Deletion of the presynaptic scaffold cast reduces active zone size in rod photoreceptors and impairs visual processing

Journal of Neuroscience

Volumn 32, Issue 35, 2012, Pages 12192-12203

  Dieck, Susanne Tom ^a   Specht, Dana ^a,b   Strenzke, Nicola ^c   Hida, Yamato ^d   Krishnamoorthy, Vidhyasankar ^c   Schmidt, Karl Friedrich ^e   Inoue, Eiji ^f   Ishizaki, Hiroyoshi ^f   Tanaka Okamoto, Miki ^g   Miyoshi, Jun ^g   Hagiwara, Akari ^d   Brandstatter, Johann H ^b   Löwel, Siegrid ^e   Gollisch, Tim ^c   Ohtsuka, Toshihisa ^d   Moser, Tobias ^c  

^a MAX PLANCK INSTITUTE FOR BRAIN RESEARCH   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

^d UNIVERSITY OF YAMANASHI   (Japan)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

^f Knowledge Action Network Research Institute   (Japan)

^g OSAKA MEDICAL CENTER FOR CANCER AND CARDIOVASCULAR DISEASES   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALBINDIN; CALCIUM CHANNEL; DYSTROGLYCAN; METABOTROPIC RECEPTOR 6; PROTEIN KINASE C ALPHA;

A WAVE; ANIMAL TISSUE; ARTICLE; CAST GENE; CONTRAST SENSITIVITY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; FEMALE; GENE; IMMUNOCYTOCHEMISTRY; IMMUNOFLUORESCENCE TEST; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRESYNAPTIC ACTIVE ZONE; PRESYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETINA BIPOLAR GANGLION CELL; RETINA HORIZONTAL NERVE CELL; RETINA ROD; SOUTHERN BLOTTING; SPATIAL FREQUENCY DISCRIMINATION; SYNAPTIC TRANSMISSION; VISUAL ACUITY; WESTERN BLOTTING;

ACTION POTENTIALS; ANIMALS; CHIMERA; CYTOSKELETAL PROTEINS; FEMALE; GENE DELETION; MALE; MICE; MICE, KNOCKOUT; PHOTIC STIMULATION; PRESYNAPTIC TERMINALS; RETINAL ROD PHOTORECEPTOR CELLS; SYNAPTIC TRANSMISSION; VISUAL PERCEPTION;

EID: 84865521772     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0752-12.2012     Document Type: Article

References (56)

