Bee venom phospholipase A2 protects against acetaminophen-induced acute liver injury by modulating regulatory T cells and IL-10 in mice

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Kim, Hyunseong ^a   Keum, Dong June ^a   Kwak, Jung Won ^a   Chung, Hwan Suck ^a   Bae, Hyunsu ^a  

^a Kyung Hee University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BEE VENOM; CD4 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; NITRIC OXIDE; PARACETAMOL; PHOSPHOLIPASE A2; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE; IL10 PROTEIN, MOUSE; PROTECTIVE AGENT;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CD4+ CD25+ FOXP3 T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG EFFICACY; DRUG MEGADOSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HISTOPATHOLOGY; IMMUNOMODULATION; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; REGULATORY T LYMPHOCYTE; SINGLE DRUG DOSE; T CELL DEPLETION; TOXIC HEPATITIS; TREATMENT DURATION; ANIMAL; BLOOD; C57BL MOUSE; CHEMICAL AND DRUG INDUCED LIVER INJURY; CHEMISTRY; DRUG EFFECTS; METABOLISM;

APOIDEA; MUS;

ACETAMINOPHEN; ALANINE TRANSAMINASE; ANIMALS; ASPARTATE AMINOTRANSFERASES; BEE VENOMS; CHEMICAL AND DRUG INDUCED LIVER INJURY; CYTOKINES; INTERLEUKIN-10; MALE; MICE, INBRED C57BL; PHOSPHOLIPASES A2; PROTECTIVE AGENTS; T-LYMPHOCYTES, REGULATORY;

EID: 84916896670     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0114726     Document Type: Article

References (50)

