Metabolic Turnover of Synaptic Proteins: Kinetics, Interdependencies and Implications for Synaptic Maintenance
Open accessAbstract
Chemical synapses contain multitudes of proteins, which in common with all proteins, have finite lifetimes and therefore need to be continuously replaced. Given the huge numbers of synaptic connections typical neurons form, the demand to maintain the protein contents of these connections might be expected to place considerable metabolic demands on each neuron. Moreover, synaptic proteostasis might differ according to distance from global protein synthesis sites, the availability of distributed protein synthesis facilities, trafficking rates and synaptic protein dynamics. To date, the turnover kinetics of synaptic proteins have not been studied or analyzed systematically, and thus metabolic demands or the aforementioned relationships remain largely unknown. In the current study we used dynamic Stable Isotope Labeling with Amino acids in Cell culture (SILAC), mass spectrometry (MS), Fluorescent Non-Canonical Amino acid Tagging (FUNCAT), quantitative immunohistochemistry and bioinformatics to systematically measure the metabolic half-lives of hundreds of synaptic proteins, examine how these depend on their pre/postsynaptic affiliation or their association with particular molecular complexes, and assess the metabolic load of synaptic proteostasis. We found that nearly all synaptic proteins identified here exhibited half-lifetimes in the range of 2-5 days. Unexpectedly, metabolic turnover rates were not significantly different for presynaptic and postsynaptic proteins, or for proteins for which mRNAs are consistently found in dendrites. Some functionally or structurally related proteins exhibited very similar turnover rates, indicating that their biogenesis and degradation might be coupled, a possibility further supported by bioinformatics-based analyses. The relatively low turnover rates measured here (∼0.7% of synaptic protein content per hour) are in good agreement with imaging-based studies of synaptic protein trafficking, yet indicate that the metabolic load synaptic protein turnover places on individual neurons is very substantial.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
CaMKII is known to turn over rapidly, with a half-life of 2-4 days.
“In particular, CaMKII is known to turn over rapidly, with a half-life of 2–4 days (403–405).”
From Synaptic memory and CaMKII (2023) · cites this paper as [403]
The Results table reports a 3.81-day half-life for CaMKIIβ2 in cultured cortical neurons, within the claimed range. It also reports 5.03 days for CaMKIIγ, so the 2–4-day range is not supported for CaMKII generally. (LLM, conf=0.86)
Experimental — accuracy not yet measuredMost synaptic proteins generally have half-lives of 2-5 days.
“Although memories can last for the entire span of an animal’s life, most synaptic proteins generally have half-lives of 2–5 days (403, 404).”
From Synaptic memory and CaMKII (2023) · cites this paper as [403]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855 · see citing works
Mass spectrometry-based proteomics
Aebersold, R., & Mann, M. (2003) · Nature · doi:10.1038/nature01511 · Cited by 6,955 · see citing works
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · cited 1× · see citing works
“Interestingly, a comparison with protein turnover in HeLa cells [32] shows that protein turnover in primary cultures of cortical neurons is generally slower than that observed in this immortalized cell line.”
BackgroundGOrilla: a tool for discovery and visualization of enriched GO terms in ranked gene lists
Eden, E., Navon, R., Steinfeld, I., Lipson, D., & Yakhini, Z. (2009) · BMC Bioinformatics · doi:10.1186/1471-2105-10-48 · Cited by 3,356 · see citing works
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373 · see citing works
Neuroligins and neurexins link synaptic function to cognitive disease
Südhof, T. C. (2008) · Nature · doi:10.1038/nature07456 · Cited by 1,849 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · cited 1× · see citing works
“6): 1) presynaptic vesicle proteins [37]; 2) presynaptic active zone molecules [38,39]; 3) postsynaptic density (PSD) proteins of glutamatergic synapses [40]; and 4) proteins for which dendritically located mRNAs are consistently found [41–51] (reviewed in [52–54]).”
BackgroundThe Postsynaptic Architecture of Excitatory Synapses: A More Quantitative View
Sheng, M., & Hoogenraad, C. C. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060805.160029 · Cited by 1,003 · see citing works
Quantitative ultrastructural analysis of hippocampal excitatory synapses
Schikorski, T., & Stevens, C. F. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-15-05858.1997 · Cited by 997 · see citing works
Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system
Ehlers, M. D. (2003) · Nature Neuroscience · doi:10.1038/nn1013 · Cited by 977 · see citing works
Hoffman, P. N., & Lasek, R. J. (1975) · The Journal of Cell Biology · doi:10.1083/jcb.66.2.351 · Cited by 941 · see citing works
A practical recipe for stable isotope labeling by amino acids in cell culture (SILAC)
Ong, S., & Mann, M. (2006) · Nature Protocols · doi:10.1038/nprot.2006.427 · Cited by 898 · see citing works
Dendritic Protein Synthesis, Synaptic Plasticity, and Memory
Sutton, M. A., & Schuman, E. M. (2006) · Cell · doi:10.1016/j.cell.2006.09.014 · Cited by 894 · see citing works
Cajigas, I. J., Tushev, G., Will, T. J., tom Dieck, S., Fuerst, N., & Schuman, E. M. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.036 · Cited by 709 · see citing works
Steward, O., & Levy, W. (1982) · The Journal of Neuroscience · doi:10.1523/jneurosci.02-03-00284.1982 · Cited by 676 · see citing works
Dendritic mRNA: transport, translation and function
Bramham, C. R., & Wells, D. G. (2007) · Nature reviews. Neuroscience · doi:10.1038/nrn2150 · Cited by 574 · see citing works
Synaptic Strength Regulated by Palmitate Cycling on PSD-95
