Deficiency of Interleukin-15 Enhances Susceptibility to Acetaminophen-Induced Liver Injury in Mice

PLoS ONE

Volumn 7, Issue 9, 2012, Pages

  Hou, Hsein San ^a   Liao, Ching Len ^a   Sytwu, Huey Kang ^a   Liao, Nan Shih ^a,b   Huang, Tien Yu ^c   Hsieh, Tsai Yuan ^c   Chu, Heng Cheng ^a,c  

^a NATIONAL DEFENSE MEDICAL CENTER   (Taiwan)

^b INSTITUTE OF MOLECULAR BIOLOGY   (Taiwan)

^c TRI SERVICE GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

GALACTOSAMINE; GAMMA INTERFERON; GLUTATHIONE; HEME OXYGENASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 15; INTERLEUKIN 1BETA; PARACETAMOL; RECOMBINANT INTERLEUKIN 15; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE PREDISPOSITION; DRUG METABOLISM; KNOCKOUT MOUSE; KUPFFER CELL; LIVER CELL; MALE; MONOCYTE; MOUSE; NEUTROPHIL; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; SURVIVAL; TOXIC HEPATITIS; WILD TYPE;

ACETAMINOPHEN; ANIMALS; ANTIBODIES, NEUTRALIZING; DISEASE SUSCEPTIBILITY; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; ENZYME INDUCTION; GENE KNOCKOUT TECHNIQUES; HEME OXYGENASE-1; HEPATITIS; INTERLEUKIN-15; KUPFFER CELLS; LIVER; MALE; MICE; MICE, INBRED C57BL; NITRIC OXIDE SYNTHASE TYPE II; ORGAN SPECIFICITY; RECOMBINANT PROTEINS; TRANSCRIPTION, GENETIC;

ANIMALIA; MUS;

EID: 84866489528     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0044880     Document Type: Article

References (60)

