Ferulic acid attenuates ischemia/reperfusion-induced hepatocyte apoptosis via inhibition of JNK activation

European Journal of Pharmaceutical Sciences

Volumn 45, Issue 5, 2012, Pages 708-715

  Kim, Hyo Yeon ^a   Lee, Sun Mee ^a  

^a Sungkyunkwan University   (South Korea)

Author keywords

Apoptosis; Ferulic acid; Ischemia reperfusion; Liver; Oxidative stress

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BCL 2 LIKE PROTEIN 11; CASPASE 3; CASPASE 8; CYTOCHROME C; FERULIC ACID; GLUTATHIONE; GLUTATHIONE DISULFIDE; MITOGEN ACTIVATED PROTEIN KINASE 9; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BID; STRESS ACTIVATED PROTEIN KINASE 1; TRUNCATED BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED DEATH DOMAIN PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; ATTENUATION; CELL PROTECTION; CONTROLLED STUDY; CYTOSOL; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; IN VIVO STUDY; LIPID PEROXIDATION; LIVER CELL; LIVER ISCHEMIA; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; REPERFUSION INJURY; UPREGULATION;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BCL-2-ASSOCIATED X PROTEIN; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; CASPASE 3; CASPASE 8; COUMARIC ACIDS; CYTOCHROMES C; CYTOSOL; GLUTATHIONE; HEPATOCYTES; LIPID PEROXIDATION; LIVER; MALE; MAP KINASE KINASE 4; MEMBRANE PROTEINS; MICE; MICE, INBRED ICR; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TNF RECEPTOR-ASSOCIATED DEATH DOMAIN PROTEIN; TNF RECEPTOR-ASSOCIATED FACTOR 2; TRANSAMINASES; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 84862785799     PISSN: 09280987     EISSN: 18790720     Source Type: Journal    
DOI: 10.1016/j.ejps.2012.01.010     Document Type: Article

References (47)

