Role of drug-independent stress factors in liver injury associated with diclofenac intake

Toxicology

Volumn 312, Issue 1, 2013, Pages 83-96

  Ramm, Susanne ^a   Mally, Angela ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Diclofenac; Drug safety; Hepatotoxicity; Inflammation

Indexed keywords

BUTHIONINE SULFOXIMINE; CYTOKINE INDUCED NEUTROPHIL CHEMOATTRACTANT; DICLOFENAC; GAMMA INTERFERON; GLUTATHIONE; HEAT SHOCK PROTEIN 90; HEME OXYGENASE 1; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; LIVER ENZYME; MANGANESE SUPEROXIDE DISMUTASE; POLYINOSINIC POLYCYTIDYLIC ACID; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEGENERATION; CONTROLLED STUDY; DOWN REGULATION; DRUG METABOLISM; ENZYME ACTIVITY; ENZYME BLOOD LEVEL; GENE EXPRESSION; LIVER CELL; LIVER INJURY; LIVER PARENCHYMA; LIVER TOXICITY; LIVER WEIGHT; MALE; NEUTROPHIL; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; UPREGULATION; VIRUS INFECTION;

ACTIVATOR PROTEIN 1; AP1; BSO; CINC-1; CYTOKINE-INDUCED NEUTROPHIL CHEMOATTRACTANT 1; DCL; DCL ACYL GLUCURONIDE; DCL MERCAPTURIC ACID; DCL-AG; DCL-MA; DICLOFENAC; DL-BUTHIONINE SULFOXIMINE; DRUG SAFETY; HEPATOTOXICITY; HIGH MOBILITY GROUP BOX 1; HMGB1; IDIOSYNCRATIC DRUG REACTION; IDR; IL-1; INFLAMMATION; INTERLEUKIN 1; LIPOPOLYSACCHARIDE; LPS; MAPK; MITOGEN ACTIVATED PROTEIN KINASE; NEUTROPHIL GELATINASE-ACTIVATED LIPOCALIN; NFΚB; NGAL; NONSTEROIDAL ANTI-INFLAMMATORY DRUG; NRF2; NSAID; NUCLEAR FACTOR-ΚB; NUCLEAR FACTOR-E2-RELATED FACTOR 2; PIC; POLY I:C; TNF-Α; TUMOR NECROSIS FACTOR Α;

ACUTE-PHASE PROTEINS; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BUTHIONINE SULFOXIMINE; DICLOFENAC; DRUG-INDUCED LIVER INJURY; LIPOCALINS; LIPOPOLYSACCHARIDES; MALE; NF-KAPPA B; POLY I-C; PROTO-ONCOGENE PROTEINS; RATS; RATS, SPRAGUE-DAWLEY; STRESS, PHYSIOLOGICAL;

EID: 84883291987     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2013.08.002     Document Type: Article

References (93)

