Drug-induced allergic hepatitis develops in mice when myeloid-derived suppressor cells are depleted prior to halothane treatment

Hepatology

Volumn 62, Issue 2, 2015, Pages 546-557

  Chakraborty, Mala ^a   Fullerton, Aaron M ^a   Semple, Kenrick ^a   Chea, Lynette S ^a   Proctor, William R ^a   Bourdi, Mohammed ^a   Kleiner, David E ^b   Zeng, Xiangbin ^a   Ryan, Pauline M ^a   Dagur, Pradeep K ^a   Berkson, Julia D ^a   Reilly, Timothy P ^c   Pohl, Lance R ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c BRISTOL MYERS SQUIBB   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD4 ANTIGEN; CD8 ANTIGEN; HALOTHANE; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G1 ANTIBODY; INTERLEUKIN 4; NITRIC OXIDE; ALANINE AMINOTRANSFERASE;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY RESPONSE; ARTICLE; CELL FRACTIONATION; CELL INFILTRATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG RECHALLENGE; EOSINOPHIL; FEMALE; IMMUNOGLOBULIN BLOOD LEVEL; IMMUNOLOGICAL TOLERANCE; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; T CELL DEPLETION; T LYMPHOCYTE; TOXIC HEPATITIS; ANALYSIS OF VARIANCE; ANIMAL; BAGG ALBINO MOUSE; BONE MARROW CELL; CD8+ T LYMPHOCYTE; DISEASE MODEL; DRUG EFFECTS; FLOW CYTOMETRY; HEPATITIS; IMMUNOHISTOCHEMISTRY; IMMUNOLOGY; METABOLISM; PATHOLOGY; RANDOMIZATION;

ALANINE TRANSAMINASE; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; CD8-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; FEMALE; FLOW CYTOMETRY; HALOTHANE; HEPATITIS; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED BALB C; MYELOID CELLS; NITRIC OXIDE; RANDOM ALLOCATION;

EID: 84938058043     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27764     Document Type: Article

References (37)

