Docosahexaenoic acid homeostasis, brain aging and Alzheimer's disease: Can we reconcile the evidence?

Prostaglandins Leukotrienes and Essential Fatty Acids

Volumn 88, Issue 1, 2013, Pages 61-70

  Cunnane, Stephen C ^a   Chouinard Watkins, Raphael ^a   Castellano, Christian A ^a   Barberger Gateau, Pascale ^b,c  

^a UNIVERSITÉ DE SHERBROOKE   (Canada)

^b INSERM   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Aging; Aging related cognitive decline; Alzheimer's disease; Apolipoprotein E; Cognition; Docosahexaenoic acid; Omega 3 fatty acids

Indexed keywords

APOLIPOPROTEIN E; DOCOSAHEXAENOIC ACID; TRACER;

AGING; ALZHEIMER DISEASE; ARTICLE; AUTOPSY; BRAIN FUNCTION; BRAIN LEVEL; COGNITIVE DEFECT; DIET SUPPLEMENTATION; DISEASE ASSOCIATION; DISEASE MODEL; DRUG HALF LIFE; ESSENTIAL FATTY ACID DEFICIENCY; FATTY ACID ANALYSIS; FATTY ACID BLOOD LEVEL; FATTY ACID METABOLISM; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; HOMEOSTASIS; HUMAN; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RISK FACTOR; SINGLE DRUG DOSE;

AGING; ALZHEIMER DISEASE; ANIMALS; APOLIPOPROTEINS E; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; BRAIN; DIETARY FATS; DIETARY SUPPLEMENTS; DOCOSAHEXAENOIC ACIDS; EVIDENCE-BASED MEDICINE; GLUCOSE; HOMEOSTASIS; HUMANS; NEURONS; NEUROPROTECTIVE AGENTS; REPRODUCIBILITY OF RESULTS;

ANIMALIA;

EID: 84872051707     PISSN: 09523278     EISSN: 15322823     Source Type: Journal    
DOI: 10.1016/j.plefa.2012.04.006     Document Type: Article

References (100)

