Partial neurorescue effects of DHA following a 6-OHDA lesion of the mouse dopaminergic system

Journal of Nutritional Biochemistry

Volumn 30, Issue , 2016, Pages 133-142

  Coulombe, Katherine ^a,b   Saint Pierre, Martine ^b   Cisbani, Giulia ^a,b   St Amour, Isabelle ^a,b   Gibrat, Claire ^a,b   Giguère Rancourt, Ariane ^a,b   Calon, Frédéric ^a,b   Cicchetti, Francesca ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b Université Laval   (Canada)

Author keywords

6 Hydroxydopamine; Docosahexaenoic acid; Dopamine; Neurorescue; Neurorestoration; Parkinson's disease

Indexed keywords

CENTRAL NERVOUS SYSTEM AGENTS; DOCOSAHEXAENOIC ACID; DOPAMINE; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL BODY; CELL LOSS; CONTROLLED STUDY; CORPUS STRIATUM; DENERVATION; DOPAMINERGIC SYSTEM; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID DIET; LOCOMOTION; MALE; MOUSE; NERVE CELL DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; SUBSTANTIA NIGRA PARS COMPACTA; ANIMAL; C57BL MOUSE; MOTOR ACTIVITY;

ANIMALS; DOCOSAHEXAENOIC ACIDS; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; OXIDOPAMINE;

EID: 84962071218     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2015.11.014     Document Type: Article

References (56)

