The Anti-Obesogenic Effect of Lean Fish Species is Influenced by the Fatty Acid Composition in Fish Fillets
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
FINS 900842
Fiskeri - og havbruksnæringens forskningsfond
PubMed
33022997
PubMed Central
PMC7600456
DOI
10.3390/nu12103038
PII: nu12103038
Knihovny.cz E-zdroje
- Klíčová slova
- DHA, EPA, endocannabinoids, marine protein source, n-3 PUFA, nutrition, obesity and mice, phospholipids, seafood,
- MeSH
- dieta s vysokým obsahem proteinů metody MeSH
- dieta s vysokým obsahem tuků metody MeSH
- drůbeží výrobky MeSH
- Gadus morhua * MeSH
- kyselina eikosapentaenová metabolismus MeSH
- kyseliny dokosahexaenové metabolismus MeSH
- kyseliny mastné omega-3 analýza MeSH
- látky proti obezitě analýza MeSH
- mastné kyseliny analýza MeSH
- metabolismus lipidů MeSH
- myši inbrední C57BL MeSH
- myši MeSH
- potrava z moře (živočišná) analýza MeSH
- sumci * MeSH
- tuková tkáň metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- myši MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- kyselina eikosapentaenová MeSH
- kyseliny dokosahexaenové MeSH
- kyseliny mastné omega-3 MeSH
- látky proti obezitě MeSH
- mastné kyseliny MeSH
Fillets from marine fish species contain n-3 polyunsaturated fatty acids (PUFAs) in the form of phospholipids (PLs). To investigate the importance of PL-bound n-3 PUFAs in mediating the anti-obesogenic effect of lean seafood, we compared the anti-obesogenic properties of fillets from cod with fillets from pangasius, a fresh water fish with a very low content of PL-bound n-3 PUFAs. We prepared high-fat/high-protein diets using chicken, cod and pangasius as the protein sources, and fed male C57BL/6J mice these diets for 12 weeks. Mice fed the diet containing cod gained less adipose tissue mass and had smaller white adipocytes than mice fed the chicken-containing diet, whereas mice fed the pangasius-containing diet were in between mice fed the chicken-containing diet and mice fed the cod-containing diet. Of note, mice fed the pangasius-containing diet exhibited reduced glucose tolerance compared to mice fed the cod-containing diet. Although the sum of marine n-3 PUFAs comprised less than 2% of the total fatty acids in the cod-containing diet, this was sufficient to significantly increase the levels of eicosapentaenoic acid (EPA) and docosahexaenoic acids (DHA) in mouse tissues and enhance production of n-3 PUFA-derived lipid mediators as compared with mice fed pangasius or chicken.
Department Institute of Marine Research NO 5817 Bergen Norway
Department of Biology University of Copenhagen DK 2100 Copenhagen Denmark
Zobrazit více v PubMed
Fogelholm M., Anderssen S., Gunnarsdottir I., Lahti-Koski M. Dietary macronutrients and food consumption as determinants of long-term weight change in adult populations: A systematic literature review. Food Nutr. Res. 2012;56 doi: 10.3402/fnr.v56i0.19103. PubMed DOI PMC
Mozaffarian D., Hao T., Rimm E.B., Willett W.C., Hu F.B. Changes in diet and lifestyle and long-term weight gain in women and men. N. Engl. J. Med. 2011;364:2392–2404. doi: 10.1056/NEJMoa1014296. PubMed DOI PMC
