S-Adenosylmethionine increases circulating very-low density lipoprotein clearance in non-alcoholic fatty liver disease

Journal of Hepatology

Volumn 62, Issue 3, 2015, Pages 673-681

  Martínez Uña, Maite ^a,b   Varela Rey, Marta ^c   Mestre, Daniela ^a,b   Fernández Ares, Larraitz ^a,b   Fresnedo, Olatz ^a   Fernandez Ramos, David ^c   Juan, Virginia Gutiérrez De ^c   Martin Guerrero, Idoia ^a   García Orad, Africa ^a   Luka, Zigmund ^d   Wagner, Conrad ^d   Lu, Shelly C ^e   García Monzón, Carmelo ^f,h   Finnell, Richard H ^g   Aurrekoetxea, Igor ^a,b   Buqué, Xabier ^a,b   Martínez Chantar, M Luz ^a,c   Mato, José M ^c   Aspichueta, Patricia ^a,b  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^b BioCruces Health Research Institute   (Spain)

^c CIC BIOGUNE   (Spain)

^d VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^f HOSPITAL UNIVERSITARIO SANTA CRISTINA   (Spain)

^g University of Texas at Austin   (United States)

^h INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; APOLIPOPROTEIN E; DIACYLGLYCEROL ACYLTRANSFERASE; GLYCINE METHYLTRANSFERASE; MESSENGER RNA; MICROSOMAL TRIGLYCERIDE TRANSFER PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; S ADENOSYLMETHIONINE; TRIACYLGLYCEROL; TRIACYLGLYCEROL LIPASE; VERY LOW DENSITY LIPOPROTEIN; GNMT PROTEIN, MOUSE; MEMBRANE PROTEIN; PERILIPIN 2;

AMINO ACID METABOLISM; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CLEARANCE; CONTROLLED STUDY; DNA METHYLATION; ENZYME ACTIVITY; FOOD INTAKE; GENE DELETION; GENE EXPRESSION; HUMAN; HUMAN TISSUE; HYPERTRIGLYCERIDEMIA; LIPID DIET; LIPID HOMEOSTASIS; LIPID STORAGE; LIPOGENESIS; LIPOPROTEIN BLOOD LEVEL; LIPOPROTEIN METABOLISM; LIPOPROTEIN SECRETION; LIVER WEIGHT; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN CONTENT; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SECRETION RATE; SHIFT TO THE LEFT; TRIACYLGLYCEROL BLOOD LEVEL; TURNOVER TIME; VERY LOW DENSITY LIPOPROTEIN CLEARANCE; WILD TYPE; ADULT; ADVERSE EFFECTS; AGED; ANIMAL; BIOLOGICAL MODEL; BLOOD; DEFICIENCY; DISEASE MODEL; FEMALE; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM; MIDDLE AGED; NON-ALCOHOLIC FATTY LIVER DISEASE; PATHOLOGY; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; ANIMALS; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FEMALE; GLYCINE N-METHYLTRANSFERASE; HUMANS; LIPOPROTEINS, VLDL; LIVER; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MIDDLE AGED; MODELS, BIOLOGICAL; NON-ALCOHOLIC FATTY LIVER DISEASE; S-ADENOSYLMETHIONINE; TRIGLYCERIDES; YOUNG ADULT;

EID: 84922969505     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.10.019     Document Type: Article

References (46)

