Dendritic spine loss and synaptic alterations in Alzheimer's disease

Molecular Neurobiology

Volumn 37, Issue 1, 2008, Pages 73-82

  Knobloch, Marlen ^a   Mansuy, Isabelle M ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Alzheimer's disease; A ; A oligomers; Cytoskeleton; Dendritic spines; Molecular mechanisms; Synaptic loss

Indexed keywords

AMYLOID BETA PROTEIN; CYCLOSPORIN; MEMANTINE; NEUROTRANSMITTER RECEPTOR; TACROLIMUS; TAU PROTEIN;

ALZHEIMER DISEASE; BRAIN REGION; CELL LOSS; CELL STRUCTURE; COGNITION; CYTOSKELETON; DENDRITIC SPINE; DRUG MECHANISM; HUMAN; IMMEDIATE EARLY GENE; LONG TERM POTENTIATION; NERVE CELL PLASTICITY; NONHUMAN; PATHOGENESIS; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC MEMBRANE; SYNAPTIC TRANSMISSION; ANIMAL; BRAIN CORTEX; COGNITIVE DEFECT; METABOLISM; NERVE DEGENERATION; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SYNAPSE;

ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; ANIMALS; CEREBRAL CORTEX; COGNITION DISORDERS; CYTOSKELETON; DENDRITIC SPINES; HUMANS; NERVE DEGENERATION; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 50349083093     PISSN: 08937648     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12035-008-8018-z     Document Type: Review

References (118)

1. Glickstein M (2001) Ramón y Cajal, Santiago. Encyclopedia of life sciences. Wiley, Chichester. Available at http://www.els.net
2. Mazzarello P (2001) Golgi, Camillo. Encyclopedia of life sciences. Wiley, Chichester. Available at http://www.els.net
3. EA Nimchinsky BL Sabatini K Svoboda 2002 Structure and function of dendritic spines Annu Rev Physiol 64 313 353
4. W Denk JH Strickler WW Webb 1990 Two-photon laser scanning fluorescence microscopy Science 248 73 76
5. K Svoboda R Yasuda 2006 Principles of two-photon excitation microscopy and its applications to neuroscience Neuron 50 823 839
6. JT Trachtenberg BE Chen GW Knott G Feng JR Sanes E Welker K Svoboda 2002 Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex Nature 420 788 794
7. J Grutzendler N Kasthuri WB Gan 2002 Long-term dendritic spine stability in the adult cortex Nature 420 812 816
8. A Mizrahi JC Crowley E Shtoyerman LC Katz 2004 High-resolution in vivo imaging of hippocampal dendrites and spines J Neurosci 24 3147 3151
9. AK Majewska JR Newton M Sur 2006 Remodeling of synaptic structure in sensory cortical areas in vivo J Neurosci 26 3021 3029
10. VA Alvarez BL Sabatini 2007 Anatomical and physiological plasticity of dendritic spines Annu Rev Neurosci 30 79 97
11. AJ Holtmaat JT Trachtenberg L Wilbrecht GM Shepherd X Zhang GW Knott K Svoboda 2005 Transient and persistent dendritic spines in the neocortex in vivo Neuron 45 279 291
12. A Holtmaat L Wilbrecht GW Knott E Welker K Svoboda 2006 Experience-dependent and cell-type-specific spine growth in the neocortex Nature 441 979 983
13. GW Knott A Holtmaat L Wilbrecht E Welker K Svoboda 2006 Spine growth precedes synapse formation in the adult neocortex in vivo Nat Neurosci 9 1117 1124
14. KM Harris JK Stevens 1989 Dendritic spines of CA 1 pyramidal cells in the rat hippocampus: serial electron microscopy with reference to their biophysical characteristics J Neurosci 9 2982 2997
15. Y Takumi V Ramirez-Leon P Laake E Rinvik OP Ottersen 1999 Different modes of expression of AMPA and NMDA receptors in hippocampal synapses Nat Neurosci 2 618 624
16. Y Zuo G Yang E Kwon WB Gan 2005 Long-term sensory deprivation prevents dendritic spine loss in primary somatosensory cortex Nature 436 261 265
17. Y Zuo A Lin P Chang WB Gan 2005 Development of long-term dendritic spine stability in diverse regions of cerebral cortex Neuron 46 181 189
