Hostname: page-component-8448b6f56d-wq2xx Total loading time: 0 Render date: 2024-04-17T20:46:55.371Z Has data issue: false hasContentIssue false
  • English
  • Français

Robust syntaxin-4 immunoreactivity in mammalian horizontal cell processes

Published online by Cambridge University Press:  20 July 2007

ARLENE A. HIRANO ,
JOHANN HELMUT BRANDSTÄTTER ,
ALEJANDRO VILA  and
NICHOLAS C. BRECHA
ARLENE A. HIRANO
Affiliation:
Departments of Neurobiology & Medicine, Geffen School of Medicine at UCLA, Los Angeles, California VAGLAHS, Los Angeles, California
JOHANN HELMUT BRANDSTÄTTER
Affiliation:
Institute for Biology, Department of Animal Physiology, University of Erlangen-Nuernberg, Erlangen, Germany Department of Neuroanatomy, Max Planck Institute for Brain Research, Frankfurt am Main, Germany
ALEJANDRO VILA
Affiliation:
Departments of Neurobiology & Medicine, Geffen School of Medicine at UCLA, Los Angeles, California
NICHOLAS C. BRECHA
Affiliation:
Departments of Neurobiology & Medicine, Geffen School of Medicine at UCLA, Los Angeles, California Jules Stein Eye Institute, Geffen School of Medicine at UCLA, Los Angeles, California CURE Digestive Diseases Research Center, Geffen School of Medicine at UCLA, Los Angeles, California VAGLAHS, Los Angeles, California
Get access Rights & Permissions [Opens in a new window]

Abstract

Horizontal cells mediate inhibitory feed-forward and feedback communication in the outer retina; however, mechanisms that underlie transmitter release from mammalian horizontal cells are poorly understood. Toward determining whether the molecular machinery for exocytosis is present in horizontal cells, we investigated the localization of syntaxin-4, a SNARE protein involved in targeting vesicles to the plasma membrane, in mouse, rat, and rabbit retinae using immunocytochemistry. We report robust expression of syntaxin-4 in the outer plexiform layer of all three species. Syntaxin-4 occurred in processes and tips of horizontal cells, with regularly spaced, thicker sandwich-like structures along the processes. Double labeling with syntaxin-4 and calbindin antibodies, a horizontal cell marker, demonstrated syntaxin-4 localization to horizontal cell processes; whereas, double labeling with PKC antibodies, a rod bipolar cell (RBC) marker, showed a lack of co-localization, with syntaxin-4 immunolabeling occurring just distal to RBC dendritic tips. Syntaxin-4 immunolabeling occurred within VGLUT-1-immunoreactive photoreceptor terminals and underneath synaptic ribbons, labeled by CtBP2/RIBEYE antibodies, consistent with localization in invaginating horizontal cell tips at photoreceptor triad synapses. Vertical sections of retina immunostained for syntaxin-4 and peanut agglutinin (PNA) established that the prominent patches of syntaxin-4 immunoreactivity were adjacent to the base of cone pedicles. Horizontal sections through the OPL indicate a one-to-one co-localization of syntaxin-4 densities at likely all cone pedicles, with syntaxin-4 immunoreactivity interdigitating with PNA labeling. Pre-embedding immuno-electron microscopy confirmed the subcellular localization of syntaxin-4 labeling to lateral elements at both rod and cone triad synapses. Finally, co-localization with SNAP-25, a possible binding partner of syntaxin-4, indicated co-expression of these SNARE proteins in the same subcellular compartment of the horizontal cell. Taken together, the strong expression of these two SNARE proteins in the processes and endings of horizontal cells at rod and cone terminals suggests that horizontal cell axons and dendrites are likely sites of exocytotic activity.

