Skip to main content
SpringerLink
Log in

Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

We hypothesized that replacing fish oil with 18:3n-3-rich linseed oil may enable salmon to maintain the levels of tissue n-3HUFA levels through a combination of increased desaturation activity and increased substrate fatty acid provision. To this end we investigated desaturation/elongation of [1-14C18:3n-3 in hepatocytes and intestinal enterocytes, and determined the extent to which 18:3n-3 was oxidized and desaturated by measuring both simultaneously in a combined assay. Salmon smolts were stocked randomly into five seawater pens and fed for 40 weeks on diets in which the fish oil was replaced in a graded manner by linseed oil. At the end of the trial, fatty acyl desaturation/elongation and oxidation activities were determined in isolated hepatocytes and intestinal enterocytes using [1-14C]18:3n-3 as substrate, and samples of liver and intestinal tissue were collected for analysis of lipid and fatty acid composition. The results showed that, despite increased desaturation of [1-14C]18:3n-3 in hepatocytes, provision of dietary 18:3n-3 did not prevent the decrease in tissue n-3HUFA in fish fed linseed oil. Intestinal enterocytes were a site of significant fatty acid desaturation but, in contrast to hepatocytes, the activity was not increased by feeding linseed oil and was generally lower in fish fed linseed oil compared to fish fed only fish oil. In contrast, oxidation of [1-14C]18:3n-3 in enterocytes was generally increased in fish fed linseed oil compared to fish fed the diet containing only fish oil. However, oxidation of [1-14C]18:3n-3 in hepatocytes was 4- to 8-fold lower than in enterocytes and was not affected by diet. Furthermore, oxidation of [1-14C]18:3n-3 in enterocytes exceeded desaturation irrespective of dietary treatment, whereas similar amounts of [1-14C]18:3n-3 were desaturated and oxidized in hepatocytes from fish fed only fish oil and desaturation exceeded oxidation by 3-fold in fish fed the diet containing 100% linseed oil. The molecular mechanisms underpinning these results were discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ackman, R.G. 1980. Fish lipids, part 1. In: Advances in Fish Science and Technology. pp. 87–103. Edited by Connell, J.J. Fishing News Books, Farnham, U.K.

    Google Scholar 

  • Barlow, S. 2000. Fishmeal and oil: sustainable feed ingredients for aquafeeds. Global Aquacult. Advocate 4: 85–88.

    Google Scholar 

  • Bell, J. G., Dick, J. R., McVicar, A. H., Sargent, J. R. and Thompson, K. D. 1993. Dietary sunflower, linseed and fish oils affect phospholipid fatty acid composition, development of cardiac lesion, phospholipase activity and eicosanoid production in Atlantic salmon (Salmo salar). Prostaglandins, Leukotrienes Essent. Fatty Acids 49: 665–673.

    Article  CAS  Google Scholar 

  • Bell, J.G., McEvoy, J., Tocher, D.R., McGhee, F., Campbell, P.J. and Sargent, J.R. 2001a. Replacement of fish oil with rape seed oil in diets of Atlantic salmon (Salmo salar) affects tissue lipid compositions and hepatocyte fatty acid metabolism. J. Nutr. 131: 1535–1543.

    PubMed  CAS  Google Scholar 

  • Bell, J.G., Henderson, R.J., Tocher, D.R., McGhee, F., Dick, J.R., Porter, A., Smullen, R. and Sargent, J.R. 2002. Substituting fish oil with crude palm oil in the diet of Atlantic salmon (Salmo salar) affects tissue fatty acid compositions and hepatic fatty acid metabolism. J. Nutr.132: 222–230.

    PubMed  CAS  Google Scholar 

  • Bell, J.G., Tocher, D.R., Farndale, B.M., Cox, D.I., McKinney, R.W. and Sargent, J.R. 1997. The effect of dietary lipid on polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Lipids 32: 515–525.

    PubMed  CAS  Google Scholar 

  • Bell, M.V., Dick, J.R. and Porter, A.E.A. 2001b. Biosynthesis and tissue deposition of docosahexaenoic acid (22:6n-3) in rainbow trout (Oncorhynchus mykiss). Lipids 36: 1153–1159.

    PubMed  CAS  Google Scholar 

  • Bell, M.V., Dick, J.R. and Porter, A.E.A. 2003. Pyloric ceca are a major site of 22:6n-3 synthesis in rainbow trout (Oncorhynchus mykiss). Lipids 39: 39–44.

