Abstract
Photoreceptor cells are sensory neurons and does not possess dendrites, whereas photoreceptor axonal terminals develop a specialized synaptic structure called ribbon synapses that contains electro-dense horseshoe-like ribbons. Photoreceptor ribbon synapses have connections with dendritic terminals of bipolar cells and tips of horizontal cell processes, and therefore are critical for visual transduction. In both humans and genetically modified mice, loss of function in photoreceptor synaptic components and its regulators often causes visual impairment and retinal diseases including retinitis pigmentosa and night blindness. In this chapter, we review and discuss the development of photoreceptor ribbon synapses and the functions of ribbon synapse key components.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Babai N, Bartoletti TM, Thoreson WB (2010) Calcium regulates vesicle replenishment at the cone ribbon synapse. J Neurosci 30:15866–15877
Barnes S, Kelly ME (2002) Calcium channels at the photoreceptor synapse. Adv Exp Med Biol 514:465–476
Bech-Hansen NT, Naylor MJ, Maybaum TA, Sparkes RL, Koop B, Birch DG, Bergen AA, Prinsen CF, Polomeno RC, Gal A, Drack AV, Musarella MA, Jacobson SG, Young RS, Weleber RG (2000) Mutations in NYX, encoding the leucine-rich proteoglycan nyctalopin, cause X-linked complete congenital stationary night blindness. Nat Genet 26:319–323
Bessant DA, Payne AM, Mitton KP, Wang QL, Swain PK, Plant C, Bird AC, Zack DJ, Swaroop A, Bhattacharya SS (1999) A mutation in NRL is associated with autosomal dominant retinitis pigmentosa. Nat Genet 21:355–356
Blanks JC, Adinolfi AM, Lolley RN (1974) Synaptogenesis in the photoreceptor terminal of the mouse retina. J Comp Neurol 156:81–93
Boycott B, Wassle H (1999) Parallel processing in the mammalian retina: the Proctor Lecture. Invest Ophthalmol Vis Sci 40:1313–1327
Burghes AH, Logan C, Hu X, Belfall B, Worton RG, Ray PN (1987) A cDNA clone from the Duchenne/Becker muscular dystrophy gene. Nature 328:434–437
Dick O, tom Dieck S, Altrock WD, Ammermuller J, Weiler R, Garner CC, Gundelfinger ED, Brandstatter JH (2003) The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775–786
Dresbach T, Qualmann B, Kessels MM, Garner CC, Gundelfinger ED (2001) The presynaptic cytomatrix of brain synapses. Cell Mol Life Sci 58:94–116
Fisher LJ (1979) Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol 187:359–372
Fitzgerald KM, Cibis GW, Giambrone SA, Harris DJ (1994) Retinal signal transmission in Duchenne muscular dystrophy: evidence for dysfunction in the photoreceptor/depolarizing bipolar cell pathway. J Clin Invest 93:2425–2430
Frank T, Rutherford MA, Strenzke N, Neef A, Pangrsic T, Khimich D, Fejtova A, Gundelfinger ED, Liberman MC, Harke B, Bryan KE, 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 68:724–738
Freund CL, Gregory-Evans CY, Furukawa T, Papaioannou M, Looser J, Ploder L, Bellingham J, Ng D, Herbrick JA, Duncan A, Scherer SW, Tsui LC, Loutradis-Anagnostou A, Jacobson SG, Cepko CL, Bhattacharya SS, McInnes RR (1997) Cone-rod dystrophy due to mutations in a novel photoreceptor-specific homeobox gene (CRX) essential for maintenance of the photoreceptor. Cell 91:543–553
Furukawa T, Morrow EM, Cepko CL (1997) Crx, a novel otx-like homeobox gene, shows photoreceptor-specific expression and regulates photoreceptor differentiation. Cell 91:531–541
