GKAP orchestrates activity-dependent postsynaptic protein remodeling and homeostatic scaling
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How does chronic activity modulation lead to global remodeling of proteins at synapses and synaptic scaling? Here we report that guanylate kinase-associated protein (GKAP; also known as SAPAP), a scaffolding molecule linking NMDA receptor-PSD-95 to Shank-Homer complexes, acts in these processes. Overexcitation removes GKAP from synapses via the ubiquitin-proteasome system, whereas inactivity induces synaptic accumulation of GKAP in rat hippocampal neurons. Bidirectional changes in synaptic GKAP amounts are controlled by specific CaMKII isoforms coupled to different Ca(2+) channels. CaMKIIα activated by the NMDA receptor phosphorylates GKAP Ser54 to induce polyubiquitination of GKAP. In contrast, CaMKIIβ activation via L-type voltage-dependent calcium channels promotes GKAP recruitment by phosphorylating GKAP Ser340 and Ser384, which uncouples GKAP from myosin Va motor complex. Overexpressing GKAP turnover mutants not only hampers activity-dependent remodeling of PSD-95 and Shank but also blocks bidirectional synaptic scaling. Therefore, activity-dependent turnover of PSD proteins orchestrated by GKAP is critical for homeostatic plasticity.
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When Ca2+ is high, activated βCaMKII can participate in SAPAP trafficking and increase AMPAR incorporation, enabling spine remodeling and synaptic strengthening.
“In contrast, when Ca2+ is high, activated βCaMKII can participate in SAPAP trafficking and increase incorporation of AMPARs, enabling spine remodeling and synaptic strengthening (Shin et al., 2012).”
From Unifying Views of Autism Spectrum Disorders: A Consideration of Autoregulatory Feedback Loops (2016) · cites this paper as Shin et al., 2012
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Aggresomes, inclusion bodies and protein aggregation
Kopito, R. R. (2000) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01852-3 · Cited by 1,906 · see citing works
The self-tuning neuron: synaptic scaling of excitatory synapses
Turrigiano, G. G. (2008) · Cell · doi:10.1016/j.cell.2008.10.008 · Cited by 1,533 · see citing works
Mechanisms of CaMKII action in long-term potentiation
Lisman, J., Yasuda, R., & Raghavachari, S. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3192 · Cited by 1,134 · see citing works
Receptor trafficking and synaptic plasticity
Collingridge, G. L., Isaac, J. T. R., & Wang, Y. T. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1556 · Cited by 1,046 · see citing works
Naisbitt, S., Kim, E., Tu, J. C., Xiao, B., Sala, C., Valtschanoff, J., Weinberg, R. J., Worley, P. F., & Sheng, M. (1999) · Neuron · doi:10.1016/s0896-6273(00)80809-0 · Cited by 1,009 · see citing works
Self-citationThe 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
Self-citationActivity 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
Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice
Welch, J. M., Lu, J., Rodriguiz, R. M., Trotta, N. C., Peca, J., Ding, J.-D., Feliciano, C., Chen, M., Adams, J. P., Luo, J., et al. (2007) · Nature · doi:10.1038/nature06104 · Cited by 852 · see citing works
The Multifunctional Calcium/Calmodulin-Dependent Protein Kinase: From Form to Function
Braun, A. P., & Schulman, H. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.002221 · Cited by 820 · see citing works
Arc/Arg3.1 Mediates Homeostatic Synaptic Scaling of AMPA Receptors
Shepherd, J. D., Rumbaugh, G., Wu, J., Chowdhury, S., Plath, N., Kuhl, D., Huganir, R. L., & Worley, P. F. (2006) · Neuron · doi:10.1016/j.neuron.2006.08.034 · Cited by 779 · see citing works
