Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-20T00:08:50.095Z Has data issue: false hasContentIssue false

The dynamic architecture of photoreceptor ribbon synapses: Cytoskeletal, extracellular matrix, and intramembrane proteins

Published online by Cambridge University Press:  22 December 2011

AARON J. MERCER
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Nebraska Medical Center, Omaha, Nebraska Department of Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
WALLACE B. THORESON*
Affiliation:
Department of Ophthalmology & Visual Sciences, University of Nebraska Medical Center, Omaha, Nebraska Department of Pharmacology & Experimental Neuroscience, University of Nebraska Medical Center, Omaha, Nebraska
*
*Address correspondence and reprint requests to: Wallace B. Thoreson, Department of Ophthalmology & Visual Sciences, University of Nebraska Medical Center, 4050 Durham Research Center, Omaha, NE 68198-5840. E-mail: wbthores@unmc.edu

Abstract

Rod and cone photoreceptors possess ribbon synapses that assist in the transmission of graded light responses to second-order bipolar and horizontal cells of the vertebrate retina. Proper functioning of the synapse requires the juxtaposition of presynaptic release sites immediately adjacent to postsynaptic receptors. In this review, we focus on the synaptic, cytoskeletal, and extracellular matrix proteins that help to organize photoreceptor ribbon synapses in the outer plexiform layer. We examine the proteins that foster the clustering of release proteins, calcium channels, and synaptic vesicles in the presynaptic terminals of photoreceptors adjacent to their postsynaptic contacts. Although many proteins interact with one another in the presynaptic terminal and synaptic cleft, these protein–protein interactions do not create a static and immutable structure. Instead, photoreceptor ribbon synapses are remarkably dynamic, exhibiting structural changes on both rapid and slow time scales.

Type
Review Article
Copyright
Copyright © Cambridge University Press 2011

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

Aartsen, W.M., Arsanto, J.P., Chauvin, J.P., Vos, R.M., Versteeg, I., Cardozo, B.N., Bivic, A.L. & Wijnholds, J. (2009). PSD95beta regulates plasma membrane Ca2+ pump localization at the photoreceptor synapse. Molecular and Cellular Neurosciences 41, 156165.Google Scholar
Aartsen, W.M., Kantardzhieva, A., Klooster, J., van Rossum, A.G., van de Pavert, S.A., Versteeg, I., Cardozo, B.N., Tonagel, F., Beck, S.C., Tanimoto, N., Seeliger, M.W. & Wijnholds, J. (2006). Mpp4 recruits Psd95 and Veli3 towards the photoreceptor synapse. Human Molecular Genetics 15, 12911302.Google Scholar
Abe, H. & Yamamoto, T.Y. (1984). Diurnal changes in synaptic ribbons of rod cells of the turtle. Journal of Ultrastructure Research 86, 246251.CrossRefGoogle ScholarPubMed
Adato, A., Michel, V., Kikkawa, Y., Reiners, J., Alagramam, K.N., Weil, D., Yonekawa, H., Wolfrum, U., El-Amraoui, A. & Petit, C. (2005). Interactions in the network of Usher syndrome type 1 proteins. Human Molecular Genetics 14, 347356.CrossRefGoogle Scholar
Adato, A., Vreugde, S., Joensuu, T., Avidan, N., Hamalainen, R., Belenkiy, O., Olender, T., Bonne-Tamir, B., Ben-Asher, E., Espinos, C., Millán, J.M., Lehesjoki, A.E., Flannery, J.G., Avraham, K.B., Pietrokovski, S., Sankila, E.M., Beckmann, J.S. & Lancet, D. (2002). USH3A transcripts encode clarin-1, a four-transmembrane-domain protein with a possible role in sensory synapses. European Journal of Human Genetics 10, 339350.Google Scholar
Adler, E.M., Augustine, G.J., Duffy, S.N. & Charlton, M.P. (1991). Alien intracellular calcium chelators attenuate neurotransmitter release at the squid giant synapse. The Journal of Neuroscience 11, 14961507.CrossRefGoogle ScholarPubMed
Adly, M.A., Spiwoks-Becker, I. & Vollrath, L. (1999). Ultrastructural changes of photoreceptor synaptic ribbons in relation to time of day and illumination. Investigative Ophthalmology & Visual Science 40, 21652172.Google ScholarPubMed
Ahmed, Z.M., Riazuddin, S., Riazuddin, S. & Wilcox, E.R. (2003). The molecular genetics of Usher syndrome. Clinical Genetics 63, 431444.CrossRefGoogle ScholarPubMed
Alpadi, K., Magupalli, V.G., Käppel, S., Köblitz, L., Schwarz, K., Seigel, G.M., Sung, C.H. & Schmitz, F. (2008). RIBEYE recruits Munc119, a mammalian ortholog of the Caenorhabditis elegans protein unc 119, to synaptic ribbons of photoreceptor synapses. The Journal of Biological Chemistry 283, 2646126467.CrossRefGoogle ScholarPubMed
Altrock, W.D., tom Dieck, S., Sokolov, M., Meyer, A.C., Sigler, A., Brakebusch, C., Fässler, R., Richter, K., Boeckers, T.M., Potschka, H., Brandt, C., Löscher, W., Grimberg, D., Dresbach, T., Hempelmann, A., Hassan, H., Balschun, D., Frey, J.U., Brandstätter, J.H., Garner, C.C., Rosenmund, C. & Gundelfinger, E.D. (2003). Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 37, 787800.Google Scholar
Babai, N., Bartoletti, T.M. & Thoreson, W.B. (2010). Calcium regulates vesicle replenishment at the cone ribbon synapse. The Journal of Neuroscience 30, 1586615877.Google Scholar
Bader, C.R., Bertrand, D. & Schwartz, E.A. (1982). Voltage-activated and calcium-activated currents studied in solitary rod inner segments from the salamander retina. The Journal of Physiology 331, 253284.CrossRefGoogle ScholarPubMed
Bahadori, R., Biehlmaier, O., Zeitz, C., Labhart, T., Makhankov, Y.V., Forster, U., Gesemann, M., Berger, W. & Neuhauss, S.C. (2006). Nyctalopin is essential for synaptic transmission in the cone dominated zebrafish retina. The European Journal of Neuroscience 24, 16641674.Google Scholar
Balkema, G.W., Cusick, K. & Nguyen, T.H. (2001). Diurnal variation in synaptic ribbon length and visual threshold. Visual Neuroscience 18, 789797.CrossRefGoogle ScholarPubMed
Ball, S.L., Pardue, M.T., McCall, M.A., Gregg, R.G. & Peachey, N.S. (2003). Immunohistochemical analysis of the outer plexiform layer in the nob mouse shows no abnormalities. Visual Neuroscience 20, 267272.CrossRefGoogle ScholarPubMed
Ball, S.L., Powers, P.A., Shin, H.S., Morgans, C.W., Peachey, N.S. & Gregg, R.G. (2002). Role of the beta(2) subunit of voltage-dependent calcium channels in the retinal outer plexiform layer. Investigative Ophthalmology & Visual Science 43, 15951603.Google ScholarPubMed
Barnes, S. & Hille, B. (1989). Ionic channels of the inner segment of tiger salamander cone photoreceptors. The Journal of General Physiology 94, 719743.Google Scholar
Bartoletti, T.M., Babai, N. & Thoreson, W.B. (2010). Vesicle pool size at the salamander cone ribbon synapse. Journal of Neurophysiology 103, 419423.Google Scholar
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Pearce, W.G., Koop, B., Fishman, G.A., Mets, M., Musarella, M.A. & Boycott, K.M. (1998). Loss-of-function mutations in a calcium-channel alpha1-subunit gene in Xp11.23 cause incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 264267.CrossRefGoogle Scholar
Bech-Hansen, N.T., Naylor, M.J., Maybaum, T.A., Sparkes, R.L., Koop, B., Birch, D.G., Bergen, A.A., Prinsen, C.F., Polomeno, R.C., Gal, A., Drack, A.V., Musarella, M.A., Jacobson, S.G., Young, R.S. & Weleber, R.G. (2000). Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nature Genetics 26, 319333.Google Scholar
Bennis, M., Versaux-Botteri, C., Repérant, J. & Armengol, J.A. (2005). Calbindin, calretinin and parvalbumin immunoreactivity in the retina of the chameleon (Chamaeleo chamaeleon). Brain, Behavior and Evolution 65, 177187.Google Scholar
Bergmann, M., Grabs, D. & Rager, G. (2000). Expression of presynaptic proteins is closely correlated with the chronotopic pattern of axons in the retinotectal system of the chick. The Journal of Comparative Neurology 418, 361372.Google Scholar
Berntson, A.K. & Morgans, C.W. (2003). Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas. Journal of Vision 3, 274280.CrossRefGoogle ScholarPubMed
Betz, A., Okamoto, M., Benseler, F. & Brose, N. (1997). Direct interaction of the rat unc-13 homologue Munc13-1 with the N terminus of syntaxin. The Journal of Biological Chemistry 272, 25202526.Google Scholar
Beutner, D., Voets, T., Neher, E. & Moser, T. (2001). Calcium dependence of exocytosis and endocytosis at the cochlear inner hair cell afferent synapse. Neuron 29, 681690.CrossRefGoogle ScholarPubMed
Biehlmaier, O., Makhankov, Y. & Neuhauss, S.C. (2007). Impaired retinal differentiation and maintenance in zebrafish laminin mutants. Investigative Ophthalmology & Visual Science 48, 28872894.CrossRefGoogle ScholarPubMed
Blank, M., Koulen, P., Blake, D.J. & Kröger, S. (1999). Dystrophin and beta-dystroglycan in photoreceptor terminals from normal and mdx3Cv mouse retinae. The European Journal of Neuroscience 11, 21212133.CrossRefGoogle ScholarPubMed
Blank, M., Koulen, P. & Kröger, S. (1997). Subcellular concentration of beta-dystroglycan in photoreceptors and glial cells of the chick retina. The Journal of Comparative Neurology 389, 668678.Google Scholar
Boëda, B., El-Amraoui, A., Bahloul, A., Goodyear, R., Daviet, L., Blanchard, S., Perfettini, I., Fath, K.R., Shorte, S., Reiners, J., Houdusse, A., Legrain, P., Wolfrum, U., Richardson, G. & Petit, C. (2002). Myosin VIIa, harmonin and cadherin 23, three Usher I gene products that cooperate to shape the sensory hair cell bundle. The EMBO Journal 21, 66896699.Google Scholar
Bollmann, J.H., Sakmann, B. & Borst, J.G. (2000). Calcium sensitivity of glutamate release in a calyx-type terminal. Science 289, 953957.Google Scholar
Brandstätter, J.H., Löhrke, S., Morgans, C.W. & Wässle, H. (1996 a). Distributions of two homologous synaptic vesicle proteins, synaptoporin and synaptophysin, in the mammalian retina. The Journal of Comparative Neurology 370, 110.Google Scholar
Brandstätter, J.H., Fletcher, E.L., Garner, C.C., Gundelfinger, E.D. & Wässle, H. (1999). Differential expression of the presynaptic cytomatrix protein bassoon among ribbon synapses in the mammalian retina. The European Journal of Neuroscience 11, 36833693.Google Scholar
Brandstätter, J.H., Wässle, H., Betz, H. & Morgans, C.W. (1996 b). The plasma membrane protein SNAP-25, but not syntaxin, is present at photoreceptor and bipolar cell synapses in the rat retina. The European Journal of Neuroscience 8, 823828.Google Scholar