Furukawa T, Morrow EM, Li T, Davis FC, Cepko CL (1999) Retinopathy and attenuated circadian entrainment in Crx-deficient mice. Nat Genet 23:466–470
Haeseleer F, Imanishi Y, Maeda T, Possin DE, 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. Nat Neurosci 7:1079–1087
Henry MD, Campbell KP (1996) Dystroglycan: an extracellular matrix receptor linked to the cytoskeleton. Curr Opin Cell Biol 8:625–631
Hoffman EP, Brown RH Jr, Kunkel LM (1987) Dystrophin: the protein product of the Duchenne muscular dystrophy locus. Cell 51:919–928
Howard PL, Dally GY, Wong MH, Ho A, Weleber RG, Pillers DA, Ray PN (1998) Localization of dystrophin isoform Dp71 to the inner limiting membrane of the retina suggests a unique functional contribution of Dp71 in the retina. Hum Mol Genet 7:1385–1391
Hsiau TH, Diaconu C, Myers CA, Lee J, Cepko CL, Corbo JC (2007) The cis-regulatory logic of the mammalian photoreceptor transcriptional network. PLoS One 2:e643
Ibraghimov-Beskrovnaya O, Ervasti JM, Leveille CJ, Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophin-associated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696–702
Ibraghimov-Beskrovnaya O, Milatovich A, Ozcelik T, Yang B, Koepnick K, Francke U, Campbell KP (1993) Human dystroglycan: skeletal muscle cDNA, genomic structure, origin of tissue specific isoforms and chromosomal localization. Hum Mol Genet 2:1651–1657
Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH (2009) Role of the synaptic ribbon in transmitting the cone light response. Nat Neurosci 12:303–310
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. Hum Mol Genet 6:2195–2203
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. J Biol Chem 285:31208–31216
Kunkel LM et al (1986) Analysis of deletions in DNA from patients with Becker and Duchenne muscular dystrophy. Nature 322:73–77
Livesey FJ, Furukawa T, Steffen MA, Church GM, Cepko CL (2000) Microarray analysis of the transcriptional network controlled by the photoreceptor homeobox gene Crx. Curr Biol 10:301–310
Mansergh F, Orton NC, Vessey JP, Lalonde MR, Stell WK, Tremblay F, Barnes S, Rancourt DE, Bech-Hansen NT (2005) Mutation of the calcium channel gene Cacna1f disrupts calcium signaling, synaptic transmission and cellular organization in mouse retina. Hum Mol Genet 14:3035–3046
Masland RH (2001) The fundamental plan of the retina. Nat Neurosci 4:877–886
McLaughlin BJ (1976) A fine structural and E-PTA study of photoreceptor synaptogenesis in the chick retina. J Comp Neurol 170:347–364
Monaco AP, Neve RL, Colletti-Feener C, Bertelson CJ, Kurnit DM, Kunkel LM (1986) Isolation of candidate cDNAs for portions of the Duchenne muscular dystrophy gene. Nature 323:646–650
Morrow EM, Furukawa T, Raviola E, Cepko CL (2005) Synaptogenesis and outer segment formation are perturbed in the neural retina of Crx mutant mice. BMC Neurosci 6:5
Ohtsuka T, Takao-Rikitsu E, Inoue E, Inoue M, Takeuchi M, Matsubara K, Deguchi-Tawarada M, Satoh K, Morimoto K, Nakanishi H, Takai Y (2002) Cast: a novel protein of the cytomatrix at the active zone of synapses that forms a ternary complex with RIM1 and munc13-1. J Cell Biol 158:577–590
Olney JW (1968) An electron microscopic study of synapse formation, receptor outer segment development, and other aspects of developing mouse retina. Invest Ophthalmol 7:250–268
Omori Y, Araki F, Chaya T, Kajimura N, Irie S, Terada K, Muranishi Y, Tsujii T, Ueno S, Koyasu T, Tamaki Y, Kondo M, Amano S, Furukawa T (2012) Presynaptic dystroglycan-pikachurin complex regulates the proper synaptic connection between retinal photoreceptor and bipolar cells. J Neurosci 32:6126–6137