    Google Scholar 

  • Berge, R.K., Madsen, L., Vaagenes, H., Tronstad, K.J., Gottlicher, M. and Rustan, A.C. 1999. 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. Biochem. J. 343: 191–197.

    Article  PubMed  CAS  Google Scholar 

  • Brenner, R.R. 1981. Nutritional and hormonal factors influencing desaturation of essential fatty acids. Prog. Lipid Res. 20: 41–47.

    Article  PubMed  CAS  Google Scholar 

  • Cho, H. P., Nakamura, M.T. and Clarke, S.D. 1999a. Cloning, expression, and nutritional regulation of the mammalian Δ-6 desaturase. J. Biol. Chem. 274: 471–477.

    Article  PubMed  CAS  Google Scholar 

  • Cho, H. P., Nakamura, M.T. and Clarke, S.D. 1999b. Cloning, expression, and fatty acid regulation of the human Δ-5 desaturase. J. Biol. Chem. 274: 37335–37339.

    Article  PubMed  CAS  Google Scholar 

  • Christie, W.W. (1982) Lipid Analysis, 2nd Edition. P.207. Pergamon Press, Oxford.

    Google Scholar 

  • Folch, J., Lees, M. and Sloane-Stanley, G.H. 1957. A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226: 497–509.

    PubMed  CAS  Google Scholar 

  • Frøyland, L., Asiedu, D.K., Vaagenes, H., Garras, A., Lie, Ø., Totland, G.K. and Berge, R.K. 1995. Tetradecylthioacetic acid incorporated into very low density lipoprotein: Changes in the fatty acid composition and reduced plasma lipids in cholesterol-fed hamsters. J. Lipid. Res. 36: 2529–2540.

    PubMed  Google Scholar 

  • Frøyland, L., Helland, K., Totland, G.K., Kryvi, H. and Berge, R.K. 1996. A hypolipidemic peroxisome proliferating fatty acid induces polydispersity of rat liver mitochondria. Biol. Cell. 87: 105–112.

    Article  PubMed  Google Scholar 

  • Frøyland, L., Lie, Ø. and Berge, R.K. 2000. Mitochondrial and peroxisomal beta-oxidation capacities in various tissues from Atlantic salmon Salmo salar. Aquaculture Nutr. 6: 85–89.

    Article  Google Scholar 

  • Frøyland, L., Madsen. L., Eckhoff, K.M., Lie, Ø. and Berge, R. 1998. Carnitine palmitoyltransferase I, carnitine palmitoyl transferase II, and acyl-CoA oxidase activities in Atlantic salmon (Salmo salar). Lipids 33: 923–930.

    PubMed  Google Scholar 

  • Ghioni, C., Tocher, D.R. and Sargent, J.R. 1997. The effect of culture on morphology, lipid and fatty acid composition, and polyunsaturated fatty acid metabolism of rainbow trout (Oncorhynchus mykiss) skin cells. Fish Physiol. Biochem. 16: 499–513.

    Article  CAS  Google Scholar 

  • Grønn, M., Christensen, E., Hagve, T.-A. and Christophersen, B.O. 1992a. Effects of dietary purified eicosapentaenoic acid (20:5 (n-3)) and docosahexaenoic acid (22:6(n-3)) on fatty acid desaturation and oxidation in isolated rat liver cells. Biochim. Biophys. Acta 1125: 35–43.

    PubMed  Google Scholar 

  • Grønn, M., Christensen, E., Hagve, T.-A. and Christophersen, B.O. 1992b. Effects of clofibrate feeding on essential fatty acid desaturation and oxidation in isolated rat liver cells. Biochim. Biophys. Acta 1123: 170–176.

    PubMed  Google Scholar 

  • Henderson, R. J. and Tocher, D. R. 1987. Lipid composition and biochemistry of freshwater fish. Prog. Lipid Res. 26: 281–347.

    Article  PubMed  CAS  Google Scholar 

  • Henderson, R.J. and Tocher, D.R. 1992. Thin-layer chromatography. In: Lipid Analysis: A Practical Approach. pp. 65–111. Edited by Hamilton, R.J. and Hamilton, S. Oxford University Press, Oxford.

