Abstract
Monoalkyldiacylglycerol (MADG), an ether analog of triacylglycerols, is abundant in some marine animals such as deep-sea sharks and echinoderms. The present study aims to investigate the effects of an MADG-rich neutral lipid derived from Berryteuthis magister (MNB) on the lipid metabolism of diabetic/obese KK-Ay mice. Male mice (5 weeks old) were fed soybean oil (control group), MNB, or fish oil (FO) which contain the same amount of EPA and DHA in the form of triacylglycerols. MNB or FO supplementation resulted in a decrease in adipose tissue weights and blood glucose levels compared to the control mice. Interestingly, serum lipid levels in the MNB group were significantly lower than those of the control and FO groups. Although there was no difference in EPA and DHA levels in the tissues between the FO and MNB groups, a decrease in the number of lipoprotein particles was characteristically observed in the mice fed with MNB. Our results suggest that the MADG structure-dependent effect on lipoprotein synthesis and/or secretion partly accounted for the reduced serum lipids in KK-Ay mice by dietary MNB. This study advances the understanding of MADG as a nutraceutical and provides insights into the role of ether lipids in lipoprotein metabolism that can contribute to the development of prevention and treatment strategies for hyperlipidemia.
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References
Bakes MJ, Nichols PD (1995) Lipid, fatty acid and squalene composition of liver oil from six species of deep-sea sharks collected in southern Australian waters. Comp Biochem Physiol B Biochem Mol Biol 110(1):267–275
Benjamin EJ, Muntner P, Alonso A, Bittencourt MS, Callaway CW, Carson AP et al (2019) Heart disease and stroke statistics-2019 update: a report from the American Heart Association. Circulation 139(10):e56–e528
Buchman AL, Dubin MD, Moukarzel AA, Jenden DJ, Roch M, Rice KM et al (1995) Choline deficiency: a cause of hepatic steatosis during parenteral nutrition that can be reversed with intravenous choline supplementation. Hepatology 22(5):1399–1403
Destaillats F, Oliveira M, Bastic Schmid V, Masserey-Elmelegy I, Giuffrida F, Thakkar SK et al (2018) Comparison of the incorporation of DHA in circulatory and neural tissue when provided as triacylglycerol (TAG), monoacylglycerol (MAG) or phospholipids (PL) provides new insight into fatty acid bioavailability. Nutrients 10(5):620
Einarson TR, Acs A, Ludwig C, Panton UH (2018) Prevalence of cardiovascular disease in type 2 diabetes: a systematic literature review of scientific evidence from across the world in 2007–2017. Cardiovasc Diabetol 17(1):83
Ermolenko E, Latyshev N, Sultanov R, Kasyanov S (2016) Technological approach of 1-O-alkyl-sn-glycerols separation from Berryteuthis magister squid liver oil. J Food Sci Technol 53(3):1722–1726
Hashidate-Yoshida T, Harayama T, Hishikawa D, Morimoto R, Hamano F, Tokuoka SM et al (2015) Fatty acid remodeling by LPCAT3 enriches arachidonate in phospholipid membranes and regulates triglyceride transport. eLLife 4:e06328
Hayashi K, Kishimura H (2002) Amount and composition of diacyl glyceryl ethers in various tissue lipids of the deep-sea squid Berryteuthis magister. J Oleo Sci 51(8):523–530
Horrocks LA, Chapter IX (1972) Content, composition, and metabolism of mammalian and avian lipids that contain ether groups. Ether lipids chemistry and biology. Academic Press, Cambridge, pp 177–272
Iannitti T, Palmieri B (2010) An update on the therapeutic role of alkylglycerols. Mar Drugs 8(8):2267–2300
Magnusson CD, Haraldsson GG (2011) Ether lipids. Chem Phys Lipids 164(5):315–340
McDonagh TA, Metra M, Adamo M, Gardner RS, Baumbach A, Böhm M et al (2022) 2021 ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure: Developed by the task force for the diagnosis and treatment of acute and chronic heart failure of the European Society of Cardiology with the special contribution of the Heart Failure Association of the ESC. Revista Espanola De Cardiologia (English Ed) 75(6):523
Murota K, Takagi M, Watanabe Y, Tokumura A, Ohkubo T (2018) Roe-derived phospholipid administration enhances lymphatic docosahexaenoic acid-containing phospholipid absorption in unanesthetized rats. Prostaglandins Leukot Essent Fatty Acids 139:40–48
Parri A, Fitó M, Torres CF, Muñoz-Aguayo D, Schröder H, Cano JF et al (2016) Alkylglycerols reduce serum complement and plasma vascular endothelial growth factor in obese individuals. Inflammopharmacology 24(2–3):127–131
Paul S, Smith AAT, Culham K, Gunawan KA, Weir JM, Cinel MA et al (2021a) Shark liver oil supplementation enriches endogenous plasmalogens and reduces markers of dyslipidemia and inflammation. J Lipid Res 62:100092
Paul S, Rasmiena AA, Huynh K, Smith AAT, Mellett NA, Jandeleit-Dahm K et al (2021b) Oral supplementation of an alkylglycerol mix comprising different alkyl chains effectively modulates multiple endogenous plasmalogen species in mice. Metabolites 11(5):299
Prevot AF (1976) Utilization des colonnes capillaries de verre pour l’analyse des corps gras par chromotographie en phase gazeuse. Rev Fr Corps 23:409–423
Rong X, Wang B, Dunham MM, Hedde PN, Wong JS, Gratton E et al (2015) Lpcat3-dependent production of arachidonoyl phospholipids is a key determinant of triglyceride secretion. Elife 4:e06557
Usui S, Hara Y, Hosaki S, Okazaki M (2002) A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J Lipid Res 43(5):805–814
van der Veen JN, Kennelly JP, Wan S, Vance JE, Vance DE, Jacobs RL (2017) The critical role of phosphatidylcholine and phosphatidylethanolamine metabolism in health and disease. Biochim Biophys Acta Biomembr 1859(9, Part B):1558–1572
Verkade HJ, Fast DG, Rusiñol AE, Scraba DG, Vance DE (1993) Impaired biosynthesis of phosphatidylcholine causes a decrease in the number of very low density lipoprotein particles in the Golgi but not in the endoplasmic reticulum of rat liver. J Biol Chem 268(33):24990–24996
Yamamoto N, St Claire DA Jr, Homma S, Ngwenya BZ (1988) Activation of mouse macrophages by alkylglycerols, inflammation products of cancerous tissues. Cancer Res 48(21):6044–6049
Acknowledgements
We thank Dr. Toshio Kawai for providing squid samples. This work was supported by JSPS KAKENHI Grant number 20K06221 and The South Hokkaido Science Promotion Foundation.
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MK: conceptualization, methodology, investigation, data analysis, writing—visualization. NT: investigation, writing—review and editing. MH: data analysis, writing—review and editing, funding acquisition. FB: conceptualization, methodology, data analysis, resources, writing—original draft, visualization, supervision, funding acquisition.
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Kakimoto, M., Takatani, N., Hosokawa, M. et al. Reduction of serum lipid levels in diabetic obese KK-Ay mice using monoalkyldiacylglycerol-rich oil derived from Berryteuthis magister. Fish Sci 89, 243–251 (2023). https://doi.org/10.1007/s12562-022-01655-5
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DOI: https://doi.org/10.1007/s12562-022-01655-5