Bacterial- and Viral-Induced Inflammation Increases Sensitivity to Acetaminophen Hepatotoxicity

REFERENCES

• Ackerman , Z. , Flugelman , M. Y. , Wax , Y. , Shouval , D. and Levy , M. 1989 . Hepatitis during measles in young adults: Possible role of antipyretic drugs . Hepatology , 10 : 203 – 206 .
   PubMed Web of Science ®Google Scholar
• Barton , E. S. , Youree , B. E. , Ebert , D. H. , Forrest , J. C. , Connolly , J. L. , Valyi-Nagy , T. , Washington , K. , Wetzel , J. D. and Dermody , T. S. 2003 . Utilization of sialic acid as a coreceptor is required for reovirus-induced biliary disease . J. Clin. Invest. , 111 : 1823 – 1833 .
   PubMedGoogle Scholar
• Bode , C. and Bode , J. C. 2005 . Activation of the innate immune system and alcoholic liver disease: Effects of ethanol per se or enhanced intestinal translocation of bacterial toxins induced by ethanol? . Alcohol Clin. Exp. Res. , 29 : 166S – 171S .
   Web of Science ®Google Scholar
• Buchweitz , J. P. , Ganey , P. E. , Bursian , S. J. and Roth , R. A. 2002 . Underlying endotoxemia augments toxic responses to chlorpromazine: Is there a relationship to drug idiosyncrasy? . J. Pharmacol. Exp. Ther. , 300 : 460 – 467 .
   PubMed Web of Science ®Google Scholar
• 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 .
   PubMed Web of Science ®Google Scholar
• Cuff , C. F. , Cebra , C. K. , Rubin , D. H. and Cebra , J. J. 1993 . Developmental relationship between cytotoxic alpha/beta T cell receptor-positive intraepithelial lymphocytes and Peyer's patch lymphocytes . Eur. J. Immunol , 23 : 1333 – 1339 .
   PubMed Web of Science ®Google Scholar
• Fan , J. Y. , Boyce , C. S. and Cuff , C. F. 1998 . T‐Helper 1 and T-helper 2 cytokine responses in gut-associated lymphoid tissue following enteric reovirus infection . Cell Immunol , 188 : 55 – 63 .
   PubMedGoogle Scholar
• Farone , A. L. , O'Donnell , S.M , Brooks , C. S. , Young , K. M. , Pierce , J. M. , Wetzel , J. D. , Dermody , T. S. and Farone , M. B. 2006 . Reovirus strain-dependent inflammatory cytokine responses and replication patterns in a human monocyte cell line . Viral Immunol. , 19 : 546 – 557 .
   PubMedGoogle Scholar
• Ganey , P. E. , Luyendyk , J. P. , Maddox , J. F. and Roth , R. A. 2004 . Adverse hepatic drug reactions: inflammatory episodes as consequence and contributor . Chem. Biol. Interact. , 150 : 35 – 51 .
   PubMed Web of Science ®Google Scholar
• Ganey , P. E. , Luyendyk , J. P. , Newport , S. W. , Eagle , T. M. , Maddox , J. F. , Mackman , N. and Roth , R. A. 2007 . Role of the coagulation system in acetaminophen-induced hepatotoxicity in mice . Hepatology , 46 : 1177 – 1186 .
   PubMedGoogle Scholar
• Gardner , C. R. , Laskin , J. D. , Dambach , D. M. , Chiu , H. , Durham , S. K. , Zhou , P. , Bruno , M. , Gerecke , D. R. , Gordon , M. K. and Laskin , D. L. 2003 . Exaggerated hepatotoxicity of acetaminophen in mice lacking tumor necrosis factor receptor-1. Potential role of inflammatory mediators . Toxicol. Appl. Pharmacol. , 192 : 119 – 130 .
   PubMed Web of Science ®Google Scholar
• Gardner , C. R. , Laskin , J. D. , Dambach , D. M. , Sacco , M. , Durham , S. K. , Bruno , M. K. , Cohen , S. D. , Gordon , M. K. , Gerecke , D. R. , Zhou , P. and Laskin , D. L. 2002 . Reduced hepatotoxicity of acetaminophen in mice lacking inducible nitric oxide synthase: Potential role of tumor necrosis factor-alpha and interleukin-10 . Toxicol. Appl. Pharmacol. , 184 : 27 – 36 .
   PubMed Web of Science ®Google Scholar
• Gunawan , B. K. and Kaplowitz , N. 2007 . Mechanisms of drug-induced liver disease . Clin. Liver Dis. , 11 : 459 – 475 .
   PubMedGoogle Scholar
• Himeno , Y. , Etoh , T. , Matsumoto , T. , Ohta , M. , Nishizono , A. and Kitano , S. 2005 . Efficacy of oncolytic reovirus against liver metastasis from pancreatic cancer in immunocompetent models . Int. J. Oncol. , 27 : 901 – 906 .
