Oxidative stress and down syndrome: A route toward Alzheimer-like dementia

Current Gerontology and Geriatrics Research

Volumn 2012, Issue , 2012, Pages

  Perluigi, Marzia ^a   Butterfield, D Allan ^b,c  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF KENTUCKY   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84855583479     PISSN: 16877063     EISSN: 16877071     Source Type: Journal    
DOI: 10.1155/2012/724904     Document Type: Review

References (95)

1. Dierssen M., Herault Y., Estivill X., Aneuploidy: from a physiological mechanism of variance to Down syndrome Physiological Reviews 2009 89 3 887 920
2. Patterson D., Molecular genetic analysis of Down syndrome Human Genetics 2009 126 1 195 214
3. Das I., Reeves R. H., The use of mouse models to understand and improve cognitive deficits in down syndrome DMM Disease Models and Mechanisms 2011 4 5 596 606
4. Iannello R. C., Crack P. J., De Haan J. B., Kola I., Oxidative stress and neural dysfunction in Down syndrome Journal of Neural Transmission, Supplement 1999 57 257 267
5. Patterson D., Costa A. C. S., Down syndrome and geneticsa case of linked histories Nature Reviews Genetics 2005 6 2 137 147 (Pubitemid 40179536)
6. Roy A., Roberts I., Norton A., Vyas P., Acute megakaryoblastic leukaemia (AMKL) and transient myeloproliferative disorder (TMD) in Down syndrome: a multi-step model of myeloid leukaemogenesis British Journal of Haematology 2009 147 1 3 12
7. Roizen N. J., Patterson D., Down's syndrome The Lancet 2003 361 9365 1281 1289 (Pubitemid 36428586)
8. Bittles A. H., Glasson E. J., Clinical, social, and ethical implications of changing life expectancy in Down syndrome Developmental Medicine and Child Neurology 2004 46 4 282 286 (Pubitemid 38455820)
9. Bush A., Beail N., Risk factors for dementia in people with down syndrome: issues in assessment and diagnosis American Journal on Mental Retardation 2004 109 2 83 97
10. Zana M., Janka Z., Klmn J., Oxidative stress: a bridge between Down's syndrome and Alzheimer's disease Neurobiology of Aging 2007 28 5 648 676 (Pubitemid 46349350)
11. Capone G. T., Down syndrome: advances in molecular biology and the neurosciences Journal of Developmental and Behavioral Pediatrics 2001 22 1 40 59 (Pubitemid 33040477)
12. Krasuski J. S., Alexander G. E., Horwitz B., Rapoport S. I., Schapiro M. B., Relation of medial temporal lobe volumes to age and memory function in nondemented adults with Down's syndrome: implications for the prodromal phase of Alzheimer's disease American Journal of Psychiatry 2002 159 1 74 81 (Pubitemid 41070730)
13. Conti A., Fabbrini F., D'Agostino P., Negri R., Greco D., Genesio R., D'Armiento M., Olla C., Paladini D., Zannini M., Nitsch L., Altered expression of mitochondrial and extracellular matrix genes in the heart of human fetuses with chromosome 21 trisomy BMC Genomics 2007 8, article 268
14. Busciglio J., Yankner B. A., Apoptosis and increased generation of reactive oxygen species in Down's syndrome neurons in vitro Nature 1995 378 6559 776 779 (Pubitemid 26004408)
15. Jovanovic S. V., Clements D., MacLeod K., Biomarkers of oxidative stress are significantly elevated in Down syndrome Free Radical Biology and Medicine 1998 25 9 1044 1048 (Pubitemid 28558330)
16. Pallard F. V., Degan P., d'ischia M., Kelly F. J., Zatterale A., Calzone R., Castello G., Fernandez-Delgado R., Dunster C., Lloret A., Manini P., Pisanti M. A., Vuttariello E., Pagano G., Multiple evidence for an early age pro-oxidant state in Down Syndrome patients Biogerontology 2006 7 4 211 220
