Enriched endogenous n-3 polyunsaturated fatty acids alleviate cognitive and behavioral deficits in a mice model of Alzheimer's disease

Neuroscience

Volumn 333, Issue , 2016, Pages 345-355

  Wu, Kefeng ^a   Gao, Xiang ^a   Shi, Baoyan ^a,b   Chen, Shiyu ^a,b   Zhou, Xin ^a   Li, Zhidong ^a   Gan, Yuhong ^a   Cui, Liao ^a   Kang, Jing xuan ^c   Li, Wende ^a,b   Huang, Ren ^b  

^a GUANGDONG MEDICAL UNIVERSITY   (China)

^b Guangdong Laboratory Animal Monitoring Institute   (China)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Alzheimer's disease; amyloid precursor protein; polyunsaturated fatty acids

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; ACYL COENZYME A DESATURASE; APP PROTEIN, HUMAN; CAENORHABDITIS ELEGANS PROTEIN; FAT-1 PROTEIN, C ELEGANS;

ALZHEIMER DISEASE; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; CELL ACTIVATION; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE SEVERITY; ELEVATED PLUS MAZE TEST; FAT 1 GENE; FATTY ACID ANALYSIS; GENE; GENE EXPRESSION; GENETIC ANALYSIS; HISTOPATHOLOGY; MACROGLIA; MORRIS WATER MAZE TEST; MOUSE; NERVE CELL NECROSIS; NEUROPROTECTION; NONHUMAN; OPEN FIELD TEST; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DETERMINATION; SPATIAL LEARNING; SPATIAL MEMORY; ANIMAL; ASTROCYTE; BRAIN; C57BL MOUSE; CAENORHABDITIS ELEGANS; COGNITION; DIET; DISEASE MODEL; GENETICS; HUMAN; MAZE TEST; METABOLISM; MOTOR ACTIVITY; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; TIME FACTOR; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ASTROCYTES; BRAIN; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; COGNITION; COGNITION DISORDERS; DIET; DISEASE MODELS, ANIMAL; FATTY ACID DESATURASES; FATTY ACIDS, OMEGA-6; HUMANS; MAZE LEARNING; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; NEURONS; NF-KAPPA B; TIME FACTORS;

EID: 84980479812     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2016.07.038     Document Type: Article

References (67)