   PubMed Web of Science ®Google Scholar
• Hinson , J. A. , Reid , A. B. , McCullough , S. S. and James , L. P. 2004 . Acetaminophen-induced hepatotoxicity: Role of metabolic activation, reactive oxygen/nitrogen species, and mitochondrial permeability transition . Drug Metab. Rev. , 36 : 805 – 822 .
   PubMed Web of Science ®Google Scholar
• Ishida , Y. , Kondo , T. , Tsuneyama , K. , Lu , P. , Takayasu , T. and Mukaida , N. 2004 . The pathogenic roles of tumor necrosis factor receptor p55 in acetaminophen-induced liver injury in mice . J. Leukocyte Biol. , 75 : 59 – 67 .
   PubMed Web of Science ®Google Scholar
• Ishikawa , M. , Tanno , K. , Sasaki , M. , Takayanagi , Y. and Sasaki , K. 1990 . Antidotal effect of lipopolysaccharide against acetaminophen-induced mortality in mice . Pharmacol. Toxicol. , 67 : 387 – 391 .
   PubMedGoogle Scholar
• Ito , Y , Abril , E. R. , Bethea , N. W. and McCuskey , R. S. 2004 . Role of nitric oxide in hepatic microvascular injury elicited by acetaminophen in mice . Am. J. Physiol. Gastrointest. Liver Physiol. , 286 : G60 – G67 .
   PubMed Web of Science ®Google Scholar
• Kim , H. J. , Tsoyi , K. , Heo , J. M. , Kang , Y. J. , Park , M. K. , Lee , Y. S. , Lee , J. H. , Seo , H. G. , Yun-Choi , H. S. and Chang , K. C. 2007 . Regulation of lipopolysaccharide-induced inducible nitric-oxide synthase expression through the nuclear factor-kappaB pathway and interferon-beta/tyrosine kinase 2/Janus tyrosine kinase 2-signal transducer and activator of transcription-1 signaling cascades by 2-naphthylethyl-6,7-dihydroxy-1,2,3,4-tetrahydroisoquinoline (THI 53), a new synthetic isoquinoline alkaloid . J. Pharmacol. Exp. Ther. , 320 : 782 – 789 .
   PubMedGoogle Scholar
• Kinser , S. , Sneed , R. , Roth , R. and Ganey , P. 2004 . Neutrophils contribute to endotoxin enhancement of allyl alcohol hepatotoxicity . J. Toxicol. Environ. Health A , 67 : 911 – 928 .
   PubMed Web of Science ®Google Scholar
• Larson , A. M. , Polson , J. , Fontana , R. J. , Davern , T. J. , Lalani , E. , Hynan , L. S. , Reisch , J. S. , Schiodt , F. V. , Ostapowicz , G. , Shakil , A. O. and Lee , W. M. 2005 . Acetaminophen-induced acute liver failure: Results of a United States multicenter, prospective study . Hepatology , 42 : 1364 – 1372 .
   PubMed Web of Science ®Google Scholar
• Laskin , D. L. , Gardner , C. R. , Price , V. F. and Jollow , D. J. 1995 . Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen . Hepatology , 21 : 1045 – 1050 .
   PubMed Web of Science ®Google Scholar
• Lee , W. M. 2004 . Acetaminophen and the U.S. Acute Liver Failure Study Group: Lowering the risks of hepatic failure . Hepatology , 40 : 6 – 9 .
   PubMed Web of Science ®Google Scholar
• Li , M. , Cuff , C. F. and Pestka , J. 2005 . Modulation of murine host response to enteric reovirus infection by the trichothecene deoxynivalenol . Toxicol. Sci. , 87 : 134 – 145 .
   PubMedGoogle Scholar
• Li , M. , Harkema , J. R , Cuff , C. F. and Pestka , J. J. 2007 . Deoxynivalenol exacerbates viral bronchopneumonia induced by respiratory reovirus infection . Toxicol. Sci. , 95 : 412 – 426 .
   PubMedGoogle Scholar
• Lind , R. C. , Gandolfi , A. J. , Sipes , I. G. and Brown , B. R. Jr. 1984 . The involvement of endotoxin in halothane-associated liver injury . Anesthesiology , 61 : 544 – 550 .
   PubMed Web of Science ®Google Scholar
• Liu , J. , Sendelbach , L. E. , Parkinson , A. and Klaassen , C. D. 2000 . Endotoxin pretreatment protects against the hepatotoxicity of acetaminophen and carbon tetrachloride: Role of cytochrome P450 suppression . Toxicology , 147 : 167 – 176 .