1. J.M. Antony, G. van Marle, W. Opii, D.A. Butterfield, F. Mallet, V.W. Yong, J.L. Wallace, R.M. Deacon, K. Warren, and C. Power Human endogenous retrovirus glycoprotein-mediated induction of redox reactants causes oligodendrocyte death and demyelination Nat. Neurosci. 7 2004 1088 1095 (Pubitemid 41184449)
2. S. Balakrishnan, S. Manoharan, L.M. Alias, and M.R. Nirmal Effect of curcumin and ferulic acid on modulation of expression pattern of p53 and bcl-2 proteins in 7,12-dimethylbenz[a]anthracene-induced hamster buccal pouch carcinogenesis Indian J. Biochem. Biophys. 47 2010 7 12
3. J.A. Buege, and S.D. Aust Microsomal lipid peroxidation Methods Enzymol. 52 1978 302 310
4. V. Calabrese, E. Guagliano, M. Sapienza, M. Panebianco, S. Calafato, E. Puleo, G. Pennisi, C. Mancuso, D.A. Butterfield, and A.G. Stella Redox regulation of cellular stress response in aging and neurodegenerative disorders: role of vitagenes Neurochem. Res. 32 2007 757 773 (Pubitemid 46481305)
5. C.A. Camargo Jr., J.F. Madden, W. Gao, R.S. Selvan, and P.A. Clavien Interleukin-6 protects liver against warm ischemia/reperfusion injury and promotes hepatocyte proliferation in the rodent Hepatology 26 1997 1513 1520 (Pubitemid 27520017)
6. L. Chang, H. Kamata, G. Solinas, J.L. Luo, S. Maeda, K. Venuprasad, Y.C. Liu, and M. Karin The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover Cell 124 2006 601 613 (Pubitemid 43199444)
7. H.M. Chao, Y.H. Chen, J.H. Liu, S.M. Lee, F.L. Lee, Y. Chang, P.H. Yeh, W.H. Pan, C.W. Chi, T.Y. Liu, W.Y. Lui, L.T. Ho, C.D. Kuo, D.E. Lin, C.C. Chan, D.M. Yang, A.M. Lin, and F.P. Chao Iron-generated hydroxyl radicals kill retinal cells in vivo: effect of ferulic acid Hum. Exp. Toxicol. 27 2008 327 339
8. H.P. Chen, Z.P. Liao, Q.R. Huang, and M. He Sodium ferulate attenuates anoxia/reoxygenation-induced calcium overload in neonatal rat cardiomyocytes by NO/cGMP/PKG pathway Eur. J. Pharmacol. 603 2009 86 92
9. C.Y. Cheng, S.Y. Su, N.Y. Tang, T.Y. Ho, S.Y. Chiang, and C.L. Hsieh Ferulic acid provides neuroprotection against oxidative stress-related apoptosis after cerebral ischemia/reperfusion injury by inhibiting ICAM-1 mRNA expression in rats Brain Res. 1209 2008 136 150
10. R. Cursio, J. Gugenheim, J.E. Ricci, D. Crenesse, P. Rostagno, L. Maulon, M.C. Saint-Paul, B. Ferrua, and A.P. Auberger A caspase inhibitor fully protects rats against lethal normothermic liver ischemia by inhibition of liver apoptosis FASEB J. 13 1999 253 261 (Pubitemid 29072402)
11. N. Donovan, E.B. Becker, Y. Konishi, and A. Bonni JNK phosphorylation and activation of BAD couples the stress-activated signaling pathway to the cell death machinery J. Biol. Chem. 277 2002 40944 40949 (Pubitemid 35215682)
12. A.A. El-Bahy, L.A. Kassem, O.A. Heikal, and L.G. Mahran Antiapoptotic effect of DDB against hepatic ischemia-reperfusion injury J. Toxicol. Sci. 36 2011 145 154
13. M.L. Entman, and C.W. Smith Postreperfusion inflammation: a model for reaction to injury in cardiovascular disease Cardiovasc. Res. 28 1994 1301 1311 (Pubitemid 24300430)
14. H.A. Eum, Y.N. Cha, and S.M. Lee Necrosis and apoptosis: sequence of liver damage following reperfusion after 60 min ischemia in rats Biochem. Biophys. Res. Commun. 358 2007 500 505
15. A.R. Fetoni, C. Mancuso, S.L. Eramo, M. Ralli, R. Piacentini, E. Barone, G. Paludetti, and D. Troiani In vivo protective effect of ferulic acid against noise-induced hearing loss in the guinea-pig Neuroscience 169 2010 1575 1588
16. P. Georgiev, F. Dahm, R. Graf, and P.A. Clavien Blocking the path to death: anti-apoptotic molecules in ischemia/reperfusion injury of the liver Curr. Pharm. Des. 12 2006 2911 2921 (Pubitemid 44184625)
17. 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 (Pubitemid 44015744)
18. H. Jaeschke Mechanisms of Liver Injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions Am. J. Physiol. Gastrointest. Liver Physiol. 290 2006 G1083 G1088 (Pubitemid 43788288)
19. Y. Jin, E.Z. Yan, Y. Fan, X.L. Guo, Y.J. Zhao, Z.H. Zong, and Z. Liu Neuroprotection by sodium ferulate against glutamate-induced apoptosis is mediated by ERK and PI3 kinase pathways Acta Pharmacol. Sin. 28 2007 1881 1890 (Pubitemid 350198331)
20. H.Y. Kim, J. Park, K.H. Lee, D.U. Lee, J.H. Kwak, Y.S. Kim, and S.M. Lee Ferulic acid protects against carbon tetrachloride-induced liver injury in mice Toxicology 282 2011 104 111
21. J.S. Kim, X.M. Cai, L.K. Smith, Y.G. Jin, A. Uchiyama, and J.J. Lemasters Mitochondrial permeability transition-mediated apoptosis after ischemia/reperfusion of cultured mouse hepatocytes: Role of X-linked inhibitor of apoptosis protein (XIAP) Gastroenterology 128 2005 A708
22. Y. Kodama, K. Taura, K. Miura, B. Schnabl, Y. Osawa, and D.A. Brenner Antiapoptotic effect of c-Jun N-terminal Kinase-1 through Mcl-1 stabilization in TNF-induced hepatocyte apoptosis Gastroenterology 136 2009 1423 1434