1. Alzheimer's, A., Alzheimer's disease facts and figures. Alzheimers Dement 9 (2013), 208–245.
2. Amihaesei, I.C., Cojocarut, E., Mungiu, O.C., Alzheimer–certitudes and hypotheses. Rev Med Chir Soc Med Nat Iasi 117 (2013), 119–126.
3. Balk, E.M., Horsley, T.A., Newberry, S.J., Lichtenstein, A.H., Yetley, E.A., Schachter, H.M., Moher, D., MacLean, C.H., Lau, J., A collaborative effort to apply the evidence-based review process to the field of nutrition: challenges, benefits, and lessons learned. Am J Clin Nutr 85 (2007), 1448–1456.
4. Bourasset, F., Ouellet, M., Tremblay, C., Julien, C., Do, T.M., Oddo, S., LaFerla, F., Calon, F., Reduction of the cerebrovascular volume in a transgenic mouse model of Alzheimer's disease. Neuropharmacology 56 (2009), 808–813.
5. Bourre, J.M., Dumont, O., Piciotti, M., Clement, M., Chaudiere, J., Bonneil, M., Nalbone, G., Lafont, H., Pascal, G., Durand, G., Essentiality of omega 3 fatty acids for brain structure and function. World Rev Nutr Diet 66 (1991), 103–117.
6. Brendel, M., Pogarell, O., Xiong, G., Delker, A., Bartenstein, P., Rominger, A., Alzheimer's Disease Neuroimaging I. Depressive symptoms accelerate cognitive decline in amyloid-positive MCI patients. Eur J Nucl Med Mol Imaging 42 (2015), 716–724.
7. Calon, F., Omega-3 polyunsaturated fatty acids in Alzheimer's disease: key questions and partial answers. Curr Alzheimer Res 8 (2011), 470–478.
8. Cederholm, T., Salem, N. Jr., Palmblad, J., Omega-3 fatty acids in the prevention of cognitive decline in humans. Adv Nutr 4 (2013), 672–676.
9. 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 32 (2008), 1538–1544.
10. Conklin, S.M., Gianaros, P.J., Brown, S.M., Yao, J.K., Hariri, A.R., Manuck, S.B., Muldoon, M.F., Long-chain omega-3 fatty acid intake is associated positively with corticolimbic gray matter volume in healthy adults. Neurosci Lett 421 (2007), 209–212.
11. Cunnane, S.C., Chouinard-Watkins, R., Castellano, C.A., Barberger-Gateau, P., Docosahexaenoic acid homeostasis, brain aging and Alzheimer's disease: can we reconcile the evidence?. Prostaglandins Leukot Essent Fatty Acids 88 (2013), 61–70.
12. Dacks, P.A., Shineman, D.W., Fillit, H.M., Current evidence for the clinical use of long-chain polyunsaturated n-3 fatty acids to prevent age-related cognitive decline and Alzheimer's disease. J Nutr Health Aging 17 (2013), 240–251.
13. Das, U.N., Puskas, L.G., Transgenic fat-1 mouse as a model to study the pathophysiology of cardiovascular, neurological and psychiatric disorders. Lipids Health Dis, 8, 2009, 61.
14. De-Paula, V.J., Radanovic, M., Diniz, B.S., Forlenza, O.V., Alzheimer's disease. Subcell Biochem 65 (2012), 329–352.
15. De Lorgeril, M., Salen, P., New insights into the health effects of dietary saturated and omega-6 and omega-3 polyunsaturated fatty acids. BMC Med, 10, 2012, 50.
16. Dong-mei W, Wan-bo L, Shu-min Y, Xiong-zhi Q, Hai-tao Z, Chun-mei M, Xing-shui C, Lian-feng Z (2011) Establishment of APP695 transgenic mouse model and analysis of the development of pathological phenotypes. Chin J Comp Med 5–9+25+94.
17. Donovan, N.J., Amariglio, R.E., Zoller, A.S., Rudel, R.K., Gomez-Isla, T., Blacker, D., Hyman, B.T., Locascio, J.J., Johnson, K.A., Sperling, R.A., Marshall, G.A., Rentz, D.M., Subjective cognitive concerns and neuropsychiatric predictors of progression to the early clinical stages of Alzheimer disease. Am J Geriatr Psychiatry 22 (2014), 1642–1651.
18. Donovan, N.J., Hsu, D.C., Dagley, A.S., Schultz, A.P., Amariglio, R.E., Mormino, E.C., Okereke, O.I., Rentz, D.M., Johnson, K.A., Sperling, R.A., Marshall, G.A., Depressive symptoms and biomarkers of Alzheimer's disease in cognitively normal older adults. J Alzheimers Dis, 2015.
19. Eikelenboom, P., Bate, C., Van Gool, W.A., Hoozemans, J.J., Rozemuller, J.M., Veerhuis, R., Williams, A., Neuroinflammation in Alzheimer's disease and prion disease. Glia 40 (2002), 232–239.
20. 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 5 (2009), 140–152.
21. 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 63 (2006), 1402–1408.
22. Gladman, S.J., Huang, W., Lim, S.N., Dyall, S.C., Boddy, S., Kang, J.X., Knight, M.M., Priestley, J.V., Michael-Titus, A.T., Improved outcome after peripheral nerve injury in mice with increased levels of endogenous omega-3 polyunsaturated fatty acids. J Neurosci 32 (2012), 563–571.
23. Godoy, J.A., Rios, J.A., Zolezzi, J.M., Braidy, N., Inestrosa, N.C., Signaling pathway cross talk in Alzheimer's disease. Cell Commun Signal, 12, 2014, 23.
