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 Chemical Synapses (AG Gundelfinger)

 Molecular organization of the postsynaptic density

The PSD at excitatory synapses is a molecular device …

  • to anchor and cluster neurotransmitter receptors, ion channels and cell adhesion molecules in the postsynaptic membrane;
  • to recruit components of signaling cascades to the postsynaptic receptor apparatus;
  • and to link these structures to the neuronal cytoskeleton.

The PSD is a highly dynamic structure acting as substrate for the expression of postsynaptic plasticity.

Several PSD components including membrane-associated guanylate kinase homologs (MAGuKs, e.g. SAP90/PSD-95, SAP97 and SAP102) and proline-rich synapse associated proteins (ProSAPs/Shanks) and their associated proteins were identified and are studied in the department. Both MAGuKs and ProSAPs are adaptor proteins that play an essential role in the structural and functional organization of the PSD as well as in the dynamics of dendritic spines and synaptic plasticity. This project is pursued in tight collaboration with AG ‘Molecular Mechanisms of Plasticity' and Research Group ‘Membrane Trafficking and Cytoskeleton' .

In collaboration with Ka wan Li and Guus Smit, Amsterdam, the proteome of the postsynaptic density has been investigated (synaptoproteomics).

Localization of ProSAP1 in the CA3 region of rat hippocampus (Fig. 8). Py, pyramidal neuron. Members of ProSAP protein family are specifically localized at the PSD (Fig. 9) and are supposed to be major organizers of this highly daynamic structure.

Figure 8, 9: Localization of ProSAP1 in the CA3 region of rat hippocampus (Fig. 8). Py, pyramidal neuron. Members of ProSAP protein family are specifically localized at the PSD (Fig. 9) and are supposed to be major organizers of this highly dynamic structure.

Collaborators in the project:

  • Gustavo Acuna Sanhueza
  • Michael Kreutz
  • Carsten Reissner
  • Karl-Heinz Smalla
  • Christina Spilker
  • Uli Thomas

External collaborations:

Selected publications:

Baron MK, Boeckers TM, Vaida B, Faham S, Gingery M, Sawaya MR, Salyer D, Gundelfinger ED, Bowie JU (2006) An architectural framework that may lie at the core of the postsynaptic density. Science 311(5760):531-535.[Link]

Wendholt D, Spilker C, Schmitt A, Dolnik A, Smalla KH, Proepper C, Bockmann J, Sobue K, Gundelfinger ED, Kreutz MR, Boeckers TM (2006) ProSAP interacting protein 1(ProSAPiP1), a novel protein of the postsynaptic density that links the spine associated RapGap (SPAR) to the scaffolding protein ProSAP2 / Shank3. J Biol Chem 281(19):13805-13816.[Link]

Boeckers TM, Liedtke T, Spilker C, Dresbach T, Bockmann J, Kreutz MR, Gundelfinger ED (2005) C-terminal synaptic targeting elements for postsynaptic density proteins ProSAP1/Shank2 and ProSAP2/Shank3. J Neurochem 92(3):519-524.[Link]

Burkhardt C, Muller M, Badde A, Garner CC, Gundelfinger ED, Puschel AW (2005) Semaphorin 4B interacts with the post-synaptic density protein PSD-95/SAP90 and is recruited to synapses through a C-terminal PDZ-binding motif. FEBS Lett 579(17):3821-3828.[Link]

Li K, Hornshaw MP, van Minnen J, Smalla KH, Gundelfinger ED, Smit AB (2005) 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 4(3):725-733.[Link]

Bockers TM, Segger-Junius M, Iglauer P, Bockmann J, Gundelfinger ED, Kreutz MR, Richter D, Kindler S, Kreienkamp HJ (2004) Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3' untranslated region of Shank1 mRNA. Mol Cell Neurosci 26(1):182-190.[Link]

Bresler T, Shapira M, Boeckers T, Dresbach T, Futter M, Garner CC, Rosenblum K, Gundelfinger ED, Ziv NE (2004) Postsynaptic density assembly is fundamentally different from presynaptic active zone assembly. J Neurosci 24(6):1507-1520.[Link]

Dresbach T, Neeb A, Meyer G, Gundelfinger ED, Brose N (2004) Synaptic targeting of neuroligin is independent of neurexin and SAP90/PSD95 binding. Mol Cell Neurosci 27(3):227-235.[Link]

Li KW, Hornshaw MP, Van Der Schors RC, Watson R, Tate S, Casetta B, Jimenez CR, Gouwenberg Y, Gundelfinger ED, Smalla KH, Smit AB (2004) Proteomics analysis of rat brain postsynaptic density. Implications of the diverse protein functional groups for the integration of synaptic physiology. J Biol Chem 279(2):987-1002.[Link]

