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The appearance of rods in the eyes of herring and increased di-docosahexaenoyl molecular species of phospholipids

Published online by Cambridge University Press:  11 May 2009

M. V. Bell
Affiliation:
NERC Unit of Aquatic Biochemistry, School of Natural Sciences, University of Stirling, Stirling, FK9 4LA
J. R. Dick
Affiliation:
NERC Unit of Aquatic Biochemistry, School of Natural Sciences, University of Stirling, Stirling, FK9 4LA

Extract

The retina of larval herring (Clupea harengus L.) contains only cones, with rods recruited progressively from about eight weeks onwards. The molecular species composition of phospholipids from the eyes of herring of different ages was determined to find whether the appearance of di-docosahexaenoyl molecular species (di22:6n-3) of phospholipids, which are characteristic of rod outer segment membranes in higher vertebrates, coincided with the appearance of rods. In the eyes of larval herring (cone-only retina) di22:6n-3 molecular species comprised 25.9% of phosphatidylethanolamine (PE), 22.9% of phosphatidylserine (PS) and 4.2% of phosphatidylcholine (PC). In the eyes of adult herring (rod:cone ratio of about 20:1) the proportion of di22:6n-3 molecular species had increased to 49.5%, 39.0% and 16.8% in PE, PS and PC, respectively. Juvenile herring had intermediate values of di22:6n-3 phospholipids. The results confirm the hypothesis that the amounts of di22:6n-3 molecular species of phospholipids in retina increase during development as rods appear, and also show that cones contain smaller amounts of these unique lipids. Three other molecular species containing docosahexaenoic acid, 16:0/22:6n-3, 18:1/22:6n-3 and 18:0/22:6n-3 were also major components of eye phospholipids, emphasizing the important role of 22:6n-3 in vision.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1993