1. Lee WM (2008) Acetaminophen-related acute liver failure in the United States. Hepatol Res 38 Suppl 1:: S3-S8.
2. Liu J, Liu Y, Madhu C, Klaassen CD (1993) Protective effects of oleanolic acid on acetaminopheninduced hepatotoxicity in mice. J Pharmacol Exp Ther 266: 1607-1613.
3. Patterson AD, Shah YM, Matsubara T, Krausz KW, Gonzalez FJ (2012) Peroxisome proliferatoractivated receptor alpha induction of uncoupling protein 2 protects against acetaminophen-induced liver toxicity. Hepatology 56: 281-290.
4. Wang AY, Lian LH, Jiang YZ, Wu YL, Nan JX (2010) Gentiana manshurica Kitagawa prevents acetaminophen-induced acute hepatic injury in mice via inhibiting JNK/ERK MAPK pathway. World J Gastroenterol 16: 384-391.
5. Yin H, Cheng L, Holt M, Hail N Jr, Maclaren R, et al. (2010) Lactoferrin protects against acetaminophen-induced liver injury in mice. Hepatology 51: 1007-1016.
6. Zhao X, Cong X, Zheng L, Xu L, Yin L, et al. (2012) Dioscin, a natural steroid saponin, shows remarkable protective effect against acetaminophen-induced liver damage in vitro and in vivo. Toxicol Lett 214: 69-80.
7. Sakaguchi S, Yamaguchi T, Nomura T, Ono M (2008) Regulatory T cells and immune tolerance. Cell 133: 775-787.
8. Sakaguchi S (2005) Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6: 345-352.
9. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, et al. (2006) Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212: 8-27.
10. Vignali DA, Collison LW, Workman CJ (2008) How regulatory T cells work. Nat Rev Immunol 8: 523- 532.
11. Kobayashi N, Hiraoka N, Yamagami W, Ojima H, Kanai Y, et al. (2007) FOXP3+ regulatory T cells affect the development and progression of hepatocarcinogenesis. Clin Cancer Res 13: 902-911.
12. Stross L, Gunther J, Gasteiger G, Asen T, Graf S, et al. (2012) Foxp3+ regulatory T cells protect the liver from immune damage and compromise virus control during acute experimental hepatitis B virus infection in mice. Hepatology 56: 873-883.
13. Wang WH, Jiang CL, Yan W, Zhang YH, Yang JT, et al. (2010) FOXP3 expression and clinical characteristics of hepatocellular carcinoma. World J Gastroenterol 16: 5502-5509.
14. Erhardt A, Biburger M, Papadopoulos T, Tiegs G (2007) IL-10, regulatory T cells, and Kupffer cells mediate tolerance in concanavalin A-induced liver injury in mice. Hepatology 45: 475-485.
15. Bradham CA, Plumpe J, Manns MP, Brenner DA, Trautwein C (1998) Mechanisms of hepatic toxicity. I. TNF-induced liver injury. Am J Physiol 275: G387-G392.
16. Burke JE, Dennis EA (2009) Phospholipase A2 structure/function, mechanism, and signaling. J Lipid Res 50 Suppl: S237-S242.
17. Monti MC, Casapullo A, Santomauro C, D'Auria MV, Riccio R, et al. (2006) The molecular mechanism of bee venom phospholipase A2 inactivation by bolinaquinone. Chembiochem 7: 971-980.
18. Zhao H, Kinnunen PK (2003) Modulation of the activity of secretory phospholipase A2 by antimicrobial peptides. Antimicrob Agents Chemother 47: 965-971.
19. Jeong JK, Moon MH, Bae BC, Lee YJ, Seol JW, et al. (2011) Bee venom phospholipase A2 prevents prion peptide induced-cell death in neuronal cells. Int J Mol Med 28: 867-873.
20. Lopez-Vales R, Ghasemlou N, Redensek A, Kerr BJ, Barbayianni E, et al. (2011) Phospholipase A2 superfamily members play divergent roles after spinal cord injury. FASEB J 25: 4240-4252.
21. 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.
22. Bleibel W, Kim S, D'Silva K, Lemmer ER (2007) Drug-induced liver injury: review article. Dig Dis Sci 52: 2463-2471.
23. Malhi H, Gores GJ (2008) Cellular and molecular mechanisms of liver injury. Gastroenterology 134: 1641-1654.
24. Park BK, Kitteringham NR, Maggs JL, Pirmohamed M, Williams DP (2005) The role of metabolic activation in drug-induced hepatotoxicity. Annual review of pharmacology and toxicology 45: 177-202.
25. Clemens MG (1999) Nitric oxide in liver injury. Hepatology 30: 1-5.
26. Dey A, Cederbaum AI (2006) Alcohol and oxidative liver injury. Hepatology 43: S63-S74.
27. Olaleye MT, Rocha BT (2008) Acetaminophen-induced liver damage in mice: effects of some medicinal plants on the oxidative defense system. Experimental and toxicologic pathology: official journal of the Gesellschaft fur Toxikologische Pathologie 59: 319-327.
28. Masubuchi Y, Suda C, Horie T (2005) Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice. Journal of hepatology 42: 110-116.
29. Bedda S, Laurent A, Conti F, Chereau C, Tran A, et al. (2003) Mangafodipir prevents liver injury induced by acetaminophen in the mouse. Journal of hepatology 39: 765-772.
30. Sennello JA, Fayad R, Morris AM, Eckel RH, Asilmaz E, et al. (2005) Regulation of T cell-mediated hepatic inflammation by adiponectin and leptin. Endocrinology 146: 2157-2164.
31. Speletas M, Argentou N, Germanidis G, Vasiliadis T, Mantzoukis K, et al. (2011) Foxp3 expression in liver correlates with the degree but not the cause of inflammation. Mediators Inflamm 2011: 827565.
32. Choi MS, Park S, Choi T, Lee G, Haam KK, et al. (2013) Bee venom ameliorates ovalbumin induced allergic asthma via modulating CD4+CD25+ regulatory T cells in mice. Cytokine 61: 256-265.
33. Chung ES, Kim H, Lee G, Park S, Bae H (2012) Neuro-protective effects of bee venom by suppression of neuroinflammatory responses in a mouse model of Parkinson's disease: role of regulatory T cells. Brain Behav Immun 26: 1322-1330.
34. Kim H, Lee G, Park S, Chung HS, Lee H, et al. (2013) Bee Venom Mitigates Cisplatin-Induced Nephrotoxicity by Regulating CD4(+)CD25(+)Foxp3(+) Regulatory T Cells in Mice. Evid Based Complement Alternat Med 2013: 879845.
35. Schaloske RH, Dennis EA (2006) The phospholipase A2 superfamily and its group numbering system. Biochim Biophys Acta 1761: 1246-1259.
36. Darwish SF, El-Bakly WM, Arafa HM, El-Demerdash E (2013) Targeting TNF-alpha and NF-kappaB activation by bee venom: role in suppressing adjuvant induced arthritis and methotrexate hepatotoxicity in rats. PLoS One 8: e79284.
37. Dudler T, Machado DC, Kolbe L, Annand RR, Rhodes N, et al. (1995) A link between catalytic activity, IgE-independent mast cell activation, and allergenicity of bee venom phospholipase A2. J Immunol 155: 2605-2613.
38. Palm NW, Rosenstein RK, Yu S, Schenten DD, Florsheim E, et al. (2013) Bee venom phospholipase A2 induces a primary type 2 response that is dependent on the receptor ST2 and confers protective immunity. Immunity 39: 976-985.
39. Laskin DL, Gardner CR, Price VF, Jollow DJ (1995) Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology 21: 1045-1050.
40. Waters E, Wang JH, Redmond HP, Wu QD, Kay E, et al. (2001) Role of taurine in preventing acetaminophen-induced hepatic injury in the rat. Am J Physiol Gastrointest Liver Physiol 280: G1274- G1279.
41. Whyte IM, Francis B, Dawson AH (2007) Safety and efficacy of intravenous N-acetylcysteine for acetaminophen overdose: Analysis of the Hunter Area Toxicology Service (HATS) database. Curr Med Res Opin 23: 2359-2368.
42. Moncada S, Erusalimsky JD (2002) Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 3: 214-220.
43. Gardner CR, Heck DE, Yang CS, Thomas PE, Zhang XJ, et al. (1998) Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology 27: 748-754.
44. Ito Y, Abril ER, Bethea NW, McCuskey RS (2004) Role of nitric oxide in hepatic microvascular injury elicited by acetaminophen in mice. Am J Physiol Gastrointest Liver Physiol 286: G60-G67.
45. Kuo PC, Schroeder RA, Loscalzo J (1997) Nitric oxide and acetaminophen-mediated oxidative injury: modulation of interleukin-1-induced nitric oxide synthesis in cultured rat hepatocytes. J Pharmacol Exp Ther 282: 1072-1083.
46. Crispe IN (2003) Hepatic T cells and liver tolerance. Nat Rev Immunol 3: 51-62.
47. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, et al. (2008) Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28: 546-558.
48. Nguyen K, D'Mello C, Le T, Urbanski S, Swain MG (2012) Regulatory T cells suppress sickness behaviour development without altering liver injury in cholestatic mice. Journal of hepatology 56: 626- 631.
49. Louis H, Le Moine O, Peny MO, Gulbis B, Nisol F, et al. (1997) Hepatoprotective role of interleukin 10 in galactosamine/lipopolysaccharide mouse liver injury. Gastroenterology 112: 935-942.
50. James LP, Mayeux PR, Hinson JA (2003) Acetaminophen-induced hepatotoxicity. Drug Metab Dispos 31: 1499-1506.