The intersection of amyloid beta and tau in glutamatergic synaptic dysfunction and collapse in Alzheimer's disease

Ageing Research Reviews

Volumn 12, Issue 3, 2013, Pages 757-763

  Crimins, Johanna L ^a   Pooler, Amy ^b,c   Polydoro, Manuela ^c   Luebke, Jennifer I ^a   Spires Jones, Tara L ^c  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KING'S COLLEGE LONDON   (United Kingdom)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Alzheimer; Amyloid beta; Synapse; Tau

Indexed keywords

AMYLOID BETA PROTEIN; OLIGOMER; TAU PROTEIN;

ALZHEIMER DISEASE; HUMAN; IN VITRO STUDY; IN VIVO STUDY; NERVE CELL NETWORK; NERVE DEGENERATION; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; NONHUMAN; PROTEIN AGGREGATION; PROTEIN DEPLETION; PROTEIN FUNCTION; REVIEW; SOLUBILITY; SYNAPSE; SYNAPTIC TRANSMISSION;

ALZHEIMER; AMYLOID BETA; SYNAPSE; TAU;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; HUMANS; SYNAPSES; TAU PROTEINS;

EID: 84881546833     PISSN: 15681637     EISSN: 18729649     Source Type: Journal    
DOI: 10.1016/j.arr.2013.03.002     Document Type: Review

References (97)

1. Alonso A.D., Grundke-Iqbal I., Barra H.S., Iqbal K. Abnormal phosphorylation of tau and the mechanism of Alzheimer neurofibrillary degeneration: sequestration of microtubule-associated proteins 1 and 2 and the disassembly of microtubules by the abnormal tau. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:298-303.
2. Alzheimer A. Ubereine eigenartige Erkrankung der Hirnrinde. Allgemeine Zeitschrift fur Psychiatrie und Psychisch-Gerichtliche Medizin 1907, 64:146-148.
3. Arendt T. Synaptic degeneration in Alzheimer's disease. Acta Neuropathologica 2009, 118:167-179.
4. Association, A.s., 2012. Alzheimer's disease facts and figures.
5. Balietti M., Giorgetti B., Casoli T., Solazzi M., Tamagnini F., Burattini C., Aicardi G., Fattoretti P. Early selective vulnerability of synapses and synaptic mitochondria in the hippocampal CA1 region of the Tg2576 mouse model of Alzheimer's disease. Journal of Alzheimer's Disease 2013.
6. Ballatore C., Lee V.M., Trojanowski J.Q. Tau-mediated neurodegeneration in Alzheimer's disease and related disorders. Nature Reviews. Neuroscience 2007, 8:663-672.
7. Bertram L., Tanzi R.E. Thirty years of Alzheimer's disease genetics: the implications of systematic meta-analyses. Nature Reviews. Neuroscience 2008, 9:768-778.
8. Boekhoorn K., Terwel D., Biemans B., Borghgraef P., Wiegert O., Ramakers G.J., de Vos K., Krugers H., Tomiyama T., Mori H., Joels M., van Leuven F., Lucassen P.J. Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy. Journal of Neuroscience 2006, 26:3514-3523.
9. Bourne J.N., Harris K.M. Balancing structure and function at hippocampal dendritic spines. Annual Review of Neuroscience 2008, 31:47-67.
10. Braak E., Braak H. Alzheimer's disease: transiently developing dendritic changes in pyramidal cells of sector CA1 of the Ammon's horn. Acta Neuropathologica 1997, 93:323-325.
11. Caroni P., Donato F., Muller D. Structural plasticity upon learning: regulation and functions. Nature Reviews. Neuroscience 2012, 13:478-490.
12. Cleary J.P., Walsh D.M., Hofmeister J.J., Shankar G.M., Kuskowski M.A., Selkoe D.J., Ashe K.H. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nature Neuroscience 2005, 8:79-84.
13. Coleman P.D., Yao P.J. Synaptic slaughter in Alzheimer's disease. Neurobiology of Aging 2003, 24:1023-1027.
14. Crimins J.L., Rocher A.B., Luebke J.I. Electrophysiological changes precede morphological changes to frontal cortical pyramidal neurons in the rTg4510 mouse model of progressive tauopathy. Acta Neuropathologica 2012.
