How to make a synaptic ribbon: RIBEYE deletion abolishes ribbons in retinal synapses and disrupts neurotransmitter release

EMBO Journal

Volumn 35, Issue 10, 2016, Pages 1098-1114

  Maxeiner, Stephan ^a,b   Luo, Fujun ^a   Tan, Alison ^a   Schmitz, Frank ^b   Südhof, Thomas C ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

CtBP2; GCamP3; photoreceptors; RIBEYE knockout; tonic release

Indexed keywords

CALCIUM ION; CRE RECOMBINASE; RIBBON SPECIFIC PROTEIN; SCAFFOLD PROTEIN; UNCLASSIFIED DRUG; AGENTS INTERACTING WITH TRANSMITTER, HORMONE OR DRUG RECEPTORS; CALCIUM; CALCIUM CHANNEL; CTBP2 PROTEIN, MOUSE; DNA BINDING PROTEIN; PHOSPHOPROTEIN;

ADULT; ANIMAL CELL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CALCIUM TRANSPORT; CELL DENSITY; CELL SPECIFICITY; CONTROLLED STUDY; CYTOSOL; EMBRYO; EMBRYONIC STEM CELL; EXOCYTOSIS; EXON; EXTRACELLULAR SPACE; GENE DELETION; IMMUNOFLUORESCENCE; MOUSE; NERVE DEGENERATION; NERVE ENDING; NEUROFILAMENT; NEUROTRANSMITTER RELEASE; NONHUMAN; PHOTORECEPTOR CELL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RETINA AMACRINE CELL; RETINAL SLICE; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC RIBBON; TRANSMISSION ELECTRON MICROSCOPY; VOLTAGE CLAMP TECHNIQUE; ANIMAL; FEMALE; GENETICS; MALE; PHYSIOLOGY; RETINA; SYNAPTIC TRANSMISSION; TRANSGENIC MOUSE;

ANIMALS; CALCIUM; CALCIUM CHANNELS; DNA-BINDING PROTEINS; FEMALE; MALE; MICE, TRANSGENIC; NEUROTRANSMITTER AGENTS; PHOSPHOPROTEINS; RETINA; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84959266814     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592701     Document Type: Article

References (61)