Keywords

SNARE complexExocytosisVesicular release
Type
Research Article
Information
Visual Neuroscience , Volume 24 , Issue 4 , July 2007 , pp. 489 - 502
Copyright
© 2007 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Bennett, M.K., García-Arraras, J.E., Elferink, L.A., Peterson, K., Fleming, A.M., Hazuka, C.D. & Scheller, R.H. (1993). The syntaxin family of vesicular transport receptors. Cell 74, 863–873.CrossRefGoogle Scholar
Björkland, A. & Lindvall, O. (1975). Dopamine in dendrites of substantia nigra neurons: Suggestion for a role in dendritic terminals. Brain Research 83, 531–537.CrossRefGoogle Scholar
Blank, U., Cyprien, B., Martin-Verdeaux, S., Paumet, F., Pombo, I., Rivera, J., Roa, M. & Varin-Blank, N. (2001). SNARES and associated regulators in the control of exocytosis in the RBL-2H3 mast cell line. Molecular Immunology 38, 1341–1345.Google Scholar
Blanks, J.C. & Johnson, L.V. (1984). Specific binding of peanut lectin to a class of retinal photoreceptor cells. A species comparison. Investigative Ophthalmology & Visual Science 25, 546–557.Google Scholar
Brandstätter, J.H., Dick, O. & Boeckers, T.M. (2004). The postsynaptic scaffold proteins ProSAP1/Shank2 and Homer 1 are associated with glutamate receptor complexes at rat retinal synapses. The Journal of Comparative Neurology 475, 551–563.CrossRefGoogle Scholar
Bustos, G., Abarca, K., Campusano, J., Bustos, V., Noriega, V. & Aliaga, E. (2004). Functional interactions between somatodendritic dopamine release, glutamate receptors and brain-derived neurotrophic factor expression in mesencephalic structures of the brain. Brain Research Reviews 47, 126–144.CrossRefGoogle Scholar
Chen, B.T. & Rice, M.E. (2001). Novel Ca2+ dependence and time course of somatodendritic dopamine release: Substantia nigra versus striatum. The Journal of Neuroscience 21, 7841–7847.Google Scholar
Chen, D., Lemons, P.P., Schraw, T. & Whiteheart, S.W. (2000). Molecular mechanisms of platelet exocytosis: Role of SNAP-23 and syntaxin 2 and 4 in lysosome release. Blood 96, 1782–1788.Google Scholar
Chen, Y.A. & Scheller, R.H. (2001). SNARE-mediated membrane fusion. Nature Reviews. Molecular Cell Biology 2, 98–106.CrossRefGoogle Scholar
Cragg, S.J. & Rice, M.E. (2004). Dancing past the DAT at a DA synapse. Trends in Neurosciences 27, 270–277.CrossRefGoogle Scholar
Cueva, J.G., Haverkamp, S., Reimer, R.J., Edwards, R., Wässle, H. & Brecha, N.C. (2002). Vesicular gamma-aminobutyric acid transporter expression in amacrine and horizontal cells. The Journal of Comparative Neurology 445, 227–237.CrossRefGoogle Scholar
Dacey, D., Packer, O.S., Diller, L., Brainard, D., Peterson, B. & Lee, B. (2000). Center surround receptive field structure of cone bipolar cells in primate retina. Vision Research 40, 1801–1811.CrossRefGoogle Scholar
De-Miguel, F.F. & Trueta, C. (2005). Synaptic and extrasynaptic secretion of serotonin. Cellular and Molecular Neurobiology 25, 297–312.CrossRefGoogle Scholar
Dowling, J.E. & Boycott, B.B. (1966). Organization of the primate retina: Electron microscopy. Proceedings of the Royal Society of London Series B Biological Sciences 166, 80–111.CrossRefGoogle Scholar
Dowling, J.E., Brown, J.E. & Major, D. (1966). Synapses of horizontal cells in rabbit and cat retinas. Science 153, 1639–1641.CrossRefGoogle Scholar
Duebel, J., Haverkamp, S., Schleich, W., Feng, G., Augustine, G.J., Kuner, T. & Euler, T. (2006). Two-photon imaging reveals somatodendritic chloride gradient in retinal ON-type bipolar cells expressing the biosensor Clomeleon. Neuron 49, 81–94.CrossRefGoogle Scholar
Enz, R., Brandstätter, J.H., Wässle, H. & Bormann, J. (1996). Immunocytochemical localization of GABAc receptor rho subunits in the mammalian retina. The Journal of Comparative Neurology 16, 4479–4490.Google Scholar
Feigenspan, A. & Weiler, R. (2004). Electrophysiological properties of mouse horizontal cell GABAA receptors. Journal of Neurophysiology 92, 2789–2801.CrossRefGoogle Scholar
Fortin, G.D., Desrosiers, C.C., Yamaguchi, N. & Trudeau, L.E. (2006). Basal somatodendritic dopamine release requires snare proteins. Journal of Neurochemistry 96, 1740–1749.CrossRefGoogle Scholar
