Metformin ameliorates acetaminophen hepatotoxicity via Gadd45β-dependent regulation of JNK signaling in mice

Journal of Hepatology

Volumn 63, Issue 1, 2015, Pages 75-82

  Kim, Yong Hoon ^a   Hwang, Jung Hwan ^a   Kim, Kyoung Shim ^a   Noh, Jung Ran ^a   Choi, Dong Hee ^a   Kim, Don Kyu ^b   Tadi, Surendar ^c   Yim, Yong Hyeon ^c   Choi, Hueng Sik ^b   Lee, Chul Ho ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Chonnam National University   (South Korea)

^c Korea Research Institute of Standards and Science   (South Korea)

Author keywords

Acetaminophen; Gadd45b; Hepatotoxicity; JNK; Metformin

Indexed keywords

GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45 BETA; METFORMIN; PARACETAMOL; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; ANTIDIABETIC AGENT; DIFFERENTIATION ANTIGEN; GADD45B PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL DEATH; CELL ISOLATION; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; ENZYME REGULATION; KNOCKOUT MOUSE; LIVER CELL; LIVER CELL CULTURE; LIVER INJURY; LIVER TOXICITY; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; THERAPY EFFECT; WILD TYPE; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION;

ACETAMINOPHEN; ANIMALS; ANTIGENS, DIFFERENTIATION; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; HEPATOCYTES; HYPOGLYCEMIC AGENTS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; METFORMIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; SIGNAL TRANSDUCTION;

EID: 84931578159     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2015.02.008     Document Type: Article

References (48)