17. Cenini G., Dowling A. L., Beckett T. L., Association between frontal cortex oxidative damage and beta-amyloid as a function of age in Down Syndrome. Biochimica et Biophysica Acta. In press
18. Nunomura A., Perry G., Aliev G., Hirai K., Takeda A., Balraj E. K., Jones P. K., Ghanbari H., Wataya T., Shimohama S., Chiba S., Atwood C. S., Petersen R. B., Smith M. A., Oxidative damage is the earliest event in Alzheimer disease Journal of Neuropathology and Experimental Neurology 2001 60 8 759 767 (Pubitemid 32678256)
19. Rao K. S., Mechanisms of disease: DNA repair defects and neurological disease Nature Clinical Practice Neurology 2007 3 3 162 172 (Pubitemid 46403943)
20. Benzi G., Moretti A., Are reactive oxygen species involved in Alzheimer's disease? Neurobiology of Aging 1995 16 4 661 674
21. de Haan J. B., Cristiano F., Iannello R. C., Kola I., Cu/Zn-superoxide dismutase and glutathione peroxidase during aging Biochemistry and Molecular Biology International 1995 35 6 1281 1297 (Pubitemid 26172940)
22. Snchez-Font M. F., Sebasti J., Sanfeliu C., Cristfol R., Marfany G., Gonzlez-Duarte R., Peroxiredoxin 2 (PRDX2), an antioxidant enzyme, is under-expressed in Down syndrome fetal brains Cellular and Molecular Life Sciences 2003 60 7 1513 1523 (Pubitemid 36900532)
23. Shin J. H., London J., Le Pecheur M., Hger H., Pollak D., Lubec G., Aberrant neuronal and mitochondrial proteins in hippocampus of transgenic mice overexpressing human Cu/Zn superoxide dismutase 1 Free Radical Biology and Medicine 2004 37 5 643 653 (Pubitemid 38993511)
24. Gulesserian T., Engidawork E., Fountoulakis M., Lubec G., Antioxidant proteins in fetal brain: superoxide dismutase-1 (SOD-1) protein is not overexpressed in fetal Down syndrome Journal of Neural Transmission, Supplement 2001 61 71 84 (Pubitemid 38085073)
25. Pratic D., Iuliano L., Amerio G., Tang L. X., Rokach J., Sabatino G., Violi F., Down's syndrome is associated with increased 8,12-iso-iPF(2 )-VI levels: evidence for enhanced lipid peroxidation in vivo Annals of Neurology 2000 48 5 795 798
26. Campos C., Guzmn R., Lpez-Fernndez E., Casado A., Evaluation of urinary biomarkers of oxidative/nitrosative stress in adolescents and adults with Down syndrome Biochimica et Biophysica Acta 2011 1812 7 760 768
27. Ishihara K., Amano K., Takaki E., Ebrahim A. S., Shimohata A., Shibazaki N., Inoue I., Takaki M., Ueda Y., Sago H., Epstein C. J., Yamakawa K., Increased lipid peroxidation in Down's syndrome mouse models Journal of Neurochemistry 2009 110 6 1965 1976
28. Butterfield D. A., Drake J., Pocernich C., Castegna A., Evidence of oxidative damage in Alzheimer's disease brain: central role for amyloid -peptide Trends in Molecular Medicine 2001 7 12 548 554 (Pubitemid 33127140)
29. Butterfield D. A., Lauderback C. M., Lipid peroxidation and protein oxidation in Alzheimer's disease brain: potential causes and consequences involving amyloid -peptide-associated free radical oxidative stress Free Radical Biology and Medicine 2002 32 11 1050 1060 (Pubitemid 34603342)
30. Butterfield D. A., Galvan V., Lange M. B., Tang H., Sowell R. A., Spilman P., Fombonne J., Gorostiza O., Zhang J., Sultana R., Bredesen D. E., In vivo oxidative stress in brain of Alzheimer disease transgenic mice: requirement for methionine 35 in amyloid -peptide of APP Free Radical Biology and Medicine 2010 48 1 136 144
31. Mazur-Kolecka B., Golabek A., Nowicki K., Flory M., Frackowiak J., Amyloid- impairs development of neuronal progenitor cells by oxidative mechanisms Neurobiology of Aging 2006 27 9 1181 1192 (Pubitemid 44067306)
32. Head E., Lott I. T., Down syndrome and beta-amyloid deposition Current Opinion in Neurology 2004 17 2 95 100 (Pubitemid 38446448)
