Impact of omega-3 fatty acids in Parkinson's disease

Ageing Research Reviews

Volumn 10, Issue 4, 2011, Pages 453-463

  Bousquet, Mélanie ^a,b   Calon, Frédéric ^a,b   Cicchetti, Francesca ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Alpha synuclein; Docosahexaenoic acid (DHA); Dopaminergic system; Dyskinesias; Neuroprotection; Non motor symptoms

Indexed keywords

ALPHA SYNUCLEIN; NEUROTROPHIC FACTOR; OMEGA 3 FATTY ACID;

APOPTOSIS; DOPAMINERGIC ACTIVITY; DRUG MECHANISM; DYSKINESIA; HUMAN; LONG TERM CARE; NEUROPROTECTION; NEUROTRANSMISSION; NONHUMAN; OXIDATIVE STRESS; PARKINSON DISEASE; REVIEW; THERAPY EFFECT;

ANIMALS; APOPTOSIS; FATTY ACIDS, OMEGA-3; HUMANS; NEUROPROTECTIVE AGENTS; OXIDATIVE STRESS; PARKINSON DISEASE; REACTIVE OXYGEN SPECIES;

EID: 80052340822     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2011.03.001     Document Type: Review

References (157)

1. Aarsland D., Zaccai J., Brayne C. A systematic review of prevalence studies of dementia in Parkinson's disease. Mov. Disord. 2005, 20:1255-1263.
2. Ahmad S.O., Park J.H., Radel J.D., Levant B. Reduced numbers of dopamine neurons in the substantia nigra pars compacta and ventral tegmental area of rats fed an n-3 polyunsaturated fatty acid-deficient diet: a stereological study. Neurosci. Lett. 2008, 438:303-307.
3. Alves da Costa C., Checler F. Apoptosis in Parkinson's disease: is p53 the missing link between genetic and sporadic Parkinsonism?. Cell. Signal. 2011, 23:963-968.
4. Angot E., Steiner J.A., Hansen C., Li J.Y., Brundin P. Are synucleinopathies prion-like disorders?. Lancet Neurol. 2010, 9:1128-1138.
5. Assies J., Lok A., Bockting C.L., Weverling G.J., Lieverse R., Visser I., Abeling N.G., Duran M., Schene A.H. Fatty acids and homocysteine levels in patients with recurrent depression: an explorative pilot study. Prostaglandins Leukot. Essent. Fatty Acids 2004, 70:349-356.
6. Austin S.A., Floden A.M., Murphy E.J., Combs C.K. Alpha-synuclein expression modulates microglial activation phenotype. J. Neurosci. 2006, 26:10558-10563.
7. Barcelo-Coblijn G., Hogyes E., Kitajka K., Puskas L.G., Zvara A., Hackler L., Nyakas C., Penke Z., Farkas T. Modification by docosahexaenoic acid of age-induced alterations in gene expression and molecular composition of rat brain phospholipids. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11321-11326.
8. Barcelo-Coblijn G., Murphy E.J. Alpha-linolenic acid and its conversion to longer chain n-3 fatty acids: benefits for human health and a role in maintaining tissue n-3 fatty acid levels. Prog. Lipid Res. 2009, 48:355-374.
9. Bazan N.G. Neuroprotectin D1 (NPD1): a DHA-derived mediator that protects brain and retina against cell injury-induced oxidative stress. Brain Pathol. 2005, 15:159-166.
10. Bazinet R.P., Rao J.S., Chang L., Rapoport S.I., Lee H.J. Chronic valproate does not alter the kinetics of docosahexaenoic acid within brain phospholipids of the unanesthetized rat. Psychopharmacology (Berl.) 2005, 182:180-185.
11. Bohnen N.I., Albin R.L., Koeppe R.A., Wernette K.A., Kilbourn M.R., Minoshima S., Frey K.A. Positron emission tomography of monoaminergic vesicular binding in aging and Parkinson disease. J. Cereb. Blood Flow Metab. 2006, 26:1198-1212.
12. Boudrault C., Bazinet R.P., Kang J.X., Ma D.W. Cyclooxygenase-2 and n-6 PUFA are lower and DHA is higher in the cortex of fat-1 mice. Neurochem. Int. 2010, 56:585-589.
13. 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, 20:1-10.
14. Bousquet M., Gibrat C., Saint-Pierre M., Julien C., Calon F., Cicchetti F. Modulation of brain-derived neurotrophic factor as a potential neuroprotective mechanism of action of omega-3 fatty acids in a parkinsonian animal model. Prog. Neuropsychopharmacol. Biol. Psychiatry 2009, 33:1401-1408.
15. Bousquet M., Gue K., Emond V., Julien P., Kang J.X., Cicchetti F., Calon F. Transgenic conversion of omega-6 into omega-3 fatty acids in a mouse model of Parkinson's disease. J. Lipid Res. 2011, 52:263-271.