1. W. Bernal, G. Auzinger, A. Dhawan, and J. Wendon Acute liver failure Lancet 376 2010 190 201
2. D.G. Davidson, and W.N. Eastham Acute liver necrosis following overdose of paracetamol Br Med J 2 1966 497 499
3. W. Bernal Changing patterns of causation and the use of transplantation in the United Kingdom Semin Liver Dis 23 2003 227 237
4. P.J. Gow, R.M. Jones, J.L. Dobson, and P.W. Angus Etiology and outcome of fulminant hepatic failure managed at an Australian liver transplant unit J Gastroenterol Hepatol 19 2004 154 159
5. A.M. Larson, J. Polson, R.J. Fontana, T.J. Davern, E. Lalani, and L.S. Hynan Acetaminophen-induced acute liver failure: results of a United States multicenter, prospective study Hepatology 42 2005 1364 1372
6. G. Wei, A. Bergquist, U. Broome, S. Lindgren, S. Wallerstedt, and S. Almer Acute liver failure in Sweden: etiology and outcome J Intern Med 262 2007 393 401
7. S.D. Nelson Molecular mechanisms of the hepatotoxicity caused by acetaminophen Semin Liver Dis 10 1990 267 278
8. J.R. Mitchell, D.J. Jollow, W.Z. Potter, D.C. Davis, J.R. Gillette, and B.B. Brodie Acetaminophen-induced hepatic necrosis. I. Role of drug metabolism J Pharmacol Exp Ther 187 1973 185 194
9. D.J. Jollow, J.R. Mitchell, W.Z. Potter, D.C. Davis, J.R. Gillette, and B.B. Brodie Acetaminophen-induced hepatic necrosis. II. Role of covalent binding in vivo J Pharmacol Exp Ther 187 1973 195 202
10. J.R. Mitchell, D.J. Jollow, W.Z. Potter, J.R. Gillette, and B.B. Brodie Acetaminophen-induced hepatic necrosis. IV. Protective role of glutathione J Pharmacol Exp Ther 187 1973 211 217
11. E. Seki, D.A. Brenner, and M. Karin A liver full of JNK: signaling in regulation of cell function and disease pathogenesis, and clinical approaches Gastroenterology 143 2012 307 320
12. B.K. Gunawan, Z.X. Liu, D. Han, N. Hanawa, W.A. Gaarde, and N. Kaplowitz C-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity Gastroenterology 131 2006 165 178
13. H. Nakagawa, S. Maeda, Y. Hikiba, T. Ohmae, W. Shibata, and A. Yanai Deletion of apoptosis signal-regulating kinase 1 attenuates acetaminophen-induced liver injury by inhibiting c-Jun N-terminal kinase activation Gastroenterology 135 2008 1311 1321
14. J. Tian, and J. Locker Gadd45 in the liver: signal transduction and transcriptional mechanisms Adv Exp Med Biol 793 2013 69 80
15. D.A. Liebermann, and B. Hoffman Gadd45 in stress signaling J Mol Signal 3 2008 15
16. A.I. Su, L.G. Guidotti, J.P. Pezacki, F.V. Chisari, and P.G. Schultz Gene expression during the priming phase of liver regeneration after partial hepatectomy in mice Proc Natl Acad Sci U S A 99 2002 11181 11186
17. J. Locker, J. Tian, R. Carver, D. Concas, C. Cossu, and G.M. Ledda-Columbano A common set of immediate-early response genes in liver regeneration and hyperplasia Hepatology 38 2003 314 325
18. J. Tian, H. Huang, B. Hoffman, D.A. Liebermann, G.M. Ledda-Columbano, and A. Columbano Gadd45beta is an inducible coactivator of transcription that facilitates rapid liver growth in mice J Clin Invest 121 2011 4491 4502
19. E. De Smaele, F. Zazzeroni, S. Papa, D.U. Nguyen, R. Jin, and J. Jones Induction of gadd45beta by NF-kappaB downregulates pro-apoptotic JNK signalling Nature 414 2001 308 313
20. S. Papa, F. Zazzeroni, C. Bubici, S. Jayawardena, K. Alvarez, and S. Matsuda Gadd45 beta mediates the NF-kappa B suppression of JNK signalling by targeting MKK7/JNKK2 Nat Cell Biol 6 2004 146 153
21. S. Papa, F. Zazzeroni, Y.X. Fu, C. Bubici, K. Alvarez, and K. Dean Gadd45beta promotes hepatocyte survival during liver regeneration in mice by modulating JNK signaling J Clin Invest 118 2008 1911 1923
22. D.M. Nathan, J.B. Buse, M.B. Davidson, E. Ferrannini, R.R. Holman, and R. Sherwin Medical management of hyperglycaemia in type 2 diabetes mellitus: a consensus algorithm for the initiation and adjustment of therapy: a consensus statement from the American Diabetes Association and the European Association for the Study of Diabetes Diabetologia 52 2009 17 30
23. L. Harborne, R. Fleming, H. Lyall, J. Norman, and N. Sattar Descriptive review of the evidence for the use of metformin in polycystic ovary syndrome Lancet 361 2003 1894 1901
24. K. Landin, L. Tengborn, and U. Smith Treating insulin resistance in hypertension with metformin reduces both blood pressure and metabolic risk factors J Intern Med 229 1991 181 187
25. G. Marchesini, M. Brizi, G. Bianchi, S. Tomassetti, M. Zoli, and N. Melchionda Metformin in non-alcoholic steatohepatitis Lancet 358 2001 893 894
