Alcoholic liver injury in the rat is associated with reduced expression of peroxisome proliferator-α (PPARα)-regulated genes and is ameliorated by PPARα activation

Journal of Pharmacology and Experimental Therapeutics

Volumn 310, Issue 1, 2004, Pages 417-424

  Nanji, Amin A ^a   Dannenberg, Andrew J ^b   Jokelainen, Kalle ^c   Bass, Nathan M ^d  

^a HOSPITAL OF THE UNIVERSITY OF PENNSYLVANIA   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c HELSINKI UNIVERSITY CENTRAL HOSPITAL   (Finland)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL COENZYME A DEHYDROGENASE; ALCOHOL; BETA ACTIN; CLOFIBRATE; CORN OIL; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; CYTOCHROME P450 4A11; FATTY ACID BINDING PROTEIN; FISH OIL; GLUCOSE; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; THIOBARBITURIC ACID REACTIVE SUBSTANCE; TUMOR NECROSIS FACTOR ALPHA;

ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAT INTAKE; FATTY ACID METABOLISM; FATTY ACID OXIDATION; FATTY LIVER; GENE CONTROL; GENE EXPRESSION; HEPATITIS; HISTOPATHOLOGY; LIPID PEROXIDATION; LIVER NECROSIS; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ACYL-COA OXIDASE; ANIMALS; CARRIER PROTEINS; CLOFIBRATE; CYCLOOXYGENASE 2; ETHANOL; FATTY ACID-BINDING PROTEINS; FATTY LIVER; GENE EXPRESSION REGULATION; ISOENZYMES; LIPID PEROXIDATION; LIVER DISEASES, ALCOHOLIC; MALE; NF-KAPPA B; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; RATS; RATS, WISTAR; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTION FACTORS; TUMOR NECROSIS FACTOR-ALPHA; UP-REGULATION;

EID: 3042635055     PISSN: 00223565     EISSN: None     Source Type: Journal    
DOI: 10.1124/jpet.103.064717     Document Type: Article

References (73)

