α-linolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid

Journal of Neurochemistry

Volumn 94, Issue 4, 2005, Pages 1063-1076

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

^a NATIONAL INSTITUTE ON AGING   (United States)

Author keywords

linolenic; Brain; Docosahexaenoic; Incorporation; Phospholipid; Rat

Indexed keywords

DOCOSAHEXAENOIC ACID; LINOLEIC ACID; LIPID; PHOSPHOLIPID; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ESTERIFICATION; FAT INTAKE; LIPID ANALYSIS; LIPID BLOOD LEVEL; LIPID OXIDATION; LIPOGENESIS; MALE; NONHUMAN; PRIORITY JOURNAL; RADIOACTIVITY; RAT;

ALPHA-LINOLENIC ACID; ANIMALS; BRAIN; DIET; DOCOSAHEXAENOIC ACIDS; HOMEOSTASIS; INJECTIONS, INTRAVENOUS; LIPID METABOLISM; LIPIDS; MALE; OSMOLAR CONCENTRATION; OXIDATION-REDUCTION; PHOSPHOLIPIDS; RATS; RATS, INBRED F344; TRIGLYCERIDES;

ANIMALIA;

EID: 23844432885     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2005.03258.x     Document Type: Article

References (78)

1. Abedin L., Lien E. L., Vingrys A. J. and Sinclair A. J. (1999) The effect of dietary α-linolenic acid compared with docosahexaenoic acid on brain, retina, liver, and heart in the guinea pig. Lipids 34, 475-482.
2. 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.
3. Burdge G. C. and Wootton S. A. (2002) Conversion of α-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. Br. J. Nutr. 88, 411-420.
4. Burdge G. C., Jones A. E. and Wootton S. A. (2002) Eicosapentaenoic and docosapentaenoic acids are the principal products of α-linolenic acid metabolism in young men. Br. J. Nutr. 88, 355-363.
5. 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.
6. Chang M. C., Contreras M. A., Rosenberger T. A., Rintala J. J., Bell J. M. and Rapoport S. I. (2001) Chronic valproate treatment decreases the in vivo turnover of arachidonic acid in brain phospholipids: a possible common effect of mood stabilizers. J. Neurochem. 77, 796-803.
7. 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.
8. Cho H. P., Nakamura M. and Clarke S. D. (1999) Cloning, expression, and fatty acid regulation of the human δ-5 desaturase. J. Biol. Chem. 274, 37 335-37 339.
9. Clarke S. D. (2001) Polyunsaturated fatty acid regulation of gene transcription: a molecular mechanism to improve the metabolic syndrome. J. Nutr. 131, 1129-1132.
10. Cohen S. R. and Bemsohn J. (1978) The in vivo incorporation of linolenic acid into neuronal and glial cells and myelin. J. Neurochem. 30, 661-669.
11. 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.
12. Contreras M. A., Greiner R. S., Chang M. C., Myers C. S., Salem N. Jr and Rapoport S. I. (2000) Nutritional deprivation of α-linolenic acid decreases but does not abolish turnover and availability of unacylated docosahexaenoic acid and docosahexaenoyl-CoA in rat brain. J. Neurochem. 15, 2392-2400,
13. 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 α-linolenic acid does not affect n-6 arachidonic acid recycling within brain phospholipids of awake rats. J. Neurochem, 79, 1090-1099.
14. Cook H. W., Byers D. M., Palmer F. B., Spence M. W., Rakoff H., Duval S. M. and Emken E. A. (1991) Alternative pathways in the desaturation and chain elongation of linolenic acid, 18:3(n-3), in cultured glioma cells. J. Lipid Res. 32, 1265-1273.
15. Cunnane S. C. (2001) New developments in α-linolenate metabolism with emphasis on the importance of β-oxidation and carbon recycling. World Rev. Nutr. Diet 88, 178-183.
16. 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 α-linolenate. Prostaglandins Leukot. Essent. Fatty Acids 60, 387-392.
17. 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.
