Impact of DHA intake in a mouse model of synucleinopathy

Experimental Neurology

Volumn 301, Issue , 2018, Pages 39-49

  Coulombe, Katherine ^a,b,c   Kerdiles, Olivier ^a,b,c   Tremblay, Cyntia ^b   Emond, Vincent ^b   Lebel, Manon ^a,b   Boulianne, Anne Sophie ^a   Plourde, Mélanie ^d   Cicchetti, Francesca ^a,b   Calon, Frédéric ^a,b,c  

^a UNIVERSITÉ LAVAL   (Canada)

^b Université Laval   (Canada)

^c NutriNeuro Bordeaux University   (France)

^d UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

Docosahexaenoic acid; Dopamine; Parkinson; Polyunsaturated fatty acids omega 3; Synaptic proteins; Thy1 Syn; synuclein

Indexed keywords

ALPHA SYNUCLEIN; DOCOSAHEXAENOIC ACID; ICOSAPENTAENOIC ACID; NEURON SPECIFIC NUCLEAR PROTEIN; OMEGA 3 FATTY ACID; POSTSYNAPTIC DENSITY PROTEIN 95; SYNAPTOPHYSIN; VESICULAR ACETYLCHOLINE TRANSPORTER; SNCA PROTEIN, HUMAN;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BRAIN CORTEX; CELL SURVIVAL; CONTROLLED STUDY; CYLINDER TEST; DIET SUPPLEMENTATION; DIETARY INTAKE; DOPAMINERGIC SYSTEM; FOOD COMPOSITION; GAS CHROMATOGRAPHY; GENOTYPE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LONGEVITY; MALE; MORTALITY RATE; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; OLIGOMERIZATION; PARKINSON DISEASE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SUBSTANTIA NIGRA; SURVIVAL RATE; SYNUCLEINOPATHY; WESTERN BLOTTING; ANIMAL; BRAIN; C57BL MOUSE; DIETARY SUPPLEMENT; DISEASE MODEL; DRUG EFFECT; GENETICS; HUMAN; PARKINSONISM; PATHOLOGY; TRANSGENIC MOUSE;

ALPHA-SYNUCLEIN; ANIMALS; BRAIN; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; HUMANS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PARKINSONIAN DISORDERS;

EID: 85038817589     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2017.12.002     Document Type: Article

References (67)

