Protection against phalloidin-induced liver injury by oleanolic acid involves Nrf2 activation and suppression of Oatp1b2

Toxicology Letters

Volumn 232, Issue 1, 2015, Pages 326-332

  Lu, Yuan Fu ^a,b   Liu, Jie ^a,b   Wu, Kai Connie ^a   Klaassen, Curtis D ^a  

^a UNIVERSITY OF KANSAS MEDICAL CENTER   (United States)

^b ZUNYI MEDICAL UNIVERSITY   (China)

Author keywords

Inflammation; Keap1 HKO mice; Nrf2 null mice; Oatp1b2; Oleanolic acid; Phalloidin hepatotoxicity

Indexed keywords

ALANINE AMINOTRANSFERASE; CXCL3 CHEMOKINE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; KERATINOCYTE DERIVED CHEMOKINE; MALONALDEHYDE; MESSENGER RNA; OLEANOLIC ACID; PHALLOIDIN; PROTEIN CHOP10; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE) 1; SOLUTE CARRIER ORGANIC ANION TRANSPORTER 1B2; STRESS ACTIVATED PROTEIN KINASE; THIOBARBITURIC ACID; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; AUTACOID; KEAP1 PROTEIN, MOUSE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; NFE2L2 PROTEIN, MOUSE; ORGANIC ANION TRANSPORTER; SLC21A10 PROTEIN, RAT;

ACUTE PHASE RESPONSE; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DRUG MECHANISM; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVITY; GENE EXPRESSION; GENETIC VARIABILITY; GENOTYPE; HISTOPATHOLOGY; LIPID LIVER LEVEL; LIPID PEROXIDATION; LIVER HEMORRHAGE; LIVER INJURY; LIVER NECROSIS; LIVER PROTECTION; LIVER TOXICITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; WILD TYPE; ANIMAL; C57BL MOUSE; CELL PROTECTION; CHEMICAL AND DRUG INDUCED LIVER INJURY; DEFICIENCY; DISEASE MODEL; DRUG EFFECTS; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; PATHOLOGY;

MUS;

ANIMALS; CHEMICAL AND DRUG INDUCED LIVER INJURY; CYTOPROTECTION; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; INFLAMMATION MEDIATORS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; LIPID PEROXIDATION; LIVER; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; OLEANOLIC ACID; ORGANIC ANION TRANSPORTERS, SODIUM-INDEPENDENT; PHALLOIDINE; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84911916049     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.09.027     Document Type: Article

References (32)