Fournier, K.M. & Robinson, M.B. (2006). A dominant-negative variant of SNAP-23 decreases the cell surface expression of the neuronal glutamate transporter EAAC1 by slowing constitutive delivery. Neurochemistry International 48, 596–603.CrossRefGoogle Scholar
Fujiwara, T., Mishima, T., Kofuji, T., Chiba, T., Tanaka, K., Yamamoto, A. & Akagawa, K. (2006). Analysis of knock-out mice to determine the role of HPC-1/syntaxin 1A in expressing synaptic plasticity. The Journal of Neuroscience 26, 5767–5776.CrossRefGoogle Scholar
Fyk-Kolodziej, B., Dzhagaryan, A., Qin, P. & Pourcho, R.G. (2004). Immunocytochemical localization of three vesicular glutamate transporters in the cat retina. The Journal of Comparative Neurology 475, 518–530.CrossRefGoogle Scholar
Geffen, L.B., Jessell, T.M., Cuello, A.C. & Iversen, L.L. (1976). Nigral and striatal dopamine release under sensory stimuli. Nature 269, 340–342.Google Scholar
González, M.I. & Robinson, M.B. (2004). Neurotransmitter transporters: Why dance with so many partners? Current Opinion in Pharmacology 4, 30–35.Google Scholar
Gouraud, S., Laera, A., Calamita, G., Carmosino, M., Procino, G., Rossetto, O., Mannucci, R., Rosenthal, W., Svelto, M. & Valenti, G. (2002). Functional involvement of VAMP/synaptobrevin-2 in cAMP-stimulated aquaporin-2 translocation in renal collecting duct cells. Journal of Cell Science 115, 3667–3674.CrossRefGoogle Scholar
Greferath, U., Grünert, U., Fritschy, J.M., Stephenson, A., Möhler, H. & Wässle, H. (1995). GABAA receptor subunits have differential distributions in the rat retina: In situ hybridization and immunohistochemistry. The Journal of Comparative Neurology 353, 553–571.CrossRefGoogle Scholar
Greferath, U., Grünert, U., Müller, F. & Wässle, H. (1994). Localization of GABAA receptors in the rabbit retina. Cell and Tissue Research 276, 295–307.CrossRefGoogle Scholar
Greferath, U., Grünert, U. & Wässle, H. (1990). Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. The Journal of Comparative Neurology 301, 433–442.CrossRefGoogle Scholar
Grigorenko, E.V. & Yeh, H.H. (1994). Expression profiling of GABAA receptor beta-subunits in the rat retina. Visual Neuroscience 11, 279–387.Google Scholar
Grünert, U. & Wässle, H. (1993). Immunocytochemical localization of glycine receptors in the mammalian retina. The Journal of Comparative Neurology 335, 523–537.CrossRefGoogle Scholar
Grusovin, J. & Macaulay, S.L. (2003). Snares for GLUT4—mechanisms directing vesicular trafficking of GLUT4. Frontiers in Bioscience 8, d620–641.Google Scholar
Hack, I., Frech, M., Dick, O., Peichl, L. & Brandstätter, J.H. (2001). Heterogeneous distribution of AMPA glutamate receptor subunits at the photoreceptor synapses of rodent retina. European Journal of Neuroscience 13, 15–24.Google Scholar
Hack, I., Peichl, L. & Brandstätter, J.H. (1999). An alternative pathway for rod signals in the rodent retina: rod photoreceptors, cone bipolar cells, and the localization of glutamate receptors. Proceedings of the National Academy of Sciences of the United States of America 96, 14130–14135.CrossRefGoogle Scholar
Hansen, N.J., Antonin, W. & Edwardson, J.M. (1999). Identification of SNAREs involved in regulated exocytosis in the pancreatic acinar cell. The Journal of Biological Chemistry 274, 22871–22876.CrossRefGoogle Scholar
Haverkamp, S., Grünert, U. & Wässle, H. (2000). The cone pedicle, a complex synapse. Neuron 27, 85–95.CrossRefGoogle Scholar
Haverkamp, S. & Wässle, H. (2000). Immunocytochemical analysis of the mouse retina. The Journal of Comparative Neurology 424, 1–23.Google Scholar
Hirano, A.A., Brandstätter, J.H. & Brecha, N.C. (2005a). Cellular distribution and subcellular localization of molecular components of vesicular transmitter release in horizontal cells of rabbit retina. The Journal of Comparative Neurology 488, 70–81.Google Scholar
Hirano, A.A., Brandstätter, J.H., Morgans, C.W. & Brecha, N.C. (2005b). SNAP-25 expression in mammalian horizontal cells. Program No. 741.1. 2005 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2005. Online.
