Differential Involvement of Synaptic Vesicle and Presynaptic Plasma Membrane Proteins in Alzheimer's Disease
Abstract
Alzheimer's disease (AD) is characterized by progressive cognitive decline. Recent studies have shown that synaptic loss in the cortex is the major correlate of cognitive decline in AD. In the present study we assessed synaptic proteins such as synaptobrevin, synaptophysin, synaptotagmin, synaptosomal-associated protein 25 (SNAP-25), and syntaxin1/HPC-1 in control and AD brains to determine whether synaptic proteins are equally or differentially affected in AD. Western analysis showed that in AD levels of synaptobrevin and synaptophysin were decreased by some 30% from amounts in controls, while those of synaptotagmin, SNAP-25, and syntaxin 1/HPC-1 were decreased by only about 10%. As synaptobrevin and synaptophysin are localized mainly in transmitter-containing synaptic vesicles while SNAP-25 and syntaxin 1/HPC-1 are found in presynaptic plasma membranes, these results suggest differential involvement of synaptic components in AD.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Synaptic proteins are involved in differential pathological processes in patients with Alzheimer's disease, and several synaptic proteins are associated with total Tau and phosphorylated Tau levels in CSF.
“Synaptic proteins are involved in differential pathological processes in patients with AD and several of these proteins are also associated with their corresponding total Tau (Tau) and phosphorylated tau (PTau) levels in CSF [7, 8].”
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Mirra, S. S., Heyman, A., McKeel, D., Sumi, S. M., Crain, B. J., Brownlee, L. M., Vogel, F. S., Hughes, J. P., Belle, G. V., Berg, L., et al. (1991) · Neurology · doi:10.1212/wnl.41.4.479 · Cited by 4,961 · see citing works
Terry, R. D., Masliah, E., Salmon, D. P., Butters, N., DeTeresa, R., Hill, R., Hansen, L. A., & Katzman, R. (1991) · Annals of Neurology · doi:10.1002/ana.410300410 · Cited by 4,397 · see citing works
Wiedenmann, B. J., & Franke, W. W. (1985) · Cell · doi:10.1016/s0092-8674(85)80082-9 · Cited by 1,432 · see citing works
Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E. L. F., Billingsley, M. L., Bloom, F. E., & Wilson, M. C. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.3039 · Cited by 809 · see citing works
Katzman, R. (1986) · New England Journal of Medicine · doi:10.1056/nejm198604103141506 · Cited by 801 · see citing works
Navone, F., Jahn, R., Gioia, G. D., Stukenbrok, H., Greengard, P., & Camilli, P. V. D. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.6.2511 · Cited by 674 · see citing works
Baumert, M., Maycox, P. R., Navone, F., Camilli, P. V. D., & Jahn, R. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb03388.x · Cited by 518 · see citing works
Immunohistochemical quantification of the synapse-related protein synaptophysin in Alzheimer disease
Masliah, E., Terry, R. D., DeTeresa, R. M., & Hansen, L. A. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90582-x · Cited by 363 · see citing works
Domain structure of synaptotagmin (p65)
Perin, M., Brose, N., Jahn, R., & Südhof, T. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)52480-7 · Cited by 329 · see citing works
A marker of early amacrine cell development in rat retina
Barnstable, C. J., Hofstein, R., & Akagawa, K. (1985) · Developmental Brain Research · doi:10.1016/0165-3806(85)90116-6 · Cited by 324 · see citing works
Self-citationCortical and subcortical patterns of synaptophysinlike immunoreactivity in Alzheimer's disease.
Masliah, E., Terry, R. D., Alford, M. F., DeTeresa, R. M., & Hansen, L. A. (1991) · PubMed Central · Cited by 296 · see citing works
HPC-1 is associated with synaptotagmin and omega-conotoxin receptor.
