Half-lives of docosahexaenoic acid in rat brain phospholipids are prolonged by 15 weeks of nutritional deprivation of n-3 polyunsaturated fatty acids

Journal of Neurochemistry

Volumn 91, Issue 5, 2004, Pages 1125-1137

  DeMar Jr , James C ^a   Ma, Kaizong ^a   Bell, Jane M ^a   Rapoport, Stanley I ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

Brain; Deprivation; Docosahexaenoic; N 3 polyunsaturated fatty acids; Phospholipids; Rat

Indexed keywords

BRAIN PROTEIN; DOCOSAHEXAENOIC ACID; LINOLEIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHOLIPID DERIVATIVE; POLYUNSATURATED FATTY ACID; TRACER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BIOAVAILABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DECOMPOSITION; DEGRADATION KINETICS; DRUG BRAIN LEVEL; DRUG DISTRIBUTION; DRUG HALF LIFE; EXPERIMENTAL TEST; INJECTION; INTERMETHOD COMPARISON; MALE; NEUROCHEMISTRY; NEWBORN; NONHUMAN; NUTRITIONAL DEFICIENCY; PRIORITY JOURNAL; PROTEIN DEFICIENCY; RADIOACTIVITY; RAT;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BRAIN; BRAIN CHEMISTRY; DIET; DOCOSAHEXAENOIC ACIDS; FATTY ACIDS, OMEGA-3; FATTY ACIDS, UNSATURATED; FOOD DEPRIVATION; HALF-LIFE; INJECTIONS, INTRAVENTRICULAR; MALE; PHOSPHOLIPIDS; PLASMA; RADIOACTIVITY; RATS; RATS, LONG-EVANS; TIME FACTORS; TRIGLYCERIDES; TRITIUM;

ANIMALIA;

EID: 9744284920     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2004.02789.x     Document Type: Article

References (106)

1. Auestad N., Scott D. T., Janowsky J. S. et al. (2003) Visual, cognitive, and language assessments at 39 months: a follow-up study of children fed formulas containing long-chain polyunsaturated fatty acids to 1 year of age. Pediatrics 112, 177-183.
2. Axelrod J. (1990) Receptor-mediated activation of phospholipase A2 and arachidonic acid release in signal transduction. Biochem. Soc. Trans. 18, 503-507.
3. Bazan N. G., Rodriguez de Turco E. B. and Gordon W. C. (1994) Docosahexaenoic acid supply to the retina and its conservation in photoreceptor cells by active retinal pigment epithelium-mediated recycling. World Rev. Nutr. Diet 75, 120-123.
4. Birch E. E., Garfield S., Hoffman D. R., Uauy R. and Birch D. G. (2000) A randomized controlled trial of early dietary supply of long-chain polyunsaturated fatty acids and mental development in term infants. Dev. Med. Child. Neurol. 42, 174-181.
5. Bourre J. M., Francois M., Youyou A., Dumont O., Piciotti M., Pascal G. and Durand G. (1989) The effects of dietary α-linolenic acid on the composition of nerve membranes, enzymatic activity, amplitude of electrophysiological parameters, resistance to poisons and performance of learning tasks in rats. J. Nutr. 119, 1880-1892.
6. Bourre J. M., Dumont O. S., Piciotti M. J., Pascal G. A. and Durand G. A. (1992) Dietary alpha-linolenic acid deficiency in adult rats for 7 months does not alter brain docosahexaenoic acid content, in contrast to liver, heart and testes. Biochim. Biophys. Acta 1124, 119-122.
7. Brossard N., Croset M., Pachiaudi C., Riou J. P., Tayot J. L. and Lagarde M. (1996) Retroconversion and metabolism of [13C]22: 6n-3 in humans and rats after intake of a single dose of [13C]22: 6n-3-triacylglycerols. Am. J. Clin. Nutr. 64, 577-586.
