Nanoscale dynamics of synaptic vesicle trafficking and fusion at the presynaptic active zone

eLife

Volumn 5, Issue FEBRUARY2016, 2016, Pages

  Vaithianathan, Thirumalini ^a   Henry, Diane ^a   Akmentin, Wendy ^a   Matthews, Gary ^a,b  

^a STONY BROOK UNIVERSITY   (United States)

^b STONY BROOK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE; DIFFUSION; IMAGING; NEUROTRANSMITTER RELEASE; RETINA; SYNAPSE VESICLE; SYNAPTOSOME; ANIMAL; MACROMOLECULE; METABOLISM; MICROSCOPY; NERVE ENDING; PATCH CLAMP TECHNIQUE; TRANSGENIC ANIMAL; TRANSPORT AT THE CELLULAR LEVEL; ZEBRA FISH;

MACROMOLECULE;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BIOLOGICAL TRANSPORT; MACROMOLECULAR SUBSTANCES; MICROSCOPY; PATCH-CLAMP TECHNIQUES; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES; ZEBRAFISH;

EID: 84961934910     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.13245     Document Type: Article

References (26)

1. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF. 2006. Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645. doi: 10.1126/science.1127344
2. Francis AA, Mehta B, Zenisek D. 2011. Development of new peptide-based tools for studying synaptic ribbon function. Journal of Neurophysiology 106:1028-1037. doi: 10.1152/jn.00255.2011
3. Granseth B, Odermatt B, Royle SJ, Lagnado L. 2006. Clathrin-mediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51:773-786. doi: 10.1016/j.neuron.2006.08.029
4. Graydon CW, Zhang J, Oesch NW, Sousa AA, Leapman RD, Diamond JS. 2014. Passive diffusion as a mechanism underlying ribbon synapse vesicle release and resupply. Journal of Neuroscience 34:8948-8962. doi: 10.1523/JNEUROSCI.1022-14.2014
5. Gundelfinger ED, Fejtova A. 2012. Molecular organization and plasticity of the cytomatrix at the active zone. Current Opinion in Neurobiology 22:423-430. doi: 10.1016/j.conb.2011.10.005
6. Hallermann S, Silver RA. 2013. Sustaining rapid vesicular release at active zones: potential roles for vesicle tethering. Trends in Neurosciences 36:185-194. doi: 10.1016/j.tins.2012.10.001
7. Heidelberger R, Matthews G. 1992. Calcium influx and calcium current in single synaptic terminals of goldfish retinal bipolar neurons. The Journal of Physiology 447:235-256. doi: 10.1113/jphysiol.1992.sp019000
8. Holt M, Cooke A, Neef A, Lagnado L. 2004. High mobility of vesicles supports continuous exocytosis at a ribbon synapse. Current Biology 14:173-183. doi: 10.1016/j.cub.2003.12.053
9. Joselevitch C, Zenisek D. 2009. Imaging exocytosis in retinal bipolar cells with TIRF microscopy. Journal of Visualized Experiments 28:1305. doi: 10.3791/1305
10. Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB. 2007. The Tol2kit: a multisite gateway-based construction kit forTol2 transposon transgenesis constructs. Developmental Dynamics 236:3088-3099. doi: 10.1002/dvdy.21343
11. Matthews G, Sterling P. 2008. Evidence that vesicles undergo compound fusion on the synaptic ribbon. Journal of Neuroscience 28:5403-5411. doi: 10.1523/JNEUROSCI.0935-08.2008
12. Matthews G, Fuchs P. 2010. The diverse roles of ribbon synapses in sensory neurotransmission. Nature Reviews Neuroscience 11:812-822. doi: 10.1038/nrn2924
13. 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. Nature Neuroscience 10:1268-1276. doi: 10.1038/nn1963
14. Sankaranarayanan S, De Angelis D, Rothman JE, Ryan TA. 2000. The use of pHluorins for optical measurements of presynaptic activity. Biophysical Journal 79:2199-2208. doi: 10.1016/S0006-3495(00)76468-X
15. Sigrist SJ, Schmitz D. 2011. Structural and functional plasticity of the cytoplasmic active zone. Current Opinion in Neurobiology 21:144-150. doi: 10.1016/j.conb.2010.08.012
16. Subach FV, Patterson GH, Renz M, Lippincott-Schwartz J, Verkhusha VV. 2010. Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells. Journal of the American Chemical Society 132:6481-6491. doi: 10.1021/ja100906g
17. Sudhof TC. 2012. The presynaptic active zone. Neuron 75:11-25. doi: 10.1016/j.neuron.2012.06.012
18. Vaithianathan T, Zanazzi G, Henry D, Akmentin W, Matthews G. 2013. Stabilization of spontaneous neurotransmitter release at ribbon synapses by ribbon-specific subtypes of complexin. Journal of Neuroscience 33:8216-8226. doi: 10.1523/JNEUROSCI.1280-12.2013
19. Vaithianathan T, Matthews G. 2014. Visualizing synaptic vesicle turnover and pool refilling driven by calcium nanodomains at presynaptic active zones of ribbon synapses. Proceedings of the National Academy of Sciences of the United States of America 111:8655-8660. doi: 10.1073/pnas.1323962111
20. Voglmaier SM, Kam K, Yang H, Fortin DL, Hua Z, Nicoll RA, Edwards RH. 2006. Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51:71-84. doi: 10.1016/j.neuron.2006.05.027
21. Zenisek D, Steyer JA, Almers W. 2000. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature 406:849-854. doi: 10.1038/35022500
22. Zenisek D, Steyer JA, Feldman ME, Almers W. 2002. A membrane marker leaves synaptic vesicles in milliseconds after exocytosis in retinal bipolar cells. Neuron 35:1085-1097. doi: 10.1016/S0896-6273(02)00896-6
23. Zenisek D, Davila V, Wan L, Almers W. 2003. Imaging calcium entry sites and ribbon structures in two presynaptic cells. The Journal of Neuroscience 23:2538-2348.
24. Zenisek D, Horst NK, Merrifield C, Sterling P, Matthews G. 2004. Visualizing synaptic ribbons in the living cell. Journal of Neuroscience 24:9752-9759. doi: 10.1523/JNEUROSCI.2886-04.2004
25. Zenisek D. 2008. Vesicle association and exocytosis at ribbon and extraribbon sites in retinal bipolar cell presynaptic terminals. Proceedings of the National Academy of Sciences of the United States of America 105: 4922-4927. doi: 10.1073/pnas.0709067105
26. Zhu Y, Xu J, Heinemann SF. 2009. Two pathways of synaptic vesicle retrieval revealed by single-vesicle imaging. Neuron 61:397-411. doi: 10.1016/j.neuron.2008.12.024