Postsynaptic degeneration as revealed by PSD-95 reduction occurs after advanced Aβ and tau pathology in transgenic mouse models of Alzheimer's disease

Acta Neuropathologica

Volumn 122, Issue 3, 2011, Pages 285-292

  Shao, Charles Y ^a   Mirra, Suzanne S ^a   Sait, Hameetha B R ^c   Sacktor, Todd C ^b   Sigurdsson, Einar M ^c  

^a SUNY Downstate Medical Center   (United States)

^b SUNY DOWNSTATE MEDICAL CENTER   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

5XFAD; Alzheimer's disease; Hippocampus; Hirano body; JNPL3; P301L; PSD 95; Transgenic mice

Indexed keywords

AMYLOID BETA PROTEIN; POSTSYNAPTIC DENSITY PROTEIN 95; TAU PROTEIN;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOIDOPATHY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITE; FEMALE; HIPPOCAMPUS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOREACTIVITY; MALE; MOUSE; NERVE DEGENERATION; NEUROPIL; NONHUMAN; PERIKARYON; POSTSYNAPTIC DEGENERATION; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN LOCALIZATION; TAUOPATHY; TRANSGENIC MOUSE; WILD TYPE;

AGE FACTORS; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANALYSIS OF VARIANCE; ANIMALS; BRAIN; CARBOCYANINES; CELL COUNT; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; GUANYLATE KINASE; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; MIDDLE AGED; SYNAPSES; TAU PROTEINS; TAUOPATHIES;

EID: 80054700058     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0843-x     Document Type: Article

References (38)