Regulation of Dendritic Spine Morphology and Synaptic Function by Shank and Homer
Sala, C., Piëch, V., Wilson, N. R., Passafaro, M., Liu, G., & Sheng, M. (2001) · Neuron · doi:10.1016/s0896-6273(01)00339-7 · Cited by 716 · see citing works
Self-citationHudmon, A., & Schulman, H. (2002) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.71.110601.135410 · Cited by 654 · see citing works
Sutton, M. A., Ito, H. T., Cressy, P., Kempf, C., Woo, J. C., & Schuman, E. M. (2006) · Cell · doi:10.1016/j.cell.2006.03.040 · Cited by 633 · see citing works
The Postsynaptic Organization of Synapses
Sheng, M., & Kim, E. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005678 · Cited by 603 · see citing works
Self-citationUnraveling mechanisms of homeostatic synaptic plasticity
Pozo, K., & Goda, Y. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.028 · Cited by 565 · see citing works
Songyang, Z., Lu, K. P., Kwon, Y. T., Tsai, L., Filhol, O., Cochet, C., Brickey, D. A., Soderling, T. R., Bartleson, C., Graves, D. J., et al. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.11.6486 · Cited by 550 · see citing works
Kim, E., Naisbitt, S., Hsueh, Y.-P., Rao, A., Rothschild, A., Craig, A. M., & Sheng, M. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.3.669 · Cited by 516 · see citing works
Self-citationThe Subspine Organization of Actin Fibers Regulates the Structure and Plasticity of Dendritic Spines
Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C. R., & Kasai, H. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.013 · Cited by 490 · see citing works
Adaptation to Synaptic Inactivity in Hippocampal Neurons
Thiagarajan, T. C., Lindskog, M., & Tsien, R. W. (2005) · Neuron · doi:10.1016/j.neuron.2005.06.037 · Cited by 482 · see citing works
MEMBRANE-ASSOCIATED GUANYLATE KINASES REGULATE ADHESION AND PLASTICITY AT CELL JUNCTIONS
Funke, L., Dakoji, S., & Bredt, D. S. (2005) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.74.082803.133339 · Cited by 469 · see citing works
Takeuchi, M., Hata, Y., Hirao, K., Toyoda, A., Irie, M., & Takai, Y. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.18.11943 · Cited by 359 · see citing works
Fink, C. C., Bayer, K.-U., Myers, J. W., Ferrell, J. E., Schulman, H., & Meyer, T. (2003) · Neuron · doi:10.1016/s0896-6273(03)00428-8 · Cited by 328 · see citing works
Okamoto, K.-I., Narayanan, R., Lee, S. H., Murata, K., & Hayashi, Y. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0701656104 · Cited by 328 · see citing works
Self-citationOmkumar, R. V., Kiely, M. J., Rosenstein, A. J., Min, K.-T., & Kennedy, M. B. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.49.31670 · Cited by 304 · see citing works
Targeted Protein Degradation and Synapse Remodeling by an Inducible Protein Kinase
Pak, D. T. S., & Sheng, M. (2003) · Science · doi:10.1126/science.1082475 · Cited by 299 · see citing works
Self-citationCharacterization of the Shank Family of Synaptic Proteins
Lim, S., Naisbitt, S., Yoon, J., Hwang, J.-I., Suh, P.-G., Sheng, M., & Kim, E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.41.29510 · Cited by 295 · see citing works
Self-citationThiagarajan, T. C., Piedras-Renterı́a, E. S., & Tsien, R. W. (2002) · Neuron · doi:10.1016/s0896-6273(02)01049-8 · Cited by 288 · see citing works
Kim, M. J., Futai, K., Jo, J., Hayashi, Y., Cho, K., & Sheng, M. (2007) · Neuron · doi:10.1016/j.neuron.2007.09.007 · Cited by 278 · see citing works
Self-citationDeconstruction for Reconstruction: The Role of Proteolysis in Neural Plasticity and Disease
Bingol, B., & Sheng, M. (2011) · Neuron · doi:10.1016/j.neuron.2010.11.006 · Cited by 275 · see citing works
