Rapid de-esterification and loss of eicosapentaenoic acid from rat brain phospholipids: An intracerebroventricular study

Journal of Neurochemistry

Volumn 116, Issue 3, 2011, Pages 363-373

  Chen, Chuck T ^a   Liu, Zhen ^a   Bazinet, Richard P ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

oxidation; docosahexaenoic acid; eicosapentaenoic acid; intracerebroventricular infusion; kinetics; omega 3 polyunsaturated fatty acid; palmitate; rat brain

Indexed keywords

CARBON 14; CHOLESTEROL; ICOSAPENTAENOIC ACID; MONOUNSATURATED FATTY ACID; PALMITIC ACID; PHOSPHOLIPID; SATURATED FATTY ACID;

ANIMAL EXPERIMENT; ARTICLE; BIOCHEMISTRY; BRAIN METABOLISM; CONTROLLED STUDY; ESTERIFICATION; FATTY ACID METABOLISM; FATTY ACID OXIDATION; HALF LIFE TIME; LIPID BRAIN LEVEL; MALE; MICROWAVE IRRADIATION; NONHUMAN; PRIORITY JOURNAL; RADIOACTIVITY; RAT;

ANIMALS; BRAIN; BRAIN CHEMISTRY; CARBON RADIOISOTOPES; EICOSAPENTAENOIC ACID; ESTERIFICATION; FATTY ACIDS; HALF-LIFE; INJECTIONS, INTRAVENTRICULAR; KINETICS; LIPID METABOLISM; MALE; OXIDATION-REDUCTION; PALMITIC ACID; PHOSPHOLIPIDS; RATS; RATS, SPRAGUE-DAWLEY; TIME FACTORS;

RATTUS;

EID: 78651283588     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.07116.x     Document Type: Article

References (80)