1. R. Scott, M. Donoghoe, G.F. Watts, R. O'Brien, C. Pardy, and M.R. Taskinen Impact of metabolic syndrome and its components on cardiovascular disease event rates in 4900 patients with type 2 diabetes assigned to placebo in the FIELD randomised trial Cardiovasc Diabetol 10 2011 102
2. E.M. Ooi, T.W. Ng, G.F. Watts, D.C. Chan, and P.H. Barrett Effect of fenofibrate and atorvastatin on VLDL apoE metabolism in men with the metabolic syndrome J Lipid Res 53 2012 2443 2449
3. M.J. Armstrong, L.A. Adams, A. Canbay, and W.K. Syn Extrahepatic complications of non-alcoholic fatty liver disease Hepatology 59 2014 1174 1197
4. E. Fabbrini, D. deHaseth, S. Deivanayagam, B.S. Mohammed, B.E. Vitola, and S. Klein Alterations in fatty acid kinetics in obese adolescents with increased intrahepatic triglyceride content Obesity 17 2009 25 29
5. K. Fujita, Y. Nozaki, K. Wada, M. Yoneda, Y. Fujimoto, and M. Fujitake Dysfunctional very-low-density lipoprotein synthesis and release is a key factor in non-alcoholic steatohepatitis pathogenesis Hepatology 50 2009 772 780
6. A. Cano, X. Buque, M. Martinez-Una, I. Aurrekoetxea, A. Menor, and J.L. Garcia-Rodriguez Methionine adenosyltransferase 1A gene deletion disrupts hepatic very low-density lipoprotein assembly in mice Hepatology 54 2011 1975 1986
7. H. Jo, S.S. Choe, K.C. Shin, H. Jang, J.H. Lee, and J.K. Seong Endoplasmic reticulum stress induces hepatic steatosis via increased expression of the hepatic very low-density lipoprotein receptor Hepatology 57 2013 1366 1377
8. R.A. Borchardt, and R.A. Davis Intrahepatic assembly of very low density lipoproteins. Rate of transport out of the endoplasmic reticulum determines rate of secretion J Biol Chem 262 1987 16394 16402
9. M.M. Hussain, J. Shi, and P. Dreizen Microsomal triglyceride transfer protein and its role in apoB-lipoprotein assembly J Lipid Res 44 2003 22 32
10. Z.G. Jiang, S.C. Robson, and Z. Yao Lipoprotein metabolism in non-alcoholic fatty liver disease J Biomed Res 27 2013 1 13
11. A.R. Mensenkamp, L.M. Havekes, J.A. Romijn, and F. Kuipers Hepatic steatosis and very low density lipoprotein secretion: the involvement of apolipoprotein E J Hepatol 35 2001 816 822
12. R.W. Mahley, S.C. Rall Jr., and E. Apolipoprotein Far more than a lipid transport protein Annu Rev Genomics Hum Genet 1 2000 507 537
13. H. Shimano, N. Yamada, M. Katsuki, M. Shimada, T. Gotoda, and K. Harada Overexpression of apolipoprotein E in transgenic mice: marked reduction in plasma lipoproteins except high density lipoprotein and resistance against diet-induced hypercholesterolemia Proc Natl Acad Sci U S A 89 1992 1750 1754
14. G.F. Gibbons, R. Khurana, A. Odwell, and M.C. Seelaender Lipid balance in HepG2 cells: active synthesis and impaired mobilization J Lipid Res 35 1994 1801 1808
15. D. Wiggins, and G.F. Gibbons The lipolysis/esterification cycle of hepatic triacylglycerol. Its role in the secretion of very-low-density lipoprotein and its response to hormones and sulphonylureas Biochem J 284 1992 457 462
16. D. Gilham, S. Ho, M. Rasouli, P. Martres, D.E. Vance, and R. Lehner Inhibitors of hepatic microsomal triacylglycerol hydrolase decrease very low density lipoprotein secretion FASEB J 17 2003 1685 1687
17. M.L. Martinez-Chantar, M. Vazquez-Chantada, U. Ariz, N. Martinez, M. Varela, and Z. Luka Loss of the glycine N-methyltransferase gene leads to steatosis and hepatocellular carcinoma in mice Hepatology 47 2008 1191 1199
18. A.A. Noga, Y. Zhao, and D.E. Vance An unexpected requirement for phosphatidylethanolamine N-methyltransferase in the secretion of very low density lipoproteins J Biol Chem 277 2002 42358 42365
19. M. Martinez-Una, M. Varela-Rey, A. Cano, L. Fernandez-Ares, N. Beraza, and I. Aurrekoetxea Excess S-adenosylmethionine reroutes phosphatidylethanolamine towards phosphatidylcholine and triglyceride synthesis Hepatology 58 2013 1296 1305
20. T. Nishimaki-Mogami, K. Suzuki, and A. Takahashi The role of phosphatidylethanolamine methylation in the secretion of very low density lipoproteins by cultured rat hepatocytes: rapid inhibition of phosphatidylethanolamine methylation by bezafibrate increases the density of apolipoprotein B48-containing lipoproteins Biochim Biophys Acta 1304 1996 21 31
21. K.G. Bharadwaj, Y. Hiyama, Y. Hu, L.A. Huggins, R. Ramakrishnan, and N.A. Abumrad Chylomicron- and VLDL-derived lipids enter the heart through different pathways: in vivo evidence for receptor- and non-receptor-mediated fatty acid uptake J Biol Chem 285 2010 37976 37986
22. T. Seo, M. Al-Haideri, E. Treskova, T.S. Worgall, Y. Kako, and I.J. Goldberg Lipoprotein lipase-mediated selective uptake from low density lipoprotein requires cell surface proteoglycans and is independent of scavenger receptor class B type 1 J Biol Chem 275 2000 30355 30362
23. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can J Biochem Physiol 37 1959 911 917
