Activation of flucloxacillin-specific CD8+ T-cells with the potential to promote hepatocyte cytotoxicity in a mouse model

Toxicological Sciences

Volumn 146, Issue 1, 2015, Pages 146-156

  Nattrass, Ryan ^a   Faulkner, Lee ^a   Vocanson, Marc ^b   Antoine, Daniel J ^a   Kipar, Anja ^a,c   Kenna, Gerry ^d   Nicolas, Jean Francois ^b   Park, B Kevin ^a   Naisbitt, Dean J ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

^b CENTRE INTERNATIONAL DE RECHERCHE EN INFECTIOLOGIE   (France)

^c ASTRAZENECA   (United Kingdom)

^d UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Flucloxacillin; Immunogenicity; Liver injury

Indexed keywords

ALANINE AMINOTRANSFERASE; AMOXICILLIN; BIOLOGICAL MARKER; CD4 ANTIGEN; FLUCLOXACILLIN; GAMMA INTERFERON; GRANZYME B; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; PIPERACILLIN; RETINOIC ACID; ANTIINFECTIVE AGENT;

ADAPTIVE IMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; APOPTOSIS; ARTICLE; C57BL 6 MOUSE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CONTROLLED STUDY; CYTOTOXICITY; DRUG SENSITIZATION; EX VIVO STUDY; GALLBLADDER; GALLBLADDER SWELLING; IMMUNOGENICITY; LYMPH NODE CELL; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; MOUSE; MOUSE MODEL; NONHUMAN; SWELLING; T LYMPHOCYTE ACTIVATION; TOXIC HEPATITIS; ANIMAL; DRUG EFFECTS; LIVER CELL;

ANIMALIA; MUS;

ANIMALS; ANTI-BACTERIAL AGENTS; CD8-POSITIVE T-LYMPHOCYTES; FLOXACILLIN; HEPATOCYTES; MICE;

EID: 84936750522     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv077     Document Type: Article

References (39)

