The Type of Dietary Fat Modulates Intestinal Tight Junction Integrity, Gut Permeability, and Hepatic Toll-Like Receptor Expression in a Mouse Model of Alcoholic Liver Disease

Alcoholism: Clinical and Experimental Research

Volumn 36, Issue 5, 2012, Pages 835-846

  Kirpich, Irina A ^a,b   Feng, Wenke ^a,b   Wang, Yuhua ^a,c   Liu, Yanlong ^a,d   Barker, David F ^a,b   Barve, Shirish S ^a,b   Mcclain, Craig J ^a,b,e  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c JILIN AGRICULTURAL UNIVERSITY   (China)

^d WENZHOU MEDICAL UNIVERSITY   (China)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Alcoholic Liver Disease; Gut Permeability and Intestinal TJ; Liver TLRs; Saturated and Unsaturated Fat

Indexed keywords

ALANINE AMINOTRANSFERASE; CYTOCHROME P450 2E1; ENDOTOXIN; MONOCYTE CHEMOTACTIC PROTEIN 1; SATURATED FATTY ACID; TOLL LIKE RECEPTOR; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TOLL LIKE RECEPTOR 9; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNSATURATED FATTY ACID;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ALCOHOL CONSUMPTION; ALCOHOL LIVER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; BODY COMPOSITION; BODY WEIGHT; CONTROLLED STUDY; DOWN REGULATION; FAT INTAKE; FATTY LIVER; GENE EXPRESSION; INTESTINE MUCOSA PERMEABILITY; INTESTINE TIGHT JUNCTION; LIVER HISTOLOGY; LIVER INJURY; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TIGHT JUNCTION; UPREGULATION;

ANIMALS; BODY COMPOSITION; BODY WEIGHT; DIETARY FATS, UNSATURATED; DISEASE MODELS, ANIMAL; EATING; ENDOTOXINS; ETHANOL; GASTROINTESTINAL TRACT; LIVER; LIVER DISEASES, ALCOHOLIC; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; OXIDATIVE STRESS; PERMEABILITY; TIGHT JUNCTIONS; TOLL-LIKE RECEPTORS; UP-REGULATION;

ANIMALIA; MUS; ZEA MAYS;

EID: 84860433691     PISSN: 01456008     EISSN: 15300277     Source Type: Journal    
DOI: 10.1111/j.1530-0277.2011.01673.x     Document Type: Article

References (52)

