Syntaxin 3B is essential for the exocytosis of synaptic vesicles in ribbon synapses of the retina

Neuroscience

Volumn 166, Issue 3, 2010, Pages 832-841

  Curtis, L ^a   Datta, P ^a   Liu, X ^a   Bogdanova, N ^a   Heidelberger, R ^a   Janz, R ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

Author keywords

SNAP 25; SNARE; splicing; synaptobrevin; VAMP; vesicle fusion

Indexed keywords

SYNTAXIN; SYNTAXIN 3B; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EXOCYTOSIS; GOLDFISH; IMMUNOHISTOCHEMISTRY; MOLECULAR BIOLOGY; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RETINA; RETINA BIPOLAR GANGLION CELL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPSE VESICLE;

ANIMALS; CELL MEMBRANE; EXOCYTOSIS; GOLDFISH; PATCH-CLAMP TECHNIQUES; QA-SNARE PROTEINS; RETINA; RETINAL BIPOLAR CELLS; SYNAPTIC VESICLES;

EID: 77249086561     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.12.075     Document Type: Article

References (40)

1. Augustine G.J., and Neher E. Calcium requirements for secretion in bovine chromaffin cells. J Physiol 450 (1992) 247-271
2. Berntson A.K., and Morgans C.W. Distribution of the presynaptic calcium sensors, synaptotagmin I/II and synaptotagmin III, in the goldfish and rodent retinas. J Vis 3 (2003) 274-280
3. Broadie K., Prokop A., Bellen H.J., O'Kane C.J., Schulze K.L., and Sweeney S.T. Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15 (1995) 663-673
4. Ciudad J., Cid E., Velasco A., Lara J.M., Aijon J., and Orfao A. Flow cytometry measurement of the DNA contents of G0/G1 diploid cells from three different teleost fish species. Cytometry 48 (2002) 20-25
5. Curtis L.B., Doneske B., Liu X., Thaller C., McNew J.A., and Janz R. Syntaxin 3b is a t-SNARE specific for ribbon synapses of the retina. J Comp Neurol 510 (2008) 550-559
6. Dowling J.E. The retina: an approachable part of the brain (1987), Belknap Press of Harvard University Press, Cambridge
7. Dulubova I., Sugita S., Hill S., Hosaka M., Fernandez I., Südhof T.C., and Rizo J. A conformational switch in syntaxin during exocytosis: role of munc18. EMBO J 18 (1999) 4372-4382
8. Gillis K.D. Techniques for membrane capacitance measurements. In: Neher E., and Sakmann B. (Eds). Single channel recording (1995), Plenum Press, New York 155-198
9. Heidelberger R. Adenosine triphosphate and the late steps in calcium-dependent exocytosis at a ribbon synapse. J Gen Physiol 111 (1998) 225-241
10. Heidelberger R. ATP is required at an early step in compensatory endocytosis in synaptic terminals. J Neurosci 21 (2001) 6467-6474
11. Heidelberger R., Heinemann C., Neher E., and Matthews G. Calcium dependence of the rate of exocytosis in a synaptic terminal. Nature 371 (1994) 513-515
12. Heidelberger R., and Matthews G. Inhibition of calcium influx and calcium current by gamma-aminobutyric acid in single synaptic terminals. Proc Natl Acad Sci U S A 88 (1991) 7135-7139
13. Heidelberger R., and Matthews G. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. J Physiol (Lond) 447 (1992) 235-256
14. Heidelberger R., and Matthews G. Dopamine enhances Ca2+ responses in synaptic terminals of retinal bipolar neurons. Neuroreport 5 (1994) 729-732
15. Heidelberger R., Sterling P., and Matthews G. Roles of ATP in depletion and replenishment of the releasable pool of synaptic vesicles. J Neurophysiol 88 (2002) 98-106
16. Heidelberger R., Zhou Z.Y., and Matthews G. Multiple components of membrane retrieval in synaptic terminals revealed by changes in hydrostatic pressure. J Neurophysiol 88 (2002) 2509-2517
17. Heidelberger R., Wang M.M., and Sherry D.M. Differential distribution of synaptotagmin immunoreactivity among synapses in the goldfish, salamander, and mouse retina. Vis Neurosci 20 (2003) 37-49
18. Heidelberger R., Thoreson W.B., and Witkovsky P. Synaptic transmission at retinal ribbon synapses. Prog Retin Eye Res 24 (2005) 682-720
