Ketone body therapy protects from lipotoxicity and acute liver failure upon Ppar α deficiency

Molecular Endocrinology

Volumn 29, Issue 8, 2015, Pages 1134-1143

  Pawlak, Michal ^a   Baugé, Eric ^a   Lalloyer, Fanny ^a   Lefebvre, Philippe ^a   Staels, Bart ^a  

^a INSTITUT PASTEUR DE LILLE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

3 HYDROXYBUTYRIC ACID; ALANINE AMINOTRANSFERASE; AMMONIA; ASPARTATE AMINOTRANSFERASE; FISH OIL; KETONE BODY; MALONALDEHYDE; OMEGA 3 FATTY ACID; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; REACTIVE OXYGEN METABOLITE; FATTY ACID; TRIACYLGLYCEROL;

ACUTE LIVER FAILURE; ADENO ASSOCIATED VIRUS 8; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; COMA; CONTROLLED STUDY; DEATH; FATTY ACID OXIDATION; FEMALE; KETOGENESIS; LIPID PEROXIDATION; LIPOTOXICITY; LIVER PROTECTION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CHEMISTRY; DEFICIENCY; FATTY LIVER; LIVER; LIVER FAILURE, ACUTE; METABOLISM; MITOCHONDRION; OXIDATION REDUCTION REACTION; PEROXISOME;

HELIANTHUS; MUS;

3-HYDROXYBUTYRIC ACID; ANIMALS; FATTY ACIDS; FATTY LIVER; FEMALE; KETONE BODIES; LIPID PEROXIDATION; LIVER; LIVER FAILURE, ACUTE; MICE; MICE, INBRED C57BL; MITOCHONDRIA; OXIDATION-REDUCTION; OXIDATIVE STRESS; PEROXISOMES; PPAR ALPHA; REACTIVE OXYGEN SPECIES; TRIGLYCERIDES;

EID: 84938322085     PISSN: 08888809     EISSN: 19449917     Source Type: Journal    
DOI: 10.1210/me.2014-1383     Document Type: Article

References (58)