1. Akiba, H., Kehren, J., Ducluzeau, M. T., Krasteva, M., Horand, F., Kaiserlian, D., Kaneko, F., and Nicolas, J. F. (2002). Skin inflammation during contact hypersensitivity is mediated by early recruitment of CD8+ T cytotoxic 1 cells inducing keratinocyte apoptosis. J. Immunol. 168, 3079-3087.
2. Antoine, D. J., Williams, D. P., Kipar, A., Jenkins, R. E., Regan, S. L., Sathish, J. G., Kitteringham, N. R., and Park, B. K. (2009). High-mobility group box-1 protein and keratin-18, circulating serum proteins informative of acetaminopheninduced necrosis and apoptosis in vivo. Toxicol. Sci. 112, 521-531.
3. Antoine, D. J., Dear, J. W., Lewis, P. S., Platt, V., Coyle, J., Masson, M., Thanacoody, R. H., Gray, A. J., Webb, D. J., Moggs, J. G., et al. (2013). Mechanistic biomarkers provide early and sensitive detection of acetaminophen-induced acute liver injury at first presentation to hospital. Hepatology 58, 777-787.
4. Bird, G. L., and Williams, R. (1989). Detection of antibodies to a halothane metabolite hapten in sera from patients with halothane-associated hepatitis. J. Hepatol. 9, 366-373.
5. Carey, M. A., and van Pelt, V.P. (2005). Immunochemical detection of flucloxacillin adduct formation in livers of treated rats. Toxicology 216, 41-48.
6. Daly, A. K., Donaldson, P. T., Bhatnagar, P., Shen, Y., Pe'er, I., Floratos, A., Daly, M. J., Goldstein, D. B., John, S., Nelson, M. R., et al. (2009). HLA-B*5701 genotype is a major determinant of drug-induced liver injury due to flucloxacillin. Nat. Genet. 41, 816-819.
7. Eksteen, B., Grant, A. J., Miles, A., Curbishley, S. M., Lalor, P. F., Hübscher, S. G., Briskin, M., Salmon, M., and Adams, D. H. (2004). Hepatic endothelial CCL25 mediates the recruitment of CCR9+ gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J. Exp. Med. 200, 1511-1517.
8. Eksteen, B., Mora, J. R., Haughton, E. L., Henderson, N. C., Lee-Turner, L., Villablanca, E. J., Curbishley, S. M., Aspinall, A. I., von Andrian, U. H., and Adams, D. H. (2009). Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells. Gastroenterology 137, 320-329.
9. Eckstein, R. P., Dowsett, J. F., and Lunzer, M. R. (1993). Flucloxacillin induced liver disease: histopathological findings at biopsy and autopsy. Pathology 25, 223-228.
10. Hecht, T. T., Longo, D. L., and Matis, L. A. (1983). The relationship between immune interferon production and proliferation in antigen-specific, MHC-restricted T cell lines and clones. J. Immunol. 131, 1049-1055.
11. Ju, C., and Reilly, T. (2012). Role of immune reactions in drug-induced liver injury (DILI). Drug Metab. Rev. 44, 107-115.
12. Kehren, J., Desvignes, C., Krasteva, M., Ducluzeau, M. T., Assossou, O., Horand, F., Hahne, M., Kagi, D., Kaiserlian, D., and Nicolas, J. F. (1999). Cytotoxicity is mandatory for CD8(+) T cell-mediated contact hypersensitivity. J. Exp. Med. 189, 779-786.
13. Kenna, J. G., Knight, T. L., and van Pelt, F. N. (1993). Immunity to halothane metabolite-modified proteins in halothane hepatitis. Ann. New York Acad. Sci. 685, 646-661.
14. Kish, D. D., Gorbachev, A. V., and Fairchild, R. L. (2007). Regulatory function of CD4+CD25+ T cells from Class II MHC-deficient mice in contact hypersensitivity responses. J. Leukoc. Biol. 82, 85-92.
15. Knight, T. L., Scatchard, K. M., Van Pelt, F. N., and Kenna, J. G. (1994). Sera from patients with halothane hepatitis contain antibodies to halothane-induced liver antigens which are not detectable by immunoblotting. J. Pharmacol. Exp. Ther. 270, 1325-1333.
16. Maria, V. A., and Victorino, R. M. (1997). Diagnostic value of specific T cell reactivity to drugs in 95 cases of drug induced liver injury. Gut 41, 534-540.
17. Mauri-Hellweg, D., Zanni, M., Frei, E., Bettens, F., Brander, C., Mauri, D., Padovan, E., Weltzien, H. U., and Pichler, W. J. (1996). Cross-reactivity of T cell lines and clones to betalactam antibiotics. J. Immunol. 157, 1071-1079.
18. Mousavi, T., Shahsavar, F., Farnia, P., Tajik, N., and Soofi, M. (2011). Study of KIR expression and HLA ligands in CD56+ lymphocytes of drug resistant tuberculosis patients. Iran. J. Allergy, Asthma, Imunol. 10, 189-194.
19. Monshi, M. M., Faulkner, L., Gibson, A., Jenkins, R. E., Farrell, J., Earnshaw, C. J., Alfirevic, A., Cederbrant, K., Daly, A. K., French, N., et al. (2013). Human leukocyte antigen (HLA)-B*57:01-restricted activation of drug-specific T cells provides the immunological basis for flucloxacillin-induced liver injury. Hepatology 57, 727-739.
20. Neumann, K., Kruse, N., Szilagyi, B., Erben, U., Rudolph, C., Flach, A., Zeitz, M., Hamann, A., and Klugewitz, A. (2012). Connecting liver and gut: murine liver sinusoidal endothelium induces gut tropism of CD4+ T cells via retinoic acid. Hepatology 55, 1976-1984.
