Cited by 55Neuroscience and Neuropharmacology ResearchAdvanced Proteomics Techniques and ApplicationsGenetics and Neurodevelopmental Disorders

Correlation profiling of brain sub-cellular proteomes reveals co-assembly of synaptic proteins and subcellular distribution

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Pandya, Nikhil J., Koopmans, Frank, Slotman, Johan A., Paliukhovich, Iryna, Houtsmuller, Adriaan B., Smit, August B., Li, Ka Wan·2017·Scientific Reports

Abstract

Protein correlation profiling might assist in defining co-assembled proteins and subcellular distribution. Here, we quantified the proteomes of five biochemically isolated mouse brain cellular sub-fractions, with emphasis on synaptic compartments, from three brain regions, hippocampus, cortex and cerebellum. We demonstrated the expected co-fractionation of canonical synaptic proteins belonging to the same functional groups. The enrichment profiles also suggested the presence of many novel pre- and post-synaptic proteins. Using super-resolution microscopy on primary neuronal culture we confirmed the postsynaptic localization of PLEKHA5 and ADGRA1. We further detected profound brain region specific differences in the extent of enrichment for some functionally associated proteins. This is exemplified by different AMPA receptor subunits and substantial differences in sub-fraction distribution of their potential interactors, which implicated the differences of AMPA receptor complex compositions. This resource aids the identification of proteins partners and subcellular distribution of synaptic proteins.

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  • GluA3 subunits are the most enriched within the PSD under basal conditions.

    “A recent proteomics study has even found that GluA3 subunits are the most enriched within the PSD under basal conditions (Pandya et al., 2017).”

    From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Pandya et al., 2017

    In Results and Discussion, “Glutamate receptors and their interacting proteins” (page unavailable), GRIA3/GluA3 shows strong PSD association, but GRIA4 has the same reported 0.99 correlation. The paper therefore supports GluA3 as highly PSD-enriched, not as uniquely the most enriched subunit; it also does not explicitly characterize the comparison as being under basal conditions. (LLM, conf=0.86)

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Research works printed but not linked: 46

