Fish oil and krill oil supplementations differentially regulate lipid catabolic and synthetic pathways in mice

Nutrition and Metabolism

Volumn 11, Issue 1, 2014, Pages

  Tillander, Veronika ^a   Bjørndal, Bodil ^b   Burri, Lena ^b,d   Bohov, Pavol ^b   Skorve, Jon ^b   Berge, Rolf K ^b,c   Alexson, Stefan Eh ^a  

^a KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^b UNIVERSITY OF BERGEN   (Norway)

^c HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^d former employee of Aker BioMarine Antarctic AS   (Norway)

Author keywords

Gene regulation; High fat diet; Krill oil; Omega 3 fatty acids; Plasma lipids

Indexed keywords

ARACHIDONIC ACID; CHOLESTEROL; FATTY ACID; FISH OIL; ISOPRENOID; KRILL OIL; LARD; LIPID; LIPOPROTEIN; OMEGA 3 FATTY ACID; SOYBEAN OIL; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOAVAILABILITY; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; FATTY ACID METABOLISM; GENE CONTROL; GENE EXPRESSION; INTESTINE EPITHELIUM; KRILL; LIPID ANALYSIS; LIPID BLOOD LEVEL; LIPID COMPOSITION; LIPID DIET; LIPID LIVER LEVEL; LIPID METABOLISM; LIPID OXIDATION; LIPOGENESIS; LIPOPROTEIN BLOOD LEVEL; LIVER WEIGHT; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; WEIGHT GAIN;

EUPHAUSIACEA; MUS;

EID: 84899931945     PISSN: None     EISSN: 17437075     Source Type: Journal    
DOI: 10.1186/1743-7075-11-20     Document Type: Article

References (58)