El-Husseini, A., Schnell, E., Dakoji, S., Sweeney, N. T., Zhou, Q., Prange, O., Gauthier-Campbell, C., Aguilera-Moreno, A., Nicoll, R. A., & Bredt, D. S. (2002) · Cell · doi:10.1016/s0092-8674(02)00683-9 · Cited by 569 · see citing works
Burgin, K., Waxham, M., Rickling, S., Westgate, S., Mobley, W. C., & Kelly, P. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-06-01788.1990 · Cited by 564 · see citing works
Selective localization of messenger RNA for cytoskeletal protein MAP2 in dendrites
Garner, C. C., Tucker, R. P., & Matus, A. I. (1988) · Nature · doi:10.1038/336674a0 · Cited by 558 · see citing works
Activity-dependent regulation of dendritic synthesis and trafficking of AMPA receptors
Ju, W. H., Morishita, W., Tsui, J., Gaietta, G. M., Deerinck, T. J., Adams, S., Garner, C. C., Tsien, R. Y., Ellisman, M. H., & Malenka, R. C. (2004) · Nature Neuroscience · doi:10.1038/nn1189 · Cited by 524 · see citing works
Miller, S., Yasuda, M., Coats, J., Jones, Y., Martone, M. E., & Mayford, M. R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00978-9 · Cited by 507 · see citing works
Characterization of the proteome, diseases and evolution of the human postsynaptic density
Bayés, À., van de Lagemaat, L. N., Collins, M. O., Croning, M. D. R., Whittle, I. R., Choudhary, J. S., & Grant, S. G. N. (2011) · Nature Neuroscience · doi:10.1038/nn.2719 · Cited by 499 · see citing works
Jung, H., Yoon, B. C., & Holt, C. E. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3210 · Cited by 487 · see citing works
In situ visualization and dynamics of newly synthesized proteins in rat hippocampal neurons
Dieterich, D. C., Hodas, J. J. L., Gouzer, G., Shadrin, I. Y., Ngo, J. T., Triller, A., Tirrell, D. A., & Schuman, E. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2580 · Cited by 470 · see citing works
Self-citationOstroff, L. E., Fiala, J. C., Allwardt, B., & Harris, K. M. (2002) · Neuron · doi:10.1016/s0896-6273(02)00785-7 · Cited by 461 · see citing works
Dynamics of Protein Turnover, a Missing Dimension in Proteomics
Pratt, J. M., Petty, J., Riba‐Garcia, I., Robertson, D. H. L., Gaskell, S. J., Oliver, S. G., & Beynon, R. J. (2002) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m200046-mcp200 · Cited by 390 · see citing works
A Quantitative Spatial Proteomics Analysis of Proteome Turnover in Human Cells
Boisvert, F.-M., Ahmad, Y., Gierliński, M., Charrière, F., Lamont, D., Scott, M., Barton, G., & Lamond, A. I. (2012) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m111.011429 · Cited by 387 · see citing works
Compartmentalized Synthesis and Degradation of Proteins in Neurons
Steward, O., & Schuman, E. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00635-4 · Cited by 377 · see citing works
bioDBnet: the biological database network
Mudunuri, U. S., Che, A., Yi, M., & Stephens, R. M. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btn654 · Cited by 366 · see citing works
Analysis of proteome dynamics in the mouse brain
Price, J. C., Guan, S., Burlingame, A., Prusiner, S. B., & Ghaemmaghami, S. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1006551107 · Cited by 357 · see citing works
Turnover of the Human Proteome: Determination of Protein Intracellular Stability by Dynamic SILAC
Doherty, M. K., Hammond, D. E., Clague, M. J., Gaskell, S. J., & Beynon, R. J. (2009) · Journal of Proteome Research · doi:10.1021/pr800641v · Cited by 340 · see citing works
Molecular organization of the presynaptic active zone
Schoch, S., & Gundelfinger, E. D. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0244-y · Cited by 334 · see citing works
HIPPIE: Integrating Protein Interaction Networks with Experiment Based Quality Scores
Schaefer, M. H., Fontaine, J., Vinayagam, A., Porras, P., Wanker, E. E., & Andrade-Navarro, M. A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031826 · Cited by 334 · see citing works
Activity-Dependent Dendritic Targeting of BDNF and TrkB mRNAs in Hippocampal Neurons
Tongiorgi, E., Righi, M., & Cattaneo, A. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09492.1997 · Cited by 328 · see citing works
Cellular and molecular mechanisms of presynaptic assembly
Ziv, N. E., & Garner, C. C. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1370 · Cited by 306 · see citing works
Self-citationSurface trafficking of receptors between synaptic and extrasynaptic membranes: and yet they do move!
Triller, A., & Choquet, D. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.01.001 · Cited by 285 · see citing works
Mechanisms Of Fast And Slow Axonal Transport
Vallee, R. B., & Bloom, G. S. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.000423 · Cited by 267 · see citing works
Regulation of AMPA receptor surface diffusion by PSD-95 slots
Opazo, P., Sainlos, M., & Choquet, D. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.010 · Cited by 234 · see citing works
Synaptic regulation of translation of dendritic mRNAs
Schuman, E. M., Dynes, J. L., & Steward, O. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.1796-06.2006 · Cited by 230 · see citing works
RNA Trafficking and Local Protein Synthesis in Dendrites: An Overview
Martin, K. C., & Zukin, R. S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1801-06.2006 · Cited by 218 · see citing works
Redistribution and Stabilization of Cell Surface Glutamate Receptors during Synapse Formation
Mammen, A. L., Huganir, R. L., & O’Brien, R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-19-07351.1997 · Cited by 211 · see citing works
Differential subcellular localization of particular mRNAs in hippocampal neurons in culture
Kleiman, R. J., Banker, G. A., & Steward, O. (1990) · Neuron · doi:10.1016/0896-6273(90)90341-c · Cited by 200 · see citing works
SCRAPPER-Dependent Ubiquitination of Active Zone Protein RIM1 Regulates Synaptic Vesicle Release
Yao, I., Takagi, H., Ageta, H., Kahyo, T., Sato, S., Hatanaka, K., Fukuda, Y., Chiba, T., Morone, N., Yuasa, S., et al. (2007) · Cell · doi:10.1016/j.cell.2007.06.052 · Cited by 200 · see citing works
