Dynamic bi-directional phosphorylation events associated with the reciprocal regulation of synapses during homeostatic up- and down-scaling

Aakalu, 2001, Dynamic visualization of local protein synthesis in hippocampal neurons, Neuron, 30, 489, 10.1016/S0896-6273(01)00295-1 Amir, 1999, Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2, Nat. Genet., 23, 185, 10.1038/13810 Bai, 2020, Deep Multilayer Brain Proteomics Identifies Molecular Networks in Alzheimer’s Disease Progression, Neuron, 105, 975, 10.1016/j.neuron.2019.12.015 Bambah-Mukku, 2014, A positive autoregulatory BDNF feedback loop via C/EBPβ mediates hippocampal memory consolidation, J. Neurosci., 34, 12547, 10.1523/JNEUROSCI.0324-14.2014 Bates, 2015, Fitting linear mixed-effects models using lme4, J. Stat. Softw., 67 Bats, 2007, The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking, Neuron, 53, 719, 10.1016/j.neuron.2007.01.030 Benjamini, 1995, Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing, J. R. Stat. Soc. B, 57, 289 Blackman, 2012, A critical and cell-autonomous role for MeCP2 in synaptic scaling up, J. Neurosci., 32, 13529, 10.1523/JNEUROSCI.3077-12.2012 Blum, 1999, A mitogen-activated protein kinase cascade in the CA1/CA2 subfield of the dorsal hippocampus is essential for long-term spatial memory, J. Neurosci., 19, 3535, 10.1523/JNEUROSCI.19-09-03535.1999 Brüning, 2019, Sleep-wake cycles drive daily dynamics of synaptic phosphorylation, Science, 366, eaav3617, 10.1126/science.aav3617 Castillo, 2002, RIM1α is required for presynaptic long-term potentiation, Nature, 415, 327, 10.1038/415327a Chen, 2003, Derepression of BDNF transcription involves calcium-dependent phosphorylation of MeCP2, Science, 302, 885, 10.1126/science.1086446 Cox, 2008, MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification, Nat. Biotechnol., 26, 1367, 10.1038/nbt.1511 Cox, 2014, Accurate proteome-wide label-free quantification by delayed normalization and maximal peptide ratio extraction, termed MaxLFQ, Mol. Cell. Proteomics, 13, 2513, 10.1074/mcp.M113.031591 Czernik, 1987, Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I, Proc. Natl. Acad. Sci. USA, 84, 7518, 10.1073/pnas.84.21.7518 Davis, 2006, Homeostatic control of neural activity: from phenomenology to molecular design, Annu. Rev. Neurosci., 29, 307, 10.1146/annurev.neuro.28.061604.135751 Diering, 2017, Homer1a drives homeostatic scaling-down of excitatory synapses during sleep, Science, 355, 511, 10.1126/science.aai8355 Dörrbaum, 2020, Proteome dynamics during homeostatic scaling in cultured neurons, eLife, 9, e52939, 10.7554/eLife.52939 Dosemeci, 2010, Regulation of phosphorylation at the postsynaptic density during different activity states of Ca2+/calmodulin-dependent protein kinase II, Biochem. Biophys. Res. Commun., 391, 78, 10.1016/j.bbrc.2009.10.167 Ehlers, 2003, Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system, Nat. Neurosci., 6, 231, 10.1038/nn1013 Engholm-Keller, 2019, The temporal profile of activity-dependent presynaptic phospho-signalling reveals long-lasting patterns of poststimulus regulation, PLoS Biol., 17, e3000170, 10.1371/journal.pbio.3000170 Fahs, 2016, Approaches to Study Phosphatases, ACS Chem. Biol., 11, 2944, 10.1021/acschembio.6b00570 Farley, 1991, Protein kinase C inhibitors prevent induction and continued expression of cell memory in Hermissenda type B photoreceptors, Proc. Natl. Acad. Sci. USA, 88, 2016, 10.1073/pnas.88.5.2016 Ferrero, 2007, Ca2+/calmodulin kinase II increases ryanodine binding and Ca2+-induced sarcoplasmic reticulum Ca2+ release kinetics