Yoshida, A., Oho, C., Omori, A., Kuwahara, R., Ito, T., & Takahashi, M. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)73984-2 · Cited by 274 · see citing works
Multiple palmitoylation of synaptotagmin and the t‐SNARE SNAP‐25
Veit, M., Söllner, T. H., & Rothman, J. E. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00362-6 · Cited by 251 · see citing works
Localization of synaptotagmin-binding domains on syntaxin
Yun, K., & Scheller, R. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-06-01975.1996 · Cited by 154 · see citing works
Synaptotagmin, a synaptic vesicle protein, is present in human cerebrospinal fluid
Davidsson, P., Jahn, R., Bergquist, J., Ekman, R., & Blennow, K. (1996) · Molecular and Chemical Neuropathology · doi:10.1007/bf02815094 · Cited by 88 · see citing works
Human fetal hippocampal development: II. The neuronal cytoskeleton
Arnold, S. E., & Trojanowski, J. Q. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960401)367:2 · Cited by 87 · see citing works
Fatty Acylation of Synaptotagmin in PC12 Cells and Synaptosomes
Chapman, E. R., Blasi, J., An, S., Brose, N., Johnston, P. A., Südhof, T. C., & Jahn, R. (1996) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1996.1174 · Cited by 71 · see citing works
Sesack, S. R., & Snyder, C. L. (1995) · Neuroscience · doi:10.1016/0306-4522(95)00087-y · Cited by 52 · see citing works
Jagadish, M. N., Fernandez, C. S., Hewish, D. R., Macaulay, S. L., Gough, K. H., Grusovin, J., Verkuylen, A. J., Cosgrove, L. J., ALAFACI, A., Frenkel, M. J., et al. (1996) · Biochemical Journal · doi:10.1042/bj3170945 · Cited by 48 · see citing works
Flagged first, then by citations
1 of the 21 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Classification and basic pathology of Alzheimer disease
Duyckaerts, C., Delatour, B., & Potier, M.-C. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0532-1 · Cited by 1,031 · see citing works
Synaptic degeneration in Alzheimer's disease
Arendt, T. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0536-x · Cited by 517 · see citing works
Suthram, S., Dudley, J. T., Chiang, A. P.-F., Chen, R., Hastie, T. J., & Butte, A. J. (2010) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1000662 · Cited by 323 · see citing works
Antoine, J.-C. G., Cinotti, L., Tilikete, C., Bouhour, F., Camdessanch�, J. P., Confavreux, C., Vighetto, A., Renault‐Mannel, V., Michel, D., & Honnorat, J. (2000) · Annals of Neurology · doi:10.1002/1531-8249(200007)48:1 · Cited by 86 · see citing works
Brinkmalm, A., Brinkmalm, G., Honer, W. G., Frölich, L., Hausner, L., Minthon, L., Hansson, O., Wallin, A., Zetterberg, H., Blennow, K., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-53 · Cited by 293 · see citing works
Mild cognitive impairment: pathology and mechanisms
Mufson, E. J., Binder, L. I., Counts, S., DeKosky, S. T., deToledo‐Morrell, L., Ginsberg, S. D., Ikonomović, M. D., Perez, S. E., & Scheff, S. W. (2011) · Acta Neuropathologica · doi:10.1007/s00401-011-0884-1 · Cited by 258 · see citing works
Counts, S., Nadeem, M., Lad, S. P., Wuu, J., & Mufson, E. J. (2006) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-200606000-00007 · Cited by 211 · see citing works
Arendt, T. (2003) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2003.09.007 · Cited by 188 · see citing works