1. Dubois B., Feldman H.H., Jacova C., et al. Revising the definition of Alzheimer's disease: a new lexicon. Lancet Neurol. 2010, 9:1118-1127.
2. Peres K., Chrysostome V., Fabrigoule C., et al. Restriction in complex activities of daily living in MCI: impact on outcome. Neurology 2006, 67:461-466.
3. Fotuhi M., Mohassel P., Yaffe K. Fish consumption, long-chain omega-3 fatty acids and risk of cognitive decline or Alzheimer disease: a complex association. Nat. Clin. Pract. Neurol. 2009, 5:140-152.
4. Cunnane S.C., Plourde M., Pifferi F., et al. Fish, docosahexaenoic acid and Alzheimer's disease. Prog. Lipid. Res. 2009, 48:239-256.
5. P. Barberger Gateau, C. Feart, C. Samieri, L. Letenneur, Dietary patterns and dementia, in: K. Yaffe (Ed.), Chronic Medical Disease and Cognitive Aging: Toward a Healthy Body and Brain. Oxford University Press, in press.
6. Kim H.Y., Akbar M., Kim Y.S. Phosphatidylserine-dependent neuroprotective signaling promoted by docosahexaenoic acid. Prostag. Leukotr. Ess. 2010, 82:165-172.
7. Bazan N.G., Molina M.F., Gordon W.C. Docosahexaenoic acid signalolipidomics in nutrition: significance in aging, neuroinflammation, macular degeneration, Alzheimer's, and other neurodegenerative diseases. Annu. Rev. Nutr. 2011, 31:321-351.
8. Sidhu V.K., Huang B.X., Kim H.Y. Effects of docosahexaenoic acid on mouse brain synaptic plasma membrane proteome analyzed by mass spectrometry and (16)O/(18)O labeling. J. Proteome. Res. 2011, 10:5472-5480.
9. Calon F., Cole G. Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostag. Leukotr. Ess. 2007, 77(5-6):287-293.
10. Boudrault C., Bazinet R.P., Ma D.W. Experimental models and mechanisms underlying the protective effects of n-3 polyunsaturated fatty acids in Alzheimer's disease. J. Nutr. Biochem. 2009, 20(1):1-10.
11. Yaffe K. Treatment of Alzheimer disease and prognosis of dementia: time to translate research to results. J. Am. Med. Assoc. 2010, 304:1952-1953.
12. Quinn J.F., Raman R., Thomas R.G., et al. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. J. Am. Med. Assoc. 2010, 304:1903-1911.
13. Freund-Levi Y., Eriksdotter-Jönhagen M., Cederholm T., et al. Omega-3 fatty acid treatment in 174 patients with mild to moderate Alzheimer disease: OmegAD study: a randomized double-blind trial. Arch. Neurol. 2006, 63:1402-1408.
14. Barberger-Gateau P., Samieri C., Féart C., et al. Dietary omega-3 polyunsaturated fatty acids and Alzheimer's Disease: interaction with apolipoprotein E genotype. Curr. Alzheimer. Res. 2011, 8:479-491.
15. Plourde M., Fortier M., Vandal M., et al. , Unresolved issues in the link between docosahexaenoic acid and Alzheimer's disease. Prostag. Leukotr. Ess. 2007, 77:301-308.
16. Castellano C., Chouinard-Watkins R., Brenna J.T., et al. Does aging change docosahexaenoic acid homeostasis? Implications for the challenge to cognitive health in elderly. Oléagineux, Corps gras, lipides 2011, 18:175-180.
17. Brenna J.T., Diau G.Y. The influence of dietary docosahexaenoic acid and arachidonic acid on central nervous system polyunsaturated fatty acid composition. Prostag. Leukotr. Ess. 2007, 77:247-250.
18. Oster T., Pillot T. Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. Biochim. Biophys. Acta 1801, 2010:791-798.
19. Connor W.E., Neuringer M., Reisbick S. Essentiality of omega 3 fatty acids: evidence from the primate model and implications for human nutrition. World Rev. Nutr. Diet 1991, 66:118-132.
20. Soderberg M., Edlund C., Kristensson K., Dallner G. Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease. Lipids 1991, 26:421-425.
21. Lukiw W.J., Cui J.G., Marcheselli V.L., et al. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J. Clin. Invest. 2005, 115:2774-2783.