1. Akbar, M., Calderon, F., Wen, Z., Kim, H.-Y., Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. PNAS 102 (2005), 10858–10863.
2. Arsenault, D., Julien, C., Tremblay, C., Calon, F., DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS One, 6, 2011, e17397.
3. Assayag, K., Yakunin, E., Loeb, V., Selkoe, D.J., Sharon, R., Polyunsaturated fatty acids induce alpha-synuclein-related pathogenic changes in neuronal cells. Am. J. Pathol. 171 (2007), 2000–2011.
4. Barrett, P.J., Greenamyre, T.J., Post-translational modification of alpha-synuclein in Parkinson's disease. Brain Res. 1628 (2015), 247–253.
5. Bartels, T., Choi, J.G., Selkoe, D.J., α-Synuclein occurs physiologically as a helically folded tetramer that resists aggregation. Nature 477 (2011), 107–110.
6. Bezard, E., Przedborski, S., A tale on animal models of Parkinson's disease. Mov. Disord. 26 (2011), 993–1002.
7. Bezard, E., Yue, Z., Kirik, D., Spillantini, M.G., Animal models of Parkinson's disease: limits and relevance to neuroprotection studies. Mov. Disord. 28 (2013), 61–70.
8. Bourre, J.M., Pascal, G., Durand, M., Masson, M., Dumont, O., Piciotti, M., Alterations in the fatty acid composition of rat brain cells (neurons, astrocytes, and oligodendrocytes) and of subcellular fractions (myelin and synaptosomes) induced by a diet devoid of n-3 fatty acids. J. Neurochem. 43 (1984), 342–348.
9. Bousquet, M., Saint-Pierre, M., Julien, C., Salem, N. Jr., 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 22 (2008), 1213–1225.
10. 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. Neuro-Psychopharmacol. Biol. Psychiatry 33 (2009), 1401–1408.
11. Bousquet, M., Calon, F., Cicchetti, F., Impact of omega-3 fatty acids in Parkinson's disease. Ageing Res. Rev. 10 (2011), 453–463.
12. 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. 52 (2011), 263–271.
13. Brooks, S.P., Dunnett, S.B., Tests to assess motor phenotype in mice: a user's guide. Nat. Rev. Neurosci. 10 (2009), 519–529.
14. Calder, P.C., n-3 fatty acids, inflammation and immunity: new mechanisms to explain old actions. Proc. Nutr. Soc. 72 (2013), 326–336.
15. Calon, F., Cicchetti, F., Can we prevent Parkinson's disease with n-3 polyunsaturated fatty acids?. Futur. Lipidol. 3 (2008), 133–137.
16. Calon, F., Lavertu, N., Lemieux, A.-M., Morissette, M., Goulet, M., Grondin, R., Blanchet, P., Bédard, P., Di Paolo, T., Effect of MPTP-induced denervation on basal ganglia GABAB receptors: correlation with dopamine concentrations and dopamine transporter. Synapse 40 (2001), 225–234.
17. 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 43 (2004), 633–645.
18. Cardoso, H.D., dos Santos Junior, E.F., de Santana, D.F., Goncalves-Pimentel, C., Angelim, M.K., Isaac, A.R., Lagranha, C.J., Guedes, R.C., Beltrao, E.I., Morya, E., Rodrigues, M.C., Andrade-da-Costa, B.L., Omega-3 deficiency and neurodegeneration in the substantia nigra: involvement of increased nitric oxide production and reduced BDNF expression. Biochim. Biophys. Acta 1840 (2014), 1902–1912.
19. Chalon, S., Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot. Essent. Fat. Acids 75 (2006), 259–269.
20. Chesselet, M.F., Richter, F., Zhu, C., Magen, I., Watson, M.B., Subramaniam, S.R., A progressive mouse model of Parkinson's disease: the Thy1-aSyn (“line 61”) mice. Neurotherapeutics 9 (2012), 297–314.
21. Chu, Y., Kordower, J.H., Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: is this the target for Parkinson's disease?. Neurobiol. Dis. 25 (2007), 134–149.