1. Amet Y, Adas F, and Nanji AA (1998) Fatty acid omega-and (omega-1) - hydroxylation in experimental alcoholic liver disease: relationship to different dietary fatty acids. Alcohol Clin Exp Res 22:1493-1500.
2. Amet Y, Berthou F, GoasduffT, Salaun JP, Breton L, and Menez JF (1994) Evidence that cytochrome P450 2E1 is involved in the (omega-1)-hydroxylation of lauric acid in rat liver microsomes. Biochem Biophys Res Commun 203:1168-1174.
3. Bass NM (1993) Cellular binding proteins for fatty acids and retinoids: similar or specialized functions? Mol Cell Biochem 123:191-202.
4. Bass NM (1996) Interaction of fatty-acid binding-proteins (FABP) with the peroxisome proliferator-activated receptor alpha (PPARα): evidence for FABP modulation of the gene response to fatty acid overload, in Frontiers in Bioactive Lipids (Vanderhoek JY ed). XXVI Washington International Spring Symposium on Bioactive Lipids, 1995, Washington, DC, pp 67-72, Plenum Press, New York.
5. Bass NM, Barker ME, Manning JA, Jones AL, and Ockner RK (1989) Acinar heterogeneity of fatty acid binding protein expression in the livers of male female and clofibrate-treated rats. Hepatology 9:12-21.
6. Bass NM, Kaikaus RM, and Ockner RK (1993a) Physiology and molecular biology of hepatic cytosolic fatty acid-binding protein, in Hepatic Transport and Bile secretion: Physiology and Pathophysiology (Tavaloni N and Berk PD eds) pp 421-446, Raven Press, New York.
7. Bass NM, Sadovsky Y, Appel RA, and Kushner PJ (1993b) Dicarboxylic fatty acids activate the peroxisome-proliferator-activated receptor (PPAR) in rat HTC hepatoma cells. Hepatology 18:125A.
8. Bell DR, Bars RG, and Elcombe CR (1992) Differential tissue-specific expression and induction of cytochrome P450IVA1 and acyl-CoA oxidase. Eur J Biochem 206:979-986.
9. Braissant O, Foufelle F, Scotto C, Dauca M, and Wahli W (1996) Differential expression of peroxisome proliferator-activated receptors (PPARs): tissue distribution of PPAR-alpha, -beta, and -gamma in the adult rat. Endocrinology 137:354-366.
10. Chevalier S and Roberts RA (2000) Perturbation of rodent hepatocyte growth control by nongenotoxic hepatocarcinogens: mechanism and lack of relevance for human health. Oncol Res 5:1319-1327.
11. Chomczynski P and Sacchi N (1997) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chlofoform extraction. Anal Biochem 162:156-159.
12. Costet P, Legendre C, More J, Edgar A, Galtier P, and Pineau T (1998) Peroxisome proliferator-activated receptor alpha-isoform deficiency leads to progressive dyslipidemia with sexually dimorphic obesity and steatosis. J Biol Chem 273:29577-29585.
13. Delerive P, Gervois P, Fruchart JC, and Staels B (2000) Induction of IkappaBalpha expression as a mechanism contributing to the anti-inflammatory activities of peroxisome proliferator-activated receptor-alpha activators. J Biol Chem 275:36703-36707.
14. Duplus E, Glorian M, and Forest C (2000) Fatty acid regulation of gene transcription. J Biol Chem 275:30749-30752.
15. Eaton S, Zaitoun AM, Record CO, and Bartlett K (1996) β-Oxidation in human alcoholic and non-alcoholic hepatic steatosis. Clin Sci 90:307-313.
16. Enoch T, Zinn K, and Maniatis T (1986) Activation of the human beta-interferon gene requires an interferon-inducible factor. Mol Cell Biol 6:801-810.
17. Fan CY, Pan J, Ususa N, Yeldandi AV, Rao MS, and Reddy JK (1998) Steatohepatitis, spontaneous peroxisome proliferation and liver tumors in mice lacking peroxisomal fatty acyl-CoA oxidase: implications for peroxisome proliferator-activated receptor alpha natural ligand metabolism. J Biol Chem 273:15639-15646.
18. Fischer M, You M, Matsumoto M, and Crabb DW (2003) Peroxisome proliferator-activated receptor α (PPARα) agonist treatment reverses PPARα dysfunction and abnormalities in hepatic lipid metabolism in ethanol-fed mice. J Biol Chem 278:27997-28004.
19. Forman BM, Chen J, and Evans RM (1997) Hypolipidemic drugs, polyunsaturated fatty acids and eicosanoids are ligands for peroxisome proliferator-activated receptors alpha and delta. Proc Natl Acad Sci USA 94:4312-4317.
20. French SW, Miyamoto K, and Tsukamoto H (1986) Ethanol-induced fibrosis in the rat: role of the amount of dietary fat. Alcohol Clin Exp Res 10:13S-19S.
21. French SW, Morimoto M, Reitz RC, Koop D, Klopfenstein B, Estes K, Clot P, Ingelman-Sundberg M, and Albano E (1997) Lipid peroxidation, CYP E21 and arachidonic acid metabolism in alcoholic liver disease in rats. J Nutr 127:9075-9115.
22. Fromenty B and Pessayre D (1995) Inhibition of mitochondrial beta-oxidation as a mechanism of hepatoxicity. Pharmacol Ther 67:101-154.