15. Crimins J.L., Rocher A.B., Peters A., Shultz P., Lewis J., Luebke J.I. Homeostatic responses by surviving cortical pyramidal cells in neurodegenerative tauopathy. Acta Neuropathologica 2011, 122:551-564.
16. D'Amelio M., Cavallucci V., Middei S., Marchetti C., Pacioni S., Ferri A., Diamantini A., De Zio D., Carrara P., Battistini L., Moreno S., Bacci A., Ammassari-Teule M., Marie H., Cecconi F. Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease. Nature Neuroscience 2011, 14:69-76.
17. DeKosky S.T., Scheff S.W. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Annals of Neurology 1990, 27:457-464.
18. Dixit R., Ross J.L., Goldman Y.E., Holzbaur E.L. Differential regulation of dynein and kinesin motor proteins by tau. Science 2008, 319:1086-1089.
19. Dubey M., Chaudhury P., Kabiru H., Shea T.B. Tau inhibits anterograde axonal transport and perturbs stability in growing axonal neurites in part by displacing kinesin cargo: neurofilaments attenuate tau-mediated neurite instability. Cell Motility and the Cytoskeleton 2008, 65:89-99.
20. Eckermann K., Mocanu M.M., Khlistunova I., Biernat J., Nissen A., Hofmann A., Schonig K., Bujard H., Haemisch A., Mandelkow E., Zhou L., Rune G., Mandelkow E.M. The beta-propensity of Tau determines aggregation and synaptic loss in inducible mouse models of tauopathy. Journal of Biological Chemistry 2007, 282:31755-31765.
21. Fox L.M., William C.M., Adamowicz D.H., Pitstick R., Carlson G.A., Spires-Jones T.L., Hyman B.T. Soluble tau species, not neurofibrillary aggregates, disrupt neural system integration in a tau transgenic model. Journal of Neuropathology and Experimental Neurology 2011, 70:588-595.
22. Glenner G.G., Wong C.W. Alzheimer's disease: initial report of the purification and characterization of a novel cerebrovascular amyloid protein. Biochemical and Biophysical Research Communications 1984, 120:885-890.
23. Goedert M., Spillantini M.G. A century of Alzheimer's disease. Science 2006, 314:777-781.
24. Gomez-Isla T., Spires T., de Calignon A., Hyman B.T. Neuropathology of Alzheimer's disease. Handbook of Clinical Neurology 2008, Elsevier, Edinburgh. M.J. Aminoff, F. Boller, D.F. Swaab (Eds.).
25. Hall G.F., Lee V.M., Lee G., Yao J. Staging of neurofibrillary degeneration caused by human tau overexpression in a unique cellular model of human tauopathy. American Journal of Pathology 2001, 158:235-246.
26. Hoover B.R., Reed M.N., Su J., Penrod R.D., Kotilinek L.A., Grant M.K., Pitstick R., Carlson G.A., Lanier L.M., Yuan L.-L., Ashe K.H., Liao D. Tau mislocalization to dendritic spines mediates synaptic dysfunction independently of neurodegeneration. Neuron 2010, 68:1067-1081.
27. Hsieh H., Boehm J., Sato C., Iwatsubo T., Tomita T., Sisodia S., Malinow R. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 2006, 52:831-843.
28. Ingelsson M., Fukumoto H., Newell K.L., Growdon J.H., Hedley-Whyte E.T., Frosch M.P., Albert M.S., Hyman B.T., Irizarry M.C. Early Abeta accumulation and progressive synaptic loss, gliosis, and tangle formation in AD brain. Neurology 2004, 62:925-931.
29. Iqbal K., Alonso Adel C., Grundke-Iqbal I. Cytosolic abnormally hyperphosphorylated tau but not paired helical filaments sequester normal MAPs and inhibit microtubule assembly. Journal of Alzheimer's Disease 2008, 14:365-370.
30. Ishihara T., Hong M., Zhang B., Nakagawa Y., Lee M.K., Trojanowski J.Q., Lee V.M. Age-dependent emergence and progression of a tauopathy in transgenic mice overexpressing the shortest human tau isoform. Neuron 1999, 24:751-762.