Self-citationAutophosphorylated CaMKIIα Acts as a Scaffold to Recruit Proteasomes to Dendritic Spines
Bingol, B., Wang, C.-F., Arnott, D., Cheng, D., Peng, J., & Sheng, M. (2010) · Cell · doi:10.1016/j.cell.2010.01.024 · Cited by 268 · see citing works
Self-citationMotor protein–dependent transport of AMPA receptors into spines during long-term potentiation
Correia, S. S., Bassani, S., Brown, T. C., Lisé, M.-F., Backos, D. S., El-Husseini, A., Passafaro, M., & Esteban, J. A. (2008) · Nature Neuroscience · doi:10.1038/nn2063 · Cited by 260 · see citing works
Naisbitt, S. R., Valtschanoff, J. G., Allison, D. W., Sala, C., Kim, E., Craig, A. M., Weinberg, R. J., & Sheng, M. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-12-04524.2000 · Cited by 259 · see citing works
Self-citationSeeburg, D. P., Feliú-Mójer, M. I., Gaiottino, J., Pak, D. T. S., & Sheng, M. (2008) · Neuron · doi:10.1016/j.neuron.2008.03.021 · Cited by 230 · see citing works
Self-citationKuriu, T., Inoue, A., Bito, H., Sobue, K., & Okabe, S. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.0522-06.2006 · Cited by 206 · see citing works
Guillaud, L., Wong, R. W.-C., & Hirokawa, N. (2007) · Nature Cell Biology · doi:10.1038/ncb1665 · Cited by 188 · see citing works
Arc-dependent synapse-specific homeostatic plasticity
Béïque, J.-C., Na, Y., Kuhl, D., Worley, P. F., & Huganir, R. L. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1017914108 · Cited by 179 · see citing works
UBIQUITIN-DEPENDENT REGULATION OF THE SYNAPSE
DiAntonio, A., & Hicke, L. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.27.070203.144317 · Cited by 175 · see citing works
Functional Implications of the Subunit Composition of Neuronal CaM Kinase II
Brocke, L., Chiang, L. W., Wagner, P. D., & Schulman, H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.32.22713 · Cited by 161 · see citing works
Borgesius, N. Z., van Woerden, G. M., Buitendijk, G. H. S., Keijzer, N., Jaarsma, D., Hoogenraad, C. C., & Elgersma, Y. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5105-10.2011 · Cited by 124 · see citing works
DAP‐1, a novel protein that interacts with the guanylate kinase‐like domains of hDLG and PSD‐95
Satoh, K., Yanai, H., Senda, T., Kohu, K., Nakamura, T., Okumura, N., Matsumine, A., Kobayashi, S., Toyoshima, K., & Akiyama, T. (1997) · Genes to Cells · doi:10.1046/j.1365-2443.1997.1310329.x · Cited by 122 · see citing works
Tippens, A. L., Paré, J., Langwieser, N. N., Moosmang, S., Milner, T. A., Smith, Y., & Lee, A. (2007) · The Journal of Comparative Neurology · doi:10.1002/cne.21567 · Cited by 112 · see citing works
Lo, K. W. ‐., Kan, H.-M., Chan, L.-N., Xu, W., Wang, K., Wu, Z., Sheng, M., & Zhang, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m411408200 · Cited by 111 · see citing works
Self-citationMicrotubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95
Passafaro, M., Sala, C., Niethammer, M., & Sheng, M. (1999) · Nature Neuroscience · doi:10.1038/15990 · Cited by 110 · see citing works
Self-citationHung, A. Y., Sung, C. C., Brito, I. L., & Sheng, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009842 · Cited by 106 · see citing works
Self-citationLTP and adaptation to inactivity: Overlapping mechanisms and implications for metaplasticity
Thiagarajan, T. C., Lindskog, M., Malgaroli, A., & Tsien, R. W. (2007) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.030 · Cited by 99 · see citing works
Romorini, S., Piccoli, G., Jiang, M., Grossano, P., Tonna, N., Passafaro, M., Zhang, M., & Sala, C. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3314-04.2004 · Cited by 96 · see citing works
Plk2 attachment to NSF induces homeostatic removal of GluA2 during chronic overexcitation