16. Bousquet M., Saint-Pierre M., Julien C., Salem N., Cicchetti F., Calon F. Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson's disease. FASEB J. 2008, 22:1213-1225.
17. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
18. Brenna J.T., Salem N., Sinclair A.J., Cunnane S.C. alpha-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot. Essent. Fatty Acids 2009, 80:85-91.
19. Cabin D.E., Shimazu K., Murphy D., Cole N.B., Gottschalk W., McIlwain K.L., Orrison B., Chen A., Ellis C.E., Paylor R., Lu B., Nussbaum R.L. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J. Neurosci. 2002, 22:8797-8807.
20. Calder P.C. Polyunsaturated fatty acids and inflammation. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:197-202.
21. Calon F. Nonpatentable drugs and the cost of our ignorance. CMAJ 2006, 174:483-484.
22. Calon, F. Omega-3 polyunsaturated fatty acids in Alzheimer's disease: key questions and partial answers. Curr. Alzheimer Res., in press.
23. Calon F., Cole G. Neuroprotective action of omega-3 polyunsaturated fatty acids against neurodegenerative diseases: evidence from animal studies. Prostaglandins Leukot. Essent. Fatty Acids 2007, 77:287-293.
24. Calon F., Lim G.P., Morihara T., Yang F., Ubeda O., Salem N., Frautschy S.A., Cole G.M. Dietary n-3 polyunsaturated fatty acid depletion activates caspases and decreases NMDA receptors in the brain of a transgenic mouse model of Alzheimer's disease. Eur. J. Neurosci. 2005, 22:617-626.
25. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., Rostaing P., Triller A., Salem N., Ashe K.H., Frautschy S.A., Cole G.M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645.
26. Calon F., Morissette M., Rajput A.H., Hornykiewicz O., Bedard P.J., Di Paolo T. Changes of GABA receptors and dopamine turnover in the postmortem brains of parkinsonians with levodopa-induced motor complications. Mov. Disord. 2003, 18:241-253.
27. Cansev M., Ulus I.H., Wang L., Maher T.J., Wurtman R.J. Restorative effects of uridine plus docosahexaenoic acid in a rat model of Parkinson's disease. Neurosci. Res. 2008, 62:206-209.
28. Castagnet P.I., Golovko M.Y., Barcelo-Coblijn G.C., Nussbaum R.L., Murphy E.J. Fatty acid incorporation is decreased in astrocytes cultured from alpha-synuclein gene-ablated mice. J. Neurochem. 2005, 94:839-849.
29. Chalon S., Delion-Vancassel S., Belzung C., Guilloteau D., Leguisquet A.M., Besnard J.C., Durand G. Dietary fish oil affects monoaminergic neurotransmission and behavior in rats. J. Nutr. 1998, 128:2512-2519.
30. 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, 166:363-373.
31. Chen C.T., Ma D.W., Kim J.H., Mount H.T., Bazinet R.P. The low density lipoprotein receptor is not necessary for maintaining mouse brain polyunsaturated fatty acid concentrations. J. Lipid Res. 2008, 49:147-152.
32. Cheng S.Y., Trombetta L.D. The induction of amyloid precursor protein and alpha-synuclein in rat hippocampal astrocytes by diethyldithiocarbamate and copper with or without glutathione. Toxicol. Lett. 2004, 146:139-149.
33. Chiu C.C., Su K.P., Cheng T.C., Liu H.C., Chang C.J., Dewey M.E., Stewart R., Huang S.Y. The effects of omega-3 fatty acids monotherapy in Alzheimer's disease and mild cognitive impairment: a preliminary randomized double-blind placebo-controlled study. Prog. Neuropsychopharmacol. Biol. Psychiatry 2008, 32:1538-1544.
34. Choi W., Zibaee S., Jakes R., Serpell L.C., Davletov B., Crowther R.A., Goedert M. Mutation E46K increases phospholipid binding and assembly into filaments of human alpha-synuclein. FEBS Lett. 2004, 576:363-368.
35. Collins N., Tighe A.P., Brunton S.A., Kris-Etherton P.M. Differences between dietary supplement and prescription drug omega-3 fatty acid formulations: a legislative and regulatory perspective. J. Am. Coll. Nutr. 2008, 27:659-666.
36. Conway K.A., Harper J.D., Lansbury P.T. Accelerated in vitro fibril formation by a mutant alpha-synuclein linked to early-onset Parkinson disease. Nat. Med. 1998, 4:1318-1320.
37. Costall B., Kelly M.E., Naylor R.J. The antidyskinetic action of dihomo-gamma-linolenic acid in the rodent. Br. J. Pharmacol. 1984, 83:733-740.