18. 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 nutritional deprivation of n-3 polyunsaturated fatty acids. J. Neurochem. 91, 1125-1137.
19. DeMar. J. C. Jr, Ma K., Chang L., Bell J. M. and Rapoport S. I. (2004b) Linolenic acid does not contribute appreciably to the brain synthesis of docosahexaenoic acid in the adult rat. ISFAAL 6th Congress Abstracts, Lipids as Determinant of Cell Function and Health, Brighton, England (UK).
20. Deutsch J., Grange E., Rapoport S. I. and Purdon A. D. (1994) Isolation and quantitation of long-chain acyl-coenzyme A esters in brain tissue by solid-phase extraction. Anal. Biochem. 220, 321-323.
21. Dhopeshwarkar G. A. and Subramanian C. (1976) Biosynthesis of polyunsaturated fatty acids in the developing brain. I. Metabolic transformations of intracranially administered 1-14C linolenic acid. Lipids 11, 67-71.
22. Dwyer B. E. and Bernsohn J. (1979) The effect of essential fatty acid deprivation on the metabolic transformations of [1(-14)C]linolenate in developing rat brain. Biochim. Biophys. Acta 575, 309-317.
23. Edmond J. (2001) Essential polyunsaturated fatty acids and the barrier to the brain: the components of a model for transport. J. Mol. Neurosci. 16, 181-193.
24. Emken E. A., Adlof R. O., Duval S. M. and Nelson G. J. (1999) Effect of dietary docosahexaenoic acid on desaturation and uptake in vivo of isotope-labeled oleic, linoleic, and linolenic acids by male subjects. Lipids 34, 785-791.
25. 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.
26. Gavino G. R. and Gavino V. C. (1991) Rat liver outer mitochondrial camitine palmitoyltransferase activity towards long-chain polyunsaturated fatty acids and their CoA esters. Lipids 26, 266-270.
27. Grange E., Deutsch J., Smith Q. R., Chang M., Rapoport S. I. and Purdon A. D. (1995) Specific activity of brain palmitoyl-CoA pool provides rates of incorporation of palmitate in brain phospholipids in awake rats. J. Neurochem. 65, 2290-2298.
28. Hajra A. K. and Bishop J. E. (1986) Preparation of radioactive acyl coenzyme A. Meth. Enzymol. 122, 50-53.
29. Innis S. M. (2000) The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev. Neurosci. 22, 474-480.
30. Innis S. M. (2003) Perinatal biochemistry and physiology of long-chain polyunsaturated fatty acids. J. Pediatr. 143, S1-S8.
31. Kack P. E. Jr, Hibbeln J., McElroy S. L. et al. (2004) Omega-3 fatty acid blood concentrations and response in bipolar depression and rapid cycling bipolar disorder. Acta Psychiat. Scand. 110, 23.
32. Kidd P. M. (2004) Bipolar disorder and cell membrane dysfunction. Progress toward integrative management. Altern. Med. Rev. 9, 107-135.
33. Lands W. E. M. and Crawford G. C. (1976) Enzymes of membrane phospholipid metabolism, in The Enzymes of Biological Membranes (Marinosi, A., ed.), pp. 3-85. Plenum, New York.
34. 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 α-linolenic acid. J. Neurosci. Res. 74, 134-141.
35. Lefkowitz W., Lim S. Y., Lin Y. and Salem N. Jr (2005) Where does the developing brain obtain its doscosahexaenoic acid? Relative contributions of dietary α-linolenic acid, docosahexaenoic acid, and body stores in the developing rat. Pediatr. Res. 57, 157-165.
36. Marangell L. B., Martinez J. M., Zboyan H. A., Chong H. and Puryear L. J. (2004) Omega-3 fatty acids for the prevention of postpartum depression: negative data from a preliminary, open-label pilot study. Depress. Anxiety 19, 20-23.
37. Marcel Y. L. and Suzue G. (1972) Kinetic studies on the specificity of long chain acyl coenzyme A synthetase from rat liver microsomes. J. Biol. Chem. 247, 4433-4436.
38. Matsuzaka T., Shimano H., Yahagi N. et al. (2002) Dual regulation of mouse Δ(5)- and Δ(6)-desaturase gene expression by SREBP-1 and PPARα. J. Lipid Res. 43, 107-114.