Bucurenciu, I., Kulik, A., Schwaller, B., Frotscher, M. & Jonas, P. (2008). Nanodomain coupling between Ca2+ channels and Ca2+ sensors promotes fast and efficient transmitter release at a cortical GABAergic synapse. Neuron 57, 536545.CrossRefGoogle Scholar
Bunt, A.H. (1971). Enzymatic digestion of synaptic ribbons in amphibian retinal photoreceptors. Brain Research 25, 571577.CrossRefGoogle ScholarPubMed
Buraei, Z. & Yang, J. (2010). The b subunit of voltage-gated Ca2+ channels. Physiological Reviews 90, 14611506.Google Scholar
Burnside, B. (1986). Microtubules and actin filaments in teleost visual cone elongation and contraction. Journal of Supramolecular Structure 5, 257275.Google Scholar
Cao, Y., Posokhova, E. & Martemyanov, K.A. (2011). TRPM1 forms complexes with nyctalopin in vivo and accumulates in postsynaptic compartment of ON-bipolar neurons in mGluR6-dependent manner. The Journal of Neuroscience 31, 1152111526.Google Scholar
Carter-Dawson, L.D. & LaVail, M.M. (1979). Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. The Journal of Comparative Neurology 188, 245262.Google Scholar
Cases-Langhoff, C., Voss, B., Garner, A.M., Appeltauer, U., Takei, K., Kindler, S., Veh, R.W., De Camilli, P., Gundelfinger, E.D. & Garner, C.C. (1996). Piccolo, a novel 420 kDa protein associated with the presynaptic cytomatrix. European Journal of Cell Biology 69, 214223.Google Scholar
Chang, B., Heckenlively, J.R., Bayley, P.R., Brecha, N.C., Davisson, M.T., Hawes, N.L., Hirano, A.A., Hurd, R.E., Ikeda, A., Johnson, B.A., McCall, M.A., Morgans, C.W., Nusinowitz, S., Peachey, N.S., Rice, D.S., Vessey, K.A. & Gregg, R.G. (2006). The nob2 mouse, a null mutation in Cacna1f: Anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Visual Neuroscience 23, 1124.CrossRefGoogle Scholar
Chang-Ileto, B., Frere, S.G., Chan, R.B., Voronov, S.V., Roux, A. & Di Paolo, G. (2011). Synaptojanin 1-mediated PI(4,5)P2 hydrolysis is modulated by membrane curvature and facilitates membrane fission. Developmental Cell 20, 206218.CrossRefGoogle ScholarPubMed
Chen, Y.H., Li, M.H., Zhang, Y., He, L.L., Yamada, Y., Fitzmaurice, A., Shen, Y., Zhang, H., Tong, L. & Yang, J. (2004). Structural basis of the alpha1-beta subunit interaction of voltage-gated Ca2+ channels. Nature 429, 675680.CrossRefGoogle ScholarPubMed
Choi, S.Y., Jackman, S., Thoreson, W.B. & Kramer, R.H. (2008). Light regulation of Ca2+ in the cone photoreceptor synaptic terminal. Visual Neuroscience 25, 693700.CrossRefGoogle ScholarPubMed
Cia, D., Bordais, A., Varela, C., Forster, V., Sahel, J.A., Rendon, A. & Picaud, S. (2005). Voltage-gated channels and calcium homeostasis in mammalian rod photoreceptors. Journal of Neurophysiology 93, 14681475.CrossRefGoogle ScholarPubMed
Cibis, G.W., Fitzgerald, K.M., Harris, D.J., Rothberg, P.G. & Rupani, M. (1993). The effects of dystrophin gene mutations on the ERG in mice and humans. Investigative Ophthalmology & Visual Science 34, 36463652.Google Scholar
Claudepierre, T., Manglapus, M.K., Marengi, N., Radner, S., Champliaud, M.F., Tasanen, K., Bruckner-Tuderman, L., Hunter, D.D. & Brunken, W.J. (2005). Collagen XVII and BPAG1 expression in the retina: Evidence for an anchoring complex in the central nervous system. The Journal of Comparative Neurology 487, 190203.CrossRefGoogle ScholarPubMed
Cooper, N.G. & McLaughlin, B.J. (1984). The distribution of filipin-sterol complexes in photoreceptor synaptic membranes. The Journal of Comparative Neurology 230, 437443.CrossRefGoogle ScholarPubMed
Coppola, T., Magnin-Luthi, S., Perret-Menoud, V., Gattesco, S., Schiavo, G. & Regazzi, R. (2001). Direct interaction of the Rab3 effector RIM with Ca2+ channels, SNAP-25, and synaptotagmin. The Journal of Biological Chemistry 276, 3275632762.Google Scholar
Corey, D.P., Dubinsky, J.M. & Schwartz, E.A. (1984). The calcium current in inner segments of rods from the salamander (Ambystoma tigrinum) retina. The Journal of Physiology 354, 557575.CrossRefGoogle ScholarPubMed
Cristofanilli, M. & Akopian, A. (2006). Calcium channel and glutamate receptor activities regulate actin organization in salamander retinal neurons. The Journal of Physiology 575, 543554.CrossRefGoogle ScholarPubMed
Cristofanilli, M., Mizuno, F. & Akopian, A. (2007). Disruption of actin cytoskeleton causes internalization of Ca(v)1.3 (alpha 1D) L-type calcium channels in salamander retinal neurons. Molecular Vision 13, 14961507.Google ScholarPubMed
Cui, G., Meyer, A.C., Calin-Jageman, I., Neef, J., Haeseleer, F., Moser, T. & Lee, A. (2007). Ca2+-binding proteins tune Ca2+-feedback to Cav1.3 channels in mouse auditory hair cells. The Journal of Physiology 585, 791803.Google Scholar
Curtis, L.B., Doneske, B., Liu, X., Thaller, C., McNew, J.A. & Janz, R. (2008). Syntaxin 3b is a t-SNARE specific for ribbon synapses of the retina. The Journal of Comparative Neurology 510, 550559.CrossRefGoogle ScholarPubMed
Davies, A., Douglas, L., Hendrich, J., Wratten, J., Tran Van Minh, A., Foucault, I., Koch, D., Pratt, W.S., Saibil, H.R. & Dolphin, A.C. (2006). The calcium channel alpha2delta-2 subunit partitions with CaV2.1 into lipid rafts in cerebellum: Implications for localization and function. The Journal of Neuroscience 26, 87488757.CrossRefGoogle ScholarPubMed
Deguchi-Tawarada, M., Inoue, E., Takao-Rikitsu, E., Inoue, M., Kitajima, I., Ohtsuka, T. & Takai, Y. (2006). Active zone protein CAST is a component of conventional and ribbon synapses in mouse retina. The Journal of Comparative Neurology 495, 480496.CrossRefGoogle ScholarPubMed
Deng, L., Kaeser, P.S., Xu, W. & Südhof, T.C. (2011). RIM proteins activate vesicle priming by reversing autoinhibitory homodimerization of Munc13. Neuron 69, 317331.CrossRefGoogle ScholarPubMed
den Hollander, A.I., ten Brink, J.B., de Kok, Y.J., van Soest, S., van den Born, L.I., van Driel, M.A., van de Pol, D.J., Payne, A.M., Bhattacharya, S.S., Kellner, U., Hoyng, C.B., Westerveld, A., Brunner, H.G., Bleeker-Wagemakers, E.M., Deutman, A.F., Heckenlively, J.R., Cremers, F.P. & Bergen, A.A. (1999). Mutations in a human homologue of Drosophila crumbs cause retinitis pigmentosa (RP12). Nature Genetics 23, 217221.CrossRefGoogle Scholar
Dick, O., Hack, I., Altrock, W.D., Garner, C.C., Gundelfinger, E.D. & Brandstätter, J.H. (2001). Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: Comparison with Bassoon. The Journal of Comparative Neurology 439, 224234.CrossRefGoogle ScholarPubMed
Dick, O., tom Dieck, S., Altrock, W.D., Ammermüller, J., Weiler, R., Garner, C.C., Gundelfinger, E.D. & Brandstätter, J.H. (2003). The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37, 775786.CrossRefGoogle ScholarPubMed
Doussau, F. & Augustine, G.J. (2000). The actin cytoskeleton and neurotransmitter release: An overview. Biochimie 82, 353363.CrossRefGoogle ScholarPubMed
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, 80111.Google Scholar
Drenckhahn, D., Holbach, M., Ness, W., Schmitz, F. & Anderson, L.V. (1996). Dystrophin and the dystrophin-associated glycoprotein, beta-dystroglycan, co-localize in photoreceptor synaptic complexes of the human retina. Neuroscience 73, 605612.Google Scholar
Dresbach, T., Torres, V., Wittenmayer, N., Altrock, W.D., Zamorano, P., Zuschratter, W., Nawrotzki, R., Ziv, N.E., Garner, C.C. & Gundelfinger, E.D. (2006). Assembly of active zone precursor vesicles: Obligatory trafficking of presynaptic cytomatrix proteins Bassoon and Piccolo via a trans-Golgi compartment. The Journal of Biological Chemistry 281, 60386047.CrossRefGoogle Scholar
D’Souza, V.N., Nguyen, T.M., Morris, G.E., Karges, W., Pillers, D.A. & Ray, P.N. (1995). A novel dystrophin isoform is required for normal retinal electrophysiology. Human Molecular Genetics 4, 837842.CrossRefGoogle ScholarPubMed
Dulubova, I., Lou, X., Lu, J., Huryeva, I., Alam, A., Schneggenburger, R., Südhof, T.C. & Rizo, J. (2005). A Munc13/RIM/Rab3 tripartite complex: From priming to plasticity? The EMBO Journal 24, 28392850.CrossRefGoogle ScholarPubMed
Duncan, G., Rabl, K., Gemp, I., Heidelberger, R. & Thoreson, W.B. (2010). Quantitative analysis of synaptic release at the photoreceptor synapse. Biophysical Journal 98, 21022110.Google Scholar
Duncan, J.L., Yang, H., Doan, T., Silverstein, R.S., Murphy, G.J., Nune, G., Liu, X., Copenhagen, D., Tempel, B.L., Rieke, F. & Krizaj, D. (2006). Scotopic visual signaling in the mouse retina is modulated by high-affinity plasma membrane calcium extrusion. The Journal of Neuroscience 26, 72017211.CrossRefGoogle ScholarPubMed
Dyka, F.M., Wu, W.W., Pfeifer, T.A., Molday, L.L., Grigliatti, T.A. & Molday, R.S. (2008). Characterization and purification of the discoidin domain-containing protein retinoschisin and its interaction with galactose. Biochemistry 47, 90989106.Google Scholar
El-Amraoui, A. & Petit, C. (2005). Usher I syndrome: Unravelling the mechanisms that underlie the cohesion of the growing hair bundle in inner ear sensory cells. Journal of Cell Science 118, 45934603.Google Scholar
El-Amraoui, A., Sahly, I., Picaud, S., Sahel, J., Abitbol, M. & Petit, C. (1996). Human Usher 1B/mouse shaker-1: The retinal phenotype discrepancy explained by the presence/absence of myosin VIIA in the photoreceptor cells. Human Molecular Genetics 5, 11711178.Google Scholar
Elluru, R.G., Bloom, G.S. & Brady, S.T. (1995). Fast axonal transport of kinesin in the rat visual system: Functionality of kinesin heavy chain isoforms. Molecular Biology of the Cell 6, 2140.Google Scholar
Fan, S.S., Chen, M.S., Lin, J.F., Chao, W.T. & Yang, V.C. (2003). Use of gain-of-function study to delineate the roles of crumbs in Drosophila eye development. Journal of Biomedical Science 10, 766773.Google ScholarPubMed
Fedchyshyn, M.J. & Wang, L.Y. (2005). Developmental transformation of the release modality at the calyx of Held synapse. The Journal of Neuroscience 25, 41314140.CrossRefGoogle ScholarPubMed
Feng, W. & Zhang, M. (2009). Organization and dynamics of PDZ-domain-related supramodules in the postsynaptic density. Nature Reviews. Neuroscience 10, 8799.CrossRefGoogle ScholarPubMed