1. Adan Y., Shibata K., Sato M., Ikeda I., and, Imaizumi K., (1999) Effects of docosahexaenoic and eicosapentaenoic acid on lipid metabolism, eicosanoid production, platelet aggregation and atherosclerosis in hypercholesterolemic rats. Biosci. Biotechnol. Biochem. 63, 111-119.
2. Ahmed A. A., and, Holub B. J., (1984) Alteration and recovery of bleeding times, platelet aggregation and fatty acid composition of individual phospholipids in platelets of human subjects receiving a supplement of cod-liver oil. Lipids 19, 617-624.
3. Amminger G. P., Schafer M. R., Papageorgiou K., Klier C. M., Cotton S. M., Harrigan S. M., Mackinnon A., McGorry P. D., and, Berger G. E., (2010) Long-chain omega-3 fatty acids for indicated prevention of psychotic disorders: a randomized, placebo-controlled trial. Arch. Gen. Psychiatry 67, 146-154.
4. Aveldano M. I., VanRollins M., and, Horrocks L. A., (1983) Separation and quantitation of free fatty acids and fatty acid methyl esters by reverse phase high pressure liquid chromatography. J. Lipid Res. 24, 83-93.
5. Berridge M. J., Downes C. P., and, Hanley M. R., (1989) Neural and developmental actions of lithium: a unifying hypothesis. Cell 59, 411-419.
6. Black K. L., Hoff J. T., Radin N. S., and, Deshmukh G. D., (1984a) Eicosapentaenoic acid: effect on brain prostaglandins, cerebral blood flow and edema in ischemic gerbils. Stroke; J. Cerebral Circ. 15, 65-69.
7. Black K. L., Hsu S., Radin N. S., and, Hoff J. T., (1984b) Effect of intravenous eicosapentaenoic acid on cerebral blood flow, edema and brain prostaglandins in ischemic gerbils. Prostaglandins 28, 545-556.
8. Brenna J. T., and, Diau G. Y., (2007) The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostaglandins Leukot. Essent. Fatty Acids 77, 247-250.
9. Burgess J. R., Stevens L., Zhang W., and, Peck L., (2000) Long-chain polyunsaturated fatty acids in children with attention-deficit hyperactivity disorder. Am. J. Clin. Nutr. 71, 327S-330S.
10. Cantrill R. C., and, Carey E. M., (1975) Changes in the activities of de novo fatty acid synthesis and palmitoyl-CoA synthetase in relation to myelination in rabbit brain. Biochim. Biophys. Acta 380, 165-175.
11. Carey E. M., (1975) A comparative study of the metabolism of de novo synthesized fatty acids from acetate and glucose, and exogenous fatty acids, in slices of rabbit cerebral cortex during development. J. Neurochem. 24, 237-244.
12. Chang M. C., Grange E., Rabin O., Bell J. M., Allen D. D., and, Rapoport S. I., (1996) Lithium decreases turnover of arachidonate in several brain phospholipids. Neurosci. Lett. 220, 171-174.
13. 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.
14. Chen C. T., Green J. T., Orr S. K., and, Bazinet R. P., (2008a) Regulation of brain polyunsaturated fatty acid uptake and turnover. Prostaglandins Leukot. Essent. Fatty Acids 79, 85-91.
15. Chen C. T., Ma D. W., Kim J. H., Mount H. T., and, Bazinet R. P., (2008b) The low density lipoprotein receptor is not necessary for maintaining mouse brain polyunsaturated fatty acid concentrations. J. Lipid Res. 49, 147-152.
16. Chen C. T., Liu Z., Ouellet M., Calon F., and, Bazinet R. P., (2009) Rapid beta-oxidation of eicosapentaenoic acid in mouse brain: an in situ study. Prostaglandins Leukot. Essent. Fatty Acids 80, 157-163.
17. Contreras M. A., Chang M. C., Kirkby D., Bell J. M., and, Rapoport S. I., (1999) Reduced palmitate turnover in brain phospholipids of pentobarbital-anesthetized rats. Neurochem. Res. 24, 833-841.
18. 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.
19. 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.
20. Corso T. N., and, Brenna J. T., (1997) High-precision position-specific isotope analysis. Proc. Natl Acad. Sci. USA 94, 1049-1053.
21. Crawford M. A., and, Sinclair A. J., (1971) Nutritional influences in the evolution of mammalian brain. In: lipids, malnutrition & the developing brain. Ciba Found. Symp. 267-292.
