Cited by 320Advanced Proteomics Techniques and ApplicationsNeuroscience and Neuropharmacology ResearchProtein Kinase Regulation and GTPase Signaling

The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.

Proteomic Analysis of in Vivo Phosphorylated Synaptic Proteins

Open access

Collins, Mark O., Yu, Lu, Coba, Marcelo P., Husi, Holger, Campuzano, Iain, Blackstock, Walter P., Choudhary, Jyoti S., Grant, Seth G.N.·2005·Journal of Biological Chemistry

DOI 10.1074/jbc.m411220200

Open this paper in CoChat — free account

Abstract

In the nervous system, protein phosphorylation is an essential feature of synaptic function. Although protein phosphorylation is known to be important for many synaptic processes and in disease, little is known about global phosphorylation of synaptic proteins. Heterogeneity and low abundance make protein phosphorylation analysis difficult, particularly for mammalian tissue samples. Using a new approach, combining both protein and peptide immobilized metal affinity chromatography and mass spectrometry data acquisition strategies, we have produced the first large scale map of the mouse synapse phosphoproteome. We report over 650 phosphorylation events corresponding to 331 sites (289 have been unambiguously assigned), 92% of which are novel. These represent 79 proteins, half of which are novel phosphoproteins, and include several highly phosphorylated proteins such as MAP1B (33 sites) and Bassoon (30 sites). An additional 149 candidate phosphoproteins were identified by profiling the composition of the protein immobilized metal affinity chromatography enrichment. All major synaptic protein classes were observed, including components of important pre- and postsynaptic complexes as well as low abundance signaling proteins. Bioinformatic and in vitro phosphorylation assays of peptide arrays suggest that a small number of kinases phosphorylate many proteins and that each substrate is phosphorylated by many kinases. These data substantially increase existing knowledge of synapse pro…

Integrity signals

Registry

Crossref · 10.1074/jbc.m411220200

Cites

43 of 43 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

We couldn’t retrieve this paper’s full text, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