Furuichi, T., Simon‐Chazottes, D., Fujino, I., Yamada, N., Hasegawa, M. L., Miyawaki, A., Yoshikawa, S., Jl, G., & Mikoshiba, K. (1993) · PubMed · Cited by 200 · see citing works
Álvarez, J., Giuditta, A., & KOENIG, E. C. (2000) · Progress in Neurobiology · doi:10.1016/s0301-0082(99)00062-3 · Cited by 188 · see citing works
Spatially restricting gene expression by local translation at synapses
Wang, D. O., Martin, K. C., & Zukin, R. S. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.01.005 · Cited by 187 · see citing works
Mutch, S. A., Kensel-Hammes, P., Gadd, J. C., Fujimoto, B. S., Allen, R. W., Schiro, P. G., Lorenz, R. M., Kuyper, C. L., Kuo, J. S., Bajjalieh, S. M., et al. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3805-10.2011 · Cited by 185 · see citing works
Protein homeostasis and synaptic plasticity
Cajigas, I. J., Will, T. J., & Schuman, E. M. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.173 · Cited by 185 · see citing works
Synaptic stability and plasticity in a floating world
Gerrow, K., & Triller, A. (2010) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2010.06.010 · Cited by 171 · see citing works
Identification of acis-Acting Dendritic Targeting Element in MAP2 mRNAs
Blichenberg, A., Schwanke, B., Rehbein, M., Garner, C. C., Richter, D., & Kindler, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-20-08818.1999 · Cited by 171 · see citing works
Liao, L., Park, S. K., Xu, T., Vanderklish, P. W., & Yates, J. R. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0804678105 · Cited by 170 · see citing works
Long-Term Relationships between Synaptic Tenacity, Synaptic Remodeling, and Network Activity
Minerbi, A., Kahana, R., Goldfeld, L., Kaufman, M., Marom, S., & Ziv, N. E. (2009) · PLoS Biology · doi:10.1371/journal.pbio.1000136 · Cited by 166 · see citing works
Self-citationLocal Sharing as a Predominant Determinant of Synaptic Matrix Molecular Dynamics
Tsuriel, S., Geva, R., Zamorano, P. L., Dresbach, T., Boeckers, T. M., Gundelfinger, E. D., Garner, C. C., & Ziv, N. E. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040271 · Cited by 164 · see citing works
Self-citationKrueger, S., Kolar, A., & Fitzsimonds, R. M. (2003) · Neuron · doi:10.1016/s0896-6273(03)00729-3 · Cited by 161 · see citing works
Neurexin-Neuroligin Adhesions Capture Surface-Diffusing AMPA Receptors through PSD-95 Scaffolds
Mondin, M., Labrousse, V. F., Hosy, E., Heine, M., Tessier, B., Levet, F., Poujol, C., Blanchet, C., Choquet, D., & Thoumine, O. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6439-10.2011 · Cited by 150 · see citing works
Stable Isotopic Labeling by Amino Acids in Cultured Primary Neurons
Spellman, D. S., Deinhardt, K., Darie, C. C., Chao, M. V., & Neubert, T. A. (2008) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700387-mcp200 · Cited by 124 · see citing works
The Turnover Kinetics of Major Histocompatibility Complex Peptides of Human Cancer Cells
Milner, E., Barnea, E., Beer, I., & Admon, A. (2006) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m500241-mcp200 · Cited by 122 · see citing works
Mechanistic Logic Underlying the Axonal Transport of Cytosolic Proteins
Scott, D. A., Das, U., Tang, Y., & Roy, S. (2011) · Neuron · doi:10.1016/j.neuron.2011.03.022 · Cited by 119 · see citing works
Huang, F.-S., Chotiner, J. K., & Steward, O. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1779-05.2005 · Cited by 112 · see citing works
Organization and translation of mRNA in sympathetic axons
Lee, S.-K., & Hollenbeck, P. J. (2003) · Journal of Cell Science · doi:10.1242/jcs.00745 · Cited by 108 · see citing works
Neural timescales or lack thereof
Marom, S. (2009) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2009.10.003 · Cited by 106 · see citing works
Viable cultured neurons in ambient carbon dioxide and hibernation storage for a month
Brewer, G. J., & Price, P. J. (1996) · Neuroreport · doi:10.1097/00001756-199606170-00014 · Cited by 102 · see citing works
Molecular dynamics of postsynaptic receptors and scaffold proteins
Renner, M. L., Specht, C. G., & Triller, A. (2008) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2008.09.009 · Cited by 91 · see citing works
Dobie, F. A., & Craig, A. M. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6023-10.2011 · Cited by 89 · see citing works
Kalla, S., Stern, M., Basu, J., Varoqueaux, F., Reim, K., Rosenmund, C., Ziv, N. E., & Brose, N. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4330-06.2006 · Cited by 87 · see citing works
Self-citationJung, H., Yoon, B. C., & Holt, C. E. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3274 · Cited by 79 · see citing works
Fluorescent and photo-oxidizing TimeSTAMP tags track protein fates in light and electron microscopy
Butko, M. T., Yang, J. Y., Yang, G., Kim, H. J., Jeon, N. L., Shu, X., Mackey, M. R., Ellisman, M. H., Tsien, R. Y., & Lin, M. Z. (2012) · Nature Neuroscience · doi:10.1038/nn.3246 · Cited by 72 · see citing works
Signals, synapses, and synthesis: how new proteins control plasticity
Zukin, R. S. (2009) · Frontiers in Neural Circuits · doi:10.3389/neuro.04.014.2009 · Cited by 70 · see citing works
Axonal transport of synapsin I-like proteins in rabbit retinal ganglion cells
Baitinger, C., & Willard, M. B. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-11-03723.1987 · Cited by 67 · see citing works
Exchange and Redistribution Dynamics of the Cytoskeleton of the Active Zone Molecule Bassoon
Tsuriel, S., Fisher-Lavie, A., Wittenmayer, N., Dresbach, T., Garner, C. C., & Ziv, N. E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4777-08.2009 · Cited by 66 · see citing works
Self-citationArchibald, K., Perry, M. J., Molnár, E., & Henley, J. M. (1998) · Neuropharmacology · doi:10.1016/s0028-3908(98)00135-x · Cited by 64 · see citing works
RNA Binding Proteins Accumulate at the Postsynaptic Density with Synaptic Activity
Zhang, G., Neubert, T. A., & Jordan, B. A. (2012) · Journal of Neuroscience · doi:10.1523/jneurosci.2463-11.2012 · Cited by 60 · see citing works