8. Carlson S. E. and Neuringer M. (1999) Polyunsaturated fatty acid status and neurodevelopment: a summary and critical analysis of the literature. Lipids 34, 171-178.
9. Catalan J., Moriguchi T., Slotnick B., Murthy M., Greiner R. S. and Salem N., Jr (2002) Cognitive deficits in docosahexaenoic acid-deficient rats. Behav. Neurosci. 116, 1022-1031.
10. Chalon S., Delion-Vancassel S., Belzung C., Guilloteau D., Leguisquet A. M., Besnard J. C. and Durand G. (1998) Dietary fish oil affects monoaminergic neurotransmission and behavior in rats. J. Nutr. 128, 2512-2519.
11. Champoux M., Hibbeln J. R., Shannon C., Majchrzak S., Suomi S. J., Salem N., Jr and Higley J. D. (2002) Fatty acid formula supplementation and neuromotor development in rhesus monkey neonates. Pediatr. Res. 51, 273-281.
12. Chang M. C., Bell J. M., Purdon A. D., Chikhale E. G. and Grange E. (1999) Dynamics of docosahexaenoic acid metabolism in the central nervous system: lack of effect of chronic lithium treatment. Neurochem. Res. 24, 399-406.
13. Chen H. and Anderson R. E. (1992) Quantitation of phenacyl esters of retinal fatty acids by high-performance liquid chromatography. J. Chromatogr. 578, 124-129.
14. Clarke S. D., Thuillier P., Baillie R. A. and Sha X. (1999) Peroxisome proliferator-activated receptors: a family of lipid-activated transcription factors. Am. J. Clin. Nutr. 70, 566-571.
15. Conquer J. A., Tierney M. C., Zecevic J., Bettger W. J. and Fisher R. H. (2000) Fatty acid analysis of blood plasma of patients with Alzheimer's disease, other types of dementia, and cognitive impairment. Lipids 35, 1305-1312.
16. Contreras M. A., Greiner R. S., Chang M. C., Myers C. S., Salem N., Jr and Rapoport S. I. (2000) Nutritional deprivation of alpha-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain. J. Neurochem. 75, 2392-2400.
17. Contreras M. A., Chang M. C., Rosenberger T. A., Greiner R. S., Myers C. S., Salem N., Jr and Rapoport S. I. (2001) Chronic nutritional deprivation of n-3 alpha-linolenic acid does not affect n-6 arachidonic acid recycling within brain phospholipids of awake rats. J. Neurochem. 79, 1090-1099.
18. Corey E. J., Shih C. and Cashman J. R. (1983) Docosahexaenoic acid is a strong inhibitor of prostaglandin but not leukotriene biosynthesis. Proc. Natl Acad. Sci. USA 80, 3581-3584.
19. Cunnane S. C. and Anderson M. J. (1997) Pure linoleate deficiency in the rat: influence on growth, accumulation of n-6 polyunsaturates, and [1-14C]linoleate oxidation. J. Lipid Res. 38, 805-812.
20. Cunnane S. C., Menard C. R., Likhodii S. S., Brenna J. T. and Crawford M. A. (1999) Carbon recycling into de novo lipogenesis is a major pathway in neonatal metabolism of linoleate and alpha-linolenate. Prostaglandins Leukot. Essent. Fatty Acids 60, 387-392.
21. 14C]arachidonate to examine regional brain lipid metabolism in unanesthetized rats. J. Neurosci. Res. 24, 413-423.
22. DeGeorge J. J., Nariai T., Yamazaki S., Williams W. M. and Rapoport S. I. (1991) Arecoline-stimulated brain incorporation of intravenously administered fatty acids in unanesthetized rats. J. Neurochem. 56, 352-355.
23. Delion S., Chalon S., Guilloteau D., Besnard J. C. and Durand G. (1996) Alpha-linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. J. Neurochem. 66, 1582-1591.
