Fluid markers of synapse degeneration in synucleinopathies
Abstract
The abnormal accumulation of α-synuclein in the brain is a common feature of Parkinson's disease (PD), PD dementia (PDD), dementia with Lewy bodies (DLB) and multiple system atrophy (MSA), and synucleinopathies that present with overlapping but distinct clinical symptoms that include motor and cognitive deficits. Synapse degeneration is the crucial neuropathological event in these synucleinopathies and the neuropathological correlate of connectome dysfunction. The cognitive and motor deficits resulting from the connectome dysfunction are currently measured by scalar systems that are limited in their sensitivity and largely subjective. Ideally, a marker of synapse degeneration would correlate with measures of cognitive or motor impairment, and could therefore be used as a more objective, surrogate biomarker of the core clinical features of these diseases. Furthermore, an objective surrogate biomarker that can detect and monitor the progression of synapse degeneration would improve patient management and clinical trial design, and could provide a measure of therapeutic response. Here, we review the published findings relating to candidate biomarkers of synapse degeneration in PD, PDD, DLB, and MSA patient-derived biofluids and discuss the findings in the context of the mechanisms associated with α-synuclein-mediated synapse degeneration. Understanding these mechanisms is essential not only for discovery of biomarkers, but also to improve our understanding of the earliest changes in disease pathogenesis of synucleinopathies.
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?
Neuronal pentraxins, including NPTX2, are involved in synaptic plasticity, and their lower levels have been reported in patients with dementia with Lewy bodies, frontotemporal dementia, and Parkinson's disease.
“Neuronal pentraxins, including NPTX2, are involved in synaptic plasticity, and their lower levels have been reported in patients with DLB, FTD, and PD as well [16].”
GluR4 is a subunit of the AMPAR complex that is present in the postsynaptic domain and is responsible for excitatory signal transmission.
“GluR4 is a subunit of the α-amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptor (AMPAR) complex that is present in the postsynaptic domain and is responsible for excitatory signal transmission [16].”
Cites
Staging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777 · see citing works
Hughes, A. J., Daniel, S. E., Kilford, L., & Lees, A. J. (1992) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp.55.3.181 · Cited by 10,378 · see citing works
Spillantini, M. G., Schmidt, M. L., Lee, V. M.-Y., Trojanowski, J. Q., Jakes, R., & Goedert, M. (1997) · Nature · doi:10.1038/42166 · Cited by 8,382 · see citing works
MDS clinical diagnostic criteria for Parkinson’s disease
Postuma, R. B., Berg, D., Stern, M., Poewe, W., Olanow, C. W., Oertel, W., Obeso, J., Marek, K., Litvan, I., Lang, A. E., et al. (2015) · Movement Disorders · doi:10.1002/mds.26424 · Cited by 7,653 · see citing works
Diagnosis and management of dementia with Lewy bodies: Third report of the DLB consortium
McKeith, I. G., Dickson, D. W., Lowe, J., Emre, M., O'Brien, J. T., Feldman, H., Cummings, J., Duda, J. E., Lippa, C., Perry, E. K., et al. (2005) · Neurology · doi:10.1212/01.wnl.0000187889.17253.b1 · Cited by 5,069 · see citing works
Diagnosis and management of dementia with Lewy bodies: Fourth consensus report of the DLB Consortium
McKeith, I. G., Boeve, B. F., Dickson, D. W., Halliday, G., Taylor, J.-P., Weintraub, D., Aarsland, D., Galvin, J., Attems, J., Ballard, C. G., et al. (2017) · Neurology · doi:10.1212/wnl.0000000000004058 · Cited by 4,476 · see citing works
McKeith, I. G., Galasko, D., Kosaka, K., Perry, E. K., Dickson, D. W., Hansen, L. A., Salmon, D. P., Lowe, J., Mirra, S. S., Byrne, E. J., et al. (1996) · Neurology · doi:10.1212/wnl.47.5.1113 · Cited by 3,960 · see citing works
Second consensus statement on the diagnosis of multiple system atrophy
Gilman, S., Wenning, G. K., Low, P. A., Brooks, D. J., Mathias, C. J., Trojanowski, J. Q., Wood, N. W., Colosimo, C., Dürr, A., Fowler, C. J., et al. (2008) · Neurology · doi:10.1212/01.wnl.0000324625.00404.15 · Cited by 3,140 · see citing works
Hyman, B. T., Phelps, C. H., Beach, T. G., Bigio, E. H., Cairns, N. J., Carrillo, M. C., Dickson, D. W., Duyckaerts, C., Frosch, M. P., Masliah, E., et al. (2012) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2011.10.007 · Cited by 3,092 · see citing works
Diagnostic Criteria for Parkinson Disease