24. Grimm, M.O., Haupenthal, V.J., Mett, J., Stahlmann, C.P., Blumel, T., Mylonas, N.T., Endres, K., Grimm, H.S., Hartmann, T., Oxidized docosahexaenoic acid species and lipid peroxidation products increase amyloidogenic amyloid precursor protein processing. Neurodegener Dis 16 (2016), 44–54.
25. Halle, A., Hornung, V., Petzold, G.C., Stewart, C.R., Monks, B.G., Reinheckel, T., Fitzgerald, K.A., Latz, E., Moore, K.J., Golenbock, D.T., The NALP3 inflammasome is involved in the innate immune response to amyloid-beta. Nat Immunol 9 (2008), 857–865.
26. Hashimoto, M., Shahdat, H.M., Yamashita, S., Katakura, M., Tanabe, Y., Fujiwara, H., Gamoh, S., Miyazawa, T., Arai, H., Shimada, T., Shido, O., Docosahexaenoic acid disrupts in vitro amyloid beta(1–40) fibrillation and concomitantly inhibits amyloid levels in cerebral cortex of Alzheimer's disease model rats. J Neurochem 107 (2008), 1634–1646.
27. He, C., Qu, X., Cui, L., Wang, J., Kang, J.X., Improved spatial learning performance of fat-1 mice is associated with enhanced neurogenesis and neuritogenesis by docosahexaenoic acid. Proc Natl Acad Sci U S A 106 (2009), 11370–11375.
28. Hossain, S., Hashimoto, M., Katakura, M., Miwa, K., Shimada, T., Shido, O., Mechanism of docosahexaenoic acid-induced inhibition of in vitro Abeta1-42 fibrillation and Abeta1-42-induced toxicity in SH-S5Y5 cells. J Neurochem 111 (2009), 568–579.
29. Igarashi, M., DeMar, J.C. Jr., Ma, K., Chang, L., Bell, J.M., Rapoport, S.I., Docosahexaenoic acid synthesis from alpha-linolenic acid by rat brain is unaffected by dietary n-3 PUFA deprivation. J Lipid Res 48 (2007), 1150–1158.
30. Jack, C.R. Jr., Holtzman, D.M., Biomarker modeling of Alzheimer's disease. Neuron 80 (2013), 1347–1358.
31. Jicha, G.A., Markesbery, W.R., Omega-3 fatty acids: potential role in the management of early Alzheimer's disease. Clin Interv Aging 5 (2010), 45–61.
32. Kaltschmidt, B., Uherek, M., Volk, B., Baeuerle, P.A., Kaltschmidt, C., Transcription factor NF-kappaB is activated in primary neurons by amyloid beta peptides and in neurons surrounding early plaques from patients with Alzheimer disease. Proc Natl Acad Sci U S A 94 (1997), 2642–2647.
33. Kang, J.X., Wang, J., Wu, L., Kang, Z.B., Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature, 427, 2004, 504.
34. Koivisto, H., Grimm, M.O., Rothhaar, T.L., Berkecz, R., Lutjohann, D.D., Giniatullina, R., Takalo, M., Miettinen, P.O., Lahtinen, H.M., Giniatullin, R., Penke, B., Janaky, T., Broersen, L.M., Hartmann, T., Tanila, H., Special lipid-based diets alleviate cognitive deficits in the APPswe/PS1dE9 transgenic mouse model of Alzheimer's disease independent of brain amyloid deposition. J Nutr Biochem 25 (2014), 157–169.
35. Labrousse, V.F., Nadjar, A., Joffre, C., Costes, L., Aubert, A., Gregoire, S., Bretillon, L., Laye, S., Short-term long chain omega3 diet protects from neuroinflammatory processes and memory impairment in aged mice. PLoS One, 7, 2012, e36861.
36. Laursen, B., Mork, A., Plath, N., Kristiansen, U., Bastlund, J.F., Cholinergic degeneration is associated with increased plaque deposition and cognitive impairment in APPswe/PS1dE9 mice. Behav Brain Res 240 (2013), 146–152.
37. Lebbadi, M., Julien, C., Phivilay, A., Tremblay, C., Emond, V., Kang, J.X., Calon, F., Endogenous conversion of omega-6 into omega-3 fatty acids improves neuropathology in an animal model of Alzheimer's disease. J Alzheimers Dis 27 (2011), 853–869.
38. Li, L., Wu, W., Huang, W., Hu, G., Yuan, W., Li, W., NF-kappaB RNAi decreases the Bax/Bcl-2 ratio and inhibits TNF-alpha-induced apoptosis in human alveolar epithelial cells. Inflamm Res 62 (2013), 387–397.
39. Liang, J., Luan, Y., Lu, B., Zhang, H., Luo, Y.N., Ge, P., Protection of ischemic postconditioning against neuronal apoptosis induced by transient focal ischemia is associated with attenuation of NF-kappaB/p65 activation. PLoS One, 9, 2014, e96734.
40. Loef, M., Walach, H., The omega-6/omega-3 ratio and dementia or cognitive decline: a systematic review on human studies and biological evidence. J Nutr Gerontol Geriatr 32 (2013), 1–23.
41. Luo, C., Ren, H., Wan, J.B., Yao, X., Zhang, X., He, C., So, K.F., Kang, J.X., Pei, Z., Su, H., Enriched endogenous omega-3 fatty acids in mice protect against global ischemia injury. J Lipid Res 55 (2014), 1288–1297.
42. Marshall, G.A., Donovan, N.J., Lorius, N., Gidicsin, C.M., Maye, J., Pepin, L.C., Becker, J.A., Amariglio, R.E., Rentz, D.M., Sperling, R.A., Johnson, K.A., Apathy is associated with increased amyloid burden in mild cognitive impairment. J Neuropsychiatry Clin Neurosci 25 (2013), 302–307.
