Acute ANIT toxicity in male IL-10 knockout and wild-type mice

Toxicologic Pathology

Volumn 38, Issue 5, 2010, Pages 745-755

  Faiola, Brenda ^a,b   Peterson, Richard A ^b   Kimbrough, Carrie L ^c   Jordan, Holly L ^b   Cullen, John M ^d  

^a RTI INTERNATIONAL   (United States)

^b GLAXOSMITHKLINE   (United States)

^c Social and Statistical Sciences   (United States)

^d NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

animal models; hepatobiliary system; histopathology; knockout mouse; liver; mouse pathology.; toxicologic pathology

Indexed keywords

1 NAPHTHYL ISOTHIOCYANATE; INTERLEUKIN 10;

ACUTE TOXICITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; CONVALESCENCE; EPITHELIUM; HISTOPATHOLOGY; INNATE IMMUNITY; KNOCKOUT MOUSE; LIVER CELL; LIVER CELL DAMAGE; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; DRUG-INDUCED LIVER INJURY; GALLBLADDER; IMMUNOHISTOCHEMISTRY; INTERLEUKIN-10; ISOTHIOCYANATES; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

ANIMALIA; MUS;

EID: 77958585736     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623310374970     Document Type: Article

References (44)

1. Blazka, M.E., Elwell, M.R., Holladay, S.D., Wilson, R.E., and Luster, M.I. (1996). Histopathology of acetaminophen-induced liver changes: role of interleukin 1 alpha and tumor necrosis factor alpha. Toxicol Pathol 24, 181-189.
2. 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.
3. Bourdi, M., Masubuchi, Y., Reilly, T.P., Amouzadeh, H.R., Martin, J.L., George, J.W., Shah, A.G., 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.
4. Carpenter-Deyo, L., Marchand, D.H., Jean, P.A., Roth, R.A., and Reed, D.J. (1991). Involvement of glutathione in 1-naphthylisothiocyanate (ANIT) metabolism and toxicity to isolated hepatocytes. Biochem Pharmacol 42, 2171-2180.
5. Couper, K.N., Blount, D.G., and Riley, E.M. (2008). IL-10: the master regulator of immunity to infection. J Immunol 180, 5771-5777.
6. Cover, C., Liu, J., Farhood, A., Malle, E., Waalkes, M.P., Bajt, M.L., and Jaeschke, H. (2006). Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 216, 98-107.
7. Dahm, L.J., Schultze, A.E., and Roth, R.A. (1991). An antibody to neutrophils attenuates alpha-naphthylisothiocyanate-induced liver injury. J Pharmacol Exp Ther 256, 412-420.
8. Dambach, D.M., Durham, S.K., Laskin, J.D., and Laskin, D.L. (2006). Distinct roles of NF-kappaB p50 in the regulation of acetaminophen-induced inflammatory mediator production and hepatotoxicity. Toxicol Appl Pharmacol 211, 157-165.
9. Dietrich, C.G., Ottenhoff, R., de Waart, D.R., and Oude Elferink, R.P. (2001). Role of MRP2 and GSH in intrahepatic cycling of toxins. Toxicology 167, 73-81.
10. Fromenty, B. and Pessayre, D. (1997). Impaired mitochondrial function in microvesicular steatosis. Effects of drugs, ethanol, hormones and cytokines. J Hepatol 26 Suppl 2, 43-53.
11. Giles, G.I., Tasker, K.M., and Jacob, C. (2002). Oxidation of biological thiols by highly reactive disulfide-S-oxides. Gen Physiol Biophys 21, 65-72.
12. Glaser, S., Francis, H., Demorrow, S., Lesage, G., Fava, G., Marzioni, M., Venter, J., and Alpini, G. (2006). Heterogeneity of the intrahepatic biliary epithelium. World J Gastroenterol 12, 3523-3536.
13. Goldfarb, S., Singer, E.J., and Popper, H. (1962). Experimental cholangitis due to alpha-naphthyl-isothiocyanate (ANIT). Am J Pathol 40, 685-698.
14. Gunawan, B.K., and Kaplowitz, N. (2007). Mechanisms of drug-induced liver disease. Clin Liver Dis 11, 459-475.
15. Hill, D.A., Jean, P.A., and Roth, R.A. (1999). Bile duct epithelial cells exposed to alpha-naphthylisothiocyanate produce a factor that causes neutrophil-dependent hepatocellular injury in vitro. Toxicol Sci 47, 118-125.
16. Hill, D.A., and Roth, R.A. (1998). Alpha-naphthylisothiocyanate causes neutrophils to release factors that are cytotoxic to hepatocytes. Toxicol Appl Pharmacol 148, 169-175.
17. Jaeschke, H. (2008). Innate immunity and acetaminophen-induced liver injury: why so many controversies ? Hepatology 48, 699-701.
18. Jaeschke, H., and Bajt, M.L. (2006). Intracellular signaling mechanisms of acetaminophen-induced liver cell death. Toxicol Sci 89, 31-41.
19. Jaeschke, H., and Liu, J. (2007). Neutrophil depletion protects against murine acetaminophen hepatotoxicity: another perspective. Hepatology 45, 1588-1589 ; author reply 1589.
