Membrane lipid modifications and therapeutic effects mediated by hydroxydocosahexaenoic acid on Alzheimer's disease

Biochimica et Biophysica Acta - Biomembranes

Volumn 1838, Issue 6, 2014, Pages 1680-1692

  Torres, Manuel ^a   Price, Samantha L ^b   Fiol Deroque, Maria A ^a   Marcilla Etxenike, Amaia ^a   Ahyayauch, Hasna ^c   Barceló Coblijn, Gwendolyn ^a   Terés, Silvia ^a   Katsouri, Loukia ^b   Ordinas, Margarita ^a   López, David J ^a   Ibarguren, Maitane ^a   Goñi, Félix M ^c   Busquets, Xavier ^a   Vitorica, Javier ^d   Sastre, Magdalena ^b   Escribá, Pablo V ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

^d HOSPITAL UNIVERSITARIO VIRGEN DEL ROCÍO   (Spain)

Author keywords

Alzheimer's disease; Amyloid ; DHA; Lipid; Lipid rafts; Membrane; Tau phosphorylation

Indexed keywords

ALZHEIMER'S DISEASE; AMYLOID-Β; DHA; LIPID; LIPID RAFTS; MEMBRANE; TAU PHOSPHORYLATION;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BRAIN; CHOLESTEROL; DISEASE MODELS, ANIMAL; DOCOSAHEXAENOIC ACIDS; EMBRYO, NONMAMMALIAN; HUMANS; MALE; MEMBRANE LIPIDS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROBLASTOMA; PHOSPHOLIPIDS; PHOSPHORYLATION; PRESENILIN-1; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPHINGOLIPIDS; TAU PROTEINS; TUMOR CELLS, CULTURED; UNILAMELLAR LIPOSOMES; ZEBRAFISH;

EID: 84899411996     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2013.12.016     Document Type: Article

References (79)