Smith J.D., Hou T., Ludwig D.S., Rimm E.B., Willett W., Hu F.B., Mozaffarian D. Changes in intake of protein foods, carbohydrate amount and quality, and long-term weight change: Results from 3 prospective cohorts. Am. J. Clin. Nutr. 2015;101:1216–1224. doi: 10.3945/ajcn.114.100867. PubMed DOI PMC
Liaset B., Øyen J., Jacques H., Kristiansen K., Madsen L. Seafood intake and the development of obesity, insulin resistance and type 2 diabetes. Nutr. Res. Rev. 2019;32:146–167. doi: 10.1017/S0954422418000240. PubMed DOI PMC
Madsen L., Petersen R.K., Kristiansen K. Regulation of adipocyte differentiation and function by polyunsaturated fatty acids. Biochim. Biophys. Acta. 2005;30:266–286. doi: 10.1016/j.bbadis.2005.03.001. PubMed DOI
Huang C.W., Chien Y.S., Chen Y.J., Ajuwon K.M., Mersmann H.M., Ding S.T. Role of n-3 Polyunsaturated Fatty Acids in Ameliorating the Obesity-Induced Metabolic Syndrome in Animal Models and Humans. Int. J. Mol. Sci. 2016;17:1689. doi: 10.3390/ijms17101689. PubMed DOI PMC
Kuda O., Rossmeisl M., Kopecky J. Omega-3 fatty acids and adipose tissue biology. Mol. Asp. Med. 2018;64:147–160. doi: 10.1016/j.mam.2018.01.004. PubMed DOI
Spitze A.R., Wong D.L., Rogers Q.R., Fascetti A.J. Taurine concentrations in animal feed ingredients; cooking influences taurine content. J. Anim. Physiol. Anim. Nutr. 2003;87:251–262. doi: 10.1046/j.1439-0396.2003.00434.x. PubMed DOI
Borck P.C., Vettorazzi J.F., Branco R.C.S., Batista T.M., Santos-Silva J.C., Nakanishi V.Y., Boschero A.C., Ribeiro R.A., Carneiro E.M. Taurine supplementation induces long-term beneficial effects on glucose homeostasis in ob/ob mice. Amino Acids. 2018;50:765–774. doi: 10.1007/s00726-018-2553-3. PubMed DOI
Kim K.S., Doss H.M., Kim H.J., Yang H.I. Taurine Stimulates Thermoregulatory Genes in Brown Fat Tissue and Muscle without an Influence on Inguinal White Fat Tissue in a High-Fat Diet-Induced Obese Mouse Model. Foods. 2020;9:688. doi: 10.3390/foods9060688. PubMed DOI PMC
Kim K.S., Jang M.J., Fang S., Yoon S.G., Kim I.Y., Seong J.K., Yang H.I., Hahm D.H. Anti-obesity effect of taurine through inhibition of adipogenesis in white fat tissue but not in brown fat tissue in a high-fat diet-induced obese mouse model. Amino Acids. 2019;51:245–254. doi: 10.1007/s00726-018-2659-7. PubMed DOI
Liaset B., Madsen L., Hao Q., Criales G., Mellgren G., Marschall H.U., Hallenborg P., Espe M., Frøyland L., Kristiansen K. Fish protein hydrolysate elevates plasma bile acids and reduces visceral adipose tissue mass in rats. Biochim. Biophys. Acta. 2009;4:254–262. doi: 10.1016/j.bbalip.2009.01.016. PubMed DOI
Liaset B., Hao Q., Jørgensen H., Hallenborg P., Du Z.Y., Ma T., Marschall H.U., Kruhøffer M., Li R., Li Q., et al. Nutritional regulation of bile acid metabolism is associated with improved pathological characteristics of the metabolic syndrome. J. Biol. Chem. 2011;286:28382–28395. doi: 10.1074/jbc.M111.234732. PubMed DOI PMC
López Y.R., Pérez-Torres I., Zúñiga-Muñoz A., Lans V.G., Díaz-Díaz E., Castro E.S., Espejel R.V. Effect of Glycine on Adipocyte Hypertrophy in a Metabolic Syndrome Rat Model. Curr. Drug. Deliv. 2016;13:158–169. doi: 10.2174/156720181301160314151554. PubMed DOI