22. Astarita G., Jung K.M., Berchtold N.C., et al. Deficient liver biosynthesis of docosahexaenoic acid correlates with cognitive impairment in Alzheimer's disease. PLoS ONE 2010, 5:1-8.
23. Cunnane S., Schneider J., Tangney C. Plasma and brain fatty acid profiles in mild cognitive impairment and Alzheimer's disease. J. Alz. Dis. 2012, 29:691-697.
24. Fraser T., Tayler H., Love S. Fatty acid composition of frontal, temporal and parietal neocortex in the normal human brain and in Alzheimer's disease. Neurochem. Res. 2010, 35:503-513.
25. Guan Z., Wang Y., Cairns N.J., et al. Decrease and structural modifications of phosphatidylethanolamine plasmalogen in the brain with Alzheimer disease. J. Neuropath Exper. Neurol. 1999, 58:740-747.
26. Prasad M.R., Lovell M.A., Yatin M., et al. Regional membrane phospholipid alterations in Alzheimer's disease. Neurochem. Res. 1998, 23:81-88.
27. Corrigan F.M., Horrobin D.F., Skinner E.R., et al. Abnormal content of n-6 and n-3 long-chain unsaturated fatty acids in the phosphoglycerides and cholesterol esters of parahippocampal cortex from Alzheimer's disease patients and its relationship to acetyl CoA content. Int. J. Biochem. Cell Biol. 1998, 30:197-207.
28. Svennerholm L., Boström K., Jungbjer B. Changes in weight and compositions of major membrane components of human brain during the span of adult human life of Swedes. Acta Neuropathol. 1997, 94:345-352.
29. Aizenstein H.J., Nebes R.D., Saxton J.A., et al. Frequent amyloid deposition without significant cognitive impairment among the elderly. Arch. Neurol. 2008, 65:1509-1517.
30. Braak H., Braak E. Frequency of stages of Alzheimer-related lesions in different age categories. Neurobiol. Aging 1997, 18:351-357.
31. Duyckaerts C., Hauw J.J. Prevalence, incidence and duration of Braak's stages in the general population: can we know?. Neurobiol. Aging 1997, 18:362-369.
32. Umhau J.C., Zhou W., Carson R.E., et al. Imaging incorporation of circulating docosahexaenoic acid into the human brain using positron emission tomography. J. Lipid Res. 2009, 50:1259-1268.
33. Chen C.T., Green J.T., Orr S.K., et al. Regulation of brain polyunsaturated fatty acid uptake and turnover. Prostag. Leukotr. Ess. 2008, 79:85-91.
34. Serhan C.N., Petasis N.A. Resolvins and protectins in inflammation resolution. Chem. Rev. 2011, 111:5922-5943.
35. McNamara R.K., Jandacek R. Investigation of postmortem brain polyunsaturated fatty acid composition in psychiatric disorders: limitations, challenges, and future directions. J. Psychiatr. Res. 2011, 45:44-46.
36. Moriguchi T., Greiner R.S., Salem N. Behavioral deficits associated with dietary induction of decreased brain docosahexaenoic acid concentration. J. Neurochem. 2000, 75:2563-2573.
37. J.F. Mead, G.A. Dhopeshwarkar, Types of fatty acids in brain lipids, their derivation and function, in: Lipids, Malnutrition and the Developing Brain, Ciba Found Symposium 1971 59-72.
38. Walker B.L. Recovery of rat tissue lipids from essential fatty acid deficiency: brain, heart and testes. J. Nutr. 1968, 94:469-474.
39. M.A. Crawford, A.J. Sinclair, Nutritional influences in the evolution of mammalian brain, in: Lipids, Malnutrition and the Developing Brain, Ciba Found Symposium 1971 267-292.
40. Bernsohn J., Spitz F.J. Linoleic- and linolenic acid dependency of some brain membrane-bound enzymes after lipid deprivation in rats. Biochem. Biophys. Res. Commun. 1974, 57:293-298.
41. Connor W.E., Neuringer M., Lin D.S. Dietary effects on brain fatty acid composition: the reversibility of n-3 fatty acid deficiency and turnover of docosahexaenoic acid in the brain, erythrocytes, and plasma of rhesus monkeys. J. Lipid Res. 1990, 31:237-247.