1. K. Mullane, and M. Williams Alzheimer's therapeutics: continued clinical failures question the validity of the amyloid hypothesis-but what lies beyond? Biochem. Pharmacol. 85 2013 289 305
2. N.E. Shepardson, G.M. Shankar, and D.J. Selkoe Cholesterol level and statin use in Alzheimer disease: I. Review of epidemiological and preclinical studies Arch. Neurol. 68 2011 1239 1244
3. N.E. Shepardson, G.M. Shankar, and D.J. Selkoe Cholesterol level and statin use in Alzheimer disease: II. Review of human trials and recommendations Arch. Neurol. 68 2011 1385 1392
4. J.J.M. Hoozemans, R. Veerhuis, J.M. Rozemuller, and P. Eikelenboom Soothing the inflamed brain: effect of non-steroidal anti-inflammatory drugs on Alzheimer's disease pathology CNS Neurol. Disord. Drug Targets 10 2011 57 67
5. H.-M. Su Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance J. Nutr. Biochem. 21 2010 364 373
6. E. Kawakita, M. Hashimoto, and O. Shido Docosahexaenoic acid promotes neurogenesis in vitro and in vivo Neuroscience 139 2006 991 997
7. N. Salem, B. Litman, H.Y. Kim, and K. Gawrisch Mechanisms of action of docosahexaenoic acid in the nervous system Lipids 36 2001 945 959
8. G. Astarita, K.-M. Jung, N.C. Berchtold, V.Q. Nguyen, D.L. Gillen, E. Head, C.W. Cotman, and D. Piomelli Deficient liver biosynthesis of docosahexaenoic acid correlates with cognitive impairment in Alzheimer's disease PLoS One 5 2010 e12538
9. T. Fraser, H. Tayler, and S. Love Fatty acid composition of frontal, temporal and parietal neocortex in the normal human brain and in Alzheimer's disease Neurochem. Res. 35 2010 503 513
10. D. Arsenault, C. Julien, C. Tremblay, and F. Calon DHA improves cognition and prevents dysfunction of entorhinal cortex neurons in 3xTg-AD mice PLoS One 6 2011 e17397
11. G.P. Lim, F. Calon, T. Morihara, F. Yang, B. Teter, O. Ubeda, N. Salem, S.A. Frautschy, and G.M. Cole A diet enriched with the omega-3 fatty acid docosahexaenoic acid reduces amyloid burden in an aged Alzheimer mouse model J. Neurosci. 25 2005 3032 3040
12. M.O.W. Grimm, J. Kuchenbecker, S. Grösgen, V.K. Burg, B. Hundsdörfer, T.L. Rothhaar, P. Friess, M.C. de Wilde, L.M. Broersen, B. Penke, M. Péter, L. Vígh, H.S. Grimm, and T. Hartmann Docosahexaenoic acid reduces amyloid β production via multiple pleiotropic mechanisms J. Biol. Chem. 286 2011 14028 14039
13. K.N. Green, H. Martinez-Coria, H. Khashwji, E.B. Hall, K.A. Yurko-Mauro, L. Ellis, and F.M. LaFerla Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid-β and tau pathology via a mechanism involving presenilin 1 levels J. Neurosci. 27 2007 4385 4395
14. M.C. Morris, D.A. Evans, J.L. Bienias, C.C. Tangney, D.A. Bennett, R.S. Wilson, N. Aggarwal, and J. Schneider Consumption of fish and n-3 fatty acids and risk of incident Alzheimer disease Arch. Neurol. 60 2003 940 946
15. E.J. Johnson, and E.J. Schaefer Potential role of dietary n-3 fatty acids in the prevention of dementia and macular degeneration Am. J. Clin. Nutr. 83 2006 1494S 1498S
16. Y. Freund-Levi, M. Eriksdotter-Jönhagen, T. Cederholm, H. Basun, G. Faxén-Irving, A. Garlind, I. Vedin, B. Vessby, L.O. Wahlund, and J. Palmblad 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
17. J.F. Quinn, R. Raman, R.G. Thomas, K. Yurko-Mauro, E.B. Nelson, C. Van Dyck, J.E. Galvin, J. Emond, C.R. Jack, M. Weiner, L. Shinto, and P.S. Aisen Docosahexaenoic acid supplementation and cognitive decline in Alzheimer disease: a randomized trial JAMA 304 2010 1903 1911