Tastesen H.S., Keenan A.H., Madsen L., Kristiansen K., Liaset B. Scallop protein with endogenous high taurine and glycine content prevents high-fat, high-sucrose-induced obesity and improves plasma lipid profile in male C57BL/6J mice. Amino Acids. 2014;46:1659–1671. doi: 10.1007/s00726-014-1715-1. PubMed DOI PMC
Aakre I., Næss S., Kjellevold M., Markhus M.W., Alvheim A.R., Dalane J., Kielland E., Dahl L. New data on nutrient composition in large selection of commercially available seafood products and its impact on micronutrient intake. Food Nutr. Res. 2019;63 doi: 10.29219/fnr.v63.3573. PubMed DOI PMC
Lie O., Lambertsen G. Fatty acid composition of glycerophospholipids in seven tissues of cod (Gadus morhua), determined by combined high-performance liquid chromatography and gas chromatography. J. Chromatogr. 1991;565:119–129. doi: 10.1016/0378-4347(91)80376-N. PubMed DOI
Zhang T.T., Xu J., Wang Y.M., Xue C.H. Health benefits of dietary marine DHA/EPA-enriched glycerophospholipids. Prog. Lipid. Res. 2019;75:20. doi: 10.1016/j.plipres.2019.100997. PubMed DOI
Fauske K.R., Bernhard A., Fjaere E., Myrmel L.S., Froyland L., Kristiansen K., Liaset B., Madsen L. Effects of Frozen Storage on Phospholipid Content in Atlantic Cod Fillets and the Influence on Diet-Induced Obesity in Mice. Nutrients. 2018;10:695. doi: 10.3390/nu10060695. PubMed DOI PMC
Schuchardt J.P., Hahn A. Bioavailability of long-chain omega-3 fatty acids. Prostaglandins Leukot. Essent. Fat. Acids. 2013;89:1–8. doi: 10.1016/j.plefa.2013.03.010. PubMed DOI
Ghasemifard S., Turchini G.M., Sinclair A.J. Omega-3 long chain fatty acid “bioavailability”: A review of evidence and methodological considerations. Prog. Lipid. Res. 2014;56:92–108. doi: 10.1016/j.plipres.2014.09.001. PubMed DOI
Ulven S.M., Holven K.B. Comparison of bioavailability of krill oil versus fish oil and health effect. Vasc. Health Risk. Manag. 2015;11:511–524. doi: 10.2147/VHRM.S85165. PubMed DOI PMC
Cholewski M., Tomczykowa M., Tomczyk M. A Comprehensive Review of Chemistry, Sources and Bioavailability of Omega-3 Fatty Acids. Nutrients. 2018;10:1662. doi: 10.3390/nu10111662. PubMed DOI PMC
Liisberg U., Fauske K.R., Kuda O., Fjaere E., Myrmel L.S., Norberg N., Froyland L., Graff I.E., Liaset B., Kristiansen K., et al. Intake of a Western diet containing cod instead of pork alters fatty acid composition in tissue phospholipids and attenuates obesity and hepatic lipid accumulation in mice. J. Nutr. Biochem. 2016;33:119–127. doi: 10.1016/j.jnutbio.2016.03.014. PubMed DOI
Rossmeisl M., Jilkova Z.M., Kuda O., Jelenik T., Medrikova D., Stankova B., Kristinsson B., Haraldsson G.G., Svensen H., Stoknes I., et al. 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. 2012;7:e38834. doi: 10.1371/journal.pone.0038834. PubMed DOI PMC
Zhang L.Y., Ding L., Shi H.H., Xu J., Xue C.H., Zhang T.T., Wang Y.M. Eicosapentaenoic acid in the form of phospholipids exerts superior anti-atherosclerosis effects to its triglyceride form in ApoE(-/-) mice. Food Funct. 2019;10:4177–4188. doi: 10.1039/C9FO00868C. PubMed DOI
Batetta B., Griinari M., Carta G., Murru E., Ligresti A., Cordeddu L., Giordano E., Sanna F., Bisogno T., Uda S., et al. Endocannabinoids may mediate the ability of (n-3) fatty acids to reduce ectopic fat and inflammatory mediators in obese Zucker rats. J. Nutr. 2009;139:1495–1501. doi: 10.3945/jn.109.104844. PubMed DOI