  1. [2]Milovanovic D Jahn R Organization and dynamics of SNARE proteins in the presynaptic membrane Front Physiol 2015 6 89 10.3389/fphys.2015.00089 25852575 PMC4365744 · DOI
  2. [3]Ackermann F Waites CL Garner CC Presynaptic active zones in invertebrates and vertebrates EMBO Rep 2015 16 923 938 10.15252/embr.201540434 26160654 PMC4552486 · DOI · Paper page
  3. [4]Chua JJ Kindler S Boyken J Jahn R The architecture of an excitatory synapse J Cell Sci 2010 123 819 823 10.1242/jcs.052696 20200227 · DOI
  4. [5]Sheng, M. & Kim, E. The postsynaptic organization of synapses. Cold Spring Harb Perspect Biol3, 10.1101/cshperspect.a005678 (2011). PMC3225953 22046028 · DOI · Paper page
  5. [6]Zhu J Shang Y Zhang M Mechanistic basis of MAGUK-organized complexes in synaptic development and signalling Nat Rev Neurosci 2016 17 209 223 10.1038/nrn.2016.18 26988743 · DOI
  6. [7]Li KW Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology J Biol Chem 2004 279 987 1002 10.1074/jbc.M303116200 14532281 · DOI
  7. [9]Dosemeci A Composition of the synaptic PSD-95 complex Mol Cell Proteomics 2007 6 1749 1760 10.1074/mcp.M700040-MCP200 17623647 PMC2096750 · DOI
  8. [10]Volknandt W Karas M Proteomic analysis of the presynaptic active zone Exp Brain Res 2012 217 449 461 10.1007/s00221-012-3031-x 22354101 · DOI
  9. [11]Distler U In-depth protein profiling of the postsynaptic density from mouse hippocampus using data-independent acquisition proteomics Proteomics 2014 14 2607 2613 10.1002/pmic.201300520 25211037 · DOI
  10. [12]Bayes A Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins PLoS One 2012 7 e46683 10.1371/journal.pone.0046683 23071613 PMC3465276 · DOI · Paper page
  11. [13]Wilhelm BG Composition of isolated synaptic boutons reveals the amounts of vesicle trafficking proteins Science 2014 344 1023 1028 10.1126/science.1252884 24876496 · DOI · Paper page
  12. [14]Sialana FJ Mass spectrometric analysis of synaptosomal membrane preparations for the determination of brain receptors, transporters and channels Proteomics 2016 16 2911 2920 10.1002/pmic.201600234 27759936 · DOI
  13. [15]Li KW Organelle proteomics of rat synaptic proteins: correlation-profiling by isotope-coded affinity tagging in conjunction with liquid chromatography-tandem mass spectrometry to reveal post-synaptic density specific proteins J Proteome Res 2005 4 725 733 10.1021/pr049802+ 15952719 · DOI
  14. [16]Borner GH Fractionation profiling: a fast and versatile approach for mapping vesicle proteomes and protein-protein interactions Mol Biol Cell 2014 25 3178 3194 10.1091/mbc.E14-07-1198 25165137 PMC4196868 · DOI
  15. [17]Lund-Johansen F MetaMass, a tool for meta-analysis of subcellular proteomics data Nat Methods 2016 13 837 840 10.1038/nmeth.3967 27571551 · DOI
  16. [18]Schwenk J High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes Neuron 2012 74 621 633 10.1016/j.neuron.2012.03.034 22632720 · DOI · Paper page
  17. [19]Chen N Interaction proteomics reveals brain region-specific AMPA receptor complexes J Proteome Res 2014 13 5695 5706 10.1021/pr500697b 25337787 · DOI
  18. [20]Schwenk J Regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain Neuron 2014 84 41 54 10.1016/j.neuron.2014.08.044 25242221 · DOI
  19. [21]Piehowski PD Sources of technical variability in quantitative LC-MS proteomics: human brain tissue sample analysis J Proteome Res 2013 12 2128 2137 10.1021/pr301146m 23495885 PMC3695475 · DOI
  20. [22]Chen N Interaction proteomics of canonical Caspr2 (CNTNAP2) reveals the presence of two Caspr2 isoforms with overlapping interactomes Biochim Biophys Acta 2015 1854 827 833 10.1016/j.bbapap.2015.02.008 25707359 · DOI
  21. [23]Kapitein LC Hoogenraad CC Building the Neuronal Microtubule Cytoskeleton Neuron 2015 87 492 506 10.1016/j.neuron.2015.05.046 26247859 · DOI
  22. [24]Yun-Hong Y Chih-Fan C Chia-Wei C Yen-Chung C A study of the spatial protein organization of the postsynaptic density isolated from porcine cerebral cortex and cerebellum Mol Cell Proteomics 2011 10 M110 007138 10.1074/mcp.M110.007138 21715321 PMC3205859 · DOI
  23. [25]Sans N Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway J Neurosci 2001 21 7506 7516 11567040 PMC6762903
  24. [26]Jeyifous O SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway Nat Neurosci 2009 12 1011 1019 10.1038/nn.2362 19620977 PMC2779056 · DOI
  25. [27]Walch L Emerging role of the scaffolding protein Dlg1 in vesicle trafficking Traffic 2013 14 964 973 10.1111/tra.12089 23829493 · DOI
  26. [28]Constals A Glutamate-induced AMPA receptor desensitization increases their mobility and modulates short-term plasticity through unbinding from Stargazin Neuron 2015 85 787 803 10.1016/j.neuron.2015.01.012 25661182 · DOI
  27. [29]Gratacos-Batlle E Yefimenko N Cascos-Garcia H Soto D AMPAR interacting protein CPT1C enhances surface expression of GluA1-containing receptors Front Cell Neurosci 2014 8 469 25698923 PMC4313699
  28. [30]Bats C Groc L Choquet D The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking Neuron 2007 53 719 734 10.1016/j.neuron.2007.01.030 17329211 · DOI · Paper page
  29. [31]Shaikh SA Stargazin Modulation of AMPA Receptors Cell Rep 2016 17 328 335 10.1016/j.celrep.2016.09.014 27705782 PMC5088782 · DOI
  30. [32]Yamasaki M TARP gamma-2 and gamma-8 Differentially Control AMPAR Density Across Schaffer Collateral/Commissural Synapses in the Hippocampal CA1 Area J Neurosci 2016 36 4296 4312 10.1523/JNEUROSCI.4178-15.2016 27076426 PMC6601775 · DOI · Paper page
  31. [33]Bayes A Characterization of the proteome, diseases and evolution of the human postsynaptic density Nat Neurosci 2011 14 19 21 10.1038/nn.2719 21170055 PMC3040565 · DOI · Paper page
  32. [34]Fredriksson R Gloriam DE Hoglund PJ Lagerstrom MC Schioth HB There exist at least 30 human G-protein-coupled receptors with long Ser/Thr-rich N-termini Biochem Biophys Res Commun 2003 301 725 734 10.1016/S0006-291X(03)00026-3 12565841 · DOI
  33. [35]Lagerstrom MC The evolutionary history and tissue mapping of GPR123: specific CNS expression pattern predominantly in thalamic nuclei and regions containing large pyramidal cells J Neurochem 2007 100 1129 1142 10.1111/j.1471-4159.2006.04281.x 17212699 · DOI
  34. [36]Hamann J International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G protein-coupled receptors Pharmacol Rev 2015 67 338 367 10.1124/pr.114.009647 25713288 PMC4394687 · DOI
  35. [37]Fernandez E Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins Mol Syst Biol 2009 5 269 10.1038/msb.2009.27 19455133 PMC2694677 · DOI
  36. [38]Yamada K Nomura N Yamano A Yamada Y Wakamatsu N Identification and characterization of splicing variants of PLEKHA5 (Plekha5) during brain development Gene 2012 492 270 275 10.1016/j.gene.2011.10.018 22037487 · DOI
  37. [39]Jamain S Common and rare variant analysis in early-onset bipolar disorder vulnerability PLoS One 2014 9 e104326 10.1371/journal.pone.0104326 25111785 PMC4128749 · DOI
  38. [40]Breckels LM Learning from Heterogeneous Data Sources: An Application in Spatial Proteomics PLoS Comput Biol 2016 12 e1004920 10.1371/journal.pcbi.1004920 27175778 PMC4866734 · DOI
  39. [41]von Engelhardt J CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus Science 2010 327 1518 1522 10.1126/science.1184178 20185686 · DOI
  40. [42]Pandya NJ Group 1 metabotropic glutamate receptors 1 and 5 form a protein complex in mouse hippocampus and cortex Proteomics 2016 16 2698 2705 10.1002/pmic.201500400 27392515 PMC5129514 · DOI
  41. [43]Carney KE Proteomic analysis of gliosomes from mouse brain: identification and investigation of glial membrane proteins J Proteome Res 2014 13 5918 5927 10.1021/pr500829z 25308431 · DOI
  42. [44]Cox J Mann M MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification Nat Biotechnol 2008 26 1367 1372 10.1038/nbt.1511 19029910 · DOI · Paper page
  43. [45]Vizcaino JA 2016 update of the PRIDE database and its related tools Nucleic Acids Res 2016 44 11033 10.1093/nar/gkw880 27683222 PMC5159556 · DOI
  44. [46]Frischknecht R Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity Nat Neurosci 2009 12 897 904 10.1038/nn.2338 19483686 · DOI · Paper page
  45. [47]Schneider CA Rasband WS Eliceiri KW NIH Image to ImageJ: 25 years of image analysis Nat Methods 2012 9 671 675 10.1038/nmeth.2089 22930834 PMC5554542 · DOI · Paper page
  46. [48]Schindelin J Fiji: an open-source platform for biological-image analysis Nat Methods 2012 9 676 682 10.1038/nmeth.2019 22743772 PMC3855844 · DOI · Paper page