Hirano, A.A., Vila, A. & Brecha, N.C. (2006). Syntaxin-4 expression in mammalian horizontal cells. Investigative Ophthalmology & Visual Science 47, E-Abstract 391.Google Scholar
Jahn, R. & Scheller, R.H. (2006). SNAREs—engines for membrane fusion. Nature Reviews. Molecular Cell Biology 7, 631–643.CrossRefGoogle Scholar
Jarvis, S.E. & Zamponi, G.W. (2005). Masters or slaves? Vesicle release machinery and the regulation of presynaptic calcium channels. Cell Calcium 37, 483–488.CrossRefGoogle Scholar
Jellali, A., Stussi-Garaud, C., Gasnier, B., Rendon, A., Sahel, J.A., Dreyfus, H. & Picaud, S. (2002). Cellular localization of the vesicular inhibitory amino acid transporter in the mouse and human retina. The Journal of Comparative Neurology 449, 76–87.CrossRefGoogle Scholar
Johnson, J., Chen, T.K., Rickman, D.W., Evans, C. & Brecha, N.C. (1996). Multiple gamma-aminobutyric acid plasma membrane transporters (GAT-1, GAT-2, GAT-3) in the rat retina. The Journal of Comparative Neurology 375, 212–224.3.0.CO;2-5>CrossRefGoogle Scholar
Johnson, J., Tian, N., Caywood, M.S., Reimer, R.J., Edwards, R.H. & Copenhagen, D.R. (2003). Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. The Journal of Neuroscience 23, 518–529.Google Scholar
Keith, R.K., Poage, R.E., Yokoyama, C.T., Catterall, W.A. & Meriney, S.D. (2007). Bidirectional modulation of transmitter release by calcium channel/syntaxin interactions in vivo. The Journal of Neuroscience 27, 265–269.CrossRefGoogle Scholar
Koulen, P., Malitschek, B., Kuhn, R., Bettler, B., Wässle, H. & Brandstätter, J.H. (1998). Presynaptic and postsynaptic localization of GABAB receptors in neurons of the rat retina. European Journal of Neuroscience 10, 1446–1456.CrossRefGoogle Scholar
Lemons, P.P., Chen, D. & Whiteheart, S.W. (2000). Molecular mechanisms of platelet exocytosis: Requirements for alpha-granule release. Biochemical and Biophysical Research Communications 267, 875–880.CrossRefGoogle Scholar
Linberg, K.A. & Fisher, S.K. (1988). Ultrastructural evidence that horizontal cell axon terminals are presynaptic in the human retina. The Journal of Comparative Neurology 268, 281–297.CrossRefGoogle Scholar
Logan, M.R., Odemuyiwa, S.O. & Moqbel, R. (2003). Understanding exocytosis in immune and inflammatory cells: The molecular basis of mediator secretion. The Journal of Allergy and Clinical Immunology 111, 923–932.CrossRefGoogle Scholar
Madison, D.L., Krueger, W.H., Cheng, D., Trapp, B.D. & Pfeiffer, S.E. (1999). SNARE complex proteins, including the cognate pair VAMP-2 and syntaxin-4, are expressed in cultured oligodendrocytes. Journal of Neurochemistry 72, 988–998.CrossRefGoogle Scholar
Massey, S.C. & Mills, S.L. (1996). A calbindin-immunoreactive cone bipolar cell type in the rabbit retina. The Journal of Comparative Neurology 366, 15–33.3.0.CO;2-N>CrossRefGoogle Scholar
