2,3,7,8-TCDD enhances the sensitivity of mice to concanavalin A immune-mediated liver injury

Toxicology and Applied Pharmacology

Volumn 266, Issue 2, 2013, Pages 317-327

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

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

2,3,7,8 TCDD; Concanavalin A; Hepatotoxicity; Inflammatory cytokines; Innate immunity

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ANTISERUM; CONCANAVALIN A; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 22; INTERLEUKIN 4; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOLYSIS; DISEASE EXACERBATION; DOSE RESPONSE; EFFECTOR CELL; EXPERIMENTAL MODEL; HISTOPATHOLOGY; IMMUNOTOXICITY; INFLAMMATION; LIVER INJURY; LIVER PARENCHYMA; LYMPHOCYTE ACTIVATION; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PROTEIN EXPRESSION;

ANIMALS; CONCANAVALIN A; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; ENVIRONMENTAL POLLUTANTS; FAS LIGAND PROTEIN; GENE EXPRESSION REGULATION; INFLAMMATION; INTERFERON-GAMMA; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NATURAL KILLER T-CELLS; TETRACHLORODIBENZODIOXIN; TIME FACTORS;

MURINAE; MUS;

EID: 84871167454     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.11.009     Document Type: Article

References (50)

1. Birnbaum L.S., DeVito M.J. Use of toxic equivalency factors for risk assessment for dioxins and related compounds. Toxicology 1995, 105:391-401.
2. Birnbaum L.S., Tuomisto J. Non-carcinogenic effects of TCDD in animals. Food Addit. Contam. 2000, 17:275-288.
3. Bonder C.S., Ajuebor M.N., Zbytnuik L.D., Kubes P., Swain M.G. Essential role for neutrophil recruitment to the liver in concanavalin A-induced hepatitis. J. Immunol. 2004, 172:45-53.
4. Boverhof D.R., Burgoon L.D., Tashiro C., Chittim B., Harkema J.R., Jump D.B., Zacharewski T.R. Temporal and dose-dependent hepatic gene expression patterns in mice provide new insights into TCDD-mediated hepatotoxicity. Toxicol. Sci. 2005, 85:1048-1063.
5. Clark G., Taylor M., Tritscher A., Lucier G. Tumor necrosis factor involvement in 2,3,7,8-tetrachlorodibenzo-p-dioxin-mediated endotoxin hypersensitivity in C57BL/6J mice congenic at the Ah locus. Toxicol. Appl. Pharmacol. 1991, 111:422-431.
6. DeVito M.J., Birnbaum L.S., Farland W.H., Gasiewicz T.A. Comparisons of estimated human body burdens of dioxinlike chemicals and TCDD body burdens in experimentally exposed animals. Environ. Health Perspect. 1995, 103:820-831.
7. Diliberto J.J., Akubue P.I., Luebke R.W., Birnbaum L.S. Dose-response relationships of tissue distribution and induction of CYP1A1 and CYP1A2 enzymatic activities following acute exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in mice. Toxicol. Appl. Pharmacol. 1995, 130:197-208.
8. Dong Z., Wei H., Sun R., Tian Z. The roles of innate immune cells in liver injury and regeneration. Cell. Mol. Immunol. 2007, 4:241-252.
9. Esser C., Rannug A., Stockinger B. The aryl hydrocarbon receptor in immunity. Trends Immunol. 2009, 30:447-454.
10. Fingerhut M.A., Halperin W.E., Marlow D.A., Piacitelli L.A., Honchar P.A., Sweeney M.H., Greife A.L., Dill P.A., Steenland K., Suruda A.J. Cancer mortality in workers exposed to 2,3,7,8-tetrachlorodibenzo-p-dioxin. N. Engl. J. Med. 1991, 324:212-218.
11. Gantner F., Leist M., Lohse A.W., Germann P.G., Tiegs G. Concanavalin A-induced T-cell-mediated hepatic injury in mice: the role of tumor necrosis factor. Hepatology 1995, 21:190-198.
12. Gantner F., Leist M., Küsters S., Vogt K., Volk H.-D., Tiegs G. T cell stimulus-induced crosstalk between lymphocytes and liver macrophages results in augmented cytokine release. Exp. Cell Res. 1996, 229:137-146.
13. Gasiewicz T.A., Geiger L.E., Rucci G., Neal R.A. Distribution, excretion, and metabolism of 2,3,7,8-tetrachlorodibenzo-p-dioxin in C57BL/6J, DBA/2J, and B6D2F1/J mice. Drug Metab. Dispos. 1983, 11:397-403.