42. Moriguchi T., Salem N. Recovery of brain docosahexaenoate leads to recovery of spatial task performance. J. Neurochem. 2003, 87:297-309.
43. Plourde M., Cunnane S.C. Extremely limited synthesis of long chain polyunsaturates in adults: implications for their dietary essentiality and use as supplements. Appl. Physiol. Nutr. Metab. 2007, 32:619-634.
44. Samieri C., Féart C., Proust-Lima C., et al. Omega-3 fatty acids and cognitive decline: modulation by ApoEε4 allele and depression. Neurobiol. Aging 2011, 32:2317.
45. Cherubini A., Andres-Lacueva C., Martin A., et al. Low plasma N-3 fatty acids and dementia in older persons: the InCHIANTI study. J. Gerontol-Series A Biol. Sci. Medical. Sci. 2007, 62:1120-1126.
46. Conquer J.A., Tierney M.C., Zecevic J., et al. Fatty acid analysis of blood plasma of patients with Alzheimer's disease, other types of dementia, and cognitive impairment. Lipids 2000, 35:1305-1312.
47. Corrigan F.M., Van Rhijn A.G., Ijomah G., et al. Tin and fatty acids in dementia. Prostag. Leukotr. Ess. 1991, 43:229-238.
48. Tully A.M., Roche H.M., Doyle R., et al. Low serum cholesteryl ester-docosahexaenoic acid levels in Alzheimer's disease: a case-control study. Brit. J. Nutr. 2003, 89:483-489.
49. Beydoun M.A., Kaufman J.S., Satia J.A., et al. Plasma n-3 fatty acids and the risk of cognitive decline in older adults: the atherosclerosis risk in communities study. Amer. J. Clin. Nutr. 2007, 85:1103-1111.
50. Manzato E., Roselli della Rovere G., Zambon S., et al. Cognitive functions are not affected by dietary fatty acids in elderly subjects in the Pro.V.A. study population. Aging Clin. Exp. Res. 2003, 15:83-86.
51. Laurin D., Verreault R., Lindsay J., et al. Omega-3 fatty acids and risk of cognitive impairment and dementia. J. Alz. Dis. 2003, 5:315-322.
52. Fortier M., Tremblay-Mercier J., Plourde M., et al. Higher plasma n-3 fatty acid status in the moderately healthy elderly in southern Québec: higher fish intake or aging-related change in n-3 fatty acid metabolism?. Prostag. Leukotr. Ess. 2010, 82:277-280.
53. De Groot R.H.M., Van Boxtel M.P.J., Schiepers O.J.G., et al. Age dependence of plasma phospholipid fatty acid levels: potential role of linoleic acid in the age-associated increase in docosahexaenoic acid and eicosapentaenoic acid concentrations. Brit. J. Nutr. 2009, 102:1058-1064.
54. Vandal M., Freemantle E., Tremblay-Mercier J., et al. Plasma omega-3 fatty acid response to a fish oil supplement in the healthy elderly. Lipids 2008, 43:1085-1089.
55. Rees D., Miles E.A., Banerjee T., et al. Dose-related effects of eicosapentaenoic acid on innate immune function in healthy humans: a comparison of young and older men. Amer J. Clin. Nutr. 2006, 83:331-342.
56. Rodríguez-Palmero M., López-Sabater M.C., Castellote-Bargallo A.I., et al. Administration of low doses of fish oil derived N-3 fatty acids to elderly subjects. Europ. J. Clin. Nutr. 1997, 51:554-560.
57. 13C-docosahexaenoic acid in the elderly. Nutr. Metab. 2011, 27(8):5.
58. Jack C.R., Petersen R.C., Xu Y.C., et al. Hippocampal atrophy and apolipoprotein E genotype are independently associated with Alzheimer's disease. Ann. Neurol. 1998, 43:303-310.
59. Jack C.R., Knopman D.S., Jagust W.J., et al. Hypothetical model of dynamic biomarkers of the Alzheimer's pathological cascade. Lancet. Neurol. 2010, 9:119-128.
60. Huang T.L., Zandi P.P., Tucker K.L., et al. Benefits of fatty fish on dementia risk are stronger for those without APOE epsilon4. Neurology 2005, 65:1409-1414.
61. Barberger-Gateau P., Raffaitin C., Letenneur L., et al. Dietary patterns and risk of dementia: the three-city cohort study. Neurology 2007, 69:1921-1930.