1. CG Almeida D Tampellini RH Takahashi, et al. 2005 Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses Neurobiol Dis 20 187 198 16242627 10.1016/j.nbd.2005.02.008 1:CAS:528: DC%2BD2MXhtFCjs7jN (Pubitemid 41476246)
2. E Aronica DW Dickson Y Kress JH Morrison RS Zukin 1998 Non-plaque dystrophic dendrites in Alzheimer hippocampus: a new pathological structure revealed by glutamate receptor immunocytochemistry Neuroscience 82 979 991 9466422 10.1016/S0306-4522(97)00260-1 1:CAS:528:DyaK2sXnsF2lu7g%3D (Pubitemid 27502043)
3. AA Asuni A Boutajangout D Quartermain EM Sigurdsson 2007 Immunotherapy targeting pathological tau conformers in a tangle mouse model reduces brain pathology with associated functional improvements J Neurosci 27 9115 9129 17715348 10.1523/JNEUROSCI.2361-07.2007 1:CAS:528:DC%2BD2sXhtVSnsLbN (Pubitemid 47312068)
4. TA Blanpied JM Kerr MD Ehlers 2008 Structural plasticity with preserved topology in the postsynaptic protein network Proc Natl Acad Sci USA 105 12587 12592 18723686 10.1073/pnas.0711669105 1:CAS:528:DC%2BD1cXhtVOjsbjP
5. K Boekhoorn D Terwel B Biemans, et al. 2006 Improved long-term potentiation and memory in young tau-P301L transgenic mice before onset of hyperphosphorylation and tauopathy J Neurosci 26 3514 3523 16571759 10.1523/JNEUROSCI.5425-05.2006 1:CAS:528:DC%2BD28Xjs1yktbY%3D
6. X Chen C Winters R Azzam, et al. 2008 Organization of the core structure of the postsynaptic density Proc Natl Acad Sci USA 105 4453 4458 18326622 10.1073/pnas.0800897105 1:CAS:528:DC%2BD1cXkt1eiurY%3D (Pubitemid 351754401)
7. JF Crary CY Shao SS Mirra AI Hernandez TC Sacktor 2006 Atypical protein kinase C in neurodegenerative disease I: PKMzeta aggregates with limbic neurofibrillary tangles and AMPA receptors in Alzheimer disease J Neuropathol Exp Neurol 65 319 326 16691113 10.1097/01.jnen.0000218442.07664.04 1:CAS:528:DC%2BD28XltFequrc%3D (Pubitemid 44264829)
8. CA Davies DM Mann PQ Sumpter PO Yates 1987 A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease J Neurol Sci 78 151 164 3572454 10.1016/0022-510X(87)90057-8 1:STN:280:DyaL2s7pslCjsQ%3D%3D (Pubitemid 17031709)
9. ST DeKosky SW Scheff 1990 Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity Ann Neurol 27 457 464 2360787 10.1002/ana.410270502 1:STN:280:DyaK3c3pslGntg%3D%3D (Pubitemid 20149963)
10. DW Dickson HA Crystal C Bevona, et al. 1995 Correlations of synaptic and pathological markers with cognition of the elderly Neurobiol Aging 16 285 298 7566338 10.1016/0197-4580(95)00013-5 1:STN:280:DyaK28%2FjsVynsw%3D%3D (discussion 98-304)
11. D El-Husseini Ael E Schnell S Dakoji, et al. 2002 Synaptic strength regulated by palmitate cycling on PSD-95 Cell 108 849 863 10.1016/S0092-8674(02) 00683-9 (Pubitemid 34327535)
12. P Fischer S Jungwirth S Zehetmayer, et al. 2007 Conversion from subtypes of mild cognitive impairment to Alzheimer dementia Neurology 68 288 291 17242334 10.1212/01.wnl.0000252358.03285.9d 1:STN:280:DC%2BD2s%2Fkt1Ojuw%3D%3D (Pubitemid 46148341)
13. PG Galloway G Perry P Gambetti 1987 Hirano body filaments contain actin and actin-associated proteins J Neuropathol Exp Neurol 46 185 199 3029338 10.1097/00005072-198703000-00006 1:CAS:528:DyaL2sXhvFCjsr4%3D (Pubitemid 17037778)
14. JE Goldman 1983 The association of actin with Hirano bodies J Neuropathol Exp Neurol 42 146 152 6186777 10.1097/00005072-198303000-00004 1:CAS:528:DyaL3sXhslOitLk%3D (Pubitemid 13114125)
15. KH Gylys JA Fein F Yang, et al. 2004 Synaptic changes in Alzheimer's disease: increased amyloid-beta and gliosis in surviving terminals is accompanied by decreased PSD-95 fluorescence Am J Pathol 165 1809 1817 15509549 10.1016/S0002-9440(10)63436-0 1:CAS:528:DC%2BD2cXhtVCgsbrE (Pubitemid 39435178)
16. A Hirano 1994 Hirano bodies and related neuronal inclusions Neuropathol Appl Neurobiol 20 3 11 8208338 10.1111/j.1365-2990.1994.tb00951.x 1:STN:280:DyaK2c3mvVKitg%3D%3D (Pubitemid 24078160)
17. A Hirano HM Dembitzer LT Kurland HM Zimmerman 1968 The fine structure of some intraganglionic alterations. Neurofibrillary tangles, granulovacuolar bodies and "rod-like" structures as seen in Guam amyotrophic lateral sclerosis and parkinsonism-dementia complex J Neuropathol Exp Neurol 27 167 182 5646193 10.1097/00005072-196804000-00001 1:STN:280:DyaF1c7pvVansA%3D%3D
18. CA Hunt LJ Schenker MB Kennedy 1996 PSD-95 is associated with the postsynaptic density and not with the presynaptic membrane at forebrain synapses J Neurosci 16 1380 1388 8778289 1:CAS:528:DyaK28XhtVWmsbg%3D (Pubitemid 26145918)