22. Cunnane S. C., Williams S. C., Bell J. D., Brookes S., Craig K., Iles R. A., and, Crawford M. A., (1994) Utilization of uniformly labeled 13C-polyunsaturated fatty acids in the synthesis of long-chain fatty acids and cholesterol accumulating in the neonatal rat brain. J. Neurochem. 62, 2429-2436.
23. Cunnane S. C., Ryan M. A., Nadeau C. R., Bazinet R. P., Musa-Veloso K., and, McCloy U., (2003) Why is carbon from some polyunsaturates extensively recycled into lipid synthesis? Lipids 38, 477-484.
24. Cunnane S. C., Ryan M. A., Lin Y. H., Lim S. Y., and, Salem N. Jr, (2006) Suckling rats actively recycle carbon from alpha-linolenate into newly synthesized lipids even during extreme dietary deficiency of n-3 polyunsaturates. Pediatr. Res. 59, 107-110.
25. DeMar J. C. Jr, Ma K., Bell J. M., and, Rapoport S. I., (2004) 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.
26. Demar J. C. Jr, Ma K., Chang L., Bell J. M., and, Rapoport S. I., (2005) alpha-Linolenic acid does not contribute appreciably to docosahexaenoic acid within brain phospholipids of adult rats fed a diet enriched in docosahexaenoic acid. J. Neurochem. 94, 1063-1076.
27. DeMar J. C. Jr, Lee H. J., Ma K., Chang L., Bell J. M., Rapoport S. I., and, Bazinet R. P., (2006) Brain elongation of linoleic acid is a negligible source of the arachidonate in brain phospholipids of adult rats. Biochim. Biophys. Acta 1761, 1050-1059.
28. DeMar J. C. Jr, DiMartino C., Baca A. W., Lefkowitz W., and, Salem N. Jr, (2008) Effect of dietary docosahexaenoic acid on biosynthesis of docosahexaenoic acid from alpha-linolenic acid in young rats. J. Lipid Res. 49, 1963-1980.
29. Dhopeshwarkar G. A., and, Mead J. F., (1969) Fatty acid uptake by the brain. II. Incorporation of [I-14C] palmitic acid into the adult rat brain. Biochim. Biophys. Acta 187, 461-467.
30. Dhopeshwarkar G. A., Maier R., and, Mead J. F., (1969) Incorporation of [I-14C] acetate into the fatty acids of the developing rat brain. Biochim. Biophys. Acta 187, 6-12.
31. Dhopeshwarkar G. A., Subramanian C., and, Mead J. F., (1973) Metabolism of (I-14 C)palmitic acid in the developing brain: persistence of radioactivity in the carboxyl carbon. Biochim. Biophys. Acta 296, 257-264.
32. Diagne A., Fauvel J., Record M., Chap H., and, Douste-Blazy L., (1984) Studies on ether phospholipids. II. Comparative composition of various tissues from human, rat and guinea pig. Biochim. Biophys. Acta 793, 221-231.
33. Ding D., and, Greenberg M. L., (2003) Lithium and valproate decrease the membrane phosphatidylinositol/phosphatidylcholine ratio. Mol. Microbiol. 47, 373-381.
34. Duncan R. E., and, Bazinet R. P., (2010) Brain arachidonic acid uptake and turnover: implications for signaling and bipolar disorder. Curr. Opin. Clin. Nutr. Metab. Care 13, 130-138.
35. Edmond J., Higa T. A., Korsak R. A., Bergner E. A., and, Lee W. N., (1998) Fatty acid transport and utilization for the developing brain. J. Neurochem. 70, 1227-1234.
36. 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.
37. Frangou S., Lewis M., and, McCrone P., (2006) Efficacy of ethyl-eicosapentaenoic acid in bipolar depression: randomised double-blind placebo-controlled study. Br. J. Psychiatry 188, 46-50.
38. Frangou S., Lewis M., Wollard J., and, Simmons A., (2007) Preliminary in vivo evidence of increased N-acetyl-aspartate following eicosapentanoic acid treatment in patients with bipolar disorder. J. Psychopharmacol. 21, 435-439.
39. Fux M., Benjamin J., and, Nemets B., (2004) A placebo-controlled cross-over trial of adjunctive EPA in OCD. J. Psychiatr. Res. 38, 323-325.
40. 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.
41. Gnaedinger J. M., Miller J. C., Latker C. H., and, Rapoport S. I., (1988) Cerebral metabolism of plasma [14C]palmitate in awake, adult rat: subcellular localization. Neurochem. Res. 13, 21-29.
