Effect of fish and krill oil supplementation on glucose tolerance in rabbits with experimentally induced obesity

European Journal of Nutrition

Volumn 54, Issue 7, 2015, Pages 1055-1067

  Ivanova, Zhenya ^a   Bjørndal, Bodil ^b   Grigorova, Natalia ^a   Roussenov, Anton ^a   Vachkova, Ekaterina ^a   Berge, Kjetil ^c   Burri, Lena ^c   Berge, Rolf ^b   Stanilova, Spaska ^a   Milanova, Anelia ^a   Penchev, Georgi ^a   Vik, Rita ^b   Petrov, Vladimir ^a   Georgieva, Teodora Mircheva ^a   Bivolraski, Boycho ^a   Georgiev, Ivan Penchev ^a  

^a TRAKIA UNIVERSITY   (Bulgaria)

^b UNIVERSITY OF BERGEN   (Norway)

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

Author keywords

Fish oil; Gene expression; Glucose tolerance; Krill oil; Lipogenesis; Obesity

Indexed keywords

3 HYDROXY 3 METHYLGLUTARYL COA SYNTHASE 2; ACETYL COENZYME A CARBOXYLASE; ACETYL COENZYME A CARBOXYLASE ALPHA; CARNITINE PALMITOYLTRANSFERASE; CARNITINE PALMITOYLTRANSFERASE 2; CD36 ANTIGEN; FISH OIL; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A SYNTHASE; INSULIN; KRILL OIL; OIL; OMEGA 3 FATTY ACID; SYNTHETASE; UNCLASSIFIED DRUG; GLUCOSE BLOOD LEVEL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CELL FUNCTION; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENZYME ACTIVITY; EXPERIMENTAL OBESITY; GLUCOSE BLOOD LEVEL; GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INTRAVENOUS GLUCOSE TOLERANCE TEST; LIVER HISTOLOGY; MALE; NEW ZEALAND WHITE (RABBIT); NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; SKELETAL MUSCLE; TREATMENT DURATION; WEIGHT GAIN; ANIMAL; BLOOD; CARBOHYDRATE METABOLISM; DIETARY SUPPLEMENT; DRUG EFFECTS; FISH; GENE EXPRESSION REGULATION; GENETICS; INSULIN RESISTANCE; KRILL; LIVER; METABOLISM; OBESITY; RABBIT;

ACETYL-COA CARBOXYLASE; ANIMALS; BLOOD GLUCOSE; CARBOHYDRATE METABOLISM; CARNITINE O-PALMITOYLTRANSFERASE; DIETARY SUPPLEMENTS; EUPHAUSIACEA; FISH OILS; FISHES; GENE EXPRESSION REGULATION; HYDROXYMETHYLGLUTARYL-COA SYNTHASE; INSULIN; INSULIN RESISTANCE; LIVER; MALE; MUSCLE, SKELETAL; OBESITY; RABBITS;

EID: 84942316424     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-014-0782-0     Document Type: Article

References (63)

