Ethanol and fish oil induce NFκB transactivation of the collagen α2(I) promoter through lipid peroxidation-driven activation of the PKC-PI3K-akt pathway

Hepatology

Volumn 45, Issue 6, 2007, Pages 1433-1445

  Nieto, Natalia ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL; AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BETA GALACTOSIDASE; CATALASE; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA1; COLLAGEN TYPE 1 ALPHA2; COLLAGENASE 3; CYTOCHROME P450 2E1; FATTY ACID; FISH OIL; GLUTATHIONE; GLUTATHIONE PEROXIDASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN KINASE B; PROTEIN KINASE C; SUPEROXIDE DISMUTASE; UNCLASSIFIED DRUG;

ALCOHOL BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FOOD COMPOSITION; LIPID PEROXIDATION; LIVER INJURY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PRIORITY JOURNAL; STEATOSIS; UPREGULATION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIOXIDANTS; CELLS, CULTURED; CENTRAL NERVOUS SYSTEM DEPRESSANTS; COCULTURE TECHNIQUES; COLLAGEN; COLLAGEN TYPE I; DRUG SYNERGISM; ETHANOL; FISH OILS; GENE EXPRESSION REGULATION; HEPATOCYTES; I-KAPPA B PROTEINS; LIPID PEROXIDATION; MICE; MICE, TRANSGENIC; NF-KAPPA B; PROMOTER REGIONS (GENETICS); PROTEIN KINASE C; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 34250315771     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.21659     Document Type: Article

References (74)

1. French SW, Miyamoto K, Tsukamoto H. Ethanol-induced hepatic fibrosis in the rat: role of the amount of dietary fat. Alcohol Clin Exp Res 1986;10:13S-19S.
2. Nanji AA, Tsukamoto H, French SW. Relationship between fatty liver and subsequent development of necrosis, inflammation and fibrosis in experimental alcoholic liver disease. Exp Mol Pathol 1989;51:141-148.
3. Nanji AA, Griniuviene B, Sadrzadeh SM, Levitsky S, McCully JD. Effect of type of dietary fat and ethanol on antioxidant enzyme mRNA induction in rat liver. J Lipid Res 1995;36:736-744.
4. Nanji AA, Mendenhall CL, French SW. Beef fat prevents alcoholic liver disease in the rat. Alcohol Clin Exp Res 1989;13:15-19.
5. Diep QN, Touyz RM, Schiffrin EL. Docosahexaenoic acid, a peroxisome proliferator-activated receptor-alpha ligand, induces apoptosis in vascular smooth muscle cells by stimulation of p38 mitogen-activated protein kinase. Hypertension 2000;36:851-855.
6. Ukropec J, Reseland JE, Gasperikova D, Demcakova E, Madsen L, Berge RK, et al. The hypotriglyceridemic effect of dietary n-3 FA is associated with increased beta-oxidation and reduced leptin expression. Lipids 2003;38:1023-1029.
7. Adas F, Salaun JP, Berthou F, Picart D, Simon B, Amet Y. Requirement for omega and (omega;-1)-hydroxylations of fatty acids by human cytochromes P450 2E1 and 4A11. J Lipid Res 1999;40:1990-1997.
8. Adas F, Berthou F, Salaun JP, Dreano Y, Amet Y. Interspecies variations in fatty acid hydroxylations involving cytochromes P450 2E1 and 4A. Toxicol Lett 1999;110:43-55.
9. Davidson MH. Mechanisms for the hypotriglyceridemic effect of marine omega-3 fatty acids. Am J Cardiol 2006;98:27i-33i.
10. Gottlicher M, Demoz A, Svensson D, Tollet P, Berge RK, Gustafsson JA. Structural and metabolic requirements for activators of the peroxisome proliferator-activated receptor. Biochem Pharmacol 1993;46:2177-2184.
11. Moya-Camarena SY, Van den Heuvel JP, Belury MA. Conjugated linoleic acid activates peroxisome proliferator-activated receptor alpha and beta subtypes but does not induce hepatic peroxisome proliferation in Sprague-Dawley rats. Biochim Biophys Acta 1999;1436:331-342.