43. Masood, A., Stark, K.D., Salem, N. Jr., A simplified and efficient method for the analysis of fatty acid methyl esters suitable for large clinical studies. J Lipid Res 46 (2005), 2299–2305.
44. Mohajeri, M.H., Troesch, B., Weber, P., Inadequate supply of vitamins and DHA in the elderly: implications for brain aging and Alzheimer-type dementia. Nutrition 31 (2015), 261–275.
45. Morales, I., Farias, G., Maccioni, R.B., Neuroimmunomodulation in the pathogenesis of Alzheimer's disease. NeuroImmunoModulation 17 (2010), 202–204.
46. Naslund, J., Haroutunian, V., Mohs, R., Davis, K.L., Davies, P., Greengard, P., Buxbaum, J.D., Correlation between elevated levels of amyloid beta-peptide in the brain and cognitive decline. JAMA 283 (2000), 1571–1577.
47. Nicolas, M., Hassan, B.A., Amyloid precursor protein and neural development. Development 141 (2014), 2543–2548.
48. Oddo, S., Caccamo, A., Kitazawa, M., Tseng, B.P., LaFerla, F.M., Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 24 (2003), 1063–1070.
49. Oster, T., Pillot, T., Docosahexaenoic acid and synaptic protection in Alzheimer's disease mice. Biochim Biophys Acta 1801 (2010), 791–798.
50. 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 55 (2009), 476–482.
51. Palacios-Pelaez, R., Lukiw, W.J., Bazan, N.G., Omega-3 essential fatty acids modulate initiation and progression of neurodegenerative disease. Mol Neurobiol 41 (2010), 367–374.
52. Pietrzak, R.H., Lim, Y.Y., Neumeister, A., Ames, D., Ellis, K.A., Harrington, K., Lautenschlager, N.T., Restrepo, C., Martins, R.N., Masters, C.L., Villemagne, V.L., Rowe, C.C., Maruff, P., Australian Imaging B, Lifestyle Research G. Amyloid-beta, anxiety, and cognitive decline in preclinical Alzheimer disease: a multicenter, prospective cohort study. JAMA Psychiatry 72 (2015), 284–291.
53. Pimplikar, S.W., Nixon, R.A., Robakis, N.K., Shen, J., Tsai, L.H., Amyloid-independent mechanisms in Alzheimer's disease pathogenesis. J Neurosci 30 (2010), 14946–14954.
54. Prior, P.L., Galduroz, J.C., (N-3) Fatty acids: molecular role and clinical uses in psychiatric disorders. Adv Nutr 3 (2012), 257–265.
55. 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. Jr., Weiner, M., Shinto, L., Aisen, P.S., Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial. JAMA 304 (2010), 1903–1911.
56. Rapoport, S.I., Chang, M.C., Spector, A.A., Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J Lipid Res 42 (2001), 678–685.
57. Reitz, C., Mayeux, R., Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol 88 (2014), 640–651.
58. Simopoulos, A.P., Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed Pharmacother 60 (2006), 502–507.
59. Small, B.J., Gagnon, E., Robinson, B., Early identification of cognitive deficits: preclinical Alzheimer's disease and mild cognitive impairment. Geriatrics 62 (2007), 19–23.
60. Swanson, D., Block, R., Mousa, S.A., Omega-3 fatty acids EPA and DHA: health benefits throughout life. Adv Nutr 3 (2012), 1–7.
61. Wang, S., Yang, H., Yu, L., Jin, J., Qian, L., Zhao, H., Xu, Y., Zhu, X., Oridonin attenuates Abeta1-42-induced neuroinflammation and inhibits NF-kappaB pathway. PLoS One, 9, 2014, e104745.
62. White, J.A., Manelli, A.M., Holmberg, K.H., Van Eldik, L.J., Ladu, M.J., Differential effects of oligomeric and fibrillar amyloid-beta 1–42 on astrocyte-mediated inflammation. Neurobiol Dis 18 (2005), 459–465.
63. Xuan, A.G., Pan, X.B., Wei, P., Ji, W.D., Zhang, W.J., Liu, J.H., Hong, L.P., Chen, W.L., Long, D.H., Valproic acid alleviates memory deficits and attenuates amyloid-beta deposition in transgenic mouse model of Alzheimer's disease. Mol Neurobiol 51 (2015), 300–312.
64. Yaffe, K., Treatment of Alzheimer disease and prognosis of dementia: time to translate research to results. JAMA 304 (2010), 1952–1953.
65. Zhang, J., Wu, X., Qin, C., Qi, J., Ma, S., Zhang, H., Kong, Q., Chen, D., Ba, D., He, W., A novel recombinant adeno-associated virus vaccine reduces behavioral impairment and beta-amyloid plaques in a mouse model of Alzheimer's disease. Neurobiol Dis 14 (2003), 365–379.
66. Zhao, Y., Calon, F., Julien, C., Winkler, J.W., Petasis, N.A., Lukiw, W.J., Bazan, N.G., Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARgamma-mediated mechanisms in Alzheimer's disease models. PLoS One, 6, 2011, e15816.
67. Zhu, X., Wang, S., Yu, L., Yang, H., Tan, R., Yin, K., Jin, J., Zhao, H., Guan, D., Xu, Y., TL-2 attenuates beta-amyloid induced neuronal apoptosis through the AKT/GSK-3beta/beta-catenin pathway. Int J Neuropsychopharmacol 17 (2014), 1511–1519.