl sulfoxide. Hepatology 48:889-897.
20. Metushi, I. G., Nakagawa, T., and Uetrecht, J. 2012. Direct oxidation and covalent binding of isoniazid to rodent liver and human hepatic microsomes: Humans are more like mice than rats. Chem. Res. Toxicol. 25:2567-2576.
21. Metushi, I. G., Sanders, C., Lee, W. M., and Uetrecht, J. 2013. Detection of anti-isoniazid and anti-cyp antibodies in patients with isoniazidinduced liver failure. Hepatology 59:1084-1093.
22. Metushi, I. G., and Uetrecht, J. (2013). Isoniazid-induced liver injury and immune response in mice. J. Immunotoxicol. (Epub ahead of print).
23. Mishra, S. K., Singh, P., and Rath, S. K. 2011. A study of toxicity and differential gene expression in murine liver following exposure to anti-malarial drugs: Amodiaquine and sulphadoxine-pyrimethamine. Malaria J. 10:109.
24. Neftel, K. A., Woodtly, W., Schmid, M., et al. 1986. Amodiaquine induced agranulocytosis and liver damage. Br. Med. J. 292:721-723.
25. Ng, W., Lobach, A. R., Zhu, X., et al. 2012. Animal models of idiosyncratic drug reactions. Adv. Pharmacol. 63:81-135.
26. Pardoll, D. M. 2012. The blockade of immune checkpoints in cancer immunotherapy. Nat. Rev. Cancer 12:252-264.
27. Pure, E., and Cuff, C. A. 2001. A crucial role for CD44 in inflammation. Trends Mol. Med. 7:213-221.
28. Rouveix, B., Coulombel, L., Aymard, J. P., et al. 1989. Amodiaquineinduced immune agranulocytosis. Br. J. Hematol. 71:7-11.
29. Russo, M. W., Galanko, J. A., Shrestha, R., et al. 2004. Liver transplantation for acute liver failure from drug induced liver injury in the United States. Liver Transplant. 10:1018-1023.
30. Sallusto, F., Geginat, J., and Lanzavecchia, A. 2004. Central memory and effector memory T-cell subsets: Function, generation, and maintenance. Annu. Rev. Immunol. 22:745-763.
31. Senior, J. R. 2007. Drug hepatotoxicity from a regulatory perspective. Clin. Liver Dis. 11:507-524.
32. Sgro, C., Clinard, F., Ouazir, K., et al. 2002. Incidence of drug-induced hepatic injuries: A French population-based study. Hepatology 36: 451-455.
33. Shimizu, S., Atsumi, R., Itokawa, K., et al. 2009. Metabolism-dependent hepatotoxicity of amodiaquine in glutathione-depleted mice. Arch. Toxicol. 83:701-707.
34. Siegelman, M. H., Degrendele, H. C., and Estess, P. 1999. Activation and interaction of CD44 and hyaluronan in immunological systems. J. Leukocyte Biol. 66:315-321.
35. Singer, A. J., and Clark, R. A. 1999. Cutaneous wound healing. New Engl. J. Med. 341:738-746.
36. Tian, Z., Chen, Y., and Gao, B. 2013. Natural killer cells in liver disease. Hepatology 57:1654-1662.
37. Tujios, S., and Fontana, R. J. 2011. Mechanisms of drug-induced liver injury: From bedside to bench. Nat. Rev. Gastroenterol. Hepatol. 8: 202-211.
38. Uetrecht, J. 2009. Immunoallergic drug-induced liver injury in humans. Sem. Liver Dis. 29:383-392.
39. Watkins, P. B. 2005. Idiosyncratic liver injury: Challenges and approaches. Toxicol. Pathol. 33:1-5.
40. White, N. J., Looareesuwan, S., Edwards, G., et al. 1987. Pharmacokinetics of intravenous amodiaquine. Br. J. Clin. Pharmacol. 23:127-135.
41. Yang, S., Liu, F., Wang, Q. J., et al. 2011. The shedding of CD62L (L-selectin) regulates the acquisition of lytic activity in human tumor reactive T-lymphocytes. PLoS One 6:e22560.
42. Ziegler, S. F., Ramsdell, F., and Alderson, M. R. 1994. The activation antigen CD69. Stem Cells 12:456-465.