Piscitelli F., Carta G., Bisogno T., Murru E., Cordeddu L., Berge K., Tandy S., Cohn J.S., Griinari M., Banni S., et al. Effect of dietary krill oil supplementation on the endocannabinoidome of metabolically relevant tissues from high-fat-fed mice. Nutr. Metab. 2011;8:1743–7075. doi: 10.1186/1743-7075-8-51. PubMed DOI PMC
Alvheim A.R., Malde M.K., Osei-Hyiaman D., Lin Y.H., Pawlosky R.J., Madsen L., Kristiansen K., Froyland L., Hibbeln J.R. Dietary linoleic acid elevates endogenous 2-AG and anandamide and induces obesity. Obesity (Silver Spring) 2012;20:1984–1994. doi: 10.1038/oby.2012.38. PubMed DOI PMC
Rossmeisl M., Medrikova D., van Schothorst E.M., Pavlisova J., Kuda O., Hensler M., Bardova K., Flachs P., Stankova B., Vecka M., et al. Omega-3 phospholipids from fish suppress hepatic steatosis by integrated inhibition of biosynthetic pathways in dietary obese mice. Biochim. Biophys. Acta. 2014;2:267–278. doi: 10.1016/j.bbalip.2013.11.010. PubMed DOI
Tillander V., Bjørndal B., Burri L., Bohov P., Skorve J., Berge R.K., Alexson S.E. Fish oil and krill oil supplementations differentially regulate lipid catabolic and synthetic pathways in mice. Nutr. Metab. 2014;11:1743–7075. doi: 10.1186/1743-7075-11-20. PubMed DOI PMC
Ahmmed M.K., Ahmmed F., Tian H., Carne A., Bekhit A.E. Marine omega-3 (n-3) phospholipids: A comprehensive review of their properties, sources, bioavailability, and relation to brain health. Compr. Rev. Food Sci. Food Saf. 2020;19:64–123. doi: 10.1111/1541-4337.12510. PubMed DOI
Liisberg U., Myrmel L.S., Fjaere E., Ronnevik A.K., Bjelland S., Fauske K.R., Holm J.B., Basse A.L., Hansen J.B., Liaset B., et al. The protein source determines the potential of high protein diets to attenuate obesity development in C57BL/6J mice. Adipocyte. 2016;5:196–211. doi: 10.1080/21623945.2015.1122855. PubMed DOI PMC
Mariotti F., Tomé D., Mirand P.P. Converting nitrogen into protein--beyond 6.25 and Jones’ factors. Crit. Rev. Food Sci. Nutr. 2008;48:177–184. doi: 10.1080/10408390701279749. PubMed DOI
Fjaere E., Aune U.L., Roen K., Keenan A.H., Ma T., Borkowski K., Kristensen D.M., Novotny G.W., Mandrup-Poulsen T., Hudson B.D., et al. Indomethacin Treatment Prevents High Fat Diet-induced Obesity and Insulin Resistance but Not Glucose Intolerance in C57BL/6J Mice. J. Biol. Chem. 2014;289:16032–16045. doi: 10.1074/jbc.M113.525220. PubMed DOI PMC
Lillefosse H.H., Tastesen H.S., Du Z.Y., Ditlev D.B., Thorsen F.A., Madsen L., Kristiansen K., Liaset B. Hydrolyzed casein reduces diet-induced obesity in male C57BL/6J mice. J. Nutr. 2013;143:1367–1375. doi: 10.3945/jn.112.170415. PubMed DOI
Dumlao D.S., Buczynski M.W., Norris P.C., Harkewicz R., Dennis E.A. High-throughput lipidomic analysis of fatty acid derived eicosanoids and N-acylethanolamines. Biochim. Biophys. Acta. 2011;1811:724–736. doi: 10.1016/j.bbalip.2011.06.005. PubMed DOI PMC
Holm J.B., Ronnevik A., Tastesen H.S., Fjaere E., Fauske K.R., Liisberg U., Madsen L., Kristiansen K., Liaset B. Diet-induced obesity, energy metabolism and gut microbiota in C57BL/6J mice fed Western diets based on lean seafood or lean meat mixtures. J. Nutr. Biochem. 2016;31:127–136. doi: 10.1016/j.jnutbio.2015.12.017. PubMed DOI