Firth, S.I., Morgan, I.G., Boelen, M.K. & Morgans, C.W. (2001). Localization of voltage-sensitive L-type calcium channels in the chicken retina. Clinical & Experimental Ophthalmology 29, 183187.CrossRefGoogle ScholarPubMed
Fitzgerald, K.M., Cibis, G.W., Giambrone, S.A. & Harris, D.J. (1994). Retinal signal transmission in Duchenne muscular dystrophy: Evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. The Journal of Clinical Investigation 93, 24252430.Google Scholar
Fouquet, W., Owald, D., Wichmann, C., Mertel, S., Depner, H., Dyba, M., Hallermann, S., Kittel, R.J., Eimer, S. & Sigrist, S.J. (2009). Maturation of active zone assembly by Drosophila Bruchpilot. The Journal of Cell Biology 186, 129145.Google Scholar
Fox, M.A. & Sanes, J.R. (2007). Synaptotagmin I and II are present in distinct subsets of central synapses. The Journal of Comparative Neurology 503, 280296.Google Scholar
Frank, T., Rutherford, M.A., Strenzke, N., Neef, A., PangršiČ, T., Khimich, D., Fetjova, A., Gundelfinger, E.D., Liberman, M.C., Harke, B., Bryan, K.E., Lee, A., Egner, A., Riedel, D. & Moser, T. (2010). Bassoon and the synaptic ribbon organize Ca2+ channels and vesicles to add release sites and promote refilling. Neuron 68, 724738.CrossRefGoogle ScholarPubMed
Friedman, T.B., Schultz, J.M., Ahmed, Z.M., Tsilou, E.T. & Brewer, C.C. (2011). Usher syndrome: Hearing loss with vision loss. Advances in Oto-rhino-laryngology 70, 5665.CrossRefGoogle ScholarPubMed
Friedrich, U., Stöhr, H., Hilfinger, D., Loenhardt, T., Schachner, M., Langmann, T. & Weber, B.H. (2011). The Na/K-ATPase is obligatory for membrane anchorage of retinoschisin, the protein involved in the pathogenesis of X-linked juvenile retinoschisis. Human Molecular Genetics 20, 11321142.CrossRefGoogle ScholarPubMed
Fuchs, M., Sendelbeck, A. & Brandstätter, J.H. (2011). Examining the molecular basis of light adaptation at the photoreceptor ribbon synapse. Investigative Ophthalmology & Visual Science 52, ARVO E-Abstract 1177.Google Scholar
Fukuda, M. (2003). Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. The Journal of Biological Chemistry 278, 1537315380.Google Scholar
Fukuda, J., Kameyama, M. & Yamaguchi, K. (1981). Breakdown of cytoskeletal filaments selectively reduces Na and Ca spikes in cultured mammal neurons. Nature 294, 8285.Google Scholar
Gebhart, M., Juhasz-Vedres, G., Zuccotti, A., Brandt, N., Engel, J., Trockenbacher, A., Kaur, G., Obermair, G.J., Knipper, M., Koschak, A. & Striessnig, J. (2010). Modulation of Cav1.3 Ca2+ channel gating by Rab3 interacting molecule. Molecular and Cellular Neurosciences 44, 246259.CrossRefGoogle ScholarPubMed
Geppert, M., Goda, Y., Stevens, C.F. & Südhof, T.C. (1997). The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature 387, 810814.Google Scholar
Gil, C., Soler-Jover, A., Blasi, J. & Aguilera, J. (2004). Synaptic proteins and SNARE complexes are localized in lipid rafts from rat brain synaptosomes. Biochemical and Biophysical Research Communications 329, 117124.Google Scholar
Gonzalez-Bellido, P.T., Wardill, T.J., Kostyleva, R., Meinertzhagen, I.A. & Juusola, M. (2009). Overexpressing temperature-sensitive dynamin decelerates phototransduction and bundles microtubules in Drosophila photoreceptors. The Journal of Neuroscience 29, 1419914210.CrossRefGoogle ScholarPubMed
Gosens, I., den Hollander, A.I., Cremers, F.P. & Roepman, R. (2008). Composition and function of the Crumbs protein complex in the mammalian retina. Experimental Eye Research 86, 713726.CrossRefGoogle ScholarPubMed
Gover, T.D., Moreira, T.H., Kao, J.P. & Weinreich, D. (2007). Calcium regulation in individual peripheral sensory nerve terminals of the rat. The Journal of Physiology 578, 481490.CrossRefGoogle ScholarPubMed
Gracheva, E.O., Hadwiger, G., Nonet, M.L. & Richmond, J.E. (2008). Direct interactions between C. elegans RAB-3 and Rim provide a mechanism to target vesicles to the presynaptic density. Neuroscience Letters 444, 137142.Google Scholar
Gray, E.G. (1976). Microtubules in synapses of the retina. Journal of Neurocytology 5, 361370.Google Scholar
Gray, E.G. & Pease, H.L. (1971). On understanding the organisation of the retinal receptor synapses. Brain Research 35, 115.Google Scholar
Grayson, C., Reid, S.N., Ellis, J.A., Rutherford, A., Sowden, J.C., Yates, J.R., Farber, D.B. & Trump, D. (2000). Retinoschisin, the X-linked retinoschisis protein, is a secreted photoreceptor protein, and is expressed and released by Weri-Rb1 cells. Human Molecular Genetics 9, 18731879.CrossRefGoogle ScholarPubMed
Greenlee, M.H., Roosevelt, C.B. & Sakaguchi, D.S. (2001). Differential localization of SNARE complex proteins SNAP-25, syntaxin, and VAMP during development of the mammalian retina. The Journal of Comparative Neurology 430, 306320.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Greenlee, M.H., Swanson, J.J., Simon, J.J., Elmquist, J.K., Jacobson, C.D. & Sakaguchi, D.S. (1996). Postnatal development and the differential expression of presynaptic terminal-associated proteins in the developing retina of the Brazilian opossum, Monodelphis domestica. Brain Research. Developmental Brain Research 96, 159172.Google Scholar
Gregg, R.G., Kamermans, M., Klooster, J., Lukasiewicz, P.D., Peachey, N.S., Vessey, K.A. & McCall, M.A. (2007). Nyctalopin expression in retinal bipolar cells restores visual function in a mouse model of complete X-linked congenital stationary night blindness. Journal of Neurophysiology 98, 30233033.Google Scholar
Gregg, R.G., Mukhopadhyay, S., Candille, S.I., Ball, S.L., Pardue, M.T., McCall, M.A. & Peachey, N.S. (2003). Identification of the gene and the mutation responsible for the mouse nob phenotype. Investigative Ophthalmology & Visual Science 44, 378384.Google Scholar
Gregory, F.D., Bryan, K.E., Pangršič, T., Calin-Jageman, I.E., Moser, T. & Lee, A. (2011). Harmonin inhibits presynaptic Ca(v)1.3 Ca(2+) channels in mouse inner hair cells. Nature Neuroscience 14, 11091111.CrossRefGoogle ScholarPubMed
Griessmeier, K., Cuny, H., Rötzer, K., Griesbeck, O., Harz, H., Biel, M. & Wahl-Schott, C. (2009). Calmodulin is a functional regulator of Cav1.4 L-type Ca2+ channels. The Journal of Biological Chemistry 284, 2980929816.Google Scholar
Grossman, G.H., Pauer, G.J., Narendra, U., Peachey, N.S. & Hagstrom, S.A. (2009). Early synaptic defects in tulp1-/- mice. Investigative Ophthalmology & Visual Science 50, 30743083.CrossRefGoogle ScholarPubMed
Guan, R., Dai, H. & Rizo, J. (2008). Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. Biochemistry 47, 14741481.Google Scholar
Haeseleer, F. (2008). Interaction and colocalization of CaBP4 and Unc119 (MRG4) in photoreceptors. Investigative Ophthalmology & Visual Science 49, 23662375.CrossRefGoogle ScholarPubMed
Haeseleer, F., Imanishi, Y., Maeda, T., Possin, D.E., Maeda, A., Lee, A., Rieke, F. & Palczewski, K. (2004). Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nature Neuroscience 7, 10791087.Google Scholar
Hallermann, S., Fejtova, A., Schmidt, H., Weyhersmüller, A., Silver, R.A., Gundelfinger, E.D. & Eilers, J. (2010). Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68, 710723.Google Scholar
Hamanaka, Y. & Meinertzhagen, I.A. (2010). Immunocytochemical localization of synaptic proteins to photoreceptor synapses of Drosophila melanogaster. The Journal of Comparative Neurology 518, 11331155.Google Scholar
Han, Y., Kaeser, P.S., Südhof, T.C. & Schneggenburger, R. (2011). RIM determines Ca2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69, 304316.Google Scholar
Hasegawa, A., Hisatomi, O., Yamamoto, S., Ono, E. & Tokunaga, F. (2007). Stathmin expression during newt retina regeneration. Experimental Eye Research 85, 518527.Google Scholar
Heidelberger, R. (1998). Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. The Journal of General Physiology 111, 225241.Google Scholar
Heidelberger, R., Heinemann, C., Neher, E. & Matthews, G. (1994). Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371, 513515.Google Scholar
Heidelberger, R., Thoreson, W.B. & Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Progress in Retinal and Eye Research 24, 682720.Google Scholar
Heidelberger, R., Wang, M.M. & Sherry, D.M. (2003). Differential distribution of synaptotagmin immunoreactivity among synapses in the goldfish, salamander, and mouse retina. Visual Neuroscience 20, 3749.Google Scholar
Heine, M., Groc, L., Frischknecht, R., Béïque, J.C., Lounis, B., Rumbaugh, G., Huganir, R.L., Cognet, L. & Choquet, D. (2008). Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320, 201205.Google Scholar
Henderson, D., Doerr, T.A., Gottesman, J. & Miller, R.F. (2001). Calcium channel immunoreactivity in the salamander retina. Neuroreport 12, 14931499.CrossRefGoogle ScholarPubMed
Hibino, H., Pironkova, R., Onwumere, O., Vologodskaia, M., Hudspeth, A.J. & Lesage, F. (2002). RIM binding proteins (RBPs) couple Rab3-interacting molecules (RIMs) to voltage-gated Ca(2+) channels. Neuron 34, 411423.Google Scholar
Hida, Y. & Ohtsuka, T. (2010). CAST and ELKS proteins: Structural and functional determinants of the presynaptic active zone. Journal of Biochemistry 148, 131137.CrossRefGoogle ScholarPubMed
Higashide, T., McLaren, M.J. & Inana, G. (1998). Localization of HRG4, a photoreceptor protein homologous to Unc-119, in ribbon synapse. Investigative Ophthalmology & Visual Science 39, 690698.Google ScholarPubMed
Holmberg, K. & Ohman, P. (1976). Fine structure of retinal synaptic organelles in lamprey and hagfish photoreceptors. Vision Research 16, 237239.Google Scholar
Holt, M., Cooke, A., Neef, A. & Lagnado, L. (2004). High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Current Biology 14, 173183.Google Scholar
Holzhausen, L.C., Lewis, A.A., Cheong, K.K. & Brockerhoff, S.E. (2009). Differential role for synaptojanin 1 in rod and cone photoreceptors. The Journal of Comparative Neurology 517, 633644.Google Scholar
Hosoi, N., Holt, M. & Sakaba, T. (2009). Calcium dependence of exo- and endocytotic coupling at a glutamatergic synapse. Neuron 63, 216229.Google Scholar
Hosoya, O., Tsutsui, K. & Tsutsui, K. (2004). Localized expression of amphiphysin Ir, a retina-specific variant of amphiphysin I, in the ribbon synapse and its functional implication. The European Journal of Neuroscience 19, 21792187.Google Scholar
