Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Site Tools

  • AAAS
  • Subscribe
  • Feedback

Site Search

Search Advanced

Originally published in Science Express on 29 April 2004
Science 18 June 2004:
Vol. 304. no. 5678, pp. 1815 - 1819
DOI: 10.1126/science.1097468
Prev | Table of Contents | Next

Reports

Vesicular Glutamate Transporters 1 and 2 Target to Functionally Distinct Synaptic Release Sites

Robert T. Fremeau, Jr.,1,2* Kaiwen Kam,2,3* Tayyaba Qureshi,5 Juliette Johnson,2,4 David R. Copenhagen,2,4 Jon Storm-Mathisen,5 Farrukh A. Chaudhry,5 Roger A. Nicoll,2,3{dagger} Robert H. Edwards1,2{dagger}

Vesicular glutamate transporters (VGLUTs) 1 and 2 show a mutually exclusive distribution in the adult brain that suggests specialization for synapses with different properties of release. Consistent with this distribution, inactivation of the VGLUT1 gene silenced a subset ofexcitatory neurons in the adult. However, the same cell populations exhibited VGLUT1-independent transmission early in life. Developing hippocampal neurons transiently coexpressed VGLUT2 and VGLUT1 at distinct synaptic sites with different short-term plasticity. The loss of VGLUT1 also reduced the reserve pool of synaptic vesicles. Thus, VGLUT1 plays an unanticipated role in membrane trafficking at the nerve terminal.

1 Department of Neurology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, CA 94143, USA.
2 Department of Physiology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, CA 94143, USA.
3 Department of Cellular and Molecular Pharmacology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, CA 94143, USA.
4 Department of Ophthalmology, Graduate Programs in Neuroscience and Cell Biology, University of California San Francisco School of Medicine, CA 94143, USA.
5 Anatomical Institute and Centre for Molecular Biology and Neuroscience, University of Oslo, Post Office Box 1105 Blindern, N-0317 Oslo, Norway.


* These authors contributed equally to this work.

{dagger} To whom correspondence should be addressed. E-mail: edwards{at}itsa.ucsf.edu (R.H.E.); nicoll{at}cmp.ucsf.edu (R.A.N.)