Qualmann B, Boeckers TM, Jeromin M, Gundelfinger ED, Kessels MM (2004) Linkage of the actin cytoskeleton to the postsynaptic density via direct interactions of Abp1 with the ProSAP/Shank family. J Neurosci 24(10):2481-2495.[Link]

Schuetz G, Rosario M, Grimm J, Boeckers TM, Gundelfinger ED, Birchmeier W (2004) The neuronal scaffold protein Shank3 mediates signaling and biological function of the receptor tyrosine kinase Ret in epithelial cells. J Cell Biol 167(5):945-952.[Link]

Seidenbecher CI, Landwehr M, Smalla KH, Kreutz M, Dieterich DC, Zuschratter W, Reissner C, Hammarback JA, Bockers TM, Gundelfinger ED, Kreutz MR (2004) Caldendrin but not calmodulin binds to light chain 3 of MAP1A/B: an association with the microtubule cytoskeleton highlighting exclusive binding partners for neuronal Ca(2+)-sensor proteins. J Mol Biol 336(4):957-970.[Link]

Marzban H, Khanzada U, Shabir S, Hawkes R, Langnaese K, Smalla KH, Boeckers TM, Gundelfinger ED, Gordon-Weeks PR, Beesley PW (2003) Expression of the immunoglobulin superfamily neuroplastin adhesion molecules in adult and developing mouse cerebellum and their localisation to parasagittal stripes. J Comp Neurol 462(3):286-301.[Link]

Redecker P, Kreutz MR, Bockmann J, Gundelfinger ED, Boeckers TM (2003) Brain synaptic junctional proteins at the acrosome of rat testicular germ cells. J Histochem Cytochem 51(6):809-819.[Link]

Smalla KH, Seidenbecher CI, Tischmeyer W, Schicknick H, Wyneken U, Boeckers TM, Gundelfinger ED, Kreutz MR (2003) Kainate-induced epileptic seizures induce a recruitment of caldendrin to the postsynaptic density in rat brain. Brain Res Mol Brain Res 116(1-2):159-162.[Link]

Wyneken U, Marengo JJ, Villanueva S, Soto D, Sandoval R, Gundelfinger ED, Orrego F (2003) Epilepsy-induced Changes in Signaling Systems of Human and Rat Postsynaptic Densities. Epilepsia 44(2):243-246.[Link]

Bockmann J, Kreutz MR, Gundelfinger ED, Boeckers TM (2002) ProSAP/Shank postsynaptic density proteins interact with insulin receptor tyrosine kinase substrate IRSp53. J Neurochem 83(4):1013-1017.[Link]

Boeckers TM, Bockmann J, Kreutz MR, Gundelfinger ED (2002) ProSAP/Shank proteins - a family of higher order organizing molecules of the postsynaptic density with an emerging role in human neurological disease. J Neurochem 81(5):903-910.[Link]

Garner CC, Zhai RG, Gundelfinger ED, Ziv NE (2002) Molecular mechanisms of CNS synaptogenesis. Trends Neurosci 25(5):243-251.

Laube G, Seidenbecher CI, Richter K, Dieterich DC, Hoffmann B, Landwehr M, Smalla KH, Winter C, Boeckers TM, Wolf G, Gundelfinger ED, Kreutz MR (2002) The neuron-specific Ca2+-binding protein caldendrin: gene structure, splice isoforms, and expression in the rat central nervous system. Mol Cell Neurosci 19(3):459-475.[Link]

Boeckers TM, Mameza MG, Kreutz MR, Bockmann J, Weise C, Buck F, Richter D, Gundelfinger ED, Kreienkamp HJ (2001) Synaptic scaffolding proteins in rat brain. Ankyrin repeats of the multidomain Shank protein family interact with the cytoskeletal protein alpha-fodrin. J Biol Chem 276(43):40104-40112.[Link]

Kreutz MR, Langnaese K, Dieterich DC, Seidenbecher CI, Zuschratter W, Beesley PW, Gundelfinger ED (2001) Distribution of transcript and protein isoforms of the synaptic glycoprotein neuroplastin in rat retina. Invest Ophthalmol Vis Sci 42(8):1907-1914.[Link]

Redecker P, Gundelfinger ED, Boeckers TM (2001) The cortactin-binding postsynaptic density protein ProSAP1 in non-neuronal cells. J Histochem Cytochem 49(5):639-648.[Link]

Schultze W, Eulenburg V, Lessmann V, Herrmann L, Dittmar T, Gundelfinger ED, Heumann R, Erdmann KS (2001) Semaphorin4F interacts with the synapse-associated protein SAP90/PSD-95. 78(3):482-489.[Link]

Wyneken U, Smalla KH, Marengo JJ, Soto D, de la Cerda A, Tischmeyer W, Grimm R, Boeckers TM, Wolf G, Orrego F, Gundelfinger ED (2001) Kainate-induced seizures alter protein composition and N-methyl-D-aspartate receptor function of rat forebrain postsynaptic densities. Neuroscience 102(1):65-74.