    Google Scholar 

  • Holman, R.T. 1986. Control of polyunsaturated fatty acids in tissue lipids. J. Am. Coll. Nutr. 5: 183–211.

    PubMed  CAS  Google Scholar 

  • Ji, H., Bradley, T.M. and Tremblay, G.C. 1996. Atlantic salmon (Salmo salar) fed L-carnitine exhibit altered intermediary metabolism and reduced tissue lipid, but no change in growth rate. J. Nutr. 126: 1937–1950.

    PubMed  CAS  Google Scholar 

  • Jump, D. B. 2002. The biochemistry of n-3 polyunsaturated fatty acids. J. Biol. Chem. 277: 8755–8758.

    Article  PubMed  CAS  Google Scholar 

  • Jump, D. B., Thelen, A., Ren, B. and Mater, M. 1999. Multiple mechanisms for polyunsaturated fatty acid regulation of hepatic gene transcription. Prostaglandins Leukotrienes Essent. Fatty Acids 60: 345–349.

    Article  CAS  Google Scholar 

  • Leaver, M. J., Wright, J. and George, S.G. 1998. A peroxisome proliferator activated receptor gene from the marine flatfish, the plaice (Pleuronectes platessa). Mar. Env. Res. 46: 75–79.

    Article  CAS  Google Scholar 

  • Lowry, O.H., Rosebrough, N.J., Farr, A.L. and Randall, R.J. 1951. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193: 265–275.

    PubMed  CAS  Google Scholar 

  • Madsen, L., Frøyland, L., Dyroy, E., Helland, K. and Berge, R.K. 1998. Docosahexaenoic and eicosapentaenoic acids are differently metabolized in rat liver during mitochondria and peroxisome proliferation. J. Lipid Res. 39: 583–593.

    PubMed  CAS  Google Scholar 

  • Madsen, L., Rustan, A.C., Vaagenes, H., Berge, K., Dyroy, E. and Berge, R.K. 1999. Eicosapentaenoic and docosahexaenoic acid affect mitochondrial and peroxisomal fatty acid oxidation in relation to substrate preference. Lipids 34: 951–963.

    PubMed  CAS  Google Scholar 

  • Padley, F.B., Gunstone, F.D. and Harwood, J.L. 1986. Occurrence and characteristics of oils and fats. pp. 49–170. In: The Lipid Handbook. Edited by Gunstone, F.D., Harwood, J.L. and Padley, F.B. Chapman and Hall, London.

    Google Scholar 

  • Ruyter, B. Andersen, O., Dehli, A., Ostlund Farrants, A.-K., Gjoen, T. and Thomassen, M.S. 1997. Peroxisome proliferator activated receptors in Atlantic salmon (Salmo salar): effects on PPAR transcription and acyl-CoA oxidase activity in hepatocytes by peroxisome proliferators and fatty acids. Biochim. Biophys. Acta 1348: 331–338.

    PubMed  CAS  Google Scholar 

  • Sargent J.R. and Tacon, A. 1999. Development of farmed fish: a nutritionally necessary alternative to meat. Proc. Nutr. Soc. 58: 377–383.

    PubMed  CAS  Google Scholar 

  • Sargent, J.R., Bell, J.G., Bell, M.V., Henderson, R.J. and Tocher, D.R. 1995. Requirement criteria for essential fatty acids. J. Appl. Ichthyol. 11: 183–198.

    CAS  Google Scholar 

  • Sargent, J.R., Bell, J.G., McEvoy, L., Tocher, D.R. and Estevez, A. 1999. Recent developments in the essential fatty acid nutrition of fish. Aquaculture 177: 191–199.

    Article  CAS  Google Scholar 

  • Sargent, J. R., Tocher, D. R. and Bell, J. G. 2002. The lipids. pp. 181–257. In: Fish Nutrition. Edited by Halver, J. E. and Hardy, R.W. Academic Press, San Diego.

    Google Scholar 

  • Seiliez, I., Panseat, S., Kaushik, S. and Bergot, P. 2001. Cloning, tissue distribution and nutritional regulation of a Δ6–desaturaselike enzyme in rainbow trout. Comp. Biochem. Physiol. 130B: 83–93.