24. DeMar J. C., Jr, Ma K., Bell J. and Rapoport S. I. (2003) Half-lives of docosahexaenoate in rat brain phospholipids are prolonged by nutritional deprivation of n-3 polyunsaturated fatty acids, in Gordon Research Conference Abstracts (36), Lipids and Molecular and Cellular Biology, Kimball Union Academy, NH.
25. DeMar J. C., Jr, Ma K., Bell J. M. and Rapoport S. I. (2004a) Half-lives of docosahexaenoic acid in rat brain phospholipids are prolonged by 15 weeks of deprivation of n-3 polyunsaturated fatty acids, in ISSFAL 6th Congress Abstracts, Lipids as Determinant of Cell Function and Health, Abstract 6-1. Brighton, England (UK).
26. DeMar J. C., Jr, Ma K., Bell J. M. and Rapoport S. I. (2004b) α-Linonenic acid does not contribute appreciably to the brain synthesis of docosahexaenoic acid in the adult rat, in ISSFAL 6th Congress Abstracts, Lipids as Determinant of Cell Function and Health, Abstract E2. Brighton, England (UK).
27. Diez E., Louis-Flamberg P., Hall R. H. and Mayer R. J. (1992) Substrate specificities and properties of human phospholipases A2 in a mixed vesicle model. J. Biol. Chem. 267, 18 342-18 348.
28. Farooqui A. A. and Horrocks L. A. (2001) Plasmalogens: workhorse lipids of membranes in normal and injured neurons and glia. Neuroscientist 7, 232-245.
29. Farooqui A. A., Horrocks L. A. and Farooqui T. (2000) Deacylation and reacylation of neural membrane glycerophospholipids. J. Mol. Neurosci. 14, 123-135.
30. Folch J., Lees M. and Sloane Stanley G. H. (1957) A simple method for the isolation and purification of total lipides from animal tissues. J. Biol. Chem. 226, 497-509.
31. Gatti C., Noremberg K., Brunetti M., Teolato S., Calderini G. and Gaiti A. (1986) Turnover of palmitic and arachidonic acids in the phospholipids from different brain areas of adult and aged rats. Neurochem. Res. 11, 241-252.
32. Gazzah N., Gharib A., Croset M., Bobillier P., Lagarde M. and Sarda N. (1995) Decrease of brain phospholipid synthesis in free-moving ri-3 fatty acid deficient rats. J. Neurochem. 64, 908-918.
33. Giovacchini G., Chang M. C., Channing M. A. et al. (2002) Brain incorporation of [11C]arachidonic acid in young healthy humans measured with positron emission tomography. J. Cereb. Blood Flow Metab. 22, 1453-1462.
34. Giovacchini G., Lerner A., Toczek M. T., Fraser C., Ma K., DeMar J. C., Herscovitch P., Eckelman W. C., Rapoport S. I. and Carson R. E. (2004) Brain incorporation of [11C]arachidonic acid, blood volume, and blood flow in health aging: a study with partial volume correction. J. Nucl. Med. 45, 1471-1479.
35. Greiner R. S., Moriguchi T., Hutton A., Slotnick B. M. and Salem N., Jr (1999) Rats with low levels of brain docosahexaenoic acid show impaired performance in olfactory-based and spatial learning tasks. Lipids 34, S239-S243.
36. Hamano H., Nabekura J., Nishikawa M. and Ogawa T. (1996) Docosahexaenoic acid reduces GABA response in substantia nigra neuron of rat. J. Neurophysiol. 75, 1264-1270.
37. Hamilton L., Greiner R., Salem N., Jr and Kim H. Y. (2000) n-3 Fatty acid deficiency decreases phosphatidylserine accumulation selectively in neuronal tissues. Lipids 35, 863-869.
38. Harel Z., Riggs S., Vaz R., White L. and Menzies G. (2001) Omega-3 polyunsaturated fatty acids in adolescents: knowledge and consumption. J. Adolesc. Health 28, 10-15.
39. Heird W. C., Prager T. C. and Anderson R. E. (1997) Docosahexaenoic acid and the development and function of the infant retina. Curr. Opin. Lipidol. 8, 12-16.
