Peroxisome proliferator-activated receptor alpha induction of uncoupling protein 2 protects against acetaminophen-induced liver toxicity

Hepatology

Volumn 56, Issue 1, 2012, Pages 281-290

  Patterson, Andrew D ^a,b   Shah, Yatrik M ^a,c   Matsubara, Tsutomu ^a   Krausz, Kristopher W ^a   Gonzalez, Frank J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FENOFIBRATE; GLUTATHIONE; HYDROGEN PEROXIDE; PARACETAMOL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PIRINIXIC ACID; PROTEIN C FOS; PROTEIN C JUN; REACTIVE OXYGEN METABOLITE; STRESS ACTIVATED PROTEIN KINASE; UNCOUPLING PROTEIN 2;

ARTICLE; DRUG INDUCED DISEASE; ENZYME PHOSPHORYLATION; GENE OVEREXPRESSION; LIVER PROTECTION; LIVER TOXICITY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN FUNCTION;

ACETAMINOPHEN; ANALYSIS OF VARIANCE; ANIMALS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG-INDUCED LIVER INJURY; IMMUNOHISTOCHEMISTRY; INJECTIONS, INTRAPERITONEAL; ION CHANNELS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MITOCHONDRIAL PROTEINS; OXIDATIVE STRESS; PPAR ALPHA; PYRIMIDINES; RANDOM ALLOCATION; REFERENCE VALUES;

EID: 84863522631     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25645     Document Type: Article

References (33)