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References

Anderson, G. J., Connor, W. E. & Corliss, J. D., 1990. Docosahexaenoic acid is the preferred dietary n-3 fatty acid for the development of the brain and retina. Pediatric Research, 27, 8997.CrossRefGoogle ScholarPubMed
Arbuckle, L. D., Rioux, F. M., Mackinnon, M. J., Hrboticky, N. & Innis, S. M., 1991. Response of (n-3) and (n-6) fatty acids in piglet brain, liver and plasma to increasing, but low, fish oil supplementation of formula. Journal of Nutrition, 121, 15361547.CrossRefGoogle ScholarPubMed
Bell, M. V., 1989. Molecular species analysis of phosphoglycerides from the ripe roes of cod (Gadus morhua). Lipids, 24, 585588.CrossRefGoogle Scholar
Bell, M. V. & Dick, J. R., 1991. Molecular species composition of the major diacyl glycerophospholipids from muscle, liver, retina and brain of cod (Gadus morhua). Lipids, 26, 565573.CrossRefGoogle Scholar
Bell, M. V. & Tocher, D. R., 1989. Molecular species composition of the major phospholipids in brain and retina from rainbow trout (Salmo gairdneri). Occurrence of high levels of di-(n-3) polyun-saturated fatty acid species. Biochemical Journal, 264, 909915.CrossRefGoogle ScholarPubMed
Blaxter, J. H. S. & Jones, M. P., 1967. The development of the retina and retinomotor responses in the herring. Journal of the Marine Biological Association of the United Kingdom, 47, 677697.CrossRefGoogle Scholar
Blaxter, J. H. S. & Staines, M., 1970. Pure-cone retinae and retinomotor responses in larval teleosts. Journal of the Marine Biological Association of the United Kingdom, 50, 449460.CrossRefGoogle Scholar
Bourre, J. M., Pascal, G., Durand, G., Masson, M., Dumont, O. & Piciotti, M., 1984. Alterations in the fatty acid composition of rat brain cells (neurons, astrocytes and oligodendrocytes) and of subcellular fractions (myelin and synaptosomes) induced by a diet devoid of n-3 fatty acids. Journal of Neurochemistry, 43, 342348.CrossRefGoogle ScholarPubMed
Chen, H. & Anderson, R. E., 1992. Lipids of frog retinal pigment epithelium: comparison with rod outer segments, retina, plasma and red blood cells. Current Eye Research, 11, 793800.CrossRefGoogle ScholarPubMed
Connor, W. E., Neuringer, M., Barstad, L. & Lin, D. S., 1984. Dietary deprivation of linolenic acid in rhesus monkeys: effects on plasma and tissue fatty acid composition and on visual function. Transactions of the Association of American Physicians, 97, 19.Google ScholarPubMed
Dratz, E. A. & Deese, A. J., 1986. The role of docosahexaenoic acid (22:6n-3) in biological membranes: examples from photoreceptors and model membrane bilayers. In Health effects of polyunsatu-rated fatty acids in seafoods (ed. Simopoulos, A. P.), pp. 319351. New York: Academic Press.CrossRefGoogle Scholar
Dyer, J. R. & Greenwood, C. E., 1991. Neural 22-carbon fatty acids in the weanling rat respond rapidly and specifically to a range of dietary linoleic to α-linolenic fatty acid ratios. Journal of Neurochemistry, 56, 19211931.CrossRefGoogle ScholarPubMed
Enslen, M., Milon, H. & Malnoe, A., 1991. Effect of low intake of n-3 fatty acids during development on brain phospholipid fatty acid composition and exploratory behaviour in rats. Lipids, 26, 203208.CrossRefGoogle ScholarPubMed
Fliesler, S. J. & Anderson, R. E., 1983. Chemistry and metabolism of lipids in the vertebrate retina. Progress in Lipid Research, 22, 79131.CrossRefGoogle ScholarPubMed
Folch, J., Lees, M. & Sloane, Stanley G. H., 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497509.CrossRefGoogle ScholarPubMed
Goto, J., Goto, N., Shamsa, F., Saito, M., Komatsu, S., Suzaki, K. & Nambara, T., 1983. New sensitive derivatization of hydroxysteroids for high-performance liquid chromatography with fluorescence detection. Analytica Chimica Acta, 147, 397400.CrossRefGoogle Scholar
Louie, K., Wiegand, R. D. & Anderson, R. E., 1988. Docosahexaenoate-containing molecular species of glycerophospholipids from frog retinal rod outer segments show different rates of biosynthesis and turnover. Biochemistry, 27, 90149020.CrossRefGoogle ScholarPubMed
Neuringer, M., Anderson, G. T. & Connor, W. E., 1988. The essentiality of n-3 fatty acids for the development and function of the retina and brain. Annual Review of Nutrition, 8, 517541.CrossRefGoogle ScholarPubMed
Neuringer, M., Connor, W. E., Lin, D. S., Barstad, L. & Luck, S., 1986. Biochemical and functional effects of prenatal and postnatal ω3 fatty acid deficiency on retina and brain in rhesus monkeys. Proceedings of the National Academy of Sciences of the United States of America, 83, 40214025.CrossRefGoogle Scholar
Neuringer, M., Connor, W. E., Petten, C. Van & Barstad, L., 1984. Dietary omega-3 fatty acid deficiency and visual loss in infant rhesus monkeys. Journal of Clinical Investigation, 73, 272276.CrossRefGoogle ScholarPubMed
Nicol, J. A. C., Arnott, H. J., Mizuno, G. R., Ellison, E. C. & Chipault, J. R., 1972. Occurrence of glyceryl tridocosahexaenoate in the eye of the sand trout Cynoscion arenarius. Lipids, 7, 171177.CrossRefGoogle ScholarPubMed
Renkonen, O., 1965. Individual molecular species of different phospholipid classes. Part II. A method of analysis. Journal of the American Oil Chemists Society, 42, 298304.CrossRefGoogle Scholar
Rodriguez, De Turco E. B., Gordon, W. C., & Bazan, N. G., 1991. Rapid and selective uptake, metabolism, and cellular distribution of docosahexaenoic acid among rod and cone photoreceptor cells in the frog retina. Journal of Neuroscience, 11, 36673678.CrossRefGoogle Scholar
Rodriguez, De Turco E. B., Gordon, W. C., Peyman, G. A. & Bazan, N. G., 1990. Preferential uptake and metabolism of docosahexaenoic acid in membrane phospholipids from rod and cone photoreceptor cells of human and monkey retinas. Journal of Neuroscience Research, 27, 522532.Google Scholar
Salem, N., Kim, H.-Y. & Yergey, J. A., 1986. Docosahexaenoic acid: membrane function and metabolism. In Health effects of polyunsaturated fatty acids in seafoods (ed. Simopoulos, A. P.), pp. 263317. New York: Academic Press.CrossRefGoogle Scholar
Sargent, J. R., Bell, M. V. & Tocher, D. R., 1993. Docosahexaenoic acid and the development of brain and retina in marine fish. In Omega-3 fatty acids, metabolism and biological effects (ed. Drevon, C. A.et al.), pp. 139149. Basel, Switzerland: Birkhauser Verlag.Google Scholar
Sargent, J. R., Henderson, R. J. & Tocher, D. R., 1989. The lipids. In Fish nutrition, 2nd ed. (ed. Halver, J. E.), pp. 153218. San Diego: Academic Press.Google Scholar
Stinson, A. M., Wiegand, R. D. & Anderson, R. E., 1991. Fatty acid and molecular species compositions of phospholipids and diacylglycerols from rat retinal membranes. Experimental Eye Research, 52, 213218.CrossRefGoogle ScholarPubMed
Takamura, H. & Kito, M., 1991. A highly sensitive method for quantitative analysis of phospholipid molecular species by high-performance liquid chromatography. Journal of Biochemistry, 109, 436439.CrossRefGoogle ScholarPubMed
Tinoco, J., 1982. Dietary requirements and functions of α-linolenic acid in animals. Progress in Lipid Research, 21, 145.CrossRefGoogle ScholarPubMed
Vandenheuvel, F. A. & Farmer, E. H., 1951. The hydrogen value-refractivity relationship of unsaturated fatty acids of natural origin. Journal of the American Oil Chemists Society, 28, 512513.CrossRefGoogle Scholar
Vitiello, F. & Zanetta, J.-P., 1978. Thin-layer chromatography of phospholipids. Journal ofChromatography, 166, 637640.CrossRefGoogle ScholarPubMed
Wainwright, P. E., Huang, Y. S., Bulmanfleming, B., Mills, D. E., Redden, P. & McCutcheon, D., 1991. The role of n-3 essential fatty acids in brain and behavioural development - a cross-fostering study in the mouse. Lipids, 26, 3745.CrossRefGoogle ScholarPubMed