38. Croisier E., Moran L.B., Dexter D.T., Pearce R.K., Graeber M.B. Microglial inflammation in the parkinsonian substantia nigra: relationship to alpha-synuclein deposition. J. Neuroinflamm. 2005, 2:14.
39. Cunnane S.C., Anderson M.J. The majority of dietary linoleate in growing rats is beta-oxidized or stored in visceral fat. J. Nutr. 1997, 127:146-152.
40. Cunnane S.C., Plourde M., Pifferi F., Begin M., Feart C., Barberger-Gateau P. Fish, docosahexaenoic acid and Alzheimer's disease. Prog. Lipid Res. 2009, 48:239-256.
41. da Silva T.M., Munhoz R.P., Alvarez C., Naliwaiko K., Kiss A., Andreatini R., Ferraz A.C. Depression in Parkinson's disease: a double-blind, randomized, placebo-controlled pilot study of omega-3 fatty-acid supplementation. J. Affect Disord. 2008, 111:351-359.
42. de Lau L.M., Bornebroek M., Witteman J.C., Hofman A., Koudstaal P.J., Breteler M.M. Dietary fatty acids and the risk of Parkinson disease: the Rotterdam study. Neurology 2005, 64:2040-2045.
43. Delattre A.M., Kiss A., Szawka R.E., Anselmo-Franci J.A., Bagatini P.B., Xavier L.L., Rigon P., Achaval M., Iagher F., de David C., Marroni N.A., Ferraz A.C. Evaluation of chronic omega-3 fatty acids supplementation on behavioral and neurochemical alterations in 6-hydroxydopamine-lesion model of Parkinson's disease. Neurosci. Res. 2009, 66:256-264.
44. Delion S., Chalon S., Guilloteau D., Besnard J.C., Durand G. alpha-Linolenic acid dietary deficiency alters age-related changes of dopaminergic and serotoninergic neurotransmission in the rat frontal cortex. J. Neurochem. 1996, 66:1582-1591.
45. Delion S., Chalon S., Herault J., Guilloteau D., Besnard J.C., Durand G. Chronic dietary alpha-linolenic acid deficiency alters dopaminergic and serotoninergic neurotransmission in rats. J. Nutr. 1994, 124:2466-2476.
46. DeMar J.C., Lee H.J., Ma K., Chang L., Bell J.M., Rapoport S.I., Bazinet R.P. Brain elongation of linoleic acid is a negligible source of the arachidonate in brain phospholipids of adult rats. Biochim. Biophys. Acta 2006, 1761:1050-1059.
47. DeMar J.C., Ma K., Chang L., Bell J.M., Rapoport S.I. 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. 2005, 94:1063-1076.
48. Ethier I., Kagechika H., Shudo K., Rouillard C., Levesque D. Docosahexaenoic acid reduces haloperidol-induced dyskinesias in mice: involvement of Nur77 and retinoid receptors. Biol. Psychiatry 2004, 56:522-526.
49. Fahn S. The history of dopamine and levodopa in the treatment of Parkinson's disease. Mov. Disord. 2008, 23(Suppl. 3):S497-508.
50. FDA Guidance for Industry: Estimating the Maximum Safe Starting Dose in Initial Clinical Trials for Therapeutics in Adult Healthy Volunteers 2005.
51. Fedorova I., Salem N. Omega-3 fatty acids and rodent behavior. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:271-289.
52. Freund-Levi Y., Eriksdotter-Jonhagen M., Cederholm T., Basun H., Faxen-Irving G., Garlind A., Vedin I., Vessby B., Wahlund L.O., Palmblad J. 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.
53. Frey K.A., Koeppe R.A., Kilbourn M.R., Vander Borght T.M., Albin R.L., Gilman S., Kuhl D.E. Presynaptic monoaminergic vesicles in Parkinson's disease and normal aging. Ann. Neurol. 1996, 40:873-884.
54. Fuchs J., Tichopad A., Golub Y., Munz M., Schweitzer K.J., Wolf B., Berg D., Mueller J.C., Gasser T. Genetic variability in the SNCA gene influences alpha-synuclein levels in the blood and brain. FASEB J. 2008, 22:1327-1334.
55. Gao X., Chen H., Fung T.T., Logroscino G., Schwarzschild M.A., Hu F.B., Ascherio A. Prospective study of dietary pattern and risk of Parkinson disease. Am. J. Clin. Nutr. 2007, 86:1486-1494.
56. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
57. Golovko M.Y., Barcelo-Coblijn G., Castagnet P.I., Austin S., Combs C.K., Murphy E.J. The role of alpha-synuclein in brain lipid metabolism: a downstream impact on brain inflammatory response. Mol. Cell. Biochem. 2009, 326:55-66.
58. Golovko M.Y., Murphy E.J. Brain prostaglandin formation is increased by alpha-synuclein gene-ablation during global ischemia. Neurosci. Lett. 2008, 432:243-247.