Kashani, A., Lepicard, E. M., Poirel, O., Videau, C., David, J. P., Fallet‐Bianco, C., Simon, A., Delacourte, A., Bruno Giros, A., Epelbaum, J., et al. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.04.010 · Cited by 175 · see citing works
Alzheimer's disease as a disorder of mechanisms underlying structural brain self-organization
Arendt, T. (2001) · Neuroscience · doi:10.1016/s0306-4522(00)00516-9 · Cited by 168 · see citing works
Cerebrospinal Fluid Biomarkers of Alzheimer’s Disease: Current Evidence and Future Perspectives
McGrowder, D. A., Miller, F. G., Vaz, K., Nwokocha, C. R., Wilson-Clarke, C. F., Anderson, M., Brown, J., Anderson-Jackson, L., Williams, L., Latore, L., et al. (2021) · Brain Sciences · doi:10.3390/brainsci11020215 · Cited by 167 · see citing works
Selective regional loss of exocytotic presynaptic vesicle proteins in Alzheimer’s disease brains
Sze, C., Bi, H., Kleinschmidt-DeMasters, B. K., Filley, C. M., & Martin, L. J. (2000) · Journal of the Neurological Sciences · doi:10.1016/s0022-510x(00)00285-9 · Cited by 161 · see citing works
Abnormalities of SNARE Mechanism Proteins in Anterior Frontal Cortex in Severe Mental Illness
Honer, W. G. (2002) · Cerebral Cortex · doi:10.1093/cercor/12.4.349 · Cited by 149 · see citing works
Target Identification for CNS Diseases by Transcriptional Profiling
Altar, C. A., Vawter, M. P., & Ginsberg, S. D. (2008) · Neuropsychopharmacology · doi:10.1038/npp.2008.172 · Cited by 139 · see citing works
Ravetti, M. G., Rosso, O. A., Berretta, R. E., & Moscato, P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0010153 · Cited by 140 · see citing works
Abnormalities in the synaptic vesicle fusion machinery in Huntington’s disease
Morton, A. J., Faull, R. L. M., & Edwardson, J. M. (2001) · Brain Research Bulletin · doi:10.1016/s0361-9230(01)00611-6 · Cited by 132 · see citing works
Agliardi, C., Guerini, F. R., Zanzottera, M., Bianchi, A., Nemni, R., & Clerici, M. (2019) · Molecular Neurobiology · doi:10.1007/s12035-019-1501-x · Cited by 130 · see citing works
Pathology of presynaptic proteins in Alzheimer's disease: more than simple loss of terminals
Honer, W. (2003) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2003.04.005 · Cited by 135 · see citing works
Staring, a Novel E3 Ubiquitin-Protein Ligase That Targets Syntaxin 1 for Degradation
Chin, L., Vavalle, J. P., & Li, L. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m203300200 · Cited by 121 · see citing works
Ando, S., Kobayashi, S., Waki, H., Kon, K., Fukui, F., Tadenuma, T., Iwamoto, M., Takeda, Y., Izumiyama, N., Watanabe, K., et al. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10443 · Cited by 110 · see citing works
Prion protein expression in senile plaques in Alzheimer's disease
Ferrer, I., Blanco, R. E., Carmona, M., Puig, B., Ribera, R., Rey, M. J., & Ribalta, T. (2001) · Acta Neuropathologica · doi:10.1007/s004010000271 · Cited by 104 · see citing works
Kivisäkk, P., Carlyle, B. C., Sweeney, T., Quinn, J. P., Ramirez, C. E., Trombetta, B. A., Mendes, M., Brock, M., Rubel, C., Czerkowicz, J., et al. (2022) · Alzheimer's Research & Therapy · doi:10.1186/s13195-022-01002-x · Cited by 98 · see citing works