1. Aithal G.P., Day C.P. Nonsteroidal anti-inflammatory drug-induced hepatotoxicity. Clin. Liver Dis. 2007, 11:563-575. vi-vii.
2. Aithal G.P., et al. Hepatic adducts, circulating antibodies, and cytokine polymorphisms in patients with diclofenac hepatotoxicity. Hepatology 2004, 39:1430-1440.
3. Andersson U., et al. High mobility group 1 protein (HMG-1) stimulates proinflammatory cytokine synthesis in human monocytes. J. Exp. Med. 2000, 192:565-570.
4. Bahmani P., et al. Neutrophil gelatinase-associated lipocalin induces the expression of heme oxygenase-1 and superoxide dismutase 1, 2. Cell Stress Chaperones 2010, 15:395-403.
5. Bhatia M., et al. Treatment with neutralising antibody against cytokine induced neutrophil chemoattractant (CINC) protects rats against acute pancreatitis associated lung injury. Gut 2000, 47:838-844.
6. Bjornsson E., Olsson R. Suspected drug-induced liver fatalities reported to the WHO database. Dig. Liver Dis. 2006, 38:33-38.
7. Boelsterli U.A. Diclofenac-induced liver injury: a paradigm of idiosyncratic drug toxicity. Toxicol. Appl. Pharmacol. 2003, 192:307-322.
8. Bolze S., et al. Development of an in vitro screening model for the biosynthesis of acyl glucuronide metabolites and the assessment of their reactivity toward human serum albumin. Drug Metab. Dispos. 2002, 30:404-413.
9. Bruyere A., et al. Development of an optimized procedure for the preparation of rat intestinal microsomes: comparison of hepatic and intestinal microsomal cytochrome P450 enzyme activities in two rat strains. Xenobiotica 2009, 39:22-32.
10. Campbell S.J., et al. CINC-1 is an acute-phase protein induced by focal brain injury causing leukocyte mobilization and liver injury. FASEB J. 2003, 17:1168-1170.
11. Cassio D., et al. Expression, localization, and inducibility by bile acids of hepatobiliary transporters in the new polarized rat hepatic cell lines, Can 3-1 and Can 10. Cell Tissue Res. 2007, 330:447-460.
12. Chan M.M., Moore A.R. Resolution of inflammation in murine autoimmune arthritis is disrupted by cyclooxygenase-2 inhibition and restored by prostaglandin E2-mediated lipoxin A4 production. J. Immunol. 2010, 184:6418-6426.
13. Chen G.Y., et al. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 2009, 323:1722-1725.
14. Cheng L., et al. Effect of polyI:C cotreatment on halothane-induced liver injury in mice. Hepatology 2009, 49:215-226.
15. Colletti L.M., et al. The role of cytokine networks in the local liver injury following hepatic ischemia/reperfusion in the rat. Hepatology 1996, 23:506-514.
16. Cotto J.J., et al. Activation of heat shock factor 1 DNA binding precedes stress-induced serine phosphorylation. Evidence for a multistep pathway of regulation. J. Biol. Chem. 1996, 271:3355-3358.
17. Daly A.K., et al. Genetic susceptibility to diclofenac-induced hepatotoxicity: contribution of UGT2B7, CYP2C8, and ABCC2 genotypes. Gastroenterology 2007, 132:272-281.
18. de Vera M.E., et al. Heat shock response inhibits cytokine-inducible nitric oxide synthase expression in rat hepatocytes. Hepatology 1996, 24:1238-1245.
19. Deng X., et al. Inflammatory stress and idiosyncratic hepatotoxicity: hints from animal models. Pharmacol. Rev. 2009, 61:262-282.
20. Deng X., et al. Modest inflammation enhances diclofenac hepatotoxicity in rats: role of neutrophils and bacterial translocation. J. Pharmacol. Exp. Ther. 2006, 319:1191-1199.
21. Donner M.G., et al. Enhanced expression of basolateral multidrug resistance protein isoforms Mrp3 and Mrp5 in rat liver by LPS. Biol. Chem. 2004, 385:331-339.
22. Fredriksson L., et al. Diclofenac inhibits tumor necrosis factor-alpha-induced nuclear factor-kappaB activation causing synergistic hepatocyte apoptosis. Hepatology 2011, 53:2027-2041.
23. Ganey P.E., et al. Adverse hepatic drug reactions: inflammatory episodes as consequence and contributor. Chem. Biol. Interact. 2004, 150:35-51.
