Fibroblast growth factor 21 protects against acetaminophen-induced hepatotoxicity by potentiating peroxisome proliferator-activated receptor coactivator protein-1α-mediated antioxidant capacity in mice

Hepatology

Volumn 60, Issue 3, 2014, Pages 977-989

  Ye, Dewei ^a,b   Wang, Yudong ^a,b   Li, Huating ^c   Jia, Weiping ^c   Man, Kwan ^b   Lo, Chung Mau ^b   Wang, Yu ^a,b   Lam, Karen S L ^a,b   Xu, Aimin ^a,b  

^a UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A OXIDASE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BUPIVACAINE; CYTOCHROME P450; CYTOCHROME P450 2E1; CYTOCHROME P450 4A10; FIBROBLAST GROWTH FACTOR 10; FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR 21; GAMMA GLUTAMYL CYSTEINE LIGASE CATALYTIC SUBUNIT; GLUCOSE 6 PHOSPHATE DEHYDROGENASE; GLUTATHIONE; GLUTATHIONE PEROXIDASE 1; LIGASE; LUCIFERASE; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; MITOCHONDRIAL DNA; PARACETAMOL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR COACTIVATOR PROTEIN 1 ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; RECOMBINANT CYTOKINE; RECOMBINANT FIBROBLAST GROWTH FACTOR 21; RECOMBINANT GROWTH FACTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 2; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

ADENOVIRUS; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; CELL DEATH; CONTROLLED STUDY; DNA FRAGMENTATION; DRUG OVERDOSE; ENZYME PHOSPHORYLATION; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LIVER; LIVER CELL; LIVER INJURY; LIVER NECROSIS; LIVER PROTECTION; LIVER TOXICITY; MALE; MORTALITY; MOUSE; MUSCLE INJURY; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SCAVENGING SYSTEM; TRANSCRIPTION INITIATION; UPREGULATION;

ACETAMINOPHEN; ANALGESICS, NON-NARCOTIC; ANIMALS; ANTIOXIDANTS; DRUG SYNERGISM; DRUG-INDUCED LIVER INJURY; FIBROBLAST GROWTH FACTORS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; REACTIVE OXYGEN SPECIES; TRANSCRIPTION FACTORS;

EID: 84906487180     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.27060     Document Type: Article

References (38)

1. Bernal W, Auzinger G, Dhawan A, Wendon J. Acute liver failure. Lancet 2010;376:190-201.
2. Jaeschke H, McGill MR, Williams CD, Ramachandran A. Current issues with acetaminophen hepatotoxicity-a clinically relevant model to test the efficacy of natural products. Life Sci 2011;88:737-745.
3. Tirmenstein MA, Nelson SD. Subcellular binding and effects on calcium homeostasis produced by acetaminophen and a nonhepatotoxic regioisomer, 3′-hydroxyacetanilide, in mouse-liver. J Biol Chem 1989;264:9814-9819.
4. McGill MR, Sharpe MR, Williams CD, Taha M, Curry SC, Jaeschke H. The mechanism underlying acetaminophen-induced hepatotoxicity in humans and mice involves mitochondrial damage and nuclear DNA fragmentation. J Clin Invest 2012;122:1574-1583.
5. Jaeschke H, Williams CD, Ramachandran A, Bajt ML. Acetaminophen hepatotoxicity and repair: the role of sterile inflammation and innate immunity. Liver Int 2012;32:8-20.
6. Jaeschke H, McGill MR, Ramachandran A. Oxidant stress, mitochondria, and cell death mechanisms in drug-induced liver injury: lessons learned from acetaminophen hepatotoxicity. Drug Metab Rev 2012;44:88-106.
7. Itoh N, Ornitz DM. Fibroblast growth factors: from molecular evolution to roles in development, metabolism and disease. J Biochem 2011;149:121-130.
8. Kliewer SA, Mangelsdorf DJ. Fibroblast growth factor 21: from pharmacology to physiology. Am J Clin Nutr 2010;91:254S-257S.
9. Kharitonenkov A, Shiyanova TL, Koester A, Ford AM, Micanovic R, Galbreath EJ, et al. FGF-21 as a novel metabolic regulator. J Clin Invest 2005;115:1627-1635.
10. Kharitonenkov A, Wroblewski VJ, Koester A, Chen YF, Clutinger CK, Tigno XT, et al. The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 2007;148:774-781.
11. Potthoff MJ, Inagaki T, Satapati S, Ding X, He T, Goetz R, et al. FGF21 induces PGC-1alpha and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc Natl Acad Sci U S A 2009;106:10853-10858.
12. Inagaki T, Dutchak P, Zhao G, Ding X, Gautron L, Parameswara V, et al. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab 2007;5:415-425.
13. Inagaki T, Lin VY, Goetz R, Mohammadi M, Mangelsdorf DJ, Kliewer SA. Inhibition of growth hormone signaling by the fasting-induced hormone FGF21. Cell Metab 2008;8:77-83.
14. Zhang X, Yeung DC, Karpisek M, Stejskal D, Zhou ZG, Liu F, et al. Serum FGF21 levels are increased in obesity and are independently associated with the metabolic syndrome in humans. Diabetes 2008;57:1246-1253.
15. Xiao Y, Xu A, Law LS, Chen C, Li H, Li X, et al. Distinct changes in serum fibroblast growth factor 21 levels in different subtypes of diabetes. J Clin Endocrinol Metab 2012;97:E54-58.
16. Li H, Fang Q, Gao F, Fan J, Zhou J, Wang X, et al. Fibroblast growth factor 21 levels are increased in nonalcoholic fatty liver disease patients and are correlated with hepatic triglyceride. J Hepatol 2010;53:934-940.
17. Johnson CL, Weston JY, Chadi SA, Fazio EN, Huff MW, Kharitonenkov A, et al. Fibroblast growth factor 21 reduces the severity of cerulein-induced pancreatitis in mice. Gastroenterology 2009;137:1795-1804.
18. Feingold KR, Grunfeld C, Heuer JG, Gupta A, Cramer M, Zhang T, et al. FGF21 is increased by inflammatory stimuli and protects leptin-deficient ob/ob mice from the toxicity of sepsis. Endocrinology 2012;153:2689-2700.
19. Hotta Y, Nakamura H, Konishi M, Murata Y, Takagi H, Matsumura S, et al. Fibroblast growth factor 21 regulates lipolysis in white adipose tissue but is not required for ketogenesis and triglyceride clearance in liver. Endocrinology 2009;150:4625-4633.
20. Ye D, Li FY, Lam KS, Li H, Jia W, Wang Y, et al. Toll-like receptor-4 mediates obesity-induced non-alcoholic steatohepatitis through activation of X-box binding protein-1 in mice. Gut 2012;61:1058-1067.
21. Zhou M, Xu A, Tam PK, Lam KS, Chan L, Hoo RL, et al. Mitochondrial dysfunction contributes to the increased vulnerabilities of adiponectin knockout mice to liver injury. Hepatology 2008;48:1087-1096.
22. Chen W, Hoo RL, Konishi M, Itoh N, Lee PC, Ye HY, et al. Growth hormone induces hepatic production of fibroblast growth factor 21 through a mechanism dependent on lipolysis in adipocytes. J Biol Chem 2011;286:34559-34566.
23. Badman MK, Pissios P, Kennedy AR, Koukos G, Flier JS, Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab 2007;5:426-437.
24. 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.
25. Ahmed MM, Wang T, Luo Y, Ye S, Wu Q, Guo Z, et al. Aldo-keto reductase-7A protects liver cells and tissues from acetaminophen-induced oxidative stress and hepatotoxicity. Hepatology 2011;54:1322-1332.
26. Ma Q, He X. Molecular basis of electrophilic and oxidative defense: promises and perils of Nrf2. Pharmacol Rev 2012;64:1055-1081.
27. Clark J, Simon DK. Transcribe to survive: transcriptional control of antioxidant defense programs for neuroprotection in Parkinson's disease. Antioxid Redox Signal 2009;11:509-528.
28. Aquilano K, Baldelli S, Pagliei B, Cannata SM, Rotilio G, Ciriolo MR. p53 orchestrates the PGC-1alpha-mediated antioxidant response upon mild redox and metabolic imbalance. Antioxid Redox Signal 2013;18:386-399.
29. Fisher FM, Kleiner S, Douris N, Fox EC, Mepani RJ, Verdeguer F, et al. FGF21 regulates PGC-1alpha and browning of white adipose tissues in adaptive thermogenesis. Genes Dev 2012;26:271-281.
30. Kon K, Kim JS, Jaeschke H, Lemasters JJ. Mitochondrial permeability transition in acetaminophen-induced necrosis and apoptosis of cultured mouse hepatocytes. Hepatology 2004;40:1170-1179.
31. Masubuchi Y, Suda C, Horie T. Involvement of mitochondrial permeability transition in acetaminophen-induced liver injury in mice. J Hepatol 2005;42:110-116.
32. 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.
33. Gunawan BK, Liu ZX, Han D, Hanawa N, Gaarde WA, Kaplowitz N. c-Jun N-terminal kinase plays a major role in murine acetaminophen hepatotoxicity. Gastroenterology 2006;131:165-178.
34. Baird L, Dinkova-Kostova AT. The cytoprotective role of the Keap1-Nrf2 pathway. Arch Toxicol 2011;85:241-272.
35. Enomoto A, Itoh K, Nagayoshi E, Haruta J, Kimura T, O'Connor T, et al. High sensitivity of Nrf2 knockout mice to acetaminophen hepatotoxicity associated with decreased expression of ARE-regulated drug metabolizing enzymes and antioxidant genes. Toxicol Sci 2001;59:169-177.
36. Okawa H, Motohashi H, Kobayashi A, Aburatani H, Kensler TW, Yamamoto M. Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity. Biochem Biophys Res Commun 2006;339:79-88.
37. Liu C, Lin JD. PGC-1 coactivators in the control of energy metabolism. Acta Biochim Biophys Sin (Shanghai) 2011;43:248-257.
38. Baldelli S, Aquilano K, Ciriolo MR. Punctum on two different transcription factors regulated by PGC-1alpha: nuclear factor erythroid-derived 2-like 2 and nuclear respiratory factor 2. Biochim Biophys Acta 2013;1830:4137-4146.