Morigiwa, K. & Vardi, N. (1999). Differential expression of ionotropic glutamate receptor subunits in the outer retina. The Journal of Comparative Neurology 405, 173–184.3.0.CO;2-L>CrossRefGoogle Scholar
Negishi, K., Sato, S. & Teranishi, T. (1988). Dopamine cells and rod bipolar cells contain protein kinase C-like immunoreactivity in some vertebrate retinas. Neuroscience Letters 94, 247–252.CrossRefGoogle Scholar
Nicoll, R.A., Tomita, S. & Bredt, D.S. (2006). Auxiliary subunits assist AMPA-type glutamate receptors. Science 311, 1253–1256.CrossRefGoogle Scholar
Nirenberg, M.J., Chan, J., Liu, Y., Edwards, R.H. & Pickel, V.M. (1996a). Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: Potential sites for somatodendritic storage and release of dopamine. The Journal of Neuroscience 16, 4135–4145.Google Scholar
Nirenberg, M.J., Vaughan, R.A., Uhl, G.R., Kuhar, M.J. & Pickel, V.M. (1996b). The dopamine transporter is localized to dendritic and axonal plasma membranes of nigrostriatal dopaminergic neurons. The Journal of Neuroscience 16, 437–447.Google Scholar
Noda, Y. & Sasaki, S. (2005). Trafficking mechanisms of water channel aquaporin-2. Biology of the Cell 97, 885–892.CrossRefGoogle Scholar
Olson, A.L., Knight, J.B. & Pessin, J.E. (1997). Syntaxin 4, VAMP2, and/or VAMP3/cellubrevin are functional target membrane and vesicle SNAP receptors for insulin-stimulated GLUT4 translocation in adipocytes. Molecular and Cellular Biology 17, 2425–2435.CrossRefGoogle Scholar
Pagan, J.K., Wylie, F.G., Joseph, S., Widberg, C., Bryant, N.J., James, D.E. & Stow, J.L. (2003). The t-SNARE syntaxin 4 is regulated during macrophage activation to function in membrane traffic and cytokine secretion. Current Biology 13, 156–160.CrossRefGoogle Scholar
Pan, F. & Massey, S.C. (2007). Rod and cone input to horizontal cells in the rabbit retina. The Journal of Comparative Neurology 500, 815–831.CrossRefGoogle Scholar
Pattnaik, B., Jellali, A., Sahel, J., Dreyfus, H. & Picaud, S. (2000). GABAC receptors are localized with microtubule-associated protein 1B in mammalian cone photoreceptors. The Journal of Neuroscience 20, 6789–6796.Google Scholar
Peichl, L., Sandmann, D. & Boycott, B.B. (1998). Comparative anatomy and function of mammalian horizontal cells. In Development and Organization of the Retina, eds. Chalupa L.M., Finlay B.L., pp. 147–172. New York: Plenum Press.CrossRef
Peichl, L. & González-Soriano, J. (1994). Morphological types of horizontal cell in rodent retinae: A comparison of rat, mouse, gerbil, and guinea pig. Visual Neuroscience 11, 501–517.CrossRefGoogle Scholar
Peters, A., Palay, S.L. & Webster, H. deF. (1991). The Fine Structure of the Nervous System. Neurons and their Supporting Cells Third Edition. New York: Oxford University Press.
