Omega-3 phospholipids from fish suppress hepatic steatosis by integrated inhibition of biosynthetic pathways in dietary obese mice

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1841, Issue 2, 2014, Pages 267-278

  Rossmeisl, Martin ^a   Medrikova, Dasa ^a,d   Van Schothorst, Evert M ^b   Pavlisova, Jana ^a   Kuda, Ondrej ^a   Hensler, Michal ^a   Bardova, Kristina ^a   Flachs, Pavel ^a   Stankova, Barbora ^c   Vecka, Marek ^c   Tvrzicka, Eva ^c   Zak, Ales ^c   Keijer, Jaap ^b   Kopecky, Jan ^a  

^a INSTITUTE OF MATHEMATICS   (Czech Republic)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c CHARLES UNIVERSITY   (Czech Republic)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

High fat diet; Lipogenesis; Marine phospholipids; NAFLD; Obesity; PUFA

Indexed keywords

DOCOSAHEXAENOIC ACID; FARNESOID X RECEPTOR; FISH OIL; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; PHOSPHATIDYLCHOLINE; ROSIGLITAZONE;

ABDOMINAL FAT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CALORIC INTAKE; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL SYNTHESIS; CONTROLLED STUDY; DOWN REGULATION; DYSLIPIDEMIA; ENERGY BALANCE; FATTY LIVER; FISH; GLUCOSE INTOLERANCE; GLUCOSE TOLERANCE TEST; HERRING; IN VIVO STUDY; INSULIN RESISTANCE; LIPID DIET; LIPOGENESIS; LIVER WEIGHT; LOW DRUG DOSE; MALE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OBESITY; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT GAIN;

ANIMALS; BIOSYNTHETIC PATHWAYS; CHOLESTEROL; FATTY ACIDS, OMEGA-3; FATTY LIVER; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, OBESE; PHOSPHOLIPIDS; TRIGLYCERIDES;

EID: 84890836120     PISSN: 13881981     EISSN: 18792618     Source Type: Journal    
DOI: 10.1016/j.bbalip.2013.11.010     Document Type: Article

References (56)