Syntaxin1A Lateral Diffusion Reveals Transient and Local SNARE Interactions
Ribrault, C., Reingruber, J., Petković, M., Galli, T., Ziv, N. E., Holcman, D., & Triller, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4065-11.2011 · Cited by 60 · see citing works
Self-citationSynProt: A Database for Proteins of Detergent-Resistant Synaptic Protein Preparations
Pielot, R., Smalla, K., Müller, A., Landgraf, P., Lehmann, A., Eisenschmidt, E., Haus, U., Weismantel, R., Gundelfinger, E. D., & Dieterich, D. C. (2012) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2012.00001 · Cited by 60 · see citing works
Self-citationInsights into the roles of local translation from the axonal transcriptome
Deglincerti, A., & Jaffrey, S. R. (2012) · Open Biology · doi:10.1098/rsob.120079 · Cited by 48 · see citing works
The dynamics of synaptic scaffolds
Specht, C. G., & Triller, A. (2008) · BioEssays · doi:10.1002/bies.20831 · Cited by 44 · see citing works
Accelerators, Brakes, and Gears of Actin Dynamics in Dendritic Spines
Pontrello, C. G., & Ethell, I. M. (2009) · The Open Neuroscience Journal · doi:10.2174/1874082000903020067 · Cited by 43 · see citing works
Kjøller, C., & Diemer, N. H. (2000) · Neurochemistry International · doi:10.1016/s0197-0186(00)00008-5 · Cited by 42 · see citing works
Dendritic compartmentation of NMDA receptor mRNA in cultured hippocampal neurons
Benson, D. L. (1997) · Neuroreport · doi:10.1097/00001756-199703030-00004 · Cited by 41 · see citing works
Neuroligin-1 Loss Is Associated with Reduced Tenacity of Excitatory Synapses
Zeidan, A., & Ziv, N. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0042314 · Cited by 38 · see citing works
Self-citationShare and share alike: trading of presynaptic elements between central synapses
Staras, K. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.04.005 · Cited by 36 · see citing works
Sharing vesicles between central presynaptic terminals: implications for synaptic function
Staras, K. (2010) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2010.00020 · Cited by 35 · see citing works
Petrucci, T. C., Macioce, P., & Paggi, P. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-09-02938.1991 · Cited by 32 · see citing works
Long-term Relationships between Cholinergic Tone, Synchronous Bursting and Synaptic Remodeling
Kaufman, M., Corner, M. A., & Ziv, N. E. (2012) · PLoS ONE · doi:10.1371/journal.pone.0040980 · Cited by 28 · see citing works
Self-citationIijima, T., Imai, T., Kimura, Y., Bernstein, A., Okano, H. J., Yuzaki, M., & Okano, H. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504684102 · Cited by 27 · see citing works
Link, A. J., Vink, M. K. S., & Tirrell, D. A. (2007) · Nature Protocols · doi:10.1038/nprot.2007.269 · Cited by 13 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins
Wilhelm, B. G., Mandad, S., Truckenbrodt, S., Kröhnert, K., Schäfer, C., Rammner, B., Koo, S. J., Claßen, G. A., Krauss, M., Haucke, V., et al. (2014) · Science · doi:10.1126/science.1252884 · Cited by 770 · see citing works
Local translation in neurons: visualization and function
Holt, C. E., Martin, K. C., & Schuman, E. M. (2019) · Nature Structural & Molecular Biology · doi:10.1038/s41594-019-0263-5 · Cited by 515 · see citing works
Axonal transport: Driving synaptic function
Guedes-Dias, P., & Holzbaur, E. L. F. (2019) · Science · doi:10.1126/science.aaw9997 · Cited by 355 · see citing works
Is plasticity of synapses the mechanism of long-term memory storage?
Abraham, W. C., Jones, O. D., & Glanzman, D. L. (2019) · npj Science of Learning · doi:10.1038/s41539-019-0048-y · Cited by 368 · see citing works
Spatially Stable Mitochondrial Compartments Fuel Local Translation during Plasticity
Rangaraju, V., Lauterbach, M. A., & Schuman, E. M. (2019) · Cell · doi:10.1016/j.cell.2018.12.013 · Cited by 355 · see citing works
Fornasiero, E. F., Mandad, S., Wildhagen, H., Alevra, M., Rammner, B., Keihani, S., Opazo, F., Urban, I., Ischebeck, T., Sakib, M. S., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-06519-0 · Cited by 340 · see citing works
Direct visualization of newly synthesized target proteins in situ
Dieck, S. T., Kochen, L., Hanus, C., Heumüller, M., Bartnik, I., Nassim-Assir, B., Merk, K., Mosler, T., Garg, S., Bunse, S., et al. (2015) · Nature Methods · doi:10.1038/nmeth.3319 · Cited by 294 · see citing works
Kinetic Analysis of Protein Stability Reveals Age-Dependent Degradation
McShane, E., Sin, C., Zauber, H., Wells, J. N., Donnelly, N., Wang, X., Hou, J., Chen, W., Štorchová, Z., Marsh, J. A., et al. (2016) · Cell · doi:10.1016/j.cell.2016.09.015 · Cited by 291 · see citing works
Local and global influences on protein turnover in neurons and glia
Dörrbaum, A. R., Kochen, L., Langer, J. D., & Schuman, E. M. (2018) · eLife · doi:10.7554/elife.34202 · Cited by 249 · see citing works
Ashrafi, G., de Juan‐Sanz, J., Farrell, R. J., & Ryan, T. A. (2019) · Neuron · doi:10.1016/j.neuron.2019.11.020 · Cited by 229 · see citing works
Molecular Mechanisms of Presynaptic Membrane Retrieval and Synaptic Vesicle Reformation
Kononenko, N. L., & Haucke, V. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.016 · Cited by 220 · see citing works
Astrocyte lipid metabolism is critical for synapse development and function in vivo
van Deijk, A. F., Camargo, N., Timmerman, J., Heistek, T., Brouwers, J. F., Mogavero, F., Mansvelder, H. D., Smit, A. B., & Verheijen, M. H. G. (2017) · Glia · doi:10.1002/glia.23120 · Cited by 201 · see citing works
mRNA transport & local translation in neurons
Glock, C., Heumüller, M., & Schuman, E. M. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.05.005 · Cited by 199 · see citing works
Role of Bassoon and Piccolo in Assembly and Molecular Organization of the Active Zone
Gundelfinger, E. D., Reissner, C., & Garner, C. C. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00019 · Cited by 203 · see citing works
Local translation in neuronal compartments: how local is local?