Evers, D. M., Matta, J. A., Hoe, H., Zarkowsky, D. S., Lee, S. H., Isaac, J. T. R., & Pak, D. T. S. (2010) · Nature Neuroscience · doi:10.1038/nn.2624 · Cited by 73 · see citing works
Self-citationA CaMKIIβ signaling pathway at the centrosome regulates dendrite patterning in the brain
Puram, S. V., Kim, A. H., Ikeuchi, Y., Wilson‐Grady, J., Merdes, A., Gygi, S. P., & Bonni, A. (2011) · Nature Neuroscience · doi:10.1038/nn.2857 · Cited by 71 · see citing works
Phosphorylation state of postsynaptic density proteins
Trinidad, J. C., Thalhammer, A., Specht, C. G., Schoepfer, R., & Burlingame, A. L. (2005) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02943.x · Cited by 70 · see citing works
Groth, R. D., Lindskog, M., Thiagarajan, T. C., Li, L., & Tsien, R. W. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018022108 · Cited by 64 · see citing works
Roselli, F., Livrea, P., & Almeida, O. F. X. (2011) · PLoS ONE · doi:10.1371/journal.pone.0023097 · Cited by 37 · see citing works
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Leal, G., Afonso, P. M., Salazar, I. L., & Duarte, C. B. (2015) · Brain Research · doi:10.1016/j.brainres.2014.10.019 · Cited by 410 · see citing works
What is memory? The present state of the engram
Poo, M.-M., Pignatelli, M., Ryan, T. J., Tonegawa, S., Bonhoeffer, T., Martin, K. C., Rudenko, A., Tsai, L., Tsien, R. W., Fishell, G., et al. (2016) · BMC Biology · doi:10.1186/s12915-016-0261-6 · Cited by 391 · see citing works
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Hell, J. W. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.024 · Cited by 351 · see citing works
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Gross, G. G., Junge, J. A., Mora, R. J., Kwon, H., Olson, C. A., Takahashi, T. T., Liman, E. R., Ellis‐Davies, G. C. R., McGee, A. W., Sabatini, B. L., et al. (2013) · Neuron · doi:10.1016/j.neuron.2013.04.017 · Cited by 357 · see citing works
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Zhang, W., Wu, J., Ward, M. D., Yang, S., Chuang, Y.-A., Xiao, M.-F., Li, R., Leahy, D. J., & Worley, P. F. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.030 · Cited by 162 · see citing works
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Modeling the Dynamic Interaction of Hebbian and Homeostatic Plasticity
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Siddoway, B. A., Hou, H., & Xia, H. (2013) · Neuropharmacology · doi:10.1016/j.neuropharm.2013.07.009 · Cited by 91 · see citing works
Delling, J. P., & Boeckers, T. M. (2021) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-021-09397-8 · Cited by 96 · see citing works
Schrott, R., Acharya, K. S., Itchon-Ramos, N., Hawkey, A. B., Pippen, E., Mitchell, J. T., Kollins, S. H., Levin, E. D., & Murphy, S. K. (2019) · Epigenetics · doi:10.1080/15592294.2019.1656158 · Cited by 91 · see citing works
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Kral, A., Yusuf, P., & Land, R. (2017) · Hearing Research · doi:10.1016/j.heares.2016.08.017 · Cited by 81 · see citing works
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Levy, J. M., Chen, X.-B., Reese, T., & Nicoll, R. (2015) · Neuron · doi:10.1016/j.neuron.2015.07.015 · Cited by 77 · see citing works
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Scudder, S. L., Goo, M. S., Cartier, A. E., Molteni, A., Schwarz, L. A., Wright, R., & Patrick, G. N. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.2452-14.2014 · Cited by 81 · see citing works
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Lu, H. E., MacGillavry, H. D., Frost, N. A., & Blanpied, T. A. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.4364-13.2014 · Cited by 78 · see citing works
