A role for vesicular glutamate transporter 1 in synaptic vesicle clustering and mobility

European Journal of Neuroscience

Volumn 37, Issue 10, 2013, Pages 1631-1642

  Siksou, Léa ^a,b,c,h   Silm, Kätlin ^b,d,e   Biesemann, Christoph ^f   Nehring, Ralf B ^g   Wojcik, Sonja M ^f   Triller, Antoine ^a,b,c   El Mestikawy, Salah ^b,d,e   Marty, Serge ^a,b,c   Herzog, Etienne ^b,d,e,i  

^a ECOLE NORMALE SUPÉRIEURE   (France)

^b INSERM   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d CNRS   (France)

^e SORBONNE UNIVERSITÉ   (France)

^f MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

^g BAYLOR COLLEGE OF MEDICINE   (United States)

^h FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

ⁱ UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

Electron tomography; High pressure freezing; Mouse; Synaptic vesicle superpool; Vesicular glutamate transporters

Indexed keywords

ALDEHYDE; GLUTAMIC ACID; GREEN FLUORESCENT PROTEIN; SYNAPTOBREVIN 2; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOCHEMISTRY; CELL COMPOSITION; CELL FRACTIONATION; CELL STRUCTURE; CELL TRANSPORT; CONTROLLED STUDY; ELECTRON TOMOGRAPHY; ENDOCYTOSIS; IMMOBILIZATION; MOUSE; NERVE ENDING; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN TRANSPORT; SYNAPSE; SYNAPSE VESICLE;

ANIMALS; CELLS, CULTURED; HIPPOCAMPUS; MICE; MICE, KNOCKOUT; PRESYNAPTIC TERMINALS; SYNAPTIC VESICLES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 84878020478     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/ejn.12199     Document Type: Article

References (55)