23. Fukuda T, Imai Y, Komori M, Nakamura M, Kusunose E, Satouchi K, and Kususnose M (1994) Different mechanisms of regioselection of fatty acid hydroxylation by laurate (ω-1) hydroxylating P450s P450 2C2 and P450 2EI. J Biochem 115:338-344.
24. Galli A, Pinnaire J, Fischer M, Dorris R, and Crabb DW (2001) The transcriptional and DNA binding activity of peroxisome proliferator-activated receptor α is inhibited by ethanol metabolism. J Biol Chem 276:68-75.
25. Galli EL and Crabb D (2000) The role of hepatic peroxisome proliferator-activated receptors (PPARs) in health and disease. Liver 20:191-199.
26. Gibson GG (1992) Co-induction of cytochrome P450 IV A1 and peroxisome proliferation: a causal or casual relationship? Xenobiotica 22:1101-1109.
27. Glatz JF and van der Vusse GJ (1996) Cellular fatty acid-binding proteins: their function and physiological significance. Prog Lipid Res 35:243-282.
28. Gottlicher M, Widmark E, Li Q, and Gustafsson JA (1992) Fatty acids activate a chimera of the clofibric acid-activated receptor and the glucocorticoid receptor. Proc Natl Acad Sci USA 89:4653-4657.
29. Guzman M and Geelan MJ (1993) Regulation of fatty acid oxidation in mammalian liver. Biochem Biophys Acta 1167:227-241.
30. Hashimoto T, Cook WS, Qi C, Yeldani AV, Reddy JK, and Rao MS (2000) Defect in peroxisome-proliferator activated receptor α-inducible fatty acid oxidation determines the severity of hepatic steatosis in response to fasting. J Biol Chem 275:28918-28928.
31. Kaikaus RM, Chan WK, Lysenko N, Ray R, Ortiz de Montellano PR, and Bass NM (1993a) Induction of peroxisomal fatty acid β-oxidation and liver fatty acid-binding protein by peroxisome proliferators: mediation via the cytochrome P450 IV A1 ω-hydroxylase pathway. J Biol Chem 268:9593-9603.
32. Kaikaus RM, Chan WK, Ortiz de Montellano PR, and Bass NM (1993b) Mechanisms of regulation of liver fatty acid-binding protein. Mol Cell Biochem 123:93-100.
33. Kaikus RM, Sui Z, Lysenko N, Wu NY, Ortiz de Montellano P, Ockner RK, and Bass NM (1993c) Regulation of pathways of extramitochondrial fatty acid oxidation and liver fatty acid binding protein by long chain monocarboxylic fatty acids in hepatocytes: effect of inhibition of carnitine palmitoyltransferase. J Biol Chem 268:26866-26871.
34. Kersten S, Desvergne B, and Wahli W (2000) Roles of PPARs in health and disease. Nature (Lond) 405:421-424.
35. Kliewer SA, Sundseth SS, Jones SA, Brown PJ, Wisely GB, Koble CS, Devchand P, Wahli W, Wilson TM, Lenhard JM, et al. (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors alpha and gamma. Proc Natl Acad Sci USA 94:4318-4323.
36. Kono H, Wheeler MD, Rusyn I, Lin M, Seabra V, Rivera CA, Bradford BU, and Thurman RG (2000) Gender differences in early alcohol-induced liver injury: role of CD14, NF-κB and TNF-α. Am J Physiol Gastrointest Liver Physiol 278:G652-G661.
37. Lambe KG, Woodyatt NJ, Macdonald N, Chevalier S, and Roberts RA (1999) Species differences in sequence and activity of the peroxisome proliferator response element (PPRE) with the acyl CoA oxidase gene promoter. Toxicol Lett 110:119-127.
38. Lee SS, Pineau T, Drago J, Lee EJ, Owens JW, Kroetz DL, Fernandez-Salguero PM, Westphal H, and Gonzalez FJ (1995) 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 15:3012-3022.
39. Lieber CS and Schmid R (1961) The effect of ethanol on fatty acid metabolism: stimulation of hepatic fatty acid synthesis in vitro. J Clin Investig 40:394-399.
40. Lieber CS (1994) (1997) Alcohol and the liver: 1994 update. Gastroenterology 106:1085-1105.
41. Lin M, Rippe RA, Niemela O, Britteham G, and Tsukamoto GH (1997) Role of iron in NF-κB activation and cytokine gene expression by rat hepatic macrophages. Am J Physiol 272:G1355-G1364.
42. 4-induced hepatic injury is associated with inhibition of nuclear factor kappa B binding. Hepatology 22:1474-1481.
43. Luxon BA, Milliano M, and Weisinger RA (2000) Induction of hepatic cytosolic fatty acid binding protein with clofibrate accelerants both membrane and cytoplasmic transport of palmitate. Biochem Biophys Acta 1487:309-318.
44. Ma X, Baraona E, Goozner BG, and Lieber CS (1999) Gender differences in medium chain dicarboxylic aciduria in alcoholic men and women. Am J Med 106:70-75.
45. Ma XL, Baraona E, and Lieber CS (1993) Alcohol consumption enhances fatty acid omega-oxidation with a greater increase in male than in female rats. Hepatology 18:1247-1253.
46. Merrimen RB, Aouizerat BE, Molly MJ, Kane JP, Bacon B, and Bass NM (2001) A genetic mutation in the peroxisome proliferator-activated receptor alpha gene in patients with non-alcoholic steatohepatitis. Hepatology 34:441A.
47. Milliano M and Luxon BA (2001) The peroxisomal proliferator clofibrate enhances the hepatic cytoplasmic movement of fatty acids in rats. Hepatology 33:413-418.