1. Grundy SM, Brewer HB, Cleeman JI, Smith SC, Lenfant C (2004) Definition of metabolic syndrome. Report of the National Heart, Lung and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109:433–438
2. Carpentier YA, Portois L, Malaisse WJ (2006) N-3 fatty acids and the metabolic syndrome. Am J Clin Nutr 83:1499–1504
3. Despres J, Lemieux I (2006) Abdominal obesity and metabolic syndrome. Nature 444:881–887
4. Lombardo YB, Hein G, Chicco A (2007) Metabolic syndrome: effects of n-3 PUFAs on a model of dyslipidemia, insulin resistance and adiposity. Lipids 42:427–437
5. Stumvoll M (2007) Metabolic syndrome in humans. In: Furl M (ed) Proceedings of the 13-th international conference production diseases in farm animals, Leipzig, pp 207–213
6. Hajer GR, van Haeften WT, Visseren FLJ (2008) Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 29:2959–2971
7. Weiss R (2007) Fat distribution and storage: how much, where, and how. Eur J Endocrinol 157:39–45
8. Dimitrova S, Penchev Georgiev I (2007) Relative contribution of decreased insulin sensitivity to deterioration of glucose homeostasis. Bulg J Vet Med 10:205–221
9. Corcoran MP, Fava SL, Fielding RA (2007) Skeletal muscle lipid deposition and insulin resistance: effect of dietary fatty acids and exercise. Am J Clin Nutr 85:662–677
10. Schenk S, Saberi M, Olefsky JM (2008) Insulin sensitivity: modulation by nutrients and inflammation. J Clin Invest 118:2992–3002
11. Fedor D, Kelley DS (2009) Prevention of insulin resistance by n-3 polyunsaturated fatty acids. Curr Opin Clin Nutr Metab Care 12:138–146
12. Ajiro K, Sawamura M, Ikeda K, Nara Y, Nishimura M, Ishida H, Seino Y, Yamori Y (2000) Beneficial effects of fish oil on glucose metabolism in spontaneously hypertensive rats. Clin Exp Pharmacol Physiol 27:412–415
13. Lombardo YB, Chicco A (2006) Effects of dietary polyunsaturated n-3 fatty acids on dyslipidemia and insulin resistance in rodents and humans. A review. J Nutr Biochem 17:1–13
14. Tandy S, Chung RWS, Wat E, Kamili A, Berge К, Griinari M, Cohn JS (2009) Dietary krill oil supplementation reduces hepatic steatosis, glycemia, and hypercholesterolemia in high-fat-fed mice. J Agric Food Chem 57:9339–9345
15. Ulven S, Kirkhus B, Lamglait A, Basu S, Elind E, Haider T, Berge K, Vik H, Pedersen J (2011) Metabolic effects of krill oil are essentially similar to those of fish oil but at lower dose of EPA and DHA, in healthy volunteers. Lipids 46:37–46
16. Burri L, Hoem N, Banni S, Berge K (2012) Marine omega-3 phospholipids: metabolism and biological activities. Int J Mol Sci 13:15401–15419
17. Burri L, Berge K, Wibrand K, Berge RK, Barger JL (2011) Differential effects of krill oil and fish oil on the hepatic transcriptome in mice. Front Genet 2:1–8
18. Ferramosca A, Conte A, Burri L, Berge K, De Nuccio F, Giudetti AM, Zara V (2012) A krill oil supplemented diet suppresses hepatic steatosis in high-fat fed rats. PLoS One 7:38797
19. Piscitelli F, Carta G, Bisogno T, Murru E, Cordeddu L, Berge K, Tandy S, Cohn JS, Griinari M, Banni S, Di Marzo V (2011) Effect of dietary krill oil supplementation on the endocannabinoidome of metabolically relevant tissues from high fat-fed mice. Nutr Metab (Lond) 8:51
20. Ferramosca A, Conte L, Zara V (2011) A krill oil supplemented diet reduces the activities of the mitochondrial tricarboxylate carrier and of the cytosolic lipogenic enzymes in rats. J Anim Physiol Anim Nutr 96:295–306
21. Vigerust NF, Bjorndal B, Bohov P, Brattelid T, Svardal A, Berge RK (2012) Krill oil versus fish oil in modulation of inflammation and lipid metabolism in mice transgenic for TNF-alpha. Eur J Nutr 52:1315–1325
22. Grimstad T, Bjorndal B, Cacabelos D, Aasprong OG, Janssen E, Omdal R, Svardal A, Hausken T, Bohov P, Portero-Otin M, Pamplona R, Berge RK (2012) Dietary supplementation of krill oil attenuates inflammation and oxidative stress in experimental ulcerative colitis in rats. Scand J Gastroenterol 47:49–58
23. Bunea R, El Farrah K, Deutsch L (2004) Evaluation of the effects of Neptune krill oil on the clinical course of hyperlipidemia. Altern Med Rev 9:420–428
