The role of damage associated molecular pattern molecules in acetaminophen-induced liver injury in mice

Toxicology Letters

Volumn 192, Issue 3, 2010, Pages 387-394

  Martin Murphy, Brittany V ^a   Holt, Michael P ^a   Ju, Cynthia ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Acetaminophen; Damage associated molecular pattern molecules; Heat shock proteins; High mobility group box 1; Liver; Macrophages

Indexed keywords

HEAT SHOCK PROTEIN 70; HIGH MOBILITY GROUP B1 PROTEIN; PARACETAMOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; KUPFFER CELL; LIVER CELL CULTURE; LIVER TOXICITY; MACROPHAGE ACTIVATION; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; TOXICITY TESTING;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; CELL LINE; DRUG-INDUCED LIVER INJURY; FEMALE; HMGB1 PROTEIN; HSP70 HEAT-SHOCK PROTEINS; IMMUNOBLOTTING; INTERLEUKIN-1BETA; INTERLEUKIN-6; LIVER; MACROPHAGE ACTIVATION; MICE; MICE, INBRED C57BL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA;

MURINAE; MUS;

EID: 75349095405     PISSN: 03784274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.toxlet.2009.11.016     Document Type: Article

References (59)

1. Asea A., Kraeft S.K., Kurt-Jones E.A., Stevenson M.A., Chen L.B., Finberg R.W., Koo G.C., and Calderwood S.K. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat. Med. 6 (2000) 435-442
2. Asea A., Rehli M., Kabingu E., Boch J.A., Bare O., Auron P.E., Stevenson M.A., and Calderwood S.K. Novel signal transduction pathway utilized by extracellular HSP70: role of toll-like receptor (TLR) 2 and TLR4. J. Biol. Chem. 277 (2002) 15028-15034
3. Biragyn A., Ruffini P.A., Leifer C.A., Klyushnenkova E., Shakhov A., Chertov O., Shirakawa A.K., Farber J.M., Segal D.M., Oppenheim J.J., and Kwak L.W. Toll-like receptor 4-dependent activation of dendritic cells by beta-defensin 2. Science 298 (2002) 1025-1029
4. Blazka M.E., Elwell M.R., Holladay S.D., Wilson R.E., and Luster M.I. Histopathology of acetaminophen-induced liver changes: role of interleukin 1 alpha and tumor necrosis factor alpha. Toxicol. Pathol. 24 (1996) 181-189
5. Blazka M.E., Wilmer J.L., Holladay S.D., Wilson R.E., and Luster M.I. Role of proinflammatory cytokines in acetaminophen hepatotoxicity. Toxicol. Appl. Pharmacol. 133 (1995) 43-52
6. Bourdi M., Masubuchi Y., Reilly T.P., Amouzadeh H.R., Martin J.L., George J.W., Shah A.G., and Pohl L.R. Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase. Hepatology 35 (2002) 289-298
7. Bourdi M., Reilly T.P., Elkahloun A.G., George J.W., and Pohl L.R. Macrophage migration inhibitory factor in drug-induced liver injury: a role in susceptibility and stress responsiveness. Biochem. Biophys. Res. Commun 294 (2002) 225-230
8. Chen G.Y., Tang J., Zheng P., and Liu Y. CD24 and Siglec-10 selectively repress tissue damage-induced immune responses. Science 323 (2009) 1722-1725
9. Chen W., Syldath U., Bellmann K., Burkart V., and Kolb H. Human 60-kDa heat-shock protein: a danger signal to the innate immune system. J. Immunol. 162 (1999) 3212-3219
10. Cover C., Liu J., Farhood A., Malle E., Waalkes M.P., Bajt M.L., and Jaeschke H. Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity. Toxicol. Appl. Pharmacol. 216 (2006) 98-107
11. Fennekohl A., Sugimoto Y., Segi E., Maruyama T., Ichikawa A., and Puschel G.P. Contribution of the two Gs-coupled PGE2-receptors EP2-receptor and EP4-receptor to the inhibition by PGE2 of the LPS-induced TNFalpha-formation in Kupffer cells from EP2- or EP4-receptor-deficient mice. Pivotal role for the EP4-receptor in wild type Kupffer cells. J. Hepatol. 36 (2002) 328-334
12. Gunawan B.K., and Kaplowitz N. Mechanisms of drug-induced liver disease. Clin. Liver Dis. 11 (2007) 459-475
13. Hickman-Miller H.D., and Hildebrand W.H. The immune response under stress: the role of HSP-derived peptides. Trends Immunol. 25 (2004) 427-433
14. Imaeda A.B., Watanabe A., Sohail M.A., Mahmood S., Mohamadnejad M., Sutterwala F.S., Flavell R.A., and Mehal W.Z. Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J. Clin. Invest. 119 (2009) 305-314