Gelb, D. J., Oliver, E., & Gilman, S. (1999) · Archives of Neurology · doi:10.1001/archneur.56.1.33 · Cited by 2,822 · see citing works
α-Synuclein Promotes SNARE-Complex Assembly in Vivo and in Vitro
Burré, J., Sharma, M., Tsetsenis, T., Buchman, V. L., Etherton, M. R., & Südhof, T. C. (2010) · Science · doi:10.1126/science.1195227 · Cited by 1,817 · see citing works
Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal
Maroteaux, L., Campanelli, J., & Scheller, R. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-08-02804.1988 · Cited by 1,646 · see citing works
(1998) · Europe PMC (PubMed Central) · Cited by 1,594 · see citing works
Consensus statement on the diagnosis of multiple system atrophy
Gilman, S., Low, P. A., Quinn, N. P., Albanese, A., Ben‐Shlomo, Y., Fowler, C. J., Kaufmann, H., Klockgether, T., Lang, A. E., Lantos, P. L., et al. (1998) · Clinical Autonomic Research · doi:10.1007/bf02309628 · Cited by 1,316 · see citing works
Nemani, V. M., Lü, W., Berge‐Seidl, V., Nakamura, K., Onoa, B., Lee, M. K., Chaudhry, F. A., Nicoll, R. A., & Edwards, R. H. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.023 · Cited by 1,051 · see citing works
Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria
Dickson, D. W., Braak, H., Duda, J. E., Duyckaerts, C., Gasser, T., Halliday, G. M., Hardy, J., Leverenz, J. B., Del Tredici, K., Wszolek, Z. K., et al. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70238-8 · Cited by 972 · see citing works
SynGO: An Evidence-Based, Expert-Curated Knowledge Base for the Synapse
Koopmans, F., van Nierop, P., Andres-Alonso, M., Byrnes, A., Cijsouw, T., Coba, M. P., Cornelisse, L. N., Farrell, R. J., Goldschmidt, H. L., Howrigan, D. P., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.002 · Cited by 938 · see citing works
Research criteria for the diagnosis of prodromal dementia with Lewy bodies
McKeith, I. G., Ferman, T. J., Thomas, A. J., Blanc, F., Boeve, B. F., Fujishiro, H., Kantarci, K., Muscio, C., O'Brien, J. T., Postuma, R. B., et al. (2020) · Neurology · doi:10.1212/wnl.0000000000009323 · Cited by 782 · see citing works
Update of the MDS research criteria for prodromal Parkinson's disease
Heinzel, S., Berg, D., Gasser, T., Chen, H., Yao, C. W., Postuma, R. B., & the MDS Task Force on the Definition of Parkinson's Disease (2019) · Movement Disorders · doi:10.1002/mds.27802 · Cited by 779 · see citing works
Zinc in the physiology and pathology of the CNS
Sensi, S. L., Paoletti, P., Bush, A. I., & Sekler, I. (2009) · Nature Reviews Neuroscience · doi:10.1038/nrn2734 · Cited by 759 · see citing works
Mahul-Mellier, A.-L., Burtscher, J., Maharjan, N., Weerens, L., Croisier, M., Kuttler, F., Leleu, M., Knott, G. W., & Lashuel, H. A. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1913904117 · Cited by 710 · see citing works
ZnT-3, a putative transporter of zinc into synaptic vesicles
Palmiter, R. D., Cole, T. B., Quaife, C. J., & Findley, S. D. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.25.14934 · Cited by 708 · see citing works
the Arizona Parkinson’s Disease Consortium, Beach, T. G., Adler, C. H., Lue, L., Sue, L. I., Bachalakuri, J., Henry-Watson, J., Sasse, J., Boyer, S., Shirohi, S., et al. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0538-8 · Cited by 698 · see citing works
Dementia associated with Parkinson's disease
Emre, M. (2003) · The Lancet Neurology · doi:10.1016/s1474-4422(03)00351-x · Cited by 686 · see citing works
High-Affinity Zinc Inhibition of NMDA NR1–NR2A Receptors
Paoletti, P., Ascher, P., & Neyton, J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05711.1997 · Cited by 650 · see citing works
Fairfoul, G., McGuire, L. I., Pal, S., Ironside, J. W., Neumann, J., Christie, S., Joachim, C., Esiri, M., Evetts, S. G., Rolinski, M., et al. (2016) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.338 · Cited by 608 · see citing works
Modified hippocampal long-term potentiation in PKCγ-mutant mice
Abeliovich, A., Chen, C., Goda, Y., Silva, A. J., Stevens, C. F., & Tonegawa, S. (1993) · Cell · doi:10.1016/0092-8674(93)90613-u · Cited by 524 · see citing works
EFNS / MDS ‐ ES recommendations for the diagnosis of P arkinson's disease
Berardelli, A., Wenning, G. K., Antonini, A., Berg, D., Bloem, B. R., Bonifati, V., Brooks, D. J., Burn, D. J., Colosimo, C., Fanciulli, A., et al. (2012) · European Journal of Neurology · doi:10.1111/ene.12022 · Cited by 491 · see citing works
Shahnawaz, M., Tokuda, T., Waragai, M., Méndez, N., Ishii, R., Trenkwalder, C., Mollenhauer, B., & Soto, C. A. (2016) · JAMA Neurology · doi:10.1001/jamaneurol.2016.4547 · Cited by 485 · see citing works
Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product narp.