59. Golovko M.Y., Rosenberger T.A., Faergeman N.J., Feddersen S., Cole N.B., Pribill I., Berger J., Nussbaum R.L., Murphy E.J. Acyl-CoA synthetase activity links wild-type but not mutant alpha-synuclein to brain arachidonate metabolism. Biochemistry 2006, 45:6956-6966.
60. Golovko M.Y., Rosenberger T.A., Feddersen S., Faergeman N.J., Murphy E.J. Alpha-synuclein gene ablation increases docosahexaenoic acid incorporation and turnover in brain phospholipids. J. Neurochem. 2007, 101:201-211.
61. Guschina I., Millership S., O'Donnell V., Ninkina N., Harwood J., Buchman V. Lipid classes and fatty acid patterns are altered in the brain of gamma-synuclein null mutant mice. Lipids 2011, 46:121-130.
62. Hamilton J.A., Brunaldi K. A model for fatty acid transport into the brain. J. Mol. Neurosci. 2007, 33:12-17.
63. Hansen C., Angot E., Bergstrom A.L., Steiner J.A., Pieri L., Paul G., Outeiro T.F., Melki R., Kallunki P., Fog K., Li J.Y., Brundin P. alpha-Synuclein propagates from mouse brain to grafted dopaminergic neurons and seeds aggregation in cultured human cells. J. Clin. Invest. 2011, 121:715-725.
64. Harrington K.A., Augood S.J., Kingsbury A.E., Foster O.J., Emson P.C. Dopamine transporter (Dat) and synaptic vesicle amine transporter (VMAT2) gene expression in the substantia nigra of control and Parkinson's disease. Brain Res. Mol. Brain Res. 1996, 36:157-162.
65. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
66. Hong S., Gronert K., Devchand P.R., Moussignac R.L., Serhan C.N. Novel docosatrienes and 17S-resolvins generated from docosahexaenoic acid in murine brain, human blood, and glial cells. Autacoids in anti-inflammation. J. Biol. Chem. 2003, 278:14677-14687.
67. Hooijmans C.R., Van der Zee C.E., Dederen P.J., Brouwer K.M., Reijmer Y.D., van Groen T., Broersen L.M., Lutjohann D., Heerschap A., Kiliaan A.J. DHA and cholesterol containing diets influence Alzheimer-like pathology, cognition and cerebral vasculature in APPswe/PS1dE9 mice. Neurobiol. Dis. 2009, 33:482-498.
68. Jakes R., Spillantini M.G., Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett. 1994, 345:27-32.
69. Jicha G.A., Markesbery W.R. Omega-3 fatty acids: potential role in the management of early Alzheimer's disease. Clin. Interv. Aging 2010, 5:45-61.
70. Julien C., Berthiaume L., Hadj-Tahar A., Rajput A.H., Bedard P.J., Di Paolo T., Julien P., Calon F. Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and parkinsonian monkeys. Neurochem. Int. 2006, 48:404-414.
71. Kaasinen V., Nurmi E., Bruck A., Eskola O., Bergman J., Solin O., Rinne J.O. Increased frontal [(18)F]fluorodopa uptake in early Parkinson's disease: sex differences in the prefrontal cortex. Brain 2001, 124:1125-1130.
72. Kehagia A.A., Barker R.A., Robbins T.W. Neuropsychological and clinical heterogeneity of cognitive impairment and dementia in patients with Parkinson's disease. Lancet Neurol. 2010, 9:1200-1213.
73. Kitajka K., Sinclair A.J., Weisinger R.S., Weisinger H.S., Mathai M., Jayasooriya A.P., Halver J.E., Puskas L.G. Effects of dietary omega-3 polyunsaturated fatty acids on brain gene expression. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:10931-10936.
74. Kodas E., Page G., Zimmer L., Vancassel S., Guilloteau D., Durand G., Chalon S. Neither the density nor function of striatal dopamine transporters were influenced by chronic n-3 polyunsaturated fatty acid deficiency in rodents. Neurosci. Lett. 2002, 321:95-99.
75. Kordower J.H., Chu Y., Hauser R.A., Freeman T.B., Olanow C.W. Lewy body-like pathology in long-term embryonic nigral transplants in Parkinson's disease. Nat. Med. 2008, 14:504-506.
76. Kotani S., Sakaguchi E., Warashina S., Matsukawa N., Ishikura Y., Kiso Y., Sakakibara M., Yoshimoto T., Guo J., Yamashima T. Dietary supplementation of arachidonic and docosahexaenoic acids improves cognitive dysfunction. Neurosci. Res. 2006, 56:159-164.