24. Graham D.Y., et al. Nonsteroidal anti-inflammatory effect of sulindac sulfoxide and sulfide on gastric mucosa. Clin. Pharmacol. Ther. 1985, 38:65-70.
25. Grillo M.P., et al. Mechanistic studies on the bioactivation of diclofenac: identification of diclofenac-S-acyl-glutathione in vitro in incubations with rat and human hepatocytes. Chem. Res. Toxicol. 2003, 16:1410-1417.
26. Harris H.E., Raucci A. Alarmin(g) news about danger: workshop on innate danger signals and HMGB1. EMBO Rep. 2006, 7:774-778.
27. Hermening A., et al. Gemfibrozil and its oxidative metabolites: quantification of aglycones, acyl glucuronides, and covalent adducts in samples from preclinical and clinical kinetic studies. J. Chromatogr. B: Biomed. Sci. Appl. 2000, 741:129-144.
28. Hoffmann D., et al. Evaluation of a urinary kidney biomarker panel in rat models of acute and subchronic nephrotoxicity. Toxicology 2010, 277:49-58.
29. Hudson N., et al. Enhanced gastric mucosal leukotriene B4 synthesis in patients taking non-steroidal anti-inflammatory drugs. Gut 1993, 34:742-747.
30. Jurivich D.A., et al. Effect of sodium salicylate on the human heat shock response. Science 1992, 255:1243-1245.
31. Kaplowitz N. Idiosyncratic drug hepatotoxicity. Nat. Rev. Drug Discov. 2005, 4:489-499.
32. Kishida T., et al. Increase in covalent binding of 5-hydroxydiclofenac to hepatic tissues in rats co-treated with lipopolysaccharide and diclofenac: involvement in the onset of diclofenac-induced idiosyncratic hepatotoxicity. J. Toxicol. Sci. 2012, 37:1143-1156.
33. Kovarik J.M., et al. Cyclosporine and nonsteroidal antiinflammatory drugs: exploring potential drug interactions and their implications for the treatment of rheumatoid arthritis. J. Clin. Pharmacol. 1997, 37:336-343.
34. Kretz-Rommel A., Boelsterli U.A. Mechanism of covalent adduct formation of diclofenac to rat hepatic microsomal proteins. Retention of the glucuronic acid moiety in the adduct. Drug Metab. Dispos. 1994, 22:956-961.
35. Kumar S., et al. Extrapolation of diclofenac clearance from in vitro microsomal metabolism data: role of acyl glucuronidation and sequential oxidative metabolism of the acyl glucuronide. J. Pharmacol. Exp. Ther. 2002, 303:969-978.
36. Kunkel S.L., et al. Regulation of macrophage tumor necrosis factor production by prostaglandin E2. Biochem. Biophys. Res. Commun. 1986, 137:404-410.
37. Lagas J.S., et al. Hepatic clearance of reactive glucuronide metabolites of diclofenac in the mouse is dependent on multiple ATP-binding cassette efflux transporters. Mol. Pharmacol. 2010, 77:687-694.
38. Li A.P. A review of the common properties of drugs with idiosyncratic hepatotoxicity and the "multiple determinant hypothesis" for the manifestation of idiosyncratic drug toxicity. Chem. Biol. Interact. 2002, 142:7-23.
39. Li J., Uetrecht J.P. The danger hypothesis applied to idiosyncratic drug reactions. Handb. Exp. Pharmacol. 2010, 493-509.
40. Lotze M.T., Tracey K.J. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 2005, 5:331-342.
41. Luyendyk J.P., et al. Coagulation-mediated hypoxia and neutrophil-dependent hepatic injury in rats given lipopolysaccharide and ranitidine. J. Pharmacol. Exp. Ther. 2005, 314:1023-1031.
42. Masoodi M., Nicolaou A. Lipidomic analysis of twenty-seven prostanoids and isoprostanes by liquid chromatography/electrospray tandem mass spectrometry. Rapid Commun. Mass Spectrom. 2006, 20:3023-3029.
43. Masubuchi Y., et al. Mechanism-based inactivation of CYP2C11 by diclofenac. Drug Metab. Dispos. 2001, 29:1190-1195.
44. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 1994, 12:991-1045.
45. Matzinger P. The danger model: a renewed sense of self. Science 2002, 296:301-305.
46. Miyamoto G., et al. Oxidation of diclofenac to reactive intermediates by neutrophils, myeloperoxidase, and hypochlorous acid. Chem. Res. Toxicol. 1997, 10:414-419.
