Munc13-independent vesicle priming at mouse photoreceptor ribbon synapses

Journal of Neuroscience

Volumn 32, Issue 23, 2012, Pages 8040-8052

  Cooper, Benjamin ^a   Hemmerlein, Maike ^b   Ammermüller, Josef ^c   Imig, Cordelia ^a   Reim, Kerstin ^a   Lipstein, Noa ^a   Kalla, Stefan ^a,e   Kawabe, Hiroshi ^a   Brose, Nils ^a,d   Brandstätter, Johann Helmut ^b   Varoqueaux, Frédérique ^a,d  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF OLDENBURG   (Germany)

^d Deutsche Forschungsgemeinschaft   (Germany)

^e QIAGEN GMBH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; MEMBRANE PROTEIN; MUNC13 PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRORETINOGRAPHY; EXOCYTOSIS; GENE DELETION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; KNOCKOUT MOUSE; MALE; MICROSCOPY; MOLECULAR CLONING; MOUSE; NONHUMAN; PHOTORECEPTOR RIBBON SYNAPSE; PHOTOSTIMULATION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN LOCALIZATION; RETINA; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; WESTERN BLOTTING;

AMACRINE CELLS; ANIMALS; CLONING, MOLECULAR; DNA, COMPLEMENTARY; ELECTRORETINOGRAPHY; EXOCYTOSIS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; ISOMERISM; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; NERVE TISSUE PROTEINS; RETINA; RNA; SYNAPSES; SYNAPTIC VESICLES; TRANSCRIPTION, GENETIC;

EID: 84861862931     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4240-11.2012     Document Type: Article

References (61)