Brockington, A., Wharton, S. B., Fernando, M. S., Gelsthorpe, C., Baxter, L., Ince, P. G., Lewis, C. E., & Shaw, P. J. (2006) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/01.jnen.0000196134.51217.74 · Cited by 97 · see citing works
Functional and Pathological Effects of α-Synuclein on Synaptic SNARE Complexes
Gao, V., Briano, J. A., Komer, L. E., & Burré, J. (2022) · Journal of Molecular Biology · doi:10.1016/j.jmb.2022.167714 · Cited by 96 · see citing works
Antagonizing β-amyloid peptide neurotoxicity of the anti-aging fungus Ganoderma lucidum
Lai, C. S.-W., Yu, M.-S., Yuen, W.-H., So, K., Zee, S., & Chang, R. C. (2007) · Brain Research · doi:10.1016/j.brainres.2007.10.103 · Cited by 93 · see citing works
Synaptic protein levels altered in vascular dementia
Sinclair, L. I., Tayler, H. M., & Love, S. (2015) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12215 · Cited by 87 · see citing works
Inhibition of SNAP25 expression by HIV‐1 Tat involves the activity of mir‐128a
Eletto, D., Russo, G. M., Passiatore, G., Valle, L. D., Giordano, A., Khalili, K., Gualco, E., & Peruzzi, F. (2008) · Journal of Cellular Physiology · doi:10.1002/jcp.21452 · Cited by 78 · see citing works
Single cell gene expression profiling in Alzheimer’s disease
Ginsberg, S. D., Che, S., Counts, S., & Mufson, E. J. (2006) · NeuroRx · doi:10.1016/j.nurx.2006.05.007 · Cited by 76 · see citing works
Synaptic Pathology in Prefrontal Cortex is Present Only with Severe Dementia in Alzheimer Disease
Minger, S. L., Honer, W. G., Esiri, M. M., McDonald, B., Keene, J., Nicoll, J. A. R., Carter, J., Hope, T., & Francis, P. T. (2001) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/60.10.929 · Cited by 76 · see citing works
Synaptic Vesicle-Recycling Machinery Components as Potential Therapeutic Targets
Li, Y. C., & Kavalali, E. T. (2017) · Pharmacological Reviews · doi:10.1124/pr.116.013342 · Cited by 73 · see citing works
Anandamide Effects in a Streptozotocin-Induced Alzheimer’s Disease-Like Sporadic Dementia in Rats
Moreira‐Silva, D., Carrettiero, D. C., Oliveira, A. S., Rodrigues, S., dos Santos-Lopes, J., Canas, P. M., Cunha, R. A., Almeida, M. C., & Ferreira, T. L. (2018) · Frontiers in Neuroscience · doi:10.3389/fnins.2018.00653 · Cited by 64 · see citing works
The iTRAPs: Guardians of Synaptic Vesicle Cargo Retrieval During Endocytosis
Gordon, S. L., & Cousin, M. A. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00001 · Cited by 62 · see citing works
Nutrition and neurodevelopment: mechanisms of developmental dysfunction and disease in later life
Dauncey, M. J., & Bicknell, R. J. (1999) · Nutrition Research Reviews · doi:10.1079/095442299108728947 · Cited by 61 · see citing works
Das, S., Goossens, J., Jacobs, D., Dewit, N., Pijnenburg, Y. A. L., In ‘t Veld, S. G. J. G., Teunissen, C. E., & Vanmechelen, E. (2023) · Alzheimer's Research & Therapy · doi:10.1186/s13195-023-01212-x · Cited by 50 · see citing works
Differential Expression of Rat Brain Synaptic Proteins in Development and Aging
Shimohama, S., Fujimoto, S., Sumida, Y., Akagawa, K., Shirao, T., Matsuoka, Y., & Taniguchi, T. (1998) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1998.9480 · Cited by 57 · see citing works
Self-citationRegional alteration of synapsin I in the hippocampal formation of Alzheimer?s disease patients