18. K. Yurko-Mauro, D. McCarthy, D. Rom, E.B. Nelson, A.S. Ryan, A. Blackwell, N. Salem, M. Stedman, and M. Investigators Beneficial effects of docosahexaenoic acid on cognition in age-related cognitive decline Alzheimers Dement. 6 2010 456 464
19. M.A. Fiol-Deroque, R. Gutierrez-Lanza, S. Terés, M. Torres, P. Barceló, R.V. Rial, A. Verkhratsky, P.V. Escribá, X. Busquets, and J.J. Rodríguez Cognitive recovery and restoration of cell proliferation in the dentate gyrus in the 5XFAD transgenic mice model of Alzheimer's disease following 2-hydroxy-DHA treatment Biogerontology 14 2013 763 775
20. Y. Zhao, F. Calon, C. Julien, J.W. Winkler, N.A. Petasis, W.J. Lukiw, and N.G. Bazan Docosahexaenoic acid-derived neuroprotectin D1 induces neuronal survival via secretase- and PPARγ-mediated mechanisms in Alzheimer's disease models PLoS One 6 2011 e15816
21. W.J. Lukiw, J.-G. Cui, V.L. Marcheselli, M. Bodker, A. Botkjaer, K. Gotlinger, C.N. Serhan, and N.G. Bazan A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease J. Clin. Invest. 115 2005 2774 2783
22. P.V. Escribá Membrane-lipid therapy: a new approach in molecular medicine Trends Mol. Med. 12 2006 34 43
23. H. Oakley, S.L. Cole, S. Logan, E. Maus, P. Shao, J. Craft, A. Guillozet-Bongaarts, M. Ohno, J. Disterhoft, L. Van Eldik, R. Berry, and R. Vassar Intraneuronal beta-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer's disease mutations: potential factors in amyloid plaque formation J. Neurosci. 26 2006 10129 10140
24. B.A. Wirsching, R.J. Beninger, K. Jhamandas, R.J. Boegman, and S.R. El-Defrawy Differential effects of scopolamine on working and reference memory of rats in the radial maze Pharmacol. Biochem. Behav. 20 1984 659 662
25. E.G. Bligh, and W.J. Dyer A rapid method of total lipid extraction and purification Can. J. Biochem. Physiol. 37 1959 911 917
26. J.M. Jiménez-López, M.P. Carrasco, C. Marco, and J.L. Segovia Hexadecylphosphocholine disrupts cholesterol homeostasis and induces the accumulation of free cholesterol in HepG2 tumour cells Biochem. Pharmacol. 71 2006 1114 1121
27. D. Canals, D. Mormeneo, G. Fabriàs, A. Llebaria, J. Casas, and A. Delgado Synthesis and biological properties of Pachastrissamine (jaspine B) and diastereoisomeric jaspines Bioorg. Med. Chem. 17 2009 235 241
28. A. Garanto, N.A. Mandal, M. Egido-Gabás, G. Marfany, G. Fabriàs, R.E. Anderson, J. Casas, and R. Gonzàlez-Duarte Specific sphingolipid content decrease in Cerkl knockdown mouse retinas Exp. Eye Res. 110 2013 96 106
29. R.E. Kingston, C.A. Chen, and H. Okayama Current Protocols in Immunology 2001 John Wiley & Sons, Inc.
30. A. Jämsä, K. Hasslund, R.F. Cowburn, A. Bäckström, and M. Vasänge The retinoic acid and brain-derived neurotrophic factor differentiated SH-SY5Y cell line as a model for Alzheimer's disease-like tau phosphorylation Biochem. Biophys. Res. Commun. 319 2004 993 1000
31. R.M. Gill, R. Slack, M. Kiess, and P.A. Hamel Regulation of expression and activity of distinct pRB, E2F, D-type cyclin, and CKI family members during terminal differentiation of P19 cells Exp. Cell Res. 244 1998 157 170
32. A. Marcilla-Etxenike, M.L. Martín, M.A. Noguera-Salvà, J.M. García-Verdugo, M. Soriano-Navarro, I. Dey, P.V. Escribá, and X. Busquets 2-Hydroxyoleic acid induces ER stress and autophagy in various human glioma cell lines PLoS One 7 2012 e48235