1. Amet Y, Adas F, 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. Amin PB, Diebel LN, Liberati DM (2009) Dose-dependent effects of ethanol and E. coli on gut permeability and cytokine production. J Surg Res 157:187-192.
3. Banan A, Choudhary S, Zhang Y, Fields JZ, Keshavarzian A (1999) Ethanol-induced barrier dysfunction and its prevention by growth factors in human intestinal monolayers: evidence for oxidative and cytoskeletal mechanisms. J Pharmacol Exp Ther 291:1075-1085.
4. Banan A, Fields JZ, Decker H, Zhang Y, Keshavarzian A (2000) Nitric oxide and its metabolites mediate ethanol-induced microtubule disruption and intestinal barrier dysfunction. J Pharmacol Exp Ther 294:997-1008.
5. Bode C, Kolepke R, Schafer K, Bode JC (1993) Breath hydrogen excretion in patients with alcoholic liver disease-evidence of small intestinal bacterial overgrowth. Z Gastroenterol 31:3-7.
6. Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, Burcelin R (2008) Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57:1470-1481.
7. Farhadi A, Keshavarzian A, Ranjbaran Z, Fields JZ, Banan A (2006) The role of protein kinase C isoforms in modulating injury and repair of the intestinal barrier. J Pharmacol Exp Ther 316:1-7.
8. Fukui H, Brauner B, Bode JC, Bode C (1991) Plasma endotoxin concentrations in patients with alcoholic and non-alcoholic liver disease: reevaluation with an improved chromogenic assay. J Hepatol 12:162-169.
9. Ghoshal S, Witta J, Zhong J, de Villiers W, Eckhardt E (2009) Chylomicrons promote intestinal absorption of lipopolysaccharides. J Lipid Res 50:90-97.
10. Gustot T, Lemmers A, Moreno C, Nagy N, Quertinmont E, Nicaise C, Franchimont D, Louis H, Deviere J, Le Moine O (2006) Differential liver sensitization to toll-like receptor pathways in mice with alcoholic fatty liver. Hepatology 43:989-1000.
11. Hennig B, Lei W, Arzuaga X, Ghosh DD, Saraswathi V, Toborek M (2006) Linoleic acid induces proinflammatory events in vascular endothelial cells via activation of PI3K/Akt and ERK1/2 signaling. J Nutr Biochem 17:766-772.
12. Hritz I, Mandrekar P, Velayudham A, Catalano D, Dolganiuc A, Kodys K, Kurt-Jones E, Szabo G (2008) The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 48:1224-1231.
13. Jarvelainen HA, Fang C, Ingelman-Sundberg M, Lukkari TA, Sippel H, Lindros KO (2000) Kupffer cell inactivation alleviates ethanol-induced steatosis and CYP2E1 induction but not inflammatory responses in rat liver. J Hepatol 32:900-910.
14. Keshavarzian A, Fields JZ, Vaeth J, Holmes EW (1994) The differing effects of acute and chronic alcohol on gastric and intestinal permeability. Am J Gastroenterol 89:2205-2211.
15. Keshavarzian A, Jacyno M, Urban G, Winship D, Fields JZ (1996) The role of nitric oxide in ethanol-induced gastrointestinal dysfunction. Alcohol Clin Exp Res 20:1618-1624.
16. Kirpich IA, Gobejishvili LN, Homme MB, Waigel S, Cave M, Arteel G, Barve SS, McClain CJ, Deaciuc IV (2011) Integrated hepatic transcriptome and proteome analysis of mice with high-fat diet-induced nonalcoholic fatty liver disease. J Nutr Biochem 22:38-45.
17. Kono H, Enomoto N, Connor HD, Wheeler MD, Bradford BU, Rivera CA, Kadiiska MB, Mason RP, Thurman RG (2000) Medium-chain triglycerides inhibit free radical formation and TNF-alpha production in rats given enteral ethanol. Am J Physiol Gastrointest Liver Physiol 278:G467-G476.
18. Kono H, Fujii H, Asakawa M, Yamamoto M, Matsuda M, Maki A, Matsumoto Y (2003) Protective effects of medium-chain triglycerides on the liver and gut in rats administered endotoxin. Ann Surg 237:246-255.
19. Lieber CS, Cao Q, DeCarli LM, Leo MA, Mak KM, Ponomarenko A, Ren C, Wang X (2007) Role of medium-chain triglycerides in the alcohol-mediated cytochrome P450 2E1 induction of mitochondria. Alcohol Clin Exp Res 31:1660-1668.
20. Lu Y, Wang X, Cederbaum AI (2005) Lipopolysaccharide-induced liver injury in rats treated with the CYP2E1 inducer pyrazole. Am J Physiol Gastrointest Liver Physiol 289:G308-G319.
21. Lu Y, Zhuge J, Wang X, Bai J, Cederbaum AI (2008) Cytochrome P450 2E1 contributes to ethanol-induced fatty liver in mice. Hepatology 47:1483-1494.
22. Ma TY, Iwamoto GK, Hoa NT, Akotia V, Pedram A, Boivin MA, Said HM (2004) TNF-alpha-induced increase in intestinal epithelial tight junction permeability requires NF-kappa B activation. Am J Physiol Gastrointest Liver Physiol 286:G367-G376.
23. Ma TY, Nguyen D, Bui V, Nguyen H, Hoa N (1999) Ethanol modulation of intestinal epithelial tight junction barrier. Am J Physiol 276:G965-G974.
24. Mandrekar P, Szabo G (2009) Signalling pathways in alcohol-induced liver inflammation. J Hepatol 50:1258-1266.
25. Mencin A, Kluwe J, Schwabe RF (2009) Toll-like receptors as targets in chronic liver diseases. Gut 58:704-720.
26. Nanji AA (2004) Role of different dietary fatty acids in the pathogenesis of experimental alcoholic liver disease. Alcohol 34:21-25.
27. Nanji AA, French SW (1986) Dietary factors and alcoholic cirrhosis. Alcohol Clin Exp Res 10:271-273.
28. Nanji AA, French SW (1989) Dietary linoleic acid is required for development of experimentally induced alcoholic liver injury. Life Sci 44:223-227.
