Aberrant function and structure of retinal ribbon synapses in the absence of complexin 3 and complexin 4

Journal of Cell Science

Volumn 122, Issue 9, 2009, Pages 1352-1361

  Reim, Kerstin ^a   Regus Leidig, Hanna ^b   Ammermüller, Josef ^c   El Kordi, Ahmed ^a   Radyushkin, Konstantin ^a   Ehrenreich, Hannelore ^a   Brandstätter, Johann Heimut ^b   Brose, Nils ^a  

^a MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^b UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

^c UNIVERSITY OF OLDENBURG   (Germany)

Author keywords

Bipolar cells; Complexin; ERG; Exocytosis; Photoreceptors; Ribbon synapse; SNARE

Indexed keywords

BINDING PROTEIN; COMPLEXIN 3; COMPLEXIN 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; B WAVE; CONTROLLED STUDY; EMBRYO; FEMALE; GENE MUTATION; KNOCKOUT MOUSE; MALE; MOUSE; MOUSE MUTANT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA BIPOLAR GANGLION CELL; RETINA INNER PLEXIFORM LAYER; RETINA NERVE CELL; SYNAPSE; SYNAPTIC TRANSMISSION; VISUAL DISORDER;

ANIMALS; BEHAVIOR, ANIMAL; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; ELECTRORETINOGRAPHY; EYE PROTEINS; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; PHOSPHOPROTEINS; PHOTORECEPTOR CELLS; RETINA; SNARE PROTEINS; SYNAPSES; SYNAPTIC TRANSMISSION; VISION DISORDERS;

MUS; VERTEBRATA;

EID: 67649339374     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.045401     Document Type: Article

References (34)