Hotulainen, P. & Hoogenraad, C.C. (2010). Actin in dendritic spines: Connecting dynamics to function. The Journal of Cell Biology 189, 619629.CrossRefGoogle ScholarPubMed
Hu, H., Li, J., Zhang, Z. & Yu, M. (2011). Pikachurin interaction with dystroglycan is diminished by defective O-mannosyl glycosylation in congenital muscular dystrophy models and rescued by LARGE overexpression. Neuroscience Letters 489, 1015.Google Scholar
Hull, C., Studholme, K., Yazulla, S. & von Gersdorff, H. (2006). Diurnal changes in exocytosis and the number of synaptic ribbons at active zones of an ON-type bipolar cell terminal. Journal of Neurophysiology 96, 20252033.Google Scholar
Ibraghimov-Beskrovnaya, O., Ervasti, J.M., Leveille, C.J., Slaughter, C.A., Sernett, S.W. & Campbell, K.P. (1992). Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355, 696702.Google Scholar
Innocenti, B. & Heidelberger, R. (2008). Mechanisms contributing to tonic release at the cone photoreceptor ribbon synapse. Journal of Neurophysiology 99, 2536.Google Scholar
Inoue, E., Deguchi-Tawarada, M., Takao-Rikitsu, E., Inoue, M., Kitajima, I., Ohtsuka, T. & Takai, Y. (2006). ELKS, a protein structurally related to the active zone protein CAST, is involved in Ca2+-dependent exocytosis from PC12 cells. Genes to Cells 11, 659672.Google Scholar
Isayama, T., Goodman, S.R. & Zagon, I.S. (1991). Spectrin isoforms in the mammalian retina. The Journal of Neuroscience 11, 35313538.Google Scholar
Isosomppi, J., Västinsalo, H., Geller, S.F., Heon, E., Flannery, J.G. & Sankila, E.M. (2009). Disease-causing mutations in the CLRN1 gene alter normal CLRN1 protein trafficking to the plasma membrane. Molecular Vision 15, 18061818.Google Scholar
Jackman, S.L., Choi, S.Y., Thoreson, W.B., Rabl, K., Bartoletti, T.M. & Kramer, R.H. (2009). Role of the synaptic ribbon in transmitting the cone light reponse. Nature Neuroscience 12, 303310.Google Scholar
Jarsky, T., Tian, M. & Singer, J.H. (2010). Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. The Journal of Neuroscience 30, 1188511895.Google Scholar
Jastrow, H., Koulen, P., Altrock, W.D. & Kröger, S. (2006). Identification of a beta-dystroglycan immunoreactive subcompartment in photoreceptor terminals. Investigative Ophthalmology & Visual Science 47, 1724.Google Scholar
Job, C. & Lagnado, L. (1998). Calcium and protein kinase C regulate the actin cytoskeleton in the synaptic terminal of retinal bipolar cells. The Journal of Cell Biology 143, 16611672.CrossRefGoogle ScholarPubMed
Johnson, B.D. & Byerly, L. (1993). A cytoskeletal mechanism for Ca2+ channel metabolic dependence and inactivation by intracellular Ca2+. Neuron 10, 797804.CrossRefGoogle ScholarPubMed
Johnson, S.L., Franz, C., Kuhn, S., Furness, D.N., Rüttiger, L., Münkner, S., Rivolta, M.N., Seward, E.P., Herschman, H.R., Engel, J., Knipper, M. & Marcotti, W. (2010). Synaptotagmin IV determines the linear Ca2+ dependence of vesicle fusion at auditory ribbon synapses. Nature Neuroscience 13, 4552.Google Scholar
Johnson, J.E. Jr., Perkins, G.A., Giddabasappa, A., Chaney, S., Xiao, W., White, A.D., Brown, J.M., Waggoner, J., Ellisman, M.H. & Fox, D.A. (2007). Spatiotemporal regulation of ATP and Ca2+ dynamics in vertebrate rod and cone ribbon synapses. Molecular Vision 13, 887919.Google Scholar
Juhaszova, M., Church, P., Blaustein, M.P. & Stanley, E.F. (2000). Location of calcium transporters at presynaptic terminals. The European Journal of Neuroscience 12, 839846.Google Scholar
Kaeser, P.S., Deng, L., Wang, Y., Dulubova, I., Liu, X., Rizo, J. & Südhof, T.C. (2011). RIM proteins tether Ca2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144, 282295.CrossRefGoogle Scholar
Kameya, S., Araki, E., Katsuki, M., Mizota, A., Adachi, E., Nakahara, K., Nonaka, I., Sakuragi, S., Takeda, S. & Nabeshima, Y. (1997). Dp260 disrupted mice revealed prolonged implicit time of the b-wave in ERG and loss of accumulation of beta-dystroglycan in the outer plexiform layer of the retina. Human Molecular Genetics 6, 21952203.CrossRefGoogle ScholarPubMed
Kamphuis, W. & Hendriksen, H. (1998). Expression patterns of voltage-dependent calcium channel alpha 1 subunits (alpha 1A-alpha 1E) mRNA in rat retina. Brain Research. Molecular Brain Research 55, 209220.Google Scholar
Kanagawa, M., Omori, Y., Sato, S., Kobayashi, K., Miyagoe-Suzuki, Y., Takeda, S., Endo, T., Furukawa, T. & Toda, T. (2010). Post-translational maturation of dystroglycan is necessary for pikachurin binding and ribbon synaptic localization. The Journal of Biological Chemistry 285, 3120831216.Google Scholar
Kantardzhieva, A., Alexeeva, S., Versteeg, I. & Wijnholds, J. (2006). MPP3 is recruited to the MPP5 protein scaffold at the retinal outer limiting membrane. The FEBS Journal 273, 11521165.CrossRefGoogle Scholar
Kantardzhieva, A., Gosens, I., Alexeeva, S., Punte, I.M., Versteeg, I., Krieger, E., Neefjes-Mol, C.A., den Hollander, A.I., Letteboer, S.J., Klooster, J., Cremers, F.P., Roepman, R. & Wijnholds, J. (2005). MPP5 recruits MPP4 to the CRB1 complex in photoreceptors. Investigative Ophthalmology & Visual Science 46, 21922201.Google Scholar
Karim, Z., Vepachedu, R., Gorska, M. & Alam, R. (2010). UNC119 inhibits dynamin and dynamin-dependent endocytic processes. Cellular Signalling 22, 128137.Google Scholar
Katsumata, O., Ohara, N., Tamaki, H., Niimura, T., Naganuma, H., Watanabe, M. & Sakagami, H. (2009). IQ-ArfGEF/BRAG1 is associated with synaptic ribbons in the mouse retina. The European Journal of Neuroscience 30, 15091516.Google Scholar
Kersten, F.F., van Wijk, E., van Reeuwijk, J., van der Zwaag, B., Märker, T., Peters, T.A., Katsanis, N., Wolfrum, U., Keunen, J.E., Roepman, R. & Kremer, H. (2010). Association of whirlin with Cav1.3 (alpha1D) channels in photoreceptors, defining a novel member of the usher protein network. Investigative Ophthalmology & Visual Science 51, 23382346.CrossRefGoogle ScholarPubMed
Khan, N.W., Kondo, M., Hiriyanna, K.T., Jamison, J.A., Bush, R.A. & Sieving, P.A. (2005). Primate retinal signaling pathways: Suppressing ON-pathway activity in monkey with glutamate analogues mimics human CSNB1-NYX genetic night blindness. Journal of Neurophysiology 93, 481492.Google Scholar
Khimich, D., Nouvian, R., Pujol, R., Tom Dieck, S., Egner, A., Gundelfinger, E.D. & Moser, T. (2005). Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434, 889894.Google Scholar
Kikuchi, M., Chiba, A. & Aoki, K. (2000). Daily melatonin injections entrain the circadian change of synaptic ribbon number in the pineal organ of the Japanese newt. Neuroscience Letters 285, 181184.Google Scholar
Kim, J.H. & von Gersdorff, H. (2009). Traffic jams during vesicle cycling lead to synaptic depression. Neuron 63, 143145.Google Scholar
Kiyonaka, S., Wakamori, M., Miki, T., Uriu, Y., Nonaka, M., Bito, H., Beedle, A.M., Mori, E., Hara, Y., De Waard, M., Kanagawa, M., Itakura, M., Takahashi, M., Campbell, K.P. & Mori, Y. (2007). RIM1 confers sustained activity and neurotransmitter vesicle anchoring to presynaptic Ca2+ channels. Nature Neuroscience 10, 691701.Google Scholar
Klingauf, J. & Neher, E. (1997). Modeling buffered Ca2+ diffusion near the membrane: Implications for secretion in neuroendocrine cells. Biophysical Journal 72, 674690.CrossRefGoogle ScholarPubMed
Koike, C., Obara, T., Uriu, Y., Numata, T., Sanuki, R., Miyata, K., Koyasu, T., Ueno, S., Funabiki, K., Tani, A., Ueda, H., Kondo, M., Mori, Y., Tachibana, M. & Furukawa, T. (2010). TRPM1 is a component of the retinal ON bipolar cell transduction channel in the mGluR6 cascade. Proceedings of the National Academy of Sciences of the United States of America 107, 332337.Google Scholar
Koontz, M.A. & Hendrickson, A.E. (1993). Comparison of immunolocalization patterns for the synaptic vesicle proteins p65 and synapsin I in macaque monkey retina. Synapse 14, 268282.Google Scholar
Kotova, S., Vijayasarathy, C., Dimitriadis, E.K., Ikonomou, L., Jaffe, H. & Sieving, P.A. (2010). Retinoschisin (RS1) interacts with negatively charged lipid bilayers in the presence of Ca2+: An atomic force microscopy study. Biochemistry 2049, 70237032.Google Scholar
Koulen, P., Fletcher, E.L., Craven, S.E., Bredt, D.S. & Wässle, H. (1998). Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. The Journal of Neuroscience 18, 1013610149.CrossRefGoogle ScholarPubMed
Knust, E. & Bossinger, O. (2002). Composition and formation of intercellular junctions in epithelial cells. Science 298, 19551959.CrossRefGoogle ScholarPubMed
Kreft, M., Krizaj, D., Grilc, S. & Zorec, R. (2003). Properties of exocytotic response in vertebrate photoreceptors. Journal of Neurophysiology 90, 218225.CrossRefGoogle ScholarPubMed
Kremer, H., van Wijk, E., Märker, T., Wolfrum, U. & Roepman, R. (2006). Usher syndrome: Molecular links of pathogenesis, proteins and pathways. Human Molecular Genetics 15(Suppl. 2), R262R270.Google Scholar
Krizaj, D. & Copenhagen, D.R. (2002). Calcium regulation in photoreceptors. Frontiers in Bioscience 7, d2023d2044.Google Scholar
Krizaj, D., Demarco, S.J., Johnson, J., Strehler, E.E. & Copenhagen, D.R. (2002). Cell-specific expression of plasma membrane calcium ATPase isoforms in retinal neurons. The Journal of Comparative Neurology 451, 121.Google Scholar
Krizaj, D., Lai, F.A. & Copenhagen, D.R. (2003). Ryanodine stores and calcium regulation in the inner segments of salamander rods and cones. The Journal of Physiology 547, 761774.Google Scholar
Krizaj, D., Liu, X. & Copenhagen, D.R. (2004). Expression of calcium transporters in the retina of the tiger salamander (Ambystoma tigrinum). The Journal of Comparative Neurology 475, 463480.CrossRefGoogle ScholarPubMed
Kurumado, K. & Mori, W. (1977). A morphological study of the circadian cycle of the pineal gland of the rat. Cell and Tissue Research 182, 565568.Google Scholar
Küssel-Andermann, P., El-Amraoui, A., Safieddine, S., Nouaille, S., Perfettini, I., Lecuit, M., Cossart, P., Wolfrum, U. & Petit, C. (2000). Vezatin, a novel transmembrane protein, bridges myosin VIIA to the cadherin-catenins complex. The EMBO Journal 19, 60206029.Google Scholar
Lagnado, L., Cervetto, L. & McNaughton, P.A. (1998). Ion transport by the Na-Ca exchange in isolated rod outer segments. Proceedings of the National Academy of Sciences of the United States of America 85, 45484552.Google Scholar