1. Circulating and dietary omega-3 and omega-6 polyunsaturated fatty acids and incidence of CVD in the Multi-Ethnic Study of Atherosclerosis. de Oliveira Otto MC, Wu JH, Baylin A, Vaidya D, Rich SS, Tsai MY, Jacobs DR Jr, Mozaffarian D, J Am Heart Assoc 2013 2 6 000506 10.1161/JAHA.113.000506 24351702
2. Eicosapentaenoic acid and prevention of thrombosis and atherosclerosis? Dyerberg J, Bang HO, Stoffersen E, Moncada S, Vane JR, Lancet 1978 2 8081 117 119 78322
3. A quantitative analysis of fish consumption and coronary heart disease mortality. Konig A, Bouzan C, Cohen JT, Connor WE, Kris-Etherton PM, Gray GM, Lawrence RS, Savitz DA, Teutsch SM, Am J Prev Med 2005 29 4 335 346 10.1016/j.amepre.2005.07.001 16242600
4. Update on cardiometabolic health effects of omega-3 fatty acids. Kromhout D, de Goede J, Curr Opin Lipidol 2014 25 1 85 90 10.1097/MOL.0000000000000041 24345990
5. Role of omega-3 fatty acids in obesity, metabolic syndrome, and cardiovascular diseases: a review of the evidence. Lorente-Cebrian S, Costa AG, Navas-Carretero S, Zabala M, Martinez JA, Moreno-Aliaga MJ, J Physiol Biochem 2013 69 3 633 651 10.1007/s13105-013-0265-4 23794360
6. Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Kris-Etherton PM, Harris WS, Appel LJ, Arterioscler Thromb Vasc Biol 2003 23 2 20 e30 10.1161/01.ATV.0000038493.65177.94 12588785
7. Omega-3 fatty acids and cardiovascular disease: new recommendations from the American Heart Association. Kris-Etherton PM, Harris WS, Appel LJ, Arterioscler Thromb Vasc Biol 2003 23 2 151 152 10.1161/01.ATV.0000057393.97337. AE 12588750
8. Marine omega-3 phospholipids: metabolism and biological activities. Burri L, Hoem N, Banni S, Berge K, Int J Mol Sci 2012 13 11 15401 15419 23203133
9. Interannual and between species comparison of the lipids, fatty acids and sterols of Antarctic krill from the US AMLR Elephant Island survey area. Phleger CF, Nelson MM, Mooney BD, Nichols PD, Comp Biochem Physiol B: Biochem Mol Biol 2002 131 4 733 747 10.1016/S1096-4959(02)00021-0 11923086
10. Krill for human consumption: nutritional value and potential health benefits. Tou JC, Jaczynski J, Chen YC, Nutr Rev 2007 65 2 63 77 17345959
11. Elucidation of phosphatidylcholine composition in krill oil extracted from Euphausia superba. Winther B, Hoem N, Berge K, Reubsaet L, Lipids 2011 46 1 25 36 10.1007/s11745-010-3472-6 20848234
12. Krill oil supplementation increases plasma concentrations of eicosapentaenoic and docosahexaenoic acids in overweight and obese men and women. Maki KC, Reeves MS, Farmer M, Griinari M, Berge K, Vik H, Hubacher R, Rains TM, Nutr Res 2009 29 9 609 615 10.1016/j.nutres.2009.09.004 19854375
13. Metabolic effects of krill oil are essentially similar to those of fish oil but at lower dose of EPA and DHA, in healthy volunteers. Ulven SM, Kirkhus B, Lamglait A, Basu S, Elind E, Haider T, Berge K, Vik H, Pedersen JI, Lipids 2011 46 1 37 46 10.1007/s11745-010-3490-4 21042875
14. Incorporation of EPA and DHA into plasma phospholipids in response to different omega-3 fatty acid formulations - a comparative bioavailability study of fish oil vs. krill oil. Schuchardt JP, Schneider I, Meyer H, Neubronner J, Von Schacky C, Hahn A, Lipids Health Dis 2011 10 145 10.1186/1476-511X-10-145 21854650
15. Krill oil supplementation lowers serum triglycerides without increasing low-density lipoprotein cholesterol in adults with borderline high or high triglyceride levels. Berge K, Musa-Veloso K, Harwood M, Hoem N, Burri L, Nutr Res 2014 34 2 126 133 10.1016/j.nutres.2013.12.003 24461313
16. Enhanced increase of omega-3 index in healthy individuals with response to 4-week n-3 fatty acid supplementation from krill oil versus fish oil. Ramprasath VR, Eyal I, Zchut S, Jones PJ, Lipids Health Dis 2013 12 178 10.1186/1476-511X-12-178 24304605
17. Metabolic effects of n-3 PUFA as phospholipids are superior to triglycerides in mice fed a high-fat diet: possible role of endocannabinoids. Rossmeisl M, Jilkova ZM, Kuda O, Jelenik T, Medrikova D, Stankova B, Kristinsson B, Haraldsson GG, Svensen H, Stoknes I, Sjovall P, Magnusson Y, Balvers MG, Verhoeckx KC, Tvrzicka E, Bryhn M, Kopecky J, PLoS One 2012 7 6 38834 10.1371/journal.pone.0038834 22701720
18. Very-long-chain and branched-chain fatty acyl-CoAs are high affinity ligands for the peroxisome proliferator-activated receptor alpha (PPARalpha). Hostetler HA, Kier AB, Schroeder F, Biochemistry 2006 45 24 7669 7681 10.1021/bi060198l 16768463
