Choline supplementation protects against liver damage by normalizing cholesterol metabolism in Pemt/Ldlr knockout mice fed a high-fat diet

Journal of Nutrition

Volumn 144, Issue 3, 2014, Pages 252-257

  Al Rajabi, Ala ^a   Castro, Gabriela S F ^b   da Silva, Robin P ^a   Nelson, Randy C ^a   Thiesen, Aducio ^a   Vannucchi, Helio ^b   Vine, Donna F ^a   Proctor, Spencer D ^a   Field, Catherine J ^a   Curtis, Jonathan M ^a   Jacobs, René L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; CHOLESTEROL; CHOLESTEROL ESTERS; CHOLINE; DIET, HIGH-FAT; FATTY LIVER; LIPID METABOLISM; LIVER; MALE; MICE; MICE, KNOCKOUT; PHOSPHATIDYLETHANOLAMINE N-METHYLTRANSFERASE; RECEPTORS, LDL; TRIGLYCERIDES;

EID: 84894279706     PISSN: 00223166     EISSN: 15416100     Source Type: Journal    
DOI: 10.3945/jn.113.185389     Document Type: Article

References (51)

1. Powell EE, Cooksley WG, Hanson R, Searle J, Halliday JW, Powell LW. The natural history of nonalcoholic steatohepatitis: a follow-up study of forty-two patients for up to 21 years. Hepatology. 1990;11:74-80.
2. Marchesini G, Brizi M, Bianchi G, Tomassetti S, Bugianesi E, Lenzi M, McCullough AJ, Natale S, Forlani G, Melchionda N. Nonalcoholic fatty liver disease: a feature of the metabolic syndrome. Diabetes. 2001;50:1844-50.
3. Teli MR, James OF, Burt AD, Bennett MK, Day CP. The natural history of nonalcoholic fatty liver: a follow-up study. Hepatology. 1995;22: 1714-9.
4. Matteoni CA, Younossi ZM, Gramlich T, Boparai N, Liu YC, McCullough AJ. Nonalcoholic fatty liver disease: a spectrum of clinical and pathological severity. Gastroenterology. 1999;116:1413-9.
5. Cohen JC, Horton JD, Hobbs HH. Human fatty liver disease: old questions and new insights. Science. 2011;332:1519-23.
6. Chalasani N, Younossi Z, Lavine JE, Diehl AM, Brunt EM, Cusi K, Charlton M, Sanyal AJ. The diagnosis and management of nonalcoholic fatty liver disease: practice Guideline by the American Association for the Study of Liver Diseases, American College of Gastroenterology, and the American Gastroenterological Association. Hepatology. 2012;55:2005-23.
7. Kennedy EP, Weiss SB. The function of cytidine coenzymes in the biosynthesis of phospholipides. J Biol Chem. 1956;222:193-214.
8. Kennedy EP. Metabolism of lipides. Annu Rev Biochem. 1957;26:119-48.
9. Vance DE, Li Z, Jacobs RL. Hepatic phosphatidylethanolamine N-methyltransferase, unexpected roles in animal biochemistry and physiology. J Biol Chem. 2007;282:33237-41.
10. Zeisel SH, Da Costa KA, Franklin PD, Alexander EA, Lamont JT, Sheard NF, Beiser A. Choline, an essential nutrient for humans. FASEB J. 1991;5:2093-8.
11. Vance DE, Ridgway ND. The methylation of phosphatidylethanolamine. Prog Lipid Res. 1988;27:61-79.
12. Vance DE. Role of phosphatidylcholine biosynthesis in the regulation of lipoprotein homeostasis. Curr Opin Lipidol. 2008;19:229-34.
13. DeLong CJ, Shen YJ, Thomas MJ, Cui Z. Molecular distinction of phosphatidylcholine synthesis between the CDP-choline pathway and phosphatidylethanolamine methylation pathway. J Biol Chem. 1999; 274:29683-8.
14. Walkey CJ, Donohue LR, Bronson R, Agellon LB, Vance DE. Disruption of the murine gene encoding phosphatidylethanolamine Nmethyltransferase. Proc Natl Acad Sci USA. 1997;94:12880-5.
15. Verkade HJ, Havinga R, Shields DJ, Wolters H, Bloks VW, Kuipers F, Vance DE, Agellon LB. The phosphatidylethanolamine N-methyltransferase pathway is quantitatively not essential for biliary phosphatidylcholine secretion. J Lipid Res. 2007;48:2058-64.