Lajoie, P., Goetz, J.G., Dennis, J.W. & Nabi, I.R. (2009). Lattices, rafts, and scaffolds: Domain regulation of receptor signaling at the plasma membrane. The Journal of Cell Biology 185, 381385.Google Scholar
Lang, T., Bruns, D., Wenzel, D., Riedel, D., Holroyd, P., Thiele, C. & Jahn, R. (2001). SNAREs are concentrated in cholesterol-dependent clusters that define docking and fusion sites for exocytosis. The EMBO Journal 20, 22022213.Google Scholar
Lasansky, A. (1973). Organization of the outer synaptic layer in the retina of the larval tiger salamander. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 265, 471489.Google ScholarPubMed
Lasater, E.M. & Witkovsky, P. (1991). The calcium current of turtle cone photoreceptor axon terminals. Neuroscience Research Supplement 15, S165S173.Google ScholarPubMed
Lazarides, E., Nelson, W.J. & Kasamatsu, T. (1984). Segregation of two spectrin forms in the chicken optic system: A mechanism for establishing restricted membrane-cytoskeletal domains in neurons. Cell 36, 269278.Google Scholar
Lazzell, D.R., Belizaire, R., Thakur, P., Sherry, D.M. & Janz, R. (2004). SV2B regulates synaptotagmin 1 by direct interaction. The Journal of Biological Chemistry 279, 5212452131.Google Scholar
Lee, A., Jimenez, A., Cui, G. & Haeseleer, F. (2007). Phosphorylation of the Ca2+-binding protein CaBP4 by protein kinase C zeta in photoreceptors. The Journal of Neuroscience 27, 1274312754.Google Scholar
Leenders, A.G., Lopes da Silva, F.H., Ghijsen, W.E. & Verhage, M. (2001). Rab3a is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Molecular Biology of the Cell 12, 30953102.Google Scholar
Lenne, P.F., Wawrezinieck, L., Conchonaud, F., Wurtz, O., Boned, A., Guo, X.J., Rigneault, H., He, H.T. & Marguet, D. (2006). Dynamic molecular confinement in the plasma membrane by microdomains and the cytoskeleton meshwork. The EMBO Journal 25, 32453256.Google Scholar
Leroy, B.P., Budde, B.S., Wittmer, M., De Baere, E., Berger, W. & Zeitz, C. (2009). A common NYX mutation in Flemish patients with X linked CSNB. The British Journal of Ophthalmology 93, 692696.Google Scholar
Liang, Y. & Tavalin, S.J. (2007). Auxiliary beta subunits differentially determine pka utilization of distinct regulatory sites on Cav1.3 L type Ca2+ channels. Channels (Austin) 1, 102112.Google Scholar
Libby, R.T., Champliaud, M.F., Claudepierre, T., Xu, Y., Gibbons, E.P., Koch, M., Burgeson, R.E., Hunter, D.D. & Brunken, W.J. (2000). Laminin expression in adult and developing retinae: Evidence of two novel CNS laminins. The Journal of Neuroscience 20, 65176528.CrossRefGoogle ScholarPubMed
Libby, R.T., Lavallee, C.R., Balkema, G.W., Brunken, W.J. & Hunter, D.D. (1999). Disruption of laminin beta2 chain production causes alterations in morphology and function in the CNS. The Journal of Neuroscience 19, 93999411.CrossRefGoogle ScholarPubMed
Linetti, A., Fratangeli, A., Taverna, E., Valnegri, P., Francolini, M., Cappello, V., Matteoli, M., Passafaro, M. & Rosa, P. (2010). Cholesterol reduction impairs exocytosis of synaptic vesicles. Journal of Cell Science 123, 595605.CrossRefGoogle ScholarPubMed
Lin-Jones, J., Parker, E., Wu, M., Knox, B.E. & Burnside, B. (2003). Disruption of kinesin II function using a dominant negative-acting transgene in Xenopus laevis rods results in photoreceptor degeneration. Investigative Ophthalmology & Visual Science 44, 36143621.Google Scholar
LoGiudice, L., Sterling, P. & Matthews, G. (2008). Mobility and turnover of vesicles at the synaptic ribbon. The Journal of Neuroscience 28, 31503158.Google Scholar
Lotery, A.J., Jacobson, S.G., Fishman, G.A., Weleber, R.G., Fulton, A.B., Namperumalsamy, P., Héon, E., Levin, A.V., Grover, S., Rosenow, J.R., Kopp, K.K., Sheffield, V.C. & Stone, E.M. (2001). Mutations in the CRB1 gene cause Leber congenital amaurosis. Archives of Ophthalmology 119, 415420.Google Scholar
Maeda, T., Lem, J., Palczewski, K. & Haeseleer, F. (2005). A critical role of CaBP4 in the cone synapse. Investigative Ophthalmology & Visual Science 46, 43204327.Google Scholar
Maerker, T., van Wijk, E., Overlack, N., Kersten, F.F., McGee, J., Goldmann, T., Sehn, E., Roepman, R., Walsh, E.J., Kremer, H. & Wolfrum, U. (2008). A novel Usher protein network at the periciliary reloading point between molecular transport machineries in vertebrate photoreceptor cells. Human Molecular Genetics 17, 7186Google Scholar
Magupalli, V.G., Schwarz, K., Alpadi, K., Natarajan, S., Seigel, G.M. & Schmitz, F. (2008). Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. The Journal of Neuroscience 28, 79547967.Google Scholar
Mandell, J.W., MacLeish, P.R. & Townes-Anderson, E. (1993). Process outgrowth and synaptic varicosity formation by adult photoreceptors in vitro. The Journal of Neuroscience 13, 35333548.CrossRefGoogle ScholarPubMed
Mandell, J.W., Townes-Anderson, E., Czernik, A.J., Cameron, R., Greengard, P. & De Camilli, P. (1990). Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses. Neuron 5, 1933.Google Scholar
Mansergh, F., Orton, N.C., Vessey, J.P., Lalonde, M.R., Stell, W.K., Tremblay, F., Barnes, S., Rancourt, D.E. & Bech-Hansen, N.T. (2005). Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Human Molecular Genetics 14, 30353046.CrossRefGoogle ScholarPubMed
Matteoli, M., Takei, K., Cameron, R., Hurlbut, P., Johnston, P.A., Südhof, T.C., Jahn, R. & De Camilli, P. (1991). Association of Rab3A with synaptic vesicles at late stages of the secretory pathway. The Journal of Cell Biology 115, 625633.Google Scholar
McCall, M.A. & Gregg, R.G. (2008). Comparisons of structural and functional abnormalities in mouse B-wave mutants. The Journal of Physiology 586, 43854392.Google Scholar
Mehalow, A.K., Kameya, S., Smith, R.S., Hawes, N.L., Denegre, J.M., Young, J.A., Bechtold, L., Haider, N.B., Tepass, U., Heckenlively, J.R., Chang, B., Naggert, J.K. & Nishina, P.M. (2003). CRB1 is essential for external limiting membrane integrity and photoreceptor morphogenesis in the mammalian retina. Human Molecular Genetics 12, 21792189.Google Scholar
Mercer, A.J., Chen, M. & Thoreson, W.B. (2011 a). Lateral mobility of presynaptic L-type calcium channels at photoreceptor ribbon synapses. The Journal of Neuroscience 31, 43974406.Google Scholar
Mercer, A.J., Rabl, K., Riccardi, G.E., Brecha, N.C., Stella, S.L. Jr. & Thoreson, W.B. (2011 b). Location of release sites and calcium-activated chloride channels relative to calcium channels at the photoreceptor ribbon synapse. Journal of Neurophysiology 105, 321335.CrossRefGoogle ScholarPubMed
Meuleman, J., van de Pavert, S.A. & Wijnholds, J. (2004). Crumbs homologue 1 in polarity and blindness. Biochemical Society Transactions 32, 828830.Google Scholar
Migdale, K., Herr, S., Klug, K., Ahmad, K., Linberg, K., Sterling, P. & Schein, S. (2003). Two ribbon synaptic units in rod photoreceptors of macaque, human, and cat. The Journal of Comparative Neurology 455, 100112.Google Scholar
Miller, R.J. (1991). The control of neuronal Ca2+ homeostasis. Progress in Neurobiology 37, 255285.Google Scholar
Mizuno, F., Barabas, P., Krizaj, D. & Akopian, A. (2010). Glutamate-induced internalization of Ca(v)1.3 L-type Ca(2+) channels protects retinal neurons against excitotoxicity. The Journal of Physiology 588, 953966.Google Scholar
Molday, L.L., Wu, W.W. & Molday, R.S. (2007). Retinoschisin (RS1), the protein encoded by the X-linked retinoschisis gene, is anchored to the surface of retinal photoreceptor and bipolar cells through its interactions with a Na/K ATPase-SARM1 complex. The Journal of Biological Chemistry 282, 3279232801.Google Scholar
Morgans, C. & Brandstätter, J.H. (2000). SNAP-25 is present on the Golgi apparatus of retinal neurons. Neuroreport 11, 8588.Google Scholar
Morgans, C.W. (1999). Calcium channel heterogeneity among cone photoreceptors in the tree shrew retina. The Europena Journal of Neuroscience 11, 29892993.Google Scholar
Morgans, C.W. (2000). Presynaptic proteins of ribbon synapses in the retina. Microscopy Research and Technique 50, 141150.Google Scholar
Morgans, C.W. (2001). Localization of the alpha(1F) calcium channel subunit in the rat retina. Investigative Ophthalmology & Visual Science 42, 24142418.Google Scholar
Morgans, C.W., Bayley, P.R., Oesch, N.W., Ren, G., Akileswaran, L. & Taylor, W.R. (2005). Photoreceptor calcium channels: Insight from night blindness. Visual Neuroscience 22, 561568.CrossRefGoogle ScholarPubMed
Morgans, C.W., Brandstätter, J.H., Kellerman, J., Betz, H. & Wässle, H. (1996). A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. The Journal of Neuroscience 16, 67136721.Google Scholar
Morgans, C.W., Brown, R.L. & Duvoisin, R.M. (2010). TRPM1: The endpoint of the mGluR6 signal transduction cascade in retinal ON-bipolar cells. BioEssays 32, 609614.Google Scholar
Morgans, C.W., El Far, O., Berntson, A., Wässle, H. & Taylor, W.R. (1998). Calcium extrusion from mammalian photoreceptor terminals. The Journal of Neuroscience 18, 24672474.Google Scholar
Morgans, C.W., Gaughwin, P. & Maleszka, R. (2001). Expression of the alpha1F calcium channel subunit by photoreceptors in the rat retina. Molecular Vision 7, 202209.Google Scholar
Mukherjee, K., Yang, X., Gerber, S.H., Kwon, H.B., Ho, A., Castillo, P.E., Liu, X. & Südhof, T.C. (2010). Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proceedings of the National Academy of Sciences of the United States of America 107, 65046509.Google Scholar
Muresan, V., Lyass, A. & Schnapp, B.J. (1999). The kinesin motor KIF3A is a component of the presynaptic ribbon in vertebrate photoreceptors. The Journal of Neuroscience 19, 10271037.Google Scholar
Nachman-Clewner, M., St Jules, R. & Townes-Anderson, E. (1999). L-type calcium channels in the photoreceptor ribbon synapse: Localization and role in plasticity. The Journal of Comparative Neurology 415, 116.Google Scholar
Nagle, B.W., Okamoto, C., Taggart, B. & Burnside, B. (1986). The teleost cone cytoskeleton. Localization of actin, microtubules, and intermediate filaments. Investigative Ophthalmology & Visual Science 27, 689701.Google Scholar