77. Lang A.E., Lozano A.M. Parkinson's disease. First of two parts. N. Engl. J. Med. 1998, 339:1044-1053.
78. Lang A.E., Lozano A.M. Parkinson's disease. Second of two parts. N. Engl. J. Med. 1998, 339:1130-1143.
79. Langston J.W., Forno L.S., Tetrud J., Reeves A.G., Kaplan J.A., Karluk D. Evidence of active nerve cell degeneration in the substantia nigra of humans years after 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure. Ann. Neurol. 1999, 46:598-605.
80. Lansbury P.T., Lashuel H.A. A century-old debate on protein aggregation and neurodegeneration enters the clinic. Nature 2006, 443:774-779.
81. Lapillonne A., Clarke S.D., Heird W.C. Polyunsaturated fatty acids and gene expression. Curr. Opin. Clin. Nutr. Metab. Care 2004, 7:151-156.
82. Lee F.J., Liu F., Pristupa Z.B., Niznik H.B. Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J. 2001, 15:916-926.
83. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
84. Lesperance F., Frasure-Smith N., St-Andre E., Turecki G., Lesperance P., Wisniewski S.R. The efficacy of omega-3 supplementation for major depression: a randomized controlled trial. J. Clin. Psychiatry 2010, [Epub ahead of print]. 10.4088/JCP.10m05966blu.
85. Li J.Y., Englund E., Holton J.L., Soulet D., Hagell P., Lees A.J., Lashley T., Quinn N.P., Rehncrona S., Bjorklund A., Widner H., Revesz T., Lindvall O., Brundin P. Lewy bodies in grafted neurons in subjects with Parkinson's disease suggest host-to-graft disease propagation. Nat. Med. 2008, 14:501-503.
86. Lichtenstein A.H., Appel L.J., Brands M., Carnethon M., Daniels S., Franch H.A., Franklin B., Kris-Etherton P., Harris W.S., Howard B., Karanja N., Lefevre M., Rudel L., Sacks F., Van Horn L., Winston M., Wylie-Rosett J. Diet and lifestyle recommendations revision 2006: a scientific statement from the American Heart Association Nutrition Committee. Circulation 2006, 114:82-96.
87. Lim S.Y., Lang A.E. The nonmotor symptoms of Parkinson's disease-an overview. Mov. Disord. 2010, 25(Suppl. 1):S123-S130.
88. Lucas M., Asselin G., Plourde M., Cunnane S.C., Dewailly E., Dodin S. n-3 Fatty acid intake from marine food products among Quebecers: comparison to worldwide recommendations. Public Health Nutr. 2010, 13:63-70.
89. Mamalakis G., Tornaritis M., Kafatos A. Depression and adipose essential polyunsaturated fatty acids. Prostaglandins Leukot. Essent. Fatty Acids 2002, 67:311-318.
90. Marangell L.B., Martinez J.M., Zboyan H.A., Kertz B., Kim H.F., Puryear L.J. A double-blind, placebo-controlled study of the omega-3 fatty acid docosahexaenoic acid in the treatment of major depression. Am. J. Psychiatry 2003, 160:996-998.
91. Marcheselli V.L., Hong S., Lukiw W.J., Tian X.H., Gronert K., Musto A., Hardy M., Gimenez J.M., Chiang N., Serhan C.N., Bazan N.G. Novel docosanoids inhibit brain ischemia-reperfusion-mediated leukocyte infiltration and pro-inflammatory gene expression. J. Biol. Chem. 2003, 278:43807-43817.
92. Mashek D.G., Li L.O., Coleman R.A. Rat long-chain acyl-CoA synthetase mRNA, protein, and activity vary in tissue distribution and in response to diet. J. Lipid Res. 2006, 47:2004-2010.
93. McGeer P.L., McGeer E.G. Inflammation and neurodegeneration in Parkinson's disease. Parkinsonism Relat. Disord. 2004, 10(Suppl. 1):S3-7.
94. McNamara R.K., Jandacek R., Rider T., Tso P., Dwivedi Y., Pandey G.N. Selective deficits in erythrocyte docosahexaenoic acid composition in adult patients with bipolar disorder and major depressive disorder. J. Affect. Disord. 2010, 126:303-311.
95. Mellor J.E., Laugharne J.D., Peet M. Schizophrenic symptoms and dietary intake of n-3 fatty acids. Schizophr. Res. 1995, 18:85-86.
96. Miller G.W., Erickson J.D., Perez J.T., Penland S.N., Mash D.C., Rye D.B., Levey A.I. Immunochemical analysis of vesicular monoamine transporter (VMAT2) protein in Parkinson's disease. Exp. Neurol. 1999, 156:138-148.
97. Mischoulon D., Papakostas G.I., Dording C.M., Farabaugh A.H., Sonawalla S.B., Agoston A.M., Smith J., Beaumont E.C., Dahan L.E., Alpert J.E., Nierenberg A.A., Fava M. A double-blind, randomized controlled trial of ethyl-eicosapentaenoate for major depressive disorder. J. Clin. Psychiatry 2009, 70:1636-1644.