15. Ishida Y., Kondo T., Kimura A., Tsuneyama K., Takayasu T., and Mukaida N. Opposite roles of neutrophils and macrophages in the pathogenesis of acetaminophen-induced acute liver injury. Eur. J. Immunol. 36 (2006) 1028-1038
16. Ishida Y., Kondo T., Ohshima T., Fujiwara H., Iwakura Y., and Mukaida N. A pivotal involvement of IFN-gamma in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J. 16 (2002) 1227-1236
17. James L.P., McCullough S.S., Lamps L.W., and Hinson J.A. Effect of N-acetylcysteine on acetaminophen toxicity in mice: relationship to reactive nitrogen and cytokine formation. Toxicol. Sci. 75 (2003) 458-467
18. Ju C., Reilly T.P., Bourdi M., Radonovich M.F., Brady J.N., George J.W., and Pohl L.R. Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem. Res. Toxicol. 15 (2002) 1504-1513
19. Kaplowitz N. Drug-induced liver disorders: implications for drug development and regulation. Drug Saf. 24 (2001) 483-490
20. Kaplowitz N. Acetaminophen hepatoxicity: what do we know, what don't we know, and what do we do next?. Hepatology 40 (2004) 23-26
21. Kaplowitz N. Idiosyncratic drug hepatotoxicity. Nat. Rev. Drug Discov. 4 (2005) 489-499
22. Kawamura H., Aswad F., Minagawa M., Govindarajan S., and Dennert G. P2X7 receptors regulate NKT cells in autoimmune hepatitis. J. Immunol. 176 (2006) 2152-2160
23. Laskin D.L., and Laskin J.D. Role of macrophages and inflammatory mediators in chemically induced toxicity. Toxicology 160 (2001) 111-118
24. Lee S.S., Buters J.T., Pineau T., Fernandez-Salguero P., and Gonzalez F.J. Role of CYP2E1 in the hepatotoxicity of acetaminophen. J. Biol. Chem. 271 (1996) 12063-12067
25. Lee W.M. Drug-induced hepatotoxicity. N. Engl. J. Med. 349 (2003) 474-485
26. Lee W.M. Acetaminophen and the U.S. Acute Liver Failure Study Group: lowering the risks of hepatic failure. Hepatology 40 (2004) 6-9
27. Lee W.M., and Senior J.R. Recognizing drug-induced liver injury: current problems, possible solutions. Toxicol. Pathol. 33 (2005) 155-164
28. Liu Z.X., Govindarajan S., and Kaplowitz N. Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 127 (2004) 1760-1774
29. Liu Z.X., Han D., Gunawan B., and Kaplowitz N. Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 43 (2006) 1220-1230
30. Lotze M.T., and Tracey K.J. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat. Rev. Immunol. 5 (2005) 331-342
31. Mambula S.S., and Calderwood S.K. Heat shock protein 70 is secreted from tumor cells by a nonclassical pathway involving lysosomal endosomes. J. Immunol. 177 (2006) 7849-7857
32. Martin C.A., Carsons S.E., Kowalewski R., Bernstein D., Valentino M., and Santiago-Schwarz F. Aberrant extracellular and dendritic cell (DC) surface expression of heat shock protein (hsp)70 in the rheumatoid joint: possible mechanisms of hsp/DC-mediated cross-priming. J. Immunol. 171 (2003) 5736-5742
33. Masson M.J., Carpenter L.D., Graf M.L., and Pohl L.R. Pathogenic role of natural killer T and natural killer cells in acetaminophen-induced liver injury in mice is dependent on the presence of dimethyl sulfoxide. Hepatology 48 (2008) 889-897
34. Masubuchi Y., Bourdi M., Reilly T.P., Graf M.L., George J.W., and Pohl L.R. Role of interleukin-6 in hepatic heat shock protein expression and protection against acetaminophen-induced liver disease. Biochem. Biophys. Res. Commun. 304 (2003) 207-212
35. Matzinger P. Tolerance, danger, and the extended family. Annu. Rev. Immunol. 12 (1994) 991-1045
36. Michael S.L., Pumford N.R., Mayeux P.R., Niesman M.R., and Hinson J.A. Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 30 (1999) 186-195
37. Minagawa M., Oya H., Yamamoto S., Shimizu T., Bannai M., Kawamura H., Hatakeyama K., and Abo T. Intensive expansion of natural killer T cells in the early phase of hepatocyte regeneration after partial hepatectomy in mice and its association with sympathetic nerve activation. Hepatology 31 (2000) 907-915
38. Nelson S.D. Molecular mechanisms of the hepatotoxicity caused by acetaminophen. Semin. Liver Dis. 10 (1990) 267-278