1. Bernal W, Wendon J. Acute liver failure. N Engl J Med. 2013;369: 2525-2534.
2. Gotthardt D, Riediger C, Weiss KH, et al. Fulminant hepatic failure: etiology and indications for liver transplantation. Nephrol Dial Transplant. 2007;22(suppl 8):viii5-viii8.
3. McGill MR, Staggs VS, Sharpe MR, Lee WM, Jaeschke H. Serum mitochondrial biomarkers and damage-associated molecular patterns are higher in acetaminophen overdose patients with poor out-come. Hepatology. 2014;60:1336-1345.
4. Liu H, Han T, Tian J, et al. Monitoring oxidative stress in acuteon-chronic liver failure by advanced oxidation protein products. Hepatol Res. 2012;42:171-180.
5. Bantel H, Schulze-Osthoff K. Mechanisms of cell death in acute liver failure. Front Physiol. 2012;3:79
6. 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
7. Baruteau J, Sachs P, Broué P, et al. Clinical and biological features at diagnosis in mitochondrial fatty acidoxidation defects: a French pediatric study of 187 patients. J Inherit Metab Dis. 2013; 36:795-803.
8. Alonso EM. Acute liver failure in children: the role of defects in fatty acid oxidation. Hepatology. 2005;41:696-699.
9. Natarajan SK, Thangaraj KR, Eapen CE, et al. Liver injury in acute fatty liver of pregnancy: possible link to placental mitochondrial dysfunction and oxidative stress. Hepatology. 2010;51:191-200.
10. Heard KJ. Acetylcysteine for acetaminophen poisoning. N Engl J Med. 2008;359:285-292.
11. Ferret PJ, Hammoud R, Tulliez M, et al. Detoxification of reactive oxygen species by a nonpeptidyl mimic of superoxide dismutase cures acetaminophen-induced acute liver failure in the mouse. Hepatology. 2001;33:1173-1180.
12. Gulick T, Cresci S, Caira T, Moore DD, Kelly DP. The peroxisome proliferator-activated receptor regulates mitochondrial fatty acid oxidative enzyme gene expression. Proc Natl Acad Sci USA. 1994; 91:11012-11016.
13. Leone TC, Weinheimer CJ, Kelly DP. A critical role for the peroxisome proliferator-activated receptor (PPAR) in the cellular fasting response: the PPAR-null mouse as a model of fatty acid oxidation disorders. Proc Natl Acad Sci USA. 1999;96:7473-7478.
14. Lu Y, Boekschoten MV, Wopereis S, Müller M, Kersten S. Comparative transcriptomic and metabolomic analysis of fenofibrate and fish oil treatments in mice. Physiol Genomics. 2011;43:1307-1318.
15. Martin PG, Guillou H, Lasserre F, et al. Novel aspects of PPAR mediated regulation of lipid and xenobiotic metabolism revealed through a nutrigenomic study. Hepatology. 2007;45:767-777.
16. Ip E, Farrell G, Hall P, Robertson G, Leclercq I. Administration of the potent PPAR agonist, Wy-14,643, reverses nutritional fibrosis and steatohepatitis in mice. Hepatology. 2004;39:1286-1296.
17. Patterson AD, Shah YM, Matsubara T, Krausz KW, Gonzalez FJ. Peroxisome proliferator-activated receptor induction of uncoupling protein 2 protects against acetaminophen-induced liver toxicity. Hepatology. 2012;56:281-290.
18. Nakajima T, Kamijo Y, Tanaka N, et al. Peroxisome proliferatoractivated receptor protects against alcohol-induced liver damage. Hepatology. 2004;40:972-980.
19. Toyama T, Nakamura H, Harano Y, et al. PPAR ligands activate antioxidant enzymes and suppress hepatic fibrosis in rats. Biochem Biophys Res Commun. 2004;324:697-704.
20. Ashibe B, Motojima K. Fatty aldehyde dehydrogenase is up-regulated by polyunsaturated fatty acid via peroxisome proliferatoractivated receptor and suppresses polyunsaturated fatty acid-induced endoplasmic reticulum stress. FEBS J. 2009;276:6956-6970.
21. Pawlak M, Lefebvre P, Staels B. Molecular mechanism of PPAR action and its impact on lipid metabolism, inflammation and fibrosis in non-alcoholic fatty liver disease. J Hepatol. 2015;62:720-733.
22. Kersten S, Seydoux J, Peters JM, Gonzalez FJ, Desvergne B, Wahli W. Peroxisome proliferator-activated receptor mediates the adaptive response to fasting. J Clin Invest. 1999;103:1489-1498.
23. Patsouris D, Reddy JK, Müller M, Kersten S. Peroxisome proliferator-activated receptor mediates the effects of high-fat diet on hepatic gene expression. Endocrinology. 2006;147:1508-1516.
24. Ikeda I, Cha JY, Yanagita T, et al. Effects of dietary-linolenic, eicosapentaenoic and docosahexaenoic acids on hepatic lipogenesis and oxidation in rats. Biosci Biotechnol Biochem. 1998;62:675-680
25. Dallongeville J, Baugé E, Tailleux A, et al. Peroxisome proliferatoractivated receptor is not rate-limiting for the lipoprotein-lowering action of fish oil. J Biol Chem. 2001;276:4634-4639.
26. Kim HJ, Takahashi M, Ezaki O. Fish oil feeding decreases mature sterol regulatory element-binding protein 1 (SREBP-1) by downregulation of SREBP-1c mRNA in mouse liver. A possible mecha-nism for down-regulation of lipogenic enzyme mRNAs. J Biol Chem. 1999;274:25892-25898.
27. Miret S, Sáiz MP, Mitjavila MT. Effects of fish oil-and olive oil-rich diets on iron metabolism and oxidative stress in the rat. Br J Nutr. 2003;89:11-18.
28. Takahashi M, Tsuboyama-Kasaoka N, Nakatani T, et al. Fish oil feeding alters liver gene expressions to defend against PPAR activation and ROS production. Am J Physiol Gastrointest Liver Physiol. 2002;282:G338-G348.
29. Feillet-Coudray C, Aoun M, Fouret G, et al. Effects of long-term administration of saturated and n-3 fatty acid-rich diets on lipid utilisation and oxidative stress in rat liver and muscle tissues. Br J Nutr. 2013;110:1789-1802.