1. Dahlin DC, Miwa GT, Lu AY, Nelson SD, (1984) N-acetyl-p-benzoquinone imine: a cytochrome P-450-mediated oxidation product of acetaminophen. Proc Natl Acad Sci U S A 81: 1327-1331.
2. Mitchell JR, Jollow DJ, Potter WZ, Gillette JR, Brodie BB, (1973) Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione. J Pharmacol Exp Ther 187: 211-217.
3. Jaeschke H, (1990) Glutathione disulfide formation and oxidant stress during acetaminophen-induced hepatotoxicity in mice in vivo: the protective effect of allopurinol. J Pharmacol Exp Ther 255: 935-941.
4. Kon K, Kim JS, Jaeschke H, Lemasters JJ, (2004) Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 40: 1170-1179.
5. Chiu H, Brittingham JA, Laskin DL, (2002) Differential induction of heme oxygenase-1 in macrophages and hepatocytes during acetaminophen-induced hepatotoxicity in the rat: effects of hemin and biliverdin. Toxicol Appl Pharmacol 181: 106-115.
6. Kaplowitz N, (2005) Idiosyncratic drug hepatotoxicity. Nat Rev Drug Discov 4: 489-499.
7. Liu ZX, Govindarajan S, Kaplowitz N, (2004) Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 127: 1760-1774.
8. Liu ZX, Han D, Gunawan B, Kaplowitz N, (2006) Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 43: 1220-1230.
9. Connolly MK, Ayo D, Malhotra A, Hackman M, Bedrosian AS, et al. (2011) Dendritic cell depletion exacerbates acetaminophen hepatotoxicity. Hepatology 54: 959-968.
10. Michael SL, Pumford NR, Mayeux PR, Niesman MR, Hinson JA, (1999) Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 30: 186-195.
11. Ju C, Reilly TP, Bourdi M, Radonovich MF, Brady JN, et al. (2002) Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem Res Toxicol 15: 1504-1513.
12. Masson MJ, Carpenter LD, Graf ML, Pohl LR, (2008) 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: 889-897.
13. Cover C, Liu J, Farhood A, Malle E, Waalkes MP, et al. (2006) Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 216: 98-107.
14. Bourdi M, Masubuchi Y, Reilly TP, Amouzadeh HR, Martin JL, et al. (2002) Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase. Hepatology 35: 289-298.
15. Masubuchi Y, Bourdi M, Reilly TP, Graf ML, George JW, et al. (2003) Role of interleukin-6 in hepatic heat shock protein expression and protection against acetaminophen-induced liver disease. Biochem Biophys Res Commun 304: 207-212.
16. Yee SB, Bourdi M, Masson MJ, Pohl LR, (2007) Hepatoprotective role of endogenous interleukin-13 in a murine model of acetaminophen-induced liver disease. Chem Res Toxicol 20: 734-744.
17. Blazka ME, Wilmer JL, Holladay SD, Wilson RE, Luster MI, (1995) Role of proinflammatory cytokines in acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 133: 43-52.
18. Ishida Y, Kondo T, Ohshima T, Fujiwara H, Iwakura Y, et al. (2002) A pivotal involvement of IFN-gamma in the pathogenesis of acetaminophen-induced acute liver injury. FASEB J 16: 1227-1236.
19. Imaeda AB, Watanabe A, Sohail MA, Mahmood S, Mohamadnejad M, et al. (2009) Acetaminophen-induced hepatotoxicity in mice is dependent on Tlr9 and the Nalp3 inflammasome. J Clin Invest 119: 305-314.
20. Budagian V, Bulanova E, Paus R, Bulfone-Paus S, (2006) IL-15/IL-15 receptor biology: a guided tour through an expanding universe. Cytokine Growth Factor Rev 17: 259-280.
21. Ma A, Koka R, Burkett P, (2006) Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 24: 657-679.
22. Ohteki T, Suzue K, Maki C, Ota T, Koyasu S, (2001) Critical role of IL-15-IL-15R for antigen-presenting cell functions in the innate immune response. Nat Immunol 2: 1138-1143.
23. Bouchard A, Ratthe C, Girard D, (2004) Interleukin-15 delays human neutrophil apoptosis by intracellular events and not via extracellular factors: role of Mcl-1 and decreased activity of caspase-3 and caspase-8. J Leukoc Biol 75: 893-900.
24. Alleva DG, Kaser SB, Monroy MA, Fenton MJ, Beller DI, (1997) IL-15 functions as a potent autocrine regulator of macrophage proinflammatory cytokine production: evidence for differential receptor subunit utilization associated with stimulation or inhibition. J Immunol 159: 2941-2951.
25. Li B, Sun R, Wei H, Gao B, Tian Z, (2006) Interleukin-15 prevents concanavalin A-induced liver injury in mice via NKT cell-dependent mechanism. Hepatology 43: 1211-1219.
26. Bulfone-Paus S, Ungureanu D, Pohl T, Lindner G, Paus R, et al. (1997) Interleukin-15 protects from lethal apoptosis in vivo. Nat Med 3: 1124-1128.
27. Ohteki T, Tada H, Ishida K, Sato T, Maki C, et al. (2006) Essential roles of DC-derived IL-15 as a mediator of inflammatory responses in vivo. J Exp Med 203: 2329-2338.
28. Kuwajima S, Sato T, Ishida K, Tada H, Tezuka H, et al. (2006) Interleukin 15-dependent crosstalk between conventional and plasmacytoid dendritic cells is essential for CpG-induced immune activation. Nat Immunol 7: 740-746.
29. Suzuki A, McCall S, Choi SS, Sicklick JK, Huang J, et al. (2006) Interleukin-15 increases hepatic regenerative activity. J Hepatol 45: 410-418.
30. Grabstein KH, Eisenman J, Shanebeck K, Rauch C, Srinivasan S, et al. (1994) Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 264: 965-968.
31. Misra I, Griffith OW, (1998) Expression and purification of human gamma-glutamylcysteine synthetase. Protein Expr Purif 13: 268-276.
32. Ferret PJ, Hammoud R, Tulliez M, Tran A, Trebeden H, et al. (2001) Detoxification of reactive oxygen species by a nonpeptidyl mimic of superoxide dismutase cures acetaminophen-induced acute liver failure in the mouse. Hepatology 33: 1173-1180.