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Zhu, J., Zhou, Q., Shang, Y., Li, H., Peng, M., Ke, X., Weng, Z., Zhang, R., Huang, X., Li, S. S. C., et al. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.11.107 · Cited by 68 · see citing works
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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
Proteasome-independent polyubiquitin linkage regulates synapse scaffolding, efficacy, and plasticity
Ma, Q., Ruan, H., Peng, L., Zhang, M., Gack, M. U., & Yao, W. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1620153114 · Cited by 53 · see citing works
Mohanan, A. G., Gunasekaran, S., Jacob, R. S., & Omkumar, R. V. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.855752 · Cited by 57 · see citing works
Ubiquitin-dependent trafficking and turnover of ionotropic glutamate receptors
Goo, M. S., Scudder, S. L., & Patrick, G. N. (2015) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2015.00060 · Cited by 49 · see citing works
Protein Modifications with Ubiquitin as Response to Cerebral Ischemia-Reperfusion Injury
Hochrainer, K. (2017) · Translational Stroke Research · doi:10.1007/s12975-017-0567-x · Cited by 50 · see citing works
Zhang, W., Chuang, Y.-A., Na, Y., Ye, Z., Yang, L., Lin, R., Zhou, J., Wu, J., Qiu, J., Savonenko, A. V., et al. (2019) · Molecular Cell · doi:10.1016/j.molcel.2019.05.004 · Cited by 45 · see citing works
Differential Distribution of Shank and GKAP at the Postsynaptic Density
Tao-Cheng, J.-H., Yang, Y., Reese, T. S., & Döṣemeci, A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0118750 · Cited by 46 · see citing works
Subcellular organization of camkii in rat hippocampal pyramidal neurons
Ding, J., Kennedy, M. B., & Weinberg, R. J. (2013) · Journal of Comparative Neurology · doi:10.1002/cne.23372 · Cited by 45 · see citing works
Jang, S.-S., Royston, S. E., Xu, J., Cavaretta, J. P., Vest, M. O., Lee, K. Y., Lee, S., Jeong, H. G., Lombroso, P. J., & Chung, H. J. (2015) · Molecular Brain · doi:10.1186/s13041-015-0148-4 · Cited by 45 · see citing works
Self-citationde Bartolomeis, A., Buonaguro, E. F., Latte, G., Rossi, R., Marmo, F., Iasevoli, F., & Tomasetti, C. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00240 · Cited by 44 · see citing works
Long-term optical stimulation of channelrhodopsin-expressing neurons to study network plasticity
Lignani, G., Ferrea, E., Difato, F., Amarù, J., Ferroni, E., Lugarà, E., Espinoza, S., Gainetdinov, R. R., Baldelli, P., & Benfenati, F. (2013) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2013.00022 · Cited by 43 · see citing works
Lee, K. Y., Royston, S. E., Vest, M. O., Ley, D. J., Lee, S., Bolton, E. C., & Chung, H. J. (2015) · Molecular Brain · doi:10.1186/s13041-015-0094-1 · Cited by 44 · see citing works
Self-citationRole of physical and mental training in brain network configuration
Foster, P. P. (2015) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2015.00117 · Cited by 44 · see citing works
TRIM3 Regulates the Motility of the Kinesin Motor Protein KIF21B
Labonté, D., Thies, E., Pechmann, Y., Groffen, A. J. A., Verhage, M., Smit, A. B., van Kesteren, R. E., & Kneussel, M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0075603 · Cited by 42 · see citing works
The Role of Zinc and NMDA Receptors in Autism Spectrum Disorders
Lee, K. C., Mills, Z., Cheung, P. Y., Cheyne, J. E., & Montgomery, J. M. (2022) · Pharmaceuticals · doi:10.3390/ph16010001 · Cited by 40 · see citing works
O’Connor, E. C., Bariselli, S., & Bellone, C. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12510 · Cited by 38 · see citing works
Hebbian and Homeostatic Synaptic Plasticity—Do Alterations of One Reflect Enhancement of the Other?