Rangaraju, V., Dieck, S. T., & Schuman, E. M. (2017) · EMBO Reports · doi:10.15252/embr.201744045 · Cited by 193 · see citing works
Bassoon Controls Presynaptic Autophagy through Atg5
Okerlund, N. D., Schneider, K., Leal‐Ortiz, S., Montenegro‐Venegas, C., Kim, S. A., Garner, L. C., Waites, C. L., Gundelfinger, E. D., Reimer, R. J., & Garner, C. C. (2017) · Neuron · doi:10.1016/j.neuron.2017.01.026 · Cited by 189 · see citing works
Regulation of Neuronal Differentiation, Function, and Plasticity by Alternative Splicing
Furlanis, E., & Scheiffele, P. (2018) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-100617-062826 · Cited by 171 · see citing works
The roles of protein expression in synaptic plasticity and memory consolidation
Rosenberg, T., Gal-Ben-Ari, S., Dieterich, D. C., Kreutz, M. R., Ziv, N. E., Gundelfinger, E. D., & Rosenblum, K. (2014) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2014.00086 · Cited by 165 · see citing works
Self-citationIdentification of long-lived synaptic proteins by proteomic analysis of synaptosome protein turnover
Heo, S., Diering, G. H., Na, C. H., Nirujogi, R. S., Bachman, J. L., Pandey, A., & Huganir, R. L. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1720956115 · Cited by 163 · see citing works
Proteome Turnover in the Spotlight: Approaches, Applications, and Perspectives
Ross, A. B., Langer, J. D., & Jovanović, M. (2020) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r120.002190 · Cited by 151 · see citing works
Kinesin-3 responds to local microtubule dynamics to target synaptic cargo delivery to the presynapse
Guedes-Dias, P., Nirschl, J. J., Abreu, N., Tokito, M. K., Janke, C., Magiera, M. M., & Holzbaur, E. L. F. (2019) · Current Biology · doi:10.1016/j.cub.2018.11.065 · Cited by 153 · see citing works
Nascent Proteome Remodeling following Homeostatic Scaling at Hippocampal Synapses
Schanzenbächer, C. T., Sambandan, S., Langer, J. D., & Schuman, E. M. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.058 · Cited by 137 · see citing works
Presynaptic active zones in invertebrates and vertebrates
Ackermann, F., Waites, C. L., & Garner, C. C. (2015) · The EMBO Reports · doi:10.15252/embr.201540434 · Cited by 139 · see citing works
Proteostasis in complex dendrites
Hanus, C., & Schuman, E. M. (2013) · Nature reviews. Neuroscience · doi:10.1038/nrn3546 · Cited by 130 · see citing works
Direct Detection of Biotinylated Proteins by Mass Spectrometry
Schiapparelli, L., McClatchy, D. B., Liu, H.-H., Sharma, P., Yates, J. R., & Cline, H. T. (2014) · Journal of Proteome Research · doi:10.1021/pr5002862 · Cited by 127 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
Newly produced synaptic vesicle proteins are preferentially used in synaptic transmission
Truckenbrodt, S., Viplav, A., Jähne, S., Vogts, A., Denker, A., Wildhagen, H., Fornasiero, E. F., & Rizzoli, S. O. (2018) · The EMBO Journal · doi:10.15252/embj.201798044 · Cited by 123 · see citing works
Activity-Dependent Degradation of Synaptic Vesicle Proteins Requires Rab35 and the ESCRT Pathway
Sheehan, P., Zhu, M. J., Beskow, A., Vollmer, C., & Waites, C. L. (2016) · Journal of Neuroscience · doi:10.1523/jneurosci.0725-16.2016 · Cited by 112 · see citing works
Robust nanoscopy of a synaptic protein in living mice by organic-fluorophore labeling
Masch, J.-M., Steffens, H., Fischer, J., Engelhardt, J., Hubrich, J., Keller‐Findeisen, J., D’Este, E., Urban, N. T., Grant, S. G. N., Sahl, S. J., et al. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1807104115 · Cited by 119 · see citing works
A brain atlas of synapse protein lifetime across the mouse lifespan
Bulovaite, E., Qiu, Z., Kratschke, M., Zgraj, A., Fricker, D. G., Tuck, E. J., Gokhale, R., Koniaris, B., Jami, S. A., Merino-Serrais, P., et al. (2022) · Neuron · doi:10.1016/j.neuron.2022.09.009 · Cited by 111 · see citing works
The Regulation of Synaptic Protein Turnover
Alvarez-Castelao, B., & Schuman, E. M. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.r115.657130 · Cited by 110 · see citing works
Voltage-Gated Calcium Channels: Key Players in Sensory Coding in the Retina and the Inner Ear
Pangršič, T., Singer, J. H., & Koschak, A. (2018) · Physiological Reviews · doi:10.1152/physrev.00030.2017 · Cited by 113 · see citing works
Cell-selective labelling of proteomes in Drosophila melanogaster
Erdmann, I., Marter, K., Kobler, O., Niehues, S., Abele, J., Müller, A., Bussmann, J., Storkebaum, E., Ziv, T., Thomas, U., et al. (2015) · Nature Communications · doi:10.1038/ncomms8521 · Cited by 98 · see citing works
Self-citationProteome dynamics during homeostatic scaling in cultured neurons
Dörrbaum, A. R., Alvarez‐Castelao, B., Nassim-Assir, B., Langer, J. D., & Schuman, E. M. (2020) · eLife · doi:10.7554/elife.52939 · Cited by 92 · see citing works
Memory Erasure Experiments Indicate a Critical Role of CaMKII in Memory Storage