33. M. Sastre, I. Dewachter, G.E. Landreth, T.M. Willson, T. Klockgether, F. van Leuven, and M.T. Heneka Nonsteroidal anti-inflammatory drugs and peroxisome proliferator-activated receptor-gamma agonists modulate immunostimulated processing of amyloid precursor protein through regulation of beta-secretase J. Neurosci. 23 2003 9796 9804
34. L. Katsouri, C. Parr, N. Bogdanovic, M. Willem, and M. Sastre PPARγ co-activator-1α (PGC-1α) reduces amyloid-β generation through a PPARγ-dependent mechanism J. Alzheimers Dis. 25 2011 151 162
35. S. Taylor, M. Wakem, G. Dijkman, M. Alsarraj, and M. Nguyen A practical approach to RT-qPCR-Publishing data that conform to the MIQE guidelines Methods 50 2010 S1 S5
36. B. Ramos, D. Baglietto-Vargas, J.C. del Rio, I. Moreno-Gonzalez, C. Santa-Maria, S. Jimenez, C. Caballero, J.F. Lopez-Tellez, Z.U. Khan, D. Ruano, A. Gutierrez, and J. Vitorica Early neuropathology of somatostatin/NPY GABAergic cells in the hippocampus of a PS1xAPP transgenic model of Alzheimer's disease Neurobiol. Aging 27 2006 1658 1672
37. M. Torres, S. Jiménez, R. Sánchez-Varo, V. Navarro, L. Trujillo-Estrada, E. Sánchez-Mejias, I. Carmona, J.C. Davila, M. Vizuete, A. Gutiérrez, and J. Vitorica Defective lysosomal proteolysis and axonal transport are early pathogenic events that worsen with age leading to increased APP metabolism and synaptic Abeta in transgenic APP/PS1 hippocampus Mol. Neurodegener. 7 2012 59
38. M. Gobbi, F. Re, M. Canovi, M. Beeg, M. Gregori, S. Sesana, S. Sonnino, D. Brogioli, C. Musicanti, P. Gasco, M. Salmona, and M.E. Masserini Lipid-based nanoparticles with high binding affinity for amyloid-beta1-42 peptide Biomaterials 31 2010 6519 6529
39. L.D. Mayer, M.J. Hope, and P.R. Cullis Vesicles of variable sizes produced by a rapid extrusion procedure Biochim. Biophys. Acta 858 1986 161 168
40. M.B. Ruiz-Argüello, G. Basáñez, F.M. Goñi, and A. Alonso Different effects of enzyme-generated ceramides and diacylglycerols in phospholipid membrane fusion and leakage J. Biol. Chem. 271 1996 26616 26621
41. C. Arnulphi, J. Sot, M. García-Pacios, J.-L.R. Arrondo, A. Alonso, and F.M. Goñi Triton X-100 partitioning into sphingomyelin bilayers at subsolubilizing detergent concentrations: effect of lipid phase and a comparison with dipalmitoylphosphatidylcholine Biophys. J. 93 2007 3504 3514
42. H. Ahyayauch, M. Raab, J.V. Busto, N. Andraka, J.-L.R. Arrondo, M. Masserini, I. Tvaroska, and F.M. Goñi Binding of β-amyloid (1-42) peptide to negatively charged phospholipid membranes in the liquid-ordered state: modeling and experimental studies Biophys. J. 103 2012 453 463
43. L. Yang, N.Y. Ho, R. Alshut, J. Legradi, C. Weiss, M. Reischl, R. Mikut, U. Liebel, F. Müller, and U. Strähle Zebrafish embryos as models for embryotoxic and teratological effects of chemicals Reprod. Toxicol. 28 2009 245 253
44. M. Ibarguren, D.J. López, J.A. Encinar, J.M. González-Ros, X. Busquets, and P.V. Escribá Partitioning of liquid-ordered/liquid- disordered membrane microdomains induced by the fluidifying effect of 2-hydroxylated fatty acid derivatives Biochim. Biophys. Acta 1828 2013 2553 2563
45. C.Y. Shao, S.S. Mirra, H.B.R. Sait, T.C. Sacktor, and E.M. Sigurdsson Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Aβ and tau pathology in transgenic mouse models of Alzheimer's disease Acta Neuropathol. 122 2011 285 292
46. S. Jawhar, A. Trawicka, C. Jenneckens, T.A. Bayer, and O. Wirths Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer's disease Neurobiol. Aging 33 2012 e129 140 (196)
