Vesicular glutamate transporter 1 orchestrates recruitment of other synaptic vesicle cargo proteins during synaptic vesicle recycling

Journal of Biological Chemistry

Volumn 290, Issue 37, 2015, Pages 22593-22601

  Pan, Ping Yue ^a   Marrs, Julia ^a   Ryan, Timothy A ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MOLECULAR BIOLOGY;

CARGO PROTEINS; ENDOCYTIC SORTING; GLUTAMATE TRANSPORTERS; NERVE TERMINALS; SYNAPTIC VESICLE; TRANS-MEMBRANE PROTEINS;

PROTEINS;

CARRIER PROTEIN; CLATHRIN; DYNAMIN; ENDOPHILIN; SHORT HAIRPIN RNA; SYNAPTOBREVIN 2; SYNAPTOPHYSIN; SYNAPTOTAGMIN I; SYNATIC VESICLE CARGO PROTEIN; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; SLC17A7 PROTEIN, RAT;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; ENDOCYTOSIS; GENE EXPRESSION; INTERNALIZATION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; PROTON TRANSPORT; RAT; STEADY STATE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; ANIMAL; CELL CULTURE; CYTOLOGY; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; CA1 REGION, HIPPOCAMPAL; CA3 REGION, HIPPOCAMPAL; CELLS, CULTURED; ENDOCYTOSIS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 84941591674     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.651711     Document Type: Article

References (27)

1. Raimondi, A., Ferguson, S. M., Lou, X., Armbruster, M., Paradise, S., Giovedi, S., Messa, M., Kono, N., Takasaki, J., Cappello, V., O'Toole, E., Ryan, T. A., and De Camilli, P. (2011) Overlapping role of dynamin isoforms in synaptic vesicle endocytosis. Neuron 70, 1100-1114
2. Granseth, B., Odermatt, B., Royle, S. J., and Lagnado, L. (2006) Clathrinmediated endocytosis is the dominant mechanism of vesicle retrieval at hippocampal synapses. Neuron 51, 773-786
3. Kim, S. H., and Ryan, T. A. (2009) Synaptic vesicle recycling at CNS synapses without AP-2. J. Neurosci. 29, 3865-3874
4. Robinson, M. S. (2004) Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167-174
5. Fernández-Alfonso, T., Kwan, R., and Ryan, T. A. (2006) Synaptic vesicles interchange their membrane proteins with a large surface reservoir during recycling. Neuron 51, 179-186
6. Wienisch, M., and Klingauf, J. (2006) Vesicular proteins exocytosed and subsequently retrieved by compensatory endocytosis are nonidentical. Nat. Neurosci. 9, 1019-1027
7. Dittman, J., and Ryan, T. A. (2009) Molecular circuitry of endocytosis at nerve terminals. Annu. Rev. Cell Dev. Biol. 25, 133-160
8. Haucke, V., Neher, E., and Sigrist, S. J. (2011) Protein scaffolds in the coupling of synaptic exocytosis and endocytosis. Nat. Rev. Neurosci. 12, 127-138
9. Kwon, S. E., and Chapman, E. R. (2011) Synaptophysin regulates the kinetics of synaptic vesicle endocytosis in central neurons. Neuron 70, 847-854
10. Gordon, S. L., Leube, R. E., and Cousin, M. A. (2011) Synaptophysin is required for synaptobrevin retrieval during synaptic vesicle endocytosis. J. Neurosci. 31, 14032-14036
11. Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., Müller, S. A., Rammner, B., Gräter, F., Hub, J. S., De Groot, B. L., Mieskes, G., Moriyama, Y., Klingauf, J., Grubmüller, H., Heuser, J., Wieland, F., and Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell 127, 831-846
12. Balaji, J., and Ryan, T. A. (2007) Single-vesicle imaging reveals that synaptic vesicle exocytosis and endocytosis are coupled by a single stochastic mode. Proc. Natl. Acad. Sci. U. S. A. 104, 20576-20581
13. Armbruster, M., and Ryan, T. A. (2011) Synaptic vesicle retrieval time is a cell-wide rather than individual-synapse property. Nat. Neurosci. 14, 824-826
14. Armbruster, M., Messa, M., Ferguson, S. M., De Camilli, P., and Ryan, T. A. (2013) Dynamin phosphorylation controls optimization of endocytosis for brief action potential bursts. ELife 2, e00845
15. Ryan, T. A. (1999) Inhibitors of myosin light chain kinase block synaptic vesicle pool mobilization during action potential firing. J. Neurosci. 19, 1317-1323
16. Ferguson, S. M., Brasnjo, G., Hayashi, M., Wölfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L. W., Ariel, P., Paradise, S., O'Toole, E., Flavell, R., Cremona, O., Miesenböck, G., Ryan, T. A., and De Camilli, P. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science 316, 570-574
17. Voglmaier, S. M., Kam, K., Yang, H., Fortin, D. L., Hua, Z., Nicoll, R. A., and Edwards, R. H. (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron 51, 71-84
18. Kelly, B. T., McCoy, A. J., Späte, K., Miller, S. E., Evans, P. R., Höning, S., and Owen, D. J. (2008) A structural explanation for the binding of endocytic dileucine motifs by the AP2 complex. Nature 456, 976-979
19. Kim, S. H., and Ryan, T. A. (2009) Adistributed set of interactions controls μ2 functionality in the role of AP-2 as a sorting adaptor in synaptic vesicle endocytosis. J. Biol. Chem. 284, 32803-32812
20. Shaner, N. C., Lin, M. Z., McKeown, M. R., Steinbach, P. A., Hazelwood, K. L., Davidson, M. W., and Tsien, R. Y. (2008) Improving the photostability of bright monomeric orange and red fluorescent proteins. Nat. Methods 5, 545-551
21. Sankaranarayanan, S., De Angelis, D., Rothman, J. E., and Ryan, T. A. (2000) The use of pHluorins for optical measurements of presynaptic activity. Biophys. J. 79, 2199-2208
22. Fremeau, R. T., Jr., Kam, K., Qureshi, T., Johnson, J., Copenhagen, D. R., Storm-Mathisen, J., Chaudhry, F. A., Nicoll, R. A., and Edwards, R. H. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304, 1815-1819
23. Wojcik, S. M., Rhee, J. S., Herzog, E., Sigler, A., Jahn, R., Takamori, S., Brose, N., and Rosenmund, C. (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl. Acad. Sci. U. S. A. 101, 7158-7163
24. Koch, M., and Holt, M. (2012) Coupling exo- and endocytosis: an essential role for PIP2 at the synapse. Biochim. Biophys. Acta 1821, 1114-1132
25. Yao, J., Nowack, A., Kensel-Hammes, P., Gardner, R. G., and Bajjalieh, S. M. (2010) Cotrafficking of SV2 and synaptotagmin at the synapse. J. Neurosci. 30, 5569-5578
26. Willox, A. K., and Royle, S. J. (2012) Stonin 2 is a major adaptor protein for clathrin-mediated synaptic vesicle retrieval. Curr. Biol. 22, 1435-1439
27. Watanabe, S., Trimbuch, T., Camacho-Pérez, M., Rost, B. R., Brokowski, B., Söhl-Kielczynski, B., Felies, A., Davis, M. W., Rosenmund, C., and Jorgensen, E. M. (2014) Clathrin regenerates synaptic vesicles from endosomes. Nature 515, 228-233