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Dietary ALA from Spinach Enhances Liver n-3 Fatty Acid Content to Greater Extent than Linseed Oil in Mice Fed Equivalent Amounts of ALA

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Lipids

Abstract

Although several works have reported absorption rate differences of n-3 polyunsaturated fatty acids (PUFA) bound to different lipid forms, such as ethyl ester, triacylglycerol (TAG), and phospholipids, no studies have investigated the effect of n-3 PUFA from glycolipids (GL). The present study compared the fatty acid contents of tissue and serum lipids from normal C57BL/6J mice fed two types of α-linolenic acid (ALA)-rich lipids, spinach lipid (SPL), and linseed oil (LO). ALA was primarily present as the GL form in SPL, while it existed as TAG in LO. Supplementation of both lipids increased ALA and its n-3 metabolites, eicosapentaenoic acid (EPA), docosapentaenoic acid (DPA), and docosahexaenoic acid, and decreased n-6 PUFA, linoleic acid and arachidonic acid, in the livers, small intestines, and sera of the treated mice compared with those of the control group. When the comparison between the SPL and LO diets containing the same amount of ALA was conducted, the EPA and DPA levels in the liver lipids from mice fed the SPL diet were significantly higher than those fed the LO diet. Additionally, the total contents of n-3 PUFA of lipids from the livers, small intestines, and sera of the SPL group were higher than those of the LO group.

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Abbreviations

ALA:

α-Linolenic acid

ARA:

Arachidonic acid

DGDG:

Digalactosyl diacylglycerol

DHA:

Docosahexaenoic acid

DPA:

Docosapentaenoic acid

EE:

Ethyl esters

EPA:

Eicosapentaenoic acid

FFA:

Free fatty acid

GC:

Gas chromatography

GL:

Galactolipids

LA:

Linoleic acid

LO:

Linseed oil

MGDG:

Monogalactosyl diacylglycerol

PC:

Phosphatidyl choline

PL:

Phospholipids

SPL:

Spinach lipids

SQDG:

Sulfoquinovosyl diacylglycerol

TAG:

Triacylglycerol

TL:

Total lipids

TLC:

Thin layer chromatography

References

  1. Harwood JL (1979) The synthesis of acyl lipids in plant tissues. Prog Lipid Res 18:55–86

    Article  PubMed  CAS  Google Scholar 

  2. Kamogawa H, Hosokawa M, Abe M, Miyashita K (2012) Carotenoid contents in Chlorella pyrenoidosa and concentration by saponification. Bull Fish Sci Hokkaido Univ 62:83–88 (Japanese)

    CAS  Google Scholar 

  3. Harwood JL (1980) Plant acyl lipids: structure, distribution and analysis. In: Stump PK, Conn EE (eds) Biochemistry of plants, vol 4. Academic Press, New York, pp 1–55

    Google Scholar 

  4. Block MA, Dorne AJ, Joyard J, Douce R (1983) Preparation and characterization of membrane fractions enriched in outer and inner envelope membranes from spinach chloroplasts. J Biol Chem 258:13281–13286

    PubMed  CAS  Google Scholar 

  5. Whitaker BD (1986) Fatty-acid composition of polar lipids in fruit and leaf chloroplasts of “16:3”—and “18:3”—plant species. Planta 169:313–319

    Article  PubMed  CAS  Google Scholar 

  6. O’Brien JS, Benson AA (1964) Isolation and fatty acid composition of the plant sulfolipid and galactolipids. J Lipid Res 5:432–436

    PubMed  Google Scholar 

  7. Bahl J, Francke B, Monéger R (1976) Lipid composition of envelopes, prolamellar bodies and other plastid membranes in etiolated, green and greening wheat leaves. Planta 129:193–201

    Article  PubMed  CAS  Google Scholar 

  8. Nichols BW (1965) The lipids of moss (Hypnum cupressiforme) and of the leaves of green holly (Ilex aquifolium). Phytochemistry 4:769–772

    Article  CAS  Google Scholar 

  9. Kim K-B, Nam YA, Kim HS, Hayes AW, Lee B-M (2014) α-Linolenic acid: nutraceutical, pharmacological and toxicological evaluation. Food Chem Toxicol 70:163–178

    Article  PubMed  CAS  Google Scholar 

  10. Allayee H, Roth N, Hodis HN (2009) Polyunsaturated fatty acids and cardiovascular disease: implications for nutrigenetics. J Nutrigenet Nutrigenomics 2:140–148

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  11. Harris WS, Miller M, Tighe AP, Davidson MH, Schaefer EJ (2008) Omega-3 fatty acids and coronary heart disease risk: clinical and mechanistic perspectives. Atherosclerosis 197:12–24