21. Ng, W., Lobach, A. R., Zhu, X., Chen, X., Liu, F., Metushi, I. G., Sharma, A., Li, J., Cai, P., Ip, J., Novalen, M., Popovic, M., Zhang, X., Tanino, T., Nakagawa, T., Li, Y., and Uetrecht, J. (2012). Animal models of idiosyncratic drug reactions. Adv. Pharmacol. 63, 81-135.
22. Nhim, C., Delluc, S., Halgand, F., de Chaisemartin, L., Weaver, R.J., Claude, N., Joseph, D., Maillere, B., and Pallardy, M. (2013). Identification and frequency of circulating CD4(+) T lymphocytes specific to Benzylpenicillin in healthy donors. Allergy 68, 899i-905.
23. Prasad, B. R., Mullins, G., Nikolskaya, N., Connolly, D., Smith, T. J., Gerard, V. A., Byrne, S. J., Davies, G. L., Gun'ko, Y. K., and Rochev, Y. (2012). Effects of long-term exposure of gelatinated and non-gelatinated cadmium telluride quantum dots on differentiated PC12 cells. J. Nanobiotechnol. 10, 4.
24. Proctor, W. R., Chakraborty, M., Chea, L. S., Morrison, J. C., Berkson, J. D., Semple, K., Bourdi, M., and Pohl, L. R. (2013). Eosinophils mediate the pathogenesis of halothane-induced liver injury in mice. Hepatology 57, 2026-2036.
25. Rozieres, A., Vocanson, M., Rodet, K., Benetiere, J., Bienvenu, J., Berard, F., Hennino, A., and Nicolas, J. F. (2010). CD8+ T cells mediate skin allergy to amoxicillin in a mouse model. Allergy 65, 996-1003.
26. Smith, G. C., Kenna, J. G., Harrison, D. J., Tew, D., and Wolf, C. R. (1993). Autoantibodies to hepatic microsomal carboxylesterase in halothane hepatitis. Lancet 342, 963-964.
27. Spanou, Z., Keller, M., Britschgi, M., Yawalkar, N., Fehr, T., Neuweiler, J., Gugger, M., Mohaupt, M., and Pichler, W. J. (2006). Involvement of drug-specific T cells in acute drug-induced interstitial nephritis. J. Am. Soc. Nephrol. 17, 2919-2927.
28. Takai, S., Higuchi, S., Yano, A., Tsuneyama, K., Fukami, T., Nakajima, M., and Yokoi, T. (2014). Involvement of immuneand inflammatory-related factors in flucloxacillin-induced liver injury in mice. J. Appl. Toxicol. 35, 142-151.
29. Traidl, C., Sebastiani, S., Albanesi, C., Merk, H. F., Puddu, P., Girolomoni, G., and Cavani, A. (2000). Disparate cytotoxic activity of nickel-specific CD8+ and CD4+ T cell subsets against keratinocytes. J. Immunol. 165, 3058-3064.
30. Uetrecht, J., and Naisbitt, D. J. (2013). Idiosyncratic adverse drug reactions: current concepts. Pharmacol. Rev. 65, 779-808.
31. Vocanson, M., Hennino, A., Cluzel-Tailhardat, M., Saint-Mezard, P., Benetiere, J., Chavagnac, C., Berard, F., Kaiserlian, D., and Nicolas, J. F. (2006). CD8+ T cells are effector cells of contact dermatitis to common skin allergens in mice. J. Invest. Dermatol. 126, 815-820.
32. Vocanson, M., Hennino, A., Rozieres, A., Cluzel-Tailhardat, M., Poyet, G., Valeyrie, M., Benetiere, J., Tedone, R., Kaiserlian, D., and Nicolas, J. F. (2009). Skin exposure to weak and moderate contact allergens induces IFNgamma production by lymph node cells of CD4+ T-cell-depleted mice. J. Invest. Dermatol. 129, 1185-1191.
33. Warner, D. J., Chen, H., Cantin, L. D., Kenna, J. D., Stahl, S., Walker, C. L., and Noeske, T. (2012). Mitigating the inhibition of human bile salt export pump by drugs: opportunities provided by physicochemical property modulation, in silico modeling, and structural modification. Drug Metab. Dispos. 40, 2332-2341.
34. Whitaker, P., Meng, X., Lavergne, S. N., El-Ghaiesh, S., Monshi, M., Earnshaw, C., Peckham, D., Gooi, J., Conway, S., Pirmohamed, M., et al. (2011). Mass spectrometric characterization of circulating and functional antigens derived from piperacillin in patients with cystic fibrosis. J. Immunol. 187, 200-211.
35. Woolbright, B. L., Li, F., Xie, Y., Farhood, A., Fickert, P., Trauner, M., and Jaeschke, H. (2014). Lithocholic acid feeding results in direct hepato-toxicity independent of neutrophil function in mice. Toxicol. Lett. 228, 56-66.
36. Woolbright, B. L., Antoine, D. J., Jenkins, R. E., Bajt, M. L., Park, B. K., and Jaeschke, H. (2013). Plasma biomarkers of liver injury and inflammation demonstrate a lack of apoptosis during obstructive cholestasis in mice. Toxicol. Appl. Pharmacol. 273, 524-531.
37. Wuillemin, N., Adam, J., Fontana, S., Krahenbuhl, S., Pichler, W. J., and Yerly, D. (2013). HLA haplotype determines hapten or p-i T cell reactivity to flucloxacillin. J. Immunol. 190, 4956-4964.
38. Wuillemin, N., Terracciano, L., Beltraminelli, H., Schlapbach, C., Fontana, S., Krahenbuhl, S., Pichler, W. J., and Yerly, D. (2014). T cells infiltrate the liver and kill hepatocytes in HLA-B57:01-associated floxacillin-induced liver injury. Am. J. Pathol. 184, 1677-1682.
39. You, Q., Cheng, L., Reilly, T. P., Wegmann, D., and Ju, C. (2006). Role of neutrophils in a mouse model of halothane-induced liver injury. Hepatology 44, 1421-1431.