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Journal of Neuroscience, Vol 15, 2354-2366, Copyright © 1995 by Society for Neuroscience

ARTICLE

Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein

BM Muller, U Kistner, RW Veh, C Cases-Langhoff, B Becker, ED Gundelfinger and CC Garner
Center for Molecular Neurobiology, University of Hamburg, Germany.

Synapses are highly specialized sites of cell-cell contact involved in signal transfer. The molecular mechanisms modulating the assembly and stability of synapses are unknown. We previously reported the identification of a 90 kDa synapse-associated protein, SAP90, that is localized at the presynaptic termini of inhibitory GABAergic synapses. SAP90 is a mosaic protein composed of three 90 amino acid residue repeats, an SH3 domain and a region homologous to guanylate kinases. SAP90 shares domain specific homology with a family of proteins involved in the assembly and possibly stability of sites of cell contact. These include the product of the lethal(1) discs-large-1 (dlgA) tumor suppressor gene and the zonula occludens proteins ZO-1, ZO- 2. The further characterization of cDNA clones encoding components of synaptic junctions has lead to the identification of a 97 kDa protein, called SAP97, that exhibits a strong overall sequence similarity to SAP90. The present study was undertaken to determine the spatial distribution of SAP97, and to reveal further clues to the possible roles of these proteins in synapses. Light and immunoelectron microscopic analysis of the rat hippocampal formation revealed that SAP97 is localized in the presynaptic nerve termini of excitatory synapses. In other brain regions, SAP97 is found in and along bundles of unmyelinated axons. SAP97 is not restricted to the CNS, but is also present at the basal lateral membrane between a variety of epithelial cells. In cultured T84 cells, it is restricted to the cytoplasmic surface of the plasma membranes between adjacent cells, but not at the edges of cells lacking cell-cell contact suggesting a role for SAP97 in cell adhesion. These data suggest that members of the SAP90/SAP97 subfamily may be involved in the site specific assembly, stability or functions of membrane specialization at sites of cell-cell contact.

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				M. Deguchi, Y. Hata, M. Takeuchi, N. Ide, K. Hirao, I. Yao, M. Irie, A. Toyoda, and Y. Takai BEGAIN (Brain-enriched Guanylate Kinase-associated Protein), a Novel Neuronal PSD-95/SAP90-binding Protein J. Biol. Chem., October 9, 1998; 273(41): 26269 - 26272. [Abstract] [Full Text] [PDF]

				A. S. Leonard, M. A. Davare, M. C. Horne, C. C. Garner, and J. W. Hell SAP97 Is Associated with the alpha -Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptor GluR1 Subunit J. Biol. Chem., July 31, 1998; 273(31): 19518 - 19524. [Abstract] [Full Text] [PDF]

				S. Dieck, L. Sanmarti-Vila, K. Langnaese, K. Richter, S. Kindler, A. Soyke, H. Wex, K.-H. Smalla, U. Kampf, J.-T. Franzer, et al. Bassoon, a Novel Zinc-finger CAG/Glutamine-repeat Protein Selectively Localized at the Active Zone of Presynaptic Nerve Terminals J. Cell Biol., July 27, 1998; 142(2): 499 - 509. [Abstract] [Full Text] [PDF]

				Y.-P. Hsueh, F.-C. Yang, V. Kharazia, S. Naisbitt, A. R. Cohen, R. J. Weinberg, and M. Sheng Direct Interaction of CASK/LIN-2 and Syndecan Heparan Sulfate Proteoglycan and Their Overlapping Distribution in Neuronal Synapses J. Cell Biol., July 13, 1998; 142(1): 139 - 151. [Abstract] [Full Text] [PDF]

				L. Dytrych, D. L. Sherman, C. S. Gillespie, and P. J. Brophy Two PDZ Domain Proteins Encoded by the Murine Periaxin Gene Are the Result of Alternative Intron Retention and Are Differentially Targeted in Schwann Cells J. Biol. Chem., March 6, 1998; 273(10): 5794 - 5800. [Abstract] [Full Text] [PDF]

				E. C. Cooper, A. Milroy, Y. N. Jan, L. Y. Jan, and D. H. Lowenstein Presynaptic Localization of Kv1.4-Containing A-Type Potassium Channels Near Excitatory Synapses in the Hippocampus J. Neurosci., February 1, 1998; 18(3): 965 - 974. [Abstract] [Full Text] [PDF]

				H Wu, S. Reuver, S Kuhlendahl, W. Chung, and C. Garner Subcellular targeting and cytoskeletal attachment of SAP97 to the epithelial lateral membrane J. Cell Sci., January 8, 1998; 111(16): 2365 - 2376. [Abstract] [PDF]

				S. Reuver and C. Garner E-cadherin mediated cell adhesion recruits SAP97 into the cortical cytoskeleton J. Cell Sci., January 4, 1998; 111(8): 1071 - 1080. [Abstract] [PDF]

				S. Einheber, G. Zanazzi, W. Ching, S. Scherer, T. A. Milner, E. Peles, and J. L. Salzer The Axonal Membrane Protein Caspr, a Homologue of Neurexin IV, Is a Component of the Septate-like Paranodal Junctions That Assemble during Myelination J. Cell Biol., December 15, 1997; 139(6): 1495 - 1506. [Abstract] [Full Text] [PDF]

				I. Dobrosotskaya, R. K. Guy, and G. L. James MAGI-1, a Membrane-associated Guanylate Kinase with a Unique Arrangement of Protein-Protein Interaction Domains J. Biol. Chem., December 12, 1997; 272(50): 31589 - 31597. [Abstract] [Full Text] [PDF]