Pillers DA, Weleber RG, Woodward WR, Green DG, Chapman VM, Ray PN (1995) mdxCv3 mouse is a model for electroretinography of Duchenne/Becker muscular dystrophy. Invest Ophthalmol Vis Sci 36:462–466
Pillers DA, Bulman DE, Weleber RG, Sigesmund DA, Musarella MA, Powell BR, Murphey WH, Westall C, Panton C, Becker LE et al (1993) Dystrophin expression in the human retina is required for normal function as defined by electroretinography. Nat Genet 4:82–86
Rao-Mirotznik R, Harkins AB, Buchsbaum G, Sterling P (1995) Mammalian rod terminal: architecture of a binary synapse. Neuron 14:561–569
Rehemtulla A, Warwar R, Kumar R, Ji X, Zack DJ, Swaroop A (1996) The basic motif-leucine zipper transcription factor Nrl can positively regulate rhodopsin gene expression. Proc Natl Acad Sci USA 93:191–195
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. Nat Neurosci 11:923–931
Schmitt EA, Dowling JE (1999) Early retinal development in the zebrafish, Danio rerio: light and electron microscopic analyses. J Comp Neurol 404:515–536
Schmitz F, Drenckhahn D (1997) Localization of dystrophin and beta-dystroglycan in bovine retinal photoreceptor processes extending into the postsynaptic dendritic complex. Histochem Cell Biol 108:249–255
Schmitz F, Konigstorfer A, Sudhof TC (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28:857–872
Schnee ME, Santos-Sacchi J, Castellano-Munoz M, Kong JH, Ricci AJ (2011) Calcium-dependent synaptic vesicle trafficking underlies indefatigable release at the hair cell afferent fiber synapse. Neuron 70:326–338
Snellman J, Mehta B, Babai N, Bartoletti TM, Akmentin W, Francis A, Matthews G, Thoreson W, Zenisek D (2011) Acute destruction of the synaptic ribbon reveals a role for the ribbon in vesicle priming. Nat Neurosci 14:1135–1141
Sohocki MM, Sullivan LS, Mintz-Hittner HA, Birch D, Heckenlively JR, Freund CL, McInnes RR, Daiger SP (1998) A range of clinical phenotypes associated with mutations in CRX, a photoreceptor transcription-factor gene. Am J Hum Genet 63:1307–1315
Specht D, Wu SB, Turner P, Dearden P, Koentgen F, Wolfrum U, Maw M, Brandstatter JH, tom Dieck S (2009) Effects of presynaptic mutations on a postsynaptic Cacna1s calcium channel colocalized with mGluR6 at mouse photoreceptor ribbon synapses. Invest Ophthalmol Vis Sci 50:505–515
Sterling P, Matthews G (2005) Structure and function of ribbon synapses. Trends Neurosci 28:20–29
Strettoi E, Mears AJ, Swaroop A (2004) Recruitment of the rod pathway by cones in the absence of rods. J Neurosci 24:7576–7582
Strom TM, Nyakatura G, Apfelstedt-Sylla E, Hellebrand H, Lorenz B, Weber BH, Wutz K, Gutwillinger N, Ruther 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. Nat Genet 19:260–263
Swain PK, Chen S, Wang QL, Affatigato LM, Coats CL, Brady KD, Fishman GA, Jacobson SG, Swaroop A, Stone E, Sieving PA, Zack DJ (1997) Mutations in the cone-rod homeobox gene are associated with the cone-rod dystrophy photoreceptor degeneration. Neuron 19:1329–1336
Swain PK, Hicks D, Mears AJ, Apel IJ, Smith JE, John SK, Hendrickson A, Milam AH, Swaroop A (2001) Multiple phosphorylated isoforms of NRL are expressed in rod photoreceptors. J Biol Chem 276:36824–36830