22. Coulombe, K., Saint-Pierre, M., Cisbani, G., St-Amour, I., Gibrat, C., Giguere-Rancourt, A., Calon, F., Cicchetti, F., Partial neurorescue effects of DHA following a 6-OHDA lesion of the mouse dopaminergic system. J. Nutr. Biochem. 30 (2016), 133–142.
23. 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. 111:2–3 (2008), 351–359.
24. De Franceschi, G., Frare, E., Bubacco, L., Mammi, S., Fontana, A., de Laureto, P.P., Molecular insights into the interaction between alpha-synuclein and docosahexaenoic acid. J. Mol. Biol. 394:1 (2009), 94–107.
25. De Franceschi, G., Fecchio, C., Sharon, R., Schapira, A.H.V., Proukakis, C., Bellotti, V., de Laureto, P.P., Alpha-Synuclein structural features inhibit harmful polyunsaturated fatty acid oxidation, suggesting roles in neuroprotection. J. Biol. Chem. 292:17 (2017), 6927–6937.
26. de Lau, L.M.L., Bornebroek, M., Witteman, J.C.M., Hofman, A., Koudstaal, P.J., Breteler, M.M.B., Dietary fatty acids and the risk of Parkinson disease: the Rotterdam study. Neurology 64 (2005), 2040–2045.
27. Dehay, B., Bourdenx, M., Gorry, P., Przedborski, S., Vila, M., Hunot, S., Singleton, A., Olanow, C.W., Merchant, K.M., Bezard, E., Petsko, G.A., Meissner, W.G., Targeting α-synuclein for treatment of Parkinson's disease: mechanistic and therapeutic considerations. Lancet Neurol. 14 (2015), 855–866.
28. 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.P., Ferraz, A.C., Evaluation of chronic omega-3 fatty acids supplementation on behavioral and neurochemical alterations in 6-hydroxydopamine-lesion model of Parkinson’ disease. Neurosci. Res. 66 (2010), 256–264.
29. Dickson, D.W., Braak, H., Duda, J.E., Duyckaerts, C., Gasser, T., Halliday, G.M., Hardy, J., Leverenz, J.B., Del Tredici, K., Wszolek, Z.K., Litvan, I., Neuropathological assessment of Parkinson's disease: refining the diagnostic criteria. Lancet Neurol. 8 (2009), 1150–1157.
30. Drouin-Ouellet, J., LeBel, M., Filali, M., Cicchetti, F., MyD88 deficiency results in both cognitive and motor impairments in mice. Brain Behav. Immun. 26 (2012), 880–885.
31. Drucker-Colín, R., García-Hernández, F., A new motor test sensitive to aging and dopaminergic function. J. Neurosci. Methods 39 (1991), 153–161.
32. Dyall, S.C., Long-chain omega-3 fatty acids and the brain: a review of the independent and shared effects of EPA, DPA and DHA. Front. Aging Neurosci., 7, 2015, 52.
33. Emanuele, M., Chieregatti, E., Mechanisms of alpha-synuclein action on neurotransmission: cell-autonomous and non-cell autonomous role. Biomol. Ther. 5 (2015), 865–892.
34. Fleming, S.M., Chesselet, M.-F., Behavioral phenotypes and pharmacology in genetic mouse models of Parkinsonism. Behav. Pharmacol. 17 (2006), 383–392.
35. Fleming, S.M., Salcedo, J., Fernagut, P.O., Rockenstein, E., Masliah, E., Levine, M.S., Chesselet, M.F., Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J. Neurosci. 24 (2004), 9434–9440.
36. Gibrat, C., Saint-Pierre, M., Bousquet, M., Levesque, D., Rouillard, C., Cicchetti, F., Differences between subacute and chronic MPTP mice models: investigation of dopaminergic neuronal degeneration and alpha-synuclein inclusions. J. Neurochem. 109 (2009), 1469–1482.
37. Glajch, K.E., Fleming, S.M., Surmeier, D.J., Osten, P., Sensorimotor assessment of the unilateral 6-hydroxydopamine mouse model of Parkinson's disease. Behav. Brain Res. 230 (2012), 309–316.
38. Hashimoto, M., Rockenstein, E., Masliah, E., Transgenic models of α-synuclein pathology. Ann. N. Y. Acad. Sci. 991 (2003), 171–188.