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Corticostriatal and Thalamostriatal Synapses Have Distinctive Properties.
J. Ding, J. D. Peterson, and D. J. Surmeier (2008)
J. Neurosci. 28, 6483-6492
   Abstract »    Full Text »    PDF »
Vesicular Glutamate and GABA Transporters Sort to Distinct Sets of Vesicles in a Population of Presynaptic Terminals.
J.-L. Boulland, M. Jenstad, A. J. Boekel, F. G. Wouterlood, R. H. Edwards, J. Storm-Mathisen, and F. A. Chaudhry (2008)
Cereb Cortex
   Abstract »    Full Text »    PDF »
Agouti-Related Peptide and MC3/4 Receptor Agonists Both Inhibit Excitatory Hypothalamic Ventromedial Nucleus Neurons.
L.-Y. Fu and A. N. van den Pol (2008)
J. Neurosci. 28, 5433-5449
   Abstract »    Full Text »    PDF »
Vesicular Glutamate Transporter 3 Is Required for Synaptic Transmission in Zebrafish Hair Cells.
N. Obholzer, S. Wolfson, J. G. Trapani, W. Mo, A. Nechiporuk, E. Busch-Nentwich, C. Seiler, S. Sidi, C. Sollner, R. N. Duncan, et al. (2008)
J. Neurosci. 28, 2110-2118
   Abstract »    Full Text »    PDF »
Kalirin-7 Is an Essential Component of both Shaft and Spine Excitatory Synapses in Hippocampal Interneurons.
X.-M. Ma, Y. Wang, F. Ferraro, R. E. Mains, and B. A. Eipper (2008)
J. Neurosci. 28, 711-724
   Abstract »    Full Text »    PDF »
TrkB is necessary for pruning at the climbing fibre-Purkinje cell synapse in the developing murine cerebellum.
E. M. Johnson, E. T. Craig, and H. H. Yeh (2007)
J. Physiol. 582, 629-646
   Abstract »    Full Text »    PDF »
Vesicular Glutamate Transporter 1 Is Required for Photoreceptor Synaptic Signaling But Not For Intrinsic Visual Functions.
J. Johnson, R. T. Fremeau Jr, J. L. Duncan, R. C. Renteria, H. Yang, Z. Hua, X. Liu, M. M. LaVail, R. H. Edwards, and D. R. Copenhagen (2007)
J. Neurosci. 27, 7245-7255
   Abstract »    Full Text »    PDF »
Regulation of CNS synapses by neuronal MHC class I.
C. A. Goddard, D. A. Butts, and C. J. Shatz (2007)
PNAS 104, 6828-6833
   Abstract »    Full Text »    PDF »
The Origin of Quantal Size Variation: Vesicular Glutamate Concentration Plays a Significant Role.
X.-S. Wu, L. Xue, R. Mohan, K. Paradiso, K. D. Gillis, and L.-G. Wu (2007)
J. Neurosci. 27, 3046-3056
   Abstract »    Full Text »    PDF »
Spatial mapping of protein abundances in the mouse brain by voxelation integrated with high-throughput liquid chromatography-mass spectrometry.
V. A. Petyuk, W.-J. Qian, M. H. Chin, H. Wang, E. A. Livesay, M. E. Monroe, J. N. Adkins, N. Jaitly, D. J. Anderson, D. G. Camp II, et al. (2007)
Genome Res. 17, 328-336
   Abstract »    Full Text »    PDF »
Vesicular Glutamate Transporter 2 Is Required for Central Respiratory Rhythm Generation But Not for Locomotor Central Pattern Generation..
A. Wallen-Mackenzie, H. Gezelius, M. Thoby-Brisson, A. Nygard, A. Enjin, F. Fujiyama, G. Fortin, and K. Kullander (2006)
J. Neurosci. 26, 12294-12307
   Abstract »    Full Text »    PDF »
Vesicular Glutamate Transporter VGLUT2 Expression Levels Control Quantal Size and Neuropathic Pain..
D. Moechars, M. C. Weston, S. Leo, Z. Callaerts-Vegh, I. Goris, G. Daneels, A. Buist, M. Cik, P. van der Spek, S. Kass, et al. (2006)
J. Neurosci. 26, 12055-12066
   Abstract »    Full Text »    PDF »
From the Cover: Indispensability of the glutamate transporters GLAST and GLT1 to brain development.
T. R. Matsugami, K. Tanemura, M. Mieda, R. Nakatomi, K. Yamada, T. Kondo, M. Ogawa, K. Obata, M. Watanabe, T. Hashikawa, et al. (2006)
PNAS 103, 12161-12166
   Abstract »    Full Text »    PDF »
Stereotyped Axon Pruning via Plexin Signaling Is Associated with Synaptic Complex Elimination in the Hippocampus.
X.-B. Liu, L. K. Low, E. G. Jones, and H.-J. Cheng (2005)
J. Neurosci. 25, 9124-9134
   Abstract »    Full Text »    PDF »
Homeostatic Scaling of Vesicular Glutamate and GABA Transporter Expression in Rat Neocortical Circuits.
S. De Gois, M. K.-H. Schafer, N. Defamie, C. Chen, A. Ricci, E. Weihe, H. Varoqui, and J. D. Erickson (2005)
J. Neurosci. 25, 7121-7133
   Abstract »    Full Text »    PDF »
Presynaptic Regulation of Quantal Size by the Vesicular Glutamate Transporter VGLUT1.
N. R. Wilson, J. Kang, E. V. Hueske, T. Leung, H. Varoqui, J. G. Murnick, J. D. Erickson, and G. Liu (2005)
J. Neurosci. 25, 6221-6234
   Abstract »    Full Text »    PDF »
G{alpha}o2 Regulates Vesicular Glutamate Transporter Activity by Changing Its Chloride Dependence.
S. Winter, I. Brunk, D. J. Walther, M. Holtje, M. Jiang, J.-U. Peter, S. Takamori, R. Jahn, L. Birnbaumer, and G. Ahnert-Hilger (2005)
J. Neurosci. 25, 4672-4680
   Abstract »    Full Text »    PDF »
Early expression of AMPA receptors and lack of NMDA receptors in developing rat climbing fibre synapses.
P. Lachamp, B. Balland, F. Tell, A. Baude, C. Strube, M. Crest, and J.-P. Kessler (2005)
J. Physiol. 564, 751-763
   Abstract »    Full Text »    PDF »
Hippocampal Complexin Proteins and Cognitive Dysfunction in Schizophrenia.
K. Sawada, A. M. Barr, M. Nakamura, K. Arima, C. E. Young, A. J. Dwork, P. Falkai, A. G. Phillips, and W. G. Honer (2005)
Arch Gen Psychiatry 62, 263-272
   Abstract »    Full Text »    PDF »
A Novel Pathway for Presynaptic Mitogen-Activated Kinase Activation via AMPA Receptors.
U. Schenk, E. Menna, T. Kim, M. Passafaro, S. Chang, P. De Camilli, and M. Matteoli (2005)
J. Neurosci. 25, 1654-1663
   Abstract »    Full Text »    PDF »
Normal Biogenesis and Cycling of Empty Synaptic Vesicles in Dopamine Neurons of Vesicular Monoamine Transporter 2 Knockout Mice.
B. G. Croft, G. D. Fortin, A. T. Corera, R. H. Edwards, A. Beaudet, L.-E. Trudeau, and E. A. Fon (2005)
Mol. Biol. Cell 16, 306-315
   Abstract »    Full Text »    PDF »
Increased Expression of the Drosophila Vesicular Glutamate Transporter Leads to Excess Glutamate Release and a Compensatory Decrease in Quantal Content.
R. W. Daniels, C. A. Collins, M. V. Gelfand, J. Dant, E. S. Brooks, D. E. Krantz, and A. DiAntonio (2004)
J. Neurosci. 24, 10466-10474
   Abstract »    Full Text »    PDF »
Gonadotropin-Releasing Hormone Neurons: Multiple Inputs, Multiple Outputs.
A. C. Gore (2004)
Endocrinology 145, 4016-4017
   Full Text »    PDF »


ADVERTISEMENT
Click Me!

ADVERTISEMENT
Click Me!

To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)