    Article  PubMed  CAS  Google Scholar 

  12. Mori TA (2014) Dietary n-3 PUFA and CVD: a review of the evidence. Proc Nutr Soc 73:57–64

    Article  PubMed  CAS  Google Scholar 

  13. Superko HR, Superko AR, Lundberg GP, Margolis B, Garrett BC, Nasir K, Agatston AS (2014) Omega-3 fatty acid blood levels clinical significance update. Curr Cardiovasc Risk Rep 8:407

    Article  PubMed  PubMed Central  Google Scholar 

  14. Wachira JK, Larson MK, Harris WS (2014) n-3 Fatty acids affect haemostasis but do not increase the risk of bleeding: clinical observations and mechanistic insights. Br J Nutr 111:1652–1662

    Article  PubMed  CAS  Google Scholar 

  15. Carnielli VP, Simonato M, Verlato G, Luijendijk I, De Curtis M, Sauer PJJ, Cogo PE (2007) Synthesis of long-chain polyunsaturated fatty acids in preterm newborns fed formula with long-chain polyunsaturated fatty acids. Am J Clin Nutr 86:1323–1330

    PubMed  CAS  Google Scholar 

  16. Williams CM, Burdge G (2006) Long-chain n-3 PUFA: plant v. marine sources. Proc Nutr Soc 65:42–50

    Article  PubMed  CAS  Google Scholar 

  17. Brenna JT, Salem N Jr, Sinclair AJ, Cunnane SC (2009) α-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fatty Acids 80:85–91

    Article  PubMed  CAS  Google Scholar 

  18. Domenichiello AF, Chen CT, Trepanier M-T, Stavro PM, Bazinet RP (2014) Whole body synthesis rates of DHA from α-linolenic acid are greater than brain DHA accretion and uptake rates in adult rats. J Lipid Res 55:62–74

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  19. Barceló-Coblijn G, Murphy EJ (2009) Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog Lipid Res 48:355–374

    Article  PubMed  CAS  Google Scholar 

  20. Kris-Etherton PM, Harris WS, Appel LJ (2002) Fish consumption, fish oil, omega-3 fatty acids, and cardiovascular disease. Circulation 106:2747–2757

    Article  PubMed  Google Scholar 

  21. Andersson L, Bratt C, Arnoldsson KC, Herslöf B, Olsson NU, Sternby B, Nilsson Å (1995) Hydrolysis of galactolipids by human pancreatic lipolytic enzymes and duodenal contents. J Lipid Res 36:1392–1400

    PubMed  CAS  Google Scholar 

  22. Sugawara T, Miyazawa T (2000) Digestion of plant monogalactosyldiacylglycerol and digalactosyldiacylglycerol in rat alimentary canal. J Nutr Biochem 11:147–152

    Article  PubMed  CAS  Google Scholar 

  23. Dyerberg J, Madsen P, Møller JM, Aardestrup I, Schmidt EB (2010) Bioavailability of marine n-3 fatty acid formulations. Prostaglandins Leukot Essent Fatty Acids 83:137–141

    Article  PubMed  CAS  Google Scholar 

  24. 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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Ramíreza M, Amatea L, Gil A (2001) Absorption and distribution of dietary fatty acids from different sources. Early Hum Dev 65:S95–S101

    Article  Google Scholar 

  26. Tanaka Y, Ohkubo T, Fukuda N, Hibino H (2003) Effect of molecular forms on distribution of docosahexaenoic acid into organs in mice. J Oleo Sci 52:89–97

    Article  CAS  Google Scholar 

  27. Tang X, Li Z-J, Xu J, Xue Y, Li J-Z, Wang J-F, Yanagita T, Xue C-H, Wang Y-M (2012) Short term effects of different omega-3 fatty acid formulation on lipid metabolism in mice fed high or low fat diet. Lipids Health Dis 11:70

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Ulven SM, Kirkhus B, Lamglait A, Basu S, Elind E, Haider T, Berge K, Vik H, Pedersen JI (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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Prevot AF, Mordret FX (1976) Utilisation des colonnes capillaries de verre pour l’analyse des corps gras par chromotographie en phase gazeuse. Rev Fse Corps Gras 23:409–423

    CAS  Google Scholar 

  30. Folch J, Lees M, Stanley GHS (1957) A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509

    PubMed  CAS  Google Scholar 

  31. Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917

    Article  PubMed  CAS  Google Scholar 

  32. Blanchard H, Pédrono F, Boulier-Monthéan N, Catheline D, Rioux V, Legrand P (2013) Comparative effects of well-balanced diets enriched in α-linolenic or linoleic acids on LC-PUFA metabolism in rat tissues. Prostaglandins Leukot Essent Fatty Acids 88:383–389

    Article  PubMed  CAS  Google Scholar 

  33. Delplanque B, Du Q, Agnani G, LeRuyet P, Martin JC (2013) A dairy fat matrix providing alpha-linolenic acid (ALA) is better than a vegetable fat mixture to increase brain DHA accretion in young rats. Prostaglandins Leukot Essent Fatty Acids 88:115–120