39. Menard C. R., Goodman K. J., Corso T. N., Brenna J. T. and Cunnane S. C. (1998) Recycling of carbon into lipids synthesized de novo is a quantitatively important pathway of α-[U-13C]linolenate utilization in the developing rat brain. J. Neurochem. 71, 2151-2158.
40. Moore S. A. (2001) Polyunsaturated fatty acid synthesis and release by brain-derived cells in vitro. J. Mol. Neurosci. 16, 195-200.
41. 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.
42. Morris M. C., Evans D. A., Bienias J. L., Tangney C. C., Bennett D. A., Wilson R. S., Aggarwal N. and Schneider J. (2003) Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease. Arch. Neurol. 60, 940-946.
43. Nakamura M. T. and Nara T. Y. (2003) Essential fatty acid synthesis and its regulation in mammals. Prostaglandins Leukot. Essent. Fatty Acids 68, 145-150.
44. Nara T. Y., He W. S., Tang C., Clarke S. D. and Nakamura M. T. (2002) The E-box like sterol regulatory element mediates the suppression of human Δ-6 desaturase gene by highly unsaturated fatty acids. Biochem. Biophys. Res. Commun. 296, 111-117.
45. Noaghiul S. and Hibbeln J. R. (2003) Cross-national comparisons of seafood consumption and rates of bipolar disorders. Am. J. Psychiatry. 160, 2222-2227.
46. Pawlosky R. J. and Salem N. Jr (1999) Alcohol consumption in rhesus monkeys depletes tissues of polyunsaturated fatty acids and alters essential fatty acid metabolism. Alcohol Clin. Exp. Res. 23, 311-317.
47. Pawlosky R. J., Hibbeln J. R., Novotny J. A. and Salem N. Jr (2001) Physiological compartmental analysis of α-linolenic acid metabolism in adult humans. J. Lipid Res. 42, 1257-1265.
48. 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.
49. Purdon D., Arai T. and Rapoport S. I. (1997) No evidence for direct incorporation of esterified palmitic acid from plasma into brain lipids of awake adult rat. J. Lipid Res. 38, 526-530.
50. Puskas L. G., Bereczki E., Santha M., Vigh L., Csanadi G., Spener F., Ferdinandy P., Onochy A. and Kitajka K. (2004) Cholesterol and cholesterol plus DHA diet-induced gene expression and fatty acid changes in mouse eye and brain. Biochemie 86, 817-824.
51. Rapoport S. I. (2001) In vivo fatty acid incorporation into brain phosholipids in relation to plasma availability, signal transduction and membrane remodeling. J. Mol. Neurosci. 16, 243-261.
52. Rapoport S. I. (2003) In vivo approaches to quantifying and imaging brain arachidonic and docosahexaenoic acid metabolism. J. Pediatr. 143, S26-S34.
53. Rapoport S. I., Purdon D., Shetty H. U., Grange E., Smith Q., Jones C. and Chang M. C. (1997) In vivo imaging of fatty acid incorporation into brain to examine signal transduction and neuroplasticity involving phospholipids. Ann. NY Acad. Sci. 820, 56-73.
54. Rapoport S. I., Chang M. C. and Spector A. A. (2001) Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J. Lipid Res. 42, 678-685.
55. Robinson P. J. and Rapoport S. I. (1986) Kinetics of protein binding determine rates of uptake of drugs by brain. Am. J. Physiol. 251, R1212-R1220.
56. 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. Brain Res. Rev. 17, 187-214.
57. Salem N. Jr, Litman B., Kim H. Y. and Gawrisch K. (2001) Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 36, 945-959.
58. Sastry P. S. (1985) Lipids of nervous tissue: composition and metabolism. Prog. Lipid Res. 24, 69-176.
59. Sauerwald T. U., Hachey D. L., Jensen C. L., Chen H., Anderson R. E. and Heird W. C. (1996) Effect of dietary α-linolenic acid intake on incorporation of docosahexaenoic and arachidonic acids into plasma phospholipids of term infants. Lipids 31, S131-S135.