Galanis, C., & Vlachos, A. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2020.00050 · Cited by 39 · see citing works
Schreiber, J., Végh, M. J., Dawitz, J., Kroon, T., Loos, M., Labonté, D., Li, K. W., van Nierop, P., van Diepen, M. T., Zeeuw, C. I. D., et al. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201506048 · Cited by 37 · see citing works
de Bartolomeis, A., Barone, A., Buonaguro, E. F., Tomasetti, C., Vellucci, L., & Iasevoli, F. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104596 · Cited by 37 · 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
Chen, X., Jia, B., Araki, Y., Liu, B., Ye, F., Huganir, R. L., & Zhang, M. (2022) · Cell Research · doi:10.1038/s41422-022-00697-9 · Cited by 34 · see citing works
USP8 Deubiquitinates SHANK3 to Control Synapse Density and SHANK3 Activity-Dependent Protein Levels
Campbell, M. K., & Sheng, M. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.3305-17.2018 · Cited by 34 · see citing works
Self-citationWills, T. A., Baucum, A. J., Holleran, K. M., Chen, Y., Pasek, J. G., Delpire, E. J., Tabb, D. L., Colbran, R. J., & Winder, D. G. (2015) · Addiction Biology · doi:10.1111/adb.12319 · Cited by 33 · see citing works
Hallin, E. I., Eriksen, M. S., Baryshnikov, S., Nikolaienko, O., Grødem, S., Hosokawa, T., Hayashi, Y., Bramham, C. R., & Kursula, P. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14556 · Cited by 32 · see citing works
Hadar, A., Milanesi, E., Squassina, A., Niola, P., Chillotti, C., Pasmanik-Chor, M., Yaron, O., Pavel Martasek, E., Rehavi, M., Weissglas‐Volkov, D., et al. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.179 · Cited by 31 · see citing works
Wu, H., Chen, X., Shen, Z., Li, H., Liang, S., Lu, Y., & Zhang, M. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.11.011 · Cited by 30 · see citing works
Katsumata, Y., Nelson, P. T., Estus, S., & Fardo, D. W. (2019) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2018.10.017 · Cited by 30 · see citing works
A kinome-wide RNAi screen identifies ERK2 as a druggable regulator of Shank3 stability
Wang, L., Adamski, C. J., Bondar, V. V., Craigen, E., Collette, J. R., Pang, K., Han, K., Jain, A., Jung, S. Y., Liu, Z., et al. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0325-9 · Cited by 30 · see citing works
A bidirectional switch in the Shank3 phosphorylation state biases synapses toward up- or downscaling
Wu, C.-H., Tatavarty, V., Beltran, P. M., Guerrero, A., Keshishian, H., Krug, K., MacMullan, M. A., Li, L., Carr, S. A., Cottrell, J. R., et al. (2022) · eLife · doi:10.7554/elife.74277 · Cited by 27 · see citing works
Lee, K. Y., & Chung, H. J. (2014) · Neuroscience · doi:10.1016/j.neuroscience.2014.07.038 · Cited by 28 · see citing works
Persistent synaptic scaling independent of AMPA receptor subunit composition
Altimimi, H. F., & Stellwagen, D. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.1102-13.2013 · Cited by 25 · see citing works
Drugging the methylome: DNA methylation and memory
Kennedy, A. J., & Sweatt, J. D. (2016) · Critical Reviews in Biochemistry and Molecular Biology · doi:10.3109/10409238.2016.1150958 · Cited by 24 · see citing works
SAPAP Scaffold Proteins: From Synaptic Function to Neuropsychiatric Disorders
Bai, Y., Wang, H., & Li, C. (2022) · Cells · doi:10.3390/cells11233815 · Cited by 24 · see citing works
Structural basis for PDZ domain interactions in the post‐synaptic density scaffolding protein Shank3