Piatigorsky, J. (2001). Dual use of the transcriptional repressor (CtBP2)/ribbon synapse (RIBEYE) gene: How prevalent are multifunctional genes? Trends in Neurosciences 24, 555–557.Google Scholar
Picaud, S., Pattnaik, B., Hicks, D., Forster, V., Fontaine, V., Sahel, J. & Dreyfus, H. (1998). GABAA and GABAC receptors in adult porcine cones: Evidence from a photoreceptor-glia co-culture model. Journal of Physiology 513, 33–42.CrossRefGoogle Scholar
Pickel, V.M., Nirenberg, M.J. & Milner, T.A. (1996). Ultrastructural view of central catecholaminergic transmission: Immunocytochemical localization of synthesizing enzymes, transporters and reporters. Journal of Neurocytology 25, 843–856.CrossRefGoogle Scholar
Qin, P. & Pourcho, R.G. (1999a). Localization of AMPA-selective glutamate receptor subunits in the cat retina: A light- and electron-microscopic study. Visual Neuroscience 16, 169–77.Google Scholar
Qin, P. & Pourcho, R.G. (1999b). AMPA-selective glutamate receptor subunits GluR2 and GluR4 in the cat retina: An immunocytochemical study. Visual Neuroscience 16, 1105–1114.Google Scholar
Quick, M.W. (2006). The role of SNARE proteins in trafficking and function of neurotransmitter transporters. Handbook of Experimental Pharmacology 175, 181–196.CrossRefGoogle Scholar
Rivera, L., Blanco, R. & de la Villa, P. (2001). Calcium-permeable glutamate receptors in horizontal cells of the mammalian retina. Visual Neuroscience 18, 995–1002.Google Scholar
Rizo, J. & Südhof, T.C. (2002). SNAREs and Munc 18 in synaptic vesicle fusion. Nature Reviews. Neuroscience 3, 641–653.CrossRefGoogle Scholar
Robinson, M.B. (2006). Acute regulation of sodium-dependent glutamate transporters: A focus on constitutive and regulated trafficking. Handbook of Experimental Pharmacology 175, 252–275.CrossRefGoogle Scholar
Röhrenbeck, J., Wässle, H. & Heizmann, C.W. (1987). Immunocytochemical labelling of horizontal cells in mammalian retina using antibodies against calcium-binding proteins. Neuroscience Letters 77, 255–260.CrossRefGoogle Scholar
Salaün, C., James, D.J., Greaves, J. & Chamberlain, L.H. (2004). Plasma membrane targeting of exocytic SNARE proteins. Biochimica et Biophysica Acta 1693, 81–89.CrossRefGoogle Scholar
Sassoé-Pognetto, M., Wässle, H. & Grünert, U. (1994). Glycinergic synapses in the rod pathway of the rat retina: cone bipolar cells express the α1 subunit of the glycine receptor. The Journal of Neuroscience 14, 5131–5146.Google Scholar
Satoh, H., Kaneda, M. & Kaneko, A. (2001). Intracellular chloride concentration is higher in rod bipolar cells than in cone bipolar cells of the mouse retina. Neuroscience Letters 310, 161–164.CrossRefGoogle Scholar
Schmitz, F., Konigstorfer, A. & Südhof, T.C. (2000). RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28, 857–872.CrossRefGoogle Scholar
Schubert, T., Weiler, R. & Feigenspan, A. (2006). Intracellular calcium is regulated by different pathways in horizontal cells of the mouse retina. Journal of Neurophysiology 96, 1278–1292.CrossRefGoogle Scholar
Schwartz, E.A. (2002). Transport-mediated synapses in the retina. Physiological Reviews 82, 875–891.CrossRefGoogle Scholar
Sherry, D.M., Mitchell, R., Standifer, K.M. & du Plessis, B. (2006). Distribution of plasma membrane-associated syntaxins 1 through 4 indicates distinct trafficking functions in the synaptic layers of the mouse retina. BioMed Central Neuroscience 7, 54.Google Scholar
Sherry, D.M., Wang, M.M., Bates, J. & Frishman, L.J. (2003). Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. The Journal of Comparative Neurology 465, 480–498.Google Scholar
Spiwoks-Becker, I., Vollrath, L., Seeliger, M.W., Jaissle, G., Eshkind, L.G. & Leube, R.E. (2001). Synaptic vesicle alterations in rod photoreceptors of synaptophysin-deficient mice. Neuroscience 107, 127–142.CrossRefGoogle Scholar