Song, Q., Hu, X., Xu, H., & Zhou, J. (2004) · Acta Neuropathologica · doi:10.1007/s00401-003-0800-4 · Cited by 55 · see citing works
Sihver, W., Gillberg, P.-G., Svensson, A., & Nordberg, A. K. (1999) · Neuroscience · doi:10.1016/s0306-4522(99)00295-x · Cited by 53 · see citing works
Yoo, B. C., Cairns, N. J., Fountoulakis, M., & Lübec, G. (2001) · Dementia and Geriatric Cognitive Disorders · doi:10.1159/000051261 · Cited by 54 · see citing works
Chauhan, N. B., & Siegel, G. J. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10286 · Cited by 53 · see citing works
Furuya, T. K., Silva, P. N., Payão, S. L. M., Bertolucci, P. H. F., Rasmussen, L. T., de Lábio, R. W., Braga, I. L. S., Chen, E., Turecki, G., Mechawar, N., et al. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.06.035 · Cited by 53 · see citing works
Dysfunction of the SNARE complex in neurological and psychiatric disorders
Chen, F., Chen, H., Chen, Y., Wei, W., Sun, Y., Zhang, L., Cui, L., & Wang, Y. (2021) · Pharmacological Research · doi:10.1016/j.phrs.2021.105469 · Cited by 52 · see citing works
Wang, W., Zhao, F., Lu, Y., Siedlak, S. L., Fujioka, H., Feng, H., Perry, G. L., & Zhu, X. (2023) · Acta Neuropathologica Communications · doi:10.1186/s40478-023-01552-7 · Cited by 49 · see citing works
Kusdra, L., McGuire, D., & Pulliam, L. (2002) · AIDS · doi:10.1097/00002030-200201040-00005 · Cited by 48 · see citing works
Tremblay, C., François, A., Delay, C., Freland, L., Vandal, M., Bennett, D. A., & Calon, F. (2017) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlw109 · Cited by 44 · see citing works
Ikemoto, A., Akiguchi, I., Hirano, A., & Nakamura, S. (2002) · Acta Neuropathologica · doi:10.1007/s004010100449 · Cited by 45 · see citing works
Marksteiner, J., Lechner, T., Kaufmann, W. A., Gurka, P., Humpel, C., Nowakowski, C., Maier, H., & Jellinger, K. A. (2000) · Acta Neuropathologica · doi:10.1007/s004010000239 · Cited by 44 · see citing works
Downes, E. C., Robson, J., Grailly, E., Abdel‐All, Z., Xuereb, J. H., Brayne, C., Holland, A. J., Honer, W. G., & Mukaetova‐Ladinska, E. B. (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00899.x · Cited by 43 · see citing works
Yan, M., Zhang, S., Zhao, H., Xia, S., Jin, Z., Xu, Y., Yang, L. C., Qu, Y., Huang, S., Duan, M.-J., et al. (2020) · Cell Communication and Signaling · doi:10.1186/s12964-020-00551-8 · Cited by 40 · see citing works
Freeman, W., & Morton, A. J. (2004) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2003.12.004 · Cited by 40 · see citing works
Gene-based GWAS and biological pathway analysis of the resilience of executive functioning
Initiative, A. D. N., Mukherjee, S., Kim, S., Ramanan, V. K., Gibbons, L. E., Nho, K. T., Glymour, M. M., Ertekin‐Taner, N., Montine, T. J., Saykin, A. J., et al. (2013) · Brain Imaging and Behavior · doi:10.1007/s11682-013-9259-7 · Cited by 38 · see citing works
Kaneai, N., Arai, M., Takatsu, H., Fukui, K., & Urano, S. (2012) · Journal of Alzheimer s Disease · doi:10.3233/jad-2011-111133 · Cited by 34 · see citing works
Neuropathology of Alzheimer's Disease and its Variants
Duyckaerts, C. J., & Dickson, D. W. (2011) · Wiley eBooks · doi:10.1002/9781444341256.ch10 · Cited by 34 · see citing works