47. Morgan E.T. Impact of infectious and inflammatory disease on cytochrome P450-mediated drug metabolism and pharmacokinetics. Clin. Pharmacol. Ther. 2009, 85:434-438.
48. Morita M., et al. Drug-induced hepatotoxicity test using gamma-glutamylcysteine synthetase knockdown rat. Toxicol. Lett. 2009, 189:159-165.
49. Morteau O., et al. Impaired mucosal defense to acute colonic injury in mice lacking cyclooxygenase-1 or cyclooxygenase-2. J. Clin. Invest. 2000, 105:469-478.
50. North T.E., et al. PGE2-regulated wnt signaling and N-acetylcysteine are synergistically hepatoprotective in zebrafish acetaminophen injury. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:17315-17320.
51. Ong M.M., et al. Troglitazone-induced hepatic necrosis in an animal model of silent genetic mitochondrial abnormalities. Toxicol. Sci. 2007, 97:205-213.
52. Petrovic V., Piquette-Miller M. Impact of polyinosinic/polycytidylic acid on placental and hepatobiliary drug transporters in pregnant rats. Drug Metab. Dispos. 2010, 38:1760-1766.
53. Pirmohamed M., et al. Idiosyncratic drug reactions. Metabolic bioactivation as a pathogenic mechanism. Clin. Pharmacokinet. 1996, 31:215-230.
54. Poon G.K., et al. Bioactivation of diclofenac via benzoquinone imine intermediates-identification of urinary mercapturic acid derivatives in rats and humans. Drug Metab. Dispos. 2001, 29:1608-1613.
55. Quiroga J., Prieto J. Liver cytoprotection by prostaglandins. Pharmacol. Ther. 1993, 58:67-91.
56. Reilly T.P., et al. A protective role for cyclooxygenase-2 in drug-induced liver injury in mice. Chem. Res. Toxicol. 2001, 14:1620-1628.
57. Repetto G., et al. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat. Protoc. 2008, 3:1125-1131.
58. Reuter B.K., et al. Exacerbation of inflammation-associated colonic injury in rat through inhibition of cyclooxygenase-2. J. Clin. Invest. 1996, 98:2076-2085.
59. Rossi A., et al. Inhibition of nuclear factor kappa B by prostaglandin A1: an effect associated with heat shock transcription factor activation. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:746-750.
60. Roth J., et al. Influence of systemic treatment with cyclooxygenase inhibitors on lipopolysaccharide-induced fever and circulating levels of cytokines and cortisol in guinea-pigs. Pflugers Arch. 2002, 443:411-417.
61. Roth R.A., et al. Inflammation and drug idiosyncrasy-is there a connection?. J. Pharmacol. Exp. Ther. 2003, 307:1-8.
62. Sayeh E., Uetrecht J.P. Factors that modify penicillamine-induced autoimmunity in Brown Norway rats: failure of the Th1/Th2 paradigm. Toxicology 2001, 163:195-211.
63. Scaffidi P., et al. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 2002, 418:191-195.
64. Scarim A.L., et al. Heat shock inhibits cytokine-induced nitric oxide synthase expression by rat and human islets. Endocrinology 1998, 139:5050-5057.
65. Schett G., et al. Enhanced expression of heat shock protein 70 (hsp70) and heat shock factor 1 (HSF1) activation in rheumatoid arthritis synovial tissue. Differential regulation of hsp70 expression and hsf1 activation in synovial fibroblasts by proinflammatory cytokines, shear stress, and antiinflammatory drugs. J. Clin. Invest. 1998, 102:302-311.
66. Seguin B., et al. Gene expression profiling in a model of d-penicillamine-induced autoimmunity in the Brown Norway rat: predictive value of early signs of danger. Chem. Res. Toxicol. 2005, 18:1193-1202.
67. Seitz S., et al. Selective protein adduct formation of diclofenac glucuronide is critically dependent on the rat canalicular conjugate export pump (Mrp2). Chem. Res. Toxicol. 1998, 11:513-519.
68. Seong S.Y., Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 2004, 4:469-478.
69. Serrano M.A., et al. Effect of ursodeoxycholic acid on the impairment induced by maternal cholestasis in the rat placenta-maternal liver tandem excretory pathway. J. Pharmacol. Exp. Ther. 2003, 305:515-524.