Naraghi, M. & Neher, E. (1997). Linearized buffered Ca2+ diffusion in microdomains and its implications for calculation of [Ca2+] at the mouth of a calcium channel. The Journal of Neuroscience 17, 69616973.Google Scholar
Neher, E. & Sakaba, T. (2008). Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59, 861872.Google Scholar
Nourry, C., Grant, S.G. & Borg, J.P. (2003). PDZ domain proteins: Plug and play! Science’s STKE 2003, RE7.Google Scholar
Nouvian, R., Neef, J., Bulankina, A.V., Reisinger, E., Pangršič, T., Frank, T., Sikorra, S., Brose, N., Binz, T. & Moser, T. (2011). Exocytosis at the hair cell ribbon synapse apparently operates without neuronal SNARE proteins. Nature Neuroscience 14, 411413.Google Scholar
Oertner, T.G. & Matus, A. (2005). Calcium regulation of actin dynamics in dendritic spines. Cell Calcium 37, 477482.Google Scholar
Ohara-Imaizumi, M., Ohtsuka, T., Matsushima, S., Akimoto, Y., Nishiwaki, C., Nakamichi, Y., Kikuta, T., Nagai, S., Kawakami, H., Watanabe, T. & Nagamatsu, S. (2005). ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic beta cells and functions in insulin exocytosis: Interaction of ELKS with exocytotic machinery analyzed by total internal reflection fluorescence microscopy. Molecular Biology of the Cell 16, 32893300.Google Scholar
Pang, Z.P. & Südhof, T.C. (2010). Cell biology of Ca2+-triggered exocytosis. Current Opinion in Cell Biology 22, 496505.Google Scholar
Park, J.B., Kim, J.S., Lee, J.Y., Kim, J., Seo, J.Y. & Kim, A.R. (2002). GTP binds to Rab3A in a complex with Ca2+/calmodulin. The Biochemical Journal 362, 651657.Google Scholar
Park, T.K., Wu, Z., Kjellstrom, S., Zeng, Y., Bush, R.A., Sieving, P.A. & Colosi, P. (2009). Intravitreal delivery of AAV8 retinoschisin results in cell type-specific gene expression and retinal rescue in the Rs1-KO mouse. Gene Therapy 16, 916926.Google Scholar
Pearring, J.N., Bojang, P. Jr., Shen, Y., Koike, C., Furukawa, T., Nawy, S. & Gregg, R.G. (2011). A role for nyctalopin, a small leucine-rich repeat protein, in localizing the TRP melastatin 1 channel to retinal depolarizing bipolar cell dendrites. The Journal of Neuroscience 31, 1006010066.Google Scholar
Petrini, E.M., Lu, J., Cognet, L., Lounis, B., Ehlers, M.D. & Choquet, D. (2009). Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63, 92105.Google Scholar
Pillers, D.A., Fitzgerald, K.M., Duncan, N.M., Rash, S.M., White, R.A., Dwinnell, S.J., Powell, B.R., Schnur, R.E., Ray, P.N., Cibis, G.W. & Weleber, R.G. (1999). Duchenne/Becker muscular dystrophy: Correlation of phenotype by electroretinography with sites of dystrophin mutations. Human Genetics 105, 29.Google Scholar
Prescott, E.D. & Zenisek, D. (2005). Recent progress towards understanding the synaptic ribbon. Current Opinion in Neurobiology 15, 431436.Google Scholar
Pusch, C.M., Zeitz, C., Brandau, O., Pesch, K., Achatz, H., Feil, S., Scharfe, C., Maurer, J., Jacobi, F.K., Pinckers, A., Andreasson, S., Hardcastle, A., Wissinger, B., Berger, W. & Meindl, A. (2000). The complete form of X-linked congenital stationary night blindness is caused by mutations in a gene encoding a leucine-rich repeat protein. Nature Genetics 26, 324327.Google Scholar
Qu, Y., Baroudi, G., Yue, Y., El-Sherif, N. & Boutjdir, M. (2005). Localization and modulation of {alpha}1D (Cav1.3) L-type Ca channel by protein kinase A. American Journal of Physiology. Heart and Circulatory Physiology 288, H2123H2130.Google Scholar
Raviola, E. & Gilula, N.B. (1975). Intramembrane organization of specialized contacts in the outer plexiform layer of the retina. A freeze-fracture study in monkeys and rabbits. The Journal of Cell Biology 65, 192222.CrossRefGoogle ScholarPubMed
Raviola, E. & Raviola, G. (1982). Structure of the synaptic membranes in the inner plexiform layer of the retina: A freeze-fracture study in monkeys and rabbits. The Journal of Comparative Neurology 209, 233248.Google Scholar
Rea, R., Li, J., Dharia, A., Levitan, E.S., Sterling, P. & Kramer, R.H. (2004). Streamlined synaptic vesicle cycle in cone photoreceptor terminals. Neuron 41, 755766.Google Scholar
Regus-Leidig, H., tom Dieck, S. & Brandstätter, J.H. (2010). Absence of functional active zone protein Bassoon affects assembly and transport of ribbon precursors during early steps of photoreceptor synaptogenesis. European Journal of Cell Biology 89, 468475.Google Scholar
Regus-Leidig, H., tom Dieck, S., Specht, D., Meyer, L. & Brandstätter, J.H. (2009). Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: The involvement of precursor spheres. The Journal of Comparative Neurology 512, 814824.Google Scholar
Reim, K., Wegmeyer, H., Brandstätter, J.H., Xue, M., Rosenmund, C., Dresbach, T., Hofmann, K. & Brose, N. (2005). Structurally and functionally unique complexins at retinal ribbon synapses. The Journal of Cell Biology 169, 669680.Google Scholar
Reiners, J., Märker, T., Jürgens, K., Reidel, B. & Wolfrum, U. (2005 a). Photoreceptor expression of the Usher syndrome type 1 protein protocadherin 15 (USH1F) and its interaction with the scaffold protein harmonin (USH1C). Molecular Vision 11, 347355.Google Scholar
Reiners, J., Nagel-Wolfrum, K., Jürgens, K., Märker, T. & Wolfrum, U. (2006). Molecular basis of human Usher syndrome: Deciphering the meshes of the Usher protein network provides insights into the pathomechanisms of the Usher disease. Experimental Eye Research 83, 97119.Google Scholar
Reiners, J., Reidel, B., El-Amraoui, A., Boëda, B., Huber, I., Petit, C. & Wolfrum, U. (2003). Differential distribution of harmonin isoforms and their possible role in Usher-1 protein complexes in mammalian photoreceptor cells. Investigative Ophthalmology & Visual Science 44, 50065015.Google Scholar
Reiners, J., van Wijk, E., Märker, T., Zimmermann, U., Jürgens, K., te Brinke, H., Overlack, N., Roepman, R., Knipper, M., Kremer, H. & Wolfrum, U. (2005 b). Scaffold protein harmonin (USH1C) provides molecular links between Usher syndrome type 1 and type 2. Human Molecular Genetics 14, 39333943.Google Scholar
Renner, M., Choquet, D. & Triller, A. (2009). Control of the postsynaptic membrane viscosity. The Journal of Neuroscience 29, 29262937.Google Scholar
Richardson, G.P., de Monvel, J.B. & Petit, C. (2011). How the genetics of deafness illuminates auditory physiology. Annual Review of Physiology 73, 311334.Google Scholar
Richter, K., Langnaese, K., Kreutz, M.R., Olias, G., Zhai, R., Scheich, H., Garner, C.C. & Gundelfinger, E.D. (1999). Presynaptic cytomatrix protein bassoon is localized at both excitatory and inhibitory synapses of rat brain. The Journal of Comparative Neurology 408, 437448.Google Scholar
Rieke, F. & Schwartz, E.A. (1996). Asynchronous transmitter release: Control of exocytosis and endocytosis at the salamander rod synapse. The Journal of Physiology 493, 18.Google Scholar
Roux, I., Safieddine, S., Nouvian, R., Grati, M., Simmler, M.C., Bahloul, A., Perfettini, I., Le Gall, M., Rostaing, P., Hamard, G., Triller, A., Avan, P., Moser, T. & Petit, C. (2006). Otoferlin, defective in a human deafness form, is essential for exocytosis at the auditory ribbon synapse. Cell 127, 277289.Google Scholar
Rusakov, D.A. (2006). Ca2+-dependent mechanisms of presynaptic control at central synapses. The Neuroscientist 12, 317326.Google Scholar
Rust, M.B., Gurniak, C.B., Renner, M., Vara, H., Morando, L., Görlich, A., Sassoè-Pognetto, M., Banchaabouchi, M.A., Giustetto, M., Triller, A., Choquet, D. & Witke, W. (2010). Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. The EMBO Journal 29, 18891902.CrossRefGoogle ScholarPubMed
Rzadzinska, A.K., Schneider, M.E., Davies, C., Riordan, G.P. & Kachar, B. (2004). An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. The Journal of Cell Biology 164, 887897.Google Scholar
Sakaba, T. & Neher, E. (2001). Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse. Neuron 32, 11191131.Google Scholar
Salaün, C., Gould, G.W. & Chamberlain, L.H. (2005). The SNARE proteins SNAP-25 and SNAP-23 display different affinities for lipid rafts in PC12 cells. Regulation by distinct cysteine-rich domains. The Journal of Biological Chemistry 280, 12361240.Google Scholar
Sato, S., Omori, Y., Katoh, K., Kondo, M., Kanagawa, M., Miyata, K., Funabiki, K., Koyasu, T., Kajimura, N., Miyoshi, T., Sawai, H., Kobayashi, K., Tani, A., Toda, T., Usukura, J., Tano, Y., Fujikado, T. & Furukawa, T. (2008). Pikachurin, a dystroglycan ligand, is essential for photoreceptor ribbon synapse formation. Nature Neuroscience 11, 923931.CrossRefGoogle ScholarPubMed
Satz, J.S., Philp, A.R., Nguyen, H., Kusano, H., Lee, J., Turk, R., Riker, M.J., Hernández, J., Weiss, R.M., Anderson, M.G., Mullins, R.F., Moore, S.A., Stone, E.M. & Campbell, K.P. (2009). Visual impairment in the absence of dystroglycan. The Journal of Neuroscience 29, 1313613146.Google Scholar
Schaeffer, S.F., Raviola, E. & Heuser, J.E. (1982). Membrane specializations in the outer plexiform layer of the turtle retina. The Journal of Comparative Neurology 204, 253267.Google Scholar
Schmitz, F. (2009). The making of synaptic ribbons: How they are built and what they do. The Neuroscientist 15, 611624.Google Scholar
Schmitz, F. & Drenckhahn, D. (1993). Distribution of actin in cone photoreceptor synapses. Histochemistry 100, 3540.Google Scholar
Schmitz, F. & Drenckhahn, D. (1997). Localization of dystrophin and beta-dystroglycan in bovine retinal photoreceptor processes extending into the postsynaptic dendritic complex. Histochemistry and Cell Biology 108, 249255.Google Scholar
Schmitz, F., Holbach, M. & Drenckhahn, D. (1993). Colocalization of retinal dystrophin and actin in postsynaptic dendrites of rod and cone photoreceptor synapses. Histochemistry 100, 473479.Google Scholar
Schmitz, F., Königstorfer, 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, 857872.Google Scholar
Schmitz, F., Tabares, L., Khimich, D., Strenzke, N., de la Villa-Polo, P., Castellano-Muñoz, M., Bulankina, A., Moser, T., Fernández-Chacón, R. & Südhof, T.C. (2006). CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proceedings of the National Academy of Sciences of the United States of America 103, 29262931.Google Scholar
Schneggenburger, R. & Neher, E. (2000). Intracellular calcium dependence of transmitter release rates at a fast central synapse. Nature 406, 889893.Google Scholar