98. Miyazawa D., Yasui Y., Yamada K., Ohara N., Okuyama H. Regional differences of the mouse brain in response to an alpha-linolenic acid-restricted diet: neurotrophin content and protein kinase activity. Life Sci. 2010, 87:490-494.
99. Mogi M., Togari A., Kondo T., Mizuno Y., Komure O., Kuno S., Ichinose H., Nagatsu T. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 1999, 270:45-48.
100. Muntane G., Janue A., Fernandez N., Odena M.A., Oliveira E., Boluda S., Portero-Otin M., Naudi A., Boada J., Pamplona R., Ferrer I. Modification of brain lipids but not phenotype in alpha-synucleinopathy transgenic mice by long-term dietary n-3 fatty acids. Neurochem. Int. 2010, 56:318-328.
101. Murakami K., Sasaki S. Dietary intake and depressive symptoms: a systematic review of observational studies. Mol. Nutr. Food Res. 2010, 54:471-488.
102. Murphy D.D., Rueter S.M., Trojanowski J.Q., Lee V.M. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 2000, 20:3214-3220.
103. Murphy E.J., Owada Y., Kitanaka N., Kondo H., Glatz J.F. Brain arachidonic acid incorporation is decreased in heart fatty acid binding protein gene-ablated mice. Biochemistry 2005, 44:6350-6360.
104. Narayanan V., Guo Y., Scarlata S. Fluorescence studies suggest a role for alpha-synuclein in the phosphatidylinositol lipid signaling pathway. Biochemistry 2005, 44:462-470.
105. Narhi L., Wood S.J., Steavenson S., Jiang Y., Wu G.M., Anafi D., Kaufman S.A., Martin F., Sitney K., Denis P., Louis J.C., Wypych J., Biere A.L., Citron M. Both familial Parkinson's disease mutations accelerate alpha-synuclein aggregation. J. Biol. Chem. 1999, 274:9843-9846.
106. Nariai T., DeGeorge J.J., Greig N.H., Genka S., Rapoport S.I., Purdon A.D. Differences in rates of incorporation of intravenously injected radiolabeled fatty acids into phospholipids of intracerebrally implanted tumor and brain in awake rats. Clin. Exp. Metastasis 1994, 12:213-225.
107. Nemets B., Stahl Z., Belmaker R.H. Addition of omega-3 fatty acid to maintenance medication treatment for recurrent unipolar depressive disorder. Am. J. Psychiatry 2002, 159:477-479.
108. Obeso J.A., Rodriguez-Oroz M.C., Goetz C.G., Marin C., Kordower J.H., Rodriguez M., Hirsch E.C., Farrer M., Schapira A.H., Halliday G. Missing pieces in the Parkinson's disease puzzle. Nat. Med. 2010, 16:653-661.
109. Olanow C.W., Prusiner S.B. Is Parkinson's disease a prion disorder?. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:12571-12572.
110. Olanow C.W., Rascol O., Hauser R., Feigin P.D., Jankovic J., Lang A., Langston W., Melamed E., Poewe W., Stocchi F., Tolosa E. A double-blind, delayed-start trial of rasagiline in Parkinson's disease. N. Engl. J. Med. 2009, 361:1268-1278.
111. Orr S.K., Bazinet R.P. The emerging role of docosahexaenoic acid in neuroinflammation. Curr. Opin. Investig. Drugs 2008, 9:735-743.
112. Ouellet M., Emond V., Chen C.T., Julien C., Bourasset F., Oddo S., LaFerla F., Bazinet R.P., Calon F. Diffusion of docosahexaenoic and eicosapentaenoic acids through the blood-brain barrier: an in situ cerebral perfusion study. Neurochem. Int. 2009, 55:476-482.
113. Ozsoy O., Tanriover G., Derin N., Uysal N., Demir N., Gemici B., Kencebay C., Yargicoglu P., Agar A., Aslan M. The effect of docosahexaenoic acid on visual evoked potentials in a mouse model of Parkinson's disease: the role of cyclooxygenase-2 and nuclear factor kappa-B. Neurotox. Res. 2011, [Epub ahead of print]. 10.1007/s12640-011-9238-y.
114. Parain K., Murer M.G., Yan Q., Faucheux B., Agid Y., Hirsch E., Raisman-Vozari R. Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra. Neuroreport 1999, 10:557-561.
115. Payton J.E., Perrin R.J., Woods W.S., George J.M. Structural determinants of PLD2 inhibition by alpha-synuclein. J. Mol. Biol. 2004, 337:1001-1009.
116. Perez R.G., Waymire J.C., Lin E., Liu J.J., Guo F., Zigmond M.J. A role for alpha-synuclein in the regulation of dopamine biosynthesis. J. Neurosci. 2002, 22:3090-3099.