O’Brien, R. J., Xu, D., Petralia, R. S., Steward, O., Huganir, R. L., & Worley, P. (1999) · Neuron · doi:10.1016/s0896-6273(00)80782-5 · Cited by 471 · see citing works
β-Synuclein Inhibits α-Synuclein Aggregation
Hashimoto, M., Rockenstein, E., Mante, M., Mallory, M., & Masliah, E. (2001) · Neuron · doi:10.1016/s0896-6273(01)00462-7 · Cited by 398 · see citing works
Proposed neuropathological criteria for the <i>post mortem</i> diagnosis of multiple system atrophy
Trojanowski, J. Q., Revesz, T., & the Neuropathology Working Group on MSA (2007) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2007.00907.x · Cited by 349 · see citing works
Pissadaki, E. K., & Bolam, J. P. (2013) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2013.00013 · Cited by 349 · see citing works
Neuropathological spectrum of synucleinopathies
Jellinger, K. A. (2003) · Movement Disorders · doi:10.1002/mds.10557 · Cited by 338 · see citing works
C-terminal calcium binding of α-synuclein modulates synaptic vesicle interaction
Lautenschläger, J., Stephens, A. D., Fusco, G., Ströhl, F., Curry, N., Zacharopoulou, M., Michel, C. H., Laine, R. F., Nespovitaya, N., Fantham, M., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-03111-4 · Cited by 335 · see citing works
Copper(II)-induced self-oligomerization of α-synuclein
Paik, S. R., Shin, H.-J., Lee, J., Chang, C., & Kim, J. (1999) · Biochemical Journal · doi:10.1042/bj3400821 · Cited by 332 · see citing works
Tsui, C., Copeland, N., Gilbert, D., Jenkins, N., Barnes, C., & Worley, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02463.1996 · Cited by 315 · see citing works
Concomitant loss of dynorphin, NARP, and orexin in narcolepsy
Crocker, A., España, R. A., Papadopoulou, M., Saper, C. B., Faraco, J., Sakurai, T., Honda, M., Mignot, E., & Scammell, T. E. (2005) · Neurology · doi:10.1212/01.wnl.0000168173.71940.ab · Cited by 301 · see citing works
SNARE protein redistribution and synaptic failure in a transgenic mouse model of Parkinson’s disease
Garcia-Reitboeck, P., Anichtchik, O. V., Bellucci, A., Iovino, M., Ballini, C., Fineberg, E., Ghetti, B. F., Corte, L., Spano, P., Tofaris, G. K., et al. (2010) · Brain · doi:10.1093/brain/awq132 · Cited by 293 · see citing works
Xu, D., Hopf, C., Reddy, R., Cho, R. W., Guo, L., Lanahan, A., Petralia, R. S., Wenthold, R. J., O'Brien, R. J., & Worley, P. (2003) · Neuron · doi:10.1016/s0896-6273(03)00463-x · Cited by 265 · see citing works
Magdalinou, N. K., Paterson, R. W., Schott, J. M., Fox, N. C., Mummery, C. J., Blennow, K., Bhatia, K. P., Morris, H. R., Giunti, P., Warner, T. T., et al. (2015) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2014-309562 · Cited by 250 · see citing works
Denny, J. B. (2006) · Current Neuropharmacology · doi:10.2174/157015906778520782 · Cited by 244 · see citing works
Sjögren, M. J. C., Minthon, L., Davidsson, P., Granérus, A., Clarberg, A., Vanderstichele, H., Vanmechelen, E., Wallin, A., & Blennow, K. (2000) · Journal of Neural Transmission · doi:10.1007/s007020070079 · Cited by 237 · see citing works
Increased CSF neurogranin concentration is specific to Alzheimer disease
Wellington, H., Paterson, R. W., Portelius, E., Törnqvist, U., Magdalinou, N., Fox, N. C., Blennow, K., Schott, J. M., & Zetterberg, H. (2016) · Neurology · doi:10.1212/wnl.0000000000002423 · Cited by 232 · see citing works
Microglia affect α-synuclein cell-to-cell transfer in a mouse model of Parkinson’s disease
George, S., Rey, N. L., Tyson, T., Esquibel, C., Meyerdirk, L., Schulz, E., Pierce, S., Burmeister, A. R., Madaj, Z., Steiner, J. A., et al. (2019) · Molecular Neurodegeneration · doi:10.1186/s13024-019-0335-3 · Cited by 229 · see citing works
Copper Ions and Parkinson’s Disease: Why Is Homeostasis So Relevant?
Bisaglia, M., & Bubacco, L. (2020) · Biomolecules · doi:10.3390/biom10020195 · Cited by 226 · see citing works
Eusebi, P., Giannandrea, D., Biscetti, L., Abraha, I., Chiasserini, D., Orso, M., Calabresi, P., & Parnetti, L. (2017) · Movement Disorders · doi:10.1002/mds.27110 · Cited by 222 · see citing works
Synaptic markers of cognitive decline in neurodegenerative diseases: a proteomic approach
Bereczki, E., Branca, R. M., Francis, P. T., Pereira, J. B., Baek, J.-H., Hortobágyi, T., Winblad, B., Ballard, C., Lehtiö, J., & Aarsland, D. (2018) · Brain · doi:10.1093/brain/awx352 · Cited by 220 · see citing works
Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression.