1. Bracher, A., Kadlec, J., Betz, H. and Weissenhorn, W. (2002). X-ray structure of a neuronal complexin-SNARE complex from squid. J. Biol. Chem. 277, 26517-26523.
2. Brose, N. (2008). For better or for worse: Complexins regulate SNARE function and vesicle fusion. Traffic 9, 1403-1413.
3. 2+-triggered exocytosis by facilitating vesicle priming. Proc. Natl. Acad. Sci. USA 105, 19538-19543.
4. Chen, X.; Tomchick, D. R., Kovrigin, E., Arac, D., Machius, M., Südhof, T. C. and Rizo, J. (2002). Three-dimensional structure of the complexin/SNARE complex. Neuron 33, 397-409.
5. Crowley, J. N. (1999). Behavioral phenotyping of transgenic and knockout mice: Experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 835, 18-26.
6. Dick, O., Hack, I., Altrock, W. D., Garner, C. C., Gundelfinger, E. D. and Brandstätter, J. H. (2001). Localization of the presynaptic protein Piccolo at ribbon and conventional synapses in the rat retina: Comparison with Bassoon. J. Comp. Neurol. 439, 224-234.
7. Dick, O., tom Dieck, S, Altrock, W. D., Ammermüller, J, Weiler, R., Garner, C. C., Gundelfinger, E. D. and Brandstätter, J. H. (2003). The presynaptic active zone protein Bassoon is essential for photoreceptor ribbon synapse formation in the retina. Neuron 37 775-786.
8. Giraudo, C. G., Eng, W. S., Melia, T. J. and Rothman, J. E. (2006). A clamping mechanism involved in SNARE-dependent exocytosis. Science 313, 676-680.
9. 2+-binding protein (CABP) subfamily with similarity to calmodulin. J. Biol. Chem. 275, 1247-1260.
10. Heidelberger, R. (1998). Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. J. Gen. Physiol. 111, 225-241.
11. Heidelberger, R. Sterling, P. and Matthews, G. (2002). Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J. Neurophysiol. 88, 98-106.
12. Heidelberger, R. Thoreson, W. B. and Witkovsky, P. (2005). Synaptic transmission at retinal ribbon synapses. Prog. Retin. Eye Res. 24, 682-720.
13. Huntwork, S. and Littleton, J. T. (2007). A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth. Nat. Neurosci. 10, 1235-1237.
14. Jahn, R. and Scheller, R. H. (2006). SNAREs - engines for membrane fusion. Nat. Rev. Mol. Cell. Biol. 7, 631-643.
15. LoGludice, L., Sterling, P. and Matthews, G. (2008). Mobility and turnover of vesicles at the synaptic ribbon. J. Neurosci. 28 3150-3158.
16. Morgans, C. W., Brandstätter, J. H., Kellermann, J., Betz, H. and Wässle, H. (1996). A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J. Neurosci. 16, 6713-6721.
17. Nusinowitz, S. and Heckenlively, J. R. (2006). Evaluating retinal function in the mouse retina with the electroretinogram. In Principles and Practice of Clinical Electrophysiology of Vision. 2nd edn (ed. J. R. Heckenlively and G. B. Arden), pp. 899-909. Cambridge, MA: MIT Press.
18. Parson, T. D. and Sterling, P. (2003). Synaptic ribbon: Conveyor belt or safety belt? Neuron 37, 379-382.
19. Regus-Leidig, H., tom Dieck, S., Specht, D., Meyer, L. and Brandstätter, J. H. (2009). Early steps in the assembly, of photoreceptor ribbon synapses: The involvement of precursor spheres. J. Comp. Neurol. 512, 814-824.
20. 2+-dependent neurotransmitter release. Cell 104, 71-81.
21. Reim, K., Wegmeyer, H., Brandstätter, J. H., Xue, M., Rosenmund, C., Dresbach, T., Hofmann, K. and Brose, N. (2005). Structurally and functionally unique complexins at retinal ribbon synapses. J. Cell Biol. 169, 669-680.
22. 2+-synaptotagmin I. Nat. Struct. Mol. Biol. 13, 748-750.
23. Schmitz, F., Königstorfer, A. and Südhof, T. C. (2000). RIBEYE, a component of synaptic ribbons: A protein's journey through evolution provides insights into synaptic ribbon function. Neuron 28, 857-872.
24. Sterling, P. and Matthews, G. (2005). Structure and function of ribbon synapses. Trends Neurosci. 28, 20-29.
25. Tang, J., Maximov, A., Shin, O. H., Dai, H., Rizo, J. and Südhof, T. C. (2006). A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 126, 1175-1187.
26. Thomas, K. R. and Capecchi, M. R. (1987). Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51, 503-512.
27. tom Dieck, S., Sanmartí-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K., Kämph, U., Fränzer, J. et al. (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.
28. tom Dieck, S., Altrock, W. D., Kessels, M. M., Qualmann, B., Regus, H., Brauner, D., Fejtova, A., Bracko, O., Gundelfinger, E. D. and Brandstätter, J. H. (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.
29. Varoqueaux, F., Sons, M. S., Plomp, J. J. and Brose, N. (2005). Aberrant morphology and residual transmitter release at the Munc13-deficient mouse neuromuscular synapse. Mol. Cell. Biol. 25, 5973-5984.
30. Weymouth, A. E. and Vingrys, A. J. (2008). Rodent electroretinography: Methods for extraction and interpretation of rod and cone responses. Prog. Retin. Eye Res. 27, 1-44.
31. Wojcik, S. M. and Brose, N. (2007). Regulation of membrane fusion in synaptic excitation-secretion coupling: Speed and accuracy matter. Neuron 55, 11-24.
32. Xue, M., Reim, K., Chen, X., Chao, H. T., Deng, H., Rizo, J., Brose, N. and Rosenmund, C. (2007). Distinct domains of Complexin I differentially regulate neurotransmitter release. Nat. Stuct Mol. Biol. 14, 949-958.
33. Xue, M., Stradomska, A., Chen, H., Brose, N., Zhang, W., Rosenmund, C. and Reim, K. (2008). Complexins are facilitators of neurotransmitter release at mammalian central excitatory and inhibitory synapses. Proc. Natl. Acad. Sci. USA 105, 7875-7880.
34. Zhou, Z. Y., Wan, Q. F., Thakur, P. and Heidelberger, R. (2006). Capacitance measurements in the mouse rod bipolar cell identify a pool of releasable synaptic vesicles. J. Neurophysiol. 96, 2539-2548.