47. P. Osenkowski, W. Ye, R. Wang, M.S. Wolfe, and D.J. Selkoe Direct and potent regulation of gamma-secretase by its lipid microenvironment J. Biol. Chem. 283 2008 22529 22540
48. L. Kalvodova, N. Kahya, P. Schwille, R. Ehehalt, P. Verkade, D. Drechsel, and K. Simons Lipids as modulators of proteolytic activity of BACE: involvement of cholesterol, glycosphingolipids, and anionic phospholipids in vitro J. Biol. Chem. 280 2005 36815 36823
49. Z. Amtul, M. Keet, L. Wang, P. Merrifield, D. Westaway, and R.F. Rozmahel DHA supplemented in peptamen diet offers no advantage in pathways to amyloidosis: is it time to evaluate composite lipid diet? PLoS One 6 2011 e24094
50. B. De Strooper Aph-1, Pen-2, and Nicastrin with Presenilin generate an active gamma-Secretase complex Neuron 38 2003 9 12
51. S.L. Cole, and R. Vassar BACE1 structure and function in health and Alzheimer's disease Curr. Alzheimer Res. 5 2008 100 120
52. C. Haass, and D.J. Selkoe Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat. Rev. Mol. Cell Biol. 8 2007 101 112
53. R. Williamson, A. Usardi, D.P. Hanger, and B.H. Anderton Membrane-bound β-amyloid oligomers are recruited into lipid rafts by a fyn-dependent mechanism FASEB J. 22 2008 1552 1559
54. T. Kawarabayashi, M. Shoji, L.H. Younkin, L. Wen-Lang, D.W. Dickson, T. Murakami, E. Matsubara, K. Abe, K.H. Ashe, and S.G. Younkin Dimeric amyloid β protein rapidly accumulates in lipid rafts followed by apolipoprotein E and phosphorylated tau accumulation in the Tg2576 mouse model of Alzheimer's disease J. Neurosci. 24 2004 3801 3809
55. B. De Strooper, R. Vassar, and T. Golde The secretases: enzymes with therapeutic potential in Alzheimer disease Nat. Rev. Neurol. 6 2010 99 107
56. C. Gao, C. Hölscher, Y. Liu, and L. Li GSK3: a key target for the development of novel treatments for type 2 diabetes mellitus and Alzheimer disease Rev. Neurosci. 23 2012 1 11
57. B.D. Levy Resolvins and protectins: natural pharmacophores for resolution biology Prostaglandins Leukot. Essent. Fatty Acids 82 2010 327 332
58. K.H. Weylandt, C.-Y. Chiu, B. Gomolka, S.F. Waechter, and B. Wiedenmann Omega-3 fatty acids and their lipid mediators: towards an understanding of resolvin and protectin formation Prostaglandins Other Lipid Mediat. 97 2012 73 82
59. M. Söderberg, C. Edlund, K. Kristensson, and G. Dallner Fatty acid composition of brain phospholipids in aging and in Alzheimer's disease Lipids 26 1991 421 425
60. Z. Guan, Y. Wang, N.J. Cairns, P.L. Lantos, G. Dallner, and P.J. Sindelar Decrease and structural modifications of phosphatidylethanolamine plasmalogen in the brain with Alzheimer disease J. Neuropathol. Exp. Neurol. 58 1999 740 747
61. M.R. Prasad, M.A. Lovell, M. Yatin, H. Dhillon, and W.R. Markesbery Regional membrane phospholipid alterations in Alzheimer's disease Neurochem. Res. 23 1998 81 88
62. J.T. Wood, J.S. Williams, L. Pandarinathan, D.R. Janero, C.J. Lammi-Keefe, and A. Makriyannis Dietary docosahexaenoic acid supplementation alters select physiological endocannabinoid-system metabolites in brain and plasma J. Lipid Res. 51 2010 1416 1423
63. I. Ottestad, S. Hassani, G.I. Borge, A. Kohler, G. Vogt, T. Hyötyläinen, M. Orešič, K.W. Brønner, K.B. Holven, S.M. Ulven, and M.C.W. Myhrstad Fish oil supplementation alters the plasma lipidomic profile and increases long-chain PUFAs of phospholipids and triglycerides in healthy subjects PLoS One 7 2012 e42550