18. Y Sekino N Kojima T Shirao 2007 Role of actin cytoskeleton in dendritic spine morphogenesis Neurochem Int 51 92 104
19. A Matus 2005 Growth of dendritic spines: a continuing story Curr Opin Neurobiol 15 67 72
20. V Schubert CG Dotti 2007 Transmitting on actin: synaptic control of dendritic architecture J Cell Sci 120 205 212
21. J Hardy DJ Selkoe 2002 The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 353 356
22. C Haass DJ Selkoe 2007 Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid beta-peptide Nat Rev Mol Cell Biol 8 101 112
23. DM Walsh DJ Selkoe 2007 A beta oligomers-a decade of discovery J Neurochem 101 1172 1184
24. RD Terry E Masliah DP Salmon N Butters R DeTeresa R Hill LA Hansen R Katzman 1991 Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann Neurol 30 572 580
25. SW Scheff DA Price 2006 Alzheimer's disease-related alterations in synaptic density: neocortex and hippocampus J Alzheimer's Dis 9 101 115
26. E Masliah L Crews L Hansen 2006 Synaptic remodeling during aging and in Alzheimer's disease J Alzheimer's Dis 9 91 99
27. DJ Selkoe 2002 Alzheimer's disease is a synaptic failure Science 298 789 791
28. SW Scheff DA Price FA Schmitt EJ Mufson 2006 Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment Neurobiol Aging 27 1372 1384
29. SW Scheff DA Price FA Schmitt ST DeKosky EJ Mufson 2007 Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment Neurology 68 1501 1508
30. WG Honer 2003 Pathology of presynaptic proteins in Alzheimer's disease: more than simple loss of terminals Neurobiol Aging 24 1047 1062
31. PH Reddy G Mani BS Park J Jacques G Murdoch W Whetsell Jr J Kaye M Manczak 2005 Differential loss of synaptic proteins in Alzheimer's disease: implications for synaptic dysfunction J Alzheimer's Dis 7 103 17
32. M Ingelsson H Fukumoto KL Newell JH Growdon ET Hedley-Whyte MP Frosch MS Albert BT Hyman MC Irizarry 2004 Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain Neurology 62 925 931
33. JS Jacobsen CC Wu JM Redwine TA Comery R Arias M Bowlby R Martone JH Morrison MN Pangalos PH Reinhart FE Bloom 2006 Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease Proc Natl Acad Sci USA 103 5161 5166
34. CC Wu F Chawla D Games RE Rydel S Freedman D Schenk WG Young JH Morrison FE Bloom 2004 Selective vulnerability of dentate granule cells prior to amyloid deposition in PDAPP mice: digital morphometric analyses Proc Natl Acad Sci USA 101 7141 7146
35. TA Lanz DB Carter KM Merchant 2003 Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype Neurobiol Dis 13 246 253
36. TL Spires-Jones M Meyer-Luehmann JD Osetek PB Jones EA Stern BJ Bacskai BT Hyman 2007 Impaired spine stability underlies plaque-related spine loss in an Alzheimer's disease mouse model Am J Pathol 171 1304 1311
37. J Grutzendler K Helmin J Tsai WB Gan 2007 Various dendritic abnormalities are associated with fibrillar amyloid deposits in Alzheimer's disease Ann N Y Acad Sci 1097 30 39
38. H Dong MV Martin S Chambers JG Csernansky 2007 Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice J Comp Neurol 500 311 321
39. TL Spires M Meyer-Luehmann EA Stern PJ McLean J Skoch PT Nguyen BJ Bacskai BT Hyman 2005 Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy J Neurosci 25 7278 7287
40. J Tsai J Grutzendler K Duff WB Gan 2004 Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches Nat Neurosci 7 1181 1183
41. A Alpar U Ueberham MK Bruckner G Seeger T Arendt U Gartner 2006 Different dendrite and dendritic spine alterations in basal and apical arbors in mutant human amyloid precursor protein transgenic mice Brain Res 1099 189 198
42. BP Rutten NM Van der Kolk S Schafer MA van Zandvoort TA Bayer HW Steinbusch C Schmitz 2005 Age-related loss of synaptophysin immunoreactive presynaptic boutons within the hippocampus of APP751SL, PS1M146L, and APP751SL/PS1M146L transgenic mice Am J Pathol 167 161 173