40. Hong S., Gronert K., Devchand P. R., Moussignac R. L. and Serhan C. N. (2003) Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J. Biol. Chem. 278, 14 677-14 687.
41. Horrocks L. (1985) Metabolism and function of fatty acids in brain, in Phospholipids in Nervous Tissues (Eichberg, J., ed.), pp. 173-199. John Wiley, New York.
42. Innis S. M. (2000a) Essential fatty acids in infant nutrition: lessons and limitations from animal studies in relation to studies on infant fatty acid requirements. Am. J. Clin. Nutr. 71, 238S-244S.
43. Innis S. M. (2000b) The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev. Neurosci. 22, 474-480.
44. Innis S. M. and Dyer R. A. (2002) Brain astrocyte synthesis of docosahexaenoic acid from n-3 fatty acids is limited at the elongation of docosapentaenoic acid. J. Lipid Res. 43, 1529-1536.
45. Jones C. R., Arai T. and Rapoport S. I. (1997) Evidence for the involvement of docosahexaenoic acid in cholinergic stimulated signal transduction at the synapse. Neurochem. Res. 22, 663-670.
46. Kang M. J., Fujino T., Sasano H., Minekura H., Yabuki N., Nagura H., Iijima H. and Yamamoto T. T. (1997) A novel arachidonate-preferring acyl-CoA synthetase is present in steroidogenic cells of the rat adrenal, ovary, and testis. Proc. Natl Acad. Sci. USA 94, 2880-2884.
47. Khair-El-Din T., Sicher S. C., Vazquez M. A., Chung G. W., Stallworth K. A., Kitamura K., Miller R. T. and Lu C. Y. (1996) Transcription of the murine iNOS gene is inhibited by docosahexaenoic acid, a major constituent of fetal and neonatal sera as well as fish oils. J. Exp. Med. 183, 1241-1246.
48. Kim H. Y., Karanian J. W., Shingu T. and Salem N., Jr (1990) Stereochemical analysis of hydroxylated docosahexaenoates produced by human platelets and rat brain homogenate. Prostaglandins 40, 473-490.
49. Lands W. E. M. and Crawford C. G. (1976) Enzymes of membrane phospholipid metabolism, in The Enzymes of Biological Membranes (Martonosi, A., ed.), pp. 3-85. Plenum, New York.
50. Langelier B., Furet J. P., Perruchot M. H. and Alessandri J. M. (2003) Docosahexaenoic acid membrane content and mRNA expression of acyl-CoA oxidase and of peroxisome proliferator-activated receptor-delta are modulated in Y79 retinoblastoma cells differently by low and high doses of alpha-linolenic acid. J. Neurosci. Res. 74, 134-141.
51. Laposata M., Reich E. L. and Majerus P. W. (1985) Arachidonoyl-CoA synthetase. Separation from nonspecific acyl-CoA synthetase and distribution in various cells and tissues. J. Biol. Chem. 260, 11 016-11 020.
52. MacDonald J. I. and Sprecher H. (1991) Phospholipid fatty acid remodeling in mammalian cells. Biochim. Biophys. Acta 1084, 105-121.
53. Makrides M., Neumann M. A., Byard R. W., Simmer K. and Gibson R. A. (1994) Fatty acid composition of brain, retina, and erythrocytes in breast- and formula-fed infants. Am. J. Clin. Nutr. 60, 189-194.
54. Makrides M., Neumann M. A., Jeffrey B., Lien E. L. and Gibson R. A. (2000) A randomized trial of different ratios of linoleic to α-linolenic acid in the diet of term infants: effects on visual function and growth. Am. J. Clin. Nutr. 71, 120-129.
55. Marangell L. B., Martinez J. M., Zboyan H. A., Kertz B., Kim H. F. and Puryear L. J. (2003) A double-blind, placebo-controlled study of the omega-3 fatty acid docosahexaenoic acid in the treatment of major depression. Am. J. Psychiat. 160, 996-998.