33. Mehta P. D., Capone G., Jewell A., Freedland R. L., Increased amyloid protein levels in children and adolescents with Down syndrome Journal of the Neurological Sciences 2007 254 1-2 22 27 (Pubitemid 46330403)
34. Schupf N., Zigman W. B., Tang M. X., Pang D., Mayeux R., Mehta P., Silverman W., Change in plasma A peptides and onset of dementia in adults with Down syndrome Neurology 2010 75 18 1639 1644
35. Anandatheerthavarada H. K., Biswas G., Robin M. A., Avadhani N. G., Mitochondrial targeting and a novel transmembrane arrest of Alzheimer's amyloid precursor protein impairs mitochondrial function in neuronal cells Journal of Cell Biology 2003 161 1 41 54 (Pubitemid 36459078)
36. Simn A.-M., Schiapparelli L., Salazar-Colocho P., Cuadrado-Tejedor M., Escribano L., Lpez de Maturana R., Del Ro J., Pérez-Mediavilla A., Frechilla D., Overexpression of wild-type human APP in mice causes cognitive deficits and pathological features unrelated to A levels Neurobiology of Disease 2009 33 3 369 378
37. Azkona G., Levannon D., Groner Y., Dierssen M., In vivo effects of APP are not exacerbated by BACE2 co-overexpression: behavioural characterization of a double transgenic mouse model Amino Acids 2010 39 5 1571 1580
38. Balcz B., Kirchner L., Cairns N., Fountoulakis M., Lubec G., Increased brain protein levels of carbonyl reductase and alcohol dehydrogenase in Down Syndrome and Alzheimer's disease Journal of Neural Transmission, Supplement 2001 61 193 201 (Pubitemid 38085082)
39. Reed T., Perluigi M., Sultana R., Pierce W. M., Klein J. B., Turner D. M., Coccia R., Markesbery W. R., Butterfield D. A., Redox proteomic identification of 4-Hydroxy-2-nonenal-modified brain proteins in amnestic mild cognitive impairment: insight into the role of lipid peroxidation in the progression and pathogenesis of Alzheimer's disease Neurobiology of Disease 2008 30 1 107 120
40. Munke M., Kraus J. P., Ohura T., Francke U., The gene for cystathionine -synthase (CBS) maps to the subtelomeric region on human chromosome 21q and to proximal mouse chromosome 17 American Journal of Human Genetics 1988 42 4 550 559
41. Hensley K., Venkova K., Christov A., Emerging biological importance of central nervous system lanthionines Molecules 2010 15 8 5581 5594
42. Eto K., Asada T., Arima K., Makifuchi T., Kimura H., Brain hydrogen sulfide is severely decreased in Alzheimer's disease Biochemical and Biophysical Research Communications 2002 293 5 1485 1488 (Pubitemid 34681045)
43. Ichinohe A., Kanaumi T., Takashima S., Enokido Y., Nagai Y., Kimura H., Cystathionine -synthase is enriched in the brains of Down's patients Biochemical and Biophysical Research Communications 2005 338 3 1547 1550 (Pubitemid 41608425)
44. Kamoun P., Belardinelli M. C., Chabli A., Lallouchi K., Chadefaux-Vekemans B., Endogenous hydrogen sulfide overproduction in Down syndrome American Journal of Medical Genetics 2003 116 3 310 311 (Pubitemid 36056753)
45. Kamoun P., Mental retardation in Down syndrome: a hydrogen sulfide hypothesis Medical Hypotheses 2001 57 3 389 392 (Pubitemid 32822439)
46. Beyer K., Lao J. I., Carrato C., Rodriguez-Vila A., Latorre P., Matar M., Llopis M. A., Mate J. L., Ariza A., Cystathionine beta synthase as a risk factor for Alzheimer disease Curr Alzheimer Res 2004 1 2 127 133
47. Knox A. J., Graham C., Bleskan J., Brodsky G., Patterson D., Mutations in the Chinese hamster ovary cell GART gene of de novo purine synthesis Gene 2009 429 1-2 23 30
48. Zitnanova I., Korytr P., Aruoma O. I., ustrov M., Garaiov I., Muchov J., Kalnoviov T., Pueschel S., urakov Z., Uric acid and allantoin levels in Down syndrome: antioxidant and oxidative stress mechanisms? Clinica Chimica Acta 2004 341 1-2 139 146 (Pubitemid 38210325)