Berglund, E., Murai, K., Fredette, B., Sekerkovâ, G., Marturano, B., Weber, L., Mugnaini, E., & Ranscht, B. (1999) · Neuron · doi:10.1016/s0896-6273(00)81126-5 · Cited by 216 · see citing works
He, Q., Dent, E. W., & Meiri, K. F. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-10-03515.1997 · Cited by 216 · see citing works
Prots, I., Grosch, J., Brazdis, R.-M., Simmnacher, K., Veber, V., Havlicek, S., Hannappel, C., Krach, F., Krumbiegel, M., Schütz, O., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713129115 · Cited by 213 · see citing works
Gao, L., Tang, H., Nie, K., Wang, L., Zhao, J., Gan, R., Huang, J., Zhu, R., Feng, S., Duan, Z., et al. (2014) · International Journal of Neuroscience · doi:10.3109/00207454.2014.961454 · Cited by 204 · see citing works
Review: Parkinson's disease: from synaptic loss to connectome dysfunction
Bellucci, A., Mercuri, N. B., Venneri, A., Faustini, G., Longhena, F., Pizzi, M., Missale, C., & Spano, P. (2015) · Neuropathology and Applied Neurobiology · doi:10.1111/nan.12297 · Cited by 203 · see citing works
Cerebrospinal Fluid Patterns and the Risk of Future Dementia in Early, Incident Parkinson Disease
Bäckström, D. C., Domellöf, M. E., Linder, J., Olsson, B., Öhrfelt, A., Trupp, M., Zetterberg, H., Blennow, K., & Forsgren, L. (2015) · JAMA Neurology · doi:10.1001/jamaneurol.2015.1449 · Cited by 197 · see citing works
Holahan, M. R. (2017) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2017.00266 · Cited by 197 · see citing works
SNAP-25 Palmitoylation and Plasma Membrane Targeting Require a Functional Secretory Pathway
Gonzalo, S., & Linder, M. E. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.3.585 · Cited by 196 · see citing works
Elevated CSF GAP‐43 is Alzheimer's disease specific and associated with tau and amyloid pathology
Sandelius, Å., Portelius, E., Källén, Å., Zetterberg, H., Rot, U., Olsson, B., Toledo, J. B., Shaw, L. M. J., Lee, V. M. ‐., Irwin, D. J., et al. (2018) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2018.08.006 · Cited by 191 · see citing works
Diagnostic value of cerebrospinal fluid alpha-synuclein seed quantification in synucleinopathies
Poggiolini, I., Gupta, V., Lawton, M., Lee, S., El-Turabi, A., Querejeta-Coma, A., Trenkwalder, C., Sixel-Döring, F., Foubert-Samier, A., Pavy-Le Traon, A., et al. (2022) · Brain · doi:10.1093/brain/awab431 · Cited by 191 · see citing works
How to diagnose dementia with Lewy bodies: State of the art
Geser, F., Wenning, G. K., Poewe, W. H., & McKeith, I. G. (2005) · Movement Disorders · doi:10.1002/mds.20535 · Cited by 184 · see citing works
Improving diagnostic accuracy of multiple system atrophy: a clinicopathological study
Miki, Y., Foti, S. C., Asi, Y. T., Tsushima, E., Quinn, N. P., Ling, H., & Holton, J. L. (2019) · Brain · doi:10.1093/brain/awz189 · Cited by 181 · see citing works
Synaptic Changes in Parkinson Disease Assessed with in vivo Imaging
Matuskey, D., Tinaz, S., Wilcox, K. C., Naganawa, M., Toyonaga, T., Dias, M., Henry, S. E., Pittman, B. P., Ropchan, J. R., Nabulsi, N., et al. (2020) · Annals of Neurology · doi:10.1002/ana.25682 · Cited by 180 · see citing works
Dekker, L. V., Graan, P. N. E. D., Versteeg, D. H. G., et al. (1989) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1989.tb10893.x · Cited by 179 · see citing works
Cerebrospinal fluid neurogranin and <scp>YKL</scp> ‐40 as biomarkers of Alzheimer's disease
Janelidze, S., Hertze, J., Zetterberg, H., Landqvist Waldö, M., Santillo, A., Blennow, K., & Hansson, O. (2016) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.266 · Cited by 179 · see citing works
Differential role of CSF alpha-synuclein species, tau, and Aβ42 in Parkinson's Disease
Parnetti, L., Farotti, L., Eusebi, P., Chiasserini, D., Carlo, C. D., Giannandrea, D., Salvadori, N., Lisetti, V., Tambasco, N., Rossi, A., et al. (2014) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2014.00053 · Cited by 177 · see citing works
Sorrentino, Z. A., Giasson, B. I., & Chakrabarty, P. (2019) · Acta Neuropathologica · doi:10.1007/s00401-019-01977-2 · Cited by 177 · see citing works
Multiscale causal networks identify VGF as a key regulator of Alzheimer’s disease
Beckmann, N. D., Lin, W.-J., Wang, M., Cohain, A. T., Charney, A. W., Wang, P., Ma, W., Wang, Y.-C., Jiang, C., Audrain, M., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-17405-z · Cited by 172 · see citing works
Synaptic failure and α‐synuclein
Calò, L., Węgrzynowicz, M., Santivañez‐Perez, J., & Spillantini, M. G. (2016) · Movement Disorders · doi:10.1002/mds.26479 · Cited by 170 · see citing works
Synaptic proteins predict cognitive decline in Alzheimer's disease and Lewy body dementia
Bereczki, E., Francis, P. T., Howlett, D., Pereira, J. B., Höglund, K., Bogstedt, A., Cedazo‐Minguez, A., Baek, J., Hortobágyi, T., Attems, J., et al. (2016) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2016.04.005 · Cited by 167 · see citing works