Crispino, M., Stone, D. J., Wei, M., Anderson, C. P., Tocco, G., Finch, C. E., & Baudry, M. (1999) · Experimental Neurology · doi:10.1006/exnr.1999.7186 · Cited by 33 · see citing works
Network Analysis of a Membrane-Enriched Brain Proteome across Stages of Alzheimer’s Disease
Higginbotham, L., Dammer, E., Duong, D., Modeste, E., Montine, T., Lah, J., Levey, A., & Seyfried, N. (2019) · Proteomes · doi:10.3390/proteomes7030030 · Cited by 32 · see citing works
Kartawy, M., Халиулин, И. Г., & Amal, H. (2020) · Scientific Reports · doi:10.1038/s41598-020-70383-6 · Cited by 29 · see citing works
The role of synaptic biomarkers in the spectrum of neurodegenerative diseases
Mazzucchi, S., Palermo, G., Campese, N., Galgani, A., Vecchia, A. D., Vergallo, A., Siciliano, G., Ceravolo, R., Hampel, H. J., & Baldacci, F. (2020) · Expert Review of Proteomics · doi:10.1080/14789450.2020.1831388 · Cited by 32 · see citing works
Targeting Synaptic Pathology with a Novel Affinity Mass Spectrometry Approach
Brinkmalm, A., Brinkmalm, G., Honer, W. G., Moreno, J. A., Jakobsson, J., Mallucci, G. R., Zetterberg, H., Blennow, K., & Öhrfelt, A. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.040113 · Cited by 31 · see citing works
Xia, Z., Wang, F., Zhou, S., Zhang, R., Wang, F., Huang, J. H., Wu, E., Zhang, Y., & Hu, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.17951 · Cited by 30 · see citing works
APOE ε4 is associated with higher levels of CSF SNAP-25 in prodromal Alzheimer’s disease
Wang, S., Zhang, J., & Pan, T. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.08.029 · Cited by 27 · see citing works
Serum miRNAs Expression and SNAP-25 Genotype in Alzheimer’s Disease
Agostini, S., Mancuso, R., Liuzzo, G., Bolognesi, E., Costa, A. S., Bianchi, A., & Clerici, M. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00052 · Cited by 27 · see citing works
Kitamura, Y., Tsuchiya, D., Takata, K., Shibagaki, K., Taniguchi, T., Smith, M. A., Perry, G. L., Miki, H., Takenawa, T., & Shimohama, S. (2003) · Neuroscience Letters · doi:10.1016/s0304-3940(03)00506-8 · Cited by 27 · see citing works
Self-citationNao-omi, O. M. O. I., Masaya, A. R. A. I., Saito, M., Takatsu, H., Shibata, A., Fukuzawa, K., Sato, K., Abe, K., Fukui, K., & Urano, S. (2006) · Journal of Nutritional Science and Vitaminology · doi:10.3177/jnsv.52.248 · Cited by 26 · see citing works
Qin, T., Prins, S., Groeneveld, G. J., van Westen, G. J. P., de Vries, H. E., Wong, Y. C., Bischoff, L. J. M., & de Lange, E. C. M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21093158 · Cited by 23 · see citing works
Szklarczyk, A., Conant, K. E., Owens, D. F., Ravin, R., McKay, R. D. G., & Gerfen, C. R. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.07.032 · Cited by 22 · see citing works
Aly, A., Laszlo, Z. I., Rajkumar, S., Demir, T., Hindley, N., Lamont, D. J., Lehmann, J., Seidel, M., Sommer, D., Franz-Wachtel, M., et al. (2023) · Acta Neuropathologica · doi:10.1007/s00401-023-02611-y · Cited by 21 · see citing works
Liu, Q., Liu, H., Zhang, S., Yang, Q., Shen, L. H., & Jiao, B. (2022) · Journal of Alzheimer s Disease · doi:10.3233/jad-215696 · Cited by 15 · see citing works
Clinical Utility of the Pathogenesis-Related Proteins in Alzheimer’s Disease
