Structural organization and function of mouse photoreceptor ribbon synapses involve the immunoglobulin protein synaptic cell adhesion molecule 1

Journal of Comparative Neurology

Volumn 522, Issue 4, 2014, Pages 900-920

  Ribic, Adema ^a   Liu, Xinran ^b   Crair, Michael C ^b   Biederer, Thomas ^a  

^a YALE UNIVERSITY   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

CADM; Electroretinography; Nectin like protein; Retina; Ribbon synapse; Rod; SynCAM

Indexed keywords

CELL ADHESION MOLECULE; SYNAPTIC CELL ADHESION MOLECULE 1; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ELECTRORETINOGRAM; FEMALE; IMMUNOBLOTTING; IMMUNOELECTRON MICROSCOPY; IMMUNOHISTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PERINATAL PERIOD; PHOTORECEPTOR; PHOTORECEPTOR RIBBON SYNAPSE; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA; RETINA INNER PLEXIFORM LAYER; RETINA ROD; SYNAPSE;

CADM; ELECTRORETINOGRAPHY; NECTIN-LIKE PROTEIN; RETINA; RIBBON SYNAPSE; ROD; SYNCAM;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CELL ADHESION MOLECULES; DNA-BINDING PROTEINS; ELECTRORETINOGRAPHY; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMUNOGLOBULINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROSCOPY, IMMUNOELECTRON; NERVE TISSUE PROTEINS; PHOSPHOPROTEINS; RECEPTORS, METABOTROPIC GLUTAMATE; RETINA; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPSES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 84892446898     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23452     Document Type: Article

References (99)