12. Moya-Camarena SY, Vanden Heuvel JP, Blanchard SG, Leesnitzer LA, Belury MA. Conjugated linoleic acid is a potent naturally occurring ligand and activator of PPARalpha. J Lipid Res 1999:40:1426-1433.
13. Belury MA, Moya-Camarena SY, Sun H, Snyder E, Davis JW, Cunningham ML, et al. Comparison of dose-response relationships for induction of lipid metabolizing and growth regulatory genes by peroxisome proliferators in rat liver. Toxicol Appl Pharmacol 1998:151:254-261.
14. Erol E, Kumar LS, Cline GW, Shulman GI, Kelly DP, Binas B. Liver fatty acid binding protein is requited for high rates of hepatic fatty acid oxidation but not for the action of PPARalpha in fasting mice. FASEB J 2004;18:347-349.
15. Zhou X, Jamil A, Nash A, Chan J, Trim N, Iredale JP, et al. Impaired proteolysis of collagen I inhibits proliferation of hepatic stellate cells: implications for regulation of liver fibrosis. J Biol Chem 2006.
16. Greenwel P, Dominguez-Rosales JA, Mavi G, Rivas-Estilla AM, Rojkind M. Hydrogen peroxide: a link between acetaldehyde-elicited alpha 1(I) collagen gene up-regulation and oxidative stress in mouse hepatic stellate cells. HEPATOLOGY 2000;31:109-116.
17. Garcia-Trevijano ER, Iraburu MJ, Fontana L, Dominguez-Rosales JA, Auster A, Covarrubias-Pinedo A, et al. Transforming growth factor beta1 induces the expression of alpha 1(I) procollagen mRNA by a hydrogen peroxide-C/EBPbeta- dependent mechanism in rat hepatic stellate cells. HEPATOLOGY 1999:29:960-970.
18. Nieto N, Friedman SL, Cederbaum AL Cytochrome P450 2E1-derived reactive oxygen species mediate paracrine stimulation of collagen I protein synthesis by hepatic stellate cells. J Biol Chem 2002;277:9853-9864.
19. Nieto N, Friedman SL, Cederbaum AI. Stimulation and proliferation of primary rat hepatic stellate cells by cytochrome P450 2EI-derived reactive oxygen species. HEPATOLOGY 2002;35:62-73.
20. Nieto N, Friedman SL, Greenwel P, Cederbaum AI. CYP2E1-mediated oxidative stress induces collagen type I expression in rat hepatic stellate cells. HEPATOLOGY 1999;30:987-996.
21. Nieto N, Greenwel P, Friedman SL, Zhang F, Dannenberg AJ, Cederbaum AI. Ethanol and arachidonic acid increase alpha 2(I) collagen expression in rat hepatic stellate cells overexpressing cytochrome P450 2E1. Role of H2O2 and cyclooxygenase-2. J Biol Chem 2000;275:20136-20145.
22. Svegliati-Baroni G, Inagaki Y, Rincon-Sanchez AR, Else C, Saccomanno S, Benedetti A, et al. Early response of alpha2(I) collagen to acetaldehyde in human hepatic stellate cells is TGF-beta independent. HEPATOLOGY 2005;42:343-352.
23. Fontana L, Jerez D, Rojas-Valencia L, Solis-Herruzo JA, Greenwel P, Rojkind M. Ethanol induces the expression of alpha 1(I) procollagen mRNA in a co-culture system containing a liver stellate cell-line and freshly isolated hepatocytes. Biochim Biophys Acta 1997;1362:135-144.
24. Li J, Kim CI, Leo MA, Mak KM, Rojkind M, Lieber CS. Polyunsaturated lecithin prevents acetaldehyde-mediated heparic collagen accumulation by stimulating collagenase activity in cultured lipocytes. HEPATOLOGY 1992;15:373-381.