during β-adrenergic stimulation, J. Mol. Cell. Cardiol., 43, 281, 10.1016/j.yjmcc.2007.05.022 Franceschini, 2013, STRING v9.1: protein-protein interaction networks, with increased coverage and integration, Nucleic Acids Res., 41, D808, 10.1093/nar/gks1094 Fukunaga, 1993, Long-term potentiation is associated with an increased activity of Ca2+/calmodulin-dependent protein kinase II, J. Biol. Chem., 268, 7863, 10.1016/S0021-9258(18)53037-4 Glock, 2020, The mRNA translation landscape in the synaptic neuropil, bioRxiv Greengard, 1993, Synaptic vesicle phosphoproteins and regulation of synaptic function, Science, 259, 780, 10.1126/science.8430330 Hornbeck, 2015, PhosphoSitePlus, 2014: mutations, PTMs and recalibrations, Nucleic Acids Res., 43, D512, 10.1093/nar/gku1267 Huke, 2008, Ryanodine receptor phosphorylation at Serine 2030, 2808 and 2814 in rat cardiomyocytes, Biochem. Biophys. Res. Commun., 376, 80, 10.1016/j.bbrc.2008.08.084 Humphrey, 2015, Protein Phosphorylation: A Major Switch Mechanism for Metabolic Regulation, Trends Endocrinol. Metab., 26, 676, 10.1016/j.tem.2015.09.013 Ibata, 2008, Rapid synaptic scaling induced by changes in postsynaptic firing, Neuron, 57, 819, 10.1016/j.neuron.2008.02.031 Jang, 2015, Regulation of STEP61 and tyrosine-phosphorylation of NMDA and AMPA receptors during homeostatic synaptic plasticity, Mol. Brain, 8, 55, 10.1186/s13041-015-0148-4 Kalashnikova, 2010, SynDIG1: an activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development, Neuron, 65, 80, 10.1016/j.neuron.2009.12.021 Kim, 2004, PDZ domain proteins of synapses, Nat. Rev. Neurosci., 5, 771, 10.1038/nrn1517 Ko, 2006, SALM synaptic cell adhesion-like molecules regulate the differentiation of excitatory synapses, Neuron, 50, 233, 10.1016/j.neuron.2006.04.005 Kohansal-Nodehi, 2016, Analysis of protein phosphorylation in nerve terminal reveals extensive changes in active zone proteins upon exocytosis, eLife, 5, 1, 10.7554/eLife.14530 Kolde, 2019 Lee, 2006, Synaptic plasticity and phosphorylation, Pharmacol. Ther., 112, 810, 10.1016/j.pharmthera.2006.06.003 Li, 2016, Long-term potentiation modulates synaptic phosphorylation networks and reshapes the structure of the postsynaptic interactome, Sci. Signal., 9, rs8, 10.1126/scisignal.aaf6716 Lisman, 1988, Feasibility of long-term storage of graded information by the Ca2+/calmodulin-dependent protein kinase molecules of the postsynaptic density, Proc. Natl. Acad. Sci. USA, 85, 5320, 10.1073/pnas.85.14.5320 Lisman, 2015, Biochemical principles underlying the stable maintenance of LTP by the CaMKII/NMDAR complex, Brain Res., 1621, 51, 10.1016/j.brainres.2014.12.010 Malinow, 1988, Persistent protein kinase activity underlying long-term potentiation, Nature, 335, 820, 10.1038/335820a0 Marder, 2003, Current compensation in neuronal homeostasis, Neuron, 37, 2, 10.1016/S0896-6273(02)01173-X Martin, 1997, MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia, Neuron, 18, 899, 10.1016/S0896-6273(00)80330-X Miller, 1986, Regulation of brain type II Ca2+/calmodulin-dependent protein kinase by autophosphorylation: a Ca2+-triggered molecular switch, Cell, 44, 861, 10.1016/0092-8674(86)90008-5 Nestler, 1983, Protein phosphorylation in the brain, Nature, 305, 583, 10.1038/305583a0 O’Brien, 1998, Activity-dependent modulation of synaptic AMPA receptor accumulation, Neuron, 21, 1067, 10.1016/S0896-6273(00)80624-8 Pedersen, 2017, Site-Specific Phosphorylation of PSD-95 PDZ Domains Reveals Fine-Tuned Regulation of Protein-Protein Interactions, ACS Chem. Biol., 12, 2313, 10.1021/acschembio.7b00361 