Portelius, E., Olsson, B., Höglund, K., Cullen, N. C., Kvartsberg, H., Andréasson, U., Zetterberg, H., Sandelius, Å., Shaw, L. M. J., Lee, V. M. ‐., et al. (2018) · Acta Neuropathologica · doi:10.1007/s00401-018-1851-x · Cited by 167 · see citing works
Multiple system atrophy: a clinical and neuropathological perspective
Ubhi, K. K., Low, P. A., & Masliah, E. (2011) · Trends in Neurosciences · doi:10.1016/j.tins.2011.08.003 · Cited by 159 · see citing works
Roles of Glutamate Receptors in Parkinson’s Disease
Zhang, Z., Zhang, S., Fu, P., Zhang, Z., Lin, K., Ko, J. K.-S., & Yung, K. K. L. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20184391 · Cited by 159 · see citing works
Vos, A. D., Jacobs, D., Struyfs, H., Fransén, E., Andersson, K., Portelius, E., Andréasson, U., Surgeloose, D. D., Hernalsteen, D., Sleegers, K., et al. (2015) · Alzheimer s & Dementia · doi:10.1016/j.jalz.2015.05.012 · Cited by 158 · see citing works
α‐Synuclein RT‐QuIC assay in cerebrospinal fluid of patients with dementia with Lewy bodies
Bongianni, M., Ladogana, A., Capaldi, S., Klotz, S., Baiardi, S., Cagnin, A., Perra, D., Fiorini, M., Poleggi, A., Legname, G., et al. (2019) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.50897 · Cited by 155 · see citing works
Activity-Regulated N-Cadherin Endocytosis
Tai, C., Mysore, S. P., Chiu, C., & Schuman, E. M. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.013 · Cited by 153 · see citing works
Longitudinal CSF biomarkers in patients with early Parkinson disease and healthy controls
Mollenhauer, B., Caspell‐Garcia, C., Coffey, C. S., Taylor, P., Shaw, L. M. J., Trojanowski, J. Q., Singleton, A. B., Frasier, M. A., Marek, K., Galasko, D. R., et al. (2017) · Neurology · doi:10.1212/wnl.0000000000004609 · Cited by 153 · see citing works
Monitoring of 30 marker candidates in early Parkinson disease as progression markers
Mollenhauer, B., Zimmermann, J., Sixel‐Döring, F., Focke, N. K., Wicke, T., Ebentheuer, J., Schaumburg, M., Lang, E., Trautmann, E., Zetterberg, H., et al. (2016) · Neurology · doi:10.1212/wnl.0000000000002651 · Cited by 151 · see citing works
Biochemical Interactions of the Neuronal Pentraxins
Kirkpatrick, L., Matzuk, M. M., Dodds, D. C., & Perin, M. S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002254200 · Cited by 149 · see citing works
Presynaptic neuronal pentraxin receptor organizes excitatory and inhibitory synapses
Lee, S.-J., Wei, M., Zhang, C., Maxeiner, S., Pak, C., Calado Botelho, S., Trotter, J., Sterky, F. H., & Südhof, T. C. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2768-16.2016 · Cited by 146 · see citing works
Wennström, M., Surova, Y., Hall, S., Nilsson, C., Minthon, L., Boström, F., Hansson, O., & Nielsen, H. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0053250 · Cited by 141 · see citing works
Oeckl, P., Metzger, F., Nagl, M., Arnim, C. A. F. V., Halbgebauer, S., Steinacker, P., Ludolph, A. C., & Otto, M. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m116.059915 · Cited by 135 · see citing works
Quadalti, C., Buonaura, G. C., Baiardi, S., Mastrangelo, A., Rossi, M., Zenesini, C., Giannini, G., Candelise, N., Sambati, L., Polischi, B., et al. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00232-4 · Cited by 133 · see citing works
Brockmann, K., Quadalti, C., Lerche, S., Rossi, M., Wurster, I., Baiardi, S., Röeben, B., Mammana, A., Zimmermann, M., Hauser, A., et al. (2021) · Acta Neuropathologica Communications · doi:10.1186/s40478-021-01276-6 · Cited by 132 · see citing works
Singer, W., Schmeichel, A. M., Shahnawaz, M., Schmelzer, J. D., Boeve, B. F., Sletten, D. M., Gehrking, T. L., Gehrking, J. A., Olson, A. D., Savica, R., et al. (2020) · Annals of Neurology · doi:10.1002/ana.25824 · Cited by 131 · see citing works
Brain region‐dependent differential expression of alpha‐synuclein
Taguchi, K., Watanabe, Y., Tsujimura, A., & Tanaka, M. (2015) · The Journal of Comparative Neurology · doi:10.1002/cne.23901 · Cited by 124 · see citing works
Peraza, L. R., Kaiser, M., Firbank, M., Graziadio, S., Bonanni, L., ONOFRJ, M. C., Colloby, S. J., Blamire, A. M., O'Brien, J. T., & Taylor, J. (2014) · NeuroImage Clinical · doi:10.1016/j.nicl.2014.03.013 · Cited by 121 · see citing works
Durante, V., de Iure, A., Loffredo, V., Vaikath, N. N., Risi, M. D., Paciotti, S., Quiroga‐Varela, A., Chiasserini, D., Mellone, M., Mazzocchetti, P., et al. (2019) · Brain · doi:10.1093/brain/awz065 · Cited by 117 · see citing works
Angiotensinogen Gene and Blood Pressure in the Japanese Population
Iwai, N., Shimoike, H., Ohmichi, N., et al. (1995) · Hypertension · doi:10.1161/01.hyp.25.4.688 · Cited by 113 · see citing works
α-Synuclein and Its A30P Mutant Affect Actin Cytoskeletal Structure and Dynamics
Sousa, V. L., Bellani, S., Giannandrea, M., Yousuf, M., Valtorta, F., Meldolesi, J., & Chieregatti, E. (2009) · Molecular Biology of the Cell · doi:10.1091/mbc.e08-03-0302 · Cited by 112 · see citing works