1. H.M. Parker, N.A. Johnson, C.A. Burdon, J.S. Cohn, H.T. O'Connor, and J. George Omega-3 supplementation and non-alcoholic fatty liver disease: a systematic review and meta-analysis J. Hepatol. 56 2012 944 951
2. P.M. Kris-Etherton, W.S. Harris, and L.J. Appel Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease Circulation 106 2002 2747 2757 (Pubitemid 35364932)
3. D. Mozaffarian, R.N. Lemaitre, I.B. King, X. Song, H. Huang, F.M. Sacks, E.B. Rimm, M. Wang, and D.S. Siscovick Plasma phospholipid long-chain omega-3 fatty acids and total and cause-specific mortality in older adults: a cohort study Ann. Intern. Med. 158 2013 515 525
4. O. Kuda, T. Jelenik, Z. Jilkova, P. Flachs, M. Rossmeisl, M. Hensler, L. Kazdova, N. Ogston, M. Baranowski, J. Gorski, P. Janovska, V. Kus, J. Polak, V. Mohamed-Ali, R. Burcelin, S. Cinti, M. Bryhn, and J. Kopecky n-3 Fatty acids and rosiglitazone improve insulin sensitivity through additive stimulatory effects on muscle glycogen synthesis in mice fed a high-fat diet Diabetologia 52 2009 941 951
5. M. Rossmeisl, J.Z. Macek, O. Kuda, T. Jelenik, D. Medrikova, B. Stankova, B. Kristinsson, G.G. Haraldsson, H. Svensen, I. Stoknes, P. Sjovall, Y. Magnusson, M.G. Balvers, K.C. Verhoeckx, E. Tvrzicka, M. Bryhn, and J. Kopecky Metabolic effects of n-3 PUFA as phospholipids are superior to triglycerides in mice fed a high-fat diet: possible role of endocannabinoids PLoS One 7 2012 e38834
6. A. Ferramosca, A. Conte, L. Burri, K. Berge, N.F. De, A.M. Giudetti, and V. Zara A krill oil supplemented diet suppresses hepatic steatosis in high-fat fed rats PLoS One 7 2012 e38797
7. H.M. Roche, and M.J. Gibney Effect of long-chain n-3 polyunsaturated fatty acids on fasting and postprandial triacylglycerol metabolism Am. J. Clin. Nutr. 71 2000 232S 237S (Pubitemid 30046122)
8. B.K. Itariu, M. Zeyda, E.E. Hochbrugger, A. Neuhofer, G. Prager, K. Schindler, A. Bohdjalian, D. Mascher, S. Vangala, M. Schranz, M. Krebs, M.G. Bischof, and T.M. Stulnig Long-chain n-3 PUFAs reduce adipose tissue and systemic inflammation in severely obese nondiabetic patients: a randomized controlled trial Am. J. Clin. Nutr. 96 2012 1137 1149
9. T.A. Mori, D.Q. Bao, V. Burke, I.B. Puddey, G.F. Watts, and L.J. Beilin Dietary fish as a major component of a weight-loss diet: effect on serum lipids, glucose, and insulin metabolism in overweight hypertensive subjects Am. J. Clin. Nutr. 70 1999 817 825 (Pubitemid 29512906)
10. P. Flachs, R. Ruhl, M. Hensler, P. Janovska, P. Zouhar, V. Kus, J.Z. Macek, E. Papp, O. Kuda, M. Svobodova, M. Rossmeisl, G. Tsenov, V. Mohamed-Ali, and J. Kopecky Synergistic induction of lipid catabolism and anti-inflammatory lipids in white fat of dietary obese mice in response to calorie restriction and n-3 fatty acids Diabetologia 54 2011 2626 2638
11. T. Jelenik, M. Rossmeisl, O. Kuda, Z.M. Jilkova, D. Medrikova, V. Kus, M. Hensler, P. Janovska, I. Miksik, M. Baranowski, J. Gorski, S. Hebrard, T.E. Jensen, P. Flachs, S. Hawley, B. Viollet, and J. Kopecky AMP-activated protein kinase alpha2 subunit is required for the preservation of hepatic insulin sensitivity by n-3 polyunsaturated fatty acids Diabetes 59 2010 2737 2746
12. C.E. Friedberg, M.J. Janssen, R.J. Heine, and D.E. Grobbee Fish oil and glycemic control in diabetes. A meta-analysis Diabetes Care 21 1998 494 500 (Pubitemid 28172922)