THE SYNAPTIC VESICLE CYCLE
Südhof, T. C. (2004) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131412 · Cited by 2,491
Phosphoproteome analysis by mass spectrometry and its application to Saccharomyces cerevisiae
Ficarro, S. B., McCleland, M. L., Stukenberg, P. T., Burke, D. J., Ross, M. M., Shabanowitz, J., Hunt, D. F., & White, F. M. (2002) · Nature Biotechnology · doi:10.1038/nbt0302-301 · Cited by 1,636
Scansite 2.0: proteome-wide prediction of cell signaling interactions using short sequence motifs
Obenauer, J. C. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkg584 · Cited by 1,609
Large-scale characterization of HeLa cell nuclear phosphoproteins
Beausoleil, S. A., Jedrychowski, M. P., Schwartz, D., Elias, J. E., Villén, J., Li, J., Cohn, M. A., Cantley, L. C., & Gygi, S. P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0404720101 · Cited by 1,376
Synaptic Vesicle Phosphoproteins and Regulation of Synaptic Function
Greengard, P., Valtorta, F., Czernik, A. J., & Benfenati, F. (1993) · Science · doi:10.1126/science.8430330 · Cited by 1,311
Proteomic analysis of NMDA receptor–adhesion protein signaling complexes
Husi, H., Ward, M. A., Choudhary, J. S., Blackstock, W. P., & Grant, S. G. N. (2000) · Nature Neuroscience · doi:10.1038/76615 · Cited by 1,194
Self-citation
Homer Binds a Novel Proline-Rich Motif and Links Group 1 Metabotropic Glutamate Receptors with IP3 Receptors
Tu, J. C., Xiao, B., Yuan, J. P., Lanahan, A. A., Leoffert, K., Li, M., Linden, D. J., & Worley, P. F. (1998) · Neuron · doi:10.1016/s0896-6273(00)80589-9 · Cited by 862
Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities.
Carlin, R. K., Grab, D. J., Cohen, R. S., & Siekevitz, P. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.86.3.831 · Cited by 788
Isolation of phosphoproteins by immobilized metal (Fe3+) affinity chromatography
Andersson, L., & Porath, J. O. (1986) · Analytical Biochemistry · doi:10.1016/0003-2697(86)90523-3 · Cited by 774
Aberrant Cdk5 activation by p25 triggers pathological events leading to neurodegeneration and neurofibrillary tangles
Cruz, J. C., Tseng, H.-C., Goldman, J. A., Shih, H., & Tsai, L.-H. (2003) · Neuron · doi:10.1016/s0896-6273(03)00627-5 · Cited by 609
Large-scale Analysis of in Vivo Phosphorylated Membrane Proteins by Immobilized Metal Ion Affinity Chromatography and Mass Spectrometry
Nühse, T. S., Stensballe, A., Jensen, O. N., & Peck, S. C. (2003) · Molecular & Cellular Proteomics · doi:10.1074/mcp.t300006-mcp200 · Cited by 545
Phosphoproteomics of the Arabidopsis Plasma Membrane and a New Phosphorylation Site Database[W]
Nühse, T. S., Stensballe, A., Jensen, O. N., & Peck, S. C. (2004) · The Plant Cell · doi:10.1105/tpc.104.023150 · Cited by 478
Semiquantitative Proteomic Analysis of Rat Forebrain Postsynaptic Density Fractions by Mass Spectrometry
Peng, J., Kim, M. J., Cheng, D., Duong, D. M., Gygi, S. P., & Sheng, M. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400103200 · Cited by 473
Targeting of PKA to Glutamate Receptors through a MAGUK-AKAP Complex
Colledge, M., Dean, R. A., Scott, G. K., Langeberg, L. K., Huganir, R. L., & Scott, J. D. (2000) · Neuron · doi:10.1016/s0896-6273(00)00013-1 · Cited by 467
Studies on the phosphorylation of myelin basic protein by protein kinase C and adenosine 3‘:5‘-monophosphate-dependent protein kinase.
Kishimoto, A., Nishiyama, K., Nakanishi, H., Uratsuji, Y., Nomura, H., Takeyama, Y., & Nishizuka, Y. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)38898-1 · Cited by 417
Identification of PSD-95 as a Regulator of Dopamine-Mediated Synaptic and Behavioral Plasticity
Yao, W., Gainetdinov, R. R., Arbuckle, M. I., Sotnikova, T. D., Cyr, M., Beaulieu, J., Torres, G. E., Grant, S. G. N., & Caron, M. G. (2004) · Neuron · doi:10.1016/s0896-6273(04)00048-0 · Cited by 390
Self-citation
Unitary Assembly of Presynaptic Active Zones from Piccolo-Bassoon Transport Vesicles
Shapira, M., Zhai, R. G., Dresbach, T., Bresler, T., Torres, V. I., Gundelfinger, E. D., Ziv, N. E., & Garner, C. C. (2003) · Neuron · doi:10.1016/s0896-6273(03)00207-1 · Cited by 363
Phosphoproteomic Analysis of the Developing Mouse Brain
Ballif, B. A., Villén, J., Beausoleil, S. A., Schwartz, D., & Gygi, S. P. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m400085-mcp200 · Cited by 345
Molecular organization of the postsynaptic specialization
Sheng, M. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111146298 · Cited by 343
Proteomics Analysis of Rat Brain Postsynaptic Density
Li, K. W., Hornshaw, M. P., van der Schors, R. C., Watson, R. B., Tate, S. A., Casetta, B., Jiménez, C. R., Gouwenberg, Y., Gundelfinger, E. D., Smalla, K., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m303116200 · Cited by 249
Phosphorylation of RIM1α by PKA Triggers Presynaptic Long-Term Potentiation at Cerebellar Parallel Fiber Synapses
Lónárt, G., Schoch, S., Kaeser, P. S., Larkin, C. J., Südhof, T. C., & Linden, D. J. (2003) · Cell · doi:10.1016/s0092-8674(03)00727-x · Cited by 248
Protein phosphorylation and the regulation of synaptic membrane traffic
Turner, K. M., Burgoyne, R. D., & Morgan, A. (1999) · Trends in Neurosciences · doi:10.1016/s0166-2236(99)01436-8 · Cited by 240
Structure of the SH3-Guanylate Kinase Module from PSD-95 Suggests a Mechanism for Regulated Assembly of MAGUK Scaffolding Proteins