Olanow, C. W., Savolainen, M., Chu, Y., Halliday, G. M., & Kordower, J. H. (2019) · Brain · doi:10.1093/brain/awz104 · Cited by 112 · see citing works
Rossi, M., Baiardi, S., Teunissen, C. E., Quadalti, C., Beek, M. H. C. T. V., Mammana, A., Maserati, M. S., van der Flier, W. M., Sambati, L., Zenesini, C., et al. (2021) · Neurology · doi:10.1212/wnl.0000000000012438 · Cited by 111 · see citing works
Agliardi, C., Meloni, M., Guerini, F. R., Zanzottera, M., Bolognesi, E., Baglio, F., & Clerici, M. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.105185 · Cited by 106 · see citing works
Alpha-synuclein activates BV2 microglia dependent on its aggregation state
Hoffmann, A., Ettle, B., Bruno, A., Kulinich, A. O., Hoffmann, A.-C., von Wittgenstein, J., Winkler, J., Xiang, W., & Schlachetzki, J. C. M. (2016) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2016.09.109 · Cited by 105 · see citing works
α‐Synuclein species as potential cerebrospinal fluid biomarkers for dementia with lewy bodies
van Steenoven, I., Majbour, N. K., Vaikath, N. N., Berendse, H. W., van der Flier, W. M., van de Berg, W. D. J., Teunissen, C. E., Lemstra, A. W., & El‐Agnaf, O. M. A. (2018) · Movement Disorders · doi:10.1002/mds.111 · Cited by 103 · see citing works
Endogenous Zinc Inhibits GABAAReceptors in a Hippocampal Pathway
Ruiz, A. J., Walker, M. C., Fabian‐Fine, R., & Kullmann, D. M. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00755.2003 · Cited by 100 · see citing works
Remnestål, J., Just, D., Mitsios, N., Fredolini, C., Mulder, J., Schwenk, J. M., Uhlén, M., Kultima, K., Ingelsson, M., Kilander, L., et al. (2016) · PROTEOMICS - CLINICAL APPLICATIONS · doi:10.1002/prca.201500150 · Cited by 97 · see citing works
Loss of Presynaptic Terminal Integrity in the Substantia Nigra in Early Parkinson's Disease
Delva, A., Weehaeghe, D. V., Koole, M. J. B., Laere, K. V., & Vandenberghe, W. (2020) · Movement Disorders · doi:10.1002/mds.28216 · Cited by 97 · see citing works
Resting-state fMRI study on drug-naive patients with Parkinson's disease and with depression
Luo, C., Chen, Q., Song, W., Chen, K., Guo, X., Yang, J., Huang, X., Gong, Q., & Shang, H. (2013) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2013-306237 · Cited by 92 · see citing works
Lou, X., Kim, J., Hawk, B. J. D., & Shin, Y. (2017) · Biochemical Journal · doi:10.1042/bcj20170200 · Cited by 91 · see citing works
Targeted Mass Spectrometry Suggests Beta-Synuclein as Synaptic Blood Marker in Alzheimer’s Disease
Oeckl, P., Halbgebauer, S., Anderl‐Straub, S., Arnim, C. A. F. V., Diehl‐Schmid, J., Froelich, L., Grimmer, T., Hausner, L., Denk, J., Jahn, H., et al. (2020) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00824 · Cited by 91 · see citing works
Andersen, K. B., Hansen, A. K., Damholdt, M. F., Horsager, J., Skjærbæk, C., Gottrup, H., Klit, H., Schacht, A. C., Danielsen, E. H., Brooks, D. J., et al. (2021) · Movement Disorders · doi:10.1002/mds.28617 · Cited by 84 · see citing works
Khundakar, A. A., Hanson, P. S., Erskine, D., Lax, N. Z., Roscamp, J., Karyka, E., Tsefou, E., Singh, P., Cockell, S., Gribben, A., et al. (2016) · Acta Neuropathologica Communications · doi:10.1186/s40478-016-0334-3 · Cited by 83 · see citing works
Zhao, B., Tang, Y., Zhang, B., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms21010299 · Cited by 83 · see citing works
van Steenoven, I., Koel-Simmelink, M. J. A., Vergouw, L. J. M., Tijms, B. M., Piersma, S. R., Pham, T. V., Bridel, C., Ferri, G.-L., Cocco, C., Noli, B., et al. (2020) · Molecular Neurodegeneration · doi:10.1186/s13024-020-00388-2 · Cited by 83 · see citing works
Cocco, C., D’Amato, F., Noli, B., Ledda, A., Brancia, C., Bongioanni, P., & Ferri, G. (2010) · Journal of Anatomy · doi:10.1111/j.1469-7580.2010.01309.x · Cited by 75 · see citing works
Synaptic proteins in CSF relate to Parkinson’s disease stage markers
Bereczki, E., Bogstedt, A., Höglund, K., Tsitsi, P., Brodin, L., Ballard, C., Svenningsson, P., & Aarsland, D. (2017) · npj Parkinson's Disease · doi:10.1038/s41531-017-0008-2 · Cited by 72 · see citing works
Lowther, E. R., O'Brien, J. T., Firbank, M., & Blamire, A. M. (2014) · Psychiatry Research Neuroimaging · doi:10.1016/j.pscychresns.2014.06.004 · Cited by 71 · see citing works
Synaptic Zinc: An Emerging Player in Parkinson’s Disease
Sikora, J., & Ouagazzal, A. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22094724 · Cited by 71 · see citing works
Reduced alpha‐synuclein in cerebrospinal fluid in synucleinopathies: Evidence from a meta‐analysis
Sako, W., Murakami, N., Izumi, Y., et al. (2014) · Movement Disorders · doi:10.1002/mds.26036 · Cited by 70 · see citing works
Moran, L. B., Hickey, L., Michael, G. J., Derkacs, M., Christian, L. M., Kalaitzakis, M. E., Pearce, R. K. B., & Graeber, M. B. (2008) · Acta Neuropathologica · doi:10.1007/s00401-007-0309-3 · Cited by 69 · see citing works