42. Golovko M. Y., and, Murphy E. J., (2006) Uptake and metabolism of plasma-derived erucic acid by rat brain. J. Lipid Res. 47, 1289-1297.
43. 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.
44. Green J. T., Liu Z., and, Bazinet R. P., (2010) Brain phospholipid arachidonic acid half-lives are not altered following 15 weeks of N-3 polyunsaturated fatty acid adequate or deprived diet. J. Lipid Res. 51, 535-543.
45. Hamilton J. A., Johnson R. A., Corkey B., and, Kamp F., (2001) Fatty acid transport: the diffusion mechanism in model and biological membranes. J. Mol. Neurosci. 16, 99-108. discussion 151-107.
46. Hasturk H., Kantarci A., Goguet-Surmenian E., Blackwood A., Andry C., Serhan C. N., and, Van Dyke T. E., (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J. Immunol. 179, 7021-7029.
47. Huang M. C., Muddana S., Horowitz E. N., McCormick C. C., Infante J. P., and, Brenna J. T., (2000) High-precision isotope ratio mass spectrometry and stable isotope precursors for tracer studies in cell culture. Anal. Biochem. 287, 80-86.
48. Igarashi M., Ma K., Gao F., Kim H. W., Greenstein D., Rapoport S. I., and, Rao J. S., (2010) Brain lipid concentrations in bipolar disorder. J. Psychiatr. Res. 44, 177-182.
49. Ishida T., Yoshida M., Arita M., et al. (2010) Resolvin E1, an endogenous lipid mediator derived from eicosapentaenoic acid, prevents dextran sulfate sodium-induced colitis. Inflamm. Bowel Dis. 16, 87-95.
50. Jope R. S., Song L., Li P. P., Young L. T., Kish S. J., Pacheco M. A., and, Warsh J. J., (1996) The phosphoinositide signal transduction system is impaired in bipolar affective disorder brain. J. Neurochem. 66, 2402-2409.
51. Kaduce T. L., Chen Y., Hell J. W., and, Spector A. A., (2008) Docosahexaenoic acid synthesis from n-3 fatty acid precursors in rat hippocampal neurons. J. Neurochem. 105, 1525-1535.
52. Katayama Y., Katsumata T., Muramatsu H., Usuda K., Obo R., and, Terashi A., (1997) Effect of long-term administration of ethyl eicosapentate (EPA-E) on local cerebral blood flow and glucose utilization in stroke-prone spontaneously hypertensive rats (SHRSP). Brain Res. 761, 300-305.
53. Katsumata T., Katayama Y., Obo R., Muramatsu H., Ohtori T., and, Terashi A., (1999) Delayed administration of ethyl eicosapentate improves local cerebral blood flow and metabolism without affecting infarct volumes in the rat focal ischemic model. Eur. J. Pharmacol. 372, 167-174.
54. Kawamura N., and, Kishimoto Y., (1981) Characterization of water-soluble products of palmitic acid beta-oxidation by a rat brain preparation. J. Neurochem. 36, 1786-1791.
55. Keck P. E. Jr, Mintz J., McElroy S. L., et al. (2006) Double-blind, randomized, placebo-controlled trials of ethyl-eicosapentanoate in the treatment of bipolar depression and rapid cycling bipolar disorder. Biol. Psychiatry 60, 1020-1022.
56. Lee W. N., Bassilian S., Ajie H. O., Schoeller D. A., Edmond J., Bergner E. A., and, Byerley L. O., (1994a) In vivo measurement of fatty acids and cholesterol synthesis using D2O and mass isotopomer analysis. Am. J. Physiol. 266, E699-E708. (Pubitemid 24173580)
57. Lee W. N., Bassilian S., Guo Z., Schoeller D., Edmond J., Bergner E. A., and, Byerley L. O., (1994b) Measurement of fractional lipid synthesis using deuterated water (2H2O) and mass isotopomer analysis. Am. J. Physiol. 266, E372-E383. (Pubitemid 24115791)
58. Marbois B. N., Ajie H. O., Korsak R. A., Sensharma D. K., and, Edmond J., (1992) The origin of palmitic acid in brain of the developing rat. Lipids 27, 587-592.
59. Miller J. C., Gnaedinger J. M., and, Rapoport S. I., (1987) Utilization of plasma fatty acid in rat brain: distribution of [14C]palmitate between oxidative and synthetic pathways. J. Neurochem. 49, 1507-1514.