31. Ittner L.M., Gotz J. Amyloid-beta and tau-a toxic pas de deux in Alzheimer's disease. Nature Reviews. Neuroscience 2011, 12:65-72.
32. Ittner L.M., Ke Y.D., Delerue F., Bi M., Gladbach A., van Eersel J., Wolfing H., Chieng B.C., Christie M.J., Napier I.A., Eckert A., Staufenbiel M., Hardeman E., Gotz J. Dendritic function of tau mediates amyloid-beta toxicity in Alzheimer's disease mouse models. Cell 2010, 142:387-397.
33. Ittner L.M., Ke Y.D., Gotz J. Phosphorylated Tau interacts with c-Jun N-terminal kinase-interacting protein 1 (JIP1) in Alzheimer disease. Journal of Biological Chemistry 2009, 284:20909-20916.
34. Jaworski T., Lechat B., Demedts D., Gielis L., Devijver H., Borghgraef P., Duimel H., Verheyen F., Kugler S., Van Leuven F. Dendritic degeneration, neurovascular defects, and inflammation precede neuronal loss in a mouse model for tau-mediated neurodegeneration. American Journal of Pathology 2011, 179:2001-2015.
35. Jin M., Shepardson N., Yang T., Chen G., Walsh D., Selkoe D.J. Soluble amyloid beta-protein dimers isolated from Alzheimer cortex directly induce Tau hyperphosphorylation and neuritic degeneration. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:5819-5824.
36. Kang J., Lemaire H.G., Unterbeck A., Salbaum J.M., Masters C.L., Grzeschik K.H., Multhaup G., Beyreuther K., Muller-Hill B. The precursor of Alzheimer's disease amyloid A4 protein resembles a cell-surface receptor. Nature 1987, 325:733-736.
37. Karran E., Mercken M., De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nature Reviews. Drug Discovery 2011, 10:698-712.
38. Katsuse O., Lin W.L., Lewis J., Hutton M.L., Dickson D.W. Neurofibrillary tangle-related synaptic alterations of spinal motor neurons of P301L tau transgenic mice. Neuroscience Letters 2006, 409:95-99.
39. Koffie R.M., Hashimoto T., Tai H.C., Kay K.R., Serrano-Pozo A., Joyner D., Hou S., Kopeikina K.J., Frosch M.P., Lee V.M., Holtzman D.M., Hyman B.T., Spires-Jones T.L. Apolipoprotein E4 effects in Alzheimer's disease are mediated by synaptotoxic oligomeric amyloid-beta. Brain: A Journal of Neurology 2012, 135:2155-2168.
40. Koffie R.M., Hyman B.T., Spires-Jones T.L. Alzheimer's disease: synapses gone cold. Molecular Neurodegeneration 2011, 6:63.
41. Koffie R.M., Meyer-Luehmann M., Hashimoto T., Adams K.W., Mielke M.L., Garcia-Alloza M., Micheva K.D., Smith S.J., Kim M.L., Lee V.M., Hyman B.T., Spires-Jones T.L. Oligomeric amyloid beta associates with postsynaptic densities and correlates with excitatory synapse loss near senile plaques. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:4012-4017.
42. Kopeikina K.J., Carlson G.A., Pitstick R., Ludvigson A.E., Peters A., Luebke J.I., Koffie R.M., Frosch M.P., Hyman B.T., Spires-Jones T.L. Tau accumulation causes mitochondrial distribution deficits in neurons in a mouse model of tauopathy and in human Alzheimer's disease brain. American Journal of Pathology 2011, 179:2071-2082.
43. Kopeikina K.J., Hyman B.T., Spires-Jones T.L. Soluble forms of tau are toxic in Alzheimer's disease. Translational Neuroscience 2012, 3:223-233.
44. Kopeikina K.J., Polydoro M., Tai H.C., Yaeger E., Carlson G.A., Pitstick R., Hyman B.T., Spires-Jones T.L. Synaptic alterations in the rTg4510 mouse model of tauopathy. Journal of Comparative Neurology 2012.
45. Kuchibhotla K.V., Goldman S.T., Lattarulo C.R., Wu H.Y., Hyman B.T., Bacskai B.J. Abeta plaques lead to aberrant regulation of calcium homeostasis in vivo resulting in structural and functional disruption of neuronal networks. Neuron 2008, 59:214-225.