Fu, Y., & Huang, Z. J. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1011233108 · Cited by 68 · see citing works
Relevance of presynaptic actin dynamics for synapse function and mouse behavior
Rust, M. B., & Maritzen, T. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2014.12.020 · Cited by 66 · see citing works
Prodynorphin storage and processing in axon terminals and dendrites
Yakovleva, T., Bazov, I., Cebers, G., et al. (2006) · The FASEB Journal · doi:10.1096/fj.06-6174fje · Cited by 66 · see citing works
Zhou, B., Wen, M., Yu, W., Zhang, C., & Jiao, L. (2015) · Parkinson s Disease · doi:10.1155/2015/567386 · Cited by 65 · see citing works
Wang, Z., Danscher, G., Kim, Y. K., et al. (2002) · Neuroscience Letters · doi:10.1016/s0304-3940(01)02560-5 · Cited by 64 · see citing works
Order and disorder in the physiological membrane binding of α-synuclein
Fusco, G., Sanz-Hernández, M., & Simone, A. D. (2017) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2017.09.004 · Cited by 64 · see citing works
Parkinson’s disease dementia: Diagnostic criteria and risk factor review
Vasconcellos, L. F., & Pereira, J. S. (2015) · Journal of Clinical and Experimental Neuropsychology · doi:10.1080/13803395.2015.1073227 · Cited by 61 · see citing works
Sourty, M., Thoraval, L., Roquet, D., Armspach, J., Foucher, J., & Blanc, F. (2016) · Frontiers in Computational Neuroscience · doi:10.3389/fncom.2016.00060 · Cited by 60 · see citing works
Beta-synuclein in cerebrospinal fluid as an early diagnostic marker of Alzheimer’s disease
Halbgebauer, S., Oeckl, P., Steinacker, P., et al. (2020) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp-2020-324306 · Cited by 60 · see citing works
Stoeckli, E. T. (2010) · Cell Adhesion & Migration · doi:10.4161/cam.4.4.12733 · Cited by 55 · see citing works
SNARE Regulatory Proteins in Synaptic Vesicle Fusion and Recycling
Sauvola, C. W., & Littleton, J. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.733138 · Cited by 53 · see citing works
Dependence of the histofluorescently reactive zinc pool on zinc transporter-3 in the normal brain
Lee, J. Y., Kim, J. S., Byun, H.-R., et al. (2011) · Brain Research · doi:10.1016/j.brainres.2011.08.055 · Cited by 52 · see citing works
Dynamic Control of Synaptic Adhesion and Organizing Molecules in Synaptic Plasticity
Rudenko, G. (2017) · Neural Plasticity · doi:10.1155/2017/6526151 · Cited by 52 · see citing works
Lopantsev, V., Wenzel, H. J., Cole, T. B., Palmiter, R. D., & Schwartzkroin, P. A. (2003) · Neuroscience · doi:10.1016/s0306-4522(02)00570-5 · Cited by 51 · see citing works
F3/Contactin promotes hippocampal neurogenesis, synaptic plasticity, and memory in adult mice
Puzzo, D., Bizzoca, A., Privitera, L., Furnari, D., Giunta, S., Girolamo, F., Pinto, M. F., Gennarini, G., & Palmeri, A. (2013) · Hippocampus · doi:10.1002/hipo.22186 · Cited by 51 · see citing works
Alterations in peptide levels in Parkinson's disease and incidental Lewy body disease
Fernandez, A., CEBALLOS, M. L. D., Rose, S., et al. (1996) · Brain · doi:10.1093/brain/119.3.823 · Cited by 50 · see citing works
Cadherin-Based Transsynaptic Networks in Establishing and Modifying Neural Connectivity
Friedman, L. G., Benson, D. L., & Huntley, G. W. (2015) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2014.11.025 · Cited by 47 · see citing works
Soldan, A., Moghekar, A., Walker, K. A., Pettigrew, C. A., Hou, X., Lu, H., Miller, M. I., Alfini, A. J., Albert, M., Xu, D., et al. (2019) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2019.00132 · Cited by 46 · see citing works
Anantharam, A., Axelrod, D., & Holz, R. W. (2012) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2012.07816.x · Cited by 42 · see citing works
VGF Peptides in Cerebrospinal Fluid of Patients with Dementia with Lewy Bodies
van Steenoven, I., Noli, B., Cocco, C., Ferri, G., Oeckl, P., Otto, M., Koel‐Simmelink, M. J. A., Bridel, C., van der Flier, W. M., Lemstra, A. W., et al. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20194674 · Cited by 42 · see citing works
Boiten, W., van Steenoven, I., Xiao, M.-F., Worley, P., Noli, B., Cocco, C., Ferri, G.-L., Lemstra, A., & Teunissen, C. (2020) · Cells · doi:10.3390/cells10010038 · Cited by 42 · see citing works
Beyer, K., Domingo-Sàbat, M., dos Santos, C. M. P., TOLOSA, E. S., Ferrer, I., & Ariza, A. (2010) · Brain · doi:10.1093/brain/awq275 · Cited by 41 · see citing works
McCormack, A., Keating, D. J., Chegeni, N., et al. (2019) · Neurotoxicity Research · doi:10.1007/s12640-019-00014-0 · Cited by 37 · see citing works
Cerebrospinal Fluid Levels of Neurogranin in Parkinsonian Disorders
Hall, S., Janelidze, S., Zetterberg, H., Brix, B., Mattsson, N., Surova, Y., Blennow, K., & Hansson, O. (2019) · Movement Disorders · doi:10.1002/mds.27950 · Cited by 36 · see citing works
Synaptic adhesion molecule OBCAM; synaptogenesis and dynamic internalization