49. Esposito G., De Filippis D., Cirillo C., Sarnelli G., Cuomo R., Iuvone T., The astroglial-derived S100 protein stimulates the expression of nitric oxide synthase in rodent macrophages through p38 MAP kinase activation Life Sciences 2006 78 23 2707 2715
50. Royston M. C., McKenzie J. E., Gentleman S. M., Sheng J. G., Mann D. M. A., Griffin W. S. T., Mrak R. E., Overexpression of S100 in Down's syndrome: correlation with patient age and with β-amyloid deposition Neuropathology and Applied Neurobiology 1999 25 5 387 393 (Pubitemid 29495686)
51. Odetti P., Angelini G., Dapino D., Zaccheo D., Garibaldi S., Dagna-Bricarelli F., Piombo G., Perry G., Smith M., Traverso N., Tabaton M., Early glycoxidation damage in brains from Down's syndrome Biochemical and Biophysical Research Communications 1998 243 3 849 851 (Pubitemid 28414171)
52. Nunomura A., Perry G., Pappolla M. A., Friedland R. P., Hirai K., Chiba S., Smith M. A., Neuronal oxidative stress precedes amyloid- deposition in down syndrome Journal of Neuropathology and Experimental Neurology 2000 59 11 1011 1017
53. Campos C., Guzmn R., Lpez-Fernndez E., Casado A., Urinary biomarkers of oxidative/nitrosative stress in healthy smokers Inhalation Toxicology 2011 23 3 148 156
54. Liu C., Belichenko P. V., Zhang L., Mouse models for down syndrome-associated developmental cognitive disabilities. Developmental Neuroscience. In press
55. Olson L. E., Roper R. J., Baxter L. L., Carlson E. J., Epstein C. J., Reeves R. H., Down syndrome mouse models Ts65Dn, Ts1Cje, and Ms1Cje/Ts65Dn exhibit variable severity of cerebellar phenotypes Developmental Dynamics 2004 230 3 581 589 (Pubitemid 38802484)
56. Richtsmeier J. T., Zumwalt A., Carlson E. J., Epstein C. J., Reeves R. H., Craniofacial phenotypes in segmentally trisomic mouse models for Down syndrome American Journal of Medical Genetics 2002 107 4 317 324 (Pubitemid 34062085)
57. Sago H., Carlson E. J., Smith D. J., Kilbridge J., Rubin E. M., Mobley W. C., Epstein C. J., Huang T. T., Ts1Cje, a partial trisomy 16 mouse model for Down syndrome, exhibits learning and behavioral abnormalities Proceedings of the National Academy of Sciences of the United States of America 1998 95 11 6256 6261 (Pubitemid 28248999)
58. Butterfield D. A., Bader Lange M. L., Sultana R., Involvements of the lipid peroxidation product, HNE, in the pathogenesis and progression of Alzheimer's disease Biochimica et Biophysica Acta 2010 1801 8 924 929
59. Perluigi M., Sultana R., Cenini G., Di Domenico F., Memo M., Pierce W. M., Coccia R., Butterfield D. A., Redox proteomics identification of 4-hydroxynonenalmodified brain proteins in Alzheimer's disease: role of lipid peroxidation in Alzheimer's disease pathogenesis ProteomicsClinical Applications 2009 3 6 682 693
60. Underwood M. A., Gilbert W. M., Sherman M. P., Amniotic fluid: not just fetal urine anymore Journal of Perinatology 2005 25 5 341 348 (Pubitemid 40645606)
61. Cho C. K. J., Smith C. R., Diamandis E. P., Amniotic fluid proteome analysis from down syndrome pregnancies for biomarker discovery Journal of Proteome Research 2010 9 7 3574 3582
62. Kolialexi A., Tounta G., Mavrou A., Tsangaris G. T., Proteomic analysis of amniotic fluid for the diagnosis of fetal aneuploidies Expert Review of Proteomics 2011 8 2 175 185
63. Perluigi M., di Domenico F., Fiorini A., Cocciolo A., Giorgi A., Foppoli C., Butterfield D. A., Giorlandino M., Giorlandino C., Eugenia Schinin M., Coccia R., Oxidative stress occurs early in Down syndrome pregnancy: a redox proteomics analysis of amniotic fluid ProteomicsClinical Applications 2011 5 3-4 167 178