25. Casini A, Cunningham M, Rojkind M, Lieber CS. Acetaldehyde increases procollagen type I and fibronectin gene rranscription in cultured rat fat-storing cells through a protein synthesis-dependent mechanism. HEPATOLOGY 1991;13:758-765.
26. Buttner C, Skupin A, Rieber EP. Transcriptional activation of the type 1 collagen genes COL1A1 and COL1A2 in fibroblasts by interleukin-4: analysis of the functional collagen promoter sequences. J Cell Physiol 2004;198:248-258.
27. Bowie A, O'Neill LA. Oxidative stress and nuclear factor-kappaB activation: a reassessment of the evidence in the light of recent discoveries. Biochem Pharmacol 2000;59:13-23.
28. Nieto N, Cederbaum Al. S-adenosylmethionine blocks collagen I production by preventing transforming growth factor-beta induction of the COL1A2 promoter. J Biol Chem 2005;280:30963-30974.
29. Antoniv TT, De Val S, Wells D, Denton CP, Rabe C, de Crombrugghe B, et al. Characterization of an evolutionarily conserved far-upstream enhancer in the human alpha 2(I) collagen (COL1A2) gene. J Biol Chem 2001;276:21754-21764.
30. Bou-Gharios G, Garrett LA, Rossert J, Niederreither K, Eberspaecher H, Smith C, et al. A potent fat-upstream enhancer in the mouse pro alpha 2(1) collagen gene regulates expression of reporter genes in transgenic mice. J Cell Biol 1996;134:1333-1344.
31. Kinbara T, Shirasaki F, Kawara S, Inagaki Y, de Crombrugghe B, Takehara K. Transforming growth factor-beta isoforms differently stimulate proalpha2 (I) collagen gene expression during wound healing process in transgenic mice. J Cell Physiol 2002;190:375-381.
32. Inagaki Y, Nemoto T, Kushida M, Sheng Y, Higashi K, Ikeda K, et al. Interferon alfa down-regulates collagen gene transcription and suppresses experimental hepatic fibrosis in mice. HEPATOLOGY 2003:38:890-899.
33. De Val SPM, Antoniv TT, Wells DJ, Abraham D, Partridge T, Bou-Gharios G. Identification of the key regions within the mouse pro-alpha 2(1) collagen gene far-upstream enhancer. J Biol Chem 2002;277:9286-9292.
34. Carmiel-Haggai M, Cederbaum Al, Nieto N. A high fat diet leads to the progression of non-alcoholic fatty liver disease in obese rats. FASEB J 2005;19:136-138.
35. Tietze F. Enzymatic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 1969;27:502-522.
36. Flohe L. Assays of glutethione peroxidase. Methods Enzymol 1984;106:114-121.
37. Claiborne A, Fridovich I. Purification of the o-dianisidine peroxidase from Escherichia coli B. Physicochemical characerization and analysis of its dual catalytic and peroxidatic activities. J Biol Chem 1979;254:4245-4252.
38. Paoletti F, Mocali A. Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol 1990;186:209-220.
39. Lowry O, Rosebrough NJ, Farr AL, Randal RJ. Protein measurements with the folin phenol reagent. J Biol Chem 1951;193:265-275.
40. Nieto N, Cederbaum AI. Increased Sp1-dependent transactivation of the LAMgamma 1 promoter in hepatic stellate cells co-cultured with HepG2 cells overexpressing cytochrome P450 2E1. J Biol Chem 2003;278:15360-15372.
41. Nieto N. Oxidative-sttess and IL-6 mediate the fibrogenic effects of rodent Kupffer cells on stellate cells. HEPATOLOGY 2006;44:1487-1501.
42. Boast S, Su MW, Ramirez F, Sanchez M, Avvedimento EV. Functional analysis of cis-acting DNA sequences controlling transcription of the human type I collagen genes. J Biol Chem 1990;265:13351-13356.
43. Nieto N, Mari M, Cederbaum AL Cytochrome P450 2E1 responsiveness in the promoter of glutamate-cysteine ligase catalytic subunit. HEPATOLOGY 2003;37:96-106.