29. Nanji AA, Griniuviene B, Sadrzadeh SM, Levitsky S, McCully JD (1995a) Effect of type of dietary fat and ethanol on antioxidant enzyme mRNA induction in rat liver. J Lipid Res 36:736-744.
30. Nanji AA, Jokelainen K, Tipoe GL, Rahemtulla A, Dannenberg AJ (2001) Dietary saturated fatty acids reverse inflammatory and fibrotic changes in rat liver despite continued ethanol administration. J Pharmacol Exp Ther 299:638-644.
31. Nanji AA, Khettry U, Sadrzadeh SM, Yamanaka T (1993) Severity of liver injury in experimental alcoholic liver disease. Correlation with plasma endotoxin, prostaglandin E2, leukotriene B4, and thromboxane B2. Am J Pathol 142:367-373.
32. Nanji AA, Sadrzadeh SM, Yang EK, Fogt F, Meydani M, Dannenberg AJ (1995b) Dietary saturated fatty acids: a novel treatment for alcoholic liver disease. Gastroenterology 109:547-554.
33. Nanji AA, Zhao S, Lamb RG, Dannenberg AJ, Sadrzadeh SM, Waxman DJ (1994a) 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 18:902-908.
34. Nanji AA, Zhao S, Sadrzadeh SM, Dannenberg AJ, Tahan SR, 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.
35. Parlesak A, Schafer C, Schutz T, Bode JC, Bode C (2000) Increased intestinal permeability to macromolecules and endotoxemia in patients with chronic alcohol abuse in different stages of alcohol-induced liver disease. J Hepatol 32:742-747.
36. Petrasek J, Mandrekar P, Szabo G (2010) Toll-like receptors in the pathogenesis of alcoholic liver disease. Gastroenterol Res Pract doi: 10.1155/2010/710381 [pii: 710381, Epub ahead of print].
37. Purohit V, Bode JC, Bode C, Brenner DA, Choudhry MA, Hamilton F, Kang YJ, Keshavarzian A, Rao R, Sartor RB, Swanson C, Turner JR (2008) Alcohol, intestinal bacterial growth, intestinal permeability to endotoxin, and medical consequences: summary of a symposium. Alcohol 42:349-361.
38. Rao RK (1998) Acetaldehyde-induced increase in paracellular permeability in Caco-2 cell monolayer. Alcohol Clin Exp Res 22:1724-1730.
39. Rao RK, Seth A, Sheth P (2004) Recent advances in alcoholic liver disease I. Role of intestinal permeability and endotoxemia in alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol 286:G881-G884.
40. Ronis MJ, Korourian S, Zipperman M, Hakkak R, Badger TM (2004) Dietary saturated fat reduces alcoholic hepatotoxicity in rats by altering fatty acid metabolism and membrane composition. J Nutr 134:904-912.
41. Rozen S, Skaletsky HJ (2000) Primer3 on the WWW for general users and for biologist programmers, in Bioinformatics Methods and Protocols: Methods in Molecular Biology (Krawetz S, Misener S eds), pp. 365-386. Humana Press, Totowa, NJ.
42. Rusyn I, Bradham CA, Cohn L, Schoonhoven R, Swenberg JA, Brenner DA, Thurman RG (1999) Corn oil rapidly activates nuclear factor-kappaB in hepatic Kupffer cells by oxidant-dependent mechanisms. Carcinogenesis 20:2095-2100.
43. Takahashi H, Johansson I, French SW, Ingelman-Sundberg M (1992) Effects of dietary fat composition on activities of the microsomal ethanol oxidizing system and ethanol-inducible cytochrome P450 (CYP2E1) in the liver of rats chronically fed ethanol. Pharmacol Toxicol 70:347-351.
44. Tang Y, Banan A, Forsyth CB, Fields JZ, Lau CK, Zhang LJ, Keshavarzian A (2008) Effect of alcohol on miR-212 expression in intestinal epithelial cells and its potential role in alcoholic liver disease. Alcohol Clin Exp Res 32:355-364.
45. Tang Y, Forsyth CB, Farhadi A, Rangan J, Jakate S, Shaikh M, Banan A, Fields JZ, Keshavarzian A (2009) Nitric oxide-mediated intestinal injury is required for alcohol-induced gut leakiness and liver damage. Alcohol Clin Exp Res 33:1220-1230.
46. Urbaschek R, McCuskey RS, Rudi V, Becker KP, Stickel F, Urbaschek B, Seitz HK (2001) Endotoxin, endotoxin-neutralizing-capacity, sCD14, sICAM-1, and cytokines in patients with various degrees of alcoholic liver disease. Alcohol Clin Exp Res 25:261-268.
47. Ye D, Ma I, Ma TY (2006) Molecular mechanism of tumor necrosis factor-alpha modulation of intestinal epithelial tight junction barrier. Am J Physiol Gastrointest Liver Physiol 290:G496-G504.
48. Yoo JS, Ning SM, Pantuck CB, Pantuck EJ, Yang CS (1991) Regulation of hepatic microsomal cytochrome P450IIE1 level by dietary lipids and carbohydrates in rats. J Nutr 121:959-965.
49. You M, Cao Q, Liang X, Ajmo JM, Ness GC (2008) Mammalian sirtuin 1 is involved in the protective action of dietary saturated fat against alcoholic fatty liver in mice. J Nutr 138:497-501.
50. You M, Considine RV, Leone TC, Kelly DP, Crabb DW (2005) Role of adiponectin in the protective action of dietary saturated fat against alcoholic fatty liver in mice. Hepatology 42:568-577.
51. Zarember KA, Godowski PJ (2002) Tissue expression of human Toll-like receptors and differential regulation of Toll-like receptor mRNAs in leukocytes in response to microbes, their products, and cytokines. J Immunol 168:554-561.
52. Zhong W, McClain CJ, Cave M, Kang YJ, Zhou Z (2010) The role of zinc deficiency in alcohol-induced intestinal barrier dysfunction. Am J Physiol Gastrointest Liver Physiol 298:G625-G633.