The role of the hemostatic system in murine liver injury induced by coexposure to lipopolysaccharide and trovafloxacin, a drug with idiosyncratic liability

Toxicology and Applied Pharmacology

Volumn 236, Issue 3, 2009, Pages 293-300

  Shaw, Patrick J ^a   Fullerton, Aaron M ^a   Scott, Michael A ^b   Ganey, Patricia E ^a   Roth, Robert A ^a  

^a National Food Safety and Toxicology Center   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

Adverse drug reaction; Fibrin; Hemostatic system; Hepatotoxicity; Idiosyncratic toxicity; Inflammation; Liver injury; PAI 1; Trovafloxacin

Indexed keywords

ALANINE AMINOTRANSFERASE; CYTOKINE; DIMER; FIBRINOGEN; GAMMA INTERFERON; HEPARIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE CHEMOATTRACTANT; LIPOPOLYSACCHARIDE; MONOCYTE CHEMOTACTIC PROTEIN 1; PLASMINOGEN ACTIVATOR INHIBITOR 1; THROMBIN; THROMBIN ANTITHROMBIN COMPLEX; TROVAFLOXACIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; EXPOSURE; FIBRIN DEPOSITION; FIBRINOGEN BLOOD LEVEL; HEMOSTASIS; LIVER INJURY; LIVER TOXICITY; MALE; MOUSE; NONHUMAN; WILD TYPE;

ANIMALS; ANTICOAGULANTS; CYTOKINES; FLUOROQUINOLONES; HEMOSTASIS; HEPARIN; LIPOPOLYSACCHARIDES; LIVER; MICE; MICE, KNOCKOUT; NAPHTHYRIDINES; PLASMINOGEN ACTIVATOR INHIBITOR 1;

MURINAE; MUS;

EID: 63649113233     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.01.018     Document Type: Article

References (44)