1. Altrock WD, tom Dieck S, Sokolov M, Meyer AC, Sigler A, Brakebusch C, Fassler R, Richter K, Boeckers TM, Potschka H, Brandt C, Loscher W, Grimberg D, Dresbach T, Hempelmann A, Hassan H, Balschun D, Frey JU, Brandstatter JH, Garner CC, et al. (2003) Functional inactivation of a fraction of excitatory synapses in mice deficient for the active zone protein bassoon. Neuron 37:787-800.
2. Astigarraga S, Hofmeyer K, Farajian R, Treisman JE (2010) Three Drosoph-ila liprins interact to control synapse formation. J Neurosci 30:15358-15368.
3. Bolinger D, Gollisch T (2012) Closed-loop measurements of iso-response stimuli reveal dynamic nonlinear stimulus integration in the retina. Neuron 73:333-346.
4. Brandt A, Khimich D, Moser T (2005) Few CaV1. 3 channels regulate the exocytosis of a synaptic vesicle at the hair cell ribbon synapse. J Neurosci 25:11577-11585.
5. 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.
6. Dai Y, Taru H, Deken SL, Grill B, Ackley B, Nonet ML, Jin Y (2006) SYD-2 Liprin-a organizes presynaptic active zone formation through ELKS. Nat Neurosci 9:1479-1487.
7. Deguchi-Tawarada M, Inoue E, Takao-Rikitsu E, Inoue M, Kitajima I, Oht-suka T, Takai Y (2006) Active zone protein CAST is a component of conventional and ribbon synapses in mouse retina. J Comp Neurol 495:480 - 496.
8. Dick O, Hack I, Altrock WD, Garner CC, Gundelfinger ED, Brandstatter JH (2001) Localization of the presynaptic cytomatrix protein Piccolo at ribbon and conventional synapses in the rat retina: comparison with Bassoon. J Comp Neurol 439:224-234.
9. Dick O, tom Dieck S, Altrock WD, Ammermüller 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.
10. Douglas RM, Alam NM, Silver BD, McGill TJ, Tschetter WW, Prusky GT (2005) Independent visual threshold measurements in the two eyes of freely moving rats and mice using a virtual-reality optokinetic system. Vis Neurosci 22:677-684.
11. Fejtova A, Gundelfinger ED (2006) Molecular organization and assembly of the presynaptic active zone of neurotransmitter release. Results Probl Cell Differ 43:49-68.
12. + channels and vesicles to add release sites and promote refilling. Neuron 68:724-738.
13. Goetze B, Schmidt KF, Lehmann K, Altrock WD, Gundelfinger ED, Lowel S (2010) Vision and visual cortical maps in mice with a photoreceptor synaptopathy: reduced but robust visual capabilities in the absence of synaptic ribbons. Neuroimage 49:1622-1631.
14. Gundelfinger ED, Fejtova A (2012) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol 22:423-430.
15. +-binding protein 4, aCav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7:1079-1087.
16. Hallermann S, Fejtova A, Schmidt H, Weyhersmüller A, Silver RA, Gundelfinger ED, Eilers J (2010) Bassoon speeds vesicle reloading at a central excitatory synapse. Neuron 68:710-723.
17. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 69:304-316.
18. Harlow ML, Ress D, Stoschek A, Marshall RM, McMahan UJ (2001) The architecture of active zone material at the frog's neuromuscular junction. Nature 409:479-484.
19. Hida Y, Ohtsuka T (2010) CAST and ELKS proteins: structural and functional determinants of the presynaptic active zone. J Biochem 148:131-137.
20. 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 96:2025-2033.
21. 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.
22. Jarsky T, Tian M, Singer JH (2010) Nanodomain control of exocytosis is responsible for the signaling capability of a retinal ribbon synapse. J Neurosci 30:11885-11895.
23. Jarsky T, Cembrowski M, Logan SM, Kath WL, Riecke H, Demb JB, Singer JH (2011) A synaptic mechanism for retinal adaptation to luminance and contrast. J Neurosci 31:11003-11015.
24. Kaeser PS, Deng L, Chavez AE, Liu X, Castillo PE, Südhof TC (2009) ELKS2alpha/CAST deletion selectively increases neurotransmitter release at inhibitory synapses. Neuron 64:227-239.
25. Kaufmann N, DeProto J, Ranjan R, Wan H, Van Vactor D (2002) Drosoph-ila liprin-alpha and the receptor phosphatase Dlar control synapse morphogenesis. Neuron 34:27-38.
26. 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.
27. + channel clustering, and vesicle release. Science 312:1051-1054.
28. Lazarevic V, Schone C, Heine M, Gundelfinger ED, Fejtova A (2011) Extensive remodeling of the presynaptic cytomatrix upon homeostatic adaptation to network activity silencing. J Neurosci 31:10189-10200.
29. 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.