19. R Kimura M Ohno 2009 Impairments in remote memory stabilization precede hippocampal synaptic and cognitive failures in 5XFAD Alzheimer mouse model Neurobiol Dis 33 229 235 19026746 10.1016/j.nbd.2008.10.006 1:CAS:528: DC%2BD1MXnslSlug%3D%3D
20. PN Lacor MC Buniel L Chang, et al. 2004 Synaptic targeting by Alzheimer's-related amyloid beta oligomers J Neurosci 24 10191 10200 15537891 10.1523/JNEUROSCI.3432-04.2004 1:CAS:528:DC%2BD2cXhtVeqtb7E (Pubitemid 39492046)
21. G Leuba A Savioz A Vernay, et al. 2008 Differential changes in synaptic proteins in the Alzheimer frontal cortex with marked increase in PSD-95 postsynaptic protein J Alzheimers Dis 15 139 151 18780974 1:CAS:528: DC%2BD1cXhtVKmtb3J
22. G Leuba C Walzer A Vernay, et al. 2008 Postsynaptic density protein PSD-95 expression in Alzheimer's disease and okadaic acid induced neuritic retraction Neurobiol Dis 30 408 419 18424056 10.1016/j.nbd.2008.02.012 1:CAS:528:DC%2BD1cXmtlShs74%3D
23. J Lewis E McGowan J Rockwood, et al. 2000 Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein Nat Genet 25 402 405 10932182 10.1038/78078 1:CAS:528: DC%2BD3cXlvVertbc%3D (Pubitemid 32983430)
24. S Love LK Siew D Dawbarn, et al. 2006 Premorbid effects of APOE on synaptic proteins in human temporal neocortex Neurobiol Aging 27 797 803 15979210 10.1016/j.neurobiolaging.2005.04.008 1:CAS:528:DC%2BD28XksVajsbc%3D
25. E Masliah M Mallory M Alford, et al. 2001 Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease Neurology 56 127 129 11148253 1:STN:280:DC%2BD3MzmvFWguw%3D%3D (Pubitemid 32059669)
26. E Masliah RD Terry M Alford R DeTeresa LA Hansen 1991 Cortical and subcortical patterns of synaptophysin like immunoreactivity in Alzheimer's disease Am J Pathol 138 235 246 1899001 1:STN:280:DyaK3M7gtlamuw%3D%3D
27. SS Mirra A Heyman D McKeel, et al. 1991 The Consortium to Establish a Registry for Alzheimer's Disease (CERAD) Part II. Standardization of the neuropathologic assessment of Alzheimer's disease Neurology 41 479 486 2011243 1:STN:280:DyaK3M7oslajsQ%3D%3D
28. H Oakley SL Cole S Logan, et al. 2006 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 10129 10140 17021169 10.1523/JNEUROSCI.1202-06.2006 1:CAS:528:DC%2BD28XhtVymurbK (Pubitemid 44527407)
29. M Ohno 2009 Failures to reconsolidate memory in a mouse model of Alzheimer's disease Neurobiol Learn Mem 92 455 459 19435612 10.1016/j.nlm.2009. 05.001
30. C Peterson Y Kress R Vallee JE Goldman 1988 High molecular weight microtubule-associated proteins bind to actin lattices (Hirano bodies) Acta Neuropathol (Berl) 77 168 174 1:CAS:528:DyaL1MXptlSjtQ%3D%3D (Pubitemid 19015554)
31. DT Proctor EJ Coulson PR Dodd 2010 Reduction in post-synaptic scaffolding PSD-95 and SAP-102 protein levels in the Alzheimer inferior temporal cortex is correlated with disease pathology J Alzheimers Dis 21 795 811 20634587 1:CAS:528:DC%2BC3cXhtFKmurjI
32. M Ramsden L Kotilinek C Forster, et al. 2005 Age-dependent neurofibrillary tangle formation, neuron loss, and memory impairment in a mouse model of human tauopathy (P301L) J Neurosci 25 10637 10647 16291936 10.1523/JNEUROSCI.3279-05.2005 1:CAS:528:DC%2BD2MXht1Kqsb%2FL (Pubitemid 41681911)
33. DJ Selkoe 1994 Alzheimer's disease: a central role for amyloid J Neuropathol Exp Neurol 53 438 447 8083687 10.1097/00005072-199409000-00003 1:CAS:528:DyaK2cXmsFamsbk%3D (Pubitemid 24276802)
34. CY Shao JF Crary C Rao TC Sacktor SS Mirra 2006 Atypical protein kinase C in neurodegenerative disease II: PKCiota/lambda in tauopathies and alpha-synucleinopathies J Neuropathol Exp Neurol 65 327 335 16691114 10.1097/01.jnen.0000218441.00040.82 1:CAS:528:DC%2BD28XltFequ74%3D (Pubitemid 44264830)
35. LK Siew S Love D Dawbarn GK Wilcock SJ Allen 2004 Measurement of pre- and post-synaptic proteins in cerebral cortex: effects of post-mortem delay J Neurosci Methods 139 153 159 15488227 10.1016/j.jneumeth.2004.04.020 1:CAS:528:DC%2BD2cXos1ensLc%3D (Pubitemid 39370840)
36. PJ Sjostrom EA Rancz A Roth M Hausser 2008 Dendritic excitability and synaptic plasticity Physiol Rev 88 769 840 18391179 10.1152/physrev.00016.2007 1:CAS:528:DC%2BD1cXls1KhsLg%3D (Pubitemid 351520092)
37. CI Sze JC Troncoso C Kawas, et al. 1997 Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease J Neuropathol Exp Neurol 56 933 944 9258263 10.1097/00005072-199708000-00011 1:STN:280:DyaK2svgt1yrtw%3D%3D (Pubitemid 27329114)
38. RD Terry E Masliah DP Salmon, et al. 1991 Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann Neurol 30 572 580 1789684 10.1002/ana.410300410 1:STN:280:DyaK387mtFOntw%3D%3D