1. de Lau L.M.L., Breteler M.M.B. Epidemiology of Parkinson's disease. Lancet Neurol 2006, 5:525-535. 10.1016/S1474-4422(06)70471-9.
2. 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. 10.1096/fj.07-9677com.
3. Bousquet M., Calon F., Cicchetti F. Impact of omega-3 fatty acids in Parkinson's disease. Ageing Res Rev 2011, 10:453-463. 10.1016/j.arr.2011.03.001.
4. Bousquet M., Gue K., Emond V., Julien P., Kang J.X., Cicchetti F., et al. 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. 10.1194/jlr.M011692.
5. Olanow C.W., Schapira A.H.V. Therapeutic prospects for Parkinson disease. Ann Neurol 2013, 74:337-347. 10.1002/ana.24011.
6. Meissner W.G., Frasier M., Gasser T., Goetz C.G., Lozano A., Piccini P., et al. Priorities in Parkinson's disease research. Nat Rev Drug Discov 2011, 10:377-393. 10.1038/nrd3430.
7. Julien C., Berthiaume L., Hadj-Tahar A., Rajput A.H., Bédard P.J., Paolo T.D., et al. Postmortem brain fatty acid profile of levodopa-treated Parkinson disease patients and parkinsonian monkeys. Neurochem Int 2006, 48:404-414. 10.1016/j.neuint.2005.12.002.
8. Salem N., Litman B., Kim H.Y., Gawrisch K. Mechanisms of action of docosahexaenoic acid in the nervous system. Lipids 2001, 36:945-959. 10.1007/s11745-001-0805-6.
9. Calon F., Lim G.P., Yang F., Morihara T., Teter B., Ubeda O., et al. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 2004, 43:633-645. 10.1016/j.neuron.2004.08.013.
10. Bazan N.G. The docosanoid neuroprotectin D1 induces homeostatic regulation of neuroinflammation and cell survival. Prostaglandins Leukot Essent Fat Acids 2013, 88:127-129. 10.1016/j.plefa.2012.08.008.
11. Paterniti I., Impellizzeri D., Di Paola R., Esposito E., Gladman S., Yip P., et al. Docosahexaenoic acid attenuates the early inflammatory response following spinal cord injury in mice: in-vivo and in-vitro studies. J Neuroinflammation 2014, 11:6. 10.1186/1742-2094-11-6.
12. Lalancette-Hébert M., Julien C., Cordeau P., Bohacek I., Weng Y.-C., Calon F., et al. Accumulation of dietary docosahexaenoic acid in the brain attenuates acute immune response and development of postischemic neuronal damage. Stroke 2011, 42:2903-2909. 10.1161/STROKEAHA.111.620856.
13. Akbar M., Calderon F., Wen Z., Kim H.-Y. Docosahexaenoic acid: a positive modulator of Akt signaling in neuronal survival. Proc Natl Acad Sci U S A 2005, 102:10858-10863. 10.1073/pnas.0502903102.
14. Arsenault D., Julien C., Tremblay C., Calon F. DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice. PLoS ONE 2011, 6:e17397. 10.1371/journal.pone.0017397.
15. Ahmad A., Murthy M., Moriguchi T., Salem N., Greiner R.S. A decrease in cell size accompanies a loss of docosahexaenoate in the rat hippocampus. Nutr Neurosci 2002, 5:103-113. 10.1080/10284150290018973.
16. 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. 10.1016/j.pnpbp.2009.07.018.
17. Cardoso H.D., Santos Junior dos E.F., de Santana D.F., Gonçalves-Pimentel C., Angelim M.K., Isaac A.R., et al. Omega-3 deficiency and neurodegeneration in the substantia nigra: involvement of increased nitric oxide production and reduced BDNF expression, Biochim Biophys Acta. 2010, 1840:1-11. 10.1016/j.bbagen.2013.12.023.
18. Cisbani G., Drouin-Ouellet J., Gibrat C., Saint-Pierre M., Lagacé M., Badrinarayanan S., et al. Cystamine/cysteamine rescues the dopaminergic system and shows neurorestorative properties in an animal model of Parkinson's disease. Neurobiol Dis 2015, 82:430-444. 10.1016/j.nbd.2015.07.012.
19. Paxinos G., Franklin K.B.J. The mouse brain in stereotaxic coordinates 2008, Academic Press.
20. 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 2012, 230:309-316. 10.1016/j.bbr.2011.12.007.
21. Calon F., Lavertu N., Lemieux A.M., Morissette M., Goulet M., Grondin R., et al. Effect of MPTP-induced denervation on basal ganglia GABA(B) receptors: correlation with dopamine concentrations and dopamine transporter. Synapse 2001, 40:225-234. 10.1002/syn.1045.
22. Drouin-Ouellet J., Gibrat C., Bousquet M., Calon F., Kriz J., Cicchetti F. The role of the MYD88-dependent pathway in MPTP-induced brain dopaminergic degeneration. J Neuroinflammation 2011, 8:137. 10.1186/1742-2094-8-137.
23. Gibrat C., Saint-Pierre M., Bousquet M., Lévesque D., Rouillard C., Cicchetti F. Differences between subacute and chronic MPTP mice models: investigation of dopaminergic neuronal degeneration and α-synuclein inclusions. J Neurochem 2009, 109:1469-1482. 10.1111/j.1471-4159.2009.06072.x.
24. Arsenault D., Julien C., Calon F. Chronic dietary intake of α-linolenic acid does not replicate the effects of DHA on passive properties of entorhinal cortex neurons. Br J Nutr 2011, 107:1099-1111. 10.1017/S0007114511004089.
25. Chalon S. Omega-3 fatty acids and monoamine neurotransmission. Prostaglandins Leukot Essent Fat Acids 2006, 75:259-269. 10.1016/j.plefa.2006.07.005.
26. Shin S.S., Dixon C.E. Oral fish oil restores striatal dopamine release after traumatic brain injury. Neurosci Lett 2011, 496:168-171. 10.1016/j.neulet.2011.04.009.
27. Delattre A.M., Kiss Ã.G., Szawka R.E., Anselmo-Franci J.A., Bagatini P.B., Leal Xavier der L.Ã., et al. Evaluation of chronic omega-3 fatty acids supplementation on behavioral and neurochemical alterations in 6-hydroxydopamine-lesion model of Parkinson's disease. Neurosci Res 2010, 66:256-264. 10.1016/j.neures.2009.11.006.
28. Bezard E., Przedborski S. A tale on animal models of Parkinson's disease. Mov Disord 2011, 26:993-1002. 10.1002/mds.23696.
29. Bezard E. A call for clinically driven experimental design in assessing neuroprotection in experimental Parkinsonism. Behav Pharmacol 2006, 17:379-382. [PMID 16940758].