1. Abd-El-Barr MM, Pennesi ME, Saszik SM, Barrow AJ, Lem J, Bramblett DE, Paul DL, Frishman LJ, Wu SM. 2009. Genetic dissection of rod and cone pathways in the dark-adapted mouse retina. J Neurophysiol 102:1945-1955.
2. Balkema GW, Drager UC. 1985. Light-dependent antibody labelling of photoreceptors. Nature 316:630-633.
3. Bayley PR, Morgans CW. 2007. Rod bipolar cells and horizontal cells form displaced synaptic contacts with rods in the outer nuclear layer of the nob2 retina. J Comp Neurol 500:286-298.
4. Biederer T, Sara Y, Mozhayeva M, Atasoy D, Liu X, Kavalali ET, Südhof TC. 2002. SynCAM, a synaptic adhesion molecule that drives synapse assembly. Science 297:1525-1531.
5. Blanks JC, Adinolfi AM, Lolley RN. 1974a. Photoreceptor degeneration and synaptogenesis in retinal-degenerative (rd) mice. J Comp Neurol 156:95-106.
6. Blanks JC, Adinolfi AM, Lolley RN. 1974b. Synaptogenesis in the photoreceptor terminal of the mouse retina. J Comp Neurol 156:81-93.
7. Bloomfield SA, Volgyi B. 2009. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat Rev Neurosci 10:495-506.
8. Bramblett DE, Pennesi ME, Wu SM, Tsai MJ. 2004. The transcription factor Bhlhb4 is required for rod bipolar cell maturation. Neuron 43:779-793.
9. Brockerhoff SE, Hurley JB, Niemi GA, Dowling JE. 1997. A new form of inherited red-blindness identified in zebrafish. J Neurosci 17:4236-4242.
10. Brown KT, Watanabe K. 1962a. Isolation and identification of a receptor potential from the pure cone fovea of the monkey retina. Nature 193:958-960.
11. Brown KT, Watanabe K. 1962b. Rod receptor potential from the retina of the night monkey. Nature 196:547-550.
12. Brown KT, Watanabe K, Murakami M. 1965. The early and late receptor potentials of monkey cones and rods. Cold Spring Harbor Symp Quant Biol 30:457-482.
13. Carter-Dawson LD, LaVail MM. 1979. Rods and cones in the mouse retina. I. Structural analysis using light and electron microscopy. J Comp Neurol 188:245-262.
14. Chang B, Heckenlively JR, Bayley PR, Brecha NC, Davisson MT, Hawes NL, Hirano AA, Hurd RE, Ikeda A, Johnson BA, McCall MA, Morgans CW, Nusinowitz S, Peachey NS, Rice DS, Vessey KA, Gregg RG. 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. Vis Neurosci 23:11-24.
15. Cheadle L, Biederer T. 2012. The novel synaptogenic protein Farp1 links postsynaptic cytoskeletal dynamics and transsynaptic organization. J Cell Biol 199:985-1001.
16. Cooper B, Hemmerlein M, Ammermüller J, Imig C, Reim K, Lipstein N, Kalla S, Kawabe H, Brose N, Brandstätter JH, Varoqueaux F. 2012. Munc13-independent vesicle priming at mouse photoreceptor ribbon synapses. J Neurosci 32:8040-8052.
17. Dang TM, Tsai TI, Vingrys AJ, Bui BV. 2011. Post-receptoral contributions to the rat scotopic electroretinogram a-wave. Doc Ophthalmol Adv Ophthalmol 122:149-156.
18. Dick O, tom Dieck S, Altrock WD, Ammermüller J, Weiler R, Garner CC, Gundelfinger ED, Brandstätter JH. 2003. The presynaptic active zone protein bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37:775-786.
19. Duncan JL, Yang H, Doan T, Silverstein RS, Murphy GJ, Nune G, Liu X, Copenhagen D, Tempel BL, Rieke F, Krizaj D. 2006. Scotopic visual signaling in the mouse retina is modulated by high-affinity plasma membrane calcium extrusion. J Neurosci 26:7201-7211.
20. Ekesten B, Gouras P, Moschos M. 1998. Cone properties of the light-adapted murine ERG. Doc Ophthalmol Adv Ophthalmol 97:23-31.
21. Eroglu C, Barres BA. 2010. Regulation of synaptic connectivity by glia. Nature 468:223-231.
22. Fisher LJ. 1979. Development of synaptic arrays in the inner plexiform layer of neonatal mouse retina. J Comp Neurol 187:359-372.
23. Fogel AI, Akins MR, Krupp AJ, Stagi M, Stein V, Biederer T. 2007. SynCAMs organize synapses through heterophilic adhesion. J Neurosci 27:12516-12530.
24. Fogel AI, Stagi M, Perez de Arce K, Biederer T. 2011. Lateral assembly of the immunoglobulin protein SynCAM 1 controls its adhesive function and instructs synapse formation. EMBO J 30:4728-4738.
25. Fuerst PG, Burgess RW. 2009. Adhesion molecules in establishing retinal circuitry. Curr Opin Neurobiol 19:389-394.