24. Maki KC, Reeves MS, Farmer M, Griinari M, Berge K, Vik H, Hubacher R, Rains TM (2009) Krill oil supplementation increases plasma concentrations of eicosapentaenoic and docosahexaenoic acids in overweight and obese men and women. Nutr Res 29:609–615
25. Skarpańska-Stejnborn A, Pilaczyńska-Szcześniak L, Basta P, Foriasz J, Arlet J (2010) Effects of supplementation with Neptune krill oil (Euphasia superba) on selected redox parameters and pro-inflammatory markers in athletes during exhaustive exercise. J Hum Kinet 25:49–57
26. Banni S, Carta G, Murru E, Cordeddu L, Giordano E, Sirigu AR, Berge K, Vik H, Maki KC, Di Marzo V, Griinari M (2011) Krill oil significantly decreases 2-arachidonoylglycerol plasma levels in obese subjects. Nutr Metab (Lond) 8:7
27. Schuchardt JP, Schneider I, Meyer H, Neubronner J, von Schacky C, Hahn A (2011) 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. Lipids Health Dis 10:145
28. Fan J, Unoki H, Kojima N, Sun H, Shimoyamada H, Deng H, Okazaki M, Shikama H, Yamada N, Watanabe T (2001) Overexpression of lipoprotein lipase in transgenic rabbits inhibits diet-induced hypercholesterolemia and atherosclerosis. J Biol Chem 276:40071–40079
29. Kitajima S, Morimoto M, Liu E, Koike T, Higaki Y, Taura Y, Mamba K, Itamoto K, Watanabe T, Tsutsumi K, Yamada N, Fan J (2004) Overexpression of lipoprotein lipase improves insulin resistance induced by a high-fat diet in transgenic rabbits. Diabetologia 47:1202–1209
30. Kawai T, Ito T, Ohwada K, Mera Y, Matsushita M, Tomoike H (2006) Hereditary postprandial hypertriglyceridemic rabbit exhibits insulin resistance and central obesity. A novel model of metabolic syndrome. Arterioscler Thromb Vasc Biol 26:2752–2757
31. Georgiev IP, Georgieva TM, Ivanov V, Dimitrova S, Kanelov I, Vlaykova T, Tanev S, Zaprianova D, Dichlianova E, Penchev G, Lazarov L, Vachkova E, Roussenov A (2011) Effects of castration-induced visceral obesity and antioxidant treatment on lipid profile and insulin sensitivity in New Zealand white rabbits. Res Vet Sci 90:196–204
32. Neschen S, Morino K, Dong J, Wang-Fischer Y, Cline G, Romanelli AJ, Rossbacher JC, Moore I, Regittnig W, Munoz DS, Kim JH, Shulman GI (2007) N-3 fatty acids preserve insulin sensitivity in vivo in a peroxisome proliferator-activated receptor-α-dependent manner. Diabetes 56:1034–1041
33. Kopecky J, Rossmeisl M, Flachs P, Kuda O, Brauner P, Jilkova Z, Stankova B, Tvrzicka E, Bryhn M (2009) N-3 PUFA: bioavailability and modulation of adipose tissue function. Proc Nutr Soc 68:361–369
34. Buckley JD, Howe PR (2009) Anti-obesity effects of long-chain omega3 polyunsaturated fatty acids. Obes Rev 10:648–659
35. Yamazaki RK, Brito GA, Coelho I, Pequitto DC, Yamaguchi AA, Borghetti G, Schiessel DL, Kryczyk M, Machado J, Rocha RE, Aikawa J, Iagher F, Naliwaiko K, Tanhoffer RA, Nunes EA, Fernandes LC (2011) Low fish oil intake improves insulin sensitivity, lipid profile and muscle metabolism on insulin resistant MSG-obese rats. Lipids Health Dis 10:66
36. Liu E, Kitajima S, Higaki Y, Morimoto M, Sun H, Watanabe T, Yamada N, Fan J (2005) High lipoprotein lipase activity increases insulin sensitivity in transgenic rabbits. Metabolism 54:132–138
37. Zhao S, Chu Y, Zhang C, Lin Y, Xu K, Yang P, Fan J, Liu E (2007) Diet-induced central obesity and insulin resistance in rabbits. J Anim Physiol Anim Nutr 92:105–111
38. Appleton DJ, Rand JS, Sunvold GD (2005) Basal plasma insulin and homeostasis model assessment (HOMA) are indicators of insulin sensitivity in cats. J Feline Med Surg 7:183–193
39. Mattheeuws D, Rottiers R, Kaneko JJ, Vermeulen A (1984) Diabetes mellitus in dogs: relationship of obesity to glucose tolerance and insulin response. Am J Vet Res 45:98–103
40. Chen H, Sullivan G, Quon MJ (2005) Assessing the predictive accuracy of QUICKI as a surrogate index for insulin sensitivity using a calibration model. Diabetes 54:1914–1925
41. Ciampelli M, Leoni F, Cucinelli F, Mancuso S, Panunzi S, De Gaetano A, Lanzone A (2005) Assessment of insulin sensitivity from measurements in the fasting state and during an oral glucose tolerance test in polycystic ovary syndrome and menopausal patients. J Clin Endocrinol Metab 90:1398–1406
42. Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27:1487–1495