14. Hakk H., Diliberto J.J., Birnbaum L.S. The effect of dose on 2,3,7,8-TCDD tissue distribution, metabolism and elimination in CYP1A2 (-/-) knockout and C57BL/6N parental strains of mice. Toxicol. Appl. Pharmacol. 2009, 241:119-126.
15. Kaneko Y., Harada M., Kawano T., Yamashita M., Shibata Y., Gejyo F., Nakayama T., Taniguchi M. Augmentation of Vα14 Nkt cell-mediated cytotoxicity by interleukin 4 in an autocrine mechanism resulting in the development of concanavalin a-induced hepatitis. J. Exp. Med. 2000, 191:105-114.
16. Klintman D., Schramm R., Menger M.D., Thorlacius H. Leukocyte recruitment in hepatic injury: selectin-mediated leukocyte rolling is a prerequisite for CD18-dependent firm adhesion. J. Hepatol. 2002, 36:53-59.
17. Kopec A.K., Boverhof D.R., Burgoon L.D., Ibrahim-Aibo D., Harkema J.R., Tashiro C., Chittim B., Zacharewski T.R. Comparative toxicogenomic examination of the hepatic effects of PCB126 and TCDD in immature, ovariectomized C57BL/6 mice. Toxicol. Sci. 2008, 102:61-75.
18. Ksontini R., Colagiovanni D.B., Josephs M.D., Edwards C.K., Tannahill C.L., Solorzano C.C., Norman J., Denham W., Clare-Salzler M., MacKay S.L., Moldawer L.L. Disparate roles for TNF-alpha and Fas ligand in concanavalin A-induced hepatitis. J. Immunol. 1998, 160:4082-4089.
19. Kusters S., Gantner F., Kunstle G., Tiegs G. Interferon gamma plays a critical role in T cell-dependent liver injury in mice initiated by concanavalin A. Gastroenterology 1996, 111:462-471.
20. Leist M., Gantner F., Kunstle G., Bohlinger I., Tiegs G., Bluethmann H., Wendel A. The 55-kB tumor necrosis factor receptor and CD95 independently signal murine hepatocyte apoptosis and subsequent liver failure. Mol. Med. 1996, 2:109-124.
21. Louis H., Le Moine O., Peny M.O., Quertinmont E., Fokan D., Goldman M., Deviere J. Production and role of interleukin-10 in concanavalin A-induced hepatitis in mice. Hepatology 1997, 25:1382-1389.
22. Matsumoto G., Tsunematsu S., Tsukinoki K.-i, Ohmi Y., Iwamiya M., Oliveira-dos-Santos A., Tone D., Shindo J., Penninger J.M. Essential role of the adhesion receptor LFA-1 for T cell-dependent fulminant hepatitis. J. Immunol. 2002, 169:7087-7096.
23. Mizuhara H., O'Neill E., Seki N., Ogawa T., Kusunoki C., Otsuka K., Satoh S., Niwa M., Senoh H., Fujiwara H. T cell activation-associated hepatic injury: mediation by tumor necrosis factors and protection by interleukin 6. J. Exp. Med. 1994, 179:1529-1537.
24. Mizuhara H., Kuno M., Seki N., Yu W.-G., Yamaoka M., Yamashita M., Ogawa T., Kaneda K., Fujii T., Senoh H., Fujiwara H. Strain difference in the induction of T-cell activation-associated, interferon gamma-dependent hepatic injury in mice. Hepatology 1998, 27:513-519.
25. Moos A., Baecher-Steppan L., Kerkvliet N. Acute inflammatory response to sheep red blood cells in mice treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin: the role of proinflammatory cytokines, IL-1 and TNF. Toxicol. Appl. Pharmacol. 1994, 127:331-335.
26. Morita A., Itoh Y., Toyama T., Fujii H., Nishioji K., Kirishima T., Makiyama A., Yamauchi N., Okanoue T. Activated Kupffer cells play an important role in intra-hepatic Th1-associated necro-inflammation in concanavalin A-induced hepatic injury in mice. Hepatol. Res. 2003, 27:143-150.
27. Needham L.L., Gerthoux P.M., Patterson D.G., Brambilla P., Turner W.E., Beretta C., Pirkle J.L., Colombo L., Sampson E.J., Tramacere P.L., Signorini S., Meazza L., Carreri V., Jackson R.J., Mocarelli P. Serum dioxin levels in Seveso, Italy, population in 1976. Teratog. Carcinog. Mutagen. 1997, 17:225-240.
28. Nishikage T., Seki S., Toyabe S., Abo T., Kagata Y., Iwai T., Hiraide H. Inhibition of concanavalin A-induced hepatic injury of mice by bacterial lipopolysaccharide via the induction of IL-6 and the subsequent reduction of IL-4: the cytokine milieu of concanavalin A hepatitis. J. Hepatol. 1999, 31:18-26.