1. Balaji, J., Armbruster, M. & Ryan, T.A. (2008) Calcium control of endocytic capacity at a CNS synapse. J. Neurosci., 28, 6742-6749.
2. Bellocchio, E.E., Reimer, R.J., Fremeau, R.T. & Edwards, R.H. (2000) Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science, 289, 957-960.
3. 2+-dependent recycling of synaptic vesicles at the frog neuromuscular junction. J. Cell Biol., 87, 297-303.
4. Ceccarelli, B., Hurlbut, W.P. & Mauro, A. (1973) Turnover of transmitter and synaptic vesicles at the frog neuromuscular junction. J. Cell Biol., 57, 499-524.
5. Croft, B.G., Fortin, G.D., Corera, A.T., Edwards, R.H., Beaudet, A., Trudeau, L.-E. & Fon, E.A. (2005) Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice. Mol. Biol. Cell, 16, 306-315.
6. Daniels, R.W., Collins, C.A., Chen, K., Gelfand, M.V., Featherstone, D.E. & DiAntonio, A. (2006) A single vesicular glutamate transporter is sufficient to fill a synaptic vesicle. Neuron, 49, 11-16.
7. Darcy, K.J., Staras, K., Collinson, L.M. & Goda, Y. (2006) Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nat. Neurosci., 9, 315-321.
8. Ferguson, S.M., Brasnjo, G., Hayashi, M., Wolfel, M., Collesi, C., Giovedi, S., Raimondi, A., Gong, L.W., Ariel, P., Paradise, S., O'Toole, E., Flavell, R., Cremona, O., Miesenbock, G., Ryan, T.A. & De Camilli, P. (2007) A selective activity-dependent requirement for dynamin 1 in synaptic vesicle endocytosis. Science, 316, 570-574.
9. Fernández-Busnadiego, R., Zuber, B., Maurer, U.E., Cyrklaff, M., Baumeister, W. & Lucic, V. (2010) Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography. J. Cell Biol., 188, 145-156.
10. Fornasiero, E.F., Raimondi, A., Guarnieri, F.C., Orlando, M., Fesce, R., Benfenati, F. & Valtorta, F. (2012) Synapsins contribute to the dynamic spatial organization of synaptic vesicles in an activity-dependent manner. J. Neurosci., 32, 12214-12227.
11. Fremeau, R.T., Troyer, M.D., Pahner, I., Nygaard, G.O., Tran, C.H., Reimer, R.J., Bellocchio, E.E., Fortin, D.L., Storm-Mathisen, J. & Edwards, R.H. (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron, 31, 247-260.
12. Fremeau, R.T., Burman, J., Qureshi, T., Tran, C.H., Proctor, J., Johnson, J., Zhang, H., Sulzer, D., Copenhagen, D.R., Storm-Mathisen, J., Reimer, R.J., Chaudhry, F.A. & Edwards, R.H. (2002) The identification of vesicular glutamate transporter 3 suggests novel modes of signaling by glutamate. Proc. Natl. Acad. Sci. USA, 99, 14488-14493.
13. Fremeau, R.T., Kam, K., Qureshi, T., Johnson, J., Copenhagen, D.R., Storm-Mathisen, J., Chaudhry, F.A., Nicoll, R.A. & Edwards, R.H. (2004) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science, 304, 1815-1819.
14. Gaffield, M.A. & Betz, W.J. (2007) Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. J. Neurosci., 27, 13691-13700.
15. Gras, C., Herzog, E., Bellenchi, G.C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., Giros, B. & Mestikawy El, S. (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci., 22, 5442-5451.
16. Herzog, E., Bellenchi, G.C., Gras, C., Bernard, V., Ravassard, P., Bedet, C., Gasnier, B., Giros, B. & Mestikawy El, S. (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J. Neurosci., 21, RC181.
17. Herzog, E., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Giros, B., Gaspar, P. & Mestikawy El, S. (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience, 123, 983-1002.
18. Herzog, E., Takamori, S., Jahn, R., Brose, N. & Wojcik, S.M. (2006) Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J. Neurochem., 99, 1011-1018.
19. Herzog, E., Nadrigny, F., Silm, K., Biesemann, C., Helling, I., Bersot, T., Steffens, H., Schwartzmann, R., Nägerl, U.V., Mestikawy El, S., Rhee, J., Kirchhoff, F. & Brose, N. (2011) In vivo imaging of intersynaptic vesicle exchange using VGLUT1Venus knock-in mice. J. Neurosci., 31, 15544-15559.
20. Heuser, J.E. (1989) Review of electron microscopic evidence favouring vesicle exocytosis as the structural basis for quantal release during synaptic transmission. Q. J. Exp. Physiol., 74, 1051-1069.
21. Heuser, J.E. & Reese, T.S. (1973) Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol., 57, 315-344.
22. Hohenberg, H., Tobler, M. & Muller, M. (1996) High-pressure freezing of tissue obtained by fine-needle biopsy. J. Microsc., 183, 133-139.
23. Jones, D.H. & Matus, A.I. (1974) Isolation of synaptic plasma membrane from brain by combined flotation-sedimentation density gradient centrifugation. Biochim. Biophys. Acta, 356, 276-287.
24. Koch, D., Spiwoks-Becker, I., Sabanov, V., Sinning, A., Dugladze, T., Stellmacher, A., Ahuja, R., Grimm, J., Schüler, S., Müller, A., Angenstein, F., Ahmed, T., Diesler, A., Moser, M., Tom Dieck, S., Spessert, R., Boeckers, T.M., Fässler, R., Hübner, C.A., Balschun, D., Gloveli, T., Kessels, M.M. & Qualmann, B. (2011) Proper synaptic vesicle formation and neuronal network activity critically rely on syndapin I. EMBO J., 30, 4955-4969.
25. Kremer, J.R., Mastronarde, D.N. & McIntosh, J.R. (1996) Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol., 116, 71-76.
26. Lisman, J.E., Raghavachari, S. & Tsien, R.W. (2007) The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat. Rev. Neurosci., 8, 597-609.
27. Mutch, S., Kensel-Hammes, P., Gadd, J., Fujimoto, B., Allen, R., Schiro, P., Lorenz, R., Kuyper, C., Kuo, J., Bajjalieh, S.M. & Chiu, D. (2011) Protein quantification at the single vesicle level reveals that a subset of synaptic vesicle proteins are trafficked with high precision. J. Neurosci., 31, 1461.