13. J.A. Nettleton, and R. Katz n-3 long-chain polyunsaturated fatty acids in type 2 diabetes: a review J. Am. Diet. Assoc. 105 2005 428 440 (Pubitemid 40326734)
14. A. Gonzalez-Periz, R. Horrillo, N. Ferre, K. Gronert, B. Dong, E. Moran-Salvador, E. Titos, M. Martinez-Clemente, M. Lopez-Parra, V. Arroyo, and J. Claria Obesity-induced insulin resistance and hepatic steatosis are alleviated by omega-3 fatty acids: a role for resolvins and protectins FASEB J. 23 2009 1946 1957
15. B. Batetta, M. Griinari, G. Carta, E. Murru, A. Ligresti, L. Cordeddu, E. Giordano, F. Sanna, T. Bisogno, S. Uda, M. Collu, I. Bruheim, M.V. Di, and S. Banni Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats J. Nutr. 139 2009 1495 1501
16. S. Tandy, R.W. Chung, E. Wat, A. Kamili, K. Berge, M. Griinari, and J.S. Cohn Dietary krill oil supplementation reduces hepatic steatosis, glycemia, and hypercholesterolemia in high-fat-fed mice J. Agric. Food Chem. 57 2009 9339 9345
17. L. Spadaro, O. Magliocco, D. Spampinato, S. Piro, C. Oliveri, C. Alagona, G. Papa, A.M. Rabuazzo, and F. Purrello Effects of n-3 polyunsaturated fatty acids in subjects with nonalcoholic fatty liver disease Dig. Liver Dis. 40 2008 194 199 (Pubitemid 351181793)
18. N. Tanaka, K. Sano, A. Horiuchi, E. Tanaka, K. Kiyosawa, and T. Aoyama Highly purified eicosapentaenoic acid treatment improves nonalcoholic steatohepatitis J. Clin. Gastroenterol. 42 2008 413 418 (Pubitemid 351450629)
19. L.M. Sanderson, P.J. de Groot, G.J. Hooiveld, A. Koppen, E. Kalkhoven, M. Muller, and S. Kersten Effect of synthetic dietary triglycerides: a novel research paradigm for nutrigenomics PLoS One 3 2008 e1681
20. H. Sampath, and J.M. Ntambi Polyunsaturated fatty acid regulation of genes of lipid metabolism Annu. Rev. Nutr. 25 2005 317 340 (Pubitemid 41209005)
21. P. Flachs, M. Rossmeisl, M. Bryhn, and J. Kopecky Cellular and molecular effects of n-3 polyunsaturated fatty acids on adipose tissue biology and metabolism Clin. Sci. (Lond.) 116 2009 1 16
22. P. Flachs, V. Mohamed-Ali, O. Horakova, M. Rossmeisl, M.J. Hosseinzadeh-Attar, M. Hensler, J. Ruzickova, and J. Kopecky Polyunsaturated fatty acids of marine origin induce adiponectin in mice fed high-fat diet Diabetologia 49 2006 394 397 (Pubitemid 43185410)
23. F. Piscitelli, G. Carta, T. Bisogno, E. Murru, L. Cordeddu, K. Berge, S. Tandy, J.S. Cohn, M. Griinari, S. Banni, and V. Di Marzo Effect of dietary krill oil supplementation on the endocannabinoidome of metabolically relevant tissues from high fat-fed mice Nutr. Metab. (Lond.) 8 2011 51
24. P. Flachs, O. Horakova, P. Brauner, M. Rossmeisl, P. Pecina, N.L. Franssen-van Hal, J. Ruzickova, J. Sponarova, Z. Drahota, C. Vlcek, J. Keijer, J. Houstek, and J. Kopecky Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat Diabetologia 48 2005 2365 2375 (Pubitemid 41618929)
25. L. Burri, K. Berge, K. Wibrand, R.K. Berge, and J.L. Barger Differential effects of krill oil and fish oil on the hepatic transcriptome in mice Front. Genet. 2 2011 45
26. L. Burri, N. Hoem, S. Banni, and K. Berge Marine omega-3 phospholipids: metabolism and biological activities Int. J. Mol. Sci. 13 2012 15401 15419
27. O. Kuda, B. Stankova, E. Tvrzicka, M. Hensler, T. Jelenik, M. Rossmeisl, P. Flachs, and J. Kopecky Prominent role of liver in elevated plasma palmitooleate levels in response to rosiglitazone in mice fed high-fat diet J. Physiol. Pharmacol. 60 2009 135 140