Zhou, B., & Fukushima, M. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21228661 · Cited by 9 · see citing works
Neuropathologie morphologique et moléculaire de la maladie d’Alzheimer
Duyckaerts, C. J., Panchal, M., Delatour, B., & Potier, M. (2009) · Annales Pharmaceutiques Françaises · doi:10.1016/j.pharma.2009.01.001 · Cited by 8 · see citing works
Aging potentiates Aβ-induced depletion of SNAP-25 in mouse hippocampus
Chauhan, N. B., Lichtor, T., & Siegel, G. J. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03011-7 · Cited by 8 · see citing works
Kivisäkk, P., Carlyle, B. C., Sweeney, T., Quinn, J. P., Ramirez, C. E., Trombetta, B. A., Mendes, M., Brock, M. J., Rubel, C. E., Czerkowicz, J., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1366881/v1 · Cited by 7 · see citing works
Effect of APOE Genotype on Synaptic Proteins in Earlier Adult Life
Sinclair, L. I., & Love, S. (2017) · Journal of Alzheimer s Disease · doi:10.3233/jad-170316 · Cited by 4 · see citing works
Kärkkäinen, E., Yavich, L., Miettinen, P. O., & Tanila, H. (2015) · Brain Research · doi:10.1016/j.brainres.2015.07.006 · Cited by 4 · see citing works
Kaneai, N., Fukui, K., Koike, T., & Urano, S. (2013) · Biological and Pharmaceutical Bulletin · doi:10.1248/bpb.b13-00147 · Cited by 4 · see citing works
Single cell gene expression profiling in Alzheimer’s disease
Ginsberg, S. D., Che, S., Counts, S., & Mufson, E. J. (2006) · Neurotherapeutics · doi:10.1007/bf03206654 · Cited by 4 · see citing works
An astrocyte-derived cytokine TIMP-1 restores synaptic plasticity in an Alzheimer’s disease modelPreprint
Sarkar, S., Gharami, K., Paidi, R. K., Srikumar, B. N., & Biswas, S. C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.18.533245 · Cited by 4 · see citing works
Le diagnostic : de la neuropathologie à l’imagerie cérébrale
Dhénain, M., Lehéricy, S., & Duyckaerts, C. J. (2002) · médecine/sciences · doi:10.1051/medsci/20021867697 · Cited by 3 · see citing works
A radioassay for synaptic core complex assembly: Screening of herbal extracts for effectors
Riley, L. G., Roufogalis, B. D., Li, G. Q., & Weiss, A. S. (2006) · Analytical Biochemistry · doi:10.1016/j.ab.2006.05.036 · Cited by 3 · see citing works
Vegh, C., Walach, G., Dube, K., Dobson, B., Talukdar, R., Wear, D., Jayawardena, H., Dufault, K., Culmone, L., Srikantha, S., et al. (2025) · Nutrients · doi:10.3390/nu17162701 · Cited by 2 · see citing works
Luo, D., Lian, T., Wei, N., Guo, P., He, M., Zhang, Y., Huang, Y. M., Liu, G., Li, J., Li, J., et al. (2025) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2025.1552535 · Cited by 2 · see citing works
Duyckaerts, C. J. (2014) · Cambridge University Press eBooks · doi:10.1017/cbo9781107588660.007 · Cited by 2 · see citing works
Greber, S., Lübec, G., Cairns, N. J., & Fountoulakis, M. (1999) · doi:10.1002/9783527613489.ch45 · Cited by 2 · see citing works
Copolymer-1 as a potential therapy for mild cognitive impairment
Abraham, D. I., Salazar, F. E., & Ibarra, A. (2022) · Brain and Cognition · doi:10.1016/j.bandc.2022.105892 · Cited by 1 · see citing works
Detection and Analysis of Synaptosis
Cole, G. M., & Gylys, K. H. (2002) · Neuromethods · doi:10.1385/1-59259-188-4:177 · Cited by 1 · see citing works
