Ursodeoxycholyl lysophosphatidylethanolamide improves steatosis and inflammation in murine models of nonalcoholic fatty liver disease

Hepatology

Volumn 55, Issue 5, 2012, Pages 1369-1378

  Pathil, Anita ^a   Mueller, Jan ^a   Warth, Arne ^a   Chamulitrat, Walee ^a   Stremmel, Wolfgang ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYL COENZYME A SYNTHETASE; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; CASPASE 8; CHOLESTEROL; CHOLINE; DIACYLGLYCEROL ACYLTRANSFERASE 1; DIACYLGLYCEROL ACYLTRANSFERASE 2; FATTY ACID SYNTHASE; LACTATE DEHYDROGENASE; LIPID HYDROPEROXIDE; LYSOPHOSPHATIDYLCHOLINE; METHIONINE; MONOCYTE CHEMOTACTIC PROTEIN 1; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; URSODEOXYCHOLIC ACID DERIVATIVE; URSODEOXYCHOLYLLYSOPHOSPHATIDYLETHANOLAMIDE; VASCULAR CELL ADHESION MOLECULE 1;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; BILE ACID SYNTHESIS; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; ENZYME ACTIVATION; ENZYME ACTIVITY; FATTY ACID DESATURATION; GENE EXPRESSION; HEPATITIS; HYPERLIPIDEMIA; LIPID DIET; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID PEROXIDATION; LIPOGENESIS; LIVER HISTOLOGY; LIVER INJURY; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; BIOPSY, NEEDLE; CASPASE 8; DIET; DISEASE MODELS, ANIMAL; DOWN-REGULATION; FATTY LIVER; HEPATITIS; IMMUNOHISTOCHEMISTRY; LIPID PEROXIDATION; LIPOGENESIS; LIVER FUNCTION TESTS; MALE; MICE; MICE, INBRED C57BL; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; SENSITIVITY AND SPECIFICITY; TRANSAMINASES; TRIGLYCERIDES; URSODEOXYCHOLIC ACID;

EID: 84859998884     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25531     Document Type: Article

References (51)