60. Nieuwenhuys C. M., and, Hornstra G., (1998) The effects of purified eicosapentaenoic and docosahexaenoic acids on arterial thrombosis tendency and platelet function in rats. Biochim. Biophys. Acta 1390, 313-322.
61. Ouellet M., Emond V., Chen C. T., Julien C., Bourasset F., Oddo S., LaFerla F., Bazinet R. P., and, Calon F., (2009) Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem. Int. 55, 476-482.
62. Peet M., and, Horrobin D. F., (2002) A dose-ranging study of the effects of ethyl-eicosapentaenoate in patients with ongoing depression despite apparently adequate treatment with standard drugs. Arch. Gen. Psychiatry 59, 913-919.
63. Peet M., Brind J., Ramchand C. N., Shah S., and, Vankar G. K., (2001) Two double-blind placebo-controlled pilot studies of eicosapentaenoic acid in the treatment of schizophrenia. Schizophr. Res. 49, 243-251.
64. Peterson L. D., Jeffery N. M., Thies F., Sanderson P., Newsholme E. A., and, Calder P. C., (1998) Eicosapentaenoic and docosahexaenoic acids alter rat spleen leukocyte fatty acid composition and prostaglandin E2 production but have different effects on lymphocyte functions and cell-mediated immunity. Lipids 33, 171-180.
65. Philbrick D. J., Mahadevappa V. G., Ackman R. G., and, Holub B. J., (1987) Ingestion of fish oil or a derived n-3 fatty acid concentrate containing eicosapentaenoic acid (EPA) affects fatty acid compositions of individual phospholipids of rat brain, sciatic nerve and retina. J. Nutr. 117, 1663-1670.
66. Puri B. K., Leavitt B. R., Hayden M. R., et al. (2005) Ethyl-EPA in Huntington disease: a double-blind, randomized, placebo-controlled trial. Neurology 65, 286-292.
67. Rapoport S. I., (1999) In vivo fatty acid incorporation into brain phospholipids in relation to signal transduction and membrane remodeling. Neurochem. Res. 24, 1403-1415.
68. 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. N Y Acad. Sci. 820, 56-73. discussion 73-54.
69. 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.
70. Rapoport S. I., Rao J. S., and, Igarashi M., (2007) Brain metabolism of nutritionally essential polyunsaturated fatty acids depends on both the diet and the liver. Prostaglandins Leukot. Essent. Fatty Acids 77, 251-261. (Pubitemid 350214520)
71. 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.
72. Ross B. M., Seguin J., and, Sieswerda L. E., (2007) Omega-3 fatty acids as treatments for mental illness: which disorder and which fatty acid? Lipids Health Dis. 6, 21.
73. Silverstone P. H., Wu R. H., O'Donnell T., Ulrich M., Asghar S. J., and, Hanstock C. C., (2002) Chronic treatment with both lithium and sodium valproate may normalize phosphoinositol cycle activity in bipolar patients. Hum. Psychopharmacol. 17, 321-327.
74. Sorgi P. J., Hallowell E. M., Hutchins H. L., and, Sears B., (2007) Effects of an open-label pilot study with high-dose EPA/DHA concentrates on plasma phospholipids and behavior in children with attention deficit hyperactivity disorder. Nutr. J. 6, 16.
75. 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.
76. Sun G. Y., and, Horrocks L. A., (1968) The fatty acid and aldehyde composition of the major phospholipids of mouse brain. Lipids 3, 79-83.
77. Sun G. Y., and, Horrocks L. A., (1973) Metabolism of palmitic acid in the subcellular fractions of mouse brain. J. Lipid Res. 14, 206-214.
78. Svennerholm L., (1964) The Distribution of Lipids in the Human Nervous System. I. Analytical Procedure. Lipids of Foetal and Newborn Brain. J. Neurochem. 11, 839-853.
79. Thies F., Nebe-von-Caron G., Powell J. R., Yaqoob P., Newsholme E. A., and, Calder P. C., (2001) Dietary supplementation with eicosapentaenoic acid, but not with other long-chain n-3 or n-6 polyunsaturated fatty acids, decreases natural killer cell activity in healthy subjects aged >55 y. Am. J. Clin. Nutr. 73, 539-548.
80. 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.