Endogenous interleukin-4 regulates glutathione synthesis following acetaminophen-induced liver injury in mice

Chemical Research in Toxicology

Volumn 25, Issue 1, 2012, Pages 83-93

  Ryan, Pauline M ^a   Bourdi, Mohammed ^a   Korrapati, Midhun C ^a   Proctor, William R ^a   Vasquez, Ronald A ^a   Yee, Steven B ^a   Quinn, Timothy D ^a   Chakraborty, Mala ^a   Pohl, Lance R ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL NUCLEUS DNA; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; INTERLEUKIN 4; MESSENGER RNA; PARACETAMOL; RECOMBINANT INTERLEUKIN 4; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL STRESS; CONTROLLED STUDY; DNA BINDING; ENZYME PHOSPHORYLATION; GENE EXPRESSION; LIVER INJURY; LIVER PROTECTION; MALE; MOUSE; NONHUMAN;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; CYTOCHROME P-450 CYP2E1; DRUG-INDUCED LIVER INJURY; GLUTAMATE-CYSTEINE LIGASE; GLUTATHIONE; INTERLEUKIN-4; JNK MITOGEN-ACTIVATED PROTEIN KINASES; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2;

MUS;

EID: 84855833450     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/tx2003992     Document Type: Article

References (62)

1. Fontana, R. J. (2008) Acute liver failure due to drugs Semin. Liver Dis. 8, 175-187 (Pubitemid 351632957)
2. Li, A. P. (2002) A review of the common properties of drugs with idiosyncratic hepatotoxicity and the 'multiple determinant hypothesis' for the manifestation of idiosyncratic toxicity Chem.-Biol. Interact. 142, 7-23 (Pubitemid 35232550)
3. FDA (2008) Recommendations for FDA Interventions to Decrease the Occurrence of Acetaminophen Hepatotoxicity (T.A.H.W. Group, Ed.) pp 1-286, Centre for Drug Evaluation and Research, Food and Drug Administration, Washington, DC.
4. Manyike, P. T., Kharasch, E. D., Kalhorn, T. F., and Slattery, J. T. (2000) Contribution of CYP2E1 and CYP3A to acetaminophen reactive metabolite formation Clin. Pharmacol. Ther. 67, 275-282 (Pubitemid 30176386)
5. Pumford, N. R., Halmes, C. N., Martin, B. M., Cook, R. J., Wagner, C., and Hinson, J. A. (1997) Covalent binding of acetaminophen to N -10-Formyl-Tetrahydrofolate dehydrogenase in mice J. Pharmacol. Exp. Ther. 280, 501-505 (Pubitemid 27171440)
6. Hinson, J. A., Roberts, D. W., and James, L. P. (2010) Mechanisms of acetaminophen-induced liver necrosis Handb. Exp. Pharmacol. 196, 368-405
7. Boelsterli, U. A. and Lim, P. L. K. (2007) Mitochondrial abnormalities-a link to idiosyncratic drug hepatotoxicity Toxicol. Appl. Pharmacol. 220, 92-107 (Pubitemid 46427861)
8. Masson, M. J., Collins, L. A., and Pohl, L. R. (2010) The role of cytokines in the mechanism of adverse drug reactions Handb. Exp. Pharmacol. 196, 195-231
9. Yee, S. B., Bourdi, M., Masson, M. J., and Pohl, L. R. (2007) Hepatoprotective role of endogenous interleukin-13 in a murine model of acetaminophen-induced liver disease Chem. Res. Toxicol. 20, 734-744 (Pubitemid 46953680)
10. Masson, M. J., Carpenter, L. D., Graf, M. L., and Pohl, L. R. (2008) Pathogenic role of natural killer T and natural killer cell in acetaminophen-induced liver injury in mice is dependent on the presence of dimethyl sulfoxide Hepatology 2 (48) 889-897
11. Imaeda, A. B., Watanabe, A., Sohail, M. A., Mahmood, S., Mohamadnejad, M., Sutterwala, F. S., Flavell, R. A., and Mehal, W. Z. (2009) Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome J. Clin. Invest. 119, 305-314
12. Masson, M. J., Collins, L. A., Carpenter, L. D., Graf, M. L., Ryan, P. M., Bourdi, M., and Pohl, L. R. (2010) Pathologic role of stressed-induced glucocorticoids in drug-induced liver injury in mice Biochem. Biophys. Res. Commun. 397, 453-458