60. Scott B. L. and Bazan N. G. (1989) Membrane docosahexaenoate is supplied to the developing brain and retina by the liver. Proc. Natl. Acad. Sci. USA 86, 2903-2907.
61. Sheaff Greiner R. C., Zhang Q., Goodman K., Giussani D. A., Nathanielsz P. W. and Breena J. T. (1996) Linoleate, α-linolenate, and docosahexaenoate recycling into saturated and monounsaturated fatty acids is a major pathway in pregnant or lactating adults and fetal or infant rhesus monkeys. J. Lipid Res. 27, 2675-2686.
62. 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.
63. Skipski V. P., Good J. J., Barclay M. and Reggio R. B. (1968) Quantitative analysis of simple lipid classes by thin-layer chromatography. Biochim. Biophys. Acta 152, 10-19.
64. Spector A. A. (2001) Plasma free fatty acid and lipoproteins as sources of polyunsaturated fatty acid for the brain. J. Mol. Neurosci. 16, 159-165.
65. Sprecher H. (2000) Metabolism of highly unsarurated n-3 and n-6 fatty acids. Biochim. Biophys. Acta 1486, 219-231.
66. Stoll A. L., Severus W. E., Freeman M. P., Rueter S., Zboyan H. A., Diamond E., Cress K. K. and Marangell L. B. (1999) Omega 3 fatty acids in bipolar disorder: a preliminary double-blind, placebo-controlled trial. Arch. Gen. Psychiatry 56, 407-412.
67. Su H. M., Bernardo L., Mirmiran M., Ma X. H., Corso T. N., Nathanielsz P. W. and Breena J. T. (1999) Bioequivalence of dietary α-linolenic and docosahexaenoic acids as sources of docosahexaenoate accretion in brain and associated organs of neonatal baboons. Pediatr. Res. 45, 87-93.
68. Tang C., Cho H. P., Nakamura M. T. and Clarke S. D. (2003) Regulation of human δ-6 desarurase gene transcription: identification of a functional direct repeat-1 element. J. Lipid Res. 44, 686-695.
69. Tanskanen A., Hibbeln J. R., Hintikka J., Haatainen K., Honkalampi K. and Viinamaki H. (2001) Fish consumption, depression, and suicidality in a general population. Arch. Gen. Psychiatry 58, 512-513.
70. de Tomas M. E., Mercuri O. and Serres C. (1991) Metabolic transformation of intracraneally injected [1-14C]linoleic and [1-14C]α-linolenic acids in malnourished developing rats. Lipids 26, 891-894.
71. Van Aerde J. E. and Clandinin M. T. (1993) Controversy in fatty acid balance. Can. J. Physiol. Pharmacol. 71, 707-712.
72. Waku K. (1992) Origins and fates of fatty acyl-CoA esters. Biochim. Biophys. Acta 1124, 101-111.
73. Washizaki K., Smith Q. R., Rapoport S. I. and Purdon A. D. (1994) Brain arachidonic acid incorporation and precursor pool specific activity during intravenous infusion of unesterified [3H]arachidonate in the anesthetized rat. J. Neurochem. 63, 727-736.
74. Whalley L. J., Fox H. C., Wahle K. W., Starr J. M. and Deary I. J. (2004) Cognitive aging, childhood intelligence, and the use of food supplements: possible involvement of n-3 fatty acids. Am. J. Clin. Nutr. 80, 1650-1657.
75. Williard D. E., Harmon S. D., Kaduce T. L., Preuss M., Moore S. A., Robbins M. E. and Spector A. A. (2001) Docosahexaenoic acid synthesis from n-3 polyunsaturated fatty acids in differentiated rat brain astrocytes. J. Lipid Res. 42, 1368-1376.
76. Yamashita A., Sugiura T. and Waku K. (1997) Acyltransferases and transacylases involved in fatty acid remodeling of phospholipids and metabolism of bioactive lipids in mammalian cells. J. Biochem. (Tokyo) 122, 1-16.
77. Yang J. and Cunnane S. C. (1994) Quantitative measurements of dietary and [1-14C]linoleate metabolism in pregnant rats: specific influence of moderate zinc depletion independent of food intake. Can. J. Physiol. Pharmacol. 72, 1180-1185.
78. Youdim K. A., Martin A. and Joseph J. A. (2000) Essential fatty acids and the brain: possible health implications. Int. J. Dev. Neurosci. 18, 383-399.