56. Martin R. E. (1998) Docosahexaenoic acid decreases phospholipase A2 activity in the neurites/nerve growth cones of PC12 cells. J. Neurosci. Res. 54, 805-813.
57. Masuzawa Y., Sugiura T., Sprecher H. and Waku K. (1989) Selective acyl transfer in the reacylation of brain glycerophospholipids. Comparison of three acylation systems for 1-alk-1′-enylglycero-3-phophoethanolamine, 1-acylglycero-3-phosphoethanolamine and 1-acylglycero-3-phosphocholine in rat brain microsomes. Biochim. Biophys. Acta 1005, 1-12.
58. Matsumoto K., Morita I., Hibino H. and Murota S. (1993) Inhibitory effect of docosahexaenoic acid-containing phospholipids on 5-lipoxygenase in rat basophilic leukemia cells. Prostaglandins Leukot. Essent. Fatty Acids 49, 861-866.
59. McGahon B. M., Murray C. A., Horrobin D. F. and Lynch M. A. (1999) Age-related changes in oxidative mechanisms and LTP are reversed by dietary manipulation. Neurobiol. Aging 20, 643-653.
60. Mischoulon D. and Fava M. (2000) Docosahexanoic acid and omega-3 fatty acids in depression. Psychiatr. Clin. North Am. 23, 785-794.
61. Moore S. A. (2001) Polyunsaturated fatty acid synthesis and release by brain-derived cells in vitro. J. Mol. Neurosci. 16, 195-200; discussion 215-221.
62. Moore S. A., Yoder E., Murphy S., Dutton G. R. and Spector A. A. (1991) Astrocytes, not neurons, produce docosahexaenoic acid (22:6 omega-3) and arachidonic acid (20:4 omega 6). J. Neurochem. 56, 518-524.
63. Moriguchi T., Loewke J., Garrison M., Catalan J. N. and Salem N., Jr (2001) Reversal of docosahexaenoic acid deficiency in the rat brain, retina, liver, and serum. J. Lipid Res. 42, 419-427.
64. Murthy M., Hamilton J., Greiner R. S., Moriguchi T., Salem N., Jr and Kim H. Y. (2002) Differential effects of n-3 fatty acid deficiency on phospholipid molecular species composition in the rat hippocampus. J. Lipid Res. 43, 611-617.
65. Neuringer M. (2000) Infant vision and retinal function in studies of dietary long-chain polyunsaturated fatty acids: methods, results, and implications. Am. J. Clin. Nutr. 71, 256S-267S.
66. Neuringer M., Connor W. E., Lin D. S., Barstad L. and Luck S. (1986) Biochemical and functional effects of prenatal and postnatal omega-3 fatty acid deficiency on retina and brain in rhesus monkeys. Proc. Natl Acad. Sci. USA 83, 4021-4025.
67. Noble E. P., Wurtman R. J. and Axelrod J. (1967) A simple and rapid method for injecting H3-norepinephrine into the lateral ventricle of the rat brain. Life Sci. 6, 281-291.
68. O'Connor D. L., Hall R., Adamkin D. et al. (2001) Growth and development in preterm infants fed long-chain polyunsaturated fatty acids: a prospective, randomized controlled trial. Pediatrics 108, 359-371.
69. Otto S. J., de Groot R. H. and Hornstra G. (2003) Increased risk of postpartum depressive symptoms is associated with slower normalization after pregnancy of the functional docosahexaenoic acid status. Prostaglandins Leukot. Essent. Fatty Acids 69, 237-243.
70. Pawlosky R. J., Hibbeln J. R., Lin Y., Goodson S., Riggs P., Sebring N., Brown G. L. and Salem N., Jr (2003) Effects of beef- and fish-based diets on the kinetics of n-3 fatty acid metabolism in human subjects. Am. J. Clin. Nutr. 77, 565-572.
