Ursodeoxycholyl lysophosphatidylethanolamide inhibits lipoapoptosis by shifting fatty acid pools toward monosaturated and polyunsaturated fatty acids in mouse hepatocytes

Molecular Pharmacology

Volumn 84, Issue 5, 2013, Pages 696-709

  Chamulitrat, Walee ^a   Liebisch, Gerhard ^b   Xu, Weihong ^c   Gan Schreier, Hongying ^a   Pathil, Anita ^a   Schmitz, Gerd ^b   Stremmel, Wolfgang ^a  

^a Gastroenterology and Infectious Diseases   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c HANGZHOU FIRST PEOPLE'S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DOCOSAHEXAENOIC ACID; DOCOSAPENTAENOIC ACID; LIVER PROTECTIVE AGENT; MONOUNSATURATED FATTY ACID; OLEIC ACID; PALMITIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLSERINE; PHOSPHOLIPID; POLYUNSATURATED FATTY ACID; UNCLASSIFIED DRUG; URSODEOXYCHOLYL LYSOPHOSPHATIDYLETHANOLAMIDE;

ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CATALYSIS; CELL PROTECTION; CONTROLLED STUDY; LIPID METABOLISM; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

ANIMALS; APOPTOSIS; CYCLIC AMP; CYTOPROTECTION; FATTY ACIDS; HEPATOCYTES; LYSOPHOSPHOLIPIDS; MALE; MICE; MICE, INBRED C57BL; STEAROYL-COA DESATURASE; URSODEOXYCHOLIC ACID;

EID: 84886049979     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.113.088039     Document Type: Article

References (50)