McGee, A. W., Dakoji, S., Olsen, O., Bredt, D. S., Lim, W. A., & Prehoda, K. E. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00411-7 · Cited by 239
Molecular constituents of the postsynaptic density fraction revealed by proteomic analysis using multidimensional liquid chromatography‐tandem mass spectrometry
Yoshimura, Y., Yamauchi, Y., Shinkawa, T., Taoka, M., Donai, H., Takahashi, N., Isobe, T., & Yamauchi, T. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02136.x · Cited by 208
Large-scale synthesis of peptides
Andersson, L. I., Blomberg, L., Flegel, M., Lepša, L., Nilsson, B., & Verlander, M. S. (2000) · Biopolymers · doi:10.1002/1097-0282(2000)55:3 · Cited by 198
IRBIT, a Novel Inositol 1,4,5-Trisphosphate (IP3) Receptor-binding Protein, Is Released from the IP3 Receptor upon IP3 Binding to the Receptor
Ando, H., Mizutani, A., Matsuura, T., & Mikoshiba, K. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210119200 · Cited by 195
Type II regulatory subunit dimerization determines the subcellular localization of the cAMP-dependent protein kinase.
Scott, J. D., Stofko, R. E., McDonald, J. R., Comer, J., Vitalis, E. A., & Mangili, J. A. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)45777-8 · Cited by 186
Structural Characterization of the Intramolecular Interaction between the SH3 and Guanylate Kinase Domains of PSD-95
Tavares, G., Panepucci, E. H., & Brünger, A. T. (2001) · Molecular Cell · doi:10.1016/s1097-2765(01)00416-6 · Cited by 163
Persistent and transcriptionally-dependent increase in protein phosphorylation in long-term facilitation ofAplysia sensory neurons
Sweatt, J. D., & Kandel, E. R. (1989) · Nature · doi:10.1038/339051a0 · Cited by 132
Neuropathic Sensitization of Behavioral Reflexes and Spinal NMDA Receptor/CaM Kinase II Interactions Are Disrupted in PSD-95 Mutant Mice
Garry, E. M., Moss, A., Delaney, A., O’Neill, F., Blakemore, J., Bowen, J., Husi, H., Mitchell, R., Grant, S. G. N., & Fleetwood-Walker, S. M. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00084-8 · Cited by 125
Self-citation
Co-stimulation of mGluR5 and N-Methyl-D-aspartate Receptors Is Required for Potentiation of Excitatory Synaptic Transmission in Hippocampal Neurons
Kotecha, S. A., Jackson, M. F., Al‐Mahrouki, A., Roder, J., Orser, B. A., & MacDonald, J. F. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301946200 · Cited by 114
CaMKII-dependent Phosphorylation Regulates SAP97/NR2A Interaction
Gardoni, F., Mauceri, D., Fiorentini, C., Bellone, C., Missale, C., Cattabeni, F., & Luca, M. D. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303576200 · Cited by 105
Molecular Basis for the Substrate Specificity of NIMA-related Kinase-6 (NEK6)
Lizcano, J. M., Deák, M., MORRICE, N. A., Kieloch, A., Hastie, C. J., Dong, L., Schutkowski, M., Reimer, U., & Alessi, D. R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m202042200 · Cited by 105
Phosphorylation–dependent interaction of the N‐methyl‐ d ‐aspartate receptor ε2 subunit with phosphatidylinositol 3‐kinase
Hisatsune, C., Umemori, H., Mishina, M., & Yamamoto, T. S. (1999) · Genes to Cells · doi:10.1046/j.1365-2443.1999.00287.x · Cited by 85
Proteomic analysis of native metabotropic glutamate receptor 5 protein complexes reveals novel molecular constituents
Farr, C. D., Gafken, P. R., Norbeck, A. D., Doneanu, C. E., Stapels, M. D., Barofsky, D. F., Minami, M., & Saugstad, J. A. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02735.x · Cited by 82
Target Specificity Analysis of the Abl Kinase using Peptide Microarray Data
Rychlewski, L., Kschischo, M., Dong, L., Schutkowski, M., & Reimer, U. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2003.12.052 · Cited by 78
Diversity of Calcium Signaling by Metabotropic Glutamate Receptors
Kawabata, S., Kohara, A., Tsutsumi, R., Itahana, H., Hayashibe, S., Yamaguchi, T., & Okada, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.28.17381 · Cited by 72
Analysis of Protein Phosphorylation by Hypothesis-Driven Multiple-Stage Mass Spectrometry
Chang, E. J., Archambault, V., McLachlin, D. T., Krutchinsky, A. N., & Chait, B. T. (2004) · Analytical Chemistry · doi:10.1021/ac049637h · Cited by 71
Identification of Phosphoproteins and Their Phosphorylation Sites in the WEHI-231 B Lymphoma Cell Line
Shu, H., Chen, S., Bi, Q., Mumby, M. C., & Brekken, D. L. (2004) · Molecular & Cellular Proteomics · doi:10.1074/mcp.d300003-mcp200 · Cited by 70
Physiological regulation of Munc18/nSec1 phosphorylation on serine‐313
Craig, T. J., Evans, G. J., & Morgan, A. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01955.x · Cited by 65
Regulation of neuronal plasticity in the central nervous system by phosphorylation and dephosphorylation
Tokuda, M., & Hatase, O. (1998) · Molecular Neurobiology · doi:10.1007/bf02802028 · Cited by 59
Identification of PSD-93 as a Substrate for the Src Family Tyrosine Kinase Fyn
Nada, S., Shima, T., Yanai, H., Husi, H., Grant, S. G. N., Okada, M., & Akiyama, T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m303873200 · Cited by 59
Self-citation
Synapse signalling complexes and networks: machines underlying cognition
Grant, S. G. N. (2003) · BioEssays · doi:10.1002/bies.10381 · Cited by 48
Self-citation