28. Nakajima, Y. & Reese, T.S. (1983) Inhibitory and excitatory synapses in crayfish stretch receptor organs studied with direct rapid-freezing and freeze-substitution. J. Comp. Neurol., 213, 66-73.
29. Orenbuch, A., Shalev, L., Marra, V., Sinai, I., Lavy, Y., Kahn, J., Burden, J.J., Staras, K. & Gitler, D. (2012) Synapsin selectively controls the mobility of resting pool vesicles at hippocampal terminals. J. Neurosci., 32, 3969-3980.
30. Peters, A., Palay, S. & Webster, H. (1991) The Fine Structure of the Nervous System. Oxford University Press, New York.
31. 2+/calmodulin-dependent protein kinase II. J. Neurosci., 22, 4406-4411.
32. Rasband, W.S. (1997) ImageJ. U.S. National Institutes of Health, Bethesda, MD, USA. Available http://rsb.info.nih.gov/ij/.
33. Rostaing, P., Real, E., Siksou, L., Lechaire, J.-P., Boudier, T., Boeckers, T.M., Gertler, F., Gundelfinger, E.D., Triller, A. & Marty, S. (2006) Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci., 24, 3463-3474.
34. Sankaranarayanan, S. & Ryan, T.A. (2001) Calcium accelerates endocytosis of vSNAREs at hippocampal synapses. Nat. Neurosci., 4, 129-136.
35. Schäfer, M.K.-H., Varoqui, H., Defamie, N., Weihe, E. & Erickson, J.D. (2002) Molecular cloning and functional identification of mouse vesicular glutamate transporter 3 and its expression in subsets of novel excitatory neurons. J. Biol. Chem., 277, 50734-50748.
36. Schenck, S., Wojcik, S.M., Brose, N. & Takamori, S. (2009) A chloride conductance in VGLUT1 underlies maximal glutamate loading into synaptic vesicles. Nat. Neurosci., 12, 156-162.
37. Siksou, L., Rostaing, P., Lechaire, J.-P., Boudier, T., Ohtsuka, T., Fejtová, A., Kao, H.-T., Greengard, P., Gundelfinger, E.D., Triller, A. & Marty, S. (2007) Three-dimensional architecture of presynaptic terminal cytomatrix. J. Neurosci., 27, 6868-6877.
38. Siksou, L., Triller, A. & Marty, S. (2009a) An emerging view of presynaptic structure from electron microscopic studies. J. Neurochem., 108, 1336-1342.
39. Siksou, L., Varoqueaux, F., Pascual, O., Triller, A., Brose, N. & Marty, S. (2009b) A common molecular basis for membrane docking and functional priming of synaptic vesicles. Eur. J. Neurosci., 30, 49-56.
40. Somogyi, J., Baude, A., Omori, Y., Shimizu, H., Mestikawy El, S., Fukaya, M., Shigemoto, R., Watanabe, M. & Somogyi, P. (2004) GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur. J. Neurosci., 19, 552-569.
41. Staras, K., Branco, T., Burden, J.J., Pozo, K., Darcy, K., Marra, V., Ratnayaka, A. & Goda, Y. (2010) A vesicle superpool spans multiple presynaptic terminals in hippocampal neurons. Neuron, 66, 37-44.
42. Stoppini, L., Buchs, P.A. & Muller, D. (1991) A simple method for organotypic cultures of nervous tissue. J. Neurosci. Meth., 37, 173-182.
43. Sudhof, T.C. (2004) The synaptic vesicle cycle. Annu. Rev. Neurosci., 27, 509-547.
44. Takamori, S., Rhee, J.S., Rosenmund, C. & Jahn, R. (2000) Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature, 407, 189-194.
45. 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. & Jahn, R. (2006) Molecular anatomy of a trafficking organelle. Cell, 127, 831-846.
46. Tatsuoka, H. & Reese, T.S. (1989) New structural features of synapses in the anteroventral cochlear nucleus prepared by direct freezing and freeze-substitution. J. Comp. Neurol., 290, 343-357.
47. Tordera, R.M., Totterdell, S., Wojcik, S.M., Brose, N., Elizalde, N., Lasheras, B. & Del Rio, J. (2007) Enhanced anxiety, depressive-like behaviour and impaired recognition memory in mice with reduced expression of the vesicular glutamate transporter 1 (VGLUT1). Eur. J. Neurosci., 25, 281-290.
48. Uchizono, K. (1965) Characteristics of excitatory and inhibitory synapses in the central nervous system of the cat. Nature, 207, 642-643.
49. Valdivia, O. (1971) Methods of fixation and the morphology of synaptic vesicles. J. Comp. Neurol., 142, 257-273.
50. Vinatier, J., Herzog, E., Plamont, M.-A., Wojcik, S.M., Schmidt, A., Brose, N., Daviet, L., Mestikawy El, S. & Giros, B. (2006) Interaction between the vesicular glutamate transporter type 1 and endophilin A1, a protein essential for endocytosis. J. Neurochem., 97, 1111-1125.
51. Voglmaier, S.M., Kam, K., Yang, H., Fortin, D.L., Hua, Z., Nicoll, R.A. & Edwards, R.H. (2006) Distinct endocytic pathways control the rate and extent of synaptic vesicle protein recycling. Neuron, 51, 71-84.
52. Wallén-Mackenzie, A., Gezelius, H., Thoby-Brisson, M., Nygård, A., Enjin, A., Fujiyama, F., Fortin, G. & Kullander, K. (2006) Vesicular glutamate transporter 2 is required for central respiratory rhythm generation but not for locomotor central pattern generation. J. Neurosci., 26, 12294-12307.
53. Westphal, V., Rizzoli, S., Lauterbach, M., Kamin, D., Jahn, R. & Hell, S. (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science, 320, 246-249.
54. Wojcik, S.M., Rhee, J.S., Herzog, E., Sigler, A., Jahn, R., Takamori, S., Brose, N. & Rosenmund, C. (2004) An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc. Natl. Acad. Sci. USA, 101, 7158-7163.
55. Zhou, Q., Petersen, C.C. & Nicoll, R.A. (2000) Effects of reduced vesicular filling on synaptic transmission in rat hippocampal neurones. J. Physiol. (Lond.), 525(Pt 1), 195-206.