Spurlin, B.A., Park, S.Y., Nevins, A.K., Kim, J.K. & Thurmond, D.C. (2004). Syntaxin 4 transgenic mice exhibit enhanced insulin-mediated glucose uptake in skeletal muscle. Diabetes 53, 2223–2231.CrossRefGoogle Scholar
Spurlin, B.A. & Thurmond, D.C. (2006). Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic beta-cells. Molecular Endocrinology 20, 183–193.CrossRefGoogle Scholar
Stow, J.L., Manderson, A.P. & Murray, R.Z. (2006). SNAREing immunity: The role of SNAREs in the immune system. Nature Reviews. Immunology 6, 919–929.CrossRefGoogle Scholar
Südhof, T.C. (2004). The synaptic vesicle cycle. Annual Review of Neuroscience 27, 509–547.CrossRefGoogle Scholar
Suzuki, S., Tachibana, M. & Kaneko, A. (1990). Effects of glycine and GABA on isolated bipolar cells of the mouse retina. Journal of Physiology 421, 645–662.CrossRefGoogle Scholar
Teng, F.Y.H., Wang, Y. & Tang, B.L. (2001). The syntaxins. Genome Biology 2, 3012.1–3012.7.Google Scholar
ter Beest, M.B., Chapin, S.J., Avrahami, D. & Mostov, K.E. (2005). The role of syntaxins in the specificity of vesicle targeting in polarized epithelial cells. Molecular Biology of the Cell 16, 5784–5792.CrossRefGoogle Scholar
Todd, A.J., Hughes, D.I., Polgár, E., Nagy, G.G., Mackie, M., Ottersen, O.P. & Maxwell, D.J. (2003). The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. European Journal of Neuroscience 17, 13–27.CrossRefGoogle Scholar
tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtova, A., Bracko, O., Gundelfinger, E.D. & Brandstätter, J.H. (2005). Molecular dissection of the photoreceptor ribbon synapse: Physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. The Journal of Cell Biology 168, 825–836.CrossRefGoogle Scholar
tom Dieck, S. & Brandstätter, J.H. (2006). Ribbon synapses of the retina. Cell and Tissue Research 326, 339–346.CrossRefGoogle Scholar
Vardi, N., Masarachia, P. & Sterling, P. (1992). Immunoreactivity to GABAA receptor in the outer plexiform layer of the cat retina. The Journal of Comparative Neurology 320, 394–397.CrossRefGoogle Scholar
Vardi, N., Morigiwa, K., Want, T.L., Shi, Y.J. & Sterling, P. (1998). Neurochemistry of the mammalian cone ‘synaptic complex’. Vision Research 38, 1359–1369.CrossRefGoogle Scholar
Vardi, N. & Sterling, P. (1994). Subcellular localization of GABAA receptor on bipolar cells in macaque and human retina. Vision Research 34, 1235–46.CrossRefGoogle Scholar
Vardi, N., Zhang, L.L., Payne, J.A. & Sterling, P. (2000). Evidence that different cation chloride cotransporters in retinal neurons allow opposite responses to GABA. The Journal of Neuroscience 20, 7657–7663.Google Scholar
Varela, C., Blanco, R. & De la Villa, P. (2005). Depolarizing effect of GABA in rod bipolar cells of the mouse retina. Vision Research 45, 2659–2667.CrossRefGoogle Scholar
Vu, T.Q., Payne, J.A. & Copenhagen, D.R. (2000). Localization and developmental expression patterns of the neuronal K-Cl cotransporter (KCC2) in the rat retina. The Journal of Neuroscience 20, 1414–1423.Google Scholar
Wang, Y. & Tang, B.L. (2006). SNAREs in neurons—beyond synaptic vesicle exocytosis. Molecular Membrane Biology 23, 377–384.CrossRefGoogle Scholar
Wässle, H., Koulen, P., Brandstätter, J.H., Fletcher, E.L. & Becker, C.M. (1998). Glycine and GABA receptors in the mammalian retina. Vision Research 38, 1411–1430.CrossRefGoogle Scholar
Xia, Y., Carroll, R.C. & Nawy, S. (2006). State-dependent AMPA receptor trafficking in the mammalian retina. The Journal of Neuroscience 26, 5028–5036.CrossRefGoogle Scholar
Yang, X.L. (2004). Characterization of receptors for glutamate and GABA in retinal neurons. Progress in Neurobiology 73, 127–150.CrossRefGoogle Scholar