Molecular profiling of synaptic vesicle docking sites reveals novel proteins but few differences between glutamatergic and GABAergic synapses

Neuron

Volumn 78, Issue 2, 2013, Pages 285-297

  Boyken, Janina ^a   Grønborg, Mads ^a,c   Riedel, Dietmar ^a   Urlaub, Henning ^a,b   Jahn, Reinhard ^a   Chua, JohnJiaEn ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^c HAGEDORN RESEARCH INSTITUTE   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID CARRIER; 4 AMINOBUTYRIC ACID CARRIER GAT1; ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; EXCITATORY AMINO ACID TRANSPORTER 2; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 2; GLUTAMIC ACID; KALIRIN; MEMBRANE PROTEIN; NEUROMODULIN; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN HOMER 1; PROTEIN SYNGAP1; SUCCINATE DEHYDROGENASE; SUCCINATE DEHYDROGENASE COMPLEX SUBUNIT A; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; SYNAPTOSOMAL ASSOCIATED PROTEIN 25; SYNTAXIN 1; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; COMPARATIVE STUDY; COMPLEX FORMATION; CONTROLLED STUDY; DISSOCIATION; DOCKING COMPLEX; EXOCYTOSIS; GABAERGIC SYNAPSE; GENETIC CONSERVATION; GLUTAMATERGIC SYNAPSE; MOLECULAR DOCKING; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CLEAVAGE; PROTEIN DEGRADATION; PROTEIN LOCALIZATION; PROTEOMICS; QUANTITATIVE ANALYSIS; RAT; SYNAPSE; SYNAPSE VESICLE; SYNAPTOSOME;

ANIMALS; BRAIN; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; PRESYNAPTIC TERMINALS; PROTEIN TRANSPORT; PROTEOMICS; RATS; SYNAPSES; SYNAPTIC VESICLES; TRYPSIN; VESICULAR TRANSPORT PROTEINS;

EID: 84876809468     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.02.027     Document Type: Article

References (47)