30. 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 2005, 64:2040-2045. 10.1212/01.WNL.0000166038.67153.9F.
31. Bezard E., Yue Z., Kirik D., Spillantini M.G. Animal models of Parkinson's disease: limits and relevance to neuroprotection studies. Mov Disord 2012, 28:61-70. 10.1002/mds.25108.
32. Mitsumoto Y., Watanabe A., Mori A., Koga N. Spontaneous regeneration of nigrostriatal dopaminergic neurons in MPTP-treated C57BL/6 mice. Biochem Biophys Res Commun 1998, 248:660-663. 10.1006/bbrc.1998.8986.
33. L'Episcopo F., Tirolo C., Testa N., Caniglia S., Morale M.C., Deleidi M., et al. Plasticity of subventricular zone neuroprogenitors in MPTP (1-Methyl-4-Phenyl-1,2,3,6-Tetrahydropyridine) mouse model of Parkinson's disease involves cross talk between inflammatory and Wnt/-Catenin signaling pathways: functional consequences for neuroprotection and repair. J Neurosci 2012, 32:2062-2085. 10.1523/JNEUROSCI.5259-11.2012.
34. Date I., Felten D.L., Felten S.Y. Long-term effect of MPTP in the mouse brain in relation to aging: neurochemical and immunocytochemical analysis. Brain Res 1990, 519:266-276. 10.1016/0006-8993(90)90088-S.
35. Schneider J.S., Rothblat D.S. Neurochemical evaluation of the striatum in symptomatic and recovered MPTP-treated cats. Neuroscience 1991, 44:421-429. 10.1016/0306-4522(91)90066-W.
36. Jackson-Lewis V., Blesa J., Przedborski S. Animal models of Parkinson's disease. Parkinsonism Relat Disord 2012, 18(Suppl. 1):S183-S185. 10.1016/S1353-8020(11)70057-8.
37. Mandel S., Grünblatt E., Riederer P., Gerlach M., Levites Y., Youdim M.B.H. Neuroprotective strategies in Parkinson's disease. CNS Drugs 2003, 17:729-762. 10.2165/00023210-200317100-00004.
38. Airavaara M., Voutilainen M.H., Wang Y., Hoffer B. Neurorestoration. Parkinsonism Relat Disord 2012, 18:S143-S146. 10.1016/S1353-8020(11)70045-1.
39. Bezard E., Gross C.E., Brotchie J.M. Presymptomatic compensation in Parkinson's disease is not dopamine-mediated. Trends Neurosci 2003, 26:215-221. 10.1016/S0166-2236(03)00038-9.
40. Elsworth J.D., Deutch A.Y., Redmond D.E., Sladek J.R., Roth R.H. MPTP-induced parkinsonism: relative changes in dopamine concentration in subregions of substantia nigra, ventral tegmental area and retrorubral field of symptomatic and asymptomatic vervet monkeys. Brain Res 1990, 513:320-324. 10.1016/0006-8993(90)90474-P.
41. Bezard E., Dovero S., Prunier C., Ravenscroft P., Chalon S., Guilloteau D., et al. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J Neurosci 2001, 21:6853-6861. [PMID 11517273].
42. Stoessl A.J. Neuroimaging in Parkinson's disease. Neurotherapeutics 2011, 8:72-81. 10.1007/s13311-010-0007-z.
43. Berti V., Pupi A., Mosconi L. PET/CT in diagnosis of movement disorders. Ann N Y Acad Sci 2011, 1228:93-108. 10.1111/j.1749-6632.2011.06025.x.
44. Schroeder J.A., Schneider J.S. GABA-opioid interactions in the globus pallidus: [D-Ala2]-Met-enkephalinamide attenuates potassium-evoked GABA release after nigrostriatal lesion. J Neurochem 2002, 82:666-673. 10.1046/j.1471-4159.2002.01010.x.
45. Rothblat D.S., Schneider J.S. Spontaneous functional recovery from parkinsonism is not due to reinnervation of the dorsal striatum by residual dopaminergic neurons. Brain Res Bull 1994, 34:309-312. 10.1016/0361-9230(94)90068-x.
46. Calon F., Rajput A.H., Hornykiewicz O., Bédard P.J., Di Paolo T. Levodopa-induced motor complications are associated with alterations of glutamate receptors in Parkinson's disease. Neurobiol Dis 2003, 14:404-416. 10.1016/j.nbd.2003.07.003.
47. Day M., Wang Z., Ding J., An X., Ingham C.A., Shering A.F., et al. Selective elimination of glutamatergic synapses on striatopallidal neurons in Parkinson disease models. Nat Neurosci 2006, 9:251-259. 10.1038/nn1632.
48. Brotchie J., Fitzer-Attas C. Mechanisms compensating for dopamine loss in early Parkinson disease. Neurology 2009, 72:S32-S38. 10.1212/WNL.0b013e318198e0e9.
49. Anglade P., Mouatt-Prigent A., Agid Y., Hirsch E. Synaptic plasticity in the caudate nucleus of patients with Parkinson's disease. Neurodegeneration 1996, 5:121-128. 10.1006/neur.1996.0018.
50. Passos P.P., Borba J.M.C., Rocha-de-Melo A.P., Guedes R.C.A., da Silva R.P., Filho W.T.M., et al. Dopaminergic cell populations of the rat substantia nigra are differentially affected by essential fatty acid dietary restriction over two generations. J Chem Neuroanat 2012, 44:66-75. 10.1016/j.jchemneu.2012.05.003.
51. Joffre C., Nadjar A., Lebbadi M., Calon F., Laye S. n-3 LCPUFA improves cognition_ the young, the old and the sick. Prostaglandins Leukot Essent Fat Acids 2014, 91:1-20. 10.1016/j.plefa.2014.05.001.
52. Darios F., Davletov B. Omega-3 and omega-6 fatty acids stimulate cell membrane expansion by acting on syntaxin 3. Nature 2006, 440:813-817. 10.1038/nature04598.
53. Robson L.G., Dyall S., Sidloff D., Michael-Titus A.T. Omega-3 polyunsaturated fatty acids increase the neurite outgrowth of rat sensory neurones throughout development and in aged animals. Neurobiol Aging 2010, 31:678-687. 10.1016/j.neurobiolaging.2008.05.027.
54. Ho A., Blum M. Induction of interleukin-1 associated with compensatory dopaminergic sprouting in the denervated striatum of young mice: model of aging and neurodegenerative disease. J Neurosci 1998, 18:5614-5629. [PMID 9671653].
55. Sauer H., Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience 1994, 59:401-415. 10.1016/0306-4522(94)90605-X.
56. Politis M. Neuroimaging in Parkinson disease: from research setting to clinical practice. Nat Publ Group 2014, 10:708-722. 10.1038/nrneurol.2014.205.