26. Fuerst PG, Bruce F, Tian M, Wei W, Elstrott J, Feller MB, Erskine L, Singer JH, Burgess RW. 2009. DSCAM and DSCAML1 function in self-avoidance in multiple cell types in the developing mouse retina. Neuron 64:484-497.
27. Fujita E, Urase K, Soyama A, Kouroku Y, Momoi T. 2005. Distribution of RA175/TSLC1/SynCAM, a member of the immunoglobulin superfamily, in the developing nervous system. Brain Res Dev Brain Res 154:199-209.
28. Fujita E, Kouroku Y, Ozeki S, Tanabe Y, Toyama Y, Maekawa M, Kojima N, Senoo H, Toshimori K, Momoi T. 2006. Oligo-astheno-teratozoospermia in mice lacking RA175/TSLC1/SynCAM/IGSF4A, a cell adhesion molecule in the immunoglobulin superfamily. Mol Cell Biol 26:718-726.
29. Fujita E, Tanabe Y, Hirose T, Aurrand-Lions M, Kasahara T, Imhof BA, Ohno S, Momoi T. 2007. Loss of partitioning-defective-3/isotype-specific interacting protein (par-3/ASIP) in the elongating spermatid of RA175 (IGSF4A/SynCAM)-deficient mice. Am J Pathol 171:1800-1810.
30. Gu C, Gu Y. 2011. Clustering and activity tuning of Kv1 channels in myelinated hippocampal axons. J Biol Chem 286:25835-25847.
31. 2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7:1079-1087.
32. Haverkamp S, Wässle H. 2000. Immunocytochemical analysis of the mouse retina. J Comp Neurol 424:1-23.
33. Heidelberger R, Thoreson WB, Witkovsky P. 2005. Synaptic transmission at retinal ribbon synapses. Prog Ret Eye Res 24:682-720.
34. Hirano AA, Brandstätter JH, Morgans CW, Brecha NC. 2011. SNAP25 expression in mammalian retinal horizontal cells. J Comp Neurol 519:972-988.
35. Hoon M, Bauer G, Fritschy JM, Moser T, Falkenburger BH, Varoqueaux F. 2009. Neuroligin 2 controls the maturation of GABAergic synapses and information processing in the retina. J Neurosci 29:8039-8050.
36. Hoon M, Soykan T, Falkenburger B, Hammer M, Patrizi A, Schmidt KF, Sassoe-Pognetto M, Lowel S, Moser T, Taschenberger H, Brose N, Varoqueaux F. 2011. Neuroligin-4 is localized to glycinergic postsynapses and regulates inhibition in the retina. Proc Natl Acad Sci U S A 108:3053-3058.
37. Howes KA, Pennesi ME, Sokal I, Church-Kopish J, Schmidt B, Margolis D, Frederick JM, Rieke F, Palczewski K, Wu SM, Detwiler PB, Baehr W. 2002. GCAP1 rescues rod photoreceptor response in GCAP1/GCAP2 knockout mice. EMBO J 21:1545-1554.
38. Jinno S, Aika Y, Fukuda T, Kosaka T. 1998. Quantitative analysis of GABAergic neurons in the mouse hippocampus, with optical disector using confocal laser scanning microscope. Brain Res 814:55-70.
39. Johnson J, Tian N, Caywood MS, Reimer RJ, Edwards RH, Copenhagen DR. 2003. Vesicular neurotransmitter transporter expression in developing postnatal rodent retina: GABA and glycine precede glutamate. J Neurosci 23:518-529.
40. Kamermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R. 2001. Hemichannel-mediated inhibition in the outer retina. Science 292:1178-1180.
41. 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.
42. Kim TS, Maeda A, Maeda T, Heinlein C, Kedishvili N, Palczewski K, Nelson PS. 2005. Delayed dark adaptation in 11-cis-retinol dehydrogenase-deficient mice: a role of RDH11 in visual processes in vivo. J Biol Chem 280:8694-8704.
43. Knop GC, Seeliger MW, Thiel F, Mataruga A, Kaupp UB, Friedburg C, Tanimoto N, Muller F. 2008. Light responses in the mouse retina are prolonged upon targeted deletion of the HCN1 channel gene. Eur J Neurosci 28:2221-2230.
44. Koulen P, Fletcher EL, Craven SE, Bredt DS, Wässle H. 1998. Immunocytochemical localization of the postsynaptic density protein PSD-95 in the mammalian retina. J Neurosci 18:10136-10149.
45. Kranz K, Dorgau B, Pottek M, Herrling R, Schultz K, Bolte P, Monyer H, Penuela S, Laird DW, Dedek K, Weiler R, Janssen-Bienhold U. 2012. Expression of Pannexin1 in the outer plexiform layer of the mouse retina and physiological impact of its knock-out. J Comp Neurol (in press).
46. Kueng-Hitz N, Rol P, Niemeyer G. 1999. The electroretinogram (ERG) of the mouse: normal values, optimal stimulation and recording. Klin Monatsblatter Augenheilkunde 214:288-290.
47. Lefebvre JL, Zhang Y, Meister M, Wang X, Sanes JR. 2008. Gamma-protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development 135:4141-4151.