1. Balakrishnan A, Wring SA, Coop A, and Polli JE (2006) Influence of charge and steric bulk in the C-24 region on the interaction of bile acids with human apical sodiumdependent bile acid transporter. Mol Pharm 3:282-292. (Pubitemid 44021434)
2. Balogh G, Péter M, Liebisch G, Horváth I, Török Z, Nagy E, Maslyanko A, Benko S, Schmitz G, and Harwood JL et al. (2010) Lipidomics reveals membrane lipid remodelling and release of potential lipid mediators during early stress responses in a murine melanoma cell line. Biochim Biophys Acta 1801:1036-1047.
3. Beraza N, Ofner-Ziegenfuss L, Ehedego H, Boekschoten M, Bischoff SC, Mueller M, Trauner M, and Trautwein C (2011) Nor-ursodeoxycholic acid reverses hepatocytespecific nemo-dependent steatohepatitis. Gut 60:387-396.
4. Briz O, Serrano MA, Rebollo N, Hagenbuch B, Meier PJ, Koepsell H, and Marin JJ (2002) Carriers involved in targeting the cytostatic bile acid-cisplatin derivatives cis-diammine-chloro-cholylglycinate-platinum (II) and cis-diammine-bisursodeoxycholateplatinum (II) toward liver cells. Mol Pharmacol 61:853-860. (Pubitemid 34273165)
5. Cantrel C, Zachowski A, and Geny B (2009) Over-expression of the anti-apoptotic protein Bcl-2 affects membrane lipid composition in HL-60 cells. Lipids 44:499-509.
6. Chamulitrat W, Burhenne J, Rehlen T, Pathil A, and Stremmel W (2009) Bile saltphospholipid conjugate ursodeoxycholyl lysophosphatidylethanolamide as a hepatoprotective agent. Hepatology 50:143-154.
7. Chamulitrat W, Zhang W, Xu W, Pathil A, Setchell K, and Stremmel W (2012) Hepatoprotectant ursodeoxycholyl lysophosphatidylethanolamide increasing phosphatidylcholine levels as a potential therapy of acute liver injury. Front Physiol 3:24-32.
8. Collins JM, Neville MJ, Hoppa MB, and Frayn KN (2010) De novo lipogenesis and stearoyl-CoA desaturase are coordinately regulated in the human adipocyte and protect against palmitate-induced cell injury. J Biol Chem 285:6044-6052.
9. Dent P, Fang Y, Gupta S, Studer E, Mitchell C, Spiegel S, and Hylemon PB (2005) Conjugated bile acids promote ERK1/2 and AKT activation via a pertussis toxin-sensitive mechanism in murine and human hepatocytes. Hepatology 42:1291-1299. (Pubitemid 43260031)
10. Depner CM, Philbrick KA, and Jump DB (2013) Docosahexaenoic acid attenuates hepatic inflammation, oxidative stress, and fibrosis without decreasing hepatosteatosis in a Ldlr (-/-) mouse model of western diet-induced nonalcoholic steatohepatitis. J Nutr 143:315-323.
11. Diehl AM (1999) Nonalcoholic steatohepatitis. Semin Liver Dis 19:221-229.
12. Ecker J, Scherer M, Schmitz G, and Liebisch G (2012) A rapid GC-MS method for quantification of positional and geometric isomers of fatty acid methyl esters. J Chromatogr B Analyt Technol Biomed Life Sci 897:98-104.
13. Fickert P, Wagner M, Marschall HU, Fuchsbichler A, Zollner G, Tsybrovskyy O, Zatloukal K, Liu J, Waalkes MP, and Cover C, et al. (2006) 24-norUrsodeoxycholic acid is superior to ursodeoxycholic acid in the treatment of sclerosing cholangitis in Mdr2 (Abcb4) knockout mice. Gastroenterology 130:465-481. (Pubitemid 43202044)
14. Goto M, Okamoto Y, Yamamoto M, and Aki H (2001) Anti-inflammatory effects of 5-aminosalicylic acid conjugates with chenodeoxycholic acid and ursodeoxycholic acid on carrageenan-induced colitis in guinea-pigs. J Pharm Pharmacol 53:1711-1720. (Pubitemid 34044260)
15. Green CD, Ozguden-Akkoc CG, Wang Y, Jump DB, and Olson LK (2010) Role of fatty acid elongases in determination of De novo synthesized monounsaturated fatty acid species. J Lipid Res 51:1871-1877.
16. Hall D, Poussin C, Velagapudi VR, Empsen C, Joffraud M, Beckmann JS, Geerts AE, Ravussin Y, Ibberson M, and Oresic M et al. (2010) Peroxisomal and microsomal lipid pathways associated with resistance to hepatic steatosis and reduced proinflammatory state. J Biol Chem 285:31011-31023.
17. Hutchinson DS, Summers RJ, and Bengtsson T (2008) Regulation of AMP-activated protein kinase activity by G-protein coupled receptors: potential utility in treatment of diabetes and heart disease. Pharmacol Ther 119:291-310.
18. Imarisio C, Alchera E, Sutti S, Valente G, Boccafoschi F, Albano E, and Carini R (2012) Adenosine A (2a) receptor stimulation prevents hepatocyte lipotoxicity and non-alcoholic steatohepatitis (NASH) in rats. Clin Sci (Lond) 123:323-332.
19. Jump DB, Botolin D, Wang Y, Xu J, Demeure O, and Christian B (2008) Docosahexaenoic acid (DHA) and hepatic gene transcription. Chem Phys Lipids 153:3-13.
20. Jung UJ, Millman PN, Tall AR, and Deckelbaum RJ (2011) n-3 fatty acids ameliorate hepatic steatosis and dysfunction after LXR agonist ingestion in mice. Biochim Biophys Acta 1811:491-497.
21. Kim HY, Akbar M, and Kim YS (2010) Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid. Prostaglandins Leukot Essent Fatty Acids 82:165-172.
22. Kwon G, Pappan KL, Marshall CA, Schaffer JE, and McDaniel ML (2004) cAMP dose-dependently prevents palmitate-induced apoptosis by both protein kinase A- and cAMP-guanine nucleotide exchange factor-dependent pathways in beta-cells. J Biol Chem 279:8938-8945. (Pubitemid 38295955)
23. Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, and Vance DE (2006) The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab 3:321-331.
24. Li ZZ, Berk M, McIntyre TM, and Feldstein AE (2009) Hepatic lipid partitioning and liver damage in nonalcoholic fatty liver disease: role of stearoyl-CoA desaturase. J Biol Chem 284:5637-5644.
25. Liebisch G, Lieser B, Rathenberg J, Drobnik W, and Schmitz G (2004) Highthroughput quantification of phosphatidylcholine and sphingomyelin by electrospray ionization tandem mass spectrometry coupled with isotope correction algorithm. Biochim Biophys Acta 1686:108-117. (Pubitemid 39446883)