Sanderson, 2018, Control of Homeostatic Synaptic Plasticity by AKAP-Anchored Kinase and Phosphatase Regulation of Ca2+-Permeable AMPA Receptors, J. Neurosci., 38, 2863, 10.1523/JNEUROSCI.2362-17.2018 Schanzenbächer, 2016, Nascent Proteome Remodeling following Homeostatic Scaling at Hippocampal Synapses, Neuron, 92, 358, 10.1016/j.neuron.2016.09.058 Schanzenbächer, 2018, Time- and polarity-dependent proteomic changes associated with homeostatic scaling at central synapses, eLife, 7, 1, 10.7554/eLife.33322 Seabold, 2008, The SALM family of adhesion-like molecules forms heteromeric and homomeric complexes, J. Biol. Chem., 283, 8395, 10.1074/jbc.M709456200 Selcher, 1999, A necessity for MAP kinase activation in mammalian spatial learning, Learn. Mem., 6, 478, 10.1101/lm.6.5.478 Shannon, 2003, Cytoscape: a software environment for integrated models of biomolecular interaction networks, Genome Res., 13, 2498, 10.1101/gr.1239303 Sharma, 2015, Cell type- and brain region-resolved mouse brain proteome, Nat. Neurosci., 18, 1819, 10.1038/nn.4160 Simsek-Duran, 2004, Adapter protein 14-3-3 is required for a presynaptic form of LTP in the cerebellum, Nat. Neurosci., 7, 1296, 10.1038/nn1348 Smolen, 2008, Bistable MAP kinase activity: a plausible mechanism contributing to maintenance of late long-term potentiation, Am. J. Physiol. Cell Physiol., 294, C503, 10.1152/ajpcell.00447.2007 Thiagarajan, 2005, Adaptation to synaptic inactivity in hippocampal neurons, Neuron, 47, 725, 10.1016/j.neuron.2005.06.037 Thomas, 2004, MAPK cascade signalling and synaptic plasticity, Nat. Rev. Neurosci., 5, 173, 10.1038/nrn1346 Turrigiano, 2008, The self-tuning neuron: synaptic scaling of excitatory synapses, Cell, 135, 422, 10.1016/j.cell.2008.10.008 Turrigiano, 2012, Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function, Cold Spring Harb. Perspect. Biol., 4, a005736, 10.1101/cshperspect.a005736 Turrigiano, 1998, Activity-dependent scaling of quantal amplitude in neocortical neurons, Nature, 391, 892, 10.1038/36103 Tyanova, 2016, The Perseus computational platform for comprehensive analysis of (prote)omics data, Nat. Methods, 13, 731, 10.1038/nmeth.3901 Ubersax, 2007, Mechanisms of specificity in protein phosphorylation, Nat. Rev. Mol. Cell Biol., 8, 530, 10.1038/nrm2203 Vallejo, 2017, Posttranslational Modifications Regulate the Postsynaptic Localization of PSD-95, Mol. Neurobiol., 54, 1759, 10.1007/s12035-016-9745-1 van Gelder, 2020, Temporal quantitative proteomics of mGluR-induced protein translation and phosphorylation in neurons, Mol. Cell. Proteomics, 19, 1952, 10.1074/mcp.RA120.002199 Vizcaíno, 2013, The PRoteomics IDEntifications (PRIDE) database and associated tools: status in 2013, Nucleic Acids Res., 41, D1063, 10.1093/nar/gks1262 Wang, 2006, A novel family of adhesion-like molecules that interacts with the NMDA receptor, J. Neurosci., 26, 2174, 10.1523/JNEUROSCI.3799-05.2006 Wiredja, 2017, The KSEA App: a web-based tool for kinase activity inference from quantitative phosphoproteomics, Bioinformatics, 33, 3489, 10.1093/bioinformatics/btx415 Yong, 2020, Tyrosine phosphorylation of the AMPA receptor subunit GluA2 gates homeostatic synaptic plasticity, Proc. Natl. Acad. Sci. USA, 117, 4948, 10.1073/pnas.1918436117 Zhou, 2006, Brain-specific phosphorylation of MeCP2 regulates activity-dependent Bdnf transcription, dendritic growth, and spine maturation, Neuron, 52, 255, 10.1016/j.neuron.2006.09.037 Zhu, 2002, Ras and Rap control AMPA receptor trafficking during synaptic plasticity, Cell, 110, 443, 10.1016/S0092-8674(02)00897-8