19. Lagnado L., Gomis A., and Job C. Continuous vesicle cycling in the synaptic terminal of retinal bipolar cells. Neuron 17 (1996) 957-967
20. Lindau M., and Neher E. Patch-clamp techniques for time-resolved capacitance measurements in single cells. Pflügers Arch 411 (1988) 137-146
21. Low S.H., Chapin S.J., Wimmer C., Whiteheart S.W., Kömüves L.K., Mostov K.E., and Weimbs T. The SNARE machinery is involved in apical plasma membrane trafficking in MDCK cells. J Cell Biol 141 (1998) 1503-1513
22. Matthews G., and Sterling P. Evidence that vesicles undergo compound fusion on the synaptic ribbon. J Neurosci 28 (2008) 5403-5411
23. Mishima T., Fujiwara T., and Akagawa K. Reduction of neurotransmitter release by the exogenous H3 domain peptide of HPC-1/syntaxin 1A in cultured rat hippocampal neurons. Neurosci Lett 329 (2002) 273-276
24. Mochida S., Saisu H., Kobayashi H., and Abe T. Impairment of syntaxin by botulinum neurotoxin C1 or antibodies inhibits acetylcholine release but not Ca2+ channel activity. Neuroscience 65 (1995) 905-915
25. Morgans C.W., Brandstätter J.H., Kellerman J., Betz H., and Wässle H. A SNARE complex containing syntaxin 3 is present in ribbon synapses of the retina. J Neurosci 16 (1996) 6713-6721
26. O'Connor V., Heuss C., De Bello W.M., Dresbach T., Charlton M.P., Hunt J.H., Pellegrini L.L., Hodel A., Burger M.M., Betz H., Augustine G.J., and Schäfer T. Disruption of syntaxin-mediated protein interactions blocks neurotransmitter secretion. Proc Natl Acad Sci U S A 94 (1997) 12186-12191
27. Reim K., Wegmeyer H., Brandstäatter J.H., Xue M., Rosenmund C., Dresbach T., Hofmann K., and Brose N. Structurally and functionally unique complexins at retinal ribbon synapses. J Cell Biol 169 (2005) 669-680
28. Risinger C., and Larhammar D. Multiple loci for synapse protein SNAP-25 in the tetraploid goldfish. Proc Natl Acad Sci U S A 90 (1993) 10598-10602
29. Risinger C., Salaneck E., Soderberg C., Gates M., Postlethwait J.H., and Larhammar D. Cloning of two loci for synapse protein Snap25 in zebrafish: comparison of paralogous linkage groups suggests loss of one locus in the mammalian lineage. J Neurosci Res 54 (1998) 563-573
30. Rizo J., and Rosenmund C. Synaptic vesicle fusion. Nat Struct Mol Biol 15 (2008) 665-674
31. Sherry D.M., Mitchell R., Standifer K.M., and du Plessis B. Distribution of plasma membrane-associated syntaxins 1 through 4 indicates distinct trafficking functions in the synaptic layers of the mouse retina. BMC Neurosci 7 (2006) 54
32. Sherry D.M., Wang M.M., and Frishman L.J. Differential distribution of vesicle associated membrane protein isoforms in the mouse retina. Mol Vis 9 (2003) 673-688
33. Südhof T.C., and Rothman J.E. Membrane fusion: grappling with SNARE and SM proteins. Science 323 (2009) 474-477
34. von Gersdorff H., and Matthews G. Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals. Nature 367 (1994) 735-739
35. von Gersdorff H., and Matthews G. Depletion and replenishment of vesicle pools at a ribbon-type synaptic terminal. J Neurosci 17 (1997) 1919-1927
36. von Gersdorff H., Vardi E., Matthews G., and Sterling P. Evidence that vesicles on the synaptic ribbon of retinal bipolar neurons can be rapidly released. Neuron 16 (1996) 1221-1227
37. von Kriegstein K., and Schmitz F. The expression pattern and assembly profile of synaptic membrane proteins in ribbon synapses of the developing mouse retina. Cell Tissue Res 311 (2003) 159-173
38. von Kriegstein K., Schmitz F., Link E., and Sudhof T.C. Distribution of synaptic vesicle proteins in the mammalian retina identifies obligatory and facultative components of ribbon synapses. Eur J Neurosci 11 (1999) 1335-1348
39. Wang M.M., Janz R., Belizaire R., Frishman L.J., and Sherry D.M. Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina. J Comp Neurol 460 (2003) 106-122
40. Zenisek D., Steyer J.A., and Almers W. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406 (2000) 849-854