24. J.I. Ruiz, and B. Ochoa Quantification in the subnanomolar range of phospholipids and neutral lipids by monodimensional thin-layer chromatography and image analysis J Lipid Res 38 1997 1482 1489
25. C.A. Moylan, H. Pang, A. Dellinger, A. Suzuki, M.E. Garrett, and C.D. Guy Hepatic gene expression profiles differentiate presymptomatic patients with mild versus severe non-alcoholic fatty liver disease Hepatology 59 2014 471 482
26. S.K. Murphy, H. Yang, C.A. Moylan, H. Pang, A. Dellinger, and M.F. Abdelmalek Relationship between methylome and transcriptome in patients with non-alcoholic fatty liver disease Gastroenterology 145 2013 1076 1087
27. S.Q. Ye, C.A. Reardon, and G.S. Getz Inhibition of apolipoprotein E degradation in a post-Golgi compartment by a cysteine protease inhibitor J Biol Chem 268 1993 8497 8502
28. C. Wenner, S. Lorkowski, T. Engel, and P. Cullen Apolipoprotein E in macrophages and hepatocytes is eegraded via the proteasomal pathway Biochem Biophys Res Commun 282 2001 608 614
29. B. Magnusson, L. Asp, P. Bostrom, M. Ruiz, P. Stillemark-Billton, and D. Linden Adipocyte differentiation-related protein promotes fatty acid storage in cytosolic triglycerides and inhibits secretion of very low-density lipoproteins Arterioscler Thromb Vasc Biol 26 2006 1566 1571
30. S. Senthivinayagam, A.L. McIntosh, K.C. Moon, and B.P. Atshaves Plin2 inhibits cellular glucose uptake through interactions with SNAP23, a SNARE complex protein PLoS One 8 2013 e73696
31. A.L. McIntosh, S.M. Storey, and B.P. Atshaves Intracellular lipid droplets contain dynamic pools of sphingomyelin: ADRP binds phospholipids with high affinity Lipids 45 2010 465 477
32. M. Sundaram, and Z. Yao Recent progress in understanding protein and lipid factors affecting hepatic VLDL assembly and secretion Nutr Metab (Lond) 7 2010 35
33. P.C. Rensen, N. Herijgers, M.H. Netscher, S.C. Meskers, M. van Eck, and T.J. van Berkel Particle size determines the specificity of apolipoprotein E-containing triglyceride-rich emulsions for the LDL receptor versus hepatic remnant receptor in vivo J Lipid Res 38 1997 1070 1084
34. J.C. Perman, P. Bostrom, M. Lindbom, U. Lidberg, M. StAhlman, and D. Hagg The VLDL receptor promotes lipotoxicity and increases mortality in mice following an acute myocardial infarction J Clin Invest 121 2011 2625 2640
35. G. Horl, A. Wagner, L.K. Cole, R. Malli, H. Reicher, and P. Kotzbeck Sequential synthesis and methylation of phosphatidylethanolamine promote lipid droplet biosynthesis and stability in tissue culture and in vivo J Biol Chem 286 2011 17338 17350
36. K. Yamaguchi, L. Yang, S. McCall, J. Huang, X.X. Yu, and S.K. Pandey Diacylglycerol acyltranferase 1 anti-sense oligonucleotides reduce hepatic fibrosis in mice with non-alcoholic steatohepatitis Hepatology 47 2008 625 635
37. K. Yamaguchi, L. Yang, S. McCall, J. Huang, X.X. Yu, and S.K. Pandey Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with non-alcoholic steatohepatitis Hepatology 45 2007 1366 1374
38. L.K. Cole, V.W. Dolinsky, J.R. Dyck, and D.E. Vance Impaired phosphatidylcholine biosynthesis reduces atherosclerosis and prevents lipotoxic cardiac dysfunction in ApoE-/- Mice Circ Res 108 2011 686 694
39. E.A. Karavia, D.J. Papachristou, I. Kotsikogianni, I. Giopanou, and K.E. Kypreos Deficiency in apolipoprotein E has a protective effect on diet-induced non-alcoholic fatty liver disease in mice FEBS J 278 2011 3119 3129
40. L.P. Bechmann, R.K. Gieseler, J.P. Sowa, A. Kahraman, J. Erhard, and I. Wedemeyer Apoptosis is associated with CD36/fatty acid translocase upregulation in non-alcoholic steatohepatitis Liver Int 30 2010 850 859
41. S. Sydor, Y. Gu, M. Schlattjan, L.P. Bechmann, U. Rauen, and J. Best Steatosis does not impair liver regeneration after partial hepatectomy Lab Invest 93 2013 20 30
42. X. Buqué, A. Cano, M.E. Miquilena-Colina, C. García-Monzón, B. Ochoa, and P. Aspichueta High insulin levels are required for FAT/CD36 plasma membrane translocation and enhanced fatty acid uptake in obese Zucker rat hepatocytes Am J Physiol Endocrinol Metab 303 2012 E504 14
43. C. Wang, Y. Yan, L. Hu, L. Zhao, P. Yang, and J.F. Moorhead Rapamycin-mediated CD36 translational suppression contributes to alleviation of hepatic steatosis Biochem Biophys Res Commun 447 2014 57 63
44. C. Wang, L. Hu, L. Zhao, P. Yang, J.F. Moorhead, and Z. Varghese Inflammatory stress increases hepatic CD36 translational efficiency via activation of the mTOR signalling pathway PLoS One 9 2014 e103071 10.1371/journal.pone.0103071
45. P.C. Rensen, M.C. Jong, L.C. van Vark, H. van der Boom, W.L. Hendriks, and T.J. van Berkel Apolipoprotein E is resistant to intracellular degradation in vitro and in vivo. Evidence for retroendocytosis J Biol Chem 275 2000 8564 8571
46. J. Ye, J.Z. Li, Y. Liu, X. Li, T. Yang, and X. Ma Cideb, an ER- and lipid droplet-associated protein, mediates VLDL lipidation and maturation by interacting with apolipoprotein B Cell Metab 9 2009 177 190