1. Allwardt BA, Lall AB, Broeckerhoff S, Dowling JE, (2001) Synapse formation is arrested in retinal photoreceptors of the zebrafish nrc mutant. J Neurosci 21: 2330-2342
2. Alpadi K, Magupalli VG, Käppel S, Köblitz L, Schwarz K, Seigel GM, Sung CH, Schmitz F, (2008) RIBEYE recruits Munc119, a mammalian ortholog of the Caenorhabditis elegans protein unc119, to synaptic ribbons of photoreceptor synapses. J Biol Chem 283: 26461-26467
3. Boucard AA, Maxeiner S, Südhof TC, (2014) Latrophilins function as heterophilic cell-adhesion molecules by binding to teneurins: regulation by alternative splicing. J Biol Chem 289: 387-402
4. Buran BN, Strenzke N, Neef A, Gundelfinger ED, Moser T, Liberman MC, (2010) Onset coding is degraded in auditory nerve fibers from mutant mice lacking synaptic ribbons. J Neurosci 30: 7587-7597
5. Dembla M, Wahl S, Katiyar R, Schmitz F, (2014) ArfGAP3 is a component of the photoreceptor synaptic ribbon complex and forms an NAD(H)-regulated, redox-sensitive complex with RIBEYE that is important for endocytosis. J Neurosci 34: 5245-5260
6. 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 ribbon synapse formation in the retina. Neuron 37: 775-786
7. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtova A, Bracko O, Gundelfinger ED, Brandstätter 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
8. 2+-channels and vesicles to add release sites and promote refilling. Neuron 68: 724-738
9. 2+-stimulated release in mouse rod photoreceptors. J Neurosci 38: 13133-13147
10. Heidelberger R, Thoreson WB, Witkovsky P, (2005) Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24: 682-720
11. Hildebrand JD, Soriano P, (2002) Overlapping and unique roles for C-terminal binding protein 1 (CtBP1) and CtBP2 during mouse development. Mol Cell Biol 22: 5296-5307
12. 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. J Neurophysiol 96: 2015-2033
13. Jackman SL, Choi SY, Thoreson WB, Rabl K, Bartoletti TM, Kramer RH, (2009) Role of the synaptic ribbon in transmitting the cone light response. Nature Neurosci 12: 303-310
14. Jarsky T, Tian M, Singer JH, (2010) Nanodomain coupling of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J Neurosci 30: 11885-11895
15. Jing Z, Rutherford MA, Takago H, Frank T, Fejtova A, Khimich D, Moser T, Strenzke N, (2013) Disruption of the presynaptic cytomatrix protein bassoon degrades ribbon anchorage, multiquantal release and sound encoding at the hair cell afferent synapse. J Neurosci 33: 4456-4467
16. 2+-channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 144: 282-295
17. Kaeser PS, Regehr WG, (2014) Molecular mechanisms for synchronous, asynchronous, and spontaneous neurotransmitter release. Annu Rev Physiol 76: 333-363
18. Katiyar R, Weissgerber P, Roth E, Dörr J, Sothilingam V, Garcia Garrido M, Beck SC, Seeliger M, Beck A, Schmitz F, Flockerzi V, (2015) Influence of the β2-subunit of L-type voltage-gated Cav channels on the structural and functional development of photoreceptor ribbon synapses. Invest Ophthalmol Vis Sci 15: 2312-2324
19. Kavalali ET, (2015) The mechanisms and functions of spontaneous neurotransmitter release. Nat Rev Neurosci 16: 5-16
20. Khimich D, Nouvian R, Pujol R, tom Dieck S, Egner A, Gundelfinger ED, Moser T, (2005) Hair cell synaptic ribbons are essential for synchronous auditory signalling. Nature 434: 889-894
21. 2+channels and exocytosis at sensory synapses. J Physiol 591: 3167-3178
22. 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
23. Lee YB, Glover CP, Cosgrave AS, Bienemann A, Uney JB, (2005) Optimizing regulatable gene expression using adenoviral vectors. Exp Physiol 90: 33-37
24. Libby RT, Lavallee CR, Balkema GW, Brunken WJ, Hunter DD, (1999) Disruption of laminin b2-chain production causes alterations in morphology and function of CNS. J Neurosci 19: 9399-9411
25. 2+-dependent vesicle priming in retinal ribbon synapses. J Neurosci 35: 11024-11033
26. Lv C, Gould TJ, Bewersdorf J, Zenisek D, (2012) High-resolution optical imaging of zebrafish larval ribbon synapse protein RIBEYE, RIM2, and CaV 1.4 by stimulation emission depletion microscopy. Microsc Microanal 18: 745-752
27. Magupalli VG, Schwarz K, Alpadi K, Natarajan S, Seigel GM, Schmitz F, (2008) Multiple RIBEYE-RIBEYE interactions create a dynamic scaffold for the formation of synaptic ribbons. J Neurosci 28: 7954-7967
28. Matthews G, Fuchs P, (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11: 812-822
29. Mehta B, Snellman J, Chen S, Li W, Zenisek D, (2013) Synaptic ribbons influence the size and frequency of miniature-like evoked postsynaptic currents. Neuron 77: 516-527