48. Leterrier C, Brachet A, Dargent B, Vacher H. 2011. Determinants of voltage-gated sodium channel clustering in neurons. Semin Cell Dev Biol 22:171-177.
49. Li J, Cline HT. 2010. Visual deprivation increases accumulation of dense core vesicles in developing optic tectal synapses in Xenopus laevis. J Comp Neurol 518:2365-2381.
50. Liu J, Timmers AM, Lewin AS, Hauswirth WW. 2005. Ribozyme knockdown of the gamma-subunit of rod cGMP phosphodiesterase alters the ERG and retinal morphology in wild-type mice. Invest Ophthalmol Vis Sci 46:3836-3844.
51. Liu X, Hirano AA, Sun X, Brecha NC, Barnes S. 2013. Calcium channels in rat horizontal cells regulate feedback inhibition of photoreceptors through an unconventional GABA- and pH-sensitive mechanism. J Physiol (in press).
52. Lyubarsky AL, Pugh EN Jr. 1996. Recovery phase of the murine rod photoresponse reconstructed from electroretinographic recordings. J Neurosci 16:563-571.
53. 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.
54. Matsuoka RL, Jiang Z, Samuels IS, Nguyen-Ba-Charvet KT, Sun LO, Peachey NS, Chedotal A, Yau KW, Kolodkin AL. 2012. Guidance-cue control of horizontal cell morphology, lamination, and synapse formation in the mammalian outer retina. J Neurosci 32:6859-6868.
55. 2+ channels to synaptic vesicle exocytosis. Nature 423:939-948.
56. Missler M, Südhof TC, Biederer T. 2012. Synaptic cell adhesion. Cold Spring Harbor Perspect Biol (in press).
57. Peachey NS, Ball SL. 2003. Electrophysiological analysis of visual function in mutant mice. Doc Ophthalmol Adv Ophthalmol 107:13-36.
58. Pietri T, Easley-Neal C, Wilson C, Washbourne P. 2008. Six cadm/SynCAM genes are expressed in the nervous system of developing zebrafish. Dev Dyn 237:233-246.
59. Pinto LH, Invergo B, Shimomura K, Takahashi JS, Troy JB. 2007. Interpretation of the mouse electroretinogram. Doc Ophthalmol Adv Ophthalmol 115:127-136.
60. Regus-Leidig H, Tom Dieck S, Specht D, Meyer L, Brandstätter JH. 2009. Early steps in the assembly of photoreceptor ribbon synapses in the mouse retina: the involvement of precursor spheres. J Comp Neurol 512:814-824.
61. Regus-Leidig H, tom Dieck S, Brandstätter JH. 2010. Absence of functional active zone protein Bassoon affects assembly and transport of ribbon precursors during early steps of photoreceptor synaptogenesis. Eur J Cell Biol 89:468-475.
62. Reim K, Regus-Leidig H, Ammermüller J, El-Kordi A, Radyushkin K, Ehrenreich H, Brandstätter JH, Brose N. 2009. Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4. J Cell Sci 122:1352-1361.
63. Robbins EM, Krupp AJ, Perez de Arce K, Ghosh AK, Fogel AI, Boucard A, Südhof TC, Stein V, Biederer T. 2010. SynCAM 1 adhesion dynamically regulates synapse number and impacts plasticity and learning. Neuron 68:894-906.
64. Robson JG, Frishman LJ. 1998. Dissecting the dark-adapted electroretinogram. Doc Ophthalmol Adv Ophthalmol 95:187-215.
65. Ruether K, Feigenspan A, Pirngruber J, Leitges M, Baehr W, Strauss O. 2010. PKCα is essential for the proper activation and termination of rod bipolar cell response. Invest Ophthalmol Vis Sci 51:6051-6058.
66. Samuel MA, Zhang Y, Meister M, Sanes JR. 2011. Age-related alterations in neurons of the mouse retina. J Neurosci 31:16033-16044.
67. 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.
68. Schmitz F. 2009. The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15:611-624.
69. Schmitz F, Konigstorfer A, Südhof TC. 2000. RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 28:857-872.
70. Seeliger MW, Brombas A, Weiler R, Humphries P, Knop G, Tanimoto N, Muller F. 2011. Modulation of rod photoreceptor output by HCN1 channels is essential for regular mesopic cone vision. Nat Commun 2:532.
71. Shapiro L, Love J, Colman DR. 2007. Adhesion molecules in the nervous system: structural insights into function and diversity. Annu Rev Neurosci 30:451-474.
72. Sharma RK, O'Leary TE, Fields CM, Johnson DA. 2003. Development of the outer retina in the mouse. Brain Res Dev Brain Res 145:93-105.
73. Sherry DM, Wang MM, Bates J, Frishman LJ. 2003. Expression of vesicular glutamate transporter 1 in the mouse retina reveals temporal ordering in development of rod vs. cone and ON vs. OFF circuits. J Comp Neurol 465:480-498.
