Human post-mortem synapse proteome integrity screening for proteomic studies of postsynaptic complexes

Molecular Brain

Volumn 7, Issue 1, 2014, Pages

  Bayés, Àlex ^a,b   Collins, Mark O ^c   Galtrey, Clare M ^d   Simonnet, Clémence ^e   Roy, Marcia ^e   Croning, Mike D R ^e   Gou, Gemma ^a,b   Van De Lagemaat, Louie N ^e   Milward, David ^f   Whittle, Ian R ^e   Smith, Colin ^e   Choudhary, Jyoti S ^g   Grant, Seth G N ^e  

^a BIOMEDICAL RESEARCH INSTITUTE SANT PAU IIB SANT PAU   (Spain)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^c UNIVERSITY OF SHEFFIELD   (United Kingdom)

^d ST GEORGE S HOSPITAL   (United Kingdom)

^e UNIVERSITY OF EDINBURGH   (United Kingdom)

^f LINGUAMATICS LTD   (United Kingdom)

^g WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

MAGUK; Mass spectrometry; Post mortem brain; Proteomics; Psychiatric disorder; Supercomplex; Synapse

Indexed keywords

MEMBRANE ASSOCIATED GUANYLATE CYCLASE KINASE; PROTEOME; MEMBRANE PROTEIN; NERVE PROTEIN; POSTSYNAPTIC DENSITY PROTEINS;

ARTICLE; BRAIN REGION; CORRELATIONAL STUDY; GENE MUTATION; HUMAN; HUMAN TISSUE; NEOCORTEX; POSTMORTEM CHANGE; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEOMICS; SIGNAL TRANSDUCTION; SYNAPSE; AFFINITY CHROMATOGRAPHY; BRAIN CORTEX; CELL FRACTIONATION; METABOLISM; TISSUE BANK;

CEREBRAL CORTEX; CHROMATOGRAPHY, AFFINITY; HUMANS; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; POSTMORTEM CHANGES; PROTEOME; PROTEOMICS; SIGNAL TRANSDUCTION; SUBCELLULAR FRACTIONS; SYNAPSES; TISSUE BANKS;

EID: 84955477826     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/s13041-014-0088-4     Document Type: Article

References (37)