Myrmel L.S., Fauske K.R., Fjære E., Bernhard A., Liisberg U., Hasselberg A.E., Øyen J., Kristiansen K., Madsen L. The Impact of Different Animal-Derived Protein Sources on Adiposity and Glucose Homeostasis during Ad Libitum Feeding and Energy Restriction in Already Obese Mice. Nutrients. 2019;11:1153. doi: 10.3390/nu11051153. PubMed DOI PMC
Fjaere E., Myrmel L.S., Lutzhoft D.O., Andersen H., Holm J.B., Kiilerich P., Hannisdal R., Liaset B., Kristiansen K., Madsen L. Effects of exercise and dietary protein sources on adiposity and insulin sensitivity in obese mice. J. Nutr. Biochem. 2019;66:98–109. doi: 10.1016/j.jnutbio.2019.01.003. PubMed DOI
Flachs P., Horakova O., Brauner P., Rossmeisl M., Pecina P., Franssen-van Hal N., Ruzickova J., Sponarova J., Drahota Z., Vlcek C., et al. Polyunsaturated fatty acids of marine origin upregulate mitochondrial biogenesis and induce beta-oxidation in white fat. Diabetologia. 2005;48:2365–2375. doi: 10.1007/s00125-005-1944-7. PubMed DOI
Huang X.F., Xin X., McLennan P., Storlien L. Role of fat amount and type in ameliorating diet-induced obesity: Insights at the level of hypothalamic arcuate nucleus leptin receptor, neuropeptide Y and pro-opiomelanocortin mRNA expression. Diabetes Obes. Metab. 2004;6:35–44. doi: 10.1111/j.1463-1326.2004.00312.x. PubMed DOI
Mori T., Kondo H., Hase T., Tokimitsu I., Murase T. Dietary fish oil upregulates intestinal lipid metabolism and reduces body weight gain in C57BL/6J mice. J. Nutr. 2007;137:2629–2634. doi: 10.1093/jn/137.12.2629. PubMed DOI
Rossmeisl M., Jelenik T., Jilkova Z., Slamova K., Kus V., Hensler M., Medrikova D., Povysil C., Flachs P., Mohamed-Ali V., et al. Prevention and reversal of obesity and glucose intolerance in mice by DHA derivatives. Obesity (Silver Spring) 2009;17:1023–1031. doi: 10.1038/oby.2008.602. PubMed DOI
Ruzickova J., Rossmeisl M., Prazak T., Flachs P., Sponarova J., Veck M., Tvrzicka E., Bryhn M., Kopecky J. Omega-3 PUFA of marine origin limit diet-induced obesity in mice by reducing cellularity of adipose tissue. Lipids. 2004;39:1177–1185. doi: 10.1007/s11745-004-1345-9. PubMed DOI
Ukropec J., Reseland J.E., Gasperikova D., Demcakova E., Madsen L., Berge R.K., Rustan A.C., Klimes I., Drevon C.A., Sebokova E. The hypotriglyceridemic effect of dietary n-3 FA is associated with increased beta-oxidation and reduced leptin expression. Lipids. 2003;38:1023–1029. doi: 10.1007/s11745-006-1156-z. PubMed DOI
Wang H., Storlien L.H., Huang X.F. Effects of dietary fat types on body fatness, leptin, and ARC leptin receptor, NPY, and AgRP mRNA expression. Am. J. Physiol. Endocrinol Metab. 2002;282:E1352–E1359. doi: 10.1152/ajpendo.00230.2001. PubMed DOI
Salem N., Kuratko C.N. A reexamination of krill oil bioavailability studies. Lipids Health Dis. 2014;13 doi: 10.1186/1476-511X-13-137. PubMed DOI PMC
Alvheim A.R., Torstensen B.E., Lin Y.H., Lillefosse H.H., Lock E.-J., Madsen L., Hibbeln J.R., Malde M.K. Dietary linoleic acid elevates endogenous 2-arachidonoylglycerol and anandamide in Atlantic salmon (Salmo salar L.) and mice, and induces weight gain and inflammation in mice. Br. J. Nutr. 2013;109:1508–1517. doi: 10.1017/S0007114512003364. PubMed DOI PMC