16. Noga AA, Vance DE. A gender-specific role for phosphatidylethanolamine N-methyltransferase-derived phosphatidylcholine in the regulation of plasma high density and very low density lipoproteins in mice. J Biol Chem. 2003;278:21851-9.
17. Jacobs RL, Zhao Y, Koonen DP, Sletten T, Su B, Lingrell S, Cao G, Peake DA, Kuo MS, Proctor SD, et al. Impaired de novo choline synthesis explains why phosphatidylethanolamine N-methyltransferasedeficient mice are protected from diet-induced obesity. J Biol Chem. 2010;285:22403-13.
18. Walkey CJ, Yu L, Agellon LB, Vance DE. Biochemical and evolutionary significance of phospholipid methylation. J Biol Chem. 1998;273: 27043-6.
19. Li Z, Agellon LB, Vance DE. Phosphatidylcholine homeostasis and liver failure. J Biol Chem. 2005;280:37798-802.
20. Li Z, Agellon LB, Allen TM, Umeda M, Jewell L, Mason A, Vance DE. The ratio of phosphatidylcholine to phosphatidylethanolamine influences membrane integrity and steatohepatitis. Cell Metab. 2006;3: 321-31.
21. Zhao Y, Su B, Jacobs RL, Kennedy B, Francis GA, Waddington E, Brosnan JT, Vance JE, Vance DE. Lack of phosphatidylethanolamine N-methyltransferase alters plasma VLDL phospholipids and attenuates atherosclerosis in mice. Arterioscler Thromb Vasc Biol. 2009;29:1349-55.
22. 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;94:2467-74.
23. Kuksis A, Myher JJ. Gas chromatographic analysis of plasma lipids. Adv Chromatogr. 1989;28:267-332.
24. Xiong Y, Zhao YY, Goruk S, Oilund K, Field CJ, Jacobs RL, Curtis JM. Validation of an LC-MS/MS method for the quantification of cholinerelated compounds and phospholipids in foods and tissues.J Chromatogr B Analyt Technol Biomed Life Sci. 2012;911:170-9.
25. Niebergall LJ, Jacobs RL, Chaba T, Vance DE. Phosphatidylcholine protects against steatosis in mice but not non-alcoholic steatohepatitis. Biochim Biophys Acta. 2011;1811:1177-85.
26. Chavin KD, Yang S, Lin HZ, Chatham J, Chacko VP, Hoek JB, Walajtys-Rode E, Rashid A, Chen CH, Huang CC, et al. Obesity induces expression of uncoupling protein-2 in hepatocytes and promotes liver ATP depletion. J Biol Chem. 1999;274:5692-700.
27. Gundermann KJ, Kuenker A, Kuntz E, Drozdzik M. Activity of essential phospholipids (EPL) from soybean in liver diseases. Pharmacol Rep. 2011;63:643-59.
28. Zeisel SH, Niculescu MD. Perinatal choline influences brain structure and function. Nutr Rev. 2006;64:197-203.
29. Ling J, Chaba T, Zhu LF, Jacobs RL, Vance DE. Hepatic ratio of phosphatidylcholine to phosphatidylethanolamine predicts survival after partial hepatectomy in mice. Hepatology. 2012;55:1094-102.
30. Kumar VV. Complementary molecular shapes and additivity of the packing parameter of lipids. Proc Natl Acad Sci USA. 1991;88:444-8.
31. Phillips R, Ursell T, Wiggins P, Sens P. Emerging roles for lipids in shaping membrane-protein function. Nature. 2009;459:379-85.
32. Attili AF, Angelico M, Cantafora A, Alvaro D, Capocaccia L. Bile acidinduced liver toxicity: relation to the hydrophobic-hydrophilic balance of bile acids. Med Hypotheses. 1986;19:57-69.
33. Galle PR, Theilmann L, Raedsch R, Otto G, Stiehl A. Ursodeoxycholate reduces hepatotoxicity of bile salts in primary human hepatocytes. Hepatology. 1990;12:486-91.
34. Spivey JR, Bronk SF, Gores GJ. Glycochenodeoxycholate-induced lethal hepatocellular injury in rat hepatocytes. Role of ATP depletion and cytosolic free calcium. J Clin Invest. 1993;92:17-24.