1. Andrews-Zwilling YS, Kawabe H, Reim K, Varoqueaux F, Brose N (2006) Binding to Rab3A-interacting molecule RIM regulates the presynaptic recruitment of Munc13-1 and ubMunc13-2. J Biol Chem 281:19720-19731.
2. Augustin I, Betz A, Herrmann C, Jo T, Brose N (1999a) Differential expression of two novel Munc13 proteins in rat brain. Biochem J 337:363-371.
3. Augustin I, Rosenmund C, Südhof TC, BroseN (1999b) Munc13-1 is essential for fusion competence of glutamatergic synaptic vesicles. Nature 400:457-461.
4. Augustin I, Korte S, Rickmann M, Kretzschmar HA, Südhof TC, Herms JW, Brose N (2001) The cerebellum-specific Munc13 isoform Munc13-3 regulates cerebellar synaptic transmission and motor learning in mice. J Neurosci 21:10-17.
5. Basu J, Shen N, Dulubova I, Lu J, Guan R, Guryev O, Grishin NV, Rosenmund C, Rizo J (2005) A minimal domain responsible for Munc13 activity. Nat Struct Mol Biol 12:1017-1018.
6. Betz A, Ashery U, Rickmann M, Augustin I, Neher E, Südhof TC, Rettig J, Brose N (1998) Munc13-1 is a presynaptic phorbol ester receptor that enhances neurotransmitter release. Neuron 21:123-136.
7. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J, Brose N (2001) Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30:183-196.
8. Breustedt J, Gundlfinger A, Varoqueaux F, Reim K, Brose N, Schmitz D (2010) Munc13-2 differentially affects hippocampal synaptic transmission and plasticity. Cereb Cortex 20:1109-1120.
9. Brose N, Hofmann K, Hata Y, Südhof TC (1995) Mammalian homologues of Caenorhabditis elegans unc-13 gene define novel family of C2-domain proteins. J Biol Chem 270:25273-25280.
10. Curtis LB, Doneske B, Liu X, Thaller C, McNew JA, Janz R (2008) Syntaxin 3b is a t-SNARE specific for ribbon synapses of the retina. J Comp Neurol 510:550-559.
11. 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.
12. Dimova K, Kawabe H, Betz A, Brose N, Jahn O (2006) Characterization of the Munc13-calmodulin interaction by photoaffinity labeling. Biochim Biophys Acta 1763:1256-1265.
13. Feldmann J, Callebaut I, Raposo G, Certain S, Bacq D, Dumont C, Lambert N, Ouachée-Chardin M, Chedeville G, Tamary H, Minard-Colin V, Vilmer E, Blanche S, Le Deist F, Fischer A, de Saint Basile G (2003) Munc13-4 is essential for cytolytic granules fusion and is mutated in a form of familial hemophagocytic lymphohistiocytosis (FHL3). Cell 115:461-473.
14. Gracheva EO, Burdina AO, Holgado AM, Berthelot-Grosjean M, Ackley BD, Hadwiger G, Nonet ML, Weimer RM, Richmond JE (2006) Tomosyn inhibits synaptic vesicle priming in Caenorhabditis elegans. PLoS Biol 4:e261.
15. Greferath U, Grünert U, Wässle H (1990) Rod bipolar cells in the mammalian retina show protein kinase C-like immunoreactivity. J Comp Neurol 301:433-442.
16. Gundelfinger ED, Fejtova A (2011) Molecular organization and plasticity of the cytomatrix at the active zone. Curr Opin Neurobiol. Advance online publication. Retrieved April 24, 2012. doi:10.1016/j.conb. 2011.10.005.
17. Hammarlund M, Palfreyman MT, Watanabe S, Olsen S, Jorgensen EM (2007) Open syntaxin docks synaptic vesicles. PLoS Biol 5:e198.
18. Heidelberger R, Sterling P, Matthews G (2002) Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J Neurophysiol 88:98-106.
19. 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.
20. 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.
21. Kalla S, Stern M, Basu J, Varoqueaux F, Reim K, Rosenmund C, Ziv NE, Brose N (2006) Molecular dynamics of a presynaptic active zone protein studied in Munc13-1-enhanced yellow fluorescent protein knock-in mutant mice. J Neurosci 26:13054-13066.
22. Koch H, Hofmann K, Brose N (2000) Definition of Munc13-homologydomains and characterization of a novel ubiquitously expressed Munc13 isoform. Biochem J 349:247-253.
23. Koyasu T, Kondo M, Miyata K, Ueno S, Miyata T, Nishizawa Y, Terasaki H (2008) Photopic electroretinograms of mGluR6-deficient mice. Curr Eye Res 33:91-99.
24. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71-76.
25. Lakso M, Pichel JG, Gorman JR, Sauer B, Okamoto Y, Lee E, Alt FW, Westphal H (1996) Efficient in vivo manipulation of mouse genomic sequences at the zygote stage. Proc Natl Acad Sci U S A 93:5860-5865.
26. Li W, Ma C, Guan R, Xu Y, Tomchick DR, Rizo J (2011) The crystal structure of a Munc13 C-terminal module exhibits a remarkable similarity to vesicle tethering factors. Structure 19:1443-1455.
27. Limbach C, Laue MM, Wang X, Hu B, Thiede N, Hultqvist G, KilimannMW (2011) Molecular in situ topology of Aczonin/Piccolo and associated proteins at the mammalian neurotransmitter release site. Proc Natl Acad Sci U S A 108:E392-E401.
28. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343-352.
29. Matsubara A, Laake JH, Davanger S, Usami S, Ottersen OP (1996) Organization of AMPA receptor subunits at a glutamate synapse: a quantitative immunogold analysis of hair cell synapses in the rat organ of Corti. J Neurosci 16:4457-4467.
30. Matthews G, Fuchs P (2010) The diverse roles of ribbon synapses in sensory neurotransmission. Nat Rev Neurosci 11:812-822.