   PubMed Web of Science ®Google Scholar
• Liu , Z. X. , Govindarajan , S. and Kaplowitz , N. 2004 . Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity . Gastroenterology , 127 : 1760 – 1774 .
   PubMed Web of Science ®Google Scholar
• Liu , Z. X. , Han , D. , Gunawan , B. and Kaplowitz , N. 2006 . Neutrophil depletion protects against murine acetaminophen hepatotoxicity . Hepatology , 43 : 1220 – 1230 .
   PubMed Web of Science ®Google Scholar
• Loo , Y. M. , Fornek , J. , Crochet , N. , Bajwa , G. , Perwitasari , O. , Martinez-Sobrido , L. , Akira , S. , Gill , M. A. , Garcia-Sastre , A. , Katze , M. G. and Gale , M. Jr. 2008 . Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity . J. Virol. , 82 : 335 – 345 .
   PubMed Web of Science ®Google Scholar
• Lores , A. S. , Llesuy , S. , Cutrin , J. C. and Boveris , A. 1995 . Oxidative stress by acute acetaminophen administration in mouse liver . Free Radical Biol. Med. , 19 : 303 – 310 .
   PubMedGoogle Scholar
• Major , A. S. and Cuff , C. F. 1996 . Effects of the route of infection on immunoglobulin G subclasses and specificity of the reovirus-specific humoral immune response . J. Virol. , 70 : 5968 – 5974 .
   PubMedGoogle Scholar
• Marriott , I. , Bost , K. L. and Huet-Hudson , Y. M. 2006 . Sexual dimorphism in expression of receptors for bacterial lipopolysaccharides in murine macrophages: A possible mechanism for gender-based differences in endotoxic shock susceptibility . J. Reprod. Immunol. , 71 : 12 – 27 .
   PubMed Web of Science ®Google Scholar
• Masubuchi , Y. , Sugiyama , S. and Horie , T. 2009 . Th1/Th2 cytokine balance as a determinant of acetaminophen-induced liver injury . Chem. Biol. Interact. , 179 : 273 – 279 .
   PubMed Web of Science ®Google Scholar
• Mathers , A. R. and Cuff , C. F. 2004 . Role of interleukin-4 (IL-4) and IL-10 in serum immunoglobulin G antibody responses following mucosal or systemic reovirus infection . J. Virol. , 78 : 3352 – 3360 .
   PubMed Web of Science ®Google Scholar
• McClain , C. J. , Kromhout , J. P. , Peterson , F. J. and Holtzman , J. L. 1980 . Potentiation of acetaminophen hepatotoxicity by alcohol . J. Am. Med. Assoc. , 244 : 251 – 253 .
   PubMed Web of Science ®Google Scholar
• McConnachie , L. A. , Mohar , I. , Hudson , F. N. , Ware , C. B. , Ladiges , W. C. , Fernandez , C. , Chatterton-Kirchmeier , S. , White , C. C. , Pierce , R. H. and Kavanagh , T. J. 2007 . Glutamate cysteine ligase modifier subunit deficiency and gender as determinants of acetaminophen-induced hepatotoxicity in mice . Toxicol. Sci. , 99 : 628 – 636 .
   PubMed Web of Science ®Google Scholar
• 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 .
   PubMed Web of Science ®Google Scholar
• Nibert , M. L. , Margraf , R. L. and Coombs , K. M. 1996 . Nonrandom segregation of parental alleles in reovirus reassortants . J. Virol. , 70 : 7295 – 7300 .
   PubMedGoogle Scholar
• Norman , K. L. and Lee , P. W. 2005 . Not all viruses are bad guys: The case for reovirus in cancer therapy . Drug Discov. Today , 10 : 847 – 855 .
   PubMed Web of Science ®Google Scholar
• Overbergh , L. , Giulietti , A. , Valckx , D. , Decallonne , R. , Bouillon , R. and Mathieu , C. 2003 . The use of real-time reverse transcriptase PCR for the quantification of cytokine gene expression . J. Biomol. Technol. , 14 : 33 – 43 .
   PubMedGoogle Scholar
• Piccoli , D. A. , Witzleben , C. L. , Guico , C. J. , Morrison , A. and Rubin , D. H. 1990 . Synergism between hepatic injuries and a nonhepatotropic reovirus in mice. Enhanced hepatic infection and death . J. Clin. Invest. , 86 : 1038 – 1045 .
   PubMedGoogle Scholar
• Placke , M. E. , Ginsberg , G. L. , Wyand , D. S. and Cohen , S. D. 1987 . Ultrastructural changes during acute acetaminophen-induced hepatotoxicity in the mouse: A time and dose study . Toxicol. Pathol. , 15 : 431 – 438 .