43. DL Moolman OV Vitolo JP Vonsattel ML Shelanski 2004 Dendrite and dendritic spine alterations in Alzheimer models J Neurocytol 33 377 387
44. L Mucke E Masliah GQ Yu M Mallory EM Rockenstein G Tatsuno K Hu D Kholodenko K Johnson-Wood L McConlogue 2000 High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: synaptotoxicity without plaque formation J Neurosci 20 4050 4058
45. Hauptmann S, Scherping I, Drose S, Brandt U, Schulz KL, Jendrach M, Leuner K, Eckert A, Muller WE (2008) Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging (in press)
46. Z Li K Okamoto Y Hayashi M Sheng 2004 The importance of dendritic mitochondria in the morphogenesis and plasticity of spines and synapses Cell 119 873 887
47. JJ Palop J Chin L Mucke 2006 A network dysfunction perspective on neurodegenerative diseases Nature 443 768 773
48. E McGowan J Eriksen M Hutton 2006 A decade of modeling Alzheimer's disease in transgenic mice Trends Genet 22 281 289
49. DM Hartley DM Walsh CP Ye T Diehl S Vasquez PM Vassilev DB Teplow DJ Selkoe 1999 Protofibrillar intermediates of amyloid beta-protein induce acute electrophysiological changes and progressive neurotoxicity in cortical neurons J Neurosci 19 8876 8884
50. QS Chen BL Kagan Y Hirakura CW Xie 2000 Impairment of hippocampal long-term potentiation by Alzheimer amyloid beta-peptides J Neurosci Res 60 65 72
51. DM Walsh I Klyubin JV Fadeeva WK Cullen R Anwyl MS Wolfe MJ Rowan DJ Selkoe 2002 Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo Nature 416 535 539
52. HW Wang JF Pasternak H Kuo H Ristic MP Lambert B Chromy KL Viola WL Klein WB Stine GA Krafft BL Trommer 2002 Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus Brain Res 924 133 140
53. I Klyubin DM Walsh WK Cullen JV Fadeeva R Anwyl DJ Selkoe MJ Rowan 2004 Soluble Arctic amyloid beta protein inhibits hippocampal long-term potentiation in vivo Eur J Neurosci 19 2839 2846
54. M Knobloch M Farinelli U Konietzko RM Nitsch IM Mansuy 2007 Abeta oligomer-mediated long-term potentiation impairment involves protein phosphatase 1-dependent mechanisms J Neurosci 27 7648 7653
55. JP Cleary DM Walsh JJ Hofmeister GM Shankar MA Kuskowski DJ Selkoe KH Ashe 2005 Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function Nat Neurosci 8 79 84
56. S Lesne MT Koh L Kotilinek R Kayed CG Glabe A Yang M Gallagher KH Ashe 2006 A specific amyloid-beta protein assembly in the brain impairs memory Nature 440 352 357
57. A Demuro E Mina R Kayed SC Milton I Parker CG Glabe 2005 Calcium dysregulation and membrane disruption as a ubiquitous neurotoxic mechanism of soluble amyloid oligomers J Biol Chem 280 17294 17300
58. WL Klein 2006 Synaptic targeting by Abeta oligomers (ADDLS) as a basis for memory loss in early Alzheimer's disease Alzheimer's and Dementia 2 43 55
59. PN Lacor MC Buniel PW Furlow AS Clemente PT Velasco M Wood KL Viola WL Klein 2007 Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease J Neurosci 27 796 807
60. EM Snyder Y Nong CG Almeida S Paul T Moran EY Choi AC Nairn MW Salter PJ Lombroso GK Gouras P Greengard 2005 Regulation of NMDA receptor trafficking by amyloid-beta Nat Neurosci 8 1051 1058
61. GM Shankar BL Bloodgood M Townsend DM Walsh DJ Selkoe BL Sabatini 2007 Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway J Neurosci 27 2866 2875
62. B Calabrese GM Shaked IV Tabarean J Braga EH Koo S Halpain 2007 Rapid, concurrent alterations in pre- and postsynaptic structure induced by naturally-secreted amyloid-beta protein Mol Cell Neurosci 35 183 193