31. Midorikawa M, Tsukamoto Y, Berglund K, Ishii M, Tachibana M (2007) Different roles of ribbon-associated and ribbon-free active zones in retinal bipolar cells. Nat Neurosci 10:1268-1276.
32. Möbius W, Cooper B, Kaufmann WA, Imig C, Ruhwedel T, Snaidero N, Saab AS, Varoqueaux F (2010) Electron microscopy of the mouse central nervous system. Methods Cell Biol 96:475-512.
33. Morgans CW, Brandstätter JH, Kellerman J, Betz H, Wässle H (1996) A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J Neurosci 16:6713-6721.
34. Nakajima Y, Iwakabe H, Akazawa C, Nawa H, Shigemoto R, Mizuno N, Nakanishi S (1993) Molecular characterization of a novel retinal metabotropic glutamate receptor mGluR6 with a high agonist selectivity for L-2-amino-4-phosphonobutyrate. J Biol Chem 268:11868-11873.
35. Nusinowitz S, RidderWH3rd, Pang JJ, Chang B, Noorwez SM, Kaushal S, Hauswirth WW, Heckenlively JR (2006) Cortical visual function in the rd12 mouse model of Leber congenital amarousis (LCA) after gene replacement therapy to restore retinal function. Vision Res 46:3926-3934.
36. Parsons TD, Sterling P (2003) Synaptic ribbon. Conveyor belt or safety belt? Neuron 37:379-382.
37. Peichl L, González-Soriano J (1994) Morphological types of horizontal cell in rodent retinae: a comparison of rat, mouse, gerbil, and guinea pig. Vis Neurosci 11:501-517.
38. Pivot-Pajot C, Varoqueaux F, de Saint Basile G, Bourgoin SG (2008) Munc13-4 regulates granule secretion in human neutrophils. J Immunol 180:6786-6797.
39. 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.
40. Rhee JS, Betz A, Pyott S, Reim K, Varoqueaux F, Augustin I, Hesse D, Südhof TC, Takahashi M, Rosenmund C, Brose N (2002) Beta phorbol esterand diacylglycerol-induced augmentation of transmitter release is mediated by Munc13s and not by PKCs. Cell 108:121-133.
41. Rosenmund C, Sigler A, Augustin I, Reim K, Brose N, Rhee JS (2002) Differential control of vesicle priming and short-term plasticity by Munc13 isoforms. Neuron 33:411-424.
42. 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 28:857-872.
43. Schmitz F, Augustin I, Brose N (2001) The synaptic vesicle priming protein Munc13-1 is absent from tonically active ribbon synapses of the rat retina. Brain Res 895:258-263.
44. Sherry DM, WangMM, Frishman LJ (2003) Differential distribution of vesicle associated membrane protein isoforms in the mouse retina. Mol Vis 9:673-688.
45. Sherry DM, Mitchell R, Standifer KM, 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 Neurosci 7:54.
46. 2+ regulator of synaptic exocytosis. Nat Struct Mol Biol 17:280-288.
47. Siksou L, Varoqueaux F, Pascual O, Triller A, Brose N, Marty S (2009) A common molecular basis for membrane docking and functional priming of synaptic vesicles. Eur J Neurosci 30:49-56.
48. Song Y, Ailenberg M, Silverman M (1998) Cloning of a novel gene in the human kidney homologous to rat munc13s: its potential role in diabetic nephropathy. Kidney Int 53:1689-1695.
49. Stevens DR, Wu ZX, Matti U, Junge HJ, Schirra C, Becherer U, Wojcik SM, Brose N, Rettig J (2005) Identification of the minimal protein domain required for priming activity of Munc13-1. Curr Biol 15:2243-2248.
50. Südhof TC, Rizo J (2011) Synaptic vesicle exocytosis. Cold Spring Harb Perspect Biol 3:pii:a005637.
51. tom Dieck S, Brandstätter JH (2006) Ribbon synapses of the retina. Cell Tissue Res 326:339-346.
52. 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.
53. Varoqueaux F, Sigler A, Rhee JS, Brose N, Enk C, Reim K, Rosenmund C (2002) Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming. Proc Natl Acad Sci U S A 99:9037-9042.
54. Varoqueaux F, Sons MS, Plomp JJ, Brose N (2005) Aberrant morphology and residual transmitter release at the Munc13-deficient mouse neuromuscular synapse. Mol Cell Biol 25:5973-5984.
55. Verhage M, Sørensen JB (2008) Vesicle docking in regulated exocytosis. Traffic 9:1414-1424.
56. von Gersdorff H (2001) Synaptic ribbons: versatile signal transducers. Neuron 29:7-10.
57. Wang X, Hu B, Zieba A, Neumann NG, Kasper-Sonnenberg M, Honsbein A, Hultqvist G, Conze T, Witt W, Limbach C, Geitmann M, Danielson H, Kolarow R, Niemann G, Lessmann V, Kilimann MW (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. J Neurosci 29:12584-12596.
58. Weimer RM, Gracheva EO, Meyrignac O, Miller KG, Richmond JE, Bessereau JL (2006) UNC-13 and UNC-10/rim localize synaptic vesicles to specific membrane domains. J Neurosci 26:8040-8047.
59. Wojcik SM, Brose N (2007) Regulation of membrane fusion in synaptic excitation-secretion coupling: speed and accuracy matter. Neuron 55:11-24.
60. -/-baseline secretion defect reveals source of oligomeric mucins in mouse airways. J Physiol 586:1977-1992.
61. Zikich D, Mezer A, Varoqueaux F, Sheinin A, Junge HJ, Nachliel E, Melamed R, Brose N, Gutman M, Ashery U (2008) Vesicle priming and recruitment by ubMunc13-2 are differentially regulated by calcium and calmodulin. J Neurosci 28:1949-1960.