39. Okamura Y., Watari M., Jerud E.S., Young D.W., Ishizaka S.T., Rose J., Chow J.C., and Strauss III J.F. The extra domain A of fibronectin activates Toll-like receptor 4. J. Biol. Chem. 276 (2001) 10229-10233
40. Ostapowicz G., Fontana R.J., Schiodt F.V., Larson A., Davern T.J., Han S.H., McCashland T.M., Shakil A.O., Hay J.E., Hynan L., Crippin J.S., Blei A.T., Samuel G., Reisch J., and Lee W.M. Results of a prospective study of acute liver failure at 17 tertiary care centers in the United States. Ann. Intern. Med. 137 (2002) 947-954
41. Peitsch M.C., Tschopp J., Kress A., and Isliker H. Antibody-independent activation of the complement system by mitochondria is mediated by cardiolipin. Biochem. J. 249 (1988) 495-500
42. Pumford N.R., Halmes N.C., and Hinson J.A. Covalent binding of xenobiotics to specific proteins in the liver. Drug Metab. Rev. 29 (1997) 39-57
43. Raucy J.L., Lasker J.M., Lieber C.S., and Black M. Acetaminophen activation by human liver cytochromes P450IIE1 and P450IA2. Arch. Biochem. Biophys. 271 (1989) 270-283
44. Reilly T.P., Brady J.N., Marchick M.R., Bourdi M., George J.W., Radonovich M.F., Pise-Masison C.A., and Pohl L.R. A protective role for cyclooxygenase-2 in drug-induced liver injury in mice. Chem. Res. Toxicol. 14 (2001) 1620-1628
45. Rumack B.H. Acetaminophen misconceptions. Hepatology 40 (2004) 10-15
46. Sapozhnikov A.M., Ponomarev E.D., Tarasenko T.N., and Telford W.G. Spontaneous apoptosis and expression of cell surface heat-shock proteins in cultured EL-4 lymphoma cells. Cell Prolif. 32 (1999) 363-378
47. Scaffidi P., Misteli T., and Bianchi M.E. Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418 (2002) 191-195
48. Seong S.Y., and Matzinger P. Hydrophobicity: an ancient damage-associated molecular pattern that initiates innate immune responses. Nat. Rev. Immunol. 4 (2004) 469-478
49. Shi Y., Evans J.E., and Rock K.L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425 (2003) 516-521
50. Smedsrod B., and Pertoft H. Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J. Leukoc. Biol. 38 (1985) 213-230
51. Termeer C., Benedix F., Sleeman J., Fieber C., Voith U., Ahrens T., Miyake K., Freudenberg M., Galanos C., and Simon J.C. Oligosaccharides of Hyaluronan activate dendritic cells via toll-like receptor 4. J. Exp. Med. 195 (2002) 99-111
52. Theriault J.R., Mambula S.S., Sawamura T., Stevenson M.A., and Calderwood S.K. Extracellular HSP70 binding to surface receptors present on antigen presenting cells and endothelial/epithelial cells. FEBS Lett. 579 (2005) 1951-1960
53. Tsung A., Sahai R., Tanaka H., Nakao A., Fink M.P., Lotze M.T., Yang H., Li J., Tracey K.J., Geller D.A., and Billiar T.R. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion. J. Exp. Med. 201 (2005) 1135-1143
54. Vabulas R.M., Ahmad-Nejad P., da Costa C., Miethke T., Kirschning C.J., Hacker H., and Wagner H. Endocytosed HSP60s use toll-like receptor 2 (TLR2) and TLR4 to activate the toll/interleukin-1 receptor signaling pathway in innate immune cells. J. Biol. Chem. 276 (2001) 31332-31339
55. Vabulas R.M., Ahmad-Nejad P., Ghose S., Kirschning C.J., Issels R.D., and Wagner H. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J. Biol. Chem. 277 (2002) 15107-15112
56. Wallin R.P., Lundqvist A., More S.H., von Bonin A., Kiessling R., and Ljunggren H.G. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 23 (2002) 130-135
57. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S., Borovikova L., Manogue K.R., Faist E., Abraham E., Andersson J., Andersson U., Molina P.E., Abumrad N.N., Sama A., and Tracey K.J. HMG-1 as a late mediator of endotoxin lethality in mice. Science 285 (1999) 248-251
58. Welch K.D., Reilly T.P., Bourdi M., Hays T., Pise-Masison C.A., Radonovich M.F., Brady J.N., Dix D.J., and Pohl L.R. Genomic identification of potential risk factors during acetaminophen-induced liver disease in susceptible and resistant strains of mice. Chem. Res. Toxicol. 19 (2006) 223-233
59. Yang D., Chen Q., Yang H., Tracey K.J., Bustin M., and Oppenheim J.J. High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin. J. Leukoc. Biol. 81 (2007) 59-66