44. Guichardant M, Chantegrel B, Deshayes C, Doutheau A, Moliere P, Lagarde M. Specific markers of lipid peroxidation issued from n-3 and n-6 fatty acids. Biochem Soc Trans 2004;32:139-140.
45. Sampey BP, Korourian S, Ronis MJ, Badger TM, Petersen DR. Immunohistochemical characterization of hepatic malondialdehyde and 4-hydroxynonenal modified proteins during early stages of ethanol-induced liver injury. Alcohol Clin Exp Res 2003;27:1015-1022.
46. Caro AA, Cederbaum AL Role of phosphatidylinositol 3-kinase/AKT as a survival pathway against CYP2E1-dependent toxicity. J Pharmacol Exp Ther 2006;318:360-372.
47. Wu D, Cederbaum A. Glutathione depletion in CYP2E1-expressing liver cells induces toxicity due to the activation of p38 mitogen-activated protein kinase and reduction of nuclear factor-kappaB DNA binding activity. Mol Pharmacol 2004;66:749-760.
48. Wu D, Cederbaum AL Role of p38 MAPK in CYP2E1-dependent arachidonic acid toxicity. J Biol Chem 2003;278:1115-1124.
49. Cao Q, Mak KM, Lieber CS. Leptin enhances alpha1(I) collagen gene expression in LX-2 human hepatic stellate cells through JAK-mediated H2O2-dependent MAPK pathways. J Cell Biochem 2006;97:188-197.
50. Davis BH, Chen A, Beno DW. Raf and mitogen-activated protein kinase regulate stellate cell collagen gene expression. J Biol Chem 1996;271:11039-11042.
51. Fromenty B, Grimbert S, Mansouri A, Beaugrand M, Erlinger S, Rotig A, et al. Hepatic mitochondrial DNA deletion in alcoholics: association with microvesicular steatosis. Gastroenterology 1995;108:193-200.
52. Kaikaus RM, Sui Z, Lysenko N, Wu NY, Ortiz de Montellano PR, Ockner RK, et al. Regulation of pathways of extramitochondrial fatty acid oxidation and liver fatty acid-binding protein by long-chain monocatboxylic fatty acids in hepatocytes. Effect of inhibition of carnitine palmitoyltransferase I. J Biol Chem 1993;268:26866-26871.
53. Kaikaus RM, Chan WK, Lysenko N, Ray R, Ortiz de Montellano PR, Bass NM. Induction of peroxisomal fatty acid beta-oxidation and liver fatty acid-binding protein by peroxisome proliferators. Mediation via the cytochrome P-450IVA1 omega-hydroxylase pathway. J Biol Chem 1993;268:9593-9603.
54. Ockner RK, Kaikaus RM, Bass NM. Fatty-acid metabolism and the pathogenesis of hepatocellular carcinoma: review and hypothesis. HEPATOLOGY 1993:18:669-676.
55. Amet Y, Berthou F, Goasduff T, Salaun JP, Le Breton L, Menez JF. Evidence that cytochrome P450 2E1 is involved in the (omega-1)-hydroxylation of lauric acid in rat liver microsomes. Biochem Biophys Res Commun 1994;203:1168-1174.
56. Sampath H, Ntambi JM. Polyunsatutated fatty acid regulation of gene expression. Nutt Rev 2004:62:333-339.
57. Roche HM, Gibney MJ. Long-chain n-3 polyunsaturated fatty acids and triacylglycerol metabolism in the postprandial state. Lipids 1999;34(Suppl):259-265.
58. Hau MF, Smelt AH, Bindels AJ, Sijbrands EJ, Van der Laarse A, Onkenhout W, et al. Effects of fish oil on oxidation resistance of VLDL in hypertriglyceridemic patients. Artetioscler Thromb Vase Biol 1996;16:1197-1202.
59. Nieto N, Fernandez MI, Torres MI, Rios A, Suarez MD, Gil A. Dietary monounsatutated n-3 and n-6 long-chain polyunsaturated fatty acids affect cellular antioxidant defense system in rats with experimental ulcerative colitis induced by trinitrobenzene sulfonic acid. Dig Dis Sci 1998;43:2676-2687.