46. Lacor P.N., Buniel M.C., Chang L., Fernandez S.J., Gong Y., Viola K.L., Lambert M.P., Velasco P.T., Bigio E.H., Finch C.E., Krafft G.A., Klein W.L. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. Journal of Neuroscience 2004, 24:10191-10200.
47. Lambert M.P., Barlow A.K., Chromy B.A., Edwards C., Freed R., Liosatos M., Morgan T.E., Rozovsky I., Trommer B., Viola K.L., Wals P., Zhang C., Finch C.E., Krafft G.A., Klein W.L. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proceedings of the National Academy of Sciences of the United States of America 1998, 95:6448-6453.
48. Lanz T.A., Carter D.B., Merchant K.M. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiology of Disease 2003, 13:246-253.
49. Lasagna-Reeves C.A., Castillo-Carranza D.L., Sengupta U., Clos A.L., Jackson G.R., Kayed R. Tau oligomers impair memory and induce synaptic and mitochondrial dysfunction in wild-type mice. Molecular Neurodegeneration 2011, 6:39.
50. Lee S., Kim W., Li Z., Hall G.F. Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model. International Journal of Alzheimers Disease 2012, 2012. 172837.
51. Leroy K., Bretteville A., Schindowski K., Gilissen E., Authelet M., De Decker R., Yilmaz Z., Buee L., Brion J.P. Early axonopathy preceding neurofibrillary tangles in mutant tau transgenic mice. American Journal of Pathology 2007, 171:976-992.
52. Leuner K., Müller W., Reichert A. From mitochondrial dysfunction to amyloid beta formation: novel insights into the pathogenesis of Alzheimer's disease. Molecular Neurobiology 2012, 46:186-193.
53. Li S., Hong S., Shepardson N.E., Walsh D.M., Shankar G.M., Selkoe D. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009, 62:788-801.
54. Li S., Jin M., Koeglsperger T., Shepardson N.E., Shankar G.M., Selkoe D.J. Soluble Abeta oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. Journal of Neuroscience 2011, 31:6627-6638.
55. Lin W.L., Lewis J., Yen S.H., Hutton M., Dickson D.W. Ultrastructural neuronal pathology in transgenic mice expressing mutant (P301L) human tau. Journal of Neurocytology 2003, 32:1091-1105.
56. Lorincz A., Notomi T., Tamas G., Shigemoto R., Nusser Z. Polarized and compartment-dependent distribution of HCN1 in pyramidal cell dendrites. Nature Neuroscience 2002, 5:1185-1193.
57. Ludvigson A.E., Luebke J.I., Lewis J., Peters A. Structural abnormalities in the cortex of the rTg4510 mouse model of tauopathy: a light and electron microscopy study. Brain Structure & Function 2011, 216:31-42.
58. Luebke J.I., Weaver C.M., Rocher A.B., Rodriguez A., Crimins J.L., Dickstein D.L., Wearne S.L., Hof P.R. Dendritic vulnerability in neurodegenerative disease: insights from analyses of cortical pyramidal neurons in transgenic mouse models. Brain Structure & Function 2010, 214:181-199.
59. Magee J.C. Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons. Journal of Neuroscience 1998, 18:7613-7624.
60. Masters C.L., Simms G., Weinman N.A., Multhaup G., McDonald B.L., Beyreuther K. Amyloid plaque core protein in Alzheimer disease and Down syndrome. Proceedings of the National Academy of Sciences of the United States of America 1985, 82:4245-4249.
61. McKee A.C., Kowall N.W., Kosik K.S. Microtubular reorganization and dendritic growth response in Alzheimer's disease. Annals of Neurology 1989, 26:652-659.
62. Micheva K.D., Busse B., Weiler N.C., O'Rourke N., Smith S.J. Single-Synapse Analysis of a Diverse Synapse Population: Proteomic Imaging Methods and Markers. Neuron 2010, 68:639-653.
63. Micheva K.D., Smith S.J. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 2007, 55:25-36.
64. Moolman D.L., Vitolo O.V., Vonsattel J.P., Shelanski M.L. Dendrite and dendritic spine alterations in Alzheimer models. Journal of Neurocytology 2004, 33:377-387.