63. Dewachter I, Filipkowski RK, Priller C, Ris L, Neyton J, Croes S, Terwel D, Gysemans M, Devijver H, Borghgraef P, Godaux E, Kaczmarek L, Herms J, Van Leuven F (2007) Deregulation of NMDA-receptor function and down-stream signaling in APP[V717I] transgenic mice. Neurobiol Aging (in press)
64. H Hsieh J Boehm C Sato T Iwatsubo T Tomita S Sisodia R Malinow 2006 AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss Neuron 52 831 843
65. CG Almeida D Tampellini RH Takahashi P Greengard MT Lin EM Snyder GK Gouras 2005 Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses Neurobiol Dis 20 187 198
66. F Roselli M Tirard J Lu P Hutzler P Lamberti P Livrea M Morabito OF Almeida 2005 Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses J Neurosci 25 11061 11070
67. EH Chang MJ Savage DG Flood JM Thomas RB Levy V Mahadomrongkul T Shirao C Aoki PT Huerta 2006 AMPA receptor downscaling at the onset of Alzheimer's disease pathology in double knockin mice Proc Natl Acad Sci USA 103 3410 3415
68. N Bastrikova GA Gardner JM Reece A Jeromin SM Dudek 2008 Synapse elimination accompanies functional plasticity in hippocampal neurons Proc Natl Acad Sci USA 105 3123 3127
69. JJ Palop J Chin ED Roberson J Wang MT Thwin N Bien-Ly J Yoo KO Ho GQ Yu A Kreitzer S Finkbeiner JL Noebels L Mucke 2007 Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease Neuron 55 697 711
70. IM Mansuy S Shenolikar 2006 Protein serine/threonine phosphatases in neuronal plasticity and disorders of learning and memory Trends Neurosci 29 679 686
71. Q Tian J Wang 2002 Role of serine/threonine protein phosphatase in Alzheimer's disease NeuroSignals 11 262 269
72. F Liu I Grundke-Iqbal K Iqbal Y Oda K Tomizawa CX Gong 2005 Truncation and activation of calcineurin A by calpain I in Alzheimer disease brain J Biol Chem 280 37755 37762
73. CM Norris I Kadish EM Blalock KC Chen V Thibault NM Porter PW Landfield SD Kraner 2005 Calcineurin triggers reactive/inflammatory processes in astrocytes and is upregulated in aging and Alzheimer's models J Neurosci 25 4649 4658
74. QS Chen WZ Wei T Shimahara CW Xie 2002 Alzheimer amyloid beta-peptide inhibits the late phase of long-term potentiation through calcineurin-dependent mechanisms in the hippocampal dentate gyrus Neurobiol Learn Mem 77 354 371
75. MD Kaytor HT Orr 2002 The GSK3 beta signaling cascade and neurodegenerative disease Curr Opin Neurobiol 12 275 278
76. E Rockenstein M Torrance A Adame M Mante P Bar-on JB Rose L Crews E Masliah 2007 Neuroprotective effects of regulators of the glycogen synthase kinase-3beta signaling pathway in a transgenic model of Alzheimer's disease are associated with reduced amyloid precursor protein phosphorylation J Neurosci 27 1981 1991
77. S Peineau C Taghibiglou C Bradley TP Wong L Liu J Lu E Lo D Wu E Saule T Bouschet P Matthews JT Isaac ZA Bortolotto YT Wang GL Collingridge 2007 LTP inhibits LTD in the hippocampus via regulation of GSK3beta Neuron 53 703 717
78. LQ Zhu SH Wang D Liu YY Yin Q Tian XC Wang Q Wang JG Chen JZ Wang 2007 Activation of glycogen synthase kinase-3 inhibits long-term potentiation with synapse-associated impairments J Neurosci 27 12211 12220
79. MP Mazanetz PM Fischer 2007 Untangling tau hyperphosphorylation in drug design for neurodegenerative diseases Nat Rev Drug Discov 6 464 479
80. JC Cruz D Kim LY Moy MM Dobbin X Sun RT Bronson LH Tsai 2006 p25/cyclin-dependent kinase 5 induces production and intraneuronal accumulation of amyloid beta in vivo J Neurosci 26 10536 10541
81. BA Samuels YP Hsueh T Shu H Liang HC Tseng CJ Hong SC Su J Volker RL Neve DT Yue LH Tsai 2007 Cdk5 promotes synaptogenesis by regulating the subcellular distribution of the MAGUK family member CASK Neuron 56 823 837