Yamada, M., Hashimoto, T., Hayashi, N., Higuchi, M., Murakami, A., Nakashima, T., Maékawa, S., & Miyata, S. (2007) · Brain Research · doi:10.1016/j.brainres.2007.04.062 · Cited by 34 · see citing works
Dynamin−SNARE interactions control trans-SNARE formation in intracellular membrane fusion
Alpadi, K., Kulkarni, A., Namjoshi, S., et al. (2013) · Nature Communications · doi:10.1038/ncomms2724 · Cited by 33 · see citing works
Chatterjee, M., del Campo, M., Morrema, T. H. J., de Waal, M. W. J., van der Flier, W. M., Hoozemans, J. J. M., & Teunissen, C. E. (2018) · Alzheimer s Research & Therapy · doi:10.1186/s13195-018-0383-x · Cited by 33 · see citing works
Impaired synaptic function is linked to cognition in Parkinson's disease
Selnes, P., Stav, A. L., Johansen, K. K., Bjørnerud, A., Coello, C. S., Auning, E., Kalheim, L. F., Almdahl, I. S., Hessen, E., Zetterberg, H., et al. (2017) · Annals of Clinical and Translational Neurology · doi:10.1002/acn3.446 · Cited by 31 · see citing works
Mobilization of the cell adhesion glycoprotein F3/contactin to axonal surfaces is activity dependent
Pierre, K., Dupouy, B., Michèle Allard, A., Poulain, D. A., & Theodosis, D. T. (2001) · European Journal of Neuroscience · doi:10.1046/j.0953-816x.2001.01682.x · Cited by 30 · see citing works
11C-UCB-J synaptic PET and multimodal imaging in dementia with Lewy bodies
Nicastro, N., Holland, N., Savulich, G., Carter, S. F., Mak, E., Hong, Y. T., Milicevic Sephton, S., Fryer, T. D., Aigbirhio, F. I., Rowe, J. B., et al. (2020) · European Journal of Hybrid Imaging · doi:10.1186/s41824-020-00093-9 · Cited by 28 · see citing works
Koob, A. O., Shaked, G. M., Bender, A., Bisquertt, A., Rockenstein, E. M., & Masliah, E. (2014) · Brain Research · doi:10.1016/j.brainres.2014.10.013 · Cited by 25 · see citing works
Vallortigara, J., Rangarajan, S., Whitfield, D., Alghamdi, A. A., Howlett, D. R., Hortobágyi, T., Johnson, M. A., Attems, J., Ballard, C. G., Thomas, A. J., et al. (2014) · F1000Research · doi:10.12688/f1000research.3786.1 · Cited by 25 · see citing works
Chatterjee, M., van Steenoven, I., Huisman, E., Oosterveld, L. P., Berendse, H. W., van der Flier, W. M., del Campo, M., Lemstra, A. W., van de Berg, W. D. J., & Teunissen, C. E. (2020) · Biomolecules · doi:10.3390/biom10081177 · Cited by 25 · see citing works
Ninkina, N. N., Millership, S. J., Peters, O. M., Connor‐Robson, N., Chaprov, K., Kopylov, A. T., Montoya, A., Kramer, H., Withers, D. J., & Buchman, V. L. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101375 · Cited by 25 · see citing works
Sevlever, D., Zou, F., Ma, L., Carrasquillo, S., Crump, M., Culley, O. J., Hunter, T. A., Bisceglio, G. D., Younkin, L. H., Allen, M., et al. (2015) · Molecular Neurodegeneration · doi:10.1186/s13024-015-0015-x · Cited by 22 · see citing works
Self-citationEnache, D., Pereira, J. B., Jelić, V., Winblad, B. G., Nilsson, P., Aarsland, D., & Bereczki, E. (2020) · Journal of Alzheimer s Disease · doi:10.3233/jad-200498 · Cited by 21 · see citing works
Regulated interactions of the norepineprhine transporter by the actin and microtubule cytoskeletons
Jeannotte, A. M., & Sidhu, A. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05258.x · Cited by 16 · see citing works
Broderick, P. A., Wenning, L., & Li, Y.-S. (2016) · Journal of Neural Transmission · doi:10.1007/s00702-016-1633-3 · Cited by 16 · see citing works
Prevalence of dementia and regional brain syndromes in long-standing Parkinson's disease
Wallin, A., Jennersjö, C., & Granérus, A. (1999) · Parkinsonism & Related Disorders · doi:10.1016/s1353-8020(99)00018-8 · Cited by 11 · see citing works
Kinetic Study on the Reactivity of Azanone (HNO) toward Cyclic C-Nucleophiles
Artelska, A., Rola, M., Rostkowski, M., et al. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222312982 · Cited by 9 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
- Authors
- Cervantes González, A., & Belbin, O.
- Affiliations
- Hospital de Sant Pau (ES)
- Corresponding author
- Belbin, Olivia
- ORCID
- Belbin, Olivia
- Venue
- Journal of Neural Transmission
- Published
- 2022-02
- Volume
- 129
- Issue
- 2
- Pages
- 187-206
- ISSN
- 0300-9564 (ISSN-L)
- 1435-1463
- OpenAlex
- W4211017991
- Cited by
- 7
- References
- 149
- Citations by year
- 2025: 2 · 2023: 4 · 2022: 1
- FWCI
- 0.25
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Neural Transmission (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Instituto de Salud Carlos III (PI18/00327)
- Agència de Gestió d’Ajuts Universitaris i de Recerca (2019 PROD 000088)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Keywords
- synaptic degeneration, synucleinopathies, alpha-synuclein, Parkinson's disease, Parkinson's disease dementia, dementia with Lewy bodies, multiple system atrophy, biomarkers, biological fluids, disease progression, treatment response monitoring
- MeSH terms
- Synucleinopathies, Humans, Synapses, Biomarkers, Multiple System Atrophy, Lewy Body Disease, alpha-Synuclein
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