13. Chen, G. Y., Tang, J., Zheng, P., and Liu, Y. (2009) CD24 and Siglec-10 selectively repress tissue damage-induced immune responses Science 323, 1722-1725
14. Enomoto, A., Itoh, K., Nagayoshi, E., Haruta, J., Kimura, T., O'Connor, T., Harada, T., and Yamamoto, M. (2001) High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes Toxicol. Sci. 59, 169-177 (Pubitemid 32117993)
15. Akai, S., Hosomi, H., Tsuneyama, K., Katoh, M., Nakajima, M., and Yokoi, T. (2007) Knock down of gamma-glutamylcysteine synthetase in rat causes acetaminophen-induced hepatotoxicity J. Biol. Chem. 282, 23996-24003 (Pubitemid 47328017)
16. Bourdi, M., Eiras, D. P., Holt, M. P., Webster, M. R., Reilly, T. P., Welch, K. D., and Pohl, L. R. (2007) Role of IL-6 in an IL-10 and IL-4 double knockout mouse model uniquely susceptible to acetaminophen-induced liver injury Chem. Res. Toxicol. 20, 208-216 (Pubitemid 46408857)
17. Bartolone, J. B., Sparks, K., Cohen, S. D., and Khairallah, E. A. (1987) Immunochemical detection of acetaminophen-bound liver proteins Biochem. Pharmacol. 36, 1193-1196 (Pubitemid 17083171)
18. Jaruga, B., Hong, F., Sun, R., Radaeva, S., and Gao, B. (2003) Crucial role of IL-4/STAT6 in T cell-mediated hepatitis: Up-regulating eotaxins and IL-5 and recruiting leukocytes J. Immunol. 171, 3233-3244 (Pubitemid 37093550)
19. Matthews, A. M., Roberts, D. W., Hinson, J. A., and Pumford, N. R. (1996) Acetaminophen-induced hepatotoxicity: analysis of total covalent binding versus specific binding to cysteine Drug Metab. Dispos. 24, 1192-1196 (Pubitemid 26423058)
20. Tietze, F. (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal. Biochem. 27, 502-522
21. Blazka, M. E., Bruccoleri, A., Simeonova, P. P., Germolec, D. R., Pennypacker, K. R., and Luster, M. I. (1996) Acetaminophen-induced hepatotoxicity is associated with early changes in AP-1 DNA binding activity Res. Commun. Mol. Pathol. Pharmacol. 92, 259-273 (Pubitemid 26243047)
22. Lambert, G. H. and Thorgeirsson, S. S. (1976) Glutathione in the developing mouse liver-I. Developmental curve and depletion after acetaminophen treatment Biochem. Pharmacol. 25, 1777-1781
23. Jaeschke, H. (1990) Glutathione disulphide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: The protective effect of allopurinol J. Pharmacol. Exp. Ther. 255, 935-941
24. Arnaiz, S. L., Llesuy, S., Cutrín, J. C., and Bovers, A. (1995) Oxidative stress by acute acetaminophen administration in mouse liver Free Radical Biol. Med. 19, 303-310
25. Tirmenstein, M. A. and Nelson, S. D. (1989) Subcellular binding and effects on calcium homeostasis produced by acetaminophen and a nonhepatotoxic regioisomer, 3′-hydroxyacetanilide, in mouse liver J. Biol. Chem. 264, 9814-9819 (Pubitemid 19159244)
26. Griffith, O. W. and Mulcahy, R. T. (1999) The enzymes of glutathione synthesis: γ- glutamylcysteine synthetase Adv. Enzymol. Relat. Areas Mol. Biol. 73, 209-267
27. Jeyapaul, J. and Jaiswal, A. K. (2000) Nrf-2 and c-Jun regulation of antioxidant response element (ARE) mediated expression and induction of γ-glutamylcysteine synthetase heavy subunit gene Biochem. Pharmacol. 59, 1433-1439 (Pubitemid 30177361)
28. Kitteringham, N. R., Powell, H., Clement, Y. N., Dodd, C. C., Tettey, J. N. A., Pirmohamed, P., Smith, D. A., McLellan, L. I., and Park, K. B. (2000) Hepatocellular response to chemical stress in CD-1 mice: Induction of early genes and γ-glutamylcysteine synthetase Hepatology 32, 321-333 (Pubitemid 30614665)
29. Goldring, C. E., Kitteringham, N. R., Elsby, R., Randle, L. E., Clement, Y. N., Williams, D. P., McMahon, M., Hayes, J. D., Itoh, K., Yamamoto, M., and Park, B. K. (2004) Activation of hepatic Nrf2 in vivo by acetaminophen in CD-1 mice Hepatology 39, 1267-1276 (Pubitemid 38569048)
30. Hanawa, N., Shinohara, M., Saberi, B., Gaarde, W. A., and Han, D. (2008) Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury J. Biol. Chem. 283, 13565-13577
31. Saito, C., Lemasters, J. L., and Jaeschke, H. (2010) c-Jun N-terminal kinase modulates oxidant stress and peroxynitrite formation independent of inducible nitric oxide synthase in acetaminophen hepatotoxicity Toxicol. Appl. Pharmacol. 246, 8-17
32. Guillot, C., Coathalem, H., Chetritt, J., David, A., Lowenstein, P., Gilbert, E., Tesson, L., Van Rooijen, N., Cuturi, M. C., Soulillou, J. P., and Anegon, I. (2001) Lethal hepatitis after gene transfer of IL-4 in the liver is independent of immune responses and dependent on apoptosis of hepatocytes: A rodent model of IL-4-induced hepatitis J. Immunol. 166, 5225-5235 (Pubitemid 32280739)
33. Njoku, D. B., Li, Z., Washington, N. D., Mellerson, J. L., Talor, M. V, Sharma, R., and Rose, N. R. (2009) Suppressive and pro-inflammatory roles for IL-4 in the pathogenesis of experimental drug-induced liver injury Eur. J. Immunol. 39, 1652-1663
34. Aithal, G. P., Ramsay, L., Daly, A. K., Sonchit, N., Leatherart, J. B. S., Alexander, G., Kenna, G. J., Caldwell, J., and Day, C. P. (2004) Hepatic adducts, circulating antibodies and cytokine polymorphisms in patients with diclofenac hepatotoxicity Hepatology 39, 1430-1440 (Pubitemid 38569066)
35. La Flamme, A. C., Patton, E. A., Bauman, B., and Pearce, E. J. (2001) IL-4 plays a crucial role in regulating oxidative damage in the liver during schistosomiasis J. Immunol. 166, 1903-1911 (Pubitemid 32114677)
36. Kato, A., Yoshidome, H., Edwards, M. J., and Lentsch, A. B. (2000) Reduced hepatic ischemia/reperfusion injury by IL-4: potential anti-inflammatory role of STAT6 Inflammation Res. 49, 275-279 (Pubitemid 30451610)
37. Junttila, I. S., Mizukami, K, Dickensheets, H., Meier-Schellersheim, M., Yamane, H., Donnelly, R. P., and Paul, W. E. (2008) Tuning sensitivity to IL-4 and IL-13: differential expression of IL-4Rα, IL-13Rα1, and γc regulates relative cytokine sensitivity J. Exp. Med. 205, 2595-2608
38. Galizzi, J. P., Zuber, C. E., Cabrillat, H., Djossou, O., and Banchereau, J. (1989) Internalization of human interleukin-4 and transient down-regulation of its receptor in the CD23-inducible Jijoye cells J. Biol. Chem. 264, 6984-6989 (Pubitemid 19114814)
39. Bourdi, M., Masubuchi, Y., Reilly, T. P., Amouzadeh, H. R., Martin, J. L., and Pohl, L. R. (2002) Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase Hepatology 35, 289-298 (Pubitemid 34106367)
40. Abdel-Razzak, Z., Loyer, P., Fautrel, A., Gautier, J., Corcos, L., Turlin, B., Beune, P., and Guillouzo, A. (1993) Cytokines down-regulate expression of major cytochrome P-450 enzymes in adult human hepatocytes in primary culture Mol. Pharmacol. 44, 707-715 (Pubitemid 23317282)
41. Lagadic-Gossmann, D., Lerche, C., Rissel, M., Joannard, F., Galisteo, M., Guillouzo, A., and Corcos, L. (2000) The induction of the human hepatic CYP2E1 gene by interleukin-4 is transcriptional and regulated by protein kinase C Cell Biol. Toxicol. 16, 221-233
42. Wendel, A. and Cikryt, P. (1981) Binding of paracetamol metabolites to mouse liver glutathione S-transferases Res. Commun. Chem. Pathol. Pharmacol. 33, 463-473 (Pubitemid 11014884)
43. Backos, D. S., Fritz, K. S., Roede, J. R., Petersen, D. R., and Franklin, C. C. (2011) Posttranslational modification and regulation of glutamate-cysteine ligase by the α,β-unsaturated aldehyde 4-hydroxy-2-noneal Free Radical Biol. Med. 50, 14-26
44. 12,14-PGJ2 is metabolized by hepG2 cells via conjugation with glutathione Chem. Res. Toxicol. 20, 1528-1535 (Pubitemid 350057223)
45. Nelson, S. D., Timenstein, M. A., Rashed, M. S., and Myers, T. G. (1991) Acetaminophen protein thiol modification Adv. Exp. Med. Biol. 283, 579-588
46. Richman, P. G. and Meister, A. (1975) Regulation of gamma-glutamyl- cysteine synthetase by nonallosteric feedback inhibition by glutathione J. Biol. Chem. 250, 1422-1426
47. Jain, A. K. and Jaiswal, A. K. (2007) GSK3β acts up stream of Fyn kinase in regulation of nuclear transport and degradation of NE-E2 related factor 2 J. Biol. Chem. 282, 16502-16510 (Pubitemid 47100395)
48. Bogoyevitch, M. A. and Kobe, B. (2006) Uses for JNK: the many and varied substrates of the c-Jun N-terminal kinases Microbiol. Mol. Biol. Rev. 170, 1061-1095 (Pubitemid 44958264)
49. Baker, S. J., Kerppola, T. K., Luk, D., Vandenberg, M. T., Marshak, D. R., Curran, T., and Abate, C. (1992) Jun is phosphorylated by several protein kinases at the same sites that are modified in serum-stimulated fibroblast Mol. Cell. Biol. 12, 4694-4705
50. Bode, A. M. and Dong, Z. (2007) The functional contrariety of JNK Mol. Carcinog. 46, 591-598 (Pubitemid 47255173)
51. Arrda, S. and Ho, J. L. (1992) IL-4 receptor signal transduction in human monocytes is associated with protein kinase C translocation J. Imumunol. 149, 1258-1264
52. Jones, D. P. (2006) Redefining oxidative stress Antioxid. Redox Signaling 8, 1865-1879 (Pubitemid 44726359)
53. Nakawagawa, H., Maeda, S., Hikiba, Y., Ohmae, T., Shibata, W., Yanai, A., Sakamoto, K., Ogura, K., Noguchi, T., Karin, M., Ichijo, H., and Omata, M. (2008) Deletion of apoptosis signal-regulating kinase 1 attenuates acetaminophen-induced liver injury by inhibiting c-Jun N-terminal kinase activation Gastroenterology 135, 1311-1321
54. Shinohara, M., Ybanez, M. D., Win, S., Than, T. A., Jain, S., Gaarde, W. A., Han, D., and Kaplowitz, N. (2010) Silencing glycogen synthase kinase-3β inhibits acetaminophen hepatoxicity and attenuates JNK activation and loss of glutamate cysteine ligase and myeloid cell leukemia sequence 1 J. Biol. Chem. 285, 8244-8255
55. Uehara, T., Benett, B., Sakata, S., Satoh, Y., Bilter, G., Westwick, J., and Brenner, D. A. (2005) JNK mediates hepatitis ischemia perfusion injury Hepatology 42, 850-859 (Pubitemid 40693202)
56. Akaiwa, M., Yu, B., Umeshita-suyama, R., Terada, N., Suto, H., Koga, T., Arima, K., Matsushita, S., Saito, H., Ogawa, H., Hamasaki, N, Ohshima, K., and Izuhara, K. (2001) Localization of human interleukin-13 receptor in non-haematopoietic cells Cytokine 13, 75-84 (Pubitemid 32579312)
57. Klein, W., Tromm, A., Griga, T., Fricke, H., Folwaczny, C., Hocke, M., Eitner, K., Marx, M, Duerig, N., and Epplen, J. T. (2001) Interleukin-4 and interleukin-4 receptor gene polymorphisms in inflammatory bowel diseases Genes Immun. 5, 287-289 (Pubitemid 33681715)
58. Steinke, J. W. and Borish, L. (2001) Th2 cytokines and asthma, interleukin-4: its role in the pathogenesis of asthma, and targeting it for asthma treatment with interleukin-4 receptor antagonists Respir. Res. 2, 66-77
59. Li-Weber, M. and Krammer, P. H. (2003) Regulation of IL-4 gene expression by T cells and therapeutic perspectives Nature 3, 534-543 (Pubitemid 37328673)
60. Cianferoni, A., Schroeder, T., Kim, J., Schmidt, J. W., Lichtenstein, L. M., Georas, S. N., and Casolaro, V. (2001) Selective inhibition of interleukin-4 gene expression in human T cells by aspirin Blood 97, 1742-1749 (Pubitemid 32217242)
61. Townsend, D. M., Tew, K. D., and Tapiero, H. (2003) The importance of glutathione in human disease Biomed. Pharmacother. 57, 145-155 (Pubitemid 36740460)
62. Dröge, W. and Breitkreutz, R. (2000) Glutathione and immune function Proc. Nutr. Soc. 59, 595-600 (Pubitemid 32002990)