Swaroop A, Wang QL, Wu W, Cook J, Coats C, Xu S, Chen S, Zack DJ, Sieving PA (1999) Leber congenital amaurosis caused by a homozygous mutation (R90W) in the homeodomain of the retinal transcription factor CRX: direct evidence for the involvement of CRX in the development of photoreceptor function. Hum Mol Genet 8:299–305
Swaroop A, Xu JZ, Pawar H, Jackson A, Skolnick C, Agarwal N (1992) A conserved retina-specific gene encodes a basic motif/leucine zipper domain. Proc Natl Acad Sci USA 89:266–270
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. J Cell Biol 164:301–311
Tian M, Xu CS, Montpetit R, Kramer RH (2012) Rab3A mediates vesicle delivery at photoreceptor ribbon synapses. J Neurosci 32:6931–6936
tom Dieck S, Brandstatter JH (2006) Ribbon synapses of the retina. Cell Tissue Res 326:339–346
tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstatter JH (2005) Molecular dissection of the photoreceptor ribbon synapse: physical interaction of Bassoon and RIBEYE is essential for the assembly of the ribbon complex. J Cell Biol 168:825–836
tom Dieck S, Sanmarti-Vila L, Langnaese K, Richter K, Kindler S, Soyke A, Wex H, Smalla KH, Kampf U, Franzer JT, Stumm M, Garner CC, Gundelfinger ED (1998) Bassoon, a novel zinc-finger CAG/glutamine-repeat protein selectively localized at the active zone of presynaptic nerve terminals. J Cell Biol 142:499–509
tom Dieck S, Specht D, Strenzke N, Hida Y, Krishnamoorthy V, Schmidt KF, Inoue E, Ishizaki H, Tanaka-Okamoto M, Miyoshi J, Hagiwara A, Brandstatter JH, Lowel S, Gollisch T, Ohtsuka T, Moser T (2012) Deletion of the presynaptic scaffold CAST reduces active zone size in rod photoreceptors and impairs visual processing. J Neurosci 32:12192–12203
Wahl S, Katiyar R, Schmitz F (2013) A local, periactive zone endocytic machinery at photoreceptor synapses in close vicinity to synaptic ribbons. J Neurosci 33:10278–10300
Williamson RA, Henry MD, Daniels KJ, Hrstka RF, Lee JC, Sunada Y, Ibraghimov-Beskrovnaya O, Campbell KP (1997) Dystroglycan is essential for early embryonic development: disruption of Reichert’s membrane in Dag1-null mice. Hum Mol Genet 6:831–841
Yoshida S, Mears AJ, Friedman JS, Carter T, He S, Oh E, Jing Y, Farjo R, Fleury G, Barlow C, Hero AO, Swaroop A (2004) Expression profiling of the developing and mature Nrl−/− mouse retina: identification of retinal disease candidates and transcriptional regulatory targets of Nrl. Hum Mol Genet 13:1487–1503
Zeitz C, Kloeckener-Gruissem B, Forster U, Kohl S, Magyar I, Wissinger B, Matyas G, Borruat FX, Schorderet DF, Zrenner E, Munier FL, Berger W (2006) Mutations in CABP4, the gene encoding the Ca2+-binding protein 4, cause autosomal recessive night blindness. Am J Hum Genet 79:657–667
Zhu X, Brown B, Li A, Mears AJ, Swaroop A, Craft CM (2003) GRK1-dependent phosphorylation of S and M opsins and their binding to cone arrestin during cone phototransduction in the mouse retina. J Neurosci 23:6152–6160
Ziff EB (1997) Enlightening the postsynaptic density. Neuron 19:1163–1174
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Japan
About this chapter
Cite this chapter
Omori, Y., Furukawa, T. (2014). Structure and Development of the Photoreceptor Ribbon Synapse. In: Furukawa, T., Hurley, J., Kawamura, S. (eds) Vertebrate Photoreceptors. Springer, Tokyo. https://doi.org/10.1007/978-4-431-54880-5_8
Download citation
DOI: https://doi.org/10.1007/978-4-431-54880-5_8
Published:
Publisher Name: Springer, Tokyo
Print ISBN: 978-4-431-54879-9
Online ISBN: 978-4-431-54880-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)