1. Barriault C., Audet M., Yousef I.M., Tuchweber B. Protection by indomethacin against the lethality and hepatotoxicity of phalloidin in mice. Toxicol. Lett. 1994, 71:257-269.
2. Barriault C., Audet M., Yousef I.M., Tuchweber B. Effect of agents which modify reticuloendothelial system function on acute phalloidin-induced lethality and hepatotoxicity in mice. Toxicol. Appl. Pharmacol. 1995, 131:206-215.
3. Barriault C., Petit J.L., Gascon-Barré M., Huet P.M., Yousef I.M., Tuchweber B. Effect of phalloidin on cholestasis, hemodynamics, and microcirculation in isolated perfused rat liver. Hepatology 1996, 23:294-302.
4. Bouchard G., Yousef I.M., Barriault C., Tuchweber B. Role of glutathione and oxidative stress in phalloidin-induced cholestasis. J. Hepatol. 2000, 32:550-560.
5. Chan K., Lu R., Chang J.C., Kan Y.W. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:13943-13948.
6. Dorman R.B., Gujral J.S., Bajt M.L., Farhood A., Jaeschke H. Generation and functional significance of CXC chemokines for neutrophil-induced liver injury during endotoxemia. Am. J. Physiol. Gastrointest. Liver Physiol. 2005, 288:G880-G886.
7. Frimmer M. What we have learned from phalloidin. Toxicol. Lett. 1987, 35:169-182.
8. Ghosh A.S., Wang B., Pozniak C.D., Chen M., Watts R.J., Lewcock J.W. DLK induces developmental neuronal degeneration via selective regulation of proapoptotic JNK activity. J. Cell Biol. 2011, 194:751-764.
9. Guinda A., Rada M., Delgado T., Gutie'rrez-Ada'nez P., Castellano J.M. Pentacyclic from olive fruit and leaf. J. Agric. Food Chem. 2010, 58:9685-9691.
10. Herraez E., Macias R.I., Vazquez-Tato J., Hierro C., Monte M.J., Marin J.J. Protective effect of bile acid derivatives in phalloidin-induced rat liver toxicity. Toxicol. Appl. Pharmacol. 2009, 239:21-28.
11. Ho H.K., White C.C., Fernandez C., Fausto N., Kavanagh T.J., Nelson S.D., Bruschi S.A. Nrf2 activation involves an oxidative-stress independent pathway in tetrafluoroethylcysteine-induced cytotoxicity. Toxicol. Sci. 2005, 86:354-364.
12. Kang K.W., Lee S.J., Park J.W., Kim S.G. Phosphatidylinositol 3-kinase regulates nuclear translocation of NF-E2-related factor 2 through actin rearrangement in response to oxidative stress. Mol. Pharmacol. 2002, 62:1001-1010.
13. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
14. Klaassen C.D., Liu J., Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 1999, 39:267-294.
15. Klaassen C.D., Reisman S.A. Nrf2 the rescue: effects of the antioxidative/electrophilic response on the liver. Toxicol. Appl. Pharmacol. 2010, 244:57-65.
16. Laszczyk M.N. Pentacyclic triterpenes of the lupane, oleanane and ursane group as tools in cancer therapy. Planta Med. 2009, 75:1549-1560.
17. Liu J., Liu Y., Klaassen C.D. Protective effect of oleanolic acid against chemical-induced acute necrotic liver injury in mice. Zhongguo Yao Li Xue Bao 1995, 16:97-102.
18. Liu J., Wu K.C., Lu Y.F., Ekuase E., Klaassen C.D. NRF2 protection against liver injury produced by various hepatotoxicants. Oxid. Med. Cell Longev. 2013, 2013:305861.
19. Liu J., Lu Y.F., Zhang Y., Wu K.C., Fan F., Klaassen C.D. Oleanolic acid alters bile acid metabolism and produces cholestatic liver injury in mice. Toxicol. Appl. Pharmacol. 2013, 272:816-824.
20. Lu H., Choudhuri S., Ogura K., Csanaky I.L., Lei X., Cheng X., Song P.Z., Klaassen C.D. Characterization of organic anion transporting polypeptide 1b2-null mice: essential role in hepatic uptake/toxicity of phalloidin and microcystin-LR. Toxicol. Sci. 2008, 103:35-45.
21. Mengs U., Trost W. Acute phalloidin poisoning in dogs. Arch. Toxicol. 1981, 48:61-67.
22. Meier-Abt F., Faulstich H., Hagenbuch B. Identification of phalloidin uptake systems of rat and human liver. Biochim. Biophys. Acta 2004, 1664:64-69.
23. Nagy G., Kardon T., Wunderlich L., Szarka A., Kiss A., Schaff Z., Bánhegyi G., Mandl J. Acetaminophen induces ER dependent signaling in mouse liver. Arch. Biochem. Biophys. 2006, 459:273-279.
24. Okada K., Shoda J., Taguchi K., Maher J.M., Ishizaki K., Inoue Y., Ohtsuki M., Goto N., Sugimoto H., Utsunomiya H., et al. Nrf2 counteracts cholestatic liver injury via stimulation of hepatic defense systems. Biochem. Biophys. Res. Commun. 2009, 389:431-436.
25. Pearson G., Robinson F., Beers Gibson T., Xu B.E., Karandikar M., Berman K., Cobb M.H. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr. Rev. 2001, 22:153-183.
26. Pollier J., Goossens A. Oleanolic acid. Phytochemistry 2012, 77:10-15.
27. Reisman S.A., Aleksunes L.M., Klaassen C.D. Oleanolic acid activates Nrf2 and protects from acetaminophen hepatotoxicity via Nrf2-dependent and Nrf2-independent processes. Biochem. Pharmacol. 2009, 77:1273-1282.
28. Sass G., Barikbin R., Tiegs G. The multiple functions of heme oxygenase-1 in the liver. Z. Gastroenterol. 2012, 50:34-40.
29. Wu K.C., Cui J.Y., Klaassen C.D. Beneficial role of Nrf2 in regulating NADPH generation and consumption. Toxicol. Sci. 2011, 123:590-600.
30. Wu K.C., Liu J.J., Klaassen C.D. Nrf2 activation prevents cadmium-induced acute liver injury. Toxicol. Appl. Pharmacol. 2012, 263:14-20.
31. Wu K.C., Cui J.Y., Klaassen C.D. Effect of graded Nrf2 activation on phase-I and -II drug metabolizing enzymes and transporters in mouse liver. PLoS One 2012, 7:e39006.
32. Wu K.C., Liu J., Klaassen C.D. Role of Nrf2 in preventing ethanol-induced oxidative stress and lipid accumulation. Toxicol. Appl. Pharmacol. 2012, 262:321-329.