Gundelfinger ED, tom Dieck S (2000) Molecular organization of excitatory chemical synapses in the mammalian brain. Naturwissenschaften 87(12):513-523.

Kreienkamp HJ, Zitzer H, Gundelfinger ED, Richter D, Bockers TM (2000) The calcium-independent receptor for alpha-latrotoxin from human and rodent brains interacts with members of the ProSAP/SSTRIP/Shank family of multidomain proteins. J Biol Chem 275(42):32387-32390.[Link]

Smalla KH, Matthies H, Langnase K, Shabir S, Bockers TM, Wyneken U, Staak S, Krug M, Beesley PW, Gundelfinger ED (2000) The synaptic glycoprotein neuroplastin is involved in long-term potentiation at hippocampal CA1 synapses. Proc Natl Acad Sci U S A 97(8):4327-4332.[Link]

Wu H, Reissner C, Kuhlendahl S, Coblentz B, Reuver S, Kindler S, Gundelfinger ED, Garner CC (2000) Intramolecular interactions regulate SAP97 binding to GKAP. Embo J 19(21):5740-5751.[Link]

Boeckers TM, Kreutz MR, Winter C, Zuschratter W, Smalla KH, Sanmarti-Vila L, Wex H, Langnaese K, Bockmann J, Garner CC, Gundelfinger ED (1999) Proline-rich synapse-associated protein-1/cortactin binding protein 1 (ProSAP1/CortBP1) is a PDZ-domain protein highly enriched in the postsynaptic density. J Neurosci 19(15):6506-6518.[Link]

Langnaese K, Mummery R, Gundelfinger ED, Beesley PW (1998) Immunoglobulin superfamily members gp65 and gp55: tissue distribution of glycoforms. FEBS Lett 429(3):284-288.

Seidenbecher CI, Langnaese K, Sanmarti-Vila L, Boeckers TM, Smalla KH, Sabel BA, Garner CC, Gundelfinger ED, Kreutz MR (1998) Caldendrin, a novel neuronal calcium-binding protein confined to the somato-dendritic compartment. J Biol Chem 273(33):21324-21331.

Smalla KH, Angenstein F, Richter K, Gundelfinger ED, Staak S (1998) Identification of fucose alpha(1-2) galactose epitope-containing glycoproteins from rat hippocampus. Neuroreport 9(5):813-817.[Link]

Langnaese K, Beesley PW, Gundelfinger ED (1997) Synaptic membrane glycoproteins gp65 and gp55 are new members of the immunoglobulin superfamily. J Biol Chem 272(2):821-827.

Chung WJ, Kindler S, Seidenbecher C, Garner CC (1996) MAP2a, an alternatively spliced variant of microtubule-associated protein 2. J Neurochem 66(3):1273-1281.

Langnaese K, Seidenbecher C, Wex H, Seidel B, Hartung K, Appeltauer U, Garner A, Voss B, Mueller B, Garner CC, Gundelfinger ED (1996) Protein components of a rat brain synaptic junctional protein preparation. Brain Res Mol Brain Res 42(1):118-122.

Mueller BM, Kistner U, Kindler S, Chung WJ, Kuhlendahl S, Fenster SD, Lau LF, Veh RW, Huganir RL, Gundelfinger ED, Garner CC (1996) SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17(2):255-265.[Link]

Mueller BM, Kistner U, Veh RW, Cases-Langhoff C, Becker B, Gundelfinger ED, Garner CC (1995) Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J Neurosci 15(3 Pt 2):2354-2366.

Seidel B, Zuschratter W, Wex H, Garner CC, Gundelfinger ED (1995) Spatial and sub-cellular localization of the membrane cytoskeleton-associated protein alpha-adducin in the rat brain. Brain Res 700(1-2):13-24.

Garner CC, Garner A, Voss B, Appeltauer U, Gundelfinger ED (1993) Identifying novel synapse-associated proteins. In: Neuronal Cytoskeleton - Morphogenesis, Transport and Synaptic Transmission (Hirokawa N, ed), pp 317-329. London, UK: Japan Scientific Societies Press, CRC Press.[Link]

Kistner U, Wenzel BM, Veh RW, Cases-Langhoff C, Garner AM, Appeltauer U, Voss B, Gundelfinger ED, Garner CC (1993) SAP90, a rat presynaptic protein related to the product of the Drosophila tumor suppressor gene dlg-A. J Biol Chem 268(7):4580-4583.

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