Ponna, S. K., Ruskamo, S., Myllykoski, M., Keller, C., Boeckers, T. M., & Kursula, P. (2018) · Journal of Neurochemistry · doi:10.1111/jnc.14322 · Cited by 25 · see citing works
Latina, V., Caioli, S., Zona, C., Ciotti, M. T., Borreca, A., Calissano, P., & Amadoro, G. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00487 · Cited by 26 · see citing works
Remodeling of the Homer-Shank interactome mediates homeostatic plasticity
Heavner, W. E., Lautz, J. D., Speed, H. E., Gniffke, E. P., Immendorf, K. B., Welsh, J. P., Baertsch, N. A., & Smith, S. E. P. (2021) · Science Signaling · doi:10.1126/scisignal.abd7325 · Cited by 24 · see citing works
Salazar, I. L., Caldeira, M. V., Curcio, M., & Duarte, C. B. (2015) · Neurochemical Research · doi:10.1007/s11064-015-1752-5 · Cited by 25 · see citing works
Shanks — multidomain molecular scaffolds of the postsynaptic density
Kursula, P. (2019) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.01.007 · Cited by 23 · see citing works
de Bartolomeis, A., Avagliano, C., Vellucci, L., D'Ambrosio, L., Manchia, M., D'Urso, G., Buonaguro, E., & Iasevoli, F. (2019) · Neuroscience and Biobehavioral Reviews · doi:10.1016/j.neubiorev.2019.08.019 · Cited by 17 · see citing works
The Ubiquitinated Axon: Local Control of Axon Development and Function by Ubiquitin
Pinto, M. J., Tomé, D., & Almeida, R. D. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.2251-20.2021 · Cited by 19 · see citing works
Hippocampal monoamine receptor complex levels linked to spatial memory decline in the aging C57BL/6J
Saroja, S. R., Kim, E., Shanmugasundaram, B., Höger, H., & Lübec, G. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.01.042 · Cited by 18 · see citing works
Structural properties and peptide ligand binding of the capsid homology domains of human Arc
Hallin, E. I., Bramham, C. R., & Kursula, P. (2021) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2021.100975 · Cited by 15 · see citing works
Vellucci, L., Ciccarelli, M., Buonaguro, E. F., Fornaro, M., D’Urso, G., Simone, G. D., Iasevoli, F., Barone, A., & de Bartolomeis, A. (2023) · Biomolecules · doi:10.3390/biom13081220 · Cited by 16 · see citing works
Structure of the GH1 domain of guanylate kinase-associated protein from Rattus norvegicus
Tong, J., Yang, H., Eom, S. H., Chun, C., & Im, Y. J. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.08.073 · Cited by 14 · see citing works
Neuronal Synapses: Microscale Signal Processing Machineries Formed by Phase Separation?
Feng, Z., Zeng, M., Chen, X., & Zhang, M. (2018) · Biochemistry · doi:10.1021/acs.biochem.8b00313 · Cited by 13 · see citing works
SAPAP3 regulates epileptic seizures involving GluN2A in post-synaptic densities
Zhang, Y., Wu, J., Yan, Y., Gu, Y., Ma, Y., Wang, M., Zhang, H., Tao, K., Lü, Y., Yu, W., et al. (2022) · Cell Death and Disease · doi:10.1038/s41419-022-04876-9 · Cited by 13 · see citing works
Stoichiometry of scaffold complexes in living neurons - DLC2 as a dimerization engine for GKAP
Moutin, E., Compan, V., Raynaud, F., Clerté, C., Bouquier, N., Labesse, G., Ferguson, M., Fagni, L., Royer, C. A., & Perroy, J. (2014) · Journal of Cell Science · doi:10.1242/jcs.145748 · Cited by 15 · see citing works
Katano, T., Fukuda, M., Furue, H., Yamazaki, M., Abe, M., Watanabe, M., Nishida, K., Yao, I., Yamada, A., Hata, Y., et al. (2016) · eNeuro · doi:10.1523/eneuro.0110-16.2016 · Cited by 13 · see citing works