1. Bayés A, Grant SGN: Neuroproteomics: understanding the molecular organization and complexity of the brain. Nat Rev Neurosci 2009, 10:635-646.
2. Bayés A, Van De Lagemaat LN, Collins MO, Croning MDR, Whittle IR, Choudhary JS, Grant SGN: Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat Neurosci 2011, 14:19-21.
3. Bayés A, Collins MO, Croning MDR, Van De Lagemaat LN, Choudhary JS, Grant SGN: Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins. PLoS One 2012, 7:e46683.
4. Grant SG: Synaptopathies: diseases of the synaptome. Curr Opin Neurobiol 2012, 22:522-529.
5. Hahn C-G, Banerjee A, Macdonald ML, Cho D-S, Kamins J, Nie Z, Borgmann-Winter KE, Grosser T, Pizarro A, Ciccimaro E, Arnold SE, Wang H-Y, Blair IA: The post-synaptic density of human postmortem brain tissues: An experimental study paradigm for neuropsychiatric illnesses. PLoS One 2009, 4:e5251.
6. Macdonald ML, Ciccimaro E, Prakash A, Banerjee A, Seeholzer SH, Blair IA, Hahn C-G: Biochemical fractionation and stable isotope dilution liquid chromatography-mass spectrometry for targeted and microdomain-specific protein quantification in human postmortem brain tissue. Mol Cell Proteomics 2012, 11:1670-1681.
7. Chang RYK, Nouwens AS, Dodd PR, Etheridge N: The synaptic proteome in Alzheimer's disease. Alzheimers Dement 2013, 9:499-511.
8. Zhou J, Jones DR, Duong DM, Levey AI, Lah JJ, Peng J: Proteomic analysis of postsynaptic density in Alzheimer's disease. Clin Chim Acta 2013, 420:62-68.
9. Etheridge N, Lewohl JM, Mayfield RD, Harris RA, Dodd PR: Synaptic proteome changes in the superior frontal gyrus and occipital cortex of the alcoholic brain. Proteomics Clin Appl 2009, 3:730-742.
10. Kennedy MB: The postsynaptic density at glutamatergic synapses. Trends Neurosci 1997, 20:264-268.
11. Grant SGN: SnapShot: organizational principles of the postsynaptic proteome. Neuron 2013, 80:534-534.e1.
12. Husi H, Ward MA, Choudhary JS, Blackstock WP, Grant SG: Proteomic analysis of NMDA receptor-Adhesion protein signaling complexes. Nat Neurosci 2000, 3:661-669.
13. Fernandez E, Collins MO, Uren RT, Kopanitsa MV, Komiyama NH, Croning MD, Zografos L, Armstrong JD, Choudhary JS, Grant SG: Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins. Mol Syst Biol 2009, 5:269.
14. Husi H, Grant SG: Isolation of 2000-kDa complexes of N-methyl-D-Aspartate receptor and postsynaptic density 95 from mouse brain. J Neurochem2001, 77:281-291.
15. Kirov G, Pocklington AJ, Holmans P, Ivanov D, Ikeda M, Ruderfer D, Moran J, Chambert K, Toncheva D, Georgieva L, Grozeva D, Fjodorova M, Wollerton R, Rees E, Nikolov I, van de Lagemaat LN, Bayés A, Fernandez E, Olason PI, Böttcher Y, Komiyama NH, Collins MO, Choudhary J, Stefansson K, Stefansson H, Grant SGN, Purcell S, Sklar P, O'Donovan MC, Owen MJ, et al: De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Mol Psychiatry 2011, 17:142-53.
16. Fromer M, Pocklington AJ, Kavanagh DH, Williams HJ, Dwyer S, Gormley P, Georgieva L, Rees E, Palta P, Ruderfer DM, Carrera N, Humphreys I, Johnson JS, Roussos P, Barker DD, Banks E, Milanova V, Grant SG, Hannon E, Rose SA, Chambert K, Mahajan M, Scolnick EM, Moran JL, Kirov G, Palotie A, McCarroll SA, Holmans P, Sklar P, Owen MJ, et al: De novo mutations in schizophrenia implicate synaptic networks. Nature 2014, 506:179-184.
17. Huguet G, Ey E, Bourgeron T: The genetic landscapes of autism spectrum disorders. Annu Rev Genomics Hum Genet 2013, 14:191-213.
18. Pavlowsky A, Chelly J, Billuart P: Emerging major synaptic signaling pathways involved in intellectual disability. Mol Psychiatry 2011, 17:682-693.
19. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, He Y, Ramsay MF, Morris RG, Morrison JH, O'Dell TJ, Grant SG: Enhanced long-Term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 1998, 396:433-439.
20. Cuthbert PC, Stanford LE, Coba MP, Ainge JA, Fink AE, Opazo P, Delgado JY, Komiyama NH, O'Dell TJ, Grant SG: Synapse-Associated protein 102/dlgh3 couples the NMDA receptor to specific plasticity pathways and learning strategies. J Neurosci 2007, 27:2673-2682.
21. Nithianantharajah J, Komiyama NH, McKechanie A, Johnstone M, Blackwood DH, St Clair D, Emes RD, Van De Lagemaat LN, Saksida LM, Bussey TJ, Grant SGN: Synaptic scaffold evolution generated components of vertebrate cognitive complexity. Nat Publish Group 2013, 16:16-24.
22. Carlin RK, Grab DJ, Cohen RS, Siekevitz P: Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 1980, 86:831-845.
23. Wang Y, TesFaye E, Yasuda RP, Mash DC, Armstrong DM, Wolfe BB: Effects of post-mortem delay on subunits of ionotropic glutamate receptors in human brain. Brain Res Mol Brain Res 2000, 80:123-131.
24. Doyle DA, Lee A, Lewis J, Kim E, Sheng M, MacKinnon R: Crystal structures of a complexed and peptide-free membrane protein-binding domain: molecular basis of peptide recognition by PDZ. Cell 1996, 85:1067-1076.
25. Cohen LD, Zuchman R, Sorokina O, Möller A, Dieterich DC, Armstrong JD, Ziv T, Ziv NE: Metabolic turnover of synaptic proteins: kinetics, interdependencies and implications for synaptic maintenance. PLoS One 2013, 8:e63191.
26. McKusick VA: Mendelian inheritance in man and its online version, OMIM. Am J Hum Genet 2007, 80:588-604.
27. Hill WD, Davies G, van de Lagemaat LN, Christoforou A, Marioni RE, Fernandes CPD, Liewald DC, Croning MDR, Payton A, Craig LCA, Whalley LJ, Horan M, Ollier W, Hansell NK, Wright MJ, Martin NG, Montgomery GW, Steen VM, Le Hellard S, Espeseth T, Lundervold AJ, Reinvang I, Starr JM, Pendleton N, Grant SGN, Bates TC, Deary IJ: Human cognitive ability is influenced by genetic variation in components of postsynaptic signalling complexes assembled by NMDA receptors and MAGUK proteins. Transl Psychiatry 2014, 4:e341.
28. Coba MP, Pocklington AJ, Collins MO, Kopanitsa MV, Uren RT, Swamy S, Croning MD, Choudhary JS, Grant SG: Neurotransmitters drive combinatorial multistate postsynaptic density networks. Sci Signal 2009, 2:ra19.
29. Villasana LE, Klann E, Tejada-Simon MV: Rapid isolation of synaptoneurosomes and postsynaptic densities from adult mouse hippocampus. J Neurosci Methods 2006, 158:30-36.
30. Niethammer M, Kim E, Sheng M: Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-Associated guanylate kinases. J Neurosci 1996, 16:2157-2163.
31. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH: Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 1995, 269:1737-1740.
32. Hsu J-L, Huang S-Y, Chow N-H, Chen S-H: Stable-isotope dimethyl labeling for quantitative proteomics. Anal Chem 2003, 75:6843-6852.
33. Boersema PJ, Aye TT, van Veen TAB, Heck AJR, Mohammed S: Triplex protein quantification based on stable isotope labeling by peptide dimethylation applied to cell and tissue lysates. Proteomics 2008, 8:4624-4632.
34. 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.
35. Pagliuca FW, Collins MO, Lichawska A, Zegerman P, Choudhary JS, Pines J: Quantitative proteomics reveals the basis for the biochemical specificity of the cell-cycle machinery. Mol Cell 2011, 43:406-417.
36. Stelzer G, Dalah I, Stein TI, Satanower Y, Rosen N, Nativ N, Oz-Levi D, Olender T, Belinky F, Bahir I, Krug H, Perco P, Mayer B, Kolker E, Safran M, Lancet D: In-silico human genomics with GeneCards. Hum Genomics 2011, 5:709-717.
37. Milward D, Bjäreland M, Hayes W, Maxwell M, Oberg L, Tilford N, Thomas J, Hale R, Knight S, Barnes J: Ontology-based interactive information extraction from scientific abstracts. Comp Funct Genomics 2005, 6:67-71.