Rossetti, T., Banerjee, S., Kim, C., Leubner, M., Lamar, C., Gupta, P., Lee, B., Neve, R., & Lisman, J. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.010 · Cited by 94 · see citing works
Krishnaswamy, V. R., Benbenishty, A., Blinder, P., & Sagi, I. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03182-6 · Cited by 92 · see citing works
Landgraf, P., Antileo, E. R., Schuman, E. M., & Dieterich, D. C. (2015) · Methods in Molecular Biology · doi:10.1007/978-1-4939-2272-7_14 · Cited by 78 · see citing works
Self-citationUnc13: A multifunctional synaptic marvel
Dittman, J. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.12.011 · Cited by 78 · see citing works
Adaikkan, C., Taha, E., Barrera, I., David, O., & Rosenblum, K. (2017) · Biological Psychiatry · doi:10.1016/j.biopsych.2017.11.028 · Cited by 77 · see citing works
Arike, L., Seiman, A., van der Post, S., Rodríguez-Piñeiro, A. M., Ermund, A., Schütte, A., Bäckhed, F., Johansson, M., & Hansson, G. C. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.068 · Cited by 75 · see citing works
Light-Activated ROS Production Induces Synaptic Autophagy
Hoffmann, S., Orlando, M., Andrzejak, E., Bruns, C., Trimbuch, T., Rosenmund, C., Garner, C. C., & Ackermann, F. (2019) · Journal of Neuroscience · doi:10.1523/jneurosci.1317-18.2019 · Cited by 73 · see citing works
Proteomics of the Synapse – A Quantitative Approach to Neuronal Plasticity
Dieterich, D. C., & Kreutz, M. R. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.r115.051482 · Cited by 73 · see citing works
Self-citationFonkeu, Y., Kraynyukova, N., Hafner, A., Kochen, L., Sartori, F., Schuman, E. M., & Tchumatchenko, T. (2019) · Neuron · doi:10.1016/j.neuron.2019.06.022 · Cited by 72 · see citing works
Kluever, V., Russo, B., Mandad, S., Kumar, N. H., Alevra, M., Ori, A., Rizzoli, S. O., Urlaub, H., Schneider, A., & Fornasiero, E. F. (2022) · Science Advances · doi:10.1126/sciadv.abn4437 · Cited by 69 · see citing works
Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) for Quantitative Proteomics
Hoedt, E., Zhang, G., & Neubert, T. A. (2019) · Advances in experimental medicine and biology · doi:10.1007/978-3-030-15950-4_31 · Cited by 69 · see citing works
A Presynaptic Perspective on Transport and Assembly Mechanisms for Synapse Formation
Rizalar, F. S., Roosen, D. A., & Haucke, V. (2020) · Neuron · doi:10.1016/j.neuron.2020.09.038 · Cited by 63 · see citing works
Proteostatic regulation in neuronal compartments
Giandomenico, S. L., Alvarez‐Castelao, B., & Schuman, E. M. (2021) · Trends in Neurosciences · doi:10.1016/j.tins.2021.08.002 · Cited by 61 · see citing works
Bayés, À., Collins, M. O., Galtrey, C. M., Simonnet, C., Roy, M. M., Croning, M. D. R., Gou, G., van de Lagemaat, L. N., Milward, D., Whittle, I. R., et al. (2014) · Molecular Brain · doi:10.1186/s13041-014-0088-4 · Cited by 62 · see citing works
Scheyer, A. F., Wolf, M. E., & Tseng, K. Y. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4940-13.2014 · Cited by 60 · see citing works
The stability of memories during brain remodeling: A perspective
Blackiston, D. J., Shomrat, T., & Levin, M. G. (2015) · Communicative & Integrative Biology · doi:10.1080/19420889.2015.1073424 · Cited by 60 · see citing works
Vti1a/b regulate synaptic vesicle and dense core vesicle secretion via protein sorting at the Golgi
Emperador-Melero, J., Huson, V., van Weering, J. R. T., Bollmann, C., von Mollard, G. F., Toonen, R. F. G., & Verhage, M. (2018) · Nature Communications · doi:10.1038/s41467-018-05699-z · Cited by 59 · see citing works
Ligand-directed two-step labeling to quantify neuronal glutamate receptor trafficking
Ojima, K., Shiraiwa, K., Soga, K., Doura, T., Takato, M., Komatsu, K., Yuzaki, M., Hamachi, I., & Kiyonaka, S. (2021) · Nature Communications · doi:10.1038/s41467-021-21082-x · Cited by 55 · see citing works
The effects of proteasomal inhibition on synaptic proteostasis
Hakim, V., Cohen, L. D., Zuchman, R., Ziv, T., & Ziv, N. E. (2016) · The EMBO Journal · doi:10.15252/embj.201593594 · Cited by 52 · see citing works
Self-citationCompetition for synaptic building blocks shapes synaptic plasticity
Triesch, J., Vo, A. D., & Hafner, A. (2018) · eLife · doi:10.7554/elife.37836 · Cited by 53 · see citing works
Biochemical principles underlying the stable maintenance of LTP by the CaMKII/NMDAR complex
Lisman, J. E., & Raghavachari, S. (2014) · Brain Research · doi:10.1016/j.brainres.2014.12.010 · Cited by 51 · see citing works
On the research of time past: the hunt for the substrate of memory
Queenan, B. N., Ryan, T. J., Gazzaniga, M. S., & Gallistel, C. R. (2017) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.13348 · Cited by 51 · see citing works
Topoisomerase 1 inhibition reversibly impairs synaptic function
Mabb, A. M., Kullmann, P. H. M., Twomey, M. A., Miriyala, J., Philpot, B. D., & Zylka, M. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1413204111 · Cited by 49 · see citing works