1. Abul-Husn N.S., Bushlin I., Morón J.A., Jenkins S.L., Dolios G., Wang R., Iyengar R., Ma'ayan A., Devi L.A. Systems approach to explorecomponents and interactions in the presynapse. Proteomics 2009, 9:3303-3315.
2. Beites C.L., Campbell K.A., Trimble W.S. The septin Sept5/CDCrel-1 competes with alpha-SNAP for binding to the SNARE complex. Biochem. J. 2005, 385:347-353.
3. Benson D.L., Isackson P.J., Gall C.M., Jones E.G. Contrasting patterns in the localization of glutamic acid decarboxylase and Ca2+/calmodulin protein kinase gene expression in the rat central nervous system. Neuroscience 1992, 46:825-849.
4. Berninghausen O., Rahman M.A., Silva J.P., Davletov B., Hopkins C., Ushkaryov Y.A. Neurexin Ibeta and neuroligin are localized on opposite membranes in mature central synapses. J. Neurochem. 2007, 103:1855-1863.
5. Bukalo O., Dityatev A. Synaptic cell adhesion molecules. Adv. Exp. Med. Biol. 2012, 970:97-128.
6. Burger P.M., Mehl E., Cameron P.L., Maycox P.R., Baumert M., Lottspeich F., De Camilli P., Jahn R. Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate. Neuron 1989, 3:715-720.
7. Burré J., Beckhaus T., Schägger H., Corvey C., Hofmann S., Karas M., Zimmermann H., Volknandt W. Analysis of the synaptic vesicle proteome using three gel-based protein separation techniques. Proteomics 2006, 6:6250-6262.
8. Carlin R.K., Grab D.J., Cohen R.S., Siekevitz P. Isolation andcharacterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J. Cell Biol. 1980, 86:831-845.
9. Catterall W.A., Few A.P. Calcium channel regulation and presynaptic plasticity. Neuron 2008, 59:882-901.
10. Chaudhry F.A., Lehre K.P., van Lookeren Campagne M., Ottersen O.P., Danbolt N.C., Storm-Mathisen J. Glutamate transporters in glial plasma membranes: highly differentiated localizations revealed by quantitative ultrastructural immunocytochemistry. Neuron 1995, 15:711-720.
11. Chua J.J., Kindler S., Boyken J., Jahn R. The architecture of an excitatory synapse. J. Cell Sci. 2010, 123:819-823.
12. Cooper B., Werner H.B., Flügge G. Glycoprotein M6a is present in glutamatergic axons in adult rat forebrain and cerebellum. Brain Res. 2008, 1197:1-12.
13. Craig A.M., Banker G., Chang W., McGrath M.E., Serpinskaya A.S. Clustering of gephyrin at GABAergic but not glutamatergic synapses in cultured rat hippocampal neurons. J. Neurosci. 1996, 16:3166-3177.
14. Davis G.A., Bloom F.E. Isolation of synaptic junctional complexes from rat brain. Brain Res. 1973, 62:135-153.
15. Fischer von Mollard G., Südhof T.C., Jahn R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 1991, 349:79-81.
16. Fiszer S., Robertis E.D. Action of triton X-100 on ultrastructure and membrane-bound- enzymes of isolated nerve endings from rat brain. Brain Res. 1967, 5:31-44.
17. Garbelli R., Inverardi F., Medici V., Amadeo A., Verderio C., Matteoli M., Frassoni C. Heterogeneous expression of SNAP-25 in rat and human brain. J. Comp. Neurol. 2008, 506:373-386.
18. Gray E.G. Electron microscopy of presynaptic organelles of the spinal cord. J. Anat. 1963, 97:101-106.
19. Grønborg M., Pavlos N.J., Brunk I., Chua J.J., Münster-Wandowski A., Riedel D., Ahnert-Hilger G., Urlaub H., Jahn R. Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J. Neurosci. 2010, 30:2-12.
20. Hu H., Shao L.R., Chavoshy S., Gu N., Trieb M., Behrens R., Laake P., Pongs O., Knaus H.G., Ottersen O.P., Storm J.F. Presynaptic Ca2+-activated K+ channels in glutamatergic hippocampal terminals and their role in spike repolarization and regulation of transmitter release. J. Neurosci. 2001, 21:9585-9597.
21. Huang Z., Lujan R., Kadurin I., Uebele V.N., Renger J.J., Dolphin A.C., Shah M.M. Presynaptic HCN1 channels regulate Cav3.2 activity and neurotransmission at select cortical synapses. Nat. Neurosci. 2011, 14:478-486.
22. Jones E.G., Huntley G.W., Benson D.L. Alpha calcium/calmodulin-dependent protein kinase II selectively expressed in a subpopulation of excitatory neurons in monkey sensory-motor cortex: comparison with GAD-67 expression. J. Neurosci. 1994, 14:611-629.
23. Knaus H.G., Schwarzer C., Koch R.O., Eberhart A., Kaczorowski G.J., Glossmann H., Wunder F., Pongs O., Garcia M.L., Sperk G. Distribution of high-conductance Ca(2+)-activated K+ channels in rat brain: targeting to axons and nerve terminals. J. Neurosci. 1996, 16:955-963.