62. Whalley L.J., Deary I.J., Starr J.M., et al. n-3 Fatty acid erythrocyte membrane content, APOE varepsilon4, and cognitive variation: an observational follow-up study in late adulthood. Am. J. Clin. Nutr. 2008, 87:449-454.
63. Plourde M., Vohl M.C., Vandal M., et al. Plasma n-3 fatty acid response to an n-3 fatty acid supplement is modulated by apoE 4 but not by the common PPAR- L162V polymorphism in men. Brit. J. Nutr. 2009, 102:1121-1124.
64. R. Chouinard-Watkins, C. Rioux-Perreault, M. Fortier, et al., Metabolism of 13C-docosahexaenoic acid according to Apo E genotype, in: Proceedings of the Conference abstract, Quebec Aging Research Network annual scientific conference, Magog, Quebec, Canada, October 2011.
65. McCloy U., Ryan M.A., Pencharz P.B., et al. A comparison of the metabolism of eighteen-carbon 13C-unsaturated fatty acids in healthy women. J. Lipid. Res. 2004, 45:474-485.
66. Sanders T.A.B., Hinds A., Pereira C.C. Influence of n-3 fatty acids on blood lipids in normal subjects. J. Intern. Med. 1989, 225(Suppl):99-104.
67. Bazan N.G. Cell survival matters: docosahexaenoic acid signaling, neuroprotection and photoreceptors. Trends Neurosci. 2006, 29:263-271.
68. Chen C.T., Liu Z., Bazinet R.P. Rapid de-esterification and loss of eicosapentaenoic acid from rat brain phospholipids: an intracerebroventricular study. J. Neurochem. 2011, 116:363-373.
69. Harris W.S., Mozaffarian D., Lefevre M., et al. Towards establishing dietary reference intakes for eicosapentaenoic and docosahexaenoic acids. J. Nutr. 2009, 139:804S-819SS.
70. Kris-Etherton P.M., Grieger J.A., Etherton T.D. Dietary reference intakes for DHA and EPA. Prostag. Leukotr. Ess. 2009, 81:99-104.
71. Meyer B. Are we consuming enough long chain omega-3 polyunstaurated fatty acids for optimal health?. Prostag. Leukotr. Ess. 2011, 85(5):275-280.
72. James M.J., Ursin V.M., Cleland L.G. Metabolism of stearidonic acid in human subjects: comparison with the metabolism of other n-3 fatty acids. Am. J. Clin. Nutr. 2003, 77:1140-1145.
73. Fokkema M.R., Brouwer D.A.J., Hasperhoven I.A., et al. Short-term supplementation of low-dose γ-linolenic acid (GLA), α-linolenic acid (ALA), or GLA plus ALA does not augment LCPω3 status of Dutch vegans to an appreciable extent. Prostag. Leukotr. Ess. 2000, 63(5):287-292.
74. Horrobin D., Fokkema M.R., Muskiet F.A.J. The effects on plasma, red cell and platelet fatty acids of taking 12g/day of ethyl-eicosapentaenoate for 16 months: dihomogammalinolenic, arachidonic and docosahexaenoic acids and relevance to Inuit metabolism. Prostag. Leukotr. Ess. 2003, 68:301-304.
75. Cunnane S., Nugent S., Roy M., et al. Brain fuel metabolism, aging, and Alzheimer's disease. Nutrition 2011, 27:3-20.
76. Tan Z.S., Harris W.S., Beiser A.S., et al. Red blood cell omega-3 fatty acid levels and markers of accelerated brain aging. Neurology 2012, 78(9):658-664.
77. Krikorian R., Shidler M.D., Dangelo K., et al. Dietary ketosis enhances memory in mild cognitive impairment. Neurobiol. Aging 2012, 33(2):e19-e27. 425.
78. Pifferi F., Jouin M., Alessandri J.M., et al. N-3 long-chain fatty acids and regulation of glucose transport in two models of rat brain endothelial cells. Neurochem. Internat. 2010, 56:703-710.
79. Freemantle E., Vandal M., Tremblay-Mercier J., et al. Omega-3 fatty acids, energy substrates, and brain function during aging. Prostag. Leukotr. Ess. 2006, 75:213-220.
80. Ximenes da Silva A., Lavialle F., Gendrot G., et al. Glucose transport and utilization are altered in the brain of rats deficient in n-3 polyunsaturated fatty acids. J. Neurochem. 2002, 81:1328-1337.
81. Sublette M.E., Milak M.S., Hibbeln J.R., Freed P.J., Oquendo M.A., Malone K.M., Parsey R.V., Mann J.J. Plasma polyunsaturated fatty acids and regional cerebral glucose metabolism in major depression. Prostag. Leukotr. Ess. 2009, 80(1):57-64.