71. Paxinos G. and Watson C. (1987) The Rat Brain in Stereotaxic Coordinates, 3nd edn. Academic Press, New York.
72. Poling J. S., Karanian J. W., Salem N., Jr and Vicini S. (1995) Time- and voltage-dependent block of delayed rectifier potassium channels by docosahexaenoic acid. Mol. Pharmacol. 47, 381-390.
73. Porcellati G., Goracci G. and Arienti G. (1983) Lipid turnover, in Handbook of Neurochemistry (Lajtha, A., ed.), Vol. 5, pp. 277-294. Plenum, New York.
74. Price P. T., Nelson C. M. and Clarke S. D. (2000) Omega-3 polyunsaturated fatty acid regulation of gene expression. Curr. Opin. Lipidol. 11, 3-7.
75. Purdon A. D. and Rapoport S. I. (1998) Energy requirements for two aspects of phospholipid metabolism in mammalian brain. Biochem. J. 335, 313-318.
76. Rapoport S. I. (2001) In vivo fatty acid incorporation into brain phospholipids in relation to plasma availability, signal transduction and membrane remodeling. J. Mol. Neurosci. 16, 243-261.
77. Rapoport S. I. (2003) In vivo approaches to quantifying and imaging brain arachidonic and docosahexaenoic acid metabolism in vivo. J. Pediat. 143, S26-S34.
78. Rapoport S. I., Chang M. C. J. and Spector A. A. (2001) Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J. Lipid Res. 42, 678-685.
79. Reeves P. G., Nielsen F. H. and Fahey G. C., Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J. Nutr. 123, 1939-1951.
80. Reinboth J. J., Clausen M. and Reme C. E. (1996) Light elicits the release of docosahexaenoic acid from membrane phospholipids in the rat retina in vitro. Exp. Eye Res. 63, 277-284.
81. Ringbom T., Huss U., Stenholm A., Flock S., Skattebol L., Perera P. and Bohlin L. (2001) Cox-2 inhibitory effects of naturally occurring and modified fatty acids. J. Nat. Prod. 64, 745-749.
82. Robinson P. J., Noronha J., DeGeorge J. J., Freed L. M., Nariai T. and Rapoport S. I. (1992) A quantitative method for measuring regional in vivo fatty-acid incorporation into and turnover within brain phospholipids: Review and critical analysis. Brain Res. Rev. 17, 187-214.
83. Rojas C. V., Greiner R. S., Fuenzalida L. C., Martinez J. I., Salem N., Jr and Uauy R. (2002) Long-term n-3 FA deficiency modifies peroxisome proliferator-activated receptor beta mRNA abundance in rat ocular tissues. Lipids 37, 367-374.
84. Rouser G., Fleischer S. and Yamamoto A. (1970) Two dimensional then layer chromatographic separation of polar lipids and determination of phospholipids by phosphorous analysis of spots. Lipids 5, 494-496.
85. Salem N., Jr and Nieblylski C. D. (1995) The nervous system has an absolute molecular species requirement for proper function. Mol. Membrane Biol. 12, 131-134.
86. SanGiovanni J. P., Berkey C. S., Dwyer J. T. and Colditz G. A. (2000) Dietary essential fatty acids, long-chain polyunsaturated fatty acids, and visual resolution acuity in healthy full term infants: a systematic review. Early Hum. Dev. 57, 165-188.
87. Serhan C. N., Hong S., Gronert K., Colgan S. P., Devchand P. R., Mirick G. and Moussignac R. L. (2002) Resolvins: a family of bioactive products of omega-3 fatty acid transformation circuits initiated by aspirin treatment that counter proinflammation signals. J. Exp. Med. 196, 1025-1037.
88. Shetty H. U., Smith Q. R., Washizaki K., Rapoport S. I. and Purdon A. D. (1996) Identification of two molecular species of rat brain phosphatidylcholine that rapidly incorporate and turn over arachidonic acid in vivo. J. Neurochem. 67, 1702-1710.