82. A Fischer F Sananbenesi PT Pang B Lu LH Tsai 2005 Opposing roles of transient and prolonged expression of p25 in synaptic plasticity and hippocampus-dependent memory Neuron 48 825 838
83. WY Fu Y Chen M Sahin XS Zhao L Shi JB Bikoff KO Lai WH Yung AK Fu ME Greenberg NY Ip 2007 Cdk5 regulates EphA4-mediated dendritic spine retraction through an ephexin1-dependent mechanism Nat Neurosci 10 67 76
84. AH Hawasli DR Benavides C Nguyen JW Kansy K Hayashi P Chambon P Greengard CM Powell DC Cooper JA Bibb 2007 Cyclin-dependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation Nat Neurosci 10 880 886
85. L Zhao QL Ma F Calon ME Harris-White F Yang GP Lim T Morihara OJ Ubeda S Ambegaokar JE Hansen RH Weisbart B Teter SA Frautschy GM Cole 2006 Role of p21-activated kinase pathway defects in the cognitive deficits of Alzheimer disease Nat Neurosci 9 234 242
86. ML Hayashi SY Choi BS Rao HY Jung HK Lee D Zhang S Chattarji A Kirkwood S Tonegawa 2004 Altered cortical synaptic morphology and impaired memory consolidation in forebrain- specific dominant-negative PAK transgenic mice Neuron 42 773 787
87. D Zhao JB Watson CW Xie 2004 Amyloid beta prevents activation of calcium/calmodulin-dependent protein kinase II and AMPA receptor phosphorylation during hippocampal long-term potentiation J Neurophysiol 92 2853 2858
88. M Townsend T Mehta DJ Selkoe 2007 Soluble abeta inhibits specific signal transduction cascades common to the insulin receptor pathway J Biol Chem 282 33305 33312
89. M Mayford 2007 Protein kinase signaling in synaptic plasticity and memory Curr Opin Neurobiol 17 313 317
90. M Yamamoto-Sasaki H Ozawa T Saito M Rosler P Riederer 1999 Impaired phosphorylation of cyclic AMP response element binding protein in the hippocampus of dementia of the Alzheimer type Brain Res 824 300 303
91. B Gong Z Cao P Zheng OV Vitolo S Liu A Staniszewski D Moolman H Zhang M Shelanski O Arancio 2006 Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory Cell 126 775 788
92. L Tong PL Thornton R Balazs CW Cotman 2001 Beta-amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival Is not compromised J Biol Chem 276 17301 17306
93. OV Vitolo A Sant'Angelo V Costanzo F Battaglia O Arancio M Shelanski 2002 Amyloid beta-peptide inhibition of the PKA/CREB pathway and long-term potentiation: reversibility by drugs that enhance cAMP signaling Proc Natl Acad Sci USA 99 13217 13221
94. D Puzzo O Vitolo F Trinchese JP Jacob A Palmeri O Arancio 2005 Amyloid-beta peptide inhibits activation of the nitric oxide/cGMP/cAMP- responsive element-binding protein pathway during hippocampal synaptic plasticity J Neurosci 25 6887 6897
95. PH Reddy S McWeeney 2006 Mapping cellular transcriptosomes in autopsied Alzheimer's disease subjects and relevant animal models Neurobiol Aging 27 1060 1077
96. CA Dickey MN Gordon JE Mason NJ Wilson DM Diamond JF Guzowski D Morgan 2004 Amyloid suppresses induction of genes critical for memory consolidation in APP + PS1 transgenic mice J Neurochem 88 434 442
97. CA Dickey JF Loring J Montgomery MN Gordon PS Eastman D Morgan 2003 Selectively reduced expression of synaptic plasticity-related genes in amyloid precursor protein + presenilin-1 transgenic mice J Neurosci 23 5219 5226
98. AV Tzingounis RA Nicoll 2006 Arc/Arg3.1: linking gene expression to synaptic plasticity and memory Neuron 52 403 407
99. S Chowdhury JD Shepherd H Okuno G Lyford RS Petralia N Plath D Kuhl RL Huganir PF Worley 2006 Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking Neuron 52 445 459
100. N Plath O Ohana B Dammermann ML Errington D Schmitz C Gross X Mao A Engelsberg C Mahlke H Welzl U Kobalz A Stawrakakis E Fernandez R Waltereit A Bick-Sander E Therstappen SF Cooke V Blanquet W Wurst B Salmen MR Bosl HP Lipp SG Grant TV Bliss DP Wolfer D Kuhl 2006 Arc/Arg3.1 is essential for the consolidation of synaptic plasticity and memories Neuron 52 437 444