				C. D. Hough, D. F. Woods, S. Park, and P. J. Bryant Organizing a functional junctional complex requires specific domains of the Drosophila MAGUK Discs large Genes & Dev., December 1, 1997; 11(23): 3242 - 3253. [Abstract] [Full Text] [PDF]

				S. Naisbitt, E. Kim, R. J. Weinberg, A. Rao, F.-C. Yang, A. M. Craig, and M. Sheng Characterization of Guanylate Kinase-Associated Protein, a Postsynaptic Density Protein at Excitatory Synapses That Interacts Directly with Postsynaptic Density-95/Synapse-Associated Protein 90 J. Neurosci., August 1, 1997; 17(15): 5687 - 5696. [Abstract] [Full Text] [PDF]

				S. S. Lee, R. S. Weiss, and R. T. Javier Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein PNAS, June 24, 1997; 94(13): 6670 - 6675. [Abstract] [Full Text] [PDF]

				H. Hibino, Y. Horio, A. Inanobe, K. Doi, M. Ito, M. Yamada, T. Gotow, Y. Uchiyama, M. Kawamura, T. Kubo, et al. An ATP-Dependent Inwardly Rectifying Potassium Channel, KAB-2 (Kir4.1), in Cochlear Stria Vascularis of Inner Ear: Its Specific Subcellular Localization and Correlation with the Formation of Endocochlear Potential J. Neurosci., June 15, 1997; 17(12): 4711 - 4721. [Abstract] [Full Text] [PDF]

				Y. Horio, H. Hibino, A. Inanobe, M. Yamada, M. Ishii, Y. Tada, E. Satoh, Y. Hata, Y. Takai, and Y. Kurachi Clustering and Enhanced Activity of an Inwardly Rectifying Potassium Channel, Kir4.1, by an Anchoring Protein, PSD-95/SAP90 J. Biol. Chem., May 16, 1997; 272(20): 12885 - 12888. [Abstract] [Full Text] [PDF]

				E. Kim, S. Naisbitt, Y.-P. Hsueh, A. Rao, A. Rothschild, A. M. Craig, and M. Sheng GKAP, a Novel Synaptic Protein That Interacts with the Guanylate Kinase-like Domain of the PSD-95/SAP90 Family of Channel Clustering Molecules J. Cell Biol., February 10, 1997; 136(3): 669 - 678. [Abstract] [Full Text] [PDF]

				J. E. Brenman, K. S. Christopherson, S. E. Craven, A. W. McGee, and D. S. Bredt Cloning and Characterization of Postsynaptic Density 93, a Nitric Oxide Synthase Interacting Protein J. Neurosci., December 1, 1996; 16(23): 7407 - 7415. [Abstract] [Full Text] [PDF]

				L.-F. Lau, A. Mammen, M. D. Ehlers, S. Kindler, W. J. Chung, C. C. Garner, and R. L. Huganir Interaction of the N-Methyl--aspartate Receptor Complex with a Novel Synapse-associated Protein, SAP102 J. Biol. Chem., August 30, 1996; 271(35): 21622 - 21628. [Abstract] [Full Text] [PDF]

				M Takahisa, S Togashi, T Suzuki, M Kobayashi, A Murayama, K Kondo, T Miyake, and R Ueda The Drosophila tamou gene, a component of the activating pathway of extramacrochaetae expression, encodes a protein homologous to mammalian cell-cell junction-associated protein ZO-1. Genes & Dev., July 15, 1996; 10(14): 1783 - 1795. [Abstract] [PDF]

				W. A. Brady, M. S. Kokoris, M. Fitzgibbon, and M. E. Black Cloning, Characterization, and Modeling of Mouse and Human Guanylate Kinases J. Biol. Chem., July 12, 1996; 271(28): 16734 - 16740. [Abstract] [Full Text] [PDF]

				R Hoskins, A. Hajnal, S. Harp, and S. Kim The C. elegans vulval induction gene lin-2 encodes a member of the MAGUK family of cell junction proteins Development, January 1, 1996; 122(1): 97 - 111. [Abstract] [PDF]

				T. Hanada, L. Lin, E. V. Tibaldi, E. L. Reinherz, and A. H. Chishti GAKIN, a Novel Kinesin-like Protein Associates with the Human Homologue of the Drosophila Discs Large Tumor Suppressor in T Lymphocytes J. Biol. Chem., September 8, 2000; 275(37): 28774 - 28784. [Abstract] [Full Text] [PDF]

				S. L. Nix, A. H. Chishti, J. M. Anderson, and Z. Walther hCASK and hDlg Associate in Epithelia, and Their Src Homology 3 and Guanylate Kinase Domains Participate in Both Intramolecular and Intermolecular Interactions J. Biol. Chem., December 22, 2000; 275(52): 41192 - 41200. [Abstract] [Full Text] [PDF]

				M. Deguchi, T. Iizuka, Y. Hata, W. Nishimura, K. Hirao, I. Yao, H. Kawabe, and Y. Takai PAPIN. A NOVEL MULTIPLE PSD-95/Dlg-A/ZO-1 PROTEIN INTERACTING WITH NEURAL PLAKOPHILIN-RELATED Armadillo REPEAT PROTEIN/delta -CATENIN AND p0071 J. Biol. Chem., September 15, 2000; 275(38): 29875 - 29880. [Abstract] [Full Text] [PDF]

				S. Inagaki, Y. Ohoka, H. Sugimoto, S. Fujioka, M. Amazaki, H. Kurinami, N. Miyazaki, M. Tohyama, and T. Furuyama Sema4C, a Transmembrane Semaphorin, Interacts with a Post-synaptic Density Protein, PSD-95 J. Biol. Chem., March 16, 2001; 276(12): 9174 - 9181. [Abstract] [Full Text] [PDF]

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