89. Shimizu T. and Wolfe L. S. (1990) Arachidonic acid cascade and signal transduction. J. Neurochem. 55, 1-15.
90. Sprecher H. (2000) Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim. Biophys. Acta 1486, 219-231.
91. Stinson A. M., Wiegand R. D. and Anderson R. E. (1991) Recycling of docosahexaenoic acid in rat retinas during n-3 fatty acid deficiency. J. Lipid Res. 32, 2009-2017.
92. Strokin M., Sergeeva M. and Reiser G. (2003) Docosahexaenoic acid and arachidonic acid release in rat brain astrocytes is mediated by two separate isoforms of phospholipase A2 and is differently regulated by cyclic AMP and Ca2+. Br. J. Pharmacol. 139, 1014-1022.
93. Su H. M., Keswick L. A. and Brenna J. T. (1996) Increasing dietary linoleic acid in young rats increases and then decreases docosahexaenoic acid in retina but not in brain. Lipids 31, 1289-1298.
94. Su H. M., Bernardo L., Mirmiran M., Ma X. H., Corso T. N., Nathanielsz P. W. and Brenna J. T. (1999) Bioequivalence of dietary alpha-linolenic and docosahexaenoic acids as sources of docosahexaenoate accretion in brain and associated organs of neonatal baboons. Pediatr. Res. 45, 87-93.
95. Sun G. Y. (1977) Metabolism of arachidonate and stearate injected simultaneously into the mouse brain. Lipids 12, 661-665.
96. Sun G. Y. and Su K. L. (1979) Metabolism of arachidonoyl phosphoglycerides in mouse brain subcellular fractions. J. Neurochem. 32, 1053-1059.
97. Suzuki H., Morikawa Y. and Takahashi H. (2001) Effect of DHA oil supplementation on intelligence and visual acuity in the elderly. World Rev. Nutr. Diet 88, 68-71.
98. Tully A. M., Roche H. M., Doyle R., Fallon C., Brace I., Lawlor B., Coakley D. and Gibney M. J. (2003) Low serum cholesteryl esterdocosahexaenoic acid levels in Alzheimer's disease: a case-control study. Br. J. Nutr. 89, 483-489.
99. Uauy R., Mena P. and Rojas C. (2000) Essential fatty acids in early life: structural and functional role. Proc. Nutr. Soc. 59, 3-15.
100. Van Aerde J. E. and Clandinin M. T. (1993) Controversy in fatty acid balance. Can. J. Physiol. Pharmacol. 71, 707-712.
101. Ward G. R., Huang Y. S., Bobik E., Xing H. C., Mutsaers L., Auestad N., Montalto M. and Wainwright P. (1998) Long-chain polyunsaturated fatty acid levels in formulae influence deposition of docosahexaenoic acid and arachidonic acid in brain and red blood cells of artificially reared neonatal rats. J. Nutr. 128, 2473-2487.
102. Williard D. E., Harmon S. D., Kaduce T. L., Preuss M., Moore S. A., Robbins M. E. and Spector A. A. (2001a) Docosahexaenoic acid synthesis from n-3 polyunsaturated fatty acids in differentiated rat brain astrocytes. J. Lipid Res. 42, 1368-1376.
103. Williard D. E., Harmon S. D., Preuss M. A., Kaduce T. L., Moore S. A. and Spector A. A. (2001b) Production and release of docosahexaenoic acid by differentiated rat brain astrocytes. World Rev. Nutr. Diet 88, 168-172.
104. Woods J., Ward G. and Salem N., Jr (1996) Is docosahexaenoic acid necessary in infant formula? Evaluation of high linolenate diet in the neonatal rat. Pediatr. Res. 40, 687-694.
105. Yavin E., Brand A. and Green P. (2002) Docosahexaenoic acid abundance in the brain: a biodevice to combat oxidative stress. Nutr. Neurosci. 5, 149-157.
106. Young R. W. (1976) Visual cells and the concept of renewal. Invest. Ophthalmol Vis. Sci. 15, 700-725.