24. Langnaese K., Seidenbecher C., Wex H., Seidel B., Hartung K., Appeltauer U., Garner A., Voss B., Mueller B., Garner C.C., Gundelfinger E.D. Protein components of a rat brain synaptic junctional protein preparation. Brain Res. Mol. Brain Res. 1996, 42:118-122.
25. Li K.W., Hornshaw M.P., Van Der Schors R.C., Watson R., Tate S., Casetta B., Jimenez C.R., Gouwenberg Y., Gundelfinger E.D., Smalla K.H., Smit A.B. 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.
26. Morciano M., Burré J., Corvey C., Karas M., Zimmermann H., Volknandt W. Immunoisolation of two synaptic vesicle pools from synaptosomes: a proteomics analysis. J. Neurochem. 2005, 95:1732-1745.
27. Morciano M., Beckhaus T., Karas M., Zimmermann H., Volknandt W. The proteome of the presynaptic active zone: from docked synaptic vesicles to adhesion molecules and maxi-channels. J. Neurochem. 2009, 108:662-675.
28. Müller C.S., Haupt A., Bildl W., Schindler J., Knaus H.G., Meissner M., Rammner B., Striessnig J., Flockerzi V., Fakler B., Schulte U. Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc. Natl. Acad. Sci. USA 2010, 107:14950-14957.
29. Muto Y., Yoshioka T., Kimura M., Matsunami M., Saya H., Okano Y. An evolutionarily conserved leucine-rich repeat protein CLERC is a centrosomal protein required for spindle pole integrity. Cell Cycle 2008, 7:2738-2748.
30. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
31. 2+-triggered exocytosis. J. Neurosci. 2010, 30:13441-13453.
32. Peng J., Kim M.J., Cheng D., Duong D.M., Gygi S.P., Sheng M. Semiquantitative proteomic analysis of rat forebrain postsynaptic density fractions by mass spectrometry. J. Biol. Chem. 2004, 279:21003-21011.
33. Phillips G.R., Huang J.K., Wang Y., Tanaka H., Shapiro L., Zhang W., Shan W.S., Arndt K., Frank M., Gordon R.E., et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 2001, 32:63-77.
34. Phillips G.R., Florens L., Tanaka H., Khaing Z.Z., Fidler L., Yates J.R., Colman D.R. Proteomic comparison of two fractions derived from the transsynaptic scaffold. J. Neurosci. Res. 2005, 81:762-775.
35. Richter K., Langnaese K., Kreutz M.R., Olias G., Zhai R., Scheich H., Garner C.C., Gundelfinger E.D. Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. J. Comp. Neurol. 1999, 408:437-448.
36. Rose E.M., Koo J.C., Antflick J.E., Ahmed S.M., Angers S., Hampson D.R. Glutamate transporter coupling to Na,K-ATPase. J. Neurosci. 2009, 29:8143-8155.
37. Ross P.L., Huang Y.N., Marchese J.N., Williamson B., Parker K., Hattan S., Khainovski N., Pillai S., Dey S., Daniels S., et al. Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. Mol. Cell. Proteomics 2004, 3:1154-1169.
38. Skene J.H., Jacobson R.D., Snipes G.J., McGuire C.B., Norden J.J., Freeman J.A. A protein induced during nerve growth (GAP-43) is a major component of growth-cone membranes. Science 1986, 233:783-786.
39. Südhof T.C. The presynaptic active zone. Neuron 2012, 75:11-25.
40. Takamori S., Rhee J.S., Rosenmund C., Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 2000, 407:189-194.
41. Takamori S., Riedel D., Jahn R. Immunoisolation of GABA-specific synaptic vesicles defines a functionally distinct subset of synaptic vesicles. J. Neurosci. 2000, 20:4904-4911.
42. Takamori S., Rhee J.S., Rosenmund C., Jahn R. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGLUT2). J. Neurosci. 2001, 21:RC182.
43. Takamori S., Holt M., Stenius K., Lemke E.A., Grønborg M., Riedel D., Urlaub H., Schenck S., Brügger B., Ringler P., et al. Molecular anatomy of a trafficking organelle. Cell 2006, 127:831-846.
44. Varoqueaux F., Jamain S., Brose N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 2004, 83:449-456.
45. Verderio C., Pozzi D., Pravettoni E., Inverardi F., Schenk U., Coco S., Proux-Gillardeaux V., Galli T., Rossetto O., Frassoni C., Matteoli M. SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 2004, 41:599-610.
46. Walch-Solimena C., Blasi J., Edelmann L., Chapman E.R., von Mollard G.F., Jahn R. The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 1995, 128:637-645.
47. Xue J., Tsang C.W., Gai W.P., Malladi C.S., Trimble W.S., Rostas J.A., Robinson P.J. Septin 3 (G-septin) is a developmentally regulated phosphoprotein enriched in presynaptic nerve terminals. J. Neurochem. 2004, 91:579-590.