28. M. Rossmeisl, T. Jelenik, Z. Jilkova, K. Slamova, V. Kus, M. Hensler, D. Medrikova, C. Povysil, P. Flachs, V. Mohamed-Ali, M. Bryhn, K. Berge, A.K. Holmeide, and J. Kopecky Prevention and reversal of obesity and glucose intolerance in mice by DHA derivatives Obesity 17 2009 1023 1031
29. C.A. Argmann, S.M. Houten, M.F. Champy, and J. Auwerx Lipid and bile acid analysis Curr. Protoc. Mol. Biol. 29 2006 29B.2.1-29B.2.24
30. J. Folch, M. Lees, and G.H. Sloane Stanley A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 226 1957 497 509
31. E.F. Hoek-van den Hil, J. Keijer, A. Bunschoten, J.J. Vervoort, B. Stankova, M. Bekkenkamp, L. Herreman, D. Venema, P.C. Hollman, E. Tvrzicka, I.M. Rietjens, and E.M. van Schothorst Quercetin induces hepatic lipid omega-oxidation and lowers serum lipid levels in mice PLoS One 8 2013 e51588
32. M. Rossmeisl, J. Kovar, I. Syrovy, P. Flachs, D. Bobkova, F. Kolar, R. Poledne, and J. Kopecky Triglyceride-lowering effect of respiratory uncoupling in white adipose tissue Obes. Res. 13 2005 835 844
33. G. Haemmerle, R. Zimmermann, J.G. Strauss, D. Kratky, M. Riederer, G. Knipping, and R. Zechner Hormone-sensitive lipase deficiency in mice changes the plasma lipid profile by affecting the tissue-specific expression pattern of lipoprotein lipase in adipose tissue and muscle1 J. Biol. Chem. 277 2002 12946 12952 (Pubitemid 34952662)
34. A. Subramanian, P. Tamayo, V.K. Mootha, S. Mukherjee, B.L. Ebert, M.A. Gillette, A. Paulovich, S.L. Pomeroy, T.R. Golub, E.S. Lander, and J.P. Mesirov Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles Proc. Natl. Acad. Sci. U. S. A. 102 2005 15545 15550 (Pubitemid 41528093)
35. S. Modica, R.M. Gadaleta, and A. Moschetta Deciphering the nuclear bile acid receptor FXR paradigm Nucl. Recept. Signal. 8 2010 e005
36. A.R. Alvheim, M.K. Malde, D. Osei-Hyiaman, L.Y. Hong, R.J. Pawlosky, L. Madsen, K. Kristiansen, L. Froyland, and J.R. Hibbeln Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity Obesity (Silver Spring) 20 2012 1984 1994
37. S. Banni, and V. Di Marzo Effect of dietary fat on endocannabinoids and related mediators: consequences on energy homeostasis, inflammation and mood Mol. Nutr. Food Res. 54 2010 82 92
38. A.J. Rampone, and L.W. Long The effect of phosphatidylcholine and lysophosphatidylcholine on the absorption and mucosal metabolism of oleic acid and cholesterol in vitro Biochim. Biophys. Acta 486 1977 500 510 (Pubitemid 8054534)
39. J. Fiamoncini, N. Turner, S.M. Hirabara, T.M. Salgado, A.C. Marcal, S. Leslie, S.M. da Silva, F.C. Deschamps, J. Luz, G.J. Cooney, and R. Curi Enhanced peroxisomal beta-oxidation is associated with prevention of obesity and glucose intolerance by fish oil-enriched diets Obesity (Silver Spring) 21 2013 1200 1207
40. F. Sofi, I. Giangrandi, F. Cesari, I. Corsani, R. Abbate, G.F. Gensini, and A. Casini Effects of a 1-year dietary intervention with n-3 polyunsaturated fatty acid-enriched olive oil on non-alcoholic fatty liver disease patients: a preliminary study Int. J. Food Sci. Nutr. 61 2010 792 802
41. H.M. de Vogel-van den Bosch, N.J. de Wit, G.J. Hooiveld, H. Vermeulen, J.N. van der Veen, S.M. Houten, F. Kuipers, M. Muller, and R. van der Meer A cholesterol-free, high-fat diet suppresses gene expression of cholesterol transporters in murine small intestine Am. J. Physiol. Gastrointest. Liver Physiol. 294 2008 G1171 G1180