117. Pollanen M.S., Dickson D.W., Bergeron C. Pathology and biology of the Lewy body. J. Neuropathol. Exp. Neurol. 1993, 52:183-191.
118. Porter N.A., Caldwell S.E., Mills K.A. Mechanisms of free radical oxidation of unsaturated lipids. Lipids 1995, 30:277-290.
119. Quinn J.F., Raman R., Thomas R.G., Yurko-Mauro K., Nelson E.B., Van Dyck C., Galvin J.E., Emond J., Jack C.R., Weiner M., Shinto L., Aisen P.S. Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 2010, 304:1903-1911.
120. Rao J.S., Ertley R.N., Lee H.J., DeMar J.C., Arnold J.T., Rapoport S.I., Bazinet R.P. n-3 polyunsaturated fatty acid deprivation in rats decreases frontal cortex BDNF via a p38 MAPK-dependent mechanism. Mol. Psychiatry 2007, 12:36-46.
121. Rapoport S.I., Chang M.C., Spector A.A. Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J. Lipid Res. 2001, 42:678-685.
122. Ravina B., Eidelberg D., Ahlskog J.E., Albin R.L., Brooks D.J., Carbon M., Dhawan V., Feigin A., Fahn S., Guttman M., Gwinn-Hardy K., McFarland H., Innis R., Katz R.G., Kieburtz K., Kish S.J., Lange N., Langston J.W., Marek K., Morin L., Moy C., Murphy D., Oertel W.H., Oliver G., Palesch Y., Powers W., Seibyl J., Sethi K.D., Shults C.W., Sheehy P., Stoessl A.J., Holloway R. The role of radiotracer imaging in Parkinson disease. Neurology 2005, 64:208-215.
123. Richter-Landsberg C., Gorath M., Trojanowski J.Q., Lee V.M. alpha-synuclein is developmentally expressed in cultured rat brain oligodendrocytes. J. Neurosci. Res. 2000, 62:9-14.
124. Riedel M., Goldbaum O., Wille M., Richter-Landsberg C. Membrane lipid modification by docosahexaenoic acid (DHA) promotes the formation of alpha-synuclein inclusion bodies immunopositive for SUMO-1 in oligodendroglial cells after oxidative stress. J. Mol. Neurosci. 2011, 43:290-302.
125. Salem N., Hullin F., Yoffe A.M., Karanian J.W., Kim H.Y. Fatty acid and phospholipid species composition of rat tissues after a fish oil diet. Adv. Prostaglandin Thromboxane Leukot. Res. 1989, 19:618-622.
126. Salem N., Litman B., Kim H.Y., Gawrisch K. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 2001, 36:945-959.
127. Samadi P., Gregoire L., Rouillard C., Bedard P.J., Di Paolo T., Levesque D. Docosahexaenoic acid reduces levodopa-induced dyskinesias in 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine monkeys. Ann. Neurol. 2006, 59:282-288.
128. Saravanan P., Davidson N.C., Schmidt E.B., Calder P.C. Cardiovascular effects of marine omega-3 fatty acids. Lancet 2010, 376:540-550.
129. Saucedo-Cardenas O., Quintana-Hau J.D., Le W.D., Smidt M.P., Cox J.J., De Mayo F., Burbach J.P., Conneely O.M. Nurr1 is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:4013-4018.
130. Schapira A.H., Tolosa E. Molecular and clinical prodrome of Parkinson disease: implications for treatment. Nat. Rev. Neurol. 2010, 6:309-317.
131. Schwarting R.K., Huston J.P. Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog. Neurobiol. 1996, 49:215-266.
132. Schwarz J., Storch A., Koch W., Pogarell O., Radau P.E., Tatsch K. Loss of dopamine transporter binding in Parkinson's disease follows a single exponential rather than linear decline. J. Nucl. Med. 2004, 45:1694-1697.
133. Serhan C.N., Gotlinger K., Hong S., Arita M. Resolvins, docosatrienes, and neuroprotectins, novel omega-3-derived mediators, and their aspirin-triggered endogenous epimers: an overview of their protective roles in catabasis. Prostaglandins Other Lipid Mediat. 2004, 73:155-172.
134. Shulman L.M., Taback R.L., Bean J., Weiner W.J. Comorbidity of the nonmotor symptoms of Parkinson's disease. Mov. Disord. 2001, 16:507-510.
135. Simopoulos A.P. Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed. Pharmacother. 2006, 60:502-507.
136. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M.R., Muenter M., Baptista M., Miller D., Blancato J., Hardy J., Gwinn-Hardy K. alpha-Synuclein locus triplication causes Parkinson's disease. Science 2003, 302:841.
137. Smith W.L. Nutritionally essential fatty acids and biologically indispensable cyclooxygenases. Trends Biochem. Sci. 2008, 33:27-37.