1. Angulo P. Nonalcoholic fatty liver disease. N Engl J Med 2002; 346: 1221-1231.
2. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC, et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. HEPATOLOGY 2004; 40: 1387-1395.
3. Clark JM, Diehl AM. Nonalcoholic fatty liver disease: an underrecognized cause of cryptogenic cirrhosis. JAMA 2003; 289: 3000-3004.
4. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, Cheung O, et al. A lipidomic analysis of nonalcoholic fatty liver disease. HEPATOLOGY 2007; 46: 1081-1090.
5. Li Z, Agellon LB, Vance DE. Phosphatidylcholine homeostasis and liver failure. J Biol Chem 2005; 280: 37798-37802.
6. Treede I, Braun A, Sparla R, Kuhnel M, Giese T, Turner JR, et al. Anti-inflammatory effects of phosphatidylcholine. J Biol Chem 2007; 282: 27155-27164.
7. Oneta CM, Mak KM, Lieber CS. Dilinoleoylphosphatidylcholine selectively modulates lipopolysaccharide-induced Kupffer cell activation. J Lab Clin Med 1999; 134: 466-470.
8. Lieber CS, Weiss DG, Groszmann R, Paronetto F, Schenker S. II. Veterans Affairs Cooperative Study of polyenylphosphatidylcholine in alcoholic liver disease. Alcohol Clin Exp Res 2003; 27: 1765-1772.
9. Chamulitrat W, Burhenne J, Rehlen T, Pathil A, Stremmel W. Bile salt-phospholipid conjugate ursodeoxycholyl lysophosphatidylethanolamide as a hepatoprotective agent. HEPATOLOGY 2009; 50: 143-154.
10. Fiorucci S, Mencarelli A, Palazzetti B, Del Soldato P, Morelli A, Ignarro LJ. An NO derivative of ursodeoxycholic acid protects against Fas-mediated liver injury by inhibiting caspase activity. Proc Natl Acad Sci U S A 2001; 98: 2652-2657.
11. Goto M, Okamoto Y, Yamamoto M, Aki H. Anti-inflammatory effects of 5-aminosalicylic acid conjugates with chenodeoxycholic acid and ursodeoxycholic acid on carrageenan-induced colitis in guinea-pigs. J Pharm Pharmacol 2001; 53: 1711-1720.
12. Pathil A, Warth A, Chamulitrat W, Stremmel W. The synthetic bile acid-phospholipid conjugate ursodeoxycholyl lysophosphatidylethanolamide suppresses TNFalpha-induced liver injury. J Hepatol 2011; 54: 674-684.
13. Kudo H, Takahara T, Yata Y, Kawai K, Zhang W, Sugiyama T. Lipopolysaccharide triggered TNF-alpha-induced hepatocyte apoptosis in a murine non-alcoholic steatohepatitis model. J Hepatol 2009; 51: 168-175.
14. Tomita K, Tamiya G, Ando S, Ohsumi K, Chiyo T, Mizutani A, et al. Tumour necrosis factor alpha signalling through activation of Kupffer cells plays an essential role in liver fibrosis of non-alcoholic steatohepatitis in mice. Gut 2006; 55: 415-424.
15. 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.
16. Brunt EM, Janney CG, Di Bisceglie AM, Neuschwander-Tetri BA, Bacon BR. Nonalcoholic steatohepatitis: a proposal for grading and staging the histological lesions. Am J Gastroenterol 1999; 94: 2467-2474.
17. Folch J, Lees M, Sloane Stanley GH. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 1957; 226: 497-509.
18. Kishimoto T, Soda Y, Matsuyama Y, Mizuno K. An enzymatic assay for lysophosphatidylcholine concentration in human serum and plasma. Clin Biochem 2002; 35: 411-416.
19. Leuschner UF, Lindenthal B, Herrmann G, Arnold JC, Rossle M, Cordes HJ, et al. High-dose ursodeoxycholic acid therapy for nonalcoholic steatohepatitis: a double-blind, randomized, placebo-controlled trial. HEPATOLOGY 2010; 52: 472-479.
20. Ratziu V, de Ledinghen V, Oberti F, Mathurin P, Wartelle-Bladou C, Renou C, et al. A randomized controlled trial of high-dose ursodesoxycholic acid for nonalcoholic steatohepatitis. J Hepatol 2011; 54: 1011-1019.
21. Lindor KD, Kowdley KV, Heathcote EJ, Harrison ME, Jorgensen R, Angulo P, et al. Ursodeoxycholic acid for treatment of nonalcoholic steatohepatitis: results of a randomized trial. HEPATOLOGY 2004; 39: 770-778.
22. Rizki G, Arnaboldi L, Gabrielli B, Yan J, Lee GS, Ng RK, et al. Mice fed a lipogenic methionine-choline-deficient diet develop hypermetabolism coincident with hepatic suppression of SCD-1. J Lipid Res 2006; 47: 2280-2290.
23. Ito M, Suzuki J, Tsujioka S, Sasaki M, Gomori A, Shirakura T, et al. Longitudinal analysis of murine steatohepatitis model induced by chronic exposure to high-fat diet. Hepatol Res 2007; 37: 50-57.
24. Haukeland JW, Damas JK, Konopski Z, Loberg EM, Haaland T, Goverud I, et al. Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2. J Hepatol 2006; 44: 1167-1174.
25. Clement S, Juge-Aubry C, Sgroi A, Conzelmann S, Pazienza V, Pittet-Cuenod B, et al. Monocyte chemoattractant protein-1 secreted by adipose tissue induces direct lipid accumulation in hepatocytes. HEPATOLOGY 2008; 48: 799-807.
26. Weisberg SP, Hunter D, Huber R, Lemieux J, Slaymaker S, Vaddi K, et al. CCR2 modulates inflammatory and metabolic effects of high-fat feeding. J Clin Invest 2006; 116: 115-124.