101. JD Shepherd G Rumbaugh J Wu S Chowdhury N Plath D Kuhl RL Huganir PF Worley 2006 Arc/Arg3.1 mediates homeostatic synaptic scaling of AMPA receptors Neuron 52 475 484
102. EM Rial Verde J Lee-Osbourne PF Worley R Malinow HT Cline 2006 Increased expression of the immediate-early gene arc/arg3.1 reduces AMPA receptor-mediated synaptic transmission Neuron 52 461 474
103. J Chin JJ Palop J Puolivali C Massaro N Bien-Ly H Gerstein K Scearce-Levie E Masliah L Mucke 2005 Fyn kinase induces synaptic and cognitive impairments in a transgenic mouse model of Alzheimer's disease J Neurosci 25 9694 9703
104. JJ Palop J Chin N Bien-Ly C Massaro BZ Yeung GQ Yu L Mucke 2005 Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice J Neurosci 25 9686 9693
105. SD Ginsberg SE Hemby VM Lee JH Eberwine JQ Trojanowski 2000 Expression profile of transcripts in Alzheimer's disease tangle-bearing CA1 neurons Ann Neurol 48 77 87
106. MT Maloney JR Bamburg 2007 Cofilin-mediated neurodegeneration in Alzheimer's disease and other amyloidopathies Mol Neurobiol 35 21 44
107. L Heredia P Helguera S de Olmos G Kedikian F Sola Vigo F LaFerla M Staufenbiel J de Olmos J Busciglio A Caceres A Lorenzo 2006 Phosphorylation of actin-depolymerizing factor/cofilin by LIM-kinase mediates amyloid beta-induced degeneration: a potential mechanism of neuronal dystrophy in Alzheimer's disease J Neurosci 26 6533 6542
108. PH Gibson BE Tomlinson 1977 Numbers of Hirano bodies in the hippocampus of normal and demented people with Alzheimer's disease J Neurol Sci 33 199 206
109. LY Chen CS Rex MS Casale CM Gall G Lynch 2007 Changes in synaptic morphology accompany actin signaling during LTP J Neurosci 27 5363 5372
110. V Fedulov CS Rex DA Simmons L Palmer CM Gall G Lynch 2007 Evidence that long-term potentiation occurs within individual hippocampal synapses during learning J Neurosci 27 8031 8039
111. E Messaoudi T Kanhema J Soule A Tiron G Dagyte B da Silva CR Bramham 2007 Sustained Arc/Arg3.1 synthesis controls long-term potentiation consolidation through regulation of local actin polymerization in the dentate gyrus in vivo J Neurosci 27 10445 10455
112. N Kojima T Shirao 2007 Synaptic dysfunction and disruption of postsynaptic drebrin-actin complex: a study of neurological disorders accompanied by cognitive deficits Neurosci Res 58 1 5
113. F Calon GP Lim F Yang T Morihara B Teter O Ubeda P Rostaing A Triller N Salem Jr KH Ashe SA Frautschy GM Cole 2004 Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model Neuron 43 633 645
114. H Takahashi T Mizui T Shirao 2006 Down-regulation of drebrin A expression suppresses synaptic targeting of NMDA receptors in developing hippocampal neurones J Neurochem 97 Suppl 1 110 115
115. M Buttini E Masliah R Barbour H Grajeda R Motter K Johnson-Wood K Khan P Seubert S Freedman D Schenk D Games 2005 Beta-amyloid immunotherapy prevents synaptic degeneration in a mouse model of Alzheimer's disease J Neurosci 25 9096 90101
116. FG De Felice PT Velasco MP Lambert K Viola SJ Fernandez ST Ferreira WL Klein 2007 Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine J Biol Chem 282 11590 11601
117. BR Shrestha OV Vitolo P Joshi T Lordkipanidze M Shelanski A Dunaevsky 2006 Amyloid beta peptide adversely affects spine number and motility in hippocampal neurons Mol Cell Neurosci 33 274 282
118. KT Dineley D Hogan WR Zhang G Taglialatela 2007 Acute inhibition of calcineurin restores associative learning and memory in Tg2576 APP transgenic mice Neurobiol Learn Mem 88 217 224