    CAS  Google Scholar 

  • Small, G.M. and Connock, M.J. 1981. Palmitoyl-CoA oxidase in goldfish (Carassius auratus): detection in several tissues and subcellular localization in intestinal peroxisomes. Comp. Biochem. Physiol. 68B: 151–153

    CAS  Google Scholar 

  • Tidwell, J.H. and Allan, G.L. 2002. Fish as food: aquaculture's contribution. World Aquaculture 33: 44–48.

    Google Scholar 

  • Tocher, D.R. and Harvie, D.G. 1988. Fatty acid compositions of the major phosphoglycerides from fish neural tissues: (n-3) and (n-6) polyunsaturated fatty acids in rainbow trout (Salmo gairdneri, L.) and cod (Gadus morhua) brains and retinas. Fish Physiol. Biochem. 5: 229–239.

    Article  CAS  Google Scholar 

  • Tocher, D.R. and Sargent, J.R. 1993. No relationship between morphology changes and metabolism of α-linolenate and eicosapentaenoate in rainbow trout (Oncorhynchus mykiss) astroglial cells in primary culture. Comp. Biochem. Physiol. 106C: 211–219.

    CAS  Google Scholar 

  • Tocher, D.R., Bell, J.G., Dick, J.R. and Sargent, J.R. 1997. Fatty acyl desaturation in isolated hepatocytes from Atlantic salmon (Salmo salar): Stimulation by dietary borage oil containing γ-linolenic acid. Lipids 32: 1237–1247.

    PubMed  CAS  Google Scholar 

  • Tocher, D.R., Bell, J.G., Henderson, R.J., McGhee, F., Mitchell, D. and Morris, P.C. 2000. The effect of dietary linseed and rapeseed oils on polyunsaturated fatty acid metabolism in Atlantic salmon (Salmo salar) undergoing parr-smolt transformation. Fish. Physiol. Biochem. 23: 59–73.

    Article  CAS  Google Scholar 

  • Tocher, D.R., Bell, J.G., MacGlaughlin, P., McGhee, F. and Dick, J.R. 2001. Hepatocyte fatty acid desaturation and polyunsaturated fatty acid composition of liver in salmonids: Effects of dietary vegetable oil. Comp. Biochem Physiol. 130: 257–270.

    Article  CAS  Google Scholar 

  • Tocher, D.R., Bell, J.G. and Sargent, J.R. 1996. Induction of Δ9–fatty acyl desaturation in rainbow trout (Oncorhynchus mykiss) liver by dietary manipulation. Comp. Biochem. Physiol. 113B: 205–212.

    CAS  Google Scholar 

  • Tocher, D.R., Sargent, J.R. and Frerichs, G.N. 1988. The fatty acid compositions of established fish cell lines after long-term culture in mammalian sera. Fish Physiol. Biochem. 5: 219–227.

    Article  CAS  Google Scholar 

  • Torstensen, B.E., Li, Ø. and Frøyland, L. 2000. Lipid metabolism and tissue composition in Atlantic salmon (Salmo salar L.)-Effects of capelin-, palm-and oleic acid enriched sunflower oil as dietary lipid sources. Lipids 35: 653–664.

    PubMed  CAS  Google Scholar 

  • U.S. National Research Council. 1993. Nutrient requirements of fish, National Academy Press, Washington D.C.

    Google Scholar 

  • Wilson, R. and Sargent, J.R. 1992. High resolution separation of polyunsaturated fatty acids by argentation thin-layer chromatography. J. Chromatogr. 623: 403–407.

    Article  CAS  Google Scholar 

  • Zar, J.H. 1984. Biostatistical Analysis, 2nd Edition. Prentice-Hall, Englewood Cliffs.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Aquaculture, University of Stirling, Stirling, FK9 4LA, Scotland

    Douglas R. Tocher, Jorge Fonseca-Madrigal, J. Gordon Bell, James R. Dick, R. James Henderson & John R. Sargent

Authors
  1. Douglas R. Tocher
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge Fonseca-Madrigal
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. Gordon Bell
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. James R. Dick
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. James Henderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. John R. Sargent
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tocher, D.R., Fonseca-Madrigal, J., Bell, J.G. et al. Effects of diets containing linseed oil on fatty acid desaturation and oxidation in hepatocytes and intestinal enterocytes in Atlantic salmon (Salmo salar). Fish Physiology and Biochemistry 26, 157–170 (2002). https://doi.org/10.1023/A:1025416731014

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1025416731014

Search

Navigation