26. H.Z. Lin, S.Q. Yang, C. Chuckaree, F. Kuhajda, G. Ronnet, and A.M. Diehl Metformin reverses fatty liver disease in obese, leptin-deficient mice Nat Med 6 2000 998 1003
27. I. Bergheim, L. Guo, M.A. Davis, J.C. Lambert, J.I. Beier, and I. Duveau Metformin prevents alcohol-induced liver injury in the mouse: Critical role of plasminogen activator inhibitor-1 Gastroenterology 130 2006 2099 2112
28. M.K. Poon, P.Y. Chiu, D.H. Mak, and K.M. Ko Metformin protects against carbon tetrachloride hepatotoxicity in mice J Pharmacol Sci 93 2003 501 504
29. N.R. Hadi, F.G. Al-Amran, and A. Swadi Metformin ameliorates methotrexate-induced hepatotoxicity J Pharmacol Pharmacother 3 2012 248 253
30. M.R. McGill, M.R. Sharpe, C.D. Williams, M. Taha, S.C. Curry, and H. Jaeschke The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation J Clin Invest 122 2012 1574 1583
31. J.A. Hinson, S.L. Pike, N.R. Pumford, and P.R. Mayeux Nitrotyrosine-protein adducts in hepatic centrilobular areas following toxic doses of acetaminophen in mice Chem Res Toxicol 11 1998 604 607
32. G. Zhou, R. Myers, Y. Li, Y. Chen, X. Shen, and J. Fenyk-Melody Role of AMP-activated protein kinase in mechanism of metformin action J Clin Invest 108 2001 1167 1174
33. L.P. James, P.R. Mayeux, and J.A. Hinson Acetaminophen-induced hepatotoxicity Drug Metab Dispos 31 2003 1499 1506
34. B. Saberi, M.D. Ybanez, H.S. Johnson, W.A. Gaarde, D. Han, and N. Kaplowitz Protein kinase C (PKC) participates in acetaminophen hepatotoxicity through c-jun-N-terminal kinase (JNK)-dependent and -independent signaling pathways Hepatology 59 2014 1543 1554
35. M. Gupta, S.K. Gupta, B. Hoffman, and D.A. Liebermann Gadd45a and Gadd45b protect hematopoietic cells from UV-induced apoptosis via distinct signaling pathways, including p38 activation and JNK inhibition J Biol Chem 281 2006 17552 17558
36. N. Hanawa, M. Shinohara, B. Saberi, W.A. Gaarde, D. Han, and N. Kaplowitz Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury J Biol Chem 283 2008 13565 13577
37. S. Win, T.A. Than, D. Han, L.M. Petrovic, and N. Kaplowitz C-Jun N-terminal kinase (JNK)-dependent acute liver injury from acetaminophen or tumor necrosis factor (TNF) requires mitochondrial Sab protein expression in mice J Biol Chem 286 2011 35071 35078
38. J. Zhang, W. Huang, S.S. Chua, P. Wei, and D.D. Moore Modulation of acetaminophen-induced hepatotoxicity by the xenobiotic receptor CAR Science 298 2002 422 424
39. P. Wei, J. Zhang, M. Egan-Hafley, S. Liang, and D.D. Moore The nuclear receptor CAR mediates specific xenobiotic induction of drug metabolism Nature 407 2000 920 923
40. H. Yang, B. Garzel, S. Heyward, T. Moeller, P. Shapiro, and H. Wang Metformin represses drug-induced expression of CYP2B6 by modulating the constitutive androstane receptor signaling Mol Pharmacol 85 2014 249 260
41. A.H. Boulares, C. Giardina, M.S. Inan, E.A. Khairallah, and S.D. Cohen Acetaminophen inhibits NF-kappaB activation by interfering with the oxidant signal in murine Hepa 1-6 cells Toxicol Sci 55 2000 370 375
42. M.E. Blazka, D.R. Germolec, P. Simeonova, A. Bruccoleri, K.R. Pennypacker, and M.I. Luster Acetaminophen-induced hepatotoxicity is associated with early changes in NF-kB and NF-IL6 DNA binding activity J Inflamm 47 1995 138 150
43. H.G. Kim, T.T. Hien, E.H. Han, Y.P. Hwang, J.H. Choi, and K.W. Kang Metformin inhibits P-glycoprotein expression via the NF-kappaB pathway and CRE transcriptional activity through AMPK activation Br J Pharmacol 162 2011 1096 1108
44. Y. Hattori, K. Suzuki, S. Hattori, and K. Kasai Metformin inhibits cytokine-induced nuclear factor kappaB activation via AMP-activated protein kinase activation in vascular endothelial cells Hypertension 47 2006 1183 1188
45. J.H. Kim, A. Qu, J.K. Reddy, B. Gao, and F.J. Gonzalez Hepatic oxidative stress activates the Gadd45b gene by way of degradation of the transcriptional repressor STAT3 Hepatology 59 2014 695 704
46. D.E. Levy, and C.K. Lee What does Stat3 do? J Clin Invest 109 2002 1143 1148
47. C.C. Lin, H.H. Yeh, W.L. Huang, J.J. Yan, W.W. Lai, and W.P. Su Metformin enhances cisplatin cytotoxicity by suppressing signal transducer and activator of transcription-3 activity independently of the liver kinase B1-AMP-activated protein kinase pathway Am J Respir Cell Mol Biol 49 2013 241 250
48. Y. Feng, C. Ke, Q. Tang, H. Dong, X. Zheng, and W. Lin Metformin promotes autophagy and apoptosis in esophageal squamous cell carcinoma by downregulating Stat3 signaling Cell Death Dis 5 2014 e1088