43. Larson BT, Lawler DF, Spitznagel EL, Kealy RD (2003) Improved glucose tolerance with lifetime diet restriction favorably affects disease and survival in dogs. J Nutr 133:2887–2892
44. Slavov E, Penchev Georgiev I, Dzhelebov P, Kanelov I, Andonova M, Georgieva TM, Dimitrova S (2010) High-fat feeding and Staphylococcus intermedius infection impair beta cell function and insulin sensitivity in mongrel dogs. Vet Res Commun 34:205–215
45. Berge RK, Flatmark T, Osmundsen H (1984) Enhancement of long-chain acyl-CoA hydrolase activity in peroxisomes and mitochondria of rat liver by peroxisomal proliferators. Eur J Biochem 141:637–644
46. Bremer J (1981) The effect of fasting on the activity of liver carnitine palmitoyltransferase and its inhibition by malonyl-CoA. Biochim Biophys Acta 665:628–631
47. Skorve J, al-Shurbaji A, Asiedu D, Bjorkhem I, Berglund L, Berge RK (1993) On the mechanism of the hypolipidemic effect of sulfur-substituted hexadecanedioic acid (3-thiadicarboxylic acid) in normolipidemic rats. J Lipid Res 34:1177–1185
48. Madsen L, Rustan AC, Vaagenes H, Berge K, Dyroy E, Berge RK (1999) Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 34:951–963
49. Nelson RW, Himsel CA, Feldman EC, Bottoms GD (1990) Glucose tolerance and insulin response in normal-weight and obese cats. Am J Vet Res 51:1357–1362
50. Thiess S, Becskei C, Tomsa K, Lutz TA, Wanner M (2004) Effects of high carbohydrate and high fat diet on plasma metabolite levels and on i.v. glucose tolerance test in intact and neutered male cats. J Feline Med Surg 6:207–218
51. Appleton DJ, Rand JS, Sunvold GD (2001) Insulin sensitivity decreases with obesity, and lean cats with low insulin sensitivity are at greatest risk of glucose intolerance with weight gain. J Feline Med Surg 3:211–228
52. Hays NP, Galassetti PR, Coker RH (2008) Prevention and treatment of type 2 diabetes: current role of lifestyle, natural product, and pharmacological intervention. Pharmacol Ther 118:181–191
53. Sharma AM, Staels B (2007) Peroxisome proliferator-activated receptor gamma and adipose tissue-understanding obesity-related changes in regulation of lipid and glucose metabolism. J Clin Endocrinol Metab 92:386–395
54. Rosenson RS (2008) Effect of fenofibrate on adiponectin and inflammatory biomarkers in metabolic syndrome patients. Obesity 17:504–509
55. Banerji MA, Buckley MC, Chaiken RL, Gordon D, Lebovitz HE, Kral JG (1995) Liver fat, serum triglycerides and visceral adipose tissue in insulin-sensitive and insulin-resistant black men with NIDDM. Int J Obes Relat Metab Disord 19:846–850
56. Hwang JH, Stein DT, Barzilai N, Cui MH, Tonelli J, Kishore P, Hawkins M (2007) Increased intra-hepatic triglycerides is associated with peripheral insulin resistance: in vivo MR imaging and spectroscopy studies. Am J Physiol Endocrinol Metab 293:1663–1669
57. Kim HJ, Takahashi M, Ezaki O (1999) Fish oil feeding decreases mature sterol regulatory element-binding protein 1 (SREBP-1) by down-regulation of SREBP1c mRNA in mouse liver. J Biol Chem 274:25892–25898
58. Jump DB (2008) N-3 polyunsaturated fatty acid regulation of hepatic gene transcription. Curr Opin Lipidol 19:242–247
59. Buckley JD, Howe PR (2010) Long-chain omega-3 polyunsaturated fatty acids may be beneficial for reducing obesity—a review. Nutrients 2:1212–1230
60. Burri L, Thoresen GH, Berge RK (2010) The role of PPARα activation in liver and muscle. PPAR Res. doi:10.1155/2010/542359
61. Kostiuk MA, Keller BO, Berthiaume LG (2010) Palmitoylation of ketogenic enzyme HMGCS2 enhances its interaction with PPARα and transcription at the Hmgcs2 PPRE. FASEB J 24:1914–1924
62. Vilà-Brau A, De Sousa-Coelho AL, Mayordomo C, Haro D, Marrero PF (2011) Human HMGCS2 regulates mitochondrial fatty acid oxidation and FGF21 expression in HepG2 cell line. J Biol Chem 286:20423–20430
63. Yu C, Chen Y, Cline GW, Zhang D, Zong H, Wang Y, Bergeron R, Kim JK, Cushman SW, Cooney GJ, Atcheson B, White MF, Kraegen EW, Shulman GI (2002) Mechanism by which fatty acids inhibit insulin activation of insulin receptor substrate-1 (IRS-1)-associated phosphatidylinositol 3-kinase activity in muscle. J Biol Chem 277:50230–50236