19. Polyunsaturated fatty acids selectively suppress sterol regulatory element-binding protein-1 through proteolytic processing and autoloop regulatory circuit. Takeuchi Y, Yahagi N, Izumida Y, Nishi M, Kubota M, Teraoka Y, Yamamoto T, Matsuzaka T, Nakagawa Y, Sekiya M, Sekiya M, Iizuka Y, Ohashi K, Osuga J, Gotoda T, Ishibashi S, Itaka K, Kataoka K, Nagai R, Yamada N, Kadowaki T, Shimano H, J Biol Chem 2010 285 15 11681 11691 10.1074/jbc.M109.096107 20145241
20. Effect of synthetic dietary triglycerides: a novel research paradigm for nutrigenomics. Sanderson LM, de Groot PJ, Hooiveld GJ, Koppen A, Kalkhoven E, Muller M, Kersten S, PLoS One 2008 3 2 1681 10.1371/journal.pone.0001681 18301758
21. Health benefits of marine foods and ingredients. Larsen R, Eilertsen KE, Elvevoll EO, Biotechnol Adv 2011 29 5 508 518 10.1016/j.biotechadv.2011.05.017 21683131
22. Resolvins and protectins in inflammation resolution. Serhan CN, Petasis NA, Chem Rev 2011 111 10 5922 5943 10.1021/cr100396c 21766791
23. Fish oil-How does it reduce plasma triglycerides? Shearer GC, Savinova OV, Harris WS, Biochim Biophys Acta 2012 1821 5 843 851 10.1016/j.bbalip.2011. 10.011 22041134
24. Differential effects of krill oil and fish oil on the hepatic transcriptome in mice. Burri L, Berge K, Wibrand K, Berge RK, Barger JL, Front Genet 2011 2 45 22303341
25. A krill oil supplemented diet reduces the activities of the mitochondrial tricarboxylate carrier and of the cytosolic lipogenic enzymes in rats. Ferramosca A, Conte L, Zara V, J Anim Physiol Anim Nutr 2012 96 2 295 306 10.1111/j.1439-0396.2011.01135.x
26. Dietary krill oil supplementation reduces hepatic steatosis, glycemia, and hypercholesterolemia in high-fat-fed mice. Tandy S, Chung RW, Wat E, Kamili A, Berge K, Griinari M, Cohn JS, J Agric Food Chem 2009 57 19 9339 9345 10.1021/jf9016042 19761211
27. A krill oil supplemented diet suppresses hepatic steatosis in high-fat fed rats. Ferramosca A, Conte A, Burri L, Berge K, De Nuccio F, Giudetti AM, Zara V, PLoS One 2012 7 6 38797 10.1371/journal.pone.0038797 22685607
28. Krill oil versus fish oil in modulation of inflammation and lipid metabolism in mice transgenic for TNF-alpha. Vigerust NF, Bjorndal B, Bohov P, Brattelid T, Svardal A, Berge RK, Eur J Nutr 2013 52 4 1315 1325 10.1007/s00394-012-0441-2 22923017
29. Rat intestine secretes discoid high density lipoprotein. Green PH, Tall AR, Glickman RM, J Clin Invest 1978 61 2 528 534 10.1172/JCI108963 202615
30. Intestinal ABCA1 directly contributes to HDL biogenesis in vivo. Brunham LR, Kruit JK, Iqbal J, Fievet C, Timmins JM, Pape TD, Coburn BA, Bissada N, Staels B, Groen AK, Hussain MM, Parks JS, Kuipers F, Hayden MR, J Clin Invest 2006 116 4 1052 1062 10.1172/JCI27352 16543947
31. Dietary supplementation of krill oil attenuates inflammation and oxidative stress in experimental ulcerative colitis in rats. Grimstad T, Bjorndal B, Cacabelos D, Aasprong OG, Janssen EA, Omdal R, Svardal A, Hausken T, Bohov P, Portero-Otin M, Pamplona R, Berge RK, Scand J Gastroenterol 2012 47 1 49 58 22126533
32. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Livak KJ, Schmittgen TD, Methods 2001 25 4 402 408 10.1006/meth.2001.1262 11846609
33. A rapid method of total lipid extraction and purification. Bligh EG, Dyer WJ, Can J Biochem Physiol 1959 37 8 911 917 10.1139/o59-099 13671378
34. Lipoprotein profiles in plasma and interstitial fluid analyzed with an automated gel-filtration system. Parini P, Johansson L, Broijersen A, Angelin B, Rudling M, Eur J Clin Invest 2006 36 2 98 104 10.1111/j.1365-2362.2006.01597.x 16436091
35. Enhancement of long-chain acyl-CoA hydrolase activity in peroxisomes and mitochondria of rat liver by peroxisomal proliferators. Berge RK, Flatmark T, Osmundsen H, Eur J Biochem 1984 141 3 637 644 10.1111/j.1432-1033.1984.tb08239.x 6146524
36. The effect of fasting on the activity of liver carnitine palmitoyltransferase and its inhibition by malonyl-CoA. Bremer J, Biochim Biophys Acta 1981 665 3 628 631 10.1016/0005-2760(81)90282-4 7295757
37. A sensitive spectrophotometric assay for peroxisomal acyl-CoA oxidase. Small GM, Burdett K, Connock MJ, Biochem J 1985 227 1 205 210 3994682
38. On the mechanism of the hypolipidemic effect of sulfur-substituted hexadecanedioic acid (3-thiadicarboxylic acid) in normolipidemic rats. Skorve J, Al Shurbaji A, Asiedu D, Bjorkhem I, Berglund L, Berge RK, J Lipid Res 1993 34 7 1177 1185 8371065
39. The acyl-CoA thioesterase I is regulated by PPARalpha and HNF4alpha via a distal response element in the promoter. Dongol B, Shah Y, Kim I, Gonzalez FJ, Hunt MC, J Lipid Res 2007 48 8 1781 1791 10.1194/jlr.M700119-JLR200 17485727