74. Shu X, Lev-Ram V, Deerinck TJ, Qi Y, Ramko EB, Davidson MW, Jin Y, Ellisman MH, Tsien RY. 2011. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol 9:e1001041.
75. 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.
76. Song X, Vishnivetskiy SA, Seo J, Chen J, Gurevich EV, Gurevich VV. 2011. Arrestin-1 expression level in rods: balancing functional performance and photoreceptor health. Neuroscience 174:37-49.
77. Soto F, Watkins KL, Johnson RE, Schottler F, Kerschensteiner D. 2013. NGL-2 regulates pathway-specific neurite growth and lamination, synapse formation, and signal transmission in the retina. J Neurosci 33:11949-11959.
78. Stagi M, Fogel AI, Biederer T. 2010. SynCAM 1 participates in axo-dendritic contact assembly and shapes neuronal growth cones. Proc Natl Acad Sci U S A 107:7568-7573.
79. Sterio DC. 1984. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 134:127-136.
80. Sterling P, Matthews G. 2005. Structure and function of ribbon synapses. Trends Neurosci 28:20-29.
81. Strettoi E, Porciatti V, Falsini B, Pignatelli V, Rossi C. 2002. Morphological and functional abnormalities in the inner retina of the rd/rd mouse. J Neurosci 22:5492-5504.
82. Thomas LA, Akins MR, Biederer T. 2008. Expression and adhesion profiles of SynCAM molecules indicate distinct neuronal functions. J Comp Neurol 510:47-67.
83. Tokuyasu KT. 1973. A technique for ultracryotomy of cell suspensions and tissues. J Cell Biol 57:551-565.
84. tom Dieck S, Brandstätter JH. 2006. Ribbon synapses of the retina. Cell Tissue Res 326:339-346.
85. tom Dieck S, Specht D, Strenzke N, Hida Y, Krishnamoorthy V, Schmidt KF, Inoue E, Ishizaki H, Tanaka-Okamoto M, Miyoshi J, Hagiwara A, Brandstätter 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.
86. Vessey KA, Greferath U, Jobling AI, Phipps JA, Ho T, Waugh M, Fletcher EL. 2012. Ccl2/Cx3cr1 knockout mice have inner retinal dysfunction but are not an accelerated model of AMD. Invest Ophthalmol Vis Sci 53:7833-7846.
87. Vistamehr S, Tian N. 2004. Light deprivation suppresses the light response of inner retina in both young and adult mouse. Vis Neurosci 21:23-37.
88. Wahlin KJ, Moreira EF, Huang H, Yu N, Adler R. 2008. Molecular dynamics of photoreceptor synapse formation in the developing chick retina. J Comp Neurol 506:822-837.
89. Wahlin KJ, Hackler L Jr, Adler R, Zack DJ. 2010. Alternative splicing of neuroligin and its protein distribution in the outer plexiform layer of the chicken retina. J Comp Neurol 518:4938-4962.
90. Watabe K, Ito A, Koma YI, Kitamura Y. 2003. IGSF4: a new intercellular adhesion molecule that is called by three names, TSLC1, SgIGSF and SynCAM, by virtue of its diverse function. Histol Histopathol 18:1321-1329.
91. West MJ, Slomianka L, Gundersen HJ. 1991. Unbiased stereological estimation of the total number of neurons in thesubdivisions of the rat hippocampus using the optical fractionator. Anat Rec 231:482-497.
92. Weymouth AE, Vingrys AJ. 2008. Rodent electroretinography: methods for extraction and interpretation of rod and cone responses. Progr Ret Eye Res 27:1-44.
93. Witkovsky P, Dudek FE, Ripps H. 1975. Slow PIII component of the carp electroretinogram. J Gen Physiol 65:119-134.
94. Yamagata M, Sanes JR. 2008. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451:465-469.
95. Yamagata M, Sanes JR. 2012. Expanding the Ig superfamily code for laminar specificity in retina: expression and role of contactins. J Neurosci 32:14402-14414.
96. Yang J, Pawlyk B, Wen XH, Adamian M, Soloviev M, Michaud N, Zhao Y, Sandberg MA, Makino CL, 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. Hum Mol Genet 16:1017-1029.
97. Yen LH, Sibley JT, Constantine-Paton M. 1993. Fine-structural alterations and clustering of developing synapses after chronic treatments with low levels of NMDA. J Neurosci 13:4949-4960.
98. Zenisek D, Horst NK, Merrifield C, Sterling P, Matthews G. 2004. Visualizing synaptic ribbons in the living cell. J Neurosci 24:9752-9759.
99. Zhang H, Li S, Doan T, Rieke F, Detwiler PB, Frederick JM, Baehr W. 2007. Deletion of PrBP/delta impedes transport of GRK1 and PDE6 catalytic subunits to photoreceptor outer segments. Proc Natl Acad Sci U S A 104:8857-8862.