1. Ostapowicz G, Fontana RJ, Schiodt FV, Larson A, Davern TJ, Han SH, et al. Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann Intern Med 2002;137:947-954.
2. Pohl LR. Drug-induced allergic hepatitis. Semin Liver Dis 1990;10:305-315.
3. Liu ZX, Kaplowitz N. Immune-mediated drug-induced liver disease. Clin Liver Dis 2002;6:755-774.
4. Warrington RJ, Tse KS, Gorski BA, Schwenk R, Sehon AH. Evaluation of isoniazid-associated hepatitis by immunological tests. Clin Exp Immunol 1978;32:97-104.
5. Tsutsui H, Terano Y, Sakagami C, Hasegawa I, Mizoguchi Y, Morisawa S. Drug-specific T cells derived from patients with drug-induced allergic hepatitis. J Immunol 1992;149:706-716.
6. Monshi MM, Faulkner L, Gibson A, Jenkins RE, Farrell J, Earnshaw CJ, et al. Human leukocyte antigen (HLA)-B*57:01-restricted activation of drug-specific T cells provides the immunological basis for flucloxacillin-induced liver injury. Hepatology 2013;57:727-739.
7. Aithal GP, Ramsay L, Daly AK, Sonchit N, Leathart JB, Alexander G, et al. Hepatic adducts, circulating antibodies, and cytokine polymorphisms in patients with diclofenac hepatotoxicity. Hepatology 2004;39:1430-1440.
8. Bourdi M, Larrey D, Nataf J, Bernuau J, Pessayre D, Iwasaki M, et al. Anti-liver endoplasmic reticulum autoantibodies are directed against human cytochrome P-450IA2. A specific marker of dihydralazine-induced hepatitis. J Clin Invest 1990;85:1967-1973.
9. Dansette PM, Bonierbale E, Minoletti C, Beaune PH, Pessayre D, Mansuy D. Drug-induced immunotoxicity. Eur J Drug Metab Pharmacokinet 1998;23:443-451.
10. Kenna JG, Satoh H, Christ DD, Pohl LR. 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 1988;245:1103-1109.
11. Ng W, Lobach AR, Zhu X, Chen X, Liu F, Metushi IG, et al. Animal models of idiosyncratic drug reactions. Adv Pharmacol 2012;63:81-135.
12. Ju C, McCoy JP, Chung CJ, Graf ML, Pohl LR. Tolerogenic role of Kupffer cells in allergic reactions. Chem Res Toxicol 2003;16:1514-1519.
13. Invernizzi P. Liver auto-immunology: the paradox of autoimmunity in a tolerogenic organ. J Autoimmun 2013;46:1-6.
14. Chan T, Wiltrout RH, Weiss JM. Immunotherapeutic modulation of the suppressive liver and tumor microenvironments. Int Immunopharmacol 2011;11:879-889.
15. Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009;9:162-174.
16. Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ. Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 2009;58:49-59.
17. Zhang H, Liu Y, Bian Z, Huang S, Han X, You Z, et al. The critical role of myeloid-derived supressor cells and FXR activation in immune-mediated liver injury. J Autoimmun 2014;53:55-66.
18. Holgate ST. Innate and adaptive immune responses in asthma. Nat Med 2012;18:673-683.
19. Yee SB, Bourdi M, Masson MJ, Pohl LR. Hepatoprotective role of endogenous interleukin-13 in a murine model of acetaminophen-induced liver disease. Chem Res Toxicol 2007;20:734-744.
20. Butler LE, Thomassen D, Martin JL, Martin BM, Kenna JG, Pohl LR. The calcium-binding protein calreticulin is covalently modified in rat liver by a reactive metabolite of the inhalation anesthetic halothane. Chem Res Toxicol 1992;5:406-410.
21. Proctor WR, Chakraborty M, Chea LS, Morrison JC, Berkson JD, Semple K, et al. Eosinophils mediate the pathogenesis of halothane-induced liver injury in mice. Hepatology 2013;57:2026-2036.
22. Proctor WR, Chakraborty M, Fullerton AM, Korrapati MC, Ryan PM, Semple K, et al. Thymic stromal lymphopoietin and interleukin-4 mediate the pathogenesis of halothane-induced liver injury in mice. Hepatology 2014;60:1741-1752.
23. Denzler KL, Farmer SC, Crosby JR, Borchers M, Cieslewicz G, Larson KA, et al. Eosinophil major basic protein-1 does not contribute to allergen-induced airway pathologies in mouse models of asthma. J Immunol 2000;165:5509-5517.
24. Youn JI, Nagaraj S, Collazo M, Gabrilovich DI. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008;181:5791-5802.
25. Pillay J, Tak T, Kamp VM, Koenderman L. Immune suppression by neutrophils and granulocytic myeloid-derived suppressor cells: similarities and differences. Cell Mol Life Sci 2013;70:3813-3827.
26. Greifenberg V, Ribechini E, Rossner S, Lutz MB. Myeloid-derived suppressor cell activation by combined LPS and IFN-gamma treatment impairs DC development. Eur J Immunol 2009;39:2865-2876.
27. + T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol 2004;172:989-999.
28. Habibollahi P, Mahboobi N, Esmaeili S, Safari S, Dabbagh A, Alavian SM. Halothane-induced hepatitis: a forgotten issue in developing countries. Hepat Mon 2011;11:3-6.
29. You Q, Cheng L, Reilly TP, Wegmann D, Ju C. Role of neutrophils in a mouse model of halothane-induced liver injury. Hepatology 2006;44:1421-1431.
30. Bourdi M, Amouzadeh HR, Rushmore TH, Martin JL, Pohl LR. Halothane-induced liver injury in outbred guinea pigs: role of trifluoroacetylated protein adducts in animal susceptibility. Chem Res Toxicol 2001;14:362-370.
31. Kenna JG, Neuberger J, Williams R. An enzyme-linked immunosorbent assay for detection of antibodies against halothane-altered hepatocyte antigens. J Immunol Methods 1984;75:3-14.
32. Snapper CM, Finkelman FD, Stefany D, Conrad DH, Paul WE. IL-4 induces co-expression of intrinsic membrane IgG1 and IgE by murine B cells stimulated with lipopolysaccharide. J Immunol 1988;141:489-498.
33. Prussin C, Metcalfe DD. 5. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol 2006;117(2 Suppl.):S450-S456.
34. Njoku DB, Mellerson JL, Talor MV, Kerr DR, Faraday NR, Outschoorn I, et al. Role of CYP2E1 immunoglobulin G4 subclass antibodies and complement in pathogenesis of idiosyncratic drug-induced hepatitis. Clin Vaccine Immunol 2006, 13:258-265.
35. Kleiner DE, Chalasani NP, Lee WM, Fontana RJ, Bonkovsky HL, Watkins PB, et al. Hepatic histological findings in suspected drug-induced liver injury: systematic evaluation and clinical associations. Hepatology 2014;59:661-670.
36. Endo Y, Hirahara K, Yagi R, Tumes DJ, Nakayama T. Pathogenic memory type Th2 cells in allergic inflammation. Trends Immunol 2014;35:69-78.
37. -/- mice with amodiaquine and anti-CTLA4 leads to liver injury similar to idiosyncratic liver injury in patients. Hepatology 2014; doi:10.1002/hep.27549.