39. Jakowec, M., Petzinger, G.M., Sastry, S., Donaldson, D.M., McCormack, A., Langston, J.W., The native form of alpha-synuclein is not found in the cerebrospinal fluid of patients with Parkinson's disease or normal controls. Neurosci. Lett. 253 (1998), 13–16.
40. Kamel, F., Goldman, S.M., Umbach, D.M., Chen, H., Richardson, G., Barber, M.R. et al., Dietary fat intake, pesticide use, and Parkinson's disease. Parkinsonism Relat. Disord. 20:1 (2014), 82–87.
41. Lalancette-Hébert, M., Julien, C., Cordeau, P., Bohacek, I., Weng, Y.-C., Calon, F., Kriz, J., Accumulation of dietary docosahexaenoic acid in the brain attenuates acute immune response and development of postischemic neuronal damage. Stroke 42 (2011), 2903–2909.
42. Lam, H.A., Wu, N., Cely, I., Kelly, R.L., Hean, S., Richter, F., Magen, I., Cepeda, C., Ackerson, L.C., Walwyn, W., Masliah, E., Chesselet, M.-F., Levine, M.S., Maidment, N.T., Elevated tonic extracellular dopamine concentration and altered dopamine modulation of synaptic activity precede dopamine loss in the striatum of mice overexpressing human α-synuclein. J. Neurosci. Res. 89 (2011), 1091–1102.
43. Lee, V.M.Y., Trojanowski, J.Q., Mechanisms of Parkinson's disease linked to pathological alpha-synuclein: new targets for drug discovery. Neuron 52 (2006), 33–38.
44. Luchtman, D.W., Meng, Q., Song, C., Ethyl-eicosapentaenoate (E-EPA) attenuates motor impairments and inflammation in the MPTP-probenecid mouse model of Parkinson's disease. Behav. Brain Res. 226 (2012), 386–396.
45. Magen, I., Torres, E.R., Dinh, D., Chung, A., Masliah, E., Chesselet, M.F., Social cognition impairments in mice overexpressing alpha-synuclein under the Thy1 promoter, a model of pre-manifest Parkinson's disease. J. Parkinsons Dis. 5 (2015), 669–680.
46. Masliah, E., Dopaminergic loss and inclusion body formation in-synuclein mice: implications for neurodegenerative disorders. Science 287 (2000), 1265–1269.
47. Mori, M.A., Delattre, A.M., Carabelli, B., Pudell, C., Bortolanza, M., Staziaki, P.V., Visentainer, J.V., Montanher, P.F., Del Bel, E.A., Ferraz, A.C., Neuroprotective effect of omega-3 polyunsaturated fatty acids in the 6-OHDA model of Parkinson's disease is mediated by a reduction of inducible nitric oxide synthase. Nutr. Neurosci., 2017, 1–11.
48. Paxinos, G., Franklin, K.B.J., The Mouse Brain in Stereotaxic Coordinates. 2008, Academic Press, 242.
49. Plourde, M., Vohl, M.C., Vandal, M., Couture, P., Lemieux, S., Cunnane, S.C., Plasma n-3 fatty acid response to an n-3 fatty acid supplement is modulated by apoE epsilon4 but not by the common PPAR-alpha L162V polymorphism in men. Br. J. Nutr. 102 (2009), 1121–1124.
50. Richter, F., Gao, F., Medvedeva, V., Lee, P., Bove, N., Fleming, S.M., Michaud, M., Lemesre, V., Patassini, S., De La Rosa, K., Mulligan, C.K., Sioshansi, P.C., Zhu, C., Coppola, G., Bordet, T., Pruss, R.M., Chesselet, M.F., Chronic administration of cholesterol oximes in mice increases transcription of cytoprotective genes and improves transcriptome alterations induced by alpha-synuclein overexpression in nigrostriatal dopaminergic neurons. Neurobiol. Dis. 69 (2014), 263–275.
51. Rodriguez-Oroz, M.C., Jahanshahi, M., Krack, P., Litvan, I., Macias, R., Bezard, E., Obeso, J.A., Initial clinical manifestations of Parkinson's disease: features and pathophysiological mechanisms. Lancet Neurol. 8 (2009), 1128–1139.
52. Ross, O.A., Braithwaite, A.T., Skipper, L.M., Kachergus, J., Hulihan, M.M., Middleton, F.A., Nishioka, K., Fuchs, J., Gasser, T., Maraganore, D.M., Adler, C.H., Larvor, L., Chartier-Harlin, M.-C., Nilsson, C., Langston, J.W., Gwinn, K., Hattori, N., Farrer, M.J., Genomic investigation of alpha-synuclein multiplication and Parkinsonism. Ann. Neurol. 63 (2008), 743–750.