1. Peters JM, Cattley RC, Gonzalez FJ. Role of PPAR alpha in the mechanism of action of the nongenotoxic carcinogen and peroxisome proliferator Wy-14, 643. Carcinogenesis 1997; 18: 2029-2033.
2. Shah YM, Morimura K, Yang Q, Tanabe T, Takagi M, Gonzalez FJ. Peroxisome proliferator-activated receptor alpha regulates a microRNA-mediated signaling cascade responsible for hepatocellular proliferation. Mol Cell Biol 2007; 27: 4238-4247.
3. Gonzalez FJ, Shah YM. PPARalpha: mechanism of species differences and hepatocarcinogenesis of peroxisome proliferators. Toxicology 2008; 246: 2-8.
4. Aoyama T, Peters JM, Iritani N, Nakajima T, Furihata K, Hashimoto T, et al. Altered constitutive expression of fatty acid-metabolizing enzymes in mice lacking the peroxisome proliferator-activated receptor alpha (PPARalpha). J Biol Chem 1998; 273: 5678-5684.
5. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 1999; 103: 1489-1498.
6. Mandard S, Muller M, Kersten S. Peroxisome proliferator-activated receptor alpha target genes. Cell Mol Life Sci 2004; 61: 393-416.
7. Nakatani T, Tsuboyama-Kasaoka N, Takahashi M, Miura S, Ezaki O. Mechanism for peroxisome proliferator-activated receptor-alpha activator-induced up-regulation of UCP2 mRNA in rodent hepatocytes. J Biol Chem 2002; 277: 9562-9569.
8. Mailloux RJ, Seifert EL, Bouillaud F, Aguer C, Collins S, Harper ME. Glutathionylation Acts as a Control Switch for Uncoupling Proteins UCP2 and UCP3. J Biol Chem 2011; 286: 21865-21875.
9. D'Arcy PF. Paracetamol. Adverse Drug React Toxicol Rev 1997; 16: 9-14.
10. Mazer M, Perrone J. Acetaminophen-induced nephrotoxicity: pathophysiology, clinical manifestations, and management. J Med Toxicol 2008; 4: 2-6.
11. Gonzalez FJ. The 2006 Bernard B. Brodie Award Lecture. Cyp2e1. Drug Metab Dispos 2007; 35: 1-8.
12. Manautou JE, Hoivik DJ, Tveit A, Hart SG, Khairallah EA, Cohen SD. Clofibrate pretreatment diminishes acetaminophen's selective covalent binding and hepatotoxicity. Toxicol Appl Pharmacol 1994; 129: 252-263.
13. Manautou JE, Tveit A, Hoivik DJ, Khairallah EA, Cohen SD. Protection by clofibrate against acetaminophen hepatotoxicity in male CD-1 mice is associated with an early increase in biliary concentration of acetaminophen-glutathione adducts. Toxicol Appl Pharmacol 1996; 140: 30-38.
14. Chen C, Hennig GE, Whiteley HE, Corton JC, Manautou JE. Peroxisome proliferator-activated receptor alpha-null mice lack resistance to acetaminophen hepatotoxicity following clofibrate exposure. Toxicol Sci 2000; 57: 338-344.
15. Chen C, Krausz KW, Shah YM, Idle JR, Gonzalez FJ. Serum metabolomics reveals irreversible inhibition of fatty acid beta-oxidation through the suppression of PPARalpha activation as a contributing mechanism of acetaminophen-induced hepatotoxicity. Chem Res Toxicol 2009; 22: 699-707.
16. Lee SS, Pineau T, Drago J, Lee EJ, Owens JW, Kroetz DL, et al. Targeted disruption of the alpha isoform of the peroxisome proliferator-activated receptor gene in mice results in abolishment of the pleiotropic effects of peroxisome proliferators. Mol Cell Biol 1995; 15: 3012-3022.
17. Yang Q, Nagano T, Shah Y, Cheung C, Ito S, Gonzalez FJ. The PPAR alpha-humanized mouse: a model to investigate species differences in liver toxicity mediated by PPAR alpha. Toxicol Sci 2008; 101: 132-139.
18. Hong Y, Fink BD, Dillon JS, Sivitz WI. Effects of adenoviral overexpression of uncoupling protein-2 and -3 on mitochondrial respiration in insulinoma cells. Endocrinology 2001; 142: 249-256.
19. Chen C, Krausz KW, Idle JR, Gonzalez FJ. Identification of novel toxicity-associated metabolites by metabolomics and mass isotopomer analysis of acetaminophen metabolism in wild-type and Cyp2e1-null mice. J Biol Chem 2008; 283: 4543-4559.
20. Henderson NC, Pollock KJ, Frew J, Mackinnon AC, Flavell RA, Davis RJ, et al. Critical role of c-jun (NH2) terminal kinase in paracetamol-induced acute liver failure. Gut 2007; 56: 982-990.
21. Hanawa N, Shinohara M, Saberi B, Gaarde WA, Han D, Kaplowitz N. Role of JNK translocation to mitochondria leading to inhibition of mitochondria bioenergetics in acetaminophen-induced liver injury. J Biol Chem 2008; 283: 13565-13577.
22. Win S, Than TA, Han D, Petrovic LM, Kaplowitz N. 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 2011; 286: 35071-35078.
23. Nedergaard J, Cannon B. The 'novel uncoupling' proteins UCP2 and UCP3: what do they really do? Pros and cons for suggested functions. Exp Physiol 2003; 88: 65-84.
24. Brand MD, Esteves TC. Physiological functions of the mitochondrial uncoupling proteins UCP2 and UCP3. Cell Metab 2005; 2: 85-93.
25. Zaher H, Buters JTM, Ward JM, Bruno MK, Lucas AM, Stern ST, et al. Protection against acetaminophen toxicity in CYP1A2 and CYP2E1 double-null mice. Toxicol Appl Pharmacol 1998; 152: 193-199.
26. Sluse FE, Jarmuszkiewicz W, Navet R, Douette P, Mathy G, Sluse-Goffart CM. Mitochondrial UCPs: new insights into regulation and impact. Biochim Biophys Acta Bioenerg 2006; 1757: 480-485.
27. Yonezawa T, Kurata R, Hosomichi K, Kono A, Kimura M, Inoko H. Nutritional and hormonal regulation of uncoupling protein 2. IUBMB Life 2009; 61: 1123-1131.
28. Pecqueur C, Bui T, Gelly C, Hauchard J, Barbot C, Bouillaud F, et al. Uncoupling protein-2 controls proliferation by promoting fatty acid oxidation and limiting glycolysis-derived pyruvate utilization. FASEB J 2008; 22: 9-18.
29. Sluse FE, Jarmuszkiewicz W, Navet R, Douette P, Mathy G, Sluse-Goffart CM. Mitochondrial UCPs: new insights into regulation and impact. Biochim Biophys Acta 2006; 1757: 480-485.
30. Berardi MJ, Shih WM, Harrison SC, Chou JJ. Mitochondrial uncoupling protein 2 structure determined by NMR molecular fragment searching. Nature 2011; 476: 109-113.
31. Kuhla A, Hettwer C, Menger MD, Vollmar B. Oxidative stress-associated rise of hepatic protein glycation increases inflammatory liver injury in uncoupling protein-2 deficient mice. Lab Invest 2010; 90: 1189-1198.
32. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wrahli W. Peroxisome proliferator-activated receptor alpha mediates the adaptive response to fasting. J Clin Invest 1999; 103: 1489-1498.
33. Abdelmegeed MA, Moon KH, Hardwick JP, Gonzalez FJ, Song BJ. Role of peroxisome proliferator-activated receptor-alpha in fasting-mediated oxidative stress. Free Radic Biol Med 2009; 47: 767-778.