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Authors
Pandya, N. J., Koopmans, F., Slotman, J. A., Paliukhovich, I., Houtsmuller, A. B., Smit, A. B., & Li, K. W.
Affiliations
  • Amsterdam Neuroscience (NL)
  • Erasmus MC (NL)
Corresponding author
Li, Ka Wan
Venue
Scientific Reports
Published
2017-09-21
Volume
7
Issue
1
Pages
12107-12107
ISSN
2045-2322 (ISSN-L)
OpenAlex
W2756067497
Cited by
55
References
2
Citations by year
2026: 5 · 2025: 2 · 2024: 5 · 2023: 6 · 2022: 7 · 2021: 8 · 2020: 9 · 2019: 9 · 2018: 3 · 2017: 1
FWCI
2.95
Type
journal article
Language
en
Open access
Locations
  • Scientific Reports (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • EUR Research Repository (Erasmus University Rotterdam) (publishedVersion, other-oa)
  • VU Research Portal (publishedVersion, other-oa)
  • EUR Research Repository (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • RePub (Erasmus University Rotterdam) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
  • European Commission (242167)
  • Nederlandse Organisatie voor Wetenschappelijk Onderzoek (645-000-003)
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, subcellular proteome, postsynaptic localization, AMPA receptor subunits, regional brain differences, hippocampus, cerebral cortex, cerebellum, super-resolution microscopy, primary neurons
MeSH terms
Animals, Brain Chemistry, Cells, Cultured, Cerebellum, Cerebral Cortex, Hippocampus, Mice, Inbred C57BL, Neurons, Subcellular Fractions, Synapses, Proteome, Proteomics, Receptors, G-Protein-Coupled, Intracellular Signaling Peptides and Proteins, Mice, Tandem Mass Spectrometry

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