30. Ruiz-Gutiérrez V, Pérez-Espinosa A, Vázquez CM, Santa-María C. Effects of dietary fats (fish, olive and high-oleic-acid sunflower oils) on lipid composition and antioxidant enzymes in rat liver. Br J Nutr. 1999;82:233-241.
31. Larter CZ, Yeh MM, Cheng J, et al. Activation of peroxisome proliferator-activated receptor by dietary fish oil attenuates steatosis, but does not prevent experimental steatohepatitis because of hepatic lipoperoxide accumulation. J Gastroenterol Hepatol. 2008; 23:267-275.
32. Argo CK, Patrie JT, Lackner C, et al. Effects of n-3 fish oil on metabolic and histological parameters in NASH: a double-blind, randomized, placebo-controlled trial. J Hepatol. 2015;62:190-197.
33. Francque S, Verrijken A, Caron S, et al. PPAR gene expression correlates with severity and histological treatment response in patients with non-alcoholic steatohepatitis. J Hepatol. 2015;63:164-173.
34. Lee SS, Pineau T, Drago J, et al. Targeted disruption of the 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.
35. Jelinek D, Castillo JJ, Arora SL, Richardson LM, Garver WS. A high-fat diet supplemented with fish oil improves metabolic features associated with type 2 diabetes. Nutrition. 2013;29:1159-1165.
36. Pawlak M, Bauge E, Bourguet W, et al. The transrepressive activity of Ppar is necessary and sufficient to prevent liver fibrosis. Hepatology. 2014;60:1593-1606.
37. Hashimoto T, Fujita T, Usuda N, et al. Peroxisomal and mitochondrial fatty acid β-oxidation in mice nullizygous for both peroxisome proliferator-activated receptor and peroxisomal fatty acyl-CoA oxidase. Genotype correlation with fatty liver phenotype. J Biol Chem. 1999;274:19228-19236.
38. Pizzimenti S, Ciamporcero E, Daga M, et al. Interaction of aldehydes derived from lipid peroxidation and membrane proteins. Front Physiol. 2013;4:242
39. Prabhu KS, Reddy PV, Jones EC, Liken AD, Reddy CC. Characterization of a class glutathione-S-transferase with glutathione peroxidase activity in human liver microsomes. Arch Biochem Bio-phys. 2004;424:72-80.
40. Ong JP, Aggarwal A, Krieger D, et al. Correlation between ammonia levels and the severity of hepatic encephalopathy. Am J Med. 2003;114:188-193.
41. Bernal W. Lactate is important in determining prognosis in acute liver failure. J Hepatol. 2010;53:209-210.
42. SilverClman J. inical biochemistry parameters in C57BL/6J mice after blood collection from the submandibular vein and retroorbital plexus. J Am Assoc Lab Anim Sci. 2010;49:400; author reply 400.
43. Cheng B, Yang X, Chen C, Cheng D, Xu X, Zhang X. D-β-hydroxybutyrate prevents MPP-induced neurotoxicity in PC12 cells. Neurochem Res. 2010;35:444-451.
44. Shimazu T, Hirschey MD, Newman J, et al. Suppression of oxidative stress by β-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science. 2013;339:211-214.
45. Burns CP, Wagner BA. Heightened susceptibility of fish oil polyunsaturate-enriched neoplastic cells to ethane generation during lipid peroxidation. J Lipid Res. 1991;32:79-87.
46. Kristal BS, Park BK, Yu BP. 4-Hydroxyhexenal is a potent inducer of the mitochondrial permeability transition. J Biol Chem. 1996; 271:6033-6038.
47. Hashimoto T, Cook WS, Qi C, Yeldandi AV, Reddy JK, Rao MS. Defect in peroxisome proliferator-activated receptor-inducible fatty acid oxidation determines the severity of hepatic steatosis in response to fasting. J Biol Chem. 2000;275:28918-28928.
48. Palmer CN, Hsu MH, Griffin KJ, Raucy JL, Johnson EF. Peroxisome proliferator activated receptor-expression in human liver. Mol Pharmacol. 1998;53:14-22.
49. Sengupta S, Peterson TR, Laplante M, Oh S, Sabatini DM. mTORC1 controls fasting-induced ketogenesis and its modulation by ageing. Nature. 2010;468:1100-1104.
50. Nielsen NC, Fleischer S. β-Hydroxybutyrate dehydrogenase: lack in ruminant liver mitochondria. Science. 1969;166:1017-1019.
51. Tieu K, Perier C, Caspersen C, et al. D-β-hydroxybutyrate rescues mitochondrial respiration and mitigates features of Parkinson disease. J Clin Invest. 2003;112:892-901.
52. Long EK, Picklo MJ Sr. Trans-4-hydroxy-2-hexenal, a product of n-3 fatty acid peroxidation: make some room HNE. Free Radic Biol Med. 2010;49:1-8.
53. Kashiwaya Y, Takeshima T, Mori N, Nakashima K, Clarke K, Veech RL. D-β-hydroxybutyrate protects neurons in models of Alzheimer’s and Parkinson’s disease. Proc Natl Acad Sci USA. 2000; 97:5440-5444
54. Van Hove JL, Grünewald S, Jaeken J, et al. D,L-3-hydroxybutyrate treatment of multiple acyl-CoA dehydrogenase deficiency (MADD). Lancet. 2003;361:1433-1435.
55. Awasthi YC, Yang Y, Tiwari NK, et al. Regulation of 4-hydroxynonenal-mediated signaling by glutathione S-transferases. Free Radic Biol Med. 2004;37:607-619.
56. Mejía-Toiber J, Montiel T, Massieu L. D-β-hydroxybutyrate prevents glutamate-mediated lipoperoxidation and neuronal damage elicited during glycolysis inhibition in vivo. Neurochem Res. 2006; 31:1399-1408.
57. Haces ML, Hernández-Fonseca K, Medina-Campos ON, Montiel T, Pedraza-Chaverri J, Massieu L. Antioxidant capacity contributes to protection of ketone bodies against oxidative damage induced during hypoglycemic conditions. Exp Neurol. 2008;211:85-96.
58. Walsh TS, Wigmore SJ, Hopton P, Richardson R, Lee A. Energy expenditure in acetaminophen-induced fulminant hepatic failure. Crit Care Med. 2000;28:649-654