42. C. Desmarchelier, C. Dahlhoff, S. Keller, M. Sailer, G. Jahreis, and H. Daniel C57Bl/6N mice on a western diet display reduced intestinal and hepatic cholesterol levels despite a plasma hypercholesterolemia BMC Genomics 13 2012 84
43. C. Postic, and J. Girard Contribution of de novo fatty acid synthesis to hepatic steatosis and insulin resistance: lessons from genetically engineered mice J. Clin. Invest. 118 2008 829 838 (Pubitemid 351364588)
44. K.L. Donnelly, C.I. Smith, S.J. Schwarzenberg, J. Jessurun, M.D. Boldt, and E.J. Parks Sources of fatty acids stored in liver and secreted via lipoproteins in patients with nonalcoholic fatty liver disease J. Clin. Invest. 115 2005 1343 1351 (Pubitemid 40629054)
45. E. Polichetti, A. Janisson, P.L. De La Porte, H. Portugal, J. Leonardi, A. Luna, D.P. La, and F. Chanussot Dietary polyenylphosphatidylcholine decreases cholesterolemia in hypercholesterolemic rabbits: role of the hepato-biliary axis Life Sci. 67 2000 2563 2576
46. Y. Kabir, and T. Ide Effect of dietary soybean phospholipid and fats differing in the degree of unsaturation on fatty acid synthesis and oxidation in rat liver J. Nutr. Sci. Vitaminol. (Tokyo) 41 1995 635 645 (Pubitemid 2616180)
47. E. Polichetti, N. Diaconescu, P.L. De La Porte, L. Malli, H. Portugal, A.M. Pauli, H. Lafont, B. Tuchweber, I. Yousef, and F. Chanussot Cholesterol-lowering effect of soyabean lecithin in normolipidaemic rats by stimulation of biliary lipid secretion Br. J. Nutr. 75 1996 471 478
48. M.J. LeBlanc, S. Brunet, G. Bouchard, T. Lamireau, I.M. Yousef, V. Gavino, E. Levy, and B. Tuchweber Effects of dietary soybean lecithin on plasma lipid transport and hepatic cholesterol metabolism in rats J. Nutr. Biochem. 14 2003 40 48 (Pubitemid 36143750)
49. I. Mastellone, E. Polichetti, S. Gres, C. de la Maisonneuve, N. Domingo, V. Marin, A.M. Lorec, C. Farnarier, H. Portugal, G. Kaplanski, and F. Chanussot Dietary soybean phosphatidylcholines lower lipidemia: mechanisms at the levels of intestine, endothelial cell, and hepato-biliary axis J. Nutr. Biochem. 11 2000 461 466
50. X. Tang, Z.J. Li, J. Xu, Y. Xue, J.Z. Li, J.F. Wang, T. Yanagita, C.H. Xue, and Y.M. Wang Short term effects of different omega-3 fatty acid formulation on lipid metabolism in mice fed high or low fat diet Lipids Health Dis. 11 2012 70
51. Y. Tanaka, T. Ohkubo, N. Fukuda, and H. Hibino Effect of molecular forms on distribution of docosahexaenoic acid into organs in mice J. Oleo. Sci. 52 2003 89 97
52. K.C. Maki, M.S. Reeves, M. Farmer, M. Griinari, K. Berge, H. Vik, R. Hubacher, and T.M. Rains Krill oil supplementation increases plasma concentrations of eicosapentaenoic and docosahexaenoic acids in overweight and obese men and women Nutr. Res. 29 2009 609 615
53. J.P. Schuchardt, and A. Hahn Bioavailability of long-chain omega-3 fatty acids Prostaglandins Leukot. Essent. Fatty Acids 89 2013 1 8
54. D. Osei-Hyiaman, J. Liu, L. Zhou, G. Godlewski, J. Harvey-White, W.I. Jeong, S. Batkai, G. Marsicano, B. Lutz, C. Buettner, and G. Kunos Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice J. Clin. Invest. 118 2008 3160 3169
55. M.V. Chakravarthy, I.J. Lodhi, L. Yin, R.R.V. Malapaka, H.E. Xu, J. Turk, and C.F. Semenkovich Identification of a physiologically relevant endogenous ligand for PPARalfa in liver Cell 138 2009 476 488
56. J.M. Lee, Y.K. Lee, J.L. Mamrosh, S.A. Busby, P.R. Griffin, M.C. Pathak, E.A. Ortlund, and D.D. Moore A nuclear-receptor-dependent phosphatidylcholine pathway with antidiabetic effects Nature 474 2011 506 510