23. V. Kohli, J.F. Madden, R.C. Bentley, and P.A. Clavien Calpain mediates ischemic injury of the liver through modulation of apoptosis and necrosis Gastroenterology 116 1999 168 178 (Pubitemid 29013506)
24. S. Li, Y. Zhao, X. He, T.H. Kim, D.K. Kuharsky, H. Rabinowich, J. Chen, C. Du, and X.M. Yin Relief of extrinsic pathway inhibition by the Bid-dependent mitochondrial release of Smac in Fas-mediated hepatocyte apoptosis J. Biol. Chem. 277 2002 26912 26920 (Pubitemid 34951700)
25. C. Liedtke, and C. Trautwein The role of JNK2 in toxic liver injury J. Hepatol. 45 2006 762 764 (Pubitemid 44466671)
26. D.L. Liu, B. Jeppsson, C.H. Hakansson, and R. Odselius Multiple-system organ damage resulting from prolonged hepatic inflow interruption Arch. Surg. 131 1996 442 447 (Pubitemid 26113437)
27. Z.C. Ma, Q. Hong, Y.G. Wang, H.L. Tan, C.R. Xiao, Q.D. Liang, D.G. Wang, and Y. Gao Ferulic acid protects lymphocytes from radiation-predisposed oxidative stress through extracellular regulated kinase Int. J. Radiat. Biol. 87 2011 130 140
28. D.K. Maurya, V.P. Salvi, and C.K. Nair Radiation protection of DNA by ferulic acid under in vitro and in vivo conditions Mol. Cell. Biochem. 280 2005 209 217 (Pubitemid 41829820)
29. K.P. Mollen, C.A. McCloskey, H. Tanaka, J.M. Prince, R.M. Levy, B.S. Zuckerbraun, and T.R. Billiar Hypoxia activates c-Jun N-terminal kinase via Rac1-dependent reactive oxygen species production in hepatocytes Shock 28 2007 270 277 (Pubitemid 47282017)
30. H.M. Ni, X. Chen, W.X. Ding, M. Schuchmann, and X.M. Yin Differential roles of JNK in ConA/GalN and ConA-induced liver injury in mice Am. J. Pathol. 173 2008 962 972
31. I. Onishi, T. Tani, T. Hashimoto, K. Shimizu, M. Yagi, K. Yamamoto, and K. Yoshioka Activation of c-Jun N-terminal kinase during ischemia and reperfusion in mouse liver FEBS Lett. 420 1997 201 204 (Pubitemid 28037241)
32. M. Parola, G. Robino, F. Marra, M. Pinzani, G. Bellomo, G. Leonarduzzi, P. Chiarugi, S. Camandola, G. Poli, G. Waeg, P. Gentilini, and M.U. Dianzani HNE interacts directly with JNK isoforms in human hepatic stellate cells J. Clin. Invest. 102 1998 1942 1950 (Pubitemid 29001840)
33. P. Picone, M.L. Bondi, G. Montana, A. Bruno, G. Pitarresi, G. Giammona, and M. Di Carlo Ferulic acid inhibits oxidative stress and cell death induced by Ab oligomers: improved delivery by solid lipid nanoparticles Free Radic. Res. 43 2009 1133 1145
34. H.A. Rudiger, and P.A. Clavien Tumor necrosis factor alpha, but not Fas, mediates hepatocellular apoptosis in the murine ischemic liver Gastroenterology 122 2002 202 210 (Pubitemid 34049208)
35. M. Srinivasan, A.R. Sudheer, and V.P. Menon Ferulic Acid: therapeutic potential through its antioxidant property J. Clin. Biochem. Nutr. 40 2007 92 100 (Pubitemid 46623810)
36. N. Teoh, I. Leclercq, A.D. Pena, and G. Farrell Low-dose TNF-alpha protects against hepatic ischemia-reperfusion injury in mice. implications for preconditioning Hepatology 37 2003 118 128 (Pubitemid 36042152)
37. N.C. Teoh, and G.C. Farrell Hepatic ischemia reperfusion injury: pathogenic mechanisms and basis for hepatoprotection J. Gastroenterol. Hepatol. 18 2003 891 902 (Pubitemid 37056167)
38. T.P. Theruvath, M.C. Snoddy, Z. Zhong, and J.J. Lemasters Mitochondrial permeability transition in liver ischemia and reperfusion: role of c-Jun N-terminal kinase 2 Transplantation 85 2008 1500 1504
39. F. Tietze Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues Anal. Biochem. 27 1969 502 522
40. K. Tobiume, A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, and H. Ichijo ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis EMBO Rep. 2 2001 222 228 (Pubitemid 32273301)
41. T. Uchiyama, H. Otani, T. Okada, H. Ninomiya, M. Kido, H. Imamura, S. Nogi, and Y. Kobayashi Nitric oxide induces caspase-dependent apoptosis and necrosis in neonatal rat cardiomyocytes J. Mol. Cell. Cardiol. 34 2002 1049 1061 (Pubitemid 35316152)
42. T. Uehara, B. Bennett, S.T. Sakata, Y. Satoh, G.K. Bilter, J.K. Westwick, and D.A. Brenner JNK mediates hepatic ischemia reperfusion injury J. Hepatol. 42 2005 850 859 (Pubitemid 40693202)
43. M. Vairetti, P. Griffini, G. Pietrocola, P. Richelmi, and I. Freitas Cold-induced apoptosis in isolated rat hepatocytes: protective role of glutathione Free Radic. Biol. Med. 31 2001 954 961 (Pubitemid 32939391)
44. Y. Wang, R. Singh, J.H. Lefkowitch, R.M. Rigoli, and M.J. Czaja Tumor necrosis factor-induced toxic liver injury results from JNK2-dependent activation of caspase-8 and the mitochondrial death pathway J. Biol. Chem. 281 2006 15258 15267 (Pubitemid 43855115)
45. M.C. Wei, W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer Proapoptotic BAX and: BAK a requisite gateway to mitochondrial dysfunction and death Science 292 2001 727 730 (Pubitemid 32385543)
46. C.R. Weston, and R.J. Davis The JNK signal transduction pathway Curr. Opin. Cell Biol. 19 2007 142 149 (Pubitemid 46386399)
47. X.M. Yin Bid, a critical mediator for apoptosis induced by the activation of Fas/TNF-R1 death receptors in hepatocytes J. Mol. Med. 78 2000 203 211