33. Aleksunes LM, Manautou JE, (2007) Emerging role of Nrf2 in protecting against hepatic and gastrointestinal disease. Toxicol Pathol 35: 459-473.
34. Holt MP, Cheng L, Ju C, (2008) Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 84: 1410-1421.
35. Hinson JA, Bucci TJ, Irwin LK, Michael SL, Mayeux PR, (2002) Effect of inhibitors of nitric oxide synthase on acetaminophen-induced hepatotoxicity in mice. Nitric Oxide 6: 160-167.
36. Sumioka I, Matsura T, Kai M, Yamada K, (2004) Potential roles of hepatic heat shock protein 25 and 70i in protection of mice against acetaminophen-induced liver injury. Life Sci 74: 2551-2561.
37. Nussler AK, Di Silvio M, Liu ZZ, Geller DA, Freeswick P, et al. (1995) Further characterization and comparison of inducible nitric oxide synthase in mouse, rat, and human hepatocytes. Hepatology 21: 1552-1560.
38. Maley F, Tarentino AL, McGarrahan JF, Delgiacco R, (1968) The metabolism of d-galactosamine and N-acetyl-d-galactosamine in rat liver. Biochem J 107: 637-644.
39. Jaeschke H, Williams CD, Ramachandran A, Bajt ML, (2012) Acetaminophen hepatotoxicity and repair: the role of sterile inflammation and innate immunity. Liver Int 32: 8-20.
40. Sakamoto N, Sun Z, Brengman ML, Maemura K, Ozaki M, et al. (2003) Hepatic reticuloendothelial system dysfunction after ischemia-reperfusion: role of P-selectin-mediated neutrophil accumulation. Liver Transpl 9: 940-948.
41. Possamai LA, Antoniades CG, Anstee QM, Quaglia A, Vergani D, et al. (2010) Role of monocytes and macrophages in experimental and human acute liver failure. World J Gastroenterol 16: 1811-1819.
42. Harstad EB, Klaassen CD, (2002) Gadolinium chloride pretreatment prevents cadmium chloride-induced liver damage in both wild-type and MT-null mice. Toxicol Appl Pharmacol 180: 178-185.
43. Bourdi M, Davies JS, Pohl LR, (2011) Mispairing C57BL/6 substrains of genetically engineered mice and wild-type controls can lead to confounding results as it did in studies of JNK2 in acetaminophen and concanavalin A liver injury. Chem Res Toxicol 24: 794-796.
44. Hoetzel A, Vagts DA, Loop T, Humar M, Bauer M, et al. (2001) Effect of nitric oxide on shock-induced hepatic heme oxygenase-1 expression in the rat. Hepatology 33: 925-937.
45. Lehmann V, Freudenberg MA, Galanos C, (1987) Lethal toxicity of lipopolysaccharide and tumor necrosis factor in normal and D-galactosamine-treated mice. J Exp Med 165: 657-663.
46. Knight TR, Jaeschke H, (2002) Acetaminophen-induced inhibition of Fas receptor-mediated liver cell apoptosis: mitochondrial dysfunction versus glutathione depletion. Toxicol Appl Pharmacol 181: 133-141.
47. Le Moine O, Louis H, Demols A, Desalle F, Demoor F, et al. (2000) Cold liver ischemia-reperfusion injury critically depends on liver T cells and is improved by donor pretreatment with interleukin 10 in mice. Hepatology 31: 1266-1274.
48. Ruckert R, Brandt K, Ernst M, Marienfeld K, Csernok E, et al. (2009) Interleukin-15 stimulates macrophages to activate CD4+ T cells: a role in the pathogenesis of rheumatoid arthritis? Immunology 126: 63-73.
49. Nishimura H, Washizu J, Nakamura N, Enomoto A, Yoshikai Y, (1998) Translational efficiency is up-regulated by alternative exon in murine IL-15 mRNA. J Immunol 160: 936-942.
50. Meazza R, Verdiani S, Biassoni R, Coppolecchia M, Gaggero A, et al. (1996) Identification of a novel interleukin-15 (IL-15) transcript isoform generated by alternative splicing in human small cell lung cancer cell lines. Oncogene 12: 2187-2192.
51. Onu A, Pohl T, Krause H, Bulfone-Paus S, (1997) Regulation of IL-15 secretion via the leader peptide of two IL-15 isoforms. J Immunol 158: 255-262.
52. Tagaya Y, Kurys G, Thies TA, Losi JM, Azimi N, et al. (1997) Generation of secretable and nonsecretable interleukin 15 isoforms through alternate usage of signal peptides. Proc Natl Acad Sci U S A 94: 14444-14449.
53. Musikacharoen T, Oguma A, Yoshikai Y, Chiba N, Masuda A, et al. (2005) Interleukin-15 induces IL-12 receptor beta1 gene expression through PU.1 and IRF 3 by targeting chromatin remodeling. Blood 105: 711-720.
54. Mirghomizadeh F, Bullwinkel J, Orinska Z, Janssen O, Petersen A, et al. (2009) Transcriptional regulation of mouse mast cell protease-2 by interleukin-15. J Biol Chem 284: 32635-32641.
55. Yoshihara K, Yajima T, Kubo C, Yoshikai Y, (2006) Role of interleukin 15 in colitis induced by dextran sulphate sodium in mice. Gut 55: 334-341.
56. Nakamura R, Maeda N, Shibata K, Yamada H, Kase T, et al. (2010) Interleukin-15 is critical in the pathogenesis of influenza a virus-induced acute lung injury. J Virol 84: 5574-5582.
57. Shinozaki M, Hirahashi J, Lebedeva T, Liew FY, Salant DJ, et al. (2002) IL-15, a survival factor for kidney epithelial cells, counteracts apoptosis and inflammation during nephritis. J Clin Invest 109: 951-960.
58. Gomez-Nicola D, Spagnolo A, Guaza C, Nieto-Sampedro M, (2010) Aggravated experimental autoimmune encephalomyelitis in IL-15 knockout mice. Exp Neurol 222: 235-242.
59. Conti F, Frappier J, Dharancy S, Chereau C, Houssin D, et al. (2003) Interleukin-15 production during liver allograft rejection in humans. Transplantation 76: 210-216.
60. Kakumu S, Okumura A, Ishikawa T, Yano M, Enomoto A, et al. (1997) Serum levels of IL-10, IL-15 and soluble tumour necrosis factor-alpha (TNF-alpha) receptors in type C chronic liver disease. Clin Exp Immunol 109: 458-463.