Vevea, J., & Chapman, E. R. (2020) · eLife · doi:10.7554/elife.56469 · Cited by 48 · see citing works
Actin Cytoskeleton Role in the Maintenance of Neuronal Morphology and Long-Term Memory
Lamprecht, R. (2021) · Cells · doi:10.3390/cells10071795 · Cited by 45 · see citing works
A unified resource and configurable model of the synapse proteome and its role in disease
Sorokina, O., Mclean, C., Croning, M. D. R., Heil, K. F., Wysocka, E., He, X., Sterratt, D. C., Grant, S. G. N., Simpson, T. I., & Armstrong, J. D. (2021) · Scientific Reports · doi:10.1038/s41598-021-88945-7 · Cited by 47 · see citing works
Self-citationTeaching old NCATs new tricks: using non-canonical amino acid tagging to study neuronal plasticity
Hinz, F. I., Dieterich, D. C., & Schuman, E. M. (2013) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2013.07.021 · Cited by 46 · see citing works
Self-citationMechanisms controlling assembly and plasticity of presynaptic active zone scaffolds
Petzoldt, A. G., Lützkendorf, J., & Sigrist, S. J. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.04.009 · Cited by 43 · see citing works
Metabolic constraints on synaptic learning and memory
Karbowski, J. (2019) · Journal of Neurophysiology · doi:10.1152/jn.00092.2019 · Cited by 46 · see citing works
The purpose and ubiquity of turnover
Reddien, P. W. (2024) · Cell · doi:10.1016/j.cell.2024.04.034 · Cited by 42 · see citing works
Presynaptic activity and protein turnover are correlated at the single-synapse level
Jähne, S., Mikulasch, F. A., Heuer, H., Truckenbrodt, S., Agüi‐Gonzalez, P., Grewe, K., Vogts, A., Rizzoli, S. O., & Priesemann, V. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.108841 · Cited by 41 · see citing works
Presynaptic and Postsynaptic Scaffolds
Ziv, N. E., & Fisher-Lavie, A. (2014) · The Neuroscientist · doi:10.1177/1073858414523321 · Cited by 39 · see citing works
Self-citationTranslatome Regulation in Neuronal Injury and Axon Regrowth
Rozenbaum, M., Rajman, M., Rishal, I., Koppel, I., Koley, S., Medzihradszky, K. F., Osés-Prieto, J. A., Kawaguchi, R., Amieux, P. S., Burlingame, A. L., et al. (2018) · eNeuro · doi:10.1523/eneuro.0276-17.2018 · Cited by 40 · see citing works
Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC) for Quantitative Proteomics
Hoedt, E., Zhang, G., & Neubert, T. A. (2014) · Advances in experimental medicine and biology · doi:10.1007/978-3-319-06068-2_5 · Cited by 40 · see citing works
The where, what, and when of membrane protein degradation in neurons
Jin, E. J., Kiral, F. R., & Hiesinger, P. R. (2017) · Developmental Neurobiology · doi:10.1002/dneu.22534 · Cited by 38 · see citing works
Wentzel, C., Delvendahl, I., Sydlik, S., Georgiev, O., & Müller, M. (2018) · Nature Communications · doi:10.1038/s41467-017-02494-0 · Cited by 38 · see citing works
Ivanova, D., Dirks, A., & Fejtova, A. (2016) · The Journal of Physiology · doi:10.1113/jp271826 · Cited by 37 · see citing works
Crowd Control: Effects of Physical Crowding on Cargo Movement in Healthy and Diseased Neurons
Sabharwal, V., & Koushika, S. P. (2019) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00470 · Cited by 36 · see citing works
Recent insights on principles of synaptic protein degradation
Cohen, L. D., & Ziv, N. E. (2017) · F1000Research · doi:10.12688/f1000research.10599.1 · Cited by 35 · see citing works
Self-citationNMDA receptors in axons: there's no coincidence
Wong, H. H., Rannio, S., Jones, E. V., Thomazeau, A., & Sjöström, P. J. (2020) · The Journal of Physiology · doi:10.1113/jp280059 · Cited by 33 · see citing works
CaMKII knockdown affects both early and late phases of olfactory long-term memory in the honeybee
Scholl, C., Kübert, N., Muenz, T. S., & Rößler, W. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.124859 · Cited by 35 · see citing works
Yap, C. C., Digilio, L. C., McMahon, L. P., & Winckler, B. (2017) · Scientific Reports · doi:10.1038/s41598-017-07667-x · Cited by 31 · see citing works
Determining and interpreting protein lifetimes in mammalian tissues
Fornasiero, E. F., & Savas, J. N. (2022) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2022.08.011 · Cited by 35 · see citing works
The Potential Role of Protein Kinase R as a Regulator of Age-Related Neurodegeneration
Martínez, N. W., Gómez, F. E., & Matus, S. (2021) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2021.638208 · Cited by 33 · see citing works
Neuronal and synaptic protein lifetimes
Cohen, L. D., & Ziv, N. E. (2019) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.12.007 · Cited by 31 · see citing works
Self-citationStress vulnerability shapes disruption of motor cortical neuroplasticity
Gellner, A., Sitter, A., Rackiewicz, M., Sylvester, M., Philipsen, A., Zimmer, A., & Stein, V. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-01855-8 · Cited by 32 · see citing works
Temporal phases of long-term potentiation (LTP): myth or fact?