29. N'Jai A., Boverhof D.R., Dere E., Burgoon L.D., Tan Y.S., Rowlands J.C., Budinsky R.A., Stebbins K.E., Zacharewski T.R. Comparative temporal toxicogenomic analysis of TCDD- and TCDF-mediated hepatic effects in immature female C57BL/6 mice. Toxicol. Sci. 2008, 103:285-297.
30. Nohara K., Fujimaki H., Tsukumo S., Inouye K., Sone H., Tohyama C. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on T cell-derived cytokine production in ovalbumin (OVA)-immunized C57Bl/6 mice. Toxicology 2002, 172:49-58.
31. Olivero-Verbel J., Roth R.A., Ganey P.E. Dioxin alters inflammatory responses to lipopolysaccharide. Toxicol. Environ. Chem. 2011, 93:1180-1194.
32. Patterson R.M., Stachlewitz R., Germolec D. Induction of apoptosis by 2,3,7,8-tetrachlorodibenzo-p-dioxin following endotoxin exposure. Toxicol. Appl. Pharmacol. 2003, 190:120-134.
33. Poland A., Glover E. 2,3,7,8,-Tetrachlorodibenzo-p-dioxin: segregation of toxocity with the Ah locus. Mol. Pharmacol. 1980, 17:86-94.
34. Rehermann B., Nascimbeni M. Immunology of hepatitis B virus and hepatitis C virus infection. Nat. Rev. Immunol. 2005, 5:215-229.
35. Santodomingo-Garzon T., Swain M.G. Role of NKT cells in autoimmune liver disease. Autoimmun. Rev. 2011, 10:793-800.
36. Sass G., Heinlein S., Agli A., Bang R., Schümann J., Tiegs G. Cytokine expression in three mouse models of experimental hepatitis. Cytokine 2002, 19:115-120.
37. Schumann J., Wolf D., Pahl A., Brune K., Papadopoulos T., van Rooijen N., Tiegs G. Importance of Kupffer cells for T-cell-dependent liver injury in mice. Am. J. Pathol. 2000, 157:1671-1683.
38. Seino K., Kayagaki N., Takeda K., Fukao K., Okumura K., Yagita H. Contribution of Fas ligand to T cell-mediated hepatic injury in mice. Gastroenterology 1997, 113:1315-1322.
39. Shaw P.J., Ganey P.E., Roth R.A. Trovafloxacin enhances the inflammatory response to a Gram-negative or a Gram-positive bacterial stimulus, resulting in neutrophil-dependent liver injury in mice. J. Pharmacol. Exp. Ther. 2009, 330:72-78.
40. Smialowicz R.J., Riddle M.M., Williams W.C., Diliberto J.J. Effects of 2,3,7,8-tetrachlorodibenzo-P-dioxin (Tcdd) on humoral immunity and lymphocyte subpopulations - differences between mice and rats. Toxicol. Appl. Pharmacol. 1994, 124:248-256.
41. Sweeney M.H., Mocarelli P. Human health effects after exposure to 2,3,7,8-TCDD. Food Addit. Contam. 2000, 17:303-316.
42. Tagawa Y., Sekikawa K., Iwakura Y. 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. 1997, 159:1418-1428.
43. Tagawa Y.-i, Kakuta S., Iwakura Y. Involvement of Fas/Fas ligand system-mediated apoptosis in the development of concanavalin A-induced hepatitis. Eur. J. Immunol. 1998, 28:4105-4113.
44. Takeda K., Hayakawa Y., Van Kaer L., Matsuda H., Yagita H., Okumura K. Critical contribution of liver natural killer T cells to a murine model of hepatitis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:5498-5503.
45. Teske S., Bohn A.A., Regal J.F., Neumiller J.J., Lawrence B.P. Activation of the aryl hydrocarbon receptor increases pulmonary neutrophilia and diminishes host resistance to influenza A virus. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 289:L111-L124.
46. Tiegs G., Hentschel J., Wendel A. A T cell-dependent experimental liver injury in mice inducible by concanavalin A. J. Clin. Invest. 1992, 90:196-203.
47. Toyabe S., Seki S., Iiai T., Takeda K., Shirai K., Watanabe H., Hiraide H., Uchiyama M., Abo T. Requirement of IL-4 and liver NK1+ T cells for concanavalin A-induced hepatic injury in mice. J. Immunol. 1997, 159:1537-1542.
48. Veldhoen M., Duarte J.H. The aryl hydrocarbon receptor: fine-tuning the immune-response. Curr. Opin. Immunol. 2010, 22:747-752.
49. Veldhoen M., Hirota K., Westendorf A.M., Buer J., Dumoutier L., Renauld J.C., Stockinger B. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008, 453:106-109.
50. Watanabe Y., Morita M., Akaike T. Concanavalin A induces perforin-mediated but not Fas-mediated hepatic injury. Hepatology 1996, 24:702-710.