65. Noam Y., Zha Q., Phan L., Wu R.L., Chetkovich D.M., Wadman W.J., Baram T.Z. Trafficking and surface expression of hyperpolarization-activated cyclic nucleotide-gated channels in hippocampal neurons. Journal of Biological Chemistry 2010, 285:14724-14736.
66. Polydoro M., Acker C.M., Duff K., Castillo P.E., Davies P. Age-dependent impairment of cognitive and synaptic function in the htau mouse model of tau pathology. Journal of Neuroscience 2009, 29:10741-10749.
67. Probst A., Gotz J., Wiederhold K.H., Tolnay M., Mistl C., Jaton A.L., Hong M., Ishihara T., Lee V.M., Trojanowski J.Q., Jakes R., Crowther R.A., Spillantini M.G., Burki K., Goedert M. Axonopathy and amyotrophy in mice transgenic for human four-repeat tau protein. Acta Neuropathologica 2000, 99:469-481.
68. Qu J., Nakamura T., Cao G., Holland E., McKercher S., Lipton S. S-nitrosylation activates Cdk5 and contributes to synaptic spine loss induced by beta-amyloid peptide. Proceedings of the National Academy of Sciences of the United States of America 2011, 108:14330-14335.
69. Roberson E.D., Halabisky B., Yoo J.W., Yao J., Chin J., Yan F., Wu T., Hamto P., Devidze N., Yu G.Q., Palop J.J., Noebels J.L., Mucke L. Amyloid-beta/Fyn-induced synaptic, network, and cognitive impairments depend on tau levels in multiple mouse models of Alzheimer's disease. Journal of Neuroscience 2011, 31:700-711.
70. Roberson E.D., Scearce-Levie K., Palop J.J., Yan F., Cheng I.H., Wu T., Gerstein H., Yu G.Q., Mucke L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer's disease mouse model. Science 2007, 316:750-754.
71. Rocher A.B., Crimins J.L., Amatrudo J.M., Kinson M.S., Todd-Brown M.A., Lewis J., Luebke J.I. Structural and functional changes in tau mutant mice neurons are not linked to the presence of NFTs. Experimental Neurology 2010, 223:385-393.
72. Roselli F., Tirard M., Lu J., Hutzler P., Lamberti P., Livrea P., Morabito M., Almeida O.F. Soluble beta-amyloid1-40 induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. Journal of Neuroscience 2005, 25:11061-11070.
73. Rozkalne A., Hyman B.T., Spires-Jones T.L. Calcineurin inhibition with FK506 ameliorates dendritic spine density deficits in plaque-bearing Alzheimer model mice. Neurobiology of Disease 2011.
74. SantaCruz K., Lewis J., Spires T., Paulson J., Kotilinek L., Ingelsson M., Guimaraes A., DeTure M., Ramsden M., McGowan E., Forster C., Yue M., Orne J., Janus C., Mariash A., Kuskowski M., Hyman B., Hutton M., Ashe K.H. Tau suppression in a neurodegenerative mouse model improves memory function. Science 2005, 309:476-481.
75. Schindowski K., Bretteville A., Leroy K., Begard S., Brion J.P., Hamdane M., Buee L. Alzheimer's disease-like tau neuropathology leads to memory deficits and loss of functional synapses in a novel mutated tau transgenic mouse without any motor deficits. American Journal of Pathology 2006, 169:599-616.
76. Selkoe D.J. Alzheimer's disease: genes, proteins, and therapy. Physiological Reviews 2001, 81:741-766.
77. Selkoe D.J. Alzheimer's disease is a synaptic failure. Science 2002, 298:789-791.
78. Selkoe D.J. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behavioural Brain Research 2008, 192:106-113.
79. Shankar G.M., Bloodgood B.L., Townsend M., Walsh D.M., Selkoe D.J., Sabatini B.L. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. Journal of Neuroscience 2007, 27:2866-2875.
80. Shankar G.M., Li S., Mehta T.H., Garcia-Munoz A., Shepardson N.E., Smith I., Brett F.M., Farrell M.A., Rowan M.J., Lemere C.A., Regan C.M., Walsh D.M., Sabatini B.L., Selkoe D.J. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nature Medicine 2008, 14:837-842.