   PubMed Web of Science ®Google Scholar
• Rosenberg , D. M. , Meyer , A. A. , Manning , I. H. Jr. and Neelon , F. A. 1977 . Acetaminophen and hepatic dysfunction in infectious mononucleosis . South. Med. J. , 70 : 660 – 661 .
   PubMed Web of Science ®Google Scholar
• Roth , R. A. , Harkema , J. R. , Pestka , J. P. and Ganey , P. E. 1997 . Is exposure to bacterial endotoxin a determinant of susceptibility to intoxication from xenobiotic agents? . Toxicol. Appl. Pharmacol. , 147 : 300 – 311 .
   PubMed Web of Science ®Google Scholar
• Shaw , P. J. , Hopfensperger , M. J. , Ganey , P. E. and Roth , R. A. 2007 . Lipopolysaccharide and trovafloxacin coexposure in mice causes idiosyncrasy-like liver injury dependent on tumor necrosis factor-alpha . Toxicol. Sci. , 100 : 259 – 266 .
   PubMed Web of Science ®Google Scholar
• Silvey , K. J. , Hutchings , A. B. , Vajdy , M. , Petzke , M. M. and Neutra , M. R. 2001 . Role of immunoglobulin A in protection against reovirus entry into murine Peyer's patches . J. Virol. , 75 : 10870 – 10879 .
   PubMed Web of Science ®Google Scholar
• Smith , G. S. , Nadig , D. E. , Kokoska , E. R. , Solomon , H. , Tiniakos , D. G. and Miller , T. A. 1998 . Role of neutrophils in hepatotoxicity induced by oral acetaminophen administration in rats . J. Surg. Res , 80 : 252 – 258 .
   PubMed Web of Science ®Google Scholar
• Watkins , P. B. , Kaplowitz , N. , Slattery , J. T. , Colonese , C. R. , Colucci , S. V. , Stewart , P. W. and Harris , S. C. 2006 . Aminotransferase elevations in healthy adults receiving 4 grams of acetaminophen daily: A randomized controlled trial . J. Am. Med. Assoc. , 296 : 87 – 93 .
   PubMed Web of Science ®Google Scholar
• Wells , C. A. , Ravasi , T. , Faulkner , G. J. , Carninci , P. , Okazaki , Y. , Hayashizaki , Y. , Sweet , M. , Wainwright , B. J. and Hume , D. A. 2003 . Genetic control of the innate immune response . BMC Immunol , 4 : 5
   PubMedGoogle Scholar
• Whitcomb , D. C. and Block , G. D. 1994 . Association of acetaminophen hepatotoxicity with fasting and ethanol use . J. Am. Med. Assoc. , 272 : 1845 – 1850 .
   PubMed Web of Science ®Google Scholar
• Wolf , K. K. , Wood , S. G. , Allard , J. L. , Hunt , J. A. , Gorman , N. , Walton-Strong , B. W. , Szakacs , J. G. , Duan , S. X. , Hao , Q. , Court , M. H. , von Moltke , L. L. , Greenblatt , D. J. , Kostrubsky , V. , Jeffery , E. H. , Wrighton , S. A. , Gonzalez , F. J. , Sinclair , P. R. and Sinclair , J. F. 2007 . Role of CYP3A and CYP2E1 in alcohol-mediated increases in acetaminophen hepatotoxicity: Comparison of wild-type and Cyp2e1(-/-) mice . Drug Metab. Dispos. , 35 : 1223 – 1231 .
   PubMedGoogle Scholar
• Yaghi , C. , Honein , K. , Boujaoude , J. , Slim , R. , Moucari , R. and Sayegh , R. 2006 . Influence of acetaminophen at therapeutic doses on surrogate markers of severity of acute viral hepatitis . Gastroenterol. Clin. Biol. , 30 : 763 – 768 .
   PubMedGoogle Scholar
• Yee , S. B. , Bourdi , M. , Masson , M. J. and Pohl , L. R. 2007 . Hepatoprotective role of endogenous interleukin-13 in a murine model of acetaminophen-induced liver disease . Chem. Res. Toxicol. , 20 : 734 – 744 .
   PubMed Web of Science ®Google Scholar
• Yee , S. B. , Hanumegowda , U. M. , Hotchkiss , J. A. , Ganey , P. E. and Roth , R. A. 2003 . Role of neutrophils in the synergistic liver injury from monocrotaline and bacterial lipopolysaccharide exposure . Toxicol. Sci. , 72 : 43 – 56 .
   PubMedGoogle Scholar
• Zimmerman , H. J. and Maddrey , W. C. 1995 . Acetaminophen (paracetamol) hepatotoxicity with regular intake of alcohol: Analysis of instances of therapeutic misadventure . Hepatology , 22 : 767 – 773 .
   PubMed Web of Science ®Google Scholar