64. Lott I. T., Head E., Doran E., Busciglio J., Beta-amyloid, oxidative stress and down syndrome Current Alzheimer Research 2006 3 5 521 528 (Pubitemid 46066428)
65. Head E., Lott I. T., Patterson D., Doran E., Haier R. J., Possible compensatory events in adult Down syndrome brain prior to the development of Alzheimer disease neuropathology: targets for nonpharmacological intervention Journal of Alzheimer's Disease 2007 11 1 61 76 (Pubitemid 46376710)
66. Head E., Doran E., Nistor M., Hill M., Schmitt F. A., Haier R. J., Lott I. T., Plasma amyloid- as a function of age, level of intellectual disability, and presence of dementia in down syndrome Journal of Alzheimer's Disease 2011 23 3 399 409
67. Nistor M., Don M., Parekh M., Sarsoza F., Goodus M., Lopez G. E., Kawas C., Leverenz J., Doran E., Lott I. T., Hill M., Head E., Alpha- and beta-secretase activity as a function of age and beta-amyloid in Down syndrome and normal brain Neurobiology of Aging 2007 28 10 1493 1506 (Pubitemid 47238529)
68. Head E., Azizeh B. Y., Lott I. T., Tenner A. J., Cotman C. W., Cribbs D. H., Complement association with neurons and β-amyloid deposition in the brains of aged individuals with Down Syndrome Neurobiology of Disease 2001 8 2 252 265 (Pubitemid 32382479)
69. Cataldo A. M., Petanceska S., Peterhoff C. M., Terio N. B., Epstein C. J., Villar A., Carlson E. J., Staufenbiel M., Nixon R. A., App gene dosage modulates endosomal abnormalities of Alzheimer's disease in a segmental trisomy 16 mouse model of Down syndrome Journal of Neuroscience 2003 23 17 6788 6792 (Pubitemid 36951206)
70. Lott I. T., Head E., Down syndrome and alzheimer's disease: a link between development and aging Mental Retardation and Developmental Disabilities Research Reviews 2001 7 3 172 178 (Pubitemid 32843808)
71. Busciglio J., Pelsman A., Wong C., Pigino G., Yuan M., Mori H., Yankner B. A., Altered metabolism of the amyloid precursor protein is associated with mitochondrial dysfunction in Down's syndrome Neuron 2002 33 5 677 688 (Pubitemid 34219240)
72. Busciglio J., Pelsman A., Helguera P., Ashur-Fabian O., Pinhasov A., Brenneman D. E., Gozes I., NAP and ADNF-9 protect normal and Down's syndrome cortical neurons from oxidative damage and apoptosis Current Pharmaceutical Design 2007 13 11 1091 1098 (Pubitemid 46739338)
73. Perrone S., Longini M., Bellieni C. V., Centini G., Kenanidis A., De Marco L., Petraglia F., Buonocore G., Early oxidative stress in amniotic fluid of pregnancies with Down syndrome Clinical Biochemistry 2007 40 3-4 177 180 (Pubitemid 46108711)
74. Zana M., Szécsényi A., Czibula., Bjelik A., Juhsz A., Rimanczy., Szab K., Vetr., Szucs P., Vrkonyi., Pkski M., Boda K., Rask I., Janka Z., Klmn J., Age-dependent oxidative stress-induced DNA damage in Down's lymphocytes Biochemical and Biophysical Research Communications 2006 345 2 726 733 (Pubitemid 43792511)
75. Mattson M. P., Cheng B., Culwell A. R., Esch F. S., Lieberburg I., Rydel R. E., Evidence for excitoprotective and intraneuronal calcium-regulating roles for secreted forms of the β-amyloid precursor protein Neuron 1993 10 2 243 254 (Pubitemid 23079546)
76. Schubert D., Jin L. W., Saitoh T., Cole G., The regulation of amyloid protein precursor secretion and its modulatory role in cell adhesion Neuron 1989 3 6 689 694
77. Russo C., Venezia V., Repetto E., Nizzari M., Violani E., Carlo P., Schettini G., The amyloid precursor protein and its network of interacting proteins: physiological and pathological implications Brain Research Reviews 2005 48 2 257 264 (Pubitemid 40585757)