81. Sheng M., Sabatini B.L., Sudhof T.C. Synapses and Alzheimer's disease. Cold Spring Harbor Perspectives in Biology 2012, 4.
82. Snyder E.M., Nong Y., Almeida C.G., Paul S., Moran T., Choi E.Y., Nairn A.C., Salter M.W., Lombroso P.J., Gouras G.K., Greengard P. Regulation of NMDA receptor trafficking by amyloid-beta. Nature Neuroscience 2005, 8:1051-1058.
83. Spires T.L., Meyer-Luehmann M., Stern E.A., McLean P.J., Skoch J., Nguyen P.T., Bacskai B.J., Hyman B.T. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. Journal of Neuroscience 2005, 25:7278-7287.
84. Spires-Jones T., Knafo S. Spines, plasticity, and cognition in Alzheimer's model mice. Neural Plasticity 2012, 2012. 319836.
85. Spittaels K., Van den Haute C., Van Dorpe J., Bruynseels K., Vandezande K., Laenen I., Geerts H., Mercken M., Sciot R., Van Lommel A., Loos R., Van Leuven F. Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein. American Journal of Pathology 1999, 155:2153-2165.
86. Stamer K., Vogel R., Thies E., Mandelkow E., Mandelkow E.M. Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress. Journal of Cell Biology 2002, 156:1051-1063.
87. Sydow A., Van der Jeugd A., Zheng F., Ahmed T., Balschun D., Petrova O., Drexler D., Zhou L., Rune G., Mandelkow E., D'Hooge R., Alzheimer C., Mandelkow E.M. Tau-induced defects in synaptic plasticity, learning, and memory are reversible in transgenic mice after switching off the toxic Tau mutant. Journal of Neuroscience 2011, 31:2511-2525.
88. Tai H.C., Serrano-Pozo A., Hashimoto T., Frosch M.P., Spires-Jones T.L., Hyman B.T. The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. American Journal of Pathology 2012, 181:1426-1435.
89. Terry R.D., Masliah E., Salmon D.P., Butters N., DeTeresa R., Hill R., Hansen L.A., Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Annals of Neurology 1991, 30:572-580.
90. Thies E., Mandelkow E.M. Missorting of tau in neurons causes degeneration of synapses that can be rescued by the kinase MARK2/Par-1. Journal of Neuroscience 2007, 27:2896-2907.
91. Tsai J., Grutzendler J., Duff K., Gan W.B. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nature Neuroscience 2004, 7:1181-1183.
92. Walsh D.M., Klyubin I., Fadeeva J.V., Cullen W.K., Anwyl R., Wolfe M.S., Rowan M.J., Selkoe D.J. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002, 416:535-539.
93. Wang H.W., Pasternak J.F., Kuo H., Ristic H., Lambert M.P., Chromy B., Viola K.L., Klein W.L., Stine W.B., Krafft G.A., Trommer B.L. Soluble oligomers of beta amyloid (1-42) inhibit long-term potentiation but not long-term depression in rat dentate gyrus. Brain Research 2002, 924:133-140.
94. Wu H.Y., Hudry E., Hashimoto T., Kuchibhotla K., Rozkalne A., Fan Z., Spires-Jones T., Xie H., Arbel-Ornath M., Grosskreutz C.L., Bacskai B.J., Hyman B.T. Amyloid beta induces the morphological neurodegenerative triad of spine loss, dendritic simplification, and neuritic dystrophies through calcineurin activation. Journal of Neuroscience 2010, 30:2636-2649.
95. Yoshiyama Y., Higuchi M., Zhang B., Huang S.M., Iwata N., Saido T.C., Maeda J., Suhara T., Trojanowski J.Q., Lee V.M. Synapse loss and microglial activation precede tangles in a P301S tauopathy mouse model. Neuron 2007, 53:337-351.
96. Zempel H., Mandelkow E.M. Linking amyloid-beta and tau: amyloid-beta induced synaptic dysfunction via local wreckage of the neuronal cytoskeleton. Neuro-degenerative Diseases 2011, 10:64-72.
97. 2+ Elevation, missorting of endogenous tau into dendrites, tau phosphorylation, and destruction of microtubules and spines. Journal of Neuroscience 2010, 30:11938-11950.