40. Molecular basis of PCSK9 function. Lambert G, Charlton F, Rye KA, Piper DE, Atherosclerosis 2009 203 1 1 7 10.1016/j.atherosclerosis.2008.06.010 18649882
41. Peroxisome proliferator-activated receptor alpha target genes. Rakhshandehroo M, Knoch B, Muller M, Kersten S, PPAR Res 2010
42. Marine lipid-based liposomes increase in vivo FA bioavailability. Cansell M, Nacka F, Combe N, Lipids 2003 38 5 551 559 10.1007/s11745-003-1341-0 12880112
43. Absorption and distribution of dietary fatty acids from different sources. Ramirez M, Amate L, Gil A, Early Hum Dev 2001 65 Suppl 95 S101 11755040
44. Effects of krill oil intake on plasma cholesterol and glucose levels in rats fed a high-cholesterol diet. Li DM, Zhou DY, Zhu BW, Chi YL, Sun LM, Dong XP, Qin L, Qiao WZ, Murata Y, J Sci Food Agric 2013 Epub ahead of print
45. Supplementation of diet with krill oil protects against experimental rheumatoid arthritis. Ierna M, Kerr A, Scales H, Berge K, Griinari M, BMC Musculoskelet Disord 2010 11 136 10.1186/1471-2474-11-136 20587038
46. Chronic treatment with krill powder reduces plasma triglyceride and anandamide levels in mildly obese men. Berge K, Piscitelli F, Hoem N, Silvestri C, Meyer I, Banni S, Di Marzo V, Lipids Health Dis 2013 12 78 10.1186/1476-511X-12-78 23706001
47. Fenofibrate simultaneously induces hepatic fatty acid oxidation, synthesis, and elongation in mice. Oosterveer MH, Grefhorst A, van Dijk TH, Havinga R, Staels B, Kuipers F, Groen AK, Reijngoud DJ, J Biol Chem 2009 284 49 34036 34044 10.1074/jbc.M109.051052 19801551
48. Comparative transcriptomic and metabolomic analysis of fenofibrate and fish oil treatments in mice. Lu Y, Boekschoten MV, Wopereis S, Muller M, Kersten S, Physiol Genomics 2011 43 23 1307 1318 10.1152/physiolgenomics.00100.2011 21954454
49. Eicosapentaenoic acid reduces hepatic synthesis and secretion of triacylglycerol by decreasing the activity of acyl-coenzyme A:1,2-diacylglycerol acyltransferase. Rustan AC, Nossen JO, Christiansen EN, Drevon CA, J Lipid Res 1988 29 11 1417 1426 2853717
50. In contrast with docosahexaenoic acid, eicosapentaenoic acid and hypolipidaemic derivatives decrease hepatic synthesis and secretion of triacylglycerol by decreased diacylglycerol acyltransferase activity and stimulation of fatty acid oxidation. Berge RK, Madsen L, Vaagenes H, Tronstad KJ, Gottlicher M, Rustan AC, Biochem J 1999 343 Pt 1 191 197 10493929
51. Attenuated secretion of very low density lipoproteins from McA-RH7777 cells treated with eicosapentaenoic acid is associated with impaired utilization of triacylglycerol synthesized via phospholipid remodeling. Tran K, Sun F, Cui Z, Thorne-Tjomsland G, St Germain C, Lapierre LR, McLeod RS, Jamieson JC, Yao Z, Biochim Biophys Acta 2006 1761 4 463 473 10.1016/j.bbalip.2006.03.018 16675301
52. Continuous fat oxidation in acetyl-CoA carboxylase 2 knockout mice increases total energy expenditure, reduces fat mass, and improves insulin sensitivity. Choi CS, Savage DB, Abu-Elheiga L, Liu ZX, Kim S, Kulkarni A, Distefano A, Hwang YJ, Reznick RM, Codella R, Zhang D, Cline GW, Wakil SJ, Shulman GI, Proc Natl Acad Sci U S A 2007 104 42 16480 16485 10.1073/pnas.0706794104 17923673
53. The subcellular localization of acetyl-CoA carboxylase 2. Abu-Elheiga L, Brinkley WR, Zhong L, Chirala SS, Woldegiorgis G, Wakil SJ, Proc Natl Acad Sci U S A 2000 97 4 1444 1449 10.1073/pnas.97.4.1444 10677481
54. Continuous fatty acid oxidation and reduced fat storage in mice lacking acetyl-CoA carboxylase 2. Abu-Elheiga L, Matzuk MM, Abo-Hashema KA, Wakil SJ, Science 2001 291 5513 2613 2616 10.1126/science.1056843 11283375
55. Genome-wide analysis of PPARalpha activation in murine small intestine. Bunger M, van den Bosch HM, van der Meijde J, Kersten S, Hooiveld GJ, Muller M, Physiol Genomics 2007 30 2 192 204 10.1152/physiolgenomics.00198.2006 17426115
56. Dietary fish oil upregulates intestinal lipid metabolism and reduces body weight gain in C57BL/6J mice. Mori T, Kondo H, Hase T, Tokimitsu I, Murase T, J Nutr 2007 137 12 2629 2634 18029475
57. Fenofibrate, a peroxisome proliferator-activated receptor alpha agonist, alters triglyceride metabolism in enterocytes of mice. Uchida A, Slipchenko MN, Cheng JX, Buhman KK, Biochim Biophys Acta 2011 1811 3 170 176 10.1016/j.bbalip.2010.12.011 21215818
58. Fish oil feeding is associated with an increased accumulation of dietary lipids in enterocytes: results from an in vivo study in rats. Larsen LF, Marckmann P, Kornerup Hansen A, Bukhave K, Scand J Gastroenterol 2003 38 7 712 718 12889556