1. Arteel G.E. New role of plasminogen activator inhibitor-1 in alcohol-induced liver injury. J. Gastroenterol. Hepatol. 23 Suppl 1 (2008) S54-S59
2. Ball P. Adverse drug reactions: implications for the development of fluoroquinolones. J. Antimicrob. Chemother. 51 Suppl 1 (2003) 21-27
3. Bergheim I., Guo L., Davis M.A., Duveau I., and Arteel G.E. Critical role of plasminogen activator inhibitor-1 in cholestatic liver injury and fibrosis. J. Pharmacol. Exp. Ther. 316 (2006) 592-600
4. Buchweitz J.P., Ganey P.E., Bursian S.J., and Roth R.A. Underlying endotoxemia augments toxic responses to chlorpromazine: is there a relationship to drug idiosyncrasy?. J. Pharmacol. Exp. Ther. 300 (2002) 460-467
5. Chandel N.S., Maltepe E., Goldwasser E., Mathieu C.E., Simon M.C., and Schumacker P.T. Mitochondrial reactive oxygen species trigger hypoxia-induced transcription. Proc. Natl. Acad. Sci. U.S.A 95 (1998) 11715-11720
6. Chandel N.S., McClintock D.S., Feliciano C.E., Wood T.M., Melendez J.A., Rodriguez A.M., and Schumacker P.T. Reactive oxygen species generated at mitochondrial complex III stabilize hypoxia-inducible factor-1alpha during hypoxia: a mechanism of O2 sensing. J. Biol. Chem. 275 (2000) 25130-25138
7. Copple B.L., Banes A., Ganey P.E., and Roth R.A. Endothelial cell injury and fibrin deposition in rat liver after monocrotaline exposure. Toxicol. Sci. 65 (2002) 309-318
8. Dalhoff A., and Schmitz F.J. In vitro antibacterial activity and pharmacodynamics of new quinolones. Eur. J. Clin. Microbiol. Infect. Dis. 22 (2003) 203-221
9. Deng X., Lu J., Lehman-McKeeman L.D., Malle E., Crandall D.L., Ganey P.E., and Roth R.A. p38 mitogen-activated protein kinase-dependent tumor necrosis factor-alpha-converting enzyme is important for liver injury in hepatotoxic interaction between lipopolysaccharide and ranitidine. J. Pharmacol. Exp. Ther. 326 (2008) 144-152
10. Endtz H.P., Mouton J.W., den Hollander J.G., van den B.N., and Verbrugh H.A. Comparative in vitro activities of trovafloxacin (CP-99,219) against 445 gram-positive isolates from patients with endocarditis and those with other bloodstream infections. Antimicrob. Agents Chemother. 41 (1997) 1146-1149
11. Fontana R.J., and Quallich L.G. Acute liver failure. Curr. Opin. Gastroenterol. 17 (2001) 291-298
12. Forsythe J.A., Jiang B.H., Iyer N.V., Agani F., Leung S.W., Koos R.D., and Semenza G.L. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol. Cell Biol. 16 (1996) 4604-4613
13. Ganey P.E., Luyendyk J.P., Maddox J.F., and Roth R.A. Adverse hepatic drug reactions: inflammatory episodes as consequence and contributor. Chem. Biol. Interact. 150 (2004) 35-51
14. Ganey P.E., Luyendyk J.P., Newport S.W., Eagle T.M., Maddox J.F., Mackman N., and Roth R.A. Role of the coagulation system in acetaminophen-induced hepatotoxicity in mice. Hepatology 46 (2007) 1177-1186
15. Girard A.E., Girard D., Gootz T.D., Faiella J.A., and Cimochowski C.R. In vivo efficacy of trovafloxacin (CP-99,219), a new quinolone with extended activities against gram-positive pathogens, Streptococcus pneumoniae, and Bacteroides fragilis. Antimicrob. Agents Chemother. 39 (1995) 2210-2216
16. Gnant M.F., Turner E.M., and Alexander Jr. H.R. Effects of hyperthermia and tumour necrosis factor on inflammatory cytokine secretion and procoagulant activity in endothelial cells. Cytokine 12 (2000) 339-347
17. Goel K., Menzies D., and Cunha B.A. Elevated international normalized ratio associated with trovafloxacin. Ann. Intern. Med. 131 (1999) 72
18. Harada N., Okajima K., and Uchiba M. Dalteparin, a low molecular weight heparin, attenuates inflammatory responses and reduces ischemia-reperfusion-induced liver injury in rats. Crit. Care Med. 34 (2006) 1883-1891
19. Hewett J.A., and Roth R.A. The coagulation system, but not circulating fibrinogen, contributes to liver injury in rats exposed to lipopolysaccharide from gram-negative bacteria. J. Pharmacol. Exp. Ther. 272 (1995) 53-62
20. Koj A., Gauldie J., Regoeczi E., Sauder D.N., and Sweeney G.D. The acute-phase response of cultured rat hepatocytes. System characterization and the effect of human cytokines. Biochem. J. 224 (1984) 505-514
21. Kwak S.H., Wang X.Q., He Q., Fang W.F., Mitra S., Bdeir K., Ploplis V.A., Xu Z., Idell S., Cines D., and Abraham E. Plasminogen activator inhibitor-1 potentiates LPS-induced neutrophil activation through a JNK-mediated pathway. Thromb. Haemost. 95 (2006) 829-835
22. Lasser K.E., Allen P.D., Woolhandler S.J., Himmelstein D.U., Wolfe S.M., and Bor D.H. Timing of new black box warnings and withdrawals for prescription medications. JAMA 287 (2002) 2215-2220