    Article  PubMed  CAS  Google Scholar 

  34. Poudyal H, Panchal SK, Ward LC, Brown L (2013) Effects of ALA, EPA and DHA in high-carbohydrate, high-fat diet-induced metabolic syndrome in rats. J Nutr Biochem 24:1041–1052

    Article  PubMed  CAS  Google Scholar 

  35. Yamaguchi T, Sugimura R, Shimajiri J, Suda M, Abe M, Hosokawa M, Miyashita K (2012) Oxidative stability of glyceroglycolipids containing polyunsaturated fatty acids. J Oleo Sci 61:505–513

    Article  PubMed  CAS  Google Scholar 

  36. Burri L, Hoem N, Banni S, Berge K (2012) Marine omega-3 phospholipids: metabolism and biological activities. Int J Mol Sci 13:15401–15419

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  37. Mun S, Decker EA, McClements DJ (2007) Influence of emulsifier type on in vitro digestibility of lipid droplets by pancreatic lipase. Food Res Int 40:770–781

    Article  CAS  Google Scholar 

  38. Salem NM, Lin YH, Moriguchi T, Lim SY, Salem N Jr, Hibbeln JR (2015) Distribution of omega-6 and omega-3 polyunsaturated fatty acids in the whole rat body and 25 compartments. Prostaglandins Leukot Essent Fatty Acids 100:13–20

    Article  PubMed  CAS  Google Scholar 

  39. Ghasemifard S, Hermon K, Turchini GM, Sinclair AJ (2014) Metabolic fate (absorption, β-oxidation and deposition) of long-chain n-3 fatty acids is affected by sex and by the oil source (krill oil or fish oil) in the rat. Br J Nutr 114:684–692

    Article  CAS  Google Scholar 

  40. Ghasemifard S, Turchini GM, Sinclair AJ (2014) Omega-3 long chain fatty acid “bioavailability”: a review of evidence and methodological considerations. Prog Lipid Res 56:92–108

    Article  PubMed  CAS  Google Scholar 

  41. Domenichiello AF, Kitson AP, Bazinet RP (2015) Is docosahexaenoic acid synthesis from α-linolenic acid sufficient to supply the adult brain? Prog Lipid Res 59:54–66

    Article  PubMed  CAS  Google Scholar 

  42. Guichardant M, Calzada C, Bernoud-Hubac N, Lagarde M, Véricel E (2015) Omega-3 polyunsaturated fatty acids and oxygenated metabolism in atherothrombosis. Biochim Biophys Acta 1851:485–495

    Article  PubMed  CAS  Google Scholar 

  43. Bruno A, Rossi C, Marcolongo G, Di Lena A, Venzo A, Berrie CP, Corda D (2005) Selective in vivo anti-inflammatory action of the galactolipid monogalactosyldiacylglycerol. Eur J Pharmacol 524:159–168

    Article  PubMed  CAS  Google Scholar 

  44. Maeda N, Hada T, Yoshida H, Mizushina Y (2007) Inhibitory effect on replicative DNA polymerases, human cancer cell proliferation, and in vivo anti-tumor activity by glycolipids from spinach. Curr Med Chem 14:955–967

    Article  PubMed  CAS  Google Scholar 

  45. Maeda N, Kokai Y, Ohtani S, Sahara H, Kumamoto-Yonezawa Y, Kuriyama I, Hada T, Sato N, Yoshida H, Mizushina Y (2008) Anti-tumor effect of orally administered spinach glycolipid fraction on implanted cancer cells, colon-26, in mice. Lipids 43:741–748

    Article  PubMed  CAS  Google Scholar 

  46. Ma L, Lin X-M (2010) Effects of lutein and zeaxanthin on aspects of eye health. J Sci Food Agric 90:2–12

    Article  PubMed  CAS  Google Scholar 

  47. Ruban AV, Johnson MP (2010) Xanthophylls as modulators of membrane protein function. Arch Biochem Biophys 504:78–85

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the “Scientific technique research promotion program from agriculture, forestry, fisheries, and food industry” from the Ministry of Agriculture, Forestry, and Fisheries in Japan.

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Correspondence to Kazuo Miyashita.

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The authors declare that there are no conflicts of interest.

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Kuroe, M., Kamogawa, H., Hosokawa, M. et al. Dietary ALA from Spinach Enhances Liver n-3 Fatty Acid Content to Greater Extent than Linseed Oil in Mice Fed Equivalent Amounts of ALA. Lipids 51, 39–48 (2016). https://doi.org/10.1007/s11745-015-4086-9

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  • DOI: https://doi.org/10.1007/s11745-015-4086-9

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