30. Matthews G, Fuchs P (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11:812-822.
31. Matz J, Gilyan A, Kolar A, McCarvill T, Krueger SR (2010) Rapid structural alterations of the active zone lead to sustained changes in neurotransmit-ter release. Proc Natl Acad Sci U S A 107:8836-8841.
32. Moser T, Neef A, Khimich D (2006) Mechanisms underlying the temporal precision of sound coding at the inner hair cell ribbon synapse. J Physiol 576:55-62.
33. Mukherjee K, Yang X, Gerber SH, Kwon HB, Ho A, Castillo PE, Liu X, Südhof TC (2010) Piccolo and bassoon maintain synaptic vesicle clustering without directly participating in vesicle exocytosis. Proc Natl Acad Sci U S A 107:6504-6509.
34. Oesch NW, Diamond JS (2011) Ribbon synapses compute temporal contrast and encode luminance in retinal rod bipolar cells. Nat Neurosci 14:1555-1561.
35. 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.
36. Olsen O, Moore KA, Fukata M, Kazuta T, Trinidad JC, Kauer FW, Streuli M, Misawa H, Burlingame AL, Nicoll RA, Bredt DS (2005) Neurotransmit-ter release regulated by a MALS-liprin-alpha presynaptic complex. J Cell Biol 170:1127-1134.
37. Pangrsic T, Lasarow L, Reuter K, Takago H, Schwander M, Riedel D, Frank T, Tarantino LM, Bailey JS, Strenzke N, Brose N, Müller U, Reisinger E, Moser T (2010) Hearing requires otoferlin-dependent efficient replenishment of synaptic vesicles in hair cells. Nat Neurosci 13:869-876.
38. Peichl L (2005) Diversity of mammalian photoreceptor properties: adaptations to habitat and lifestyle? Anat Rec A Discov Mol Cell Evol Biol 287:1001-1012.
39. Pouzat C, Mazor O, Laurent G (2002) Using noise signature to optimize spike-sorting and to assess neuronal classification quality. J Neurosci Methods 122:43-57.
40. Prusky GT, Alam NM, Beekman S, Douglas RM (2004) Rapid quantification of adult and developing mouse spatial vision using a virtual optomotor system. Invest Ophthalmol Vis Sci 45:4611-4616.
41. Rabl K, Cadetti L, Thoreson WB (2005) Kinetics of exocytosis is faster in cones than in rods. J Neurosci 25:4633-4640.
42. 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.
43. 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.
44. Sheets L, Trapani JG, Mo W, Obholzer N, Nicolson T (2011) Ribeye is required for presynaptic CaV1.3a channel localization and afferent inner-vation of sensory hair cells. Development 138:1309-1319.
45. Specht D, Tom Dieck S, Ammermüller J, Regus-Leidig H, Gundelfinger ED, Brandstätter JH (2007) Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur J Neurosci 26:2506-2515.
46. Specht D, Wu SB, Turner P, Dearden P, Koentgen F, Wolfrum U, Maw M, Brandstätter 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.
47. Spiwoks-Becker I, Glas M, Lasarzik I, Vollrath L (2004) Mouse photoreceptor synaptic ribbons lose and regain material in response to illumination changes. Eur J Neurosci 19:1559-1571.
48. Stigloher C, Zhan H, Zhen M, Richmond J, Bessereau JL (2011) The presynaptic dense projection of the Caenorhabditis elegans cholinergic neuro-muscular junction localizes synaptic vesicles at the active zone through SYD-2/liprin and UNC-10/RIM-dependent interactions. J Neurosci 31:4388-4396.
49. 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.
50. tom Dieck S, Altrock WD, Kessels MM, Qualmann B, Regus H, Brauner D, Fejtová 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.
51. Wachman ES, Poage RE, Stiles JR, Farkas DL, Meriney SD (2004) Spatial distribution of calcium entry evoked bysingle action potentials within the presynaptic active zone. J Neurosci 24:2877-2885.
52. Zhai RG, Bellen HJ (2004) The architecture of the active zone in the presynaptic nerve terminal. Physiology 19:262-270.
53. Zhai RG, Vardinon-Friedman H, Cases-Langhoff C, Becker B, Gundelf-inger ED, Ziv NE, Garner CC (2001) Assembling the presynaptic active zone: a characterization of an active zone precursor vesicle. Neuron 29:131-143.
54. Zhai R, Olias G, Chung WJ, Lester RA, tom Dieck S, Langnaese K, Kreutz MR, Kindler S, Gundelfinger ED, Garner CC (2000) Temporal appearance of the presynaptic cytomatrix protein Bassoon during synaptogenesis. Mol Cell Neurosci 15:417-428.
55. Zhen M, Jin Y (1999) The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans. Nature 401:371-375.
56. Zürner M, Mittelstaedt T, tom Dieck S, Becker A, Schoch S (2011) Analyses of the spatiotemporal expression and subcellular localization of liprin-a proteins. J Comp Neurol 519:3019-3039.