48. Mortensen PB (1990) Mechanism of dicarboxylic aciduria and dicarboxylic acid metabolism, in Fatty Acid Oxidation: Clinical Biochemical and Molecular Aspects (Tanaka K and Coats PM eds) pp 249-264, Liss, New York.
49. Nanji AA and French SW (1989) Dietary linoleic acid is required for development of experimental alcoholic liver disease. Life Sci 44:223-227.
50. Nanji AA, Jokelainen K, Rahemtulla A, Miao L, Fogt F, Matsumoto H, Tahan SR, and Su GL (1999) Activation of nuclear factor kappa B and cytokine imbalance in experimental alcoholic liver disease in the rat. Hepatology 30:934-943.
51. Nanji AA, Khwaja S, Tahan SR, and Sadrzadeh SMH (1994a) Plasma levels of a novel noncyclooxygenase-derived prostanoid (8-isoprostane) correlates with a severity of liver injury in experimental alcoholic live disease. J Pharmacol Exp Ther 269:1280-1285.
52. Nanji AA, Mendenhall CL, and French SW (1989) Beef fat prevents alcoholic liver disease in the rat. Alcohol Clin Exp Res 13:15-19.
53. Nanji AA, Miao L, Thomas P, Rahemtulla A, Khwaja S, Zhao S, Peters D, Tahan SR, and Dannenberg AJ (1997a) Enhanced cyclooxygenase-2 gene expression in alcoholic liver disease in the rat. Gastroenterology 112:943-951.
54. Nanji AA, Sadrzadeh SMH, Yang EK, Fogt F, Meydani M, and Dannenberg AJ (1995) Dietary saturated fatty acids: a novel treatment for alcoholic liver disease. Gastroenterology 109:547-554.
55. Nanji AA, Zakim D, Rahemtulla A, Daly T, Miao L, Zhao S, Khwaja S, Tahan SR, and Dannenberg AJ (1997b) Dietary saturated fatty acids down-regulate cyclooxygenase-2 and tumor necrosis factor-α and reverse fibrosis in alcoholic liver disease in the rat. Hepatology 26:1538-1545.
56. Nanji AA, Zhao S, Sadrzadeh SM, Dannenberg AJ, Tahan SR, and Waxman DJ (1994b) Markedly enhanced cytochrome P450 2E1 induction and lipid peroxidation is associated with severe liver injury in fish oil-ethanol fed rats. Alcohol Clin Exp Res 18:1280-1285.
57. Nanji AA, Zhao S, Sadrzadeh SM, and Waxman DJ (1994c) Use of reverse transcription PCR to evaluate in-vivo cytokine gene expression in rats fed ethanol for long periods of time. Hepatology 19:1483-1487.
58. Ockner RK, Kaikaus RM, and Bass NM (1993) Fatty-acid metabolism and the pathogenesis of hepatocellular carcinoma: review and hypothesis. Hepatology 18:669-676.
59. Ohkawa H, Ohisis N, and Yagi K (1979) Assay for lipid peroxidation in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351-358.
60. Palmer CN, Hsu MH, Griffin KJ, Raucy JL, and Johnson EF (1998) Peroxisome proliferator activated receptor-alpha expression in human liver. Mol Pharmacol 53:14-22.
61. Poynter ME and Daynes RA (1998) Peroxisome proliferator-activated receptor alpha activation modulates cellular redox status represses nuclear factor-kappaB signaling and reduces inflammatory cytokine production in aging. J Biol Chem 273:32833-32841.
62. Reddy J (2001) Non alcoholic steatosis and steatohepatitis: III. Peroxisomal β-oxidation PPARα and steatohepatitis. Am J Physiol Gastrointest Liver Physiol 281: G1333-G1339.
63. Reitz RC (1979) The effects of ethanol ingestion on lipid metabolism. Prog Lipid Res 18:87-115.
64. Rhoads DD, Dixit A, and Roufa DJ (1986) Primary structure of human ribosomal protein S14 and the gene that encodes it. Mol Cell Biol 2774-2783.
65. Sharma RK, Doig MV, Lewis DF, and Gibson GG (1989) Role of hepatic and renal cytochrome P450 IV A1 the metabolism of lipid substrates. Biochem Pharmacol 38:3621-3629.
66. Tsukamoto H, Gaal K, and French SW (1990) Insights into the pathogenesis of alcoholic liver necrosis and fibrosis: status report. Hepatology 12:599-608.
67. Tsutsumi M, Lasker J, Simizu M, Rosmen A, and Lieber CS (1989) The intralobular distribution of ethanol-inducible P450 IIE1 in rat and human liver. Hepatology 10:437-446.
68. Vamecg J and Lautruffe N (1999) Medical significance of peroxisome proliferator-activated receptors. Lancet 354:141-148.
69. Vanden-Heuvel JP (1999) Peroxisome proliferator-activated receptors: a critical link among fatty acids gene expression and carcinogenesis. J Nutr 129:5758-5808.
70. Wan YJ, Morimoto M, Thurman RG, Bojes HK, and French SW (1995) Expression of peroxisome proliferator activated receptor gene is decreased in experimental alcoholic liver disease. Life Sci 56:307-317.
71. Wan YY, Cai Y, Lungo W, Fu P, Locker J, French S, and Sucow HM (2000) Peroxisome proliferator-activated receptor α-mediated pathways are altered in hepatocytes-specific retinoid X receptor α deficient mice. J Biol Chem 275:28285-28290.
72. Wang AM, Doyle MV, and Mark DF (1989) Quantitation of mRNA by the polymerase chain reaction. Proc Natl Acad Sci USA 86:9717-9721.
73. Weisiger RA (1996) Cytoplasmic transport of lipids: role of binding proteins. Comp Biochem Physiol B 115:319-331.