82. Nugent S., Croteau E., Pifferi F., Fortier M., Tremblay S., Turcotte E., Cunnane S.C. Brain and systemic glucose metabolism in the healthy elderly following fish oil supplementation. Prostag. Leukotr. Ess. 2011, 85(5):287-291.
83. Cole G.M., Ma Q.L., Frautschy S.A. Omega-3 fatty acids and dementia. Prostag. Leukotr. Ess. 2009, 81:213-221.
84. Chiu C.C., Frangou S., Chang C.J., et al. Associations between n-3 PUFA concentrations and cognitive function after recovery from late-life depression. Am. J. Clin. Nutr. 2012, 95:420-427.
85. C. Samieri, P. Maillard, F. Crivello, et al., Plasma eicosapentaenoic and docosahexaenoic acids and atrophy of the medial temporal lobe: a volumetric MRI study from the three city cohort, Neurology, in press.
86. Heude B., Ducimetière P., Berr C. Cognitive decline and fatty acid composition of erythrocyte membranes-the EVA study. Am. J. Clin. Nutr. 2003, 77:803-808.
87. Boston P.F., Bennett A., Horrobin D.F., Bennett C.N. Ethyl-EPA in Alzheimer's disease. A pilot study. Prostag. Leukotr. Ess. 2004, 71:341-346.
88. Yurko-Mauro K. Cognitive and cardiovascular benefits of docosahexaenoic acid in aging and cognitive decline. Curr. Alzheimer. Res. 2010, 7:190-196.
89. Dangour A.D., Allen E., Elbourne D., et al. Effect of 2-y n-3 long-chain polyunsaturated fatty acid supplementation on cognitive function in older people: a randomized, double-blind, controlled trial. Am. J. Clin. Nutr. 2010, 91:1725-1732.
90. Scheltens P. Moving forward with nutrition in Alzheimer's disease. Eur. J. Neurol. 2009, 16(Suppl 1):19-22.
91. Cunnane S.C. Human brain evolution: a question of solving key nutritional and metabolic constraints on mammalian brain development. Human Brain Evolution: The Influence of Freshwater and Marine Food Resources 2010, 33-64. Wiley-Blackwell. S.C. Cunnane, K.M. Stewart (Eds.).
92. Esposito G., Giovacchini G., Liow J.S., Bhattacharjee A.K., Greenstein D., Schapiro M., Hallett M., Herscovitch P., Eckelman W.C., Carson R.E., Rapoport S.I. Imaging neuroinflammation in Alzheimer's disease with radiolabeled arachidonic acid and PET. J. Nucl. Med. 2008, 49(9):1414-1421.
93. Gattaz W.F., Levy R., Cairns N.J., Forstl H., Braus D.F., Maras A. Relevance of metabolism of membrane phospholipids for Alzheimer dementia. Fortschr. Neurol. Psychiatr. 1996, 64(1):8-12.
94. Schaeffer E.L., Forlenza O.V., Gattaz W.F. Phospholipase A2 activation as a therapeutic approach for cognitive enhancement in early-stage Alzheimer disease. Psychopharmacology 2009, 202(1-3):37-51.
95. Brooksbank B.W., Martinez M. Lipid abnormalities in the brain in adult Down's syndrome and Alzheimer's disease. Mol. Chem. Neuropathol. 1989, 11:157-185.
96. Skinner E.R., Watt C., Besson J.A., Best P.V. Differences in the fatty acid composition of the grey and white matter of different regions of the brains of patients with Alzheimer's disease and control subjects. Brain 1993, 116(Pt 3):717-725.
97. Arterburn L.M., Hall E.B., Oken H. Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am. J. Clin. Nutr. 2006, 83:1467S-1476SS.
98. Lopez L.B., Kritz-Silverstein D., Barrett-Connor E. High dietary and plasma levels of the omega-3 fatty acid docosahexaenoic acid are associated with decreased dementia risk: the Rancho Bernardo study. J. Nutr. Health Aging 2011, 1-7.
99. Sublette M.E., Bosetti F., Demar J.C., et al. Plasma free polyunsaturated fatty acid levels are associated with symptom severity in acute mania. Bipolar Disord. 2007, 9:759-765.
100. Sun Q., Ma J., Campos H., et al. Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am. J. Clin. Nutr. 2007, 86:74-81.