70. Shaw P.J., et al. The role of the hemostatic system in murine liver injury induced by coexposure to lipopolysaccharide and trovafloxacin, a drug with idiosyncratic liability. Toxicol. Appl. Pharmacol. 2009, 236:293-300.
71. Shedlofsky S.I., et al. Endotoxin administration to humans inhibits hepatic cytochrome P450-mediated drug metabolism. J. Clin. Invest. 1994, 94:2209-2214.
72. Shen S., et al. Metabolic activation of diclofenac by human cytochrome P450 3A4: role of 5-hydroxydiclofenac. Chem. Res. Toxicol. 1999, 12:214-222.
73. Shi Y., et al. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 2003, 425:516-521.
74. Sieber M., et al. Comparative analysis of novel noninvasive renal biomarkers and metabonomic changes in a rat model of gentamicin nephrotoxicity. Toxicol. Sci. 2009, 109:336-349.
75. Sobel D.O., et al. Poly I:C induction of alpha-interferon in the diabetes-prone BB and normal Wistar rats. Dose-response relationships. Diabetes 1994, 43:518-522.
76. Sparidans R.W., et al. Liquid chromatography-tandem mass spectrometric assay for diclofenac and three primary metabolites in mouse plasma. J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci. 2008, 872:77-82.
77. Stafford J.B., Marnett L.J. Prostaglandin E2 inhibits tumor necrosis factor-alpha RNA through PKA type I. Biochem. Biophys. Res. Commun. 2008, 366:104-109.
78. Standeven A.M., Wetterhahn K.E. Possible role of glutathione in chromium(VI) metabolism and toxicity in rats. Pharmacol. Toxicol. 1991, 68:469-476.
79. Stierlin H., Faigle J.W. Biotransformation of diclofenac sodium (Voltaren) in animals and in man. II. Quantitative determination of the unchanged drug and principal phenolic metabolites, in urine and bile. Xenobiotica 1979, 9:611-621.
80. Stowell N.C., et al. Long-term activation of TLR3 by poly(I:C) induces inflammation and impairs lung function in mice. Respir. Res. 2009, 10:43.
81. Sultana C., et al. Lipoxygenase metabolites induced expression of adhesion molecules and transendothelial migration of monocyte-like HL-60 cells is linked to protein kinase C activation. J. Cell. Physiol. 1996, 167:477-487.
82. Suzuki C.A., Cherian M.G. Renal glutathione depletion and nephrotoxicity of cadmium-metallothionein in rats. Toxicol. Appl. Pharmacol. 1989, 98:544-552.
83. Tafazoli S., et al. Oxidative stress mediated idiosyncratic drug toxicity. Drug Metab. Rev. 2005, 37:311-325.
84. Tang W., et al. Studies on cytochrome P-450-mediated bioactivation of diclofenac in rats and in human hepatocytes: identification of glutathione conjugated metabolites. Drug Metab. Dispos. 1999, 27:365-372.
85. Tang W., et al. Roles of human hepatic cytochrome P450s 2C9 and 3A4 in the metabolic activation of diclofenac. Chem. Res. Toxicol. 1999, 12:192-199.
86. Uetrecht J. Idiosyncratic drug reactions: past, present, and future. Chem. Res. Toxicol. 2008, 21:84-92.
87. Ulrich R.G. Idiosyncratic toxicity: a convergence of risk factors. Annu. Rev. Med. 2007, 58:17-34.
88. Walker A.M. Quantitative studies of the risk of serious hepatic injury in persons using nonsteroidal antiinflammatory drugs. Arthritis Rheum. 1997, 40:201-208.
89. Yamazaki R., et al. Aceclofenac blocks prostaglandin E2 production following its intracellular conversion into cyclooxygenase inhibitors. Eur. J. Pharmacol. 1997, 329:181-187.
90. Yang D., et al. The alarmin functions of high-mobility group proteins. Biochim. Biophys. Acta 2010, 1799:157-163.
91. Zhang J., et al. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol. Endocrinol. 2008, 22:1416-1426.
92. Zou W., et al. Hepatotoxic interaction of sulindac with lipopolysaccharide: role of the hemostatic system. Toxicol. Sci. 2009, 108:184-193.
93. Zuurbier K.W., et al. Interaction of myeloperoxidase with diclofenac. Inhibition of the chlorinating activity of myeloperoxidase by diclofenac and oxidation of diclofenac to dihydroxyazobenzene by myeloperoxidase. Biochem. Pharmacol. 1990, 40:1801-1808.