Modulation of adult neural plasticity by proteolytic catabolism of lecticans
Mayer, J. (2007) · Digital Commons - University of South Florida (University of South Florida)
Neuropathology of Alzheimer’s Disease, as Seen in Fixed Tissues
Duyckaerts, C. J., Langui, D., Girardot, N., Hauw, J., & Delatour, B. (2004) · Springer eBooks · doi:10.1007/978-3-642-59300-0_1
Kashani, A. (2006) · OpenGrey (Institut de l'Information Scientifique et Technique)
Kivisäkk, P., Carlyle, B. C., Sweeney, T., Quinn, J. P., Ramirez, C. E., Trombetta, B. A., Mendes, M., Brock, M. J., Rubel, C. E., Czerkowicz, J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19643483
Yan, M.-L., Zhang, S., Zhao, H.-M., Xia, S.-N., Jin, Z., Xu, Y., Yang, L., Qu, Y., Huang, S.-Y., Duan, M.-J., et al. (2020) · Figshare · doi:10.6084/m9.figshare.12096195
Kivisäkk, P., Carlyle, B. C., Sweeney, T., Quinn, J. P., Ramirez, C. E., Trombetta, B. A., Mendes, M., Brock, M. J., Rubel, C. E., Czerkowicz, J., et al. (2022) · Figshare · doi:10.6084/m9.figshare.19643486
Das, S., Goossens, J., Jacobs, D., Dewit, N., Pijnenburg, Y. A. L., In ‘t Veld, S. G. J. G., Teunissen, C. E., & Vanmechelen, E. (2023) · Figshare · doi:10.6084/m9.figshare.22619722
Wang, W., Zhao, F., Lu, Y., Siedlak, S. L., Fujioka, H., Feng, H., Perry, G., & Zhu, X. (2024) · Figshare · doi:10.6084/m9.figshare.26579702
Auboyer, L. (2018) · theses.fr (ABES) · doi:10.70675/07243ef7zb974z4ad8z97d9zd046801798b1
Allouche, A., Colin, J., Birck, C., Schroeder, H., Tallandier, V., Baldoni, M., Muller, C., Afrassi, M., & Violle, N. (2026) · Alzheimer s Research & Therapy · doi:10.1186/s13195-026-02051-2 · Cited by 1 · see citing works
Greber (1999) · doi:10.1002/(sici)1522-2683(19990101)20:4/5
- Authors
- Shimohama, S., Kamiya, S., Taniguchi, T., Akagawa, K., & Kimura, J.
- Affiliations
- Kyoto University (JP)
- Kyoto Pharmaceutical University (JP)
- Kyorin University (JP)
- Corresponding author
- Shimohama, Shun
- Venue
- Biochemical and Biophysical Research Communications
- Publisher
- Elsevier BV
- Published
- 1997-07
- Volume
- 236
- Issue
- 2
- Pages
- 239-242
- ISSN
- 0006-291X (ISSN-L)
- OpenAlex
- W2024626366
- Cited by
- 95
- References
- 21
- Citations by year
- 2026: 1 · 2025: 2 · 2024: 1 · 2023: 5 · 2022: 7 · 2021: 2 · 2020: 6 · 2019: 3 · 2018: 3 · 2017: 4 · 2016: 1 · 2015: 3 · 2014: 3 · 2013: 2 · 2012: 2
- FWCI
- 1.84
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Biochemical and Biophysical Research Communications (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Takeda Medical Research Foundation
- Ministry of Education, Culture, Sports, Science and Technology
- Smoking Research Foundation
- Topics
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Keywords
- Alzheimer's disease, synaptic proteins, synaptic vesicles, presynaptic plasma membrane, synaptobrevin, synaptophysin, synaptotagmin, SNAP-25, syntaxin-1, synaptic loss, cognitive decline, brain
- MeSH terms
- Alzheimer Disease, Animals, Calcium-Binding Proteins, Membrane Glycoproteins, Membrane Proteins, Nerve Tissue Proteins, Synaptic Membranes, Synaptic Vesicles, Temporal Lobe, Blotting, Western, Synaptophysin, R-SNARE Proteins, Synaptosomal-Associated Protein 25, Synaptotagmins, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review