Research works printed but not linked: 1

Nourry, 2003, Science's STKE

Sorted by citations

A probability-based approach for high-throughput protein phosphorylation analysis and site localization
Beausoleil, S. A., Villén, J., Gerber, S. A., Rush, J., & Gygi, S. P. (2006) · Nature Biotechnology · doi:10.1038/nbt1240 · Cited by 1,577
Adherens and tight junctions: Structure, function and connections to the actin cytoskeleton
Hartsock, A., & Nelson, W. J. (2007) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2007.07.012 · Cited by 1,637
Proteomics by Mass Spectrometry: Approaches, Advances, and Applications
Yates, J. R., Ruse, C. I., & Nakorchevsky, A. (2009) · Annual Review of Biomedical Engineering · doi:10.1146/annurev-bioeng-061008-124934 · Cited by 1,078
The 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
An iterative statistical approach to the identification of protein phosphorylation motifs from large-scale data sets
Schwartz, D., & Gygi, S. P. (2005) · Nature Biotechnology · doi:10.1038/nbt1146 · Cited by 879

See all 320

Authors: Collins, M. O., Yu, L., Coba, M. P., Husi, H., Campuzano, I., Blackstock, W. P., Choudhary, J. S., & Grant, S. G. N.
Affiliations: Wellcome Sanger Institute (GB)
University of Edinburgh (GB)
Waters (United Kingdom) (GB)
University of Sheffield (GB)
Corresponding author: Grant, Seth G.N.
ORCID: Collins, Mark O.
Yu, Lu
Coba, Marcelo P.
Husi, Holger
Choudhary, Jyoti S.
Grant, Seth G.N.
Venue: Journal of Biological Chemistry
Publisher: Elsevier BV
Published: 2005-02
Volume: 280
Issue: 7
Pages: 5972-5982
ISSN: 0021-9258 (ISSN-L)
DOI: 10.1074/jbc.m411220200
OpenAlex: W2167791125
Cited by: 320
References: 43
Citations by year: 2026: 2 · 2025: 2 · 2024: 2 · 2023: 7 · 2022: 4 · 2021: 11 · 2020: 6 · 2019: 11 · 2018: 9 · 2017: 8 · 2016: 12 · 2015: 8 · 2014: 11 · 2013: 9 · 2012: 17
FWCI: 14.96
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor, 5736 d)
Locations: Journal of Biological Chemistry (publishedVersion, cc-by)
PubMed (publishedVersion)
Topics: Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
Keywords: synaptic proteins, protein phosphorylation, immobilized metal affinity chromatography, MAP1B, bassoon, kinase substrate specificity
MeSH terms: Animals, Cell Membrane, Phosphoproteins, Phosphorylation, Protein Binding, Protein Kinases, Solubility, Synapses, Synaptosomes, Urea, Computational Biology, Protein Array Analysis, Proteomics, Mice

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

Proteomic Analysis of in Vivo Phosphorylated Synaptic Proteins

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks