Natural killer cells mediate severe liver injury in a murine model of halothane hepatitis

Toxicological Sciences

Volumn 120, Issue 2, 2011, Pages 507-518

  Dugan, Christine M ^a   Fullerton, Aaron M ^b   Roth, Robert A ^a,b   Ganey, Patricia E ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Female sex; Halothane; Idiosyncratic adverse drug reactions; Inflammation; NK cells

Indexed keywords

CD69 ANTIGEN; GAMMA INTERFERON; HALOTHANE; NATURAL KILLER CELL RECEPTOR; PERFORIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CELL ACTIVITY; CONTROLLED STUDY; DISEASE SEVERITY; DRUG EFFECT; DRUG RESPONSE; FEMALE; HEPATITIS; LIVER CELL; LIVER INJURY; LIVER TOXICITY; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; SEX DIFFERENCE;

MURINAE; MUS; RODENTIA;

EID: 79953084405     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfr005     Document Type: Article

References (54)

1. Berke, G. (1995). The CTL's kiss of death. Cell 81, 9-12.
2. Bosch, F. X., Ribes, J., Cleries, R., and Diaz, M. (2005). Epidemiology of hepatocellular carcinoma. Clin. Liver Dis. 9, 191-211.
3. Bourdi, M., Amouzadeh, H., Rushmore, T., Martin, J., and Pohl, L. (2001). Halothane-induced liver injury in outbred guinea pigs: role of trifluoracetylated protein adducts in animal susceptibility. Chemical Res. Toxicol. 14, 362-370.
4. Cerwenka, A., Bakker, A. B., McClanahan, T., Wagner, J., Wu, J., Phillips, J. H., and Lanier, L. L. (2000). Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12, 721-727.
5. Chalasani, N., and Bjornsson, E. (2010). Risk factors for idiosyncratic druginduced liver injury. Gastroenterology 138, 2246-2259.
6. Cheng, L., You, Q., Yin, H., Holt, M., Franklin, C., and Ju, C. (2009). Effect of polyI: C cotreatment on halothane-induced liver injury in mice. Hepatology 49, 215-226.
7. Cheng, L., You, Q., Yin, H., Holt, M. P., and Ju, C. (2010). Involvement of natural killer T cells in halothane-induced liver injury in mice. Biochem. Pharmacol. 80, 255-261.
8. Curran, E. M., Berghaus, L. J., Vernetti, N. J., Saporita, A. J., Lubahn, D. B., and Estes, D. M. (2001). Natural killer cells express estrogen receptoralpha and estrogen receptor-beta and can respond to estrogen via a non-estrogen receptor-alpha-mediated pathway. Cell Immunol. 214(1), 12-20.
9. 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.
10. Eghtesadi-Araghi, P., Sohrabpour, A., Vahedi, H., and Saberi-Firoozi, M. (2008). Halothane hepatitis in Iran: a review of 59 cases. World J. Gastroenterol. 14, 5322-5326.
11. Farrar, M. A., and Schreiber, R. D. (1993). The molecular cell biology of interferon-gamma and its receptor. Annu. Rev. Immunol. 11, 571-611.
12. Farrell, G. C., Frost, L., Tapner, M., Field, J., Weltman, M., and Mahoney, J. (1996). Halothane-induced liver injury in guinea-pigs: importance of cytochrome P450 enzyme activity and hepatic blood flow. J. Gastroenterol. Hepatol. 11, 594-601.
13. Gao, B. (2005). Cytokines, STATs and liver disease. Cell Mol. Immunol. 2, 92-100.
14. Gilliver, S. C. (2010). Sex steroids as inflammatory regulators. J. Steroid Biochem. Mol. Biol. 120(2-3), 105-115.
15. Gleimer, M., and Parham, P. (2003). Stress management: MHC class I and class I-like molecules as reporters of cellular stress. Immunity 19, 469-477.
16. Goldman, J. M., Murr, A. S., and Cooper, R. L. (2007). The rodent estrous cycle: characterization of vaginal cytology and its utility in toxicological studies. Birth Defects Res. B Dev. Reprod. Toxicol. 80(2), 84-97.
17. Graff, R. J., Lappe, M. A., and Snell, G. D. (1969). The influence of the gonads and adrenal glands on the immune response to skin grafts. Transplantation 7, 105-111.
18. Gregoire, C., Chasson, L., Luci, C., Tomasello, E., Geissmann, F., Vivier, E., and Walzer, T. (2007). The trafficking of natural killer cells. Immunol. Rev. 220, 169-182.
19. Habu, S., Fukui, H., Shimamura, K., Kasai, M., Nagai, Y., Okumura, K., and Tamaoki, N. (1981). In vivo effects of anti-asialo GM1. I. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice. J. Immunol. 127, 34-38.
20. Hao, S., Zhao, J., Zhou, J., Zhao, S., Hu, Y., and Hou, Y. (2007). Modulation of 17beta-estradiol on the number and cytotoxicity of NK cells in vivo related to MCM and activating receptors. Int. Immunopharmacol. 7(13), 1765-1775.
21. Heinzel, F. P., Sadick, M. D.,Holaday,B. J., Coffman, R.L., and Locksley,R.M. (1989). Reciprocal expression of interferon gamma or interleukin 4 during the resolution or progression of murine leishmaniasis. Evidence for expansion of distinct helper T cell subsets. J. Exp. Med. 169, 59-72.
22. Hirasawa, K., and Enosawa, S. (1989). Sex differences in the prolongation of allogeneic skin graft survival in rats treated with cyclosporin A: effects of orchiectomy and pregnancy. Transplant. Proc. 21(1 Pt 1), 881-884.
23. 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.
24. Jamieson, A. M., Diefenbach, A., McMahon, C. W., Xiong, N., Carlyle, J. R., and Raulet, D. H. (2002). The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17, 19-29.
25. Jinushi, M., Takehara, T., Tatsumi, T., Kanto, T., Groh, V., Spies, T., Kimura, R., Miyagi, T., Mochizuki, K., Sasaki, Y., and Hayashi, N. (2003). Expression and role of MICA and MICB in human hepatocellular carcinomas and their regulation by retinoic acid. Int. J. Cancer. 104(3), 354-361.
26. Kasai, M., Iwamori, M., Nagai, Y., Okumura, K., and Tada, T. (1980). A glycolipid on the surface of mouse natural killer cells. Eur. J. Immunol. 10, 175-180.
27. Kellokumpu-Lehtinen, P., Iisalo, E., and Nordman, E. (1989). Hepatotoxicity of paracetamol in combination with interferon and vinblastine. Lancet 1, 1143.
28. Kenna, J. G., Satoh, H., Christ, D. D., and Pohl, L. R. (1988). Metabolic basis for a drug hypersensitivity: antibodies in sera from patients with halothane hepatitis recognize liver neoantigens that contain the trifluoroacetyl group derived from halothane. J. Pharmacol. Exp. Ther. 245, 1103-1109.
29. Lee, W. M. (2008). Etiologies of acute liver failure. Semin. Liver Dis. 28(2), 142-152.
30. Liu, Z. X., Govindarajan, S., Okamoto, S., and Dennert, G. (2000). NK cells cause liver injury and facilitate the induction of T cell-mediated immunity to a viral liver infection. J. Immunol. 164, 6480-6486.
31. Liu, Z. X., and Kaplowitz, N. (2006). Role of innate immunity in acetaminophen-induced hepatotoxicity. Expert. Opin. Drug Metab. Toxicol. 2, 493-503.
32. Ljunggren, H. G., and Karre, K. (1986). Experimental strategies and interpretations in the analysis of changes in MHC gene expression during tumour progression. Opposing influences of T cell and natural killer mediated resistance? J. Immunogenet. 13(2-3), 141-151.
33. Lunam, C. A., Cousins, M. J., and Hall, P. D. (1985). Guinea-pig model of halothane-associated hepatotoxicity in the absence of enzyme induction and hypoxia. J. Pharmacol. Exp. Ther. 232, 802-809.
34. 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 acetaminopheninduced liver injury in mice is dependent on the presence of dimethyl sulfoxide. Hepatology 48, 889-897.
35. 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.
36. Medzhitov, R., and Janeway, C., Jr. (2000). Innate immune recognition: mechanisms and pathways. Immunol. Rev. 173, 89-97.
37. Mushin, W. W., Rosen, M., Bowen, D. J., and Campbell, H. (1971). Posthalothane jaundice in relation to previous administration of halothane. BMJ 3, 18-22.