53. Ruiperez, V., Darios, F., Davletov, B., Alpha-synuclein, lipids and Parkinson's disease. Prog. Lipid Res. 49:4 (2010), 420–428.
54. Salem, N. Jr., Omega-3 fatty acids: molecular and biochemical aspects. Liss, A.R., (eds.) New Protective Roles for Selected Nutrients, 1989, Alan R Liss, New York, 109–228.
55. Sampson, T.R., Debelius, J.W., Thron, T., Janssen, S., Shastri, G.G., Ilhan, Z.E., Challis, C., Schretter, C.E., Rocha, S., Gradinaru, V., Chesselet, M.F., Keshavarzian, A., Shannon, K.M., Krajmalnik-Brown, R., Wittung-Stafshede, P., Knight, R., Mazmanian, S.K., Gut microbiota regulate motor deficits and neuroinflammation in a model of Parkinson's disease. Cell, 167(1469–1480), 2016, e1412.
56. Schulz-Schaeffer, W.J., The synaptic pathology of alpha-synuclein aggregation in dementia with Lewy bodies, Parkinson's disease and Parkinson's disease dementia. Acta Neuropathol. 120 (2010), 131–143.
57. Seidl, S.E., Santiago, J.A., Bilyk, H., Potashkin, J.A., The emerging role of nutrition in Parkinson's disease. Front. Aging Neurosci., 6, 2014, 36.
58. Sharon, R., Bar-Joseph, I., Frosch, M.P., Walsh, D.M., Hamilton, J.A., Selkoe, D.J., The formation of highly soluble oligomers of alpha-synulcein is regulated by fatty acids and enhanced in Parkinson's disease. Neuron 37 (2003), 583–595.
59. Sharon, R., Bar-Joseph, I., Mirick, G.E., Serhan, C.N., Selkoe, D.J., Altered fatty acid composition of dopaminergic neurons expressing alpha-synuclein and human brains with alpha-synucleinopathies. J. Biol. Chem. 278 (2003), 49874–49881.
60. Singleton, A., Gwinn-Hardy, K., Sharabi, Y., Li, S.T., Holmes, C., Dendi, R., Hardy, J., Singleton, A., Crawley, A., Goldstein, D.S., Association between cardiac denervation and Parkinsonism caused by alpha-synuclein gene triplication. Brain 127 (2004), 768–772.
61. Spillantini, M.G., Goedert, M., Synucleinopathies: past, present and future. Neuropathol. Appl. Neurobiol. 42 (2016), 3–5.
62. Trepanier, M.O., Hopperton, K.E., Orr, S.K., Bazinet, R.P., N-3 polyunsaturated fatty acids in animal models with neuroinflammation: an update. Eur. J. Pharmacol. 785 (2016), 187–206.
63. Vaikath, N.N., Majbour, N.K., Paleologou, K.E., Ardah, M.T., van Dam, E., van de Berg, W.D., Forrest, S.L., Parkkinen, L., Gai, W.P., Hattori, N., Takanashi, M., Lee, S.J., Mann, D.M., Imai, Y., Halliday, G.M., Li, J.Y., El-Agnaf, O.M., Generation and characterization of novel conformation-specific monoclonal antibodies for alpha-synuclein pathology. Neurobiol. Dis. 79 (2015), 81–99.
64. Volpicelli-Daley, L.A., Luk, K.C., Patel, T.P., Tanik, S.A., Riddle, D.M., Stieber, A., Meaney, D.F., Trojanowski, J.Q., Lee, V.M., Exogenous alpha-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 72 (2011), 57–71.
65. Watson, J.B., Hatami, A., David, H., Masliah, E., Roberts, K., Evans, C.E., Levine, M.S., Alterations in corticostriatal synaptic plasticity in mice overexpressing human alpha-synuclein. Neuroscience 159 (2009), 501–513.
66. Wu, N., Joshi, P.R., Cepeda, C., Masliah, E., Levine, M.S., Alpha-synuclein overexpression in mice alters synaptic communication in the corticostriatal pathway. J. Neurosci. Res. 88 (2010), 1764–1776.
67. Yakunin, E., Loeb, V., Kisos, H., Biala, Y., Yehuda, S., Yaari, Y., Selkoe, D.J., Sharon, R., Alpha-synuclein neuropathology is controlled by nuclear hormone receptors and enhanced by docosahexaenoic acid in a mouse model for Parkinson's disease. Brain Pathol. 22 (2012), 280–294.