Miski, M., Keömley-Horváth, B. M., Megyeriné, D. R., Csikász‐Nagy, A., & Gáspári, Z. (2022) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1009758 · Cited by 11 · see citing works
The ubiquitin-editing enzyme A20 regulates synapse remodeling and efficacy
Mei, S., Ruan, H., Ma, Q., & Yao, W. (2019) · Brain Research · doi:10.1016/j.brainres.2019.146569 · Cited by 12 · see citing works
Wang, Y., Lin, J., Li, J., Yan, A. L., Li, W., He, X., & Ma, H. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0146-23.2023 · Cited by 13 · see citing works
Kootar, S., Frandemiche, M., Dhib, G., Mouska, X., Lorivel, T., Poupon, G., Hunt, H., Tronche, F., Bethus, I., Barik, J., et al. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.07.001 · Cited by 11 · see citing works
Wu, X., Xiong, D., Liu, R., Lai, X., Tian, Y., Xie, Z., Chen, L., Hu, L., Duan, J., Gao, X., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-58275-7 · Cited by 11 · see citing works
Imaging of spine synapses using super-resolution microscopy
Kashiwagi, Y., & Okabe, S. (2021) · Anatomical Science International · doi:10.1007/s12565-021-00603-0 · Cited by 9 · see citing works
TDMA for Long Distance Wireless Networks
Leffler, S., & Consulting, E. (2009) · Cited by 8 · see citing works
Structural properties and peptide ligand binding of the capsid homology domains of human ArcPreprint
Hallin, E. I., Bramham, C. R., & Kursula, P. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.17.423319 · Cited by 8 · see citing works
Fu, Y., Du, L., Guo, J., Long, H., Xiao, W., Xiao, W., Feng, L., Luo, Z., & Xiao, B. (2020) · Molecular Neurobiology · doi:10.1007/s12035-020-01968-5 · Cited by 7 · see citing works
Enthalpy–entropy compensation in the binding of peptide ligands to human Arc
Kang, J., & Smidtas, L. (2021) · Biochemistry and Biophysics Reports · doi:10.1016/j.bbrep.2021.101088 · Cited by 7 · see citing works
Cai, H., Ni, L., Hu, X., & Ding, X. (2021) · Aging · doi:10.18632/aging.203413 · Cited by 6 · see citing works
- Authors
- Shin, S. M., Zhang, N., Hansen, J., Gerges, N. Z., Pak, D. T. S., Sheng, M., & Lee, S. H.
- Affiliations
- Medical College of Wisconsin (US)
- Georgetown University Medical Center (US)
- Genentech (US)
- Corresponding author
- Lee, Sang H
- Venue
- Nature Neuroscience
- Published
- 2012-11-11
- Volume
- 15
- Issue
- 12
- Pages
- 1655-1666
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC3804128
- OpenAlex
- W2079052947
- Cited by
- 126
- References
- 51
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 12 · 2021: 11 · 2020: 7 · 2019: 8 · 2018: 12 · 2017: 9 · 2016: 9 · 2015: 13 · 2014: 17 · 2013: 10
- FWCI
- 5.27
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-sa)
- Funders
- National Institute on Aging (R01AG032320)
- National Institute of Mental Health (R01MH078135)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Keywords
- GKAP, postsynaptic density, synaptic scaling, homeostatic plasticity, CaMKII, NMDA receptor, L-type calcium channels, ubiquitin-proteasome system, protein turnover, PSD-95, shank, Homer, myosin Va, hippocampal neurons
- MeSH terms
- SAP90-PSD95 Associated Proteins, Disks Large Homolog 4 Protein, Animals, Cells, Cultured, Chlorocebus aethiops, Double-Blind Method, Enzyme Activation, Homeostasis, Membrane Proteins, Nerve Tissue Proteins, Neuronal Plasticity, Synapses, COS Cells, Guanine Nucleotide Exchange Factors, Intracellular Signaling Peptides and Proteins, Rats, Synaptic Potentials
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