Midtbø L.K., Borkowska A.G., Bernhard A., Rønnevik A.K., Lock E.-J., Fitzgerald M.L., Torstensen B.E., Liaset B., Brattelid T., Pedersen T.L., et al. Intake of farmed Atlantic salmon fed soybean oil increases hepatic levels of arachidonic acid-derived oxylipins and ceramides in mice. J. Nutr. Biochem. 2015;26:585–595. doi: 10.1016/j.jnutbio.2014.12.005. PubMed DOI
Midtbø L.K., Ibrahim M.M., Myrmel L.S., Aune U.L., Alvheim A.R., Liland N.S., Torstensen B.E., Rosenlund G., Liaset B., Brattelid T. Intake of farmed Atlantic salmon fed soybean oil increases insulin resistance and hepatic lipid accumulation in mice. PLoS ONE. 2013;8:e53094. doi: 10.1371/journal.pone.0053094. PubMed DOI PMC
Naughton S.S., Mathai M.L., Hryciw D.H., McAinch A.J. Fatty Acid modulation of the endocannabinoid system and the effect on food intake and metabolism. Int. J. Endocrinol. 2013;2013:361895. doi: 10.1155/2013/361895. PubMed DOI PMC
Ravinet Trillou C., Delgorge C., Menet C., Arnone M., Soubrie P. CB1 cannabinoid receptor knockout in mice leads to leanness, resistance to diet-induced obesity and enhanced leptin sensitivity. Int. J. Obes. Relat. Metab. Disord. 2004;28:640–648. doi: 10.1038/sj.ijo.0802583. PubMed DOI
Ravinet Trillou C., Arnone M., Delgorge C., Gonalons N., Keane P., Maffrand J.P., Soubrie P. Anti-obesity effect of SR141716, a CB1 receptor antagonist, in diet-induced obese mice. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2003;284:R345–R353. doi: 10.1152/ajpregu.00545.2002. PubMed DOI
Cota D., Marsicano G., Tschop M., Grubler Y., Flachskamm C., Schubert M., Auer D., Yassouridis A., Thone-Reineke C., Ortmann S., et al. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J. Clin. Invest. 2003;112:423–431. doi: 10.1172/JCI17725. PubMed DOI PMC
Di Marzo V., Goparaju S.K., Wang L., Liu J., Batkai S., Jarai Z., Fezza F., Miura G.I., Palmiter R.D., Sugiura T., et al. Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature. 2001;410:822–825. doi: 10.1038/35071088. PubMed DOI
Osei-Hyiaman D., DePetrillo M., Pacher P., Liu J., Radaeva S., Batkai S., Harvey-White J., Mackie K., Offertaler L., Wang L., et al. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J. Clin. Invest. 2005;115:1298–1305. doi: 10.1172/JCI200523057. PubMed DOI PMC
Perwitz N., Wenzel J., Wagner I., Büning J., Drenckhan M., Zarse K., Ristow M., Lilienthal W., Lehnert H., Klein J. Cannabinoid type 1 receptor blockade induces transdifferentiation towards a brown fat phenotype in white adipocytes. Diabetes Obes. Metab. 2010;12:158–166. doi: 10.1111/j.1463-1326.2009.01133.x. PubMed DOI
Tedesco L., Valerio A., Cervino C., Cardile A., Pagano C., Vettor R., Pasquali R., Carruba M.O., Marsicano G., Lutz B., et al. Cannabinoid type 1 receptor blockade promotes mitochondrial biogenesis through endothelial nitric oxide synthase expression in white adipocytes. Diabetes. 2008;57:2028–2036. doi: 10.2337/db07-1623. PubMed DOI PMC
Guo Y.Y., Li B.Y., Peng W.Q., Guo L., Tang Q.Q. Taurine-mediated browning of white adipose tissue is involved in its anti-obesity effect in mice. J. Biol. Chem. 2019;294:15014–15024. doi: 10.1074/jbc.RA119.009936. PubMed DOI PMC