138. Souza J.M., Giasson B.I., Lee V.M., Ischiropoulos H. Chaperone-like activity of synucleins. FEBS Lett. 2000, 474:116-119.
139. Sprecher H. Metabolism of highly unsaturated n-3 and n-6 fatty acids. Biochim. Biophys. Acta 2000, 1486:219-231.
140. Sprecher H., Chen Q., Yin F.Q. Regulation of the biosynthesis of 22:5n-6 and 22:6n-3: a complex intracellular process. Lipids 1999, 34(Suppl.):S153-S156.
141. Su H.M., Moser A.B., Moser H.W., Watkins P.A. Peroxisomal straight-chain Acyl-CoA oxidase and D-bifunctional protein are essential for the retroconversion step in docosahexaenoic acid synthesis. J. Biol. Chem. 2001, 276:38115-38120.
142. Svennerholm L. The distribution of lipids in the human nervous system. I. Analytical procedure. Lipids of foetal and newborn brain. J. Neurochem. 1964, 11:839-853.
143. Tanriover G., Seval-Celik Y., Ozsoy O., Akkoyunlu G., Savcioglu F., Hacioglu G., Demir N., Agar A. The effects of docosahexaenoic acid on glial derived neurotrophic factor and neurturin in bilateral rat model of Parkinson's disease. Folia Histochem. Cytobiol. 2010, 48:434-441.
144. Tansey M.G., Goldberg M.S. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis. 2010, 37:510-518.
145. Tanskanen A., Hibbeln J.R., Hintikka J., Haatainen K., Honkalampi K., Viinamaki H. Fish consumption, depression, and suicidality in a general population. Arch. Gen. Psychiatry 2001, 58:512-513.
146. Thibaut F., Faucheux B.A., Marquez J., Villares J., Menard J.F., Agid Y., Hirsch E.C. Regional distribution of monoamine vesicular uptake sites in the mesencephalon of control subjects and patients with Parkinson's disease: a postmortem study using tritiated tetrabenazine. Brain Res. 1995, 692:233-243.
147. Thies F., Pillon C., Moliere P., Lagarde M., Lecerf J. Preferential incorporation of sn-2 lysoPC DHA over unesterified DHA in the young rat brain. Am. J. Physiol. 1994, 267:R1273-1279.
148. Vaddadi K.S. Essential fatty acids and neuroleptic drug induced tardive dyskinesia: preliminary clinical observations. IRCS Med. Sci. 1984, 12:678-679.
149. Vaddadi K.S., Courtney P., Gilleard C.J., Manku M.S., Horrobin D.F. A double-blind trial of essential fatty acid supplementation in patients with tardive dyskinesia. Psychiatry Res. 1989, 27:313-323.
150. Wada M., DeLong C.J., Hong Y.H., Rieke C.J., Song I., Sidhu R.S., Yuan C., Warnock M., Schmaier A.H., Yokoyama C., Smyth E.M., Wilson S.J., FitzGerald G.A., Garavito R.M., Sui de X., Regan J.W., Smith W.L. Enzymes and receptors of prostaglandin pathways with arachidonic acid-derived versus eicosapentaenoic acid-derived substrates and products. J. Biol. Chem. 2007, 282:22254-22266.
151. Wang Y., Botolin D., Christian B., Busik J., Xu J., Jump D.B. Tissue-specific, nutritional, and developmental regulation of rat fatty acid elongases. J. Lipid Res. 2005, 46:706-715.
152. Wersinger C., Sidhu A. Attenuation of dopamine transporter activity by alpha-synuclein. Neurosci. Lett. 2003, 340:189-192.
153. Williams-Gray C.H., Foltynie T., Brayne C.E., Robbins T.W., Barker R.A. Evolution of cognitive dysfunction in an incident Parkinson's disease cohort. Brain 2007, 130:1787-1798.
154. Yehuda S., Carasso R.L. Modulation of learning, pain thresholds, and thermoregulation in the rat by preparations of free purified alpha-linolenic and linoleic acids: determination of the optimal omega 3-to-omega 6 ratio. Proc. Natl. Acad. Sci. U.S.A. 1993, 90:10345-10349.
155. Yurko-Mauro K. Cognitive and cardiovascular benefits of docosahexaenoic acid in aging and cognitive decline. Curr. Alzheimer Res. 2010, 7:190-196.
156. Zimmer L., Delion-Vancassel S., Durand G., Guilloteau D., Bodard S., Besnard J.C., Chalon S. Modification of dopamine neurotransmission in the nucleus accumbens of rats deficient in n-3 polyunsaturated fatty acids. J. Lipid Res. 2000, 41:32-40.
157. Zimmer L., Delpal S., Guilloteau D., Aioun J., Durand G., Chalon S. Chronic n-3 polyunsaturated fatty acid deficiency alters dopamine vesicle density in the rat frontal cortex. Neurosci. Lett. 2000, 284:25-28.