23. Lazarczyk D.A., Goldstein N.S., and Gordon S.C. Trovafloxacin hepatotoxicity. Dig. Dis. Sci. 46 (2001) 925-926
24. Luyendyk J.P., Lehman-McKeeman L.D., Nelson D.M., Bhaskaran V.M., Reilly T.P., Car B.D., Cantor G.H., Deng X., Maddox J.F., Ganey P.E., and Roth R.A. Coagulation-dependent gene expression and liver injury in rats given lipopolysaccharide with ranitidine but not with famotidine. J. Pharmacol. Exp. Ther. 317 (2006) 635-643
25. Luyendyk J.P., Maddox J.F., Cosma G.N., Ganey P.E., Cockerell G.L., and Roth R.A. Ranitidine treatment during a modest inflammatory response precipitates idiosyncrasy-like liver injury in rats. J. Pharmacol. Exp. Ther. 307 (2003) 9-16
26. Luyendyk J.P., Shaw P.J., Green C.D., Maddox J.F., Ganey P.E., and Roth R.A. Coagulation-mediated hypoxia and neutrophil-dependent hepatic injury in rats given lipopolysaccharide and ranitidine. J. Pharmacol. Exp. Ther. 314 (2005) 1023-1031
27. Mandell L.A., Ball P., and Tillotson G. Antimicrobial safety and tolerability: differences and dilemmas. Clin. Infect. Dis. 32 Suppl 1 (2001) S72-S79
28. Naldini A., Morena E., Filippi I., Pucci A., Bucci M., Cirino G., and Carraro F. Thrombin inhibits IFN-gamma production in human peripheral blood mononuclear cells by promoting a Th2 profile. J. Interferon Cytokine Res. 26 (2006) 793-799
29. Owens Jr. R.C., and Ambrose P.G. Antimicrobial safety: focus on fluoroquinolones. Clin. Infect. Dis. 41 Suppl 2 (2005) S144-S157
30. Ranby M., and Brandstrom A. Biological control of tissue plasminogen activator-mediated fibrinolysis. Enzyme 40 (1988) 130-143
31. Renckens R., Pater J.M., and van der P.T. Plasminogen activator inhibitor type-1-deficient mice have an enhanced IFN-gamma response to lipopolysaccharide and staphylococcal enterotoxin. B. J. Immunol. 177 (2006) 8171-8176
32. Renckens R., Roelofs J.J., de V W., Florquin S., Lijnen H.R., Carmeliet P., and van der P.T. The role of plasminogen activator inhibitor type 1 in the inflammatory response to local tissue injury. J. Thromb. Haemost. 3 (2005) 1018-1025
33. Roth R.A., Luyendyk J.P., Maddox J.F., and Ganey P.E. Inflammation and drug idiosyncrasy-is there a connection?. J. Pharmacol. Exp. Ther. 307 (2003) 1-8
34. Shaw P.J., Ditewig A.C., Waring J.F., Liguori M.J., Blomme E.A., Ganey P.E., and Roth R.A. Coexposure of mice to trovafloxacin and lipopolysaccharide, a model of idiosyncratic hepatotoxicity, results in a unique gene expression profile and interferon gamma-dependent liver injury. Toxicol. Sci. 107 (2009) 270-280
35. Shaw P.J., Ganey P.E., and Roth R.A. Tumor necrosis factor alpha is a proximal mediator of synergistic hepatotoxicity from trovafloxacin/lipopolysaccharide coexposure. J. Pharmacol. Exp. Ther. 328 (2009) 62-68
36. Shaw P.J., Ganey P.E., and Roth R.A. Trovafloxacin enhances the inflammatory response to a gram-negative or a gram-positive stimulus, resulting in neutrophil-dependent liver injury in mice. Toxicologist 102 (2008) Ref Type: Abstract
37. Shaw P.J., Hopfensperger M.J., Ganey P.E., and Roth R.A. Lipopolysaccharide and trovafloxacin coexposure in mice causes idiosyncrasy-like liver injury dependent on tumor necrosis factor-alpha. Toxicol. Sci. 100 (2007) 259-266
38. Smith M.K., and Mooney D.J. Hypoxia leads to necrotic hepatocyte death. J. Biomed. Mater. Res. A 80 (2007) 520-529
39. Sun Q., Zhu R., Foss Jr. F.W., and Macdonald T.L. Mechanisms of trovafloxacin hepatotoxicity: studies of a model cyclopropylamine-containing system. Bioorg. Med. Chem. Lett. 17 (2007) 6682-6686
40. Uetrecht J. Idiosyncratic drug reactions: current understanding. Annu. Rev. Pharmacol. Toxicol. 47 (2007) 513-539
41. van V H., Kooistra T., van den Berg E.A., Princen H.M., Fiers W., and Emeis J.J. Tumor necrosis factor increases the production of plasminogen activator inhibitor in human endothelial cells in vitro and in rats in vivo. Blood 72 (1988) 1467-1473
42. Waring J.F., Liguori M.J., Luyendyk J.P., Maddox J.F., Ganey P.E., Stachlewitz R.F., North C., Blomme E.A., and Roth R.A. Microarray analysis of lipopolysaccharide potentiation of trovafloxacin-induced liver injury in rats suggests a role for proinflammatory chemokines and neutrophils. J. Pharmacol. Exp. Ther. 316 (2006) 1080-1087
43. Yee S.B., Hanumegowda U.M., Copple B.L., Shibuya M., Ganey P.E., and Roth R.A. Endothelial cell injury and coagulation system activation during synergistic hepatotoxicity from monocrotaline and bacterial lipopolysaccharide coexposure. Toxicol. Sci. 74 (2003) 203-214
44. Zou W., Devi S.S., Sparkenbaugh E., Younis H.S., Roth R.A., and Ganey P.E. Hepatotoxic interaction of sulindac with lipopolysaccharide: role of the hemostatic system. Toxicol. Sci (2008)