Schneider, M.E., Belyantseva, I.A., Azevedo, R.B. & Kachar, B. (2002). Rapid renewal of auditory hair bundles. Nature 418, 837838.Google Scholar
Schoch, S., Castillo, P.E., Jo, T., Mukherjee, K., Geppert, M., Wang, Y., Schmitz, F., Malenka, R.C. & Südhof, T.C. (2002). RIM1alpha forms a protein scaffold for regulating neurotransmitter release at the active zone. Nature 415, 321326.Google Scholar
Schubert, T. & Akopian, A. (2004). Actin filaments regulate voltage-gated ion channels in salamander retinal ganglion cells. Neuroscience 125, 583590.CrossRefGoogle ScholarPubMed
Sergeev, Y.V., Caruso, R.C., Meltzer, M.R., Smaoui, N., MacDonald, I.M. & Sieving, P.A. (2010). Molecular modeling of retinoschisin with functional analysis of pathogenic mutations from human X-linked retinoschisis. Human Molecular Genetics 19, 13021313.Google Scholar
Sharma, M., Burré, J. & Südhof, T.C. (2011). CSPα promotes SNARE-complex assembly by chaperoning SNAP-25 during synaptic activity. Nature Cell Biology 13, 3039.Google Scholar
Shen, Y., Heimel, J.A., Kamermans, M., Peachey, N.S., Gregg, R.G. & Nawy, S. (2009). A transient receptor potential-like channel mediates synaptic transmission in rod bipolar cells. The Journal of Neuroscience 29, 60886093.Google Scholar
Sheng, Z., Choi, S.Y., Dharia, A., Li, J., Sterling, P. & Kramer, R.H. (2007). Synaptic Ca2+ in darkness is lower in rods than cones, causing slower tonic release of vesicles. The Journal of Neuroscience 27, 50335042.Google Scholar
Sherry, D.M. & Heidelberger, R. (2005). Distribution of proteins associated with synaptic vesicle endocytosis in the mouse and goldfish retina. The Journal of Comparative Neurology 484, 440457.Google 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. BMC Neuroscience 7, 54.Google Scholar
Sherry, D.M., Yang, H. & Standifer, K.M. (2001). Vesicle-associated membrane protein isoforms in the tiger salamander retina. The Journal of Comparative Neurology 431, 424436.Google Scholar
Shi, L., Jian, K., Ko, M.L., Trump, D. & Ko, G.Y. (2009). Retinoschisin, a new binding partner for L-type voltage-gated calcium channels in the retina. The Journal of Biological Chemistry 284, 39663975.Google Scholar
Song, W. & Zinsmaier, K.E. (2003). Endophilin and synaptojanin hook up to promote synaptic vesicle endocytosis. Neuron 40, 665667.Google Scholar
Specht, C.G. & Triller, A. (2008). The dynamics of synaptic scaffolds. BioEssays 30, 10621074.Google Scholar
Specht, D., Wu, S.B., Turner, P., Dearden, P., Koentgen, F., Wolfrum, U., Maw, M., Brandstätter, J.H. & tom Dieck, S. (2009). Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Investigative Ophthalmology & Visual Science 50, 505515.Google Scholar
Spencer, M., Moon, R.T. & Milam, A.H. (1991). Membrane skeleton protein 4.1 in inner segments of retinal cones. Investigative Ophthalmology & Visual Science 32, 17.Google Scholar
Spiwoks-Becker, I., Glas, M., Lasarzik, I. & Vollrath, L. (2004). Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes. The European Journal of Neuroscience 19, 15591571.Google Scholar
Steiner-Champliaud, M.F., Sahel, J. & Hicks, D. (2006). Retinoschisin forms a multi-molecular complex with extracellular matrix and cytoplasmic proteins: Interactions with beta2 laminin and alphaB-crystallin. Molecular Vision 12, 892901.Google Scholar
Stella, S.L. Jr. & Thoreson, W.B. (2000). Differential modulation of rod and cone calcium currents in tiger salamander retina by D2 dopamine receptors and cAMP. The European Journal of Neuroscience 12, 35373548.Google Scholar
Sterling, P. & Matthews, G. (2005). Structure and function of ribbon synapses. Trends in Neurosciences 28, 2029.Google Scholar
Stöhr, H., Heisig, J.B., Benz, P.M., Schöberl, S., Milenkovic, V.M., Strauss, O., Aartsen, W.M., Wijnholds, J., Weber, B.H. & Schulz, H.L. (2009). TMEM16B, a novel protein with calcium-dependent chloride channel activity, associates with a presynaptic protein complex in photoreceptor terminals. The Journal of Neuroscience 29, 68096818.Google Scholar
Stöhr, H., Molday, L.L., Molday, R.S., Weber, B.H., Biedermann, B., Reichenbach, A. & Krämer, F. (2005). Membrane-associated guanylate kinase proteins MPP4 and MPP5 associate with Veli3 at distinct intercellular junctions of the neurosensory retina. The Journal of Comparative Neurology 481, 3141.Google Scholar
Straub, V. & Campbell, K.P. (1997). Muscular dystrophies and the dystrophin-glycoprotein complex. Current Opinion in Neurology 10, 168175.Google Scholar
Striessnig, J., Bolz, H.J. & Koschak, A. (2010). Channelopathies in Cav1.1, Cav1.3, and Cav1.4 voltage-gated L-type Ca2+ channels. Pflügers Archive 460, 361374.Google Scholar
Strom, T.M., Nyakatura, G., Apfelstedt-Sylla, E., Hellebrand, H., Lorenz, B., Weber, B.H., Wutz, K., Gutwillinger, N., Rüther, K., Drescher, B., Sauer, C., Zrenner, E., Meitinger, T., Rosenthal, A. & Meindl, A. (1998). An L-type calcium-channel gene mutated in incomplete X-linked congenital stationary night blindness. Nature Genetics 19, 260263.Google Scholar
Takada, Y., Fariss, R.N., Tanikawa, A., Zeng, Y., Carper, D., Bush, R. & Sieving, P.A. (2004). A retinal neuronal developmental wave of retinoschisin expression begins in ganglion cells during layer formation. Investigative Ophthalmology & Visual Science 45, 33023312.Google Scholar
Takada, Y., Vijayasarathy, C., Zeng, Y., Kjellstrom, S., Bush, R.A. & Sieving, P.A. (2008). Synaptic pathology in retinoschisis knockout (Rs1-/y) mouse retina and modification by rAAV-Rs1 gene delivery. Investigative Ophthalmology & Visual Science 49, 36773686.Google Scholar
Takahashi, S.X., Miriyala, J. & Colecraft, H.M. (2004). Membrane-associated guanylate kinase-like properties of beta-subunits required for modulation of voltage-dependent Ca2+ channels. Proceedings of the National Academy of Sciences of the United States of America 101, 71937198.Google Scholar
Takamori, S., Holt, M., Stenius, K., Lemke, E.A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S.A., Rammner, B., Gräter, F., Hub, J.S., De Groot, B.L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., Heuser, J., Wieland, F. & Jahn, R. (2006). Molecular anatomy of a trafficking organelle. Cell 127, 831846.Google Scholar
Takao-Rikitsu, E., Mochida, S., Inoue, E., Deguchi-Tawarada, M., Inoue, M., Ohtsuka, T. & Takai, Y. (2004). Physical and functional interaction of the active zone proteins, CAST, RIM1, and Bassoon, in neurotransmitter release. The Journal of Cell Biology 164, 301311.Google Scholar
Talts, J.F., Andac, Z., Göhring, W., Brancaccio, A. & Timpl, R. (1999). Binding of the G domains of laminin alpha1 and alpha2 chains and perlecan to heparin, sulfatides, alpha-dystroglycan and several extracellular matrix proteins. The EMBO Journal 18, 863870.Google Scholar
Tantri, A., Vrabec, T.R., Cu-Unjieng, A., Frost, A., Annesley, W.H. Jr. & Donoso, L.A. (2004). X-linked retinoschisis: A clinical and molecular genetic review. Survey of Ophthalmology 49, 214230.Google Scholar
Taverna, E., Saba, E., Linetti, A., Longhi, R., Jeromin, A., Righi, M., Clementi, F. & Rosa, P. (2007). Localization of synaptic proteins involved in neurosecretion in different membrane microdomains. Journal of Neurochemistry 100, 664677.Google Scholar
Taverna, E., Saba, E., Rowe, J., Francolini, M., Clementi, F. & Rosa, P. (2004). Role of lipid microdomains in P/Q-type calcium channel (Cav2.1) clustering and function in presynaptic membranes. The Journal of Biological Chemistry 279, 51275134.Google Scholar
Thoreson, W.B. (2007). Kinetics of synaptic transmission at ribbon synapses of rods and cones. Molecular Neurobiology 36, 205223.Google Scholar
Thoreson, W.B., Nitzan, R. & Miller, R.F. (1997). Reducing extracellular Cl− suppresses dihydropyridine-sensitive Ca2+ currents and synaptic transmission in amphibian photoreceptors. Journal of Neurophysiology 77, 21752190.Google Scholar
Thoreson, W.B., Rabl, K., Townes-Anderson, E. & Heidelberger, R. (2004). A highly Ca2+-sensitive pool of vesicles contributes to linearity at the rod photoreceptor ribbon synapse. Neuron 42, 595605.Google Scholar
Tokoro, T., Higa, S., Deguchi-Tawarada, M., Inoue, E., Kitajima, I. & Ohtsuka, T. (2007). Localization of the active zone proteins CAST, ELKS, and Piccolo at neuromuscular junctions. Neuroreport 18, 313316.Google Scholar
Tolosa de Talamoni, N., Pérez, A., Riis, R., Smith, C., Norman, M.L. & Wasserman, R.H. (2002). Comparative immunolocalization of the plasma membrane calcium pump and calbindin D28K in chicken retina during embryonic development. European Journal of Histochemistry 46, 333340.Google Scholar
tom Dieck, S., Altrock, W.D., Kessels, M.M., Qualmann, B., Regus, H., Brauner, D., Fejtová, 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, 825836.Google Scholar
tom Dieck, S. & Brandstätter, J.H. (2006). Ribbon synapses of the retina. Cell and Tissue Research 326, 339346.Google Scholar
tom Dieck, S., Sanmartí-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K.H., Kämpf, U., Fränzer, J.T., Stumm, M., Garner, C.C. & Gundelfinger, E.D. (1998). Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. The Journal of Cell Biology 142, 499509.Google Scholar
Townes-Anderson, E., MacLeish, P.R. & Raviola, E. (1985). Rod cells dissociated from mature salamander retina: Ultrastructure and uptake of horseradish peroxidase. The Journal of Cell Biology 100, 175188.Google Scholar
Ueda, H., Gohdo, T. & Ohno, S. (1998). Beta-dystroglycan localization in the photoreceptor and Müller cells in the rat retina revealed by immunoelectron microscopy. The Journal of Histochemistry and Cytochemistry 46, 185191.Google Scholar
Ueda, H., Kobayashi, T., Mitsui, K., Tsurugi, K., Tsukahara, S. & Ohno, S. (1995). Dystrophin localization at presynapse in rat retina revealed by immunoelectron microscopy. Investigative Ophthalmology & Visual Science 36, 23182322.Google Scholar
Ullrich, B. & Südhof, T.C. (1994). Distribution of synaptic markers in the retina: Implications for synaptic vesicle traffic in ribbon synapses. Journal of Physiology, Paris 88, 249257.CrossRefGoogle ScholarPubMed
Uthaiah, R.C. & Hudspeth, A.J. (2010). Molecular anatomy of the hair cell’s ribbon synapse. The Journal of Neuroscience 30, 1238712399.Google Scholar