Abbas, A.-K., Villers, A., & Ris, L. (2015) · Reviews in the Neurosciences · doi:10.1515/revneuro-2014-0072 · Cited by 29 · see citing works
Synaptic vesicle proteins are selectively delivered to axons in mammalian neurons
Watson, E. T., Pauers, M. M., Seibert, M. J., Vevea, J., & Chapman, E. R. (2023) · eLife · doi:10.7554/elife.82568 · Cited by 30 · see citing works
The presynaptic active zone: A dynamic scaffold that regulates synaptic efficacy
Michel, K., Müller, J. A., Oprişoreanu, A., & Schoch, S. (2015) · Experimental Cell Research · doi:10.1016/j.yexcr.2015.02.011 · Cited by 29 · see citing works
Hsc70 chaperone activity is required for the cytosolic slow axonal transport of synapsin
Ganguly, A., Han, X., Das, U., Wang, L., Loi, J., Sun, J., Gitler, D., Caillol, G., Leterrier, C., Yates, J. R., et al. (2017) · The Journal of Cell Biology · doi:10.1083/jcb.201604028 · Cited by 29 · see citing works
Presynaptic perspective: Axonal transport defects in neurodevelopmental disorders
Xiong, G.-J., & Sheng, Z. (2024) · The Journal of Cell Biology · doi:10.1083/jcb.202401145 · Cited by 26 · see citing works
Homeostatic Roles of the Proteostasis Network in Dendrites
Lottes, E. N., & Cox, D. N. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00264 · Cited by 26 · see citing works
Holographic two-photon activation for synthetic optogenetics
Carmi, I., Battista, M. D., Maddalena, L., Carroll, E. C., Kienzler, M. A., & Berlin, S. (2019) · Nature Protocols · doi:10.1038/s41596-018-0118-2 · Cited by 28 · see citing works
PKMζ, But Not PKCλ, Is Rapidly Synthesized and Degraded at the Neuronal Synapse
Palida, S. F., Butko, M. T., Ngo, J. T., Mackey, M. R., Gross, L. A., Ellisman, M. H., & Tsien, R. Y. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.0004-15.2015 · Cited by 27 · see citing works
Synaptic memory survives molecular turnover
Lee, J., Chen, X., & Nicoll, R. A. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2211572119 · Cited by 27 · see citing works
Mohar, B., Michel, G., Wang, Y., Hernandez, V., Grimm, J. B., Park, J.-Y., Patel, R. H., Clarke, M. D., Brown, T. A., Bergmann, C., et al. (2025) · Nature Neuroscience · doi:10.1038/s41593-025-01923-4 · Cited by 38 · see citing works
Origin of axonal proteins: Is the axon‐schwann cell unit a functional syncytium?
López‐Leal, R., Álvarez, J., & Court, F. A. (2016) · Cytoskeleton · doi:10.1002/cm.21319 · Cited by 26 · see citing works
Mitigation of synaptic and memory impairments via F-actin stabilization in Alzheimer’s disease
Haseena, P. A., Basavaraju, N., Chandran, M., Jaleel, A., Bennett, D. A., & Kommaddi, R. P. (2024) · Alzheimer s Research & Therapy · doi:10.1186/s13195-024-01558-w · Cited by 25 · see citing works
Symptomatic treatment of botulism with a clinically approved small molecule
Vazquez-Cintron, E. J., Machamer, J. B., Ondeck, C. A., Pagarigan, K. T., Winner, B. M., Bodner, P., Kelly, K. E., Pennington, M. R., & McNutt, P. M. (2020) · JCI Insight · doi:10.1172/jci.insight.132891 · Cited by 25 · see citing works
Lange, F., Agüi‐Gonzalez, P., Riedel, D., Phan, N. T. N., Jakobs, S., & Rizzoli, S. O. (2021) · PLoS ONE · doi:10.1371/journal.pone.0240768 · Cited by 24 · see citing works
Logistics of neuronal protein turnover: Numbers and mechanisms
Sun, C., & Schuman, E. M. (2022) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2022.103793 · Cited by 23 · see citing works
Phosphorylation and Degradation of Tomosyn-2 De-represses Insulin Secretion
Bhatnagar, S., Soni, M. S., Wrighton, L. S., Hebert, A. S., Zhou, A. S., Paul, P. K., Gregg, T., Rabaglia, M. E., Keller, M. P., Coon, J. J., et al. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m114.575985 · Cited by 25 · see citing works
Monitoring Newly Synthesized Proteins over the Adult Life Span of Caenorhabditis elegans
Vukoti, K., Yu, X., Sheng, Q., Saha, S., Feng, Z., Hsu, A., & Miyagi, M. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00021 · Cited by 23 · see citing works
An integrated transcriptomic and proteomic map of the mouse hippocampus at synaptic resolution
Kaulich, E., Waselenchuk, Q., Fürst, N., Desch, K., Mosbacher, J., Ciirdaeva, E., Juengling, M., Ray, R., Nassim-Assir, B., Tushev, G., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-63119-5 · Cited by 24 · see citing works
Kaulich, E., Waselenchuk, Q., Fürst, N., Desch, K., Mosbacher, J., Ciirdaeva, E., Juengling, M., Tushev, G., Langer, J., & Schuman, E. M. (2024) · doi:10.1101/2024.08.05.606570 · Cited by 22 · see citing works
Mandad, S., Rahman, R., Centeno, T. P., Vidal, R. O., Wildhagen, H., Rammner, B., Keihani, S., Opazo, F., Urban, I., Ischebeck, T., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-35277-8 · Cited by 21 · see citing works
- Authors
- Cohen, L. D., Zuchman, R., Sorokina, O., Müller, A., Dieterich, D. C., Armstrong, J. D., Ziv, T., & Ziv, N. E.
- Affiliations
- Technion – Israel Institute of Technology (IL)
- University of Edinburgh (GB)
- Otto-von-Guericke-Universität Magdeburg (DE)
- Corresponding author
- Ziv, Noam E.
- ORCID
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2013-05-02
- Volume
- 8
- Issue
- 5
- Pages
- e63191
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3642143
- OpenAlex
- W2050606229
- Cited by
- 215
- References
- 86
- Citations by year
- 2026: 8 · 2025: 10 · 2024: 16 · 2023: 16 · 2022: 16 · 2021: 18 · 2020: 21 · 2019: 26 · 2018: 20 · 2017: 20 · 2016: 11 · 2015: 15 · 2014: 15 · 2013: 2 · 2012: 1
- FWCI
- 7.03
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- Funders
- European Commission (241498)
- University of Haifa
- Technion-Israel Institute of Technology
- Universität Ulm
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- synaptic proteins, protein turnover, protein half-life, presynaptic proteins, postsynaptic proteins, dendritic mRNA, protein degradation, protein synthesis, synapse maintenance, protein complex association
- MeSH terms
- Animals, Cell Compartmentation, Kinetics, Neurons, Proteins, Synapses, Rats, Wistar, Protein Transport, Proteomics, 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