38. Nemeth, E., Baird, A. W., and O'Farrelly, C. (2009). Microanatomy of the liver immune system. Semin. Immunopathol. 31, 333-343.
39. Ostapowicz, G., Fontana, R. J., Schiodt, F. V., Larson, A., Davern, T. J., Han, S. H., McCashland, T. M., Shakil, A. O., Hay, J. E., Hynan, L., et al. (2002). Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann. Intern. Med. 137, 947-954.
40. Pohl, L. R., Satoh, H., Christ, D., and Kenna, J. (1988). The immunologic and metabolic basis of drug hypersensitivities. Annu. Rev. Pharmacol. Toxicol. 28, 367-387.
41. Renton, K. W. (1980). Methyl red azo-reductase and its induction by 3-methylcholanthrene in the liver by different species. Xenobiotica 10, 243-246.
42. Renton, K. W., Deloria, L. B., and Mannering, G. J. (1978). Effects of polyribonoinosinic acid polyribocytidylic acid and a mouse interferon preparation on cytochrome P-450-dependent monooxygenase systems in cultures of primary mouse hepatocytes. Mol. Pharmacol. 14, 672-681.
43. Roederer, M., and Hardy, R. R. (2001). Frequency difference gating: a multivariate method for identifying subsets that differ between samples. Cytometry 45(1), 56-64.
44. Roederer, M., Moore, W., Treister, A., Hardy, R. R., and Herzenberg, L. A. (2001). Probability binning comparison: a metric for quantitating multivariate distribution differences. Cytometry 45(1), 47-55.
45. Satoh, H., Fukuda, Y., Anderson, D., Ferrans, V., Gillette, J., and Pohl, L. (1985). Immunological studies on the mechanism of halothane-induced hepatotoxicity: immunohistochemical evidence of trifluoroacetylated hepatocytes. J. Pharmacol. Exp. Ther. 233, 857-862.
46. Scaffidi, P., Misteli, T., and Bianchi, M. E. (2002). Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191-195.
47. Shi, H., and Guan, S. H. (2009). Increased apoptosis in HepG2.2.15 cells with hepatitis B virus expression by synergistic induction of interferon-gamma and tumour necrosis factor-alpha. Liver Int. 29, 349-355.
48. Smyth, M. J., Cretney, E., Takeda, K., Wiltrout, R. H., Sedger, L. M., Kayagaki, N., Yagita, H., and Okumura, K. (2001). Tumor necrosis factorrelated apoptosis-inducing ligand (TRAIL) contributes to interferon gammadependent natural killer cell protection from tumor metastasis. J. Exp. Med. 193, 661-670.
49. Tagawa, Y., Sekikawa, K., and Iwakura, Y. (1997). Suppression of concanavalin A-induced hepatitis in IFN-gamma(-/-) mice, but not in TNF-alpha(-/-) mice: role for IFN-gamma in activating apoptosis of hepatocytes. J. Immunol. 159, 1418-1428.
50. Toyonaga, T., Hino, O., Sugai, S., Wakasugi, S., Abe, K., Shichiri, M., and Yamamura, K. (1994). Chronic active hepatitis in transgenic mice expressing interferon-gamma in the liver. Proc. Natl. Acad. Sci. U.S.A. 91, 614-618.
51. Trowell, J., Peto, R., and Smith, A. (1975). Controlled trial of repeated halothane anaesthetics in patients with carcinoma of the uterine cervix treated with radium. Lancet 305, 821-824.
52. van Zoelen, M. A., Yang, H., Florquin, S., Meijers, J. C., Akira, S., Arnold, B., Nawroth, P. P., Bierhaus, A., Tracey, K. J., and Poll, T. (2009). Role of toll-like receptors 2 and 4, and the receptor for advanced glycation end products in highmobility group box 1-induced inflammation in vivo. Shock 31(3), 280-284.
53. Wisse, E., van't Noordende, J. M., van der Meulen, J., and Daems, W. T. (1976). The pit cell: description of a new type of cell occurring in rat liver sinusoids and peripheral blood. Cell Tissue Res. 173(4), 423-435.
54. You, Q., Cheng, L., Reilly, T., Wegmann, D., and Ju, C. (2006). Role of neutrophils in a mouse model of halothane-induced liver injury. Hepatology 44, 1421-1431.