27. Zhang W, Kudo H, Kawai K, Fujisaka S, Usui I, Sugiyama T, et al. Tumor necrosis factor-alpha accelerates apoptosis of steatotic hepatocytes from a murine model of non-alcoholic fatty liver disease. Biochem Biophys Res Commun 2010; 391: 1731-1736.
28. Marra F, DeFranco R, Grappone C, Milani S, Pastacaldi S, Pinzani M, et al. Increased expression of monocyte chemotactic protein-1 during active hepatic fibrogenesis: correlation with monocyte infiltration. Am J Pathol 1998; 152: 423-430.
29. Marra F, Romanelli RG, Giannini C, Failli P, Pastacaldi S, Arrighi MC, et al. Monocyte chemotactic protein-1 as a chemoattractant for human hepatic stellate cells. HEPATOLOGY 1999; 29: 140-148.
30. Wilensky RL, Shi Y, Mohler ER, 3rd, Hamamdzic D, Burgert ME, Li J, et al. Inhibition of lipoprotein-associated phospholipase A2 reduces complex coronary atherosclerotic plaque development. Nat Med 2008; 14: 1059-1066.
31. Zalewski A, Macphee C. Role of lipoprotein-associated phospholipase A2 in atherosclerosis: biology, epidemiology, and possible therapeutic target. Arterioscler Thromb Vasc Biol 2005; 25: 923-931.
32. Lin MK, Farewell V, Vadas P, Bookman AA, Keystone EC, Pruzanski W. Secretory phospholipase A2 as an index of disease activity in rheumatoid arthritis. Prospective double blind study of 212 patients. J Rheumatol 1996; 23: 1162-1166.
33. Han MS, Park SY, Shinzawa K, Kim S, Chung KW, Lee JH, et al. Lysophosphatidylcholine as a death effector in the lipoapoptosis of hepatocytes. J Lipid Res 2008; 49: 84-97.
34. Kalous M, Rauchova H, Drahota Z. The effect of lysophosphatidylcholine on the activity of various mitochondrial enzymes. Biochim Biophys Acta 1992; 1098: 167-171.
35. Basanez G, Sharpe JC, Galanis J, Brandt TB, Hardwick JM, Zimmerberg J. Bax-type apoptotic proteins porate pure lipid bilayers through a mechanism sensitive to intrinsic monolayer curvature. J Biol Chem 2002; 277: 49360-49365.
36. Gubern A, Casas J, Barcelo-Torns M, Barneda D, de la Rosa X, Masgrau R, et al. Group IVA phospholipase A2 is necessary for the biogenesis of lipid droplets. J Biol Chem 2008; 283: 27369-27382.
37. Pessayre D, Fromenty B, Mansouri A. Mitochondrial injury in steatohepatitis. Eur J Gastroenterol Hepatol 2004; 16: 1095-1105.
38. Leclercq IA, Farrell GC, Field J, Bell DR, Gonzalez FJ, Robertson GR. CYP2E1 and CYP4A as microsomal catalysts of lipid peroxides in murine nonalcoholic steatohepatitis. J Clin Invest 2000; 105: 1067-1075.
39. Kohjima M, Enjoji M, Higuchi N, Kato M, Kotoh K, Yoshimoto T, et al. Re-evaluation of fatty acid metabolism-related gene expression in nonalcoholic fatty liver disease. Int J Mol Med 2007; 20: 351-358.
40. Mitsuyoshi H, Yasui K, Harano Y, Endo M, Tsuji K, Minami M, et al. Analysis of hepatic genes involved in the metabolism of fatty acids and iron in nonalcoholic fatty liver disease. Hepatol Res 2009; 39: 366-373.
41. Donnelly KL, Smith CI, Schwarzenberg SJ, Jessurun J, Boldt MD, Parks EJ. Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease. J Clin Invest 2005; 115: 1343-1351.
42. Collins JM, Neville MJ, Hoppa MB, Frayn KN. De novo lipogenesis and stearoyl-CoA desaturase are coordinately regulated in the human adipocyte and protect against palmitate-induced cell injury. J Biol Chem 2010; 285: 6044-6052.
43. Araya J, Rodrigo R, Videla LA, Thielemann L, Orellana M, Pettinelli P, et al. Increase in long-chain polyunsaturated fatty acid n - 6/n - 3 ratio in relation to hepatic steatosis in patients with non-alcoholic fatty liver disease. Clin Sci (Lond) 2004; 106: 635-643.
44. Puri P, Wiest MM, Cheung O, Mirshahi F, Sargeant C, Min HK, et al. The plasma lipidomic signature of nonalcoholic steatohepatitis. HEPATOLOGY 2009; 50: 1827-1838.
45. Di Marzo V. Arachidonic acid and eicosanoids as targets and effectors in second messenger interactions. Prostaglandins Leukot Essent Fatty Acids 1995; 53: 239-254.
46. Needleman P, Turk J, Jakschik BA, Morrison AR, Lefkowith JB. Arachidonic acid metabolism. Annu Rev Biochem 1986; 55: 69-102.
47. Day CP, James OF. Steatohepatitis: a tale of two "hits"? Gastroenterology 1998; 114: 842-845.
48. Choi SS, Diehl AM. Hepatic triglyceride synthesis and nonalcoholic fatty liver disease. Curr Opin Lipidol 2008; 19: 295-300.
49. Garbarino J, Sturley SL. Saturated with fat: new perspectives on lipotoxicity. Curr Opin Clin Nutr Metab Care 2009; 12: 110-116.
50. Schenk S, Saberi M, Olefsky JM. Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 2008; 118: 2992-3002.
51. Yamaguchi K, Yang L, McCall S, Huang J, Yu XX, Pandey SK, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. HEPATOLOGY 2007; 45: 1366-1374.