30. Mercer AJ, Thoreson WB, (2011) The dynamic architecture of photoreceptor ribbon synapses: cytoskeletal, extracellular matrix, and intramembrane proteins. Vis Neurosci 28: 453-471
31. Oesch NW, Diamond JS, (2011) Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat Neurosci 14: 1555-1561
32. Protti DA, Llano I, (1998) Calcium currents and calcium signaling in rod bipolar cells of rat retinal slices. J Neurosci 18: 3715-3724
33. 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 complexin3 and complexin4. J Cell Science 122: 1352-1361
34. Rodríguez CI, Buchholz F, Galloway J, Sequerra R, Kasper J, Ayala R, Stewart AF, Dymecki SM, (2000) High-efficiency deleter mice show that FLPe is an alternative to Cre-loxP. Nat Genet 25: 139-140
35. Schmitz F, (2009) The making of synaptic ribbons: how they are built and what they do. Neuroscientist 15: 611-624
36. Schmitz F, Königstorfer A, Südhof TC, (2000) RIBEYE, a component of synaptic ribbons: a protein's journey through evolution provides insight into synaptic ribbon function. Neuron 8: 857-872
37. Schmitz F, Tabares L, Khimich D, Strenzke N, de la Villa-Polo P, Castellano-Muñoz M, Bulankina A, Moser T, Fernández-Chacón R, Südhof TC, (2006) CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proc Natl Acad Sci USA 103: 2926-2931
38. Schwenk F, Baron U, Rajewsky K, (1995) A cre-transgenic mouse strain for the ubiquitous deletion of loxP-flanked gene segments including deletion in germ cells. Nucleic Acids Res 23: 5080-5081
39. Sheets L, Kindt KS, Nicolson T, (2012) CaV1.3 channels regulate synaptic ribbon size and are required for synaptic maintenance in sensory hair cells. J Neurosci 32: 17273-17286
40. Sheets L, Trapani JG, Mo W, Obholzer N, Nicolson T, (2011) Ribeye is required for presynaptic Ca(V)1.3a channel localization and afferent innervation of sensory hair cells. Development 138: 1309-1319
41. 2+ entry elicits transient postsynaptic currents at a retinal ribbon synapse. J Neurosci 23: 10923-10933
42. Singer JH, Lassova L, Vardi N, Diamond JS, (2004) Coordinated multivesicular release at a mammalian ribbon synapse. Nature Neurosci 7: 826-833
43. 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
44. 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
45. Tachibana M, Okada T, Arimura T, Kobayashi K, Piccolino M, (1993) Dihydropyridine-sensitive calcium current mediates neurotransmitter release from bipolar cells of the goldfish retina. J Neurosci 13: 2898-2909
46. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petrean L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL, (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6: 875-881
47. Truckenbrodt S, Rizzoli SO, (2014) Spontaneous vesicle recycling in the synaptic bouton. Front Cell Neurosci 8: 409
48. Van Epps HA, Hayashi M, Lucast L, Stearns GW, Hurley JB, De Camilli P, Brockerhoff SE, (2004) The zebrafish nrc mutant reveals a role for the polyphosphoinositide phosphatase synaptojanin1 in cone photoreceptor ribbon anchoring. J Neurosci 24: 8641-8650
49. 2+ sensor protein GCAP2 to photoreceptor synaptic ribbons. J Neurosci 30: 6559-6576
50. Veruki ML, Mørkve SH, Hartveit E, (2003) Functional properties of spontaneous EPSCs and non-NMDA receptors in rod amacrine (AII) cells in the rat retina. J Physiol 549: 759-774
51. 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
52. Wan L, Almers W, Chen W, (2005) Two ribeye genes in teleosts: the role of RIBEYE in ribbon formation and bipolar cell development. J Neurosci 25: 941-949
53. Wang Y, Okamoto M, Schmitz F, Hofmann K, Südhof TC, (1997) Rim is a putative Rab3 effector in regulating synaptic-vesicle fusion. Nature 388: 593-598
54. West MC, McDermott BM Jr, (2011) RIBEYE a-mCherry fusion protein: a novel tool for labeling synaptic ribbons of the hair cell. J Neurosci Methods 197: 274-278
55. 2+ influx to exocytosis. EMBO J 33: 247-264
56. Xu J, Morris LM, Michalakis S, Biel M, Fliesler SJ, Sherry DM, Ding XQ, (2012) CNGA3 deficiency affects cone synaptic terminal structure and function and leads to secondary rod dysfunction and degeneration. Invest Opthalmol Vis Sci 53: 1117-1129
57. 2+ sensor for spontaneous release. Nat Neurosci 12: 759-766
58. Zabouri N, Haverkamp S, (2013) Calcium channel-dependent molecular maturation of photoreceptor synapses. PLoS ONE 8: e63853
59. Zanazzi G, Matthews G, (2009) The molecular architecture of ribbon presynaptic terminals. Mol Neurobiol 39: 130-148
60. Zenisek D, Davila V, Wan L, Almers W, (2003) Imaging calcium entry sites and ribbon structures in two presynaptic cells. J Neurosci 23: 2538-2548
61. Zenisek D, Horst NK, Merrifield C, Sterling P, Matthews G, (2004) Visualizing synaptic ribbons in the living cell. J Neurosci 24: 9752-9759