20. Jean, P.A., Bailie, M.B., and Roth, R.A. (1995). 1- naphthylisothiocyanate-induced elevation of biliary glutathione. Biochem Pharmacol 49, 197-202.
21. Jean, P.A., Kessel, S.L., Hill, D.A., and Roth, R.A. (1998). Cytotoxicity of naphthylisothiocyanates in rat hepatocyte-neutrophil cocultures. Toxicol Lett 95, 155-163.
22. Jean, P.A., and Roth, R.A. (1995). Naphthylisothiocyanate disposition in bile and its relationship to liver glutathione and toxicity. Biochem Pharmacol 50, 1469-1474.
23. Ju, C., Reilly, T.P., Bourdi, M., Radonovich, M.F., Brady, J.N., George, J.W., and Pohl, L.R. (2002). Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem Res Toxicol 15, 1504-1513.
24. Kodali, P., Wu, P., Lahiji, P.A., Brown, E.J., and Maher, J.J. (2006). ANIT toxicity toward mouse hepatocytes in vivo is mediated primarily by neutrophils via CD18. Am J Physiol Gastrointest Liver Physiol 291, G355-63.
25. Kossor, D.C., Meunier, P.C., Handler, J.A., Sozio, R.S., and Goldstein, R.S. (1993). Temporal relationship of changes in hepatobiliary function and morphology in rats following alpha-naphthylisothiocyanate (ANIT) administration. Toxicol Appl Pharmacol 119, 108-114.
26. Kumagai, K., Ito, K., Ando, Y., Hakamata, S., Teranishi, M., Nakayama, H., and Manabe, S. (2009). Neutralization of IL-10 exacerbates cycloheximide-induced hepatocellular apoptosis and necrosis. Toxicol Pathol 37, 536-546.
27. Littell, R.C., Stroup, W.W., and Freund, R.J. (2002). SAS for Linear Models, Fourth Edition, John Wiley and Sons, Cary, NC.
28. Liu, Z.X., and Kaplowitz, N. (2006). Role of innate immunity in acetaminophen-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2, 493-503.
29. Lock, S., Lavigne, J., and Plaa, G.L. (1982). The effect of alpha-naphthylisothiocyanate on bile secretion prior to and during the onset of cholestasis in the rat. Toxicol Lett 10, 427-435.
30. Louis, H., Le Moine, O., Goldman, M., and Deviere, J. (2003). Modulation of liver injury by interleukin-10. Acta Gastroenterol Belg 66, 7-14.
31. Louis, H., Le Moine, O., Peny, M.O., Gulbis, B., Nisol, F., Goldman, M., and Deviere, J. (1997). Hepatoprotective role of interleukin 10 in galactosamine/lipopolysaccharide mouse liver injury. Gastroenterology 112, 935-942.
32. Louis, H., Le Moine, O., Peny, M.O., Quertinmont, E., Fokan, D., Goldman, M., and Deviere, J. (1997). Production and role of interleukin-10 in concanavalin A-induced hepatitis in mice. Hepatology 25, 1382-1389.
33. Michael, S.L., Pumford, N.R., Mayeux, P.R., Niesman, M.R., and Hinson, J.A. (1999). Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 30, 186-195.
34. Moore, K.W., de Waal Malefyt, R., Coffman, R.L., and O'sGarra, A. (2001). Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19, 683-765.
35. Nelson, S.D. (1990). Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Semin Liver Dis, 10, 267-278.
36. Orsler, D.J., Ahmed-Choudhury, J., Chipman, J.K., Hammond, T., and Cole-man, R. (1999). ANIT-induced disruption of biliary function in rat hepatocyte couplets. Toxicol Sci 47, 203-210.
37. Rajasingh, J., Bord, E., Luedemann, C., Asai, J., Hamada, H., Thorne, T., Qin, G., Goukassian, D., Zhu, Y., Losordo, D.W., and Kishore, R. (2006). IL-10-induced TNF-alpha mRNA destabilization is mediated via IL-10 suppression of p38 MAP kinase activation and inhibition of HuR expression. FASEB J 20, 2112-2114.
38. Roth, R.A., and Dahm, L.J. (1997). Neutrophil- and glutathione-mediated hepatotoxicity of alpha-naphthylisothiocyanate. Drug Metab Rev 29, 153-165.
39. Roth, R.A., and Hewett, J.A. (1990). The cholestatic agent, alpha-naphthylisothiocyanate, stimulates superoxide release by rat neutrophils in vitro. Lab Invest 62, 736-741.
40. SAS Institute Inc. (2002) GLM and MULTITEST procedure of SAS/STAT, SAS Institute Inc., Cary, NC.
41. Schaffner, F., Scharnbeck, H.H., Hutterer, F., Denk, H., Greim, H.A., and Popper, H. (1973). Mechanism of cholestasis. VII. -Naphthylisothiocyanate- induced jaundice. Lab Invest 28, 321-331.
42. Stordeur, P., and Goldman, M. (1998). Interleukin-10 as a regulatory cytokine induced by cellular stress: molecular aspects. Int Rev Immunol 16, 501-522.
43. Ungar, H., and Popp, J.A. (1976). Acute cholecystitis and persistent liver necrosis in mice provoked by isothiocyanate. Arch Pathol Lab Med 100, 127-131.
44. Zimmerman, H.J. (1999). Hepatotoxicity: The Adverse Effects of Drugs and Other Chemicals on the Liver, Lippincott Williams and Wilkins, Philadelphia, PA.