78. Keating D. J., Chen C., Pritchard M. A., Alzheimer's disease and endocytic dysfunction: clues from the Down syndrome-related proteins, DSCR1 and ITSN1 Ageing Research Reviews 2006 5 4 388 401 (Pubitemid 44437038)
79. Ermak G., Cheadle C., Becker K. G., Harris C. D., Davies K. J. A., DSCR1(Adapt78) modulates expression of SOD1 The FASEB Journal 2004 18 1 62 69 (Pubitemid 38076466)
80. Chang K. T., Min K. T., Drosophila melanogaster homolog of Down syndrome critical region 1 is critical for mitochondrial function Nature Neuroscience 2005 8 11 1577 1585 (Pubitemid 41573673)
81. Bersu E. T., Ahmad F. J., Schwei M. J., Baas P. W., Cytoplasmic abnormalities in cultured cerebellar neurons from the trisomy 16 mouse Developmental Brain Research 1998 109 1 115 120 (Pubitemid 28335629)
82. Prince J., Jia S., Bave U., Anneren G., Oreland L., Mitochondrial enzyme deficiencies in Down's syndrome Journal of Neural TransmissionParkinson's Disease and Dementia Section 1994 8 3 171 181
83. Howell N., Elson J. L., Chinnery P. F., Turnbull D. M., mtDNA mutations and common neurodegenerative disorders Trends in Genetics 2005 21 11 583 586 (Pubitemid 41429284)
84. Arbuzova S., Hutchin T., Cuckle H., Mitochondrial dysfunction and Down's syndrome BioEssays 2002 24 8 681 684 (Pubitemid 34850322)
85. Coskun P., Wyrembak J., Schriner S., A mitochondrial etiology of Alzheimer and Parkinson disease. Biochimica et Biophysica Acta. In press
86. Wallace D. C., Mitochondrial diseases in man and mouse Science 1999 283 5407 1482 1488
87. Druzhyna N., Nair R. G., Ledoux S. P., Wilson G. L., Defective repair of oxidative damage in mitochondrial DNA in Down's syndrome Mutation Research 1998 409 2 81 89 (Pubitemid 28522174)
88. Schuchmann S., Heinemann U., Increased mitochondrial superoxide generation in neurons from trisomy 16 mice: a model of Down's syndrome Free Radical Biology and Medicine 2000 28 2 235 250 (Pubitemid 30084016)
89. Bambrick L. L., Fiskum G., Mitochondrial dysfunction in mouse trisomy 16 brain Brain Research 2008 1188 1 9 16 (Pubitemid 350296061)
90. Valenti D., Manente G. A., Moro L., Marra E., Vacca R. A., Deficit of complex I activity in human skin fibroblasts with chromosome 21 trisomy and overproduction of reactive oxygen species by mitochondria: involvement of the cAMP/PKA signalling pathway Biochemical Journal 2011 435 3 679 688
91. Li H., Dryhurst G., Oxidative metabolites of 5-S-cysteinyldopamine inhibit the pyruvate dehydrogenase complex Journal of Neural Transmission 2001 108 12 1363 1374 (Pubitemid 34020442)
92. Roat E., Prada N., Ferraresi R., Giovenzana C., Nasi M., Troiano L., Pinti M., Nemes E., Lugli E., Biagioni O., Mariotti M., Ciacci L., Consolo U., Balli F., Cossarizza A., Mitochondrial alterations and tendency to apoptosis in peripheral blood cells from children with Down syndrome FEBS Letters 2007 581 3 521 525 (Pubitemid 46157228)
93. Infantino V., Castegna A., Iacobazzi F., Spera I., Scala I., Andria G., Iacobazzi V., Impairment of methyl cycle affects mitochondrial methyl availability and glutathione level in Down's syndrome Molecular Genetics and Metabolism 2011 102 3 378 382
94. Lott I. T., Doran E., Nguyen V. Q., Tournay A., Head E., Gillen D. L., Down syndrome and dementia: a randomized, controlled trial of antioxidant supplementation American Journal of Medical Genetics, Part A 2011 155 8 1939 1948
95. Lockrow J., Prakasam A., Huang P., Bimonte-Nelson H., Sambamurti K., Granholm A. C., Cholinergic degeneration and memory loss delayed by vitamin E in a Down syndrome mouse model Experimental Neurology 2009 216 2 278 289