35. Sokol RJ, McKim JM Jr, Goff MC, Ruyle SZ, Devereaux MW, Han D, Packer L, Everson G. Vitamin E reduces oxidant injury to mitochondria and the hepatotoxicity of taurochenodeoxycholic acid in the rat. Gastroenterology. 1998;114:164-74.
36. Billington D, Evans CE, Godfrey PP, Coleman R. Effects of bile salts on the plasma membranes of isolated rat hepatocytes. Biochem J. 1980;188:321-7.
37. Sokol RJ, Straka MS, Dahl R, Devereaux MW, Yerushalmi B, Gumpricht E, Elkins N, Everson G. Role of oxidant stress in the permeability transition induced in rat hepatic mitochondria by hydrophobic bile acids. Pediatr Res. 2001;49:519-31.
38. Ljubuncic P, Fuhrman B, Oiknine J, Aviram M, Bomzon A. Effect of deoxycholic acid and ursodeoxycholic acid on lipid peroxidation in cultured macrophages. Gut. 1996;39:475-8.
39. Peet DJ, Turley SD, Ma W, Janowski BA, Lobaccaro JM, Hammer RE, Mangelsdorf DJ. Cholesterol and bile acid metabolism are impaired in mice lacking the nuclear oxysterol receptor LXR alpha. Cell. 1998; 93:693-704.
40. Russell DW. Nuclear orphan receptors control cholesterol catabolism. Cell. 1999;97:539-42.
41. Eggertsen G, Olin M, Andersson U, Ishida H, Kubota S, Hellman U, Okuda KI, Bjorkhem I. Molecular cloning and expression of rabbit sterol 12alpha-hydroxylase. J Biol Chem. 1996;271:32269-75.
42. Goodwin B, Jones SA, Price RR, Watson MA, McKee DD, Moore LB, Galardi C, Wilson JG, Lewis MC, Roth ME, et al. A regulatory cascade of the nuclear receptors FXR, SHP-1, and LRH-1 represses bile acid biosynthesis. Mol Cell. 2000;6:517-26.
43. Lu TT, Makishima M, Repa JJ, Schoonjans K, Kerr TA, Auwerx J, Mangelsdorf DJ. Molecular basis for feedback regulation of bile acid synthesis by nuclear receptors. Mol Cell. 2000;6:507-15.
44. Zhang M, Chiang JY. Transcriptional regulation of the human sterol 12alpha-hydroxylase gene (CYP8B1): roles of heaptocyte nuclear factor 4alpha in mediating bile acid repression. J Biol Chem. 2001; 276:41690-9.
45. Zollner G, Wagner M, Fickert P, Geier A, Fuchsbichler A, Silbert D, Gumhold J, Zatloukal K, Kaser A, Tilg H, et al. Role of nuclear receptors and hepatocyte-enriched transcription factors for Ntcp repression in biliary obstruction in mouse liver. Am J Physiol Gastrointest Liver Physiol. 2005;289:G798-805.
46. Denson LA, Sturm E, Echevarria W, Zimmerman TL, Makishima M, Mangelsdorf DJ, Karpen SJ. The orphan nuclear receptor, shp, mediates bile acid-induced inhibition of the rat bile acid transporter, ntcp. Gastroenterology. 2001;121:140-7.
47. Calkin AC, Tontonoz P. Transcriptional integration of metabolism by the nuclear sterol-activated receptors LXR and FXR. Nat Rev Mol Cell Biol. 2012;13:213-24.
48. Lee JM, Trauner M, Soroka CJ, Stieger B, Meier PJ, Boyer JL. Expression of the bile salt export pump is maintained after chronic cholestasis in the rat. Gastroenterology. 2000;118:163-72.
49. Lehmann JM, Kliewer SA, Moore LB, Smith-Oliver TA, Oliver BB, Su JL, Sundseth SS, Winegar DA, Blanchard DE, Spencer TA, et al. Activation of the nuclear receptor LXR by oxysterols defines a new hormone response pathway. J Biol Chem. 1997;272:3137-40.
50. Kolouchova G, Brcakova E, Hirsova P, Sispera L, Tomsik P, Cermanova J, Hyspler R, Slanarova M, Fuksa L, Lotkova H, et al. Pravastatin modulates liver bile acid and cholesterol homeostasis in rats with chronic cholestasis. J Gastroenterol Hepatol. 2011;26:1544-51.
51. Song J, da Costa KA, Fischer LM, Kohlmeier M, Kwock L, Wang S, Zeisel SH. Polymorphism of the PEMT gene and susceptibility to nonalcoholic fatty liver disease (NAFLD). FASEB J. 2005;19:1266-71.