64. M. Grønn, E. Christensen, T.A. Hagve, and B.O. Christophersen Peroxisomal retroconversion of docosahexaenoic acid (22:6(n-3)) to eicosapentaenoic acid (20:5(n-3)) studied in isolated rat liver cells Biochim. Biophys. Acta 1081 1991 85 91
65. R.B. Chan, T.G. Oliveira, E.P. Cortes, L.S. Honig, K.E. Duff, S.A. Small, M.R. Wenk, G. Shui, and G. Di Paolo Comparative lipidomic analysis of mouse and human brain with Alzheimer disease J. Biol. Chem. 287 2012 2678 2688
66. A.A. Spector, and M.A. Yorek Membrane lipid composition and cellular function J. Lipid Res. 26 1985 1015 1035
67. Y. Tajima, M. Ishikawa, K. Maekawa, M. Murayama, Y. Senoo, T. Nishimaki-Mogami, H. Nakanishi, K. Ikeda, M. Arita, R. Taguchi, A. Okuno, R. Mikawa, S. Niida, O. Takikawa, and Y. Saito Lipidomic analysis of brain tissues and plasma in a mouse model expressing mutated human amyloid precursor protein/tau for Alzheimer's disease Lipids Health Dis. 12 2013 68
68. C. Sahlin, F.E. Pettersson, L.N.G. Nilsson, L. Lannfelt, and A.-S. Johansson Docosahexaenoic acid stimulates non-amyloidogenic APP processing resulting in reduced Abeta levels in cellular models of Alzheimer's disease Eur. J. Neurosci. 26 2007 882 889
69. O. Holmes, S. Paturi, W. Ye, M.S. Wolfe, and D.J. Selkoe Effects of membrane lipids on the activity and processivity of purified γ-secretase Biochemistry 51 2012 3565 3575
70. S.R. Shaikh Biophysical and biochemical mechanisms by which dietary N-3 polyunsaturated fatty acids from fish oil disrupt membrane lipid rafts J. Nutr. Biochem. 23 2012 101 105
71. K.S. Vetrivel, and G. Thinakaran Membrane rafts in Alzheimer's disease beta-amyloid production Biochim. Biophys. Acta 1801 2010 860 867
72. H. Schulze, T. Kolter, and K. Sandhoff Principles of lysosomal membrane degradation: cellular topology and biochemistry of lysosomal lipid degradation Biochim. Biophys. Acta 1793 2009 674 683
73. R.A. Nixon, J. Wegiel, A. Kumar, W.H. Yu, C. Peterhoff, A. Cataldo, and A.M. Cuervo Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study J. Neuropathol. Exp. Neurol. 64 2005 113 122
74. R. Sanchez-Varo, L. Trujillo-Estrada, E. Sanchez-Mejias, M. Torres, D. Baglietto-Vargas, I. Moreno-Gonzalez, V. De Castro, S. Jimenez, D. Ruano, M. Vizuete, J.C. Davila, J.M. Garcia-Verdugo, A.J. Jimenez, J. Vitorica, and A. Gutierrez Abnormal accumulation of autophagic vesicles correlates with axonal and synaptic pathology in young Alzheimer's mice hippocampus Acta Neuropathol. 123 2012 53 70
75. V. Schaeffer, I. Lavenir, S. Ozcelik, M. Tolnay, D.T. Winkler, and M. Goedert Stimulation of autophagy reduces neurodegeneration in a mouse model of human tauopathy Brain 135 2012 2169 2177
76. J.V. Rushworth, H.H. Griffiths, N.T. Watt, and N.M. Hooper Prion protein-mediated toxicity of amyloid-β oligomers requires lipid rafts and the transmembrane LRP1 J. Biol. Chem. 288 2013 8935 8951
77. M.L. Giuffrida, F. Caraci, B. Pignataro, S. Cataldo, P. De Bona, V. Bruno, G. Molinaro, G. Pappalardo, A. Messina, A. Palmigiano, D. Garozzo, F. Nicoletti, E. Rizzarelli, and A. Copani Beta-amyloid monomers are neuroprotective J. Neurosci. 29 2009 10582 10587
78. R. Resende, C. Pereira, P. Agostinho, A.P. Vieira, J.O. Malva, and C.R. Oliveira Susceptibility of hippocampal neurons to Abeta peptide toxicity is associated with perturbation of Ca2 + homeostasis Brain Res. 1143 2007 11 21
79. L. Texidó, M. Martín-Satué, E. Alberdi, C. Solsona, and C. Matute Amyloid β peptide oligomers directly activate NMDA receptors Cell Calcium 49 2011 184 190