26. Listenberger LL, Han X, Lewis SE, Cases S, Farese RV, Jr, Ory DS, and Schaffer JE (2003) Triglyceride accumulation protects against fatty acid-induced lipotoxicity. Proc Natl Acad Sci USA 100:3077-3082. (Pubitemid 36356542)
27. Maeda K, Kambara M, Tian Y, Hofmann AF, and Sugiyama Y (2006) Uptake of ursodeoxycholate and its conjugates by human hepatocytes: role of Na (1) - taurocholate cotransporting polypeptide (NTCP), organic anion transporting polypeptide (OATP) 1B1 (OATP-C), and oatp1B3 (OATP8). Mol Pharm 3:70-77. (Pubitemid 43331753)
28. Miller SD, Greene CM, McLean CM, Lawless MW, Taggart CC, O'Neill SJ, and McElvaney NG (2007) Tauroursodeoxycholic acid inhibits apoptosis induced by Z alpha-1 antitrypsin via inhibition of Bad. Hepatology 46:496-503. (Pubitemid 47344785)
29. Misra UK and Pizzo SV (2005) Coordinate regulation of forskolin-induced cellular proliferation in macrophages by protein kinase A/cAMP-response element-binding protein (CREB) and Epac1-Rap1 signaling: effects of silencing CREB gene expression on Akt activation. J Biol Chem 280:38276-38289. (Pubitemid 43853725)
30. Moon YA, Hammer RE, and Horton JD (2009) Deletion of ELOVL5 leads to fatty liver through activation of SREBP-1c in mice. J Lipid Res 50:412-423.
31. Niebergall LJ, Jacobs RL, Chaba T, and Vance DE (2011) Phosphatidylcholine protects against steatosis in mice but not non-alcoholic steatohepatitis. Biochim Biophys Acta 1811:1177-1185.
32. Nishina A, Kimura H, Sekiguchi A, Fukumoto RH, Nakajima S, and Furukawa S (2006) Lysophosphatidylethanolamine in Grifola frondosa as a neurotrophic activator via activation of MAPK. J Lipid Res 47:1434-1443. (Pubitemid 44079897)
33. Nobili V, Bedogni G, Alisi A, Pietrobattista A, Risé P, Galli C, and Agostoni C (2011) Docosahexaenoic acid supplementation decreases liver fat content in children with non-alcoholic fatty liver disease: double-blind randomised controlled clinical trial. Arch Dis Child 96:350-353.
34. Ntambi JM (1999) Regulation of stearoyl-CoA desaturase by polyunsaturated fatty acids and cholesterol. J Lipid Res 40:1549-1558. (Pubitemid 29418696)
35. Pathil A, Mueller J, Warth A, Chamulitrat W, and Stremmel W (2012) Ursodeoxycholyl lysophosphatidylethanolamide improves steatosis and inflammation in murine models of nonalcoholic fatty liver disease. Hepatology 55:1369-1378.
36. Pathil A, Warth A, Chamulitrat W, and Stremmel W (2011) The synthetic bile acidphospholipid conjugate ursodeoxycholyl lysophosphatidylethanolamide suppresses TNFa-induced liver injury. J Hepatol 54:674-684.
37. Pellicciari R, Costantino G, Camaioni E, Sadeghpour BM, Entrena A, Willson TM, Fiorucci S, Clerici C, and Gioiello A (2004) Bile acid derivatives as ligands of the farnesoid X receptor: synthesis, evaluation, and structure-activity relationship of a series of body and side chain modified analogues of chenodeoxycholic acid. J Med Chem 47:4559-4569. (Pubitemid 39096842)
38. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, Cheung O, Sargeant C, Contos MJ, and Sanyal AJ (2007) A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 46:1081-1090. (Pubitemid 350144772)
39. Rahman SM, Qadri I, Janssen RC, and Friedman JE (2009) Fenofibrate and PBA prevent fatty acid-induced loss of adiponectin receptor and pAMPK in human hepatoma cells and in hepatitis C virus-induced steatosis. J Lipid Res 50:2193-2202.
40. Ratziu V, Caldwell S, and Neuschwander-Tetri BA (2010) Therapeutic trials in nonalcoholic steatohepatitis: insulin sensitizers and related methodological issues. Hepatology 52:2206-2215.
41. Ratziu V, De Ledinghen V, Oberti F, Mathurin P, Wartelle-Bladou C, Renou C, Sogni P, Maynard M, Larrey D, and Serfaty L et al.; FRESGUN (2011) A randomized controlled trial of high-dose ursodesoxycholic acid for nonalcoholic steatohepatitis. J Hepatol 54:1011-1019.
42. Rodrigues CM, Fan G, Wong PY, Kren BT, and Steer CJ (1998) Ursodeoxycholic acid may inhibit deoxycholic acid-induced apoptosis by modulating mitochondrial transmembrane potential and reactive oxygen species production. Mol Med 4:165-178. (Pubitemid 28223968)
43. Satapathy SK and Sanyal AJ (2010) Novel treatment modalities for nonalcoholic steatohepatitis. Trends Endocrinol Metab 21:668-675.
44. Stubbs CD and Smith AD (1984) The modification of mammalian membrane polyunsaturated fatty acid composition in relation to membrane fluidity and function. Biochim Biophys Acta 779:89-137. (Pubitemid 14199577)
45. Studer E, Zhou X, Zhao R, Wang Y, Takabe K, Nagahashi M, Pandak WM, Dent P, Spiegel S, and Shi R et al. (2012) Conjugated bile acids activate the sphingosine-1-phosphate receptor 2 in primary rodent hepatocytes. Hepatology 55:267-276.
46. Tsochatzis EA, Gurusamy KS, Gluud C, and Burroughs AK (2009) Ursodeoxycholic acid and primary biliary cirrhosis: EASL and AASLD guidelines. J Hepatol 51:1084-1085, author reply 1085-1086.
47. Wallner S and Schmitz G (2011) Plasmalogens the neglected regulatory and scavenging lipid species. Chem Phys Lipids 164:573-589.
48. Webster CR and Anwer MS (1998) Cyclic adenosine monophosphate-mediated protection against bile acid-induced apoptosis in cultured rat hepatocytes. Hepatology 27:1324-1331. (Pubitemid 28227860)
49. Yamaguchi K, Yang L, McCall S, Huang J, Yu XX, Pandey SK, Bhanot S, Monia BP, Li YX, and Diehl AM (2007) Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 45:1366-1374. (Pubitemid 46918320)
50. Zhang LX, Liang TJ, Tan YR, Ren WH, Han GQ, Zhang J, Wang LC, and Qin CY (2010) Protective effects of ursodeoxycholic acid against immune-mediated liver fibrosis in rats. Hepatogastroenterology 57:1196-1202.