van den Hurk, J.A., Rashbass, P., Roepman, R., Davis, J., Voesenek, K.E., Arends, M.L., Zonneveld, M.N., van Roekel, M.H., Cameron, K., Rohrschneider, K., Heckenlively, J.R., Koenekoop, R.K., Hoyng, C.B., Cremers, F.P. & den Hollander, A.I. (2005). Characterization of the Crumbs homolog 2 (CRB2) gene and analysis of its role in retinitis pigmentosa and Leber congenital amaurosis. Molecular Vision 11, 263273.Google Scholar
van de Pavert, S.A., Kantardzhieva, A., Malysheva, A., Meuleman, J., Versteeg, I., Levelt, C., Klooster, J., Geiger, S., Seeliger, M.W., Rashbass, P., Le Bivic, A. & Wijnholds, J. (2004). Crumbs homologue 1 is required for maintenance of photoreceptor cell polarization and adhesion during light exposure. Journal of Cell Science 117, 41694177.Google Scholar
Van Epps, H.A., Hayashi, M., Lucast, L., Stearns, G.W., Hurley, J.B., De Camilli, P. & Brockerhoff, S.E. (2004). The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin 1 in cone photoreceptor ribbon anchoring. The Journal of Neuroscience 24, 86418650.Google Scholar
van Genderen, M.M., Bijveld, M.M., Claassen, Y.B., Florijn, R.J., Pearring, J.N., Meire, F.M., McCall, M.A., Riemslag, F.C., Gregg, R.G., Bergen, A.A. & Kamermans, M. (2009). Mutations in TRPM1 are a common cause of complete congenital stationary night blindness. American Journal of Human Genetics 85, 730736.Google Scholar
Vecino, E. & Avila, J. (2001). Distribution of the phosphorylated form of microtubule associated protein 1B in the fish visual system during optic nerve regeneration. Brain Research Bulletin 56, 131137.Google Scholar
Vijayasarathy, C., Takada, Y., Zeng, Y., Bush, R.A. & Sieving, P.A. (2007). Retinoschisin is a peripheral membrane protein with affinity for anionic phospholipids and affected by divalent cations. Investigative Ophthalmology & Visual Science 48, 9911000.Google Scholar
Vijayasarathy, C., Takada, Y., Zeng, Y., Bush, R.A. & Sieving, P.A. (2008). Organization and molecular interactions of retinoschisin in photoreceptors. Advances in Experimental Medicine and Biology 613, 291297.Google Scholar
Vollrath, L. & Spiwoks-Becker, I. (1996). Plasticity of retinal ribbon synapses. Microscopy Research and Technique 35, 472487.Google Scholar
von Kriegstein, K. & Schmitz, F. (2003). The expression pattern and assembly profile of synaptic membrane proteins in ribbon synapses of the developing mouse retina. Cell and Tissue Research 311, 159173.Google Scholar
Von Kriegstein, K., Schmitz, F., Link, E. & Südhof, T.C. (1999). Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. The European Journal of Neuroscience 11, 13351348.Google Scholar
Wagner, H.J. & Djamgoz, M.B. (1993). Spinules: A case for retinal synaptic plasticity. Trends in Neurosciences 16, 201206.Google Scholar
Wahlin, K.J., Moreira, E.F., Huang, H., Yu, N. & Adler, R. (2008). Molecular dynamics of photoreceptor synapse formation in the developing chick retina. The Journal of Comparative Neurology 506, 822837.Google Scholar
Waite, A., Tinsley, C.L., Locke, M. & Blake, D.J. (2009). The neurobiology of the dystrophin-associated glycoprotein complex. Annals of Medicine 41, 344359.Google Scholar
Wan, L., Almers, W. & Chen, W. (2005). Two ribeye genes in teleosts: The role of Ribeye in ribbon formation and bipolar cell development. The Journal of Neuroscience 25, 941949.Google Scholar
Wanaverbecq, N., Marsh, S.J., Al-Qatari, M. & Brown, D.A. (2003). The plasma membrane calcium-ATPase as a major mechanism for intracellular calcium regulation in neurones from the rat superior cervical ganglion. The Journal of Physiology 550, 83101.Google Scholar
Wang, X., Hu, B., Zieba, A., Neumann, N.G., Kasper-Sonnenberg, M., Honsbein, A., Hultqvist, G., Conze, T., Witt, W., Limbach, C., Geitmann, M., Danielson, H., Kolarow, R., Niemann, G., Lessmann, V. & Kilimann, M.W. (2009). A protein interaction node at the neurotransmitter release site: Domains of Aczonin/Piccolo, Bassoon, CAST, and rim converge on the N-terminal domain of Munc13-1. The Journal of Neuroscience 29, 1258412596.Google Scholar
Wang, Y., Okamoto, M., Schmitz, F., Hofmann, K. & Südhof, T.C. (1997). Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388, 593598.Google Scholar
Weber, B.H., Schrewe, H., Molday, L.L., Gehrig, A., White, K.L., Seeliger, M.W., Jaissle, G.B., Friedburg, C., Tamm, E. & Molday, R.S. (2002). Inactivation of the murine X-linked juvenile retinoschisis gene, Rs1h, suggests a role of retinoschisin in retinal cell layer organization and synaptic structure. Proceedings of the National Academy of Sciences of the United States of America 99, 62226227.Google Scholar
Weber, A.M., Wong, F.K., Tufford, A.R., Schlichter, L.C., Matveev, V. & Stanley, E.F. (2010). N-type Ca2+ channels carry the largest current: Implications for nanodomains and transmitter release. Nature Neuroscience 13, 13481350.Google Scholar
Wilkinson, M.F. & Barnes, S. (1996). The dihydropyridine-sensitive calcium channel subtype in cone photoreceptors. The Journal of General Physiology 107, 621630.Google Scholar
Williams, D.S. (2008). Usher syndrome: Animal models, retinal function of Usher proteins, and prospects for gene therapy. Vision Research 48, 433441.Google Scholar
Williams, D.S., Aleman, T.S., Lillo, C., Lopes, V.S., Hughes, L.C., Stone, E.M. & Jacobson, S.G. (2009). Harmonin in the murine retina and the retinal phenotypes of Ush1c-mutant mice and human USH1C. Investigative Ophthalmology & Visual Science 50, 38813889.Google Scholar
Wu, J., Marmorstein, A.D., Striessnig, J. & Peachey, N.S. (2003). Voltage-dependent calcium channel CaV1.3 subunits regulate the light peak of the electroretinogram. Journal of Neurophysiology 97, 37313735.Google Scholar
Wu, J., Marmorstein, A.D., Striessnig, J. & Peachey, N.S. (2007). Voltage-dependent calcium channel CaV1.3 subunits regulate the light peak of the electroretinogram. Journal of Neurophysiology 97, 37313735.Google Scholar
Wu, W.W. & Molday, R.S. (2003). Defective discoidin domain structure, subunit assembly, and endoplasmic reticulum processing of retinoschisin are primary mechanisms responsible for X-linked retinoschisis. The Journal of Biological Chemistry 278, 2813928146.Google Scholar
Wycisk, K.A., Budde, B., Feil, S., Skosyrski, S., Buzzi, F., Neidhardt, J., Glaus, E., Nürnberg, P., Ruether, K. & Berger, W. (2006 a). Structural and functional abnormalities of retinal ribbon synapses due to Cacna2d4 mutation. Investigative Ophthalmology & Visual Science 47, 35233530.Google Scholar
Wycisk, K.A., Zeitz, C., Feil, S., Wittmer, M., Forster, U., Neidhardt, J., Wissinger, B., Zrenner, E., Wilke, R., Kohl, S. & Berger, W. (2006 b). Mutation in the auxiliary calcium-channel subunit CACNA2D4 causes autosomal recessive cone dystrophy. American Journal of Human Genetics 79, 973977.Google Scholar
Xiao, H., Chen, X. & Steele, E.C. Jr. (2007). Abundant L-type calcium channel Ca(v)1.3 (alpha1D) subunit mRNA is detected in rod photoreceptors of the mouse retina via in situ hybridization. Molecular Vision 13, 764771.Google Scholar
Xu, J.W. & Slaughter, M.M. (2005). Large-conductance calcium-activated potassium channels facilitate transmitter release in salamander rod synapse. The Journal of Neuroscience 25, 76607668.Google Scholar
Yamagata, M. & Sanes, J.R. (2010). Synaptic localization and function of Sidekick recognition molecules require MAGI scaffolding proteins. The Journal of Neuroscience 30, 35793588.Google Scholar
Yamagata, M., Weiner, J.A. & Sanes, J.R. (2002). Sidekicks: Synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110, 649660.Google Scholar
Yan, D. & Liu, X.Z. (2010). Genetics and pathological mechanisms of Usher syndrome. Journal of Human Genetics 55, 327335.Google Scholar
Yang, P.S., Alseikhan, B.A., Hiel, H., Grant, L., Mori, M.X., Yang, W., Fuchs, P.A. & Yue, D.T. (2006). Switching of Ca2+-dependent inactivation of Ca(v)1.3 channels by calcium binding proteins of auditory hair cells. The Journal of Neuroscience 26, 1067710689.Google Scholar
Yang, J., Liu, X., Zhao, Y., Adamian, M., Pawlyk, B., Sun, X., McMillan, D.R., Liberman, M.C. & Li, T. (2010). Ablation of whirlin long isoform disrupts the USH2 protein complex and causes vision and hearing loss. PLoS Genetics 6, e1000955.Google Scholar
Yang, J., Pawlyk, B., Wen, X.H., Adamian, M., Soloviev, M., Michaud, N., Zhao, Y., Sandberg, M.A., Makino, C.L. & Li, T. (2007). Mpp4 is required for proper localization of plasma membrane calcium ATPases and maintenance of calcium homeostasis at the rod photoreceptor synaptic terminals. Human Molecular Genetics 16, 10171029.Google Scholar
Zallocchi, M., Meehan, D.T., Delimont, D., Askew, C., Garige, S., Gratton, M.A., Rothermund-Franklin, C.A. & Cosgrove, D. (2009). Localization and expression of clarin-1, the Clrn1 gene product, in auditory hair cells and photoreceptors. Hearing Research 255, 109120.Google Scholar
Zampighi, G.A., Schietroma, C., Zampighi, L.M., Woodruff, M., Wright, E.M. & Brecha, N.C. (2011). Conical tomography of a ribbon synapse: Structural evidence for vesicle fusion. PLoS One 6, e16944.Google Scholar
Zanazzi, G. & Matthews, G. (2009). The molecular architecture of ribbon presynaptic terminals. Molecular Neurobiology 39, 130148.Google Scholar
Zanazzi, G. & Matthews, G. (2010). Enrichment and differential targeting of complexins 3 and 4 in ribbon-containing sensory neurons during zebrafish development. Neural Development 5, 24.Google Scholar
Zenisek, D. (2008). Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proceedings of the National Academy of Sciences of the United States of America 105, 49224927.Google Scholar
Zenisek, D., Horst, N.K., Merrifield, C., Sterling, P. & Matthews, G. (2004). Visualizing synaptic ribbons in the living cell. The Journal of Neuroscience 24, 97529759.Google Scholar
Zhai, R.G. & Bellen, H.J. (2004). The architecture of the active zone in the presynaptic nerve terminal. Physiology (Bethesda) 19, 262270.Google Scholar
Zhang, H., Maximov, A., Fu, Y., Xu, F., Tang, T.S., Tkatch, T., Surmeier, D.J. & Bezprozvanny, I. (2005). Association of CaV1.3 L-type calcium channels with Shank. The Journal of Neuroscience 25, 10371049.Google Scholar