60. Nieto N, Torres MI, Rios A, Gil A. Dietary polyunsaturated fatty acids improve histological and biochemical alterations in rats with experimental ulcerative colitis. J Nutt 2002;132:11-19.
61. Svegliati-Baroni G, Candelaresi C, Saccomanno S, Ferretti G, Bachetti T, Marzioni M, et al. A model of insulin resistance and nonalcoholic steatohepatitis in rats: role of peroxisome proliferator-activated receptot-{alpha} and n-3 polyunsaturated fatty acid treatment on liver injury. Am J Pathol 2006;169:846-860.
62. Polavarapu R, Spitz DR, Sim JE, Follansbee MH, Obetley LW, Rahemtulla A, et al. Increased lipid peroxidation and impaired antioxidant enzyme function is associated with pathological liver injury in experimental alcoholic liver disease in rats fed diets high in corn oil and fish oil. HEPATOLOGY 1998;27:1317-1323.
63. Aleynik SI, Leo MA, Aleynik MK, Lieber CS. Increased circulating products of lipid peroxidation in patients with alcoholic liver disease. Alcohol Clin Exp Res 1998;22:192-196.
64. Shaw S, Jayatilleke E, Lieber CS. Lipid peroxidation as a mechanism of alcoholic liver injury: role of iron mobilization and microsomal induction. Alcohol 1988;5:135-140.
65. Mottaran E, Stewart SF, Rolla R, Vay D, Cipriani V, Moretti M, et al. Lipid peroxidation contributes to immune reactions associated with alcoholic liver disease. Free Radic Biol Med 2002;32:38-45.
66. Guichardant M, Bacot S, Moliere P, Lagarde M. Hydroxy-alkenals from the peroxidation of n-3 and n-6 fatty acids and urinary metabolites. Prostaglandins Leukot Essent Fatty Acids 2006;75:179-182.
67. Irwin WA, Gaspers LD, Thomas JA. Inhibition of the mitochondrial permeability transition by aldehydes. Biochem Biophys Res Commun 2002;291:215-219.
68. Bacot S, Bernoud-Hubac N, Baddas N, Chantegrel B, Deshayes C, Doutheau A, et al. Covalent binding of hydroxy-alkenals 4-HDDE, 4-HHE, and 4-HNE to ethanolamine phospholipid subclasses. J Lipid Res 2003;44:917-926.
69. George J, Pera N, Phung N, Leclercq I, Yun Hou J, Farrell G. Lipid peroxidation, stellate cell activation and hepatic fibrogenesis in a rat model of chronic steatohepatitis. J Hepatol 2003;39:756-764.
70. Colell A, Garcia-Ruiz C, Miranda M, Ardite E, Mari M, Morales A, et al. Selective glutathione depletion of mitochondria by ethanol sensitizes hepatocytes to tumor necrosis factor. Gastroenterology 1998;115:1541-1551.
71. Nanji AA, Zhao S, Sadtzadeh SM, Dannenberg AJ, Tahan SR, Waxman DJ. 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 1994;18:1280-1285.
72. Nanji AA, Zhao S, Lamb RG, Dannenbetg AJ, Sadrzadeh SM, Waxman DJ. Changes in cytochromes P-450, 2E1, 2B1, and 4A, and phospholipases A and C in the intragastric feeding rat model for alcoholic liver disease: relationship to dietary fats and pathologic liver injury. Alcohol Clin Exp Res 1994;18:902-908.
73. Duplus E, Glorian M, Forest C. Fatty acid regulation of gene transcription. J Biol Chem 2000;275:30749-30752.
74. Zhang W, Ou J, Inagaki Y, Greenwel P, Ramirez F. Synergistic cooperation between Sp1 and Smad3/Smad4 mediates transforming growth factor beta1 stimulation of alpha 2(I)-collagen (COL1A2) transcription. J Biol Chem 2000;275:39237-39245.